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Volume 1, by Francis Maitland Balfour
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Title: The Works of Francis Maitland Balfour, Volume 1
Separate Memoirs
Author: Francis Maitland Balfour
Editor: Michael Foster
Adam Sedgwick
Release Date: November 12, 2012 [EBook #41357]
Language: English
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THE WORKS
OF
FRANCIS MAITLAND BALFOUR.
VOL. I.
Memorial Edition.
Cambridge:
PRINTED BY C. J. CLAY, M.A. AND SON,
AT THE UNIVERSITY PRESS.
[Illustration: Sketch of Francis Maitland Balfour]
Memorial Edition.
THE WORKS
OF
FRANCIS MAITLAND BALFOUR,
M.A., LL.D., F.R.S.,
FELLOW OF TRINITY COLLEGE,
AND PROFESSOR OF ANIMAL MORPHOLOGY IN THE UNIVERSITY OF
CAMBRIDGE.
EDITED BY
M. FOSTER, F.R.S.,
PROFESSOR OF PHYSIOLOGY IN THE UNIVERSITY OF CAMBRIDGE;
AND
ADAM SEDGWICK, M.A.,
FELLOW AND LECTURER OF TRINITY COLLEGE, CAMBRIDGE.
VOL. I.
SEPARATE MEMOIRS.
London:
MACMILLAN AND CO.
1885
[_The Right of Translation is reserved._]
PREFACE.
Upon the death of Francis Maitland Balfour, a desire very naturally arose
among his friends and admirers to provide some memorial of him. And, at a
public meeting held at Cambridge in October 1882, the Vice-Chancellor
presiding, and many distinguished men of science being present, it was
decided to establish a 'Balfour Fund' the proceeds of which should be
applied: firstly to maintain a studentship, the holder of which should
devote himself to original research in Biology, especially in Animal
Morphology, and secondly, 'by occasional grants of money, to further in
other ways original research in the same subject'. The sum of £8446 was
subsequently raised; this was, under certain conditions, entrusted to and
accepted by the University of Cambridge; and the first 'Balfour student'
was appointed in October 1883.
The publication of Balfour's works in a collected form was not proposed as
an object on which part of the fund should be expended, since his family
had expressed their wish to take upon themselves the charge of arranging
for a memorial edition of their brother's scientific writings. That
edition, with no more delay than circumstances have rendered necessary, is
now laid before the public. It comprises four volumes.
The first volume contains, in chronological order, all Balfour's scattered
original papers, including those published by him in conjunction with his
pupils, as well as the Monograph on the Elasmobranch Fishes. The last
memoir in the volume, that on the Anatomy and Development of Peripatus
Capensis, was published after his death, from his notes and drawings, with
additions by Prof. Moseley and Mr Adam Sedgwick, who prepared the
manuscript for publication. To the volume is prefixed an introductory
biographical notice.
The second and third volumes are the two volumes of the Comparative
Embryology reprinted from the original edition without alteration, save the
correction of obvious misprints and omissions.
The fourth volume contains the plates illustrating the memoirs contained in
Vol. 1. We believe that we are consulting the convenience of readers in
adopting this plan, rather than in distributing the plates among the
memoirs to which they belong. To assist the reader the explanations of
these plates have been given twice: at the end of the memoir to which they
belong (in the case of the Monograph on Elasmobranch Fishes at the end of
each separate chapter), and in the volume of plates.
All the figures of these plates had to be redrawn on the stone, and our
best thanks are due to the Cambridge Scientific Instrument Company for the
pains which they have taken in executing this work. We are also indebted to
the Committee of Publication of the Zoological Society for the gift of
electrotypes of the woodcuts illustrating memoir no. XX. of Vol. 1.
Several photographs of Balfour, taken at different times of his life, the
last shortly before his death, are in the possession of his relatives and
friends; but these, in the opinion of many, leave much to be desired.
There is also a portrait of him in oils painted since his death by Mr John
Collier, A.R.A., and Herr Hildebrand of Florence has executed a posthumous
bust in bronze[1]. The portrait which forms the frontispiece of Vol. 1. has
been drawn on stone by Mr E. Wilson of the Cambridge Scientific Instrument
Company, after the latest photograph. Should it fail, in the eyes of those
who knew Balfour well, to have reproduced with complete success his
features and expression, we would venture to ask them to bear in mind the
acknowledged difficulties of posthumous portraiture.
Footnote 1: In possession of the family. Copies also exist in
the Library of Trinity College, and in the Morphological
Laboratory, at Cambridge.
TABLE OF CONTENTS.
PAGE
PREFACE i
INTRODUCTION 1
1872
I. On some points in the Geology of the East Lothian
Coast. By G. W. and F. M. BALFOUR 25
1873
II. The development and growth of the layers of the
blastoderm. With Plate 1 29
III. On the disappearance of the Primitive Groove in the
Embryo Chick. With Plate 1 41
IV. The development of the blood-vessels of the Chick.
With Plate 2 47
1874
V. A preliminary account of the development of the
Elasmobranch Fishes. With Plates 3 and 4 60
1875
VI. A comparison of the early stages in the development
of Vertebrates. With Plate 5 112
VII. On the origin and history of the urinogenital organs
of Vertebrates 135
VIII. On the development of the spinal nerves in Elasmobranch
Fishes. With Plates 22 and 23 168
1876
IX. On the spinal nerves of Amphioxus 197
1876-78
X. A Monograph on the development of Elasmobranch
Fishes. With Plates 6-21 203
1878
XI. On the phenomena accompanying the maturation and
impregnation of the ovum 521
XII. On the structure and development of the vertebrate
ovary. With Plates 24, 25, 26 549
1879
XIII. On the existence of a Head-kidney in the Embryo Chick,
and on certain points in the development of the
Müllerian duct. By F. M. BALFOUR and A. SEDGWICK.
With Plates 27 and 28 618
XIV. On the early development of the Lacertilia, together
with some observations on the nature and relations of
the primitive Streak. With Plate 29 644
XV. On certain points in the Anatomy of Peripatus Capensis 657
XVI. On the morphology and systematic position of the
Spongida 661
1880
XVII. Notes on the development of the Araneina. With Plates
30, 31, 32 668
XVIII. On the spinal nerves of Amphioxus 696
XIX. Address to the Department of Anatomy and Physiology
of the British Association for the Advancement of
Science 698
1881
XX. On the development of the skeleton of the paired fins of
Elasmobranchii, considered in relation to its bearings
on the nature of the limbs of the Vertebrata. With
Plate 33 714
XXI. On the evolution of the Placenta, and on the possibility
of employing the characters of the Placenta in the
classification of the Mammalia 734
1882
XXII. On the structure and development of Lepidosteus. By
F. M. BALFOUR and W. N. PARKER. With Plates
34-42 738
XXIII. On the nature of the organ in Adult Teleosteans and
Ganoids which is usually regarded as the Head-kidney
or Pronephros 848
XXIV. A renewed study of the germinal layers of the Chick. By
F. M. BALFOUR and F. DEIGHTON. With Plates
43, 44, 45 854
POSTHUMOUS, 1883
XXV. The Anatomy and Development of Peripatus Capensis.
Edited by H. N. MOSELEY and A. SEDGWICK. With
Plates 46-53 871
Francis Maitland Balfour, the sixth child and third son of James Maitland
Balfour of Whittinghame, East Lothian, and Lady Blanche, daughter of the
second Marquis of Salisbury, was born at Edinburgh, during a temporary stay
of his parents there, on the 10th November, 1851. He can hardly be said to
have known his father, who died of consumption in 1856, at the early age of
thirty-six, and who spent the greater part of the last two years of his
life at Madeira, separated from the younger children who remained at home.
He fancied at one time that he had inherited his father's constitution; and
this idea seems to have spurred him on to achieve early what he had to do.
But, though there was a period soon after he went to College, during which
he seemed delicate, and the state of his health caused considerable anxiety
to his friends, he eventually became fairly robust, and that in spite of
labours which greatly taxed his strength.
The early years of his life were spent chiefly at Whittinghame under the
loving care of his mother. She made it a point to attempt to cultivate in
all her children some taste for natural science, especially for natural
history, and in this she was greatly helped by the boys' tutor, Mr J. W.
Kitto. They were encouraged to make collections and to form a museum, and
the fossils found in the gravel spread in front of the house served as the
nucleus of a geological series. Frank soon became greatly interested in
these things, and indeed they may be said to have formed the beginnings of
his scientific career. At all events there was thus awakened in him a love
for geology, which science continued to be his favorite study all through
his boyhood, and interested him to the last. He was most assiduous in
searching for fossils in the gravel and elsewhere, and so great was his
love for his collections that while as yet quite a little boy the most
delightful birthday present he could think of was a box with trays and
divisions to hold his fossils and specimens. His mother, thinking that his
fondness for fossils was a passing fancy and that he might soon regret the
purchase of the box, purposely delayed the present. But he remained
constant to his wish and in time received his box. He must at this time
have been about seven or eight years old. In the children's museum, which
has been preserved, there are specimens labelled with his childish
round-hand, such as a piece of stone with the label "marks of some shels;"
and his sister Alice, who was at that time his chief companion, remembers
discussing with him one day after the nursery dinner, when he was about
nine years old, whether it were better to be a geologist or a naturalist,
he deciding for the former on the ground that it was better to do one thing
thoroughly than to attempt many branches of science and do them
imperfectly.
Besides fossils, he collected not only butterflies, as do most boys at some
time or other, but also birds; and he with his sister Alice, being
instructed in the art of preparing and preserving skins, succeeded in
making a very considerable collection. He thus acquired before long not
only a very large but a very exact knowledge of British birds.
In the more ordinary work of the school-room he was somewhat backward. This
may have been partly due to the great difficulty he had in learning to
write, for he was not only left-handed but, in his early years, singularly
inapt in acquiring particular muscular movements, learning to dance being a
great trouble to him. Probably however the chief reason was that he failed
to find any interest in the ordinary school studies. He fancied that the
family thought him stupid, but this does not appear to have been the case.
In character he was at this time quick tempered, sometimes even violent,
and the energy which he shewed in after life even thus early manifested
itself as perseverance, which, when he was crossed, often took on the form
of obstinacy, causing at times no little trouble to his nurses and tutors.
But he was at the same time warm-hearted and affectionate; full of strong
impulses, he disliked heartily and loved much, and in his affections was
wonderfully unselfish, wholly forgetting himself in his thought for others,
and ready to do things which he disliked to please those whom he loved.
Though, as we have said, somewhat clumsy, he was nevertheless active and
courageous; in learning to ride he shewed no signs of fear, and boldly put
his pony to every jump which was practicable.
In 1861 he was sent to the Rev. C. G. Chittenden's preparatory school at
Hoddesden in Hertfordshire, and here the qualities which had been already
visible at home became still more obvious. He found difficulty not only in
writing but also in spelling, and in the ordinary school-work he took but
little interest and made but little progress.
In 1865 he was moved to Harrow and placed in the house of the Rev. F.
Rendall. Here, as at Hoddesden, he did not show any great ability in the
ordinary school studies, though as he grew older his progress became more
marked. But happily he found at Harrow an opportunity for cultivating that
love of scientific studies which was yearly growing stronger in him. Under
the care of one of the Masters, Mr G. Griffith, the boys at Harrow were
even then taught the elements of natural science. The lessons were at that
time, so to speak, extra-academical, carried on out of school hours;
nevertheless, many of the boys worked at them with diligence and even
enthusiasm, and among these Balfour became conspicuous, not only by his
zeal but by his ability. Griffith was soon able to recognize the power of
his new pupil, and thus early began to see that the pale, earnest, somewhat
clumsy-handed lad, though he gave no promise of being a scholar in the
narrower sense of the word, had in him the makings of a man of science.
Griffith chiefly confined his teaching to elementary physics and chemistry
with some little geology, but he also encouraged natural history studies
and began the formation of a museum of comparative anatomy. Balfour soon
began to be very zealous in dissecting animals, and was especially
delighted when the Rev. A. C. Eaton, the well-known entomologist, on a
visit to Harrow, initiated Griffith's pupils in the art of dissecting under
water. The dissection of a caterpillar in this way was probably an epoch in
Balfour's life. Up to that time his rough examination of such bodies had
revealed to him nothing more than what in school-boy language he spoke of
as "squash;" but when under Eaton's deft hands the intricate organs of the
larval Arthropod floated out under water and displayed themselves as a
labyrinth of threads and sheets of silvery whiteness a new world of
observation opened itself up to Balfour, and we may probably date from this
the beginning of his exact morphological knowledge.
While thus learning the art of observing, he was at the same time
developing his power of thinking. He was by nature fond of argument, and
defended with earnestness any opinions which he had been led to adopt. He
was very active in the Harrow Scientific Society, reading papers, taking
part in the discussions, and exhibiting specimens. He gained in 1867 a
prize for an essay on coal, and when, in 1868, Mr Leaf offered a prize (a
microscope) "for the best account of some locality visited by the writer
during the Easter Holidays," two essays sent in, one by Balfour, the other
by his close friend, Mr Arthur Evans, since well known for his researches
in Illyria, were found to be of such unusual merit that Prof. Huxley was
specially requested to adjudicate between them. He judged them to be of
equal merit, and a prize was given to each. The subject of Balfour's essay
was "The Geology and Natural History of East Lothian." When biological
subjects were discussed at the Scientific Society, Balfour appears to have
spoken as a most uncompromising opponent of the views of Mr Charles Darwin,
little thinking that in after life his chief work would be to develop and
illustrate the doctrine of evolution.
The years at Harrow passed quickly away, Balfour making fair, but perhaps
not more than fair, progress in the ordinary school learning. In due course
however he reached the upper sixth form, and in his last year, became a
monitor. At the same time his exact scientific knowledge was rapidly
increasing. Geology still continued to be his favorite study, and in this
he made no mean progress. During his last years at Harrow he and his
brother Gerald worked out together some views concerning the geology of
their native county. These views they ultimately embodied in a paper, which
was published in their joint names in the _Geological Magazine_ for 1872,
under the title of "Some Points in the Geology of the East Lothian Coast,"
and which was in itself a work of considerable promise. Geology however was
beginning to find a rival in natural history. Much of his holiday time was
now spent in dredging for marine animals along the coast off Dunbar. Each
specimen thus obtained was carefully determined and exact records were kept
of the various 'finds,' so that the dredgings (which were zealously
continued after he had left Harrow and gone to Cambridge) really
constituted a serious study of the fauna of this part of the coast. They
also enabled him to make a not inconsiderable collection of shells, in the
arrangement of which he was assisted by his sister Evelyn, of crustacea and
of other animals.
Both to the masters and to his schoolfellows he became known as a boy of
great force of character. Among the latter his scrupulous and unwavering
conscientiousness made him less popular perhaps than might have been
expected from his bright kindly manner and his unselfish warmheartedness.
In the incidents of school life a too strict conscience is often an
inconvenience, and the sternness and energy with which Balfour denounced
acts of meanness and falsehood were thought by some to be unnecessarily
great. He thus came to be feared rather than liked by many, and
comparatively few grew to be sufficiently intimate with him to appreciate
the warmth of his affections and the charm of his playful moments.
At the Easter of 1870 he passed the entrance examination at Trinity
College, Cambridge, and entered into residence in the following October.
His college tutor was Mr J. Prior, but he was from the first assisted and
guided in his studies by his friend, Mr Marlborough Pryor, an old Harrow
boy, who in the same October had been, on account of his distinction in
Natural Science, elected a Fellow of the College, in accordance with
certain new regulations which then came into action for the first time, and
which provided that every three years one of the College Fellowships should
be awarded for excellence in some branch or branches of Natural Science, as
distinguished from mathematics, pure or mixed. During the whole of that
year and part of the next Mr Marlborough Pryor remained in residence, and
his influence in wisely directing Balfour's studies had a most beneficial
effect on the latter's progress.
During his first term Balfour was occupied in preparation for the Previous
Examination; and this he successfully passed at Christmas. After that he
devoted himself entirely to Natural Science, attending lectures on several
branches. During the Lent term he was a very diligent hearer of the
lectures on Physiology which I was then giving as Trinity Prælector, having
been appointed to that post in the same October that Balfour came into
residence. At this time he was not very strong, and I remember very well
noticing among my scanty audience, a pale retiring student, whose mind
seemed at times divided between a desire to hear the lecture and a feeling
that his frequent coughing was growing an annoyance to myself and the
class. This delicate-looking student, I soon learnt, was named Balfour, and
when the Rev. Coutts Trotter, Mr Pryor and myself came to examine the
candidates for the Natural Science Scholarships which were awarded at
Easter, we had no difficulty in giving the first place to him. In point of
knowledge, and especially in the thoughtfulness and exactitude displayed in
his papers and work, he was very clearly ahead of his competitors.
During the succeeding Easter term and the following winter he appears to
have studied physics, chemistry, geology and comparative anatomy, both
under Mr Marlborough Pryor and by means of lectures. He also continued to
attend my lectures, but though I gradually got to know him more and more we
did not become intimate until the Lent term of 1872. He had been very much
interested in some lectures on embryology which I had given, and, since
Marlborough Pryor had left or was about to leave Cambridge, he soon began
to consult me a good deal about his studies. He commenced practical
histological and embryological work under me, and I remember very vividly
that one day when we were making a little excursion in search of nests and
eggs of the stickleback in order that he might study the embryology of
fishes, he definitely asked my opinion as to whether he might take up a
scientific career with a fair chance of success. I had by this time formed
a very high opinion of his abilities, and learning then for the first time
that he had an income independent of his own exertions, my answer was very
decidedly a positive one. Soon after, feeling more and more impressed with
his power and increasingly satisfied both with his progress in biological
studies and his sound general knowledge of other sciences, anxious also, it
may be, at the same time that as much original inquiry as possible should
be carried on at Cambridge in my department, I either suggested to him or
acquiesced in his own suggestion that he should at once set to work on some
distinct research; and as far as I remember the task which I first proposed
to him was an investigation of the layers of the blastoderm in the chick.
It must have been about the same time that I proposed to him to join me in
preparing for publication a small work on Embryology, the materials for
this I had ready to hand in a rough form as lectures which I had previously
given. To this proposal he enthusiastically assented, and while the lighter
task of writing what was to be written fell to me, he undertook to work
over as far as was possible the many undetermined points and unsatisfactory
statements across which we were continually coming.
During his two years at College his health had improved; though still
hardly robust and always in danger of overworking himself, he obviously
grew stronger. He rejoiced exceedingly in his work, never tiring of it, and
was also making his worth felt among his fellow students, and especially
perhaps among those of his own college whose studies did not lie in the
same direction as his own. At this time he must have been altogether happy,
but a sorrow now came upon him. His mother, to whom he was passionately
attached, and to whose judicious care in his early days not only the right
development of his strong character but even his scientific leanings were
due, had for some time past been failing in health, though her condition
caused no immediate alarm. In May 1872, however, she died quite suddenly
from unsuspected heart disease. Her loss was a great blow to him, and for
some time afterward I feared his health would give way; but he bore his
grief quietly and manfully and threw himself with even increased vigour
into his work.
During the academic session of 1872-3, he continued steadily at work at his
investigations, and soon began to make rapid progress. At the beginning he
had complained to me about what he considered his natural clumsiness, and
expressed a fear that he should never be able to make satisfactory
microscopic sections; as to his being able to make drawings of his
dissections and microscopical preparations, he looked upon that at first as
wholly impossible. I need hardly say that in time he acquired great skill
in the details of microscopical _technique_, and that his drawings, if
wanting in so-called artistic finish, were always singularly true and
instructive. While thus struggling with the details which I could teach
him, he soon began to manifest qualities which no teacher could give him. I
remember calling his attention to Dursy's paper on the Primitive Streak,
and suggesting that he should work the matter over, since if such a
structure really existed, it must, most probably, have great morphological
significance. I am free to confess that I myself rather doubted the matter,
and a weaker student might have been influenced by my preconceptions.
Balfour, however, thus early had the power of seeing what existed and of
refusing to see what did not exist. He was soon able to convince me that
Dursy's streak was a reality, and the complete working out of its
significance occupied his thoughts to the end of his days.
The results of these early studies were made known in three papers which
appeared in the _Quarterly Journal of Microscopical Science_ for July 1873,
and will be found in the beginning of this volume. The summer and autumn of
that year were spent partly in a visit to Finland, in company with his
friend and old school-fellow Mr Arthur Evans, and partly in formal
preparation for the approaching Tripos examination. Into this preparation
Balfour threw himself with characteristic energy, and fully justified my
having encouraged his spending so much of the preceding time in original
research, not only by the rapidity with which he accumulated the stock of
knowledge of various kinds necessary for the examination but also by the
manner in which he acquitted himself at the trial itself. At that time the
position of the candidates in the Natural Sciences Tripos was determined by
the total number of marks, and Balfour was placed second, the first place
being gained by H. Newell Martin of Christ's College, now Professor at
Baltimore, U.S.A. In the examination, in which I took part, Balfour did not
write much, and he had not yet learnt the art of putting his statements in
the best possible form; he won his position chiefly by the firm thought and
clear insight which was present in almost all his answers.
The examination was over in the early days of Dec. 1873 and Balfour was now
free to devote himself wholly to his original work. Happily, the University
had not long before secured the use of two of the tables at the then
recently founded Stazione Zoologica at Naples. And upon the nomination of
the University, Balfour, about Christmas, started for Naples in company
with his friend Mr A. G. Dew-Smith, also of Trinity College. The latter was
about to carry on some physiological observations; Balfour had set himself
to work out as completely as he could the embryology of Elasmobranch
fishes, about which little was at that time known, but which, from the
striking characters of the adult animals could not help proving of interest
and importance.
From his arrival there at Christmas 1873 until he left in June 1874, he
worked assiduously, and with such success, that as the result of the
half-year's work he had made a whole series of observations of the greatest
importance. Of these perhaps the most striking were those on the
development of the urogenital organs, on the neurenteric canal, on the
development of the spinal nerves, on the formation of the layers and on the
phenomena of segmentation, including a history of the behaviour of nuclei
in cell division. He returned home laden with facts and views both novel
and destined to influence largely the progress of embryology.
In August of the same year he attended the meeting of the British
Association for the Advancement of Science at Belfast; and the account he
then gave of his researches formed one of the most important incidents at
the Biological Section on that occasion.
In the September of that year the triennial fellowship for Natural Science
was to be awarded at Trinity College, and Balfour naturally was a
candidate. The election was, according to the regulations, to be determined
partly by the result of an examination in various branches of science, and
partly by such evidence of ability and promise as might be afforded by
original work, published or in manuscript. He spent the remainder of the
autumn in preparation for this examination. But when the examination was
concluded it was found that in his written answers he had not been very
successful; he had not even acquitted himself so well as in the Tripos of
the year before, and had the election been determined by the results of the
examination alone, the examiners would have been led to choose the
gentleman who was Balfour's only competitor. The original work however
which Balfour sent in, including a preliminary account of the discoveries
made at Naples, was obviously of so high a merit and was spoken of in such
enthusiastic terms by the External Referee Prof. Huxley, that the examiners
did not hesitate for a moment to neglect altogether the formal written
answers (and indeed the papers of questions were only introduced as a
safeguard, or as a resource in case evidence of original power should be
wanted) and unanimously recommended him for election. Accordingly he was
elected Fellow in the early days of October.
Almost immediately after, the little book on Embryology appeared, on which
he and I had been at work, he doing his share even while his hands and mind
were full of the Elasmobranch inquiry. The title-page was kept back some
little time in order that his name might appear on it with the addition of
Fellow of Trinity, a title of which he was then, and indeed always
continued to be, proud. He also published in the October number of the
_Quarterly Journal of Microscopical Science_ a preliminary account of his
Elasmobranch researches.
He and his friends thought that after these almost incessant labours, and
the excitement necessarily contingent upon the fellowship election, he
needed rest and change. Accordingly on the 17th of October he started with
his friend Marlborough Pryor on a voyage to the west coast of South
America. They travelled thither by the Isthmus of Panama, visited Peru and
Chili, and returned home along the usual route by the Horn; reaching
England some time in Feb. 1875.
Refreshed by this holiday, he now felt anxious to complete as far as
possible his Elasmobranch work, and very soon after his return home, in
fact in March, made his way again to Naples, where he remained till the hot
weather set in in May. On his return to Cambridge, he still continued
working on the Elasmobranchii, receiving material partly from Naples,
partly from the Brighton Aquarium, the then director of which, Mr Henry
Lee, spared no pains to provide him both with embryo and adult fishes.
While at Naples, he communicated to the Philosophical Society at Cambridge
a remarkable paper on "The Early Stages of Vertebrates," which was
published in full in the _Quarterly Journal of Microscopical Science_,
July, 1875; he also sent me a paper on "The Development of the Spinal
Nerves", which I communicated to the Royal Society, and which was
subsequently published in the _Philosophical Transactions_ of 1876. He
further wrote in the course of the summer and published in the _Journal of
Anatomy and Physiology_ in October, 1875, a detailed account of his
"Observations and Views on the Development of the Urogenital Organs."
Some time in August of the same year he started in company with Mr Arthur
Evans and Mr J. F. Bullar for a second trip to Finland, the travellers on
this occasion making their way into regions very seldom visited, and having
to subsist largely on the preserved provisions which they carried with
them, and on the produce of their rods and guns. From a rough diary which
Balfour kept during this trip it would appear that while enjoying heartily
the fun of the rough travelling, he occupied himself continually with
observations on the geology and physical phenomena of the country, as well
as on the manners, antiquities, and even language of the people. It was one
of his characteristic traits, a mark of the truly scientific bent of his
mind, of his having, as Dohrn soon after Balfour's first arrival at Naples
said, 'a real scientific head,' that every thing around him wherever he
was, incited him to careful exact observation, and stimulated him to
thought.
In the early part of the Long Vacation of the same year he had made his
first essay in lecturing, having given a short course on Embryology in a
room at the New Museums, which I then occupied as a laboratory. Though he
afterwards learnt to lecture with great clearness he was not by nature a
fluent speaker, and on this occasion he was exceedingly nervous. But those
who listened to him soon forgot these small defects as they began to
perceive the knowledge and power which lay in their new teacher.
Encouraged by the result of this experiment, he threw himself, in spite of
the heavy work which the Elasmobranch investigation was entailing, with
great zeal into an arrangement which Prof. Newton, Mr J. W. Clark and
myself had in course of the summer brought about, that he and Mr A. Milnes
Marshall, since Professor at Owens College, Manchester, should between them
give a course on Animal Morphology, with practical instruction, Prof.
Newton giving up a room in the New Museums for the purpose.
In the following October (1875) upon Balfour's return from Finland, these
lectures were accordingly begun and carried on by the two lecturers during
the Michaelmas and Lent Terms. The number of students attending this first
course, conducted on a novel plan, was, as might be expected, small, but
the Lent Term did not come to an end before an enthusiasm for morphological
studies had been kindled in the members of the class.
The ensuing Easter term (1876) was spent by Balfour at Naples, in order
that he might carry on towards completion his Elasmobranch work. He had by
this time determined to write as complete a monograph as he could of the
development of these fishes, proposing to publish it in instalments in the
_Journal of Anatomy and Physiology_, and subsequently to gather together
the several papers into one volume. The first of these papers, dealing with
the ovum, appeared in Jan. 1876; most of the numbers of the Journal during
that and the succeeding year contained further portions; but the complete
monograph did not leave the publisher's hands until 1878.
He returned to England with his pupil and friend Mr J. F. Bullar some time
in the summer; on their way home they passed through Switzerland, and it
was during the few days which he then spent in sight of the snow-clad hills
that the beginnings of a desire for that Alpine climbing, which was
destined to be so disastrous, seem to have been kindled in him.
In October, 1876, he resumed the lectures on Morphology, taking the whole
course himself, his colleague, Mr Marshall, having meanwhile left
Cambridge. Indeed, from this time onward, he may be said to have made these
lectures, in a certain sense, the chief business of his life. He lectured
all three terms, devoting the Michaelmas and Lent terms to a systematic
course of Animal Morphology, and the Easter term to a more elementary
course of Embryology. These lectures were given under the auspices of Prof.
Newton; but Balfour's position was before long confirmed by his being made
a Lecturer of Trinity College, the lectures which he gave at the New
Museums, and which were open to all students of the University, being
accepted in a liberal spirit by the College as equivalent to College
Lectures. He very soon found it desirable to divide the morphological
course into an elementary and an advanced course, and to increase the
number of his lectures from three to four a week. Each lecture was followed
by practical work, the students dissecting and examining microscopically,
an animal or some animals chosen as types to illustrate the subject-matter
of the lecture; and although Balfour had the assistance at first of one[2],
and ultimately of several demonstrators, he himself put his hand to the
plough, and after the lecture always spent some time in the laboratory
among his pupils. Had Balfour been only an ordinary man, the zeal and
energy which he threw into his lectures, and into the supervision of the
practical work, added to the almost brotherly interest which he took in the
individual development of every one of the pupils who shewed any love
whatever for the subject, would have made him a most successful teacher.
But his talents and powers were such as could not be hid even from
beginners. His extensive and exact knowledge, the clearness with which in
spite of, or shall I not rather say, by help of a certain want of fluency,
he explained difficult and abstruse matters, the trenchant way in which he
lay bare specious fallacies, and the presence in almost his every word of
that power which belongs only to the man who has thought out for himself
everything which he says, these things aroused and indeed could hardly fail
to arouse in his hearers feelings which, except in the case of the very
dullest, grew to be those of enthusiasm. His class, at first slowly, but
afterwards more rapidly, increased in numbers, and, what is of more
importance, grew in quality. The room allotted to him soon became far too
small and steps were taken to provide for him, for myself, whose wants were
also urgent, and for the biological studies generally, adequate
accommodation; but it was not until Oct. 1877 that we were able to take
possession of the new quarters.
Footnote 2: His first Demonstrator up to Christmas 1877, was
Mr J. F. Bullar. In Jan. 1878, Mr Adam Sedgwick took the post
of Senior Demonstrator, and held it until Balfour's death.
Even this new accommodation soon became insufficient, and in the spring of
1882 a new morphological laboratory was commenced in accordance with plans
suggested by himself. He was to have occupied them in the October term,
1883, but did not live to see them finished.
As might have been expected from his own career, he regarded the mere
teaching of what is known as a very small part of his duties as Lecturer;
and as soon as any of his pupils became sufficiently advanced, he urged or
rather led them to undertake original investigations; and he had the
satisfaction before his death of seeing the researches of his pupils (such
as those by Messrs. Bullar, Sedgwick, Mitzikuri, Haddon, Scott, Osborne,
Caldwell, Heape, Weldon, Parker, Deighton and others) carried to a
successful end. In each of these inquiries he himself took part, sometimes
a large part, generally suggesting the problem to be solved, indicating the
methods, and keeping a close watch over the whole progress of the study.
Hence in many cases the published account bears his name as well as that of
the pupil.
In the year 1878 his _Monograph on Elasmobranch Fishes_ was published as a
complete volume, and in the same year he received the honour of being
elected a Fellow of the Royal Society, a distinction which now-a-days does
not often fall to one so young. No sooner was the Monograph completed than
in spite of the labours which his lectures entailed, he set himself to the
great task of writing a complete treatise on _Comparative Embryology_. This
not only laid upon him the heavy burden of gathering together the
observations of others, enormous in number and continually increasing,
scattered through many journals and books, and recorded in many different
languages, as well as of putting them in orderly array, and of winnowing
out the grain from the chaff (though his critical spirit found some relief
in the latter task), but also caused him much labour, inasmuch as at almost
every turn new problems suggested themselves, and demanded inquiry before
he could bring his mind to writing about them. This desire to see his way
straight before him, pursued him from page to page, and while it has
resulted in giving the book an almost priceless value, made the writing of
it a work of vast labour. Many of the ideas thus originated served as the
bases of inquiries worked out by himself or his pupils, and published in
the form of separate papers, but still more perhaps never appeared either
in the book or elsewhere and were carried with him undeveloped and
unrecorded to the grave.
The preparation of this work occupied the best part of his time for the
next three years, the first volume appearing in 1880, the second in 1881.
In the autumn of 1880, he attended the Meeting at Swansea of the British
Association for the Advancement of Science, having been appointed
Vice-President of the Biological Section with charge of the Department of
Anatomy and Physiology. At the Meetings of the Association, especially of
late years, much, perhaps too much, is expected in the direction of
explaining the new results of science in a manner interesting to the
unlearned. Popular expositions were never very congenial to Balfour, his
mind was too much occupied with the anxiety of problems yet to be solved;
he was therefore not wholly at his ease, in his position on this occasion.
Yet his introductory address, though not of a nature to interest a large
mixed audience, was a luminous, brief exposition of the modern development
and aims of embryological investigation.
During these years of travail with the _Comparative Embryology_ the amount
of work which he got through was a marvel to his friends, for besides his
lectures, and the researches, and the writing of the book, new labours were
demanded of him by the University for which he was already doing so much.
Men at Cambridge, and indeed elsewhere as well, soon began to find out that
the same clear insight which was solving biological problems could be used
to settle knotty questions of policy and business. Moreover he united in a
remarkable manner, the power of boldly and firmly asserting and maintaining
his own views, with a frank courteousness which went far to disarm
opponents. Accordingly he found himself before long a member of various
Syndicates, and indeed a very great deal of his time was thus occupied,
especially with the Museums and Library Syndicates, in both of which he
took the liveliest interest. Besides these University duties his time and
energy were also at the service of his College. In the preparation of the
New Statutes, with which about this time the College was much occupied, the
Junior Fellows of the College took a conspicuous share, and among these
Junior Fellows Balfour was perhaps the most active; indeed he was their
leader, and he threw himself into the investigation of the bearings and
probable results of this and that proposed new statute with as much zeal as
if he were attacking some morphological problem.
While he was in the midst of these various labours, his friends often
feared for his strength, for though gradually improving in health after his
first year at Cambridge, he was not robust, and from time to time he seemed
on the point of breaking down. Still, hard as he was working, he was in
reality wisely careful of himself, and as he grew older, paid more and more
attention to his health, daily taking exercise in the form either of
bicycle rides or of lawn-tennis. Moreover he continued to spend some part
of his vacations in travel. Combining business with pleasure, he made
frequent visits to Germany and France, and especially to Naples. The
Christmas of 1876-7 he spent in Greece, that of 1878-9 at Ragusa, where his
old school-fellow and friend Mr Arthur Evans was at that time residing, and
the appointment of his friend Kleinenberg to a Professorship at Messina led
to a journey there. Early in the long vacation of 1880, he went with his
sister, Mrs H. Sidgwick, and her husband to Switzerland, and was joined
there for a short time by his friend and pupil Adam Sedgwick. During this
visit he took his first lessons in Alpine climbing, making several
excursions, some of them difficult and dangerous; and the love of
mountaineering laid so firm a hold upon him, that he returned to
Switzerland later on in the autumn of the same year, in company with his
brother Gerald, and spent some weeks near Zermatt in systematic climbing,
ascending, among other mountains, the Matterhorn and the Weisshorn. In the
following summer, 1881, he and his brother Gerald again visited the Alps,
dividing their time between the Chamonix district and the Bernese Oberland.
On this occasion some of the excursions which they made were of extreme
difficulty, and such as needed not only great presence of mind and bodily
endurance, but also skilful and ready use of the limbs. As a climber indeed
Balfour soon shewed himself fearless, indefatigable, and expert in all
necessary movements as well as full of resources and expedients in the face
of difficulties, so much so that he almost at once took rank among the
foremost of distinguished mountaineers. In spite of his apparent clumsiness
in some matters, he had even as a lad proved himself to be a bold and
surefooted climber. Moreover he had been perhaps in a measure prepared for
the difficulties of Alpine climbing by his experience in deer-stalking.
This sport he had keenly and successfully pursued for many years at his
brother's place in Rosshire. When however about the year 1877, the question
of physiological experiments on animals became largely discussed in public,
he felt that to continue the pursuit of this or any other sport involving,
for the sake of mere pleasure, the pain and death of animals, was
inconsistent with the position which he had warmly taken up, as an advocate
of the right to experiment on animals; and he accordingly from that time
onward wholly gave it up.
His fame as an investigator and teacher, and as a man of brilliant and
powerful parts, was now being widely spread. Pupils came to him, not only
from various parts of England, but from America, Australia and Japan. At
the York Meeting of the British Association for the Advancement of Science,
in August, 1881, he was chosen as one of the General Secretaries. In April,
1881, the honorary degree of LL.D. was conferred upon him by the University
of Glasgow, and in November of the same year the Royal Society gave him one
of the Royal Medals in recognition of his embryological discoveries, and at
the same time placed him on its Council.
At Cambridge he was chosen, in the autumn of 1880, President of the
Philosophical Society, and in the December of that year a brilliant company
were gathered together at the Annual Dinner to do honour to their new young
President. Otherwise nothing as yet had been done for him in his own
University in the way of recognition of his abilities and services; and he
still remained a Lecturer of Trinity College, giving lectures in a
University building. An effort had been made by some of his friends to urge
the University to take some step in this direction; but it was thought at
that time impossible to do anything. In 1881 a great loss fell upon the
sister University of Oxford in the death of Prof. George Rolleston; and
soon after very vigorous efforts were made to induce Balfour to become a
candidate for the vacant chair. The prospect was in many ways a tempting
one, and Balfour seeing no very clear way in the future for him at his own
University, was at times inclined to offer himself, but eventually he
decided to remain at Cambridge. Hardly had this temptation if we may so
call it been overcome when a still greater one presented itself. Through
the lamented death of Sir Wyville Thomson in the winter of 1881-2, the
chair of Natural History at Edinburgh, perhaps the richest and most
conspicuous biological chair in the United Kingdom, became vacant. The post
was in many ways one which Balfour would have liked to hold. The teaching
duties were it is true laborious, but they had in the past been compressed
into a short time, occupying only the summer session and leaving the rest
of the year free, and it seemed probable that this arrangement might be
continued with him. The large emolument would also have been grateful to
him inasmuch as he would have felt able to devote the whole of it to
scientific ends; and the nearness to Whittinghame, his native place and
brother's home, added to the attractions; but what tempted him most was the
position which it would have given him, and the opportunities it would have
afforded, with the rich marine Fauna of the north-eastern coast close at
hand, to develop a large school of Animal Morphology. The existing
Professors at Edinburgh were most desirous that he should join them, and
made every effort to induce him to come. On the part of the Crown, in whose
hands the appointment lay, not only were distinct offers made to him, but
he was repeatedly pressed to accept the post. Nor was it until after a
considerable struggle that he finally refused, his love for his own
University in the end overcoming the many inducements to leave; he elected
to stay where he was, trusting to the future opening up for him some
suitable position. In this decision he was undoubtedly influenced by the
consideration that Cambridge, besides being the centre of his old
friendships, had become as it were a second home for his own family. By the
appointment of Lord Rayleigh to the chair of Experimental Physics his
sister Lady Rayleigh had become a resident, his sister Mrs Sidgwick had
lived there now for some years, and his brother Gerald generally spent the
summer there; their presence made Cambridge doubly dear to him.
At the close of the Michaelmas term, with feelings of relief at having
completed his _Comparative Embryology_, the preparation of the second
volume of which had led to almost incessant labour during the preceding
year, he started to spend the Christmas vacation with his friend
Kleinenberg at Messina. Stopping at Naples on his way thither he found his
pupil Caldwell, who had been sent to occupy the University table at the
Stazione Zoologica, lying ill at Capri, with what proved to be typhoid
fever. The patient was alone, without any friend to tend him, and his
mother who had been sent for had not yet arrived. Accordingly Balfour (with
the kindness all forgetful of himself which was his mark all his life
through) stayed on his journey to nurse the sick man until the mother came.
He then went on to Messina, and there seemed to be in good health, amusing
himself with the ascent of Etna. Yet in January, soon after his return
home, he complained of being unwell, and in due time distinct symptoms of
typhoid fever made their appearance. The attack at first promised to be
severe, but happily the crisis was soon safely passed and the convalescence
was satisfactory.
While yet on his sick bed, a last attempt was made to induce him to accept
the Edinburgh offer, and for the last time he refused. These repeated
offers, and the fact that the dangers of his grave illness had led the
University vividly to realize how much they would lose if Balfour were
taken away from them, encouraged his friends to make a renewed effort to
gain for him some adequate position in the University. This time the
attempt was successful, and the authorities took a step, unusual but
approved of by the whole body of resident members of the University; they
instituted a new Professorship of Animal Morphology, to be held by Balfour
during his life or as long as he should desire, but to terminate at his
death or resignation unless it should be otherwise desirable. Accordingly
in May, 1882, he was admitted into the Professoriate as Professor of Animal
Morphology.
During his illness his lectures had been carried on by his Demonstrator, Mr
Adam Sedgwick, who continued to take his place during the remainder of that
Lent Term and during the ensuing Easter Term. The spring Balfour spent
partly in the Channel Islands with his sister Alice, partly in London with
his eldest brother, but in the course of the Easter Term returned to
Cambridge and resumed his work though not his lectures. His recovery to
health was steady and satisfactory, the only drawback being a swelling over
the shin-bone of one leg, due to a blow on the rocks at Sark; otherwise he
was rapidly becoming strong. He himself felt convinced that a visit to the
Alps, with some mountaineering of not too difficult a kind, would complete
his restoration to health. In this view many of his friends coincided; for
the experience of former years had shewn them what a wonderfully beneficial
effect the Alpine air and exercise had upon his health. He used to go away
pale, thin and haggard, to return bronzed, clear, firm and almost stout;
nor was there anything in his condition which seemed to forbid his
climbing, provided that he was cautious at the outset. Accordingly, early
in June he left Cambridge for Switzerland, having long ago, during his
illness in fact, engaged his old guide, Johann Petrus, whom he had first
met in 1880, and who had always accompanied him in his expeditions since.
His first walking was in the Chamonix district; and here he very soon found
his strength and elasticity come back to him. Crossing over from Montanvert
to Courmayeur, by the Col du Géant, he was attracted by the peak called the
Aiguille Blanche de Peuteret, a virgin peak, the ascent of which had been
before attempted but not accomplished. Consulting with Petrus he determined
to try it, feeling that the fortnight, which by this time he had spent in
climbing, had brought back to him his old vigour, and that his illness was
already a thing of the past.
There is no reason to believe that he regarded the expedition as one of
unusual peril; and an incident which at the time of his death was thought
by some to indicate this was in reality nothing more than a proof of his
kindly foresight. The guide Petrus was burdened by a debt on his land
amounting to about £150. In the previous year Balfour and his brother had
come to know of this debt; and, seeing that no Alpine ascent is free from
danger, that on any expedition some accident might carry them off, had
conceived the idea of making some provision for Petrus' family in case he
might meet with sudden death in their service. This suggestion of the
previous year Balfour carried out on this occasion, and sent home to his
brother Gerald a cheque of £150 for this purpose. But the cheque was sent
from Montanvert before he had even conceived the idea of ascending the
Aiguille Blanche. It was not a provision for any specially dangerous
ascent, and must be regarded as a measure prompted not by a sense of coming
peril but rather by the donor's generous care for his servant.
On Tuesday afternoon, July 18, he and Petrus, with a porter to carry
provisions and firing to their sleeping-place on the rocks, set out from
Courmayeur, the porter returning the same night. They expected to get back
to Courmayeur some time on the Thursday, but the day passed without their
appearing. This did not cause any great anxiety because it was supposed
that they might have found it more convenient to pass over to the Chamonix
side than to return to Courmayeur. When on Friday however telegrams
dispatched to Chamonix and Montanvert brought answers that nothing had been
seen of them, it became evident that some accident had happened, and an
exploring party set out for the hills. It was not until early on the Sunday
morning that this search party found the bodies, both partly covered with
snow, lying on the Glacier de Fresney, below the impassable icefall which
separates the upper basin of the glacier from the lower portion, and at the
foot of a _couloir_ which descends by the side of the icefall. Their tracks
were visible on the snow at the top of the _couloir_. Balfour's neck was
broken, and his skull fractured in three places; Petrus' body was also
fractured in many places. The exact manner of their death will never be
known, but there can be no doubt that, in Balfour's case at all events, it
was instantaneous, and those competent to form a judgment are of opinion
that they were killed by a sudden fall through a comparatively small
height, slipping on the rocks as they were descending by the side of the
ice-fall, and not precipitated from the top of the _couloir_. There is
moreover indirect evidence which renders it probable that in the fatal fall
Petrus slipped first and carried Balfour with him. Whether they had reached
the summit of the Aiguille and were returning home after a successful
ascent or whether they were making their way back disheartened and wearied
with failure, is not and perhaps never will be known. Since the provisions
at the sleeping-place were untouched, the deaths probably took place on
Wednesday the 19th. The bringing down the bodies proved to be a task of
extreme difficulty, and it was not till Wednesday the 26th that the remains
reached Courmayeur, where M. Bertolini, the master of the hotel, and indeed
everyone, not least the officers of a small body of Italian troops
stationed there, shewed the greatest kindness and sympathy to Balfour's
brothers, Gerald and Eustace, who hastened to the spot as soon as the news
of the terrible disaster was telegraphed home. Mr Walter Leaf also and Mr
Conway, friends of Balfour, the former a very old one, who had made their
way to Courmayeur from other parts of Switzerland as soon as they heard of
the accident, rendered great assistance. The body was embalmed, brought to
England, and buried at Whittinghame on Saturday, Aug. 5, the Fellows of
Trinity College holding a service in the College Chapel at the same time.
In person he was tall, being fully six feet in height, well built though
somewhat spare. A broad forehead overhanging deeply set dark brown eyes
whose light shining from beneath strongly marked eye-brows told all the
changes of his moods, slightly prominent cheek-bones, a pale skin, at times
inclined to be even sallow, dark brown hair, allowed to grow on the face
only as a small moustache, and slight whiskers, made up a countenance which
bespoke at once strength of character and delicacy of constitution. It was
an open countenance, hiding nothing, giving sign at once, both when his
body was weary or weak, and when his mind was gladdened, angered or
annoyed.
The record of some of his thoughts and work, all that he had given to the
world will be found in the following pages. But who can tell the ideas
which had passed into his quick brain, but which as yet were known only to
himself, of which he had given no sign up to that sad day on which he made
the fatal climb? And who can say whither he might not have reached had he
lived, and his bright young life ripened as years went on? This is not the
place to attempt any judgment of his work: that may be left to other times,
and to other hands; but it may be fitting to place here on record a letter
which shews how much the greatest naturalist of this age appreciated his
younger brother. Among Balfour's papers was found a letter from Charles
Darwin, acknowledging the receipt of Vol. II. of the _Comparative
Embryology_ in the following words:
"_July 6, 1881._
DOWN, BECKENHAM, KENT.
MY DEAR BALFOUR,
I thank you heartily for the present of your grand book, and
I congratulate you on its completion. Although I read almost
all of Vol. I, I do not feel that I am worthy of your
present, unless indeed the fullest conviction that it is a
memorable work makes me worthy to receive it.
* * * * *
Once again accept my thanks, for I am proud to receive a
book from you, who, I know, will some day be the chief of
the English Biologists.
Believe me,
Yours sincerely,
CHARLES DARWIN."
The loss of him was a manifold loss. He is mourned, and will long be
mourned, for many reasons. Some miss only the brilliant investigator;
others feel that their powerful and sympathetic teacher is gone; some look
back on his memory and grieve for the charming companion whose kindly
courtesy and bright wit made the hours fly swiftly and pleasantly along;
and to yet others is left an aching void when they remember that they can
never again lean on the friend whose judgment seemed never to fail and
whose warm-hearted affection was a constant help. And to some he was all of
these. At the news of his death the same lines came to the lips of all of
us, so fittingly did Milton's words seem to speak our loss and grief--
"For Lycidas is dead, dead ere his prime,
Young Lycidas, and hath not left his peer."
M. FOSTER.
I. ON SOME POINTS IN THE GEOLOGY OF THE EAST LOTHIAN COAST[3].
Footnote 3: From the _Geological Magazine_, Vol. IX. No. 4.
April, 1872.
By G. W. and F. M. BALFOUR, Trinity College, Cambridge.
The interesting relation between the Porphyrite of Whitberry Point, at the
mouth of the Tyne, near Dunbar, and the adjacent sedimentary rocks, was
first noticed, we believe, by Professor Geikie, who speaks of it in the
_Memoirs of the Geological Survey of East Lothian_, pages 40 and 31, and
again in the new edition of Jukes's _Geology_, p. 269. The volcanic mass
which forms the point consists of a dark felspathic base with numerous
crystals of augite: it is circular in form, and is exposed for two-thirds
of its circumference in a vertical precipice facing the sea, about twenty
feet in height.
The rock is traversed by numerous joints running both in a horizontal and
in a vertical direction. The latter are by far the most conspicuous, and
give the face of the cliff, when seen from a distance, a well-marked
columnar appearance, though the columns themselves are not very distinct or
regular. They are quadrangular in form, and are evidently produced by the
intersection at right-angles of the two series of vertical joints.
It is clear that the face of the precipice has been gradually receding in
proportion as it yielded to the action of the waves; and that at a former
period the volcanic rock extended considerably further than at present over
the beds which are seen to dip beneath it. These latter consist of hard
fine-grained calcareous sandstones belonging to the Lower Carboniferous
formation. Their colour varies from red to white, and their prevailing dip
is in a N.W. direction, with an average inclination of 12-20°. If the
volcanic mass is a true intrusive rock, we should naturally expect the
strata which surround it to dip _away_ in all directions, the amount of
their inclination diminishing in proportion to their distance from it. We
find, however, that the case is precisely the reverse: as the beds approach
the base of the cliff, they dip _towards_ it from every side at perpetually
increasing angles, until at the point of junction the inclination amounts
in places to as much as 55 degrees. The exact amount of dip in the various
positions will be seen on referring to the accompanying map.
[Illustration: FIG. 1. MAP OF STRATA AT WHITBERRY POINT. Scale, 6 in. to
the mile.
_A._ Lava sheet. _B._ Sandstone Beds, dipping from every side towards the
lava. _CC._ Line of Section along which Fig. 2 is supposed to be drawn.]
We conceive that the phenomenon is to be explained by supposing the orifice
through which the lava rose and overflowed the surface of the sedimentary
strata to have been very much smaller in area than the extent of igneous
rock at present visible; and that the pressure of the erupted mass on the
soft beds beneath, aided perhaps by the abstraction of matter from below,
caused them to incline towards the central point at a gradually increasing
angle. The diagram, fig. 2, will serve further to illustrate this
hypothesis. _A_ is the neck or orifice by which the melted matter is
supposed to ascend. _C_ shews the sheet of lava after it has overspread the
surface of the sandstone beds _B_, so as to cause them to assume their
present inclination. The dotted lines represent the hypothetical extension
of the igneous mass and sandstones previous to the denudation which they
have suffered from the action of the waves.
Professor Geikie, in his admirable treatise on the Geology of the
county[4], adopts a view on this subject which is somewhat different from
that which is suggested in this paper. He considers that the whole mass is
an intrusive neck of rock with perpendicular sides; and that it once filled
up an orifice through the surrounding sedimentary strata, of which it is
now the only remnant.
Footnote 4: _Memoirs of Geological Survey of Scotland_, sheet
33, pp. 40, 41.
[Illustration: FIG. 2. VERTICAL SECTION THROUGH CC. DIAGRAM (FIG. 1).
_A._ Orifice by which the lava ascended. _B._ Sandstone Beds. _B´._
Hypothetical extension of ditto. _C._ Sheet of lava spread over the
sandstones _B_. _C´_. Hypothetical extension of ditto.]
He admits that the inclination of the sandstone beds towards the igneous
mass in the centre is a phenomenon that is somewhat difficult to explain,
and suggests that a subsequent contraction of the column may have tended to
produce such a result. To use his own words: "In the case of a solid column
of felstone or basalt, the contraction of the melted mass on cooling may
have had some effect in dragging down the sides of the orifice[5]."
Footnote 5: Note on p. 41 of _Mem. Geol. Survey of East
Lothian_.
But, apart from other objections, it is scarcely conceivable that this
result should have been produced by the contraction of the column.
In his recent edition of Jukes's _Manual of Geology_ (p. 269), in which he
also refers to this instance, he states that in other cases of "necks" it
is found to be an almost invariable rule, "that strata are bent down so as
to dip into the neck all round its margin." We are not aware to what other
instances Prof. Geikie may allude; but on referring to his _Memoir on the
Geology of East Lothian_, we find that he states in the cases of 'North
Berwick Law' and 'Traprain' (which he compares with the igneous mass at
Whitberry Point), that the beds at the base of these two necks, where
exposed, dip _away_ from them, and that at a high angle.
In support of the hypothesis which we have put forward, the following
arguments may be urged:
(1) That in one place at least the sedimentary strata are seen to be
actually dipping beneath the superincumbent basalt; and that the impression
produced by the general relation of the two rocks is, that they do so
everywhere.
(2) Since the columns into which the lava is split are vertical, the
cooling surface must have been horizontal: the mass must, therefore, have
formed a sheet, and not a dyke; for, in the latter case, the cooling
surfaces would have been vertical.
(3) It is difficult to conceive, on the supposition that the volcanic rock
is a neck with perpendicular sides, that the marine denudation should have
uniformly proceeded only so far as to lay bare the junction between the two
formations. We should have expected that in many places the igneous rock
itself would have been cut down to the general level, whereas the only
signs of such an effect are shown in a few narrow inlets where the rock was
manifestly softer than in the surrounding parts.
The last objection is greatly confirmed by the overhanging cliffs and
numerous blocks of porphyrite which lie scattered on the beach, as if to
attest the former extension of that ancient sheet of which these blocks now
form but a small remnant. Indeed, the existence of such remains appears
sufficient of itself to condemn any hypothesis which presumes the present
face of the cliff to have formed the original boundary of the mass.
It may be fairly objected to our theory, as Prof. Geikie himself has
suggested, that the high angle at which the strata dip is difficult to
account for. But, in fact, this steep inclination constitutes the very
difficulty which any hypothesis on the subject must be framed to explain;
and it is a difficulty which is not more easily solved by Prof. Geikie's
theory than by our own.
II. THE DEVELOPMENT AND GROWTH OF THE LAYERS OF THE BLASTODERM[6].
Footnote 6: From the _Quarterly Journal of Microscopical
Science_, Vol. XIII., 1873.
With Plate 1, figs. 1-5 and 9-12.
The following paper deals with the changes which take place in the cells of
the blastoderm of the hen's egg during the first thirty or forty hours of
incubation. The subject is one which has, as a general rule, not been much
followed up by embryologists, but is nevertheless of the greatest interest,
both in reference to embryology itself, and to the growth and changes of
protoplasm exhibited in simple embryonic cells. I am far from having
exhausted the subject in this paper, and in some cases I shall be able
merely to state facts, without being able to give any explanation of their
meaning.
My method of investigation has been the examination of sections and surface
views. For hardening the blastoderm I have employed, as usual, chromic
acid, and also gold chloride. It is, however, difficult to make sections of
blastoderms hardened by this latter reagent, and the sections when made are
not in all cases satisfactory. For surface views I have chiefly used silver
nitrate, which brings out the outlines of the cells in a manner which
leaves nothing to be desired as to clearness. If the outlines only of the
cells are to be examined, a very short immersion (half a minute) of the
blastoderm in a half per cent. solution of silver nitrate is sufficient,
but if the immersion lasts for a longer period the nuclei will be brought
out also. For studying the latter, however, I have found it better to
employ gold chloride or carmine in conjunction with the silver nitrate.
My observations begin with the blastoderm of a freshly laid egg. The
appearances presented by sections of this have been accurately described by
Peremeschko, "Ueber die Bildung der Keimblätter im Hühnerei,"
_Sitzungsberichte der K. Akademie der Wissenschaften in Wien_, 1868.
Oellacher, "Untersuchung über die Furchung und Blatterbildung im Hühnerei,"
_Studien aus dem Institut für Experim. Pathologie in Wien_, 1870 (pp.
54-74), and Dr Klein, lxiii. Bande der _Sitz. der K. Acadamie der Wiss. in
Wien_, 1871.
The unincubated blastoderm (Pl. 1, fig. 1) consists of two layers. The
upper layer is composed of a single row of columnar cells. Occasionally,
however, the layer may be two cells thick. The cells are filled with highly
refracting spherules of a very small size, and similar in appearance to the
finest white yolk spherules, and each cell also contains a distinct oval
nucleus. This membrane rests with its extreme edge on the white yolk, its
central portion covering in the segmentation cavity. From the very first it
is a distinct coherent membrane, and exhibits with silver nitrate a
beautiful hexagonal mosaic of the outlines (Pl. 1, fig. 6) of the cells.
The diameter of the cells when viewed from above is from 1/2000 - 1/3000 of
an inch. The under layer is very different from this: it is composed of
cells which are slightly, if at all, united, and which vary in size and
appearance, and in which a nucleus can rarely be seen. The cells of which
it is composed fill up irregularly the segmentation cavity, though a
distinct space is even at this time occasionally to be found at the bottom
of it. Later, when the blastoderm has spread and the white yolk floor has
been used as food, a considerable space filled with fluid may generally be
found.
The shape of the floor of the cavity varies considerably, but it is usually
raised in the middle and depressed near the circumference. In this case the
under layer is perhaps only two cells deep at the centre and three or four
cells deep near the circumference.
The cells of which this layer is composed vary a good deal in size; the
larger cells being, however, more numerous in the lower layers. In
addition, there are usually a few very large cells quite at the bottom of
the cavity, occasionally separated from the other cells by fluid. They were
called _formative cells_ (Bildungselemente) by Peremeschko (_loc. cit._);
and, according to Oellacher's observations (_loc. cit._), some of them, at
any rate, fall to the bottom of the segmentation cavity during the later
stages of segmentation. They do not differ from the general lower layer
cells except in size, and even pass into them by insensible gradations. All
the cells of the lower layer are granular, and are filled with highly
refracting spherules precisely similar to the smaller white yolk spherules
which line the bottom of the segmentation cavity.
The size of the ordinary cells of the lower layer varies from 1/2000 -
1/1000 of an inch. The largest of the formative cells come up to 1/300 of
an inch. It will be seen from this description that, morphologically
speaking, we cannot attach much importance to the formative cells. The fact
that they broke off from the blastoderm, towards the end of the
segmentation--even if we accept it as a normal occurrence, rather than the
result of manipulation--is not of much importance, and, except in size, it
is impossible to distinguish these cells from other cells of the lower
layer of the blastoderm.
Physiologically, however, as will be afterwards shewn, they are of
considerable importance.
The changes which the blastoderm undergoes during the first three or four
hours of incubation are not very noticeable. At about the sixth or eighth
hour, or in some cases considerably earlier, changes begin to take place
very rapidly. These changes result in the formation of a hypoblast and
mesoblast, the upper layer of cells remaining comparatively unaltered as
the epiblast.
To form the hypoblast a certain number of the cells of the lower layer
begin to undergo remarkable changes. From being spherical and, as far as
can be seen, non-nucleated, they become (vide fig. 2, _h_) flattened and
nucleated, still remaining granular, but with fewer spherules.
Here, then, is a direct change, of which all the stages can be followed, of
a cell of one kind into a cell of a totally different character. The new
cell is not formed by a destruction of the old one, but directly from it by
a process of metamorphosis. These hypoblast cells are formed first at the
centre and later at the circumference, so that from the first the cells at
the circumference are less flattened and more granular than the cells at
the centre. A number of cells of the original lower layer are enclosed
between this layer and the epiblast; and, in addition to these, the
formative cells (as has been shewn by Peremeschko, Oellacher, and Klein,
whose observations I can confirm) begin to travel towards the
circumference, and to pass in between the epiblast and hypoblast.
Both the formative cells, and the lower layer cells enclosed between the
hypoblast and epiblast, contribute towards the mesoblast, but the mode in
which the mesoblast is formed is very different from that in which the
hypoblast originates.
It is in this difference of formation that the true distinction between the
mesoblast and hypoblast is to be looked for, rather than in the original
difference of the cells from which they are derived.
The cells of the mesoblast are formed by a process which seems to be a kind
of free cell formation. The whole of the interior of each of the formative
cells, and of the other cells which are enclosed between the epiblast and
the hypoblast, become converted into new cells. These are the cells of the
mesoblast. I have not been able perfectly to satisfy myself as to the exact
manner in which this takes place, but I am inclined to think that some or
all of the spherules which are contained in the original cells develop into
nuclei for the new cells, the protoplasm of the new cells being formed from
that of the original cells.
The stages of formation of the mesoblast cells are shewn in the section
(Pl. 1, fig. 2), taken from the periphery of a blastoderm of eight hours.
The first formation of the mesoblast cells takes place in the centre of the
blastoderm, and the mass of cells so formed produces the opaque line known
as the primitive streak. This is shown in Pl. 1, fig. 9.
One statement I have made in the above description in reference to the
origin of the mesoblast cells, viz. that they are only partly derived from
the formative cells at the bottom of the segmentation cavity, is to a
certain extent opposed to the statements of the three investigators above
mentioned. They state that the mesoblast is entirely derived from the
formative cells. It is not a point to which I attach much importance,
considering that I can detect no difference between these cells and any
other cells of the original lower layer except that of size; and even this
difference is probably to be explained by their proximity to the white
yolk, whose spherules they absorb. But my reason for thinking it probable
that these cells alone do not form the mesoblast are: 1st. That the
mesoblast and hypoblast are formed nearly synchronously, and except at the
centre a fairly even sprinkling of lower layer cells is from the first to
be distinguished between the epiblast and hypoblast. 2nd. That if some of
the lower layer cells are not converted into mesoblast, it is difficult to
see what becomes of them, since they appear to be too numerous to be
converted into the hypoblast alone. 3rd. That the chief formation of
mesoblast at first takes place in the centre, while if the formative cells
alone took part in its formation, it would be natural to expect that it
would begin to be formed at the periphery.
Oellacher himself has shewn (_Zeitschrift für wissenschaftliche Zoologie_,
1873, "Beiträge zur Entwick. Gesch. der Knochenfische") that in osseous
fishes the cells which break away from the blastoderm take no share in the
formation of the mesoblast, so that we can derive no argument from the
formation of the mesoblast in these animals, for believing that in the
chick it is derived only from the formative cells.
In the later stages, however, from the twelfth to the twenty-fifth hour,
the growth of the mesoblast depends almost entirely on these cells, and
Peremeschko's discovery of the fact is of great value.
Waldeyer (_Henle und v. Pfeufer's Zeitschrift_, xxxiv. Band, für 1869) has
given a different account of the origin of the layers. There is no doubt,
however, in opposition to his statements and drawings, that from the very
first the hypoblast is distinct from the mesoblast, which is, indeed, most
conspicuously shewn in good sections; and his drawings of the derivation of
the mesoblast from the epiblast are not very correct.
The changes which have been described are also clearly shewn by means of
silver nitrate. Whereas, at first this reagent brought out no outline
markings of cells in the lower layer, by the eighth to the twelfth hour the
markings (Pl. 1, fig. 3) are very plain, and shew that the hypoblast is a
distinct coherent membrane.
In section, the cells of the hypoblast appear generally very thin and
spindle shaped, but the outlines brought out by the silver nitrate shew
that they are much expanded horizontally, but very irregular as to size,
varying even within a small area from 1/4000 - 1/400 of an inch in the
longest diameter.
At about the twelfth hour they are uniformly smaller a short way from each
extremity of its longer axis than over the rest of the blastoderm.
It is, perhaps, fair to conclude from this that growth is most rapid at
these parts.
At this time the hypoblast, both in sections and from a surface view after
treatment with silver nitrate, appears to end abruptly against the white
yolk. The surface view also shews that its cells are still filled with
highly refractive globules, making it difficult to see the nucleus. In some
cases I thought that I could (fig. 3, _a_) make out that it was hour-glass
shaped, and some cells certainly contain two nuclei. Some of the cells
(fig. 3, _b_) shew re-entrant curves, which prove that they have undergone
division.
The cells of the epiblast, up to the thirteenth hour, have chiefly
undergone change in becoming smaller.
In surface views they are about 1/4000 of an inch in diameter over the
centre of the pellucid area, and increase to 1/2000 of an inch over the
opaque area.
In the centre of the pellucid area the form of the epiblast cells is more
elongated vertically and over the opaque area more flattened than was the
case with the original upper layer cells. In the centre the epiblast is two
or three cells deep.
Before going on to the further changes of the blastodermic cells it will be
well to say a few words in reference to the origin of the mesoblast.
From the description given above it will be clear that in the chick the
mesoblast has an independent origin; it can be said neither to originate
from the epiblast nor from the hypoblast. It is formed coincidently with
the latter out of apparently similar segmentation cells. The hypoblast, as
has been long known, shews in the chick no trace of its primitive method of
formation by involution, neither does the mesoblast shew any signs of its
primitive mode of formation. In so excessively highly differentiated a type
as birds we could hardly expect to find, and certainly do not find, any
traces of the primitive origin of the mesoblast, either from the epiblast
or hypoblast, or from both. In the chick the mesoblast cells are formed
directly from the ultimate products of segmentation. From having a
secondary origin in most invertebrates the mesoblast comes to have, in the
chick, a primary origin from the segmentation spheres, precisely as we find
to be the case with the nervous layer in osseous fishes. It is true we
cannot tell which segmentation-cells will form the mesoblast, and which the
hypoblast; but the mesoblast and hypoblast are formed at the same time, and
both of them directly from segmentation spheres.
The process of formation of the mesoblast in Loligo, as observed by Mr Ray
Lankester (_Annals and Magazine of Natural History_, February, 1873), is
still more modified. Here the mesoblast arises independently of the
blastoderm, and by a process of free cell-formation in the yolk round the
edge of the blastoderm. If Oellacher's observations in reference to the
origin of formative cells are correct, then the modes of origin of the
mesoblast in Loligo and the chick would have nothing in common; but if the
formative cells are in reality derived from the white yolk, and also are
alone concerned in the formation of the mesoblast, then the modes of
formation of the mesoblast in the chick would be substantially the same as
that observed by Mr Ray Lankester in Loligo.
No very important changes take place in the actual forms of the cells
during the next few hours. A kind of fusion takes place between the
epiblast and the mesoblast along the line of the primitive streak forming
the axis-string of His; but the line of junction between the layers is
almost always more or less visible in sections. In any case it does not
appear that there is any derivation of mesoblast cells from the epiblast;
and since the fusion only takes place in the region of the primitive
groove, and not in front, where the medullary groove arises (see succeeding
paper), it cannot be considered of any importance in reference to the
possible origin of the Wolffian duct, &c., from the epiblast (as mooted by
Waldeyer, _Eierstock und Ei_, Leipzig, 1870). The primitive groove, as can
be seen in sections, begins to appear very early, generally before the
twelfth hour. The epiblast spreads rapidly over the white yolk, and the
area pellucida also increases in size.
From the mesoblast forming at first only a small mass of cells, which lies
below the primitive streak, it soon comes to be the most important layer of
the blastoderm. Its growth is effected by means of the formative cells.
These cells are generally not very numerous in an unincubated blastoderm,
but rapidly increase in numbers, probably by division; at the same time
they travel round the edge of, and in some cases through, the hypoblast,
and then become converted in the manner described into mesoblast cells.
They act as carriers of food from the white yolk to the mesoblast till,
after the formation of the vascular area, they are no longer necessary. The
numerous cases in which two nucleoli and even two nuclei can be seen in one
cell prove that the mesoblast cells also increase by division.
The growth of the hypoblast takes place in a very different way. It occurs
by a direct conversion, cell for cell, of the white yolk spheres into
hypoblast cells. This interpretation of the appearances, which I will
describe presently, was first suggested to me by Dr Foster, from an
examination of some of my specimens of about thirty-six hours, prepared
with silver nitrate. Where there is no folding at the junction between the
pellucid and opaque areas, there seems to be a perfect continuity in the
silver markings and a gradual transition in the cells, from what would be
undoubtedly called white yolk spheres, to as undoubted hypoblast cells
(vide Pl. 1, fig. 5). In passing from the opaque to the pellucid areas the
number of white yolk spherules in each cell becomes less, but it is not
till some way into the pellucid area that they quite cease to be present. I
at first thought that this was merely due to the hypoblast cells feeding on
the white yolk sphericles, but the perfect continuity of the cells, and the
perfect gradation in passing from the white yolk cells to the hypoblast,
proves that the other interpretation is the correct one, viz. that the
white yolk spheres become directly converted into the hypoblast cells. This
is well shewn in sections (vide Pl. 1, fig. 4) taken from embryos of all
ages from the fifteenth to the thirty-sixth hour and onwards. But it is,
perhaps, most easily seen in embryos of about twenty hours. In such an
embryo there is a most perfect gradation: the cells of the hypoblast
become, as they approach the edge of the pellucid area, broader, and are
more and more filled with white yolk sphericles, till at the line of
junction it is quite impossible to say whether a particular cell is a
white-yolk cell (sphere) or a hypoblast cell. The white-yolk cells near the
line of junction can frequently be seen to possess nuclei. At first the
hypoblast appears to end abruptly against the white yolk; this state of
things, however, soon ends, and there supervenes a complete and unbroken
continuity between the hypoblast and the white yolk.
Of the mode of increase of the epiblast I have but little to say. The cells
undoubtedly increase entirely by division, and the new material is most
probably derived directly from the white yolk.
Up to the sixth hour the cells of the upper layer retain their early
regular hexagonal pattern, but by the twelfth hour they have generally
entirely lost this, and are irregularly shaped and very angular. The cells
over the centre of the pellucid area remain the smallest up to the
twenty-fifth hour or later, while those over the rest of the pellucid area
are uniformly larger.
In the hypoblast the cells under the primitive groove, and on each side as
far as the fold which marks off the exterior limit of the protovertebræ are
at the eighteenth hour considerably smaller than any other cells of this
layer.
In all the embryos between the eighteenth and twenty-third hour which I
have examined for the purpose, I have found that at about two-thirds of the
distance from the anterior end of the pellucid area, and just external to
the side fold, there is a small space on each side in which the cells are
considerably larger than anywhere else in the hypoblast. These larger
cells, moreover, contain a greater number of highly refractive spherules
than any other cells. It is not easy to understand why growth should have
been less rapid here than elsewhere, as the position does not seem to
correspond to any feature in the embryo. In some specimens the hypoblast
cells at the extreme edge of the pellucid area are smaller than the cells
immediately internal to them. At about the twenty-third hour these cells
begin rapidly to lose the refractive spherules they contained in the
earlier stages of incubation, and come to consist of a nucleus surrounded
simply by granular protoplasm.
At about this period of incubation the formative cells are especially
numerous at the periphery of the blastoderm, and, no doubt, become
converted into the mass of mesoblast which is found at about the
twenty-fifth hour in the region of the vascular area. Some of them are
lobate, and appear as if they were undergoing division. At this time also
the greatest number of formative cells are to be found at the bottom of the
now large segmentation cavity.
In embryos of from thirty to forty hours the cells of the hypoblast have,
over the central portion of the pellucid area, entirely lost their highly
refractive spherules, and in the fresh state are composed of the most
transparent protoplasm. When treated with reagents they are found to
contain an oval nucleus with one or sometimes two nucleoli, imbedded in a
considerable mass of protoplasm. The protoplasm appears slightly granular
and generally contains one or two small vacuoles. I have already spoken of
the gradation of the hypoblast at the edge of the blastoderm into white
yolk. I have, therefore, only to mention the variations in the size of its
cells in different parts of the pellucid area. The points where the cells
are smallest seem generally to coincide with the points of maximum growth.
Over the embryo the cells are more regular than elsewhere. They are
elongated and arranged transversely to the long axis of the embryo. They
are somewhat hexagonal in shape, and not unlike the longer pieces in the
dental plate of a Myliobatis (Pl. 1, fig. 10). This regularity, however, is
much more marked in some specimens than in others. These cells are about
1/4000th of an inch in breadth, and 1/1000th in length. On each side of the
embryo immediately external to the protovertebræ the cells are frequently
about the same size as those over the embryo itself. In the neck, however,
and near the end of the sinus rhomboidalis, they are considerably smaller,
about 1/4000th inch each way. The reason of this small size is not very
clear, but probably shews that the greatest growth is taking place at these
two points. The cells, again, are very small at the head fold, but are very
much larger in front of this--larger, in fact, than any other cells of the
hypoblast. Outside the embryo they gradually increase in size towards the
edge of the pellucid area. Here they are about 1/1000th of an inch in
diameter, irregular in shape and rather angular.
The outlines of the cells of the epiblast at this time are easily
distinguished from the cells of the hypoblast by being more elongated and
angular; they are further distinguished by the presence of numerous small
oval cells, frequently at the meeting point of several cells, at other
times at points along the lines of junction of two cells (Pl. 1, fig. 12).
These small cells look very like the smaller stomata of endothelial
membranes, but are shewn to be cells by possessing a nucleus. There is
considerable variation in size in the cells in different parts of the
epiblast. Between the front lobes of the brain the cells are very small,
1/4000th inch, rising to 1/2000th on each side. They are about the latter
size over the greater part of the embryo. But over the sinus rhomboidalis
they fall again to from 1/3000th to 1/4000th inch. This is probably to be
explained by the growth of the medullary fold at this point, which pushes
back the primitive groove. At the sides of the head the cells are larger
than anywhere else in the epiblast, being here about 1/1000th inch in
diameter. I at present see no explanation of this fact. At the periphery of
the pellucid area and over the vascular area the cells are 1/1500th to
1/2000th inch in diameter, but at the periphery of the opaque area they are
smaller again, being about the 1/3000th of an inch. This smaller size at
the periphery of the area opaca is remarkable, since in the earlier stages
the most peripheral epiblast cells were the largest. It, perhaps, implies
that more rapid growth is at this time taking place in that part of the
epiblast which is spreading over the yolk sac.
EXPLANATION OF PLATE 1, Figs. 1-5 and 9-12.
Fig. 1. Section through an unincubated blastoderm, shewing the upper layer,
composed of a single row of columnar cells, and the lower layer, composed
of several rows of rounded cells in which no nucleus is visible. Some of
the "formative cells," at the bottom of the segmentation cavity, are seen
at (_b_).
Fig. 2. Section through the periphery of an eight hours' blastoderm,
shewing the epiblast (_p_), the hypoblast (_h_), and the mesoblast
commencing to be formed (_c_), partly by lower-layer cells enclosed between
the epiblast and hypoblast, and partly by formative cells. Formative cells
at the bottom of the segmentation cavity are seen at _b_. At _s_ is one of
the side folds parallel to the primitive groove.
Fig. 3. Portion of the hypoblast of a thirteen hours' blastoderm, treated
with silver nitrate, shewing the great variation in the size of the cells
at this period. An hour-glass shaped nucleus is seen at _a_.
Fig. 4. Periphery of a twenty-three hours' blastoderm, shewing cell for
cell the junction between the hypoblast (_h_) and white-yolk spheres (_w_).
Fig. 5. Junction between the white-yolk spheres and the hypoblast cells at
the passage from the area pellucida to the area opaca. The specimen was
treated with silver nitrate to bring out the shape of the cells. The line
of junction between the opaque and pellucid areas passes diagonally.
Fig. 9. Section through the primitive streak of an eight hours' blastoderm.
The specimen shews the mesoblast very much thickened in the immediate
neighbourhood of the primitive streak, but hardly formed at all on each
side of the streak. It also shews the primitive groove just beginning to be
formed (_pr_), and the fusion between the epiblast and the mesoblast under
the primitive groove. The hypoblast is completely formed in the central
part of the blastoderm. At _f_ is seen one of the side folds parallel to
the primitive groove. Its depth has been increased by the action of the
chromic acid.
Fig. 10. Hypoblast cells from the hinder end of a thirty-six hours' embryo,
treated with silver nitrate, shewing the regularity and elongated shape of
the cells over the embryo and the smaller cells on each side.
Fig. 11. Epiblast cells from an unincubated blastoderm, treated with silver
nitrate, shewing the regular hexagonal shape of the cells and the small
spherules they contain.
Fig. 12. Portion of the epiblast of a thirty-six hours' embryo, treated
with silver nitrate, shewing the small rounded cells frequently found at
the meeting-points of several larger cells which are characteristic of the
upper layer.
III. ON THE DISAPPEARANCE OF THE PRIMITIVE GROOVE IN THE EMBRYO CHICK[7].
Footnote 7: From the _Quarterly Journal of Microscopical
Science_, Vol. XIII, 1873.
With Plate 1, Figs. 6-8 and 13-19.
The investigations of Dursy (_Der Primitivstreif des Hühnchens_, von Dr E.
Dursy. Lahr, 1866) on the primitive groove, shewing that it is a temporary
structure, and not connected with the development of the neural canal, have
in this country either been ignored or rejected. They are, nevertheless,
perfectly accurate; and had Dursy made use of sections to support his
statements I do not think they would so long have been denied. In Germany,
it is true, Waldeyer has accepted them with a few modifications, but I have
never seen them even alluded to in any English work. The observations which
I have made corroborating Dr Dursy may, perhaps, under these circumstances
be worth recording.
After about twelve hours of incubation the pellucid area of a hen's egg has
become somewhat oval, with its longer axis at right angles to the long axis
of the egg. Rather towards the hinder (narrower) end of this an opaque
streak has appeared, with a somewhat lighter line in the centre. A section
made at the time shews that the opaque streak is due partly to a thickening
of the epiblast, but more especially to a large collection of the rounded
mesoblast cells, which along this opaque line form a thick mass between the
epiblast and the hypoblast. The mesoblast cells are in contact with both
hypoblast and epiblast, and appear to be fused with the latter. The line of
junction between them can, however, almost always be made out.
Soon after the formation of this primitive streak a groove is formed along
its central line by a pushing inwards of the epiblast. The epiblast is not
thinner where it lines the groove, but the mass of mesoblast below the
groove is considerably thinner than at its two sides. This it is which
produces the peculiar appearance of the primitive groove when the
blastoderm is viewed by transmitted light as a transparent line in the
middle of an opaque one.
This groove, as I said above, is placed at right angles to the long axis of
the egg, and nearer the hind end, that is, the narrower end of the pellucid
area. It was called "the primitive groove" by the early embryologists, and
they supposed that the neural canal arose from the closure of its edges
above. It is always easy to distinguish this groove, in transverse
sections, by several well-marked characters. In the first place, the
epiblast and mesoblast always appear more or less fused together underneath
it; in the second place, the epiblast does not become thinner where it
lines the groove; and in the third place, the mesoblast beneath it never
shews any signs of being differentiated into any organ.
As Dursy has pointed out, there is frequently to be seen in fresh
specimens, examined as transparent objects, a narrow opaque line running
down the centre of this groove. I do not know what this line is caused by,
as there does not appear to be any structural feature visible in sections
to which it can correspond.
From the twelfth to the sixteenth hour the primitive groove grows rapidly,
and by the sixteenth hour is both absolutely and considerably longer than
it was at the twelfth hour, and also proportionately longer as compared
with the length of the pellucid area.
There is a greater interval between its end and that of the pellucid area
in front than behind.
At about the sixteenth hour, or a little later, a thickening of the
mesoblast takes place in front of the primitive groove, forming an opaque
streak, which in fresh specimens looks like a continuation from the
anterior extremity of the primitive groove (vide Pl. 1, fig. 8). From
hardened specimens, however, it is easy to see that the connection of this
streak with the primitive groove is only an apparent one. Again, it is
generally possible to see that in the central line of this streak there is
a narrow groove. I do not feel certain that there is no period when this
groove may not be present, but its very early appearance has not been
recognized either by Dursy or by Waldeyer. Moreover, both these authors, as
also His, seem to have mistaken the opaque streak spoken of above for the
notochord. This, however, is not the case, and the notochord does not make
its appearance till somewhat later. The mistake is of very minor
importance, and probably arose in Dursy's case from his not sufficiently
making use of sections. At about the time the streak in front of the
primitive groove makes its appearance a semicircular fold begins to be
formed near the anterior extremity of the pellucid area, against which the
opaque streak, or as it had, perhaps, better be called, "the medullary
streak," ends abruptly.
This fold is the head fold, and the groove along the medullary streak is
the medullary groove, which subsequently forms the cavity of the medullary
or neural canal.
Everything which I have described above can without difficulty be made out
from the examination of fresh and hardened specimens under the simple
microscope; but sections bring out still more clearly these points, and
also shew other features which could not have been brought to light without
their aid. In Pl. 1, figs. 6 and 7, two sections of an embryo of about
eighteen hours are shewn. The first of these passes through the medullary
groove, and the second of them through the extreme anterior end of the
primitive groove. The points of difference in the two sections are very
obvious.
From fig. 6 it is clear that a groove has already been formed in the
medullary streak, a fact which was not obvious in the fresh specimen. In
the second place the mesoblast is thickened both under the groove and also
more especially in the medullary folds at the sides of the groove; but
shews hardly a sign of the differentiation of the notochord. So that it is
clear that the medullary streak is not the notochord, as was thought to be
the case by the authors above mentioned. In the third place there is no
adhesion between the epiblast and the mesoblast. In all the sections I have
cut through the medullary groove I have found this feature to be constant;
while (for instance, as in Pl. 1, figs. 7, 9, 17) all sections through the
primitive groove shew most clearly an adhesion between the epiblast and
mesoblast. This fact is both strongly confirmatory of the separate origins
of the medullary and primitive grooves, and is also important in itself, as
leaving no loophole for supposing that in the region of embryo there is any
separation of the cells from the epiblast to form the mesoblast.
By this time the primitive groove has attained its maximum growth, and from
this time begins both absolutely to become smaller, and also gradually to
be pushed more and more backwards by the growth of the medullary groove.
The specimen figured in Pl. 1, fig. 18, magnified about ten diameters,
shews the appearance presented by an embryo of twenty-three hours. The
medullary groove (_mc_) has become much wider and deeper than it was in the
earlier stage; the medullary folds (_A_) are also broader and more
conspicuous. The medullary groove widens very much posteriorly, and also
the medullary folds separate far apart to enclose the anterior end of the
primitive groove (_pr_).
All this can easily be seen with a simple microscope, but the sections
taken from the specimen figured also fully bear out the interpretations
given above, and at the same time shew that the notochord has at this age
begun to appear. The sections marked 13-17 pass respectively through the
lines with corresponding numbers in fig. 18. Section 1 (fig. 13) passes
through the middle of the medullary canal.
In it the following points are to be noted. (1) That the epiblast becomes
very much thinner where it lines the medullary canal (_mc_), a feature
never found in the epiblast lining the primitive groove. (2) That the
mesoblast is very much thickened to form the medullary folds at _A_, _A_,
while there is no adherence between it and the epiblast, below the
primitive groove. (3) The notochord (_ch_) has begun to be formed, though
its separation from the rest of the mesoblast is not as yet very
distinct[8].
Footnote 8: In the figure the notochord has been made too
distinct.
In fig. 14 the medullary groove has become wider and the medullary folds
broader, the notochord has also become more expanded: the other features
are the same as in section 1. In the third section (fig. 15) the notochord
is still more expanded; the bottom of the now much expanded medullary
groove has become raised to form the ridge which separates the medullary
from the primitive groove. The medullary folds are also flatter and broader
than in the previous section. Section 4 (fig. 16) passes through the
anterior end of the primitive groove. Here the notochord is no longer
visible, and the adherence between the mesoblast and epiblast below the
primitive groove comes out in marked contrast with the entire separation of
the two layers in the previous sections.
The medullary folds (_A_) are still visible outside the raised edges of the
primitive groove, and are as distinctly as possible separate and
independent formations, having no connection with the folds of the
primitive groove. In the last section (fig. 17), which is taken some way
behind section 4, no trace of the medullary folds is any longer to be seen,
and the primitive groove has become deeper. This series of sections, taken
in conjunction with the specimen figured in fig. 18, must remove all
possible doubt as to the total and entire independence of the primitive and
medullary grooves. They arise in different parts of the blastoderm; the one
reaches its maximum growth before the other has commenced to be formed; and
finally, they are distinguished by almost every possible feature by which
two such grooves could be distinguished.
Soon after the formation of the notochord, the protovertebræ begin to be
formed along the sides of the medullary groove (Pl. 1, fig. 19, _pv_). Each
new protovertebra (of those which are formed from before backwards) arises
just in front of the anterior end of the primitive groove. As growth
continues, the primitive groove becomes pushed further and further back,
and becomes less and less conspicuous, till at about thirty-six hours only
a very small and curved remnant is to be seen behind the sinus
rhomboidalis; but even up to the forty-ninth Dursy has been able to
distinguish it at the hinder end of the embryo.
The primitive groove in the chick is, then, a structure which appears very
early, and soon disappears without entering directly into the formation of
any part of the future animal, and without, so far as I can see, any
function whatever. It is clear, therefore, that the primitive groove must
be the rudiment of some ancestral feature; but whether it is a rudiment of
some structure which is to be found in reptiles, or whether of some earlier
form, I am unable to decide. It is just possible that it is the last trace
of that involution of the epiblast by which the hypoblast is formed in most
of the lower animals. The fact that it is formed in the hinder part of the
pellucid area perhaps tells slightly in favour of this hypothesis, since
the point of involution of the epiblast not unfrequently corresponds with
the position of the anus.
EXPLANATION OF PLATE 1, Figs. 6-8 and 13-19.
Figs. 6 and 7 are sections through an embryo rather earlier than the one
drawn in fig. 8. Fig. 6 passes through the just commencing medullary groove
(_md_), which appears in fresh specimens, as in fig. 8, merely as an opaque
streak coming from the end of the primitive groove. The notochord is hardly
differentiated, but the _complete_ separation of mesoblast and hypoblast
under the primitive groove is clearly shewn. Fig. 7 passes through the
anterior end of the primitive groove (_pr_), and shews the fusion between
the mesoblast and epiblast, which is always to be found under the primitive
groove.
Fig. 8 is a view from above of a twenty hours' blastoderm, seen as a
transparent object. Primitive groove (_pr_). Medullary groove (_md_), which
passes off from the anterior end of the primitive groove, and is produced
by the thickening of the mesoblast. Head fold (_pf_).
Figs. 13-17 are sections through the blastoderm, drawn in fig. 18 through
the lines 1, 2, 3, 4, 5 respectively.
The first section (fig. 13) passes through the true medullary groove
(_mc_); the two medullary folds (_A_, _A_) are seen on each side with the
thickened mesoblast, and the mesoblast cells are beginning to form the
notochord (_nc_) under the medullary groove. There is no adherence between
the mesoblast cells and the epiblast under the medullary groove.
The second (fig. 14) section passes through the medullary groove where it
has become wider. Medullary folds, _A_, _A_; notochord, _ch_.
In the third section (fig. 15) the notochord (_ch_) is broader, and the
epiblast is raised in the centre, while the medullary folds are seen far
apart at _A_.
In section fig. 16 the medullary folds (_A_) are still to be seen enclosing
the anterior end of the primitive groove (_pr_). Where the primitive groove
appears there is a fusion of the epiblast and mesoblast, and no appearance
of the notochord.
In the last section, fig. 17, no trace is to be seen of the medullary
folds.
Figs. 18 and 19 are magnified views of two hardened blastoderms. Fig. 18 is
twenty-three hours old; fig. 19 twenty-five hours. They both shew how the
medullary canal arises entirely independently of the primitive groove and
in front of it, and also how the primitive groove gets pushed backwards by
the growth of the medullary groove. _pv_, Protovertebræ; other references
as above. Fig. 18 is the blastoderm from which sections figs. 13-17 were
cut.
IV. THE DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK[9].
Footnote 9: From the _Quarterly Journal of Microscopical
Science_, Vol. XIII, 1873.
With Plate 2.
The development of the first blood-vessels of the yolk-sac of the chick has
been investigated by a large number of observers, but with very discordant
results. A good historical _résumé_ of the subject will be found in a paper
of Dr Klein (liii. Band der _K. Akad. der Wissensch. Wien_), its last
investigator.
The subject is an important one in reference to the homologies of the
blood-vascular system of the vertebrata. As I shall shew in the sequel (and
on this point my observations agree with those of Dr Klein), the
blood-vessels of the chick do not arise as spaces or channels between the
cells of the mesoblast; on the contrary, they arise as a network formed by
the united processes of mesoblast-cells, and it is through these processes,
and not in the spaces between them, that the blood flows. It is, perhaps,
doubtful whether a system of vessels arising in this way can be considered
homologous with any vascular system which takes its origin from channels
hollowed out in between the cells of the mesoblast.
My own researches chiefly refer to the development of the blood-vessels in
the pellucid area. I have worked but very slightly at their development in
the vascular area; but, as far as my observations go, they tend to prove
that the mode of their origin is the same, both for the pellucid and the
vascular area.
The method which I have principally pursued has been to examine the
blastoderm from the under surface. It is very difficult to obtain exact
notions of the mode of development of the blood-vessels by means of
sections, though these come in as a valuable confirmation of the other
method.
For the purpose of examination I have employed (1) fresh specimens; (2)
specimens treated with spirit, and then mounted in glycerine; (3) specimens
treated with chloride of gold for about half a minute, and then mounted in
glycerine; and (4) specimens treated with osmic acid.
All these methods bring out the same appearances with varying clearness;
but the successful preparations made by means of the gold chloride are the
best, and bring out the appearances with the greatest distinctness.
The first traces of the blood-vessels which I have been able to distinguish
in the pellucid area are to be seen at about the thirtieth hour or slightly
earlier, at about the time when there are four to five protovertebræ on
each side.
Fig. 1 shews the appearance at this time. Immediately above the hypoblast
there are certain cells whose protoplasm sends out numerous processes.
These processes vary considerably in thickness and size, and quickly come
in contact with similar processes from other cells, and unite with them.
I have convinced myself, by the use of the hot stage, that these processes
continually undergo alteration, sometimes uniting with other processes,
sometimes becoming either more elongated and narrower or broader and
shorter. In this way a network of somewhat granular protoplasm is formed
with nuclei at the points from which the processes start.
From the first a difference may be observed in the character of this
network in different parts of the pellucid area. In the anterior part the
processes are less numerous and thicker, the nuclei fewer, and the meshes
larger; while in the posterior part the processes are generally very
numerous, and at first thin, the meshes small, and the nuclei more
frequent. As soon as this network commences to be formed the nuclei begin
to divide. I have watched this take place with the hot stage. It begins by
the elongation of the nucleus and division of the nucleolus, the parts of
which soon come to occupy the two ends of the nucleus. The nucleus becomes
still longer and then narrows in the centre and divides. By this means the
nuclei become much more numerous, and are found in almost all the larger
processes. Whether they are carried out into the processes by the movement
of the surrounding protoplasm, or whether they move through the protoplasm,
I have been unable to determine; the former view, however, seems to be the
most probable.
It is possible that some nuclei arise spontaneously in the protoplasm, but
I am much more inclined to think that they are all formed by the division
of pre-existing nuclei--a view favoured by the number of nuclei which are
seen to possess two nucleoli. Coincidently with the formation of the new
nuclei the protoplasm of the processes, as well as that surrounding the
nuclei at the starting-points of the processes, begins to increase in
quantity.
At these points the nuclei also increase more rapidly than elsewhere, but
at first the resulting nuclei seem to be all of the same kind.
In the anterior part of the pellucid area (fig. 4) the increase in the
number of nuclei and in the amount of protoplasm at the starting-points of
the protoplasm is not very great, but in the posterior part the increase in
the amount of the protoplasm at these points is very marked, and
coincidently the increase in number of the nuclei is also great. This is
shewn in figs. 2 and 3. These are both taken from the tail end of an embryo
of about thirty-three hours, with seven or eight protovertebræ. Fig. 3
shews the processes beginning to increase in thickness, and also the
protoplasm at the starting-points increasing in quantity; at the same time
the nuclei at these points are beginning to become more numerous. Fig. 3 is
taken from a slightly higher level, _i.e._ slightly nearer the epiblast. In
it the protoplasm is seen to have increased still more in quantity, and to
be filled with nuclei. These nuclei have begun to be slightly coloured, and
one of them is seen to possess two nucleoli.
Very soon after this a change in the nuclei begins to be observed, more
especially in the hinder part of the embryo. While before this time they
were generally elongated, some of them now become more nearly circular. In
addition to this, they begin to have a yellowish tinge, and the nuclei,
when treated with gold (for in the fresh condition it is not easy to see
them distinctly), have a more jagged and irregular appearance than the
nucleoli of the other nuclei.
This change takes place especially at the starting-points of the processes,
so that the appearance presented (fig. 5) is that of spherical masses of
yellowish nuclei connected with other similar spherical masses by
protoplasmic processes, in which nuclei of the original type are seen
imbedded. These masses are surrounded by a thin layer of protoplasm, at the
edge of which a normal nucleus may here and there be detected, as at
fig. 5, _a_ and _a´_, the latter possessing two nucleoli. Some of these
processes are still very delicate, and it is exceedingly probable that they
undergo further changes of position before the final capillary system is
formed.
These differentiated nuclei are the first stage in the formation of the
blood-corpuscles. From their mode of formation it is clear that the
blood-corpuscles of the Sauropsida are to be looked upon as nuclei
containing nucleoli, rather than as cells containing nuclei; indeed, they
seem to be merely ordinary nuclei with red colouring matter.
This would make them truly instead of only functionally homologous with the
red corpuscles of the Mammalia, and would well agree with the fact that the
red corpuscles of Mammalia, in their embryonic condition, possess what have
previously been called nuclei, but which might perhaps more properly be
called nucleoli.
In the anterior part of the blastoderm the processes, as I have stated, are
longer and thinner, and the spaces enclosed between them are larger. This
is clearly brought out in Pl. 2, fig. 4. But, besides these large spaces,
there are other smaller spaces, such as that at _v_. It is, on account of
the transparency of the protoplasm, very difficult to decide whether these
are vacuoles or simply spaces enclosed by the processes, but I am inclined
to think that they are merely spaces. The difficulty of exactly determining
this point is increased by the presence of numerous white-yolk spherules in
the hypoblast above, which considerably obscure the view. At about the same
time that the blood-corpuscles appear in the posterior end of the pellucid
area, or frequently a little later, they begin to be formed in the anterior
part also. The masses of them are, however, far smaller and far fewer than
in the posterior part of the embryo. It is at the tail end of the pellucid
area that the chief formation of blood-corpuscles takes place.
The part of the pellucid area intermediate in position between the anterior
and posterior ends of the embryo is likewise intermediate as regards the
number of corpuscles formed and the size of the spaces between the
processes; the spaces being here larger than at the posterior extremity,
but smaller than the spaces in front. Close to the sides of the embryo the
spaces are, however, smaller than in any other part of the pellucid area.
It is, however, in this part that the first formation of blood-corpuscles
takes place, and that the first complete capillaries are formed.
We have then somewhat round protoplasmic masses filled with
blood-corpuscles and connected by means of processes, a few of which may
begin to contain blood-corpuscles, but the majority of which only contain
ordinary nuclei. The next changes to be noticed take place in the nuclei
which were not converted into blood-corpuscles, but which were to be seen
in the protoplasm surrounding the corpuscles. They become more numerous and
smaller, and, uniting with the protoplasm in which they were imbedded,
become converted into flat cells (spindle-shaped in section), and in a
short time form an entire investment for the masses of blood-corpuscles.
The same change also occurs in the protoplasmic processes which connect the
masses of corpuscles. In the case of those processes which contain no
corpuscles the greater part of their protoplasm seems to be converted into
the protoplasm of the spindle-shaped cells. The nuclei arrange themselves
so as completely to surround the exterior of the protoplasmic processes. In
this way each process becomes converted into a hollow tube, completely
closed in by cells formed from the investment of the original nuclei by the
protoplasm which previously formed the solid processes. The remainder of
the protoplasm probably becomes fluid, and afterwards forms the plasma in
which the corpuscles float. While these changes are taking place the
formation of the blood-corpuscles does not stand still, and by the time a
system of vessels, enclosed by cellular walls, is formed out of the
protoplasmic network, a large number of the connecting processes in this
network have become filled with blood-corpuscles. The appearances presented
by the network at a slightly later stage than this is shewn in Pl. 2,
fig. 6, but in this figure all the processes are seen to be filled with
blood-corpuscles.
This investment of the masses of corpuscles by a cellular wall occurs much
earlier in some specimens than in others, both in relation to the time of
incubation and to the completion of the network. It is generally completed
in some parts by the time there are eight or nine protovertebræ, and is
almost always formed over a great part of the pellucid area by the
thirty-sixth hour. The formation of the corpuscles, as was pointed out
above, occurs earliest in the central part of the hour-glass shaped
pellucid area, and latest in its anterior part. In the hinder part of the
pellucid area the processes, as well as their enlarged starting-points,
become entirely filled with corpuscles; this, however, is by no means the
case in its anterior part. Here, although the corpuscles are undoubtedly
developed in parts as shewn in fig. 7, yet a large number of the processes
are entirely without them. Their development, moreover, is in many cases
very much later. When the development has reached the stage described, very
little is required to complete the capillary system. There are always, of
course, a certain number of the processes which end blindly, and others are
late in their development, and are not by this time opened; but, as a
general rule, when the cellular investment is formed for the masses of
corpuscles, there is completed an open network of tubes with cellular
walls, which are more or less filled with corpuscles. These become quickly
driven into the opaque area in which at that time more corpuscles may
almost always be seen than in the pellucid area.
By the formation of a network of this kind it is clear that there must
result spaces enclosed between the walls of the capillaries; these spaces
have under the microscope somewhat the appearance of being vesicles
enclosed by walls formed of spindle-shaped cells. In reality they are only
spaces enclosed at the sides, and, as a general rule, not above and below.
They have been mistaken by some observers for vesicles in which the
corpuscles were supposed to be developed, and to escape by the rupture of
the walls into the capillary spaces between. This mistake has been clearly
pointed out by Klein (_loc. cit._).
At the time when these spaces are formed, and especially in the hinder
two-thirds of the pellucid area, and in the layer of blood-vessels
immediately above the hypoblast, a formation takes place which forms in
appearance a secondary investment of the capillaries. Dr Klein was the
first to give a correct account of this formation. It results from the
cells of the mesoblast in the meshes of the capillary system. Certain of
these cells become flattened, and send out fine protoplasmic processes.
They arrange themselves so as completely to enclose the spaces between the
capillaries, forming in this way vesicles.
Where seen on section (vide fig. 6) at the edge of the vesicles these cells
lining the vesicles appear spindle-shaped, and look like a secondary
investment of the capillaries. This investment is most noticeable in the
hinder two-thirds of the pellucid area; but, though less conspicuous, there
is a similar formation in its anterior third, where there would seem to be
only veins present. Dr Klein (_loc. cit._, fig. 12) has also drawn this
investment in the anterior third of the pellucid area. He has stated that
the vessels in the mesoblast between the splanchnopleure and the
somatopleure, and which are enclosed by prolongations from the former, do
not possess this secondary investment; he has also stated that the same is
true for the sinus terminalis; but I am rather doubtful whether the
generalisation will hold, that veins and arteries can from the first be
distinguished by the latter possessing this investment. I am also rather
doubtful whether the spaces enclosed by the protoplasmic threads between
the splanchnopleure and somatopleure are the centres of vessels at all,
since I have never seen any blood-corpuscles in them.
It is not easy to learn from sections much about the first stages in the
formation of the capillaries, and it is impossible to distinguish between a
completely-formed vessel and a mere spherical space. The fine protoplasmic
processes which connect the masses of corpuscles can rarely be seen in
sections, except when they pass vertically, as they do occasionally (vide
Pl. 2, fig. 9) in the opaque area, joining the somatopleure and the
splanchnopleure. Dr Klein considers these latter processes to be the walls
of the vessels, but they appear rather to be the processes which will
eventually become new capillaries.
From sections, however, it is easy to see that the appearances of the
capillaries in the vascular area are similar to the appearances in the
pellucid area, from which it is fair to conclude that their mode of
formation is the same in both. It is also easy to see that the first
formation of vessels occurs in the splanchnopleure, and that even up to the
forty-fifth hour but few or no vessels are found in the somatopleure. The
mesoblast of the somatopleure is continued into the opaque area as a single
layer of spindle-shaped cells.
Sections clearly shew in the case of most of the vessels that the secondary
investment of Klein is present, even in the case of those vessels which lie
immediately under the somatopleure.
In reference to the origin of particular vessels I have not much to say. Dr
Klein's account of the origin of the sinus terminalis is quite correct. It
arises by a number of the masses of blood-corpuscles, similar to those
described above, becoming connected together by protoplasmic processes. The
whole is subsequently converted into a continuous vessel in the usual way.
From the first the sinus terminalis possesses cellular walls, as is clear
from its mode of origin. I am inclined to think that Klein is right in
saying that the aortæ arise in a similar manner, but I have not worked out
their mode of origin very fully.
It will be seen from the account given above that, in reference to the
first stages in the development of the blood-vessels, my observations
differ very considerably from those of Dr Klein; as to the later stages,
however, we are in tolerable agreement. We are in agreement, moreover, as
to the fundamental fact that the blood-vessels are formed by a number of
cells becoming connected, and by a series of changes converted into a
network of vessels, and that they are not in the first instance merely
channels between the cells of the mesoblast.
By the forty-fifth hour colourless corpuscles are to be found in the blood
whose exact origin I could not determine; probably they come from the walls
of the capillaries.
In the vessels themselves the coloured corpuscles undergo increase by
division, as has already been shewn by Remak. Corpuscles in the various
stages of division may easily be found. They do not appear to show very
active amoeboid movements in the vessels, though their movements are
sometimes very active when removed from the body.
To recapitulate--some of the cells of the mesoblast of the splanchnopleure
send out processes, these processes unite with the processes from other
cells, and in this way a network is formed. The nuclei of the original
cells divide, and at the points from which the processes start their
division is especially rapid. Some of them acquire especially at these
points a red colour, and so become converted into blood-corpuscles; the
others, together with part of the protoplasm in which they are imbedded,
become converted into an endothelium both for the processes and the masses
of corpuscles; the remaining protoplasm becomes fluid, and thus the
original network of the cells becomes converted into a network of hollow
vessels, filled with fluid, in which corpuscles float.
In reference to the development of the heart, my observations are not quite
complete. It is, however, easy to prove from sections (vide figs. 10 and
11, Pl. 2) that the cavity of the heart is produced by a splitting or
absorption of central cells of the thickened mesoblast of the
splanchnopleure, while its muscular walls are formed from the remaining
cells of this thickened portion. It is produced in the following way:--When
the hypoblast is folded in to form the alimentary canal the mesoblast of
the splanchnopleure follows it closely, and where the splanchnopleure turns
round to assume its normal direction (fig. 11) its mesoblast becomes
thickened. This thickened mass of mesoblast is, as can easily be seen from
figs. 10 and 11, Pl. 2, entirely distinct from the mesoblast which forms
the outside walls of the alimentary canal. At the point where this
thickening occurs an absorption takes place to form the cavity of the
heart. The method in which the cavity is formed can easily be seen from
figs. 10 and 11. It is in fig. 11 shewn as it takes place in the mesoblast
on each side, the folds of the splanchnopleure not having united in the
middle line; and hence a pair of cavities are formed, one on each side. It
is, however, probable that, in the very first formation of the heart, the
cavity is single, being formed after the two ends of the folded mesoblast
have united (vide _hz_, fig. 10). In some cases the two folds of the
mesoblast appear not at first to become completely joined in the middle
line; in this case the cavity of the heart is still complete from side to
side, but the mesoblast-cells which form its muscular walls are deficient
above. By the process of absorption, as I said, a cavity is produced in the
thickened part of the mesoblast of the splanchnopleure, a cavity which is
single in front, but becomes divided further behind, where the folds of the
mesoblast have not united, into two cavities, to form the origin of the
omphalomeseraic veins. As the folding proceeds backwards the starting-point
of the omphalomeseraic veins is also pushed backwards, and the cavities
which were before separated become joined together. From its first
formation the heart is lined internally by an endothelium; this is formed
of flattened cells, spindle-shaped in section. The exact manner of the
origin of this lining I have not been able to determine; it is, however,
probable that some of the central mesoblast-cells are directly converted
into the cells of the endothelium.
I have obtained no evidence enabling me to determine whether Dr Klein is
correct in stating that the cells of the mesoblast in the interior of the
heart become converted partly into blood-corpuscles and partly into a
cellular lining forming the endothelium of the heart, in the same way that
the blood-vessels in the rest of the blastoderm are formed. But I should be
inclined to think that it is very probable--certainly more probable than
that the cavity of the heart is formed by a process of splitting taking
place. Where I have used the word "absorption" in speaking of the formation
of the cavity of the heart, I must be understood as implying that certain
of the interior cells become converted into the endothelium, while others
either form the plasma or become blood-corpuscles.
The originally double formation of the hinder part of the heart probably
explains Dr Afanassiev's statement (_Bullétin de l'Académ. Impériale de St
Petersb._, tom. xiii, pp. 321-335), that he finds the endothelium of the
heart originally dividing its interior into two halves; for when the
partition of the mesoblast which separated at first the two halves of the
heart became absorbed, the endothelium lining of each of the originally
separate vessels would remain complete, dividing the cavity of the heart
into two parts. The partition in the central line is, however, soon
absorbed.
The account given above chiefly differs from that of Remak by not supposing
that the mesoblast-cells which form the heart are in any way split off from
the wall of the alimentary canal.
There can be no doubt that His is wrong in supposing that the heart
originates from the mesoblast of the splanchnopleure and somatopleure
uniting to form its walls, thus leaving a cavity between them in the
centre. The heart is undoubtedly formed out of the mesoblast of the
splanchnopleure only.
Afanassiev's observations are nearer to the truth, but there are some
points in which he has misinterpreted his sections.
Sections Pl. 2, figs. 10 and 11, explain what I have just said about the
origin of the heart. Immediately around the notochord the mesoblast is not
split, but a very little way outside it is seen to be split into two parts
_so_ and _sp_; the former of these follows the epiblast, and together with
it forms the somatopleure, which has hardly begun to be folded at the line
where the sections are taken. The latter (_sp_) forms with the hypoblast
(_hy_) the splanchnopleure, and thus has become folded in to form the walls
of the alimentary canal (_d_). In fig. 11 the folds have not united in the
central line, but in fig. 10 they have so united. In fig. 11, where the
mesoblast, still following the hypoblast, turns back to assume its normal
direction, it is seen to be thickened and to have become split, so that a
cavity (_of_) (of the omphalomeseraic vein) is formed in it on each side,
lined by endothelium.
In the section immediately behind section fig. 11 the mesoblast was
thickened, but had not become split.
In fig. 10 the hypoblast folds are seen to have united in the centre, so as
to form a completely closed digestive canal (_d_); the folds of the
mesoblast have also united, so that there is only a single cavity in the
heart (_hz_), lined, as was the case with the omphalomeseraic veins, by
endothelium.
In conclusion, I have to thank Dr Foster for his assistance and suggestions
throughout the investigations which have formed the subject of these three
short papers, and which were well carried on in the apartments used by him
as a Physiological Laboratory.
EXPLANATION OF PLATE 2.
Fig. 1 is taken from the anterior part of the pellucid area of a thirty
hours' chick, with four protovertebræ. At _n_ is a nucleus with two
nucleoli.
Figs. 2 and 3 are taken from the posterior end of the pellucid area of a
chick with eight protovertebræ. In fig. 3 the nuclei are seen to have
considerably increased in number at the points of starting of the
protoplasmic processes. At _n_ is seen a nucleus with two nucleoli.
Fig. 4 is taken from the anterior part of the pellucid area of an embryo of
thirty-six hours. It shews the narrow processes characteristic of the
anterior part of the pellucid area, and the fewer nuclei. Small spaces,
which have the appearance of vacuoles, are shewn at _v_.
Fig. 5 is taken from the posterior part of the pellucid area of a
thirty-six hours' embryo. It shews the nuclei, with somewhat irregular
nucleoli, which have begun to acquire the red colour of blood-corpuscles;
the protoplasmic processes containing the nuclei; the nuclei in the
protoplasm surrounding the corpuscles, as shewn at _a_, _a´_.
Fig. 6 shews fully formed blood-vessels, in part filled with
blood-corpuscles and in part empty. The walls of the capillaries, formed of
cells, spindle-shaped in section, are shewn, and also the secondary
investment of Klein at _k_, and at _b_ is seen a narrow protoplasmic
process filled with blood-corpuscles.
Fig. 7 is taken from the anterior part of the pellucid area of a thirty-six
hours' embryo. It shews a collection of nuclei which are beginning to
become blood-corpuscles.
Figs. 1-5 are drawn with an 1/8 object-glass. Fig. 6 is on a much smaller
scale. Fig. 7 is intermediate.
Fig. 8.--A transverse section through the dorsal region of a forty-five
hours' embryo; _ao_, aorta with a few blood-corpuscles. v, Blood-vessels,
all of them being formed in the splanchnopleure, and all of them provided
with the secondary investment of Klein; _pe_, pellucid area; _op_, opaque
area.
Fig. 9.--Small portion of a section through the opaque area of a
thirty-five hours' embryo, showing protoplasmic processes, with nuclei
passing from the somatopleure to the splanchnopleure.
Fig. 10.--Section through the heart of a thirty-four hours' embryo. _a_.
Alimentary canal; _hb_, hind brain; _nc_, notochord; _e_, epiblast; _so_,
mesoblast of the somatopleure; _sp_, mesoblast of the splanchnopleure;
_hy_, hypoblast; _hz_, cavity of the heart.
Fig. 11.--Section through the same embryo as fig. 10, and passing through
the orifice of the omphalomeseraic vein. _of_, Omphalomeseraic vein; other
references as above.
These two sections shew that the heart is entirely formed from the
mesoblast of the _splanchnopleure_, and that it is formed by the splitting
of that part of the mesoblast which has turned to assume its normal
direction after being folded in to form the muscular wall of the alimentary
canal. In fig. 11 the cavities so formed on each side have not yet united,
but in fig. 10 they have united. When the folding becomes more complete the
cavities (_of_, _of_) in fig. 11 will unite, and in this way the origin of
the omphalomeseraic veins will be carried further backwards. In the section
immediately behind section 11 the mesoblast had become thickened, but had
not split.
V. A PRELIMINARY ACCOUNT OF THE DEVELOPMENT OF THE ELASMOBRANCH FISHES[10].
Footnote 10: From the _Quarterly Journal of Microscopical
Science_, Vol. XIV. 1874. Read in Section D, at the Meeting of
the British Association at Belfast.
With Plates 3 and 4.
During the spring of the present year I was studying at the Zoological
Station, founded by Dr Dohrn at Naples, and entirely through its agency was
supplied with several hundred eggs of various species of Dog-fish
(Selachii)--a far larger number than any naturalist has previously had an
opportunity of studying. The majority of the eggs belonged to an oviparous
species of _Mustelus_, but in addition to these I had a considerable number
of eggs of two or three species of _Scyllium_, and some of the Torpedo.
Moreover, since my return to England, Professor Huxley has most liberally
given me several embryos of _Scyllium stellare_ in a more advanced
condition than I ever had at Naples, which have enabled me to fill up some
lacunæ in my observations.
On many points my investigations are not yet finished, but I have already
made out a number of facts which I venture to believe will add to our
knowledge of vertebrate embryology; and since it is probable that some time
will elapse before I am able to give a complete account of my
investigations, I have thought it worth while preparing a preliminary paper
in which I have briefly, but I hope in an intelligible manner, described
some of the more interesting points in the development of the
Elasmobranchii. The first-named species (_Mustelus_ sp.?) was alone used
for the early stages, for the later ones I have also employed the other
species, whose eggs I have had; but as far as I have seen at present, the
differences between the various species in early embryonic life are of no
importance.
Without further preface I will pass on to my investigations.
_The Egg-shell._
In the eggs of all the species of Dog-fishes which I have examined the yolk
lies nearest that end of the quadrilateral shell which has the shortest
pair of strings for attachment. This is probably due to the shape of the
cavity of the shell, and is certainly not due to the presence of any
structures similar to chalazæ.
_The Yolk._
The yolk is not enclosed in any membrane comparable to the vitelline
membrane of Birds, but lies freely in a viscid albumen which fills up the
egg-capsule. It possesses considerable consistency, so that it can be
removed into a basin, in spite of the absence of a vitelline membrane,
without falling to pieces. This consistency is not merely a property of the
yolk-sphere as a whole, but is shared by every individual part of it.
With the exception of some finely granular matter around the blastoderm,
the yolk consists of rather small, elliptical, highly refracting bodies,
whose shape is very characteristic and renders them easily recognizable. A
number of striæ like those of muscle are generally visible on most of the
spherules, which give them the appearance of being in the act of breaking
up into a series of discs; but whether these striæ are normal, or produced
by the action of water I have not determined.
_Position of the Blastoderm._
The blastoderm is always situated, immediately after impregnation, near the
pole of the yolk which lies close to the end of the egg-capsule. Its
position varies a little in the different species and is not quite constant
in different eggs of the same species. But this general situation is quite
invariable. It is of about the same proportional size as the blastoderm of
a bird.
_Segmentation._
In a fresh specimen, in which segmentation has only just commenced, the
blastoderm or germinal disc appears as a circular disc, distinctly marked
off by a dark line from the rest of the yolk. This line, as is proved by
sections, is the indication of a very shallow groove. The appearance of
sharpness of distinction between the germ and the yolk is further
intensified by their marked difference of colour, the germ itself being
usually of a darker shade than the remainder of the yolk; while around its
edge, and apparently sharply separated from it by the groove before
mentioned, is a ring of a different shade which graduates at its outer
border into the normal shade of the yolk.
These appearances are proved by transverse sections to be deceptive. There
is no sharp line either at the sides or below separating the blastoderm
from the yolk. In the passage between the fine granular matter of the germ
to the coarser yolk-spheres every intermediate size of granule is present;
and, though the space between the two is rather narrow, in no sense of the
word can there be said to be any break or line between them.
This gradual passage stands in marked contrast with what we shall find to
be the case at the close of the segmentation. In the youngest egg which I
had, the germinal disc was already divided into four segments by two
furrows at right angles. These furrows, however, did not reach its edge;
and from my sections I have found that they were not cut off below by any
horizontal furrow. So that the four segments were continuous below with the
remainder of the germ without a break.
In the next youngest specimen which I had, there were already present
eighteen segments, somewhat irregular in size, but which might roughly be
divided into an outer ring of larger spheres, separated, as it were, by a
circular furrow from an inner series of smaller segments. The furrows in
this case reached quite to the edge of the germinal disc.
The remarks I made in reference to the earlier specimen about the
separation of the germ from the yolk apply in every particular to the
present one. The external limit of the blastoderm was not defined by a true
furrow, and the segmentation furrows still ended below without meeting any
horizontal furrows, so that the blastoderm was not yet separated by any
line from the remainder of the yolk, and the segments of which it was
composed were still only circumscribed upon five sides. In this particular
the segmentation in these animals differs materially from that in the Bird,
where the horizontal furrows appear very early.
In each segment a nucleus was generally to be seen in sections. I will,
however, reserve my remarks upon the nature of the nuclei till I discuss
the nuclei of the blastoderm as a whole.
For some little time the peripheral segments continue larger than the more
central ones, but this difference of size becomes less and less marked, and
before the segments have become too small to be seen with the simple
microscope, their size appears to be uniform over the whole surface of the
blastoderm.
In the blastoderms somewhat older than the one last described the segments
have already become completely separate masses, and each of them already
possesses a distinct nucleus. They form a layer one or two segments deep.
The limits of the blastoderm are not, however, defined by the already
completed segments, but outside these new segments continue to be formed
around nuclei which appear in the yolk. At this stage there is, therefore,
no line of demarcation between the germ and the yolk, but the yolk is being
bored into, so to speak, by a continuous process of fresh segmentation.
The further segmentation of the already existing spheres, and the formation
of new ones from the yolk below and to the sides, continues till the
central cells acquire their final size, the peripheral ones being still
large, and undefined towards the yolk. These also soon reach the final
size, and the blastoderm then becomes rounded off towards the yolk and
sharply separated from it.
_The Nuclei of the Yolk._
Intimately connected with the segmentation is the appearance and history of
a number of nuclei which arise in the yolk surrounding the blastoderm.
When the horizontal furrows appear which first separate the blastoderm from
the yolk, the separation does not occur along the line of passage from the
fine to the coarse yolk, but in the former at some distance from this line.
The blastoderm thus rests upon a mass of finely granular material, from
which, however, it is sharply separated. At this time there appear in this
finely granular material a number of nuclei of a rather peculiar character.
They vary immensely in size--from that of an ordinary nucleus to a size
greater than the largest blastoderm-cell.
In Pl. 3, fig. 1, _n_, is shewn their distribution in this finely granular
matter and their variation in size. But whatever may be their size, they
always possess the same characteristic structure. This is shewn in Pl. 3,
figs. 1 and 2, _n_.
They are rather irregular in shape, with a tendency when small to be
roundish, and are divided by a number of lines into distinct areas, in each
of which a nucleolus is to be seen. The lines dividing them into these
areas have a tendency (in the smaller specimens) to radiate from the
centre, as shewn in Pl. 3, fig. 1.
These nuclei colour red with hematoxylin and carmine and brown with osmic
acid, while the nucleoli or granules contained in the areas also colour
_very intensely_ with all the three above-named reagents.
With such a peculiar structure, in favourable specimens these nuclei are
very easily recognised, and their distribution can be determined without
difficulty. They are not present alone in the finely granular yolk, but
also in the coarsely granular yolk adjoining it. They form very often a
special row, sometimes still more markedly than in Pl. 3, fig. 1, along the
floor of the segmentation cavity. They are not, however, found alone in the
yolk. All the blastoderm-cells in the earlier stages possess precisely
similar nuclei! From the appearance of the first nucleus in a
segmentation-sphere till a comparatively late period in development, every
nucleus which can be distinctly seen is found to be of this character. In
Pl. 3, fig. 2, this is very distinctly shewn.
(1) We have, then, nuclei of this very peculiar character scattered through
the sub-germinal granular matter, and also universally present in the cells
of the blastoderm. (2) These nuclei are distributed in a special manner
under the floor of the segmentation cavity on which new cells are
continually appearing. Putting these two facts together, there would be the
strongest presumption that these nuclei do actually become the nuclei of
cells which enter the blastoderm, and such is actually the case. In my
account of the segmentation I have, indeed, already mentioned this, and I
will return to it, but before doing so will enter more fully into the
distribution of these nuclei in the yolk.
They appear in small numbers around the blastoderm at the close of
segmentation, and round each one of them there may at this time be seen in
osmic acid specimens, and with high powers, a fine network similar to but
finer than that represented in Pl. 3, fig. 2. This network cannot, as a
general rule, be traced far into the yolk, but in some exceptionally thin
specimens it may be seen in any part of the fine granular yolk around the
blastoderm, the meshes of the network being, however, considerably coarser
between than around the nuclei. This network may be seen in the fine
granular material around the germ till the latest period of which I have
yet cut sections of the blastoderm. In the later specimens, indeed, it is
very much more distinctly seen than in the earlier, owing to the fact that
in parts of the blastoderm, especially under the embryo, the yolk-granules
have disappeared partly or entirely, leaving only this fine network with
the nuclei in it.
A specimen of this kind is represented in Pl. 3, fig. 2, where the meshes
of the network are seen to be finer immediately around the nuclei, and
coarser in the intervals. The specimen further shows in the clearest manner
that this network is not divided into areas, each representing a cell and
each containing a nucleus. I do not know to what extent this network
extends into the yolk. I have never yet seen the limits of it, though it is
very common to see the coarsest yolk-granules lying in its meshes. Some of
these are shewn in Pl. 3, fig. 2, _yk_.
This network of lines[11] (probably bubbles) is characteristic of many
cells, especially ova. We are, therefore, forced to believe that the fine
granular and probably coarser granular yolk of this meroblastic egg
consists of an active organized basis with passive yolk-spheres imbedded in
it. The organized basis is especially concentrated at the germinal pole of
the egg, but becomes less and less in quantity, as compared with the
yolk-spheres, the further we depart from this.
Footnote 11: The interpretation of this network is entirely
due to Dr Kleinenberg, who suggested it to me on my shewing him
a number of specimens exhibiting the nuclei and network.
Admitting, as I think it is necessary to do, the organized condition of the
whole yolk-sphere, there are two possible views as to its nature. We may
either take the view that it is one gigantic cell, the ovum, which has
grown at the expense of the other cells of the egg-follicle, and that these
cells in becoming absorbed have completely lost their individuality; or we
may look upon the true formative yolk (as far as we can separate it from
the remainder of the food-yolk) as the remains of one cell (the primitive
ovum), and the remainder of the yolk as a body formed from the coalescence
of the other cells of the egg-follicle, which is adherent to, but has not
coalesced with, the primitive ovum, the cells in this case not having
completely lost their individuality; and to these cells, the nuclei, I have
found, must be supposed to belong.
The former view I think, for many reasons, the most probable. The share of
these nuclei in the segmentation, and the presence of similar nuclei in the
cells of the germ, both support it, and are at the same time difficulties
in the way of the other view. Leaving this question which cannot be
discussed fully in a preliminary paper like the present one, I will pass on
to another important question, viz.:
How do these nuclei originate? Are they formed by the division of the
pre-existing nuclei, or by an independent formation? It must be admitted
that many specimens are strongly in favour of the view that they increase
by division. In the first place, they are often seen "two together;"
examples of this will be seen in Pl. 3, fig. 1. In the second place, I have
found several specimens in which five or six appear close together, which
look very much as if there had been an actual division into six nuclei. It
is, however, possible in this case that the nuclei are really connected
below and only appear separate, owing to the crenate form of the mass.
Against this may be put the fact that the division of a nucleus is by no
means so common as has been sometimes supposed, that in segmentation it has
very rarely been observed that the nucleus of a sphere first divides[12],
and that then segmentation takes place, but segmentation generally occurs
and then a new nucleus arises in each of the newly formed spheres. Such
nuclei as I have described are rare; they have, however, been observed in
the egg of a _Nephelis_ (one of the Leeches), and have in that case been
said to divide. Dr Kleinenberg, however, by following a single egg through
the whole course of its development, has satisfied himself that this is not
the case, and that, further, these nuclei in Nephelis never form the nuclei
of newly developing cells.
Footnote 12: Kowalevsky ("Beiträge zur Entwicklungsgeschichte
der Holothurien," _Mémoires de l'Ac. Imp. de St Petersbourg_,
vii ser., Vol. XI. 1867) describes the division of nuclei
during segmentation in the Holothurians, and other observers
have described it elsewhere.
I must leave it an open question, and indeed one which can hardly be solved
from sections, whether these nuclei arise freely or increase by division,
but I am inclined to believe that both processes may possibly take place.
In any case their division does not appear to determine the segmentation or
segregation of the protoplasm around them.
As was mentioned in my account of the segmentation, these nuclei first
appear during that process, and become the nuclei of the freshly formed
segmentation spheres. At the close of segmentation a few of them are still
to be seen around the blastoderm, but they are not very numerous.
From this period they rapidly increase in number, up to the commencement of
the formation of the embryo as a body distinct from the germ. Though before
this period they probably become the nuclei of veritable cells which enter
the germ, it is not till this period, when the growth of the blastoderm
becomes very rapid and it commences to spread over the yolk, that these new
cells are formed in large numbers. I have many specimens of this age which
shew the formation of these new cells with great clearness. This is most
distinctly to be seen immediately below the embryo, where the
yolk-spherules are few in number. At the opposite end of the blastoderm I
believe that more of these cells are formed, but, owing to the presence of
numerous yolk-spherules, it is much more difficult to make certain of this.
As to the final destination of these cells, my observations are not yet
completed. Probably a large number of them are concerned in the formation
of the vascular system, but I will give reasons later on for believing that
some of them are concerned in the formation of the walls of the digestive
canal and of other parts.
I will conclude my account of these nuclei by briefly summarizing the
points I have arrived at in reference to them.
A portion, or more probably the whole, of the _yolk_ of the Dog-fish
consists of _organized material_, in which nuclei appear and increase
either by _division_ or by a process of _independent_ formation, and a
great number of these subsequently become the nuclei of cells formed around
them, frequently at a distance from the germ, which then travel up and
enter it.
The formation of cells in the yolk, apart from the general process of
segmentation, has been recognised by many observers. Kupffer (_Archiv. für
Micr. Anat._, Bd. IV. 1868) and Owsjannikow ("Entwicklung der Coregonus,"
_Bulletin der Akad. St Petersburgh_, Vol. XIX.) in osseous fishes[13], Ray
Lankester (_Annals and Mag. of Nat. Hist._ Vol. XI. 1873, p. 81) in
Cephalopoda, Götte (_Archiv. für Micr. Anat._ Vol. X.) in the chick, have
all described a new formation of cells from the so-called food-yolk. The
organized nature of the whole or part of this, previous to the formation of
the cells from it, has not, however, as a rule, been distinctly recognised.
In the majority of cases, as, for instance, in Loligo, the nucleus is not
the first thing to be formed, but a plastide is first formed, in which a
nucleus subsequently makes its appearance.
Footnote 13: Götte, at the end of a paper on "The Development
of the Layers in the Chick" (_Archiv. für Micr. Anat._, Vol. X.
1873, p. 196), mentions that the so-called cells in Osseous
fishes which Oellacher states to have migrated into the yolk,
and which are clearly the same as those mentioned by
Owsjannikow, are really not _cells_, but large _nuclei_. If
this statement is correct the phenomena in Osseous fishes are
precisely the same as those I have described in the Dog-fish.
_Formation of the Layers._
Leaving these nuclei, I will now pass on to the formation of the layers.
At the close of segmentation the surface of the blastoderm is composed of
cells of a uniform size, which, however, are too small to be seen by the
aid of the simple microscope.
The cells of this uppermost layer are somewhat columnar, and can be
distinguished from the remainder of the cells of the blastoderm as a
separate layer. This layer forms the epiblast; and the Dog-fish agree with
Birds, Batrachians, and Osseous fish in the very early differentiation of
it.
The remainder of the cells of the blastoderm form a mass, many cells deep,
in which it is impossible as yet or till a very considerably later period
to distinguish two layers. They may be called the _lower layer cells_. Some
of them near the edge of this mass are still considerably larger than the
rest, but they are, as a whole, of a fairly uniform size. Their nuclei are
of the same character as the nuclei in the yolk.
There is one point to be noticed in the shape of the blastoderm as a whole.
It is unsymmetrical, and a much larger number of its cells are found
collected at one end than at the other. This absence of symmetry is found
in all sections which are cut parallel to the long axis of the egg-capsule.
The thicker end is the region where the embryo will subsequently appear.
This very early appearance of distinction in the blastoderm between the end
at which the embryo will appear, and the non-embryonic end is important,
especially as it shews the affinity of the modes of development of Osseous
fishes and the Elasmobranchii. Oellacher (_Zeitschrift für Wiss. Zoologie_,
Vol. XXXIII. 1873) has shewn, and, though differing from him on many other
points, on this point Götte (_Arch. für Micr. Anat._ Vol. IX. 1873) agrees
with him, that a similar absence of symmetry by which the embryonic end of
the germ is marked off, occurs almost immediately after the end of
segmentation in Osseous fishes. In the early stages of development there
are a number of remarkable points of agreement between the Osseous fish and
the Dog-fish, combined with a number of equally remarkable points of
difference. Some of these I shall point out as I proceed with my
description.
The embryonic end of the germ is always the one which points towards the
pole of the yolk farthest removed from the egg-capsule.
The germ grows, but not very rapidly, and without otherwise undergoing any
very appreciable change, for some time.
The growth at these early periods appears to be particularly slow,
especially when compared with the rapid manner in which some of the later
stages of the development are passed through.
The next important change which occurs is the formation of the so-called
"segmentation cavity."
This forms a very marked feature throughout the early stages. It appears,
however, to have somewhat different relations to the blastoderm than the
homologous structure in other vertebrates. In its earliest stage which I
have observed, it appears as a small cavity in the centre of the lower
layer cells. This grows rapidly, and its roof becomes composed of epiblast
and only a thin lining of "_lower layer_" cells, while its floor is formed
by the yolk (Pl. 3, fig. 3, _sg_). In the next and third stage (Pl. 3,
fig. 4, _sg_) its floor is formed by a thin layer of cells, its roof
remaining as before. It has, however, become a less conspicuous formation
than it was; and in the last (fourth) stage in which it can be
distinguished it is very inconspicuous, and almost filled up by cells.
What I have called the second stage corresponds to a period in which no
trace of the embryo is to be seen. In the third stage the embryonic end of
the blastoderm projects outwards to form a structure which I shall speak of
as the "embryonic rim," and in the fourth and last stage a distinct
medullary groove is formed. For a considerable period during the second
stage the segmentation cavity remains of about the same size; during the
third stage it begins to be encroached upon, and becomes smaller both
absolutely, and relatively to the increased size of the germ.
The segmentation cavity of the Dog-fish most nearly agrees with that of
Osseous fishes in its mode of formation and relation to the embryo.
Dog-fish resemble Osseous fish in the fact that their embryos are entirely
formed from a portion of the germ which does not form part of the roof of
the segmentation cavity, so that the cells forming the roof of the
segmentation cavity take _no share_ at any time in the formation of their
embryos. They further agree with Osseous fish (always supposing that the
descriptions of Oellacher, _loc. cit._, and Götte, _Archiv. für Micr.
Anat._ Bd. IX. are correct) in the floor of the segmentation cavity being
formed at one period by yolk. Together with these points of similarity
there are some important differences.
(1) The segmentation cavity in the Osseous fish from the first arises as a
cavity between the yolk and the blastoderm, and its floor is never at any
period covered with cells. In the Dog-fish, as we have said above, both in
the earlier and later periods the floor is covered with cells.
(2) The roof in the Dog-fish is _invariably_ formed by the epiblast and a
row of flattened lower layer cells.
According to both Götte and Oellacher the roof of the segmentation cavity
in Osseous fishes is in the earlier stages formed _alone_ of the two layers
which correspond with the single layer forming the epiblast in the
Dog-fish. In Osseous fishes it is very difficult to distinguish the various
layers, owing to the similarity of their component cells. In Dog-fish this
is very easy, owing to the great distinctness of the epiblast, and it
appears to me, on this account, very probable that the two above-named
observers may be in error as to the constitution of its roof in the Osseous
fish. With both the Bird and the Frog the segmentation cavity of the
Dog-fish has some points of agreement, and some points of difference, but
it would take me too far from my present subject to discuss them.
When the segmentation cavity is first formed, no great changes have taken
place in the cells forming the blastoderm. The upper layer--the
_epiblast_--is composed of a single layer of columnar cells, and the
remainder of the cells of blastoderm, forming the lower layer, are of a
fairly uniform size, and polygonal from mutual pressure. The whole edge of
the blastoderm is thickened, but this thickening is especially marked at
its embryonic end.
This thickened edge of the blastoderm is still more conspicuous in the next
and second stage (Pl. 3, fig. 3).
In the second stage the chief points of progress, in addition to the
increased thickness of the edge of the blastoderm, are--
(1) The increased thickness and distinctness of the epiblast, caused by its
cells becoming more columnar, though it remains as a one-cell-thick layer.
(2) The disappearance of the cells from the floor of the segmentation
cavity.
The lower layer cells have undergone no important changes, and the
blastoderm has increased very little if at all in size.
From Pl. 3, fig. 3, it is seen that there is a far larger collection of
cells at the embryonic than at the opposite end.
Passing over some rather unimportant stages, I will come to the next
important one.
The general features of this (the third) stage in a surface view are--
(1) The increase in size of the blastoderm.
(2) The diminution in size of the segmentation cavity, both relatively and
absolutely.
(3) The appearance of a portion of the blastoderm projecting beyond the
rest over the yolk. This projecting rim extends for nearly half the
circumference of the yolk, but is most marked at the point where the embryo
will shortly appear. I will call it the "embryonic rim."
These points are still better seen from sections than from surface views,
and will be gathered at once from an inspection of Pl. 3, fig. 4.
The epiblast has become still more columnar, and is markedly thicker in the
region where the embryo will appear. But its most remarkable feature is
that at the outer edge of the "embryonic rim" (_er_) it turns round and
becomes continuous with the lower layer cells. This feature is most
important, and involves some peculiar modifications in the development. I
will, however, reserve a discussion of its meaning till the next stage.
The only other important feature of this stage is the appearance of a layer
of cells on the floor of the segmentation cavity.
Does this layer come from an ingrowth from the thickened edge of the
blastoderm, or does it arise from the formation of new cells in the yolk?
It is almost impossible to answer this question with certainty. The
following facts, however, make me believe that the newly formed cells do
play an important part in the formation of this layer.
(1) The presence at an earlier date of almost a row of nuclei under the
floor of the segmentation cavity (Pl. 3, fig. 1).
(2) The presence on the floor of the cavity of such large cells as those
represented in fig. 1, _bd_, cells which are very different, as far as the
size and granules are concerned, from the remainder of the cells of the
blastoderm.
On the other hand, from this as well as other sections, I have satisfied
myself that there is a distinct ingrowth of cells from the embryonic
swelling. It is therefore most probable that both these processes, viz. a
fresh formation and an ingrowth, have a share in the formation of the layer
of cells on the floor of the segmentation cavity.
In the next stage we find the embryo rising up as a distinct body from the
blastoderm, and I shall in future speak of the body, which now becomes
distinct as the embryo. It corresponds with what Kupffer (_loc. cit._) in
his paper on the "Osseous Fishes" has called the "embryonic keel." This
starting-point for speaking of the embryo as a distinct body is purely
arbitrary and one merely of convenience. If I wished to fix more correctly
upon a period which could be spoken of as marking the commencing formation
of the embryo, I should select the time when structures first appear to
mark out the portion of the germ from which the embryo becomes formed; this
period would be in the Elasmobranchii, as in the Osseous fish, at the
termination of segmentation, when the want of symmetry between the
embryonic end of the germ and the opposite end first appears.
I described in the last stage the appearance of the "embryonic rim." It is
in the middle point of this, where it projects most, that the formation of
the embryo takes place. There appear two parallel folds extending from the
edge of the blastoderm towards the centre, and cut off at their central end
by another transverse fold. These three folds raise up, between them, a
flat broadish ridge, "_the embryo_" (Pl. 3, fig. 5). The head end of the
embryo is the end nearest the centre of the blastoderm, the tail end being
the one formed by its (the blastoderm's) edge.
Almost from its first appearance this ridge acquires a shallow groove--the
medullary groove (Pl. 3, fig. 5, _mg_)--along its middle line, where the
epiblast and hypoblast are in absolute contact (vide fig. 6_a_, 7_a_, 7_b_,
&c.) and where the mesoblast (which is already formed by this stage) is
totally absent. This groove ends abruptly a little before the front end of
the embryo, and is deepest in the middle and wide and shallow behind.
On each side of it is a plate of mesoblast equivalent to the combined
vertebral and lateral plates of the Chick. These, though they cannot be
considered as entirely the cause of the medullary groove, may perhaps help
to make it deeper. In the parts of the germ outside the embryo the
mesoblast is again totally absent, or, more correctly, we might say that
outside the embryo the _lower layer cells_ do not become differentiated
into hypoblast and mesoblast, and remain continuous only with the lower of
the two layers into which the _lower layer cells_ become differentiated in
the body of embryo. This state of things is not really very different from
what we find in the Chick. Here outside the embryo (_i.e._ in the opaque
area) there is a layer of cells in which no differentiation into hypoblast
and mesoblast takes place, but the layer remains continuous rather with the
hypoblast than the mesoblast.
There is one peculiarity in the formation of the mesoblast which I wish to
call attention to, _i.e._ its formation as two lateral masses, one on each
side of the middle line, but not continuous across this line (vide figs.
6_a_ and 6_b_, and 7_a_ and 7_b_). Whether this remarkable condition is the
most primitive, _i.e._ whether, when in the stage before this the mesoblast
is first formed, it is only on each side of the middle line that the
differentiation of the lower layer cells into hypoblast and mesoblast takes
place, I do not certainly know, but it is undoubtedly a very early
condition of the mesoblast. The condition of the mesoblast as two plates,
one on each side of the neural canal, is precisely similar to its embryonic
condition in many of the Vermes, _e.g. Euaxes_ and _Lumbricus_. In these
there are two plates of mesoblast, one on each side of the nervous cord,
which are known as the _Germinal streaks_ (Keimstreifen) (vide Kowalevsky
"Würmern u. Arthropoden"; _Mém. de l'Acad. Imp. St Petersbourg_, 1871).
From longitudinal sections I have found that the segmentation cavity has
ceased by this stage to have any distinct existence, but that the whole
space between the epiblast and the yolk is filled up with a mass of
elongated cells, which probably are solely concerned in the formation of
the vascular system. The thickened posterior edge of the blastoderm is
still visible.
At the embryonic end of the blastoderm, as I pointed out in an earlier
stage, the epiblast and the lower layer cells are perfectly continuous.
Where they join the epiblast, the _lower layer cells_ become distinctly
divided, and this division commenced even in the earlier stage, into two
layers; a lower one, more directly continuous with the epiblast, consisting
of cells somewhat resembling the epiblast-cells, and an upper one of more
flattened cells (Pl. 3, fig. 4, _m_). The first of these forms the
hypoblast, and the latter the mesoblast. They are indicated by _hy_ and _m_
in the figures. The hypoblast, as I said before, remains continuous with
the whole of the rest of lower layer cells of the blastoderm (vide
fig. 7_b_). This division into hypoblast and mesoblast commences at the
earlier stage, but becomes much more marked during this one.
In describing the formation of the hypoblast and mesoblast in this way I
have assumed that they are formed out of the large mass of lower layer
cells which underlie the epiblast at the embryonic end of the blastoderm.
But there is another and, in some ways, rather a tempting view, viz. to
suppose that the epiblast, where it becomes continuous with the hypoblast,
in reality becomes involuted, and that from this involuted epiblast are
formed the whole mesoblast and hypoblast.
In this case we would be compelled to suppose that the mass of lower layer
cells which forms the embryonic swelling is used as food for the growth of
the involuted epiblast, or else employed solely in the growth over the yolk
of the non-embryonic portion of the blastoderm; but the latter possibility
does not seem compatible with my sections.
I do not believe that it is possible, from the examination of sections
alone, to decide which of these two views (viz. whether the epiblast is
involuted, or whether it becomes merely continuous with the lower layer
cells) is the true one. The question must be decided from other
considerations.
The following ones have induced me to take the view that there is no
involution, but that the mesoblast and hypoblast are formed from the lower
layer cells.
(1) That it would be rather surprising to find the mass of lower layer
cells which forms the "embryo swelling" playing no part in the formation of
embryo.
(2) That the view that it is the lower layer cells from which the hypoblast
and mesoblast are derived agrees with the mode of formation of these two
layers in the Bird, and also in the Frog; since although, in the latter
animal, there is an involution, this is not of the epiblast, but of the
larger cells of the lower pole of the yolk, which in part correspond with
what I have called the lower layer cells in the Dog-fish.
If the view be accepted that it is from the lower layer cells that the
hypoblast and mesoblast are formed, it becomes necessary to explain what
the continuity of the hypoblast with the epiblast means.
The explanation of this is, I believe, the keystone to the whole position.
The vertebrates may be divided as to their early development into two
classes, viz. those with _holoblastic ova_, in which the digestive canal is
formed by an _involution_ with the presence of an "_anus of Rusconi_."
This class includes "Amphioxus," the "Lamprey," the "Sturgeon," and
"Batrachians."
The second class are those with _meroblastic ova_ and no _anus of Rusconi_,
and with an alimentary canal formed by the infolding of the sheet of
hypoblast, the digestive canal remaining in communication with the
food-yolk for the greater part of embryonic life by an umbilical canal.
This class includes the "Elasmobranchii," "Osseous fish," "Reptiles," and
"Aves."
The mode of formation of the alimentary canal in the first class is clearly
the more primitive; and it is equally clear that its mode of formation in
the second class is an adaptation due to the presence of the large quantity
of food-yolk.
In the Dog-fish I believe that we can see, to a certain extent, how the
change from the one to the other of these modes of development of the
alimentary canal took place.
In all the members of the first class, viz. "_Amphioxus_," the "Lamprey,"
the "Sturgeon," and the "Batrachians," the epiblast becomes continuous with
the hypoblast at the so-called "anus of Rusconi," and the alimentary canal,
potentially in all and actually in the Sturgeon (vide Kowalevsky,
Owsjannikow, and Wagner, _Bulletin der Acad. d. St Petersbourg_, Vol. XIV.
1870, "Entwicklung der Störe"), communicates freely at its extreme hind end
with the neural canal. The same is the case in the Dog-fish. In these, when
the folding in to form the alimentary canal on the one hand, and the neural
on the other, takes place, the two foldings unite at the corner, where the
epiblast and hypoblast are in continuity, and place the two tubes, the
neural and alimentary, in free communication with each other[14].
Footnote 14: This has been already made out by Kowalevsky,
"Würmern u. Arthropoden," _loc. cit._
There is, however, nothing corresponding with the "anus of Rusconi," which
merely indicates the position of the involution of the digestive canal, and
subsequently completely closes up, though it nearly coincides in position
with the true anus in the Batrachians, &c.
This remarkable point of similarity between the Dog-fish's development and
the normal mode of development in the first class (the holoblastic) of
vertebrates, renders it quite clear that the continuity of the epiblast and
hypoblast in the Dogfish is really the remnant of a more primitive
condition, when the alimentary canal was formed by an involution. Besides
the continuity between neural and alimentary canals, we have other remnants
of the primitive involution. Amongst these the most marked is the formation
of the embryonic rim, which is nothing less than the commencement of an
involution. Its form is due to the flattened, sheet-like condition of the
germ. In the mode in which the alimentary canal is closed in front I shall
shew there are indications of the primitive mode of formation of the
alimentary canal; and in certain peculiarities of the anus, which I shall
speak of later, we have indications of the primitive anus of Rusconi; and
finally, in the general growth of the epiblast (small cells of the upper
pole of the Batrachian egg) over the yolk (lower pole of the Batrachian
egg), we have an example of the manner in which the primitive involution,
to form the alimentary canal, invariably disappears when the quantity of
yolk in an egg becomes very great.
I believe that in the Dog-fish we have before our eyes one of the steps by
which a direct mode of formation comes to be substituted for an _in_direct
one by involution. We find, in fact, in the Dog-fish, that the cells from
which are derived the mesoblast and hypoblast come to occupy their final
position in the primitive arrangement of the cells during segmentation, and
not by a subsequent and secondary involution.
This change in the mode of formation of the alimentary canal is clearly a
result of change of mechanical conditions from the presence of the large
food-yolk.
Excellent parallels to it will be found amongst the Mollusca. In this class
the presence or absence of food-yolk produces not very dissimilar changes
to those which are produced amongst vertebrates from the same cause.
The continuity of the hypoblast and epiblast at the embryonic rim is a
remnant which, having no meaning or function, except in reference to the
earlier mode of development, is likely to become lost, and in Birds no
trace of it is any longer to be found.
I will not in the present preliminary paper attempt hypothetically to trace
the steps by which the involution gradually disappeared, though I do not
think it would be very difficult to do so. Nor will I attempt to discuss
the question whether the condition with a large amount of food-yolk (as
seems more probable) was twice acquired--once by the Elasmobranchii and
Osseous fishes, and once by Reptiles and Birds--or whether only once, the
Reptiles and Birds being lineal descendants of the Dog-fish.
In reference to the former point, however, I may mention that the
Batrachians and Lampreys are to a certain extent intermediate in condition
between the _Amphioxus_ and the Dog-fishes, since in them the yolk becomes
divided during segmentation into lower layer cells and epiblast, but a
modified involution is still retained, while the Dog-fish may be looked
upon as intermediate between Birds and Batrachians, the continuity at the
hind end between the epiblast and hypoblast being retained by them, though
not the involution.
It may be convenient here to call attention to some of the similarities and
some of the differences which I have not yet spoken of between the
development of Osseous fish and the Dog-fish in the early stages. The
points of similarity are--(1) The swollen edge of the blastoderm. (2) The
embryo-swelling. (3) The embryo-keel. (4) The spreading of the blastoderm
over the yolk-sac from a point corresponding with the position of the
embryo, and not with the centre of the germ. The growth is almost nothing
at that point, and most rapid at the opposite pole of the blastoderm, being
less and less rapid along points of the circumference in proportion to
their proximity to the embryonic swelling. (5) The medullary groove.
In external appearance the early embryos of Dog-fish and Teleostei are very
similar; some of my drawings could almost be substituted for those given by
Oellacher. This similarity is especially marked at the first appearance of
the medullary groove. In the Dog-fish the medullary groove becomes
converted into the medullary canal in the same way as in Birds and all
other vertebrates, except Osseous fishes, where it comes to nothing, and
is, in fact, a rudimentary structure. But in spite of Oellacher's
assertions to the contrary, I am convinced from the similarity of its
position and appearance to the true medullary groove in the Dog-fish, that
the groove which appears in Osseous fishes is the true medullary groove;
although Oellacher and Kuppfer appear to have conclusively proved that it
does not become converted into the medullary canal. The chief difference
between the Dog-fish and Osseous fish, in addition to the point of
difference about the medullary groove, is that the epiblast is in the
Dog-fish a single layer, and not divided into nervous and epidermic layers
as in Osseous fish, and this difference is the more important, since,
throughout the whole period of development till after the commencement of
the formation of the neural canal, the epiblast remains in Dog-fish as a
one-cell-deep layer of cells, and thus the possibility is excluded of any
concealed division into a neural and epidermic layer, as has been supposed
to be the case by Stricker and others in Birds.
_Development of the Embryo._
After the embryo has become definitely established, for some time it grows
rapidly in length, without externally undergoing other important changes,
with the exception of the appearance of two swellings, one on each side of
its tail.
These swellings, which I will call the _Caudal lobes_ (figs. 8 and 9,
_ts_), are also found in Osseous fishes, and have been called by Oellacher
the _Embryonal saum_. They are caused by a thickening of mesoblast on each
side of the hind end of the embryo, at the edge of the embryonic rim, and
form a very conspicuous feature throughout the early stages of the
development of the Dog-fish, and are still more marked in the Torpedo
(Pl. 3, fig. 9). Although from the surface the other changes which are
visible are very insignificant, sections shew that the _notochord_ is
commencing to be formed.
I pointed out that beneath the medullary groove the epiblast and hypoblast
were not separated by any interposed mesoblast. Along the line (where the
mesoblast is deficient) which forms the long axis of the embryo, a rod-like
thickening of the hypoblast appears (Pl. 3, figs. 7_a_ and 7_b_, _ch_ and
_ch´_), first at the head end of the embryo, and gradually extends
backwards. This is the rudiment of the notochord; it remains attached for
some time to the hypoblast, and becomes separated from it first at the head
end of the embryo, and the separation is then carried backwards. This
thickening of the hypoblast projects up and comes in contact with the
epiblast, and in the later stages with bad (especially chromic-acid)
specimens the line of separation between the epiblast and the thickening
may become a little obscured, and might possibly lead to the supposition
that a structure similar to that which has been called the "_axis cord_"
was present. In all my best (osmic-acid) specimens the line of junction is
quite clear; and any one who is aware how easily two separate masses of
cells may be made indistinguishably to fuse together from simple pressure
will not be surprised to find the occasional obscurity of the line of
junction between the epiblast and hypoblast. In the earlier stage of the
thickening there is never in the osmic-acid preparations any appearance of
fusion except in very badly prepared ones. Its mode of formation will be
quite clear without further description from an inspection of Pl. 3, figs.
7_a_ and 7_b_, _ch_ and _ch´_. Both are taken from one embryo. In
fig. 7_b_, the most anterior of the two, the notochord has become quite
separated from the hypoblast. In fig. 7_a_, _ch_, there is only a very
marked thickening of hypoblast, which reaches up to the epiblast, but the
thickening is still attached to the hypoblast. Had I had space to insert a
drawing of a third section of the same embryo there would only have been a
slight thickening of the hypoblast. In the earlier stage it will be seen,
by referring to figs. 6_a_ and 6_b_, that there is no sign of a thickening
of the hypoblast. My numerous sections (all made from embryos hardened in
osmic acid) shewing these points are so clear that I do not think there can
be any doubt whatever of the notochord being formed as a thickening of the
hypoblast. Two interpretations of this seem possible.
I mentioned that the mesoblast appeared to be primitively formed as two
independent sheets, _split off, so to speak, from the hypoblast_, one on
each side of the middle line of the embryo. If we looked upon the notochord
as a third _median sheet of mesoblast_, split off from the hypoblast
somewhat later than the other two, we should avoid having to admit its
hypoblastic origin.
Professor Huxley, to whom I have shewn my specimens, strongly advocates
this view.
The other possibility is that the notochord is primitively a true
_hypoblastic_ structure which has only by adaptation become an apparently
_mesoblastic_ one in the higher vertebrates. In favour of this view are the
following considerations:
(1) That this is the undoubtedly natural interpretation of the sections.
(2) That the notochord becomes separated from the hypoblast after the
latter has acquired its typical structure, and differs in that respect from
the two lateral sheets of mesoblast, which are formed coincidently with the
hypoblast by a homogeneous mass of cells becoming differentiated into two
distinct layers. (3) That the first mode of looking at the matter really
proves too much, since it is clear that by the same method of reasoning we
could prove the mesoblastic origin of any organ derived from the hypoblast
and budded off into the mesoblast. We would merely have to assert that it
was really a mass of mesoblast budded off from the hypoblast rather later
than the remainder of the mesoblast. Still, it must be admitted that the
first view I have suggested is a possible, not to say a probable one,
though the mode of arguing by which it can be upheld may be rather
dangerous if generally applied. We ought not, however, for that reason
necessarily to reject it in the present case. As Mr Ray Lankester pointed
out to me, if we accept the hypoblastic origin of the notochord, we should
find a partial parallel to it in the endostyle of Tunicates, and it is
perhaps interesting to note in reference to it that the notochord is the
only _unsegmented_ portion of the axial skeleton.
Whether the strong _à priori_ difficulties of the hypoblastic origin of the
notochord are sufficient to counterbalance the natural interpretation of my
sections, cannot, I think, be decided from the single case of the Dog-fish.
It is to be hoped that more complete investigations of the Lamprey, &c.,
may throw further light upon the question.
Whichever view of the primitive origin of the notochord is the true one,
its apparent origin is very instructive as illustrating the possible way in
which an organ might come to change the layer to which it primarily
belonged.
If the notochord is a true mesoblastic structure, it is easy to be seen
how, by becoming separated from the hypoblast a little later than is the
case with the Dog-fish, its mesoblastic origin would become lost; while if,
on the other hand, it is primitively a hypoblastic structure, we see from
higher vertebrates how, by becoming separated from the hypoblast rather
earlier than in the Dog-fish, viz. at the same time as the rest of the
mesoblast, its primitive derivation from the hypoblast has become
concealed.
The view seemingly held by many embryologists of the present day, that an
organ, when it was primitively derived from one layer, can never be
apparently formed in another layer, appears to me both unreasonable on _à
priori_ grounds, and also unsupported by facts.
I see no reason for doubting that the embryo in the earliest periods of
development is as subject to the laws of natural selection as is the animal
at any other period. Indeed, there appear to me grounds for the thinking
that it is more so. The remarkable differences in allied species as to the
amount of food-yolk, which always entail corresponding alterations in the
development--the different modes of segmentation in allied species, such as
are found in the Amphipoda and Isopoda--the suppression of many stages in
freshwater species, which are retained in the allied marine species--are
all instances of modifications due to natural selection affecting the
earliest stages of development. If such points as these can be affected by
natural selection I see no reason why the arrangement of individual cells
(or rather primitive elements) should not also be modified; why, in fact, a
mass of cells which was originally derived from one layer, but in the
course of development became budded off from that layer and entered another
layer, should not by a series of small steps cease ever to be attached to
the original layer, but from the first moment it can be distinguished
should be found as a separate mass in the second layer.
The change of layers will, of course, only take place where some economy is
effected by it. The variations in the mode of development of the nervous
system may probably be explained in this way.
If we admit that organs can undergo changes, as to the primitive layer from
which they are derived, important consequences must follow.
It will, for instance, by no means be sufficient evidence of two organs not
being homologous that they are not developed from the same layer. It
renders the task of tracing out the homologies from development much more
difficult than if the ordinary view of the invariable correspondence of the
three layers throughout the animal kingdom be accepted. Although I do not
believe that this correspondence is invariable or exact, I think that we
both find and should expect to find that it is, roughly speaking, fairly
so.
Thus, the muscles, internal skeleton, and connective tissue are always
placed in the adult between the skin (epidermis) and the epithelium of the
alimentary canal.
We should therefore expect to find them, and, as a matter of fact, we
always do find them, developed from a middle layer when this is present.
The upper layer must always and does always form the epidermis, and
similarly the lower layer or hypoblast must form a part of the epithelium
of the alimentary canal. A full discussion of this question would, however,
lead me too far away from my present subject.
The only other point of interest which I can touch on in this stage is the
commencing closure of the alimentary canal in the region of the head. This
is shewn in Pl. 3, figs. 6_a_, 6_b_, 7_b_, _n.a_. From these figures it
can be seen that the closing does not take place as much by an infolding as
by an ingrowth from the side walls of the alimentary canal towards the
middle line. In this abnormal mode of closing of the alimentary canal we
have again, I believe, an intermediate stage between the mode of formation
of the alimentary canal in the Frog and the typical folding in which occurs
in Birds. There is, however, another point in reference to it which is
still more interesting. The cells to form the ingrowth from the bottom
(ventral) wall of the alimentary canal are derived by a continuous fresh
formation from the yolk, being formed around the nuclei spoken of above
(vide p. 63 et seq.). All my sections shew this with more or less
clearness, especially those a little later than fig. 6_b_, in which the
lower wall of the alimentary canal is nearly completed. This is the more
interesting since, from the mode of formation of the alimentary canal in
the Batrachians, &c., we might expect that the cells from the yolk would
take a share in its formation in the Dog-fish. I have not as yet made out
for certain the share which is taken by these freshly formed cells of the
yolk in the formation of any other organ.
By the completion of its lower wall in the way described, the throat early
becomes a closed tube, its closing taking place before any other important
changes are visible in the embryo from surface views.
A considerable increase in length is attained before other changes than an
increase in depth of the medullary groove and a more complete folding off
of the embryo from the blastoderm take place. The first important change is
the formation of the protovertebræ.
These are formed by the lateral plates of mesoblast, which I said were
equivalent at once to the vertebral and lateral plates in the Bird,
becoming split by transverse divisions into cubical masses.
At the time when this occurs, and, indeed, up till a considerably later
period, the mesoblast is not split into somatopleure and splanchnopleure,
and it is not divided into vertebral and lateral plates. The transverse
lines of division of the protovertebræ do not, however, extend to the outer
edge of the undivided lateral plates.
The differences between this mode of formation of the protovertebræ and
that occurring in Birds are too obvious to require pointing out. I will
speak of them more fully when I have given the whole history of the
protovertebræ of the Dog-fish.
I will only now say that I have had in the early stages to investigate the
formation of the protovertebræ entirely by means of sections, the objects
being too opaque to be otherwise studied.
The next change of any importance is the commencement of the formation of
the head. The region of the head first becomes distinguishable by the
flattening out of the germ at its front end.
The flattened-out portion of the germ grows rapidly, and forms a
spatula-like termination to the embryo (Pl. 3, fig. 8).
In the region of the head the medullary groove is at first totally absent
(vide section, Pl. 3, fig. 8_a_).
Indeed, as can be seen from fig. 8_b_, the laminæ dorsales, so far from
bending up at this stage, actually bend down in the opposite direction.
I am at present quite unable even to form a guess what this peculiar
feature of the brain means. It, no doubt, has some meaning in reference to
the vertebrate ancestry if we could only discover it. The peculiar
spatula-like flattened condition of the head is also (vide _loc. ant.
cit._) apparently found in the Sturgeons; it must therefore almost
undoubtedly be looked upon as not merely an accidental peculiarity.
While these changes have been taking place in the head not less important
changes have occurred in the remainder of the body. In the first place the
two caudal lobes have increased in size, and have become, as it were,
pushed in together, leaving a groove between them (fig. 8, _ts_). They are
very conspicuous objects, and, together with the spatula-like head, give
the whole embryo an almost comical appearance. The medullary canal has by
this time become completely closed in the region of the tail (figs. 8 and
8_b_).
It is still widely open in the region of the back, and, though more nearly
closed again in the neck, is, as I have said, flattened out to nothing in
the head.
The groove[15] between the two caudal lobes must not be confused (as may
easily be done) with the medullary groove, which by the time the former
groove has become conspicuous is a completely closed canal.
Footnote 15: This groove is the only structure which it seems
possible to compare with the so-called "primitive groove" of
Birds. It is, however, doubtful whether they are really
homologous.
The vertebral plates are not divided (vide fig. 7) into a somatopleuric and
splanchnopleuric layer by this stage, except in the region of the head
(vide fig. 8_b_, _pp_), where there is a distinct space between the two
layers, which is undoubtedly homologous with the pleuro-peritoneal cavity
of the hinder portion of the body.
It is probably the same cavity which Oellacher (_loc. cit._) calls in
Osseous fishes the pericardial cavity. In the Dog-fish, at least, it has no
connection with the pericardium. Of its subsequent history I shall say a
few words when I come to speak of the later stages.
The embryo does not take more than twenty-four hours in passing from this
stage, when the head is a flat plate, to the stage when the whole neural
canal (including the region of the head) is closed in. The other changes,
in addition to the closing in of the neural canal, are therefore somewhat
insignificant. The folding off of the embryo from the germ has, however,
progressed considerably, and a portion of the hind gut is closed in below.
This is accomplished, not by a tail-fold, as in Birds, but by two lateral
folds, which cause the sides of the body to meet and coalesce below. At the
extreme hind end, where the epiblast is continuous with the hypoblast, the
lateral folds turn round, so to speak, and become continuous with the
medullary folds, so that when the various folds meet each other an
uninterrupted canal is found passing round from the neural into the
alimentary canal, and placing these two in communication at the tail end of
the body. Since I have already mentioned this, and spoken of its
significance, I will not dwell on it further here.
The cranial flexure commences coincidently with the closing in of the
neural canal in the region of the brain, and the division into fore, mid,
and hind brain becomes visible at the same time as or even before the
closing of the canal occurs. The embryo has now become more or less
transparent, and protovertebræ, of which about twenty are present, can
_now_ be seen in the fresh specimens. The heart, however, is not yet
formed.
Up to this period, a period at which the embryo becomes very similar in
external appearance to any other vertebrate embryo, I have followed in my
description a chronological order. I shall now cease to do so, since it
would be too long for a preliminary notice of this kind, but shall confine
myself to the history of a few organs whose development is either more
important or more peculiar than that of the others.
_The Protovertebræ._
I have thought it worth while to give a short history of the development of
the protovertebræ, firstly, because it is very easy to follow this in the
Dog-fish, and, secondly, because I believe that the Dog-fish have more
nearly retained the primitive condition of the protovertebræ than any other
vertebrate whose embryology has hitherto been described with sufficient
detail.
I intend to describe, at the same time, the development of the spinal
nerves.
I left each lateral mass of mesoblast in my last stage as a plate which had
not yet become split into a somatic and a splanchnic sheet (Pl. 3,
fig. 8_a_, _vp_), but which had become cut by transverse lines (not,
indeed, extending to the outer limit of the sheet, but as yet not cut off
by longitudinal lines of cleavage) into segments, which I called
protovertebræ.
This sheet of mesoblast is fairly thick at its proximal (upper) end, but
thins off laterally to a sheet two cells deep, and its cells are so
arranged as to foreshadow its subsequent splitting into somatic and
splanchnic sheets. Its upper (proximal) end is at this stage level with the
bottom of the neural canal, but soon begins to grow upwards, and at the
same time the splitting into somatopleure and splanchnopleure commences
(Pl. 3, fig. 10, _so_ and _sp_).
The separation between the two sheets is first visible in its uppermost
part, and thence extends outwards. By this means each of the protovertebræ
becomes divided into two sheets, which are only connected at their upper
ends and outside the region of the body. I speak of the whole lateral sheet
as being composed of protovertebræ, because at this time no separation into
vertebral and lateral plates can be seen; but I may anticipate matters by
saying that only the upper portion of the sheet from the level of the top
of the digestive canal, becomes subsequently the true protovertebræ. From
this it is clear that the pleuro-peritoneal cavity extends primitively
quite up to the top of the protovertebræ; and that thus a portion of a
sheet of mesoblast, at first perfectly continuous with the splanchnic sheet
from which is derived the muscular wall of the alimentary canal, is
converted into a part of the voluntary muscular system of the body, having
no connection whatever with the involuntary muscular system of the
digestive tract.
The pleuro-peritoneal cavity is first distinctly formed at a time when only
two visceral clefts are present. Before the appearance of a third visceral
cleft in a part of the innermost layer of each protovertebræ (which may be
called the splanchnic layer, from its being continuous with the mesoblast
of the splanchnopleure), opposite the bottom of the neural tube, some of
the cells commence to become distinguishable from the rest, and to form a
separate mass. This mass becomes much more distinct a little later, its
cells being characterised by being spindle-shaped, and having an elongated
nucleus which becomes deeply stained by reagents (Pl. 4, fig. 11, _mp´_).
Coincidently with its appearance the young Dog-fish commences spontaneously
to move rapidly from side to side with a kind of serpentine motion, so
that, even if I had not traced the development of this differentiated mass
of cells till it becomes a band of muscles close to the notochord, I should
have had little doubt of its muscular nature. It is indicated in figs. 11,
12, 13, by the letters _mp´_. Its early appearance is most probably to be
looked upon as an adaptation consequent upon the respiratory requirements
of the young Dog-fish necessitating movements within the egg.
Shortly after this date, at a period when three visceral clefts are
present, I have detected the first traces of the spinal nerves.
At this time they appear in sections as small elliptical masses of cells,
entirely independent of the protovertebræ, and closely applied to the upper
and outer corners of the involuted epiblast of the neural canal (Pl. 4,
fig. 11, _spn_). These bodies are far removed from any mesoblastic
structures, and at the same time the cells composing them are _not_ similar
to the cells composing the walls of the neural canal, and are not attached
to these, though lying in contact with them. I have not, therefore,
sufficient evidence at present to enable me to say with any certainty where
the spinal nerves are derived from in the Dog-fish. They may be derived
from the involuted epiblast of the neural canal, and, indeed, this is the
most natural interpretation of their position.
On the other hand, it is possible that they are formed from wandering cells
of the mesoblast--a possibility which, with our present knowledge of
wandering cells, must not be thrown aside as altogether improbable.
In any case, it is clear that the condition in the Bird, where the spinal
nerves are derived from tissue of the protovertebræ, is not the primitive
one. Of this, however, I will speak again when I have concluded my account
of the development of the protovertebræ.
About the same time that the first rudiments of the nerves appear, the
division of the mesoblast of the sides of the body into a vertebral and a
lateral portion occurs. This division first appears in the region where the
oviduct (Müller's duct) is formed (Pl. 4, fig. 11, _ov_).
At this part opposite the level of the dorsal aorta the two sheets, viz.
the splanchnic and the somatic, unite together, and thus each lateral sheet
of mesoblast becomes divided into an upper portion (fig. 11, _mp_), split
up by transverse partitions into protovertebræ, and a lower portion not so
split, but consisting of an outer layer, the true somatopleure, and an
inner layer, the true splanchnopleure. These two divisions of the primitive
plate are thus separated by the line at which a fusion between the
mesoblast of the somatopleure and splanchnopleure takes place. The mass of
cells resulting from the fusion at this point corresponds with the
intermediate cell-mass of Birds (vide Waldeyer, _Eierstock und Ei_).
At the same time, in the upper of these two sheets (the protovertebræ), the
splanchnic layer sends a growth of cells inwards towards the notochord and
the neural canal. This growth is the commencement of the large quantity of
mesoblastic tissue around the notochord, which is in part converted into
the axial skeleton, and in part into the connective tissue adjoining this.
This mass of cells is at first quite continuous with the splanchnic layer
of the protovertebræ, and I see no reason for supposing that it is not
derived from the growth of the cells of this layer. The ingrowth to form it
first appears a little after the formation of the dorsal aorta; but, as far
as I have been able to see, its cells have no connection with the walls of
the aorta.
What I have said as to the development of the skeleton-forming layer will
be quite clear from figs. 11 and 12_a_; and from these it will also be
clear, especially from fig. 11_a_, that the outermost layer of this mass of
cells, which was the primitive splanchnic layer of the protovertebræ, still
retains its epithelial character, and so can easily be distinguished from
those cells which will form the skeleton. In the next stage which I have
figured (fig. 12_a_), this outer portion of the splanchnic layer is
completely separated from the skeleton-forming cells, and at the same time,
having united below as well as above with the outer (somatic) layer of the
two layers of which the protovertebræ are formed, the two together form an
independent mass (fig. 12, _mp_), similar in appearance and in every way
homologous with the muscle-plate of Birds.
On the inner side of this, which we may now call the muscle-plate, is seen
the bundle of earlier-developed muscles (fig. 12, _mp´_) which I spoke of
before.
The section represented in fig. 12 is from a very considerably later embryo
than that represented in fig. 11, so that the skeleton-forming cells, few
in number in the earlier section, have become very numerous in the later
one, and have grown up above the neural canal, and also below the
notochord, between the digestive canal and the aorta. They have, moreover,
changed their character; they were round before, now they have become
stellate. As to their further history, it need only be said that the layer
of them immediately around the notochord and neural canal forms the
cartilaginous centra and arches of the vertebræ, and that the remaining
portion of them, which becomes much more insignificant in size as compared
with the muscles, forms the connective tissue of the skeleton and of the
parts around and between the muscles.
A muscle-plate itself is at this stage (shewn in fig. 12) composed of an
inner and an outer layer of columnar cells (splanchnic and somatic) united
at the upper and lower ends of the plate, and on the inner of the two lies
the more developed mass of muscles before spoken of (_mp´_).
Each of these plates now grows both upwards and downwards; and at the same
time connective-tissue cells appear between the plates and epidermis; but
from where they come I do not know for certain; very probably they are
derived from the somatic layer of the muscle-plate.
While the muscle-plates continue to grow both upwards and downwards, the
cells of which they are composed commence to become elongated and soon
acquire an unmistakably muscular character (Pl. 4, fig. 13, _mp_).
Before this has occurred the inner mass of muscles has also undergone
further development and become a large and conspicuous band of muscles
close to the notochord (fig. 13, _mp´_).
At the same time that the muscle-plates acquire the true histological
character of muscle, septa of connective tissue grow in and divide them
into a number of distinct segments which subsequently form separate bands
of muscle. I will not say more in reference to the development of the
muscular system than that the whole of the muscles of the body (apart from
the limbs, the origin of whose muscular system I have not yet investigated)
are derived from the muscle-plates which grow upwards above the neural
canal and downwards to the ventral surface of the body.
During the time the muscle-plates have been undergoing these changes the
nerve masses have also undergone developmental changes.
They become more elongated and fibrous, their main attachment to the neural
tube being still at its posterior (dorsal) surface, near which they first
appeared. Later still they become applied closely to the sides of the
neural tube and send fibres to it below as well as above. Below (ventral
to) the neural tube a ganglion appears, forming only a slight swelling, but
containing a number of characteristic nerve-cells. The ganglion is
apparently formed just below the junction of the anterior and posterior
roots, though probably the fibres of the two roots do not mix till below
it.
The main points which deserve notice in the development of the
protovertebræ are--
(1) That at the time when the mesoblast becomes split horizontally into
somatopleure and splanchnopleure the vertebral and lateral plates are one,
and the splitting extends to the very top of the vertebral or muscle-plate,
so that the future muscle-plates are divided into a splanchnic and somatic
layer, the space between which is at first continuous with the
pleuro-peritoneal cavity.
(2) That the following parts are respectively formed by the vertebral and
lateral plates:
(_a_) Vertebral plate. From the splanchnic layer of this, or from cells
which appear close to and continuous with it, the skeleton, and connective
tissue of the upper part of the body, are derived.
The remainder of the plate, consisting of a splanchnic and somatic layer,
is entirely converted into the muscles of the trunk, all of which are
derived from it.
(_b_) Between the vertebral plate and the lateral plate is a mass of cells
where, as I mentioned above, the mesoblast of the somatopleure and
splanchnopleure fuse together. This mass of cells is the equivalent of the
_intermediate cell_ mass of Birds (vide Waldeyer, _Eierstock und Ei_).
From it are derived the Wolffian bodies and duct, the oviduct, the ovaries
and the testis, and the connective tissue of the parts adjoining these.
(_c_) The lateral plate. From the somatic layer of this is derived the
connective tissue of the ventral half of the body; the mesoblast of the
limbs, including probably the muscles, and certainly the skeleton. From its
splanchnic layer are derived the muscles and connective tissue of the
alimentary canal.
(3) The spinal nerves are developed independently of the protovertebræ, so
that the protovertebræ of the Elasmobranchii do not appear to be of such a
complicated structure as the protovertebræ of Birds.
_The Digestive Canal._
I do not intend to enter into the whole history of the digestive canal, but
to confine myself to one or two points of interest connected with it. These
fall under two heads:
(1) The history of the portion of the digestive canal between the anus and
the end of the tail where the digestive canal opens into the neural canal.
(2) Certain less well-known organs derived from the digestive canal.
The anus is a rather late formation, but its position becomes very early
marked out by the hypoblast of the digestive canal approaching at that
point close to the surface, whilst receding to some little distance from it
on either side. The portion of the digestive tract I propose at present
dealing with is that between this point, which I will call, for the sake of
brevity, the anus and the hind end of the body. This portion of the canal
is at first very short; it is elliptical in section, and of rather a larger
bore than the remainder of the canal. Its diameter becomes, however,
slightly less as it approaches the tail, dilating again somewhat at its
extreme end. It is lined by a markedly columnar epithelium. Though at first
very short, its length increases with the growth of the tail, but at the
same time its calibre continually becomes smaller as compared with the
remainder of the alimentary canal.
It commences to become smaller, first of all, near, though not quite, at
its extreme hind end, and thus becomes of a conical shape; the base of the
cone being just behind the anus, while the apex of the cone is situated a
short distance from the hind end of the embryo. The extreme hind end,
however, at the same time does not diminish in size, and becomes relatively
(if not also absolutely) much larger in diameter than it was at first, as
compared with the remainder of the digestive canal. It becomes, in fact, a
vesicle or vesicular dilatation at the end of a conical canal.
Just before the appearance of the external gills this part of the digestive
canal commences to atrophy. It begins to do so close to the terminal
vesicle, which, however, still remains as or more conspicuous than it was
before. The lumen of the canal becomes smaller and smaller, and finally it
becomes a solid string of cells, and these also soon become
indistinguishable and not a trace of the canal is left.
Almost the whole of it has disappeared before the vesicle begins to
atrophy, but very shortly after all trace of the rest of the canal has
vanished the terminal vesicle also vanishes. This occurs just about the
time or shortly after the appearance of the external gills--there being
slight differences probably in this respect in the different species.
In this history there are two points of especial interest:
(1) The terminal vesicle.
(2) The disappearance of a large and well-developed portion of the
alimentary canal.
The interest in the terminal vesicle lies in the possibility of its being
some rudimentary structure.
In Osseous fishes Kupffer has described the very early appearance of a
vesicle near the tail end, which he doubtfully speaks of as the
"allantois." The figure he gives of it in his earlier paper (_Archiv. für
Micro. Anat._ Vol. II. pl. xxiv, fig. 2) bears a very strong resemblance to
my figures of this vesicle at the time when the hind end of the alimentary
canal is commencing to disappear; and I feel fairly confident that it is
the same structure as I have found in the Dog-fish: but until the relations
of the Kupffer's vesicle to the alimentary canal are known, any comparison
between it and the terminal vesicle in the Dog-fish must be to a certain
extent guess-work.
I have, however, been quite unsuccessful in finding any other vesicular
structure which can possibly correspond to the so-called allantoic vesicle
of Osseous fish.
The disappearance of a large portion of the alimentary canal behind the
anus is very peculiar. In order, however, to understand the whole
difficulties of the case I shall be obliged to speak of the relations of
the anus of the Dog-fish to the anus of Rusconi in the Lamprey, &c.
In those vertebrates whose alimentary canal is formed by an involution, the
anus of Rusconi represents the opening of this involution, and therefore
the point where the alimentary canal primitively communicates with the
exterior. When, however, the "anus of Rusconi" becomes _closed_, the wall
of the alimentary canal still remains at that point in close juxtaposition
to the surface, and the new and final anus is formed at or close to that
point. In the Dog-fish, although the anus of Rusconi is not present, still,
during the closing of the alimentary canal, the point which would
correspond with this becomes marked out by the alimentary canal there
approaching the surface, and it is at this point that the involution to
form the true anus subsequently appears.
The anus in the Dog-fish has thus, more than a mere secondary significance.
It corresponds with the point of closing of the primitive involution. If it
was not for this peculiarity of the vertebrate anus we would naturally
suppose, from the disappearance of a considerable portion of the alimentary
canal lying behind its present termination, that in the adult the
alimentary canal once extended much farther back than at present, and that
the anus we now find was only a secondary anus, and not the primitive one.
It is perhaps possible that this hinder portion of the alimentary canal is
a result of the combined growth of the tail and the persisting continuity
(at the end of the body) of the epiblast with the hypoblast.
Whichever view is correct, it may be well to mention, in order to shew that
the difficulty about the anus of Rusconi is no mere visionary one, that
Götte ("Untersuchung über die Entwicklung der Bombinator igneus," _Archiv.
für Micro. Anat._, vol. V. 1869) has also described the disappearance of
the hind portion of the alimentary canal in Batrachians, a rudiment
(according to him) remaining in the shape of a lymphatic trunk.
It is, perhaps, possible that we have a further remnant of this "hind
portion" of the alimentary canal amongst the higher vertebrates in the
"allantois."
_Organs developed from the Digestive Canal._
In reference to the development of the liver, pancreas, &c., as far as my
observations have at present gone, the Dog-fish presents no features of
peculiar interest. The liver is developed as in the Bird, and independently
of the yolk.
There are, however, two organs derived from the hypoblast which deserve
more attention. Immediately under the notochord, and in contact with it
(vide Pl. 3, fig. 10; Pl. 4, figs. 11 and 12, _x_), a small roundish (in
section) mass of cells is to be seen in most of the sections.
Its mode of development is shewn in fig. 10, _x_. That section shows a mass
of cells becoming pinched off from the top of the alimentary canal. By this
process of pinching off from the alimentary canal a small rod-like body
close under the notochord is formed. It persists till after the appearance
of the external gills, but later than that I have not hitherto succeeded in
finding any trace of it.
It was first seen by Götte (_loc. cit._) in the Batrachians, and he gave a
correct account of its development, and added that it became the thoracic
duct.
I have not myself worked out the later stages in the development of this
body with sufficient care to be in a position to judge of the correctness
of Götte's statements as to its final fate. If it is true that it becomes
the thoracic duct it is very remarkable, and ought to throw some light upon
the homologies of the lymphatic system.
Some time before the appearance of the external gills another mass of cells
becomes, I believe, constricted off from the part of the alimentary canal
in the neighbourhood of the anus, and forms a solid rod composed at first
of dark granular cells lying between the Wolffian ducts. I have not
followed out its development quite completely, but I have very little doubt
that it is really constricted off from a portion of the alimentary canal
chiefly in front of the point where the anus appears, but also, I believe,
from a small portion behind this.
Though the cells of which it is composed are at first columnar and granular
(fig. 12, _su_, _r_), they soon begin to become altered, and in the latter
stage of its development the body forms a conspicuous rounded mass of cells
with clear protoplasm, and each provided with a large nucleus. Later still
it becomes divided into a number of separate areas of cells by septa of
connective tissue, in which (the septa) capillaries are also present. Since
I have not followed it to its condition in the adult, I cannot make any
definite statements as to the fate of this body; but I think that it
possibly becomes the so-called suprarenal organ, which in the Dog-fish
forms a yellowish elongated body lying between the two kidneys.
_The development of the Wolffian Duct and Body and of the Oviduct._
The development of the Wolffian duct and the Oviduct in the various classes
of vertebrates is at present involved in some obscurity, owing to the very
different accounts given by different observers.
The manner of development of these parts in the Dog-fish is different from
anything that previous investigators have met with in other classes, but I
believe that it gives a clearer insight into the true constitution of these
parts than vertebrate embryology has hitherto supplied, and at the same
time renders easier the task of understanding the differences in the modes
of development in the different classes.
I shall commence with a simple description of the observed facts, and then
give my view as to their meaning. At about the time of the appearance of
the third visceral cleft, and a short way behind the point up to which the
alimentary canal is closed in front, the splanchnopleure and somatopleure
fuse together opposite the level of the dorsal aorta.
From the mass of cells formed by this fusion a solid knob rises up towards
the epiblast (Pl. 4, fig. 11_b_, _ov_), and from this knob a solid rod of
cells grows backwards towards the tail (fig. 11_c_, _ov_) very closely
applied to the epiblast. This description will be rendered clear by
referring to figs. 11_b_ and _c_. Fig. 11_b_ is a section at the level of
the knob, and fig. 11_c_ is a section of the same embryo a short way behind
this point. So closely does the rod of cells apply itself to the epiblast
that it might very easily be supposed to be derived from it. Such, indeed,
was at first my view till I cut a section passing through the knob. In
order, however, to avoid all possibility of mistake I made sections of a
large number of embryos of about the age at which this appears, and
_invariably found_ the large knob in front, and from it the solid string
growing backwards.
This string is the commencement of the _Oviduct_ or _Müller's duct_, which
in the Dog-fish as in the Batrachians is the first portion of the
genito-urinary system to appear, and is in the Dog-fish undoubtedly at
first solid. All my specimens have been hardened with osmic acid, and with
specimens hardened with this reagent it is quite easy to detect even the
very smallest hole in a mass of cells.
As a solid string or rod of cells the Oviduct remains for some time; it
grows, indeed, rapidly in length, the extreme hind end of the rod being
very small and the front end continuing to remain attached to the knob. The
knob, however, travels inwards and approaches nearer and nearer to the true
pleuro-peritoneal cavity, always remaining attached to the intermediate
cell mass.
At about the time when five visceral clefts are present the Oviduct first
begins to get a lumen and to open at its front end into the
pleuro-peritoneal cavity. The cells of the rod are first of all arranged in
an irregular manner, but gradually become columnar and acquire a radiating
arrangement around a central point. At this point, where the ends of all
the cells meet, a very small hole appears, which gradually grows larger and
becomes the cavity of the duct (fig. 12, _ov_). The hole first makes its
appearance at the anterior end of the duct, and then gradually extends
backwards, so that the hind end is still without a lumen, when the lumen of
the front end is of a considerable size.
At the front knob the same alteration in the cells takes place as in the
rest of the duct, but the cells become deficient on the side adjoining the
pleuro-peritoneal cavity, so that an opening is formed into the
pleuro-peritoneal cavity, which soon becomes of a considerable size. Soon
after its first formation, indeed, the opening becomes so large that it may
be met in from two to three consecutive sections if these are very thin.
Thus is formed the lumen of the Oviduct. The duct still, at this age, ends
behind without having become attached to the cloaca, so that at this time
the Oviduct is a canal closed behind, but communicating in front by a large
opening with the pleuro-peritoneal cavity.
It has during this time been travelling downwards, and is now much nearer
the pleuro-peritoneal cavity than the epiblast.
It may be well to point out that the mode of development which I have
described is really not very different from an involution, and must, in
fact, be only looked upon as a modification of an involution. Many examples
from all classes in the animal kingdom could be selected to exemplify how
an involution may become simply a solid thickening. In the Osseous fish
nearly all the organs which are usually formed by an involution have
undergone this change in their mode of development. I shall attempt to give
reasons later on for the solid form having been acquired in this particular
case of the Oviduct.
At about the time when a lumen appears in the Oviduct the first traces of
the Wolffian duct become visible.
At intervals along the whole length, between the front and hind ends of the
Oviduct, involutions arise from the pleuro-peritoneal cavity (fig. 12_a_,
_pwd_) on the inside (nearer the middle line) of the Oviduct. The upper
ends of these numerous involutions unite together and form a string of
cells, at first solid, but very soon acquiring a lumen, and becoming a duct
which communicates (as it clearly must from its mode of formation), at
numerous points with the pleuro-peritoneal cavity. It is very probable that
there is one involution to each segment of the body between the front and
hind ends of the Oviduct. This duct is the Wolffian duct, which thus,
together with the Oviduct, is formed before the appearance of the external
gills.
For a considerable period the front end of the Oviduct does not undergo
important changes; the hind end, however, comes into connection with the
extreme end of the alimentary canal. The two Oviducts do not open together
into the cloaca, though, as my sections prove, their openings are very
close together. The whole Oviduct, as might be expected, shares in the
general growth, and its lumen becomes in both sexes very considerably
greater than it was before.
It is difficult to define the period at which I find these changes
accomplished without giving drawings of the whole embryo. The stage is one
considerably after the external gills have appeared, but before the period
at which the growth of the olfactory bulbs renders the head of an elongated
shape.
During the same period the Wolffian duct has undergone most important
changes. It has commenced to bud off diverticula, which subsequently become
the tubules of the Wolffian body (vide fig. 13, _wd_). I am fairly
satisfied that the tubules are really budded off, and are not formed
independently in the mesoblast. The Dog-fish agrees so far with Birds,
where I have also no doubt the tubules of the Wolffian body are formed as
diverticula from the Wolffian duct.
The Wolffian ducts have also become much longer than the Oviduct, and are
now found behind the anus, though they do not extend as far forward as does
the Oviduct.
They have further acquired a communication with the Oviduct, in the form of
a narrow duct passing from each of them into an Oviduct a short way before
the latter opens into the cloacal dilatation of the alimentary canal.
The canals formed by the primitive involution leading from the
pleuro-peritoneal cavity into the Wolffian duct have become much more
elongated, and at the same time narrower. One of these is shewn in fig. 13,
_pwd_.
Any doubt which could possibly be entertained as to the true character of
the ducts whose development I have described is entirely removed by the
development of the tubules of the Wolffian body. In the still later stage
than this further proofs are furnished involving the function of the
Oviduct. At the period when the olfactory lobes have become so developed as
to render the head of the typical elongated shape of the adult, I find that
the males and females can be distinguished by the presence in the former of
the clasping appendages[16]. I find at this stage that in the female the
front ends of the Oviducts have approached the middle line, dilated
considerably, and commenced to exhibit at their front ends the
peculiarities of the adult. In the male they are much less conspicuous,
though still present.
Footnote 16: For the specimens of this age I am indebted to
Professor Huxley.
At the same time the tubules of the Wolffian body become much more
numerous, the Malpighian tufts appear, and the ducts cease almost, if not
entirely, to communicate with the pleuro-peritoneal cavity. I have not made
out anything very definitely as to the development of the Malpighian tufts,
but I am inclined to believe that they arise independently in the mesoblast
of the intermediate cell mass.
The facts which I have made out in reference to the development of the
Wolffian duct, especially of its arising as a _series of involutions_ from
the pleuro-peritoneal cavity, will be found, I believe, of the greatest
importance in understanding the true constitution of the Wolffian body. To
this I will return directly, but first wish to clear the ground by
insisting upon one preliminary point.
From their development the Oviduct and Wolffian body appear to stand to
each other in the relation of the Wolffian duct being the equivalent to a
series, so to speak, of Oviducts.
I pointed out before that the mode of development of the Oviduct could only
be considered as a modification of a simple involution from the
pleuro-peritoneal cavity. Its development, both in the Birds and in the
Batrachians as an involution, still more conclusively proves the truth of
this view.
The explanation of its first appearing as a solid rod of cells which keeps
close to the epiblast is, I am inclined to think, the following. Since the
Oviduct had to grow a long way backwards from its primitive point of
involution, it was clearly advantageous for it not to bore its way through
the mesoblast of the intermediate cell mass, but to pass between this and
the epiblast. This modification having been adopted, was followed by the
knob forming the origin of the duct coming to be placed at the outside of
the intermediate cell mass rather than close to the pleuro-peritoneal
cavity, a change which necessitated the mode of development by an
involution being dropped and the solid mode of development substituted for
it, a lumen being only subsequently acquired.
In support of the modification in the development being due to this cause
is the fact that in Birds a similar modification has taken place with the
Wolffian duct. The Wolffian duct there arises differently from its mode of
development in all the lower vertebrates as a solid rod close to the
epiblast[17], instead of as an involution.
Footnote 17: If Romiti's observations (_Archives für Mikr.
Anatom._ Vol. IX. p. 200) are correct, then the ordinary view
of the Wolffian duct arising in Birds as a solid rod at the
outer corner of the protovertebræ will have to be abandoned.
If the above explanation about the Oviduct be correct, then it is clear
that similar causes have produced a similar modification in development
(only with a different organ) in Birds; while, at the same time, the
primitive mode of origin of the Oviduct (Müller's duct) has been retained
by them.
The Oviduct, then, may be considered as arising by an involution from the
pleuro-peritoneal cavity.
The Wolffian duct arises by a series of such involutions, all of which are
behind (nearer the tail) the involution to form the Oviduct.
The natural interpretation of these facts is that in the place of the
Oviduct and Wolffian body there were primitively a series of similar bodies
(probably corresponding in number with the vertebral segments), each
arising by an involution from the pleuro-peritoneal cavity; and that the
first of these subsequently became modified to carry eggs, while the rest
coalesced to form the Wolffian duct.
If we admit that the Wolffian duct is formed by the coalescence of a series
of similar organs, we shall only have to extend the suggestion of Gegenbaur
as to the homology of the Wolffian body in order to see its true nature.
Gegenbaur looks upon the whole urinogenital system as homologous with a
pair of segmental organs. Accepting its homology with the segmental organs,
its development in Elasmobranchii proves that it is not one pair, but a
series of pairs of segmental organs with which the urinogenital system is
homologous. The first of these have become modified so as to form the
Oviducts, and the remainder have coalesced to form the Wolffian ducts.
The part of a segmental organ which opens to the exterior appears to be
lost in the case of all but the last one, where this part is still
retained, and serves as the external opening for all.
Whether the external opening of the first segmental organ (Oviduct) is
retained or not is doubtful. Supposing it has been lost, we must look upon
the external opening for the Wolffian body as serving also for the Oviduct.
In the case of all other vertebrates whose development has been
investigated (but the Elasmobranchii), the Wolffian duct arises by a single
involution, or, what is equivalent to it, the other involutions having
disappeared. This even appears to be the case in the Marsipobranchii. In
the adult Lamprey the Wolffian duct terminates at its anterior end by a
large ciliated opening into the pleuro-peritoneal cavity. It will, perhaps,
be found, when the development of the Marsipobranchii is more carefully
studied, that there are _primitively_ a number of such openings[18]. The
Oviduct, when present, arises in other vertebrates as a single involution,
strongly supporting the view that its mode of formation in the Dog-fish is
fundamentally merely an involution.
Footnote 18: While correcting the proofs of this paper I have
come across a memoir of W. Müller ("Ueber die Persistenz der
Urniere bei Myxine Glutinosa," _Jenaische Zeitschrift_,
Vol. VII. 1873), in which he mentions that in Myxine the upper
end of the Wolffian duct communicates by numerous openings with
the pleuro-peritoneal cavity; this gives to the suggestion in
the text a foundation of fact.
The duct of the testes is, I have little doubt, derived from the anterior
part of the Wolffian body; if so, it must be looked upon as not precisely
equivalent to the Oviduct, but rather to a series of coalesced organs, each
equivalent to the Oviduct. The Oviduct is in the Elasmobranchii, as in
other vertebrates, primitively developed in both sexes. In the male,
however, it atrophies. I found it still visible in the male Torpedos,
though much smaller than in the females near the close of intra-uterine
life.
Whether or not these theoretical considerations as to the nature of the
Wolffian body and Oviduct are correct, I believe that the facts I have
brought to light in reference to the development of these parts in the
Dog-fish will be found of service to every one who is anxious to discover
the true relations of these parts.
Before leaving the subject I will say one or two words about the
development of the Ovary. In both sexes the germinal epithelium (fig. 13)
becomes thickened below the Oviduct, and in both sexes a knob (in section
but really a ridge) comes to project into the pleuro-peritoneal cavity on
each side of the mesentery (fig. 13, _pov_). In both sexes, but especially
the females, the epithelium on the upper surface of this ridge becomes very
much thickened, whilst subsequently it elsewhere atrophies. In the females,
however, the thickened epithelium on the knob grows more and more
conspicuous, and develops a number of especially large cells with large
nuclei, precisely similar to Waldeyer's (_loc. cit._) "primitive ova" of
the Bird. In the male the epithelium on the ridge, though containing
primitive ova, is not as conspicuous as in the female. Though I have not
worked out the matter further than this at present, I still have no doubt
that these projecting ridges become the Ovaries.
_The Head._
The study of the development of the parts of the head, on account of the
crowding of organs which occurs there, always presents greater difficulties
to the investigator than that of the remainder of the body. My observations
upon it are correspondingly incomplete. I have, however, made out a few
points connected with it in reference to some less well-known organs, which
I have thought it worth while calling attention to in this preliminary
account.
_The continuation of the Pleuro-peritoneal Cavity into the Head._
In the earlier part of this paper (p. 86) I called attention to the
extension of the separation between somatopleure and splanchnopleure into
the head, forming a space continuous with the pleuro-peritoneal cavity
(Pl. 3, fig. 8_a_, _pp_); this becomes more marked in the next stage, and,
indeed, the pleuro-peritoneal cavity is present for a considerable time in
the head before it becomes visible elsewhere. At the time of the appearance
of the second visceral cleft it has become for the most part atrophied, but
there persist two separated portions of it in front of the first cleft, and
also remnants of it less well marked between and behind the two clefts. The
visceral clefts necessarily divide it into separate parts.
The two portions in front of the first visceral cleft remain very
conspicuous till the appearance of the external gills, and above the hinder
one of the two the fifth nerve bifurcates.
These two are shewn as they appear in a surface view in fig. 14, _pp_. They
are in reality somewhat flattened spaces, lined by a mesoblastic
epithelium; the epithelium on the inner surface of the space corresponding
to the splanchnopleure, and that on the outer to the somatopleure.
I have not followed the history of these later than the time of the
appearance of the external gills.
The presence of the pleuro-peritoneal cavity in the head is interesting, as
shewing the fundamental similarity between the head and the remainder of
the body.
_The Pituitary Body._
All my sections seem to prove that it is a portion of the epiblastic
involution to form the mouth which is pinched off to form the pituitary
body, and not a portion of the hypoblast of the throat. Since Götte
(_Archiv. für Micr. Anat._ Bd. IX.) has also found that the same is the
case with the Batrachians and Mammalia, I have little doubt it will be
found to be universally the case amongst vertebrates.
Probably the observations which lead to the supposition that it was the
throat which was pinched off to form the pituitary body were made after the
opening between the mouth and throat was completed, when it would naturally
be impossible to tell whether the pinching off was from the epiblast of the
mouth involution or the hypoblast of the throat.
_The Cranial Nerves._
The cranial nerves in their early condition are so clearly visible that I
have thought it worth while giving a figure of them, and calling attention
to some points about their embryonic peculiarities.
From my figure (14) it will be seen that there is behind the auditory
vesicle a nervous tract, from which four nerves descend, and that each of
these nerves is distributed to the front portion of a visceral arch. When
the next and last arch (in this species) is developed, a branch from this
nervous mass will also pass down to it. That each of these is of an equal
morphological value can hardly be doubted.
The nerve to the third arch becomes the glosso-pharyngeal (fig. 14, _gl_),
the nerves to the other arches become the branchial branches of the vagus
nerve (fig. 14, _vg_). Thus the study of their development strongly
supports Gegenbaur's view of the nature of the vagus and glosso-pharyngeal,
viz. that the vagus is a compound nerve, each component part of it which
goes to an arch being equivalent to one nerve, such as the
glosso-pharyngeal.
Of the nerves in front of the auditory sac the posterior is the seventh
nerve (fig. 14, VII). Its mode of distribution to the second arch leaves
hardly a doubt that it is equivalent to one such nerve as those distributed
to the posterior arches. Subsequently it acquires another branch, passing
forwards towards the arch in front.
The most anterior nerve is the fifth (fig. 14, V), of which two branches
are at this stage developed. The natural interpretation of its present
condition is, that it is equivalent to two nerves, but the absence of
relation in its branches to any visceral clefts renders it more difficult
to determine the morphology of the fifth nerve than of the other nerves.
The front branch of the two is the ophthalmic branch of the adult, and the
hind branch the inferior maxillary branch. The latter branch subsequently
gives off low down, _i.e._ near its distal extremity, another branch, the
superior maxillary branch.
In its embryonic condition this latter branch does not appear like a third
branch of the fifth, equivalent to the seventh or the glosso-pharyngeal
nerves, but rather resembles the branch of the seventh nerve which passes
to the arch in front, which also is present in all the other cranial
nerves.
_Modes of Preparation._
Before concluding I will say one or two words as to my modes of
preparation.
I have used picric and chromic acids, both applied in the usual way; but
for the early stages I have found osmic acid by far the most useful
reagent. I placed the object to be hardened, in osmic acid (half per cent.)
for two hours and a half, and then for twenty four in absolute alcohol.
I then embedded and cut sections of it in the usual way, without staining
further.
I found it advantageous to cut sections of these embryos immediately after
hardening, since if kept for long in the absolute alcohol the osmic acid
specimens are apt to become brittle.
LIST OF WORKS REFERRED TO.
Gegenbaur. _Anat. der Wirbelthiere_, III Heft, Leipzig, 1873.
A. Götte. _Archiv. für Micr. Anat._, Vol. X. 1873. "Der Keim der
Forelleneies," _Archiv. für. Micr. Anat._, Vol. IX. 1873. "Untersuchung
über die Entwicklung der Bombinator igneus," _Archiv. für Micr. Anat._,
Vol. V. 1869. "Kurze Mittheilungen aus der Entwicklungsgeschichte der
Unke," _Archiv. für Micr. Anat._, Vol. IX. 1873.
Kupffer. _Archiv. für Micr. Anat._, Vol. II. 1866, p. 473. Ibid. Vol. IV.
1868, p. 209.
Kowalevsky. "Entwicklungsgeschichte der Holothurien," _Mémoires de l'Acad.
Impér. des Sciences de St Petersbourg_, vii ser. Vol. XI. 1867.
Kowalevsky, Owsjannikow, und Wagner. "Entwicklung der Störe," _Bulletin der
K. Acad. St Petersbourg_, Vol. XIV. 1873.
Kowalevsky. "Embryologische Studien an Würmern und Arthropoden," _Mémoirs
de l'Acad. Impér. des Sciences de St Petersbourg_, Vol. XVI. 1871.
E. Ray Lankester. _Annals and Mag. of Nat. History_, Vol. XI. 1873, p. 81.
W. Müller. "Ueber die Persistenz der Urniere bei Myxine Glutinosa,"
_Jenaische Zeitschrift_, Vol. VII. 1873.
Oellacher. _Zeitschrift für Wiss. Zoologie_, Vol. XXIII. 1873.
Owsjannikow. "Entwicklung der Coregonus," _Bul. der K. Akad. St
Petersbourg_, Vol. XIX.
Romiti. _Archiv. für Micr. Anat._, Vol. IX. 1873.
Waldeyer. _Eierstock u. Eie._
EXPLANATION OF PLATES 3 AND 4.
COMPLETE LIST OF REFERENCE LETTERS.
_al._ Alimentary canal. _ao._ Dorsal aorta. _auv._ Auditory vesicle. _bd._
Formative cell probably derived from the yolk. _cav._ Cardinal vein. _ch._
Notochord. _ch´._ Thickening of hypoblast to form the notochord. _eb._ Line
indicating the edge of the blastoderm. _ep._ Epiblast. _ep´._ Epidermis.
_er._ Embryonic rim. _es._ Embryonic swelling. _gl._ Glosso-pharyngeal
nerve. _h._ Head. _ht._ Heart. _hy._ Hypoblast. _ll._ Lower layer cells.
_ly._ Line of separation between the blastoderm and the yolk. _m._
Mesoblast. _mc._ Medullary canal. _mg._ Medullary groove. _mp._
Muscle-plate. _mp´._ Early formed mass of muscles. _n._ Peculiar nuclei
formed in the yolk. _n´._ Similar nuclei in the cells of the blastoderm.
_na._ Cells which help to close in the alimentary canal, and which are
derived from the yolk. _ny._ Network of lines present in the food-yolk.
_ol._ Olfactory pit. _op._ Eye. _ov._ Oviduct. _pn._ Pineal gland. _pov._
Projection which becomes the ovary. _pp._ Pleuro-peritoneal cavity. _pp´._
Remains of pleuro-peritoneal cavity in the head. _prv._ Protovertebræ.
_pwd._ Primary points of involution from the pleuro-peritoneal cavity by
the coalescence of which the Wolffian duct is formed. _sg._ Segmentation
cavity. _so._ Somatopleure. _sos._ Stalk connecting embryo with yolk-sac.
_sp._ Splanchnopleure. _spn._ Spinal nerve. _sur._ Suprarenal body. _ts._
Caudal lobes. _v._ Blood-vessel. _vg._ Vagus nerve. V. Fifth nerve. VII.
Seventh nerve. _vc_, 1, 2, 3, &c. 1st, 2nd and 3rd &c. visceral clefts.
_vp._ Vertebral plates. _wd._ Wolffian duct. _x._ Peculiar body underlying
the notochord derived from the hypoblast. _yk._ Yolk spherules.
All the figures were drawn with the Camera Lucida.
Plate 3.
Fig. 1. Section parallel with the long axis of the embryo through a
blastoderm, in which the floor of the segmentation cavity (_sg_) is not yet
completely lined by cells. The roof of the segmentation cavity is broken.
(Magnified 60 diam.) The section is intended chiefly to illustrate the
distribution of nuclei (_n_) in the yolk under the blastoderm. One of the
chief points to be noticed in their distribution is the fact that they form
almost a complete layer under the floor of the segmentation cavity. This
probably indicates that the cells whose nuclei they become take some share
in forming the layer of cells which subsequently (vide fig. 4) forms the
floor of the cavity.
Fig. 2. Small portion of blastoderm and subjacent yolk of an embryo at the
time of the first appearance of the medullary groove. (Magnified 300 diam.)
The specimen is taken from a portion of the blastoderm which will form part
of the embryo. It shews two large nuclei of the yolk (_n_) and the network
in the yolk between them; this network is seen to be closer around the
nuclei than in the intervening space. The specimen further shews that there
are no areas representing cells around the nuclei.
Fig. 3. Section parallel with the long axis of the embryo through a
blastoderm, in which the floor of the segmentation cavity is not yet
covered by a complete layer of cells. (Magnified 60 diam.)
It illustrates (1) the characters of the epiblast, (2) the embryonic
swelling (_es_), (3) the segmentation cavity (_sg_). It should have been
drawn upon the same scale as fig. 4; the line above it represents its true
length upon this scale.
Fig. 4. Longitudinal section through a blastoderm at the time of the first
appearance of the embryonic rim, and before the formation of the medullary
groove. (Magnified 45 diam.)
It illustrates (1) the embryonic rim, (2) the continuity of epiblast and
hypoblast at edge of this, (3) the continual differentiation of the lower
layer cells, to form, on the one hand, the hypoblast, which is continuous
with the epiblast, and on the other the mesoblast, between this and the
epiblast; (4) the segmentation cavity, whose floor of cells is now
completed.
N.B. The cells at the embryonic end of the blastoderm have been made rather
too large.
Fig. 5. Surface view of the blastoderm shortly after the appearance of the
medullary groove. To shew the relation of the embryo to the blastoderm.
Fig. 6_a_ and _b_. Two transverse sections of the same embryo, shortly
after the appearance of the medullary groove. (Magnified 96 diam.)
_a._ In the region of the groove. It shews (1) the two masses of mesoblast
on each side, and the deficiency of the mesoblast underneath the medullary
groove; (2) the commencement of the closing in of the alimentary canal
below, chiefly from cells (_na_) derived from the yolk.
_b._ Section in the region of the head where the medullary groove is
deficient, other points as above.
Fig. 7_a_ and _b_. Two transverse sections of an embryo about the age or
rather younger than that represented in fig. 5. (Magnified 96 diam.)
_a._ Section nearer the tail; it shews the thickening of the hypoblast to
form the notochord (_ch´_).
In _b_ the thickening has become completely separated from the hypoblast as
the notochord. In _a_ the epiblast and hypoblast are continuous at the edge
of the section, owing to the section passing through the embryonic rim.
Fig. 8. Surface view of a spatula-shaped embryo. The figure shews (1) the
flattened head (_h_) where the medullary groove is deficient, (2) the
caudal lobes, with a groove between them; it also shews that at this point,
the medullary groove has become roofed over and converted into a canal.
Fig. 8_a_. Transverse section of fig. 8, passing through the line _a_.
(Magnified 90 diam.) The section shews (1) the absence of the medullary
groove in the head and the medullary folds turning down at this time
instead of upwards; (2) the presence of the pleuro-peritoneal cavity in the
head (_pp_); (3) the completely closed alimentary canal (_al_).
Fig. 8_b_. Transverse section of fig. 8, through the line _b_. (Magnified
90 diam.) It shews (1) the neural canal completely formed; (2) the
vertebral plates of mesoblast not yet split up into somatopleure and
splanchnopleure.
Fig. 9. Side view of an embryo of the Torpedo, seen as a transparent object
a little older than the embryo represented in fig. 8. (Magnified 20 diam.)
The internal anatomy has hardly altered, with the exception of the
medullary folds having closed over above the head and the whole embryo
having become more folded off from the germ.
The two caudal lobes, and the very marked groove between them, are seen at
_ts_. The front end of the notochord became indistinct, and I could not see
its exact termination. The epithelium of the alimentary canal (_al_) is
seen closely underlying the notochord and becoming continuous with the
epiblast at the hind end of the notochord.
The first visceral cleft (1_vc_) and eye (_op_) are just commencing to be
formed, and the cranial flexure has just appeared.
Fig. 10. Section through the dorsal region of an embryo somewhat older than
the one represented in fig. 9. (Magnified 96 diam.)
It shews (1) the formation by a pinching off from the top of the alimentary
canal of a peculiar body which underlies the notochord (_x_); (2) the
primitive extension of the pleuro-peritoneal cavity up to the top of the
vertebral plates.
Plate 4.
Fig. 11_a_, _b_, and _c_. Three sections closely following each other from
an embryo in which three visceral clefts are present; _a_ is the most
anterior of the three. (Magnified 96 diam.) In all of these the
muscle-plates are shewn at _mp_. They have become separated from the
lateral plates in _b_ and _c_, but are still continuous with them in _a_.
The early formed mass of muscles is also shewn in all the figures (_mp´_).
The figures further shew (1) the formation of the spinal nerves (_spn_) as
small bodies of cells closely applied to the upper and outer edge of the
neural canal.
(2) The commencing formation of the cells which form the axial skeleton
from the inner (splanchnopleuric) layer of the muscle-plate. Sections _b_
and _c_ are given more especially to shew the mode of formation of the
oviduct (_ov_).
In _b_ it is seen as a _solid knob (ov)_, arising from the point where the
somatopleure and splanchnopleure unite, and in _c_ (the section behind _b_)
as a _solid rod (ov)_ closely applied to the epiblast, which has grown
backwards from the knob seen in _b_.
N.B. In all three sections only one side is completed.
Fig. 12_a_ and _b_. Two transverse sections of an embryo just before the
appearance of the external gills. (Magnified 96 diam.)
In _a_ there is seen to be an involution on each side (_pwd_), while _b_ is
a section from the space between two involutions from the pleuro-peritoneal
cavity, so that the Wolffian duct (at first solid) (_wd_) is not connected
as in _a_ with the pleuro-peritoneal cavity. The further points shewn in
the sections are--
(1) The commencing formation of the spiral valve (_al_).
(2) The suprarenal body (_sur_).
(3) The oviduct (_ov_), which has acquired a lumen.
(4) The increase in length of the muscle-plates, the spinal nerves,
&c.
Fig. 13. Section through the dorsal region of an embryo in which the
external gills are of considerable length. (Magnified 40 diam.) The chief
points to be noticed:
(1) The formation of the Wolffian body by outgrowths from
the Wolffian duct (_wd_).
(2) One of the still continuing connections (primitive
involutions) between the Wolffian duct and the
pleuro-peritoneal cavity (_pwd_).
(3) The oviduct largely increased in size (_ov_).
N.B. On the left side the oviduct has been accidentally made
too small.
(4) The growth downwards of the muscle-plate to form the
muscles of the abdomen.
(5) The formation of an outgrowth on each side of the
mesentery (_pov_), which will become the ovary.
(6) The spiral valve (_al_).
Fig. 14. Transparent view of the head of an embryo shortly before the
appearance of the external gills. (Magnified 20 diam.) The chief points to
be noticed are--
(1) The relation of the cranial nerves to the visceral
clefts and the manner in which the glosso-pharyngeal (_gl_)
and vagus (_vg_) are united.
(2) The remnants of the pleuro-peritoneal cavity in the head
(_pp_).
(3) The eye (_op_). The stalk, as well as the bulb of the
eye, are supposed to be in focus, so that the whole eye has
a somewhat peculiar appearance.
VI. A COMPARISON OF THE EARLY STAGES IN THE DEVELOPMENT OF VERTEBRATES[19].
Footnote 19: From the _Quarterly Journal of Microscopical
Science_, Vol. XV. 1875.
With Plate 5.
If the genealogical relationships of animals are to be mainly or largely
determined on embryological evidence, it becomes a matter of great
importance to know how far evidence of this kind is trustworthy.
The dependence to be placed on it has been generally assumed to be nearly
complete. Yet there appears to be no _à priori_ reason why natural
selection should not act during the embryonic as well as the adult period
of life; and there is no question that during their embryonic existence
animals are more susceptible to external forces than after they have become
full grown: indeed, an immense mass of evidence could be brought to shew
that these forces do act upon embryos, and produce in them great
alterations tending to obscure the genealogical inferences to be gathered
from their developmental histories. Even the time-honoured layers form to
this no exception. In _Elasmobranchii_, for instance, we find the notochord
derived from the hypoblast and the spinal ganglia derived from the
involuted epiblast of the neural canal, whilst in the higher vertebrates
both of these organs are formed in the mesoblast. Such instances are
leading embryologists to recognise the fact that the so-called layers are
not quite constant and must not be absolutely depended upon in the
determination of homologies. But though it is necessary to recognise the
fact that great changes do occur in animals during their embryonic life, it
is not necessary to conclude that all embryological evidence is thereby
vitiated; but rather it becomes incumbent on us to attempt to determine
which embryological features are ancestral and which secondary. For this
purpose it is requisite to ascertain what are the general characters of
secondary features and how they are produced. Many vertebrates have in the
first stages of their development a number of secondary characters which
are due to the presence of food material in the ovum; the present essay is
mainly an attempt to indicate how those secondary characters arose and to
trace their gradual development. At the same time certain important
ancestral characters of the early phases of the development of vertebrates,
especially with reference to the formation of the hypoblast and mesoblast,
are pointed out and their meaning discussed.
There are three orders of vertebrates of which no mention has been made,
viz., the _Mammals_, the _Osseous_ fishes, and the _Reptiles_. The first of
these have been passed over because the accounts of their development are
not sufficiently satisfactory, though as far as can be gathered from
Bischoff's account of the dog and rabbit there would be no difficulty in
shewing their relations with other vertebrates.
We also require further investigations on Osseous fishes, but it seems
probable that they develop in nearly the same manner as the Elasmobranchii.
With reference to Reptiles we have no satisfactory investigations.
* * * * *
Amphioxus is the vertebrate whose mode of development in its earliest
stages is simplest, and the modes of development of other vertebrates are
to be looked upon as modifications of this due to the presence of food
material in their ova. It is not necessary to conclude from this that
Amphioxus was the ancestor of our present vertebrates, but merely that the
earliest stages of development of this vertebrate ancestor were similar to
those of Amphioxus.
The ovum of Amphioxus contains very little food material and its
segmentation is quite uniform. The result of segmentation is a vesicle
whose wall is formed of a single layer of cells. These are all of the same
character, and the cavity of the vesicle called the segmentation cavity is
of considerable size. A section of the embryo, as we may now call the ovum,
is represented in Plate 5, fig. A I.
The first change which occurs is the pushing in of one half of the wall of
the vesicle towards the opposite half. At the same time by the narrowing of
its mouth the hollow hemisphere so formed becomes again a vesicle[20].
Footnote 20: I have been able to make at Naples observations
which confirm the account of the invagination of Amphioxus as
given by Kowalevsky, though my observations are not nearly so
complete as those of the Russian naturalist.
Owing to its mode of formation the wall of this secondary vesicle is
composed of two layers which are only separated by a narrow space, the
remnant of the segmentation cavity.
Two of the stages in the formation of the secondary vesicle by this process
of involution are shewn in Plate X, fig. A II, and A III. In the second of
these the general growth has been very considerable, rendering the whole
animal much larger than before. The cavity of this vesicle, A III, is that
of the commencing alimentary canal whose final form is due to changes of
shape undergone by this primitive cavity. The inner wall of the vesicle
becomes converted into the wall of the alimentary canal or hypoblast, and
also into part or the whole of the mesoblast.
During the involution the cells which are being involuted undergo a change
of form, and before the completion of the process have acquired a
completely different character to the cells forming the external wall of
the secondary vesicle or epiblast. This change of character in the cells is
already well marked in fig. A II. It is of great importance, since we shall
find that some of the departures from this simple mode of development,
which characterise other vertebrates, are in part due to the distinction
between the hypoblast and epiblast cells appearing during segmentation, and
not subsequently as in Amphioxus during the involution of the hypoblast.
Kowalevsky (_Entwicklungsgeschichte des Amphioxus_) originally believed
that the narrow mouth of the vesicle (according to Mr Lankester's
terminology _blastopore_) became the anus of the adult. He has since, and
certainly correctly, given up this view. The opening of the involution
becomes closed up and the adult anus is no doubt formed as in all other
vertebrates by a pushing in from the exterior, though it probably
corresponds in position very closely with the point of closing up of the
original involution.
The mode of formation of the mesoblast is not certainly known in Amphioxus;
we shall find, however, that for all other vertebrates it arises from the
cells which are homologous with the involuted cells of this animal.
Since food material is a term which will be very often employed, it will be
well to explain exactly the sense in which it will be used. It will be used
only with reference to those passive highly refractive particles which are
found embedded in most ova.
In some eggs, of which the hen's egg may be taken as a familiar example,
the yolk-spherules or food material form the larger portion of the ovum,
and a distinction is frequently made between the germinal disc and the
yolk.
This distinction is, however, apt to lead to a misconception of the true
nature of the egg. There are strong grounds for believing that the
so-called yolk, equally with the germinal disc, is composed of an active
protoplasmic basis endowed with the power of growth, in which passive
yolk-spherules are embedded; but that the part ordinarily called the yolk
contains such a preponderating amount of yolk-spherules that the active
basis escapes detection, and does not exhibit the same power of growth as
the germinal disc.
With the exception of mammals, whose development requires to be more
completely investigated, Amphioxus is as far as we know the only vertebrate
whose ovum does not contain a large amount of food material.
In none of these (vertebrate) yolk-containing ova is the food material
distributed uniformly. It is always concentrated much more at one pole than
at the other, and the pole at which it is most concentrated may be
conveniently called the lower pole of the egg.
In eggs in which the distribution of food material is not uniform
segmentation does not take place with equal rapidity through all parts of
the egg, but its rapidity is, roughly speaking, inversely proportional to
the quantity of food material.
When the quantity of food material in a part of the egg becomes very great,
segmentation does not occur at all; and even in those cases where the
quantity of food yolk is not too great to prevent segmentation the
resulting segmentation spheres are much larger than where the yolk-granules
are more sparsely scattered.
The Frog is the vertebrate whose development comes nearest to that of
Amphioxus, as far as the points we are at present considering are
concerned. But it will perhaps facilitate the understanding of their
relations shortly to explain the diagrammatic sections which I have given
of an animal supposed to be intermediate in its development between the
Frog and Amphioxus. Plate 5, fig. B I, represents a longitudinal section of
this hypothetical egg at the close of segmentation. The lower pole,
coloured yellow, represents the part containing more yolk material, and the
upper pole, coloured blue, that with less yolk. Owing to the presence of
this yolk the lower pole even at the close of segmentation is composed of
cells of a different character to those of the upper pole. In this respect
this egg can already be distinguished from that of Amphioxus, in which no
such difference between the two poles is apparent at the corresponding
period (Plate 5, fig. A I).
The segmentation cavity in this ovum is not quite so large proportionately
as in Amphioxus, and the encroachment upon it is due to the larger bulk of
the lower pole of the egg. In fig. B II the involution of the lower pole
has already commenced; this involution is (1) not quite symmetrical, and
(2) on the ventral side (the left side) the epiblast cells forming the
upper part of the egg are growing round the cells of the lower pole of the
egg or lower layer cells. Both of these peculiarities are founded upon what
happens in the Frog and the Selachian, but it is to be noticed that the
change from the lower layer cells being involuted towards the epiblast
cells, to the epiblast cells growing round the lower layer cells, is a
necessary consequence of the increased bulk of the latter.
In this involution not only are the cells of the lower pole pushed on, but
also some of those of the upper or yellow portion; so that in this as in
all other cases the true distinction between the epiblast and hypoblast
does not appear till the involution to form the latter is completed. In the
next stage, B III, the involution has become nearly completed and the
opening to the exterior or blastopore quite constricted.
The segmentation cavity has been entirely obliterated, as would have been
found to be the case with Amphioxus had the stage a little older than that
on Plate 5, A III, been represented. The cavity marked (_al_), as was the
case with Amphioxus, is that of the alimentary canal.
The similarities between the mode of formation of the hypoblast and
alimentary canal in this animal and in Amphioxus are so striking and the
differences between the two cases so slight that no further elucidation is
required. One or two points need to be spoken of in order to illustrate
what occurs in the Frog. When the involution to form the alimentary canal
occurs, certain of the lower layer cells (marked _hy_) become distinguished
from the remainder of the lower layer cells as a separate layer and form
the hypoblast which lines the alimentary canal. It is to be noticed that
the cells which form the ventral epithelium of the alimentary canal are not
so soon to be distinguished from the other lower layer cells as those which
form its dorsal epithelium. This is probably a consequence of the more
active growth, indicated by the asymmetry of the involution, on the dorsal
side, and is a fact with important bearings in the ova with more food
material. The cells marked _m_ and coloured red also become distinguished
as a separate layer from the remainder of the hypoblast and form the
mesoblast. The remainder of the lower layer cells form a mass equivalent to
the yolk-sac of many vertebrates, and are not converted directly into the
tissues of the animal.
Another point to be noticed is the different relation of epiblast cells to
the hypoblast cells at the upper and lower side of the mouth of the
involution. Above it, on its dorsal side, the epiblast and hypoblast are
continuous with one another. On its ventral side they are primitively not
so continuous. This is due to the epiblast, as was before mentioned,
growing round the lower layer cells on the ventral side, vide B II, and
merely remaining continuous with them on the dorsal. The importance of
these two points will appear when we come to speak of other vertebrates.
The next animal whose development it is necessary to speak of is the Frog,
and its differences from the mode of development are quite easy to follow
and interpret. Segmentation is again not uniform, and results in the
formation of an upper layer of smaller cells and a lower one of larger; in
the centre is a segmentation cavity. The stage at the close of segmentation
is represented in C I. From the diagram it is apparent that the lower layer
cells occupy a larger bulk than they did in the previous animal (Plate 5, B
I), and tend to encroach still more upon the segmentation cavity, otherwise
the differences between the two are unimportant. There are, however, two
points to be noted. In the first place, although the cells of the upper
pole are distinguished in the diagrams from the lower by their colour, it
is not possible at this stage to say what will become epiblast and what
hypoblast. In the second place the cells of the upper pole or epiblast
consist of two layers--an outer called the epidermic layer and an inner
called the nervous. In the previous cases the epiblast consisted of a
single layer of cells. The presence of these two layers is due to a
distinction which, arising in most other vertebrates late, in the Frog
arises early. In most other vertebrates in the later stages of development
the epiblast consists of an outer layer of passive and an inner of active
cells. In the Frog and other Batrachians these two layers become
distinguished at the commencement of development.
In the next stage (C II) we find that the involution to form the alimentary
canal has commenced (_al_), but that it is of a very different character to
the involution in the previous case. It consists in the growing inwards of
a number of cells from the point _x_ (C I) towards the segmentation cavity.
The cells which grow in this way are partly the blue cells and partly the
smaller yellow ones. At first this involuted layer of cells is only
separated by a slit from the remainder of the lower layer cells; but by the
stage represented in C II this has widened into an elongated cavity (_al_).
In its formation this involution pushes backwards the segmentation cavity,
which finally disappears in the stage C III. The point _x_ remains
practically stationary, but by the general growth of the epiblast,
mesoblast and hypoblast, becomes further removed from the segmentation
cavity in C II than in C I. On the opposite side of the embryo to that at
which the involution occurs the epiblast cells as before, grow round the
lower layer cells. The commencement of this is already apparent in C I, and
in C II the process is nearly completed, though there is still a small mass
of yolk filling up the blastopore. The features of this involution are in
the main exaggerations of what was supposed to occur in the previous
animal. The asymmetry of the involution is so great that it is completely
one-sided and results, in the first instance, in a mere slit; and the whole
process of enclosing the yolk by epiblast is effected by the epiblast cells
on the side of the egg opposite to the involution.
The true mesoblast and hypoblast are formed precisely as in the previous
case. The involuted cells become separated into two layers, one forming the
dorsal epithelium of the alimentary canal, and a layer between this and the
epiblast forming the mesoblast. There is also a layer of mesoblast
accompanying the epiblast which encloses the yolk, which is derived from
the smaller yellow cells at _y_ (C I). The edge of this mesoblast, _m´_,
forms a thickened ridge, a feature which persists in other vertebrates.
It is a point of some importance for understanding the relation between the
mode of formation of the alimentary canal in the Frog and other vertebrates
to notice that on the ventral surface the cells which are to form the
epithelium of the alimentary canal become distinguished as such very much
later than do those to form its dorsal epithelium, and are derived not from
the involuted cells but from the primitive large yolk-cells. It is indeed
probable that only a very small portion of epithelium of the ventral wall
of the mid-gut is in the end derived from these larger yolk-cells. The
remainder of the yolk-cells (C III, and C II, _yk_) form the yolk mass and
do not become directly formed into the tissues of the animal.
In the last stage I have represented for the frog, C III, there are several
features to be noticed.
The direct connection at their hind-ends between the cavities of the neural
and alimentary canals is the most important of these. This is a result of
the previous continuity of the epiblast and hypoblast at the point _x_, and
is a feature almost certainly found in Amphioxus, but which I will speak of
more fully in my account of the Selachian's development. The opening of the
blastopore called the anus of Rusconi is now quite narrowed, it does not
become the anus of the adult. It may be noticed that at the front end of
the embryo the primitive dorsal epithelium of the alimentary canal is
growing in such a way as to form the epithelium both of the dorsal and
ventral surfaces of the fore-gut.
In spite of various features rendering the development of the Frog more
difficult of comprehension than that of most other vertebrates, it is easy
to see that the step between it and Amphioxus is not a very great one, and
will very likely be bridged over at some future time, when our knowledge of
the development of other forms becomes greater.
From the Frog to the Selachian is a considerable step, but I have again
hypothetically sketched a type intermediate between them whose development
agrees in some important points with that of _Pelobates fuscus_ as
described by Bambeke. The points of agreement, though not obvious at first
sight, I shall point out in the course of my description.
The first stage (D I), at the close of segmentation, deserves careful
attention. The segmentation cavity by the increase of the food yolk is very
much diminished in size, and, what is still more important, has as it were
sunk down so as to be completely within the _lower layer cells_. The roof
of the segmentation cavity is thus formed of epiblast and lower layer
cells, a feature which Bambeke finds in _Pelobates fuscus_ and which is
certainly found in the Selachians. In the Frog we found that the
segmentation cavity began to be encroached on by the lower layer cells, and
from this it is only a small step to find these cells creeping still
further up and forming the roof of the cavity. In the lower layer cells
themselves we find an important new feature, viz. that during segmentation
they become divided in two distinct parts--one of these where the segments
owing to the presence of much food yolk are very large, and the other where
the segments are much smaller.
The separation between these two is rather sharp. Even this separation was
foreshadowed in the Frog's egg, in which a number of lower layer cells were
much smaller and more active at the two sides of the segmentation cavity
than elsewhere. The segmentation cavity at first lies completely within the
region of the small spheres. The larger cells serve almost entirely as food
yolk. The epiblast, as is normal with vertebrates, consists of a single
layer of columnar cells.
In the next stage (D II) the formation of the alimentary canal (_al_) has
commenced, but it is to be observed that there is in this case _no true
involution_.
As an accompaniment to the encroachment upon the segmentation cavity, which
was a feature of the last stage, the cells to form the walls of the
alimentary canal have come to occupy their final position during
segmentation and without the intermediation of an involution, and traces
only of the involution, are to be found in (1) a split in the lower layer
cells which passes along the line separating the small and the large lower
layer cells; and (2) in the epiblast becoming continuous with the hypoblast
on the dorsal side of the mouth of this split. It is even possible that at
this point a few cells (though certainly only a very small number) of those
marked blue in D I become involuted. This point in this, as in all other
cases, is the tail end of the embryo. The other features of this stage are
as follows:--(1) The segmentation cavity has become smaller and less
conspicuous than it was. (2) The epiblast cells have begun to grow round
the yolk even in a more conspicuous manner than they did in the Frog, and
are accompanied by a layer of mesoblast cells which again becomes thickened
at its edge. The mesoblast cells in the region of the body are formed in
the same way as before, viz. by the separation of a layer to form the
epithelium of the alimentary canal, the other cells remaining as mesoblast;
and as in the Frog, or in a more conspicuous manner, we find that the
dorsal surface only of the alimentary cavity has a wall formed of a
_distinct layer of cells_, but on the ventral side the cavity is at first
closed in by the large spheres of the yolk only. The formation of the
alimentary canal by a split and not by an involution is exactly what
Bambeke finds in _Pelobates_.
The next stage, D III, is about an equivalent age to C III in the Frog. It
exhibits the same connection between the neural and the alimentary canals
as was found there.
The alimentary canal is beginning to become closed in below, and this
occurs near the two ends earlier than in the middle. The cells to form the
ventral wall are derived from the large yolk-cells. The non-formation of
the ventral wall of the alimentary canal so soon in the middle as at the
ends is an early trace of the umbilical canal found in Birds and
Selachians, by which the alimentary tract is placed in communication with
the yolk-sac. The segmentation cavity has by this stage completely
vanished, and the epiblast with its accompanying mesoblast has spread
completely round the yolk material so as to form the ventral wall of the
body.
Though in some points this manner of development may seem to differ from
that of the Frog, there is really a fundamental agreement between the two,
and between this mode of development and that of the Selachians we shall
find the agreement to be very close.
After segmentation we find that the egg of a Selachian consists of two
parts--one of these called the germinal disc or blastoderm, and the other
the yolk. The former of these corresponds with the epiblast and the part of
the lower pole composed of smaller segments in the last-described egg, and
the latter to the larger segments of the lower pole. This latter division,
owing to the quantity of _yolk_ which it contains, has not undergone
segmentation, but its homology with the larger segments of the previous
eggs is proved (1) by its containing a number of nuclei (E I, _n_), which
become the nuclei of true cells and enter the blastoderm, and (2) by the
presence in it of a number of lines forming a network similar to that of
many cells. The segmentation cavity, as before, lies completely within the
lower layer cells.
The next stage, E II, is almost precisely similar to the second stage of
the last egg. As there, the primitive involution is merely represented by a
split separating the yolk and the germinal disc, and on the dorsal side
alone is there a true cellular wall for this split, and at the dorsal mouth
of the split the alimentary epithelium becomes continuous with the
epiblast.
The segmentation cavity has become diminished, and round the yolk the
epiblast, accompanied by a layer of mesoblast, is commencing to grow. In
this growth all parts of the blastoderm take a share except that part where
the epiblast and hypoblast are continuous. This manner of growth is
precisely what occurs in the Frog, though there it is not so easily made
out; and not all the investigators who have studied the Frog have
understood the exact meaning of the appearances they have seen and drawn.
This similarity of relation of the epiblast to the yolk in the two cases is
a further confirmation of the identity of the Selachian's yolk with the
large yolk-spheres of the previous eggs.
The next stage, E III, is in many ways identical with the corresponding
stage in the last-described egg, and in the same way as in that case the
neural and alimentary canals are placed in communication with each other.
The mode in which this occurs will be easily gathered from a comparison of
E II and E III. It is the same for the Selachians and Batrachians. The
neural canal (_nc_) is by the stage figured E III, completely formed in the
way so well known in the Bird, and between the roof of the canal and the
external epiblast a layer of mesoblast has already grown in. The floor of
the neural canal is the same layer marked _ep_ in E II, and therefore
remains continuous with the hypoblast at _x_; and when by a simultaneous
process the roof of the neural canal and the ventral wall of the alimentary
become formed by the folding over of one continuous layer (the epiblast and
hypoblast continuous at the point _x_), the two canals, viz. the neural and
alimentary, are necessarily placed in communication at their hind-ends, as
is seen in the diagram.
There are several important points of difference between E III and D III.
In the first place, owing to the larger size of the yolk mass in E III, the
epiblast, accompanied by mesoblast, has not proceeded nearly so far round
it as in the previous case. It is also worth notice that at the right as
well as at the left end of the germinal disc the epiblast is commencing to
grow round the yolk. The yolk has, however, become surrounded to a much
smaller extent on the right hand than on the left. Since, in the earlier
stage, the epiblast became continuous with the hypoblast at _x_, it is not
from sections obvious how this occurs. I have therefore appended a diagram
to explain it (E´). The blastoderm rests like a disc on the yolk and grows
over it on all sides, except at the point where the epiblast and hypoblast
are continuous (_x_). This point becomes as it were left in a bay. Next the
two sides of the bay coalesce, the bay becomes obliterated, and the effect
produced is exactly as if the blastoderm had grown round the yolk at the
point _x_ (corresponding with the tail of the embryo) as well as everywhere
else. It thus comes about that the final point where the various parts of
the blastoderm meet and completely enclose the yolk mass does not
correspond with the anus of Rusconi of the Frog, but is at some little
distance from the hind-end of the embryo. In other words, the position of
the blastopore in the Selachian is not the same as in the Frog.
Another point deserving attention is the formation of the ventral wall of
the alimentary canal. This takes place in two ways--partly by a folding-in
at the sides and end, and partly from cells formed around the nuclei (_n_)
in the yolk. From these a large portion of the ventral wall of the mid-gut
is formed.
The folding-in of the sheet of hypoblast to assist in the closing-in of the
ventral wall of the alimentary canal is a consequence of the flattened form
of the original alimentary slit which is far too wide to form the cavity of
the final canal. In the Bird whose development must next be considered this
folding-in is a still more prominent feature in the formation of the
alimentary canal. As in the last case, the alimentary canal is widely open
in the middle to the yolk at the time when its two ends are closed below
and shut off from it; still later this opening becomes very narrow and
forms the duct of the so-called umbilical cord which places the yolk-sac in
communication with the alimentary canal. As the young animal becomes larger
the yolk-sac ceases to communicate directly with the alimentary canal, and
is carried about by it for some time as an appendage and only at a later
period shrivels up.
The mesoblast is formed in a somewhat different way in the Sharks than in
other vertebrates. It becomes split off from the hypoblast, not in the form
of a single sheet as in other vertebrates, but as two lateral sheets, one
on each side of the middle line and separated from one another by a
considerable interval; whilst the notochord is derived not as in other
vertebrates from the mesoblast, but from the hypoblast (vide F. M. Balfour,
"Development of Selachians[21]," _Journal of Microscopical Science_, Oct.,
1874).
Footnote 21: Paper No. V, p. 82 _et seq._ in this edition.
Between the Selachians and the Aves there is a considerable gulf, which it
is more difficult satisfactorily to bridge over than in the previous cases;
owing to this I have not attempted to give any intermediate stage between
them.
The first stage of the Bird (F I) is very similar in many respects to the
corresponding stage in the Selachian. The segmentation cavity is, however,
a less well-defined formation, and it may even be doubted whether a true
segmentation cavity, homologous with the segmentation cavity in the
previously described eggs, is present. On the floor of the cavity which is
formed by the yolk are a few larger cells known as formative cells which,
according to Götte's observations, are derived from the yolk, in a somewhat
similar manner to the cells which were formed around the nuclei in the
Selachian egg, and which helped to form the ventral wall of the alimentary
canal. Another point to be noticed is that the segmentation cavity occupies
a central position, and not one to the side as in the Selachian.
The yolk is proportionately quite as large as in the Selachian's egg, but,
as in that case, there can be little or no doubt of its being homologous
with the largest of the segmentation spheres of the previous eggs. It does
not undergo segmentation. The epiblast is composed of columnar cells, and
extends a short way beyond the edge of the lower layer cells.
In the next stage the more important departures from the previous type of
development become visible.
The epiblast spreads uniformly over the yolk-sac and not on the one side
only as in the former eggs.
This is due to the embryo (indicated in F II by a thickening of the cells)
lying in the centre and not at the edge of the blastoderm. A necessary
consequence of this is, that the epiblast does not, as in the previous
cases, become continuous with the hypoblast at the tail end of the embryo.
This continuity, being of no functional importance, could easily be
dispensed with, and the central position of the embryo may perhaps be
explained by supposing the process, by which in the Selachian egg the
blastopore ceases to correspond in position with the opening of the
alimentary slit or anus of Rusconi (vide E´), to occur quite early during
segmentation instead of at a late period of development. For the
possibility of such a change in the date of formation, the early appearance
of the nervous and epidermic layers in the Frog affords a parallel.
The epiblast in its growth round the yolk is only partially accompanied by
mesoblast, which, however, is thickened at its extreme edge as in the Frog.
Owing to the epiblast not becoming continuous with the hypoblast at the
tail end of the embryo, the alimentary slit is not open to the exterior.
The hypoblast is formed by some of the lower layer cells becoming
distinguished as a separate layer; the remainder of the lower layer cells
become the mesoblast.
The formation of the mesoblast and hypoblast out of the lower layer cells
has been accepted for the Bird by most observers, but has been disputed by
several, and recently by Kölliker. These have supposed that the mesoblast
is derived from the epiblast. I feel convinced that these observers are in
the wrong, and that the mesoblast is genuinely derived from the lower layer
cells.
The greater portion of the alimentary cavity consists of the original
segmentation cavity (vide diagrams). This feature of the segmentation
cavity of Birds sharply distinguishes it from any segmentation cavity of
other eggs, and renders it very doubtful whether the similarly named
cavities of the Bird and of other vertebrates are homologous. On the floor
of the cavity are still to be seen some of the formative cells, but
observers have not hitherto found that they take any share in forming the
ventral wall of the alimentary canal.
The features of the next stage are the necessary consequences of those of
the last.
The ventral wall of the alimentary canal is entirely formed by a folding-in
of the sheet of hypoblast.
The more rapid folding-in at the head still indicates the previous more
vigorous growth there, otherwise there is very little difference between
the forms of the fold at the head and tail. The alimentary canal does not
of course, at this or any period, communicate with the neural tube, since
the epiblast and hypoblast are never continuous. The other features, such
as the growth of the epiblast round the yolk-sac, are merely continuations
of what took place in the last stage.
In the development of a yolk-sac as a distinct appendage, and its
absorption within the body, at a later period, the bird fundamentally
resembles the Dog-fish.
Although there are some difficulties in deriving the type of development
exhibited by the Bird directly from that of the Selachian, it is not very
difficult to do so directly from Amphioxus. Were the alimentary involution
to remain symmetrical as in Amphioxus, and the yolk-containing part of the
egg to assume the proportions it does in the Bird, we should obtain a mode
of development which would not be very dissimilar to that of the Bird. The
epiblast would necessarily overgrow the yolk uniformly on all sides and not
in the unsymmetrical fashion of the Selachian egg. A confirmation of this
view might perhaps be sought for in the complete difference between the
types of circulation of the yolk-sac in Birds and Selachians; but this is
not so important as might at first sight appear, since it is not from the
Selachian egg but from some Batrachian that it would be necessary to derive
the Reptiles' and Birds' eggs.
If this view of the Bird's egg be correct, we are compelled to suppose that
the line of ancestors of Birds and Reptiles did not include amongst them
the Selachians and the Batrachians, or at any rate Selachians and
Batrachians which develop on the type we now find.
The careful investigation of the development of some Reptiles might very
probably throw light upon this important point. In the meantime it is
better to assume that the type of development of Birds is to be derived
from that of the Frog and Selachians.
_Summary._--If the views expressed in this paper are correct, all the modes
of development found in the higher vertebrates are to be looked upon as
modifications of that of Amphioxus. It is, however, rather an interesting
question whether it is possible to suppose that the original type was _not_
that of Amphioxus, but of some other animal, say, for instance, that of the
Frog, and that this varied in two directions,--on the one hand towards
Amphioxus, in the reverse direction to the course of variation presupposed
in the text; and on the other hand in the direction towards the Selachians
as before.
The answer to this question must in my opinion be in the negative. It is
quite easy to conceive the food material of the Frog's egg completely
vanishing, but although this would entail simplifications of development
and possibly even make segmentation uniform, there would, as far as I can
see, be no cause why the essential features of difference between the
Frog's mode of development and that of Amphioxus should change. The
asymmetrical and slit-like form of involution on the one side and the
growth of the epiblast over the mesoblast on the other side, both
characteristics of the present Frog's egg, would still be features in the
development of the simplified egg.
In the Mammal's egg we probably have an example of a Reptile's egg
simplified by the disappearance of the food material; and when we know more
of Mammalian embryology it will be very interesting to trace out the exact
manner in which this simplification has affected the development. It is
also probable that the eggs of Osseous fish are fundamentally simplified
Selachian eggs; in which case we already know that the diminution of food
material has affected but very slightly the fundamental features of
development.
One common feature which appears prominently in reviewing the embryology of
vertebrates as a whole is the derivation of the mesoblast from the
hypoblast; in other words, we find that it is from the layer corresponding
to that which becomes involuted in Amphioxus so as to line the alimentary
cavity that the mesoblast is split off.
That neither the hypoblast or mesoblast can in any sense be said to be
derived from the epiblast is perfectly clear. When the egg of Amphioxus is
in the blastosphere stage we cannot speak of either an epiblast or
hypoblast. It is not till the involution or what is equivalent has
occurred, converting the single-walled vesicle into a double-walled one,
that we can speak of these two layers. It might seem scarcely necessary to
insist upon this point, so clear is it without explanation, were it not
that certain embryologists have made a confusion about it.
The derivation of the mesoblast from the hypoblast is the more interesting,
since it is not confined to the vertebrates, but has a very wide extension
amongst the invertebrates. In the cases (whose importance has been recently
insisted upon by Professor Huxley), of the Asteroids, the Echinoids,
Sagitta, and others, in which the body-cavity arises as an outgrowth of the
alimentary canal and the somatopleure and splanchnopleure are formed from
that outgrowth, it is clear without further remark that the mesoblast is
derived from the hypoblast. For the Echinoderms in which the water-vascular
system and muscular system arise as a solid outgrowth of the wall of the
alimentary canal there can also be no question as to the derivation of the
mesoblast from the hypoblast.
Amongst other worms, in addition to Sagitta, the investigations of
Kowalevsky seem to shew that in Lumbricus the mesoblast is derived from the
hypoblast.
Amongst Crustaceans, Bobretsky's[22] observations on Oniscus (_Zeitschrift
für wiss. Zoologie_, 1874) lead to the same conclusion.
Footnote 22: He says, p. 182: "Bevor aber die Hälfte der
Eioberfläche von den Embryonalzellen bedeckt ist, kommt die
erste gemeinsame Anlage des mittleren und unteren Keimblattes
zum Vorschein."
In Insects Kowalevsky's observations lead to the conclusion that mesoblast
and hypoblast arise from a common mass of cells; Ulianin's observations
bring out the same result for the abnormal Poduridæ, and Metschnikoff's
observations shew that this also holds for Myriapods.
In Molluscs the point is not so clear.
In Tunicates, even if we are not to include them amongst vertebrates[23],
the derivation of mesoblast from hypoblast is without doubt.
Footnote 23: Anton Dohrn, _Der Ursprung des Wirbelthieres_.
Leipzig, 1875.
Without going further into details it is quite clear that the derivation of
the mesoblast from the hypoblast is very general amongst invertebrates.
It will hardly be disputed that primitively the muscular system of the
body-wall could not have been derived from the layer of cells which lines
the alimentary canal. We see indeed in Hydra and the Hydrozoa that in its
primitive differentiation, as could have been anticipated beforehand, the
muscular system of the body is derived from the epiblast cells. What, then,
is the explanation of the widespread derivation of the mesoblast, including
the muscular system of the body, from the hypoblast?
The explanation of it may, I think, possibly be found, and at all events
the suggestion seems to me sufficiently plausible to be worth making, in
the fact that in many cases, and probably this applies to the ancestors of
the vertebrates, the body-cavity was primitively a part of the alimentary.
Mr Lankester, who has already entered into this line of speculation, even
suggests (_Q. J. of Micr. Science_, April, 1875) that this applies to all
higher animals. It might then be supposed that the muscular system of part
of the alimentary canal took the place of the primitive muscular system of
the body; so that the whole muscular system of higher animals would be
primitively part of the muscular system of the digestive tract.
I put this forward merely as a suggestion, in the truth of which I feel no
confidence, but which may perhaps induce embryologists to turn their
attention to the point. If we accept it for the moment, the supplanting of
the body muscular system by that of the digestive tract may hypothetically
be supposed to have occurred in the following way.
When the diverticulum or rather paired diverticula were given off from the
alimentary canal they would naturally become attached to the body-wall, and
any contractions of their intrinsic muscles would tend to cause movements
in the body-wall. So far there is no difficulty, but there is a
physiological difficulty in explaining how it can have happened that this
secondary muscular system can have supplanted the original muscular system
of the body.
The following suggestions may lessen this difficulty, though perhaps they
hardly remove it completely. If we suppose that the animal in which these
diverticula appeared had a hard test and was not locomotive, the intrinsic
muscular system of the body would naturally completely atrophy. But since
the muscular system of the diverticula from the stomach would be required
to keep up the movement of the nutritive fluid, it would not atrophy, and
were the test subsequently to become soft and the animal locomotive, would
naturally form the muscular system of the body. Or even were the animal
locomotive in which the diverticula appeared, it is conceivable that the
two systems might at first coexist together; that either (1) subsequently
owing to the greater convenience of early development, the two systems
might acquire a development from the same mass of cells and those the cells
of the inner or hypoblast layer, so that the derivation of the body muscles
from the hypoblast would only be apparent and not real, or (2) owing to
their being better nourished as they would necessarily be, and to their
possibly easier adaptability to some new form of movement of the animal,
the muscle-cells of the alimentary canal might become developed exclusively
whilst the original muscular system atrophied.
I only hold this view provisionally till some better explanation is given
of the cases of Sagitta and the Echinoderms, as well as of the nearly
universal derivation of the mesoblast from the hypoblast. The cases of this
kind may be due to some merely embryonic changes and have no meaning in
reference to the adult condition, but I think that we have no right to
assume this till some explanation of the embryonic can be suggested.
For vertebrates, I have shewn that in Selachians the body-cavity at first
extends quite to the top of what becomes the muscle plate, so that the line
or space separating the two layers of the muscle plate (vide Balfour,
'Development of Elasmobranch Fishes[24],' _Quart. Journ. of Micro. Science_
for Oct., 1874. Plate XV, fig. 11,_a_, 11_b_, 12_a_, _mp_.) is a portion of
the original body-cavity. If this is a primitive condition, which is by no
means certain, we have a condition which we might expect, in which both the
inner and the outer wall of the primitive body-cavity assists in forming
the muscular system of the body.
Footnote 24: Paper No. V, p. 60 _et seq._ of this edition,
pl. 4, figs. 11_a_, 11_b_, 12_a_, _mp_.
It is very possible that the formation of the mesoblast as two masses, one
on each side of the middle line as occurs in Selachians, and which as I
pointed out in the paper quoted above also takes place in some worms, is a
remnant of the primitive formation of the body-cavity as paired outgrowth
of the alimentary canal. This would also explain the fact that in
Selachians the body-cavity consists at first of two separate portions, one
on each side of the alimentary canal, which only subsequently become united
below and converted into a single cavity (vide _loc. cit._[25], Plate XIV,
fig. 8_b_, _pp_).
Footnote 25: Pl. 3 of this edition, fig. 8_b_, _pp_.
In the Echinoderms we find instances where the body-cavity and
water-vascular system arise as an outgrowth from the alimentary canal,
which subsequently becomes constricted off from the latter (Asteroids and
Echinoids), together with other instances (Ophiura, Synapta) where the
water-vascular system and body-cavity are only secondarily formed in a
solid mass of mesoblast originally split off from the walls of the
alimentary canal.
These instances shew us how easily a change of this kind may take place,
and remove the difficulty of understanding why in vertebrates the
body-cavity never communicates with the alimentary.
The last point which I wish to call attention to is the blastopore or anus
of Rusconi.
This is the primitive opening by which the alimentary canal communicates
with the exterior, or, in other words, the opening of the alimentary
involution. It is a distinctly marked structure in Amphioxus and the
Batrachians, and is also found in a less well-marked form in the
Selachians; in Birds no trace of it is any longer to be seen. In all those
vertebrates in which it is present, it closes up and does not become the
anus of the adult. The final anus nevertheless corresponds very closely in
position with the anus of Rusconi. Mr Lankester has shewn (_Quart. Journ.
of Micro. Science_ for April, 1875) that in invertebrates as well as
vertebrates the blastopore almost invariably closes up. It nevertheless
corresponds as a rule very nearly in position either with the mouth or with
the anus.
If this opening is viewed, as is generally done, as really being the mouth
in some cases and the anus in others, it becomes very difficult to believe
that the blastopore can in all cases represent the same structure. In a
single branch of the animal kingdom it sometimes forms the mouth and
sometimes the anus: thus for instance in Lumbricus it is the mouth
(according to Kowalevsky), in Palæmon (Bobretzky) the anus. Is it credible
that the mouth and anus have become changed, the one for the other?
If, on the other hand, we accept the view that the blastopore never becomes
either the one or the other of these openings, it is, I think, possible to
account for its corresponding in position with the mouth in some cases or
the anus in others.
That it would soon come to correspond either with the mouth or anus
(probably with the earliest formed of these in the embryo), wherever it was
primitively situated, follows from the great simplification which would be
effected by its doing so. This simplification consists in the greater
facility with which the fresh opening of either mouth or anus could be made
where the epiblast and hypoblast were in continuity than elsewhere. Even a
change of correspondence from the position of the mouth to that of the anus
or _vice versa_ could occur. The mode in which this might happen is
exemplified by the case of the Selachians. I pointed out in the course of
this paper how the final point of envelopment of the yolk became altered in
Selachians so as to cease to correspond with the anus of Rusconi; in other
words, how the position of the blastopore became changed. In such a case,
if the yolk material again became diminished, the blastopore would
correspond in position with neither mouth nor anus, and the causes which
made it correspond in position with the anus before, would again operate,
and make it correspond in position perhaps with the mouth. Thus the
blastopore might absolutely cease to correspond in position with the anus
and come to correspond in position with the mouth.
It is hardly possible to help believing that the blastopore primitively
represented a mouth. It may perhaps have lost this function owing to an
increase of food yolk in the ovum preventing its being possible for the
blastopore to develop directly into a mouth, and necessitating the
formation of a fresh mouth. If such were the case, there would be no reason
why the blastopore should ever again serve functionally as a mouth in the
descendants of the animal which developed this fresh mouth.
EXPLANATION OF PLATE 5.
COMPLETE LIST OF REFERENCES.
_al._ Cavity of alimentary canal. _bl._ Blastoderm. _ch._ Notochord. _ep._
Epiblast. _em._ Embryo. _f._ Formative cells. _hy._ Hypoblast. _ll._ Lower
layer cells. _m._ Mesoblast. _n._ Nuclei of yolk of Selachian egg. _nc._
Neural canal. _sg._ Segmentation cavity. _x._ Point where epiblast and
hypoblast are continuous at the mouth of the alimentary involution. This
point is always situated at the tail end of the embryo. _yk._ Yolk.
Epiblast is coloured blue, mesoblast red, and hypoblast yellow. The lower
layer cells before their separation into hypoblast and mesoblast are also
coloured green.
A I, A II, A III. Diagrammatic sections of Amphioxus in its early stages
(founded upon Kowalevsky's observations).
B I, B II, B III. Diagrammatic longitudinal sections of an hypothetical
animal, intermediate between Amphioxus and Batrachians, in its early
stages.
C I, C II, C III. Diagrammatic longitudinal sections of Bombinator igneus
in its early stages (founded upon Götte's observations). In C III the
neural canal is completed, which was not the case in B III. The epiblast in
C III has been diagrammatically represented as a single layer.
D I, D II, D III. Diagrammatic longitudinal sections of an animal,
intermediate between Batrachians and Selachians, in its early stages.
E I, E II, E III. Diagrammatic longitudinal sections of a Selachian in its
early stages.
E´. Surface view of the yolk of a Selachian's egg to shew the manner in
which it is enclosed by the Blastoderm. The yolk is represented yellow and
the Blastoderm blue.
F I, F II, F III. Diagrammatic longitudinal sections of a Bird in its early
stages.
VII. ON THE ORIGIN AND HISTORY OF THE URINOGENITAL ORGANS OF
VERTEBRATES[26].
Footnote 26: From the _Journal of Anatomy and Physiology_,
Vol. X. 1875.
Recent discoveries[27] as to the mode of development and anatomy of the
urinogenital system of Selachians, Amphibians, and Cyclostome fishes, have
greatly increased our knowledge of this system of organs, and have rendered
more possible a comparison of the types on which it is formed in the
various orders of vertebrates.
Footnote 27: The more important of these are:--
Semper--Ueber die Stammverwandtschaft der Wirbelthiere u.
Anneliden. _Centralblatt f. Med. Wiss._ 1874, No. 35.
Semper--Segmentalorgane bei ausgewachsenen Haien. _Centralblatt
f. Med. Wiss._ 1874, No. 52.
Semper--Das Urogenitalsystem der höheren Wirbelthiere.
_Centralblatt f. Med. Wiss._ 1874, No. 59.
Semper--Stammesverwandtschaft d. Wirbelthiere u. Wirbellosen.
_Arbeiten aus Zool. Zootom. Inst._ Würzburg. II Band.
Semper--Bildung u. Wachstum der Keimdrüsen bei den
Plagiostomen. _Centralblatt f. Med. Wiss._ 1875, No. 12.
Semper--Entw. d. Wolf. u. Müll. Gang. _Centralblatt f. Med.
Wiss._ 1875, No. 29.
Alex. Schultz--Phylogenie d. Wirbelthiere. _Centralblatt f.
Med. Wiss._ 1874, No. 51.
Spengel--Wimpertrichtern i. d. Amphibienniere. _Centralblatt f.
Med. Wiss._ 1875, No. 23.
Meyer--Anat. des Urogenitalsystems der Selachier u. Amphibien.
_Sitzb. Naturfor. Gesellschaft._ Leipzig, 30 April, 1875.
F. M. Balfour--Preliminary Account of development of
Elasmobranch fishes. _Quart. Journ. of Micro. Science_, Oct.
1874. (This edition, Paper V. p. 60 _et seq._)
W. Müller--Persistenz der Urniere bei Myxine glutinosa.
_Jenaische Zeitschrift_, 1873.
W. Müller--Urogenitalsystem d. Amphioxus u. d. Cyclostomen.
_Jenaische Zeitschrift_, 1875.
Alex. Götte--_Entwicklungsgeschichte der Unke (Bombinator
igneus)._
The following paper is an attempt to give a consecutive history of the
origin of this system of organs in vertebrates and of the changes which it
has undergone in the different orders.
For this purpose I have not made use of my own observations alone, but have
had recourse to all the Memoirs with which I am acquainted, and to which I
have access. I have commenced my account with the Selachians, both because
my own investigations have been directed almost entirely to them, and
because their urinogenital organs are, to my mind, the most convenient for
comparison both with the more complicated and with the simpler types.
On many points the views put forward in this paper will be found to differ
from those which I expressed in my paper (_loc. cit._) which give an
account of my original[28] discovery of the segmental organs of Selachians,
but the differences, with the exception of one important error as to the
origin of the Wolffian duct, are rather fresh developments of my previous
views from the consideration of fresh facts, than radical changes in them.
Footnote 28: These organs were discovered independently by
Professor Semper and myself. Professor Semper's preliminary
account appeared prior to my own which was published (with
illustrations) in the _Quarterly Journal of Mic. Science_.
Owing to my being in South America, I did not know of Professor
Semper's investigations till several months after the
publication of my paper.
* * * * *
In Selachian embryos an intermediate cell-mass, or middle plate of
mesoblast is formed, as in birds, from a partial fusion of the somatic and
splanchnic layers of the mesoblast at the outer border of the
protovertebræ. From this cell-mass the whole of the urinogenital system is
developed.
At about the time when three visceral clefts have appeared, there arises
from the intermediate cell-mass, opposite the fifth protovertebra, a solid
knob, from which a column of cells grows backwards to opposite the position
of the future anus (Fig. 1. _pd._).
[Illustration: FIG. 1. TWO SECTIONS OF A PRISTIURUS EMBRYO WITH THREE
VISCERAL CLEFTS.
The sections are to shew the development of the segmental duct (_pd_) or
primitive duct of the kidneys. In _A_ (the anterior of the two sections)
this appears as a solid knob projecting towards the epiblast. In _B_ is
seen a section of the column which has grown backwards from the knob in
_A_.
_spn._ rudiment of a spinal nerve; _mc._ medullary canal; _ch._ notochord;
_X._ string of cells below the notochord; _mp._ muscle-plate; _mp´._
specially developed portion of muscle-plate; _ao._ dorsal aorta; _pd._
segmental duct; _so._ somatopleura; _sp._ splanchnopleura; _pp._
pleuro-peritoneal or body-cavity; _ep._ epiblast; _al._ alimentary canal.]
This knob projects outwards toward the epiblast, and the column lies at
first between the mesoblast and epiblast. The knob and column do not long
remain solid. The knob becoming hollow acquires a wide opening into the
pleuro-peritoneal or body-cavity, and the column a lumen; so that by the
time that five visceral clefts have appeared, the two together form a duct
closed behind, but communicating in front by a wide opening with the
pleuro-peritoneal cavity.
Before these changes are accomplished, a series of _solid_[29] outgrowths
of elements of the 'intermediate cell-mass' appear at the uppermost corner
of the body-cavity. These soon become hollow and appear as involutions from
the body-cavity, curling round the inner and dorsal side of the previously
formed duct.
Footnote 29: These outgrowths are at first solid in both
Pristiurus, Scyllium and Torpedo, but in Torpedo attain a
considerable length before a lumen appears in them.
One involution of this kind makes its appearance for each protovertebra,
and the first belongs to the protovertebra immediately behind the anterior
end of the duct whose development has just been described. In Pristiurus
there are in all 29 of these at this period. The last two or three arise
from that portion of the body-cavity, which at this stage still exists
behind the anus. The first-formed duct and the subsequent involutions are
the rudiments of the whole of the urinary system. The duct is the primitive
duct of the kidney[30]; I shall call it in future _the segmental duct_; and
the involutions are the commencements of the segmental tubes which
constitute the body of the kidney. I shall call them in future _segmental
tubes_.
Footnote 30: This duct is often called either Müller's duct,
the oviduct, or the duct of the primitive kidneys
'Urnierengang.' None of these terms are very suitable. A
justification of the name I have given it will appear from the
facts given in the later parts of this paper. In my previous
paper I have always called it oviduct, a name which is very
inappropriate.
Soon after their formation the segmental tubes become convoluted, and their
blind ends become connected with the segmental duct of the kidney. At the
same time, or rather before this, the blind posterior termination of each
of the segmental ducts of the kidneys unites with and opens into one of the
horns of the cloaca. At this period the condition of affairs is represented
in Fig. 2.
[Illustration: FIG. 2. DIAGRAM OF THE PRIMITIVE CONDITION OF THE KIDNEY IN
A SELACHIAN EMBRYO.
_pd._ segmental duct. It opens at _o_ into the body-cavity and at its other
extremity into the cloaca; _x._ line along which the division appears which
separates the segmental duct into the Wolffian duct above and the Müllerian
duct below; _st._ segmental tubes. They open at one end into the
body-cavity, and at the other into the segmental duct.]
There is at _pd_, the segmental duct of the kidneys, opening in front (_o_)
into the body-cavity, and behind into the cloaca, and there are a series of
convoluted segmental tubes (_st_), each opening at one end into the
body-cavity, and at the other into the duct (_pd_).
The next important change which occurs is the longitudinal division of the
segmental duct of the kidneys into Müller's duct, or the oviduct, and the
duct of the Wolffian bodies or Leydig's duct. The splitting[31] is effected
by the growth of a wall of cells which divides the duct into two parts
(fig. 3, _wd._ and _md._). It takes place in such a way that the front end
of the segmental duct, anterior to the entrance of the first segmental
tube, together with the ventral half of the rest of the duct, is split off
from its dorsal half as an independent duct (vide fig. 2, _x_).
Footnote 31: This splitting was first of all discovered and an
account of it published by Semper (_Centralblatt f. Med. Wiss._
1875, No. 29). I had independently made it out for the female a
few weeks before the publication of Semper's account--but have
not yet made observations about the point for the male.
My own previous account of the origin of the Wolffian duct
(_Quart. Journ. of Micros. Science_, Oct. 1874, and this
edition, Paper V.), is completely false, and was due to my not
having had access to a complete series of my sections when I
wrote the paper.
[Illustration: FIG. 3. TRANSVERSE SECTION OF A SELACHIAN EMBRYO
ILLUSTRATING THE FORMATION OF THE WOLFFIAN AND MÜLLERIAN DUCTS BY THE
LONGITUDINAL SPLITTING OF THE SEGMENTAL DUCT.
_mc._ medullary canal; _mp._ muscle-plate; _ch._ notochord; _ao._ aorta;
_cav._ cardinal vein; _st._ segmental tube. On the one side the section
passes through the opening of a segmental tube into the body-cavity. On the
other this opening is represented by dotted lines, and the opening of the
segmental tube into the Wolffian duct has been cut through; _wd._ Wolffian
duct; _md._ Müllerian duct. The Müllerian duct and the Wolffian duct
together constitute the primitive segmental duct; _gr._ The germinal ridge
with the thickened germinal epithelium; _l._ liver; _i._ intestine with
spiral valve.]
The dorsal portion also forms an independent duct, and into it the
segmental tubes continue to open. Such at least is the method of splitting
for the female--for the male the splitting is according to Professor
Semper, of a more partial character, and consists for the most part in the
front end of the duct only being separated off from the rest. The result of
these changes is the formation in both sexes of a fresh duct which carries
off the excretions of the segmental involutions, and which I shall call the
Wolffian duct--while in the female there is formed another complete and
independent duct, which I shall call the Müllerian duct, or oviduct, and in
the male portions only of such a duct.
The next change which takes place is the formation of another duct from the
hinder portion of the Wolffian duct, which receives the secretion of the
posterior segmental tubes. This secondary duct unites with the primary or
Wolffian duct near its termination, and the primary ducts of the two sides
unite together to open to the exterior by a common papilla.
Slight modifications of the posterior terminations of these ducts are found
in different genera of Selachians (vide Semper, _Centralblatt für Med.
Wiss_. 1874, No. 59), but they are of no fundamental importance.
These constitute the main changes undergone by the segmental duct of the
kidneys and the ducts derived from it; but the segmental tubes also undergo
important changes. In the majority of Selachians their openings into the
body-cavity, or, at any rate, the openings of a large number of them,
persist through life; but the investigations of Dr Meyer[32] render it very
probable that the small portion of each segmental tube adjoining the
opening becomes separated from the rest and becomes converted into a sort
of lymph organ, so that the openings of the segmental tubes in the adult
merely lead into lymph organs and not into the gland of the kidneys.
Footnote 32: _Sitzun. der Naturfor. Gesellschaft_, Leipzig, 30
April, 1875.
These constitute the whole changes undergone in the female, but in the male
the open ends of a varying number (according to the species) of the
segmental tubes become connected with the testis and, uniting with the
testicular follicles, serve to carry away the seminal fluid[33]. The
spermatozoa have therefore to pass through a glandular portion of the
kidneys before they enter the Wolffian duct, by which they are finally
carried away to the exterior.
Footnote 33: We owe to Professor Semper the discovery of the
arrangement of the seminal ducts. _Centralblatt f. Med. Wiss._
1875, No. 12.
In the adult female, then, there are the following parts of the
urinogenital system (fig. 4):
(1) The oviduct, or Müller's duct (fig. 4, _md._), split off from the
segmental duct of the kidneys. Each oviduct opens at its upper end into the
body-cavity, and behind the two oviducts have independent communications
with the cloaca. The oviducts serve simply to carry to the exterior the
ova, and have no communication with the glandular portion of the kidneys.
[Illustration: FIG. 4. DIAGRAM OF THE ARRANGEMENT OF THE URINOGENITAL
ORGANS IN AN ADULT FEMALE SELACHIAN.
_md._ Müllerian duct; _wd._ Wolffian duct; _st._ segmental tubes; _d._ duct
of the posterior segmental tubes; _ov._ ovary.]
(2) The Wolffian ducts (fig. 4, _wd._) or the remainder of the segmental
ducts of the kidneys. Each Wolffian duct ends blindly in front, and the two
unite behind to open by a common papilla into the cloaca.
This duct receives the secretion of the whole anterior end of the
kidneys[34], that is to say, of all the anterior segmental tubes.
Footnote 34: This upper portion of the kidneys is called
Leydig's gland by Semper. It would be better to call it the
Wolffian body, for I shall attempt to shew that it is
homologous with the gland so named in Sauropsida and Mammalia.
(3) The secondary duct (fig. 4, _d._) belonging to the lower portion of the
kidneys opening into the former duct near its termination.
(4) The segmental tubes (fig. 4, _st_) from whose convolutions and
outgrowths the kidney is formed. They may be divided into two parts,
according to the duct by which their secretion is carried off.
In the male the following parts are present:
(1) The Müllerian duct (fig. 5, _md._), consisting of a small remnant,
attached to the liver, which represents the foremost end of the oviduct of
the female.
(2) The Wolffian duct (fig. 5, _wd_), which precisely corresponds to the
Wolffian duct of the female, except that, in addition to functioning as the
duct of the anterior part of the kidneys, it also serves to carry away the
semen. In the female it is straight, but has in the adult male a very
tortuous course (vide fig. 5).
[Illustration: FIG. 5. DIAGRAM OF THE ARRANGEMENT OF THE URINOGENITAL
ORGANS IN AN ADULT MALE SELACHIAN.
_md._ rudiment of Müllerian duct; _wd._ Wolffian duct, which also serves as
vas deferens; _st._ segmental tubes. The ends of three of those which in
the female open into the body-cavity, have in the male united with the
testicular follicles, and serve to carry away the products of the testis;
_d._ duct of the posterior segmental tubes; _t._ testis.]
(3) the duct (fig. 5, _d._) of the posterior portion of the kidneys, which
has the same relations as in the female.
(4) The segmental tubes (fig. 5, _st._). These have the same relations as
in the female, except that the most anterior two, three or more, unite with
the testicular follicles, and carry away the semen into the Wolffian duct.
* * * * *
The mode of arrangement and the development of these parts suggest a number
of considerations.
In the first place it is important to notice that the segmental tubes
develop primitively as completely independent organs[35], one of which
appears in each segment. If embryology is in any way a repetition of
ancestral history, it necessarily follows that these tubes were primitively
independent of each other. Ancestral history, as recorded in development,
is often, it is true, abridged; but it is clear that though abridgement
might prevent a series of primitively separate organs from appearing as
such, yet it would hardly be possible for a primitively compound organ,
which always retained this condition, to appear during development as a
series of separate ones. These considerations appear to me to prove that
the segmented ancestors of vertebrates possessed a series of independent
and segmental excretory organs.
Footnote 35: Further study of my sections has shewn me that
the initial independence of these organs is even more complete
than might be gathered from the description in my paper (_loc.
cit._). I now find, as I before conjectured, that they at first
correspond exactly with the muscle-plates, there being one for
each muscle-plate. This can be seen in the fresh embryos, but
longitudinal sections shew it in an absolutely demonstrable
manner.
Both Professor Semper and myself, on discovering these organs, were led to
compare them and state our belief in their identity with the so-called
segmental organs of Annelids.
This view has since been fairly generally accepted. The segmental organs of
annelids agree with those of vertebrates in opening at one end into the
body-cavity, but differ in the fact that each also communicates with the
exterior by an independent opening, and that they are never connected with
each other.
On the hypothesis of the identity of the vertebrate segmental tubes with
the annelid segmental organs, it becomes essential to explain how the
external openings of the former may have become lost.
This brings us at once to the origin of the segmental duct of the kidneys,
by which the secretion of all the segmental tubes was carried to the
exterior, and it appears to me that a right understanding of the vertebrate
urinogenital system depends greatly upon a correct view of the origin of
this duct. I would venture to repeat the suggestion which I made in my
original paper (_loc. cit._) that this duct is to be looked upon as the
most anterior of the segmental tubes which persist in vertebrates. In
favour of this view are the following anatomical and embryological facts.
(1) It develops in nearly the same manner as the other segmental tubes,
viz. in Selachians as a solid outgrowth from the intermediate cell-mass,
which subsequently becomes hollowed so as to open into the body-cavity: and
in Amphibians and Osseous and Cyclostome fishes as a direct involution from
the body-cavity. (2) In Amphibians, Cyclostomes and Osseous fishes its
upper end develops a glandular portion, by becoming convoluted in a manner
similar to the other segmental tubes. This glandular portion is often
called either the head-kidney or the primitive kidney. It is only an
embryonic structure, but is important as demonstrating the true nature of
the primitive duct of the kidneys.
We may suppose that some of the segmental tubes first united, possibly in
pairs, and that then by a continuation of this process the whole of them
coalesced into a common gland. One external opening sufficed to carry off
the entire secretion of the gland, and the other openings therefore
atrophied.
This history is represented in the development of the dog-fish in an
abbreviated form, by the elongation of the first segmental tube (segmental
duct of the kidney) and its junction with each of the posterior segmental
tubes. Professor Semper looks upon the primitive duct of the kidneys as a
duct which arose independently, and was not derived from metamorphosis of
the segmental organs. Against this view I would on the one hand urge the
consideration, that it is far easier to conceive of the transformation by
change of function (comp. Dohrn, _Functionswechsel_, Leipzig, 1875) of a
segmental organ into a segmental duct, than to understand the physiological
cause which should lead, in the presence of so many already formed ducts,
to the appearance of a totally new one. By its very nature a duct is a
structure which can hardly arise de novo. We must even suppose that the
segmental organs of Annelids were themselves transformations of still
simpler structures. On the other hand I would point to the development in
this very duct amongst Amphibians and Osseous fishes of a glandular portion
similar to that of a segmental tube, as an _à posteriori_ proof of its
being a metamorphosed segmental tube. The development in insects of a
longitudinal tracheal duct by the coalescence of a series of transverse
tracheal tubes affords a parallel to the formation of a duct from the
coalescence of a series of segmental tubes.
Though it must be admitted that the loss of the external openings of the
segmental organs requires further working out, yet the difficulties
involved in their disappearance are not so great as to render it improbable
that the vertebrate segmental organs are descended from typical annelidan
ones.
The primitive vertebrate condition, then, is probably that of an early
stage of Selachian development while there is as yet a segmental duct,--the
original foremost segmental tube opening in front into the body-cavity and
behind into the cloaca; with which duct all the segmental tubes
communicate. Vide Fig. 2.
The next condition is to be looked upon as an indirect result of the
segmental duct serving as well for the products of the generative organs as
the secretions of the segmental tubes.
As a consequence of this, the segmental duct became split into a ventral
portion, which served alone for the ova, and a dorsal portion which
received the secretion of the segmental tubes. The lower portion, which we
have called the oviduct, in some cases may also have received the semen as
well as the ova. This is very possibly the case with Ceratodus (vide
Günther, _Trans. of Royal Society_, 1871), and the majority of Ganoids
(Hyrtl, _Denkschriften Wien_, Vol. VIII.). In the majority of other cases
the oviduct exists in the male in a completely rudimentary form; and the
semen is carried away by the same duct as the urine.
In Selachians the transportation of the semen from the testis to the
Wolffian duct is effected by the junction of the open ends of two or three
or more segmental tubes with the testicular follicles, and the modes in
which this junction is effected in the higher vertebrates seem to be
derivatives from this. If the views here expressed are correct it is by a
complete change of function that the oviduct has come to perform its
present office. And in the bird and higher vertebrates no trace, or only
the very slightest (vide p. 165) of the primitive urinary function is
retained during embryonic or adult life.
The last feature in the anatomy of the Selachians which requires notice is
the division of the kidney into two portions, an anterior and posterior.
The anatomical similarity between this arrangement and that of higher
vertebrates (birds, &c.) is very striking. The anterior one precisely
corresponds, anatomically, to the _Wolffian body_, and the posterior one to
the true permanent _kidney_ of higher vertebrates: and when we find that in
the Selachians the duct for the anterior serves also for the semen as does
the Wolffian duct of higher vertebrates, this similarity seems almost to
amount to identity. A discussion of the differences in development in the
two cases will come conveniently with the account of the bird; but there
appear to me the strongest grounds for looking upon the kidneys of
Selachians as equivalent to both the Wolffian bodies and the true kidneys
of the higher vertebrates.
The condition of the urinogenital organs in Selachians is by no means the
most primitive found amongst vertebrates.
The organs of both Cyclostomous and Osseous fishes, as well as those of
Ganoids, are all more primitive; and in the majority of points the
Amphibians exhibit a decidedly less differentiated condition of these
organs than do the Selachians.
In Cyclostomous fishes the condition of the urinary system is very simple.
In Myxine (vide Joh. Müller _Myxinoid fishes_, and Wilhelm Müller,
_Jenaische Zeitschrift_, 1875, _Das Urogenitalsystem des Amphioxus u. d.
Cyclostomen_) there is a pair of ducts which communicate posteriorly by a
common opening with the abdominal pore. From these ducts spring a series of
transverse tubules, each terminating in a Malpighian corpuscle. These
together constitute the mass of the kidneys. About opposite the
gall-bladder the duct of the kidney (the segmental duct) narrows very much,
and after a short course ends in a largish glandular mass (the
head-kidney), which communicates with the pericardial cavity by a number of
openings.
In Petromyzon the anatomy of the kidneys is fundamentally the same as in
Myxine. They consist of the two segmental ducts, and a number of fine
branches passing off from these, which become convoluted but do not form
Malpighian tufts. The head-kidney is absent in the adult.
W. Müller (_loc. cit._) has given a short but interesting account of the
development of the urinary system of Petromyzon. He finds that the
segmental ducts develop first of all as simple involutions from the
body-cavity. The anterior end of each then develops a glandular portion
which comes to communicate by a number of openings with the body-cavity.
Subsequently to the development of this glandular portion the remainder of
the kidneys appears in the posterior portion of the body-cavity; and before
the close of embryonic life the anterior glandular portion atrophies.
The comparison of this system with that of a Selachian is very simple. The
first developed duct is the segmental duct of a Selachian, and the
glandular portion developed at its anterior extremity, which is permanent
in Myxine but embryonic in Petromyzon, is, as W. Müller has rightly
recognized, equivalent to the head-kidney of Amphibians, which remains
undeveloped in Selachians. It is, according to my previously stated view,
the glandular portion of the first segmental organ or the segmental duct.
The series of orifices by which this communicates with the body-cavity are
due to the division of the primary opening of the segmental duct. This is
shewn both by the facts of their development in Petromyzon given by Müller,
as well as by the occurrence of a similar division of the primary orifice
in Amphibians, which is mentioned later in this paper. In a note in my
original paper (_loc. cit._) I stated that these openings were equivalent
to the segmental involutions of Selachians. This is erroneous, and was due
to my not having understood the description given in a preliminary paper of
Müller (_Jenaische Zeitschrift_, 1873). The large development of this
glandular mass in the Cyclostome and Osseous fishes and in embryo
Amphibians, implies that it must at one time have been important. Its
earlier development than the remainder of the kidneys is probably a result
of the specialized function of the first segmental organ.
The remainder of the kidney in Cyclostomes is equivalent to the kidney of
Selachians. Its development from segmental involutions has not been
recognized. If these segmental involutions are really absent it may perhaps
imply that the simplicity of the Cyclostome kidneys, like that of so many
other of their organs, is a result of degeneration rather than a primitive
condition.
In Osseous fishes the segmental duct of the kidneys develops, as the
observations of Rosenberg[36] ("Teleostierniere," _Inaug. Disser. Dorpat_,
1867) and Oellacher (_Zeitschrift für Wiss. Zool._ 1873) clearly prove, by
an involution from the body-cavity. This involution grows backwards in the
form of a duct and opens into the cloaca. The upper end of this duct (the
most anterior segmental tube) becomes convoluted, and forms a glandular
body, which has no representative in the urinary apparatus of Selachians,
but whose importance, as indicating the origin of the segmental duct of the
kidneys, I have already insisted upon.
Footnote 36: I am unfortunately only acquainted with Dr
Rosenberg's paper from an abstract.
The rest of the kidney becomes developed at a later period, probably in the
same way as in Selachians; but this, as far as I know, has not been made
out.
The segmental duct of the kidneys forms the duct for this new gland, as in
embryo Selachians (Fig. 2), but, unlike what happens in Selachians,
undergoes no further changes, with the exception of a varying amount of
retrogressive metamorphosis of its anterior end. The kidneys of Osseous
fish usually extend from just behind the head to opposite the anus, or even
further back than this. They consist for the most part of a broader
anterior portion, an abdominal portion reaching from this to the anus, and,
as in those cases in which the kidneys extend further back than the anus,
of a caudal portion.
The two ducts (segmental ducts of the kidneys) lie, as a rule, in the lower
part of the kidneys on their outer borders, and open almost invariably into
a urinary bladder. In some cases they unite before opening into the
bladder, but generally have independent openings.
This bladder, which is simply a dilatation of the united lower ends of the
primitive kidney-ducts, and has no further importance, is almost invariably
present, but in many cases lies unsymmetrically either to the right or the
left. It opens to the exterior by a very minute opening in the
genito-urinary papilla, immediately behind the genital pore. There are,
however, a few cases in which the generative and urinary organs have a
common opening. For further details vide Hyrtl, _Denk. der k. Akad. Wien_,
Vol. II.
It is possible that the generative ducts of Osseous fishes are derived from
a splitting from the primitive duct of the kidney, but this is discussed
later in the paper.
In Osseous fishes we probably have an embryonic condition of the Selachian
kidneys retained permanently through life.
* * * * *
In the majority of Ganoids the division of the segmental duct of the kidney
into two would seem to occur, and the ventral duct of the two (Müllerian
duct), which opens at its upper end into the body-cavity, is said to serve
as an excretory duct for both male and female organs.
The following are the more important facts which are known about the
generative and urinary ducts of Ganoids.
In Spatularia (vide Hyrtl, Geschlechts u. Harnwerkzeuge bei den Ganoiden,
_Denkschriften der k. Akad. Wien_, Vol. VIII.) the following parts are
found in the female.
(1) The ovaries stretching along the whole length of the abdominal cavity.
(2) The kidneys, which are separate and also extend along the greater part
of the abdominal cavity.
(3) The ureters lying on the outer borders of the kidneys. Each ureter
dilates at its lower end into an elongated wide tube, which continues to
receive the ducts from the kidneys. The two ureters unite before
terminating and open behind the anus.
(4) The two oviducts (Müllerian ducts). These open widely into the
abdominal cavity, at about two-thirds of the distance from the anterior
extremity of the body-cavity. Each opens by a narrow pore into the dilated
ureter of its side.
In the male the same parts are found as in the female, but Hyrtl found that
the Müllerian duct of the left side at its entrance into the ureter became
split into two horns, one of which ended blindly. On the right side the
opening of the Müllerian duct was normal.
In the Sturgeon (vide J. Müller, _Bau u. Grenzen d. Ganoiden_, Berlin Akad.
1844; Leydig, _Fischen u. Reptilien_, and Hyrtl, _Ganoiden_) the same parts
are found as in Spatularia.
The kidneys extend along the whole length of the body-cavity; and the
ureter, which does not reach the whole length of the kidneys, is a
thin-walled wide duct lying on the outer side. On laying it open the
numerous apertures of the tubules for the kidney are exposed. The Müllerian
duct, which opens in both sexes into the abdominal cavity, ends, according
to Leydig, in the cases of some males, blindly behind without opening into
the ureter, and Müller makes the same statement for both sexes. It was open
on both sides in a female specimen I examined[37], and Hyrtl found it
invariably so in both sexes in all the specimens he examined.
Footnote 37: For this specimen I am indebted to Dr Günther.
Both Rathke and Stannius (I have been unable to refer to the original
papers) believed that the semen was carried off by transverse ducts
directly into the ureter, and most other observers have left undecided the
mechanism of the transportation of the semen to the exterior. If we suppose
that the ducts Rathke saw really exist they might perhaps be supposed to
enter not directly into the ureter, but into the kidney, and be in fact
homologous with the vasa efferentia of the Selachians. The frequent blind
posterior termination of the Müllerian duct is in favour of the view that
these ducts of Rathke are really present.
In Polypterus (vide Hyrtl, _Ganoiden_) there is, as in other Ganoids, a
pair of Müllerian ducts. They unite at their lower ends. The ureters are
also much narrower than in previously described Ganoids and, after
coalescing, open into the united oviducts. The urinogenital canal, formed
by coalescence of the Müllerian ducts and ureters, has an opening to the
exterior immediately behind the anus.
In Amia (vide Hyrtl) there is a pair of Müllerian ducts which, as well as
the ureters, open into a dilated vesicle. This vesicle appears as a
continuation of the Müllerian ducts, but receives a number of the efferent
ductules of the kidneys. There is a single genito-urinary pore behind the
anus.
In Ceratodus (Günther, _Phil. Trans._ 1871) the kidneys are small and
confined to the posterior extremity of the abdomen. The generative organs
extend however along the greater part of the length of the abdominal
cavity. In both male and female there is a long Müllerian duct, and the
ducts of the two sides unite and open by a common pore into a urinogenital
cloaca which communicates with the exterior by the same opening as the
alimentary canal. In both sexes the Müllerian duct has a wide opening near
the anterior extremity of the body-cavity. The ureters coalesce and open
together into the urinogenital cloaca dorsal to the Müllerian ducts. It is
not absolutely certain that the semen is transported to the exterior by the
Müllerian duct of the male, which is perhaps merely a rudiment as in
Amphibia. Dr Günther failed however to find any other means by which it
could be carried away.
The genital ducts of Lepidosteus differ in important particulars from those
of the other Ganoids (vide Müller, _loc. cit._ and Hyrtl, _loc. cit._).
In both sexes the genital ducts are continuous with the investments of the
genital organs.
In the female the dilated posterior extremities of the ureters completely
invest for some distance the generative ducts, whose extremities are
divided into several processes, and end in a different way on the two
sides. A similar division and asymmetry of the ducts is mentioned by Hyrtl
as occurring in the male of Spatularia, and it seems not impossible that on
the hypothesis of the genital ducts being segmental tubes these divisions
may be remnants of primitive glandular convolutions. The ureters in both
sexes dilate as in other Ganoids at their posterior extremities, and unite
with one another. The unpaired urinogenital opening is situated behind the
anus. In the male the dilated portion of the ureters is divided into a
series of partitions which are not present in the female.
Till the embryology of the secretory system of Ganoids has been worked out,
the homologies of their generative ducts are necessarily a matter of
conjecture. It is even possible that what I have called the Müllerian duct
in the male is functionless, as with Amphibians, but that, owing to the
true ducts of the testis having been overlooked, it has been supposed to
function as the vas deferens. Günther's (_loc. cit._) injection experiments
on Ceratodus militate against this view, but I do not think they can be
considered as conclusive as long as the mechanism for the transportation of
the semen to the exterior has not been completely made out. Analogy would
certainly lead us to expect the ureter to serve in Ganoids as the vas
deferens.
The position of the generative ducts might in some cases lead to the
supposition that they are not Müllerian ducts, or, in other words, the most
anterior pair of segmental organs but a pair of the posterior segmental
tubes.
What are the true homologies of the generative ducts of Lepidosteus, which
are continuous with the generative glands, is somewhat doubtful. It is very
probable that they may represent the similarly functioning ducts of other
Ganoids, but that they have undergone further changes as to their anterior
extremities.
It is, on the other hand, possible that their generative ducts are the same
structures as those ducts of Osseous fishes, which are continuous with the
generative organs. These latter ducts are perhaps related to the abdominal
pores, and had best be considered in connection with these; but a
completely satisfactory answer to the questions which arise in reference to
them can only be given by a study of their development.
In the Cyclostomes the generative products pass out by an abdominal pore,
which communicates with the peritoneal cavity by two short tubes[38], and
which also receives the ducts of the kidneys.
Footnote 38: According to Müller (_Myxinoiden_, 1845) there is
in Myxine an abdominal pore with two short canals leading into
it, and Vogt and Pappenheim (_An. Sci. Nat._ Part IV. Vol. XI.)
state that in Petromyzon there are two such pores, each
connected with a short canal.
Gegenbaur suggests that these are to be looked upon as Müllerian ducts, and
as therefore developed from the segmental ducts of the kidneys. Another
possible view is that they are the primitive external openings of a pair of
segmental organs. In Selachians there are usually stated to be a pair of
abdominal pores. In Scyllium I have only been able to find, on each side, a
large deep pocket opening to the exterior, but closed below towards the
peritoneal cavity, so that in it there seem to be no abdominal pores[39].
In the Greenland Shark (_Læmargus Borealis_) Professor Turner (_Journal of
Anat. and Phys._ Vol. VIII.) failed to find either oviduct or vas deferens,
but found a pair of large open abdominal pores, which he believes serve to
carry away the generative products of both sexes. Whether the so-called
abdominal pores of Selachians usually end blindly as in Scyllium, or, as is
commonly stated, open into the body-cavity, there can be no question that
they are homologous with true abdominal powers.
Footnote 39: My own rough examination of preserved specimens
was hardly sufficient to enable me to determine for certain the
presence or absence of these pores. Mr Bridge, of Trinity
College, has, however, since then commenced a series of
investigations on this point, and informs me that these pores
are certainly absent in Scyllium as well as in other genera.
The blind pockets of Scyllium appear very much like the remains of
primitive involutions from the exterior, which might easily be supposed to
have formed the external opening of a pair of segmental organs, and this is
probably the true meaning of abdominal pores. The presence of abdominal
pores in all Ganoids in addition to true genital ducts and of these pockets
or abdominal pores in Selachians, which are almost certainly homologous
with the abdominal pores of Ganoids and Cyclostomes, and also occur in
addition to true Müllerian ducts, speak strongly against the view that the
abdominal pores have any relation to Müllerian ducts. Probably therefore
the abdominal pores of the Cyclostomous fishes (which seem to be of the
same character as other abdominal pores) are not to be looked on as
rudimentary Müllerian ducts.
We next come to the question which I reserved while speaking of the kidneys
of Osseous fishes, as to the meaning of their genital ducts.
In the female Salmon and the male and female Eel, the generative products
are carried to the exterior by abdominal pores, and there are no true
generative ducts. In the case of most other Osseous fish there are true
generative ducts which are continuous with the investment of the generative
organs[40] and have generally, though not always, an opening or openings
independent of the ureter close behind the rectum, but no abdominal pores
are present. It seems, therefore, that in Osseous fish the generative ducts
are complementary to abdominal pores, which might lead to the view that the
generative ducts were formed by a coalescence of the investment of the
generative glands with the short duct of abdominal pore.
Footnote 40: The description of the attachment of the vas
deferens to the testis in the Carp given by Vogt and Pappenheim
(_Ann. Scien. Nat._ 1859) does not agree with what I found in
the Perch (_Perca fluvialis_). The walls of the duct are in the
Perch continuous with the investment of the testis, and the
gland of the testis occupies, as it were, the greater part of
the duct; there is, however, a distinct cavity corresponding to
what Vogt and P. call the duct, near the border of attachment
of the testis into which the seminal tubules open. I could find
at the posterior end of the testis no central cavity which
could be distinguished from the cavity of this duct.
Against this view there are, however, the following facts:
(1) In the cases of the salmon and the eel it is perfectly true that the
abdominal pore exactly corresponds with the opening of the genital duct in
other Osseous fishes, but the absence of genital ducts in these cases must
rather be viewed, as Vogt and Pappenheim (_loc. cit._) have already
insisted, as a case of degeneration than of a primitive condition. The
presence of genital ducts in the near allies of the Salmonidæ, and even in
the male salmon, are conclusive proofs of this. If we admit that the
presence of an abdominal pore in Salmonidæ is merely a result of
degeneration, it obviously cannot be used as an argument for the
complementary nature of abdominal pores and generative ducts.
(2) Hyrtl (_Denkschriften der k. Akad. Wien_, Vol. 1) states that in
Mormyrus oxyrynchus there is a pair of abdominal pores in addition to true
generative ducts. If his statements are correct, we have a strong argument
against the generative ducts of Osseous fishes being related to abdominal
pores. For though this is the solitary instance of the presence of both a
genital opening and abdominal pores known to me in Osseous fishes, yet we
have no right to assume that the abdominal pores of Mormyrus are not
equivalent to those of Ganoids and Selachians. It must be admitted, with
Gegenbaur, that embryology alone can elucidate the meaning of the genital
ducts of Osseous fishes.
In Lepidosteus, as was before mentioned, the generative ducts, though
continuous with the investment of the generative bodies, unite with the
ureters, and in this differ from the generative ducts of Osseous fishes.
The relation, indeed, of the generative ducts of Lepidosteus to the urinary
ducts is very similar to that existing in other Ganoid fishes; and this,
coupled with the fact that Lepidosteus possesses a pair of abdominal pores
on each side of the anus[41], makes it most probable that its generative
ducts are true Müllerian ducts.
Footnote 41: This is mentioned by Müller (_Ganoid fishes_,
Berlin Akad. 1844), Hyrtl (_loc. cit._), and Günther (_loc.
cit._), and through the courtesy of Dr Günther I have had an
opportunity of confirming the fact of the presence of the
abdominal pores on two specimens of Lepidosteus in the British
Museum.
* * * * *
In the Amphibians the urinary system is again more primitive than in the
Selachians.
The segmental duct of the kidneys is formed[42] by an elongated fold
arising from the outer wall of the body-cavity, in the same position as in
Selachians. This fold becomes constricted into a canal, closed except at
its anterior end, which remains open to the body-cavity. This anterior end
dilates, and grows out into two horns, and at the same time its opening
into the body-cavity becomes partly constricted, and so divided into three
separate orifices, one for each horn and a central one between the two. The
horns become convoluted, blood channels appearing between their
convolutions, and a special coil of vessels is formed arising from the
aorta and projecting into the body-cavity near the openings of the
convolutions. These formations together constitute the glandular
portion[43] of the original anterior segmental tube or segmental duct of
the kidneys. I have already pointed out the similarity which this organ
exhibits to the head-kidneys of Cyclostome fishes in its mode of formation,
especially with reference to the division of the primitive opening. The
lower end of the segmental duct unites with a horn of the cloaca.
Footnote 42: My account of the _development_ of these parts in
Amphibians is derived for the most part from Götte, _Die
Entwicklungsgeschichte der Unke_.
Footnote 43: It is called Kopfniere (head-kidney), or Urniere
(primitive kidney), by German authors. Leydig correctly looks
upon it as together with the permanent kidney constituting the
Urniere of Amphibians. The term Urniere is one which has arisen
in my opinion from a misconception; but certainly the Kopfniere
has no greater right to the appellation than the remainder of
the kidney.
After the formation of the gland just described the remainder of the kidney
is formed.
This arises in the same way as in Selachians. A series of involutions from
the body-cavity are developed; these soon form convoluted tubes, which
become branched and interlaced with one another, and also unite with the
primitive duct of the kidneys. Owing to the branching and interlacing of
the primitive segmental tubes, the kidney is not divided into distinct
segments in the same way as with the Selachians. The mode of development of
these segmental tubes was discovered by Götte. Their openings are ciliated,
and, as Spengel (_loc. cit._) and Meyer (_loc. cit._) have independently
discovered, persist in most adult Amphibians. As both these investigators
have pointed out, the segmental openings are in the adult kidneys of most
Amphibians far more numerous than the vertebral segments to which they
appertain. This is due to secondary changes, and is not to be looked upon
as the primitive state of things. At this stage the Amphibian kidneys are
nearly in the same condition as the Selachian, in the stage represented in
Fig. 2. In both there is the segmental duct of the kidneys, which is open
in front, communicates with the cloaca behind, and receives the whole
secretion from the kidneys. The parallelism between the two is closely
adhered to in the subsequent modifications of the Amphibian kidney, but the
changes are not completed so far in Amphibians as in Selachians. The
segmental duct of the Amphibian kidney becomes, as in Selachians, split
into a Müllerian duct or oviduct, and a Wolffian duct or duct for the
kidney.
The following points about this are noteworthy:
(1) The separation of the two ducts is never completed, so that they are
united together behind, and for a short distance, blend and form a common
duct; the ducts of the two sides so formed also unite before opening to the
exterior.
(2) The separation of the two ducts does not occur in the form of a simple
splitting, as in Selachians. But the efferent ductules from the kidney
gradually alter their points of entrance into the primitive duct. Their
points of entrance become carried backwards further and further, and since
this process affects the anterior ducts proportionally more than the
posterior, the efferent ducts finally all meet and form a common duct which
unites with the Müllerian duct near its posterior extremity. This process
is not always carried out with equal completeness. In the tailless
Amphibians, however, the process is generally[44] completed, and the
ureters (Wolffian ducts) are of considerable length. Bufo cinereus, in the
male of which the Müllerian ducts are very conspicuous, serves as an
excellent example of this.
Footnote 44: In Bombinator igneus, Von Wittich stated that the
embryonic condition was retained. Leydig, _Anatom. d. Amphib.
u. Reptilien_, shewed that this is not the case, but that in
the male the Müllerian duct is very small, though distinct.
In the Salamander (Salamandra maculosa), Figs. 6 and 7, the process is
carried out with greater completeness in the female than in the male, and
this is the general rule in Amphibians. In the male Proteus, the embryonic
condition would seem to be retained almost in its completeness so that the
ducts of the kidney open directly and separately into the still persisting
primitive duct of the kidney. The upper end of the duct nevertheless
extends some distance beyond the end of the kidney and opens into the
abdominal cavity. In the female Proteus, on the other hand, the separation
into a Müllerian duct and a ureter is quite complete. The Newt (Triton)
also serves as an excellent example of the formation of distinct Müllerian
and Wolffian ducts being much more complete in the female than the male. In
the female Newt all the tubules from the kidney open into a duct of some
length which unites with the Müllerian duct near its termination, but in
the male the anterior segmental tubes, including those which, as will be
afterwards seen, serve as vasa efferentia of the testis, enter the
Müllerian duct directly, while the posterior unite as in the female into a
common duct before joining the Müllerian duct. For further details as to
the variations exhibited in the Amphibians, the reader is referred to
Leydig, _Anat. Untersuchung, Fischen u. Reptilien_. Ditto, _Lehrbuch der
Histologie, Menschen u. Thiere_. Von Wittich, _Siebold u. Kölliker,
Zeitschrift_, Vol. IV. p. 125.
The different conditions of completeness of the Wolffian ducts observable
amongst the Amphibians are instructive in reference to the manner of
development of the Wolffian duct in Selachians. The _mode_ of division in
the Selachians of the segmental duct of the kidney into a Müllerian and
Wolffian duct is probably to be looked upon as an embryonic abbreviation of
the process by which these two ducts are formed in Amphibians. The fact
that this separation into Müllerian and Wolffian ducts proceeds further in
the females of most Amphibians than in the males, strikingly shews that it
is the oviductal function of the Müllerian duct which is the indirect cause
of its separation from the Wolffian duct. The Müllerian duct formed in the
way described persists almost invariably in both sexes, and in the male
sometimes functions as a sperm reservoir; _e.g._ Bufo cinereus. In the
embryo it carries at its upper end the glandular mass described above
(Kopfniere), but this generally atrophies, though remnants of it persist in
the males of some species (_e.g._ Salamandra). Its anterior end opens, in
most cases by a single opening, into the perivisceral cavity in both sexes,
and is usually ciliated. As the female reaches maturity, the oviduct
dilates very much; but it remains thin and inconspicuous in the male.
The only other developmental change of importance is the connection of the
testes with the kidneys. This probably occurs in the same manner as in
Selachians, viz. from the junction of the open ends of the segmental tubes
with the follicles of the testes. In any case the vessels which carry off
the semen constitute part of the kidney, and the efferent duct of the
testis is also that of the kidney. The vasa efferentia from the testis
either pass through one or two nearly isolated anterior portions of the
kidney (Proteus, Triton) or else no such special portion of the kidney
becomes separated from the rest, and the vasa efferentia enter the general
body of the kidney.
* * * * *
In the male Amphibian, then, the urinogenital system consists of the
following parts (Fig. 6):
(1) Rudimentary Müllerian ducts, opening anteriorly into the body-cavity,
which sometimes carry aborted _Kopfnieren_.
(2) The partially or completely formed Wolffian ducts (ureters) which also
serve as the ducts for the testes.
(3) The kidneys, parts of which also serve as the vasa efferentia, and
whose secretion, together with the testicular products, is carried off by
the Wolffian ducts.
(4) The united lower parts of Wolffian and Müllerian ducts which are really
the lower unsplit part of the segmental ducts of the kidneys.
[Illustration: FIG. 6. DIAGRAM OF THE URINOGENITAL ORGANS OF A MALE
SALAMANDER.
(_Copied from Leydig's Histologie des Menschen u. der Thiere._)
_md._ Müller's duct (rudimentary); _y._ remnant of the secretory portion of
the segmental duct Kopfniere; _Wd._ Wolffian duct; a less complete
structure in the male than in the female; _st._ segmental tubes or kidney.
The openings of these into the body-cavity are not inserted in the figure;
_t._ testis. Its efferent ducts form part of the kidney.]
In the female, there are (Fig. 7)
(1) The Müllerian ducts which function as the oviducts.
(2) The Wolffian ducts.
(3) The kidneys.
(4) The united Müllerian and Wolffian ducts as in the male.
[Illustration: FIG. 7. DIAGRAM OF THE URINOGENITAL ORGANS OF A FEMALE
SALAMANDER.
(_Copied from Leydig's Histologie des Menschen u. der Thiere_.)
_Md._ Müller's duct or oviduct; _Wd._ Wolffian duct or the duct of the
kidneys; _st._ segmental tubes or kidney. The openings of these into the
body-cavity are not inserted in the figure; _o._ ovary.]
The urinogenital organs of the adult Amphibians agree in almost all
essential particulars with those of Selachians. The ova are carried off in
both by a specialized oviduct. The Wolffian duct, or ureter, is found both
in Selachians and Amphibians, and the relations of the testis to it are the
same in both, the vasa efferentia of the testes having in both the same
anatomical peculiarities.
The following points are the main ones in which Selachians and Amphibians
differ as to the anatomy of the urinogenital organs; and in all but one of
these, the organs of the Amphibian exhibit a less differentiated condition
than do those of the Selachian.
(1) A glandular portion (Kopfniere) belonging to the first segmental organ
(segmental duct of the kidneys) is found in all embryo Amphibians, but
usually disappears, or only leaves a remnant in the adult. It has not yet
been found in any Selachian.
(2) The division of the primitive duct of the kidney into the Müllerian
duct and the Wolffian duct is not completed so far in Amphibians as
Selachians, and in the former the two ducts are confluent at their lower
ends.
(3) The permanent kidney exhibits in Amphibians no distinction into two
glands (foreshadowing the Wolffian bodies and true kidneys of higher
vertebrates), as it does in the Selachians.
(4) The Müllerian duct persists in its entirety in male Amphibians, but
only its upper end remains in male Selachians.
(5) The openings of the segmental tubes into the body-cavity correspond in
number with the vertebral segments in most Selachians, but are far more
numerous than these in Amphibians. This is the chief point in which the
Amphibian kidney is more differentiated than the Selachian.
* * * * *
The modifications in development which the urinogenital system has suffered
in higher vertebrates (Sauropsida and Mammalia) are very considerable;
nevertheless it appears to me to be possible with fair certainty to trace
out the relationship of its various parts in them to those found in the
Ichthyopsida. The development of urinogenital organs has been far more
fully worked out for the bird than for any other member of the amniotic
vertebrates; but, as far as we know, there are no essential variations
except in the later periods of development throughout the division. These
later variations, concerning for the most part the external apertures of
the various ducts, are so well known and have been so fully described as to
require no notice here. The development of these parts in the bird will
therefore serve as the most convenient basis for comparison.
In the bird the development of these parts begins by the appearance of a
column of cells on the upper surface of the intermediate cell-mass (Fig. 8,
_W.d_). As in Selachians, the intermediate cell-mass is a group of cells
between the outer edge of the protovertebræ and the upper end of the
body-cavity. The column of cells thus formed is the commencement of the
duct of the Wolffian body. Its development is strikingly similar to that of
the segmental duct of the kidney in Selachians. I shall attempt when I have
given an account of the development of the Müllerian duct to speak of the
relations between the Selachian duct and that of the bird.
Romiti (_Archiv f. Micr. Anat._ Vol. X.) has recently stated that the
Wolffian duct develops as an involution from the body-cavity. The fact that
the specimens drawn by Romiti to support this view are too old to determine
such a point, and the inspection of a number of specimens made by my friend
Mr Adam Sedgwick of Trinity College, who, at my request, has been examining
the urinogenital organs of the fowl, have led me to the conclusion that
Romiti is in error in differing from his predecessors as to the development
of the Wolffian duct. The solid string of cells to form the Wolffian duct
lies at first close to the epiblast, but, by the alteration in shape which
the protovertebræ undergo and the general growth of cells around it,
becomes gradually carried downwards till it lies close to the germinal
epithelium which lines the body-cavity. While undergoing this change of
position it also acquires a lumen, but ends blindly both in front and
behind. Towards the end of the fourth day the Wolffian duct opens into a
horn of the cloaca. The cells adjoining its inner border commence, as it
passes down on the third day, to undergo histological changes, which, by
the fourth day, result in the formation of a series of ducts and Malpighian
tufts which form the mass of the Wolffian body[45].
Footnote 45: This account of the origin of the Wolffian body
differs from that given by Waldeyer, and by Dr Foster and
myself (_Elements of Embryology_, Foster and Balfour), but I
have been led to alter my view from an inspection of Mr
Sedgwick's preparations, and I hope to shew that theoretical
considerations lead to the expectation that the Wolffian body
would develop independently of the duct.
[Illustration: FIG. 8. TRANSVERSE SECTION THROUGH THE DORSAL REGION OF AN
EMBRYO FOWL OF 45 H. TO SHEW THE MODE OF FORMATION OF THE WOLFFIAN DUCT.
_A._ epiblast; _B._ mesoblast; _C._ hypoblast; _M.c._ medullary canal;
_Pv._ Protovertebræ; _W.d._ Wolffian duct; _So._ Somatopleure; _Sp._
Splanchnopleure; _pp._ pleuro-peritoneal cavity; _ch._ notochord; _ao._
dorsal aorta; _v._ blood-vessels.]
The Müllerian duct arises in the form of an involution, whether at first
solid or hollow, of the germinal epithelium, and, as I am satisfied, quite
independently of the Wolffian duct. It is important to notice that its
posterior end soon unites with the Wolffian duct, from which however it not
long after becomes separated and opens independently into the cloaca. The
upper end remains permanently open to the body-cavity, and is situated
nearly opposite the extreme front end of the Wolffian body.
Between the 80th and 100th hour of incubation the ducts of the permanent
kidneys begin to make their appearance. Near its posterior extremity each
Wolffian duct becomes expanded, and from the dorsal side of this portion a
diverticulum is constricted off, the blind end of which points forwards.
This is the duct of the permanent kidneys, and around its end the kidneys
are found. It is usually stated that the tubules of the permanent kidneys
arise as outgrowths from the duct, but this requires to be worked over
again.
The condition of the urinogenital system in birds immediately after the
formation of the permanent kidneys is strikingly similar to its permanent
condition in adult Selachians. There is the Müllerian duct in both opening
in front into the body-cavity and behind into the cloaca. In both the
kidneys consist of two parts--an anterior and posterior--which have been
called respectively Wolffian bodies and permanent kidneys in birds and
Leydig's glands and the kidneys in Selachians.
The duct of the permanent kidney, which at first opens into that of the
Wolffian body, subsequently becomes further split off from the Wolffian
duct, and opens independently into the cloaca.
The subsequent changes of these parts are different in the two sexes.
In the female the Müllerian ducts[46] persist and become the oviducts.
Their anterior ends remain open to the body-cavity. The changes in their
lower ends in the various orders of Sauropsida and Mammalia are too well
known to require repetition here. The Wolffian body and duct atrophy: there
are left however in many cases slight remnants of the anterior extremity of
the body forming the parovarium of the bird, and also frequently remnants
of the posterior portion of the gland as well as of the duct. The permanent
kidney and its duct remain unaltered.
Footnote 46: The right oviduct atrophies in birds, and the
left alone persists in the adult.
In the male the Müllerian duct becomes almost completely obliterated. The
Wolffian duct persists and forms the vas deferens, and the anterior
so-called sexual portion of the Wolffian body also persists in an altered
form. Its tubules unite with the seminiferous tubules, and also form the
epididymis. Unimportant remnants of the posterior part of the Wolffian body
also persist, but are without function. In both sexes the so-called
permanent kidneys form the sole portion of the primitive uriniferous system
which persists in the adult.
In considering the relations between the modes of development of the
urinogenital organs of the bird and of the Selachians, the first important
point to notice is, that whereas in the Selachians the segmental duct of
the kidneys is first developed and subsequently becomes split into the
Müllerian and Wolffian ducts; in the bird these two ducts develop
independently. This difference in development would be accurately described
by saying that in birds the segmental duct of the kidneys develops as in
Selachians, but that the Müllerian duct develops independently of it.
Since in Selachians the Wolffian duct is equivalent to the segmental duct
of the kidneys with the Müllerian removed from it, when in birds the
Müllerian duct develops independently of the segmental kidney duct, the
latter becomes the same as the Wolffian duct.
The second mode of stating the difference in development in the two cases
represents the embryological facts of the bird far better than the other
method.
It explains why the Wolffian duct appears earlier than the Müllerian and
not at the same time, as one might expect according to the other way of
stating the case. If the Wolffian duct is equivalent to the segmental duct
of Selachians, it must necessarily be the first duct to develop; and not
improbably the development of the Müllerian duct would in birds be expected
to occur at the time corresponding to that at which the primitive duct in
Selachians became split into two ducts.
It probably also explains the similarity in the mode of development of the
Wolffian duct in birds and the primitive duct of the kidneys in Selachians.
This way of stating the case is also in accordance with theoretical
conclusions. As the egg-bearing function of the Müllerian duct became more
and more confirmed we might expect that the adult condition would impress
itself more and more upon the embryonic development, till finally the
Müllerian duct ceased to be at any period connected with the kidneys, and
the history of its origin ceased to be traceable in its development. This
seems to have actually occurred in the higher vertebrates, so that the only
persisting connection between the Müllerian duct and the urinary system is
the brief but important junction of the two at their lower ends on the
sixth or seventh day. This junction justly surprised Waldeyer (_Eierstock
u. Ei_, p. 129), but receives a complete and satisfactory explanation on
the hypothesis given above.
The original development of the segmental tubes is in the bird solely
retained in the tubules of the Wolffian body arising independently of the
Wolffian duct, and I have hitherto failed to find that there is a distinct
division of the Wolffian bodies into segments corresponding with the
vertebral segments.
I have compared the permanent kidneys to the lower portion of the kidneys
of Selachians. The identity of the anatomical condition of the adult
Selachian and embryonic bird which has been already pointed out speaks
strongly in favour of this view; and when we further consider that the duct
of the permanent kidneys is developed in nearly the same way as the
supposed homologous duct in Selachians, the suggested identity gains
further support. The only difficulty is the fact that in Selachians the
tubules of the part of the kidneys under comparison develop as segmental
involutions in point of time anteriorly to their duct, while in birds they
develop in a manner not hitherto certainly made out but apparently in point
of time posteriorly to their duct. But when the immense modifications in
development which the whole of the gland of the excretory organ has
undergone in the bird are considered, I do not think that the fact I have
mentioned can be brought forward as a serious difficulty.
The further points of comparison between the Selachian and the bird are
very simple. The Müllerian duct in its later stages behaves in the higher
vertebrates precisely as in the lower. It becomes in fact the oviduct in
the female and atrophies in the male. The behaviour of the Wolffian duct is
also exactly that of the duct which I have called the Wolffian duct in
Ichthyopsida, and in the tubules of the Wolffian body uniting with the
tubuli seminiferi we have represented the junction of the segmental tubes
with the testis in Selachians and Amphibians. It is probably this junction
of two independent organs which led Waldeyer to the erroneous view that the
tubuli seminiferi were developed from the tubules of the Wolffian body.
With the bird I conclude the history of the origin of the urinogenital
system of vertebrates. I have attempted, and I hope succeeded, in tracing
out by the aid of comparative anatomy and embryology the steps by which a
series of independent and simple segmental organs like those of Annelids
have become converted into the complicated series of glands and ducts which
constitute the urinogenital system of the higher vertebrates. There are no
doubt some points which require further elucidation amongst the Ganoid and
Osseous fishes. The most important points which appear to me still to need
further research, both embryological and anatomical, are the abdominal
pores of fishes, the generative ducts of Ganoids, especially Lepidosteus,
and the generative ducts of Osseous fishes.
The only further point which requires discussion is the embryonic layer
from which these organs are derived.
I have shewn beyond a doubt (_loc. cit._) that in Selachians these organs
are formed from the mesoblast. The unanimous testimony of all the recent
investigators of Amphibians leads to the same conclusion. In birds, on the
other hand, various investigators have attempted to prove that these organs
are derived from the epiblast. The proof they give is the following: the
epiblast and mesoblast appear fused in the region of the axis cord. From
this some investigators have been led to the conclusion that the whole of
the mesoblast is derived from the upper of the two primitive embryonic
layers. To these it may be replied that, even granting their view to be
correct, it is no proof of the derivation of the urinogenital organs from
the epiblast, since it is not till the complete formation of the three
layers that any one of them can be said to exist. Others look upon the
fusion of the two layers as a proof of the passage of cells from the
epiblast into the mesoblast. An assumption in itself, which however is
followed by the further assumption that it is from these epiblast cells
that the urinogenital system is derived! Whatever may have been the
primitive origin of the system, its mesoblastic origin in vertebrates
cannot in my opinion be denied.
Kowalewsky (_Embryo. Stud. an Vermen u. Arthropoda_, Mem. Akad. St
Petersbourg, 1871) finds that the segmental tubes of Annelids develop from
the mesoblast. We must therefore look upon the mesoblastic origin of the
excretory system as having an antiquity greater even than that of
vertebrates.
VIII. ON THE DEVELOPMENT OF THE SPINAL NERVES IN ELASMOBRANCH FISHES[47].
Footnote 47: [From the _Philosophical Transactions of the Royal
Society of London_, Vol. CLXVI. Pt. 1. Received _October 5_,
Read _December 16, 1875_.]
With Plates 22 and 23.
In the course of an inquiry into the development of Elasmobranch Fishes, my
attention has recently been specially directed to the first appearance and
early stages of the spinal nerves, and I have been led to results which
differ so materially from those of former investigators, that I venture at
once to lay them before the Society. I have employed in my investigations
embryos of _Scyllium canicula_, _Scyllium stellare_, _Pristiurus_, and
_Torpedo_. The embryos of the latter animal, especially those hardened in
osmic acid, have proved by far the most favourable for my purpose, though,
as will be seen from the sequel, I have been able to confirm the majority
of my conclusions on embryos of all the above-mentioned genera.
A great part of my work was done at the Zoological Station founded by Dr
Dohrn at Naples; and I have to thank both Dr Dohrn and Dr Eisig for the
uniformly obliging manner in which they have met my requirements for
investigation. I have more recently been able to fill up a number of lacunæ
in my observations by the study of embryos bred in the Brighton Aquarium;
for these I am indebted to the liberality of Mr Lee and the directors of
that institution.
_The first appearance of the Spinal Nerves in Pristiurus._
In a _Pristiurus_-embryo, at the time when two visceral clefts become
visible from the exterior (though there are as yet no openings from without
into the throat), a transverse section through the dorsal region exhibits
the following features (Pl. 22, fig. A):--
The external epiblast is formed of a single row of flattened elongated
cells. Vertically above the neural canal the cells of this layer are more
columnar, and form the rudiment of the primitively continuous dorsal fin.
The neural canal (_nc_) is elliptical in section, and its walls are
composed of oval cells two or three deep. The wall at the two sides is
slightly thicker than at the ventral and dorsal ends, and the cells at the
two ends are also smaller than elsewhere. A typical cell from the side
walls of the canal is about 1/1900 inch in its longest diameter. The
outlines of the cells are for the most part distinctly marked in the
specimens hardened in either chromic or picric acid, but more difficult to
see in those prepared with osmic acid; their protoplasm is clear, and in
the interior of each is an oval nucleus very large in proportion to the
size of its cell. The long diameter of a typical nucleus is about 1/3000
inch, or about two-thirds of that of the cell.
The nuclei are granular, and very often contain several especially large
and deeply stained granules; in other cases only one such is present, which
may then be called a nucleolus.
In sections there may be seen round the exterior of the neural tube a
distinct hyaline membrane: this becomes stained of a brown colour with
osmic acid, and purple or red with hæmatoxylin or carmine respectively.
Whether it is to be looked upon as a distinct membrane differentiated from
the outermost portion of the protoplasm of the cells, or as a layer of
albumen coagulated by the reagents applied, I am unable to decide for
certain. It makes its appearance at a very early period, long before that
now being considered; and similar membranes are present around other organs
as well as the neural tube. The membrane is at this stage perfectly
continuous round the whole exterior of the neural tube _as well on the
dorsal surface as on the ventral_.
The section figured, whose features I am describing, belongs to the middle
of the dorsal region. Anteriorly to this point the spinal cord becomes more
elliptical in section, and the spinal canal more lanceolate; posteriorly,
on the other hand, the spinal canal and tube become more nearly circular in
section. Immediately beneath the neural tube is situated the notochord
(_ch_). It exhibits at this stage a central area rich in protoplasm, and a
peripheral layer very poor in protoplasm; externally it is invested by a
distinct cuticular membrane.
Beneath the notochord is a peculiar rod of cells, constricted from the top
of the alimentary canal[48]. On each side and below this are the two aortæ,
just commencing to be formed, and ventral to these is the alimentary canal.
Footnote 48: Vide Balfour, "Preliminary account of the
Development of Elasmobranch Fishes," _Quart. Journ. of Microsc.
Science_, Oct. 1874, p. 33. [This edition, p. 96.]
On each side of the body two muscle-plates are situated; their upper ends
reach about one-third of the way up the sides of the neural tube. The two
layers which together constitute the muscle-plates are at this stage
perfectly continuous with the somatic and splanchnic layers of the
mesoblast, and the space between the two layers is continuous with the
body-cavity. In addition to the muscle-plates and their ventral
continuations, there are no other mesoblast-cells to be seen. The absence
of all mesoblastic cells dorsal to the superior extremities of the muscles
is deserving of special notice.
Very shortly after this period and, as a rule, before a third visceral
cleft has become visible, the first traces of the spinal nerves make their
appearance.
_First Stage._--The spinal nerves do not appear at the same time along the
whole length of the spinal canal, but are formed first of all in the neck
and subsequently at successive points posterior to this.
Their mode of formation will be most easily understood by referring to
Pl. 22, figs. B I, B II, B III, which are representations of three sections
taken from the same embryo. B I is from the region of the heart; B II
belongs to a part of the body posterior to this, and B III to a still
posterior region.
In most points the sections scarcely differ from Pl. 22, fig. A, which,
indeed, might very well be a posterior section of the embryo to which these
three sections belong.
The chief point, in addition to the formation of the spinal nerves, which
shews the greater age of the embryo from which the sections were taken is
the complete formation of the aortæ.
The upper ends of the muscle-plates have grown no further round the neural
canal than in fig. A, and no scattered mesoblastic connective-tissue cells
are visible.
In fig. A the dorsal surface of the neural canal was as completely rounded
off as the ventral surface; but in fig. B III this has ceased to be the
case. The cells at the dorsal surface of the neural canal have become
rounder and smaller and begun to proliferate, and the uniform outline of
the neural canal has here become broken (fig. B III, _pr_). The peculiar
membrane completely surrounding the canal in fig. A now terminates just
below the point where the proliferation of cells is taking place.
The prominence of cells which springs in this way from the top of the
neural canal is the commencing rudiment of a pair of spinal nerves. In
fig. B II, a section anterior to fig. B III, this formation has advanced
much further (fig. B II, _pr_). From the extreme top of the neural canal
there have now grown out two club-shaped masses of cells, one on each side;
they are perfectly continuous with the cells which form the extreme top of
the neural canal, and necessarily also are in contact with each other
dorsally. Each grows outwards in contact with the walls of the neural
canal; but, except at the point where they take their origin, they are not
continuous with its walls, and are perfectly well separated by a sharp line
from them.
In fig. B I, though the club-shaped processes still retain their attachment
to the summit of the neural canal, they have become much longer and more
conspicuous.
Specimens hardened in both chromic acid (Pl. 22, fig. C) and picric acid
give similar appearances as to the formation of these bodies.
In those hardened in osmic acid, though the mutual relations of the masses
of cells are very clear, yet it is difficult to distinguish the outlines of
the individual cells.
In the chromic acid specimens (fig. C) the cells of these rudiments appear
rounded, and each of them contains a large nucleus.
I have been unable to prepare longitudinal sections of this stage, either
horizontal or vertical, to shew satisfactorily the extreme summit of the
spinal cord; but I would call attention to the fact that the cells forming
the proximal portion of the outgrowth are seen in every transverse section
at this stage, and therefore exist the whole way along, whereas the
_distal_ portion is seen only in every third or fourth section, according
to the thickness of the sections. It may be concluded from this that there
appears a continuous outgrowth from the spinal canal, from which
discontinuous processes grow out.
In specimens of a very much later period (Pl. 23, fig. I) the proximal
portions of the outgrowth are unquestionably continuous with each other,
though their actual junctions with the spinal cord are very limited in
extent. The fact of this continuity at a later period is strongly in favour
of the view that the posterior branches of the spinal nerves arise from the
first as a continuous outgrowth of the spinal cord, from which a series of
distal processes take their origin. I have, however, failed to demonstrate
this point absolutely. The processes, which we may call the
nerve-rudiments, are, as appears from the later stages, equal in number to
the muscle-plates.
It may be pointed out, as must have been gathered from the description
above, that the nerve-rudiments have at this stage but one point of
attachment to the spinal cord, and that this one corresponds with the
dorsal or posterior root of the adult nerve.
The rudiments are, in fact, those of the posterior root only.
The next or second stage in the formation of these structures to which I
would call attention occurs at about the time when three to five visceral
clefts are present. The disappearance from the notochord in the anterior
extremity of the body of a special central area rich in protoplasm serves
as an excellent guide to the commencement of this epoch.
Its investigation is beset with far greater difficulties than the previous
one. This is owing partly to the fact that a number of connective-tissue
cells, which are only with great difficulty to be distinguished from the
cells which compose the spinal nerves, make their appearance around the
latter, and partly to the fact that the attachment of the spinal nerves to
the neural canal becomes much smaller, and therefore more difficult to
study.
Fortunately, however, in _Torpedo_ these peculiar features are not present
to nearly the same extent as in _Pristiurus_ and _Scyllium_.
The connective-tissue cells, though they appear earlier in _Torpedo_ than
in the two other genera, are much less densely packed, and the large
attachment of the nerves to the neural canal is retained for a longer
period.
Under these circumstances I consider it better, before proceeding with this
stage, to give a description of the occurrences in _Torpedo_, and after
that to return to the history of the nerves in the genera _Pristiurus_ and
_Scyllium_.
_The development of the Spinal Nerves in Torpedo._
The youngest _Torpedo_-embryo in which I have found traces of the spinal
nerves belongs to the earliest part of what I called the second stage.
The segmental duct[49] is just appearing, but the cells of the notochord
have not become completely vacuolated. The rudiments of the spinal nerves
extend half of the way towards the ventral side of the spinal cord; they
grow out in a most distinct manner from the dorsal surface of the spinal
cord (Pl. 22, fig. D a, _pr_); but the nerve-rudiments of the two sides are
no longer continuous with each other at the dorsal median line, as in the
earlier _Pristiurus_-embryos. The cells forming the proximal portion of the
rudiment have the same elongated form as the cells of the spinal cord, but
the remaining cells are more circular.
Footnote 49: Vide Balfour, "Origin and History of Urinogenital
Organs of Vertebrates," _Journal of Anatomy and Physiology_,
Oct. 1875. [This edition, No. VII.]
From the summit of the muscle-plates (_mp_) an outgrowth of connective
tissue has made its appearance (_c_), which eventually fills up the space
between the dorsal surface of the cord and the external epiblast. There is
not the slightest difficulty in distinguishing the connective-tissue cells
from the nerve-rudiment. I believe that in this embryo the origin of the
nerves from the neural canal was a continuous one, though naturally the
peripheral ends of the nerve-rudiments were separate from each other.
The most interesting feature of the stage is the commencing formation of
the anterior roots. Each of these arises (Pl. 22, fig. D a, _ar_) as a
small but distinct outgrowth from the epiblast of the spinal cord, near the
ventral corner of which it appears as a conical projection. Even from the
very first it has an indistinct form of termination and a fibrous
appearance, while the protoplasm of which it is composed becomes very
attenuated towards its termination.
The points of origin of the anterior roots from the spinal cord are
separated from each other by considerable intervals. In this fact, and also
in the nerves of the two sides never being united with each other in the
ventral median line, the anterior roots exhibit a marked contrast to the
posterior.
There exists, then, in _Torpedo_-embryos by the end of this stage distinct
rudiments of both the anterior and posterior roots of the spinal nerves.
These rudiments are at first quite independent of and disconnected with
each other, and both take their rise as outgrowths of the epiblast of the
neural canal.
The next _Torpedo_-embryo (Pl. 22, fig. D b), though taken from the same
female, is somewhat older than the one last described. The cells of the
notochord are considerably vacuolated; but the segmental duct is still
without a lumen. The posterior nerve-rudiments are elongated, pear-shaped
bodies of considerable size, and, growing in a ventral direction, have
reached a point nearly opposite the base of the neural canal. They still
remain attached to the top of the neural canal, though the connexion has in
each case become a pedicle so narrow that it can only be observed with
great difficulty.
It is fairly certain that by this stage each posterior nerve-rudiment has
its own separate and independent junction with the spinal cord; their
dorsal extremities are nevertheless probably connected with each other by a
continuous commissure.
The cells composing the rudiments are still round, and have, in fact,
undergone no important modifications since the last stage.
The important feature of the section figured (fig. D b), and one which it
shares with the other sections of the same embryo, is the appearance of
connective-tissue cells around the nerve-rudiment. These cells arise from
two sources; one of these is supplied by the vertebral rudiments, which at
the end of the last stage (Pl. 22, fig. C, _vr_) become split off from the
inner layer of the muscle-plates. The vertebral rudiments have in fact
commenced to grow up on each side of the neural canal, in order to form the
mass of cells out of which the neural arches are subsequently developed.
The dorsal extremities of the muscle-plates form the second source of these
connective-tissue cells. These latter cells lie dorsal and external to the
nerve-rudiments.
The presence of this connective tissue, in addition to the nerve-rudiments,
removes the possibility of erroneous interpretations in the previous stages
of the _Pristiurus_-embryo.
It might be urged that the two masses which I have called nerve-rudiments
are nothing else than mesoblastic connective tissue commencing to develop
around the neural canal, and that the appearance of attachment to the
neural canal which they present is due to bad preparation or imperfect
observation. The sections of both this and the last _Torpedo_-embryo which
I have been describing clearly prove that this is not the case. We have, in
fact, in the same sections the developing connective tissue as well as the
nerve-rudiments, and at a time when the latter still retains its primitive
attachment to the neural canal. The anterior root (fig. D b, _ar_) is still
a distinct conical prominence, but somewhat larger than in the previously
described embryo; it is composed of several cells, and the cells of the
spinal cord in its neighbourhood converge towards its point of origin.
In a _Torpedo_-embryo (Pl. 22, fig. D c) somewhat older than the one last
described, though again derived from the oviduct of the same female, both
the anterior and the posterior rudiments have made considerable steps in
development.
In sections taken from the hinder part of the body I found that the
posterior rudiments nearly agreed in size with those in fig. D b.
It is, however, still less easy than there to trace the junction of the
posterior rudiments with the spinal cord, and the upper ends of the
rudiments of the two sides do not nearly meet.
In a considerable series of sections I failed to find any case in which I
could be absolutely certain that a junction between the nerve and the
spinal cord was effected; and it is possible that in course of the change
of position which this junction undergoes there may be for a short period a
break of continuity between the nerve and the cord. This, however, I do not
think probable. But if it takes place at all, it takes place before the
nerve becomes functionally active, and so cannot be looked upon as
possessing any physiological significance.
The rudiment of the posterior nerve in the hinder portion of the body is
still approximately homogeneous, and no distinction of parts can be found
in it.
In the same region of the body the anterior rudiment retains nearly the
same condition as in the previous stage, though it has somewhat increased
in size.
In the sections taken from the anterior part of the same embryo the
posterior rudiment has both grown in size and also commenced to undergo
histological changes by which it has become divided into a root, a
ganglion, and a nerve.
The root (fig. D c, _pr_) consists of small round cells which lie close to
the spinal cord, and ends dorsally in a rounded extremity.
The ganglion (_g_) consists of larger and more elongated cells, and forms
an oval mass enclosed on the outside by the downward continuation of the
root, having its inner side nearly in contact with the spinal cord.
From its ventral end is continued the nerve, which is of considerable
length, and has a course approximately parallel to that of the
muscle-plate. It forms a continuation of the root rather than of the
ganglion.
Further details in reference to the histology of the nerve-rudiment at this
stage are given later in this paper, in the description of
_Pristiurus_-embryos, of which I have a more complete series of sections
than of the _Torpedo_-embryos.
When compared with the nerve-rudiment in the posterior part of the same
embryo, the nerve-rudiment last described is, in the first place,
considerably larger, and has secondly undergone changes, so that it is
possible to recognize in it parts which can be histologically distinguished
as nerve and ganglion.
The developmental changes which have taken place in the anterior root are
not less important than those in the posterior. The anterior root now forms
a very conspicuous cellular prominence growing out from the ventral corner
of the spinal cord (fig. D c, _ar_). It has a straight course from the
spinal cord to the muscle-plate, and there shews a tendency to turn
downwards at an open angle: this, however, is not represented in the
specimen figured. The cells of which it is composed each contain a large
oval nucleus, and are not unlike the cells which form the posterior
rudiment. The anterior and posterior nerves are still quite unconnected
with each other; and in those sections in which the anterior root is
present the posterior root of the same side is either completely absent or
only a small part is to be seen. The cells of the spinal cord exhibit a
slight tendency to converge towards the origin of the anterior nerve-root.
In the spinal cord itself the epithelium of the central canal is commencing
to become distinguished from the grey matter, but no trace of the white
matter is visible.
I have succeeded in making longitudinal vertical sections of this stage,
which prove that the ends of the posterior roots adjoining the junction
with the cord are all connected with each other (Pl. 22, fig. D d).
If the figure representing a transverse section of the embryo (fig. D c) be
examined, or better still the figure of a section of the slightly older
_Scyllium_-embryo (Pl. 23, fig. H I or I I), the posterior root will be
seen to end dorsally in a rounded extremity, and the junction with the
spinal cord to be effected, not by the extremity of the nerve, but by a
part of it at some little distance from this.
It is from these upper ends of the rudiments beyond the junction with the
spinal cord that I believe the commissures to spring which connect together
the posterior roots.
My sections shewing this for the stage under consideration are not quite as
satisfactory as is desirable; nevertheless they are sufficiently good to
remove all doubt as to the presence of these commissures.
A figure of one of these sections is represented (Pl. 22, fig. D d). In
this figure _pr_ points to the posterior roots and _x_ to the commissures
uniting them.
In a stage somewhat subsequent to this I have succeeded in making
longitudinal sections, which exhibit these junctions with a clearness which
leaves nothing to be desired.
It is there effected (Pl. 23, fig. L) in each case by a protoplasmic
commissure with imbedded nuclei[50]. Near its dorsal extremity each
posterior root dilates, and from the dilated portion is given off on each
side the commissure uniting it with the adjoining roots.
Footnote 50: This commissure is not satisfactorily represented
in the figure. Vide Explanation of Plate 23.
Considering the clearness of this formation in this embryo, as well as in
the embryo belonging to the stage under description, there cannot be much
doubt that at the first formation of the posterior rudiments a continuous
outgrowth arises from the spinal cord, and that only at a later period do
the junctions of the roots with the cord become separated and distinct for
each nerve.
I now return to the more complete series of _Pristiurus_-embryos, the
development of whose spinal nerves I have been able to observe.
_Second Stage of the Spinal Nerves in Pristiurus._
In the youngest of these (Pl. 22, fig. E) the notochord has undergone but
very slight changes, but the segmental duct has made its appearance, and is
as much developed as in the _Torpedo_-embryo from which fig. D b was taken.
(The embryo from which fig. E a was derived had three visceral clefts.)
There have not as yet appeared any connective-tissue cells dorsal to the
top of the muscle-plates, so that the posterior nerve-rudiments are still
quite free and distinct.
The cells composing them are smaller than the cells of the neural canal;
they are round and nucleated; and, indeed, in their histological
constitution the nerve-rudiments exhibit no important deviations from the
previous stage, and they have hardly increased in size. In their mode of
attachment to the neural tube an important change has, however, already
commenced to be visible.
In the previous stage the two nerve-rudiments met above the summit of the
spinal cord and were broadly attached to it there; now their points of
attachment have glided a short distance down the sides of the spinal
cord[51].
Footnote 51: [May 18, 1876.--Observations I have recently made
upon the development of the cranial nerves incline me to adopt
an explanation of the change which takes place in the point of
attachment of the spinal nerves to the cord differing from that
enunciated in the text. I look upon this change as being
apparent rather than real, and as due to a growth of the roof
of the neural canal in the median dorsal line, which tends to
separate the roots of the two sides more and more, and cause
them to assume a more ventral position.]
The two nerve-rudiments have therefore ceased to meet above the summit of
the canal; and in addition to this they appear in section to narrow very
much before becoming united with its walls, so that their junctions with
these appear in a transverse section to be effected by at most one or two
cells, and are, comparatively speaking, very difficult to observe.
In an embryo but slightly older than that represented in Fig. E a the first
rudiment of the anterior root becomes visible. This appears, precisely as
in _Torpedo_, in the form of a small projection from the ventral corner of
the spinal cord (fig. E b, _ar_).
The second step in this stage (Pl. 22, fig. F) is comparable, as far as the
connective-tissue is concerned, with the section of _Torpedo_ (Pl. 22,
fig. D d). The notochord (the histological details of whose
structure are not inserted in this figure) is rather more
developed, and the segmental duct, as was the case with the
corresponding _Torpedo_-embryo, has become hollow at its anterior
extremity.
The embryo from which the section was taken possessed five visceral clefts,
but no trace of external gills.
In the section represented, though from a posterior part of the body, the
dorsal nerve-rudiments have become considerably larger than in the last
embryo; they now extend beyond the base of the neural canal. They are
surrounded to a great extent by mesoblastic tissue, which, as in the case
of the _Torpedo_, takes its origin from two sources, (1) from the
commencing vertebral bodies, (2) from the summits of the muscle-plates.
It is in many cases very difficult, especially with chromic-acid specimens,
to determine with certainty the limits of the rudiments of the posterior
root.
In the best specimens a distinct bordering line can be seen, and it is, as
a rule, possible to state the characters by which the cells of the
nerve-rudiments and vertebral bodies differ. The more important of these
are the following:--(1) The cells of the nerve-rudiment are distinctly
smaller than those of the vertebral rudiment; (2) the cells of the
nerve-rudiment are elongated, and have their long axis arranged parallel to
the long axis of the nerve-rudiment, while the cells surrounding them are
much more nearly circular.
The cells of the nerve-rudiment measure about 1/1600 × 1/4500 to 1/1600 ×
1/3200 inch, those of the vertebral rudiment 1/1600 × 1/1900 inch. The
greater difficulty experienced in distinguishing the nerve-rudiment from
the connective-tissue in _Pristiurus_ than in _Torpedo_ arises from the
fact that the connective-tissue is much looser and less condensed in the
latter than in the former.
The connective-tissue cells which have grown out from the muscle-plates
form a continuous arch over the dorsal surface of the neural tube (vide
Pl. 22, fig. F): and in some specimens it is difficult to see
whether the arch is formed by the rudiment of the posterior root
or by connective-tissue. It is, however, quite easy with the best
specimens to satisfy one's self that it is from the
connective-tissue, and not the nerve-rudiment, that the dorsal
investment of the neural canal is derived.
As in the previous case, the upper ends of each pair of posterior
nerve-rudiments are quite separate from one another, and appear in sections
to be united by a very narrow root to the walls of the neural canal at the
position indicated in fig. F[52].
Footnote 52: The artist has not been very successful in
rendering this figure.
The cells forming the nerve-rudiments have undergone slight modifications;
they are for the most part more distinctly elongated than in the earlier
stage, and appear slightly smaller in comparison with the cells of the
neural canal.
They possess as yet no distinctive characters of nerve-cells. They stain
more deeply with osmic acid than the cells around them, but with
hæmatoxylin there is but a very slight difference in intensity between
their colouring and that of the neighbouring connective-tissue cells.
The anterior roots have grown considerably in length, but their observation
is involved in the same difficulties with chromic-acid specimens as that of
the posterior rudiments.
There is a further difficulty in observing the anterior roots, which arises
from the commencing formation of white matter in the cord. This is present
in all the anterior sections of the embryo from which fig. F is taken. When
the white matter is formed the cells constituting the junction of the
anterior nerve-root with the spinal cord undergo the same changes as the
cells which are being converted into the white matter of the cord, and
become converted into nerve-fibres; these do not stain with hæmatoxylin,
and thus an apparent space is left between the nerve-root and the spinal
cord. This space by careful examination may be seen to be filled up with
fibres. In osmic acid sections, although even in these the white matter is
stained less deeply than the other tissues, it is a matter of comparative
ease to observe the junction between the anterior nerve root and the spinal
cord.
I have been successful in preparing satisfactory longitudinal sections of
embryos somewhat older than that shewn in fig. F, and they bring to light
several important points in reference to the development of the spinal
nerves. Three of these sections are represented in Pl. 22, figs. G1, G2,
and G3.
The sections are approximately horizontal and longitudinal. G1 is the most
dorsal of the three; it is not quite horizontal though nearly longitudinal.
The section passes exactly through the point of attachment of the posterior
roots to the walls of the neural canal.
The posterior rudiments appear as slight prominences of rounded cells
projecting from the wall of the neural canal. From transverse sections the
attachment of the nerves to the wall of the neural canal is proved to be
very narrow, and from these sections it appears to be of some length in the
direction of the long axis of the embryo. A combination of the sections
taken in the two directions leads to the conclusion that the nerves at this
stage thin out like a wedge before joining the spinal cord.
The independent junctions of the posterior rudiments with the spinal cord
at this stage are very clearly shewn, though the rudiments are probably
united with each other just dorsal to their junction with the spinal cord.
The nerves correspond in number with the muscle-plates, and each arises
from the spinal cord, nearly opposite the middle line of the corresponding
muscle-plates (figs. G1 and G2).
Each nerve-rudiment is surrounded by connective-tissue cells, and is
separated from its neighbours by a considerable interval.
At its origin each nerve-rudiment lies opposite the median portion of a
muscle-plate (figs. G1 and G2); but, owing to the muscle-plate acquiring an
oblique direction, at the level of the dorsal surface of the notochord it
appears in horizontal sections more nearly opposite the interval between
two muscle-plates (figs. G2 and G3).
In horizontal sections I find masses of cells which make their appearance
on a level with the ventral surface of the spinal cord. I believe I have in
some sections successfully traced these into the spinal cord, and I have
little doubt that they are the anterior roots of the spinal nerves; they
are opposite the median line of the muscle-plates, and do not appear to
join the posterior roots (vide fig. G3, _ar_).
At the end of this period or second stage the main characters of the spinal
nerves in _Pristiurus_ are the following:--
(1) The posterior nerve-rudiments form somewhat wedge-shaped masses of
tissue attached dorsally to the spinal cord.
(2) The cells of which they are composed are typical undifferentiated
embryonic cells, which can hardly be distinguished from the
connective-tissue cells around them.
(3) The nerves of each pair no longer meet above the summit of the spinal
canal, but are independently attached to its sides.
(4) Their dorsal extremities are probably united by commissures.
(5) The anterior roots have appeared; they form small conical projections
from the ventral corner of the spinal cord, but have no connexion with the
posterior rudiments.
_The Third Stage of the Spinal Nerves in Pristiurus._
With the _third stage_ the first distinct histological differentiations of
the nerve-rudiments commence. Owing to the changes both in the nerves
themselves and in the connective-tissue around them, which becomes less
compact and its cells stellate, the difficulty of distinguishing the nerves
from the surrounding cells vanishes; and the difficulties of investigation
in the later stages are confined to the modes of attachment of the nerves
to the neural canal, and the histological changes which take place in the
rudiments themselves.
The stage may be considered to commence at the period when the external
gills first make their appearance as small buds from the walls of the
visceral clefts. Already, in the earliest rudiments of the posterior root
of this period now figured, a number of distinct parts are visible (Pl. 23,
fig. H I).
Surrounding nearly the whole structure there is present a delicate
investment similar to that which I mentioned as surrounding the neural
canal and other organs; it is quite structureless, but becomes coloured
with all staining reagents. I must again leave open the question whether it
is to be looked upon as a layer of coagulated protoplasm or as a more
definite structure. This investment completely surrounds the proximal
portion of the posterior root, but vanishes near its distal extremity.
The nerve-rudiment itself may be divided into three distinct portions:--(1)
the proximal portion, in which is situated the pedicle of attachment to the
wall of the neural canal; (2) an enlarged portion, which may conveniently,
from its future fate, be called the ganglion; (3) a distal portion beyond
this. The proximal portion presents a fairly uniform diameter, and ends
dorsally in a rounded expansion; it is attached remarkably enough, not by
its extremity, but by its side, to the spinal cord. The dorsal extremities
of the posterior nerves are therefore free; as was before mentioned, they
probably serve as the starting-point of the longitudinal commissures
between the posterior roots.
The spinal cord at this stage is still made up of fairly uniform cells,
which do not differ in any important particulars from the cells which
composed it during the last stage. The outer portion of the most peripheral
layer of cells has already begun to be converted into the white matter.
The delicate investment spoken of before still surrounds the whole spinal
cord, except at the points of junction of the cord with the
nerve-rudiments. Externally to this investment, and separated from it for
the most part by a considerable interval, a mesoblastic sheath (Pl. 23,
fig. H I, _i_) for the spinal cord is beginning to be formed.
The attachment of the nerve-rudiments to the spinal cord, on account of its
smallness, is still very difficult to observe. In many specimens where the
nerve is visible a small prominence may be seen rising up from the spinal
cord at a point corresponding to _x_ (Pl. 23, fig. H I). It is, however,
rare to see this prominence and the nerve continuous with each other: as a
rule they are separated by a slight space, and frequently one of the cells
of the mesoblastic investment of the spinal cord is interposed between the
two. In some especially favourable specimens, similar to the one figured,
there can be seen a distinct cellular prominence (fig. H I, _x_) from the
spinal cord, which becomes continuous with a small prominence on the
lateral border of the nerve-rudiment near its free extremity. The absence
of a junction between the two in a majority of sections is only what might
be expected, considering how minute the junction is.
Owing to the presence of the commissure connecting the posterior roots,
some part of a nerve is present in every section.
The proximal extremity of the nerve-rudiment itself is composed of cells,
which, by their smaller size and a more circular form, are easily
distinguished from cells forming the ganglionic portion of the nerve.
The ganglionic portion of the nerve, by its externally swollen
configuration, is at once recognizable in all the sections in which the
nerve is complete. The delicate investment before mentioned is continuous
around it. The cells forming it are larger and more elongated than the
cells forming the upper portion of the nerve-rudiment: each of them
possesses a large and distinct nucleus.
The remainder of the nerve rudiment forms the commencement of the true
nerve. It can in this stage be traced only for a very small distance, and
gradually fades away, in such a manner that its absolute termination is
very difficult to observe.
The connective-tissue cells which surround the nerve-rudiment are far
looser than in the last stage, and are commencing to throw out processes
and become branched.
The anterior root-nerve has grown very considerable since the last stage.
It projects from the same region of the cord as before, but on approaching
the muscle-plate takes a sudden bend downwards (fig. H II, _ar_).
I have failed to prove that the anterior and posterior roots are at this
stage united.
_Fourth Stage._
In an embryo but slightly more advanced than the one last described,
important steps have been made in the development of the nerve-rudiment.
The spinal cord itself now possesses a covering of white matter; this is
thickest at the ventral portion of the cord, and extends to the region of
the posterior root of the spinal nerve.
The junction of the posterior root with the spinal cord is easier to
observe than in the last stage.
It is still effected by means of unaltered cells, though the cells which
form the projection from the cord to the nerve are commencing to undergo
changes similar to those of the cells which are being converted into white
matter.
In the rudiment of the posterior root itself there are still three distinct
parts, though their arrangement has undergone some alteration and their
distinctness has become more marked (Pl. 23, fig. I I).
The root of the nerve (fig. I I, _pr_) consists, as before, of nearly
circular cells, each containing a nucleus, very large in proportion to the
size of the cell. The cells have a diameter of about 1/3000 of an inch.
This mass forms not only the junction between the ganglion and the spinal
canal, but is also continued into a layer investing the outer side of the
ganglion and continuous with the nerve beyond the ganglion.
The cells which compose the ganglion (fig. I I, _sp.g_) are easily
distinguished from those of the root. Each cell is elongated with an oval
nucleus, large in proportion to the cell; and its protoplasm appears to be
continued into an angular, not to say fibrous process, sometimes at one and
more rarely at both ends. The processes of the cells are at this stage very
difficult to observe: figs. I a, I b, I c represent three cells provided
with them and placed in the positions they occupied in the ganglion.
The relatively very small amount of protoplasm in comparison to the nucleus
is fairly represented in these figures, though not in the drawing of the
ganglion as a whole. In the centre of each nucleus is a nucleolus.
Fig. I b, in which the process points towards the root of the nerve, I
regard as a commencing nerve-fibre: its more elongated shape seems to imply
this. In the next stage special bundles of nerve-fibres become very
conspicuous in the ganglion. The long diameter of an average ganglion-cell
is about 1/1600 of an inch. The whole ganglion forms an oval mass, well
separated both from the nerve-root and the nerve, and is not markedly
continuous with either. On its outer side lies the downward process of the
nerve-root before mentioned.
The nerve itself is still, as in the last case, composed of cells which are
larger and more elongated than either the cells of the root or the
ganglion.
The condition of the anterior root at this stage is hardly altered from
what it was; it is composed of very small cells, which with hæmatoxylin
stain more deeply than any other cell of the section. A figure of it is
given in I II.
Horizontal longitudinal sections of this stage are both easy to make and
very instructive. On Pl. 23, fig. K I is represented a horizontal section
through a plane near the dorsal surface of the spinal cord: each posterior
root is seen in this section to lie nearly opposite the anterior extremity
of a muscle-plate.
In a more ventral plane (fig. K II) this relation is altered, and the
posterior roots lie opposite the hinder parts of the muscle-plates.
The nerves themselves are invested by the hyaline membrane spoken of above;
and surrounding this again there is present a delicate mesoblastic
investment of spindle-shaped cells.
Longitudinal sections also throw light upon the constitution of the
anterior nerve roots (vide fig. K II, _ar_). In the two segments on the
left-hand side in this figure the anterior roots are cut through as they
are proceeding, in a more or less horizontal course, from the spinal cord
to the muscle-plates.
Where the section (which is not quite horizontal) passes through the plane
of the notochord, as on the right-hand side, the anterior roots are cut
transversely. Each root, in fact, changes its direction, and takes a
downward course.
The anterior roots are situated nearly opposite the middle of the
muscle-plates: their section is much smaller than that of the posterior
roots, and with hæmatoxylin they stain more deeply than any of the other
cells in the preparation.
The anterior roots, so far as I have been able to observe, do not at this
stage unite with the posterior; but on this point I do not speak with any
confidence.
The period now arrived at forms a convenient break in the development of
the spinal nerves; and I hope to treat the remainder of the subject,
especially the changes in the ganglion, the development of the
ganglion-cells, and of the nerve-fibres, in a subsequent paper.
I will only add that, not long after the stage last described, the
posterior root unites with the anterior root at a considerable distance
below the cord: this is shewn in Pl. 23, fig. L. Still later the portion of
the root between the ganglion and the spinal cord becomes converted into
nerve-fibres, and the ganglion becomes still further removed from the cord,
while at the same time it appears distinctly divided into two parts.
As regards the development of the cranial nerves, I have made a few
observations, which, though confessedly incomplete, I would desire to
mention here, because, imperfect as they are, they seem to shew that in
Elasmobranch Fishes the cranial nerves resemble the spinal nerves in
arising as outgrowths from the central nervous system.
I have given a figure of the development of a posterior root of a cranial
nerve in fig. M I. The section is taken from the same embryo as figs. B I,
B II, and B III.
It passes through the anterior portion of a thickening of the external
epiblast, which eventually becomes involuted as the auditory vesicle.
The posterior root of a nerve (VII) is seen growing out from the summit of
the hind brain in precisely the same manner that the posterior roots of the
spinal nerves grow out from the spinal cord: it is the rudiment of the
seventh or facial nerve. The section behind this (fig. M II), still in the
region of the ear, has no trace of a nerve, and thus serves to shew the
early discontinuity of the posterior nerve-rudiments which arise from the
brain.
I have as yet failed to detect any cranial anterior roots like those of the
spinal nerves[53]. The similarity in development between the cranial and
spinal nerves is especially interesting, as forming an important addition
to the evidence which at present exists that the cranial nerves are only to
be looked on as spinal nerves, especially modified in connexion with the
changes which the anterior extremity of the body has undergone in existing
vertebrates.
Footnote 53: [May 18, 1876.--Subsequent observations have led
me to the conclusion that no anterior nerve-roots are to be
found in the brain.]
* * * * *
My results may be summarized as follows:--
Along the extreme dorsal summit of the spinal cord there arises on each
side a continuous outgrowth.
From each outgrowth processes corresponding in number to the muscle-plates
grow downwards. These are the posterior nerve-rudiments.
The outgrowths, at first attached to the spinal cord throughout their whole
length, soon cease to be so, and remain in connexion with it in certain
spots only, which form the junctions of the posterior roots with the spinal
cord.
The original outgrowth on each side remains as a bridge, uniting together
the dorsal extremities of all the posterior rudiments. The points of
junction of the posterior roots with the spinal cord are at first situated
at the extreme dorsal summit of the latter, but eventually travel down, and
are finally placed on the sides of the cord.
After these events the posterior nerve-rudiments grow rapidly in size, and
become differentiated into a root (by which they are attached to the spinal
canal), a ganglion, and a nerve.
The anterior roots, like the posterior, are outgrowths from the spinal
cord; but the outgrowths to form them are from the first discontinuous, and
the points from which they originally spring remain as those by which they
are permanently attached to the spinal cord, and do not, as in the case of
the posterior roots, undergo a change of position. The anterior roots
arise, not vertically below, but opposite the intervals between the
posterior roots.
The anterior roots are at first quite separate from the posterior roots;
but soon after the differentiation of the posterior rudiment into a root,
ganglion, and nerve, a junction is effected between each posterior nerve
and the corresponding anterior root. The junction is from the first at some
little distance from the ganglion.
* * * * *
Investigators have hitherto described the spinal nerves as formed from part
of the mesoblast of the protovertebræ. His alone, so far as I know, takes a
different view.
His's[54] observations lead him to the conclusion that the posterior roots
are developed as ingrowths from the external epiblast into the space
between the protovertebræ and the neural canal. These subsequently become
constricted off, unite with the neural canal and form spinal nerves.
Footnote 54: _Erste Anlage des Wirbelthier-Leibes._
These statements, which have not been since confirmed, diverge nearly to
the same extent from my own results as does the ordinary account of the
development of these parts.
Hensen (Virchow's _Archiv_, Vol. XXXI. 1864) also looks upon the spinal
nerves as developed from the epiblast, but not as a direct result of his
own observations[55].
Footnote 55: [May 18, 1876.--Since the above was written
Hensen has succeeded in shewing that in mammals the rudiments
of the posterior roots arise in a manner closely resembling
that described in the present paper; and I have myself, within
the last few days, made observations which incline me to
believe that the same holds good for the chick. My observations
are as yet very incomplete.]
Without attempting, for the present at least, to explain this divergence, I
venture to think that the facts which I have just described have distinct
bearings upon one or two important problems.
One point of general anatomy upon which they throw considerable light is
the primitive origin of nerves.
So long as it was admitted that the spinal and cerebral nerves developed in
the embryo independently of the central nervous system, their mode of
origin always presented to my mind considerable difficulties.
It never appeared clear how it was possible for a state of things to have
arisen in which the central nervous system, as well as the peripheral
terminations of nerves, whether motor or sensory, were formed independently
of each other, while between them a third structure was developed which,
growing in both directions (towards the centre and towards the periphery),
ultimately brought the two into connexion.
That such a condition could be a primitive one seemed scarcely possible.
Still more remarkable did it appear, on the supposition that the primitive
mode of formation of these parts was represented in the developmental
history of vertebrates, that we should find similar structural elements in
the central and in the peripheral nervous systems.
The central nervous system arises from the epiblast, and yet contains
precisely similar nerve-cells and nerve-fibres to the peripheral nervous
system, which, if derived, as is usually stated, from the mesoblast, was
necessarily supposed to have a completely different origin from the central
nervous system.
Both of these difficulties are to a great extent removed by the facts of
the development of these parts in Elasmobranchii.
If it be admitted that the spinal roots develop as outgrowths from the
central nervous system in Elasmobranch Fishes, the question arises, how far
can it be supposed to be possible that in other vertebrates the spinal
roots and ganglia develop independently of the spinal cord, and only
subsequently become united with it.
I have already insisted that this cannot be the primary condition; and
though I am of opinion that the origin of the nerves in higher vertebrates
ought to be worked over again, yet I do not think it impossible that, by a
secondary adaptation, the nerve-roots might develop in the mesoblast[56].
Footnote 56: [May 18, 1876.--Hensen's observations, as well as
those recently made by myself on the chick, render it almost
certain that the nerves in all Vertebrates spring from the
spinal cord.]
The presence of longitudinal commissures connecting the central ends of all
the posterior roots is very peculiar. The commissures may possibly be
looked on as outlying portions of the cord, rather than as parts of the
nerves.
I have not up to this time followed their history beyond a somewhat early
period in embryonic life, and am therefore unacquainted with their fate in
the adult.
As far as I am aware, no trace of similar structures has been met with in
other vertebrates.
The commissures have a very strong resemblance to those by which in
Elasmobranch Fishes the glossopharyngeal nerve and the branches of the
pneumogastric are united in an early embryonic stage[57].
Footnote 57: Balfour, "A Preliminary Account of the
Development of Elasmobranch Fishes," _Q. J. Micros. Sc._ 1874,
plate XV. fig. 14, _v.g._ [This edition, Pl. 4, fig. 14,
_vg_].
I think it not impossible that the commissures in the two cases represent
the same structures. If this is the case, it would seem that the junction
of a number of nerves to form the pneumogastric is not a secondary state,
but the remnant of a primary one, in which all the spinal nerves were
united, as they embryonically are in Elasmobranchii.
One point brought out in my investigations appears to me to have bearings
upon the origin of the central canal of the Vertebrate nervous system, and
in consequence upon the origin of the Vertebrate group itself.
The point I allude to is the posterior nerve-rudiments making their first
appearance at the _extreme dorsal summit_ of the spinal cord.
The transverse section of the ventral nervous cord of an ordinary segmented
worm consists of two symmetrical halves placed side by side.
If by a mechanical folding the two lateral halves of the nervous cord
became bent towards each other, while into the groove formed between the
two the external skin became pushed, we should have an approximation to the
Vertebrate spinal cord. Such a folding might take place to give extra
rigidity to the body in the absence of a vertebral column.
If this folding were then completed in such a way that the groove, lined by
external skin and situated between the two lateral columns of the nervous
system, became converted into a canal, above and below which the two
columns of the nervous system united, we should have in the transformed
nervous cord an organ strongly resembling the spinal cord of Vertebrates.
This resemblance would even extend beyond mere external form. Let the
ventral nervous cord of the common earthworm, _Lumbricus agricola_, be used
for comparison[58], a transverse section of which is represented by
Leydig[59] and Claparède. In this we find that on the ventral surface (the
Annelidan ventral surface) of the nervous cord the ganglion-cells (grey
matter) (_k_) are situated, and on the dorsal side the nerve-fibres or
white matter (_h_). If the folding that I have supposed were to take place,
the grey and white matters would have very nearly the relative situations
which they have in the Vertebrate spinal cord.
Footnote 58: The nervous cords of other Annelids resemble that
of _Lumbricus_ in the relations of the ganglion-cells of the
nerve-fibres.
Footnote 59: _Tafeln zur vergleichenden Anatomie_, Taf. iii.
fig. 8.
The grey matter would be situated in the interior and surround the
epithelium of the central canal, and the white matter would nearly surround
the grey and form the anterior white commissure. The nerves would then
arise, not from the sides of the nervous cord as in existing Vertebrates,
but from its extreme ventral summit.
One of the most striking features which I have brought to light with
reference to the development of the posterior roots, is the fact of their
growing out from the extreme dorsal summit of the neural canal--a position
analogous to the ventral summit of the Annelidan nervous cord. Thus the
posterior roots of the nerves in Elasmobranchii arise in the exact manner
which might have been anticipated were the spinal cord due to such a
folding as I have suggested. The argument from the nerves becomes the
stronger, from the great peculiarity in the position of the outgrowth, a
feature which would be most perplexing without some such explanation as I
have proposed. The central epithelium of the neural canal according to this
view represents the external skin; and its ciliation is to be explained as
a remnant of the ciliation of the external skin now found amongst many of
the lower Annelids.
I have, however, employed the comparison of the Vertebrate and Annelidan
nervous cords, not so much to prove a genetic relation between the two as
to shew the _à priori_ possibility of the formation of a _spinal canal_ and
the _à posteriori_ evidence we have of the Vertebrate spinal canal having
been formed in the way indicated.
I have not made use of what is really the strongest argument for my view,
viz. that the embryonic mode of formation of the spinal canal, by a folding
in of the external epiblast, is the very method by which I have supposed
the spinal canal to have been formed in the ancestors of Vertebrates.
My object has been to suggest a meaning for the peculiar primitive position
of the posterior roots, rather than to attempt to explain in full the
origin of the spinal canal.
EXPLANATION OF THE PLATES[60].
Footnote 60: The figures on these Plates give a fair general
idea of the appearance presented by the developing spinal
nerves; but the finer details of the original drawings have in
several cases become lost in the process of copying.
The figures which are tinted represent sections of embryos
hardened in osmic acid; those without colour sections of
embryos hardened in chromic acid.
PLATE 22.
Fig. A. Section through the dorsal region of an embryo of _Scyllium
stellare_, with the rudiments of two visceral clefts. The section
illustrates the general features at a period anterior to the appearance of
the posterior nerve-roots.
_nc._ neural canal. _mp._ muscle-plate. _ch._ notochord. _x._
subnotochordal rod. _ao._ rudiment of dorsal aorta. _so._ somatopleure.
_sp._ splanchnopleure. _al._ alimentary tract. All the parts of the section
except the spinal cord are drawn somewhat diagrammatically.
Figs. B I, B II, B III. Three sections of a _Pristiurus_-embryo. B I is
through the heart, B II through the anterior part of the dorsal region, and
B III through a point slightly behind this. Drawn with a camera. (Zeiss CC
ocul. 2.)
In B III there is visible a slight proliferation of cells from the dorsal
summit of the neural canal.
In B II this proliferation definitely constitutes two club-shaped masses of
cells (_pr_), both attached to the dorsal summit of the neural canal. The
masses are the rudiments of the posterior nerve-roots.
In B I the rudiments of the posterior roots are of considerable length.
_pr._ rudiment of posterior roots. _nc._ neural canal. _mp._ muscle-plate.
_ch._ notochord. _x._ subnotochordal rod. _ao._ dorsal aorta. _so._
somatopleure. _sp._ splanchnopleure. _al._ alimentary canal. _ht._ heart.
Fig. C. Section from a _Pristiurus_-embryo, slightly older than B. Camera.
(Zeiss CC ocul. 2.) The embryo from which this figure was taken was
slightly distorted in the process of removal from the blastoderm.
_vr._ rudiment of vertebral body. Other reference letters as in previous
figures.
Fig. D a. Section through the dorsal region of a _Torpedo_-embryo with
three visceral clefts. (Zeiss CC ocul. 2.) The section shews the formation
of the dorsal nerve-rudiments (_pr_) and of a ventral anterior
nerve-rudiment (_ar_), which at this early stage is not distinctly
cellular.
_ar._ rudiment of an anterior nerve-root. _y._ cells left behind on the
separation of the external skin from the spinal cord. _c._
connective-tissue cells springing from the summit of the muscle-plates.
Other reference letters as above.
Fig. D b. Section from dorsal region of a _Torpedo_-embryo somewhat older
than D a. Camera. (Zeiss CC ocul. 2.) The posterior nerve-rudiment is
considerably longer than in fig. Da, and its pedicle of attachment to the
spinal cord is thinner. The anterior nerve-rudiment, of which only the edge
is present in the section, is distinctly cellular.
_m._ mesoblast growing up from vertebral rudiment. _sd._ segmental duct.
Fig. D c. Section from a still older _Torpedo_-embryo. Camera. (Zeiss CC
ocul. 2.) The connective-tissue cells are omitted. The rudiment of the
ganglion (_g_) on the posterior root has appeared. The rudiment of the
posterior nerve is much longer than before, and its junction with the
spinal cord is difficult to detect. The anterior root is now an elongated
cellular structure.
_g._ ganglion.
Fig. D d. Longitudinal and vertical section through a _Torpedo_-embryo of
the same age as D c.
The section shews the commissures (_x_) uniting the posterior roots.
Fig. E a. Section of a _Pristiurus_-embryo belonging to the second stage.
Camera. (Zeiss CC ocul. 2.) The section shews the constriction of the
pedicle which attaches the posterior nerve-rudiments to the spinal cord.
_pr._ rudiment of posterior nerve-root. _nc._ neural canal. _mp._
muscle-plate. _vr._ vertebral rudiment. _sd._ segmental duct. _ch._
notochord. _so._ somatopleure. _sp._ splanchnopleure. _ao._ aorta. _al._
alimentary canal.
Fig. E b. Section of a _Pristiurus_-embryo slightly older than Ea. Camera.
(Zeiss CC ocul. 2.) The section shews the formation of the anterior
nerve-root (_ar_).
_ar._ rudiment of the anterior nerve-root.
Fig. F. Section of a _Pristiurus_-embryo with the rudiments of five
visceral clefts. Camera. (Zeiss CC ocul. 2.)
The rudiment of the posterior root is seen surrounded by connective-tissue,
from which it cannot easily be distinguished. The artist has not been very
successful in rendering this figure.
Figs. G1, G2, G3. Three longitudinal and horizontal sections of an embryo
somewhat older than F. The embryo from which these sections were taken was
hardened in osmic acid, but the sections have been represented without
tinting. G1 is most dorsal of the three sections. Camera. (Zeiss CC ocul.
1.)
_nc._ neural canal. _sp.c._ spinal cord. _pr._ rudiment of posterior root.
_ar._ rudiment of anterior root. _mp._ muscle-plate. _c._ connective-tissue
cells. _ch._ notochord.
PLATE 23.
Fig. H I. Section through the dorsal region of a _Pristiurus_-embryo in
which the rudimentary external gills are present as very small knobs.
Camera. (Zeiss CC ocul. 2.)
The section shews the commencing differentiation of the posterior
nerve-rudiment into root (_pr_), ganglion (_sp.g_), and nerve (_n_), and
also the attachment of the nerve-root to the spinal cord (_x_). The
variations in the size and shape of the cells in the different parts of the
nerve-rudiment are completely lost in the figure.
_pr._ posterior nerve-root. _sp.g._ ganglion of posterior root. _n._ nerve
of posterior root. _x._ attachment of posterior root to spinal cord. _w._
white matter of spinal cord. _i._ mesoblastic investment to the spinal
cord.
Fig. H II. Section through the same embryo as H I. (Zeiss CC ocul. 1.)
The section contains an anterior root, which takes its origin at a point
opposite the interval between two posterior roots.
The white matter has not been very satisfactorily represented by the
artist.
Figs. I I, I II. Two sections of a _Pristiurus_-embryo somewhat older than
H. Camera. (Zeiss CC ocul. 1.)
The connective-tissue cells are omitted.
Figs. I a, I b, I c. Three isolated cells from the ganglion of one of the
posterior roots of the same embryo.
Figs. K I, K II. Two horizontal longitudinal sections through an embryo in
which the external gills have just appeared. K I is the most dorsal of the
two sections. Camera. (Zeiss CC ocul. 1.)
The sections shew the relative positions of the anterior and posterior
roots at different levels.
_pr._ posterior nerve-rudiment. _ar._ anterior nerve-rudiment. _sp.c._
spinal cord. _n.c._ neural canal. _mp._ muscle-plate. _mp´._ first-formed
muscles.
Fig. L. Longitudinal and vertical section through the trunk of a
_Scyllium_-embryo after the external gills have attained their full
development. Camera. (Zeiss CC ocul. 1.)
The embryo was hardened in a mixture of chromic acid and osmic acid.
The section shews the commissures which dorsally unite the posterior roots,
and also the junction of the anterior and posterior roots. The commissures
are unfortunately not represented in the figure with great accuracy; their
outlines are in nature perfectly regular, and not, as in the figure,
notched at the junctions of the cells composing them. Their cells are
apparently more or less completely fused, and certainly not nearly so
clearly marked as in the figure. The commissures stain very deeply with the
mixture of osmic and chromic acid, and form one of the most conspicuous
features in successful longitudinal sections of embryos so hardened. In
sections hardened with chromic acid only they cannot be seen with the same
facility.
_sp.c._ spinal cord. _gr._ grey matter. _w._ white matter. _ar._ anterior
root. _pr._ posterior root. _x._ commissure uniting the posterior roots.
Figs. M I, M II. Two sections through the head of the same embryo as
fig. B. M I, the foremost of the two, passes through the anterior part of
the thickening of epiblast, which becomes involuted as the auditory
vesicle. It contains the rudiment of the seventh nerve, VII. Camera.
(Zeiss CC ocul. 2.)
VII. rudiment of seventh nerve. _au._ thickening of external epiblast,
which becomes involuted as the auditory vesicle. _n.c._ neural canal. _ch._
notochord. _pp._ body-cavity in the head. _so._ somatopleure. _sp._
splanchnopleure. _al._ throat exhibiting an outgrowth to form the first
visceral cleft.
IX. ON THE SPINAL NERVES OF AMPHIOXUS[61].
Footnote 61: From the _Journal of Anatomy and Physiology_,
Vol. X. 1876.
During a short visit to Naples in January last, I was enabled, through the
kindness of Dr Dohrn, to make some observations on the spinal nerves of
Amphioxus. These were commenced solely with the view of confirming the
statements of Stieda on the anatomy of the spinal nerves, which, if
correct, appeared to me to be of interest in connection with the
observations I had made that, in Elasmobranchii, the anterior and posterior
roots arise alternately and not in the same vertical plane. I have been led
to conclusions on many points entirely opposed to those of Stieda, but,
before recording these, I shall proceed briefly to state his results, and
to examine how far they have been corroborated by subsequent observers.
Stieda[62], from an examination of sections and isolated spinal cords, has
been led to the conclusion that, in Amphioxus, the nerves of the opposite
sides arise alternately, except in the most anterior part of the body,
where they arise opposite each other. He also states that the nerves of the
same side issue alternately from the dorsal and ventral corners of the
spinal cord. He regards two of these roots (dorsal and ventral) on the same
side as together equivalent to a single spinal nerve of higher vertebrates
formed by the coalescence of a dorsal and ventral root.
Footnote 62: _Mém. Acad. Pétersbourg_, Vol. XIX.
Langerhans[63] apparently agrees with Stieda as to the facts about the
alternation of dorsal and ventral roots, but differs from him as to the
conclusions to be drawn from those facts. He does not, for two reasons,
believe that two nerves of Amphioxus can be equivalent to a single nerve in
higher vertebrates: (1) Because he finds no connecting branch between two
succeeding nerves, and no trace of an anastomosis. (2) Because he finds
that each nerve in Amphioxus supplies a complete myotome, and he considers
it inadmissible to regard the nerves, which in Amphioxus together supply
_two myotomes_, as equivalent to those which in higher vertebrates supply a
_single myotome only_.
Footnote 63: _Archiv f. mikr. Anatomie_, Vol. XII.
Although the agreement as to facts between Langerhans and Stieda is
apparently a complete one, yet a critical examination of the statements of
these two authors proves that their results, on one important point at
least, are absolutely contradictory. Stieda, Pl. III. fig. 19, represents a
longitudinal and horizontal section through the spinal cord which exhibits
the nerves arising alternately on the two sides, and represents each
myotome supplied by _one nerve_. In his explanation of the figure he
expressly states that the nerves of one plane only (_i.e._ only those with
dorsal or only those with ventral roots) are represented; so that if all
the nerves which issue from the spinal cord had been represented double the
number figured must have been present. But since each myotome is supplied
by _one_ nerve in the figure, if all the nerves present were represented,
each myotome would be supplied by two nerves.
Since Langerhans most emphatically states that only _one nerve_ is present
for _each myotome_, it necessarily follows that he or Stieda has made an
important error; and it is not too much to say that this error is more than
sufficient to counterbalance the value of Langerhans' evidence as a
confirmation of Stieda's statements.
I commenced my investigations by completely isolating the nervous system of
Amphioxus by maceration in nitric acid according to the method recommended
by Langerhans[64]. On examining specimens so obtained it appeared that, for
the greater length of the cord, the nerves arose alternately on the two
sides, as was first stated by Owsjannikow, and subsequently by Stieda and
Langerhans; but to my surprise not a trace could be seen of a difference of
level in the origin of the nerves of the same side.
Footnote 64: _Loc. cit._
The more carefully the specimens were examined from all points of view, the
more certainly was the conclusion forced upon me, that nerves issuing from
the ventral corner of the spinal cord, as described by Stieda, had no
existence.
Not satisfied by this examination, I also tested the point by means of
sections. I carefully made transverse sections of a successfully hardened
Amphioxus, through the whole length of the body. There was no difficulty in
seeing the dorsal roots in every third section or so, but not a trace of a
ventral root was to be seen. There can, I think, be no doubt, that, had
ventral roots been present, they must, in some cases at least, have been
visible in my sections.
In dealing with questions of this kind it is no doubt difficult to prove a
negative; but, since the two methods of investigation employed by me both
lead to the same result, I am able to state with considerable confidence
that my observations lend no support to the view that the alternate spinal
nerves of Amphioxus have their roots attached to the ventral corner of the
spinal cord.
How a mistake on this point arose it is not easy to say. All who have
worked with Amphioxus must be aware how difficult it is to conserve the
animal in a satisfactory state for making sections. The spinal cord,
especially, is apt to be distorted in shape, and one of its ventral corners
is frequently produced into a horn-like projection terminating in close
contact with the sheath. In such cases the connective tissue fibres of the
sheath frequently present the appearance of a nerve-like prolongation of
the cord; and for such they might be mistaken if the sections were examined
in a superficial manner. It is not, however, easy to believe that, with
well conserved specimens, a mistake could be made on this point by so
careful and able an investigator as Stieda, especially considering that the
histological structure of the spinal nerves is very different from that of
the fibrous prolongations of the sheath of the spinal cord.
It only remains for me to suppose that the specimens which Stieda had at
his disposal, were so shrunk as to render the origin of the nerves very
difficult to determine.
The arrangement of the nerves of Amphioxus, according to my own
observations, is as follows.
The anterior end of the central nervous system presents on its left and
dorsal side a small pointed projection, into which is prolonged a
diverticulum from the dilated anterior ventricle of the brain. This may
perhaps be called the olfactory nerve, though clearly of a different
character to the other nerves. It was first accurately described by
Langerhans[65].
Footnote 65: _Loc. cit._
Vertically below the olfactory nerve there arise two nerves, which issue at
the same level from the ventral side of the anterior extremity of the
central nervous system. These form the first pair of nerves, and are the
only pair which arise from the ventral portion of the cerebro-spinal cord.
The two nerves, which form the second pair, arise also opposite each other
but from the dorsal side of the cord. The first and second pair of nerves
have both been accurately drawn and described by Langerhans: they, together
with the olfactory nerve, can easily be seen in nervous systems which have
been isolated by maceration.
In the case of the third pair of nerves, the nerve on the right-hand side
is situated not quite opposite but slightly behind that on the left. The
right nerve of the fourth pair is situated still more behind the left, and,
in the case of the fifth pair, the nerve to the right is situated so far
behind the left nerve that it occupies a position half-way between the left
nerves of the fifth and sixth pairs. In all succeeding nerves the same
arrangement holds good, so that they exactly alternate on two sides.
Such is the arrangement carefully determined by me from one specimen. It is
possible that it may not be absolutely constant, but the following general
statement almost certainly holds good.
All the nerves of Amphioxus, except the first pair, have their roots
inserted in the dorsal part of the cord. In the case of the first two pairs
the nerves of the two sides arise opposite each other; in the next few
pairs, the nerves on the right-hand side gradually shift backwards: the
remaining nerves spring alternately from the two sides of the cord.
For each myotome there is a single nerve, which enters, as in the case of
other fishes, the intermuscular septum. This point may easily be determined
by means of longitudinal sections, or less easily from an examination of
macerated specimens. I agree with Langerhans in denying the existence of
ganglia on the roots of the nerves.
X.
A MONOGRAPH
ON THE
DEVELOPMENT OF
ELASMOBRANCH FISHES.
PUBLISHED 1878.
PREFACE.
The present Monograph is a reprint of a series of papers published in the
_Journal of Anatomy and Physiology_ during the years 1876, 1877 and 1878.
The successive parts were struck off as they appeared, so that the earlier
pages of the work were in print fully two years ago. I trust the reader
will find in this fact a sufficient excuse for a certain want of coherence,
which is I fear observable, as well as for the omission of references to
several recent publications. The first and second chapters would not have
appeared in their present form had I been acquainted, at the time of
writing them, with the researches which have since been published, on the
behaviour of the germinal vesicle and on the division of nuclei. I may also
call attention to the valuable papers of Prof. His[66] on the formation of
the layers in Elasmobranchii, and of Prof. Kowalevsky[67] on the
development of Amphioxus, to both of which I would certainly have referred,
had it been possible for me to do so.
Footnote 66: _Zeitschrift f. Anat. u. Entwicklungsgeschichte_,
Bd. II.
Footnote 67: _Archiv f. Micr. Anat._ Bd. XIII.
Professor His deals mainly with the subjects treated of in Chapter III.,
and gives a description very similar to my own of the early stages of
development. His interpretations of the observed changes are, however, very
different from those at which I have arrived. Although this is not the
place for a discussion of Prof. His's views, I may perhaps state that, in
spite of the arguments he has brought forward in support of his position, I
am still inclined to maintain the accuracy of my original account. The very
striking paper on Amphioxus by Kowalevsky (the substance of which I
understand to have been published in Russia at an earlier period) contains
a confirmation of the views expressed in chapter VI. on the development of
the mesoblast, and must be regarded as affording a conclusive
demonstration, that in the case of Vertebrata the mesoblast has primitively
the form of a pair of diverticula from the walls of the archenteron.
* * * * *
The present Memoir, while differing essentially in scope and object from
the two important treatises by Professors His[68] and Götte[69], which have
recently appeared in Germany, has this much in common with them, that it
deals monographically with the development of a single type: but here the
resemblance ends. Both of these authors seek to establish, by a careful
investigation of the development of a single species, the general plan of
development of Vertebrates in general, if not of the whole animal kingdom.
Both reject the theory of descent, as propounded by Mr Darwin, and offer
completely fresh explanations of the phenomena of Embryology. Accepting, as
I do, the principle of natural selection, I have had before me, in writing
the Monograph, no such ambitious aim as the establishment of a completely
new system of Morphology. My object will have been fully attained if I have
succeeded in adding a few stones to the edifice, the foundations of which
were laid by Mr Darwin in his work on the _Origin of Species_.
Footnote 68: _Erste Anlage des Wirbelthierleibes._
Footnote 69: _Entwicklungsgeschichte der Unke._
I may perhaps call attention to one or two special points in this work
which seem to give promise of further results. The chapter on the
Development of the Spinal and Cranial Nerves contains a modification of the
previously accepted views on this subject, which may perhaps lead to a more
satisfactory conception of the origin of nerves than has before been
possible, and a more accurate account of the origin of the muscle-plates
and vertebral column. The attempt to employ the embryological relations of
the cephalic prolongations of the body-cavity, and of the cranial nerves,
in the solution of the difficult problems of the Morphology of the head,
may prove of use in the line of study so successfully cultivated by our
great English Anatomist, Professor Huxley. Lastly, I venture to hope that
my conclusions in reference to the relations of the sympathetic system and
the suprarenal body, and to the development of the mesoblast, the
notochord, the limbs, the heart, the venous system, and the excretory
organs, are not unworthy of the attention of Morphologists.
* * * * *
The masterly manner in which the systematic position of Elasmobranchii is
discussed by Professor Gegenbaur, in the introduction to his Monograph on
the Cranial Skeleton of the group, relieves me from the necessity of
entering upon this complicated question. It is sufficient for my purpose
that the Elasmobranch Fishes be regarded as forming one of the most
primitive groups among Vertebrates, a view which finds ample confirmation
in the importance of the results to which Prof. Gegenbaur and his pupils
have been led in this branch of their investigations.
* * * * *
Though I trust that the necessary references to previous contributions in
the same department of enquiry have not been omitted, the 'literature of
the subject' will nevertheless be found to occupy a far smaller share of
space than is usual in works of a similar character. This is an intentional
protest on my part against, what appears to me, the unreasonable amount of
space so frequently occupied in this way. The pages devoted to the
'previous literature' only weary the reader, who is not wise enough to skip
them, and involve a great and useless expenditure of time on the part of
any writer, who is capable of something better than the compilation of
abstracts.
* * * * *
In conclusion, my best thanks are due to Drs Dohrn and Eisig for the
uniformly kind manner in which they have forwarded my researches both at
the Zoological Station in Naples, and after my return to England; and also
to Mr Henry Lee and to the Manager and Directors of the Brighton Aquarium,
who have always been ready to respond to my numerous demands on their
liberality.
To my friend and former teacher Dr Michael Foster I tender my sincerest
thanks for the never-failing advice and assistance which he has given
throughout the whole course of the work.
TABLE OF CONTENTS.
CHAPTER I.
THE RIPE OVARIAN OVUM, pp. 213-221.
Structure of ripe ovum. Atrophy of germinal vesicle. The extrusion of its
membrane and absorption of its contents. Oellacher's observations on the
germinal vesicle. Götte's observations. Kleinenberg's observations. General
conclusions on the fate of the germinal vesicle. Germinal disc.
CHAPTER II.
THE SEGMENTATION, pp. 222-245.
Appearance of impregnated germinal disc. Stage with two furrows. Stage with
twenty-one segments. Structure of the sides of the furrows. Later stages of
segmentation. Spindle-shaped nuclei. Their presence outside the blastoderm.
Knobbed nuclei. Division of nuclei. Conclusion of segmentation. Nuclei of
the yolk. Asymmetry of the segmented blastoderm. Comparison of Elasmobranch
segmentation with that of other meroblastic ova. Literature of Elasmobranch
segmentation.
CHAPTER III.
FORMATION OF THE LAYERS, pp. 246-285.
Division of blastoderm into two layers. Formation of segmentation cavity.
Disappearance of cells from floor of segmentation cavity. Nuclei of yolk
and of blastoderm. Formation of embryonic rim. Appearance of a layer of
cells on the floor of the segmentation cavity. Formation of mesoblast.
Formation of medullary groove. Disappearance of segmentation cavity.
Comparison of segmentation cavity of Elasmobranchii with that of other
types. Alimentary cavity. Formation of mesoblast in two lateral plates.
Protoplasmic network of yolk. Summary. Nature of meroblastic ova.
Comparison of Elasmobranch development with that of other types. Its
relation to the Gastrula. Haeckel's views on vertebrate Gastrula. Their
untenable nature. Comparison of primitive streak with blastopore.
Literature.
CHAPTER IV.
GENERAL FEATURES OF THE ELASMOBRANCH EMBRYO AT SUCCESSIVE
STAGES, pp. 286-297.
Description of Stages A-Q. Enclosure of yolk by blastoderm. Relation of the
anus of Rusconi to the blastopore.
CHAPTER V.
STAGES B-G, pp. 298-314.
_General features of the epiblast._--Original uniform constitution.
Separation into lateral and central portions. _The medullary groove._--Its
conversion into the medullary canal. _The mesoblast._--Its division into
somatic and splanchnic layers. Formation of protovertebræ. The lateral
plates. The caudal swellings. The formation of the body-cavity in the head.
_The alimentary canal._--Its primitive constitution. The anus of Rusconi.
Floor formed by yolk. Formation of cellular floor from cells formed around
nuclei of the yolk. Communication behind of neural and alimentary canals.
Its discovery by Kowalevsky. Its occurrence in other instances. _General
features of the hypoblast._ _The notochord._--Its formation as a median
thickening of the hypoblast. Possible interpretations to be put on this.
Its occurrence in other instances.
CHAPTER VI.
DEVELOPMENT OF THE TRUNK DURING STAGES G TO K, pp. 315-360.
Order of treatment. _External epiblast._--Characters of epiblast. Its late
division into horny and epidermic layers. Comparison of with Amphibian
epiblast. _The unpaired fins._ _The paired fins._--Their formation as
lateral ridges of epiblast. Hypothesis that the limbs are remnants of
continuous lateral fins. _Mesoblast._--Constitution of lateral plates of
mesoblast. Their splanchnic and somatic layers. Body-cavity constituting
space between them. Their division into lateral and vertebral plates.
Continuation of body-cavity into vertebral plates. Protovertebræ. Division
into muscle-plates and vertebral bodies. Development of muscle-plates.
Disappearance of segmentation in tissue to form vertebral bodies.
Body-cavity and parietal plates. Primitive independent halves of
body-cavity. Their ventral fusion. Separation of anterior part of
body-cavity as pericardial cavity. Communication of pericardial and
peritoneal cavities. Somatopleure and splanchnopleure. _Résumé._ General
considerations on development of mesoblast. Probability of lateral plates
of mesoblast in Elasmobranchii representing alimentary diverticula. Meaning
of secondary segmentation of vertebral column. The _urinogenital
system._--Development of segmental duct and segmental tubes as solid
bodies. Formation of a lumen in them, and their opening into body-cavity.
Comparison of segmental duct and segmental tubes. Primitive ova. Their
position. Their structure. _The notochord._--The formation of its sheath.
The changes in its cells.
CHAPTER VII.
GENERAL DEVELOPMENT OF THE TRUNK FROM STAGE K TO THE
CLOSE OF EMBRYONIC LIFE, pp. 361-377.
_External epiblast._--Division into separate layers. Placoid scales.
Formation of their enamel. _Lateral line._--Previous investigations.
Distinctness of lateral line and lateral nerve. Lateral nerve a branch of
vagus. Lateral line a thickening of epiblast. Its greater width behind. Its
conversion into a canal by its cells assuming a tubular arrangement. The
formation of its segmental apertures. Mucous canals of the head. Their
nerve-supply. Reasons for dissenting from Semper's and Götte's view of
lateral nerve. _Muscle-plates._--Their growth. Conversion of both layers
into muscles. Division into dorso-lateral and ventro-lateral sections.
Derivation of limb-muscles from muscle-plates. _Vertebral column and
notochord._--Previous investigations. Formation of arches. Formation of
cartilaginous sheath of notochord and membrana elastica externa.
Differentiation of neural arches. Differentiation of hæmal arches.
Segmentation of cartilaginous sheath of notochord. Vertebral and
intervertebral regions. Notochord.
CHAPTER VIII.
DEVELOPMENT OF THE SPINAL NERVES AND OF THE SYMPATHETIC
NERVOUS SYSTEM, pp. 378-396.
_The spinal nerves._--Formation of posterior roots. Later formation of
anterior roots. Development of commissure uniting posterior roots.
Subsequent development of posterior roots. Their change in position.
Development of ganglion. Further changes in anterior roots. Junction of
anterior and posterior roots. Summary. _General considerations._--Origin of
nerves. Hypothesis explaining peripheral growth. Hensen's views. Later
investigations. Götte. Calberla. Relations between Annelidan and Vertebrate
nervous systems. Spinal canal. Dr Dohrn's views. Their difficulties.
Hypothesis of dorsal coalescence of lateral nerve cords. _Sympathetic
nervous system._--Development of sympathetic ganglia on branches of spinal
nerves. Formation of sympathetic commissure.
CHAPTER IX.
DEVELOPMENT OF THE ORGANS IN THE HEAD, pp. 397-445.
DEVELOPMENT OF THE BRAIN, pp. 397-407. General history.
_Fore-brain._--Optic vesicles. Infundibulum. Pineal gland. Olfactory lobes.
Lateral ventricles. _Mid-brain._ _Hind-brain._--Cerebellum.
Medulla.--Previous investigations. Huxley. Miklucho-Maclay. Wilder. ORGANS
OF SENSE, pp. 407-412. _Olfactory organ._--Olfactory pit. Schneiderian
folds. _Eye._ General development. Hyaloid membrane. Lens capsule.
Processus falciformis. _Auditory organs._--Auditory pit. Semicircular
canals. MOUTH INVOLUTION and PITUITARY BODY, pp. 412-414. Outgrowth of
pituitary involution. Separation of pituitary sack. Junction with
infundibulum. DEVELOPMENT OF CRANIAL NERVES, pp. 414-428. Early development
of 5th, 7th, 8th, 9th and 10th cranial nerves. Distribution of the nerves
in the adult. _The fifth nerve._--Its division into ophthalmic and
mandibular branches. Later formation of superior maxillary branch. _Seventh
and auditory nerves._--Separation of single rudiment into seventh and
auditory. Forking of seventh nerve over hyomandibular cleft. Formation of
anterior branch to form ramus ophthalmicus superficialis of adult. General
view of morphology of branches of seventh nerve. _Glossopharyngeal and
vagus nerves._--General distribution at stage L. Their connection by a
commissure. Junction of the commissure with commissure connecting posterior
roots of spinal nerves. Absence of anterior roots. Hypoglossal nerve.
MESOBLAST OF HEAD, pp. 429-432. _Body-cavity and myotomes of
head._--Continuation of body-cavity into head. Its division into segments.
Development of muscles from their walls. General mesoblast of head.
NOTOCHORD IN HEAD, p. 433. HYPOBLAST OF THE HEAD, pp. 433-434. The
formation of the gill-slits. Layer from which gills are derived.
SEGMENTATION OF THE HEAD, pp. 434-440. Indication of segmentation afforded
by (1) cranial nerves, (2) visceral clefts, (3) head-cavities. Comparison
of results obtained.
CHAPTER X.
THE ALIMENTARY CANAL, pp. 446-459.
_The solid oesophagus._--OEsophagus originally hollow. Becomes solid during
Stage K. _The postanal section of the alimentary tract._--Continuity of
neural and alimentary canals. Its discovery by Kowalevsky. The postanal
section of gut. Its history in Scyllium. Its disappearance. _The cloaca and
anus._--The formation of the cloaca. Its junction with segmental ducts.
Abdominal pockets. Anus. _The thyroid body._--Its formation in region of
mandibular arch. It becomes solid. Previous investigations. _The
pancreas._--Arises as diverticulum from dorsal side of duodenum. Its
further growth. Formation of duct. _The liver._--Arises as ventral
diverticulum of duodenum. Hepatic cylinders. Comparison with other types.
_The subnotochordal rod._--Its separation from dorsal wall of alimentary
canal. The section of it in the trunk. In the head. Its disappearance.
Views as to its meaning.
CHAPTER XI.
THE VASCULAR SYSTEM AND VASCULAR GLANDS, pp. 460-478.
_The heart._--Its development. Comparison with other types. Meaning of
double formation of heart. _The general circulation._ The venous system.
The primitive condition of. Comparison of, with Amphioxus and Annelids. The
cardinal veins. Relations of caudal vein. _The circulation of the
yolk-sack._--Previous observations. Various stages. Difference of type in
amniotic Vertebrates. _The vascular glands._--Suprarenal and interrenal
bodies. Previous investigations. _The suprarenal bodies._--Their structure
in the adult. Their development from the sympathetic ganglia. _The
interrenal body._--Its structure in the adult. Its independence of
suprarenal bodies. Its development.
CHAPTER XII.
THE ORGANS OF EXCRETION, pp. 479-520.
Previous investigations. _Excretory organs and genital ducts in adult._ _In
male._--Kidney and Wolffian body. Wolffian duct. Ureters. Cloaca. Seminal
bladders. Rudimentary oviduct. _In female._--Wolffian duct. Ureters.
Cloaca.--Segmental openings. Glandular tubuli of kidney. Malpighian bodies.
Accessory Malpighian bodies. Relations of to segmental tubes. Vasa
efferentia. Comparison of Scyllium with other Elasmobranchii. _Development
of segmental tubes._ Their junction with segmental duct. Their division
into four segments. Formation of Malpighian bodies. Connection between
successive segments. Morphological interest of. _Development of Müllerian
and Wolffian ducts._ _In female_--General account. Formation of oviduct as
nearly solid cord. Hymen. _In male_--Rudimentary Müllerian
duct.--Comparison of development of Müllerian duct in Birds and
Elasmobranchii. Own researches. Urinal cloaca. _Formation of Wolffian body
and kidney proper._--General account. Details of formation of ureters.
_Vasa efferentia._--Views of Semper and Spengel. Difficulties of Semper's
views. Unsatisfactory result of own researches. General homologies.
_Résumé._ Postscript.
CHAPTER I.
THE RIPE OVARIAN OVUM.
The ripe ovum is nearly spherical, and, after the removal of its capsule,
is found to be unprovided with any form of protecting membrane.
My investigations on the histology of the ripe ovarian ovum have been made
with the ova of the Gray Skate (_Raja batis_) only, and owing to a
deficiency of material are somewhat imperfect.
The bulk of the ovum is composed of yolk spherules, imbedded in a
protoplasmic matrix. Dr Alexander Schultz[70], who has studied with great
care the constitution of the yolk, finds, near the centre of the ovum, a
kernel of small yolk spherules, which is succeeded by a zone of spherules
which gradually increase in size as they approach the surface. But, near
the surface, he finds a layer in which they again diminish in size and
exhibit numerous transitional forms on the way to molecular yolk granules.
These Dr Schultz regards as in a retrogressive condition.
Footnote 70: _Archiv für Micro. Anat._ Vol. XI. 1875.
Another interesting feature about the yolk is the presence in it of a
protoplasmic network. Dr Schultz has completely confirmed, and on some
points enlarged, my previous observations on this subject[71]. Dr Schultz's
confirmation is the more important, since he appears to be unacquainted
with my previous investigations. In my paper (_loc. cit._), after giving a
description of the network I make the following statement as to its
distribution.
"A specimen of this kind is represented in Plate 14, fig. 2,
_n.y_, where the meshes of the network are seen to be finer
immediately around the nuclei, and coarser in the intervals.
The specimen further shews, in the clearest manner, that
this network is not divided into areas, each representing a
cell and each containing a nucleus. I do not know to what
extent this network extends into the yolk. I have never yet
seen the limits of it, though it is very common to see the
coarsest yolk-granules lying in its meshes. Some of these
are shewn in Plate 14, fig. 2, _y.k._" [This edition, p.
65.]
Footnote 71: _Quart. Journ. Micro. Science_, Oct. 1874. [This
edition, No. V.]
Dr Schultz, by employing special methods of hardening and cutting sections
of the whole egg, has been able to shew that this network extends, in the
form of fine radial lines, from the centre to the circumference; and he
rightly states, that it exhibits no cell-like structures. I have detected
this network extending throughout the whole yolk in young eggs, but have
failed to see it with the distinctness which Dr Schultz attributes to it in
the ripe ovum. Since it is my intention to enter fully both into the
structure and meaning of this network in my account of a later stage, I say
no more about it here.
At one pole of the ripe ovum a slight examination demonstrates the presence
of a small circular spot, sharply distinguished from the remainder of the
yolk by its lighter colour. Around this spot is an area which is also of a
lighter colour than the yolk, and the outer border of which gradually
shades into the normal tint of the yolk. If a section be made through this
part (vide Pl. 6, fig. 1) the circular spot will be found to be the
germinal vesicle, and the area around it a disc of yolk containing smaller
spherules than the surrounding parts. The germinal vesicle possessed the
same structure in both the ripe eggs examined by me; and, in both, it was
situated quite on the external surface of the yolk.
In one of my specimens it was flat above, but convex below; in the other
and, on the whole, the better preserved of the two, it had the somewhat
quadrangular but rather irregular section represented in Pl. 6, fig. 1. It
consisted of a thickish membrane and its primitive contents. The membrane
surrounded the upper part of the contents and exhibited numerous folds and
creases (vide fig. 1). As it extended downwards it became thinner, and
completely disappeared at some little distance from the lower end of the
contents. These, therefore, rested below on the yolk. At its circumference
the membrane of the disc was produced into a kind of fold, forming a rim
which rested on the surface of the yolk.
In neither of my specimens is the cavity in the upper part of the membrane
filled by the contents; and the upper part of the membrane is so folded and
creased that sections through almost any portion of it pass through the
folds. The regularity of the surface of the yolk is not broken by the
germinal vesicle, and the yolk around exhibits not the slightest signs of
displacement. In the germinal vesicle figured the contents are somewhat
irregular in shape; but in my other specimen they form a regular mass
concave above and convex below. In both cases they rest on the yolk, and
the floor of the yolk is exactly moulded to suit the surface of the
contents of the germinal vesicle. The contents have a granular aspect, but
differ in constitution from the surrounding yolk. Each germinal vesicle
measured about one-fiftieth of an inch in diameter.
It does not appear to me possible to suppose that the peculiar appearances
which I have drawn and described are to be looked upon as artificial
products either of the chromic acid, in which the ova were hardened, or of
the instrument with which sections of them were made. It is hardly
conceivable that chromic acid could cause a rupture of the membrane and the
ejection of the contents of the vesicle. At the same time the uniformity of
the appearances in the different sections, the regularity of the whole
outline of the egg, and the absence of any signs of disturbance in the
yolk, render it impossible to believe that the structures described are due
to faults of manipulation during or before the cutting of the sections.
We can only therefore conclude that they represent the real state of the
germinal vesicle at this period. No doubt they alone do not supply a
sufficient basis for any firm conclusions as to the fate of the germinal
vesicle. Still, if they cannot sustain, they unquestionably support certain
views. The natural interpretation of them is that the membrane of the
germinal vesicle is in the act of commencing to atrophy, preparatory to
being extruded from the egg, while the contents of the germinal vesicle are
about to be absorbed.
In favour of the extrusion of the membrane rather than its absorption are
the following features:
(1) The thickness of its upper surface. (2) The extension of its edge over
the yolk. (3) Its position external to the yolk.
In favour of the view that the contents will be left behind and absorbed
when the membrane is pushed out, are the following features of my sections:
(1) The rupture of the membrane of the germinal vesicle on its lower
surface. (2) The position of the contents almost completely below the
membrane of the vesicle and surrounded by yolk.
In connection with this subject, Oellacher's valuable observations upon the
behaviour of the germinal vesicle in Osseous Fishes and in Birds at once
suggest themselves[72]. Oellacher sums up his results upon the behaviour of
the germinal vesicle in Osseous Fishes in the following way (p. 12):
"The germinal vesicle of the Trout's egg, at a period when
the egg is very nearly ripe, lies near the surface of the
germinal disc which is aggregated together in a hollow of
the yolk.... After this a hole appears in the membrane of
the germinal vesicle, which opens into the space between the
egg-membrane and the germinal disc. The hole widens more and
more, and the membrane frees itself little by little from
the contents of the germinal vesicle, which remain behind in
the form of a ball on the floor of the cavity formed in this
way. The cavity becomes flatter and flatter and the contents
are pushed up further and further from the germinal disc.
When the hollow, in which lie the contents of the original
germinal vesicle, completely vanishes, the covering membrane
becomes inverted ... and the membrane is spread out on the
convex surface of the germinal disc as a circular, investing
structure. It is clear that by the removal of the membrane
the contents of the germinal vesicle become lost."
Footnote 72: _Archiv für Micr. Anat._ Vol. VIII. p. 1.
These very definite statements of Oellacher tell strongly against my
interpretation of the appearance presented by the germinal vesicle of the
ripe Skate's egg. Oellacher's account is so precise, and his drawings so
fully bear out his interpretations, that it is very difficult to see where
any error can have crept in.
On the other hand, with the exception of those which Oellacher has made,
there cannot be said to be any satisfactory observations demonstrating the
extrusion of the germinal vesicle from the ovum. Oellacher has observed
this definitely for the Trout, but his observations upon the same point in
the Bird would quite as well bear the interpretation that the membrane
alone became pushed out, as that this occurred to the germinal vesicle,
contents and all.
While, then, there are on the one hand Oellacher's observations on a single
animal, hitherto unconfirmed, there are on the other very definite
observations tending to shew that the germinal vesicle has in many cases an
altogether different fate. Götte[73], not to mention other observers before
him, has in the case of Batrachian's eggs traced out with great precision
the gradual atrophy of the germinal vesicle, and its final absorption into
the matter of the ovum.
Footnote 73: _Entwicklungsgeschichte der Unke._
Götte distinguishes three stages in the degeneration of the germinal
vesicle of Bombinator's egg. In the first stage the germinal vesicle has
begun to travel up towards the surface of the egg. It retains nearly its
primitive condition, but its contents have become more opaque and have
partly withdrawn themselves from the thin membrane. The germinal spots are
still circular, but in some cases have increased in size. The most
important feature of this stage is the smaller size of the germinal vesicle
than that of the cavity of the yolk in which it lies, a condition which
appears to demonstrate the commencing atrophy of the vesicle.
In the next stage the cavity containing the germinal vesicle has vanished
without leaving a trace. The germinal vesicle itself has assumed a
lens-like form, and its borders are irregular and pressed in here and there
by yolk. Of the membrane of the germinal vesicle, and of the germinal
spots, only scanty remnants are to be seen, many of which lie in the
immediately adjoining yolk.
In the last stage no further trace of a distinct germinal vesicle is
present. In its place is a mass of very finely granular matter, which is
without a distinct border and graduates into the surrounding yolk and is to
be looked on as a remnant of the germinal vesicle.
This careful investigation of Götte proves beyond a doubt that in
Batrachians neither the membrane, nor the contents of the germinal vesicle,
are extruded from the egg.
In Mammalia, Van Beneden[74] finds that the germinal vesicle becomes
invisible, though he does not consider that it absolutely ceases to exist.
He has not traced the steps of the process with the same care as Götte, but
it is difficult to believe that an extrusion of the vesicle in the way
described by Oellacher would have escaped his notice.
Footnote 74: _Recherches sur la Composition et la Signification
de l'OEuf._
Passing from Vertebrates to Invertebrates, we find that almost every
careful investigator has observed the disappearance, apparent or otherwise,
of the germinal vesicle, but that very few have watched with care the steps
of the process.
The so-called Richtungskörper has been supposed to be the extruded remnant
of the germinal vesicle. This view has been especially adopted and
supported by Oellacher (_loc. cit._), and Flemming[75].
Footnote 75: "Studien in der Entwicklungsgeschichte der
Najaden," _Sitz. d. k. Akad. Wien_, Bd. LXXI. 1875.
The latter author regards the constant presence of this body, and the
facility with which it can be stained, as proofs of its connection with the
germinal vesicle, which has, however, according to his observations,
disappeared before the appearance of the Richtungskörper.
Kleinenberg[76], to whom we are indebted for the most precise observations
we possess on the disappearance of the germinal vesicle, gives the
following account of it, pp. 41 and 42.
"We left the germinal vesicle as a vesicle with a distinct
doubly contoured membrane, and equally distributed granular
contents, in which the germinal spot had appeared.... The
germinal vesicle reaches 0.06 mm. in diameter, and at the
same time its contents undergo a separation. The greater
part withdraws itself from the membrane and collects as a
dense mass around the germinal spot, while closely adjoining
the membrane there remains only a very thin but unbroken
lining of the plasmoid material. The intermediate space is
filled with a clear fluid, but the layer which lines the
membrane retains its connection with the mass around the
germinal vesicle by means of numerous fine threads which
traverse the space filled with fluid.... At about the time
when the formation of the pseudocells in the egg is
completed the germinal spot undergoes a retrogressive
metamorphosis, it loses its circular outline and it now
appears as if coagulated; then it breaks up into small
fragments, and I am fairly confident that these become
dissolved. The germinal vesicle ... becomes, on the egg
assuming a spherical form, drawn into an eccentric position
towards the pole of the egg directed outwards, where it lies
close to the surface and only covered by a very thin layer
of plasma. In this situation its degeneration now begins,
and ends in its complete disappearance. The granular
contents become more and more fluid; at the same time part
of them pass out through the membrane. This, which so far
was firmly stretched, next collapses to a somewhat egg-like
sac, whose wall is thickened and in places folded.
"The inner mass which up to this time has remained compact
now breaks up into separate highly refractive bodies, of
spherical or angular form and of very different sizes;
between them, here and there, are scattered drops of a fluid
fat.... I am very much inclined to regard the solid bodies
in question as fat or as that peculiar modification of
albuminoid bodies which we recognise as the certain
forerunner of the formation of fat in so many pathologically
altered tissues; and therefore to refer the disappearance of
the germinal vesicle to a fatty degeneration. On one
occasion I believe that I observed an opening in the
membrane at this stage; if this is a normal condition it
would be possible to believe that its solid contents passed
out and were taken up in the surrounding plasma. What
becomes of the membrane I am unable to say; in any case the
germinal vesicle has vanished to the very last trace before
impregnation occurs."
Footnote 76: _Hydra._ Leipzig, 1872.
Kleinenberg clearly finds that the germinal vesicle disappears completely
before the appearance of the Richtungskörper, in which he states a
pseudocell or yolk-sphere is usually found.
The connection between the Richtungskörper and the germinal vesicle is not
a result of strict observation, and there can be no question that the
evidence in the case of invertebrates tends to prove that the germinal
vesicle in no case disappears owing to its extrusion from the egg, but that
if part of it is extruded from the egg as Richtungskörper this occurs when
its constituents can no longer be distinguished from the remainder of the
yolk. This is clearly the case in Hydra, where, as stated above, one of the
pseudocells or yolk-spheres is usually found imbedded in the
Richtungskörper.
My observations on the Skate tend to shew that, in its case, the membrane
of the germinal vesicle is extruded from the egg, though they do not
certainly prove this. That conclusion is however supported by the
observations of Schenk[77]. He found in the impregnated, but not yet
segmented, germinal disc a cavity which, as he suggests, might well have
been occupied by the germinal vesicle. It is not unreasonable to suppose
that the membrane, being composed of formed matter and able only to take a
passive share in vital functions, could, without thereby influencing the
constitution of the ovum, be ejected.
Footnote 77: "Die Eier von Raja quadrimaculata," _Sitz. der k.
Akad. Wien_, Bd. LXVIII.
If we suppose, and this is not contradicted by observation, that the
Richtungskörper is either only the metamorphosed membrane of the germinal
vesicle with parts of the yolk, or part of the yolk alone, and assume that
in Oellacher's observations only the membrane and not the contents were
extruded from the egg, it would be possible to frame a consistent account
of the behaviour of the germinal vesicle throughout the animal kingdom,
which may be stated in the following way.
The germinal vesicle usually before, but sometimes immediately after
impregnation undergoes atrophy and its _contents_ become indistinguishable
from the remainder of the egg. In those cases in which its membrane is very
thick and resistent, _e.g._ Osseous and Elasmobranch Fishes, Birds, etc.,
this may be incapable of complete resorption, and be extruded bodily from
the egg. In the case of most ova, it is completely absorbed, though at a
subsequent period it may be extruded from the egg as the Richtungskörper.
In all cases the contents of the germinal vesicle remain in the ovum.
In some cases the germinal vesicle is stated to persist and to undergo
division during the process of segmentation; but the observations on this
point stand in need of confirmation.
My investigations shew that the germinal vesicle atrophies in the Skate
before impregnation, and in this respect accord with very many recent
observations. Of these the following may be mentioned.
(1) Oellacher (Bird, Osseous Fish). (2) Götte (Bombinator igneus). (3)
Kupffer (Ascidia canina). (4) Strasburger (Phallusia mamillata). (5)
Kleinenberg (Hydra). (6) Metschnikoff (Geryonia, Polyzenia leucostyla,
Epibulia aurantiaca, and other Hydrozoa).
This list is sufficient to shew that the disappearance of the germinal
vesicle before impregnation is very common, and I am unacquainted with any
observations tending to shew that its disappearance is due to impregnation.
In some cases, _e.g._ Asterocanthion[78], the germinal vesicle vanishes
after the spermatozoa have begun to surround the egg; but I do not know
that its disappearance in these cases has been shewn to be due to
impregnation. To do so it would be necessary to prove that in ripe eggs let
loose from the ovary, but not fertilized, the germinal vesicle did not
undergo the same changes as in the case of fertilized eggs; and this, as
far as I know, has not been done. After the disappearance of the germinal
vesicle, and before the first act of division, a fresh nucleus frequently
appears [--vide--Auerbach (Ascaris nigrovenosa), Fol (Geryonia), Kupffer
(Ascidia canina), Strasburger (Phallusia mamillata), Flemming (Anodon),
Götte (Bombinator igneus)], which is generally stated to vanish before the
appearance of the first furrow; but in some cases (Kupffer and Götte, and
as studied with especial care, Strasburger) it is stated to divide. Upon
the second nucleus, or upon its relation to the germinal vesicle, I have no
observations; but it appears to me of great importance to determine whether
this fresh nucleus arises absolutely de novo, or is formed out of the
matter of the germinal vesicle.
Footnote 78: Agassiz, _Embryology of the Star-Fish_.
The germinal vesicle is situated in a bed of finely divided yolk-particles.
These graduate insensibly into the coarser yolk-spherules around them,
though the band of passage between the coarse and the finer yolk-particles
is rather narrow. The mass of fine yolk-granules may be called the germinal
disc. It is not to be looked upon as diverging in any essential particular
from the remainder of the yolk, for the difference between the two is one
of degree only. It contains in fact a larger bulk of active protoplasm, as
compared with yolk-granules, than does the remainder of the ovum. The
existence of this agreement in kind has been already strongly insisted on
in my preliminary paper; and Schultz (_loc. cit._) has arrived at an
entirely similar conclusion, from his own independent observations.
One interesting feature about the germinal disc at this period is its size.
My observations upon it have been made with the eggs of the Skate (Raja)
alone; but I think that it is not probable that its size in the Skate is
greater than in Scyllium or Pristiurus. If its size is the same in all
these genera, then the germinal disc of the unimpregnated ovum is very much
greater than that portion of the ovum which undergoes segmentation, and
which is usually spoken of as the germinal disc in impregnated ova.
I have no further observation on the ripe ovarian ovum; and my next
observations concern an ovum in which two furrows have already appeared.
CHAPTER II.
THE SEGMENTATION.
I have not been fortunate enough to obtain an absolutely complete series of
eggs during segmentation.
In the cases of Pristiurus and Scyllium only have I had any considerable
number of eggs in this condition, though one or two eggs of Raja in which
the process was not completed have come into my hands.
In the youngest impregnated Pristiurus eggs, which I have obtained, the
germinal disc was already divided into four segments.
The external appearance of the blastoderm, which remains nearly constant
during segmentation, has been already well described by Leydig[79].
Footnote 79: _Rochen und Haie._
The yolk has a pale greenish tinge which, on exposure to the air, acquires
a yellower hue. The true germinal disc appears as a circular spot of a
bright orange colour, and is, according to Leydig's measurements, 1-1/2m.
in diameter. Its colour renders it very conspicuous, a feature which is
further increased by its being surrounded by a narrow dark line (Pl. 6,
fig. 2), the indication of a shallow groove. Surrounding this line is a
concentric space which is lighter in colour than the remainder of the yolk,
but whose outer border passes by insensible gradations into the yolk. As
was mentioned in my preliminary paper (_loc. cit._), and as Leydig (_loc.
cit._) had before noticed, the germinal disc is always situated at the pole
of the yolk which is near the rounded end of the Pristiurus egg. It
occupies a corresponding position in the eggs of both species of Scyllium
(stellare and canicula) near the narrower end of the egg to which the
shorter pair of strings is attached. The germinal disc in the youngest egg
examined, exhibited two furrows which crossed each other at right angles in
the centre of the disc, but neither of which reached its edge. These
furrows accordingly divided the disc into four segments, completely
separated from each other at the centre of the disc, but united near its
circumference.
I made sections, though not very satisfactorily, of this germinal disc. The
sections shewed that the disc was composed of a protoplasmic basis, in
which were imbedded innumerable minute spherical yolk-globules so closely
packed as to constitute nearly the whole mass of the germinal disc.
In passing from the coarsest yolk-spheres to the fine spherules of the
germinal disc, three bands of different-sized yolk-particles have to be
traversed. These bands graduate into one another and are without sharp
lines of demarcation. The outer of the three is composed of the
largest-sized yolk-spherules which constitute the greater part of the ovum.
The middle band forms a concentric layer around the germinal disc, and is
composed of yolk-spheres considerably smaller than those outside it. Where
it cuts the surface it forms the zone of lighter colour immediately
surrounding the germinal disc. The innermost band is formed by the germinal
disc itself and is composed of spherules of the smallest size. These
features are shewn in Pl. 6, fig. 6, which is the section of a germinal
disc with twenty-one segments; in it however the outermost band of
spherules is not present.
From this description it is clear, as has already been mentioned in the
description of the ripe unimpregnated ovum, that the germinal disc is not
to be looked upon as a body entirely distinct from the remainder of the
ovum, but merely as a part of the ovum in which the protoplasm is more
concentrated and the yolk-spherules smaller than elsewhere. Sections shew
that the furrows visible on the surface end below, as indeed they do on the
surface, before they reach the external limit of the finely granular matter
of the germinal disc. There are therefore at this stage no distinct
segments: the otherwise intact germinal disc is merely grooved by two
furrows.
I failed to observe any nuclei in the germinal disc just described, but it
by no means follows that they were not present.
In the next youngest of the eggs[80] examined the germinal disc was already
divided into twenty-one segments. When viewed from the surface (Pl. 6,
fig. 3), the segments appeared divided into two distinct groups--an inner
group of eleven smaller segments, and an outer group of segments
surrounding the former. The segments of both the inner and the outer group
were very irregular in shape and varied considerably in size. The amount of
irregularity is far from constant and many germinal discs are more regular
than the one figured.
Footnote 80: The germinal disc figured was from the egg of a
Scyllium stellare and not Pristiurus, but I have also sections
of a Pristiurus egg of the same age, which do not differ
materially from the Scyllium sections.
In this case the situation of the germinal disc and its relations to the
yolk were precisely the same as in the earlier stage.
In sections of this germinal disc (Pl. 6, fig. 6), the groove which
separates it from the yolk is well marked on one side, but hardly visible
at the other extremity of the section.
Passing from the external features of this stage to those which are
displayed by sections, the striking point to be noticed is the persisting
continuity of the segments, marked out on the surface, with the floor of
the germinal disc.
The furrows which are visible on the surface merely form a pattern, but do
not isolate a series of distinct segments. They do not even extend to the
limit of the finely granular matter of the germinal disc.
The section represented, Pl. 6, fig. 6, bears out the statements about the
segments as seen on the surface. There are three smaller segments in the
middle of the section, and two larger at the two ends. These latter are
continuous with the coarser yolk-spheres surrounding the germinal disc and
are not separated from them by a segmentation furrow.
In a slightly older embryo than the one figured I met with a few completely
isolated segments at the surface. These segments were formed by the
apparent bifurcation of furrows as they neared the surface of the germinal
disc. The segments thus produced are triangular in form. They probably owe
their origin to the meeting of two oblique furrows. The last-formed of
these furrows apparently ceases to be prolonged after meeting the
first-formed furrow. I have not in any case observed an example of two
furrows crossing one another at this stage.
The furrows themselves for the most part are by no means simple slits with
parallel sides. They exhibit a beaded structure, shewn imperfectly in
Pl. 6, fig. 6, but better in Pl. 6, fig. 6_a_, which is executed on a
larger scale. They present intervals of dilatations where the protoplasms
of the segments on the two sides of the furrow are widely separated,
alternating with intervals where the protoplasms of the two segments are
almost in contact and are only separated from one another by a very narrow
space.
A closer study of the germinal disc at this period shews that the cavities
which cause the beaded structure of the furrows are not only present along
the lines of the furrows but are also found scattered generally through the
germinal disc, though far more thickly in the neighbourhood of the furrows.
Their appearance is that of vacuoles, and with these they are probably to
be compared. There can be little question that in the living germinal disc
they are filled with fluid. In some cases, they are collected in very large
numbers in the region of a furrow. Such a case as this is shewn in Pl. 6,
fig. 6_b_. In numerous other cases they occur, roughly speaking,
alternately on each side of a furrow. Some furrows, though not many, are
entirely destitute of these structures. The character of their distribution
renders it impossible to overlook the fact that these vacuole-like bodies
have important relations with the formation of the segmentation furrows.
Lining the two sides of the segmentation furrows there is present in
sections a layer which stains deeply with colouring reagents; and the
surface of the blastoderm is stained in the same manner. In neither case is
it permissible to suppose that any membrane-like structure is present. In
many cases a similar very delicate, but deeply-stained line, invests the
vacuolar cavities, but the fluid filling these remains quite unstained.
When distinct segments are formed, each of these is surrounded by a
similarly stained line.
The yolk-spherules are so numerous, and render even the thinnest section so
opaque, that I have failed to make satisfactory observations on the
behaviour of the nucleus. I find nuclei in many of the segments, though it
is very difficult even to see them, and only in very favourable specimens
can their structure be studied. In some cases, two of them lie one on each
side of a furrow; and in one case at the extreme end of a furrow I could
see two peculiar aggregations of yolk-spherules united by a band through
which the furrow, had it been continued, would have passed. The connection
(if any exists) between this appearance and the formation of the fresh
nuclei in the segments, I have been unable to elucidate.
The peculiar appearances attending the formation of fresh nuclei in
connection with cell-division, which have recently been described by so
many observers, have hitherto escaped my observation at this stage of the
segmentation, though I shall describe them in a later stage. A nucleus of
this stage is shewn on Pl. 6, fig. 6_c_. It is lobate in form and is
divided by lines into areas in each of which a deeply-stained granule is
situated.
The succeeding stages of segmentation present from the surface no fresh
features of great interest. The somewhat irregular (Pl. 6, figs. 4 and 5)
circular line, which divides the peripheral larger from the central smaller
segments, remains for a long time conspicuous. It appears to be the
representative of the horizontal furrow which, in the Batrachian ovum,
separates the smaller pigmented spheres from the larger spheres of the
lower pole of the egg.
As the segments become smaller and smaller, the distinction between the
peripheral and the central segments becomes less and less marked; but it
has not disappeared by the time that the segments become too small to be
seen with the simple lens. When the spheres become smaller than in the
germinal disc represented on Pl. 6, fig. 5, the features of segmentation
can be more easily and more satisfactorily studied by means of sections.
To the features presented in sections, both of the latter and of the
earlier blastoderms, I now return. A section of one of the earlier germinal
discs, of about the age of the one represented on Pl. 6, fig. 4, is shewn
in Pl. 6, fig. 7.
It is clear at a glance that we are now dealing with true segments
completely circumscribed on all sides. The peripheral segments are, as a
rule, larger than the more central ones, though in this respect there is
considerable irregularity. The segments are becoming smaller by repeated
division; but, in addition to this mode of increase, there is now going on
outside the germinal disc a segmentation of the yolk, by which fresh
segments are being formed from the yolk and added to those which already
exist in the germinal disc. One or two such segments are seen in the act of
being formed (Pl. 6, fig. 7, _f_); and it is to be noticed that the furrows
which will eventually mark out the segments, do so at first in a partial
manner only, and do not circumscribe the whole circumference of the segment
in the act of being formed. These fresh furrows are thus repetitions on a
small scale of the earliest segmentation furrows.
It deserves to be noticed that the portion of the germinal disc which has
already undergone segmentation, is still surrounded by a broad band of
small-sized yolk-spherules. It appears to me probable that owing to changes
taking place in the spherules of the yolk, which result in the formation of
fresh spherules of a small size, this band undergoes a continuous
renovation.
The uppermost row of segmentation spheres is now commencing to be
distinguished from the remainder as a separate layer which becomes
progressively more distinct as segmentation proceeds.
The largest segments in this section measure about the 1/100th of an inch
in diameter, and the smallest about 1/300th of an inch.
The nuclei at this stage present points of rather a special interest. In
the first place, though visible in many, and certainly present in all the
segments[81], they are not confined to these: they are also to be seen, in
small numbers, in the band of fine spherules which surrounds the already
segmented part of the germinal disc. Those found outside the germinal disc
are not confined to the spots where fresh segments are appearing, but are
also to be seen in places where there are no traces of fresh segments.
Footnote 81: In the figure of this stage, I have inserted
nuclei in all the segments. In the section from which the
figure was taken, nuclei were not to be seen in many of the
segments, but I have not a question that they were present in
all of them. The difficulty of seeing them is, in part, due to
the yolk-spherules and in part to the thinness of the section
as compared with the diameter of a segmentation sphere.
This fact, especially when taken in connection with the formation of fresh
segments outside the germinal disc and with other facts which I shall
mention hereafter, is of great morphological interest as bearing upon the
nature and homologies of the food-yolk. It also throws light upon the
behaviour and mode of increase of the nuclei. All the nuclei, both those of
the segments and those of the yolk, have the peculiar structure I described
in the last stage.
In specimens of this stage I have been able to observe certain points which
have an important bearing upon the behaviour of the nucleus during
cell-division.
Three figures, illustrating the behaviour of the nucleus, as I have seen it
in sections of blastoderms hardened in chromic acid, are shewn in Pl. 6,
figs. 7_a_, 7_b_ and 7_c_.
In the place of the nucleus is to be seen a sharply defined figure
(Fig. 7_a_) stained in the same way as the nucleus or more deeply. It has
the shape of two cones placed base to base. From the apex of each cone
there diverge towards the base a series of excessively fine striæ. At the
junction between the two cones is an irregular linear series of small
deeply stained granules which form an apparent break between the two. The
line of this break is continued very indistinctly beyond the edge of the
figure on each side.
From the apex of each cone there diverge outwards into the protoplasm of
the cell a series of indistinct markings. They are rendered obscure by the
presence of yolk-spherules, which completely surround the body just
described, but which are not arranged with any reference to these markings.
These latter striæ, diverging from the apex of the cone, are more
distinctly seen when the apex points to the observer (Fig. 7_b_), than when
a side of the cone is in view.
The striæ diverging outwards from the apices of the cones must be carefully
distinguished from the striæ of the cones themselves. The cones are bodies
quite as distinctly differentiated from the protoplasm of the cell as
nuclei, while the striæ which diverge from their apices are merely
structures in the general protoplasm of the cell.
In some cells, which contain these bodies, no trace of a commencing line of
division is visible. In other cases (Fig. 7_c_), such a line of division
does appear and passes through the junction of the two cones. In one case
of this kind I fancied I could see (and have represented) a coloured
circular body in each cone. I do not feel any confidence that these two
bodies are constantly present; and even where visible they are very
indistinct.
Instead of an ordinary nucleus a very indistinctly marked vesicular body
sometimes appears in a segment; but whether it is to be looked on as a
nucleus not satisfactorily stained, or as a nucleus in the act of being
formed, I cannot decide.
With reference to the situation of the cone-like bodies I have described I
have made an observation which appears to me to be of some interest. I find
that bodies of this kind are found in the yolk _completely outside_ the
germinal disc. I have made this observation, in at least two cases which
admitted of no doubt (vide Fig. 7, _nx´_).
We have therefore the remarkable fact, that whatever connection these
bodies may have with cell-division, they can occur in cases where this is
altogether out of the question and where an increase in the number of
nuclei can be their only product.
These are the main facts which I have been able to determine with reference
to the nuclei of this stage; but it will conduce to clearness if I now
finish what I have to say upon this subject.
At a still later stage of segmentation the same peculiar bodies are to be
seen as during the stage just described, but they are rarer; and, in
addition to them, other bodies are to be seen of a character intermediate
between ordinary nuclei and the former bodies.
Three such are represented in Pl. 6, figs. 8_a_, 8_b_, 8_c_. In all of
these there can be traced out the two cones, which are however very
irregular. The striation of the cones is still present, but is not nearly
so clear as it was in the earlier stage.
In addition to this, there are numerous deeply stained granules scattered
about the two figures which resemble exactly the granules of typical
nuclei.
All these bodies occupy the place of an ordinary nucleus, they stain like
an ordinary nucleus and are as sharply defined as an ordinary nucleus.
There is present around some of these, especially those situated in the
yolk, the network of lines of the yolk described by me in a preliminary
paper[82], and I feel satisfied that there is in some cases an actual
connection between the network and the nuclei. This network I shall
describe more fully hereafter.
Footnote 82: _Loc. cit._
Further points about these figures and the nuclei of this stage I should
like to have been able to observe more completely than I have done, but
they are so small that with the highest powers I possess (Zeiss, Immersion
No. 2 = 1/15 in.) their complete and satisfactory investigation is not
possible.
Most of the true nuclei of the cells of the germinal disc are regularly
rounded; those however of the yolk are frequently irregular in shape and
often provided with knob-like processes. The gradations are so complete
between typical nuclei and bodies like that shewn (Pl. 6, fig. 8_c_) that
it is impossible to refuse the name of nucleus to the latter.
In many cases _two nuclei_ are present in one cell.
In later stages knob-like nuclei of various sizes are scattered in very
great numbers in the yolk around the blastoderm (vide Pl. 7). In some cases
it appears to me that several of these are in close juxtaposition, as if
they had been produced by the division of one primitive nucleus. I do not
feel absolutely confident that this is the case, owing to the fact that in
the investigation of a knobbed body there is great difficulty in
ascertaining that the knobs, which appear separate in one plane, are not in
reality united in another.
I have, in spite of careful search, hitherto failed to find amongst these
later nuclei cone-like figures, similar to those I found in the yolk during
segmentation. This is the more remarkable since in the early stages of
segmentation, when very few nuclei are present in the yolk, the cone-like
figures are not uncommon; whereas, in the latter stages of development when
the nuclei of the yolk are very common and obviously increasing rapidly,
such figures are not to be met with.
In no case have I been able to see a distinct membrane round any of the
nuclei.
I have hitherto attempted to describe the appearances bearing on the
behaviour of the nuclei in as objective a manner as possible.
My observations are not as complete as could be desired; but, taken in
conjunction with those of other investigators, they appear to me to point
towards certain definite conclusions with reference to the behaviour of the
nucleus in cell-division.
The most important of these conclusions may be stated as follows. In the
act of cell-division the nuclei of the resulting cells are formed from the
nucleus of the primitive cell.
This may occur:--
(1) By the complete solution of the old nucleus within the protoplasm of
the mother cell and the subsequent reaggregation of its matter to form the
nuclei of the freshly formed daughter cells,
(2) By the simple division of the nucleus,
(3) Or by a process intermediate between these two where part of the old
nucleus passes into the general protoplasm and part remains always
distinguishable and divides; the fresh nucleus being in this case formed
from the divided parts as well as from the dissolved parts of the old
nucleus.
Included in this third process it is permissible to suppose that we may
have a series of all possible gradations between the extreme processes 1
and 2. If it be admitted, and the evidence we have is certainly in favour
of it, that in some cases, both in animal and vegetable cells, the nucleus
itself divides during cell division, and in others the nucleus completely
vanishes during the cell-division, it is more reasonable to suspect the
existence of some connection between the two processes, than to suppose
that they are entirely different in kind. Such a connection is given by the
hypothesis I have just proposed.
The evidence for this view, derived both from my own observations and those
of other investigators, may be put as follows.
The absolute division of the nucleus has been stated to occur in animal
cells, but the number of instances where the evidence is quite conclusive
are not very numerous. Recently F. E. Schultze[83] appears to have observed
it in the case of an Amoeba in an altogether satisfactory manner. The
instance is quoted by Flemming[84]. Schultze saw the nucleus assume a
dumb-bell shape, divide, and the two halves collect themselves together.
The whole process occupied a minute and a half and was shortly followed by
the division of the Amoeba, which occupied eight minutes. Amongst vegetable
cells the division of the nucleus seems to be still rarer than with animal
cells. Sachs[85] admits the division of the nucleus in the case of the
parenchyma cells of certain Dicotyledons (Sambucus, Helianthus, Lysimachia,
Polygonum, Silene) on the authority of Hanstein.
Footnote 83: _Archiv f. Micr. Anat._ XI. p. 592.
Footnote 84: "Entwicklungsgeschicte der Najaden," LXXI. Bd.
_der Sitz. der k. Acad. Wien_, 1875.
Footnote 85: _Text-Book of Botany_, English trans. p. 19.
The division of the nucleus during cell-division, though seemingly not very
common, must therefore be considered as a thoroughly well authenticated
occurrence.
The frequent disappearance of the nucleus during cell-division is now so
thoroughly recognised, both for animal and vegetable cells, as to require
no further mention.
In many cases the partial or complete disappearance of the nucleus is
accompanied by the formation of two peculiar star-like figures. Appearances
of the kind have been described by Fol[86], Flemming[87], Auerbach[88] and
possibly also Oellacher[89] as well as other observers.
Footnote 86: "Entw. d. Geryonideneies." _Jenaische
Zeitschrift_, Bd. VII.
Footnote 87: _Loc. cit._
Footnote 88: _Organologische Studien_, Zweites Heft.
Footnote 89: "Beiträge z. Entwicklungsgeschichte der
Knochenfischen." _Zeit. für Wiss. Zoologie_. Bd. XXII. 1872.
These figures[90] are possibly due to the streaming out of the protoplasm
of the nucleus into that of the cell[91]. The appearance of striation may
on this hypothesis be explained as due to the presence of granules in the
protoplasm. When the streaming out of the protoplasm of a nucleus into that
of a cell takes place, any large granule which cannot be moved by the
stream will leave behind it a slack area where there is no movement of the
fluid. Any granules which are carried into this area will remain there, and
by the continuation of a process of this kind a row of granules may be
formed, and a series of such rows would produce an appearance of striation.
In many cases, _e.g._ Anodon, vide Flemming[92], even the larger
yolk-spherules are arranged in this fashion.
Footnote 90: The memoirs of Auerbach and Strasburger
(_Zellbildung u. Zelltheilung_) have unfortunately come into my
hands too late for me to take advantage of them. Especially in
the magnificent monograph of Strasburger I find drawings
precisely resembling those from my specimens already in the
hands of the engraver. Strasburger comes to the conclusion from
his investigations that the modified nucleus always divides and
never vanishes as is usually stated. If his views on this point
are correct part of the hypothesis I have suggested above is
rendered unnecessary. The striæ of the protoplasm, which in
accordance with Auerbach's view I have considered as being due
to a streaming out of the matter of the nucleus, he regards as
resulting from a polarity of the particles in the cell and the
attraction of the nucleus. My own investigations though, as far
as they go, quite in accordance with those of Strasburger, do
not supply any grounds for deciding on the meaning of these
striæ; and in some respects they support Strasburger's views
against those of other observers, since they demonstrate that
in Elasmobranchii the modified nucleus does actually divide.
Footnote 91: This is the view which has been taken by Auerbach
(_Organologische Studien_).
Footnote 92: _Loc. cit._
On the supposition that the striation of these figures is due to the
outflow from the nucleus, the appearances presented in Elasmobranchii admit
of the following explanation.
The central body consisting of two cones (figs. 7_a_, 7_c_) is almost
without question the remnant of the primitive nucleus. This is shewn by its
occupying the same position as the primitive nucleus, staining in the same
way, and by there being a series of insensible gradations between it and a
typical nucleus. The contents must be supposed to be streaming out from the
two apices of the cones, as appears from the striæ in the body converging
on each side towards the apex, and then diverging again from it. In my
specimens the yolk-spherules are not arranged with any reference to the
radiating striation.
It is very likely that in the cases of the disappearance of the nucleus,
its protoplasm streams out in two directions, towards the two parts of the
cell which will eventually become separated from each other; and probably,
after the division, the matter of the old nucleus is again collected to
form two fresh nuclei.
In some cases of cell-division a remnant of the old nucleus is stated to be
visible after the fresh nuclei have appeared. These cases, of which I have
not seen full accounts, are perhaps analogous to what occasionally happens
with the germinal vesicle of an ovum. The whole of the contents of the
germinal vesicle become at its disappearance mingled with the protoplasm of
the ovum, but the resistant membrane remains and is eventually ejected from
the egg, vide p. 215 _et seq_. If the remnant of the old nucleus in the
cases described is nothing more than its membrane, no difficulty is offered
to the view that the constituents of the old nucleus may help to form the
new ones.
In many cases the total bulk of the new nuclei is greater than that of the
old one; in such instances part of the protoplasm of the cell necessarily
has a share in forming the new nuclei.
Although, in instances where the nucleus vanishes, an absolute
demonstration of the formation of the fresh nuclei from the matter of the
old one is not possible; yet, if cases of the division of the old nucleus
to form the new ones be admitted to exist, the derivation in the first
process of the fresh nuclei from the old ones must be postulated in order
to maintain a continuity between the two processes of formation; and, as I
have attempted to shew, all the circumstantial evidence is in favour of it.
Admitting the existence of the two extreme processes of nuclear formation,
I wish to shew that my results in Elasmobranchii tend to demonstrate the
existence of intermediate steps between them. The first figures I described
of two opposed cones, appear to me almost certainly to represent nuclei in
the act of dissolution; but though a portion of the nucleus may stream out
into the yolk, I think it impossible that the whole of it does[93].
Footnote 93: After Strasburger's observation it must be
considered very doubtful whether the streaming out of the
contents of the nucleus, in the manner implied in the text,
really takes place.
I described these bodies in two states. An earlier one, in which the two
cones were separated by an irregular row of deeply stained granules; and a
later one in which a furrow had already appeared dividing the cones as well
as the cell. In neither of these conditions could I see any signs of the
body vanishing completely. It was as clearly defined and as deeply stained
as an ordinary nucleus, and in its later condition the signs of the
streaming out of material from its pointed extremities were less marked
than in the earlier stage.
All these facts, to my mind, point to the view that these cone-like bodies
do not disappear, but form the basis for the new nuclei. Possibly the body
visible in each cone in the later stage, was the commencement of this new
nucleus. Götte[94] has figured structures somewhat similar to these bodies,
but I hardly understand either his figure or his account sufficiently
clearly to be able to pronounce upon the identity of the two. In case they
are identical, Götte gives a very different explanation of them from my
own[95].
Footnote 94: _Entwicklungsgeschite der Unke_, Pl. 1, fig. 18.
Footnote 95: As I before mentioned, Strasburger (_Zellbildung
u. Zelltheilung_) has represented bodies precisely similar to
those I have described, which appear during the segmentation in
the egg of _Phallusia mammillata_ as well as similar figures
observed by Butschli in eggs of _Cucullanus elegans_ and
_Blatta Germanica_. The figures in this monograph are the only
ones I have seen, which are identical with my own.
A second of my results, which points to a series of intermediate steps
between division and solution of the nucleus, is the distribution in time
of the peculiar cone-like bodies. These are present in fair abundance at an
early period of segmentation, when there are but few nuclei either in the
blastoderm or the yolk. But at later periods, when there are both more
nuclei, especially in the yolk, and they are also increasing in numbers
more rapidly than before, no bodies of this kind are to be seen. This fact
becomes the more striking from the lobate appearance of the later nuclei of
the yolk, an appearance which exactly suits the hypothesis of the rapid
budding off of fresh nuclei.
The observations of R. Hertwig[96] on the gemmation of _Podophrya
gemmipara_, support my interpretation of the knobbed condition of the
nuclei. Hertwig finds (p. 47) that
The horse-shoe shaped nucleus grows out into numerous
anastomosing projections. Over the free ends of the
projections little knobs appear on the surface of the body,
into which the lengthening ends of the processes of the
nucleus grow up. Here they bend themselves into a horse-shoe
form. The newly-formed nucleus then separates from the
original nucleus, and afterwards the bud containing it from
the body.
Footnote 96: _Morphologisches Jahrbuch_, Bd. 1. pp. 46, 47.
From the peculiar arrangement of the net-work of lines of the yolk around
these knobbed nuclei, it is reasonable to conclude that interchange of
material between the protoplasm of the yolk and the nuclei is still taking
place, even during the later periods.
These facts about the distribution in time of the cone-like bodies afford a
strong presumptive evidence of a change in the manner of nuclear increase.
The last argument I propose urging on this head is derived from the bodies
(Pl. 6, fig. 8_a_, _b_, _c_) which I have described as intermediate between
the true cone-like bodies and typical nuclei. They appear to afford
evidence of less and less of the matter of the nucleus streaming out into
the yolk and of a large proportion of it becoming divided.
The conclusion to be derived from all these facts is that for
Elasmobranchii in the earlier stages of segmentation, and during the
formation of fresh segments, a partial solution of the old nucleus takes
place, but all its constituents serve for the reconstruction of the fresh
nuclei.
In later periods of development a still smaller part of the nucleus becomes
dissolved, and the rest divides; but the two fresh nuclei are still derived
from the two sources. After the close of segmentation the fresh nuclei are
formed by a simple division of the older ones.
The appearance of the cone-like bodies in the yolk outside the germinal
disc is a point of some interest. It demonstrates in a conclusive manner
that whatever influence (if any) the nucleus may have in ordinary cases of
cell division, yet it may undergo changes of a precisely similar character
to those which it experiences during cell division, without exerting any
influence on the surrounding protoplasm[97]. If the lobate nuclei are also
nuclei undergoing division, we have in the egg of an Elasmobranch examples
of all the known forms of nuclear increase unaccompanied by cell division.
Footnote 97: Strasburger's (_loc. cit._) arguments about the
influence of the nucleus in cell division are not to my mind
conclusive; though not without importance. It is difficult to
reconcile his views with the facts of cell division observable
during the Elasmobranch segmentation; but even if their truth
be admitted they do not bring us much nearer to a satisfactory
understanding of cell division, unless accompanied (and at
present they are not so) by a rational explanation of the
forces which produce the division of the nucleus.
The next stage in the segmentation does not present so many features of
interest as the last one. The segments are now so small, as to be barely
visible from the surface with a simple lens. A section of an embryo of this
stage is represented in Pl. 6, fig. 8. The section, which is drawn on the
same scale as the section belonging to the last stage, serves to shew the
relative size of the segments in the two cases.
The epiblast is now more distinct than it was. The segments composing it
are markedly smaller than the remainder of the cells of the germinal disc,
but possess nuclei of an absolutely larger size than do the other cells.
They are irregular in shape, with a slight tendency to be columnar. An
average segment of this layer measures about 1/700 inch.
The cells of the lower layer are more polygonal than those of the epiblast,
and are decidedly larger. An average specimen of the larger cells of the
lower layer measures about 1/400 in. in diameter, and is therefore
considerably smaller than one of the smallest cells of the last stage. The
formation of fresh segments from the yolk still continues with fair
rapidity, but nearly comes to an end shortly after this.
Of the nuclei of the lower layer cells, there is not much to add to what
has already been said. Not infrequently two nuclei may be observed in a
single cell.
The nuclei in the yolk which surrounds the germinal disc are more numerous
than in the earlier periods, and are now to be met with in fair numbers in
every section (fig. 8, _n´_).
These are the main features which characterise the present stage, they are
in all essential points similar to those of the last stage, and the two
germinal discs hardly differ except in the size of the segments of which
they are composed.
In the last stage which I consider as belonging to the segmentation, the
cells of the whole blastoderm have become smaller (Pl. 6, fig. 9).
The epiblast (_ep_) now consists of a very marked layer of columnar cells.
It is, as far as I have been able to observe, never more than one cell
deep. The cells of the lower layer are of an approximately uniform size,
though a few of those at the circumference of the blastoderm considerably
exceed the remainder in the bulk.
There are two fresh features of importance in germinal discs of this age.
Instead of being but indistinctly separated from the surrounding yolk, the
blastoderm has now very clearly defined limits.
This is an especially marked feature of preparations made with osmic acid.
In these there may frequently be seen a deeply stained doubly contoured
line, which forms the limit of the yolk, where it surrounds the germinal
disc. Lines of this kind are often to be seen on the surface of the yolk,
or even of the blastoderm, but are probably to be regarded as products of
reagents, rather than as organised structures. The outline of the germinal
disc is well rounded, though it is occasionally broken, from the presence
of a larger cell in the act of being formed from the yolk.
It is not probable that any great importance is to be attached to the
comparative distinctness of the outline of the germinal disc at this stage,
which is in a great measure due to a cessation in the formation of fresh
cells in the surrounding yolk, and in part to the small and comparatively
uniform size of the cells of the germinal disc.
The formation of fresh cells from the yolk nearly comes to an end during
this period, but it still continues on a small scale.
The number of the nuclei around the germinal disc has increased.
Another feature of interest which first becomes apparent during this stage
is the asymmetry of the germinal disc. If a section were made through the
germinal disc, as it lay _in situ_ in the egg capsule, parallel or nearly
so to the long axis of the capsule, one end of the section would be found
to be much thicker than the other. There would in fact be a far larger
collection of cells at one extremity of the germinal disc than at the
other. The end at which this collection of cells is formed points towards
the end of the egg capsule opposite to that near which the yolk is
situated. This collection of cells is the first trace of the embryo; and
with its appearance the segmentation may be supposed to terminate.
The section I have represented, though not quite parallel to the long axis
of the egg, is sufficiently nearly so to shew the greater mass of cells at
the embryonic end of the germinal disc.
This very early appearance of a distinction in the germinal disc between
the extremity at which the embryo appears and the non-embryonic part of the
disc, besides its inherent interest, has a further importance from the fact
that in Osseous Fishes a similar occurrence takes place. Oellacher[98] and
Götte[99] both agree as to the very early period at which a thickening of
one extremity of the blastoderm in Osseous Fishes is formed, which serves
to indicate the position at which the embryo will appear. There are many
details of development in which Osseous Fish and Elasmobranchii agree,
which, although if taken individually are without any great importance, yet
serve to shew how long even insignificant features in development may be
retained.
Footnote 98: _Zeitschrift für Wiss. Zoologie_, Bd. XXIII.
1873.
Footnote 99: _Archiv für Micr. Anat._ Bd. IX. 1873.
* * * * *
The segmentation of the Elasmobranch egg presents in most of its features
great regularity, and exhibits in its mode of occurrence the closest
resemblance to that in other meroblastic vertebrate ova.
There is, nevertheless, one point with reference to which a slight
irregularity may be observed. In almost all eggs segmentation commences by,
what for convenience may be called, a vertical furrow which is followed by
a second vertical furrow at right angles to the first. The third furrow
however is a horizontal one, and cuts the other two at right angles. This
method of segmentation must be looked on as the normal one, in almost all
the important groups of the animal kingdom, both for the so-called
holoblastic and meroblastic eggs, and the gradations intermediate between
the two. The Frog amongst vertebrates exhibits a most typical instance of
this form of segmentation.
In Elasmobranchii the first two furrows are formed in a perfectly normal
manner, but though I have not observed the actual formation of the next
furrow, yet from the later stages, which I have observed, I conclude that
it is parallel to one of the first formed furrows; and it is fairly certain
that, not till a considerably later period, is a furrow homologous with the
horizontal furrow of the Batrachian egg formed. This furrow appears to be
represented in the Elasmobranch segmentation by the irregular
circumscription of a body of central smaller spheres from a ring of
peripheral larger ones (vide Pl. 6, figs. 3, 4 and 5).
In the Bird the representative of the horizontal furrow appears relatively
much earlier. It is formed when there are eight segments marked out on the
surface of the germinal disc[100]. From Oellacher's[101] account of the
segmentation in the fowl[102] it seems certain, as might be anticipated,
that this furrow is nearly parallel to the surface of the disc, so that it
cuts the earlier formed vertical furrows and causes the segments of the
germinal disc to be completely circumscribed below as well as at the
surface. In the Elasmobranch egg this is not the case; so that, even after
the smaller central segments have become separated from the outer ring of
larger ones, none of the segments of the disc are completely circumscribed,
and only appear to be so in surface views (vide Pl. 6, fig. 6).
Segmentation in the Elasmobranch egg differs in the following particulars
from that in the Bird's egg:
(1) The equivalent of the horizontal furrow of the Batrachian egg appears
much later than in the Bird.
(2) When it has appeared it travels inwards much more slowly.
Footnote 100: Vide _Elements of Embryology_, p. 23.
Footnote 101: _Stricker's Studien_, 1869, Pt. I, Pl. II. fig. 4.
Footnote 102: Unfortunately Professor Oellacher gives no
account of the surface appearance of the germinal discs of
which he describes the sections. It is therefore uncertain to
what period his sections belong.
As a result of these differences, the segments of the germinal disc of the
Birds' eggs are much earlier circumscribed on all sides than those of the
Elasmobranch egg.
As might be expected, the segmentation of the Elasmobranch egg resembles in
many points that of Osseous Fishes (vide Oellacher[103] and Klein[104]). It
may be noticed, that with Osseous as with Elasmobranch Fishes, the furrow
corresponding with the horizontal furrow of the Amphibian's egg does not
appear at as early a period as is normal. The third furrow of an Osseous
Fish egg is parallel to one of the first formed pair.
Footnote 103: _Zeitschrift für Wiss. Zool._ Bd. XXII. 1872.
Footnote 104: _Monthly Microscopical Journal_, March, 1872.
In Oellacher's[105] figures, Pl. 23, figs. 19-21, peculiar beadings of the
sides of the earlier formed furrows are distinctly shewn. No mention of
these is made in the text, but they are unquestionably similar to those I
have described in the Elasmobranch furrows. In the case of Elasmobranchii I
pointed out that not only were the sides of the furrow beaded, but that
there appeared in the protoplasm, close to the furrows, peculiar
vacuole-like cavities, precisely similar to the cavities which were the
cause of the beadings of the furrows.
Footnote 105: _Loc. cit._
The presence of these seems to shew that the molecular cohesion of the
protoplasm becomes, as compared with other parts, much diminished in the
region where a furrow is about to appear, so that before the protoplasm
finally gives way along a particular line to form a furrow, its cohesion is
broken at numerous points in this region, and thus a series of vacuole-like
spaces is formed.
If this is the true explanation of the formation of these spaces, their
presence gives considerable support to the views of Dr Kleinenberg upon the
causes of segmentation, so clearly and precisely stated in his monograph
upon Hydra; and is opposed to any view which regards the forces which come
into play during segmentation as resident in the nucleus.
I have not observed the peculiar threads of protoplasm which Oellacher[106]
describes as crossing the commencing segmentation furrows. I have also
failed to discover any signs of a concentration of the yolk-spherules,
round one or two centres, in the segmentation spheres, similar to that
observed by Oellacher in the segmenting eggs of Osseous Fish. The
appearances observed by him are probably connected with the behaviour of
the nucleus during segmentation, and are related to the curious bodies I
have already described.
Footnote 106: _Loc. cit._
With reference to the nuclei which Oellacher[107] has described as
occurring in the eggs of Osseous Fish during segmentation, there can, I
think, be little doubt that they are identical with the peculiar nuclei in
the Elasmobranch eggs.
Footnote 107: _Loc. cit._
He[108] says:
In an unsegmented germ there occurred at a certain point in
the section ... a small aggregation of round bodies. I do
not feel satisfied whether these aggregations represent one
or more nuclei.
Fig. 29 shews such aggregation; by focusing at its optical
section eleven unequally large rounded bodies measuring from
0.004 - 0.009 mm. may be distinguished. They lay as if in a
multilocular gap in the germ mass, which however they did
not quite fill. In each of these bodies there appeared
another but far smaller body. These aggregations were
distinguished from the germ by an especially beautiful
intense violet gold chloride colouration of their elements.
The smaller elements contained in the larger were still more
intensely coloured than the larger.
Footnote 108: _Loc. cit._ pp. 410, 411, &c.
He further states that these aggregations equal the segments in number, and
that the small bodies within the elements are not always to be seen with
the same distinctness.
Oellacher's description as well as his figures of these bodies leaves no
doubt in my mind that they are exactly similar bodies to those which I have
already spoken of as nuclei, and the characteristic features of which I
have shortly mentioned, and shall describe more fully at a later stage. A
moderately full description of them is to be found in my preliminary
paper[109].
Footnote 109: _Loc. cit._ p. 415. [This Edition, p. 64.]
Their division into a series of separate areas each with a deeply-stained
body, as well as the staining of the whole of them, exactly corresponds to
what I have found. That each is a single nucleus is quite certain, though
their knobbed form might occasionally lead to the view of their being
divided. This knobbed condition, observed by Oellacher as well as myself,
certainly supports the view, that they are in the act of budding off fresh
nuclei. Oellacher conceives, that the areas into which these nuclei are
divided represent a series of separate bodies--this according to my
observations is not the case. Nuclei of the same form have already been
described in Nephelis, and are probably not very rare. They pass by
insensible gradations into ordinary nuclei with numerous granules.
One marked feature of the segmentation of the Elasmobranch egg is the
continuous advance of the process of segmentation into the yolk and the
assimilation of this into the germ by the direct formation of fresh
segments out of it. Into the significance of this feature I intend to enter
fully hereafter; but it is interesting to notice that Oellacher's
descriptions point to a similar feature in the segmentation of Osseous
Fish. This however consists chiefly in the formation of fresh segments from
the lower parts of the germinal disc which in Osseous Fish is more
distinctly marked off from the food-yolk than in Elasmobranchii.
I conclude my description of the segmentation by a short account of what
other investigators have written about its features in these fishes. One of
the earliest descriptions of this process was given by Leydig[110]. To his
description of the germinal disc, I have already done full justice.
Footnote 110: _Rochen u. Haie._ It is here mentioned that
Coste observed the segmentation in these fishes.
In the first stage of segmentation which he observed 20-30 segments were
already visible on the surface. In each of these he recognized a nucleus
but no nucleolus.
He rightly states that the segments have no membrane, and describes the
yolk-spherules which fill them.
The next investigator is Gerbe[111]. I have unfortunately been unable to
refer to this elaborate paper, but I gather from an abstract that M. Gerbe
has given a careful description of the external features of segmentation.
Footnote 111: "Recherches sur la segmentation des products
adventifs de l'oeuf des Plagiostomes et particulièrement des
Raies." Robin, _Journal de l'Anatomie et de la Physiologie_, p.
609, 1872.
Schenk[112] has also made important investigations on the subject. He
considers that the ovum is invested with a very delicate membrane. This
membrane I have failed to find a trace of, and agree with Leydig[113] in
denying its existence. Schenk further found that after impregnation, but
before segmentation, the germinal disc divided itself into two layers, an
upper and a lower. Between the two a cavity made its appearance which
Schenk looks upon as the segmentation cavity. Segmentation commences in the
upper of the two layers, but Schenk does not give a precise account of the
fate of the lower. I have had no opportunity of investigating the
impregnated ovum before the commencement of segmentation, but my
observations upon the early stages of this process render it clear that no
division of the germinal disc exists subsequently to the commencement of
segmentation, and that the cavity discovered by Schenk can have no
connection whatever with the segmentation cavity. I am indeed inclined to
look upon this cavity as an artificial product. I have myself met with
somewhat similar appearances, after the completion of segmentation, which
were caused by the non-penetration of my hardening reagent beyond a certain
point.
Footnote 112: "Die Eier von Raja quadrimaculata innerhalb der
Eileiter." _Sitz. der k. Akad. Wien._ Vol. LXXIII. 1873.
Footnote 113: _Loc. cit._ My denial of the existence of this
membrane naturally applies only to the egg after impregnation,
and to the genera Scyllium and Pristiurus.
Without attempting absolutely to explain the appearances described by
Professor Schenk, I think that his observations ought to be repeated,
either by himself or some other competent observer.
Several further facts are recorded by Professor Schenk in his interesting
paper. He states that immediately after impregnation, the germinal disc
presents towards the yolk a strongly convex surface, and that at a later
period, but still before the commencement of segmentation, this becomes
flattened out. He has further detected amoeboid movements in the disc at
the same period. As to the changes of the germinal disc during
segmentation, his paper contains no facts of importance.
Next in point of time to the paper of Schenk, is my own preliminary account
of the development of the Elasmobranch Fishes[114]. In this a large number
of the facts here described in full are briefly alluded to.
Footnote 114: _Loc. cit._
The last author who has investigated the segmentation in Elasmobranchii, is
Dr Alexander Schultz[115]. He merely states that he has observed the
segmentation, and confirms Professor Schenk's statements about the amoeboid
movements of the germinal disc.
Footnote 115: "Die Embryonal Anlage der Selachier. Vorläufige
Mittheilung," _Centralblatt f. Med. Wiss._ No. 33, 1875.
EXPLANATION OF PLATE 6.
Fig. 1. Section through the germinal disc of a ripe ovarian ovum of the
Skate. _gv._ germinal vesicle.
Fig. 2. Surface-view of a germinal disc with two furrows.
Figs. 3, 4, 5. Surface-views of three germinal discs in different stages of
segmentation.
Fig. 6. Section through the germinal disc represented in fig 3. _n._
nucleus; _x._ edge of germinal disc. The engraver has not accurately copied
my original drawings in respect to the structure of the segmentation
furrows.
Figs. 6_a_ and 6_b_. Two furrows of the same germinal disc more highly
magnified.
Fig. 6_c_. A nucleus from the same germinal disc highly magnified.
Fig. 7. Section through a germinal disc of the same age as that represented
in fig. 4. _n._ nucleus; _nx._ modified nucleus; _nx´._ modified nucleus of
the yolk; _f._ furrow appearing in the yolk around the germinal disc.
Figs. 7_a_, 7_b_, 7_c_. Three segments with modified nuclei from the same
germinal disc.
Fig. 8. Section through a somewhat older germinal disc. _ep._ epiblast;
_n´._ nuclei of yolk.
Figs. 8_a_, 8_b_, 8_c_. Modified nuclei from the yolk from the same
germinal disc.
Fig. 8_d_. Segment in the act of division from the same germinal disc.
Fig. 9. Section through a germinal disc in which the segmentation is
completed. It shews the larger collection of cells at the embryonic end of
the germinal disc than at the non-embryonic. _ep._ epiblast.
CHAPTER III.
FORMATION OF THE LAYERS.
In the last chapter the blastoderm was left as a solid lens-shaped mass of
cells, thicker at one end than at the other, its uppermost row of cells
forming a distinct layer. There very soon appears in it a cavity, the
well-known segmentation cavity, or cavity of von Baer, which arises as a
small space in the midst of the blastoderm, near its non-embryonic end
(Pl. 7, fig. 1.).
This condition of the segmentation cavity, though already[116] described,
has nevertheless been met with in one case only. The circumstance of my
having so rarely met with this condition is the more striking because I
have cut sections of a considerable number of blastoderms in the hope of
encountering specimens similar to the one figured, and it can only be
explained on one of the two following hypotheses. Either the stage is very
transitory, and has therefore escaped my notice except in the one instance;
or else the cavity present in this instance is not the true segmentation
cavity, but merely some abnormal structure. That this latter explanation is
a possible one, appears from the fact that such cavities do at times occur
in other parts of the blastoderm. Dr Schultz[117] does not mention having
found any stage of this kind.
Footnote 116: _Qy. Journal of Microsc. Science_, Oct. 1874.
[This Edition, No. V.]
Footnote 117: _Centr. f. Med. Wiss._ No. 38, 1875.
The position of the cavity in question, and its general appearance, incline
me to the view that it is the segmentation cavity[118]. If this is the true
view of its nature the fact should be noted that at first its floor is
formed by the lower layer cells and not by the yolk, and that its roof is
constituted by both the lower layer cells and the epiblast cells. The
relations of the floor undergo considerable modifications in the course of
development.
Footnote 118: Professor Bambeke ("Poissons Osseux," _Mém.
Acad. Belgique_ 1875) describes a cavity in the blastoderm of
Leuciscus rutilus, which he regards as the true segmentation
cavity, but not as identical with the segmentation cavity of
Osseous Fishes, usually so called. Its relations are the same
as those of my segmentation cavity at this stage. This paper
came into my hands at too late a period for me to be able to do
more than refer to it in this place.
The other features of the blastoderm at this stage are very much those of
the previous stage.
The embryonic swelling is very conspicuous. The cells of the blastoderm are
still disposed in two layers: an upper one of slightly columnar cells one
deep, which constitutes the epiblast, and a lower one consisting of the
remaining cells of the blastoderm.
An average cell of the lower layer has a diameter of about 1/900 inch, but
the cells at the periphery of the layer are in some cases considerably
larger than the more central ones. All the cells of the blastoderm are
still completely filled with yolk spherules. In the yolk outside the
peculiar nuclei, before spoken of, are present in considerable numbers.
They seem to have been mistaken by Dr Schultz[119] for cells: there can
however be no question that they are true nuclei.
Footnote 119: _Loc. cit._
In the next stage the relations of the segmentation cavity undergo
important modifications.
The cells which form its floor disappear almost completely from that
position, and the floor becomes formed by the yolk.
The stage, during which the yolk serves as the floor of the segmentation
cavity, extends over a considerable period of time, but during it I have
been unable to detect any important change in the constitution of the
blastoderm. It no doubt gradually extends over the yolk, but even this
growth is not nearly so rapid as in the succeeding stage. Although
therefore the stage I proceed to describe is of long continuance, a
blastoderm at the beginning of it exhibits, both in its external and in its
internal features, no important deviations from one at the end of it.
Viewed from the surface (Pl. 8, fig. A) the blastoderm at this stage
appears slightly oval, but the departure from the circular form is not very
considerable. The long axis of the oval corresponds with what eventually
becomes the long axis of the embryo. From the yolk the blastoderm is still
well distinguished by its darker colour; and it is surrounded by a
concentric ring of light-coloured yolk, the outer border of which shades
insensibly into the normal yolk.
At the embryonic portion of the blastoderm is a slight swelling, clearly
shewn in Plate 8, fig. A, which can easily be detected in fresh and in
hardened embryos. This swelling is to be looked upon as a local
exaggeration of a slightly raised rim present around the whole
circumference of the blastoderm. The roof of the segmentation cavity
(fig. A, _s.c._) forms a second swelling; and in the fresh embryo this
region appears of a darker colour than other parts of the blastoderm.
It is difficult to determine the exact shape of the blastoderm, on account
of the traction exercised upon it in opening the egg; and no reliance can
be placed on the forms assumed by hardened blastoderms. This remark also
applies to the sections of blastoderms of this stage. There can be no doubt
that the minor individual variations exhibited by almost every specimen are
produced in the course of manipulations while the objects are fresh. These
variations may affect even the relative length of a particular region and
certainly the curvature of it. The roof of the segmentation cavity is
especially apt to be raised into a dome-like form.
The main internal feature of this stage is the disappearance of the layer
of cells which, during the first stage, formed the floor of the
segmentation cavity. This disappearance is nevertheless not absolute, and
it is doubtful whether there is any period in which the floor of the cavity
is quite without cells.
Dr Schultz supposes[120] that the entire segmentation cavity is, in the
living animal, filled with a number of loose cells. Though it is not in my
power absolutely to deny this, the point being one which cannot be
satisfactorily investigated in sections, yet no evidence has come under my
notice which would lead to the conclusion that more cells are present in
the segmentation cavity than are represented on Pl. 13, fig. 1, of my
preliminary paper[121], an illustration which is repeated on Pl. 7, fig. 2.
Footnote 120: _Loc. cit._
Footnote 121: _Loc. cit._
The number of cells on the floor of the cavity differs considerably in
different cases, but these cases come under the category of individual
variations, and are not to be looked upon as indications of different
states of development.
In many cases especially large cells are to be seen on the floor of the
cavity (Pl. 7, fig. 2, _bd_). In my preliminary paper[122] the view was
expressed that these are probably cells formed around the nuclei of the
yolk. This view I am inclined to abandon, and to substitute for it the
suggestion made by Dr Schultz, that they are remnants of the larger
segmentation cells which were to be seen in the previous stages.
Footnote 122: _Qy. Journal of Micros. Science_, Oct. 1874.
[This Edition, No. V.]
Plate 7, figs. 2, 3, 4 (all sections of this stage) shew the different
appearances presented by the floor of the segmentation cavity. In only one
of these sections are there any large number of cells upon the floor; and
in no case have cells been observed imbedded in the yolk forming this
floor, as described by Dr Schultz[123], but in all cases the cells simply
rested upon it.
Footnote 123: _Loc. cit._ Probably Dr Schultz, here as in
other cases, has mistaken nuclei for cells.
Passing from the segmentation cavity to the blastoderm itself, the first
feature to be noticed is the more decided differentiation of the epiblast.
This now forms a distinct layer composed of a single row of columnar cells.
These are slightly more columnar in the region of the embryonic swelling
than elsewhere, and become less elongated at the edge of the blastoderm. In
my specimens this layer was never more than one cell deep, but Dr
Schultz[124] states that, in the Elasmobranch embryos investigated by him,
the epiblast was composed of more than a single row of cells.
Footnote 124: _Loc. cit._
Each epiblast cell is filled with yolk-spherules and contains a nucleus.
Very frequently the nuclei in the layer are arranged in a regular row (vide
Pl. 7, fig. 3). In the later blastoderms of this stage there is a tendency
in the cells to assume a wedge-like form with their thin ends pointing
alternately in opposite directions. This arrangement is, however, by no
means strictly adhered to, and the regularity of it is exaggerated in Plate
7, fig. 4.
The nuclei of the epiblast cells have the same characters as those of the
lower layer cells to be presently described, but their intimate structure
can only be successfully studied in certain exceptionally favourable
sections. In most cases the yolk-spherules around them render the finer
details invisible.
There is at this stage no such obvious continuity as in the succeeding
stage between the epiblast and the lower layer cells; and this statement
holds good more especially with the best conserved specimens which have
been hardened in osmic acid (Pl. 7, fig. 4). In these it is very easy to
see that the epiblast simply thins out at the edge of the blastoderm
without exhibiting the slightest tendency to become continuous with the
lower layer cells[125].
Footnote 125: Prof. Haeckel ("Die Gastrula u. die Eifurchung
d. Thiere," _Jenaische Zeitschrift_, Vol. IX.) has
unfortunately copied a figure from my preliminary paper (_loc.
cit._) (repeated now), which I had carefully avoided using for
the purpose of describing the formation of the layers on
account of the epiblast cells in the original having been much
altered by the chromic acid, as a result of which the whole
section gives a somewhat erroneous impression of the condition
of the blastoderm at this stage. I take this opportunity of
pointing out that the colouration employed by Professor Haeckel
to distinguish the layers in this section is not founded on my
statements, but is, on the contrary, in entire opposition to
them. From the section as represented by Professor Haeckel it
might be gathered that I considered the lower layer cells to be
divided into two parts, one derived from the epiblast, while
the other constituted the hypoblast. Not only is no such
division present at this period, but no part of the lower layer
cells, or the mesoblast cells into which they become converted,
can in any sense whatever be said to be derived from the
epiblast.
The lower layer cells form a mass rather than a layer, and constitute the
whole of the blastoderm not included in the epiblast. The shape of this
mass in a longitudinal section may be gathered from an examination of Plate
7, figs. 3 and 4.
It presents an especially thick portion forming the bulk of the embryonic
swelling, and frequently contains one or two cavities, which from their
constancy I regard as normal and not as artificial products.
In addition to the mass forming the embryonic swelling there is seen in
sections another mass of lower layer cells at the opposite extremity of the
blastoderm, connected with the former by a bridge of cells, which
constitutes the roof of the segmentation cavity. The lower layer cells may
thus be divided into three distinct parts:
(1) The embryo swelling.
(2) The thick rim of cells round the edge of the remainder of the
blastoderm.
(3) The cells which form the roof of the segmentation cavity.
These three parts form a continuous whole, but in addition to these there
exist the previously mentioned cells, which rest on the floor of the
segmentation cavity.
With the exception of these latter, the lower layer is composed of cells
having a fairly uniform size, and exhibits no trace of a division into two
layers.
The cells are for the most part irregularly polygonal from mutual pressure;
and in their shape and arrangement, exhibit a marked contrast to the
epiblast cells. A few of the lower layer cells, highly magnified, are
represented in Pl. 7, fig. 2_a_. An average cell measures about 1/800 to
1/900 of an inch, but some of the larger ones on the floor attain to the
1/475 of an inch.
Owing to my having had the good fortune to prepare some especially
favourable specimens of this stage, it has been possible for me to make
accurate observations both upon the nuclei of the cells of the blastoderm,
and upon the nuclei of the yolk.
The nuclei of the blastoderm cells, both of the epiblast and lower layer,
have a uniform structure. Those of the lower layer cells are about 1/1600
of an inch in diameter. Roughly speaking each consists of a spherical mass
of clear protoplasm refracting more highly than the protoplasm of its cell.
The nucleus appears in sections to be divided by deeply stained lines into
a number of separate areas, and in each of these a deeply stained granule
is placed. In some cases two or more of such granules may be seen in a
single area. The whole of the nucleus stains with the colouring reagents
more deeply than the protoplasm of the cells; but this is especially the
case with the granules and lines.
Though usually spherical the nuclei not infrequently have a somewhat lobate
form.
Very similar to these nuclei are the nuclei of the yolk.
One of the most important differences between the two is that of size. The
majority of the nuclei present in the yolk are as large or larger than an
ordinary blastoderm cell; while many of them reach a size very much greater
than this. The examples I have measured varied from 1/500 to 1/250 of an
inch in diameter.
Though they are divided, like the nuclei of the blastoderm, with more or
less distinctness into separate areas by a network of lines, their greater
size frequently causes them to present an aspect somewhat different from
the nuclei of the blastoderm. They are moreover much less regular in
outline than these, and very many of them have lobate projections (Pl. 7,
figs. 2_a_ and 2_c_ and 3), which vary from simple knobs to projections of
such a size as to cause the nucleus to present an appearance of commencing
constriction into halves. When there are several such projections the
nucleus acquires a peculiar knobbed figure. With bodies of this form it
becomes in many cases a matter of great difficulty to decide whether or no
a particular series of knobs, which appear separate in one plane, are
united in a lower plane, whether, in fact, there is present a single
knobbed nucleus or a number of nuclei in close apposition. A nucleus in
this condition is represented in Pl. 7, fig. 2_b_.
The existence of a protoplasmic network in the yolk has already been
mentioned. This in favourable cases may be observed to be in special
connection with the nuclei just described. Its meshes are finer in the
vicinity of the nuclei, and its fibres in some cases almost appear to start
from them (Pl. 7, fig. 12). For reasons which I am unable to explain the
nuclei of the yolk and the surrounding meshwork present appearances which
differ greatly according to the reagent employed. In most specimens
hardened in osmic acid the protoplasm of the nuclei is apparently prolonged
in the surrounding meshwork (Pl. 7, fig. 12). In other specimens hardened
in osmic acid (Pl. 7, fig. 11), and in all hardened in chromic acid (Pl. 7,
fig. 2_a_ and 2_c_), the appearances are far clearer than in the previous
case, and the protoplasmic meshwork merely surrounds the nuclei, without
shewing any signs of becoming continuous with them.
There is also around each nucleus a narrow space in which the spherules of
the yolk are either much smaller than elsewhere or completely absent, vide
Pl. 7, fig. 2_b_.
It has not been possible for me to satisfy myself as to the exact meaning
of the lines dividing these nuclei into a number of distinct areas. My
observations leave the question open as to whether they are to be looked
upon as lines of division, or as protoplasmic lines such as have been
described in nuclei by Flemming[126], Hertwig[127] and Van Beneden[128].
The latter view appears to me to be the more probable one.
Footnote 126: "Entwicklungsgeschichte der Najaden," _Sitz. d.
k. Akad. Wien_, 1875.
Footnote 127: _Morphologische Jahrbuch_, Vol. 1. Heft 3.
Footnote 128: "Développement des Mammifères," _Bul. de l'Acad.
de Belgique_, XL. No. 12, 1875.
Such are the chief structural features presented by these nuclei, which are
present during the whole of the earlier periods of development and retain
throughout the same appearance. There can be little doubt that their
knobbed condition implies that they are undergoing a rapid division. The
arguments for this view I have already insisted on, and, in spite of the
observations of Dr Kleinenberg shewing that similar nuclei of Nephelis do
not undergo division, the case for their doing so in the Elasmobranch eggs
is to my mind a very strong one.
During this stage the distribution of these nuclei in the yolk becomes
somewhat altered from that in the earlier stages. Although the nuclei are
still scattered generally throughout the finer yolk-matter around the
blastoderm, yet they are especially aggregated at one or two points. In the
first place a special collection of them may be noticed immediately below
the floor of the segmentation cavity. They here form a distinct row or even
layer. If the presence of this layer is coupled with the fact that at this
period cells are beginning to appear on the floor of the segmentation
cavity, a strong argument is obtained for the supposition that around these
nuclei cells are being produced, which pass into the blastoderm to form the
floor. Of the actual formation of cells at _this_ period I have not been
able to obtain any satisfactory example, so that it remains a matter of
deduction rather than of direct observation.
Another special aggregation of nuclei is generally present at the periphery
of the blastoderm, and the same amount of doubt hangs over the fate of
these as over that of the previously mentioned nuclei.
The next stage is the most important in the whole history of the formation
of the layers. Not only does it serve to shew, that the process by which
the layers are formed in Elasmobranchii can easily be derived from a simple
gastrula type like that of Amphioxus, but it also serves as the key by
which other meroblastic types of development may be explained. At the very
commencement of this stage the embryonic swelling becomes more
conspicuously visible than it was. It now projects above the level of the
yolk in the form of a rim. At one point, which eventually forms the
termination of the axis of the embryo, this projection is at its greatest;
while on either side of this it gradually diminishes and finally vanishes.
This projection I propose calling, as in my preliminary paper[129], the
embryonic rim.
Footnote 129: _Qy. Journal Microsc. Science_, Oct. 1874. [This
Edition, No. V.]
The segmentation cavity can still be seen from the surface, and a marked
increase in the size of the blastoderm may be noticed. During the stage
last described, the growth was but very slight; hence the rather sudden and
rapid growth which now takes place becomes striking.
Longitudinal sections at this stage, as at the earlier stages, are the most
instructive. Such a section on the same scale as Pl. 7, fig. 4, is
represented in Pl. 7, fig. 5. It passes parallel to the long axis of the
embryo, through the point of greatest development of the embryonic ring.
The three fresh features of the most striking kind are (1) the complete
envelopment of the segmentation cavity within the lower layer cells, (2)
the formation of the embryonic rim, (3) the increase in distance between
the posterior end of the blastoderm and the segmentation cavity. The
segmentation cavity has by no means relatively increased in size. The roof
has precisely its earlier constitution, being composed of an internal
lining of lower layer cells and an external one of epiblast. The thin
lining of lower layer cells is, in the course of mounting the sections,
very apt to fall off; but I am absolutely satisfied that it is never
absent.
The floor of the cavity has undergone an important change, being now formed
by a layer of cells instead of by the yolk. A precisely similar but more
partial change in the constitution of the floor takes place in Osseous
Fishes[130].
Footnote 130: Götte, "Der Keim d. Forelleneies," _Arch. f.
Mikr. Anat._ Vol. IX.; Haeckel, "Die Gastrula u. die Eifurchung
d. Thiere," _Jenaische Zeitschrift_, Bd. IX.
The mode in which the floor is formed is a question of some importance. The
nuclei, which during the last stage formed a row beneath it, probably, as
previously pointed out, take some share in its formation. An additional
argument to those already brought forward in favour of this view may be
derived from the fact that during this stage such a row of nuclei is no
longer present.
This argument may be stated as follows:
Before the floor of cells for the segmentation cavity is formed a number of
nuclei are present in a suitable situation to supply the cells for the
floor; as soon as the floor of cells makes its appearance these nuclei are
no longer to be seen. From this it may be concluded that their
disappearance arises from their having become the nuclei of the cells which
form the floor.
It appears to me most probable that there is a growth inwards from the
whole peripheral wall of the cavity, and that this ingrowth, as well as the
cells derived from the yolk, assist in forming the floor of the cavity. In
Osseous Fish there appears to be no doubt that the floor is largely formed
by an ingrowth of this kind.
A great increase is observable in the distance between the posterior end of
the segmentation cavity and the edge of the blastoderm. This is due to the
rapid growth of the latter combined with the stationary condition of the
former. The growth of the blastoderm at this period is not uniform, but is
more rapid in the non-embryonic than in the embryonic parts.
The main features of the epiblast remain the same as during the last
stages. It is still composed of a very distinct layer one cell deep. Over
the segmentation cavity, and over the whole embryonic end of the
blastoderm, the cells are very thin, columnar, and, roughly speaking,
wedge-shaped with the thin ends pointing alternately in different
directions. For this reason, the nuclei form two rows; but both the rows
are situated near the upper surface of the layer (vide Pl. 7, fig. 5).
Towards the posterior end of the blastoderm the cells are flatter and
broader; and the layer terminates at the non-embryonic end of the
blastoderm without exhibiting the slightest tendency to become continuous
with the lower layer cells. At the embryonic end of the blastoderm the
relations of the epiblast and lower layer cells are very different. At this
part, throughout the whole extent of the embryonic rim, the epiblast is
reflected and becomes continuous with the lower layer cells.
The lower layer cells form, for the most part, a uniform stratum in which
no distinction into mesoblast and hypoblast is to be seen.
Both the lower layer cells and the epiblast cells are still filled with
yolk-spherules.
The structures at the embryonic rim, and the changes which are there taking
place, unquestionably form the chief features of interest at this stage.
The general relations of these parts are very fairly shewn in Pl. 7,
fig. 5, which represents a section passing through the median line of the
embryonic region. They are however more accurately represented in Pl. 7,
fig. 5_a_, taken from the same embryo, but in a lateral part of the
embryonic rim; or in Pl. 7, fig. 6, from a slightly older embryo. In all of
these figures the epiblast cells are reflected at the edge of the embryonic
rim, and become perfectly continuous with the hypoblast cells. A few of the
cells, immediately beyond the line of this reflection, precisely resemble
in character the typical epiblast cells; but the remainder exhibit a
gradual transition into typical lower layer cells. Adjoining these
transitional cells, or partly enclosed in the corner formed between them
and the epiblast, are a few unaltered lower layer cells (_m_), which at
this stage are not distinctly separated from the transitional cells. The
transitional cells form the commencement of the hypoblast (_hy_); and the
cells (_m_) between them and the epiblast form the commencement of the
mesoblast. The gradual conversion of lower layer cells into columnar
hypoblast cells, is a very clear and observable phenomenon in the best
specimens. Where the embryonic rim projects most, a larger number of cells
have assumed a columnar form. Where it projects less clearly, a smaller
number have done so. But in all cases there may be observed a series of
gradations between the columnar cells and the typical rounded lower layer
cells[131].
Footnote 131: When writing my earlier paper I did not feel so
confident about the mode of formation of the hypoblast as I now
do, and even doubted the possibility of determining it from
sections. The facts now brought forward are I hope sufficient
to remove all scepticism on this point.
In the last described embryo, although the embryonic rim had attained to a
considerable development, no trace of the medullary groove had made its
appearance. In an embryo in the next stage of which I propose describing
sections, this structure has become visible.
A surface view of a blastoderm of this age, with the embryo, is represented
on Pl. 8, fig. B; and I shall, for the sake of convenience, in future speak
of embryos of this age as belonging to period B.
The blastoderm is nearly circular. The embryonic rim is represented by a
darker shading at the edge. At one point in this rim may be seen the
embryo, consisting of a somewhat raised area with an axial groove (_mg_).
The head end of the embryo is that which points towards the centre of the
blastoderm, and its free peripheral extremity is at the edge of the
blastoderm.
A longitudinal section of an embryo of the same age as the one figured[132]
is represented on Pl. 7, fig. 7. The general growth has been very
considerable, though as before explained, it is mainly confined to that
part of the blastoderm where the embryonic rim is absent.
Footnote 132: Owing to the small size of the plates this
section has been drawn on a considerably smaller scale than
that represented in fig. 5.
A fresh feature of great importance is the complete disappearance of the
segmentation cavity, the place which was previously occupied by it being
now filled up by an irregular network of cells. There can be little
question that the obliteration of the segmentation cavity is in part due to
the entrance into the blastoderm of fresh cells formed around the nuclei of
the yolk. The formation of these is now taking place with great rapidity
and can be very easily followed.
Since the segmentation cavity ceases to play any further part in the
history of the blastoderm, it will be well shortly to review the main
points in its history.
Its earliest appearance is involved in some obscurity, though it probably
arises as a simple cavity in the midst of the lower layer cells (Pl. 7,
fig. 1). In its second phase the floor ceases to be formed of lower layer
cells, and the place of these is taken by the yolk, on which however a few
scattered cells still remain (Pl. 7, figs. 2, 3, 4). During the third
period of its history, a distinct cellular floor is again formed for it, so
that it comes a second time into the same relations with the blastoderm as
at its earliest appearance. The floor of cells which it receives is in part
due to a growth inwards from the periphery of the blastoderm, and in part
to the formation of fresh cells from the yolk. Coincidently with the
commencing differentiation of hypoblast and mesoblast the segmentation
cavity grows smaller and vanishes.
One of the most important features of the segmentation cavity in the
Elasmobranchii which I have studied, is the fact that throughout its whole
existence its roof is formed of _lower layer cells_. There is not the
smallest question that the segmentation cavity of these fishes is the
homologue of that of Amphioxus, Batrachians, etc., yet in the case of all
of these animals, the roof of the segmentation cavity is formed of epiblast
only. How comes it then to be formed of lower layer cells in
Elasmobranchii?
To this question an answer was attempted in my paper, "Upon the Early
Stages of the Development of Vertebrates[133]." It was there pointed out,
that as the food material in the ovum increases, the bulk of the lower
layer cells necessarily also increases; since these, as far as the
blastoderm is concerned, are the chief recipients of food material. This
causes the lower layer cells to encroach upon the segmentation cavity, and
to close it in not only on the sides, but also above; from the same cause
it results that the lower layer cells assume, from the first, a position
around the spot where the future alimentary cavity will be formed, and that
this cavity becomes formed by a simple split in the midst of the lower
layer cells, and not by an involution.
Footnote 133: _Quart. Journ. of Microscop. Science_, July,
1875. [This Edition, No. VI.]
All the most recent observations[134] on Osseous Fishes tend to shew that
in them, the roof of the segmentation cavity is formed alone of epiblast;
but on account of the great difficulty which is experienced in
distinguishing the layers in the blastoderms of these animals, I still
hesitate to accept as conclusive the testimony on this point.
Footnote 134: Oellacher, _Zeit. f. Wiss. Zoologie_, Bd. XXIII.
Götte, _Archiv f. Mikr. Anat._ Vol. IX. Haeckel, _loc. cit._
In the formation a second time of a cellular floor for the segmentation
cavity in the third stage, the Elasmobranch embryo seems to resemble that
of the Osseous Fish[135]. Upon this feature great stress is laid both by Dr
Götte[136] and Prof. Haeckel[137]: but I am unable to agree with the
interpretation of it offered by them. Both Dr Götte and Prof. Haeckel
regard the formation of this floor as part of an involution to which the
lower layer cells owe their origin, and consider the involution an
equivalent to the alimentary involution of Batrachians, Amphioxus, &c. To
this question I hope to return, but it may be pointed out that my
observations prove that this view can only be true in a very modified
sense; since the invagination by which hypoblast and alimentary canal are
formed in Amphioxus is represented in Elasmobranchii by a structure quite
separate from the ingrowth of cells to form the floor of the segmentation
cavity.
Footnote 135: This floor appears in most Osseous Fish to be
only partially formed. Vide Götte, _loc. cit._
Footnote 136: _Loc. cit._
Footnote 137: _Loc. cit._
The eventual _obliteration_ of the segmentation cavity by cells derived
from the yolk is to be regarded as an inherited remnant of the involution
by which this obliteration was primitively effected. The passage upwards of
cells from the yolk, may possibly be a real survival of the tendency of the
hypoblast cells to grow inwards during the process of involution.
The last feature of the segmentation cavity which deserves notice is its
excentric position. It is from the first situated in much closer proximity
to the non-embryonic than to the embryonic end of the blastoderm. This
peculiarity in position is also characteristic of the segmentation cavity
of Osseous Fishes, as is shewn by the concordant observations of
Oellacher[138] and Götte[139]. Its meaning becomes at once intelligible by
referring to the diagrams in my paper[140] on the Early Stages in the
Development of Vertebrates. It in fact arises from the asymmetrical
character of the primitive alimentary involution in all anamniotic
vertebrates with the exception of Amphioxus.
Footnote 138: _Loc. cit._
Footnote 139: _Loc. cit._
Footnote 140: _Loc. cit._
Leaving the segmentation cavity I pass on to the other features of my
sections.
There is still to be seen a considerable aggregation of cells at the
non-embryonic end of the blastoderm. The position of this, and its
relations with the portion of the blastoderm which at an earlier period
contained the segmentation cavity, indicate that the growth of the
blastoderm is not confined to its edge, but that it proceeds at all points
causing the peripheral parts to glide over the yolk.
The main features of the cells of this blastoderm are the same as they were
in the one last described. In the non-embryonic region the epiblast has
thinned out, and is composed of a single row of cells, which, in the
succeeding stages, become much flattened.
The lower layer cells over the greater part of their extent, have not
undergone any histological changes of importance. Amongst them may
frequently be seen a few exceptionally large cells, which without doubt
have been derived directly from the yolk.
The embryonic rim is now a far more considerable structure than it was.
Vide Pl. 7, fig. 7. Its elongation is mainly effected by the continuous
conversion of rounded lower layer cells into columnar hypoblast cells at
its central or anterior extremity.
This conversion of the lower layer cells into hypoblast cells is still easy
to follow, and in every section cells intermediate between the two are to
be seen. The nature of the changes which are taking place requires for its
elucidation transverse as well as longitudinal sections. Transverse
sections of a slightly older embryo than B are represented on Pl. 7,
fig. 8_a_, 8_b_ and 8_c_.
Of these sections _a_ is the most peripheral or posterior, and _c_ the most
central or anterior. By a combination of transverse and longitudinal
sections, and by an inspection of a surface view, it is rendered clear
that, though the embryonic rim is a far more considerable structure in the
region of the embryo than elsewhere (compare fig. 6 and fig. 7 and 7_a_),
yet that this gain in size is not produced by an outgrowth of the embryo
beyond the rest of the germ, but by the conversion of the lower layer cells
into hypoblast having been carried far further towards the centre of the
germ in the axial line than in the lateral regions of the rim.
The most anterior of the series of transverse sections (Pl. 7, fig. 8_c_) I
have represented, is especially instructive with reference to this point.
Though the embryonic rim is cut through at the sides of the section, yet in
these parts the rim consists of hardly more than a continuity between
epiblast and lower layer cells, and the lower layer cells shew no trace of
a division into mesoblast and hypoblast. In the axis of the embryo,
however, the columnar hypoblast is quite distinct; and on it a small cap of
mesoblast is seen on each side of the medullary groove. Had the embryonic
rim resulted from a projecting growth of the blastoderm, such a condition
could not have existed. It might have been possible to find the hypoblast
formed at the sides of the section and not at the centre; but the reverse,
as in these sections, could not have occurred. Indeed it is scarcely
necessary to have recourse to sections to prove that the growth of the
embryonic rim is towards the centre of the blastoderm. The inspection of a
surface view of a blastoderm at this period demonstrates it beyond a doubt
(Pl. 8, fig. B). The embryo, close to which the embryonic rim is alone
largely developed, does not project outwards beyond the edge of the germ,
but inwards towards its centre.
The space between the embryonic rim and the yolk (Pl. 7, fig. 7, _al._) is
the alimentary cavity. The roof of this is therefore primitively formed of
hypoblast and the floor of yolk. The external opening of this space at the
edge of the blastoderm is the exact morphological homologue of the anus of
Rusconi, or blastopore of Amphioxus, the Amphibians, &c. The importance of
the mode of growth in the embryonic rim depends upon the homology of the
cavity between it and the yolk, with the alimentary cavity of Amphioxus and
Amphibians. Since this homology exists, the direction of the growth of this
cavity ought to be, as it in fact is, the same as in Amphioxus, etc., viz.
towards the centre of the germ and original position of the segmentation
cavity. Thus though a true invagination is not present as in the other
cases, yet this is represented in Elasmobranchii by the continuous
conversion of lower layer cells into hypoblast along a line leading towards
the centre of the blastoderm.
In the parts of the rim adjoining the embryo, the lower layer cells, on
becoming continuous with the epiblast cells, assume a columnar form. At the
sides of the rim this is not strictly the case, and the lower layer cells
retain their rounded form, though quite continuous with the epiblast cells.
One curious feature of the layer of epiblast in these lateral parts of the
rim is the great thickness it acquires before being reflected and becoming
continuous with the hypoblast (Pl. 7, fig. 8_c_). In the vicinity of the
point of reflection there is often a rather large formation of cells around
the nuclei of the yolk. The cells formed here no doubt pass into the
blastoderm, and become converted into columnar hypoblast cells. In some
cases the formation of these cells is very rapid, and they produce quite a
projection on the under side of the hypoblast. Such a case is represented
in Pl. 7, fig. 8_b_, _n.al_. The cells constituting this mass eventually
become converted into the lateral and ventral walls of the alimentary
canal.
The formation of the mesoblast has progressed rapidly. While many of the
lower layer cells become columnar and form the hypoblast, others, between
these and the epiblast, remain spherical. The latter do not at once become
separated as a layer distinct from the hypoblast, and, at first, are only
to be distinguished from them through their different character, vide Plate
7, figs. 6 and 7. They nevertheless constitute the commencing mesoblast.
Thus much of the mode of formation of the mesoblast can be easily made out
in longitudinal sections, but transverse sections throw still further light
upon it.
From these it may at once be seen that the mesoblast is not formed in one
continuous sheet, but as two lateral masses, one on each side of the axial
line of the embryo[141]. In my preliminary account[142] it was stated that
this was a condition of the mesoblast at a very early period, and that it
was probably its condition from the beginning. Sections are now in my
possession which satisfy me that, from the very first, the mesoblast arises
as two distinct lateral masses, one on each side of the axial line.
Footnote 141: Professor Lieberkühn (_Gesellschaft zu Marburg_,
Jan. 1876) finds in Mammalia a bilateral arrangement of the
mesoblast, which he compares with that described by me in
Elasmobranchii. In Mammalia, however, he finds the two masses of
mesoblast connected by a very thin layer of cells, and is
apparently of opinion that a similar thin layer exists in
Elasmobranchii though overlooked by me. I can definitely state
that, whatever may be the condition of the mesoblast in
Mammalia, in Elasmobranchii at any rate no such layer exists.
Footnote 142: _Loc. cit._
In the embryo from which the sections Pl. 7, fig. 8_a_, 8_b_, 8_c_ were
taken, the mesoblast had, in most parts, not yet become separated from the
hypoblast. It still formed with this a continuous layer, though the
mesoblast cells were distinguishable by their shape from the hypoblast. In
only one section (_b_) was any part of the mesoblast quite separated from
the hypoblast.
In the hindermost part of the embryo the mesoblast is at its maximum, and
forms, on each side, a continuous sheet extending from the median line to
the periphery (fig. 8_a_). The rounder form of the mesoblast cells renders
the line of junction between the layer constituted by them and the
hypoblast fairly distinct; but towards the periphery, where the hypoblast
cells have the same rounded form as the mesoblast, the fusion between the
two layers is nearly complete.
In an anterior section the mesoblast is only present as a cap on both sides
of the medullary groove, and as a mass of cells at the periphery of the
section (fig. 8_b_); but no continuous layer of it is present. In the
foremost of the three sections (fig. 8_c_) the mesoblast can scarcely be
said to have become in any way separated from the hypoblast except at the
summit of the medullary folds (_m_).
From these and similar sections it may be certainly concluded, that the
mesoblast becomes first separated from the hypoblast as a distinct layer in
the posterior region of the embryo, and only at a later period in the
region of the head.
In an embryo but slightly more developed than B, the formation of the layer
is quite completed in the region of the embryo. To this embryo I now pass
on.
In the non-embryonic parts of the blastoderm no fresh features of interest
have appeared. It still consists of two layers. The epiblast is composed of
flattened cells, and the lower layer of a network of more rounded cells,
elongated in a lateral direction. The growth of the blastoderm has
continued to be very rapid.
In the region of the embryo (Pl. 7, fig. 9) more important changes have
occurred. The epiblast still remains as a single row of columnar cells. The
hypoblast is no longer fused with the mesoblast, and forms a distinct
dorsal wall for the alimentary cavity. Though along the axis of the embryo
the hypoblast is composed of a single row of columnar cells, yet in the
lateral part of the embryo its cells are less columnar and are one or two
deep.
Owing to the manner in which the mesoblast became split off from the
hypoblast, a continuity is maintained between the hypoblast and the lower
layer cells of the blastoderm (Pl. 7, fig. 9), while the two plates of
mesoblast are isolated and disconnected from any other masses of cells.
The alimentary cavity is best studied in transverse sections. (Vide Pl. 7,
fig. 10_a_, 10_b_ and 10_c_, three sections from the same embryo.) It is
closed in above and at the sides by the hypoblast, and below by the yolk.
In its anterior part a floor is commencing to be formed by a growth of
cells from the walls of the two sides. The cells for this growth are formed
around the nuclei of the yolk; a feature which recalls the fact that in
Amphibians the ventral wall of the alimentary cavity is similarly formed in
part from the so-called yolk cells.
We left the mesoblast as two masses not completely separated from the
hypoblast. During this stage the separation between the two becomes
complete, and there are formed two great lateral plates of mesoblast cells,
one on each side of the medullary groove. Each of these corresponds to a
united vertebral and lateral plate of the higher Vertebrates. The plates
are thickest in the middle and posterior regions (Pl. 7, fig. 10_a_ and
10_b_), but thin out and almost vanish in the region of the head. The
longitudinal section of this stage represented in Pl. 7, fig. 9, passes
through one of the lateral masses of mesoblast cells, and shews very
distinctly its complete independence of all the other cells in the
blastoderm.
From what has been stated with reference to the development of the
mesoblast, it is clear that in Elasmobranchii this layer is derived from
the same mass of cells as the hypoblast, and receives none of its elements
from the epiblast. In connection with its development, as two independent
lateral masses, I may observe, as I have previously done[143], that in this
respect it bears a close resemblance to mesoblast in Euaxes, as described
by Kowalevsky[144]. This resemblance is of some interest, as bearing on a
probable Annelid origin of Vertebrata. Kowalevsky has also shewn[145] that
the mesoblast in Ascidians is similarly formed as two independent masses,
one on each side of the middle line.
Footnote 143: _Quart. Journ. of Microsc. Science_, Oct., 1874.
[This Edition, No. V.]
Footnote 144: "Embryologische Studien an Würmern u.
Arthropoden." _Mémoires de l'Acad. S. Pétersbourg._ Vol. XIV.
1873.
Footnote 145: _Archiv für Mikr. Anat._ Vol. VII.
It ought, however, to be pointed out that a similar bilateral origin of the
mesoblast had been recently met with in Lymnæus by Carl Rabl[146]. A fact
which somewhat diminishes the genealogical value of this feature in the
mesoblast in Elasmobranchii.
Footnote 146: _Jenaische Zeitschrift_, Vol. IX. 1875. A
bilateral development of mesoblast, according to Professor
Haeckel (_loc. cit._), occurs in some Osseous Fish. Hensen,
_Zeit. für Anat. u. Entw._ Vol. 1., has recently described the
mesoblast in Mammalia as consisting of independent lateral
masses.
During the course of this stage the spherules of food-yolk immediately
beneath the embryo are used up very rapidly. As a result of this the
protoplasmic network, so often spoken of, comes very plainly into view.
Considerable areas may sometimes be seen without any yolk-spherule
whatever.
On Pl. 7, fig. 7_a_, and figs. 11 and 12, I have attempted to reproduce the
various appearances presented by this network: and these figures give a
better idea of it than any description. My observations tend to shew that
it extends through the whole yolk, and serves to hold it together. It has
not been possible for me to satisfy myself that it had any definite limits,
but on the other hand, in many parts all my efforts to demonstrate its
presence have failed. When the yolk-spherules are very thickly packed, it
is difficult to make out for certain whether it is present or absent, and I
have not succeeded in removing the yolk-spherules from the network in cases
of this kind. In medium-sized ovarian eggs this network is very easily
seen, and extends through the whole yolk. Part of such an egg is shewn in
Pl. 7, fig. 14. In full-sized ovarian eggs, according to Schultz[147], it
forms, as was mentioned in the first chapter, radiating striæ, extending
from the centre to the periphery of the egg. When examined with the highest
powers, the lines of this network appear to be composed of immeasurably
small granules arranged in a linear direction. These granules are more
distinct in chromic acid specimens than in those hardened in osmic acid,
but are to be seen in both. There can be little doubt that these granules
are imbedded in a thread or thin layer of protoplasm.
Footnote 147: _Archiv für Mikr. Anat._ Vol. XI.
I have already (p. 252) touched upon the relation of this network to the
nuclei of the yolk[148].
Footnote 148: A protoplasmic network resembling in its
essential features the one just described has been noticed by
many observers in other ova. Fol has figured and described a
network or sponge-like arrangement of the protoplasm in the
eggs of Geryonia. (_Jenaische Zeitschrift_, Vol. VII.)
Metschnikoff (_Zeitschrift f. Wiss. Zoologie_, 1874) has
demonstrated its presence in the ova of many Siphonophoriæ and
Medusæ. Flemming ("Entwicklungsgeschichte der Najaden," _Sitz.
der k. Akad. Wien_, 1875) has found it in the ovarian ova of
fresh-water mussels (Anodonta and Unio), but regards it as due
to the action of reagents, since he fails to find it in the
fresh condition. Amongst vertebrates it has been carefully
described by Eimer (_Archiv für Mikr. Anat._, Vol. VIII.) in
the ovarian ova of Reptiles. Eimer moreover finds that it is
continuous with prolongations from cells of the epithelium of
the follicle in which the ovum is contained. According to him
remnants of this network are to be met with in the ripe ovum,
but are no longer present in the ovum when taken from the
oviduct.
During the stages which have just been described specially favourable views
are frequently to be obtained of the formation of cells in the yolk and
their entrance into the blastoderm. Two representations of these are given,
in Pl. 7, fig. 7_a_, and fig. 13. In both of these distinctly circumscribed
cells are to be seen in the yolk (_c_), and in all cases are situated near
to the typical nuclei of the yolk. The cells in the yolk have such a
relation to the surrounding parts, that it is quite certain that their
presence is not due to artificial manipulation, and in some cases it is
even difficult to decide whether or no a cell area is circumscribed round a
nucleus (Pl. 7, fig. 13). Although it would be possible for cells in the
living state to pass from the blastoderm into the yolk, yet the view that
they have done so in the cases under consideration has not much to
recommend it, if the following facts be taken into consideration. (1) That
the cells in the yolk are frequently larger than those in the blastoderm.
(2) That there are present a very large number of nuclei in the yolk which
precisely resemble the nuclei of the cells under discussion. (3) That in
some cases (Pl. 7, fig. 13) cells are seen indistinctly circumscribed as if
in the act of being formed.
Between the blastoderm and the yolk may frequently be seen a membrane-like
structure, which becomes stained with hæmatoxylin, osmic acid etc. It
appears to be a layer of coagulated albumen and not a distinct membrane.
SUMMARY.
At the close of segmentation, the blastoderm forms a somewhat lens-shaped
disc, thicker at one end than at the other; the thicker end being termed
the embryonic end.
It is divided into two layers--an upper one, the epiblast, formed by a
single row of columnar cells; and a lower one, consisting of the remaining
cells of the blastoderm.
A cavity next appears in the lower layer cells, near the non-embryonic end
of the blastoderm, but the cells soon disappear from the floor of this
cavity which then comes to be constituted by yolk alone.
The epiblast in the next stage is reflected for a small arc at the
embryonic end of the blastoderm, and becomes continuous with the lower
layer cells; at the same time some of the lower layer cells of the
embryonic end of the blastoderm assume a columnar form, and constitute the
commencing hypoblast. The portion of the blastoderm, where epiblast and
hypoblast are continuous, forms a projecting structure which I have called
the embryonic rim. This rim increases rapidly by growing inwards more and
more towards the centre of the blastoderm, through the continuous
conversion of lower layer cells into columnar hypoblast.
While the embryonic rim is being formed, the segmentation cavity undergoes
important changes. In the first place, it receives a floor of lower layer
cells, partly from an ingrowth from the two sides, and partly from the
formation of cells around the nuclei of the yolk.
Shortly after the floor of cells has appeared, the whole segmentation
cavity becomes obliterated.
When the embryonic rim has attained to some importance, the position of the
embryo becomes marked out by the appearance of the medullary groove at its
most projecting part. The embryo extends from the edge of the blastoderm
inwards towards the centre.
At about the time of the formation of the medullary groove, the mesoblast
becomes definitely constituted. It arises as two independent plates, one on
each side of the medullary groove, and is entirely derived from lower layer
cells.
The two plates of mesoblast are at first unconnected with any other cells
of the blastoderm, and, on their formation, the hypoblast remains in
connection with all the remaining lower layer cells. Between the embryonic
rim and the yolk is a cavity,--the primitive alimentary cavity. Its roof is
formed of hypoblast, and its floor of yolk. Its external opening is
homologous with the anus of Rusconi, of Amphioxus and the Amphibians. The
ventral wall of the alimentary cavity is eventually derived from cells
formed in the yolk around the nuclei which are there present.
* * * * *
Since the important researches of Gegenbaur[149] upon the meroblastic
vertebrate eggs, it has been generally admitted that the ovum of every
vertebrate, however complicated may be its apparent constitution, is
nevertheless to be regarded as a simple cell. This view is, indeed, opposed
by His[150] and to a very modified extent by Waldeyer[151], and has
recently been attacked from an entirely new standpoint by Götte[152]; but,
to my mind, the objections of these authors do not upset the well founded
conclusions of previous observations.
Footnote 149: "Wirbelthiereier mit partieller Dottertheilung."
Müller's _Arch._ 1861.
Footnote 150: _Erste Anlage des Wirbelthierleibes._
Footnote 151: _Eierstock u. Ei._
Footnote 152: _Entwicklungsgeschichte der Unke._ The important
researches of Götte on the development of the ovum, though
meriting the most careful attention, do not admit of discussion
in this place.
As soon as the fact is recognised that both meroblastic and holoblastic
eggs have the same fundamental constitution, the admission follows,
naturally, though not necessarily, that the eggs belonging to these two
classes differ solely in degree, not only as regards their constitution,
but also as regards the manner in which they become respectively converted
into the embryo. As might have been anticipated, this view has gained a
wide acceptance.
Amongst the observations, which have given a strong objective support to
this view, may be mentioned those of Professor Lankester upon the
development of Cephalopoda[153], and of Dr Götte[154] upon the development
of the Hen's egg. In Loligo Professor Lankester shewed that there appeared,
in the part of the egg usually considered as food-yolk, a number of bodies,
which eventually developed a nucleus and became cells, and that these cells
entered into the blastoderm. These observations demonstrate that in the
eggs of Loligo the so-called food-yolk is merely equivalent to a part of
the egg which in other cases undergoes segmentation.
Footnote 153: _Annals and Magaz. of Natural History_, Vol. XI.
1873, p. 81.
Footnote 154: _Archiv f. Mikr. Anat._ Vol. X.
The observations of Dr Götte have a similar bearing. He made out that in
the eggs of the Hen no sharp line is to be found separating the germinal
disc from the yolk, and that, independently of the normal segmentation, a
number of cells are derived from that part of the egg hitherto regarded as
exclusively food-yolk. This view of the nature of the food-yolk was also
advanced in my preliminary account of the development of
Elasmobranchii[155], and it is now my intention to put forward the positive
evidence in favour of this view, which is supplied from a knowledge of the
phenomena of the development of the Elasmobranch ovum; and then to discuss
how far the facts of the growth of the blastoderm in Elasmobranchii accord
with the view that their large food-yolk is exactly equivalent to part of
the ovum, which in Amphibians undergoes segmentation, rather than some
fresh addition, which has no equivalent in the Amphibian or other
holoblastic ovum.
Footnote 155: _Quart. Journ. of Micr. Science_, Oct. 1874.
Taking for granted that the ripe ovum is a single cell, the question arises
whether in the case of meroblastic ova the cell is not constituted of two
parts completely separated from one another.
Is the meroblastic ovum, before or after impregnation, composed of a
germinal disc in which _all_ the protoplasm of the cell is aggregated, and
of a food-yolk in which _no_ protoplasm is present? or is the protoplasm
present _throughout_, being simply _more concentrated_ at the germinal pole
than elsewhere? If the former alternative is accepted, we must suppose that
the mass of food-yolk is a something added which is not present in
holoblastic ova. If the latter alternative is accepted, it may then be
maintained that holoblastic and meroblastic ova are constituted in the same
way and differ only in the proportions of their constituents.
My own observations in conjunction with the specially interesting
observations of Dr Schultz[156] justify the view which regards the
protoplasm as present throughout the whole ovum, and not confined to the
germinal disc. Our observations shew that a fine protoplasmic network, with
ramifications extending throughout the whole yolk, is present both before
and after impregnation.
Footnote 156: _Archiv f. Mikr. Anat._ Vol. XXI.
The presence of this network is, in itself, only sufficient to prove that
the yolk _may_ be equivalent to part of a holoblastic ovum; to demonstrate
that it is so requires something more, and this link in the chain of
evidence is supplied by the nuclei of the yolk, which have been so often
referred to.
These nuclei arise independently in the yolk, and become the nuclei of
cells which enter the germ and the bodies of which are derived from the
protoplasm of the yolk. Not only so, but the cells formed around these
nuclei play the same part in the development of Elasmobranchii as do the
largest so-called yolk cells in the development of Amphibians. Like the
homologous cells in Amphibians, they mainly serve to form the ventral wall
of the alimentary canal and the blood-corpuscles. The identity in the fate
of the so-called yolk cells of Amphibians with the cells derived from the
yolk in Elasmobranchii, must be considered as a proof of the homology of
the yolk cells in the first case with the yolk in the second; the
difference between the yolk in the two cases arising from the fact that in
the Elasmobranch ovum the yolk-spherules bear a larger proportion to the
protoplasm than they do in the Amphibian ovum. As I have suggested
elsewhere[157], the segmentation or non-segmentation of a particular part
of the ovum depends solely upon the proportion borne by the protoplasm to
the yolk particles; so that, when the latter exceed the former in a certain
fixed proportion, segmentation is no longer possible; and, as this limit is
approached, segmentation becomes slower, and the resulting segments larger
and larger.
Footnote 157: "Comparison," &c., _Quart. Journ. Micr.
Science_, July, 1875. [This Edition, No. VI.]
The question how far the facts in the developmental history of the various
vertebrate blastoderms accord with the view of the nature of the yolk just
propounded is one of considerable interest. An answer to it has already
been attempted from a general point of view in my paper[158] entitled 'The
Comparison of the early stages of development in Vertebrates'; but the
subject may be conveniently treated here in a special manner for
Elasmobranch embryos.
Footnote 158: _Loc. cit._
In the woodcut, fig. 1, _A_, _B_, _C_[159], are represented three
diagrammatic longitudinal sections of an Elasmobranch embryo. _A_ nearly
corresponds with the longitudinal section represented on Pl. 7, fig. 4, and
_B_ with Pl. 7, fig. 7. In Pl. 7, fig. 7, the segmentation cavity has
however completely disappeared, while it is still represented as present in
the diagram of the same period. If these diagrams, or better still, the
woodcuts fig. 2 _A_, _B_, _C_ (which only differ from those of the
Elasmobranch fish in the smaller amount of food-yolk), be compared with the
corresponding ones of Bombinator, fig. 3, _A_, _B_, _C_, they will be found
to be in fundamental agreement with them. First let fig. 1, _A_, or fig. 2,
_A_, or Pl. 7, fig. 4, be compared with fig. 3, _A_. In all there is
present a segmentation cavity situated not centrally but near the surface
of the egg. The roof of the cavity is thin in all, being composed in the
Amphibian of epiblast alone, and in the Elasmobranch of epiblast and _lower
layer cells_. The floor of the cavity is, in all, formed of so-called yolk
(vide Pl. 7, fig. 4), which in all forms the main mass of the egg. In the
Amphibian the yolk is segmented, and, though it is not segmented in the
Elasmobranch, it contains in compensation the nuclei so often mentioned. In
all, the sides of the segmentation cavity are formed by lower layer cells.
In the Amphibian the sides are enclosed by smaller cells (in the diagram)
which correspond exactly in function and position with the lower layer
cells of the Elasmobranch blastoderm.
Footnote 159: This figure, together with figs. 2 and 3, are
reproduced from my paper upon the comparison of the early
stages of development in vertebrates.
[Illustration: FIG. 1.
Diagrammatic longitudinal sections of an Elasmobranch embryo.
_Epiblast_ without shading. _Mesoblast_ black with clear outlines to the
cells. _Lower layer cells_ and _hypoblast_ with simple shading.
_ep._ epiblast. _m._ mesoblast. _al._ alimentary cavity. _sg._ segmentation
cavity. _nc._ neural canal. _ch._ notochord. _x._ point where epiblast and
hypoblast become continuous at the posterior end of the embryo. _n._ nuclei
of yolk.
_A._ Section of young blastoderm, with segmentation cavity in the middle of
the lower layer cells.
_B._ Older blastoderm with embryo in which hypoblast and mesoblast are
distinctly formed, and in which the alimentary slit has appeared. The
segmentation cavity is still represented as being present, though by this
stage it has in reality disappeared.
_C._ Older blastoderm with embryo in which neural canal has become formed,
and is continuous posteriorly with alimentary canal. The notochord, though
shaded like mesoblast, belongs properly to the hypoblast.]
[Illustration: FIG. 2.
Diagrammatic longitudinal sections of embryo, which develops in the same
manner as the Elasmobranch embryo, but in which the ovum contains far less
food-yolk than is the case with the Elasmobranch ovum.
_Epiblast_ without shading. _Mesoblast_ black with clear outlines to the
cells. _Lower layer cells_ and _hypoblast_ with simple shading.
_ep._ epiblast. _m._ mesoblast. _hy._ hypoblast. _sg._ segmentation cavity.
_al._ alimentary cavity. _nc._ neural canal. _hf._ head fold. _n._ nuclei
of the yolk.
The stages _A_, _B_ and _C_ are the same as in figure .][Transcriber's
note: figure number is missing in the original.]
[Illustration: FIG. 3.
Diagrammatic longitudinal sections of Bombinator igneus. Reproduced with
modifications from Götte.
_Epiblast_ without shading. _Mesoblast_ black with clear outlines to the
cells. _Lower layer cells_ and _hypoblast_ with simple shading.
_ep._ epiblast. _l.l._ lower layer cells. _y._ smaller lower layer cells at
the sides of the segmentation cavity. _m._ mesoblast. _hy._ hypoblast.
_al._ alimentary cavity. _sg._ segmentation cavity. _nc._ neural cavity.
_yk._ yolk-cells.
_A_ is the youngest stage in which the alimentary involution has not yet
appeared. _x_ is the point from which the involution will start to form the
dorsal wall of the alimentary tract. The line on each side of the
segmentation cavity, which separates the smaller lower layer cells from the
epiblast cells, is not present in Götte's original figure. The two shadings
employed in the diagram render it necessary to have some line, but at this
stage it is in reality not possible to assert which cells belong to the
epiblast and which to the lower layer.
_B._ In this stage the alimentary cavity has become formed, but the
segmentation cavity is not yet obliterated.
_x._ point where epiblast and hypoblast become continuous.
_C._ The neural canal is already formed, and communicates posteriorly with
the alimentary.
_x._ point where epiblast and hypoblast become continuous.]
The relation of the yolk to the blastoderm in the Elasmobranch embryo at
this stage of development very well suits the view of its homology with the
large cells of the Amphibian ovum. The only essential difference between
the two ova arises from the roof of the segmentation cavity being in the
Elasmobranch embryo formed of lower layer cells, which are absent in the
Amphibian embryo. This difference no doubt depends upon the greater
quantity of yolk particles present in the Elasmobranch ovum. These increase
the bulk of the lower layer cells, which are thus compelled to creep up the
sides of the segmentation cavity till they close it in above.
In the next stage for the Elasmobranch, fig. 1 and 2 _B_ and Pl. 7, fig. 7,
and for the Amphibian, fig. 3, _B_, the agreement between the two types is
again very close. In both for a small portion (_x_) of the edge of the
blastoderm the epiblast and hypoblast become continuous, while at all other
parts the epiblast, accompanied by lower layer cells, grows round the yolk
or round the large cells which correspond to it. The yolk cells of the
Amphibian ovum form a comparatively small mass, and are therefore rapidly
enveloped; while in the case of the Elasmobranch ovum, owing to the greater
mass of the yolk, the same process occupies a long period. In both ova the
portion of the blastoderm, where epiblast and hypoblast become continuous,
forms the dorsal lip of an opening--the anus of Rusconi--which leads into
the alimentary cavity. This cavity has the same relation in both ova. It is
lined dorsally by lower layer cells, and ventrally by yolk or what
corresponds with yolk; the ventral epithelium of the alimentary canal being
in both cases eventually supplied by the yolk cells.
As in the earlier stage, so in the present one, the anatomical relations of
the yolk to the blastoderm in the one case (Elasmobranch) are nearly
identical with those of the yolk cells to the blastoderm in the other
(Amphibian). The main features in which the two embryos differ, during the
stage under consideration, arise from the same cause as the solitary point
of difference during the preceding stage.
In Amphibians, the alimentary cavity is formed coincidently with a true
ingrowth of cells from the point where epiblast and hypoblast become
continuous, and from this ingrowth the dorsal wall of the alimentary cavity
is formed. The same ingrowth causes the obliteration of the segmentation
cavity.
In the Elasmobranchii, owing to the larger bulk of the lower layer cells
caused by the food-yolk, these have been compelled to arrange themselves in
their final position during segmentation, and no room is left for a true
invagination; but instead of this there is formed a simple split between
the blastoderm and the yolk. The homology of this with the primitive
invagination is nevertheless proved by the survival of a number of features
belonging to the ancestral condition in which a true invagination was
present. Amongst the more important of these are the following:--(1) The
continuity of epiblast and hypoblast at the dorsal lip of the anus of
Rusconi. (2) The continuous conversion of indifferent lower layer cells
into hypoblast, which gradually extends backwards towards the segmentation
cavity, and exactly represents the course of the invagination whereby in
Amphibians the dorsal wall of the alimentary cavity is formed. (3) The
obliteration of the segmentation cavity during the period when the
pseudo-invagination is occurring.
The asymmetry of the gastrula or pseudo-gastrula in Cyclostomes,
Amphibians, Elasmobranchii and, I believe, Osseous Fishes, is to be
explained by the form of the vertebrate body. In Amphioxus, where the small
amount of food-yolk present is distributed uniformly, there is no reason
why the invagination and resulting gastrula should not be symmetrical. In
other vertebrates, where more food-yolk is present, the shape and structure
of the body render it necessary for the food-yolk to be stored away on the
ventral side of the alimentary canal. This, combined with the unsymmetrical
position of the anus, which primitively corresponds in position with the
blastopore or anus of Rusconi, causes the asymmetry of the gastrula
invagination, since it is not possible for the part of the ovum which will
become the ventral wall of the alimentary canal, and which is loaded with
food-yolk, to be invaginated in the same fashion as the dorsal wall. From
the asymmetry, so caused, follow a large number of features in vertebrate
development, which have been worked out in some detail in my paper already
quoted[160].
Footnote 160: _Quart. Journ. of Micr. Science_, July, 1875.
[This Edition, No. VI.]
Prof. Haeckel, in a paper recently published[161], appears to imply that
because I do not find absolute invagination in Elasmobranchii, I therefore
look upon Elasmobranchii as militating against his Gastræa theory. I cannot
help thinking that Prof. Haeckel must have somewhat misunderstood my
meaning. The importance of the Gastræa theory has always appeared to me to
consist not in the fact that an actual ingrowth of certain cells occurs--an
ingrowth which might have many different meanings[162]--but in the fact
that the types of early development of all animals can be easily derived
from that of the typical gastrula. I am perfectly in accordance with
Professor Haeckel in regarding the type of Elasmobranch development to be a
simple derivative from that of the gastrula, although believing it to be
without any true ingrowth or invagination of cells.
Footnote 161: "Die Gastrula u. Eifurchung d. Thiere,"
_Jenaische Zeitschrift_, Vol. IX.
Footnote 162: For instance, in Crustaceans it does not in some
cases appear certain whether an invagination is the typical
gastrula invagination, or only an invagination by which, at a
period subsequent to the gastrula invagination, the hind gut is
frequently formed.
Professor Haeckel[163] in the paper just referred to published his view
upon the mutual relationships of the various vertebrate blastoderms. In
this paper, which appeared but shortly after my own[164] on the same
subject, he has put forward views which differ from mine in several
important details. Some of these bear upon the nature of food-yolk; and it
appears to me that Professor Haeckel's scheme of development is
incompatible with the view that the food-yolk in meroblastic eggs is the
homologue of part of the hypoblast of the holoblastic eggs.
Footnote 163: _Loc. cit._
Footnote 164: _Loc. cit._
The following is Professor Haeckel's own statement of the scheme or type,
which he regards as characteristic of meroblastic eggs, pp. 98 and 99.
Jetzt folgt der höchst wichtige und interessante Vorgang,
den ich als Einstülpung der Blastula auffasse und der zur
Bildung der Gastrula führt (Fig. 63, 64)[165]. Es schlägt
sich nämlich der verdickte Saum der Keimscheibe, der
"Randwulst" oder das _Properistom_, nach innen um und eine
dünne Zellenschicht wächst als directe Fortsetzung
desselben, wie ein immer enger werdendes Diaphragma, in die
Keimhöhle hinein. Diese Zellenschicht ist das entstehende
Entoderm (Fig. 64 _i_, 74 _i_). Die Zellen, welche dieselbe
zusammensetzen und aus dem innern Theile des Randwulstes
hervorwachsen, sind viel grösser aber flacher als die Zellen
der Keimhöhlendecke und zeigen ein dunkleres grobkörniges
Protoplasma. Auf dem Boden der Keimhöhle, d. h. also auf der
Eiweisskugel des Nahrungsdotters, liegen sie unmittelbar auf
und rücken hier durch centripetale Wanderung gegen dessen
Mitte vor, bis sie dieselbe zuletzt erreichen und nunmehr
eine zusammenhängende einschichtige Zellenlage auf dem
ganzen Keimhöhlenboden bilden. Diese ist die erste
vollständige Anlage des Darmblatts, Entoderms oder
"Hypoblasts", und von nun an können wir, im Gegensatz dazu
den gesammten übrigen Theil des Blastoderms, nämlich die
mehrschichtige Wand der Keimhöhlendecke als Hautblatt,
Exoderm oder "Epiblast" bezeichnen. Der verdickte Randwulst
(Fig. 64 _w_, 74 _w_), in welchem beide primäre Keimblätter
in einander übergehen, besteht in seinem oberen und äusseren
Theile aus Exodermzellen, in seinem unteren und inneren
Theile aus Entodermzellen.
In diesem Stadium entspricht unser Fischkeim einer
Amphiblastula, welche mitten in der Invagination begriffen
ist, und bei welcher die entstehende Urdarmhöhle eine grosse
Dotterkugel aufgenommen hat. Die Invagination wird nunmehr
dadurch vervollständigt und die Gastrulabildung dadurch
abgeschlossen, dass die Keimhöhle verschwindet. Das
wachsende Entoderm, dem die Dotterkugel innig anhängt, wölbt
sich in die letztere hinein und nähert sich so dem Exoderm.
Die klare Flüssigkeit in der Keimhöhle wird resorbirt und
schliesslich legt sich die obere convexe Fläche des
Entoderms an die untere concave des Exoderms eng an: die
Gastrula des discoblastischen Eies oder die "Discogastrula"
ist fertig (Fig. 65, 76; Meridiandurchschnitt Fig. 66, 75).
Die Discogastrula unsers Knochenfisches in diesem Stadium
der vollen Ausbildung stellt nunmehr eine kreisrunde Kappe
dar, welche wie ein gefüttertes Mützchen fast die ganze
obere Hemisphäre der hyalinen Dotterkugel eng anliegend
bedeckt (Fig. 65). Der Ueberzug des Mützchens entspricht dem
Exoderm (_e_), sein Futter dem Entoderm (_i_). Ersteres
besteht aus drei Schichten von kleineren Zellen, letzteres
aus einer einzigen Schicht von grösseren Zellen. Die
Exodermzellen (Fig. 77) messen 0.006 - 0.009 Mm., und haben
ein klares, sehr feinkörniges Protoplasma. Die
Entodermzellen (Fig. 78) messen 0.02 - 0.03 Mm. und ihr
Protoplasma ist mehr grobkörnig und trüber. Letztere bilden
auch den grössten Theil des Randwulstes, den wir nunmehr als
Urmundrand der Gastrula, als "_Properistoma_" oder auch als
"RUSCONI'schen After" bezeichnen können. Der letztere
umfasst die Dotterkugel, welche die ganze Urdarmhöhle
ausfüllt und weit aus der dadurch verstopften
Urmund-Oeffnung vorragt.
Footnote 165: The references in this quotation are to the
figures in the original.
My objections to the view so lucidly explained in the passage just quoted,
fall under two heads.
(1) That the facts of development of the meroblastic eggs of vertebrates,
are not in accordance with the views here advanced.
(2) That even if these views be accepted as representing the actual facts
of development, the explanation offered of these facts would not be
satisfactory.
* * * * *
Professor Haeckel's views are absolutely incompatible with the facts of
Elasmobranch development, if my investigations are correct.
The grounds of the incompatibility may be summed up under the following
heads:
(1) In Elasmobranchii the hypoblast cells occupy, even before the close of
segmentation, the position which, on Professor Haeckel's view, they ought
only eventually to take up after being involuted from the whole periphery
of the blastoderm.
(2) There is no sign at any period of an invagination of the periphery of
the blastoderm, and the only structure (the embryonic rim) which could be
mistaken for such an invagination is confined to a very limited arc.
(3) The growth of cells to form the floor of the segmentation cavity, which
ought to be part of this general invagination from the periphery, is mainly
due to a formation of cells from the yolk.
It is this ingrowth of cells for the floor of the segmentation cavity
which, I am inclined to think, Professor Haeckel has mistaken for a general
invagination in the Osseous Fish he has investigated.
(4) Professor Haeckel fails to give an account of the asymmetry of the
blastoderm; an asymmetry which is unquestionably also present in the
blastoderm of most Osseous Fishes, though not noticed by Professor Haeckel
in the investigations recorded in his paper.
The facts of development of Osseous Fishes, upon which Professor Haeckel
rests his views, are too much disputed, for their discussion in this place
to be profitable[166]. The eggs of Osseous Fishes appear to me
unsatisfactory objects for the study of this question, partly on account of
all the cells of the blastoderm being so much alike, that it is a very
difficult matter to distinguish between the various layers, and, partly,
because there can be little question that the eggs of existing Osseous
Fishes are very much modified, through having lost a great part of the
food-yolk possessed by the eggs of their ancestors[167]. This disappearance
of the food-yolk must, without doubt, have produced important changes in
development, which would be especially marked in a pelagic egg, like that
investigated by Professor Haeckel.
Footnote 166: A short statement by Kowalevsky on this subject
in a note to his account of the development of Ascidians, would
seem to indicate that the type of development of Osseous Fishes
is precisely the same as that of Elasmobranchii. Kowalevsky
says, _Arch. f. Mikr. Anat._ Vol. VII. p. 114, note 5,
"According to my observations on Osseous Fishes the germinal
wall consists of two layers, an upper and lower, which are
continuous with one another at the border. From the upper one
develops skin and nervous system, from the lower hypoblast and
mesoblast." This statement, which leaves unanswered a number of
important questions, is too short to serve as a basis for
supporting my views, but so far as it goes its agreement with
the facts of Elasmobranch development is undoubtedly striking.
Footnote 167: The eggs of the Osseous Fishes have, I believe,
undergone changes of the same character, but not to the same
extent, as those of Mammalia, which, according to the views
expressed both by Professor Haeckel and myself, are degenerated
from an ovum with a large food-yolk. The grounds on which I
regard the eggs of Osseous Fishes as having undergone an
analogous change, are too foreign to the subject to be stated
here.
The Avian egg has been a still more disputed object than even the egg of
the Osseous Fishes. The results of my own investigations on this subject do
not accord with those of Dr Götte, or the views of Professor Haeckel[168].
Footnote 168: I find myself unable without figures to
understand Dr Rauber's (_Centralblatt für Med. Wiss._ 1874, No.
50; 1875, Nos. 4 and 17) views with sufficient precision to
accord to them either my assent or dissent. It is quite in
accordance with the view propounded in my paper (_loc. cit._)
to regard, with Dr Rauber and Professor Haeckel, the thickened
edge of the blastoderm as the homologue of the lip of the
blastopore in Amphioxus; though an invagination, in the manner
imagined by Professor Haeckel, is no necessary consequence of
this view. If Dr Rauber regards the _whole_ egg of the bird as
the homologue of that of Amphioxus, and the inclosure of the
yolk by the blastoderm as the equivalent to the process of
invagination in Amphioxus, then his views are practically in
accordance with my own.
Apart from disputed points of development, it appears to me that a
comparative account of the development of the meroblastic vertebrate ova
ought to take into consideration the essential differences which exist
between the Avian and Piscian blastoderms, in that the embryo is situated
in the centre of the blastoderm in the first case and at the edge in the
second[169].
Footnote 169: I have suggested in a previous paper
("Comparison," &c., _Quart. Journal of Micr. Science_, July,
1875) that the position occupied by the embryo of Birds at the
centre, and not at the periphery, of the blastoderm may be due
to an abbreviation of the process by which the Elasmobranch
embryos cease to be situated at the edge of the blastoderm
(vide p. 296 and Pl. 9, fig. 1, 2). Assuming this to be the
real explanation of the position of the embryo in Birds, I feel
inclined to repeat a speculation which I made some time ago
with reference to the primitive streak in Birds (_Quart. Journ.
of Micr. Science_, 1873, p. 280). In Birds there is, as is well
known, a structure called the primitive streak, which has been
shewn by the observations of Dursy, corroborated by my
observations (_loc. cit._), to be situated behind the medullary
groove, and to take no part in the formation of the embryo. I
further shewed that the peculiar fusion of epiblast and
mesoblast, called by His the axis cord, was confined to this
structure and did not occur in other parts of the blastoderm.
Nearly similar results have been recently arrived at by Hensen
with reference to the primitive streak in Mammals. The position
of the primitive streak immediately behind the embryo suggests
the speculation that it may represent the line along which the
edges of the blastoderm coalesced, so as to give to the embryo
the central position which it has in the blastoderms of Birds
and Mammals, and that the peculiar fusion of epiblast and
mesoblast at this point may represent the primitive continuity
of epiblast and lower layer cells at the dorsal lip of the anus
of Rusconi in Elasmobranchii. I put this speculation forward as
a mere suggestion, in the hope of elucidating the peculiar
structure of the primitive streak, which not improbably may be
found to be the keystone to the nature of the blastoderm of the
higher vertebrates.
This difference entails important modifications in development, and must
necessarily affect the particular points under discussion. As a result of
the different positions of the embryo in the two cases, there is present in
Elasmobranchii and Osseous Fishes a true anus of Rusconi, or primitive
opening into the alimentary canal, which is absent in Birds. Yet in neither
Elasmobranchii[170] nor Osseous Fishes does the anus of Rusconi correspond
in position with the point where the final closing in of the yolk takes
place, but in them this point corresponds rather with the blastopore of
Birds[171].
Footnote 170: Vide p. 296 and Plate 9, fig. 1 and 2, and Self,
"Comparison," &c., _loc. cit._
Footnote 171: The relation of the anus of Rusconi and
blastopore in Elasmobranchii was fully explained in the paper
above quoted. It was there clearly shewn that neither the one
nor the other exactly corresponds with the blastopore of
Amphioxus, but that the two together do so. Professor Haeckel
states that in the Osseous Fish investigated by him the anus of
Rusconi and the blastopore coincide. This is not the case in
the Salmon.
Owing also to the respective situations of the embryo in the blastoderm,
the alimentary and neural canals communicate posteriorly in Elasmobranchii
and Osseous Fishes, but _not_ in Birds. Of all these points Professor
Haeckel makes no mention.
The support of his views which Prof. Haeckel attempts to gain from Götte's
researches in Mammalia is completely cut away by the recent discoveries of
Van Beneden[172] and Hensen[173].
Footnote 172: "Développement Embryonnaire des Mammifères,"
_Bulletin de l'Acad. r. d. Belgique_, 1875.
Footnote 173: _Loc. cit._
It thus appears that Professor Haeckel's views but ill accord with the
facts of vertebrate development; but even if they were to do so completely
it would not in my opinion be easy to give a rational explanation of them.
Professor Haeckel states that no sharp and fast line can be drawn between
the types of 'unequal' and 'discoidal' segmentation[174]. In the cases of
unequal segmentation he admits, as is certainly the case, that the larger
yolk cells (hypoblast) are simply enclosed by a growth of the epiblast
around them; which is to be looked on as a modification of the typical
gastrula invagination, necessitated by the large size of the yolk cells
(vide Professor Haeckel's paper, Taf. II. fig. 30). In these instances
there is no commencement of an ingrowth in the _manner supposed for
meroblastic ova_.
Footnote 174: For an explanation of these terms, vide Prof.
Haeckel's original paper or the abstract in _Quart. Journ. of
Micr. Science_ for January, 1876.
When the food-yolk becomes more bulky, and the hypoblast does not
completely segment, it is not easy to understand why an ingrowth, which had
no existence in the former case, should occur; nor where it is to come
from. Such an ingrowth as is supposed to exist by Professor Haeckel would,
in fact, break the continuity of development between meroblastic and
holoblastic ova, and thus destroy one of the most important results of the
Gastræa theory.
It is quite easy to suppose, as I have done, that in the cases of discoidal
segmentation, the hypoblast (including the yolk) becomes enclosed by the
epiblast in precisely the same manner as in the cases of unequal
segmentation.
But even if Professor Haeckel supposes that in the unsegmented food-yolk a
fresh element is added to the ovum, it remains quite unintelligible to me
how an ingrowth of cells from a circumferential line, to form a layer which
had no previous existence, can be equivalent to, or derived from, the
invagination of a layer, which exists before the process of invagination
begins, and which remains continuous throughout it.
If Professor Haeckel's views should eventually turn out to be in accordance
with the facts of vertebrate development, it will, in my opinion, be very
difficult to reduce them into conformity with the Gastræa theory.
Although some space has been devoted to an attempt to refute the views of
Professor Haeckel on this question, I wish it to be clearly understood that
my disagreement from his opinions concerns matters of detail only, and that
I quite accept the Gastræa theory in its general bearings.
* * * * *
Observations upon the formation of the layers in Elasmobranchii have
hitherto been very few in number. Those published in my preliminary account
of these fishes are, I believe, the earliest[175].
Footnote 175: I omit all reference to a paper published in
Russian by Prof. Kowalevsky. Being unable to translate it, and
the illustrations being too meagre to be in themselves of much
assistance, it has not been possible for me to make any use of
it.
Since then there has been published a short notice on the subject by Dr
Alex. Schultz[176]. His observations in the main accord with my own. He
apparently speaks of the nuclei of the yolk as cells, and also of the
epiblast being more than one cell deep. In Torpedo alone, amongst the
genera investigated by me, is the layer of epiblast, at about the age of
the last described embryo, composed of more than a single row of cells.
Footnote 176: _Centralblatt f. Med. Wiss._ No. 33, 1875.
EXPLANATION OF PLATE 7.
COMPLETE LIST OF REFERENCE LETTERS.
_c._ Cells formed in the yolk around the nuclei of the yolk. _ep._
Epiblast. _er._ Embryonic ring. _es._ Embryo swelling. _hy._ Hypoblast.
_ll._ Lower layer cells. _ly._ Line separating the yolk from the
blastoderm. _m._ Mesoblast. _mg._ Medullary groove. _n´._ Nuclei of yolk.
_na._ Cells to form ventral wall of alimentary canal which have been
derived from the yolk. _nal._ Cells formed around the nuclei of the yolk
which have entered the hypoblast. _sc._ Segmentation cavity. _vp._ Combined
lateral and vertebral plate of mesoblast.
Fig. 1. Longitudinal section of a blastoderm at the first appearance of the
segmentation cavity.
Fig. 2. Longitudinal section through a blastoderm after the layer of cells
has disappeared from the floor of the segmentation cavity. _bd._ Large cell
resting on the yolk, probably remaining over from the later periods of
segmentation. Magnified 60 diameters. (Hardened in chromic acid.)
The section is intended to illustrate the fact that the nuclei form a layer
in the yolk under the floor of the segmentation cavity. The roof of the
segmentation cavity is broken.
Fig. 2_a_. Portion of same blastoderm highly magnified, to shew the
characters of the nuclei of the yolk _n´_ and the nuclei in the cells of
the blastoderm.
Fig. 2_b_. Large knobbed nucleus from the same blastoderm, very highly
magnified.
Fig. 2_c_. Nucleus of yolk from the same blastoderm.
Fig. 3. Longitudinal section of blastoderm of same stage as fig. 2.
(Hardened in chromic acid.)
Fig. 4. Longitudinal section of blastoderm slightly older than fig. 2.
Magnified 45 diameters. (Hardened in osmic acid.)
It illustrates (1) the characters of the epiblast; (2) the embryonic
swelling; (3) the segmentation cavity.
Fig. 5. Longitudinal section through a blastoderm at the time of the first
appearance of the embryonic rim, and before the formation of the medullary
groove. Magnified 45 diameters.
Fig. 5_a_. Section through the periphery of the embryonic rim of the
blastoderm of which fig. 5 represents a section.
Fig. 6. Section through the embryonic rim of a blastoderm somewhat younger
than that represented on Pl. 8, fig. B.
Fig. 7. Section through the most projecting portion of the embryonic rim of
a blastoderm of the same age as that represented on Pl. 8, fig. B. The
section is drawn on a very considerably smaller scale than that on fig. 5.
It is intended to illustrate the growth of the embryonic rim and the
disappearance of the segmentation cavity.
Fig. 7_a_. Section through peripheral portion of the embryonic rim of the
same blastoderm, highly magnified. It specially illustrates the formation
of a cell (_c_) around a nucleus in the yolk. The nuclei of the blastoderm
have been inaccurately rendered by the artist.
Figs. 8_a_, 8_b_, 8_c_. Three sections of the same embryo. Inserted mainly
to illustrate the formation of the mesoblast as two independent lateral
masses of cells; only half of each section is represented. 8_a_ is the most
posterior of the three sections. In it the mesoblast forms a large mass on
each side, imperfectly separated from the hypoblast. In 8_b_, from the
anterior part of the embryo, the main mass of mesoblast is far smaller, and
only forms a cap to the hypoblast at the highest point of the medullary
fold. In 8_c_ a cap of mesoblast is present, similar to that in 8_b_,
though much smaller. The sections of these embryos were somewhat oblique,
and it has unfortunately happened that while in 8_a_ one side is
represented, in 8_b_ and 8_c_ the other side is figured, had it not been
for this the sections 8_b_ and 8_c_ would have been considerably longer
than 8_a_.
Fig. 9. Longitudinal section of an embryo belonging to a slightly later
stage than B.
This section passes through one of the medullary folds. It illustrates the
continuity of the hypoblast with the remaining lower layer cells of the
blastoderm.
Figs. 10_a_, 10_b_, 10_c_. Three sections of the same embryo belonging to a
stage slightly later than B, Pl. 8. The space between the mesoblast and the
hypoblast has been made considerably too great in the figures of the three
sections.
10_a_. The most posterior of the three sections. It shews the posterior
flatness of the medullary groove and the two isolated vertebral plates.
10_b_. This section is taken from the anterior part of the same embryo and
shews the deep medullary groove and the commencing formation of the ventral
wall of the alimentary canal from the nuclei of the yolk.
10_c_ shews the disappearance of the medullary groove and the thinning out
of the mesoblast plates in the region of the head.
Fig. 11. Small portion of the blastoderm and the subjacent yolk of an
embryo at the time of the first appearance of the medullary groove × 300.
It shews two large nuclei of the yolk (_n_) and the protoplasmic network in
the yolk between them; the network is seen to be closer round the nuclei
than in the intervening space. There are no areas representing cells around
the nuclei.
Fig. 12. Nucleus of the yolk in connection with the protoplasmic network
hardened in osmic acid.
Fig. 13. Portion of posterior end of a blastoderm of stage B, shewing the
formation of cells around the nuclei of the yolk.
Fig. 14. Section through part of a young Scyllium egg, about 1/15th of an
inch in diameter.
_nl._ Protoplasmic network in yolk. _zp._ Zona pellucida. _ch._
Structureless chorion. _fep._ Follicular epithelium. _x._ Structureless
membrane external to this.
CHAPTER IV.
THE GENERAL FEATURES OF THE ELASMOBRANCH EMBRYO AT SUCCESSIVE STAGES.
No complete series of figures, representing the various stages in
development of an Elasmobranch Embryo, has hitherto been published. With
the view of supplying this deficiency Plate 8 has been inserted. The
embryos represented in this Plate form a fairly complete series, but do not
all belong to a single species. Figs. A, B, C, D, E, F, H, I represent
embryos of Pristiurus; G being an embryo of Torpedo. The remaining figures,
excepting K, which is a Pristiurus embryo, are embryos of Scyllium
canicula. The embryos A-I were very accurately drawn from nature by my
sister, Miss A. B. Balfour. Unfortunately the exceptional beauty and
clearness of the originals is all but lost in the lithographs. To
facilitate future description, letters will be employed in the remainder of
these pages to signify that an embryo being described is of the same age as
the embryo on this Plate to which the letter used refers. Thus an embryo of
the same age as L will be spoken of hereafter as belonging to stage L.
A.
This figure represents a hardened blastoderm at a stage when the
embryo-swelling (_e.s._) has become obvious, but before the appearance of
the medullary groove. The position of the segmentation cavity is indicated
by a slight swelling of the blastoderm (_s.c_). The shape of the
blastoderm, in hardened specimens, is not to be relied upon, owing to the
traction which the blastoderm undergoes during the process of removing the
yolk from the egg-shell.
B.
B is the view of a fresh blastoderm. The projecting part of this, already
mentioned as the 'embryonic rim', is indicated by the shading. At the
middle of the embryonic rim is to be seen the rudiment of the embryo
(_m.g._). It consists of an area of the blastoderm, circumscribed on its
two sides and at one end, by a slight fold, and whose other end forms part
of the edge of the blastoderm. The end of the embryo which points towards
the _centre_ of the blastoderm is the head end, and that which forms part
of the _edge_ of the blastoderm is the tail end. To retain the nomenclature
usually adopted in treating of the development of the Bird, the fold at the
anterior end of the embryo may be called _the head fold_, and those at the
sides the _side folds_. There is in Elasmobranchii no tail fold, owing to
the position of the embryo at the periphery of the blastoderm, and it is by
the meeting of the three above-mentioned folds only, that the embryo
becomes pinched off from the remainder of the blastoderm. Along the median
line of the embryo is a shallow groove (_m.g._), the well-known medullary
groove of vertebrate embryology. It flattens out both anteriorly and
posteriorly, and is deepest in the middle part of its course.
C.
This embryo resembles in most of its features the embryo last described. It
is, however, considerably larger, and the head fold and side folds have
become more pronounced structures. The medullary groove is far deeper than
in the earlier stage, and widens out anteriorly. This anterior widening is
the first indication of a distinction between the brain and the remainder
of the central nervous system, a distinction which arises long before the
closure of the medullary canal.
D.
This embryo is far larger than the one last described, but the increase in
length does not cause it to project beyond the edge of the blastoderm, but
has been due to a growth inwards towards the centre of the blastoderm. The
head is now indicated by an anterior enlargement, and the embryo also
widens out posteriorly. The posterior widening (_t.s._) is formed by a pair
of rounded prominences, one on each side of the middle line. These are very
conspicuous organs during the earlier stages of development, and consist of
two large aggregations of mesoblast cells. In accordance with the
nomenclature adopted in my preliminary paper[177], they may be called
'tail-swellings'. Between the cephalic enlargements and the tail-swellings
is situated the rudimentary trunk of the embryo. It is more completely
pinched off from the blastoderm than in the last described embryo. The
medullary groove is of a fairly uniform size throughout the trunk of the
embryo, but flattens out and vanishes completely in the region of the head.
The blastoderm in Pristiurus and Scyllium grows very rapidly, and has by
this stage attained a very considerable size; but in Torpedo its growth is
very slow.
Footnote 177: _Quart. Journ. Micr. Science_, Oct. 1874. [This
Edition, No. V.]
E and F.
These two embryos may be considered together, for, although they differ in
appearance, yet they are of an almost identical age; and the differences
between the two are purely external. E appears to be a little abnormal in
not having the cephalic region so distinctly marked off from the trunk as
is usual. The head is proportionally larger than in the last stage, and the
tail-swellings remain as conspicuous as before. The folding off from the
blastoderm has progressed rapidly, and the head and tail are quite
separated from it. The medullary groove has become closed posteriorly in
both embryos, but the closing has extended further forwards in F than in E.
In F the medullary folds have not only united posteriorly, but have very
nearly effected a fresh junction in the region of the neck. At this point a
second junction of the two medullary folds is in fact actually effected
before the posterior closing has extended forwards so far. The later
junction in the region of the neck corresponds in position with the point,
where in the Bird the medullary folds first unite. No trace of a medullary
groove is to be met with in the head, which simply consists of a wide
flattened plate. Between the two tail-swellings surface views present the
appearance of a groove, but this appearance is deceptive, since in sections
no groove, or at most a very slight one, is perceptible.
G.
During the preceding stages growth in the embryo is very slow, and
considerable intervals of time elapse before any perceptible changes are
effected. This state of things now becomes altered, and the future changes
succeed each other with far greater rapidity. One of the most important of
these, and one which first presents itself during this stage, is the
disappearance of the yolk-spherules from the embryonic cells, and the
consequently increased transparency of the embryo. As a result of this, a
number of organs, which in the earlier stages were only to be investigated
by means of sections, now become visible in the living embryo.
The tail-swellings (_t.s._) are still conspicuous objects at the posterior
extremity of the embryo. The folding off of the embryo from the yolk has
progressed to such an extent that it is now quite possible to place the
embryo on its side and examine it from that point of view.
The embryo may be said to be attached to the yolk by a distinct stalk or
cord, which in the succeeding stages gradually narrows and elongates, and
is known as the umbilical cord (_so.s._). The medullary canal has now
become completely closed, even in the region of the brain, where during the
last stage no trace of a medullary groove had appeared. Slight
constrictions, not perceptible in views of the embryo as a transparent
object, mark off three vesicles in the brain. These vesicles are known as
the fore, mid, and hind brain. From the fore-brain there is an outgrowth on
each side, the first rudiment of the optic vesicle (_op._).
The mesoblast on each side of the body is divided into a series of
segments, known as protovertebræ or muscle-plates, the first of which lies
a little behind the head. The mesoblast of the tail has not as yet
undergone this segmentation. There are present in all seventeen segments.
These first appeared at a much earlier date, but were not visible owing to
the opacity of the embryo.
Another structure which became developed in even a younger embryo than C is
now for the first time visible in the living embryo. This is the notochord:
it extends from almost the extreme posterior to the anterior end of the
embryo. It lies between the ventral wall of the spinal canal and the dorsal
wall of the intestine; and round its posterior end these two walls become
continuous with each other (vide fig.). Anteriorly the termination of the
notochord cannot be seen, it can only be traced into a mass of mesoblast at
the base of the brain, which there separates the epiblast from the
hypoblast. The alimentary canal (_al._) is completely closed anteriorly and
posteriorly, though still widely open to the yolk-sac in the middle part of
its course. In the region of the head it exhibits on each side a slight
bulging outwards, the rudiment of the first visceral cleft. This is
represented in the figure by two lines (I _v.c._). The visceral clefts at
this stage consist of a pair of simple diverticula from the alimentary
canal, and there is no communication between the throat and the exterior.
H.
The present embryo is far larger than the last, but it has not been
possible to represent this increase in size in the drawings. Accompanying
this increase in size, the folding off of the embryo from the yolk has
considerably progressed, and the stalk which unites the embryo with the
yolk is proportionately narrower and longer than before.
The brain is now very distinctly divided into the three lobes, whose
rudiments appeared during the last stage. From the foremost of these, the
optic vesicles now present themselves as well-marked lateral outgrowths,
towards which there appears a growing in, or involution, from the external
skin (_op._) to form the lens. The opening of this involution is
represented by the dark spot in the centre.
A fresh organ of sense, the auditory sac, now for the first time becomes
visible as a shallow pit in the external skin on each side of the
hind-brain (_au.v._). The epiblast which is involuted to form this pit
becomes much thickened, and thereby the opacity, indicated in the figure,
is produced.
The muscle-plates have greatly increased in number by the formation of
fresh segments in the tail. Thirty-eight of them were present in the embryo
figured. The mesoblast at the base of the brain has increased in quantity,
and there is still a certain mass of unsegmented mesoblast which forms the
tail-swellings. The first rudiment of the heart becomes visible during this
stage as a cavity between the mesoblast of the splanchnopleure and the
hypoblast (_ht._).
The fore and hind guts are now longer than they were. A slight pushing in
from the exterior to form the mouth has appeared (_m._), and an indication
of the future position of the anus is afforded by a slight diverticulum of
the hind gut towards the exterior some little distance from the posterior
end of the embryo (_an._). The portion of the alimentary canal behind this
point, though at this stage large, and even dilated into a vesicle at its
posterior end (_al.v._), becomes eventually completely atrophied. In the
region of the throat the rudiment of a second visceral cleft has appeared
behind the first; neither of them are as yet open to the exterior. The
number of visceral clefts present in any given Pristiurus embryo affords a
very easy and simple way of determining its age.
I.
A great increase in size is again to be noticed in the embryo, but, as in
the case of the last embryo, it has not been possible to represent this in
the figure. The stalk connecting the embryo with the yolk has become
narrower and more elongated, and the tail region of the embryo
proportionately far longer than in the last stage. During this stage the
first spontaneous movements of the embryo take place, and consist in
somewhat rapid excursions of the embryo from side to side, produced by a
serpentine motion of the body.
The cranial flexure, which commenced in stage G, has now become very
evident, and the mid-brain[178] begins to project in the same manner as in
the embryo fowl on the third day, and will soon form the anterior
termination of the long axis of the embryo. The fore-brain has increased in
size and distinctness, and the anterior part of it may now be looked on as
the unpaired rudiment of the cerebral hemispheres.
Footnote 178: The part of the brain which I have here called
mid-brain, and which unquestionably corresponds to the part
called mid-brain in the embryos of higher vertebrates, becomes
in the adult what Miklucho-Maclay and Gegenbaur called the
vesicle of the third ventricle or thalamencephalon. I shall
always speak of it as the mid-brain.
Further growths have taken place in the organs of sense, especially in the
eye, in which the involution for the lens has made considerable progress.
The number of the muscle-plates has again increased, but there is still a
region of unsegmented mesoblast in the tail. The thickened portions of
mesoblast which caused the tail-swellings are still to be seen and would
seem to act as the reserve from which is drawn the matter for the rapid
growth of the tail, which occurs soon after this. The mass of the mesoblast
at the base of the brain has again increased. No fresh features of interest
are to be seen in the notochord. The heart is now much more conspicuous
than before, and its commencing flexure is very apparent. It now beats
actively. The hind gut especially is much longer than in the last specimen;
and the point where the anus will appear is very easily detected by the
bulging out of the gut towards the external skin at that point (_an._). The
alimentary vesicle, first observable during the last stage, is now a more
conspicuous organ (_al.v._). Three visceral clefts, none of which are as
yet open to the exterior, may now be seen.
K.
The figures G, H, I are representations of living and transparent embryos,
but the remainder of the figures are drawings of opaque embryos which were
hardened in chromic acid.
The stalk connecting the embryo with the yolk is now, comparatively
speaking, quite narrow, and is of sufficient length to permit the embryo to
execute considerable movements.
The tail has grown immensely, but is still dilated terminally. This
terminal dilatation is mainly due to the alimentary vesicle, but the tract
of gut connecting this with the gut in front of the anus is now a solid rod
of cells and very soon becomes completely atrophied.
The two pairs of limbs have appeared as elongated ridges of epiblast. The
anterior pair is situated just at the front end of the umbilical stalk; and
the posterior pair, which is the more conspicuous of the two, is situated
some little distance behind the stalk.
The cranial flexure has greatly increased, and the angle between the long
axis of the front part of the head and of the body is less than a right
angle. The conspicuous mid-brain forms the anterior termination of the long
axis of the body. The thin roof of the fourth ventricle may in the figure
be noticed behind the mid-brain. The auditory sac is nearly closed and its
opening is not shewn in the figure. In the eye the lens is completely
formed.
Owing to the opacity of the embryo, the muscle-plates are only indistinctly
indicated, and no other features of the mesoblast are to be seen.
The mouth is now a deep pit, whose borders are almost completely formed by
the thickening in front of the first visceral cleft, which may be called
the first visceral arch or mandibular arch.
Four visceral clefts are now visible, all of which are open to the
exterior, but in a transparent embryo one more, not open to the exterior,
would have been visible behind the last of these.
L.
This embryo is considerably older than the one last described, but growth
is not quite so rapid as might be gathered from the fact that L is nearly
twice as long as K, since the two embryos belong to different genera; and
the Scyllium embryos, of which L is an example, are larger than Pristiurus
embryos. The umbilical stalk is now quite a narrow elongated structure,
whose subsequent external changes are very unimportant, and consist for the
most part merely in an increase in its length.
The tail has again grown greatly in length, and its terminal dilatation
together with the alimentary vesicle contained in it, have both completely
vanished. A dorsal and ventral fin are now clearly visible; they are
continuous throughout their whole length. The limbs have grown and are more
easily seen than in the previous stage.
Great changes have been effected in the head, resulting in a diminution of
the cranial flexure. This diminution is nevertheless apparent rather than
real, and is chiefly due to the rapid growth of the rudiment of the
cerebral hemispheres. The three main divisions of the brain may still be
clearly seen from the surface. Posteriorly is situated the hind-brain, now
consisting of the medulla oblongata and cerebellum. At the anterior part of
the medulla is to be seen the thin roof of the fourth ventricle, and
anteriorly to this again the roof becomes thickened to form the rudiment of
the cerebellum. In front of the hind-brain lies the mid-brain, the roof of
which is formed by the optic lobes, which are still situated at the front
end of the long axis of the embryo.
Beyond the mid-brain is placed the fore-brain, whose growth is rapidly
rendering the cranial flexure imperceptible.
The rudiments of the nasal sacs are now clearly visible as a pair of small
pits. The pits are widely open to the exterior, and are situated one on
each side, near the front end of the cerebral hemispheres. Five visceral
clefts are open to the exterior, and in them the external gills have
commenced to appear (L´).
The first cleft is no longer similar to the rest, but has commenced to be
metamorphosed into the spiracle.
Accompanying the change in position of the first cleft, the mandibular arch
has begun to bend round and enclose the front as well as the side of the
mouth. By this change in the mandibular arch the mouth becomes narrowed in
an antero-posterior direction.
M.
Of this embryo the head alone has been represented. Two views of it are
given, one (M) from the side and the other (M´) from the under surface. The
growth of the front part of the head has considerably diminished the
prominence of the cranial flexure. The full complement of visceral clefts
is now present--six in all. But the first has already atrophied
considerably, and may easily be recognized as the spiracle. In Scyllium,
there are present at no period more than six visceral clefts. The first
visceral arch on each side has become bent still further round, to form the
front border of the mouth. The opening of the mouth has in consequence
become still more narrowed in an antero-posterior direction. The width of
the mouth in this direction, serves for the present and for some of the
subsequent stages as a very convenient indication of age.
N.
The limbs, or paired fins, have now acquired the general features and form
which they possess in the adult.
The unpaired fins have now also become divided in a manner not only
characteristic of the Elasmobranchii but even of the genus Scyllium.
There is a tail fin, an anal fin and two dorsal fins, both the latter being
situated behind the posterior paired fins.
In the head may be noticed a continuation of the rapid growth of the
anterior part.
The mouth has become far more narrow and slit-like; and with many other of
the organs of the period commences to approach the form of the adult.
The present and the three preceding stages shew the gradual changes by
which the first visceral arch becomes converted into the rudiments of the
upper and of the lower jaw. The fact of the conversion was first made known
through the investigations of Messrs Parker and Gegenbaur.
O.
In this stage the embryo is very rapidly approaching the form of the adult.
This is especially noticeable in the fins, which project in a manner quite
characteristic of the adult fish. The mouth is slit-like, and the openings
of the nasal sacs no longer retain their primitive circular outline. The
external gills project from all the gill-slits including the spiracle.
P.
The head is rapidly elongating by the growth of the snout, and the
divisions of the brain can no longer be seen with distinctness from the
exterior, and, with the exception of the head and of the external gills,
the embryo almost completely resembles the adult.
Q.
The snout has grown to such an extent, that the head has nearly acquired
its adult shape. In the form of its mouth the embryo now quite resembles
the adult fish.
* * * * *
This part of the subject may be conveniently supplemented by a short
description of the manner in which the blastoderm encloses the yolk. It has
been already mentioned that the growth of the blastoderm is not uniform.
The part of it in the immediate neighbourhood of the embryo remains
comparatively stationary, while the growth elsewhere is very rapid. From
this it results that that part of the edge of the blastoderm where the
embryo is attached forms a bay in the otherwise regular outline of the edge
of the blastoderm. By the time that one-half of the yolk is enclosed the
bay is a very conspicuous feature (Pl. 9, fig. 1). In this figure _bl._
points to the blastoderm, and _yk._ to the part of the yolk not yet
enclosed by the blastoderm.
Shortly subsequent to this the bay becomes obliterated by its two sides
coming together and coalescing, and the embryo ceases to lie at the edge of
the yolk.
This stage is represented on Pl. 9, fig. 2. In this figure there is only a
small patch of yolk not yet enclosed (_yk_), which is situated at some
little distance behind the embryo. Throughout all this period the edge of
the blastoderm has remained thickened, a feature which persists till the
complete investment of the yolk, which takes place shortly after the stage
last figured. In this thickened edge a circular vein arises, which brings
back the blood from the yolk-sac to the embryo. The opening in the
blastoderm (Pl. 9, fig. 2, _yk._), exposing the portion of the yolk not yet
enclosed, may be conveniently called the blastopore, according to Professor
Lankester's nomenclature.
The interesting feature which characterizes the blastopore in
Elasmobranchii is the fact of its not corresponding in position with the
opening of the anus of Rusconi. We thus have in Elasmobranchii two
structures, each of which corresponds in part with the single structure in
Amphioxus which may be called either blastopore or anus of Rusconi, which
yet do not in Elasmobranchii coincide in position. It is the blastopore of
Elasmobranchii which has undergone a change of position, owing to the
unequal growth of the blastoderm; while the anus of Rusconi retains its
normal situation. In Osseous Fishes the blastopore undergoes a similar
change of position. The possibility of a change in position of this
structure is peculiarly interesting, in that it possibly serves to explain
how the blastopore of different animals corresponds in different cases with
the anus or the mouth, and has not always a fixed situation[179].
Footnote 179: For a fuller discussion of this question vide
Self, "A comparison of the early stages of development in
vertebrates." _Quart. Journ. of Micr. Science_, July, 1875.
[This Edition, No. VI.]
EXPLANATION OF PLATES 8 and 9.
COMPLETE LIST OF REFERENCE LETTERS.
_a._ Arteries of yolk sac (red). _al._ Alimentary cavity. _alv._ Alimentary
vesicle at the posterior end of the alimentary canal. _an._ Point where
anus will appear. _auv._ Auditory vesicle. _bl._ Blastoderm. _ch._
Notochord. _es._ Embryo-swelling. _h._ Head. _ht._ Heart. _m._ Mouth. _mg._
Medullary groove. _mp._ Muscle-plate or protovertebra. _op._ Eye. _sc._
Segmentation cavity. _sos._ Somatic stalk. _ts._ Tail-swelling. _v._ Veins
of yolk sac (blue). _vc._ Visceral cleft. I. _vc._ 1st visceral cleft. _x._
Portion of blastoderm outside the arterial circle in which no blood-vessels
are present. _yk._ Yolk.
PLATE 8.
Fig. A. Surface view of blastoderm of Pristiurus hardened in chromic acid.
Fig. B. Surface view of fresh blastoderm of Pristiurus.
Figs. C, D, E, and F. Pristiurus embryos hardened in chromic acid.
Fig. G. Torpedo embryo viewed as a transparent object.
Figs. H, I. Pristiurus embryos viewed as transparent objects.
Fig. K. Pristiurus embryo hardened in chromic acid.
The remainder of the figures are representations of embryos of Scyllium
canicula hardened in chromic acid. In every case, with the exception of the
figures marked P and Q, two representations of the same embryo are given;
one from the side and one from the under surface.
PLATE 9.
Fig. 1. Yolk of a Pristiurus egg with blastoderm and embryo. About
two-thirds of the yolk have been enveloped by the blastoderm. The embryo is
still situated at the edge of the blastoderm, but at the end of a bay in
the outline of this. The thickened edge of the blastoderm is indicated by a
darker shading. Two arteries have appeared.
Fig. 2. Yolk of an older Pristiurus egg. The yolk has become all but
enveloped by the blastoderm, and the embryo ceases to lie at the edge of
the blastoderm, owing to the coalescence of the two sides of the bay which
existed in the earlier stage. The circulation is now largely developed. It
consists of an external arterial ring, and an internal venous ring, the
latter having been developed in the thickened edge of the blastoderm.
Outside the arterial ring no vessels are developed.
Fig. 3. The yolk has now become completely enveloped by the blastoderm. The
arterial ring has increased in size. The venous ring has vanished, owing to
the complete enclosure of the yolk by the blastoderm. The point where it
existed is still indicated (_y_) by the brush-like termination of the main
venous trunk in a number of small branches.
Fig. 4. Diagrammatic projection of the vascular system of the yolk sac of a
somewhat older embryo.
The arterial ring has grown much larger and the portion of the yolk where
no vessels exist is very small (_x_). The brush-like termination of the
venous trunk is still to be noticed.
The two main trunks (arterial and venous) in reality are in close contact
as in fig. 5, and enter the somatic stalk close together.
The letter _a_ which points to the venous (blue) trunk should be _v_ and
not _a_.
Fig. 5. Circulation of the yolk sac of a still older embryo, in which the
arterial circle has ceased to exist, owing to the space outside it having
become smaller and smaller and finally vanished.
CHAPTER V.
STAGES B TO G.
The present chapter deals with the history of the development of the
Elasmobranch embryo from the period when the medullary groove first arises
till that in which it becomes completely closed, and converted into the
medullary canal. The majority of the observations recorded were made on
Pristiurus embryos, a few on embryos of Torpedo. Where nothing is said to
the contrary the statements made apply to the embryos of Pristiurus only.
The general external features for this period have already been given in
sufficient detail in the last chapter; and I proceed at once to describe
consecutively the history of the three layers.
_General Features of the Epiblast._
At the commencement of this period, during the stage intermediate between B
and C, the epiblast is composed of a single layer of cells. (Pl. 10,
fig. 1.)
These are very much elongated in the region of the embryo, but flattened in
other parts of the blastoderm. Throughout they contain numerous
yolk-spherules.
In a Torpedo embryo of this age (as determined by the condition of the
notochord) the epiblast presents a very different structure. It is composed
of small spindle-shaped cells several rows deep. The nuclei of these are
very large in proportion to the cells containing them, and the
yolk-spherules are far less numerous than in the cells of corresponding
Pristiurus embryos.
During stage C the condition of the epiblast does not undergo any important
change, with the exception of the layer becoming much thickened, and its
cells two or three deep in the anterior parts of the embryo. (Pl. 10,
fig. 2.)
In the succeeding stages that part of the epiblast, which will form the
spinal cord, gradually becomes two or three cells deep. This change is
effected by a decrease in the length of the cells as compared with the
thickness of the layer. In the earlier stages the cells are wedge-shaped
with an alternate arrangement, so that a decrement in the length of the
cells at once causes the epiblast to be composed of two rows of
interlocking cells.
The lateral parts of the epiblast which form the epidermis of the embryo
are modified in quite a different manner to the nervous parts of the layer,
becoming very much diminished in thickness and composed of a single row of
flattened cells. (Pl. 10, fig. 3.)
Till the end of stage F, the epiblast cells and indeed all the cells of the
blastoderm retain their yolk-spherules, but the epiblast begins to lose
them and consequently to become transparent in stage G.
_Medullary Groove._
During stage B the medullary groove is shallow posteriorly, deeper in the
middle part, and flattened out again at the extreme anterior end of the
embryo. (Pl. 7, fig. 10_a_, _b_, _c_.)
A similar condition obtains in the stage between B and C, but the canal has
now in part become deeper. Anteriorly no trace of it is to be seen. In
stage C it exhibits the same general features. (Pl. 10, fig. 2_a_, 2_b_,
2_c_.)
By stage D we find important modifications of the canal.
It is still shallow behind and deep in the dorsal region, Pl. 10, figs.
3_d_, 3_e_, 3_f_; but the anterior flattened area in the last stage has
grown into a round flat plate which may be called the cephalic plate,
Pl. 8, D and Pl. 10, figs. 3_a_, 3_b_, 3_c_. This plate becomes converted
into the brain. Its size and form give it a peculiar appearance, but the
most remarkable feature about it is the ventral curvature of its edges. Its
edges do not, as might be expected, bend dorsalwards towards each other,
but become sharply bent in a ventral direction. This feature is for the
first time apparent at this stage, but becomes more conspicuous during the
succeeding ones, and attains its maximum in stage F (Pl. 10, fig. 5), in
which it might almost be supposed that the edges of the cephalic plate were
about to grow downwards and meet on the ventral side of the embryo.
In the stages subsequent to D the posterior part of the canal deepens much
more rapidly than the rest (vide Pl. 10, fig. 4, taken from the posterior
end of an embryo but slightly younger than F), and the medullary folds
unite and convert the posterior end of the medullary groove into a closed
canal (Pl. 8, fig. F), while the groove is still widely open
elsewhere[180]. The medullary canal does not end blindly behind, but simply
forms a tube not closed at either extremity. The importance of this fact
will appear later.
Footnote 180: Vide Preliminary Account, etc. _Q. Jl. Micros.
Science_, Oct. 1874, Pl. 14, 8_a_. [This Edition, No. V. Pl. 3,
8_a_.] This and the other section from the same embryo (stage
F) may be referred to. I have not thought it worth while
repeating them here.
In a stage but slightly subsequent to F nearly the whole of the medullary
canal becomes formed. This occurs in the usual way by the junction and
coalescence of the medullary folds. In the course of the closing of the
medullary groove the edges of the cephalic plate lose their ventral
curvature and become bent up in the normal manner (vide Pl. 10, fig. 6, a
section taken through the posterior part of the cephalic plate), and the
enlarged plate merely serves to enclose a dilated cephalic portion of the
medullary canal. The closing of the medullary canal takes place earlier in
the head and neck than in the back. The anterior end of the canal becomes
closed and does not remain open like the posterior end.
Elasmobranch embryos resemble those of the Sturgeon (Acipenser) and the
Amphibians in the possession of a spatula-like cephalic expansion: but so
far as I am aware a ventral flexure in the medullary plates of the head has
not been observed in other groups.
The medullary canal in Elasmobranchii is formed precisely on the type so
well recognised for all groups of vertebrates with the exception of the
Osseous Fishes. The only feature in any respect peculiar to these fishes is
the closing of their medullary canal first commencing behind, and then at a
second point in the cervical region. In those vertebrates in which the
medullary folds do not unite at approximately the same time throughout
their length, they appear usually to do so first in the region of the neck.
_Mesoblast._
The separation from the hypoblast of two lateral masses of mesoblast has
already been described. Till the close of stage C the mesoblast retains its
primitive bilateral condition unaltered. Throughout the whole length of the
embryo, with the exception of the extreme front part, there are present two
plates of rounded mesoblast cells, one on each side of the medullary
groove. These plates are in very close contact with the hypoblast, and also
follow with fair accuracy the outline of the epiblast. This relation of the
mesoblast plates to the epiblast must not however be supposed to indicate
that the medullary groove is due to growth in the mesoblast: a view which
is absolutely negatived by the manner of formation of the medullary groove
in the head. Anteriorly the mesoblast plates thin out and completely
vanish.
In stage D, the plates of mesoblast in the trunk undergo important changes.
The cells composing them become arranged in two layers (Pl. 10, fig. 3), a
splanchnic layer adjoining the hypoblast (_sp_), and a somatic layer
adjoining the epiblast[181] (_so_). Although these two layers are
distinctly formed, they do not become separated at this stage in the region
of the trunk, and in the trunk no true body-cavity is formed.
Footnote 181: I underestimated the distinctness of this
formation in my earlier paper, _loc. cit._, although I
recognised the fact that the mesoblast cells became arranged in
two distinct layers.
By stage D the plates of mesoblast have ceased to be quite isolated, and
are connected with the lower layer cells of the general blastoderm.
Moreover the lower layer cells outside the embryo now exhibit distinct
traces of a separation into two layers, one continuous with the hypoblast,
the other with the mesoblast. Both layers are composed of very flattened
cells, and the mesoblast layer is often more than one cell deep, and
sometimes exhibits a mesh-like arrangement of its elements.
Coincidentally with the appearance of a differentiation into a somatic and
splanchnic layer the mesoblast plates become partially split by a series of
transverse lines of division into protovertebræ. Only the proximal regions
of the plates become split in this way, while their peripheral parts remain
quite intact. As a result of this each plate becomes divided into a
proximal portion adjoining the medullary canal, which is divided into
_protovertebræ_, and may be called the _vertebral plate_, and a peripheral
portion not so divided, which may be called the _lateral plate_. These two
parts are at this stage quite continuous with each other; and, as will be
seen in the sequel, the body-cavity originally extends uninterruptedly to
the summit of the vertebral plates.
By stage D at the least ten protovertebræ have appeared.
In Torpedo the mesoblast commences to be divided into two layers much
earlier than in Pristiurus; and even before stage C this division is more
or less clearly marked.
In the head and tail the condition of the mesoblast is by no means the same
as in the body.
In the tail the plates of mesoblast become considerably thickened and give
rise to two projections, one on each side, which have already been alluded
to as caudal or tail-swellings; vide Pl. 8, figs. D, F, and Pl. 10,
fig. 3_f_ and fig. 4, _ts_.
These masses of mesoblast are neither divided into protovertebræ, nor do
they exhibit any trace of a commencing differentiation into somatopleure
and splanchnopleure.
In the head, so far as I have yet been able to observe, the mesoblastic
plates do _not_ at this stage become divided into protovertebræ. The other
changes exhibited in the cephalic region are of interest, mainly from the
fact that here appears a cavity in the mesoblast directly continuous with
the body-cavity (when that cavity becomes formed), but which appears at a
very much earlier date than the body-cavity. This cavity can only be looked
on in the light of a direct continuation of the body or peritoneal cavity
into the head. Theoretical considerations with reference to it I propose
reserving till I have described the changes which it undergoes in the
subsequent periods.
Pl. 10, figs. 3_a_, 3_b_ and 3_c_ exhibit very well the condition of the
mesoblast in the head at this period. In fig. 3_c_, a section taken through
the back part of the head, the mesoblast plates have nearly the same form
as in the sections immediately behind. The ventral continuation of the
mesoblast formed by the lateral plate has, however, become much thinner,
and the dorsal or vertebral portion has acquired a more triangular form
than in the sections through the trunk (figs. 3_d_ and 3_e_).
In the section (fig. 3_b_) in front of this the ventral portion of the
plate is no longer present, and only that part exists which corresponds
with the vertebral division of the primitive plate of mesoblast.
In this a distinct cavity, forming part of the body-cavity, has appeared.
In a still anterior section (fig. 3_a_) no cavity is any longer present in
the mesoblast; whilst in sections taken from the foremost part of the head
no mesoblast is to be seen (vide Pl. 10, fig. 5, taken from the front part
of the head of the embryo represented in Pl. 8, fig. F).
A continuation of the body-cavity into the head has already been described
by Oellacher[182] for the Trout: but he believes that the cavity in this
part is solely related to the formation of the pericardial space.
Footnote 182: _Zeitschrift f. wiss. Zoologie_, 1873.
The condition of the mesoblast undergoes no important change till the end
of the period treated of in this chapter. The masses of mesoblast which
form the tail-swellings become more conspicuous (Pl. 10, fig. 4); and
indeed their convexity is so great that the space between them has the
appearance of a median groove, even after the closure of the neural canal
in the caudal region.
In embryos of stage G, which may be considered to belong to the close of
this period, eighteen protovertebræ are present both in Pristiurus and
Torpedo embryos.
_The Alimentary Canal._
The alimentary canal at the commencement of this period (stage B) forms a
space between the embryo and the yolk, ending blindly in front, but opening
posteriorly by a widish slit-like aperture, which corresponds to the anus
of Rusconi (Pl. 7, fig. 7).
The cavity anteriorly has a more or less definite form, having lateral
walls, as well as a roof and floor (Pl. 7, figs. 10_b_ and 10_c_).
Posteriorly it is not nearly so definitely enclosed (Pl. 7, fig. 10_a_).
The ventral wall of the cavity is formed by yolk. But even in stage B there
are beginnings of a cellular ventral wall derived from an ingrowth of cells
from the two sides.
By stage C considerable progress has been made in the formation of the
alimentary canal. Posteriorly it is as flattened and indefinite as during
stage B (Pl. 10, figs. 2_b_ and 2_c_). But in the anterior part of the
embryo the cavity becomes much deeper and narrower, and a floor of cells
begins to be formed for it (Pl. 10, fig. 2); and, finally, in front, it
forms a definite space completely closed in on all sides by cells (Pl. 10,
fig. 2_a_). Two distinct processes are concerned in effecting these changes
in the condition of the alimentary cavity. One of these is a process of
folding off the embryo from the blastoderm. The other is a simple growth of
cells independent of any folding. To the first of these processes the depth
and narrowness of the alimentary cavity is due; the second is concerned in
forming its ventral wall. The combination of the two processes produces the
peculiar triangular section which characterises the anterior closed end of
the alimentary cavity at this stage. The process of the folding off of the
embryo from the blastoderm resembles exactly the similar process in the
embryo bird. The fold by which the constricting off of the embryo is
effected is a perfectly continuous one, but may be conveniently spoken of
as composed of a head fold and two lateral folds.
Of far greater interest than the nature of these folds is the formation of
the ventral wall of the alimentary canal. This, as has been said, is
effected by a growth of cells from the two sides to the middle line
(Pl. 10, fig. 2). The cells for this are however not derived from
pre-existing hypoblast cells, but are formed spontaneously around nuclei of
the yolk. This fact can be determined in a large number of sections, and is
fairly well shewn in Pl. 10, fig. 2, _na_. The cells are formed in the
yolk, as has been already mentioned, by a simple aggregation of protoplasm
around pre-existing nuclei.
The cells being described are in most cases formed close to the
pre-existing hypoblast cells, but often require to undergo a considerable
change of position before attaining their final situation in the wall of
the alimentary canal.
I have already alluded to this feature in the formation of the ventral wall
of the alimentary cavity. Its interest, as bearing on the homology of the
yolk, is considerable, owing to the fact that the so-called yolk-cells of
Amphibians play a similar part in supplying the ventral epithelium of the
alimentary cavity, as do the cells derived from the yolk in Elasmobranchii.
The fact of this feature being common to the yolk-cells of Amphibians and
the yolk of Elasmobranchii, supplies a strong argument in favour of the
homology of the yolk-cells in the one case with the yolk in the other[183].
Footnote 183: Nearly simultaneously with Chapter III. of the
present monograph on the Development of Elasmobranchii, which
dealt in a fairly complete manner with the genesis of cells
outside the blastoderm, there appeared two important papers
dealing with the same subject for Teleostei. One of these, by
Professor Bambeke, "Embryologie des Poissons Osseux," _Mém.
Cour. Acad. Belgique_, 1875, which appeared some little time
before my paper, and a second by Dr Klein, _Quart. Jour. of
Micr. Sci._ April, 1876. In both of these papers a development
of nuclei and of cells is described as occurring outside the
blastoderm in a manner which accords fairly well with my own
observations.
The conclusions of both these investigators differ however from
my own. They regard the finely granular matter, in which the
nuclei appear, as pertaining to the blastoderm, and
morphologically quite distinct from the yolk. From their
observations we can clearly recognise that the material in
which the nuclei appear is far more sharply separated off from
the yolk in Osseous Fish than in Elasmobranchii, and this sharp
separation forms the main argument for the view of these
authors. Dr Klein admits, however, that this granular matter
(which he calls parablast) graduates into the typical
food-yolk, though he explains this by supposing that the
parablast takes up part of the yolk for the purpose of growth.
It is clear that the argument from a sharp separation of yolk
and parablast cannot have much importance, when it is admitted
(1) that in Osseous Fish there is a gradation between the two
substances, while (2) in Elasmobranchii the one merges slowly
and insensibly into the other.
The only other argument used by these authors is stated by Dr
Klein in the following way. "The fact that the parablast has,
at the outset, been forming one unit with what represents the
archiblast, and, _while increasing has spread_ i.e. _grown over
the yolk_ which underlies the segmentation-cavity, is, I think,
the most absolute proof that the yolk is as much different from
the parablast as it is from the archiblast." This argument to
me merely demonstrates that certain of the nutritive elements
of the yolk become in the course of development converted into
protoplasm, a phenomenon which must necessarily be supposed to
take place on my own as well as on Dr Klein's view of the
nature of the yolk. My own views on the subject have already
been fully stated. I regard the so-called yolk as composed of a
larger or smaller amount of food-material imbedded in
protoplasm, and the meroblastic ovum as a body constituted of
the same essential parts as a holoblastic ovum, though divided
into regions which differ in the proportion of protoplasm they
contain. I do not propose to repeat the positive arguments used
by me in favour of this view, but content myself with alluding
to the protoplasmic network found by Schultz and myself
extending through the whole yolk, and to the similar network
described by Bambeke as being present in the eggs of Osseous
Fish after deposition but before impregnation. The existence of
these networks is to me a conclusive proof of the correctness
of my views. I admit that in Teleostei the 'parablast' contains
more protoplasm than the homologous material in the
Elasmobranch ovum, while it is probable that after impregnation
the true yolk of Teleostei contains little or no protoplasm;
but these facts do not appear to me to militate against my
views.
I agree with Prof. Bambeke in regarding the cells derived from
the sub-germinal matter as homologous with the so-called
yolk-cells of the Amphibian embryo.
I have recently, in some of the later stages of development,
met with very peculiar nuclei of the yolk immediately beneath
the blastoderm at some little distance from the embryo, Pl. 10,
fig. 8. They were situated not in finely sub-germinal matter,
but amongst large yolk-spherules. They were very large, and
presented still more peculiar forms than those already
described by me, being produced into numerous long filiform
processes. The processes from the various nuclei were sometimes
united together, forming a regular network of nuclei quite
unlike anything that I have previously seen described.
The sub-germinal matter, in which the nuclei are usually
formed, becomes during the later stages of development far
richer in protoplasm than during the earlier. It continually
arises at fresh points, and often attains to considerable
dimensions, no doubt by feeding on yolk-spherules. Its
development appears to be determined by the necessities of
growth in the blastoderm or embryo.
The history of the alimentary canal during the remainder of this period may
be told briefly.
The folding off and closing of the alimentary canal in the anterior part of
the body proceeds rapidly, and by stage D not only is a considerable tract
of alimentary canal formed, but a great part of the head is completely
folded off from the yolk (Pl. 10, fig. 3_a_). By stage F a still greater
part is folded off. The posterior part of the alimentary canal retains for
a long period its primitive condition. It is not until stage F that it
begins to be folded off behind. After the folding has once commenced it
proceeds with great rapidity, and before stage G the hinder part of the
alimentary canal becomes completely closed in.
The folding in of the gut is produced by two lateral folds, and the gut is
not closed posteriorly.
It may be remembered that the neural canal also remained open behind. Thus
both the neural and alimentary canals are open behind; and, since both of
them extend to the posterior end of the body, they meet there, their walls
coalesce, and a direct communication from the neural to the alimentary
canal is instituted. The process may be described in another way by saying
that the medullary folds are continuous round the end of the tail with the
lateral walls of the alimentary canal; so that, when the medullary folds
unite to form a canal, this canal becomes continuous with the alimentary
canal, which is closed in at the same time. In whatever way this
arrangement is produced, the result of it is that it becomes possible to
pass in a continuously closed passage along the neural canal round the end
of the tail and into the alimentary canal. A longitudinal section shewing
this feature is represented on Pl. 10, fig. 7.
This communication between the neural and alimentary canals, which is
coupled, as will be seen in the sequel, with the atrophy of a posterior
segment of the alimentary canal, is a feature of great interest which ought
to throw considerable light upon the meaning of the neural canal. So far as
I know, no suggestion as to the origin of it has yet been made. It is by no
means confined to Elasmobranchii, but is present in all the vertebrates
whose embryos are situated at the centre and not at the periphery of the
blastoderm. It has been described by Goette[184] in Amphibians and by
Kowalevsky, Owsjannikow and Wagner[185] in the Sturgeon (Acipenser). The
same arrangement is also stated by Kowalevsky[186] to exist in Osseous
Fishes and Amphioxus. The same investigator has shewn that the alimentary
and neural canals communicate in larval Ascidians, and we may feel almost
sure that they do so in the Marsipobranchii.
Footnote 184: _Entwicklungsgeschichte der Unke._
Footnote 185: _Mélanges Biologiques de l'Académie
Pétersbourg_, Tome VII.
Footnote 186: _Archiv. f. mikros. Anat._ Vol. VII. p. 114. In
the passage on this point Kowalevsky states that in
Elasmobranchii the neural and alimentary canals communicate.
This I believe to be the first notice published of this
peculiar arrangement.
The Reptilia, Aves, and Mammalia have usually been distinguished from other
vertebrates by the possession of a well-developed allantois and amnion. I
think that we may further say that the lower vertebrates, Pisces and
Amphibia, are to be distinguished from the three above-mentioned groups of
higher vertebrates, by the positive embryonic character that their neural
and alimentary canals at first communicate posteriorly. The presence or
absence of this arrangement depends on the different positions of the
embryo in the blastoderm. In Reptiles, Birds and Mammals, the embryo
occupies a central position in the blastoderm, and not, as in Pisces and
Amphibia, a peripheral one at its edge. We can, in fact, only compare the
blastoderm of the Bird and the Elasmobranch, by supposing that in the
blastoderm of the Bird there has occurred an abbreviation of the processes,
by which the embryo Elasmobranch is eventually placed in the centre of the
blastoderm: as a result of this abbreviation the embryo Bird occupies _from
the first a_ central position in the blastoderm[187].
Footnote 187: Vide Note on p. 281, also p. 295, and Pl. 9,
figs. 1 and 2, and Comparison, &c., _Qy. Jl. of Micros. Sci._
July, 1875, p. 219. [This Edition, No. VI. p. 125.] These
passages give an account of the change of position of the
Elasmobranch embryo, and the Note on p. 281 contains a
speculation about the nature of the primitive streak with its
contained primitive groove. I have suggested that the primitive
streak is probably to be regarded as a rudiment at the position
where the edges of the blastoderm coalesced to give to the
embryos of Birds and Mammals the central position which they
occupy.
If my hypothesis should turn out to be correct, various, now
unintelligible, features about the primitive streak would be
explained: such as its position behind the embryo, the fusion
of the epiblast and mesoblast in it, the groove it contains,
&c.
The possibility of the primitive streak representing the
blastopore, as it in fact does according to my hypothesis,
ought also to throw light on E. Van Beneden's recent researches
on the development of the Mammalian ovum.
In order clearly to understand the view here expressed, the
reader ought to refer to the passages above quoted.
The peculiar relations of the blastoderm and embryo, and the resulting
relations of the neural and alimentary canal, appear to me to be features
of quite as great an importance for classification as the presence or
absence of an amnion and allantois.
_General Features of the Hypoblast._
There are but few points to be noticed with reference to the histology of
the hypoblast cells. The cells of the dorsal wall of the alimentary cavity
are columnar and form a single row. Those derived from the yolk to form the
ventral wall are at first roundish, but subsequently assume a more columnar
form.
_The Notochord._
One of the most interesting features in the Elasmobranch development is the
formation of the notochord from the hypoblast. All the steps in the process
by which this takes place can be followed with great ease and certainty.
Up to stage B the hypoblast is in contact with the epiblast immediately
below the medullary groove, but exhibits no trace of a thickening or any
other formation at that point.
Between stage B and C the notochord first arises.
In the hindermost sections of this stage the hypoblast retains a perfectly
normal structure and uniform thickness throughout. In the next few sections
(Pl. 10, fig. 1_c_, _ch´_) a slight thickening is to be observed in the
hypoblast, immediately below the medullary canal. The layer, which
elsewhere is composed of a single row of cells, here becomes two cells
deep, but no sign of a division into two layers exhibited.
In the next few sections the thickening of the hypoblast becomes much more
pronounced; we have, in fact, a ridge projecting from the hypoblast towards
the epiblast (Pl. 10, fig. 1_b_, _ch´_).
This ridge is pressed firmly against the epiblast, and causes in it a
slight indentation. The hypoblast in the region of the ridge is formed of
two layers of cells, the ridge being entirely due to the uppermost of the
two.
In sections in front of this a cylindrical rod, which can at once be
recognised as the notochord and is continuous with the ridge just
described, begins to be split off from the hypoblast. It is difficult to
say at what point the separation of this rod from the hypoblast is
completed, since all intermediate gradations between complete separation
and complete attachment are to be seen.
Where the separation first appears, a fairly thick bridge of hypoblast is
left connecting the two lateral halves of the layer, but anteriorly this
bridge becomes excessively delicate and thin (Pl. 10, fig. 1_a_), and in
some cases is barely visible except with high powers.
From the series of sections represented, it is clear that the notochord
commences to be separated from the hypoblast anteriorly, and that the
separation gradually extends backwards.
The posterior extremity of the notochord remains for a long time attached
to the hypoblast; and it is not till the end of the period treated of in
this chapter that it becomes completely free.
A sheath is formed around the notochord, very soon after its formation, at
a stage intermediate between stages C and D. This sheath is very delicate,
though it stains with both osmic acid and hæmatoxylin. I conclude from its
subsequent history, that it is to be regarded as a product of the cells of
the notochord, but at the same time it should be stated that it precisely
resembles membrane-like structures, which I have already described as being
probably artificial.
Towards the end of this period the cells of the notochord become very much
flattened vertically, and cause the well-known stratified appearance which
characterises the notochord in longitudinal sections. In transverse
sections the outlines of the cells of the notochord appear rounded.
Throughout this period the notochord cells are filled with yolk-spherules,
and near its close small vacuoles make their appearance in them.
An account of the development of the notochord, substantially similar to
that I have just given, appeared in my preliminary paper[188] on the
development of the Elasmobranch fishes.
Footnote 188: _Loc. cit._
To the remarks which were there made, I have little to add. There are two
possible views, which can be held with reference to the development of the
notochord from the hypoblast.
We may suppose that this is the primitive mode of development of the
notochord, or we may suppose that the separation of the notochord from the
hypoblast is due to a secondary process.
If the latter view is accepted, it will be necessary to maintain that the
mesoblast becomes separated from the hypoblast as three separate masses,
two lateral, and one median, and that the latter becomes separated much
later than the two former.
We have, I think, no right to assume the truth of this view without further
proof. The general admission of assumptions of this kind is apt to lead to
an injurious form of speculation, in which every fact presenting a
difficulty in the way of some general theory is explained away by an
arbitrary assumption, while all the facts in favour of it are taken for
granted. It is however clear that no theory can ever be fairly tested so
long as logic of this kind is permitted. If, in the present instance, the
view is adopted that the notochord has in reality a mesoblastic origin, it
will be possible to apply the same view to every other organ derived from
the hypoblast, and to say that it is really mesoblastic, but has become
separated at rather a late period from the hypoblast.
If, however, we provisionally reject this explanation, and accept the other
alternative, that the notochord is derived from the hypoblast, we must be
prepared to adopt one of two views with reference to the development of the
notochord in other vertebrates. We must either suppose that the current
statements as to the development of the notochord in other vertebrates are
inaccurate, or that the notochord has only become secondarily mesoblastic.
The second of these alternatives is open to the same objections as the view
that the notochord has only apparently a hypoblastic source in
Elasmobranchii, and, provisionally at least, the first of them ought to be
accepted. The reasons for accepting this alternative fall under two heads.
In the first place, the existing accounts and figures of the development of
the notochord exhibit in almost all cases a deficiency of clearness and
precision. The exact stage necessary to complete the series never appears.
It cannot, therefore, at present be said that the existing observations on
the development of the notochord afford a strong presumption against its
hypoblastic origin.
In the second place, the remarkable investigations of Hensen[189], on the
development of the notochord in Mammalia, render it very probable that, in
this group, the notochord is developed from the hypoblast.
Footnote 189: _Zeitschrift f. Anat. u. Entwicklungsgeschichte_,
Vol. I. p. 366.
Hensen finds that in Mammalia, as in Elasmobranchii, the mesoblast forms
two independent lateral masses, one on each side of the medullary canal.
After the commencing formation of the protovertebræ the hypoblast becomes
considerably thickened beneath the medullary groove; and, though he has not
followed out all the steps of the process by which this thickening is
converted into the notochord, yet his observations go very far towards
proving that it does become the notochord.
Against the observations of Hensen, there ought, however, to be mentioned
those of Lieberkühn[190]. He believes that the two lateral masses of
mesoblast, described by Hensen (in an earlier paper than the one quoted),
are in reality united by a delicate layer of cells, and that the notochord
is formed from a thickening of these.
Footnote 190: _Sitz. der Gesell. zu Marburg_, Jan. 1876.
Lieberkühn gives no further statements or figures, and it is clear that,
even if there is present the delicate layer of mesoblast, which he fancies
he has detected, yet this cannot in any way invalidate such a section as
that represented on Pl. X. fig. 40, of Hensen's paper.
In this figure of Hensen's, the hypoblast cells become distinctly more
columnar, and the whole layer much thicker immediately below the medullary
canal than elsewhere, and this independently of any possible layer of
mesoblast.
It appears to me reasonable to conclude that Lieberkühn's statements do not
seriously weaken the certainty of Hensen's results.
In addition to the observations of Hensen's on Mammalia, those of
Kowalevsky and Kuppfer on Ascidians may fairly be pointed to as favouring
the hypoblastic origin of the notochord.
It is not too much to say that at the present moment the balance of
evidence is in favour of regarding the notochord as a hypoblastic organ.
This conclusion is, no doubt, rather startling, and difficult to
understand. The only feature of the notochord in its favour is the fact of
its being unsegmented[191].
Footnote 191: In my earlier paper I suggested that the
endostyle of Ascidians afforded an instance of a supporting
organ being derived from the hypoblast. This parallel does not
hold since the endostyle has been shewn to possess a secretory
function. I never intended (as has been imagined by Professor
Todaro) to regard the endostyle as the homologue of the
notochord.
Should it eventually turn out that the notochord is developed in most
vertebrates from the mesoblast, and only exceptionally from the hypoblast,
the further question will have to be settled as to whether it is
primitively a hypoblastic or a mesoblastic organ; but, from whatever layer
it has its source, an excellent example will be afforded of an organ
changing from the layer in which it was originally developed into another
distinct layer.
EXPLANATION OF PLATE 10.
COMPLETE LIST OF REFERENCE LETTERS.
_al._ Alimentary canal. _ch._ Chorda dorsalis or notochord. _ch´._ Ridge of
hypoblast, which will become separated off as the notochord. _ep._
Epiblast. _hy._ Hypoblast. _lp._ Coalesced lateral and vertebral plate of
mesoblast. _mg._ Medullary groove. _n._ Nucleus of yolk. _na._ Cells formed
around the nuclei of the yolk to enter into the ventral wall of the
alimentary canal. _nc._ Neural or medullary canal. _pv._ Protovertebra.
_so._ Somatopleure. _sp._ Splanchnopleure. _ts._ Mesoblast of
tail-swelling. _yk._ Yolk-spherules.
Figs. 1_a_, 1_b_, 1_c_. Three sections from the same embryo belonging to a
stage intermediate between B and C, of which fig. 1_a_ is the most
anterior. × 96 diameters.
The sections illustrate (1) The different characters of the medullary
groove in the different regions of the embryo. (2) The structure of the
coalesced lateral and vertebral plates. (3) The mode of formation of the
notochord as a thickening of the hypoblast (_ch´_), which eventually
becomes separated from the hypoblast as an elliptical rod (1_a_, _ch_).
Fig. 2. Section through the anterior part of an embryo belonging to stage
C. The section is mainly intended to illustrate the formation of the
ventral wall of the alimentary canal from cells formed around the nuclei of
the yolk. It also shews the shallowness of the medullary groove in the
anterior part of the body.
Figs. 2_a_, 2_b_, 2_c_. Three sections from the same embryo as fig. 2.
Fig. 2_a_ is the most anterior of the three sections and is taken through a
point shortly in front of fig. 2. The figures illustrate the general
features of an embryo of stage C, more especially the complete closing of
the alimentary canal in front and the triangular section which it there
presents.
Fig. 3. Section through the posterior part of an embryo belonging to stage
D. × 86 diameters.
It shews the general features of the layers during the stage, more
especially the differentiation of somatic and splanchnic layers of the
mesoblast.
Figs. 3_a_, 3_b_, 3_c_, 3_d_, 3_e_, 3_f_. Sections of the same embryo as
fig. 3 (× 60 diameters). Fig. 3 belongs to part of the embryo intermediate
between figs. 3_e_ and 3_f_.
The sections shew the features of various parts of the embryo. Figs. 3_a_,
3_b_ and 3_c_ belong to the head, and special attention should be paid to
the presence of a cavity in the mesoblast in 3_b_ and to the ventral
curvature of the medullary folds.
Fig. 3_d_ belongs to the neck, fig. 3_e_ to the back, and fig. 3_f_ to the
tail.
Fig. 4. Section through the region of the tail at the commencement of stage
F. × 60 diameters.
The section shews the character of the tail-swellings and the commencing
closure of the medullary groove.
Fig. 5. Transverse section through the anterior part of the head of an
embryo belonging to stage F (× 60 diameters). It shews (1) the ventral
curvature of the medullary folds next the head. (2) The absence of
mesoblast in the anterior part of the head. _hy_ points to the extreme
front end of the alimentary canal.
Fig. 6. Section through the head of an embryo at a stage intermediate
between F and G. × 86 diameters.
It shews the manner in which the medullary folds of the head unite to form
the medullary canal.
Fig. 7. Longitudinal and vertical section through the tail of an embryo
belonging to stage G.
It shews the direct communication which exists between the neural and
alimentary canals.
The section is not quite parallel to the long axis of the embryo, so that
the protovertebræ are cut through in its anterior part, and the neural
canal passes out of the section anteriorly.
Fig. 8. Network of nuclei from the yolk of an embryo belonging to stage H.
CHAPTER VI.
DEVELOPMENT OF THE TRUNK DURING STAGES G TO K.
By the stage when the external gills have become conspicuous objects, the
rudiments of the greater number of the important organs of the body are
definitely established.
Owing to this fact the first appearance of the external gills forms a very
convenient break in the Elasmobranch development; and in the present
chapter the history is carried on to the period of this occurrence.
While the last chapter dealt for the most part with the formation of the
main organic systems from the three embryonic layers, the present one has
for its subject the gradual differentiation of these systems into
individual organs. In treating of the development of the separate organs a
divergence from the plan of the last chapter becomes necessary, and the
following arrangement has been substituted for it. First of all an account
is given of the development of the external epiblast, which is followed by
a description of the organs derived from the mesoblast and of the
notochord.
_External Epiblast._
During stages G to I the epiblast[192] is formed of a single layer of
flattened cells; and in this, as in the earlier stages, it deserves to be
especially noticed that the epiblast is never more than _one cell deep_,
and is therefore incapable of presenting any differentiation into nervous
and epidermic layers. (Pl. 11, figs. 1-5.)
Footnote 192: Unless the contrary is stated, the facts
recorded in this chapter apply only to the genera Scyllium and
Pristiurus.
The cells which compose it are flattened and polygonal in outline, but more
or less spindle-shaped in section. They present a strong contrast to the
remaining embryonic cells of the body in possessing a considerable quantity
of clear protoplasm, which in most other cells is almost entirely absent.
Their granular nucleus is rounded or oval, and typically contains a single
nucleolus. Frequently, however, two nucleoli are present, and when this is
the case an area free from granules is to be seen around each nucleolus,
and a dark line, which could probably be resolved into granules by the use
of a sufficiently high magnifying power, divides the nucleus into two
halves. These appearances probably indicate that nuclei, in which two
nucleoli are present, are about to divide.
The epiblast cells vary in diameter from .022 to .026 Mm. and their nuclei
from .014 to .018 Mm. They present a fairly uniform character over the
greater part of the body. In Torpedo they present nearly the same
characters as in Pristiurus and Scyllium, but are somewhat more columnar.
(Pl. 11, fig. 7.)
Along the summit of the back from the end of the tail to the level of the
anus, or slightly beyond this, epiblast cells form a fold--the rudiment of
the embryonically undivided dorsal fin--and the cells forming this, unlike
the general epiblast cells, are markedly columnar; they nevertheless, here
as elsewhere, form but a single layer. (Pl. 11, fig. 3 and 5, _df._)
Although at this stage the dorsal fin is not continued as a fold anteriorly
to the level of the anus, yet a columnar thickening or ridge of epiblast,
extending along the median dorsal line nearly to the level of the heart,
forms a true morphological prolongation of the fin.
On the ventral side of the tail is present a rudiment of the ventral
unpaired fin, which stops short of the level of the anus, but, though less
prominent, is otherwise quite similar to the dorsal fin and continuous with
it round the end of the tail. At this stage the mesoblast has no share in
forming either fin.
In many sections of the tail there may be seen on each side two folds of
skin, which are very regular, and strongly simulate the rudimentary fins
just described. The cells composing them are, however, not columnar, and
the folds themselves are merely artificial products due to shrinking.
At a stage slightly younger than K an important change takes place in the
epiblast.
From being composed of a single layer of cells it becomes two cells deep.
The two layers appear first of all anteriorly, and subsequently in the
remaining parts of the body. At first, both layers are formed of flattened
cells (Pl. 11, figs. 8, 9); but at a stage slightly subsequent to that
dealt with in the present chapter, the cells of the inner of the two layers
become columnar, and thus are established the two strata always present in
the epidermis of adult vertebrates, viz. an outer layer of flattened cells
and an inner one of columnar cells[193].
Footnote 193: The layers are known as epidermic (horny) and
mucous layers by English writers, and as Hornschicht and
Schleimschicht by the Germans. For their existence in all
Vertebrates, vide Leydig _Ueber allgemeine Bedeckungen der
Amphibien_, p. 20. Bonn, 1876.
The history of the epiblast in Elasmobranchii is interesting, from the
light which it throws upon the meaning of the nervous and epidermic layers
into which the epiblast of Amphibians and some other Vertebrates is
divided. The Amphibians and Elasmobranchii present the strongest contrast
in the development of their epiblast, and it is worth while shortly to
review and compare the history of the layer in the two groups.
In Amphibians the epiblast is from the first divided into an outer stratum
formed of a single row of flattened cells, and an inner stratum composed of
several rows of more rounded cells. These two strata were called by
Stricker the nervous and epidermic layers, and these names have been very
generally adopted.
Both strata have a share in forming the general epiblast, and though
eventually they partially fuse together, there can be but little doubt that
the horny layer of the adult epiblast, where such can be
distinguished[194], is derived from the epidermic layer of the embryo, and
the mucous layer of the epiblast from the embryonic nervous layer. Both
layers of the epiblast assist in the formation of the cerebro-spinal
nervous system, and there also at first fuse together[195], though the
epidermic layer probably separates itself again, as the central epithelium
of the spinal canal. The lens and auditory sac are derived exclusively from
the nervous layer of the epidermis, while this layer also has the greater
share in forming the olfactory sac.
Footnote 194: Vide Leydig, _loc. cit._
Footnote 195: Vide Götte, _Entwicklungsgeschichte der Unke_.
In Elasmobranchii the epiblast is at first uniformly composed of a single
row of cells. The part of the layer which will form the central nervous
system next becomes two or three cells deep, but presents no distinction
into two layers; the remaining portions of the layer remain, as before, one
cell deep. Although the epiblast at first presents this simple structure,
it eventually, as we have seen, becomes divided throughout into two layers,
homologous with the two layers which arise so early in Amphibians. The
outer one of the two forms the horny layer of the epidermis and the central
epithelium of the neural canal. The inner one, the mucous layer of the
epidermis and the nervous part of the brain and spinal cord. Both layers
apparently enter into the formation of the organs of sense.
While there is no great difficulty in determining the equivalent parts of
the epidermis in Elasmobranchii and Amphibians, it still remains an open
question in which of these groups the epiblast retains its primitive
condition.
Though it is not easy to bring conclusive proofs on the one side or the
other, the balance of argument appears to me to be decidedly in favour of
regarding the condition of the epiblast in Elasmobranchii, and most other
Vertebrates, as the primitive one, and its condition in Amphibians as a
secondary one, due to the throwing back of the differentiation of their
epiblast into two layers to a very early period in their development.
In favour of this view are the following points: (1) That a _primitive_
division of the epiblast into two layers is unknown in the animal kingdom,
except amongst Amphibians and (?) Osseous Fish. (2) That it appears more
likely for a particular feature of development to be thrown back to an
earlier period, than for such an important feature as a distinction between
two primary layers to be absolutely lost during an early period of
development, and then to reappear again in later stages.
The fact of the epiblast of the neural canal being divided, like the
remainder of the layer, into nervous and epidermic parts, cannot, I think,
be used as an argument in favour of the opposite view to that here
maintained.
It seems probable that the central canal of the nervous system arose as an
involution from the exterior, and therefore that the epidermis lining it is
in reality merely a part of the external epidermis, and as such is
naturally separated from the true nervous structures adjacent to it[196].
Footnote 196: Vide Self, "Development of Spinal Nerves in
Elasmobranchii." _Phil. Transact._ 1876. [This Edition, No.
VIII.]
Leaving the general features of the external skin, I pass to the special
organs derived from it during the stage just anterior to K.
_The unpaired Fins._ The unpaired fins have grown considerably, and the
epiblast composing them becomes, like the remainder of the layer, divided
into two strata, both however composed of more or less columnar cells. The
ventral fin has now become more prominent than the dorsal fin; but the
latter extends forward as a fold quite to the anterior part of the body.
_The paired Fins._ Along each side of the body there appears during this
stage a thickened line of epiblast, which from the first exhibits two
special developments: one of these just in front of the anus, and a second
and better marked one opposite the front end of the segmental duct. These
two special thickenings are the rudiments of the paired fins, which thus
arise as special developments of a continuous ridge on each side, precisely
like the ridges of epiblast which form the rudiments of the unpaired fins.
Similar thickenings to those in Elasmobranchii are found at the ends of the
limbs in the embryos of both Birds and Mammals, in the form of caps of
columnar epiblast[197].
Footnote 197: For Birds, vide _Elements of Embryology_, Foster
and Balfour, pp. 144, 145, and for Mammals, Kölliker,
_Entwicklungsgeschichte_, p. 283.
The ridge, of which the limbs are special developments, is situated on a
level slightly ventral to that of the dorsal aorta, and extends from just
behind the head to the level of the anus. It is not noticeable in surface
views, but appears in sections as a portion of the epiblast where the cells
are more columnar than elsewhere; precisely resembling in this respect the
forward continuation of the dorsal fin. At the present stage the posterior
thickenings of this ridge which form the abdominal fins are so slight as to
be barely visible, and their real nature can only be detected by a careful
comparison between sections of this and the succeeding stages. The
rudiments of the anterior pair of limbs are more visible than those of the
posterior, though the passage between them and the remainder of the ridges
is most gradual. Thus at first the rudiments of both the limbs are nothing
more than slight thickenings of the epiblast, where its cells are more
columnar than elsewhere. During stage K the rudiments of both pairs of
limbs, but especially of the anterior pair, grow considerably, while at the
same time the thickened ridge of epiblast which connects them together
rapidly disappears. The thoracic limbs develop into an elongated projecting
fold of epiblast, in every way like the folds forming the unpaired fins;
while at the same time the cells of the subjacent mesoblast become closely
packed, and form a slight projection, at the summit of which the fold of
the epiblast is situated (Pl. 11, fig. 9). The maximum projection of the
thoracic fin is slightly in advance of the front end of the segmental duct.
The abdominal fins do not, during stage K, develop quite so fast as the
thoracic, and at its close are merely elongated areas where the epiblast is
much thickened, and below which the mesoblast is slightly condensed. In the
succeeding stages they develop into projecting folds of skin, precisely as
do the thoracic fins.
The features of the development of the limbs just described, are especially
well shewn in Torpedo; in the embryos of which the passage from the general
linear thickening of epiblast into the but slightly better marked
thickening of the thoracic fin is very gradual, and the fact of the limb
being nothing else than a special development of the linear lateral
thickening is proved in a most conclusive manner.
If the account just given of the development of the limbs is an accurate
record of what really takes place, it is not possible to deny that some
light is thrown by it upon the first origin of the vertebrate limbs. The
facts can only bear one interpretation, _viz.: that the limbs are the
remnants of continuous lateral fins_.
The unpaired dorsal fin develops as a continuous thickening, which then
grows up into a projecting fold of columnar cells. The greater part of this
eventually atrophies, but three separate lobes are left which form the two
dorsal fins and the upper lobe of the caudal fin.
The development of the limbs is almost identically similar to that of the
dorsal fins. There appears a lateral linear thickening of epiblast, which
however does not, like the similar thickening of the fins, grow into a
distinct fold. Its development becomes confined to two special points, at
each of which is formed a continuous elongated fold of columnar cells
precisely like the fold of skin forming the dorsal fins. These two folds
form the paired fins. If it be taken into consideration that the continuous
lateral fin, of which the rudiment appears in Elasmobranchii, does not
exist in any adult Vertebrate, and also that a continuous dorsal fin exists
in many Fishes, the small differences in development between the paired
fins and the dorsal fins will be seen to be exactly those which might have
been anticipated beforehand. Whereas the continuous dorsal fin, which often
persists in adult fishes, attains a considerable development before
vanishing, the originally continuous lateral one has only a very ephemeral
existence.
While the facts of development strongly favour a view which would regard
the limbs as remnants of a primitively continuous lateral fin, there is
nothing in the structure of the limbs of adult Fishes which is opposed to
this view. Externally they closely resemble the unpaired fins, and both
their position and nervous supply appear clearly to indicate that they do
not belong to one special segment of the body. They appear rather to be
connected with a varying number of segments; a fact which would receive a
simple explanation on the hypothesis here adopted[198].
Footnote 198: For the nervous supply in fishes, vide Stannius,
_Peripher. Nerv. System d. Fische_. In Osseous Fishes he states
that the thoracic fin is supplied by branches from the first
three though sometimes from the first four spinal nerves. In
Acipenser there are branches from the first six nerves. In
Spinax the limb is supplied by the rami anteriores of the
fourth and succeeding ten spinal nerves. In the Rays not only
do the sixteen anterior spinal nerves unite to supply the fin,
but in all there are rami anteriores from thirty spinal nerves
which pass to the thoracic limb.
My researches throw no light on the nature of the skeletal parts of the
limb, but the suggestion which has been made by Günther[199] with reference
to the limb of Ceratodus (the most primitive known), that it is a
modification of a series of parallel rays, would very well suit the view
here proposed.
Footnote 199: _Philosophical Transactions_, 1871.
Dr Dohrn[200] in speaking of the limbs, points out the difficulties in the
way of supposing that they can have originated _de novo_, and not by the
modification of some pre-existing organ, and suggests that the limbs are
modified gill-arches; a view similar to which has been hinted at by
Professor Gegenbaur[201].
Footnote 200: _Ursprung d. Wirbelthiere and
Functionswechsels._
Footnote 201: _Grundriss d. Vergleichenden Anat._ p. 494.
Dr Dohrn has not as yet given the grounds for his determination, so that
any judgment on his views is premature.
None of my observations on Elasmobranchii lends any support to these views;
but perhaps, while regarding the limbs as the remains of a continuous fin,
it might be permissible to suppose that the pelvic and thoracic girdles are
altered remnants of the skeletal parts of some of the gill-arches which
have vanished in existing Vertebrates.
The absence of limbs in the Marsipobranchii and Amphioxus, for reasons
already insisted upon by Dr Dohrn[202], cannot be used as an argument
against limbs having existed in still more primitive Vertebrates.
Footnote 202: _Loc. cit._
Though it does not seem probable that a dorsal and ventral fin can have
existed contemporaneously with lateral fins (at least not as continuous
fins), yet, judging from such forms as the Rays, there is no reason why
small balancing dorsal and caudal fins should not have co-existed with
fully developed lateral fins.
_Mesoblast. G-K._
The mesoblast in stage F forms two independent lateral plates, each with a
splanchnic and somatic layer, and divided, as before explained, into a
vertebral portion and a parietal portion. At their peripheral edge these
plates are continuous with the general mesoblastic tissue of the
non-embryonic part of the blastoderm; except in the free parts of the
embryo, where they are necessarily separated from the mesoblast of the
yolk-sac, and form completely independent lateral masses of cells.
During the stages G and H, the two layers of which the mesoblast is
composed cease to be in contact, and leave between them a space which
constitutes the commencement of the body-cavity (Pl. 10, fig. 1). From the
very first this cavity is more or less clearly divided into two distinct
parts; one of them in the vertebral portion of the plates of mesoblast, the
other in the parietal. The cavity in the parietal part of the plates alone
becomes the true body-cavity. It extends uninterruptedly through the
anterior parts of the embryo, but does not appear in the caudal region,
being there indicated only by the presence of two layers in the mesoblast
plates. Though fairly wide below, it narrows dorsally before becoming
continuous with the cavity in the vertebral plates. The line of junction of
the vertebral and parietal plates is a little ventral to the dorsal summit
of the alimentary canal (Pl. 10, fig. 5). Owing to the fact that the
vertebral plates are split up into a series of segments (protovertebræ),
the section of the body-cavity they enclose is necessarily also divided
into a series of segments, one for each protovertebra.
Thus the whole body-cavity consists of a continuous parietal space which
communicates by a series of apertures with a number of separate cavities
enclosed in the protovertebræ. The cavity in each of the protovertebræ is
formed of a narrowed dorsal and a dilated ventral segment, the latter on
the level of the dorsal aorta (Pl. 11, fig. 5). Cavities are present in all
the vertebral plates with the exception of a few far back in the tail; and
exist in part of the caudal region posterior to that in which a cavity in
the parietal plate is present.
_Protovertebræ._ Each protovertebra[203] or vertebral segment of the
mesoblast plate forms a flattened rectangular body, ventrally continuous
with the parietal plate of mesoblast. During stage G the dorsal edge of the
protovertebræ is throughout on about a level with the ventral third of the
spinal cord. Each vertebral plate is composed of two layers, a somatic and
a splanchnic, and encloses the already-mentioned section of the
body-cavity. The cells of both layers of the plate are columnar, and each
consists of a very large nucleus, invested by a delicate layer of
protoplasm.
Footnote 203: No attempt has been made to describe in detail
the different appearances presented by the protovertebræ in the
various parts of the body, but in each stage a protovertebra
from the dorsal region is taken as typical.
Before the end of stage H the inner or splanchnic wall of the protovertebra
loses its simple constitution, owing to the middle part of it, opposite the
dorsal two-thirds of the notochord, undergoing peculiar changes. These
changes are indicated in transverse sections (Pl. 11, figs. 5 and 6,
_mp´_), by the cells in the part we are speaking of acquiring a peculiar
angular appearance, and becoming one or two deep; and the meaning of the
changes is at once shewn by longitudinal horizontal sections. These prove
(Pl. 12, fig. 10) that the cells in this situation have become elongated in
a longitudinal direction, and, in fact, form typical spindle-shaped
embryonic muscle-cells, each with a large nucleus. Every muscle-cell
extends for the whole length of a protovertebra, and in the present stage,
or at any rate in stage I, acquires a peculiar granulation, which clearly
foreshadows transverse striation (Pl. 12, figs. 11-13).
Thus by stage H a small portion of the splanchnopleure which forms the
inner layer of each protovertebra, becomes differentiated into a distinct
band of longitudinal striated muscles; these almost at once become
functional, and produce the peculiar serpentine movements of the embryo,
spoken of in a previous chapter, p. 291.
It may be well to say at once that these muscles form but a very small part
of the muscles which eventually appear; which latter are developed at a
very much later period from the remaining cells of the protovertebræ. The
band developed at this stage appears to be a special formation, which has
arisen through the action of natural selection, to enable the embryo to
meet its respiratory requirements, by continually moving about, and so
subjecting its body to fresh oxydizing influences; and as such affords an
interesting example of an important structure acquired during and for
embryonic life.
Though the cavities in the protovertebræ are at first perfectly continuous
with the general body-cavity, of which indeed they merely form a
specialized part, yet by the close of stage H they begin to be constricted
off from the general body-cavity, and this process is continued rapidly,
and completed shortly after stage I, and considerably before the
commencement of stage K (Pl. 11, figs. 6 and 8). While this is taking
place, part of the splanchnic layer of each protovertebra, immediately
below the muscle-band just described, begins to proliferate, and produce a
number of cells, which at once grow in between the muscles and the
notochord. These cells are very easily seen both in transverse and
longitudinal sections, and form the commencing vertebral bodies (Pl. 11,
fig. 6, and Pl. 12, figs. 10 and 11, _Vr_).
At first the vertebral bodies have the same segmentation as the
protovertebræ from which they sprang; that is to say, they form masses of
embryonic cells separated from each other by narrow slits, continuous with
the slits separating the protovertebræ. They have therefore at their first
appearance a segmentation completely different from that which they
eventually acquire (Pl. 12, fig. 11).
After the separation of the vertebral bodies from the protovertebræ, the
remaining parts of the protovertebræ may be called muscle-plates; since
they become directly converted into the whole voluntary muscular system of
the trunk. At the time when the cavity of the muscle-plates has become
completely separate from the body-cavity, the muscle-plates themselves are
oblong structures, with two walls enclosing the cavity just mentioned, in
which the original ventral dilatation is still visible. The outer or
somatic wall of the plates retains its previous simple constitution. The
splanchnic wall has however a somewhat complicated structure. It is
composed dorsally and ventrally of a columnar epithelium, but in its middle
portion of the muscle-cells previously spoken of. Between these and the
central cavity of the plates the epithelium forming the remainder of the
layer commences to insert itself; so that between the first-formed muscle
and the cavity of the muscle-plate there appears a thin layer of cells, not
however continuous throughout.
At the end of the period K the muscle-plates have extended dorsally
two-thirds of the way up the sides of the spinal cord, and ventrally to the
level of the segmental duct. Their edges are not straight, but are bent
into an angular form, with the apex pointing forwards. Vide Pl. 12,
fig. 17, _mp_.
Before the end of the period a number of connective-tissue cells make their
appearance, and extend upwards from the dorsal summit of the muscle-plates
around the top of the spinal cord. These cells are at first rounded, but
become typical branched connective-tissue cells before the close of the
period (Pl. 11, figs. 7 and 8).
Between stages I and K the bodies of the vertebræ rapidly increase in size
and send prolongations downwards and inwards to meet below the notochord.
These soon become indistinguishably fused with other cells which appear in
the area between the alimentary cavity and the notochord, but probably
serve alone to form the vertebral bodies, while the cells adjoining them
form the basis for the connective tissue of the kidneys, &c.
The vertebral bodies also send prolongations dorsalwards between the sides
of the spinal cord and the muscle-plates. These grow round till they meet
above the spinal and enclose the dorsal nerve-roots. They soon however
become fused with the dorsal prolongations from the muscle-plates, at least
so far as my methods of investigation enable me to determine; but it
appears to me probable that they in reality remain distinct, and become
converted into the neural arches, while the connective-tissue cells from
the muscle-plates form the adjoining subcutaneous and inter-muscular
connective tissue.
All the cells of the vertebral rudiments become stellate and form typical
embryonic connective-tissue. The rudiments however still retain their
primitive segmentation, corresponding with that of the muscle-plates, and
do not during this period acquire their secondary segmentation. Their
segmentation is however less clear than it was at an earlier period, and in
the dorsal part of the vertebral rudiments is mainly indicated by the
dorsal nerve-roots, which always pass out in the interval between two
vertebral rudiments. Vide Pl. 12, fig. 12, _pr_.
_Intermediate Cell-mass._ At about the period when the muscle-plates become
completely free, a fusion takes place between the somatopleure and
splanchnopleure immediately above the dorsal extremity of the true
body-cavity (Pl. 11, fig. 6). The cells in the immediate neighbourhood of
this fusion form a special mass, which we may call the intermediate
cell-mass--a name originally used by Waldeyer for the homologous cells in
the Chick. Out of it are developed the urinogenital organs and the
adjoining tissues. At first it forms little more than a columnar
epithelium, but by the close of the period is divided into (1) An
epithelium on the free surface; from this are derived the glandular parts
of the kidneys and functional parts of the genital glands; and (2) a
subjacent stroma which forms the basis for the connective-tissue and
vascular parts of these organs.
To the history of these parts a special section is devoted; and I now pass
to the description of the mesoblast which lines the body-cavity and forms
the connective tissue of the body-wall, and the muscular and connective
tissue of the wall of the alimentary canal.
_Body-cavity and Parietal Plates._ By the close of stage H, as has been
already mentioned, a cavity is formed between the somatopleure and
splanchnopleure in the anterior part of the trunk, which rapidly widens
during the succeeding stages. Anteriorly, it invests the heart, which
arises during stage G, as a simple space between the ventral wall of the
throat and the splanchnopleure (Pl. 11, fig. 4). Posteriorly it ends
blindly.
This cavity forms in the region of the heart the rudiment of the
pericardial cavity. The remainder of the cavity forms the true body-cavity.
Immediately behind the heart the alimentary canal is still open to the
yolk-sac, and here naturally the two lateral halves of the body-cavity are
separated from each other. In the tail of the embryo no body-cavity has
appeared by stage I, although the parietal plates of mesoblast are
distinctly divided into somatic and splanchnic layers. In the caudal region
the lateral plates of mesoblast of the two sides do not unite ventrally,
but are, on the contrary, quite disconnected. Their ventral edge is
moreover much swollen (Pl. 11, fig. 1). At the caudal swelling the
mesoblast plates cease to be distinctly divided into somatopleure and
splanchnopleure, and more or less fuse with the hypoblast of the caudal
vesicle (Pl. 11, fig. 2).
Between stages I and K the body-cavity extends backwards behind the point
where the anus is about to appear, though it never reaches quite to the
extreme end of the tail. The backward extension of the body-cavity, as is
primitively the case everywhere, is formed of two independent lateral
halves (Pl. 11, fig. 9_a_). Anteriorly, opposite the hind end of the small
intestine, these two lateral halves unite ventrally to form a single cavity
in which hangs the small intestine (Pl. 11, fig. 8) suspended by a very
short mesentery.
The most important change which takes place in the body-cavity during this
period is the formation of a septum which separates off a pericardial
cavity from the true body-cavity.
Immediately in front of the liver the splanchnic and somatic walls of the
body come into very close contact, and I believe unite over the greater
part of their extent. The septum so formed divides the original body-cavity
into an anterior section or pericardial cavity, and a posterior section or
true body-cavity. There is left, however, on each side dorsally a rather
narrow passage which serves to unite the pericardial cavity in front with
the true body-cavity behind.
In Pl. 11, fig. 8_a_, there is seen on one side a section through this
passage, while on the other side the passage is seen to be connected with
the pericardial cavity.
It is not possible from transverse sections to determine for certain
whether the septum spoken of is complete. An examination of longitudinal
horizontal sections from an embryo belonging to the close of the stage K
has however satisfied me that this septum, by that stage at any rate, is
fully formed.
The two lateral passages spoken of above probably unite in the adult to
form the passage connecting the pericardial with the peritoneal cavity,
which, though provided with but a single orifice into the pericardial
cavity, divides into two limbs before opening into the peritoneal cavity.
The body-cavity undergoes no further changes of importance till the close
of the period.
_Somatopleure and Splanchnopleure._ Both the somatic and splanchnic walls
of the body-cavity during stage I exhibit a simple uniform character
throughout their whole extent. They are formed of columnar cells where they
line the dorsal part of the body-cavity, but ventrally of more rounded and
irregular cells (Pl. 11, fig. 5).
In them may occasionally be seen aggregations of very peculiar and large
cells with numerous highly refracting spherules; the cells forming these
are not unlike the _primitive ova_ to be described subsequently, but are
probably large cells derived from the yolk.
It is during the stage intermediate between I and K that the first changes
become visible which indicate a distinction between an epithelium
(endothelium) lining the body-cavity and the connective tissue adjoining
this.
There are at first but very few connective-tissue cells between the
epithelium of the somatic layer of the mesoblast and the epiblast, but a
connection between them is established by peculiar protoplasmic processes
which pass from the one to the other (Pl. 11, fig. 8). Towards the end of
stage K, however, there appears between the two a network of mesoblastic
cells connecting them together. In the rudimentary outgrowth to form the
limbs the mesoblast cells of the somatic layer are crowded in an especially
dense manner.
From the first the connective-tissue cells around the hypoblastic
epithelium of the alimentary tract are fairly numerous (Pl. 11, fig. 8),
and by the close of this period become concentrically arranged round the
intestinal epithelium, though not divided into distinct layers. A special
aggregation of them is present in the hollow of the rudimentary spiral
valve.
Behind the anal region the two layers of the mesoblast (somatic and
splanchnic) completely fuse during stage K, and form a mass of stellate
cells in which no distinction into two layers can be detected (Pl. 11,
figs. 9_c_, 9_d_).
The alimentary canal, which at first lies close below the aorta, becomes
during this period gradually carried further and further from this,
remaining however attached to the roof of the body-cavity by a thin layer
of the mesoblast of the splanchnopleure formed of an epithelium on each
side, and a few interposed connective-tissue cells. This is the mesentery,
which by the close of stage K is of considerable length in the region of
the stomach, though shorter elsewhere.
* * * * *
The above account of the protovertebræ and body-cavity applies solely to
the genera Pristiurus and Scyllium. The changes of these parts in Torpedo
only differ from those of Pristiurus in unimportant though fairly
noticeable details. Without entering into any full description of these it
may be pointed out that both the true body-cavity and its continuations
into the protovertebræ appear later in Torpedo than in Pristiurus and
Scyllium. In some cases even the muscle-plates become definitely separated
and independent before the true body-cavity has appeared. As a result of
this the primitive continuity of the body-cavity and cavity of the
muscle-plates becomes to a certain extent masked, though its presence may
easily be detected by the obvious continuity which at first exists between
the somatic and splanchnic layers of mesoblast and the two layers of the
muscle-plate. In the muscle-plate itself the chief point to be noticed is
the fact that the earlier formed bands of muscles (_mp´_) arise very much
later, and are less conspicuous, in Torpedo than in the genera first
described. They are however present and functional.
The anatomical relations of the body-cavity itself are precisely the same
in Torpedo as in Pristiurus and Scyllium, and the pericardial cavity
becomes separated from the peritoneal in the same way in all the genera;
the two lateral canals connecting the two cavities being also present in
all the three genera. The two independent parietal plates of mesoblast of
the posterior parts of the body have ventrally a swollen edge, as in
Pristiurus, and in this a cavity appears which forms a posterior
continuation of the true body-cavity.
_Resumé._ The primitive independent mesoblast plates of the two sides of
the body become divided into two layers, a somatic and a splanchnic
(Hautfaserblatt and Darmfaserblatt). At the same time in the dorsal part of
the mesoblast plate a series of transverse splits appear which mark out the
limits of the protovertebræ and serve to distinguish a dorsal or vertebral
part of the plate from a ventral or parietal part.
Between the somatic and splanchnic layers of the mesoblast plate a cavity
arises which is continued quite to the summit of the vertebral part of the
plate. This is the primitive body-cavity; and at first the cavity is
divided into two lateral and independent halves.
The next change which takes place is the complete separation of the
vertebral portion of the plate from the parietal; thereby the upper
segmented part of the body-cavity becomes isolated and separated from the
lower and unsegmented part. In connection with this change in the
constitution of the body-cavity there are formed a series of rectangular
plates, each composed of two layers, a somatic and a splanchnic, between
which is the cavity originally continuous with the body-cavity. The
splanchnic layer of the plates buds off cells to form the rudiments of the
vertebral bodies which are originally segmented in the same planes as the
protovertebræ. The plates themselves remain as the muscle-plates and
develop a special layer of muscle (_mp´_) in their splanchnic layer.
In the meantime the parietal plates of the two sides unite ventrally
throughout the intestinal and cardiac regions of the body, and the two
primitively isolated cavities contained in them coalesce. Posteriorly
however the plates do not unite ventrally, and their contained cavities
remain distinct.
At first the pericardial cavity is quite continuous with the body-cavity;
but by the close of the period included in the present chapter it becomes
separated from the body-cavity by a septum in front of the liver, which is
however pierced dorsally by two narrow channels.
The parts derived from the two layers of the mesoblast (not including
special organs or the vascular system) are as follow:--
From the somatic layer are formed
(1) A considerable part of the voluntary muscular system of
the body.
(2) The dermis.
(3) A large part of the intermuscular connective tissue.
(4) Part of the peritoneal epithelium.
From the splanchnic layer are formed
(1) A great part of the voluntary muscular system.
(2) Part of the intermuscular connective tissue (?).
(3) The axial skeleton.
(4) The muscular and connective-tissue wall of the
alimentary tract.
(5) A great part of the peritoneal epithelium.
_General Considerations._ In the history which has just been given of the
development of the mesoblast, there are several points which appear to me
to throw light upon the primitive origin of that layer. Before entering
into these it is however necessary to institute a comparison between the
history of the mesoblast in Elasmobranchii and in other Vertebrates, in
order to distinguish as far as possible the primitive and the secondary
characters present in the various groups.
Though the Mammals are to be looked on as the most differentiated group
amongst the Vertebrates, yet in their embryonic history they retain many
very primitive features, and, as has been recently shewn by Hensen[204],
present numerous remarkable approximations to the Elasmobranchii. We find
accordingly[205] that the primitive lateral plates of mesoblast undergo
nearly the same changes in these two groups. In Mammals there is at first a
continuous cavity extending through both the parietal and vertebral
portions of each plate, and dividing the plates into a somatic and a
splanchnic layer: this cavity is the primitive body-cavity. The vertebral
portion of each plate with its contained cavity then becomes divided off
from the parietal. The later development of these parts is not accurately
known, but it seems that the outer portion of each vertebral plate,
composed of two layers (somatic and splanchnic) enclosing between them a
remnant of the primitive body-cavity, becomes separated off as a
muscle-plate. The remainder forms a vertebral rudiment, &c. Thus the
extension of the body-cavity into the vertebral portion of the mesoblast,
and the constriction of the vertebral portion of the cavity from the
remainder, are as distinctive features of Mammals as they are of the
Elasmobranchii.
Footnote 204: _Zeitschrift f. Anat. Entwicklungsgeschichte_,
Vol. 1.
Footnote 205: Hensen _loc. cit._
In Birds[206] the horizontal splitting of the mesoblast into somatic and
splanchnic layers appears, as in Mammals, to extend at first to the summit
of the protovertebræ, but these bodies become so early separated from the
parietal plates that this fact has usually been overlooked or denied; but
even on the second day of incubation the outer layer of the protovertebræ
is continuous with the somatic layer of the lateral plates, and the inner
layer and kernel of the protovertebræ with the splanchnic layer of the
lateral plates[207]. After the isolation of the protovertebræ the primitive
position of the split which separated their somatic and splanchnic layers
becomes obscured, but when on the third day the muscle-plates are formed
they are found to be _constituted of two layers, an inner and an outer,
which enclose between them a central cavity_. This remarkable fact, which
has not received much attention, though noticeable in most figures,
receives a simple explanation as a surviving rudiment on Darwinian
principles. The central cavity of the muscle-plate is, in fact, a remnant
of the vertebral extension of the body-cavity, and is the same cavity as
that found in the muscle-plates of Elasmobranchii. The two layers of the
muscle-plate also correspond with the two layers present in Elasmobranchii,
the one belonging to the somatic, the other to the splanchnic layer of
mesoblast. The remainder of the protovertebræ internal to the muscle-plates
is very large in Birds, and is the equivalent of that portion of the
protovertebræ which in Elasmobranchii is split off to form the vertebral
bodies[208] (Pl. 11, figs. 6, 7, 8, _Vr_). Thus, though the history of the
development of the mesoblast is not precisely the same for Birds as for
Elasmobranchii, yet the differences between the two groups are of such a
character as to prove in a striking manner that the Avian development is a
derivation from a more primary form, like that of the Elasmobranchii.
Footnote 206: For the history of protovertebræ and
muscle-plates in Birds, vide _Elements of Embryology_, Foster
and Balfour. The statement there made that the horizontal
splitting of the mesoblast does not extend to the summit of the
vertebral plate, must however be regarded as doubtful.
Footnote 207: Vide _Elements of Embryology_, p. 56.
Footnote 208: Dr Götte, _Entwicklungsgeschichte der Unke_, p.
534, gives a different account of the development of the
protovertebræ from that in the text. He states that the
muscle-plates do not give rise to the main dorso-lateral
muscles, but only to some superficial ventral muscles, while
the dorso-lateral muscles are according to him formed from part
of the kernel of the protovertebræ internal to the
muscle-plates. The account given in the text is the result of
my own investigations, and accords precisely with the recent
statements of Professor Kölliker, _Entwicklungsgeschichte_,
1876.
According to the statements of Bambeke and Götte, the Amphibians present
rather remarkable peculiarities in the development of their muscular
system. Each side-plate of mesoblast is divided into a somatic and a
splanchnic layer, continuous throughout the vertebral and parietal portions
of the plate. The vertebral portions (protovertebræ) of the plates soon
become separated from the parietal, and form an independent mass of cells
constituted of two layers, which were originally continuous with the
somatic and splanchnic layers of the parietal plates. The outer or somatic
layer of the vertebral plates is formed of a single row of cells, but the
inner or splanchnic layer is made up of a central kernel of cells and an
inner single layer. This central kernel is the first portion of the
vertebral body to undergo any change, and it becomes converted into the
main dorso-lateral muscles of the body, which apparently correspond with
the muscles derived from the whole muscle-plate of the Elasmobranchii. From
the inner layer of the splanchnic division there are next formed the main
internal ventral muscles, rectus abdominis, &c., as well as the chief
connective-tissue elements of the parts surrounding the spinal cord. The
outer layer of the vertebral plates forms the dermis and subcutaneous
connective tissue, as well as some of the superficial muscles of the trunk
and the muscles of the limbs.
Dr Götte appears to think that the vertebral plates in Amphibians present a
perfectly normal development very similar to that of other Vertebrates. The
divergences between Amphibians and other Vertebrates appear, however, to
myself, to be very great, and although the very careful account given by Dr
Götte is probably to be relied on, yet some further explanation than he has
offered of the development of these parts amongst the Amphibians would seem
to be required.
A primary stage in which the two layers of the vertebral plates are
continuous with the somatic and splanchnic layers of the body-wall is
equally characteristic of Amphibians, Elasmobranchii and Mammals. In the
subsequent development, however, a great difference between the types
becomes apparent, for whereas in Elasmobranchii both layers of the
vertebral plates combine to form the muscle-plates, out of which the great
dorso-lateral muscles are formed, in Amphibians what appear to be the
equivalent muscles are derived from a few of the cells (the kernel) of the
inner layer of the vertebral plates only. The cells which form the lateral
muscles in Amphibians might be thought to correspond in position with the
cells which become, in Elasmobranchii, converted into the special early
formed band of muscles (_m.p´._), rather than, as their development seems
to indicate, with the whole Elasmobranch muscle-plates[209].
Footnote 209: The type of development of the muscle-plates of
Amphibians would become identical with that of Elasmobranchii if
their first-formed mass of muscle corresponded with the
early-formed muscles of Elasmobranchii, and the remaining cells
of both layers of the protovertebræ became in the course of
development converted into muscle-cells indistinguishable from
those formed at first. Is it possible that, owing to the
distinctness of the first-formed mass of muscle, Dr Götte can
have overlooked the fact that its subsequent growth is carried
on at the expense of the adjacent cells of the somatic layer?
Osseous Fishes are stated to agree with Amphibians in the development of
their protovertebræ and muscular system[210], but further observations on
this point are required.
Footnote 210: Ehrlich, "Ueber den peripher. Theil d.
Urwirbel." _Archiv f. Mic. Anat._ Vol. XI.
Though the development of the general muscular system and muscle-plates
does not, according to existing statements, take place on quite the same
type throughout the Vertebrate subkingdom, yet the comparison which has
been instituted between Elasmobranchii and other Vertebrates appears to
prove that there are one or two common features in their development, which
may be regarded as primitive, and as having been inherited from the
ancestors of Vertebrates. These features are (1) The extension of the
body-cavity into the vertebral plates, and subsequent enclosure of this
cavity between the two layers of the muscle-plates; (2) The primitive
division of the vertebral plate into a somatic and a splanchnic layer, and
the formation of a large part of the voluntary muscular system out of the
splanchnic layer.
* * * * *
The ultimate derivation of the mesoblast forms one of the numerous burning
questions of modern embryology, and there are advocates to be found for
almost every one of the possible views the question admits of.
All who accept the doctrine of descent are agreed that primitively only two
embryonic layers were present--the epiblast and the hypoblast--and that the
mesoblast subsequently appeared as a distinct layer, after a certain
complexity of organization had been attained.
The general agreement stops, however, at this point, and the greatest
divergence of opinion exists with reference to all further questions which
bear on the development of the mesoblast. There appear to be four
possibilities as to the origin of this layer.
It may be derived:
(1) entirely from the epiblast,
(2) partly from the epiblast, and partly from the hypoblast,
(3) entirely from the hypoblast,
(4) or may have no fixed origin.
The fourth of these possibilities may for the present be dismissed, since
it can be only maintained should it turn out that all the other views are
erroneous. The first possibility is supported by the case of the
Coelenterata, and we might almost say by that of this group only[211].
Footnote 211: The most important other instances in addition
to that of the Coelenterata which can be adduced in favour of
the epiblastic origin of the mesoblast are the Bird and Mammal,
in which according to the recent observations of Hensen for the
Mammal, and Kölliker for the Mammal and Bird, the mesoblast is
split off from the epiblast. If the views I have elsewhere put
forward about the meaning of the primitive groove be accepted,
the derivation of the mesoblast from the epiblast in these
instances would be apparent rather than real, and have no deep
morphological significance for the present question.
Other instances may be brought forward from various groups, but
none of these are sufficiently well confirmed to be of any
value in the determination of the present question.
Amongst the Coelenterata the mesoblast, when present, is unquestionably a
derivative of the epiblast, and when, as is frequently the case, a distinct
mesoblast is not present, the muscle-cells form a specialized part of the
epidermic cells.
The condition of the mesoblast in these lowly organized animals is exactly
what might _à priori_ have been anticipated, but the absence throughout the
group of a true body-cavity, or specially developed muscular system of the
alimentary tract, prevents the possibility of generalizing for other
groups, from the condition of the mesoblast in this one.
In those animals in which a body-cavity and muscular alimentary tract are
present, it would certainly appear reasonable to expect the mesoblast to be
derived from both the primitive layers: the voluntary muscular system from
epiblast, and the splanchnic system from the hypoblast. This view has been
taken and strongly advocated by so distinguished an embryologist as
Professor Haeckel, and it must be admitted, that on _à priori_ grounds
there is much to recommend it; there are, however, so far as I am aware of,
comparatively few observed facts in its favour.
Professor Haeckel's own objective arguments in support of his view are as
follows:
(1) From the fact that some investigators derive the mesoblast with
absolute confidence from the hypoblast, while others do so with equal
confidence from the epiblast, he concludes that it is really derived from
both these layers.
(2) A second argument is founded on the supposed derivation of the
mesoblast in Amphioxus from both epiblast and hypoblast. Kowalevsky's
account (on which apparently Prof. Haeckel's[212] statements are based)
appears to me, however, too vague, and his observations too imperfect, for
much confidence to be placed in his statements on this head. It does not
indeed appear to me that the formation of the layers in Amphioxus, till
better known, can be used as an argument for any special view about this
question.
Footnote 212: Vide _Anthropogenie_, p. 197.
(3) Professor Haeckel's own observations on the development of Osseous fish
form a third argument in support of his views. These observations do not,
however, accord with those of the majority of investigators, and not having
been made by means of sections, require further confirmation before they
can be definitely accepted.
(4) A fourth argument rests on the fact that the various embryonic layers
fuse together to form the primitive streak or axis-cord in higher
vertebrates. This he thinks proves that the mesoblast is derived from both
the primitive layers. The primitive streak has, however, according to my
views, quite another significance to that attributed to it by Professor
Haeckel[213]; but in any case Professor Kölliker's researches, and on this
point my own observations accord with his, appear to me to prove that the
fusion which there takes place is only capable of being used as an argument
in favour of an epiblastic origin of the mesoblast, and not of its
derivation from both epiblast and hypoblast.
Footnote 213: Vide Self, "Development of Elasmobranch Fishes,"
_Journal of Anat. and Phys._ Vol. X. note on p. 682, and also
Review of Professor Kölliker's "Entwicklungsgeschichte des
Menschen u. d. höheren Thiere," _Journal of Anat. and Phys._
Vol. X.
The objective arguments in favour of Professor Haeckel's views are not very
conclusive, and he himself does not deny that the mesoblast as a rule
apparently arises as a single and undivided mass from one of the two
primary layers, and only subsequently becomes split into somatic and
splanchnic strata. This original fusion and subsequent splitting of the
mesoblast is explained by him as a secondary condition, a possibility which
cannot by any means be thrown on one side. It seems therefore worth while
examining how far the history of the somatic and splanchnic layers of the
mesoblast in Elasmobranchii and other Vertebrates accords with the
supposition that they were primitively split off from the epiblast and the
hypoblast respectively.
It is well to consider first of all what parts of the mesoblast of the body
might be expected to be derived from the somatic and splanchnic layers on
this view of their origin[214].
Footnote 214: Professor Haeckel speaks of the splitting of the
mesoblast in Vertebrates into a somatic and splanchnic layer as
a secondary process (_Gastrula u. Eifurchung d. Thiere_), but
does not make it clear whether he regards this secondary
splitting as taking place along the old lines. It appears to me
to be fairly certain that even if the original unsplit
condition of the mesoblast is to be regarded as a secondary
condition, yet that the splitting of this must take place along
the old lines, otherwise a change in the position of the
body-cavity in the adult would have to be supposed--an unlikely
change producing unnecessary complication. The succeeding
argument is based on the assumption that the unsplit condition
is a secondary condition, but that the split which eventually
appears in this occurs along the old lines, separating the
primitive splanchnopleure from the primitive somatopleure.
From the somatic layer of the mesoblast there would no doubt be formed the
whole of the voluntary muscular system of the body, the dermis, the
subcutaneous connective tissue, and the connective tissue between the
muscles. It is probable also, though this point is less certain, that the
skeleton would be derived from the somatic layer. From the splanchnic layer
would be formed the connective tissue and muscular layers of the alimentary
tract, and possibly also the vascular system.
Turning to the actual development of these parts, the discrepancy between
theory and fact becomes very remarkable. From the somatic layer of the
mesoblast, part of the voluntary muscular system and the dermis is no doubt
derived, but the splanchnic layer supplies the material, not only for the
muscular wall of the digestive canal and the vascular system, but also for
the whole of the axial skeleton _and a great part of the voluntary muscular
system of the body, including the first-formed muscles_. Though remarkable,
it is nevertheless not inconceivable, that the skeleton might be derived
from the splanchnic mesoblast, but it is very difficult to understand how
there could be formed from it a part of the voluntary muscular system of
the body indistinguishably fused with part of the muscular system derived
from the somatopleure. No fact in my investigations comes out more clearly
than that a great part of the voluntary muscular system is formed from the
splanchnic layer of the mesoblast, yet this fact presents a most serious
difficulty to the view that the somatic and splanchnic layers of the
mesoblast in Vertebrates are respectively derived from the epiblast and
hypoblast.
In spite, therefore, of general _à priori_ considerations of a very
convincing kind which tell in favour of the double origin of the mesoblast,
this view is supported by so few objective facts, and there exists so
powerful an array of facts against it, that at present, at least, it seems
impossible to maintain it. The full strength of the facts against it will
appear more fully in a review of the present state of our knowledge as to
the development of the mesoblast in the different groups.
To this I now pass.
In a paper on the "Early stages of Development in Vertebrates[215]" a short
_resumé_ was given of the development of the mesoblast throughout the
animal kingdom, which it may be worth while repeating here with a few
additions. So far as we know at present, the mesoblast is derived from the
hypoblast in the following groups:
Echinoderms (Hensen, Agassiz, Metschnikoff, Selenka, Götte), Nematodes
(Bütschli), Sagitta (Kowalevsky, Bütschli), Lumbricus and probably other
Annelids (Kowalevsky), Brachiopoda (Kowalevsky), Crustaceans (Bobretzky),
Insects (Kowalevsky, Ulianin, Dohrn), Myriapods (Metschnikoff), Tunicates
(Kowalevsky, Kuppfer), Petromyzon (Owsjanikoff), Osseous fishes (Oellacher,
Götte, Kowalevsky), Elasmobranchii (Self), Amphibians (Remak, Stricker,
Götte).
Footnote 215: _Quart. Jl. of Micros. Science_, July, 1875.
[This Edition, No. VI.]
The list includes members from the greater number of the groups of the
animal kingdom; the most striking omissions being the Coelenterates,
Mollusks, and the Amniotic Vertebrates. The absence of the Coelenterates
has been already explained and my grounds for regarding the Amniotic
Vertebrates as apparent rather than real exceptions have also been pointed
out. The Mollusks, however, remain as a large group, in which we as yet
know very little as to the formation of the mesoblast.
Dr Rabl[216], who seems recently to have studied the development of Lymnæus
by means of sections, gives some figures shewing the origin of the
mesoblast; they are, however, too diagrammatic to be of much service in
settling the present question, and the memoirs of Professor Lankester[217]
and Dr Fol[218] are equally inconclusive for this purpose, for, though they
contain figures of elongated and branched mesoblast cells passing from the
epiblast to the hypoblast, no satisfactory representations are given of the
origin of these cells. I have myself observed in embryos of Turbo or
Trochus similar elongated cells to those figured by Lankester and Fol, but
was unable clearly to determine whence they arose. The most accurate
observations which we have on this question are those of Professor
Bobretzky[219]. In Nassa he finds that the three embryonic layers are all
established during segmentation. The outermost and smallest cells form the
epiblast, somewhat larger cells adjoining these the mesoblast, and the
large yolk-cells the hypoblast. These observations do not, however,
demonstrate from which of the primary layers the mesoblast is derived.
Footnote 216: _Jenaische Zeitschrift_, Vol. IX.
Footnote 217: _Quart. Jl. of Micros. Science_, Vol. XXV. 1874,
and _Phil. Trans._ 1875.
Footnote 218: _Archives de Zoologie_, Vol. IV.
Footnote 219: _Archiv f. Micr. Anat._ Vol. XIII.
The evidence at present existing is clearly in favour of the mesoblast
being, in almost all groups of animals, developed from the hypoblast, but
strong as this evidence is, it has not its full weight unless the actual
manner in which the mesoblast is in many groups derived from the hypoblast,
is taken into consideration. The most important of these are the
Echinoderms, Brachiopods and Sagitta.
In the Echinoderms the mesoblast is in part formed by cells budded off from
the hypoblast, _the remainder, however, arises as one or more diverticula
of the alimentary tract_. From the separate cells first budded off there
are formed the cutis, part of the connective tissue and the calcareous
skeleton[220]. The diverticula from the alimentary cavity form the
water-vascular system and the somatic and splanchnic layers of mesoblast.
_The cavity of the diverticula after the separation of the water-vascular
system, forms the body-cavity. The outer lining layer of the cavity forms
the somatic layer of mesoblast and the voluntary muscles; the inner lining
layer the splanchnic mesoblast which unites with the epithelium of the
alimentary tract._ Though this fundamental arrangement would seem to be
universal amongst Echinoderms, considerable variations of it are exhibited
in different groups.
Footnote 220: The recent researches of Selenka, _Zeitschrift
f. Wiss. Zoologie_, Vol. XXVII. 1876, demonstrate that in
Echinoderms the muscles are derived from the cells first split
off from the hypoblast, and that the diverticula only form the
water-vascular system and the epithelial lining of the
body-cavity.
There is _one_ outgrowth from the alimentary tract in Synapta; _two_ in
Echinoids, Asteroids and Ophiura; _three_ in Comatula, and four (?) in
Amphiura. The cavity of the outgrowth usually forms the body-cavity, but
sometimes in Ophiura and Amphiura (Metschnikoff) the outgrowths are from
the first or soon become solid, and only secondarily acquire a cavity,
which is however homologous with the body-cavity of the other groups.
In Sagitta[221] the formation of the mesoblast and the alimentary tract
takes place in nearly the same fashion as in the Echinoderms. The simple
invaginate alimentary cavity becomes divided into three lobes, a central
and two lateral. The two lateral lobes are gradually more and more
constricted off from the central one, and become eventually quite separated
from it; their cavities remain independent, _and form in the adult the
body-cavity_, divided by a mesentery into two distinct lateral sections.
_The inner layer of each of the two lateral lobes forms the mesoblast of
the splanchnopleure, the outer layer the mesoblast of the somatopleure._
The central division of the primitive gastræa cavity remains as the
alimentary tract of the adult.
Footnote 221: Kowalevsky, "Würmer u. Arthropoden," _Mém. Acad.
Pétersbourg_, 1871.
The remarkable observations of Kowalevsky[222] on the development of the
Brachiopoda have brought to light the unexpected fact that in two genera at
least (Argiope and Terebratula) the mesoblast and body-cavity develop as
paired constrictions from the alimentary tract in a manner almost
identically the same as in Sagitta.
Footnote 222: "Zur Entwicklungsgeschichte d. Brachiopoden",
Protokoll d. ersten Session der Versammlung Russischer
Naturforscher in Kasan, 1873. Published in _Kaiserliche
Gesellschaft Moskau_, 1874 (Russian). Abstracted in Hoffmann
and Schwalbe, _Jahresbericht f._ 1873.
It thus appears that, so far as can be determined from the facts at our
disposal, the mesoblast in almost all cases is derived from the hypoblast,
and in three widely separated groups it arises as a pair of diverticula
from the alimentary tract, each diverticulum containing a cavity which
eventually becomes the body-cavity. I have elsewhere suggested[223] that
the origin of the mesoblast from alimentary diverticula is to be regarded
as primitive for all higher animals, and that the more general cases in
which the mesoblast becomes split off, as an undivided layer, from the
hypoblast, are in reality derivates from this. The chief obstacle in the
way of this view arises from the difficulty of understanding how the whole
voluntary muscular system can have been derived at first from the
alimentary tract. That part of a voluntary system of muscles might be
derived from the contractile diverticula of the alimentary canal attached
to the body-wall is not difficult to understand, but it is not easy to
believe that the secondary system so formed could completely replace the
primitive muscular system, derived, as it must have been, from the
epiblast. In my paper above quoted will be found various speculative
suggestions for removing this difficulty, which I do not repeat here. If it
be granted, however, that in Sagitta, Brachiopods, and Echinoderms we have
genuine examples of the formation of the whole mesoblast from alimentary
diverticula, it is easy to see how the formation of the mesoblast in
Vertebrates may be a secondary derivate from an origin of this nature.
Footnote 223: Comparison of Early Stages, _Quart. Jl. Micros.
Science_, July, 1875. [This Edition, No. VI.]
An attempt has been already made to shew that the mesoblast in
Elasmobranchii is formed in a very primitive fashion, and for this reason
the Elasmobranchii appear to be especially adapted for determining whether
any signs are exhibited of a derivation of the mesoblast as paired
diverticula of the alimentary tract. There are, it appears to me, several
such features. In the first place, the mesoblast is split off from the
hypoblast not as a single mass but as a pair of distinct masses, comparable
with the paired diverticula already alluded to. Secondly, the body-cavity
when it appears in the mesoblast plates, _does not arise as a single
cavity, but as a pair of cavities, one for each plate of mesoblast_, and
these cavities remain permanently distinct in some parts of the body, and
nowhere unite till a comparatively late period. Thirdly, the primitive
body-cavity of the embryo is not confined to the region in which a
body-cavity exists in the adult, _but extends to the summit of the
muscle-plates_, at first separating parts which become completely fused in
the adult to form the great lateral muscles of the body. It is difficult to
understand how the body-cavity could have such an extension as this, on the
supposition that it represents a primitive split in the mesoblast between
the wall of the gut and the body-wall; but its extension to this part is
quite intelligible, on the supposition that it represents the cavities of
two diverticula of the alimentary tract, from whose muscular walls the
voluntary muscular system has been derived. Lastly, I would point out that
the derivation of part of the muscular system from what appears as the
splanchnopleure is quite intelligible on the assumed hypothesis, but, as
far as I see, on no other.
Such are the main features presented by the mesoblast in Elasmobranchii,
which favour the view of its having originally formed the walls of the
alimentary diverticula. Against this view of its nature are the facts (1)
of the mesoblast plates being at first solid, and (2), as a consequence of
this, of the body-cavity never communicating with the alimentary canal.
These points, in view of our knowledge of embryological modifications,
cannot be regarded as great difficulties to my view. We have many examples
of organs, which, though in most cases arising as involutions, yet appear
in other cases as solid ingrowths. Such examples are afforded by the optic
vesicle, auditory vesicle, and probably also by the central nervous system,
of Osseous Fish. In most Vertebrates these organs are formed as hollow
involutions from the exterior; in Osseous Fish, however, as solid
involutions, in which a cavity secondarily appears.
The segmental duct of Elasmobranchii or the Wolffian duct (segmental duct)
of Birds are cases of a similar kind, being organs which must originally
have been formed as hollow involutions, but which now arise as solid
bodies.
Only one more instance of this kind need be cited, taken from the
Echinoderms.
The body-cavity and the mesoblast investing it arise in the case of most
Echinoderms as hollow involutions of the alimentary tract, but in some
exceptional groups, Ophiura and Amphiura, are stated to be solid at first
and only subsequently to become hollow. Should the accuracy of
Metschnikoff's account of this point be confirmed, an almost exact parallel
to what has been supposed by me to have occurred with the mesoblast in
Elasmobranchii, and other groups, will be supplied.
The tendency of our present knowledge appears to be in favour of regarding
the body-cavity in Vertebrates as having been primitively the cavity of
alimentary diverticula, and the mesoblast as having formed the walls of the
diverticula.
This view, to say the least of it, suits the facts which we know far better
than any other theory which has been proposed, and though no doubt the _à
priori_ difficulties in its way are very great, yet it appears to me to be
sufficiently strongly supported to deserve the attention of investigators.
In the meantime, however, our knowledge of invertebrate embryology is so
new and imperfect that no certainty on a question like that which has just
been discussed can be obtained; and any generalizations made at present are
not unlikely to be upset by the discovery of fresh facts.
The only other point in connection with the mesoblast which I would call
attention to is the formation of the vertebral bodies.
My observations confirm those of Remak and Gegenbaur, shewing that there is
a primary segmentation of the vertebral bodies corresponding to that of the
muscle-plates, followed by a secondary segmentation in which the central
lines of the vertebral bodies are opposite the partitions between the
muscle-plates.
The explanation of these changes is not difficult to find. The primary
segmentation of the body is that of the muscle-plates, which must have been
present at a time when the vertebral bodies had no existence. As soon
however as the notochordal sheath was required to be strong as well as
flexible, it necessarily became divided into a series of segments.
The conditions under which the lateral muscles can cause the flexure of the
vertebral column are clearly that each muscle-segment shall be capable of
acting on two vertebræ; and this condition can only be fulfilled when the
muscle-segments are opposite the intervals between the vertebræ. Owing to
this necessity, when the vertebral segments became formed, their centres
corresponded, not with the centres of the muscle-plates, but with the
inter-muscular septa.
These considerations fully explain the secondary segmentation of the
vertebræ by which they become opposite the inter-muscular septa. On the
other hand, the primary segmentation is clearly a remnant of the time when
no vertebral bodies were present, and has no greater morphological
significance than the fact that the cells to form the unsegmented
investment of the notochord were derived from the segmented muscle-plates,
and only secondarily became fused into a continuous tube.
_The Urinogenital System._
The first traces of the urinary system become visible at about the time of
the appearance of the third visceral cleft. At about this period the
somatopleure and splanchnopleure become more or less fused together at the
level of the dorsal aorta, and thus, as has been already mentioned, each of
the original plates of mesoblast becomes divided into a vertebral plate and
lateral plate (Pl. 11, fig. 6). The mass of cells resulting from this
fusion corresponds with Waldeyer's intermediate cell-mass in the Fowl.
At about the level of the fifth protovertebra the first trace of the
urinary system appears.
From the intermediate cell-mass a solid knob grows outwards towards the
epiblast (woodcut, fig. 4, _pd_). This knob consists at first of 20-30
cells, which agree in character with the neighbouring cells of the
intermediate cell-mass, and are at this period rounded. It is mainly, if
not entirely, derived from the somatic layer of the mesoblast.
From this knob there grows backwards a solid rod of cells which keeps in
very close contact with the epiblast, and rapidly diminishes in size
towards its posterior extremity. Its hindermost part consists in section of
at most one or two cells. It keeps so close to the epiblast that it might
be supposed to be derived from that layer were it not for the sections
shewing its origin from the knob above mentioned. We have in this rod the
commencement of what I have elsewhere[224] called the segmental duct.
Footnote 224: "Urinogenital Organs of Vertebrates," _Journ. of
Anat. and Phys._ Vol. X. [This Edition, No. VII.]
[Illustration: FIG. 4. TWO SECTIONS OF A PRISTIURUS EMBRYO WITH THREE
VISCERAL CLEFTS.
The sections are to shew the development of the segmental duct (_pd_) or
primitive duct of the kidneys. In _A_ (the anterior of the two sections)
this appears as a solid knob projecting towards the epiblast. In _B_ is
seen a section of the column which has grown backwards from the knob in
_A_.
_spn._ rudiment of a spinal nerve; _mc._ medullary canal; _ch._ notochord;
_X._ string of cells below the notochord; _mp._ muscle-plate; _mp´._
specially developed portion of muscle-plate; _ao._ dorsal aorta; _pd._
segmental duct; _so._ somatopleura; _sp._ splanchnopleura; _pp._
pleuro-peritoneal or body-cavity; _ep._ epiblast; _al._ alimentary canal.]
My observations shew that the segmental duct is developed in the way just
described in both Pristiurus and Torpedo. Its origin in Pristiurus is shewn
in the adjoining woodcut, and in Torpedo in Pl. 11, fig. 7, _sd_.
At a stage somewhat older than I, the condition of the segmental duct has
not very materially altered. It has increased considerably in length, and
the knob at its front end is both absolutely smaller, and also consists of
fewer cells than before (Pl. 11, fig. 7, _sd_). These cells have become
more columnar, and have begun to arrange themselves radially; thus
indicating the early appearance of the lumen of the duct. The cells forming
the front part of the rod, as well as those of the knob, commence to
exhibit a columnar character, but in the hinder part of the rod the cells
are still rounded. In no part of it has a lumen appeared.
At this period also the knob, partly owing to the commencing separation of
the muscle-plate from the remainder of the mesoblast, begins to pass
inwards and approach the pleuro-peritoneal cavity.
At the same stage the first not very distinct traces of the remainder of
the urinary system become developed. These appear in the form of solid
outgrowths from the intermediate cell-mass just at the most dorsal part of
the body-cavity.
The outgrowths correspond in numbers with the vertebral segments, and are
at first quite disconnected with the segmental duct. At this stage they are
only distinctly visible in the first few segments behind the front end of
the segmental duct. A full description of them will come more conveniently
in the next stage.
By a stage somewhat earlier than K important changes have taken place in
the urinary system.
The segmental duct has acquired a lumen in its anterior portion, which
opens at its front end into the body-cavity. (Pl. 11, fig. 9, _sd._) The
lumen is formed by the columnar cells spoken of in the last stage,
acquiring a radiating arrangement round a central point, at which a small
hole appears. After the lumen has once become formed, it rapidly increases
in size.
The duct has also grown considerably in length, but its hind extremity is
still as thin, and lies as close to the epiblast, as at first. The
segmental involutions which commenced to be formed in the last stage, have
now appeared for every vertebral segment along the whole length of the
segmental duct, and even for two or three segments behind this.
They are simple independent outgrowths arising from the outer and uppermost
angle of the body-cavity, and are at first almost without a trace of a
lumen; though their cells are arranged as two layers. They grow in such a
way as to encircle the oviduct on its inner and upper side (Pl. 11, fig. 8
and Pl. 12, fig. 14_b_, _st_). When the hindermost ones are formed, a
slight trace of a lumen is perhaps visible in the front ones. At a stage
slightly subsequent to this, in Scyllium canicula, I noticed 29 of them;
the first of them arising in the segment immediately behind the front end
of the oviduct (Pl. 12, fig. 17, _st_), and two of them being formed in
segments just posterior to the hinder extremity of the oviduct.
Pl. 12, figs. 16 and 18 represent two longitudinal sections shewing the
segmental nature of the involutions and their relation to the segmental
duct.
Many of the points which have been mentioned can be seen by referring to
Pl. 11 and 12. Anteriorly the segmental duct opens into the
pleuro-peritoneal cavity. In the sections behind this there may be seen the
segmental duct with a distinct lumen, and also a pair of segmental
involutions (Pl. 12, fig. 14_a_). In the still posterior sections the
segmental duct would be quite without a lumen, and would closely adjoin the
epiblast.
It seems not out of place to point out that the modes of the development of
the segmental duct and of the segmental involutions are strikingly similar.
Both arise as solid involutions, from homologous parts of the mesoblast.
The segmental duct arises in the vertebral segment immediately in front of
that in which the first segmental involution appears; _so that the
segmental duct appears to be equivalent to a single segmental involution_.
The next stage corresponds with the first appearance of the external gills.
The segmental duct now communicates by a wide opening with the body-cavity
(Pl. 11, fig. 9, _sd_). It possesses a lumen along its whole length up to
the extreme hind end (Pl. 11, fig. 9_a_). It is, however, at this hinder
extremity that the most important change has taken place. This end has
grown downwards towards that part of the alimentary canal which still lies
behind the anus. This downgrowth is beginning to shew distinct traces of a
lumen, and will appear in the next stage as one of the horns by which the
segmental ducts communicate with the cloaca (Pl. 11, fig. 9_b_). All the
anterior segmental involutions have now acquired a lumen. But this is still
absent in the posterior ones (Pl. 11, fig. 9_a_).
Owing to the disappearance of the body-cavity in the region behind the
anus, the primitive involutions there remain as simple masses of cells
still disconnected with the segmental duct (Pl. 11, figs. 9_b_, 9_c_ and
9_d_).
_Primitive Ova._ The true generative products make their first appearance
as the _primitive ova_ between stages I and K.
In the sections of one of my embryos of this stage they are especially well
shewn, and the following description is taken from those displayed in that
embryo.
They are confined to the region which extends posteriorly nearly to the end
of the small intestine and anteriorly to the abdominal opening of the
segmental duct.
Their situation in this region is peculiar. There is no trace of a distinct
genital ridge, but the ova mainly lie in the dorsal portion of the
mesentery, and therefore in a part of the mesoblast which distinctly
belongs to the splanchnopleure (Pl. 12, fig. 14_a_). Some are situated
external to the segmental involutions; and others again, though this is not
common, in a part of the mesoblast which distinctly belongs to the
body-wall (Pl. 12, fig. 14_b_).
The portion of mesentery, in which the primitive ova are most densely
aggregated, corresponds to the future position of the genital ridge, but
the other positions occupied by ova are quite outside this. Some ova are in
fact situated on the outside of the segmental duct and segmented tubes, and
must therefore effect a considerable migration before reaching their final
positions in the genital ridge on the inner side of the segmental duct
(Pl. 12, fig. 14_b_).
The condition of the tissue in which the ova appear may at once be gathered
from an examination of the figures given. It consists of an irregular
epithelium of cells partly belonging to the somatopleure and partly to the
splanchnopleure, but passing uninterruptedly from one layer to the other.
The cells which compose it are irregular in shape, but frequently columnar
(Pl. 12, figs. 14_a_ and 14_b_).
They are formed of a nucleus which stains deeply, invested by a _very
delicate_ layer of protoplasm. At the junction of somatopleure and
splanchnopleure they are more rounded than elsewhere. Very few loose
connective-tissue cells are present. The cells just described vary from
.008 Mm. to .01 Mm. in diameter.
The primitive ova are situated amongst them and stand out with
extraordinary clearness, to which justice is hardly done in my figures.
The normal full-sized ova exhibit the following structure. They consist of
a mass of somewhat granular protoplasm of irregular, but more or less
rounded, form. Their size varies from .016 - .036 Mm. In their interior a
nucleus is present, which varies from .012 - .016 Mm., but its size as a
rule bears _no_ relation to the size of the containing cell.
This is illustrated by the subjoined list of measurements.
Size of Primitive ova in Size of nucleus of Primitive
degrees of micrometer scale ova in degrees of micrometer
with F. ocul 2. scale with F. ocul 2.
10 8
13 8
13 8
14 7
15 7
13 7-1/2
11 8
16 5-1/2
12 7
10 7
15 6
13 6
12 7
The numbers given refer to degrees on my micrometer scale.
Since it is the ratio alone which it is necessary to call attention to, the
numbers are not reduced to decimals of a millimeter. Each degree of my
scale is equal, however, with the object glass employed, to .002 Mm.
This series brings out the result I have just mentioned with great
clearness.
In one case we find a cell has three times the diameter of the nucleus
16 : 5-1/2; in another case 10 : 8, the nucleus has only a slightly smaller
diameter than the cell. The irrationality of the ratio is fairly shewn in
some of my figures, though none of the largest cells with very small nuclei
have been represented.
The nuclei are granular, and stain fairly well with hæmatoxylin. They
usually contain a single deeply stained nucleolus, but in many cases,
especially where large (and this independently of the size of the cell),
they contain two nucleoli (Pl. 12, figs. 14_c_ and 14_d_), and are at times
so lobed as to give an apparent indication of commencing division.
A multi-nucleolar condition of the nuclei, like that figured by Götte[225],
does not appear till near the close of embryonic life, and is then found
equally in the large ova and in those not larger than the ova which exist
at this early date.
Footnote 225: _Entwicklungsgeschichte der Unke_, Pl. 1, fig. 8.
As regards the relation of the primitive ova to each other and the
neighbouring cells, there are a few points which deserve attention. In the
first place, the ova are, as a rule, collected in masses at particular
points, and not distributed uniformly (fig. 14_a_). The masses in some
cases appear as if they had resulted from the division of one primitive
ovum, but can hardly be adduced as instances of a commencing coalescence;
since if the ova thus aggregated were to coalesce, an ovum would be
produced of a very much greater size than any which is found during the
early stages. Though at this stage no indication is present of such a
coalescence of cells to form ova as is believed to take place by Götte,
still the origin of the primitive ova is not quite clear. One would
naturally expect to find a great number of cells intermediate between
primitive ova and ordinary columnar cells. Cells which may be intermediate
are no doubt found, but not nearly so frequently as might have been
anticipated. One or two cells are shewn in Pl. 12, fig. 14_a_, _x_, which
are perhaps of an intermediate character; but in most sections it is not
possible to satisfy oneself that any such intermediate cells are present.
In one case what appeared to be an intermediate cell was measured, and
presented a diameter of .012 Mm. while its nucleus was .008 Mm. Apart from
certain features of the nucleus, which at this stage are hardly very
marked, the easiest method of distinguishing a primitive ovum from an
adjacent cell is the presence of a large quantity of protoplasm around the
nucleus. The nucleus of one of the smallest primitive ova is not larger
than the nucleus of an ordinary cell (being about .008 Mm. in both). It is
perhaps the similarity in the size of the nuclei which renders it difficult
at first to distinguish developing primitive ova from ordinary cells.
Except with the very thinnest sections a small extra quantity of protoplasm
around a nucleus might easily escape detection, and the developing cell
might only become visible when it had attained to the size of a small
typical primitive ovum.
It deserves to be noticed that the nuclei even of some of the largest
primitive ova scarcely exceed the surrounding nuclei in size. This appears
to me to be an argument of some weight in shewing that the great size of
primitive ova is not due to the fact of their having been formed by a
coalescence of different cells (in which case the nucleus would have
increased in the same proportion as the cell); but to an increase by a
normal method of growth in the protoplasm around the nucleus.
It appears to me to be a point of great importance certainly to determine
whether the primitive ova arise by a metamorphosis of adjoining cells, or
may not be introduced from elsewhere. In some of the lower animals, _e.g._
Hydrozoa, there is no question that the ova are derived from the epiblast;
we might therefore expect to find that they had the same origin in
Vertebrates. Further than this, ova are frequently capable in a young state
of executing amoeboid movements, and accordingly of migrating from one
layer to another. In the Elasmobranchii the primitive ova exhibit in a
hardened state an irregular form which might appear to indicate that they
possess a power of altering their shape, a view which is further supported
by some of them being at the present stage situated in a position very
different from that which they eventually occupy, and which they can only
reach by migration. If it could be shewn that there were no intermediate
stages between the primitive ova and the adjoining cells (their migratory
powers being admitted) a strong presumption would be offered in favour of
their having migrated from elsewhere to their present position. In view of
this possibility I have made some special investigations, which have
however led to no very satisfactory results. There are to be seen in the
stages immediately preceding the present one, numerous cells in a
corresponding position to that of the primitive ova, which might very well
be intermediate between the primitive ova and ordinary cells, but which
offer no sufficiently well marked features for a certain determination of
their true nature.
In the particular embryo whose primitive ova have been described these
bodies were more conspicuous than in the majority of cases, but at the same
time they presented no special or peculiar characters.
In a somewhat older embryo of Scyllium the cells amongst which the
primitive ova lay had become very distinctly differentiated as an
epithelium (the germinal epithelium of Waldeyer) well separated by what
might almost be called a basement membrane from the adjoining
connective-tissue cells. Hardly any indication of a germinal ridge had
appeared, but the ova were more definitely confined than in previous
embryos to the restricted area which eventually forms this. The ova on the
average were somewhat smaller than in the previous cases.
In several embryos intermediate in age between the embryo whose primitive
ova were described at the commencement of this section and the embryo last
described, the primitive ova presented some peculiarities, about the
meaning of which I am not quite clear, but which may perhaps throw some
light on the origin of these bodies.
Instead of the protoplasm around the nucleus being clear or slightly
granular, as in the cases just described, it was filled in the most typical
instances with numerous highly refracting bodies resembling yolk-spherules.
In osmic acid specimens (Pl. 12, fig. 15) these stain very darkly, and it
is then as a rule very difficult to see the nucleus; in specimens hardened
in picric acid and stained with hæmatoxylin these bodies are stained of a
deep purple colour, but the nucleus can in most cases be distinctly seen.
In addition to the instances in which the protoplasm of the ova is quite
filled with these bodies, there are others in which they only occupy a
small area adjoining the nucleus (Pl. 12, fig. 15_a_), and finally some in
which only one or two of these bodies are present. The protoplasm of the
primitive ova appears in fact to present a series of gradations between a
state in which it is completely filled with highly refracting spherules and
one in which these are completely absent.
This state of things naturally leads to the view that the primitive ova,
when they are first formed, are filled with these spherules, which are
probably yolk-spherules, but that they gradually lose them in the course of
development. Against this interpretation is the fact that the primitive ova
in the younger embryo first described are completely without these bodies;
this embryo however unquestionably presented an abnormally early
development of the ova; and I am satisfied that embryos present
considerable variations in this respect.
If the primitive ova are in reality in the first instance filled with
yolk-spherules, the question arises as to whether, considering that they
are the only mesoblast cells filled at this period with yolk-spherules, we
must not suppose that they have migrated from some peripheral part of the
blastoderm into their present position. To this question I can give no
satisfactory answer. Against a view which would regard the spherules in the
protoplasm as bodies which appear subsequently to the first formation of
the ova, is the fact that hitherto no instances in which these spherules
were present have been met with in the late stages of development; and they
seem therefore to be confined to the first stages.
_Notochord._
The changes undergone by the notochord during this period present
considerable differences according to the genus examined. One type of
development is characteristic of Scyllium and Pristiurus; a second type, of
Torpedo.
My observations being far more complete for Scyllium and Pristiurus than
for Torpedo, it is to the two former genera only that the following account
applies, unless the contrary is expressly stated. Only the development of
the parts of the notochord in the trunk are here dealt with; the cephalic
section of the notochord is treated of in a subsequent section.
During stage G the notochord is composed of flattened cells arranged
vertically, rendering the histological characters of the notochord
difficult to determine in transverse sections. In longitudinal sections,
however, the form and arrangement of the cells can be recognised with great
ease. At the beginning of stage G each cell is composed of a nucleus
invested by granular protoplasm frequently vacuolated and containing in
suspension numerous yolk-spherules. It is difficult to determine whether
there is only one vacuole for each cell, or whether in some cases there may
not be more than one.
Round the exterior of the notochord there is present a distinct though
delicate cuticular sheath.
The vacuoles are at first small, but during stage G rapidly increase in
size, while at the same time the yolk-spherules completely vanish from the
notochord.
As a result of the rapid growth of the vacuoles, the nuclei, surrounded in
each case by a small amount of protoplasm, become pushed to the centre of
the notochord, the remainder of the protoplasm being carried to the edge.
The notochord thus becomes composed during stages H and I (Pl. 11,
fig. 4-6) of a central area mainly formed of nuclei with a small quantity
of protoplasm around them, and of a thin peripheral layer of protoplasm
without nuclei, the widish space between the two being filled with clear
fluid. The exterior of the cells is indurated, so that they may be said to
be invested by a membrane[226]; the cells themselves have a flattened form,
and each extends from the edge to the centre of the notochord, the long
axis of each being rather greater than half the diameter of the cord.
Footnote 226: This membrane is better looked upon, as is done
by Gegenbaur and Götte, as intercellular matter.
The nuclei of the notochord are elliptical vesicles, consisting of a
membrane filled with granular contents, amongst which is situated a
distinct nucleolus. They stain deeply with hæmatoxylin. Their long diameter
in Scyllium is about 0.02 Mm.
The diameter of the whole notochord in Pristiurus during stage I is about
0.1 Mm. in the region of the back, and about 0.08 Mm. near the posterior
end of the body.
Owing to the form of its constituent cells, the notochord presents in
transverse sections a dark central area surrounded by a lighter peripheral
one, but its true structure cannot be unravelled without the assistance of
longitudinal sections. In these (Pl. 12, fig. 10) the nuclei form an
irregular double row in the centre of the cord. Their outlines are very
clear, but those of the individual cells cannot for certain be made out. It
is, however, easy to see that the cells have a flattened and wedge-shaped
form, with the narrow ends overlapping and interlocking at the centre of
the notochord.
By the close of stage I the cuticular sheath of the notochord has greatly
increased in thickness.
During the period intermediate between stages I and K the notochord
undergoes considerable transformations. Its cells cease to be flattened,
and become irregularly polygonal, and appear but slightly more compressed
in longitudinal sections than in transverse ones. The vacuolation of the
cells proceeds rapidly, and there is left in each cell only a very thin
layer of protoplasm around the nucleus. Each cell, as in the earlier
stages, is bounded by a membrane-like wall.
Accompanying these general changes special alterations take place in the
distribution of the nuclei and the protoplasm. The nuclei, accompanied by
protoplasm, gradually leave the centre and migrate towards the periphery of
the notochord. At the same time the protoplasm of the cells forms a special
layer in contact with the investing sheath.
The changes by which this takes place can easily be followed in
longitudinal sections. In Pl. 12, fig. 11 the migration of the nuclei has
commenced. They are still, however, more or less aggregated at the centre,
and very little protoplasm is present at the edges of the notochord. The
cells, though more or less irregularly polygonal, are still somewhat
flattened. In Pl. 12, fig. 12 the notochord has made a further progress.
The nuclei now mainly lie at the side of the notochord, where they exist in
a somewhat shrivelled state, though still invested by a layer of
protoplasm.
A large portion of the protoplasm of the cord forms an almost continuous
layer in close contact with the sheath, which is more distinctly visible in
some cases than in others.
While the changes above described are taking place the notochord increases
in size. At the age of fig. 11 it is in the anterior part of the body of
Pristiurus about 0.11 Mm. At the age of fig. 12 it is in the same species
0.12 Mm., while in Scyllium stellare it reaches about 0.17 Mm.
During stage K (Pl. 11, fig. 8) the vacuolation of the cells of the
notochord becomes even more complete than during the earlier stages, and in
the central cells hardly any protoplasm is present, though a starved
nucleus surrounded by a little protoplasm may be found in an occasional
corner.
The whole notochord becomes very delicate, and can with great difficulty be
conserved whole in transverse sections.
The layer of protoplasm which appeared during the last stage on the inner
side of the cuticular membrane of the notochord becomes during the present
stage a far thicker and more definite structure. It forms a continuous
layer with irregular prominences on its inner surface; and contains
numerous nuclei. The layer sometimes presents in transverse sections hardly
any indication of a division into a number of separate cells, but in
longitudinal sections this is generally very obvious. The cells are
directed very obliquely forwards, and consist of an oblong nucleus invested
by protoplasm. The layer formed by them is very delicate and very easily
destroyed. In one example its thickness varied from .004 to .006 Mm., in
another it reached .012 Mm. The thickness of the cuticular membrane is
about .002 Mm. or rather less.
The diameter of a notochord in the anterior part of the body of a
Pristiurus embryo of this stage is about 0.21 Mm. Round the exterior of the
notochord the mesoblast cells are commencing to arrange themselves as a
special sheath.
In Torpedo the notochord at first presents the same structure as in
Pristiurus, _i.e._ it forms a cylindrical rod of flattened cells.
The vacuolation of these cells does not however commence till a relatively
very much later period than in Pristiurus, and also presents a very
different character (Pl. 11, fig. 7).
The vacuoles are smaller, more numerous, and more rounded than in the other
genera, and there can be no question that in many cases there is more than
one vacuole in a cell. The most striking point in which the notochord of
Torpedo differs from that of Pristiurus consists in the fact that in
Torpedo there is never any aggregation of the nuclei at the centre of the
cord, but the nuclei are always distributed uniformly through it. As the
vacuolation proceeds the differences between Torpedo and the other genera
become less and less marked. The vacuoles become angular in form, and the
cells of the cord cease to be flattened, and become polygonal.
At my final stage for Torpedo (slightly younger than K) the only important
feature distinguishing the notochord from that of Pristiurus, is the
absence of any signs of nuclei or protoplasm passing to the periphery.
Around the exterior of the cord there is early found in Torpedo a special
investment of mesoblastic cells.
EXPLANATION OF PLATES 11 AND 12.
COMPLETE LIST OF REFERENCE LETTERS.
_al._ Alimentary tract. _an._ Point where anus will be formed. _ao._ Dorsal
aorta. _ar._ Rudiment of anterior root of spinal nerve. _b._ Anterior fin.
_c._ Connective-tissue cells. _cav._ Cardinal vein. _ch._ Notochord. _df._
Dorsal fin. _ep._ Epiblast. _ge._ Germinal epithelium. _ht._ Heart. _l._
Liver. _mp._ Muscle-plate. _mp´._ Early formed band of muscles from the
splanchnic layer of the muscle-plates. _nc._ Neural canal. _p._ Protoplasm
from yolk in the alimentary tract. _pc._ Pericardial cavity. _po._
Primitive ovum. _pp._ body-cavity. _pr._ Rudiment of posterior root of
spinal nerve. _sd._ Segmental duct. _sh._ Cuticular sheath of notochord.
_so._ Somatic layer of mesoblast. _sp._ Splanchnic layer of mesoblast.
_spc._ Spinal cord. _sp.v._ Spiral valve. _sr._ Interrenal body. _st._
Segmental tube. _sv._ Sinus venosus. _ua._ Umbilical artery. _um._
Umbilical cord. _uv._ Umbilical vein. _V._ Splanchnic vein. _v._
Blood-vessel. _vc._ Visceral cleft. _Vr._ Vertebral rudiment. _W._ White
matter of spinal cord. _x._ Subnotochordal rod (except in fig. 14_a_). _y._
Passage connecting the neural and alimentary canals.
PLATE 11.
Fig. 1. Section from the caudal region of a Pristiurus embryo belonging to
stage H. Zeiss C, ocul. 1. Osmic acid specimen.
It shews (1) the constriction of the subnotochordal rod (_x_) from the
summit of the alimentary canal. (2) The formation of the body-cavity in the
muscle-plate and the ventral thickening of the parietal plate.
Fig. 1_a_. Portion of alimentary wall of the same embryo, shewing the
formation of the subnotochord rod (_x_).
Fig. 2. Section through the caudal vesicle of a Pristiurus embryo belonging
to stage H. Zeiss C, ocul. 1.
It shews the bilobed condition of the alimentary vesicle and the fusion of
the mesoblast and hypoblast at the caudal vesicle.
Fig. 3_a_. Sections from the caudal region of a Pristiurus embryo belonging
to stage H. Zeiss C, ocul. 1. Picric acid specimen.
It shews the communication which exists posteriorly between the neural and
alimentary canals, and also by comparison with 3_b_ it exhibits the
dilatation undergone by the alimentary canal in the caudal vesicle.
Fig. 3_b_. Section from the caudal region of an embryo slightly younger
than 3_a_. Zeiss C, ocul. 1. Osmic acid specimen.
Fig. 4. Section from the cardiac region of a Pristiurus embryo belonging to
stage H. Zeiss C, ocul. 1. Osmic acid specimen.
It shews the formation of the heart (_ht_) as a cavity between the
splanchnopleure and the wall of the throat.
Fig. 5. Section from the posterior dorsal region of a Scyllium embryo,
belonging to stage H. Zeiss C, ocul. 1. Osmic acid specimen.
It shews the general features of an embryo of stage H, more especially the
relations of the body-cavity in the parietal and vertebral portions of the
lateral plate, and the early-formed band of muscle (_mp´_) in the
splanchnic layer of the vertebral plate.
Fig. 6. Section from the oesophageal region of Scyllium embryo belonging to
stage I. Zeiss C, ocul. 1. Chromic acid specimen.
It shews the formation of the rudiments of the posterior nerve-roots (_pr_)
and of the vertebral rudiments (_Vr_).
Fig. 7. Section of a Torpedo embryo belonging to stage slightly later than
I. Zeiss C, ocul. 1, reduced 1/3. Osmic acid specimen.
It shews (1) the formation of the anterior and posterior nerve-roots. (2)
The solid knob from which the segmental duct (_sd_) originates.
Fig. 8. Section from the dorsal region of a Scyllium embryo belonging to a
stage intermediate between I and K. Zeiss C, ocul. 1. Chromic acid
specimen.
It illustrates the structure of the primitive ova, segmental tubes,
notochord, etc.
Fig. 8_a_. Section from the caudal region of an embryo of the same age as
8. Zeiss A, ocul. 1.
It shews (1) the solid oesophagus. (2) The narrow passage connecting the
pericardial (_pc_) and body cavities (_pp_).
Fig. 9. Section of a Pristiurus embryo belonging to stage K. Zeiss A, ocul.
1. Osmic acid specimen.
It shews the formation of the liver (_l_), the structure of the anterior
fins (_b_), and the anterior opening of the segmental duct into the
body-cavity (_sd_).
Figs. 9_a_, 9_b_, 9_c_, 9_d_. Four sections through the anterior region of
the same embryo as 9. Osmic acid specimens.
The sections shew (1) the atrophy of the post-anal section of the
alimentary tract (9_b_, 9_c_, 9_d_). (2) The existence of the segmental
tubes behind the anus (9_b_, 9_c_, 9_d_). With reference to these it
deserves to be noted that the segmental tubes behind the anus are quite
disconnected, as is proved by the fact that a tube is absent on one side in
9_c_ but reappears in 9_d_. (3) The downward prolongation of the segmental
duct to join the posterior or cloacal extremity of the alimentary tract
(9_b_).
PLATE 12.
Fig. 10. Longitudinal and horizontal section of a Scyllium embryo of stage
H. Zeiss C, ocul. 1. Reduced by 1/3. Picric acid specimen.
It shews (1) the structure of the notochord; (2) the appearance of the
early formed band of muscles (_mp´_) in the splanchnic layer of the
protovertebra.
Fig. 11. Longitudinal and horizontal sections of an embryo belonging to
stage I. Zeiss C, ocul. 1. Chromic acid specimen. It illustrates the same
points as the previous section, but in addition shews the formation of the
rudiments of the vertebral bodies (_Vr_) which are seen to have the same
segmentation as the muscle-plates.
Fig. 12.[227] Longitudinal and horizontal section of an embryo belonging to
the stage intermediate between I and K. Zeiss C, ocul. 1. Osmic acid
specimen illustrating the same points as the previous section.
Footnote 227: The apparent structure in the sheath of the
notochord in this and the succeeding figure is merely the
result of an attempt on the part of the engraver to represent
the dark colour of the sheath in the original figure.
Fig. 13. Longitudinal and horizontal section of an embryo belonging to
stage K. Zeiss C, ocul. 1, and illustrating same points as previous
section.
Figs. 14_a_, 14_b_, 14_c_, 14_d_. Figures taken from preparations of an
embryo of an age intermediate between I and K, and illustrating the
structure of the primitive ova. Figs. 14_a_ and 14_b_ are portions of
transverse sections. Zeiss C, ocul. 3 reduced 1/3. Figs. 14_c_ and 14_d_
are individual ova, shewing the lobate form of nucleus. Zeiss F, ocul. 2.
Fig. 15. Osmic acid preparation of primitive ova belonging to stage K.
Zeiss immersion No. 2, ocul. 1. The protoplasm of the ova is seen to be
nearly filled with bodies resembling yolk-spherules: and one ovum is
apparently undergoing division.
Fig. 15_a_. Picric acid preparation shewing a primitive ovum partially
filled with bodies resembling yolk-spherules.
Fig. 16. Horizontal and longitudinal section of Scyllium embryo belonging
to stage K. Zeiss A, ocul. 1. Picric acid preparation. The
connective-tissue cells are omitted.
The section shews that there is one segmental tube to each vertebral
segment.
Fig. 17. Portion of a Scyllium embryo belonging to stage K, viewed as a
transparent object.
It shews the segmental duct and the segmental involutions--two of which are
seen to belong to segments behind the end of the alimentary tract.
Fig. 18. Vertical longitudinal section of a Scyllium embryo belonging to
stage K. Zeiss A, ocul. 1. Hardened in a mixture of osmic and chromic acid.
It shews
(1) the commissures connecting together the posterior roots of the spinal
nerves;
(2) the junction of the anterior and posterior roots;
(3) the relations of the segmental ducts to the segmental involutions and
the alternation of calibre in the segmental tube;
(4) the germinal epithelium lining the body-cavity.
CHAPTER VII.
GENERAL DEVELOPMENT OF THE TRUNK FROM STAGE H
TO THE CLOSE OF EMBRYONIC LIFE.
_External Epiblast._
The change already alluded to in the previous chapter (p. 317) by which the
external epiblast or epidermis becomes divided into two layers, is
completed before the close of stage L.
In the tail region at this stage three distinct strata may be recognized in
the epidermis. (1) An outer stratum of flattened horny cells, which fuse
together to form an almost continuous membrane. (2) A middle stratum of
irregular partly rounded and partly flattened cells. (3) An internal
stratum of columnar cells, bounded towards the mesoblast by a distinct
basement membrane (Pl. 13, fig. 8), unquestionably pertaining to the
epiblast. This layer is especially thickened in the terminal parts of the
paired fins (Pl. 13, fig. 1). The two former of these strata together
constitute the epidermic layer of the skin, and the latter the mucous
layer.
In the anterior parts of the body during stage L the skin only presents two
distinct strata, viz. an inner somewhat irregular layer of rounded cells,
the mucous layer, and an outer layer of flattened cells (Pl. 13, fig. 8).
The remaining history of the external epiblast, consisting as it does of a
record of the gradual increase in thickness of the epidermic strata, and a
topographical description of its variations in structure and thickness in
different parts, is of no special interest and need not detain us here.
In the late embryonic periods subsequent to stage Q the layers of the skin
cease to be so distinct as at an earlier period, partly owing to the
innermost layer becoming less columnar, and partly to the presence of a
large number of mucous cells, which have by that stage made their
appearance.
I have followed with some care the development of the placoid scales, but
my observations so completely accord with those of Dr O. Hertwig[228], that
it is not necessary to record them. The so-called enamel layer is a simple
product of the thickening and calcification of the basement membrane, and
since this membrane is derived from the mucous layer of the epidermis, the
enamel is clearly to be viewed as an epidermic product. There is no
indication of a gradual conversion of the bases of the columnar cells
forming the mucous layer of the epidermis into enamel prisms, as is
frequently stated to occur in the formation of the enamel of the teeth in
higher Vertebrates.
Footnote 228: _Jenaische Zeitschrift_, Vol. VIII.
_Lateral line._
The lateral line and the nervous structures appended to it have been
recently studied from an embryological point of view by Götte[229] in
Amphibians and by Semper[230] in Elasmobranchii.
Footnote 229: _Entwicklungsgeschichte d. Unke._
Footnote 230: _Urogenitalsystem d. Selachier._ Semper's
_Arbeiten_, Bd. II.
The most important morphological result which these two distinguished
investigators believe themselves to have arrived at is the direct
derivation of the lateral nerve from the ectoderm. On this point there is a
complete accord between them, and Semper especially explains that it is
extremely easy to establish the fact.
As will appear from the sequel, I have not been so fortunate as Semper in
elucidating the origin of the lateral nerve, and my observations bear an
interpretation not in the least in accordance with the views of my
predecessors, though not perhaps quite conclusive against them.
It must be premised that two distinct structures have to be dealt with,
viz. the _lateral line_ formed of modified epidermis, and the _lateral
nerve_ whose origin is in question.
The lateral line is the first of the two to make its appearance, at a stage
slightly subsequent to K, in the form of a linear thickening of the inner
row of cells of the external epiblast, on each side, at the level of the
notochord.
This thickening, in my youngest embryo in which it is found, has but a very
small longitudinal extension, being present through about 10 thin sections
in the last part of the head and first part of the trunk. The thickening,
though short, is very broad, measuring about 0.28 Mm. in transverse
section, and presents no signs of a commencing differentiation of nervous
structures. The large intestinal branch of the vagus can be seen in all the
anterior sections in close proximity to this line, and appears to me to
give off to it posteriorly a small special branch which can be traced
through a few sections, vide Pl. 13, fig. 2, _n.l_. But this branch is not
sufficiently well marked to enable me to be certain of its real character.
In any case the posterior part of the lateral line _is absolutely without
any adjoining nervous structures or traces of such_.
The rudiment of the epidermic part of the lateral line is formed of
specially elongated cells of the mucous layer of the epiblast, but around
the bases of these certain rounder cells of a somewhat curious appearance
are intercalated.
There is between this and my next youngest embryo an unfortunately large
gap with reference to the lateral line, although in almost every other
respect the two embryos might be regarded as belonging to the same stage.
The lateral line in the older embryo extends from the hind part of the head
to a point well behind the anus, and is accompanied by a nerve for at least
two-thirds of its length.
In the foremost section in which it appears the intestinal branch of the
vagus is situated not far from it, _and may be seen at intervals giving off
branches to it_. There is no sign that these are otherwise than perfectly
normal branches of the vagus. Near the level of the last visceral cleft the
intestinal branch of the vagus gives off a fair-sized branch, which from
the first occupies a position close to the lateral line though well within
the mesoblast (Pl. 13, fig. 3_a_, _n.l_). This branch is the lateral nerve,
and though somewhat larger, is otherwise much like the nerve I fancied I
could see originating from the intestinal branch of the vagus during the
previous stage.
It rapidly thins out posteriorly and also approaches closer and closer to
the lateral line. At the front end of the trunk it is quite in contact with
it, and a short way behind this region the cells of the lateral line
arrange themselves in a gable-like form, in the angle of which the nerve is
situated (Pl. 13, figs. 3_b_, and 3_c_). In this position the nerve though
small is still very distinct in all good sections, and is formed of a rod
of protoplasm, with scattered nuclei, in which I could not detect a
distinct indication of cell-areas. The hinder part of the nerve becomes
continually smaller and smaller, without however presenting any indication
of becoming fused with the epiblast, and eventually ceases to be visible
some considerable distance in front of the posterior end of the lateral
line.
The lateral line itself presents some points of not inconsiderable
interest. In the first place, it is very narrow anteriorly and throughout
the greater part of its length, but widens out at its hinder end, and is
widest of all at its termination, which is perfectly abrupt. The following
measurements of it were taken from an embryo belonging to stage L, which
though not quite my second youngest embryo is only slightly older. At its
hinder end it was 0.17 Mm. broad. At a point not far from this it was
0.09 Mm. broad, and anteriorly it was 0.05 Mm. broad. These measurements
clearly shew that the lateral line is broadest at what may be called its
growing-point, a fact which explains its extraordinary breadth in the
anterior part of the body at my first stage, viz. 0.28 Mm., a breadth which
strangely contrasts with the breadth, viz. 0.05 Mm., which it has in the
same part of the body at the present stage.
It still continues to form a linear area of modified epidermis, and has no
segmental characters. Anteriorly it is formed by the cells of the mucous
layer becoming more columnar (Pl. 13 fig. 3_a_). In its middle region the
cells of the mucous layer in it are still simply elongated, but, as has
been said above, have a gable-like arrangement, so as partially to enclose
the nerve (Pl. 13, fig. 3_b_). Nearer the hind end of the trunk a space
appears in it between its columnar cells and the flattened cells of the
outermost layer of the skin (Pl. 13, fig. 3_c_), and this space becomes
posteriorly invested by a very definite layer of cells. The space (Pl. 13,
fig. 3_d_) or lumen has a slit-like section, and is not formed by the
closing in of an originally open groove, but by the formation of a cavity
in the midst of the cells of the lateral line. Its walls are formed by a
layer of columnar cells on the inner side, and flattened cells on the outer
side, both layers however appearing to be derived from the mucous layer of
the epidermis. The outer layer of cells attains its greatest thickness
dorsally.
During stages M, N, O, the lateral nerve gradually passes inwards into the
connective tissue between the dorso-lateral and the ventro-lateral muscles,
and becomes even before the close of stage N completely isolated from the
lateral line.
The growth of the lateral line itself remains for some time almost
stationary; anteriorly the cells retain the gable-like arrangement which
characterised them at an earlier period, but cease to enclose the nerve;
posteriorly the line retains its original more complicated constitution as
a closed canal. In stage O the cells of the anterior part of the line, as
well as those of the posterior, commence to assume a tubular arrangement,
and the lateral line takes the form of a canal. The tubular form is due to
a hollowing out of the lateral line itself and a rearrangement of its
cells. As the lateral line becomes converted into a canal it recedes from
the surface.
In stage P the first indication of segmental apertures to the exterior make
their appearance, vide Pl. 13, fig. 4. The lateral line forms a canal
situated completely below the skin, but at intervals (corresponding with
segments) sends upwards and outwards prolongations towards the exterior.
These prolongations do not during stage P acquire external openings. As is
shewn in my figure, a special area of the inner border of the canal of the
lateral line becomes distinguished by its structure from the remainder.
No account of the lateral line would be complete without some allusion to
the similar sensory structures which have such a wide distribution on the
heads of Elasmobranchii; and this is especially important in the present
instance, owing to the light thrown by a study of their development on the
origin of the nerves which supply the sense-organs of this class. The
so-called mucous canals of the head originate in the same way as does the
lateral line; they are products of the mucous layer of the epidermis. They
eventually form either canals with numerous openings to the exterior, or
isolated tubes with terminal ampulliform dilatations.
I have not definitely determined whether the canal-system of the head
arises in connection with the lateral line, or only eventually becomes so
connected. The important point to be noticed is, that at first no nervous
structures are to be seen in connection with it. In stage O nerves for the
mucous canals make their appearance as delicate branches of the main stems.
These nerve-stems are very much ramified, and their branches have, in a
large number of instances, an obvious tendency towards a particular
sense-organ (Pl. 13, figs. 5 and 6).
I have not during stage O been able to detect a case of direct continuity
between the two. This is, however, established in the succeeding stage P,
in the case of the canals, and the facility with which it may be observed
would probably render the embryo Elasmobranch a very favourable object for
studying the connection between nerves and terminal sense-organs. The nerve
(Pl. 13, fig. 7) dilates somewhat before uniting with the sense-organ, and
the protoplasm of the nerve and the sense-organ become completely fused.
The basement membrane of the skin is not continuous across their point of
junction, and appears to unite with a delicate membrane-like structure,
which invests the termination of the nerve. The ampullæ would seem to
receive their nervous supply somewhat later than the canals, and the
terminal swellings of the nerves supplying them are larger than in the case
of the canals, and the connection between the ampullæ and the nerves not so
clear. In the case of the head, there can for Elasmobranchii be hardly a
question that the nerves which supply the mucous canals grow centrifugally
from the original cranial nerve-stems, and do not originate in a peripheral
manner from the integument.
This is an important point to make certain of in settling any doubtful
features in the nervous supply of the lateral line. Professor Semper[231],
with whom as dealing with Elasmobranchii we are more directly concerned,
makes the following statement: "At the time when at the front end the
lateral nerve has already completely separated itself from the ectoderm,
and is situated amongst the muscles, it still lies in the middle of the
body close to the ectoderm, and at the hind end of the body is not yet
completely segmented off (abgegliedert) from the ectoderm." Although the
last sentence of this quotation may seem to be opposed to my statements,
yet it appears to me probable that Professor Semper has merely seen the
lateral nerve partially enclosed in the ectoderm. This position of the
nerve no doubt affords a _presumption, but only a presumption_, in favour
of a direct origin of the lateral nerve from the ectoderm; but against this
interpretation of it are the following facts:
Footnote 231: _Loc. cit._ p. 398.
(1) That the front part of the lateral line is undoubtedly supplied by
branches which arise in the ordinary way from the intestinal branch of the
vagus; and we should not expect to find part of the lateral line supplied
by nerves which originate in one way, and the remainder supplied by a nerve
having a completely different and abnormal mode of origin.
(2) The growth of the lateral line is quite independent of that of the
lateral nerve: the latter arises subsequently to the lateral line, and, so
far as is shewn by the inconclusive observation of my earliest stage, as an
offshoot from the intestinal branch of the vagus; and though it grows along
at first in close contact with the lateral line, yet it never presents, so
far as I have seen, any indubitable indication of becoming split off from
this, or of fusing with it.
(3) The fact that the cranial representatives of the lateral line are
supplied with nerves which originate in the normal way[232], affords a
strong argument in favour of the lateral line receiving an ordinary
nerve-supply.
Footnote 232: Götte extends his statements about the lateral
nerve to the nerves supplying the mucous canals in the head;
but my observations appear to me, as far as Elasmobranchii are
concerned, nearly conclusive against such a derivation of the
nerves in the head.
Considering all these facts, I am led to the conclusion _that the lateral
nerve in Elasmobranchii arises as a branch of the vagus, and not as a
direct product of the external epiblast_.
An interesting feature about the lateral line and the similar cephalic
structures, is the fact of these being the only sense-organs in
Elasmobranchii which originate entirely from the mucous layer of the
epiblast. This, coupled with the well-known facts about the Amphibian
epiblast, and the fact that the mucous canals are the only sense-organs
which originate subsequently to the distinct differentiation of the
epiblast into mucous and horny layers, goes far to prove[233] that the
mucous layer is to be regarded as the active layer of the epiblast, and
that after this has become differentiated, an organ formed from the
epiblast is always a product of it.
Footnote 233: I believe that Götte, amongst his very numerous
valuable remarks in the _Entwicklungsgeschichte der Unke_, has
put forward a view similar to this, though I cannot put my hand
on the reference.
_Muscle-plates._
The muscle-plates at the close of stage K were flattened angular bodies
with the apex directed forwards, their ventral edge being opposite the
segmental duct, and their dorsal edge on a level with the middle of the
spinal cord. They were composed of two layers, formed for the most part of
columnar cells, but a small part of their splanchnic layer opposite the
notochord had already become differentiated into longitudinal muscles.
During stage L the growth of these plates is very rapid, and their upper
ends extend to the summit of the neural canal, and their lower ones nearly
meet in the median ventral line. The original band of muscles (Pl. 11,
fig. 8, _m.p´_), whose growth was so slow during stages I and K, now
increases with great rapidity, and forms the nucleus of the whole voluntary
muscular system. It extends upwards and downwards by the continuous
conversion of fresh cells of the splanchnic layer into muscle-cells. At the
same time it grows rapidly in thickness, but it requires some little
patience and care to unravel the details of this growth; and it will be
necessary to enter on a slight digression as to the relations of the
muscle-plates to the surrounding connective tissue.
As the muscle-plates grow dorsalwards and ventralwards their ends dive into
the general connective tissue, whose origin has already been described
(Pl. 13, fig. 1). At the same time the connective-tissue cells, which by
this process become situated between the ends of the muscle-plates and the
skin, grow upwards and downwards, and gradually form a complete layer
separating the muscle-plates from the skin. The cells forming the ends of
the muscle-plates retain unaltered their primitive undifferentiated
character, and the separation between them and the surrounding
connective-tissue cells is very marked. This however ceases to be the case
in the parts of the muscle-plates on a level with the notochord and lower
part of the medullary canal; the thinnest sections and most careful
examination are needed to elucidate the changes taking place in this
region. The cells which form the somatic layer of the muscle-plates then
begin to elongate and become converted into muscle-cells, at the same time
that they are increasing in number to meet the rapid demands upon them. One
result of these changes is the loss of the original clearness in the
external boundary between the muscle-plates and the adjoining
connective-tissue cells, which is only in exceptional cases to be seen so
distinctly as it may be in Pl. 13, figs. 1 and 8. Longitudinal horizontal
sections are the most instructive for studying the growth of the muscles,
but transverse sections are also needed. The interpretation of the
transverse ones is however rendered difficult, both by rapid alterations in
the thickness of the connective-tissue layer between the skin and the
muscle-plates (shewn in Pl. 13, fig. 8), and by the angular shape of the
muscle-plates themselves.
A careful study of both longitudinal and transverse sections has enabled me
to satisfy myself of the fact that the cells of the somatic layer of the
protovertebræ, equally with the cells of the splanchnic layer, are
converted into muscle-cells, and some of these are represented in the act
of undergoing this conversion in Pl. 13, fig. 8; but the difficulty of
distinguishing the outline of the somatic layer of the muscle-plates, at
the time its cells become converted into muscle-cells, renders it very
difficult to determine whether any cells of this layer join the surrounding
connective tissue. General considerations certainly lead me to think that
they do not; but my observations do not definitely settle the point.
From these facts it is clear, as was briefly stated in the last chapter,
_that both layers of the muscle-plate are concerned in forming the great
lateral muscle, though the splanchnic layer is converted into muscles very
much sooner than the somatic_[234].
Footnote 234: The difference between Dr Götte's account of the
development of the muscles and my own consists mainly in my
attributing to the somatic layer of the muscle-plates a share
in the formation of the great lateral muscles, which he denies
to it. In an earlier section of this Monograph, pp. 333, 334,
too much stress was unintentionally laid on the divergence of
our views; a divergence which appears to have, in part at
least, arisen, not from our observations being opposed, but
from Dr Götte's having taken the highly differentiated
Bombinator as his type instead of the less differentiated
Elasmobranch.
The remainder of the history of the muscle-plates presents no points of
special interest.
Till the close of stage L, the muscle-plates are not distinctly divided
into dorsal and ventral segments, but this division, which is so
characteristic of the adult, commences to manifest itself during stage M,
and is quite completed in the succeeding stage. It is effected by the
appearance, nearly opposite the lateral line, of a layer of connective
tissue which divides the muscles on each side into a dorso-lateral and
ventro-lateral section. Even during stage O the ends of the muscle-plates
are formed of undifferentiated columnar cells. The peculiar outlines of the
intermuscular septa gradually appear during the later stages of
development, causing the well-known appearances of the muscles in
transverse sections, but require no special notice here.
With reference to the histological features of the development of the
muscle-fibres, I have not pushed my investigations very far. The primitive
cells present the ordinary division, well known since Remak, into a
striated portion and a non-striated portion, and in the latter a nucleus is
to be seen which soon undergoes division and gives rise to several nuclei
in the non-striated part, while the striated part of each cell becomes
divided up into a number of fibrillæ. I have not however determined what
exact relation the original cells hold to the eventual primitive bundles,
or anything with reference to the development of the sarcolemma.
_The Muscles of the Limbs._--These are formed during stage O coincidently
with the cartilaginous skeleton, in the form of two bands of longitudinal
fibres on the dorsal and ventral surfaces of the limbs. Dr Kleinenberg
first called my attention to the fact that he had proved the limb-muscles
in _Lacerta_ to be derived from the muscle-plates. This I at first believed
did not hold good for Elasmobranchii, but have since determined that it
does so. Between stages K and L the muscle-plates grow downwards as far as
the limbs and then turn outwards and grow into them (Pl. 18, fig. 1). Small
portions of several muscle-plates come in this way to be situated in the
limbs, and are very soon segmented off from the remainder of the
muscle-plates. The portions of muscle-plates thus introduced into the limbs
soon lose their original distinctness, and can no longer be recognized in
stage L. There can however be but little doubt that they supply the tissue
for the muscles of the limbs. The muscle-plates themselves after giving off
these buds to the limbs grow downwards, and by stage L cease to shew any
trace of what has occurred (Pl. 13, fig. 1). This fact, coupled with the
late development of the muscles of the limbs (stage O), caused me to fall
into my original error.
_The Vertebral Column and Notochord._
In the previous chapter (p. 325) an account was given of the origin of the
tissue destined to form the vertebral bodies; it merely remains to describe
the changes undergone by this in becoming converted into the permanent
vertebræ.
This subject has already been dealt with by a considerable number of
anatomists, and my investigations coincide in the main with the results of
my predecessors. Especially the researches of Gegenbaur[235] may be singled
out as containing the pith of the whole subject, and my results, while
agreeing in all but minor points with his, do not supplement them to any
very great extent. I cannot do more than confirm Götte's[236] account of
the development of the hæmal arches, and may add that Cartier[237] has
given a good account of the later development of the centra. Under the
circumstances it has not appeared to me to be worth while recording with
great detail my investigations; but I hope to be able to give a somewhat
more complete history of the whole subject than has appeared in any single
previous memoir.
Footnote 235: _Das Kopfskelet d. Selachier_, p. 123.
Footnote 236: _Entwicklungsgeschichte d. Unke_, pp. 433-4.
Footnote 237: _Zeitschrift f. Wiss. Anat._ Bd. XXV.,
Supplement.
At their first appearance the cells destined to form the permanent vertebræ
present the same segmentation as the muscle-plates. This segmentation soon
disappears, and between stages K and L the tissue of the vertebral column
forms a continuous investment of the notochord which cannot be
distinguished from the adjoining connective tissue. Immediately surrounding
the notochord a layer formed of a single row of cells may be observed,
which is not however very distinctly marked[238].
Footnote 238: Vide pp. 356, 357.
During the stage L there appear four special concentrations of mesoblastic
tissue adjoining the notochord, two of them dorsal and two of them ventral.
They are not segmented, and form four ridges seated on the sides of the
notochord. They are united with each other by a delicate layer of tissue,
and constitute the rudiments of the neural and hæmal arches. In
longitudinal sections of stage L special concentrated wedge-shaped masses
of tissue are to be seen between the muscle-plates, which must not be
confused with these rudiments. Immediately around the notochord the
delicate investment of cells previously mentioned, is still present.
The rudiments of the arches increase in size and distinctness in the
succeeding stages, and by stage N have unquestionably assumed the
constitution of embryonic cartilage. In the meantime there has appeared
surrounding the sheath of the notochord a well-marked layer of tissue which
stains deeply with hæmatoxylin, and with the highest power may be observed
to contain flattened nuclei. It is barely thicker than the adjoining
sheath, but is nevertheless the rudiment of the vertebral bodies. Pl. 13,
fig. 9, _vb_. Whence does this layer arise? To this question I cannot give
a quite satisfactory answer. It is natural to conclude that it is derived
from the previously existing mesoblastic investment of the notochord, but
in the case of the vertebral column I have not been able to prove this.
Observations on the base of the brain afford fairly conclusive evidence
that the homologous tissue present there has this origin. Gegenbaur
apparently answers the question of the origin of this layer in the way
suggested above, and gives a figure in support of his conclusion (Pl. XXII.
fig. 3)[239].
Footnote 239: None of my specimens resembles this figure, and
the layer when first formed is in my embryos much thinner than
represented by Gegenbaur, and the histological structure of the
embryonic cartilage is very different from that of the
cartilage in the figures alluded to. Götte's very valuable
researches with reference to the origin of this layer in
Amphibians tend to confirm the view advocated in the text.
The layer of tissue which forms the vertebral bodies rapidly increases in
thickness, and very soon, at a somewhat earlier period than represented in
Gegenbaur's Pl. XXII. fig. 4, a distinct membrane (Kölliker's Membrana
Elastica Externa) may easily be recognized surrounding it and separating it
from the adjoining tissue of the arches. Gegenbaur's figure gives an
excellent representation of the appearance of this layer at the period
under consideration. It is formed of a homogeneous basis containing
elongated concentrically arranged nuclei, and constitutes a uniform
unsegmented investment for the notochord (vide Pl. 13, fig. 10).
The neural and hæmal arches now either cease altogether to be united with
each other by a layer of embryonic cartilage, or else the layer uniting
them is so delicate that it cannot be recognized as true cartilage. They
have moreover by stage P undergone a series of important changes. The
tissue of the neural arches does not any longer form a continuous sheet,
but is divided into (1) a series of arches encircling the spinal cord, and
(2) a basal portion resting on the cartilaginous sheath of the notochord.
There are two arches to each muscle-plate, one continuous with the basal
portion of the arch-tissue and forming the true arch, which springs
opposite the centre of a vertebral body, and the second not so continuous,
which forms what is usually known as the intercalated piece. Between every
pair of true arches the two roots of a single spinal nerve pass out. The
anterior root passes out in front of an intercalated piece and the
posterior behind it[240].
Footnote 240: In the adult Scyllium it is well known that the
posterior root pierces the intercalated cartilage and the
anterior root the true neural arch. This however does not seem
to be the case in the embryo at stage P.
The basal portion of the arch-tissue likewise undergoes differentiation
into a vertebral part continuous with the true arch and formed of hyaline
cartilage, and an intervertebral segment formed of a more fibrous tissue.
The hæmal arches, like the neural arches, become divided into a layer of
tissue adjoining the cartilaginous sheath of the notochord, and processes
springing out from this opposite the centres of the vertebræ. These
processes throughout the region of the trunk in front of the anus pass into
the space between the dorsal and ventral muscles, and are to be regarded as
rudiments of ribs. The tissue with which they are continuous, which is
exactly equivalent to the tissue from which the neural arches originate, is
not truly a part of the rib. In the tail, behind the anus and kidneys, the
cardinal veins fuse to form an unpaired caudal vein below the aorta, and in
this part a fresh series of processes originates on each side from the
hæmal tissue adjoining the cartilaginous sheath of the notochord, and
eventually, by the junction of the processes of the two sides, a canal
which contains the aorta and caudal vein is formed below the notochord.
These processes for a few segments coexist with small ribs (vide Pl. 13,
fig. 10), a fact which shews (1) that they cannot be regarded as modified
ribs, and (2) that the tissue from which they spring is to be viewed as a
kind of general basis for all the hæmal processes which may arise, and is
not specially connected with any one set of processes.
While these changes (all of which are effected during stage P) are taking
place in the arches, the tissue of the vertebral bodies or cartilaginous
investment of the notochord, though much thicker than before, still remains
as a continuous tube whose wall exhibits no segmental differentiations.
It is in stage Q that these differentiations first appear in the vertebral
regions opposite the origin of the neural arches. The outermost part of the
cartilage at these points becomes hyaline and almost undistinguishable in
structure from the tissue of the arches[241]. These patches of hyaline
cartilage grow larger and cause the vertebral parts of the column to
constrict the notochord, whilst the intervertebral parts remain more
passive, but become composed of cells with very little intercellular
substance. Coincidently also with these changes, part of the layer internal
to the hyaline cartilage becomes modified to form a somewhat peculiar
tissue, the intercellular substance of which does not stain, and in which
calcification eventually arises (Pl. 13, fig. 11). The innermost layer
adjoining the notochord retains its primitive fibrous character, and is
distinguishable as a separate layer through both the vertebral and the
intervertebral regions. As a result of these changes a transverse section
through the centre of the vertebral regions now exhibits three successive
rings (vide Pl. 13, fig. 11), an external ring of hyaline cartilage
invested by "the membrana elastica externa" (_m.el_), followed by a ring of
calcifying cartilage, and internal to this a ring of fibrous cartilage,
which adjoins the now slightly constricted notochord. A transverse section
of an intervertebral region shews only a thick outer and thin inner ring of
fibrous cartilage, the latter in contact with the sheath of the
unconstricted notochord.
Footnote 241: A good representation of a longitudinal section
at this stage is given by Cartier (_Zeitschrift f. Wiss.
Zoologie_, Bd. XXV., Supplement Pl. IV. fig. 1), who also gives
a fair description of the succeeding changes of the vertebral
column.
The constriction of the notochord proceeds till in the centre of the
vertebræ it merely forms a fibrous band. The tissue internal to the
calcifying cartilage then becomes hyaline, so that there is formed in the
centre of each vertebral body a ring of hyaline cartilage immediately
surrounding the fibrous band which connects the two unconstricted segments
of the notochord. The intervertebral tissue becomes more and more fibrous.
In Cartier's paper before quoted there is a figure (fig. 3) which
represents the appearance presented by a longitudinal section of the
vertebral column at this stage.
The relation of the vertebral bodies to the arches requires a short notice.
The vertebral hyaline cartilage becomes almost precisely similar to the
tissue of the arches, and the result is, that were it not for the "membrana
elastica externa" it would be hardly possible to distinguish the limits of
the two tissues. This membrane however persists till the hyaline cartilage
has become a very thick layer (Pl. 13, fig. 11), but I have failed to
detect it in the adult, so that I cannot there clearly distinguish the
arches from the body of the vertebræ. From a comparison however of the
adult with the embryo, it is clear that the arches at most form but a small
part of what is usually spoken of as the body of the vertebræ.
The changes in the notochord itself during the stages subsequent to K are
not of great importance. The central part retains for some time its
previous structure, being formed of large vacuolated cells with an
occasional triangular patch of protoplasm containing the starved nucleus
and invested by indurated layers of protoplasm. These indurated layers are
all fused, and are probably rightly regarded by Gegenbaur and Götte as
representing a sparse intercellular matter. The external protoplasmic layer
of the notochord ceases shortly after stage K to exhibit any traces of a
division into separate cells, but forms a continuous layer with irregular
prominences and numerous nuclei (Pl. 13, fig. 9). In the stages subsequent
to P further changes take place in the notochord: the remains of the cells
become more scanty and the intercellular tissue assumes a radiating
arrangement, giving to sections of the notochord the appearance of a number
of lines radiating from the centre to the periphery (Pl. 13, fig. 11).
The sheath of the notochord at first grows in thickness, and during stage L
there is no difficulty in seeing in it the fine radial markings already
noticed by Müller[242] and Gegenbaur[243], and regarded by them as
indicating pores. Closely investing the sheath of the notochord there is to
be seen a distinct membrane, which, though as a rule closely adherent to
the sheath, in some examples separates itself from it. It is perhaps the
membrane identified by W. Müller[244] (though not by Gegenbaur) as
Kölliker's "membrana elastica interna." After the formation of the
cartilaginous investment of the notochord, this membrane becomes more
difficult to see than in the earlier stage, though I still fancy that I
have been able to detect it. The sheath of notochord also appears to me to
become thinner, and its radial striation is certainly less easy to
detect[245].
Footnote 242: _Jenaische Zeitschrift_, Vol. VI.
Footnote 243: _Loc. cit._
Footnote 244: _Loc. cit._
Footnote 245: Gegenbaur makes the reserve statement with
reference to the sheath of the notochord. For my own sections
the statement in the text certainly holds good. Fortunately the
point is one of no importance.
EXPLANATION OF PLATE 13.
COMPLETE LIST OF REFERENCE LETTERS.
_al._ Alimentary tract. _ao._ Aorta. _c._ Connective tissue. _cav._
Cardinal vein. _ch._ Notochord. _ep._ Epiblast. _ha._ Hæmal arch. _l._
Liver. _ll._ Lateral line. _mc._ Mucous canal of the head. _mel._ Membrana
elastica externa. _mp._ Muscle-plate. _mp´._ Muscles of muscle-plate. _na._
Neural arch. _nl._ Nervus lateralis. _rp._ Rib process. _sd._ Segmental
duct. _sh._ Sheath of notochord. _spc._ Spinal cord. _spg._ Spinal
ganglion. _syg._ Sympathetic ganglion. _um._ Ductus choledochus. _v._
Blood-vessel. _var._ Vertebral arch. _vb._ Vertebral body. _vcau._ Caudal
vein. _vin._ Intestinal branch of the vagus. _vop._ Ramus ophthalmicus of
the fifth nerve. _x._ Subnotochordal rod.
Fig. 1. Section through the anterior part of an embryo of _Scyllium
canicula_ during stage L.
_c._ Peculiar large cells which are found at the dorsal part of the spinal
cord. Sympathetic ganglion shewn at _syg._ Zeiss A, ocul. 1.
Fig. 2. Section through the lateral line at the time of its first
formation.
The cells marked _nl_ were not sufficiently distinct to make it quite
certain that they really formed part of the lateral nerve. Zeiss B, ocul.
2.
Figs. 3_a_, 3_b_, 3_c_, 3_d_. Four sections of the lateral line from an
embryo belonging to stage L. 3_a_ is the most anterior. In 3_a_ the lateral
nerve (_nl_) is seen to lie in the mesoblast at some little distance from
the lateral line. In 3_b_ and 3_c_ it lies in immediate contact with and
partly enclosed by the modified epiblast cells of the lateral line. In
3_d_, the hindermost section, the lateral line is much larger than in the
other sections, but no trace is present of the lateral nerve. The sections
were taken from the following slides of my series of the embryo (the series
commencing at the tail end) 3_d_ (46), 3_c_ (64), 3_b_ (84), 3_a_ (93). The
figures all drawn on the same scale, but 3 _a_ is not from the same side of
the body as the other sections.
Fig. 4. Section through lateral line of an embryo of stage P at the point
where it is acquiring an opening to the exterior. The peculiar modified
cells of its innermost part deserve to be noticed. Zeiss D, ocul. 2.
Fig. 5. Mucous canals of the head with branches of the ramus ophthalmicus
growing towards them. Stage O. Zeiss A, ocul. 2.
Fig. 6. Mucous canals of head with branches of the ramus ophthalmicus
growing towards them. Stage between O and P. Zeiss a a, ocul. 2.
Fig. 7. Junction of a nerve and mucous canal. Stage P. Zeiss D, ocul. 2.
Fig. 8. Longitudinal and horizontal section through the muscle-plates and
adjoining structures at a stage intermediate between L and M. The section
is intended to shew the gradual conversion of the cells of the somatic
layer of muscle-plates into muscles.
Fig. 9. Longitudinal section through the notochord and adjoining parts to
shew the first appearance of the cartilaginous notochordal sheath which
forms the vertebral centra. Stage N.
Fig. 10. Transverse section through the tail of an embryo of stage P to
shew the coexistence of the rib-process and hæmal arches in the first few
sections behind the point where the latter appear. Zeiss C, ocul. 1.
Fig. 11. Transverse section through the centre of a caudal vertebra of an
embryo somewhat older than Q. It shews (1) the similarity between the
arch-tissue and the hyaline tissue of the outer layer of the vertebral
centrum, and (2) the separation of the two by the membrana elastica
externa[246] (_mel_). It shews also the differentiation of three layers in
the vertebral centrum: vide p. 374.
Footnote 246: The slight difference observable between these
two tissues in the arrangement of their nuclei has been much
exaggerated by the engraver.
CHAPTER VIII.
DEVELOPMENT OF THE SPINAL NERVES AND OF THE SYMPATHETIC NERVOUS SYSTEM.
_The spinal nerves._
The development of the spinal nerves has been already treated by me at
considerable length in a paper read before the Royal Society in December,
1875[247], and I have but little fresh matter to add to the facts narrated
in that paper. The succeeding account, though fairly complete, is much less
full than the previous one in the _Philosophical Transactions_, but a
number of morphological considerations bearing on this subject are
discussed.
Footnote 247: _Phil. Trans._ Vol. 166, p. 175. [This Edition,
No. VIII.]
The rudiments of the posterior roots make their appearance considerably
before those of the anterior roots. They arise during stage I, as
outgrowths from the spinal cord, at a time when the muscle-plates do not
extend beyond a third of the way up the sides of the spinal cord, and in a
part where no scattered mesoblast-cells are present. They are formed first
in the anterior part of the body and successively in the posterior parts,
in the following way. At a point where a spinal nerve is about to arise,
the cells of the dorsal part of the cord begin to proliferate, and the
uniform outline of the cord becomes broken (Pl. 14, fig. 3). There is
formed in this way a small prominence of cells springing from the summit of
the spinal cord, and constituting a rudiment of a pair of posterior roots.
In sections anterior to the point where a nerve is about to appear, the
nerve-rudiments are always very distinctly formed. Such a section is shewn
in Pl. 14, fig. 2, and the rudiments may there be seen as two club-shaped
masses of cells, which have grown outwards and downwards from the extreme
dorsal summit of the neural canal and in contact with its walls. The
rudiments of the two sides meet at their point of origin at the dorsal
median line, and are dorsally perfectly continuous with the walls of the
canal.
It is a remarkable fact that rudiments of posterior roots are to be seen in
every section. This may be interpreted as meaning that the rudiments are in
very close contact with each other, but more probably means, as I hope to
shew in the sequel, that there arises from the spinal cord a continuous
outgrowth from which discontinuous processes (the rudiments of posterior
roots) grow out.
After their first formation these rudiments grow rapidly ventralwards in
close contact with the spinal cord (vide Pl. 14, fig. 1, and Pl. 11, figs.
6 and 7), but soon meet with and become partially enclosed in the
mesoblastic tissue (Pl. 11, fig. 7). The similarity of the mesoblast and
nerve-tissue in Scyllium and Pristiurus embryos hardened in picric or
chromic acid, render the nerves in these genera, at the stage when they
first become enveloped in mesoblast, difficult objects to observe; but no
similar difficulty is encountered in the case of Torpedo embryos.
While the rudiments of the posterior roots are still quite short, those of
the anterior roots make their first appearance. Each of these (Pl. 14,
fig. 4, _a.r._) arises as a very small but distinct conical outgrowth from
a ventral corner of the spinal cord. From the very first the rudiments of
the anterior roots have an indistinct form of peripheral termination and
somewhat fibrous appearance, while the protoplasm of which they are
composed becomes attenuated towards its end. The points of origin of the
anterior roots from the spinal cord are separated by considerable
intervals. In this fact, and also in the fact of the nerves of the two
sides never being united with each other in the median line, the anterior
roots exhibit a marked contrast to the posterior. There are thus
constituted, before the close of stage I, the rudiments of both the
anterior and posterior roots of the spinal nerves. The rudiments of both of
these take their origin from the involuted epiblast of the neural canal,
and the two roots of each spinal nerve are at first quite unconnected with
each other. It is scarcely necessary to state that the pairs of roots
correspond in number with the muscle-plates.
It is not my intention to enter with any detail into the subsequent changes
of the rudiments whose origin has been described, but a few points
especially connected with their early development are sufficiently
important to call for attention.
One feature of the posterior roots at their first formation is the fact
that they appear as processes of a continuous outgrowth of the spinal cord.
This state of affairs is not of long continuance, and before the close of
stage I each posterior root has a separate junction with the spinal cord.
What then becomes of the originally continuous outgrowth? It has not been
possible for me to trace the fate of this step by step; but the discovery
that at a slightly later period (stage K) there is present a continuous
commissure independent of the spinal cord connecting the dorsal and central
extremities of all the spinal nerves, renders it very probable that the
original continuous outgrowth becomes converted into this commissure. Like
all the other nervous structures, this commissure is far more easily seen
in embryos hardened in a mixture of osmic and chromic acids or osmic acid,
than in those hardened in picric acid. Its existence must be regarded as
one of the most remarkable results of my researches upon the Elasmobranch
nervous system. At stage K it is fairly thick, though it becomes much
thinner at a slightly later period. Its condition during stage K is shewn
in Pl. 12, fig. 18, _com_. What it has been possible for me to make out of
its eventual fate is mentioned subsequently[248].
Footnote 248: It is not by any means always possible to detect
this commissure in transverse sections. As I have suggested, in
connection with a similar commissure connecting the vagus
branches, it perhaps easily falls out of the section, and is
always so small that the hole left would certainly be
invisible.
A second feature of the earliest condition of the posterior roots is their
attachment to the extreme dorsal summit of the spinal cord--a point of
attachment very different from that which they eventually acquire. Before
the commencement of stage K this state of things has become altered; and
the posterior roots spring from the spinal cord in the position normal for
Vertebrates.
This apparent migration caused me at first great perplexity, and I do not
feel quite satisfied that I have yet got completely to the bottom of its
meaning. The explanation which appears to me most probable has suggested
itself in the course of some observations on the development of the thin
roof of the fourth ventricle. A growth of cells appears to take place in
the median dorsal line of the roof of the spinal cord. This growth tends to
divaricate the two lateral parts of the cord, which are originally
contiguous in the dorsal line, and causes therefore the posterior roots,
which at first spring from the dorsal summit, to assume an apparent
attachment to the side of the cord at some little distance from the summit.
If this is the true explanation of the change of position which takes
place, it must be regarded as due rather to peculiar growths in the spinal
cord, than to any alteration in the absolute attachment of the nerves.
By stage K the rudiment of the posterior root has become greatly elongated,
and exhibits a division into three distinct portions (Pl. 14, fig. 6):
(1) A proximal portion, in which is situated the pedicle of attachment to
the wall of the neural canal.
(2) An enlarged portion, which may conveniently from its future fate be
called the spinal ganglion.
(3) A distal portion beyond this.
The proximal portion presents a fairly uniform diameter, and ends dorsally
in a rounded expansion; it is attached, remarkably enough, _not by its
extremity, but by its side, to the spinal cord. The dorsal extremities of
the posterior roots are therefore free._ It seems almost certain that the
free dorsal extremities of these roots serve as the starting points for the
dorsal commissure before mentioned, which connects the roots together. The
attachment of the posterior nerve-root to the spinal cord is, on account of
its small size, very difficult to observe. In favourable specimens there
may however be seen a distinct cellular prominence from the spinal cord,
which becomes continuous with a small prominence on the lateral border of
the nerve-root near its distal extremity. The proximal extremity of the
rudiment is composed of cells, which, by their small size and circular
form, are easily distinguished from those which form the succeeding or
ganglionic portion of the nerve. This succeeding part has a swollen
configuration, and is composed of large elongated cells with oval nuclei.
The remainder of the rudiment forms the commencement of the true nerve.
The anterior root, which, at the close of stage I, formed a small and
inconspicuous prominence from the spinal cord, grows rapidly during the
succeeding stages, and soon forms an elongated cellular structure with a
wide attachment to the spinal cord (Pl. 14, fig. 5). At first it passes
obliquely and nearly horizontally outwards, but, before reaching the
muscle-plate of its side, takes a bend downwards (Pl. 14, fig. 7).
I have not definitely made out when the anterior and posterior roots unite,
but this may easily be seen to take place before the close of stage K
(Pl. 12, fig. 18).
One feature of some interest with reference to the anterior roots, is the
fact that they arise not vertically below, but alternately with the dorsal
roots, a condition which persists in the adult.
Although I have made some efforts to determine the eventual fate of the
commissure uniting the dorsal roots, these have not hitherto been crowned
with success. It grows thinner and thinner, becoming at the same time
composed of fibrous protoplasm with imbedded nuclei (Pl. 14, figs. 8 and
9). By stage M it is so small as to be quite indistinguishable in
transverse sections; and I have failed in stage P to recognize it at all. I
can only conclude that it gradually atrophies, and finally vanishes without
leaving a trace. Both its appearance and history are very remarkable, and
deserve the careful attention of future investigators.
There can be little doubt that it is some sort of remnant of an ancestral
structure in the nervous system; and it would appear to indicate that the
central nervous system must originally have been formed of a median and two
lateral strands. At the same time I very much doubt whether it can be
brought into relation with the three rows of ganglion-cells (a median and
two lateral) which are so frequently present on the ventral side of
annelidan nerve-cords.
_My results may be summarised as follows_:--Along the extreme dorsal summit
of the spinal cord there arises on each side a continuous outgrowth. From
each outgrowth processes corresponding in number to the muscle-plates grow
downwards. These are the rudiments of the posterior nerve-roots. The
outgrowths, though at first attached to the spinal cord throughout their
whole length, soon cease to be so, and remain in connection with it at
certain points only, which form the primitive junctions of the posterior
roots with the spinal cord. The original outgrowth on each side remains as
a bridge, uniting together the dorsal extremities of all the posterior
roots. The posterior roots, though primitively attached to the dorsal
summit of the spinal cord, eventually come to arise from its sides. The
original homogeneous rudiments before the close of stage K become
differentiated into a root, a ganglion, and a nerve.
The anterior roots, like the posterior, are outgrowths from the spinal
cord, but are united independently with it, and the points from which they
spring originally, remain as those by which they are permanently attached.
The anterior roots arise, not vertically below, but in the intervals
between the posterior roots. They are at first quite separate from the
posterior roots; but before the close of stage K a junction is effected
between each posterior root and the corresponding anterior root. The
anterior root joins the posterior at some little distance below its
ganglion.
* * * * *
The results here arrived at are nearly in direct opposition to those of the
majority of investigators, though in accordance, at least so far as the
posterior roots are concerned, with the beautiful observations of Hensen
'on the Development of Mammalia[249].'
Footnote 249: _Zeit. f. Anat. u. Entwicklungsgeschichte_, Vol. I.
Mr Marshall[250] has more recently published a paper on the development of
the nerves in Birds, in which he shews in a most striking manner that the
observations recorded here for Elasmobranchii hold good for the posterior
roots of Birds. The similarity between his figures and my own is very
noticeable. A further discussion of the literature would be quite
unprofitable, and I proceed at once to certain considerations suggested by
the above observations.
Footnote 250: _Journal of Anatomy and Physiology_, Vol. XI.
April, 1877.
_General considerations._ One point of general anatomy upon which my
observations throw considerable light, is the _primitive origin of nerves_.
So long as it was admitted that the spinal and cerebral nerves developed in
the embryo independently of the central nervous system, their mode of
origin always presented to my mind considerable difficulties. It never
appeared clear how it was possible for a state of things to have arisen in
which the central nervous system as well as the peripheral terminations of
nerves, whether motor or sensory, were formed independently of each other;
while between them a third structure was developed, which, growing out
either towards the centre or towards the periphery, ultimately brought the
two into connection. That such a condition could be a primitive one seemed
scarcely possible.
Still more remarkable did it appear, on the supposition that the primitive
mode of formation of these parts was represented in the developmental
history of Vertebrates, that we should find similar structural elements in
the central and in the peripheral nervous systems. The central nervous
system arises from the epiblast, and yet contains precisely similar
nerve-cells and nerve-fibres to the peripheral nervous system, which, when
derived from the mesoblast, was necessarily supposed to have an origin
completely different from that of the central nervous system. Both of these
difficulties are to a great extent removed by the facts of the development
of these parts in Elasmobranchii.
It is possible to suppose that in their primitive differentiation
contractile and sensory systems may, as in Hydra[251], have been developed
from the protoplasm of even the same cell. As the sensory and motor systems
became more complicated, the sensory portion of a cell would become
separated by an increasing interval from the muscular part of a cell, and
the two parts of a cell would only be connected by a long protoplasmic
process. When such a condition as that was reached, the sensory portion of
the cell would be called a ganglion-cell or terminal sensory organ, the
connecting process a nerve, and the contractile portion of the cell a
muscle-cell. When these organs were in this condition, it might not
impossibly happen for the general developmental growth which tended to
separate the ganglion-cell and the muscle-cell to be so rapid as to render
it impossible for the growth of the connecting nerve to keep pace with it,
and that thus the process connecting the ganglion-cell and the muscle-cell
might become ruptured. Nevertheless the tendency of the process to grow
from the ganglion-cell to the muscle-cell, would remain, and when the rapid
developmental growth had ceased, the two would become united again by the
growth of the process which had previously been ruptured. It will be seen
that this hypothesis, which I have considered only with reference to a
single nerve and muscle-cell, might be extended so as to apply to a
complicated central nervous system and peripheral nerves and muscles, and
also could apply equally as well to the sensory as to the motor
terminations of a nerve. In the case of the sensory termination, we should
only have to suppose that the centre nervous cell became more and more
separated by the general growth from the recipient terminal sensory cell,
and that during the general growth the connection between the two was
mechanically ruptured but restored again on the termination of the more
rapid growth.
Footnote 251: Kleinenberg Hydra.
As the descendants of the animal in which the rupture occurred became
progressively more complicated, the two terminal cells must have become
widely separated at a continually earlier period, till finally they may
have been separated at a period of development when they were
indistinguishable from the surrounding embryonic cells; and since the
rupture would also occur at this period, the primitive junction between the
nerve-centre and termination would escape detection. The object of this
hypothesis is to explain the facts, so far as they are known, of the
development of the nervous system in Vertebrates.
In Vertebrates we certainly appear to have an outgrowth from the nervous
system, which eventually becomes united with the muscle or sensory terminal
organs. The ingenious hypothetical scheme of development of the nerves
given by Hensen[252] would be far preferable to the one suggested if it
could be brought into conformity with the facts. There is, however, at
present no evidence for Hensen's view, as he himself admits, but
considering how little we know of the finer details of the development of
nerves, it seems not impossible that such evidence may be eventually
forthcoming. The evidence from my own observation is, so far as it goes,
against it. At a time anterior to the outgrowth of the spinal nerves, I
have shewn[253] that the spinal cord is completely invested by a delicate
hyaline membrane. It is difficult to believe that this is pierced by a
number of fine processes, which completely escape detection, but which
must, nevertheless, be present on the hypothesis of Hensen.
Footnote 252: Virchow's _Archiv_, Vol. XXXI. 1864.
Footnote 253: _Phil. Trans._, 1876. [This Edition, No. VIII.]
The facts of the development of nerves in Vertebrates are unquestionably
still involved in considerable doubt. It may, I think, be considered as
certain, that in Elasmobranchii the roots of the spinal and cranial nerves
are outgrowths of the central nervous system. How the final terminations of
the nerves are formed is, however, far from being settled. Götte[254],
whose account of the development of the spinal ganglia is completely in
accordance with the ordinary views, yet states[255] that the growth of the
nerve fibres themselves is a centrifugal one from the ganglia. My own
investigations prove that the ganglia have a centrifugal development, and
also appear to demonstrate that the nerves themselves near the ganglion
have a similar manner of growth. Moreover, the account given in the
preceding chapter of the manner in which the nerves become connected with
the mucous canals of the head, goes far to prove that the whole growth of
the nerves is a centrifugal one. The combination of all these converging
observations tells strongly in favour of this view.
Footnote 254: _Entwicklungsgeschichte der Unke._
Footnote 255: _Loc. cit._ p. 516.
On the other hand, Calberla[256] believes that in the tails of larval
Amphibians he has seen connective-tissue cells unite with nerve-processes,
and become converted into nerves, but he admits that he cannot definitely
prove that the axis-cylinder has not a centrifugal growth, while the
connective-tissue cells merely become converted into the sheath of the
nerve. If Calberla's view be adopted, that the nerves are developed
directly out of a chain of originally indifferent cells, each cell of the
chain being converted in turn into a section of the nerve, an altogether
different origin of nerves from that I have just suggested would seem to be
indicated.
Footnote 256: _Archiv für Micros. Anat._, Vol. XI. 1875.
The obvious difficulty, already alluded to, of understanding how it is,
according to the generally accepted mode of development of the spinal
nerves, that precisely similar nerve-cells and nerves should arise in
structures which have such different origins as the central nervous system
and the spinal nerves, is completely removed if my statements on the
development of the nerves in Elasmobranch represent the truth.
One point brought out in my investigations appears to me to have bearings
upon the origin of the central canal of the vertebrate nervous system, and
in consequence upon the origin of the vertebrate nervous system itself.
This point is, that the posterior nerve-rudiments make their first
appearance at the extreme dorsal summit of the spinal cord. The transverse
section of the ventral nervous cord of an ordinary segmented Annelid
consists of two symmetrical halves placed side by side. If by a mechanical
folding the two lateral halves of the nervous cord became bent towards each
other, while into the groove between the two the external skin became
pushed, we should have an approximation to the vertebrate nervous system.
Such a folding as this might take place to give extra rigidity to the body
in the absence of a vertebral column.
If this folding were then completed in such a way that the groove, lined by
external skin and situated between the two lateral columns of the nervous
system, became converted into a canal, above and below which the two
columns of the nervous system united, we should have in the transformed
nervous cord an organ strongly resembling the spinal cord of Vertebrates.
It is well known that the nerve-cells are always situated on the ventral
side of the abdominal nerve-cord of Annelids, either as a continuous layer,
or in the form of two, or more usually, three bands. The dorsal side of the
cord is composed of nerve-fibres or white matter. If the folding I have
supposed were to take place in the Annelid nervous cord, the grey and white
matters would have very nearly the same relative situations as they have in
the Vertebrate spinal cord. The grey matter would be situated in the
interior and line the central canal, and the white matter would nearly
surround the grey. The nerves would then arise, not from the sides of the
nervous cord as in existing Annelids, but from its extreme ventral summit.
One of the most striking features which I have brought to light with
reference to the development of the posterior roots, is the fact of their
growing out from the extreme dorsal summit of the neural canal, a position
analogous to the ventral summit of the Annelidan nervous cord. Thus the
posterior roots of the nerves in Elasmobranchii[257] arise, in the exact
manner which might have been anticipated, were the spinal canal due to such
a folding as I have suggested.
Footnote 257: There are strong reasons for regarding the
posterior roots as the primitive ones. These are spoken of
later, but I may state that they depend:
(1) On the fact that only _posterior_ roots exist in the brain.
(2) That only posterior roots exist in Amphioxus.
(3) That the posterior roots develop at an earlier period than
the anterior.
The argument from the position of the outgrowth of nerves becomes the more
striking from its great peculiarity, and forms a feature which would be
most perplexing without some such explanation as I have proposed. The
central epithelium of the neural canal, according to this view, represents
the external skin, and its ciliation in certain cases may, perhaps, be
explained as a remnant of the ciliation of the external skin still found
amongst many of the lower Annelids.
I have employed the comparison of the Vertebrate and Annelidan nervous
cords, not so much to prove a genetic relation between the two, as to shew
the _à priori_ possibility of the formation of a spinal cord, and the _à
posteriori_ evidence we have of the vertebrate canal having been formed in
the way indicated. I have not made use of what is really my strongest
argument, viz. that the embryological mode of formation of the spinal canal
by a folding in of the external epiblast is the very method by which I
supposed the spinal canal to have been formed in the ancestors of
Vertebrates. My object has been to suggest a meaning for the peculiar
primitive position of the posterior roots, rather than to attempt to
explain in full the origin of the spinal canal.
Although the homologies between the Vertebrate and the Annelidan nervous
systems are not necessarily involved in the questions which arise with
reference to the formation of the spinal canal, they have nevertheless
considerable bearings on it.
Two views have recently been put forward on this subject. Professor
Gegenbaur[258] looks upon the central nervous system of Vertebrates as
equivalent to the superior oesophageal ganglia of Annelids and Arthropods
only, while Professors Leydig[259] and Semper[260] and Dr Dohrn[261]
compare it with the whole Annelidan nervous system.
Footnote 258: _Grundriss d. vergleichenden Anat._ p. 264.
Footnote 259: _Bau des thierischen Körpers._
Footnote 260: _Stammesverwandtschaft d. Wirbelthiere u.
Wirbellosen_ and _Die Verwandtschaftsbeziehungen d.
gegliederten Thiere_. This latter work, for a copy of which I
return my best thanks to the author, came into my hands after
what follows was written, and I much regret only to have been
able to make one or two passing allusions to it. The work is a
most important contribution to the questions about to be
discussed, and contains a great deal that is very suggestive;
some of the conclusions with reference to the Nervous System
appear to me however to be directly opposed to the observations
on Spinal Nerves above recorded.
Footnote 261: _Ursprung d. Wirbelthiere u. Princip des
Functionswechsels._
The first of these two views is only possible on the supposition that
Vertebrates are descended from unsegmented ancestors, and even then
presents considerable difficulties. If the ancestors of Vertebrates were
segmented animals, and several of the recent researches tend to shew that
they were, they must almost certainly have possessed a nervous cord like
that of existing Annelids. If such were the case, it is almost
inconceivable that the greater portion of the nervous system which forms
the ventral cord can have become lost, and the system reduced to the
superior oesophageal ganglia. Dr Dohrn[262], who has speculated very
profoundly on this matter, has attempted to explain and remove some of the
difficulties which arise in comparing the nervous systems of Vertebrates
and Annelids. He supposes that the segmented Annelids, from which
Vertebrates are descended, were swimming animals. He further supposes that
their alimentary canal was pierced by a number of gill-slits, and that the
anterior amongst these served for the introduction of nutriment into the
alimentary canal, in fact as supplementary mouths as well as for
respiration. Eventually the old mouth and throat atrophied, and one pair of
coalesced gill-slits came to serve as the sole mouth. Thus it came about
that on the disappearance of that portion of the alimentary canal, which
penetrated the oesophageal nervous ring, the latter structure ceased to be
visible as such, and no part of the alimentary canal was any longer
enclosed by a commissure of the central nervous system. With the change of
mouth Dr Dohrn also supposes that there took place a change, which would
for a swimming animal be one of no great difficulty, of the ventral for the
dorsal surface. This general explanation of Dr Dohrn's, apart from the
considerable difficulty of the fresh mouth, appears to me to be fairly
satisfactory. Dr Dohrn has not however in my opinion satisfactorily dealt
with the questions of detail which arise in connection with this
comparison. One of the most important points for his theory is to settle
the position where the nervous system was formerly pierced by the
oesophagus. This position he fixes in the fourth ventricle, and supports
his hypothesis by the thinness of the roof of the spinal canal in this
place, and the absence (?) of nervous structures in it.
Footnote 262: _Loc. cit._
It appears to me that this thinness cannot be used as an argument. In the
first place, if the hypothesis I have suggested as to the formation of the
spinal canal be accepted, the formation of the canal must be supposed to
have occurred in point of time either after or before the loss of the
primitive mouth. If, on the one hand, the spinal canal made its appearance
before the atrophy of the primitive mouth, the folding to form it must
necessarily have ceased behind the mouth; and, on the supposition of the
oesophageal ring having been situated in the region of the fourth
ventricle, a continuation of the spinal canal could not be present in front
of this part. If, on the other hand, the cerebro-spinal canal appeared
after the disappearance of the primitive mouth, its roof must necessarily
also be a formation subsequent to the atrophy of the mouth, and varieties
of structure in it can have no bearing upon the previous position of the
mouth.
But apart from speculations upon the origin of the spinal cord, there are
strong arguments against Dr Dohrn's view about the fourth ventricle. In the
first place, were the fourth ventricle to be the part of the nervous system
which previously formed the oesophageal commissures, we should expect to
find the opening in the nervous system at this point to be visible at an
early period of development, and at a later period to cease to be so. The
reverse is however the case. In early embryonic life the roof of the fourth
ventricle is indistinguishable from other parts of the nervous system, and
only thins out at a later period. Further than this, any explanation of the
thin roof of the fourth ventricle ought also to elucidate the nearly
similar structure in the sinus rhomboidalis, and cannot be considered
satisfactory unless it does so.
The peculiarities of the cerebro-spinal canal in the region of the brain
appear to me to present considerable difficulties in the way of comparing
the central nervous system of Vertebrates and segmented Annelids. The
manner in which the cerebro-spinal canal is prolonged into the optic
vesicles, the cerebral and the optic lobes is certainly opposed both to an
intelligible explanation of the spinal canal itself, and also to a
comparison of the two nervous systems under consideration.
Its continuation into the cerebral hemispheres and into the optic lobes
(mid-brain) may perhaps be looked upon as due to peculiar secondary growths
of those two ganglia, but it is very difficult to understand its
continuation into the optic vesicles.
If it be granted that the spinal canal has arisen from a folding in of the
external skin, then the present inner surface of the optic vesicle must
also have been its original outer surface, and it follows as a necessary
consequence that the present position of the rods and cones behind and not
in front of the nervous structures of the retina was not the primitive one.
The rods and cones arise, as is well known, from the inner surface of the
outer portion of the optic vesicle, and must, according to the above view,
be supposed originally to have been situated on the external surface, and
have only come to occupy their present position during the folding in,
which resulted in the spinal canal. On _à priori_ grounds we should
certainly expect the rods and cones to have resulted from the
differentiation of a layer of cells external to the conducting nervous
structures. The position of the rods and cones posterior to these suggests
therefore that some peculiar infolding has occurred, and may be used as an
argument to prove that the medullary groove is no mere embryonic structure,
but the embryonic repetition of an ancestral change. The supposition of
such a change of position in the rods and cones necessarily implies that
the folding in to form the spinal canal must have been a very slow one. It
must have given time to the refracting media of the eye gradually to travel
round, so as still to maintain their primitive position, while in
successive generations a rudimentary spinal furrow carrying with it the
retina became gradually converted into a canal[263].
Footnote 263: Professor Huxley informs me that he has for many
years entertained somewhat similar views to those in the text
about the position of the rods and cones, and has been
accustomed to teach them in his lectures.
If Dr Dohrn's comparison of the vertebrate nervous system with that of
segmented Annelids be accepted, the following two points must in my opinion
be admitted:--
(1) That the formation of the cerebro-spinal canal was subsequent to the
loss of the old mouth.
(2) That the position of the old mouth is still unknown.
The well-known view of looking at the pituitary and pineal growths as the
remnants of the primitive oesophagus, has no doubt some features to
recommend it. Nearly conclusive against it is the fact that the pituitary
involution is not, as used to be supposed, a growth towards the
infundibulum of the hypoblast of the oesophagus, but of the epiblast of the
mouth. It is almost inconceivable that an involution from the present mouth
can have assisted in forming part of the old oesophagus.
There is a view not involving the difficulty of the oesophageal ring, fresh
mouth[264], and of the change of the ventral to the dorsal surface, which,
though so far unsupported by any firm basis of observed facts, nevertheless
appears to me worth suggesting. It assumes that Vertebrates are descended
_not_ through the present line of segmented Vermes, but through some other
line which has now, so far as is known, completely vanished. This line must
be supposed to have originated from the same _unsegmented Vermes_ as the
present segmented Annelids. They therefore acquired fundamentally similar
segmental and other Annelidan organs.
Footnote 264: Professor Semper ("Die
Verwandtschaftsbeziehungen d. gegliederten Thiere," _Arbeiten
aus d. Zool.-zoot. Institut_, Würzburg, 1876) has some
interesting speculations on the difficult question of the
vertebrate mouth, which have unfortunately come to my knowledge
too late to be either fully discussed or incorporated in the
text. These speculations are founded on a comparison of the
condition of the mouth in Turbellarians and Nemertines. He
comes to the conclusion that there was a primitive mouth on the
cardiac side of the supra-oesophageal ganglion, which is the
existing mouth of Turbellarians and Vertebrates and the opening
of the proboscis of Nemertines, but which has been replaced by
a fresh mouth on the neural side in Annelids and Nemertines. In
Nemertines however the two mouths co-exist--the vertebrate
mouth as the opening of the proboscis, and the Annelid mouth as
the opening for the alimentary tract. This ingenious hypothesis
is supported by certain anatomical facts, which do not appear
to me of great weight, but for which the reader must refer to
the original paper. It no doubt avoids the difficulty of the
present position of the vertebrate mouth, but unfortunately at
the same time substitutes an equal difficulty in the origin of
the Annelidan mouth. This Professor Semper attempts to get over
by an hypothesis which to my mind is not very satisfactory (p.
378), which, however, and this Professor Semper does not appear
to have noticed, _could equally well be employed to explain the
origin of a Vertebrate mouth as a secondary formation
subsequent to the Annelidan mouth_. Under these circumstances
this fresh hypothesis does not bring us very much nearer to a
solution of the vertebrate-annelid mouth question, but merely
substitutes one difficulty for another; and does not appear to
me so satisfactory as the hypothesis suggested in the text.
At the same time Professor Semper's hypothesis suggests an
explanation of that curious organ the Nemertine proboscis. If
the order of changes suggested by him were altered it might be
possible to suppose that there never was more than one mouth
for all Vermes, but that the proboscis in Nemertines gradually
split itself off from the oesophagus to which it originally
belonged, and became quite free and provided with a separate
opening and perhaps carried with it the so-called vagus of
Professors Semper and Leydig.
The difference between the two branches of the Vermes lay in the nervous
system. The unsegmented ancestors of the _present_ Annelids seem to have
had a pair of super-oesophageal ganglia, from which two main nervous stems
extended backwards, one on each side of the body. Such a nervous system in
fact as is possessed by existing Nemertines or Turbellarians[265]. As the
Vermes became segmented and formed the Annelids, these side nerves seem to
have developed ganglia, corresponding in number with the segments, and
finally, approximating on the ventral surface, to have formed the ventral
cord[266].
Footnote 265: It is not of course to be supposed that the
primitive nervous system was pierced by a proboscis like that
of the Nemertines.
Footnote 266: This is Gegenbaur's view of the development of
the ventral cord, and I regard it in the meantime as the most
probable view which has been suggested.
The other branch of Vermes which I suppose to have been the ancestors of
Vertebrates started from the same stock as existing Annelids, but I
conceive the lateral nerve-cords, instead of approximating ventrally, to
have done so dorsally, and thus a dorsal cord to have become formed
analogous to the ventral cord of living Annelids, only without an
oesophageal nerve-ring[267].
Footnote 267: A dorsal instead of a ventral approximation of
the lateral nerve-cords would be possible in the descendants of
such living segmented Vermes as Saccocirrus and Polygordius.
It appears to me, (if the difficulties of comparing the Annelidan ventral
cord with the spinal cord of Vertebrates are found to be insurmountable),
that this hypothesis would involve far fewer improbabilities than one which
supposes the whole central nervous system of Vertebrates to be homologous
with the super-oesophageal ganglia. The mode of formation of a nervous
system presupposed in my hypothesis, well accords with what we know of the
formation of the ventral cord in existing Annelids.
The supposition of the existence of another branch of segmented Vermes is
not a very great difficulty. Even at the present day we have possibly more
than one branch of Vermes which have independently acquired segmentation.
viz.: the Chætopodous Annelids and the Hirudinea. If the latter is an
isolated branch, it is especially interesting from having independently
developed a series of segmental organs like those of Chætopodous Annelids,
which we must suppose the ancestors of Vertebrates also to have done if
they too form an independent branch.
In addition to the difficulty of imagining a fresh line of segmented
Vermes, there is another difficulty to my view, viz.: the fact that in
almost all Vermes, the blood flows forwards in the dorsal vessel, and
backwards in the ventral vessel. This condition of the circulation very
well suits the view of a change of the dorsal for the ventral surfaces, but
is opposed to these surfaces being the same for Vertebrates and Vermes. I
cannot however regard this point as a very serious difficulty to my view,
considering how undefined is the circulation in the unsegmented groups of
the Vermes.
_Sympathetic nervous system._
Between stages K and L there may be seen short branches from the spinal
nerves, which take a course towards the median line of the body, and
terminate in small irregular cellular masses immediately dorsal to the
cardinal veins (Pl. 18, fig. 1, _sy.g._). These form the first traces that
have come under my notice of the sympathetic nervous system. In the
youngest of my embryos in which I have detected these it has not been
possible for me either definitely to determine the antero-posterior limits
of the system, or to make certain whether the terminal masses of cells
which form the ganglia are connected by a longitudinal commissure. In a
stage slightly younger than L the ganglia are much more definite, the
anterior one is situated in the cardiac region close to the end of the
intestinal branch of the vagus, and the last of them quite at the posterior
end of the abdominal cavity. The anterior ganglia are the largest; the
commissural cord, if developed, is still very indistinct. In stage L the
commissural cord becomes definite, though not very easy to see even in
longitudinal sections, and the ganglia become so considerable as not to be
easily overlooked. They are represented in Pl. 13, fig. 1, _sy.g._ and in
Pl. 18, fig. 2, in the normal position immediately above the cardinal
veins. The branches connecting them with the trunks of the spinal nerves
may still be seen without difficulty. In later stages these branches cannot
so easily be made out in sections, but the ganglia themselves continue as
fairly conspicuous objects. The segmental arrangement of the ganglia is
shewn in Pl. 18, fig. 3, a longitudinal and vertical section of an embryo
between stages L and M with the junctions of the sympathetic ganglia and
spinal nerves. The ganglia occupy the intervals between the successive
segments of the kidneys.
The sympathetic system only came under my notice at a comparatively late
period in my investigations, and the above facts do not in all points clear
up its development[268]. My observations seem to point to the sympathetic
system arising as an off-shoot from the cerebrospinal system. Intestinal
branches would seem to be developed on the main nerve stems of this in the
thoracic and abdominal regions, each of these then develops a ganglion, and
the ganglia become connected by a longitudinal commissure. On this view a
typical spinal nerve has the following parts: two roots, a dorsal and
ventral, the dorsal one ganglionated, and three main branches, (1) a ramus
dorsalis, (2) a ramus ventralis, and (3) a ramus intestinalis. This scheme
may be advantageously compared with that of a typical cranial nerve
according to Gegenbaur. It may be noted that it brings the sympathetic
nervous system into accord with the other parts of the nervous system as a
product of the epiblast, and derived from outgrowths from the neural axis.
It is clear, however, that my investigations, though they may naturally be
interpreted in this way, do not definitely exclude a completely different
method of development for the sympathetic system.
Footnote 268: The formation out of the sympathetic ganglia of
the so-called paired suprarenal bodies is dealt with in
connection with the vascular system. The original views of
Leydig on these bodies are fully borne out by the facts of
their development.
EXPLANATION OF PLATE 14.
_This Plate illustrates the Formation of the Spinal Nerves._
COMPLETE LIST OF REFERENCE LETTERS.
_ar._ Anterior root of a spinal nerve. _ch._ Notochord. _com._ Commissure
connecting the posterior roots of the spinal nerves. _i._ Mesoblastic
investment of spinal cord. _mp._ Muscle-plate. _n._ Spinal nerve. _nc._
Neural canal. _pr._ Posterior root of a spinal nerve. _spg._ Ganglion on
posterior root of spinal nerve. _v.r._ Vertebral rudiment. _w._ White
matter of spinal cord. _y._ Point where the spinal cord became segmented
off from the superjacent epiblast.
Figs. 1, 2, and 3. Three sections of a Pristiurus embryo belonging to stage
I. Fig. 1 passes through the heart, fig. 2 through the anterior part of the
dorsal region, fig. 3 through a point slightly behind this. (Zeiss CC,
ocul. 2.) In fig. 3 there is visible a slight proliferation of cells from
the dorsal summit of the neural canal. In fig. 2 this proliferation
definitely constitutes two club-shaped masses of cells (_pr_)--the
rudiments of the posterior nerve-roots,--both attached to the dorsal summit
of the spinal cord. In fig. 1 the rudiments of the posterior roots are of
considerable length.
Fig. 4. Section through the dorsal region of a Torpedo embryo slightly
older than stage I, with three visceral clefts. (Zeiss CC, ocul. 2.) The
section shews the formation of a pair of dorsal nerve-rudiments (_pr_) and
a ventral nerve-rudiment (_ar_). The latter is shewn in its youngest
condition, and is not distinctly cellular.
Fig. 5. Section through the dorsal region of a Torpedo embryo slightly
younger than stage K. (Zeiss CC, ocul. 2.) The connective-tissue cells are
omitted. The rudiment of the ganglion (_spg_) on the posterior root has
appeared, and the junction of posterior root with the cord is difficult to
detect. The anterior root forms an elongated cellular structure.
Fig. 6. Section through the dorsal region of a Pristiurus embryo of stage
K. (Zeiss CC, ocul. 2.) The section especially illustrates the attachment
of the posterior root to the spinal cord.
Fig. 7. Section through the same embryo as fig. 6. (Zeiss CC, ocul. 1.) The
section contains an anterior root, which takes its origin at a point
opposite the interval between two posterior roots.
Fig. 8. A series of posterior roots with their central ends united by a
dorsal commissure, from a longitudinal and vertical section of a Scyllium
embryo belonging to a stage intermediate between L and M. The embryo was
hardened in a mixture of osmic and chromic acids.
Fig. 9. The central end of a posterior nerve-root from the same embryo,
with the commissure springing out from it on either side.
CHAPTER IX.
THE DEVELOPMENT OF THE ORGANS IN THE HEAD.
_The Development of the Brain._
_General History._ In stage G the brain presents a very simple constitution
(Pl. 8, fig. G), and is in fact little more than a dilated termination to
the cerebro-spinal axis. Its length is nearly one-third that of the whole
body, being proportionately very much greater than in the adult.
It is divided by very slight constrictions into three lobes, the posterior
of which is considerably the largest. These are known as the fore-brain,
the mid-brain, and the hind-brain. The anterior part of the brain is bent
slightly downwards about an axis passing through the mid-brain. The walls
of the brain, composed of several rows of elongated columnar cells, have a
fairly uniform thickness, and even the roof of the hind-brain is as thick
as any other part. Towards the end of stage G the section of the hind-brain
becomes somewhat triangular with the apex of the triangle directed
downwards.
In Pristiurus during stage H no very important changes take place in the
constitution of the brain. In Scyllium, however, indications appear in the
hind-brain of its future division into a cerebellum and medulla oblongata.
The cavity of the anterior part dilates and becomes rounded, while that of
the posterior part assumes in section an hour-glass shape, owing to an
increase in the thickness of the lateral parts of the walls. At the same
time the place of the original thick roof is taken by a very thin layer,
which is formed not so much through a change in the character and
arrangements of the cells composing the roof, as by a divarication of the
two sides of the hind-brain, and the simultaneous introduction of a fresh
structure in the form of a thin sheet of cells connecting dorsally the
diverging lateral halves of this part of the brain. By stage I, the
hind-brain in Pristiurus also acquires an hour-glass shaped section, but
the roof has hardly begun to thin out (Pl. 15, figs. 4_a_ and 4_b_).
During stages I and K the cranial flexure becomes more and more pronounced,
and causes the mid-brain definitely to form the termination of the long
axis of the embryo (Pl. 15, figs. 1, 2, etc.), and before the close of
stage K a thin coating of white matter has appeared on the exterior of the
whole brain, but no other histological changes of interest have occurred.
During stage L an apparent rectification of the cranial flexure commences,
and is completed by stage Q. The changes involved in this process may be
advantageously studied by comparing the longitudinal sections of the brain
during stages L, P, and Q, represented in Pl. 16, figs. 1_a_, 5 and 7_a_.
It will be seen, first of all, that so far from the flexure of the brain
itself being diminished, it is increased, and in P (fig. 5) the angle in
the floor of the mid-brain becomes very acute indeed; in other words, the
anterior part of the brain has been bent upon the posterior through nearly
two right angles, and the infundibulum, or primitive front end of the
brain, now points nearly directly backwards. At the same time the cerebral
hemispheres have grown directly forwards, and if figures 1_a_ and 5 in
Pl. 16 be compared it will be seen that in the older brain of the two the
cerebral hemispheres have assumed a position which might be looked on as
the result of their having been pushed dorsalwards and forwards against the
mid-brain, and having in the process pressed in and nearly obliterated the
original thalamencephalon. The thalamencephalon in fig. 1_a_, belonging to
stage L, is relatively large, but in fig. 5, belonging to stage P, it only
occupies a very small space between the front wall of the mid-brain and the
hind wall of the cerebral hemispheres. It is therefore in part by the
change in position of the cerebral hemispheres that the angle between the
trabeculæ and parachordals becomes increased, _i.e._ their flexure
_diminished_, while at the same time the flexure of the brain itself is
_increased_. More important perhaps in the apparent rectification of the
cranial flexure than any of the previously mentioned points, is the
appearance of a bend in the hind-brain which tends to correct the original
cranial flexure. The gradual growth of this fresh flexure can be studied in
the longitudinal sections which have been represented. It is at its maximum
in stage Q. This short preliminary sketch of the development of the brain
as a whole will serve as an introduction to the history of the individual
divisions of the brain.
_Fore-brain._ In its earliest condition the fore-brain forms a single
vesicle without a trace of separate divisions, but buds off very early the
optic vesicles, whose history is described with that of the eye (Pl. 15,
fig. 3, _op.v_). Between stages I and K the posterior part of the
fore-brain sends outwards a papilliform process towards the exterior, which
forms the rudiment of the pineal gland (Pl. 15, fig. 1, _pn_). Immediately
in front of the rudiment a constriction appears, causing a division of the
fore-brain into a large anterior and a small posterior portion. This
constriction is shallow at first, but towards the close of stage K becomes
much deeper (Pl. 15, fig. 2 and fig. 16_a_), leaving however the two
cavities of the two divisions of the fore-brain united ventrally by a
somewhat wide canal.
The posterior of the two divisions of the fore-brain forms the
thalamencephalon. Its anterior wall adjoining the cerebral rudiment becomes
excessively thin (Pl. 15, fig. 11); and its base till the close of stage K
is in close contact with the mouth involution, and presents but a very
inconspicuous prominence which marks the eventual position of the
infundibulum (Pl. 15, figs. 9_a_, 12, 16_a_, _in_). The anterior and larger
division of the fore-brain forms the rudiment of the cerebral hemispheres
and olfactory lobes. Up to stage K this rudiment remains perfectly simple,
and exhibits no signs, either externally or internally, of a longitudinal
constriction into two lobes. From the canal uniting the two divisions of
the fore-brain (which eventually forms part of the thalamencephalon) there
spring the hollow optic nerves. A slight ventral constriction separating
the cerebral rudiment from that part of the brain where these are attached
appears even before the close of stage K (Pl. 15, fig. 11, _op.n_).
During stage L the infundibulum becomes much produced, and forms a wide
sack in contact with the pituitary body, and its cavity communicates with
that of the third ventricle by an elongated slit-like aperture. This may be
seen by comparing Pl. 16, figs. 1_a_ and 1_c_. In fig. 1_c_ taken along the
middle line, there is present a long opening into the infundibulum (_in_),
which is shewn to be very narrow by being no longer present in fig. 1_a_
representing a section slightly to one side of the middle line. During the
same stage the pineal gland grows into a sack-like body, springing from the
roof of the thalamencephalon, fig. 1_b_, _pn_. This latter (the
thalamencephalon) is now dorsally separated from the cerebral rudiment by a
deep constriction, and also ventrally by a less well marked constriction.
At its side also a deep constriction is being formed in it, immediately
behind the pineal gland. The cerebral rudiment is still quite unpaired and
exhibits no sign of becoming constricted into two lobes.
During the next two stages the changes in the fore-brain are of no great
importance, and I pass at once to stage O. The infundibulum is now nearly
in the same condition as during stage L, though (as is well shewn in the
figure of a longitudinal section of the next stage) it points more directly
backwards than before. The remaining parts of the thalamencephalon have
however undergone considerable changes. The more important of these are
illustrated by a section of stage O, Pl. 16, fig. 3, transverse to the long
axis of the embryo, and therefore, owing to the cranial flexure, cutting
the thalamencephalon longitudinally and horizontally; and for stage P in a
longitudinal and vertical section through the brain (Pl. 16, fig. 5). In
the first place the roof of the thalamencephalon has become very much
shortened by the approximation of the cerebral rudiment to the mid-brain.
The pineal sack has also become greatly elongated, and its somewhat dilated
extremity is situated between the cerebral rudiment and the external skin.
It opens into the hind end of the third ventricle, and its posterior wall
is continuous with the front wall of the mid-brain. The sides of the
thalamencephalon have become much thickened, and form distinct optic
thalami (_op._) united by a very well marked posterior commissure (_pc._).
The anterior wall of the thalamencephalon as well as its roof are very
thin. The optic nerves have become by stage O quite solid except at their
roots, into which the ventricles of the fore-brain are for a short distance
prolonged. This solidification is arrived at, so far as I have determined,
without the intervention of a fold. The nerves are fibrous, and a
commencement of the chiasma is certainly present. From the chiasma there
appears to pass out on each side a band of fibres, which runs near the
outer surface of the brain to the base of the optic lobes (mid-brain), and
here the fibres of the two sides again cross.
By stage O important changes are perceptible in the cerebral rudiment. In
the first place there has appeared a slight fold at its anterior extremity
(Pl. 16, fig. 3, _x_), destined to form a vertical septum dividing it into
two hemispheres, and secondly, lateral outgrowths (vide Pl. 16, fig. 2,
_ol.l_), to form the olfactory lobes. Its thin posterior wall presents on
each side a fold which projects into the central cavity. From the
peripheral end of each olfactory lobe a nerve similar in its histological
constitution to any other cranial nerve makes its appearance (Pl. 16,
fig. 2); this divides into a number of branches, one of which passes into
the connective tissue between the two layers of epithelium in each
Schneiderian fold. On the root of this nerve there is a large development
of ganglionic cells. I have not definitely observed its origin, but have no
reason to doubt that it is a direct outgrowth from the olfactory lobe,
exactly similar _in its mode of development_ to any other nerve of the
body.
The cerebral rudiment undergoes great changes during stage P. In addition
to a great increase in the thickness of its walls, the fold which appeared
in the last stage has grown backwards, and now divides it in front into two
lobes, the rudiments of the cerebral hemispheres. The greater and posterior
section is still however quite undivided, and the cavities of the lobes
(lateral ventricles) though separated in front are still quite continuous
behind. At the same time, the olfactory lobes, each containing a
prolongation of the ventricle, have become much more pronounced (vide
Pl. 16, figs. 4_a_ and 4_c_, _ol.l_). The root of the olfactory nerve is
now very thick, and the ganglion cells it contains are directly prolonged
into the ganglionic portion of the olfactory bulb; in consequence of which
it becomes rather difficult to fix on the exact line of demarcation between
the bulb and the nerve.
Stage Q is the latest period in which I have investigated the development
of the brain. Its structure is represented for this stage in general view
in Pl. 16, figs. 6_a_, 6_b_, 6_c_, in longitudinal section in Pl. 16, figs.
7_a_, 7_b_, and in transverse section Pl. 16, figs. 8_a-d_. The transverse
sections are taken from a somewhat older embryo than the longitudinal. In
the thalamencephalon there is no fresh point of great importance to be
noticed. The pineal gland remains as before, and has become, if anything,
longer than it was, and extends further forwards over the summit of the
cerebrum. It is situated, as might be expected, in the connective tissue
within the cranial cavity (fig. 8_a_, _pn_), and does not extend outside
the skull, as it appears to do, according to Götte's investigations, in
Amphibians. Götte[269] compares the pineal gland with the long persisting
pore which leads into the cavity of the brain in the embryo of Amphioxus,
and we might add the Ascidians, and calls it "ein Umbildungsprodukt einer
letzten Verbindung des Hirns mit der Oberhaut." This suggestion appears to
me a very good one, though no facts have come under my notice which confirm
it. The sacci vasculosi are perhaps indicated at this stage in the two
lateral divisions of the trilobed ventricle of the infundibulum
(fig. 8_c_).
Footnote 269: _Ent. d. Unke_, p. 304.
The lateral ventricles (fig. 8_a_) are now quite separated by a median
partition, and a slight external constriction marks the lobes of the two
hemispheres; these, however, are still united by nervous structures for the
greater part of their extent. The olfactory lobes are formed of a distinct
bulb and stalk (fig. 8_a_, _ol.l_), and contain, as before, prolongations
of the lateral ventricles. The so-called optic chiasma is very distinct
(fig. 8_b_, _op.n_), but the fibres from the optic nerves appear to me
simply to cross and not to intermingle.
_The mid-brain._ The mid-brain is at first fairly marked off from both the
fore and hind brains, but less conspicuously from the latter than from the
former. Its roof becomes progressively thinner and its sides thicker up to
stage P, its cavity remaining quite simple. The thinness of the roof gives
it, in isolated brains of stage P, a bilobed appearance (vide Pl. 16,
fig. 4_b_, _mb_, in which the distinctness of this character is by no means
exaggerated): During stage Q it becomes really bilobed through the
formation in its roof of a shallow median furrow (Pl. 16, fig. 8_b_). Its
cavity exhibits at the same time the indication of a division into a
central and two lateral parts.
_The hind-brain._ The hind-brain has at first a fairly uniform structure,
but by the close of stage I, the anterior part becomes distinguished from
the remainder by the fact, that its roof does not become thin as does that
of the posterior part. This anterior, and _at first very insignificant
portion_, forms the rudiment of the cerebellum. Its cavity is quite simple
and is continued uninterruptedly into that of the remainder of the
hind-brain. The cerebellum assumes in the course of development a greater
and greater prominence, and eventually at the close of stage Q overlaps
both the optic lobes in front and the medulla behind (Pl. 16, fig. 7_a_).
It exhibits in surface-views of the hardened brain of stages P and Q the
appearance of a median constriction, and the portion of the ventricle
contained in it is prolonged into two lateral outgrowths (Pl. 16, figs.
8_c_ and 8_d_, _cb_).
The posterior section of the hind-brain which forms the medulla undergoes
changes of a somewhat complicated character. In the first place its roof
becomes in front very much extended and thinned out. At the raphe, where
the two lateral halves of the brain originally united, a separation, as it
were, takes place, and the two sides of the brain become pushed apart,
remaining united by only a very thin layer of nervous matter (Pl. 15,
fig. 6, _iv.v._). As a result of this peculiar growth in the brain, the
roots of the nerves of the two sides which were originally in contact at
the dorsal summit of the brain become carried away from one another, and
appear to rise at the sides of the brain (Pl. 15, figs. 6 and 7). Other
changes also take place in the walls of the brain. Each lateral wall
presents two projections towards the interior (Pl. 15, fig. 5_a_). The
ventral of these vanish, and the dorsal approximate so as nearly to divide
the cavity of the hind-brain, or fourth ventricle, into a large dorsal and
a small ventral channel (Pl. 15, fig. 6), and this latter becomes
completely obliterated in the later stages. The dorsal pair, while
approximating, also become more prominent, and stretch into the dorsal
moiety of the fourth ventricle (Pl. 15, fig. 6). They are still very
prominent at stage Q (Pl. 16, fig. 8_d_, _ft_), and correspond in position
with the fasciculi teretes of human anatomy. Part of the root of the
seventh nerve originates from them. They project freely in front into the
cavity of the fourth ventricle (Pl. 16, fig. 7_a_, _ft_).
By stage Q restiform tracts are indistinctly marked off from the remainder
of the brain, and are anteriorly continued into the cerebellum, of which
they form the peduncles. Near their junction with the cerebellum they form
prominent bodies (Pl. 16, fig. 7_a_, _rt_), which are regarded by
Miklucho-Maclay[270] as representing the true cerebellum.
Footnote 270: _Das Gehirn d. Selachier_, Leipzig, 1870.
By stage O the medulla presents posteriorly, projecting into its cavity, a
series of lobes which correspond with the main roots (not the branches) of
the vagus and glosso-pharyngeal nerves (Pl. 17, fig. 5). There appear to me
to be present seven or eight projections: their number cannot however be
quite certainly determined. The first of them belongs to the root of the
glosso-pharyngeal, the next one is interposed between the glosso-pharyngeal
and the first root of the vagus, and is without any corresponding
nerve-root. The next five correspond to the five main roots of the vagus.
For each projection to which a nerve pertains there is a special nucleus of
nervous matter, from which the root springs. These nuclei do not stain like
the remainder of the walls of the medulla, and stand out accordingly very
conspicuously in stained sections.
The coating of white matter which appeared at the end of stage K, on the
exterior of each lateral half of the hind-brain, extends from a point just
dorsal to the attachment of the nerve-roots to the ventral edge of the
medulla, and is specially connected with the tissue of the upper of the two
already described projections into the fourth ventricle.
A rudiment of the tela vasculosa makes its appearance during stage Q, and
is represented by the folds in the wall of the fourth ventricle in my
figure of that stage (Pl. 16, fig. 7_a_, _tv_).
* * * * *
The development of the brain in Elasmobranchii has already been worked out
by Professor Huxley, and a brief but in many respects very complete account
of it is given in his recent paper on Ceratodus[271]. He says, pp. 30 and
31, "The development of the cerebral hemispheres in Plagiostome Fishes
differs from the process by which they arise in the higher Vertebrata. In a
very early stage, when the first and second visceral clefts of the embryo
Scyllium are provided with only a few short branchial filaments, the
anterior cerebral vesicle is already distinctly divided into the
thalamencephalon (from which the large infundibulum proceeds below, and the
small tubular peduncle of the pineal gland above, while the optic nerve
leaves its sides) and a large single oval vesicle of the hemispheres. On
the ventral face of the integument covering these are two oval depressions,
the rudimentary olfactory sacs.
Footnote 271: _Proceedings of the Zoological Society_, 1876,
Pt. 1. pp. 30 and 31.
"As development proceeds the vesicle of the hemispheres becomes
divided by the ingrowth of a median longitudinal septum, and the
olfactory lobes grow out from the posterior lateral regions of each
ventricle thus formed, and eventually rise on to the dorsal faces of
the hemispheres, instead of, as in most Vertebrata, remaining on their
ventral sides. I may remark, that I cannot accept the views of
Miklucho-Maclay, whose proposal to alter the nomenclature of the parts
of the Elasmobranch's brain, appears to me to be based upon a
misinterpretation of the facts of development."
The last sentence of the paragraph brings me to the one part on which it is
necessary to say a few words, viz. the views of Miklucho-Maclay. His views
have not received any general acceptance, but the facts narrated in the
preceding pages shew, beyond a doubt, that he has 'misinterpreted' the
facts of development, and that the ordinary view of the homology of the
parts is the correct one. A comparison of the figures I have given of the
embryo brain with similar figures of the brain of higher Vertebrates shews
this point conclusively. Miklucho-Maclay has been misled by the large size
of the cerebellum, but, as we have seen, this body does not begin to be
conspicuous till late in embryonic life. Amongst the features of the
embryonic brain of Elasmobranchii, the long persisting unpaired condition
of the cerebral hemisphere, upon which so much stress has already been laid
by Professor Huxley, appears to me to be one of great importance, and may
not improbably be regarded as a real ancestral feature. Some observations
have recently been published by Professor B. G. Wilder[272] upon this
point, and upon the homologies and development of the olfactory lobes.
Fairly good figures are given to illustrate the development of the cerebral
hemispheres, but the conclusions arrived at are in part opposed to my own
results. Professor Wilder says: "The true hemispheres are the lateral
masses, more or less completely fused in the middle line, and sometimes
developing at the plane of union a bundle of longitudinal commissural
fibres. The hemispheres retain their typical condition as anterior
protrusions of the anterior vesicle; but they lie mesiad of the olfactory
lobes, _and in Mustelus at least seem to be formed after them_." The
italics are my own. From what has been said above, it is clear that the
statement italicised, for Scyllium at least, completely reverses the order
of development. Still more divergent from my conclusions are Professor
Wilder's statements on the olfactory lobes. He says: "The true olfactory
lobe, or rhinencephalon, seems, therefore, to embrace only the hollow base
of the crus, more or less thickened, and more or less distinguishable from
the main mass as a hollow process. The olfactory bulb, with the more or
less elongated crus of many Plagiostomes, seems to be developed
independently, or in connection with the olfactory sack, as are the general
nerves;" and again, "But the young and adult brains since examined shew
that the ventricle (_i.e._ the ventricle of the olfactory lobe) ends as a
rounded cul-de-sac before reaching the 'lobe.'"
Footnote 272: "Anterior brain-mass with Sharks and Skates,"
_American Journal of Science and Arts_, Vol. XII. 1876.
The majority of the statements contained in the above quotations are not
borne out by my observations. Even the few preparations of which I have
given figures, appear to me to prove that (1) the olfactory lobes (crura
and bulbs) are direct outgrowths from the cerebral rudiment, and develop
quite independently of the olfactory sack; (2) that the ventricle of the
cerebral rudiment does not stop short at the base of the crus; (3) that
from the bulb a nerve grows out which has a centrifugal growth like other
nerves of the body, and places the central olfactory lobe in communication
with the peripheral olfactory sack. In some other Vertebrates this nerve
seems hardly to be developed, but it is easily intelligible, that if in the
ordinary course of growth the olfactory sack became approximated to the
olfactory lobe, the nerve which grew out from the latter to the sack might
become so short as to escape detection.
_Organs of Sense._
_The olfactory organ._ The olfactory pit is the latest formed of the three
organs of special sense. It appears during a stage intermediate between _I_
and _K_, as a pair of slight thickenings of the external epiblast, in the
normal vertebrate position on the under side of the fore-brain immediately
in front of the mouth (Pl. 15, figs. 1 and 2, _ol_).
The epiblast cells which form this thickening are very columnar, but
present no special peculiarities. Each thickened patch of skin soon becomes
involuted as a shallow pit, which remains in this condition till the close
of the stage _K_. The epithelium very early becomes raised into a series of
folds (Schneiderian folds). These are bilaterally symmetrical, and diverge
like the barbs of a feather from a median line (Pl. 15, fig. 14). The nasal
pits at the close of stage K are still separated by a considerable interval
from the walls of the brain, and no rudiment of an olfactory lobe arises
till a later period; but a description of the development of this as an
integral part of the brain has already been given, p. 401.
_Eye._ The eye does not present in its early development any very special
features of interest. The optic vesicles arise as hollow outgrowths from
the base of the fore-brain (Pl. 15, fig. 3, _op.v_), from which they soon
become partially constricted, and form vesicles united to the base of the
brain by comparatively narrow hollow stalks, the rudiments of the optic
nerves. The constriction to which the stalk or optic nerve is due takes
place from above and backwards, so that the optic nerves open into the base
of the front part of the thalamencephalon (Pl. 15, fig. 13_a_, _op.n_).
After the establishment of the optic nerves, there take place the formation
of the lens and the pushing in of the anterior wall of the optic vesicle
towards the posterior.
The lens arises in the usual vertebrate fashion. The epiblast in front of
the optic vesicle becomes very much thickened, and then involuted as a
shallow pit, which eventually deepens and narrows. The walls of the pit are
soon constricted off as a nearly spherical mass of cells enclosing a very
small central cavity, in some cases indeed so small as to be barely
recognizable (Pl. 15, fig. 7, _l_). The pushing in of the anterior wall of
the optic vesicle towards the posterior takes place in quite the normal
manner; but, as has been already noticed by Götte[273] and others, is not a
simple mechanical result of the formation of the lens, as is shewn by the
fact that the vesicle assumes a flattened form even before the appearance
of the lens. The whole exterior of the optic cup becomes invested by
mesoblast, but _no mesoblastic cells grow in between the lens and the
adjoining wall of the optic cup_.
Footnote 273: _Entwicklungsgeschichte d. Unke._
Round the exterior of the lens, and around the exterior and interior of the
optic cup, there appear membrane-like structures, similar to those already
described round the spinal cord and other organs. These membrane-like
structures appear with a varying distinctness, but at the close of stage
_K_ stand out with such remarkable clearness as to leave no doubt that they
are not artificial products (Pl. 15, fig. 13_a_)[274]. They form the
rudiments of the hyaloid membrane and lens capsule. Similar, though less
well marked membranes, may often be seen lining the central cavity of the
lens and the space between the two walls of the optic cup. The optic cup is
at first very shallow, but owing to the rapid growth of the free edge of
its walls soon becomes fairly deep. The growth extends to the whole
circumference of the walls except the point of entrance of the optic nerve
(Pl. 15, fig. 13_a_), where no growth takes place; here accordingly a gap
is left in the walls which forms the well-known choroid slit. While this
double walled cup is increasing in size, the wall lining the cavity of the
cup becomes thick, and the outer wall very thin (fig. 13_a_). No further
differentiations arise before the close of stage K.
Footnote 274: The engraver has not been very successful in
rendering these membranes.
The lens is carried outwards with the growth of the optic cup, leaving the
cavity of the cup quite empty. It also grows in size, and its central
cavity becomes larger. Still later its anterior wall becomes very thin, and
its posterior wall thick, and doubly convex (fig. 13_a_). Its changes,
however, so exactly correspond to those already known in other Vertebrates,
that a detailed description of them would be superfluous.
_No mesoblast passes into the optic cup round its edge_, but a process of
mesoblast, accompanied by a blood-vessel, passes into the space between the
lens and the wall of the optic cup through the choroid slit (fig. 13_a_,
_ch_). This process of tissue is very easily seen, and swells out on
entering the optic cup into a mushroom-like expansion. It forms the
processus falciformis, and from it is derived the vitreous humour.
About the development of the parts of the eye, subsequently to stage _K_, I
shall not say much. The iris appears during stage O, as an ingrowing fold
of both layers of the optic cup with a layer of mesoblast on its outer
surface, which tends to close over the front of the lens. Both the epiblast
layers comprising the iris are somewhat atrophied, and the outer one is
strongly pigmented. At stage O the mesoblast first also grows in between
the external skin and the lens to form the rudiment of the mesoblastic
structures of the eye in front of the lens. The layer, when first formed,
is of a great tenuity.
The points in my observations, to which I attach the greatest importance,
are the formation of the lens capsule and the hyaloid membrane; with the
development of these may be treated also that of the vitreous humour and
rudimentary _processus falciformis_. The development of these parts in
Elasmobranchii has recently been dealt with by Dr Bergmeister[275], and his
observations with reference to the vitreous humour and processus
falciformis, the discovery of which in embryo Elasmobranchii is due to him,
are very complete. I cannot, however, accept his view that the hyaloid
membrane is a mesoblastic product. Through the choroid slit there grows, as
has been said, a process of mesoblast, the processus falciformis, which on
entering the optic cup dilates, and therefore appears mushroom-shaped in
section. At the earliest stage (K) a blood-vessel appeared in connection
with it, but no vascular structure came under my notice in the later
stages. The structure of this process during stage P is shewn in Pl. 17,
fig. 6, _p.fal._; it is there seen to be composed of mesoblast-cells with
fibrous prolongations. The cells, as has been noticed by Bergmeister, form
a special border round its dilated extremity. This process is formed much
earlier than the vitreous humour, which is first seen in stage O. In
hardened specimens this latter appears either as a gelatinous mass with a
meshwork of fibres or (as shewn in Pl. 17, fig. 6) with elongated fibres
proceeding from the end of the processus falciformis. These fibres are
probably a product of the hardening reagent, but perhaps represent some
preformed structure in the vitreous humour. I have failed to detect in it
any cellular elements. It is more or less firmly attached to the hyaloid
membrane.
Footnote 275: "Embryologie d. Coloboms," _Sitz. d. k. Akad.
Wien_, Bd. LXXI. 1875.
On each side of the processus falciformis in stage P a slight fold of the
optic cup is to be seen, but folds so large as those represented by
Bergmeister have never come under my notice, though this may be due to my
not having cut sections of such late embryos as he has. The hyaloid
membrane appears long before the vitreous humour as a delicate basement
membrane round the inner surface of the optic cup (Pl. 15, fig. 13_a_),
which is perfectly continuous with a similar membrane round the outer
surface. In the course of development the hyaloid membrane becomes thicker
than the membrane outside the optic cup, with which however it remains
continuous. This is very clear in my sections of stage M. By stage O the
membrane outside the cup has ceased to be distinguishable, but the hyaloid
membrane may nevertheless be traced to the very edge of the cup round the
developing iris; but does not unite with the lens capsule. It can also be
traced quite to the junction of the two layers of the optic cup at the side
of the choroid slit (Pl. 17, fig. 6, _hy.m_). When the vitreous humour
becomes artificially separated from the retina, the hyaloid membrane
sometimes remains attached to the former, but at other times retains in
preference its attachment to the retina. My observations do not throw any
light upon the junction of the hyaloid membrane and lens capsule to form
the suspensory ligament, nor have I ever seen (as described by Bergmeister)
the hyaloid membrane extending across the free end of the processus
falciformis and separating the latter from the vitreous humour. This
however probably appears at a period subsequent to the latest one
investigated by me. The lens capsule arises at about the same period as the
hyaloid membrane, and is a product of the cells of the lens. It can be very
distinctly seen in all the stages subsequent to its first formation. The
proof of its being a product of the epiblastic lens, and not of the
mesoblast, lies mainly in the fact of there being no mesoblast at hand to
give rise to it at the time of its formation, vide Pl. 15, fig. 13_a_. If
the above observations are correct, it is clear that the hyaloid membrane
and lens capsule are respectively products of the retina and lens; so that
it becomes necessary to go back to the older views of Kölliker and others
in preference to the more modern ones of Lieberkühn and Arnold. It would
take me too far from my subject to discuss the arguments used by the later
investigators to maintain their view that the hyaloid membrane and lens
capsule are mesoblastic products; but it will suffice to say that the
continuity of the hyaloid membrane over the pecten in birds is no
conclusive argument against its retinal origin, considering the great
amount of apparently independent growth which membranes, when once formed,
are capable of exhibiting.
Bergmeister's and my own observations on the vitreous humour clearly prove
that this is derived from an ingrowth through the choroid slit. On the
other hand, the researches of Lieberkühn and Arnold on the Mammalian Eye
appear to demonstrate that a layer of mesoblast becomes in Mammalia
involuted with the lens, and from this the vitreous humour (including the
_membrana capsulo-pupillaris_) is said to be in part formed. Lieberkühn
states that in Birds the vitreous humour is formed in a similar fashion. I
cannot, however, accept his results on this point. It appears, therefore,
that, so far as is known, all groups of Vertebrata, with the exception of
Mammalia, conform to the Elasmobranch type. The differences between the
types of Mammalia and remaining Vertebrata are, however, not so great as
might at first sight appear. They are merely dependent on slight
differences in the manner in which the mesoblast enters the optic cup. In
the one case it grows in round one specialized part of the edge of the cup,
_i.e._ the choroid slit; in the other, round the whole edge, including the
choroid slit. Perhaps the mode of formation of the vitreous humour in
Mammalia may be correlated with the early closing of the choroid slit.
_Auditory Organ._ With reference to the development of the organ of hearing
I have very little to say. Opposite the interval between the seventh and
the glosso-pharyngeal nerves the external epiblast becomes thickened, and
eventually involuted as a vesicle which remains however in communication
with the exterior by a narrow duct. Towards the close of stage K the
auditory sack presents three protuberances--one pointing forwards, a second
backwards, and a third outwards. These are respectively the rudiments of
the anterior and posterior vertical and external horizontal semicircular
canals. These rudiments are easily visible from the exterior (Pl. 15,
fig. 2).
* * * * *
As has been already pointed out, the epiblast of Elasmobranchii during the
early periods of development exhibits no division into an epidermic and a
nervous layer, and in accordance with its primitive undifferentiated
condition, those portions of the organs of sense which are at this time
directly derived from the external integument are formed indiscriminately
from the whole, and not from an inner or so-called nervous part of it only.
In the Amphibians the auditory sack and lens are derived from the nervous
division of the epiblast only, while the same division of the layer plays
the major part in forming the olfactory organ. It is also stated that in
Birds and Mammals the part of the epiblast corresponding to the nervous
layer is alone concerned in the formation of the lens, though this does not
appear to be the case with the olfactory or auditory organs in these groups
of Vertebrates.
_Mouth involution and Pituitary body._
The development of the mouth involution and the pituitary body is closely
related to that of the brain, and may conveniently be dealt with here. The
epiblast in the angle formed by the cranial flexure becomes involuted as a
hollow process situated in close proximity to the base of the brain. This
hollow process is the mouth involution, and it is bordered on its posterior
surface by the front wall of the alimentary tract, and on its anterior by
the base of the fore-brain.
The uppermost end of this does not till near the close of stage K become
markedly constricted off from the remainder, but is nevertheless the
rudiment of the pituitary body. Pl. 15, figs. 9_a_ and 12, _m_ shew in a
most conclusive manner the correctness of the above account, and
demonstrate that it is from the mouth involution, and not, as has usually
been stated, from the alimentary canal, that the pituitary body is derived.
This fact was mentioned in my preliminary account of Elasmobranch
development[276]; and has also been shewn to be the case in Amphibians by
Götte[277]; and in Birds by Mihalkowics[278]. The fact is of considerable
importance with reference to speculations as to the meaning of this body.
Footnote 276: _Quarterly Journal of Microscopic Science_, Oct.
1874.
Footnote 277: _Entwicklungsgeschichte der Unke._ Götte was the
first to draw attention to this fact. His observations were
then shewn to hold true for Elasmobranchii by myself, and
subsequently for Birds by Mihalkowics.
Footnote 278: _Arch. f. micr. Anat._ Vol. XI.
Plate 15, fig. 7 represents a transverse section through the head during a
stage between I and K; but, owing to the cranial flexure, it cuts the fore
part of the head longitudinally and horizontally, and passes through both
the fore-brain (_fb_) and the hind-brain (_iv.v._). Close to the base of
the fore-brain are seen the mouth (_m_), and the pituitary involution from
this (_pt._). In contact with the pituitary involution is the blind
anterior termination of the throat, which a little way back opens to the
exterior by the first visceral cleft (I. _v.c._). This figure alone
suffices to demonstrate the correctness of the above account of the
pituitary body; but the truth of this is still further confirmed by other
figures on the same plate (figs. 9_a_ and 12, _m_); in which the mouth
involution is in contact with, but still separated from, the front end of
the alimentary tract. By the close of stage K, the septum between the mouth
and throat becomes pierced, and the two are placed in communication. This
condition is shewn in Pl. 15, fig. 16_a_, and Pl. 16, figs. 1_a_, 1_c_,
_pt_ In these figures the pituitary involution has become very partially
constricted off from the mouth involution, though still in direct
communication with it. In later stages the pituitary involution becomes
longer and dilated terminally, while the passage connecting it with the
mouth becomes narrower and narrower, and is finally reduced to a solid
cord, which in its turn disappears. The remaining vesicle then becomes
divided into lobes, and connects itself closely with the infundibulum (Pl.
16, figs. 5 and 6 _pt_). The later stages for Elasmobranchii are fully
described by W. Müller in his important memoir on the Comparative Anatomy
and development of this organ[279].
Footnote 279: W. Müller, "Ueber Entwicklung and Bau d.
Hypophysis u. d. Processus infundibuli cerebri," _Jenaische
Zeitschrift_, Bd. VI.
_Development of the Cranial Nerves._
The present section deals with the whole development (so far as I have
succeeded in elucidating it) of the cranial nerves (excluding the optic and
olfactory nerves and the nerves of the eye-muscles) from their first
appearance to their attainment of the adult condition. My description
commences with the first development of the nerves, to this succeeds a
short description of the nerves in the adult Scyllium, and the section is
completed by an account of the gradual steps by which the adult condition
is attained.
_Early Development of the Cranial Nerves._--Before the close of stage H the
more important of the cranial nerves make their appearance. The fifth and
the seventh are the first to be formed. The fifth arises by stage G
(Pl. 15, fig. 3, V), near the anterior end of the hind-brain, as _an
outgrowth from the extreme dorsal summit of the brain, in identically the
same way as the dorsal root of a spinal nerve_.
The roots of the two sides sprout out from the summit of the brain, in
contact with each other, and grow ventralwards, one on each side of the
brain, in close contact with its walls. I have failed to detect more than
one root for the two embryonic branches of the fifth (ophthalmic and
mandibular), _and no trace of an anterior or ventral root has been met with
in any of my sections_.
The seventh nerve is formed nearly simultaneously with or shortly after the
fifth, and some little distance behind and independently of it, opposite
the anterior end of the thickening of the epiblast to form the auditory
involution. It arises precisely like the fifth, from the extreme dorsal
summit of the neural axis (Pl. 15, fig. 4_a_, VII). So far as I have been
able to determine, the auditory nerve and the seventh proper possess only a
single root common to the two. There is no anterior root for the seventh
any more than for the fifth.
Behind the auditory involution, at a stage subsequent to that in which the
fifth and seventh nerves appear, there arise a series of roots from the
dorsal summit of the hind-brain, which form the rudiments of the
glosso-pharyngeal and vagus nerves. These roots are formed towards the
close of stage H, but are still quite short at the beginning of stage I.
Their manner of development resembles that of the previously described
cranial nerves. The central ends of the roots of the opposite sides are at
first in contact with each other, and there is nothing to distinguish the
roots of the glosso-pharyngeal and of the vagus nerves from the dorsal
roots of spinal nerves. Like the dorsal roots of the spinal nerves, they
appear as a series of ventral prolongations of a continuous outgrowth from
the brain, which outgrowth is moreover continuous with that for the spinal
nerves[280]. The outgrowth of the vagus and glosso-pharyngeal nerves is not
continuous with that of the seventh nerve. This is shewn by Pl. 15, figs.
4_a_ and 4_b_. The outgrowth of the seventh nerve though present in 4_a_ is
completely absent in 4_b_ which represents a section just behind 4_a_.
Footnote 280: In the presence of this continuous outgrowth of
the brain from which spring the separate nerve stems of the
vagus, may perhaps be found a reconciliation of the apparently
conflicting statements of Götte and myself with reference to
the vagus nerve. Götte regards the vagus as a single nerve,
from its originating as an undivided rudiment; but it is clear
from my researches that, for Elasmobranchii at least, this
method of arguing will not hold good, since it would lead to
the conclusion that all the spinal nerves were branches of one
single nerve, since they too spring as processes from a
continuous outgrowth from the brain!
Thus, by the end of stage I, there have appeared the rudiments of the 5th,
7th, 8th, 9th and 10th cranial nerves, all of which spring from the
hind-brain. These nerves all develop precisely as do the posterior roots of
the spinal nerves, and it is a remarkable fact _that hitherto I have failed
to find a trace in the brain of a root of any cranial nerve arising from
the ventral corner of the brain as do the anterior roots of the spinal
nerves_[281].
Footnote 281: The conclusion here arrived at with reference to
the anterior roots, is opposed to the observations of both
Gegenbaur on Hexanchus, _Jenaische Zeitschrift_, Vol. VI., and
of Jackson and Clarke on Echinorhinus, _Journal of Anatomy and
Physiology_, Vol. X. These morphologists identify certain roots
springing from the medulla below and behind the main roots of
the vagus as true anterior roots of this nerve. The existence
of these roots is not open to question, but without asserting
that it is impossible for me to have failed to detect such
roots had they been present in the embryo, I think I may
maintain if these anterior roots are not present in the embryo,
their identification as vagus roots must be abandoned; and they
must be regarded as belonging to spinal nerves. This point is
more fully spoken of at p. 428.
It is admittedly difficult to prove a negative, and it may still turn out
that there are anterior roots of the brain similar to those of the spinal
cord; in the mean time, however, the balance of evidence is in favour of
there being none such. This at first sight appears a somewhat startling
conclusion, but a little consideration shews that it is not seriously
opposed to the facts which we know. In the first place it has been shewn by
myself[282] that in Amphioxus (whose vertebrate nature I cannot doubt) only
dorsal nerve-roots are present. Yet the nerves of Amphioxus are clearly
mixed motor and sensory nerves, and it appears to me far more probable that
Amphioxus represents a phase of development in which the nerves had not
acquired two roots, rather than one in which the anterior root has been
lost. In other words, the condition of the nerves in Amphioxus appears to
me to point to the conclusion _that primitively the cranio-spinal nerves of
vertebrates were nerves of mixed function with one root only, and that root
a dorsal one; and that the present anterior or ventral root is a secondary
acquisition_. This conclusion is further supported by the fact that the
posterior roots develop in point of time before the anterior roots. If it
be admitted that the vertebrate nerves primitively had only a single root,
then the retention of that condition in the brain implies that this became
differentiated from the remainder of the nervous system at a very early
period before the acquirement of anterior nerve-roots, and that these
eventually become developed only in the case of spinal nerves, and not in
the case of the already highly modified cranial nerves.
Footnote 282: _Journal of Anatomy and Physiology_, Vol. X.
[This Edition, No. IX.]
* * * * *
_Subsequent Changes of the Nerves._ To simplify my description of the
subsequent growth of the cranial nerves, I have inserted a short
description of their distribution in the adult. This is taken from a
dissection of Scyllium stellare, which like other species has some
individualities of its own not found in the other Elasmobranchii. For
points not touched on in this description I must refer the reader to the
more detailed accounts of my predecessors, amongst whom may specially be
mentioned Stannius[283] for Carcharias, Spinax, Raja, Chimæra, &c.;
Gegenbaur[284] for Hexanchus; Jackson and Clarke[285] for Echinorhinus.
Footnote 283: _Nervensystem d. Fische_, Rostock, 1849.
Footnote 284: _Jenaische Zeitschrift_, Vol. VI.
Footnote 285: _Journal of Anatomy and Physiology_, Vol. X.
The ordinary nomenclature has been employed for the branches of the fifth
and seventh nerves, though embryological data to be adduced in the sequel
throw serious doubts upon it. Since I am without observations on the origin
of the nerves to the muscles of the eyes, all account of these is omitted.
The fifth nerve arises from the brain by three roots[286]: (1) an
anterior more or less ventral root; (2) a root slightly behind, but
close to the former[287], formed by the coalescence of two distinct
strands, one arising from a dorsal part of the medulla, and a second
and larger from the ventral; (3) a dorsal and posterior root, in its
origin quite distinct and well separated from the other two, and
situated slightly behind the dorsal strand of the second root. This
root a little way from its attachment becomes enclosed for a short
distance in the same sheath as the dorsal part of the second root, and
a slight mixture of fibres seems to occur, but the majority of its
fibres have no connection with those of the second root. The first and
second roots of the fifth appear to me partially to unite, but before
their junction the ramus ophthalmicus profundus is given off from the
first of them.
Footnote 286: My results with reference to these roots accord
exactly, so far as they go, with the more carefully worked out
conclusions of Stannius, _loc. cit._ pp. 29 and 30.
Footnote 287: The root of the seventh nerve cannot properly be
distinguished from this root.
The fifth nerve, according to the usual nomenclature, has three main
divisions. The first of these is the ophthalmic. It is formed by the
coalescence of two entirely independent branches of the fifth, which
unite on leaving the orbit. The dorsalmost of these, or ramus
ophthalmicus superficialis, originates from the third and posterior of
the roots of the fifth, nearly the whole of which appears to enter
into its formation. This root is situated on the dorsal part of the
"lobi trigemini," _at a point posterior to that of the other roots of
the fifth or even of the seventh nerve_. The branch itself enters the
orbit by a separate foramen, and, keeping on the dorsal side of it,
reenters the cartilage at its anterior wall, and is there joined by
the _ramus ophthalmicus profundus_. This latter nerve arises from the
anterior root of the fifth, separately pierces the wall of the orbit,
and takes a course slightly ventral to the superior ophthalmic nerve,
but does not (as is usual with Elasmobranchii) run below the superior
rectus and superior oblique muscles of the eye. The nerve formed by
the coalescence of the superficial and deep ophthalmic branches
courses a short way below the surface, and supplies the mucous canals
of the front of the snout. It is a purely sensory nerve. Strong
grounds will be adduced in the sequel for regarding the _ramus
ophthalmicus superficialis_, though not the _ophthalmicus profundus_,
as in reality a branch of the seventh, and not of the fifth nerve.
The second division of the fifth nerve is the superior maxillary,
which appears to me to arise from both the first and second roots of
the fifth, though mainly from the first. It divides once into two main
branches. The first of these--the buccal nerve of Stannius--after
passing forwards along the base of the orbit takes its course
obliquely across the palatine arch and behind and below the nasal
sack, supplying by the way numerous mucous canals, and dividing at
last into two branches, one of these passing directly forwards on the
ventral surface of the snout, and the second keeping along the front
border of the mouth. The second division of the superior maxillary
nerve (superior maxillary of Stannius), after giving off a small
branch, which passes backwards in company with a branch from the
inferior maxillary nerve to the levator maxillæ superioris, itself
keeps close to the buccal nerve, and eventually divides into numerous
fine twigs to the mucous canals of the skin at the posterior region of
the upper jaw. It anastomoses with the buccal nerve. The inferior
maxillary nerve arises mainly from the second root of the fifth. After
sending a small branch to the levator maxillæ superioris, it passes
outwards along the line separating the musculus adductor mandibulæ
from the musculus levator labii superioris, and after giving branches
to these muscles takes a course forward along the border of the lower
jaw. It appears to be a mixed motor and sensory nerve.
The seventh or facial nerve arises by a root close to, but behind and
below the second root of the fifth, and is intimately fused with this.
It divides almost at once into a small anterior branch and large
posterior.
The anterior branch is the palatine nerve. It gives off at first one
or two very small twigs, which pursue a course towards the spiracle,
and probably represent the spiracular nerves of other Elasmobranchii.
Immediately after giving off these branches it divides into two stems,
a posterior smaller and an anterior larger one. The former eventually
takes a course which tends towards the angle of the jaw, and is
distributed to the mucous membrane of the roof of the mouth, while the
larger one bends forwards and supplies the mucous membrane at the edge
of the upper jaw. The main stem of the seventh, after giving off a
branch to the dorsal section of the musculus constrictor
superficialis, passes outwards to the junction of the upper and lower
jaws, where it divides into two branches, an anterior superficial
branch, which runs immediately below the skin on the surface of the
lower jaw, and a second branch, which takes a deep course along the
posterior border of the lower jaw, between it and the hyoid, and sends
a series of branches backwards to the ventral section of the musculus
constrictor superficialis. The main stem of the facial is mixed motor
and sensory. I have not noticed a dorsal branch, similar to that
described by Jackson and Clarke.
The auditory nerve arises immediately behind the seventh, but requires
no special notice here. A short way behind the auditory is situated
the root of the glossopharyngeal nerve. This nerve takes an oblique
course backwards through the skull, and gives off in its passage a
very small dorsal branch, which passes upwards and backwards through
the cartilage towards the roof of the skull. At the point where the
main stem leaves the cartilage it divides into two branches, an
anterior smaller branch to the hinder border of the hyoid arch, and a
posterior and larger one to anterior border of the first branchial
arch. It forks, in fact, over the first visceral cleft.
The vagus arises by a great number of distinct strands from the sides
of the medulla. In the example dissected there were twelve in all. The
anterior three of these were the largest; the middle one having the
most ventral origin. The next four were very small and in pairs, and
were separated by a considerable interval from the next four, also
very small, and these again by a marked interval from the hindermost
strand.
The common stem formed by the junction of these gives off immediately
on leaving the skull a branch which forks on the second branchial
cleft; a second for the third cleft is next given off; the main stem
then divides into a dorsal branch--the lateral nerve--and a ventral
one--the branchio-intestinal nerve--which, after giving off the
branches for the two last branchial clefts, supplies the heart and
intestinal tract. The lateral nerve passes back towards the posterior
end of the body, internal to the lateral line, and between the
dorso-lateral and ventro-lateral muscles. It gives off at its origin a
fine nerve, which has a course nearly parallel to its own. The main
stem of the vagus, at a short distance from its central end, receives
a nerve which springs from the ventral side of the medulla, on about a
level with the most posterior of the true roots of the vagus. This
small nerve corresponds with the ventral or anterior roots of the
vagus described by Gegenbaur, Jackson, and Clarke (though in the
species investigated by the latter authors these roots did not join
the vagus, but the anterior spinal nerves). Similar roots are also
mentioned by Stannius, who found two of them in the Elasmobranchii
dissected by him; it is possible that a second may be present in
Scyllium, but have been overlooked by me, or perhaps may have been
exceptionally absent in the example dissected.
_The Fifth Nerve._ The thinning of the roof of the brain, in the manner
already described, produces a great change in the apparent position of the
roots of all the nerves. The central ends of the rudiments of the two sides
are, as has been mentioned, at first in contact dorsally but, when by the
growth of the roof of the brain its two lateral halves become pushed apart,
the nerves also shift their position and become widely separated. The roots
of the fifth nerve are so influenced by these changes that they spring from
the brain about half way up its sides, and a little ventral to the border
of its thin roof. While this change has been taking place in the point of
attachment of the fifth nerve, it has not remained in other respects in a
stationary condition.
During stage H it already exhibits two distinct branches known as the
mandibular and ophthalmic. These branches first lie outside a section of
the body-cavity which exists in the front part of the head. The ophthalmic
branch of the fifth being situated near the anterior end of this, and the
mandibular near the posterior end.
In stage I the body-cavity in this part becomes divided into two parts one
behind the other, the posterior being situated in the mandibular arch. The
bifurcation of the nerve then takes place over the summit of the posterior
of the two divisions of the body-cavity, Pl. 15, figs. 9_b_, V, and 10, V,
&c., and at first both branches keep close to the sides of this.
The anterior or ophthalmic branch of the fifth soon leaves the walls of the
cavity just spoken of and tends towards the eye, and there comes in close
contact with the most anterior section of the body-cavity which exists in
the head. These relations it retains unchanged till the close of stage K.
Between stages I and K it may easily be seen from the surface; but, before
the close of stage K, the increased density of the tissues renders it
invisible in the living embryo.
The posterior branch of the fifth extends downwards into the mandibular
arch in close contact with the posterior and outer wall of the body space
already alluded to. At first no branches from it can be seen, but I have
detected by the close of stage K, by an examination of the living embryo, a
branch springing from it a short way from its central extremity, and
passing forwards, Pl. 15, fig. 2, V This branch I take to be the rudiment
of the superior maxillary division of the fifth nerve. It is shewn in
section, Pl. 15, fig. 15_a_, V.
In the stages after K the anatomy of the nerves becomes increasingly
difficult to follow, and accordingly I must plead indulgence for the
imperfections in my observations on all the nerves subsequently to this
date. In the fifth I find up to stage O a single ophthalmic branch (Pl. 17,
fig. 4_b_, V._op.th._), which passes forwards slightly dorsal to the eye
and parallel and ventral to a branch of the seventh, which will be
described when I come to that nerve. I have been _unable_ to observe that
this branch divides into a ramus superficialis and ramus profundus, and
subsequently to stage O I have no observations on it.
By stage O the fifth may be observed to have two very distinct roots, and a
large ganglionic mass is developed close to their junction (Gasserian
ganglion), Pl. 17, fig. 4_a_. But in addition to this ganglionic
enlargement, all of the branches have special ganglia of their own, Pl. 17,
fig. 4_b_.
_Summary._ The fifth nerve has almost from the beginning two branches, the
ophthalmic (probably the inferior ophthalmic of the adult) and the inferior
maxillary. The superior maxillary nerve arises later than the other two as
a branch from the inferior, originating comparatively far from its root.
There is at first but a single root for the whole nerve, which subsequently
becomes divided into two. Ganglionic swellings are developed on the common
stem and main branches of the nerve.
A general view of the nerve is shewn in the diagram in Pl. 17, fig. 1.
* * * * *
_Seventh and Auditory Nerves._ There appears in my earliest sections a
single large rudiment in the position of the seventh and auditory nerves;
but in longitudinal sections of an embryo somewhat older than stage I, in
which the auditory organ forms a fairly deep pit, still widely open to the
exterior, there are to be seen immediately in front of the ear the
rudiments of two nerves, which come into contact where they join the brain
and have their roots still closely connected at the end of stage K (Pl. 15,
figs. 10 and 15_a_ and 15_b_). The anterior of these pursues a straight
course to the hyoid arch (Pl. 15, fig. 10, VII), the second of the two
(Pl. 15, fig. 10, _au.n._), which is clearly the rudiment of the auditory
nerve, develops a ganglionic enlargement and, turning backward, closely
hugs the ventral wall of the auditory involution.
The observation just recorded appears to lead to the following conclusions
with reference to the development of the auditory nerve. A single rudiment
arises from the brain for the auditory and seventh nerves. This rudiment
subsequently becomes split into two parts, an anterior to form the seventh
nerve, and a posterior to form the auditory nerve. The ganglionic part of
the auditory nerve is derived from the primitive outgrowths from the brain,
and not from the auditory involution. I do not feel perfectly confident
that an independent origin of the auditory nerve might not have escaped my
notice; but, admitting the correctness of the view which attributes to the
seventh and auditory a common origin, it follows that the auditory nerve
primitively arose in connection with the seventh, of which it may either,
as Gegenbaur believes, be a distinct part--the ramus dorsalis--or else may
possibly have formed part of a commissure, homologous with that uniting the
dorsal roots of the spinal nerves, connecting the seventh with the
glossopharyngeal nerve. In either case it must be supposed secondarily to
have become separate and independent in consequence of the development of
the organ of hearing.
My sections of embryos of stage K and the subsequent stages do not bring to
light many new facts with reference to the auditory nerve: they demonstrate
however that its ganglionic part increases greatly in size, and in stage O
there is a distinct root for the auditory nerve in contact with that for
the seventh.
The history of the seventh nerve in its later stages presents points of
great interest. Near the close of stage K there may be observed, in the
living embryos and in sections, two branches of the seventh in addition to
the original trunk to the hyoid arch, both arising from its anterior side;
one passes straight forwards close to the external skin, but is at first
only traceable a short way in front of the fifth, and a second passes
downwards into the mandibular arch in such a fashion, that the seventh
nerve forks over the hyomandibular cleft (vide Pl. 15, fig. 2, VII.; 15_a_,
VII.). My sections shew both these branches with great clearness. A third
branch has also come under my notice, whose course leads me to suppose that
it supplies the roof of the palate.
In the later stages my attention has been specially directed to the very
remarkable anterior branch of the seventh. This may, in stages L to O, be
traced passing on a level with the root of the fifth nerve above the eye,
and apparently terminating in branches to the skin in front of the eye
(Pl. 17, figs. 3, VII.; 4_a_, VII,_a_). It courses close beneath the skin
(though this does not appear in the sections represented on account of
their obliqueness), and runs parallel and dorsal to the ophthalmic branch
of the fifth nerve, and may easily be seen in this position in longitudinal
sections belonging to stage O; but its changes after this stage have
hitherto baffled me, and its final fate is therefore, to a certain extent,
a matter of speculation.
The two other branches of the seventh, viz., the hyoid or main branch and
mandibular branch, retain their primitive arrangement till the close of
stage O.
The fate of the remarkable anterior branch of the seventh nerve is one of
the most interesting points which has started up in the course of my
investigations on the development of the cranial nerves, and it is a matter
of very great regret to me that I have not been able to clear up for
certain its later history.
Its primitive distribution leads to the supposition that it becomes the
nerve known in the adult as the _ramus ophthalmicus superficialis of the
fifth nerve_, and this is the view which I admit myself to be inclined to
adopt. There are several points in the anatomy of this nerve in the adult
which tell in favour of accepting this view with reference to it. In the
first place, the ramus ophthalmicus superficialis rises from the brain
(vide description above, p. 417), quite independently of the ramus
ophthalmicus profundus, and not in very close connection with the other
branches of the fifth, and also considerably behind these, quite as far
back indeed as the ventral root of the seventh. There is therefore nothing
in the position of its root opposed to its being regarded as a branch of
the seventh nerve. Secondly, its distribution, which might at first sight
be regarded as peculiar, presents no very strange features if it is looked
on as a ramus dorsalis of the seventh, whose apparent anterior instead of
dorsal course is due to the cranial flexure. If, however, the distribution
of the ramus ophthalmicus superficialis is used as an argument against my
view, a satisfactory reply is to be found in the fact that a branch of the
seventh nerve certainly has the distribution in question _in the embryo_,
and that there is no reason why it should not retain it _in the adult_.
Finally, the junction of the two rami ophthalmici, most remarkable if they
are branches of a single nerve, would present nothing astonishing when they
are regarded as branches of two separate nerves.
If this view be adopted, certain modifications of the more generally
accepted views of the morphology of the cranial nerves will be
necessitated; but this subject is treated of at the end of this section.
Some doubt hangs over the fate of the other branches of the seventh nerve,
but their destination is not so obscure as that of the anterior branch. The
branch to the roof of the mouth can be at once identified as the 'palatine
nerve', and it only remains to speak of the mandibular branch.
It may be noticed first of all with reference to this branch, that the
seventh behaves precisely like the less modified succeeding cranial nerves.
It forks in fact over a visceral cleft (the hyomandibular) the two sides of
which it supplies; the branch at the anterior side of the cleft is the
later developed and smaller of the two. There cannot be much doubt that the
mandibular branch must be identified with the spiracular nerve
(præ-spiracular branch Jackson and Clarke) of the adult, and if the chorda
tympani of Mammals is correctly regarded as the mandibular branch of the
seventh nerve, then the spiracular nerve must represent it. Jackson and
Clarke[288] take a different view of the homology of the chorda tympani,
and regard it as equivalent to the ramus mandibularis internus (one of the
two branches into which the seventh eventually divides), because this nerve
takes its course over the ligament connecting the mandible with the hyoid.
This view I cannot accept so long as it is admitted that the chorda tympani
is the branch of a cranial nerve supplying the anterior side of a cleft.
The ramus mandibularis internus, instead of forming with the main branch of
the seventh a fork over the spiracle, passes to its destination completely
behind and below the spiracle, and therefore fails to fulfil the conditions
requisite for regarding it as a branch to the anterior wall of a visceral
cleft. It is indeed clear that the ramus mandibularis internus cannot be
identified with the embryonic mandibular branch of the seventh (which
passes above the spiracle or hyomandibular cleft) when there is present in
the adult another nerve (the spiracular nerve), which exactly corresponds
in distribution with the embryonic nerve in question. My view accords
precisely with that already expressed by Gegenbaur in his masterly paper on
the nerves of Hexanchus, in which he distinctly states that he looks upon
the spiracular nerve as the homologue of an anterior branchial branch of a
division of the vagus. In the adult the spiracular nerve is sometimes
represented by one or two branches of the palatine, _e.g._ Scyllium, but at
other times arises independently from the main stem of the seventh[289].
The only difficulty in my identification of the embryonic mandibular branch
with the adult spiracular nerve, is the extremely small size of the latter
in the adult, compared with the size of mandibular in the embryo; but it is
hardly surprising to find an atrophy of the spiracular nerve accompanying
an atrophy of the spiracle itself. The palatine appears to me to have been
rightly regarded by Jackson and Clarke as the great superficial petrosal of
Mammals.
Footnote 288: _Loc. cit._
Footnote 289: Hexanchus, Gegenbaur, _Jenaische Zeitschrift_, Vol. VI.
On the common root of the branches of the seventh nerve, as well as on its
hyoid branch, ganglionic enlargements are present at an early period of
development.
_The Glossopharyngeal and Vagus Nerves._ Behind the ear there are formed a
series of five nerves which pass down to respectively the first, second,
third, fourth and fifth visceral arches.
For each arch there is thus one nerve, whose course lies close to the
posterior margin of the preceding cleft, a second anterior branch being
developed later. These nerves are connected with the brain (as I have
determined by transverse sections) by roots at first attached to the dorsal
summit, but eventually situated about half-way down the sides (Pl. 15,
fig. 6) nearly opposite the level of the process which divides the
ventricle of the hind-brain into a dorsal and a ventral moiety. The
foremost of these nerves is the glossopharyngeal. The next four are, as has
been shewn by Gegenbaur[290], equivalent to four independent nerves, but
form, together with the glossopharyngeal, a compound nerve, which we may
briefly call the vagus.
Footnote 290: _Loc. cit._
This compound nerve by stage K attains a very complicated structure, and
presents several remarkable and unexpected features. Since it has not been
possible for me completely to elucidate the origin of all its various
parts, it will conduce to clearness if I give an account of its structure
during stage K or L, and then return to what facts I can mention with
reference to its development. Its structure during these stages is
represented on the diagram, Pl. 17, fig. 1. There are present five
branches, viz. the glossopharyngeal and four branches of the vagus, arising
probably by a considerably greater number of strands from the brain[291].
All the strands from the brain are united together by a thin commissure,
_Vg.com._, continuous with the commissure of the posterior roots of the
spinal nerves, and from this commissure the five branches are continued
obliquely ventralwards and backwards, and each of them dilates into a
ganglionic swelling. They all become again united together by a second
thick commissure, which is continued backwards as the intestinal branch of
the vagus nerve _Vg.in._ The nerves, however, are continued ventralwards
each to its respective arch. From the hinder part of the intestinal nerve
springs the lateral nerve _n.l._, at a point whose relations to the
branches of the vagus I have not certainly determined.
Footnote 291: In the diagram there are only five strands
represented. This is due to the fact that I have not certainly
made out their true number.
The whole nerve-complex formed by the glossopharyngeal and the vagus nerves
cannot of course be shewn in any single section. The various roots are
shewn in Pl. 17, fig. 5. The dorsal commissure is represented in
longitudinal section in Pl. 15, fig. 15_b_, _com._, and in transverse
section in Pl. 17, fig. 2, _Vg.com_ The lower commissure continued as the
intestinal nerve is shewn in Pl. 15, fig. 15_a_, _Vg._, and as seen in the
living embryo in Pl. 15, figs. 1 and 2. The ganglia are seen in Pl. 15,
fig. 6, _Vg_. The junction of the vagus and glossopharyngeal nerves is
shewn in Pl. 15, fig. 10. My observations have not taught me much with
reference to the origin of the two commissures, viz. the dorsal one and the
one which forms the intestinal branch of the vagus. Very possibly they
originate as a single commissure which becomes longitudinally segmented. It
deserves to be noticed that the dorsal commissure has a long stretch, from
the last branch of the vagus to the first spinal nerve, during which it is
not connected with the root of any nerve; vide fig. 15_b_, _com_. This
space probably contained originally the now lost branches of the vagus. In
many transverse sections where the dorsal commissure might certainly be
expected to be present it cannot be seen, but this is perhaps due to its
easily falling out of the sections. I have not been able to prove that the
commissure is continued forwards into the auditory nerve.
The relation of the branches of the vagus and glossopharyngeal to the
branchial clefts requires no special remark. It is fundamentally the same
in the embryo as in the adult. The branches at the posterior side of the
clefts are the first to appear, those at the anterior side of the clefts
being formed subsequently to stage K.
One of the most interesting points with reference to the vagus is the
number of separate strands from the brain which unite to form it. The
questions connected with these have been worked out in a masterly manner,
both from an anatomical and a theoretical standpoint, by Professor
Gegenbaur[292]. It has not been possible for me to determine the exact
number of these in my embryos, nor have I been able to shew whether they
are as numerous at the earliest appearance of the vagus as at a later
embryonic period. The strands are connected (Pl. 17, fig. 5) with separate
ganglionic centres in the brain, though in several instances more than one
strand is connected with a single centre. In an embryo between stage O and
P more than a dozen strands are present. In an adult Scyllium I counted
twelve separate strands, but their number has been shewn by Gegenbaur to be
very variable. It is possible that they are remnants of the roots of the
numerous primary branches of the vagus which have now vanished; and this
perhaps is the explanation of their variability, since in the case of all
organs which are on the way to disappear variability is a precursor of
disappearance.
Footnote 292: _Loc. cit._
A second interesting point is the presence of the two connecting
commissures spoken of above. It was not till comparatively late in my
investigations that I detected the dorsal one. This has clearly the same
characters as the dorsal commissure already described as connecting the
roots of all the spinal nerves, and is indeed a direct prolongation of
this. It becomes gradually thinner and thinner, and finally ceases to be
observable by about the close of stage L. It is of importance as shewing
the similarity of the branches of the vagus to the dorsal roots of the
spinal nerves. The ventral of the two commissures persists in the adult as
the common stem from which all the branches of the vagus successively
originate, and is itself continued backwards as the intestinal branch of
the vagus. The glossopharyngeal nerve alone becomes eventually separated
from the succeeding branches. Stannius and Gegenbaur have, as was mentioned
above, detected in adult Elasmobranchii roots which join the vagus, and
which resemble the anterior or ventral roots of spinal nerves; and I have
myself described one such root in the adult Scyllium. I have searched for
these in my embryos, but without obtaining conclusive results. In the
earliest stages I can find no trace of them, but I have detected in stage L
one anterior root on debatable border-land, which may conceivably be the
root in question, but which I should naturally have put down for the root
of a spinal nerve. Are the roots in question to be regarded as proper roots
of the vagus, or as ventral roots of spinal nerves whose dorsal roots have
been lost? The latter view appears to me the most probable one, partly from
the embryological evidence furnished by my researches, which is clearly
opposed to the existence of anterior roots in the brain, and partly from
the condition of these roots in Echinorhinus, in which they join the
succeeding spinal nerves and not the vagus[293]. The similar relations of
the apparently homologous branch or branches in many Osseous Fish may also
be used as an argument for my view.
Footnote 293: Vide Jackson and Clarke, _loc. cit._ The authors
take a different view to that here advocated, and regard the
ventral roots described by them as having originally belonged
to the vagus.
If, as seems probable, the roots in question become the hypoglossal nerve,
this nerve must be regarded as formed from the anterior roots of one or
more spinal nerves. Without embryological evidence it does not however seem
possible to decide whether the hypoglossal nerve contains elements only of
anterior roots or of both anterior and posterior roots.
_Mesoblast of the Head._
_Body-Cavity and Myotomes of the Head._--During stage F the appearance of a
cavity on each side in the mesoblast of the head was described. (Vide
Pl. 10, figs. 3_b_ and 6, _pp_.) These cavities end in front opposite the
blind anterior extremity of the alimentary canal; behind they are
continuous with the general body-cavity. I propose calling them the
_head-cavities_. The cavities of the two sides have no communication with
each other.
Coincidently with the formation of an outgrowth from the throat to form the
first visceral cleft, the head-cavity on each side becomes divided into a
section in front of the cleft and a section behind the cleft (vide Pl. 15,
figs. 4_a_ and 4_b_, _pp._); and during stage H it becomes, owing to the
formation of a second cleft, divided into three sections: (1) a section in
front of the first or hyomandibular cleft; (2) a section in the hyoid arch
between the hyomandibular cleft and the hyobranchial or first branchial
cleft; (3) a section behind the first branchial cleft.
The section in front of the hyomandibular cleft stands in a peculiar
relation to the two branches of the fifth nerve. The ophthalmic branch of
the fifth lies close to the outer side of its anterior part, the mandibular
branch close to the outer side of its posterior part. During stage I this
front section of the head-cavity grows forward, and becomes divided,
without the intervention of a visceral cleft, into an anterior and
posterior division. The anterior lies close to the eye, and in front of the
commencing mouth involution, and is connected with the ophthalmic branch of
the fifth nerve. The posterior part lies completely within the mandibular
arch, and is closely connected with the mandibular division of the fifth
nerve.
As the rudiments of the successive visceral clefts are formed, the
posterior part of the head-cavity becomes divided into successive sections,
there being one section for each arch. Thus the whole head-cavity becomes
on each side divided into (1) a premandibular section; (2) a mandibular
section; (3) a hyoid section; (4) sections in the branchial arches.
The first of these divisions forms a space of a considerable size, with
epithelial walls of somewhat short columnar cells. It is situated close to
the eye, and presents a rounded or sometimes triangular figure in sections
(Pl. 15, figs. 7, 9_b_ and 16_b_, 1_pp._). The ophthalmic branch of the
fifth nerve passes close to its superior and outer wall.
Between stages I and K the anterior cavities of the two sides are prolonged
ventralwards and meet below the base of the fore-brain (Pl. 15, fig. 8,
1_pp._). The connection between the two cavities appears to last for a
considerable time, and still persists at the close of stage L. The anterior
or premandibular pair of cavities are the only parts of the body-cavity
within the head which unite ventrally. In the trunk, however, the
primitively independent lateral halves of the body-cavity always unite in
this way. The section of the head-cavity just described is so similar to
the remaining posterior sections that it must be considered as equivalent
to them.
The next division of the head-cavity, which from its position may be called
the mandibular cavity, presents during the stages I and K a spatulate
shape. It forms a flattened cavity, dilated dorsally, and produced
ventrally into a long thin process parallel to the hyomandibular
gill-cleft, Pl. 15, fig. 1_pp._ and fig. 7, 9_b_ and 15_a_, 2_pp_. Like the
previous space it is lined by a short columnar epithelium.
The fifth nerve, as has already been mentioned, bifurcates over its dorsal
summit, and the mandibular branch of that nerve passes down on its
posterior and outer side. The mandibular aortic arch is situated close to
its inner side, Pl. 15, fig. 7. Towards the close of this period the upper
part of the cavity atrophies. Its lower part also becomes much narrowed,
but its walls of columnar cells persist and lie close to one another. The
outer or somatic wall becomes very thin indeed, the splanchnic wall, on the
other hand, thickens and forms a layer of several rows of elongated cells.
This thicker wall is on its inner side separated from the surrounding
tissue by a small space lined by a membrane-like structure. In each of the
remaining arches there is a segment of the original body-cavity
fundamentally similar to that in the mandibular arch. A dorsal dilated
portion appears, however, to be present in the third or hyoid section
alone, and even there disappears by the close of stage K. The cavities in
the posterior parts of the head become much reduced like those in its
anterior part, though at rather a later period. Their walls however
persist, and become more columnar. In Pl. 15, fig. 13_b_, _pp._, is
represented the cavity in the last arch but one, at a period when the
cavity in the mandibular arch has become greatly reduced. It occupies the
same position on the outer side of the aortic trunk of its arch as does the
cavity in the mandibular arch (Pl. 15, fig. 7, 2 _pp_). In Torpedo embryos
the head-cavity is much smaller, and atrophies earlier than in the embryos
of Pristiurus and Scyllium.
It has been shewn that, with the exception of the most anterior, the
divisions of the body-cavity in the head become atrophied, _not so however
their walls_. The cells forming these become elongated, and by stage N
become distinctly developed into muscles. Their exact history I have not
followed in its details, but they almost unquestionably become the musculus
constrictor superficialis and musculus interbranchialis[294]; and probably
also musculus levator mandibuli and other muscles of the front part of the
head.
Footnote 294: Vide Vetter, "Die Kiemen und Kiefermusculatur d.
Fische." _Jenaische Zeitschrift_, Vol. VII.
The most anterior cavity close to the eye remains unaltered much longer
than the remaining cavities, and its two halves are still in communication
at the close of stage L. I have not yet succeeded in tracing the subsequent
fate of its walls, _but think it probable that they develop into the
muscles of the eye_. The morphological importance of the sections of the
body-cavity in the head cannot be over-estimated, and the fact that the
walls become developed into the muscular system of the head renders it
almost certain _that we must regard them as equivalent to the muscle-plates
of the body, which originally contain, equally with those of the head,
sections of the body-cavity_. If this determination is correct, there can
be no doubt that they ought to serve as valuable guides to the number of
segments which have coalesced to form the head. This point is, however,
discussed in a subsequent section.
_General mesoblast of the head._--In stage G no mesoblast is present in the
head, except that which forms the walls of the head-cavity.
During stage H a few cells of undifferentiated connective tissue appear
around the stalk of the optic vesicle, and in the space between the front
end of the alimentary tract and the base of the brain in the angle of the
cranial flexure. They are probably budded off from the walls of the
head-cavities. Their number rapidly increases, and they soon form an
investment surrounding all the organs of the head, and arrange themselves
as a layer, between the walls of the roof of the fore and mid-brain and the
external skin. At the close of stage K they are still undifferentiated and
embryonic, each consisting of a large nucleus surrounded by a very delicate
layer of protoplasm produced into numerous thread-like processes. They form
a regular meshwork, the spaces of which are filled up by an intercellular
fluid.
I have not worked out the development of the cranial and visceral skeleton;
but this has been made the subject of an investigation by Mr Parker, who is
more competent to deal with it than any other living anatomist. His results
were in part made known in his lectures before the Royal College of
Surgeons[295], and will be published in full in the _Transactions of the
Zoological Society_.
Footnote 295: A report of the lectures appeared in _Nature_.
All my efforts have hitherto failed to demonstrate any segmentation in the
mesoblast of the head, other than that indicated by the sections of the
body-cavity before-mentioned; but since these, as above stated, must be
regarded as equivalent to muscle-plates, any further segmentation of
mesoblast could not be anticipated. To this statement the posterior part of
the head forms an apparent exception. Not far behind the auditory
involution there are visible at the end of period K a few longitudinal
muscles, forming about three or four muscle-plates, the ventral part of
which is wanting. I have not the means of deciding whether they properly
belong to the head, or may not really be a part of the trunk system of
muscles which has, to a certain extent, overlapped the back part of the
head, but am inclined to accept the latter view. These cranial
muscle-plates are shewn in Pl. 15, fig. 15_b_, and in Pl. 17, fig. 2.
_Notochord in the Head._
The notochord during stage G is situated for its whole length close under
the brain, and terminates opposite the base of the mid-brain. As the
cranial flexure becomes greater and mesoblast is collected in the angle
formed by this, the termination of the notochord recedes from the base of
the brain, but remains in close contact with the front end of the
alimentary canal. At the same time its terminal part becomes very much
thinner than the remainder, ends in a point, and exhibits signs of a
retrogressive metamorphosis. It also becomes bent upon itself in a ventral
direction through an angle of 180°; vide Pl. 15, figs. 9_a_ and 16_a_. In
some cases this curvature is even more marked than is represented in these
figures.
The bending of the end of the notochord is not directly caused by the
cranial flexure, as is proved by the fact that the end of the notochord
becomes bent through a far greater angle than does the brain. During the
stages subsequent to K the ventral flexure of the notochord disappears, and
its terminal part acquires by stage O a distinct dorsal curvature.
_Hypoblast of the Head._
The only feature of the alimentary tract in the head which presents any
special interest is the formation of the gill-slits and of the thyroid
body. In the present section the development of the former alone is dealt
with; the latter body will be treated in the section devoted to the general
development of the alimentary tract.
The gill-slits arise as outgrowths of the lining of the throat towards the
external skin. In the gill-slits of Torpedo I have observed a very slight
ingrowth of the external skin towards the hypoblastic outgrowth in one
single case. In all other cases observed by me, the outgrowth from the
throat meets the passive external skin, coalesces with it, and then, by the
dissolution of the wall separating the lumen of the throat from the
exterior, a free communication from the throat outwards is effected; vide
Pl. 15, figs. 5_a_ and _b_, and 13_b_. Thus it happens that the walls
lining the clefts are entirely formed of hypoblast. The clefts are formed
successively[296], the anterior appearing first, and it is not till after
the rudiments of three have appeared, that any of them become open to the
exterior.
Footnote 296: Vide Plate 8.
In stage K, four if not five are open to the exterior, and the rudiments of
six, the full number, have appeared[297]. Towards the close of stage K
there arise, from the walls of the 2nd, 3rd and 4th clefts, very small
knob-like processes, the rudiments of the external gills. These outgrowths
are formed both by the lining of the gill-cleft and by the adjoining
mesoblast[298].
Footnote 297: The description of stage K and L, pp. 292 and
293, is a little inaccurate with reference to the number of the
visceral clefts, though the number visible in the hardened
embryos is correctly described.
Footnote 298: Vide on the development of the gills, Schenk,
_Sitz. d. k. Akad. Wien_, Vol. LXXI, 1875.
From the mode of development of the gill-clefts, it appears that their
walls are lined externally by hypoblast, and therefore that the external
gills are processes of the walls of the alimentary tract, _i.e._ are
covered by an hypoblastic, and not an epiblastic layer. It should be
remembered, however, that after the gill-slits become open, the point where
the hypoblast joins the epiblast ceases to be determinable, so that some
doubt hangs over the above statement.
The identification of the layer to which the gills belong is not without
interest. If the external gills have an epiblastic origin, they may be
reasonably regarded[299] as homologous with the external gills of Annelids;
but, if derived from the hypoblast, this view becomes, to say the least,
very much less probable.
Footnote 299: Vide Dohrn, _Ursprung d. Wirbelthiere_.
_Segmentation of the Head._
The nature of the vertebrate head and its relation to the trunk forms some
of the oldest questions of Philosophical Morphology.
The answers of the older anatomists to these questions are of a
contradictory character, but within the last few years it has been more or
less generally accepted that the head is, in part at least, merely a
modified portion of the trunk, and composed, like that, of a series of
homodynamous segments[300]. While the researches of Huxley, Parker,
Gegenbaur, Götte, and other anatomists, have demonstrated in an
approximately conclusive manner that the head is composed of a series of
segments, great divergence of opinion still exists both as to the number of
these segments, and as to the modifications which they have undergone,
especially in the anterior part of the head. The questions involved are
amongst the most difficult in the whole range of morphology, and the
investigations recorded in the preceding pages do not, I am very well
aware, go far towards definitely solving them. At the same time my
observations on the nerves and on the head-cavities appear to me to throw a
somewhat new light upon these questions, and it has therefore appeared to
me worth while shortly to state the results to which a consideration of
these organs points. There are three sets of organs, whose development has
been worked out, each of which presents more or less markedly a segmental
arrangement:--(1) The cranial nerves; (2) the visceral clefts; (3) the
divisions of the head-cavity.
Footnote 300: Semper, in his most recent work, maintains, if I
understand him rightly, that the head is in no sense a modified
part of the trunk, but admits that it is segmented in a similar
fashion to the trunk.
The first and second of these have often been employed in the solution of
the present problem, while the third, so far as is known, exists only in
the embryos of Elasmobranchii.
The development of the cranial nerves has recently been studied with great
care by Dr Götte, and his investigations have led him to adopt very
definite views on the segments of head. The arrangement of the cranial
nerves _in the adult_ has frequently been used in morphological
investigations about the skull, but there are to my mind strong grounds
against regarding it as affording a safe basis for speculation. The most
important of these depends on the fact that nerves are liable to the
greatest modification on any changes taking place in the organs they
supply. On this account it is a matter of great difficulty, amounting in
many cases to actual impossibility, to determine the morphological
significance of the different nerve-branches, or the nature of the fusions
and separations which have taken place at the roots of the nerves. It is,
in fact, only in those parts of the head which have, relatively speaking,
undergone but slight modifications, and which require no special
elucidation from the nerves, that these sufficiently retain in the adult
their primitive form to serve as trustworthy morphological guides.
I propose to examine separately the light thrown on the segmentation of the
head by the development of (1) the nerves, (2) the visceral clefts, (3) the
head-cavities; and then to compare the three sets of results so obtained.
The post-auditory nerves present no difficulties; they are all organized in
the same fashion, and, as was first pointed out by Gegenbaur, form five
separate nerves, each indicating a segment. A comparison of the
post-auditory nerves of Scyllium and other typical Elasmobranchii with
those of Hexanchus and Heptanchus proves, however, that other segments were
originally present behind those now found in the more typical forms. And
the presence in Scyllium of numerous (twelve) strands from the brain to
form the vagus, as well as the fact that a large section of the commissure
connecting the vagus roots with the posterior roots of the spinal nerves is
not connected with the brain, appear to me to shew that all traces of the
lost nerves have not yet vanished.
Passing forwards from the post-auditory nerves, we come to the seventh and
auditory nerves. The embryological evidence brought forward in this paper
is against regarding these nerves as representing two segments. Although it
must be granted that my evidence is not conclusive against an independent
formation of these two nerves, yet it certainly tells in favour of their
originating from a common rudiment, and Marshall's results on the origin of
the two nerves in Birds (published in the _Journal of Anatomy and
Physiology_, Vol. XI. Part 3) support, I have reason to believe, the same
conclusion. Even were it eventually to be proved that the auditory nerve
originated independently of the seventh, the general relations of this
nerve, embryological and otherwise, are such that, provisionally at least,
it could not be regarded as belonging to the same category as the facial or
glossopharyngeal nerves, and it has therefore no place in a discussion on
the segmentation of the head.
The seventh nerve of the embryo (Pl. 17, fig. 1, VII) is formed by the
junction of three conspicuous branches, (1) an anterior dorsal branch which
takes a more or less horizontal course above the eye (VII. _a_); (2) a main
branch to the hyoid arch (VII. _hy_); (3) a smaller branch to the posterior
edge of the mandibular arch (VII. _mn_). The first of these branches can
clearly be nothing else but the typical "ramus dorsalis," of which however
the auditory may perhaps be a specialized part. The fact that this branch
pursues an anterior and not a directly dorsal course is probably to be
explained as a consequence of the cranial flexure. The two other branches
of the seventh nerve are the same as those present in all the posterior
nerves, viz. the branches to the two sides of a branchial cleft, in the
present instance the spiracle; the seventh nerve being clearly the nerve of
the hyoid arch.
The fifth nerve presents in the arrangement of its branches a similarity to
the seventh nerve so striking that it cannot be overlooked. This similarity
is at once obvious from an inspection of the diagram of the nerves on
Pl. 17, fig. 1, V, or from an examination of the sections representing
these nerves (Pl. 17, figs. 3 and 4). It divides like the seventh nerve
into three main branches: (1) an anterior and dorsal branch (_r._
ophthalmicus profundus), whose course lies parallel to but ventral to that
of the dorsal branch of the seventh nerve; (2) a main branch to the
mandibular arch (_r._ maxillæ inferioris); and (3) an anterior branch to
the palatine arcade (_r._ maxillæ superioris). I was at first inclined to
regard the anterior branch of the fifth (ophthalmic) as representing a
separate nerve, and was supported in this view by its relation to the most
anterior of the head-cavities; but the unexpected discovery of an exactly
_similar branch_ in the seventh nerve has induced me to modify this view,
and I am now constrained to view the fifth as a single nerve, whose
branches exactly correspond with those of the seventh. The anterior branch
of the fifth is, like the corresponding branch of the seventh, the _ramus
dorsalis_, and the two other branches are the equivalent of the branches of
the seventh, which fork over the spiracle, though in the case of the fifth
nerve no distinct cleft is present unless we regard the mouth as such.
Embryology thus appears to teach us that the fifth nerve is a single nerve
supplying the mandibular arch, and not, as has been usually thought, a
complex nerve resulting from the coalescence of two or three distinct
nerves. My observations do not embrace the origin or history of the third,
fourth, and sixth nerves, but it is hardly possible to help suspecting that
in these we have the nerve of one or more segments in front of that
supplied by the fifth nerve; a view which well accords with the most recent
morphological speculations of Professor Huxley[301].
Footnote 301: Preliminary note upon the brain and skull of
Amphioxus, _Proc. of the Royal Society_, Vol. XXII.
From this enumeration of the nerves the optic nerve is excluded for obvious
reasons, and although it has been shewn above that the olfactory nerve
develops like the other nerves as an outgrowth from the brain, yet its very
late appearance and peculiar relations are, at least for the present, to my
mind sufficient grounds for excluding it from the category of segmental
cranial nerves.
The nerves then give us indications of seven cranial segments, or, if the
nerves to the eye-muscles be included, of _at the least_ eight segments,
but to these must be added a number of segments now lost, but which once
existed behind the last of those at present remaining.
The branchial clefts have been regarded as guides to segmentation by
Gegenbaur, Huxley, Semper, etc., and this view cannot I think be
controverted. In Scyllium there are six clefts which give indications of
seven segments, viz., the segments of the mandibular arch, hyoid arch, and
of the five branchial arches. If, following the views of Dr Dohrn[302], we
regard the mouth as representing a cleft, we shall have seven clefts and
eight segments; and it is possible, as pointed out in Dr Dohrn's very
suggestive pamphlet, that remnants of a still greater number of præoral
clefts may still be in existence. Whatever may be the value of these
speculations, such forms as Hexanchus and Heptanchus and Amphioxus make it
all but certain that the ancestors of Vertebrates had a number of clefts
behind those now developed.
Footnote 302: _Ursprung d. Wirbelthiere._
The last group of organs to be dealt with for our present question is that
of the Head-Cavities.
The walls of the spaces formed by the cephalic prolongations of the
body-cavity develop into muscles and resemble the muscle-plates of the
trunk, and with these they must be identified, as has been already stated.
As equivalent to the muscle-plates, they clearly are capable of serving as
very valuable guides for determining the segmentation of the head. There
are then a pair of these in front of the mandibular arch, a pair in the
mandibular arch, and a pair in each succeeding arch. In all there are eight
pairs of these cavities representing eight segments, the first of them
præoral. As was mentioned above, each of the sections of the head-cavity
(except perhaps the first) stands in a definite relation to the nerve and
artery of the arch in which it is situated.
The comparative results of these three independent methods of determining
the segmentation of the head are in the subjoined table represented in a
form in which they can be compared:--
_Table of the Cephalic Segments as determined by the Nerves, Visceral
Arches, and Head-Cavities._
+----------+---------------------+------------------+----------------+
| Segments | Nerves | Visceral Arches | Head-Cavities |
| | | | or Cranial |
| | | | Muscle-Plates |
|----------+---------------------+------------------+----------------+
|Præoral 1 |3rd and 4th and | (?) |1st head cavity |
| |? 6th nerves (perhaps| |(in my figures |
| |representing more | | 1_pp._) |
| |than one segment) | | |
| | | | |
|Postoral 2|5th nerve |Mandibular |2nd head-cavity |
| | | |(in my figures |
| | | | 2_pp._) |
| | | | |
| ---- 3|7th nerve |Hyoid |3rd head-cavity |
| | | | |
| ---- 4|Glossopharyngeal |1st branchial arch|4th head-cavity |
| |nerve | | |
| | | | |
| ---- 5|1st branch of vagus |2nd branchial arch|5th head-cavity |
| | | | |
| ---- 6|2nd branch of vagus |3rd branchial arch|6th head-cavity |
| | | | |
| ---- 7|3rd branch of vagus |4th branchial arch|7th head-cavity |
| | | | |
| ---- 8|4th branch of vagus |5th branchial arch|8th head-cavity |
+----------+---------------------+------------------+----------------+
In the above table the first column denotes the segments of the head as
indicated by a comparison of the three sets of organs employed. The second
column denotes the segments as obtained by an examination of the nerves;
the third column is for the visceral arches (which lead to the same results
as, but are more convenient for our table than, the visceral clefts), and
the fourth column is for the head-cavities. It may be noticed that from the
second segment backwards the three sets of organs lead to the same results.
The head-cavities indicate one segment in front of the mouth, and now that
the ophthalmic branch of the fifth has been dethroned from its position as
a separate nerve, the eye-nerves, or one of them, may probably be regarded
as belonging to this segment. If the suggestion made above (p. 431), that
the walls of the first cavity become the eye-muscles, be correct, the
eye-nerves would perhaps after all be the most suitable nerves to regard as
belonging to the segment of the first head-cavity.
EXPLANATION OF PLATES 15, 16, 17.
PLATE 15. (THE HEAD DURING STAGES G--K.)
COMPLETE LIST OF REFERENCE LETTERS.
1_aa_, 2_aa_, etc. 1st, 2d, etc. aortic arch. _acv._ Anterior cardinal
vein. _al._ Alimentary canal. _ao._ Aorta. _au._ Thickening of epiblast to
form the auditory pit. _aun._ Auditory nerve. _aup._ Auditory pit. _auv._
Auditory vesicle. _b._ Wall of brain. _bb._ Base of brain. _cb._
Cerebellum. _cer._ Cerebrum. _Ch._ Choroid slit. _ch._ Notochord. _com._
Commissure connecting roots of vagus nerve. 1, 2, 3 etc. _eg._ External
gills. _ep._ External epiblast. _fb._ Fore-brain. _gl._ Glossopharyngeal
nerve. _hb._ Hind-brain. _ht._ Heart. _hy._ Hyaloid membrane. _In._
Infundibulum. _l._ Lens. _M._ Mouth involution. _m._ Mesoblast at the base
of the brain. _mb._ Mid-brain. _mn._ v. Mandibular branch of fifth. _ol._
Olfactory pit. _op._ Eye. _opn._ Optic nerve. _opv._ Optic vesicle.
_opth_V. Ophthalmic branch of fifth. _p._ Posterior root of spinal nerve.
_pn._ Pineal gland. 1, 2 etc. _pp._ First, second, etc. section of
body-cavity in the head. _pt._ Pituitary body. _so._ Somatopleure. _sp._
Splanchnopleure. _spc._ Spinal cord. _Th._ Thyroid body. _v._ Blood-vessel.
iv._v._ Fourth ventricle. v. Fifth nerve. _Vc._ Visceral cleft. _Vg._
Vagus. vii. Seventh or facial nerve.
Fig. 1. Head of a Pristiurus embryo of stage K viewed as a transparent
object.
The points which deserve special attention are: (1) The sections of the
body-cavity in the head (_pp_): the first or premandibular section being
situated close to the eye, the second in the mandibular arch. Above this
one the fifth nerve bifurcates. The third at the summit of the hyoid arch.
The cranial nerves and the general appearance of the brain are well shewn
in the figure.
The notochord cannot be traced in the living embryo so far forward as it is
represented. It has been inserted according to the position which it is
seen to occupy in sections.
Fig. 2. Head of an embryo of Scyllium canicula somewhat later than stage K,
viewed as a transparent object.
The figure shews the condition of the brain; the branches of the fifth and
seventh nerves (v. vii.); the rudiments of the semicircular canals; and the
commencing appearance of the external gills as buds on both walls of 2nd,
3rd, and 4th clefts. The external gills have not appeared on the first
cleft or spiracle.
Fig. 3. Section through the head of a Pristiurus embryo during stage G. It
shews (1) the fifth nerve (v.) arising as an outgrowth from the dorsal
summit of the brain. (2) The optic vesicles not yet constricted off from
the fore-brain.
Figs. 4_a_ and 4_b_. Two sections through the head of a Pristiurus embryo
of stage I. They shew (1) the appearance of the seventh nerve. (2) The
portion of the body-cavity belonging to the first and second visceral
arches. (3) The commencing thickening of epiblast to form the auditory
involution.
In 4_b_, the posterior of the two sections, no trace of an auditory nerve
is to be seen.
Figs. 5_a_ and 5_b_. Two sections through the head of a Torpedo embryo with
3 visceral clefts. Zeiss A, ocul. 1.
5_a_ shews the formation of the thin roof of the fourth ventricle by a
divarication of the two lateral halves of the brain.
Both sections shew the commencing formation of the thyroid body (_th_) at
the base of the mandibular arch.
They also illustrate the formation of the visceral clefts by an outgrowth
from the alimentary tract without any corresponding ingrowth of the
external epiblast.
Fig. 6. Section through the hind-brain of a somewhat older Torpedo embryo.
Zeiss A, ocul. 1.
The section shews (1) the attachment of a branch of the vagus to the walls
of the hind-brain. (2) The peculiar form of the hind-brain.
Fig. 7. Transverse section through the head of a Pristiurus embryo
belonging to a stage intermediate between I and K, passing through both the
fore-brain and the hind-brain. Zeiss A, ocul. 1.
The section illustrates (1) the formation of the pituitary body (_pt_) from
the mouth involution (_m_), and proves that, although the wall of the
throat (_al_) is in contact with the mouth involution, there is by this
stage no communication between the two. (2) The eye. (3) The sections of
the body-cavity in the head (1_pp_, 2_pp_). (4) The fifth nerve (v.) and
the seventh nerve (vii).
Fig. 8. Transverse section through the brain of a rather older embryo than
fig. 7. It shews the ventral junction of the anterior sections of the
body-cavity in the head (1_pp_).
Figs. 9_a_ and 9_b_. Two longitudinal sections through the brain of a
Pristiurus embryo belonging to a stage intermediate between I and K. Zeiss
A, ocul. 1.
9_a_ is taken through the median line, but is reconstructed from two
sections. It shews (1) The divisions of the brain--The cerebrum and
thalamencephalon in the fore-brain; the mid-brain; the commencing
cerebellum in the hind-brain. (2) The relation of the mouth involution to
the infundibulum. (3) The termination of the notochord.
9_b_ is a section to one side of the same brain. It shews (1) The divisions
of the brain. (2) The point of outgrowth of the optic nerves (_opn_). (3)
The sections of the body-cavity in the head and the bifurcation of the
optic nerve over the second of these.
Fig. 10. Longitudinal section through the head of a Pristiurus embryo
somewhat younger than fig. 9. Zeiss a, ocul. 4. It shews the relation of
the nerves and the junction of the fifth, seventh, and auditory nerves with
the brain.
Fig. 11. Longitudinal section through the fore-brain of a Pristiurus embryo
of stage K, slightly to one side of the middle line. It shews the deep
constriction separating the thalamencephalon from the cerebral hemispheres.
Fig. 12. Longitudinal section through the base of the brain of an embryo of
a stage intermediate between I and K.
It shews (1) the condition of the end of the notochord; (2) the relation of
the mouth involution to the infundibulum.
Fig. 13_a_. Longitudinal and horizontal section through part of the head of
a Pristiurus embryo rather older than K. Zeiss A, ocul. 1.
The figure contains the eye cut through in the plane of the choroid slit.
Thus the optic nerve (_opn_) and choroid slit (_ch_) are both exhibited.
Through the latter is seen passing mesoblast accompanied by a blood-vessel
(_v_). _Op_ represents part of the optic vesicle to one side of the choroid
slit.
No mesoblast can be seen passing round the outside of the optic cup; and
the only mesoblast which enters the optic cup passes through the choroid
slit.
Fig. 13_b_. Transverse section through the last arch but one of the same
embryo as 13_a_. Zeiss A, ocul. 1.
The figure shews (1) The mode of formation of a visceral cleft without any
involution of the external skin. (2) The head-cavity in the arch and its
situation in relation to the aortic arch.
Fig. 14. Surface view of the nasal pit of an embryo of same age as fig. 13,
considerably magnified. The specimen was prepared by removing the nasal
pit, flattening it out and mounting in glycerine after treatment with
chromic acid. It shews the primitive arrangement of the Schneiderian folds.
One side has been injured.
Figs. 15_a_ and 15_b_. Two longitudinal and vertical sections through the
head of a Pristiurus embryo belonging to stage K. Zeiss a, ocul. 3.
15_a_ is the most superficial section of the two. It shews the constitution
of the seventh and fifth nerves, and of the intestinal branch of the vagus.
The anterior branch of the seventh nerve deserves a special notice.
15_b_ mainly illustrates the dorsal commissure of the vagus nerve (_com_)
continuous with the dorsal commissures of the posterior root of the spinal
nerves.
Fig. 16. Two longitudinal and vertical sections of the head of a Pristiurus
embryo belonging to the end of stage K. Zeiss a, ocul. 1.
16_a_ passes through the median line of the brain and shews the
infundibulum, notochord and pituitary body, etc.
The pituitary body still opens into the mouth, though the septum between
the mouth and the throat is broken through.
16_b_ is a more superficial section shewing the head-cavities _pp_ 1, 2, 3,
and the lower vagus commissure.
PLATE 16.
COMPLETE LIST OF REFERENCE LETTERS.
_auv._ Auditory vesicle. _cb._ Cerebellum. _cer._ Cerebral hemispheres.
_ch._ Notochord. _cin._ Internal carotid. _ft._ Fasciculi teretes. _in._
Infundibulum. _lv._ Lateral ventricle. _mb._ Mid-brain, or optic lobes.
_md._ Medulla oblongata. _mn._ Mandible. _ol._ Olfactory pit. _oll._
Olfactory lobe. _op._ Eye. _opn._ Optic nerve. _opth._ Optic thalamus.
_pc._ Posterior commissure. _pcl._ Posterior clinoid. _pn._ Pineal gland.
_pt._ Pituitary body. _rt._ Restiform tracts. _tv._ Tela vasculosa of the
roof of the fourth ventricle. iv._v._ Fourth ventricle. vii. Seventh nerve.
_x._ Rudiment of septum which will grow backwards and divide the unpaired
cerebral rudiment into the two hemispheres.
Figs. 1_a_, 1_b_, 1_c_. Longitudinal sections of the brain of a Scyllium
embryo belonging to stage L. Zeiss a, ocul. 1.
1_a_ is taken slightly to one side of the middle line, and shews the
general features of the brain, and more especially the infundibulum (_in_)
and pituitary body (_pt_).
1_b_ is through the median line of the pineal gland.
1_c_ is through the median line of the base of the brain, and shews the
notochord (_ch_) and pituitary body (_pt_); the latter still communicating
with the mouth. It also shews the wide opening of the infundibulum in the
middle line into the base of the brain.
Fig. 2. Section through the unpaired cerebral rudiment during stage O, to
shew the origin of the olfactory lobe and the olfactory nerve. The latter
is seen to divide into numerous branches, one of which passes into each
Schneiderian fold. At its origin are numerous ganglion cells represented by
dots. Zeiss a, ocul. 2.
Fig. 3. Horizontal section through the three lobes of the brain during
stage O. Zeiss a, ocul. 2.
The figure shews (1) the very slight indications which have appeared by
this stage of an ingrowth to divide the cerebral rudiment into two lobes
(_x_): (2) the optic thalami united by a posterior commissure, and on one
side joining the base of the mid-brain, and behind them the pineal gland:
(3) the thin posterior wall of the cerebral rudiment with folds projecting
into the cerebral cavity.
Figs. 4_a_, 4_b_, 4_c_. Views from the side, from above, and from below, of
a brain of Scyllium canicula during stage P. In the view from the side the
eye (_op_) has not been removed.
The bilobed appearance both of the mid-brain and cerebellum should be
noticed.
Fig. 5. Longitudinal section of a brain of Scyllium canicula during stage
P. Zeiss a, ocul. 2.
There should be noticed (1) the increase in the flexure of the brain
accompanying a rectification of the cranial axis; (2) the elongated pineal
gland, and (3) the structure of the optic thalamus.
Figs. 6_a_, 6_b_, 6_c_. Views from the side, from above, and from below, of
a brain of Scyllium stellare during a slightly later stage than Q.
Figs. 7_a_ and 7_b_. Two longitudinal sections through the brain of a
Scyllium embryo during stage Q. Zeiss a, ocul. 2.
7_a_ cuts the hind part of the brain nearly through the middle line; while
7_b_ cuts the cerebral hemispheres and pineal gland through the middle.
In 7_a_ the infundibulum (1), cerebellum (2), the passage of the restiform
tracts (_rt_) into the cerebellum (3), and the rudiments of the tela
vasculosa (4) are shewn. In 7_b_ the septum between the two lobes of the
cerebral hemispheres (1), the pineal gland (2), and the relations of the
optic thalami (3) are shewn.
Figs. 8_a_, 8_b_, 8_c_, 8_d_. Four transverse sections of the brain of an
embryo slightly older than Q. Zeiss a, ocul. 1.
8_a_ passes through the cerebral hemispheres at their junction with the
olfactory lobes. On the right side is seen the olfactory nerve coming off
from the olfactory lobe. At the dorsal side of the hemispheres is seen the
pineal gland (_pn_).
8_b_ passes through the mid-brain now slightly bilobed, and the opening
into the infundibulum (_in_). At the base of the section are seen the optic
nerves and their chiasma.
8_c_ passes through the opening from the ventricle of the mid-brain into
that of the cerebellum. Below the optic lobes is seen the infundibulum with
the rudiments of the sacci vasculosi.
8_d_ passes through the front end of the medulla, and shews the roots of
the seventh pair of nerves, and the overlapping of the medulla by the
cerebellum.
PLATE 17.
COMPLETE LIST OF REFERENCE LETTERS.
vii. _a._ Anterior branch of seventh nerve. _ar._ Anterior root of spinal
nerve. _auv._ Auditory vesicle. _cer._ Cerebrum. _ch._ Notochord. _ch._
Epithelial layer of choroid membrane. _gl._ Glossopharyngeal nerve.
vii. _hy._ Hyoid branch of seventh nerve. _hym._ Hyaloid membrane. _ll._
Lateral line. v. _mn._ Ramus mandibularis of fifth nerve. vii. _mn._
Mandibular (spiracular) branch of seventh nerve. v. _mx._ Ramus maxillæ
superioris of fifth nerve. _nl._ Nervus lateralis. _ol._ Olfactory pit.
_op._ Eye. v. _opth._ Ramus ophthalmicus of fifth nerve. _pch._ Parachordal
cartilage. _pfal._ Processus falciformis. _pp._ Head cavity. _pr._
Posterior root of spinal nerve. _rt._ Retina. _sp._ Spiracle. v. Fifth
nerve. vii. Seventh nerve. _vc._ Visceral cleft. _vg._ Vagus nerve.
_vg.br._ Branchial branch of vagus. _vgcom._ Commissure uniting the roots
of the vagus, and continuous with commissure uniting the posterior roots of
the spinal nerves. _vgr._ Roots of vagus nerves in the brain. _vgin._
Intestinal branch of vagus. _vh._ Vitreous humour.
Fig. 1. Diagram of cranial nerves at stage L.
A description of the part of this referring to the vagus and
glossopharyngeal nerves is given at p. 426. It should be noticed that there
are only five strands indicated as springing from the spinal cord to form
the vagus and glossopharyngeal nerves. It is however probable that there
are even from the first a greater number of strands than this.
Fig. 2. Section through the hinder part of the medulla oblongata, stage
between K and L. Zeiss A, ocul. 2.
It shews (1) the vagus commissure with branches on one side from the
medulla: (2) the intestinal branch of the vagus giving off a nerve to the
lateral line.
Fig. 3. Longitudinal and vertical section through the head of a Scyllium
embryo of stage L. Zeiss a, ocul. 2.
It shews the course of the anterior branch of the seventh nerve (vii.);
especially with relation to the ophthalmic branch of the fifth nerve
(v. _oth_).
Figs. 4_a_ and 4_b_. Two horizontal and longitudinal sections through the
head of a Scyllium embryo belonging to stage O. Zeiss a, ocul. 2.
4_a_ is the most dorsal of the two sections, and shews the course of the
anterior branch of the seventh nerve above the eye.
4_b_ is a slightly more ventral section, and shews the course of the fifth
nerve.
Fig. 5. Longitudinal and horizontal section through the hind-brain at stage
O, shewing the roots of the vagus and glossopharyngeal nerves in the brain.
Zeiss B, ocul. 2.
There appears to be one root in the brain for the glossopharyngeal, and at
least six for the vagus. The fibres from the roots divide in many cases
into two bundles before leaving the brain. Swellings of the brain towards
the interior of the fourth ventricle are in connection with the first five
roots of the vagus, and the glossopharyngeal root; and a swelling is also
intercalated between the first vagus root and the glossopharyngeal root.
Fig. 6. Horizontal section through a part of the choroid slit at stage P.
Zeiss B, ocul. 2.
The figure shews (1) the rudimentary processus falciformis (_pfal_) giving
origin to the vitreous humour; and (2) the hyaloid membrane (_hym_) which
is seen to adhere to the retina, and not to the vitreous humour or
processus falciformis.
CHAPTER X.
THE ALIMENTARY CANAL.
The present Chapter completes the history of the primitive alimentary
canal, whose formation has already been described. In order to economise
space, no attempt has been made to give a full account of the alimentary
canal and its appendages, but only those points have been dealt with which
present any features of special interest.
The development of the following organs is described in order.
(1) The solid oesophagus.
(2) The postanal section of the alimentary tract.
(3) The cloaca and anus.
(4) The thyroid body.
(5) The pancreas.
(6) The liver.
(7) The subnotochordal rod.
_The solid oesophagus._
A curious point which has turned up in the course of my investigations is
the fact that for a considerable period of embryonic life a part of the
oesophagus remains quite solid and without a lumen. The part of the
oesophagus to undergo this peculiar change is that which overlies the
heart, and extends from the front end of the stomach to the branchial
region. At first, this part of the oesophagus has the form of a tube with a
well-developed lumen like the remainder of the alimentary tract, but at a
stage slightly younger than K its lumen becomes smaller, and finally
vanishes, and the original tube is replaced by a solid rod of uniform and
somewhat polygonal cells. A section of it in this condition is represented
in Pl. 11, fig. 8_a_.
At a slightly later stage its outermost cells become more columnar than the
remainder, and between stages K and L it loses its cylindrical form and
becomes much more flattened. By stage L the external layer of columnar
cells is more definitely established, and the central rounded cells are no
longer so numerous (Pl. 18, fig. 4, _soes_).
In the succeeding stages the solid part of the oesophagus immediately
adjoining the stomach is carried farther back relatively to the heart and
overlies the front end of the liver. A lumen is not however formed in it by
the close of stage Q, and beyond that period I have not carried my
investigations, and cannot therefore state the exact period at which the
lumen reappears. The limits of the solid part of the oesophagus are very
satisfactorily shewn in longitudinal and vertical sections.
The solidification of the oesophagus belongs to a class of embryological
phenomena which are curious rather than interesting, and are mainly worth
recording from the possibility of their turning out to have some
unsuspected morphological bearings.
Up to stage Q there are no signs of a rudimentary air-bladder.
_The postanal section of the alimentary tract._
An account has already been given (p. 307) of the posterior continuity of
the neural and alimentary canals, and it was there stated that Kowalevsky
was the discoverer of this peculiar arrangement. Since that account was
published, Kowalevsky has given further details of his investigations on
this point, and more especially describes the later history of the
hindermost section of the alimentary tract. He says[303]:
The two germinal layers, epiblast and hypoblast, are
continuous with each other at the border of the germinal
disc. The primitive groove or furrow appears at the border
of the germinal disc and is continued from the upper to the
lower side. By the closing of the groove there is formed the
medullary canal above, while the part of the groove on the
under surface directed below is chiefly converted into the
hind end of the alimentary tract. The connection of the two
tubes in Acanthias persists till the formation of the anus,
and the part of the nervous tube which lies under the chorda
passes gradually upwards to the dorsal side of the chorda,
and persists there for a long time in the form of a large
thin-walled vesicle.
Footnote 303: _Archiv f. Mic. Anat._ Vol. XIII. pp. 194, 195.
The last part of the description beginning at "The connection of" does not
hold good for any of the genera which I have had an opportunity of
investigating, as will appear from the sequel.
In a previous section[304] the history of the alimentary tract was
completed up to stage G.
Footnote 304: p. 303 et seq.
In stage H the point where the anus will (at a very much later period)
appear, becomes marked out by the alimentary tract sending down a
papilliform process towards the skin. This is shewn in Pl. 8, figs. _H_ and
_I, an_.
That part of the alimentary tract which is situated behind this point may,
for convenience, be called _the postanal section_. During stage H the
postanal section begins to develop a terminal dilatation or vesicle,
connected with the remainder of the canal by a narrower stalk. The relation
in diameter between the vesicle and the stalk may be gathered by a
comparison of figs. 3_a_ and 3_b_, Pl. 11. The diameter of the vesicle
represented in section in Pl. 11, fig. 3, is 0.328 Mm.
The walls both of the vesicle and stalk are formed of a fairly columnar
epithelium. The vesicle communicates in front by a narrow passage (Pl. 11,
fig. 3_a_) with the neural canal, and behind is continued into two horns
(Pl. 11, fig. 2, _al._) corresponding with the two caudal swellings spoken
of above (p. 288). Where the canal is continued into these two horns, its
walls lose their distinctness of outline, and become continuous with the
adjacent mesoblast.
In the succeeding stages up to K the tail grows longer and longer, and with
it grows the postanal section of the alimentary tract, without however
altering in any of its essential characters.
Its features at stage K are illustrated by an optical section of the tail
of an embryo (Pl. 18, fig. 5) and by a series of transverse sections
through the tail of another embryo in Pl. 18, figs. 6_a_, 6_b_, 6_c_, 6_d_.
In the optical section there is seen a terminal vesicle (_alv._) opening
into the neural canal, and connected with the remainder of the alimentary
tract. The terminal vesicle causes the end of the tail to be dilated, as is
shewn in Pl. 8, fig. _K_. The length of the postanal section extending from
the abdominal paired fins to the end of the tail (equal to rather less than
one-third of the whole length of the embryo), may be gathered from the same
figure.
The most accurate method of studying this part of the alimentary canal is
by means of transverse sections. Four sections have been selected for
illustration (Pl. 18, figs. 6_a_, 6_b_, 6_c_, and 6_d_) out of a
fairly-complete series of about one hundred and twenty.
Posteriorly (fig. 6_a_) there is present a terminal vesicle .25 Mm. in
diameter, and therefore rather smaller than in the earlier stage, whose
walls are formed of columnar epithelium, and which communicates dorsally by
a narrow opening with the neural canal; to this is attached a stalk in the
form of a tube, also lined by columnar epithelium, and extending through
about thirty sections (Pl. 18, fig. 6_b_). Its average diameter is about
.084 Mm. Overlying its front end is the subnotochordal rod (fig. 6_b_,
_x._), but this does not extend as far back as the terminal vesicle.
The thick-walled stalk of the vesicle is connected with the cloacal section
of the alimentary tract by a very narrow thin-walled tube (Pl. 18, 6_c_,
_al._). This for the most part has a fairly uniform calibre, and a diameter
of not more than .035 Mm. Its walls are formed of a flattened epithelium.
At a point not far from the cloaca it becomes smaller, and its diameter
falls to .03 Mm. In front of this point it rapidly dilates again, and,
after becoming fairly wide, opens on the dorsal side of the cloacal section
of the alimentary canal just behind the anus (fig. 6_d_).
Near the close of stage K at a point shortly behind the anus, where the
postanal section of the canal was thinnest in the early part of the stage,
the alimentary canal becomes solid (Pl. 11, fig. 9_d_), and a rupture here
occurs in it at a slightly later period.
In stage L the posterior part of the postanal section of the canal is
represented by a small rudiment near the end of the tail. The rudiment no
longer has a terminal vesicle, _nor does it communicate with the neural
canal_. It was visible in one series for about 40 sections, and was
continued forwards by a few granular cells, lying between the aorta and the
caudal vein. The portion of the postanal section of the alimentary tract
just behind the cloaca, was in the same embryo represented by a still
smaller rudiment of the dilated part which at an earlier period opened into
the cloaca.
Later than stage L no trace of the postanal section of the alimentary canal
has come under my notice, and I conclude that it vanishes without becoming
converted into any organ in the adult. Since my preliminary account of the
development of Elasmobranch Fishes was written, no fresh light appears to
have been thrown on the question of the postanal section of the alimentary
canal being represented in higher Vertebrata by the allantois.
_The cloaca and anus._
Elasmobranchii agree closely with other Vertebrates in the formation of the
cloaca and anus, and in the relations of the cloaca to the urinogenital
ducts.
The point where the anus, or more precisely the external opening of the
cloaca, will be formed, becomes very early marked out by the approximation
of the wall of the alimentary tract and external skin. This is shewn for
stages H and I in Pl. 8 _an_.
Between stages I and K the alimentary canal on either side of this point,
which we may for brevity speak of as the anus, is far removed from the
external skin, but at the anus itself the lining of the alimentary canal
and the skin are in absolute contact. There is, however, no involution from
the exterior, but, on the contrary, the position of the anus is marked by a
distinct prominence. Opposite the anus the alimentary canal dilates and
forms the cloaca.
During stage K, just in front of the prominence of the anus, a groove is
formed between two downgrowths of the body-wall. This is shewn in Pl. 11,
fig. 9_a_. During the same stage the segmental ducts grow downwards to the
cloaca, and open into it in the succeeding stage (Pl. 11, fig. 9_b_). Up to
stage K the cloaca is connected with the præanal section of the alimentary
canal in front, and the postanal section behind; the latter, however, by
stage L, as has been stated above, atrophies, with the exception of a very
small rudiment. In stage L the posterior part of the cloaca is on a level
with the hind end of the kidneys, and is situated behind the posterior
horns of the body-cavity, which are continued backwards to about the point
where the segmental ducts open into the cloaca, and though very small at
their termination rapidly increase in size anteriorly.
Nothing very worthy of note takes place in connection with the cloaca till
stage O. By this stage we have three important structures developed. (1) An
involution from the exterior to form the mouth of the cloaca or anus. (2) A
perforation leading into the cloaca at the hind end of this. (3) The
rudiments of the abdominal pockets. All of these structures are shewn in
Pl. 19, figs. 1_a_, 1_b_, 1_c_.
The mouth of the cloaca is formed by an involution of the skin, which is
deepest in front and becomes very shallow behind (Pl. 19, figs. 1_a_,
1_b_). At first only the mucous layer of the skin takes part in it, but
when the involution forms a true groove, both layers of the skin serve to
line it. At its posterior part, where it is shallowest, there is present,
at stage O, a slit-like longitudinal perforation, leading into the
posterior part of the cloaca (Pl. 19, fig. 1_c_) and forming its external
opening. Elsewhere the wall of the cloaca and cloacal groove are merely in
contact but do not communicate. On each side of the external opening of the
cloaca there is present an involution (Pl. 19, fig. 1_c_, _ab.p._) of the
skin, which resembles the median cloacal involution, and forms the rudiment
of an abdominal pocket. These two rudiments must not be confused with two
similar ones, which are present in all the three sections represented, and
mark out the line which separates the limbs from the trunk. These latter
are not present in the succeeding stages. The abdominal pockets are only
found in sections through the opening into the cloaca, and are only visible
in the hindermost of my three sections.
All the structures of the adult cloaca appear to be already constituted by
stage O, and the subsequent changes, so far as I have investigated them,
may be dealt with in very few words. The perforation of the cloacal
involution is carried slowly forwards, so that the opening into the cloaca,
though retaining its slit-like character, becomes continuously longer; by
stage Q its size is very considerable. The cloacal involution, relatively
to the cloaca, recedes backwards. In stage O its anterior end is situated
some distance in front of the opening of the segmental duct into the
cloaca; by stage P the front end of the cloacal involution is nearly
opposite this opening, and by stage Q is situated behind it.
As I have shewn elsewhere[305], the so-called abdominal pores of Scyllium
are simple pockets open to the exterior, but without any communication with
the body-cavity. By stage Q they are considerably deeper than in stage O,
and retain their original position near the hind end of the opening into
the cloaca. The opening of the urinogenital ducts into the cloaca will be
described in the section devoted to the urinogenital system.
Footnote 305: This Edition, No. VII. p. 152.
In Elasmobranchii, as in other Vertebrata, that part of the cloaca which
receives the urinogenital ducts, is in reality the hindermost section of
the gut and not the involution of epiblast which eventually meets this.
Thus the urinogenital ducts at first open into the alimentary canal and not
to the exterior. This fact is certainly surprising, and its meaning is not
quite clear to me.
The very late appearance of the anus may be noticed as a point in which
Elasmobranchii agree with other Vertebrata, notably the Fowl[306]. The
abdominal pockets, as might be anticipated from their structure in the
adult, are simple involutions of the epiblast.
Footnote 306: Vide Gasser, _Entwicklungsgeschichte der
Allantois, etc._
_The thyroid body._
The earliest trace of the thyroid body has come under my notice in a
Torpedo embryo slightly older than I. In this embryo it appeared as a
diverticulum from the ventral surface of the throat in the region of the
_mandibular arch_, and extended from the border of the mouth to the point
where the ventral aorta divided into the two aortic branches of the
mandibular arch. In front it bounded a groove (Pl. 15, fig. 5_a_, _Th._),
directly continuous with the narrow posterior pointed end of the mouth and
open to the throat, while behind it became a solid rod attached to the
ventral wall of the oesophagus (Pl. 15, fig. 5_b_, _Th._). In a Scyllium
embryo belonging to the early part of stage K, the thyroid gland presented
the same arrangement as in the Torpedo embryo just described, with the
exception that no solid posterior section of it was present.
Towards the close of stage K the thyroid body begins to elongate and become
solid, though it still retains its attachment to the wall of the
oesophagus. The solidification is effected by the columnar cells which line
the groove elongating and meeting in the centre. As soon as the lumen is by
these means obliterated, small cells make their appearance in the interior
of the body, probably budded off from the original columnar cells.
The gland continues to grow in length, and by stage L assumes a long
sack-like form with a layer of columnar cells bounding it externally, and a
core of rounded cells filling up its interior. Anteriorly it is still
attached to the throat, and its posterior extremity lies immediately below
the end of the ventral aorta. The cells of the gland contain numerous
yellowish concretionary pigment bodies, which are also present in the later
stages.
Up to stage P the thyroid gland retains its original position. Its form and
situation are shewn in Pl. 19, fig. 3, _th._, in longitudinal and vertical
section for a stage between O and P. The external layer of columnar cells
has now vanished, and the gland is divided up by the ingrowth of
connective-tissue septa into a number of areas or lobules--the rudiments of
the future follicles. These lobules are perfectly solid without any trace
of a lumen. A capillary network following the septa is present.
By stage Q the rudimentary follicles are more distinctly marked, but still
without a lumen, and a connective-tissue sheath indistinctly separated from
the surrounding tissue has been formed. My sections do not shew a junction
between the gland and the epithelium of the throat; but the two are so
close together, that I am inclined to think that such a junction still
exists. It is certainly present up to stage P.
Dr Müller[307], in his exhaustive memoir on the thyroid body, gives an
account of its condition in two Acanthias embryos. In his earliest embryo
(which, judging from the size, is perhaps about the same age as my latest)
the thyroid body is disconnected from the throat, yet contains a lumen, and
is not divided up into lobules. It is clear from this account, that there
must be considerable differences of detail in the development of the
thyroid body in Acanthias and Scyllium.
Footnote 307: _Jenaische Zeitschrift_, Vol. VI.
In the Bird Dr Müller's figures shew that the thyroid body develops in the
region of the hyoid arch, whereas, in Elasmobranchii, it develops in the
region of the mandibular arch. Dr Götte's[308] account of this body in
Bombinator accords very completely with my own, both with reference to the
region in which it develops, and its mode of development.
Footnote 308: _Entwicklungsgeschichte d. Unke._
_The pancreas._
The pancreas arises towards the close of stage K as a somewhat rounded
hollow outgrowth from the dorsal side of that part of the gut which from
its homologies may be called the duodenum. In the region where the pancreas
is being formed the appearances presented in a series of transverse
sections are somewhat complicated (Pl. 18, fig. 1), owing to the several
parts of the gut and its appendages which may appear in a single section,
but I have detected no trace of other than a single outgrowth to form the
pancreas.
By stage L the original outgrowth from the gut has become elongated
longitudinally, but transversely compressed: at the same time its opening
into the duodenum has become somewhat narrowed.
Owing to these changes the pancreas presents in longitudinal and vertical
section a funnel-shaped appearance (Pl. 19, fig. 4). From the expanded
dorsal part of the funnel, especially from its anterior end, numerous small
tubular diverticula grow out into the mesoblast. The apex of the funnel
leads into the duodenum. From this arrangement it results that at this
period the original outgrowth from the duodenum serves as a receptacle into
which each ductule of the embryonic gland opens separately. I have not
followed in detail the further growth of the gland. It is, however, easy to
note that while the ductules grow longer and become branched, vascular
processes grow in between them, and the whole forms a compact glandular
body in the mesentery on the dorsal side of the alimentary tract, and
nearly on a level with the front end of the spiral valve. The funnel-shaped
receptacle loses its original form, and elongating, assumes the character
of a duct.
From the above account it follows that the glandular part of the pancreas,
and not merely its duct, is derived from the original hypoblastic outgrowth
from the gut. This point is extremely clear in my preparations, and does
not, in spite of Schenk's observations to the contrary[309], appear to me
seriously open to doubt.
Footnote 309: _Lehrbuch d. vergleichenden Embryologie._
_The liver._
The liver arises during stage I as a ventral outgrowth from the duodenum
immediately in front of the opening of the umbilical canal (duct of the
yolk-sack) into the intestine. Almost as soon as it is formed this
outgrowth develops two lateral diverticula opening into a median canal.
The two diverticula are the rudimentary lobes of the liver, and the median
duct is the rudiment of the common bile-duct (ductus choledochus) and
gall-bladder (Pl. 11, fig. 9).
By stage K the hepatic diverticula have begun to bud out a number of small
hollow knobs. These rapidly increase in length and number, and form the
so-called hepatic cylinders. They anastomose and unite together, so that by
stage L there is constructed a regular network. As the cylinders increase
in length their lumen becomes very small, but appears never to vanish
(Pl. 19, fig. 5).
The mode of formation of the liver parenchyma by hollow and not solid
outgrowths agrees with the suggestion made in the _Elements of Embryology_,
p. 133, and also with the results of Götte on the Amphibian liver. Schenk
has thrown doubts upon the hypoblastic nature of the secreting tissue of
the liver, but it does not appear to me, from my own investigations, that
this point is open to question.
Coincidently with the formation of the hepatic network, the umbilical vein
(Pl. 11, fig. 9, _u.v._) which unites with the subintestinal or splanchnic
vein (Pl. 11, fig. 8, _V._) breaks up into a series of channels, which form
a second network in the spaces of the hepatic network. These vascular
channels of the liver appear to me to have from the first distinct walls of
delicate spindle-shaped cells, and I have failed to find a stage similar to
that described by Götte for Amphibians in which the blood-channels are
simply lacunar spaces in the hepatic parenchyma.
The changes of the median duct of the liver are of rather a passive nature.
By stage O its anterior end has dilated into a distinct gall-bladder, whose
duct receives in succession the hepatic ducts, and so forms the ductus
choledochus. The ductus choledochus opens on the ventral side of the
intestine immediately in front of the commencement of the spiral valve.
It may be noted that the liver and pancreas are corresponding ventral and
dorsal appendages of the part of the alimentary tract immediately in front
of its junction with the yolk-sack.
_The subnotochordal rod._
The existence of this remarkable body in Vertebrata was first made known by
Dr Götte[310], who not only demonstrated its existence, but also gave a
correct account of its development. Its presence in Elasmobranchii and mode
of development were mentioned by myself in my preliminary account of the
development of these fishes[311], and it has been independently observed
and described by Professor Semper[312]. No plausible suggestion as to its
function has hitherto been made, and it is therefore a matter of some
difficulty to settle with what group of organs it ought to be treated. In
the presence of this difficulty it seemed best to deal with it in this
chapter, since it is unquestionably developed from the wall of the
alimentary canal.
Footnote 310: _Archiv für Micros. Anatomie_, Bd. V., and
_Entwicklungsgeschichte d. Unke_.
Footnote 311: _Quarterly Journal of Microscopic Science_, Oct.,
1874. [This Edition, No. V.]
Footnote 312: "Stammverwandtschaft d. Wirbelthiere u.
Wirbellosen" and "Das Urogenitalsystem d. Plagiostomen," _Arb.
Zool.-Zoot. Institut. z. Würzburg_, Bd. II.
At its full growth this body forms a rod underlying the notochord, and has
nearly the same longitudinal extension as this. It is indicated in most of
my sections by the letter _x_. We may distinguish two sections of it, the
one situated in the head, the other in the trunk. The junction between the
two occurs at the hind border of the visceral clefts.
The section in the trunk is the first to develop. It arises during stage H
in the manner illustrated in Pl. 11, figs. 1 and 1_a_. The wall of the
alimentary canal becomes thickened (Pl. 11, fig. 1) along the median dorsal
line, or else produced into a ridge into which there penetrates a narrow
prolongation of the lumen of the alimentary canal. In either case the cells
at the extreme summit of the thickening become gradually constricted off as
a rod, which lies immediately dorsal to the alimentary tract, and ventral
to the notochord. The shape of the rod varies in the different regions of
the body, but it is always more or less elliptical in section. Owing to its
small size and soft structure it is easily distorted in the process of
preparing sections.
In the hindermost part of the body its mode of formation differs somewhat
from that above described. In this part the alimentary wall is very thick
and undergoes no special growth prior to the formation of the
subnotochordal rod; on the contrary, a small linear portion of the wall
becomes scooped out along the median dorsal line, and eventually separates
from the remainder as the rod in question. In the trunk the splitting off
of the rod takes place from before backwards, so that the anterior part of
it is formed before the posterior.
The section of the subnotochordal rod in the head would appear from my
observations on Pristiurus to develop in the same way as in the trunk, and
the splitting off from the throat proceeds from before backwards (Pl. 15,
fig. 4_a_, _x_).
In Torpedo, this rod develops very much later in the head than in the
trunk; and indeed my conclusion that it develops in the head at all is only
based on grounds of analogy, since in my oldest Torpedo embryo (just
younger than K) there is no trace of it present. In a Torpedo embryo of
stage I the subnotochordal rod of the trunk terminated anteriorly by
uniting with the wall of the throat. The junction was effected by a narrow
pedicle, so that the rod appeared mushroom-shaped in section, the stalk
representing the pedicle of attachment.
On the formation of the dorsal aorta, the subnotochordal rod becomes
separated from the wall of the gut and the aorta interposed between the
two.
The subnotochordal rod attains its fullest development during stage K.
Anteriorly it terminates at a point well in front of the ear, though a
little behind the end of the notochord; posteriorly it extends very nearly
to the extremity of the tail and is almost co-extensive with the postanal
section of the alimentary tract, though it does not quite reach so far back
as the caudal vesicle (Pl. 18, fig. 6_b_, _x_). In stage L it is still
fairly large in the tail, though it has begun to atrophy anteriorly. We may
therefore conclude that its atrophy, like its development, takes place from
before backwards. In the succeeding stages I have failed to find any trace
of it, and conclude, as does Professor Semper, that it disappears
completely.
Götte[313] is of opinion that the subnotochordal rod is converted into the
dorsal lymphatic trunk, and regards it as the anterior continuation of the
postanal gut, which he believes to be also converted into a lymphatic
trunk. My observations afford no support to these views, and the fact
already mentioned, that the subnotochordal rod is nearly co-extensive with
the postanal section of the gut, renders it improbable that both these
structures are connected with the lymphatic system.
Footnote 313: _Entwicklungsgeschichte d. Unke_, p. 775.
EXPLANATION OF PLATE 18.
COMPLETE LIST OF REFERENCE LETTERS.
_Nervous System._
_ar._ Anterior root of spinal nerve. _nc._ Neural canal. _pr._ Posterior
root of spinal nerve. _spn._ Spinal nerve. _syg._ Sympathetic ganglion.
_Alimentary Canal._
_al._ Alimentary canal. _alv._ Caudal vesicle of the postanal gut. _clal._
Cloacal section of alimentary canal. _du._ Duodenum. _hpd._ Ductus
choledochus. _pan._ pancreas. _soes._ Solid oesophagus. _spv._ Intestine
with rudiment of spiral valve. _umc._ Umbilical canal.
_General._
_ao._ Dorsal aorta. _aur._ Auricle of heart. _cav._ Cardinal vein. _ch._
Notochord. _eppp._ Epithelial lining of the body-cavity. _ir._ Interrenal
body. _me._ Mesentery. _mp._ Muscle-plate. _mpl_. Muscle-plate sending a
prolongation into the limb. _po._ Primitive ovum. _pp._ Body-cavity. _sd._
Segmental duct. _st._ Segmental tube. _ts._ Tail swelling. _vcau._ Caudal
vein. _x._ Subnotochordal rod.
Fig. 1. Transverse section through the anterior abdominal region of an
embryo of a stage between K and L. Zeiss B, ocul. 2. Reduced one-third.
The section illustrates the junction of a sympathetic ganglion with a
spinal nerve and the sprouting of the muscle-plates into the limbs (_mpl_).
Fig. 2. Transverse section through the abdominal region of an embryo
belonging to stage L. Zeiss B, ocul. 2. Reduced one-third.
The section illustrates the junction of a sympathetic ganglion with a
spinal nerve, and also the commencing formation of a branch from the aorta
(still solid) which will pass through the sympathetic ganglion, and forms
the first sign of the conversion of part of a sympathetic ganglion into one
of the suprarenal bodies.
Fig. 3. Longitudinal and vertical section of an embryo of a stage between L
and M, shewing the successive junctions of the spinal nerves and
sympathetic ganglia.
Fig. 4. Section through the solid oesophagus during stage L. Zeiss A, ocul.
1. The section is taken through the region of the heart, so that the cavity
of the auricle (_aur_) lies immediately below the oesophagus.
Fig. 5. Optical section of the tail of an embryo between stages I and K,
shewing the junction between the neural and alimentary canals.
Fig. 6. Four sections through the caudal region of an embryo belonging to
stage K, shewing the condition of the postanal section of the alimentary
tract. Zeiss A, ocul. 2. An explanation of these figures is given on p.
449.
Fig. 7. Section through the interrenal body of a Scyllium embryo belonging
to stage Q. Zeiss C, ocul. 2.
Fig. 8. Portion of a section of the interrenal body of an adult Scyllium.
Zeiss C, ocul. 2.
CHAPTER XI.
THE VASCULAR SYSTEM AND VASCULAR GLANDS.
The present chapter deals with the early development of the heart, the
development of the general circulatory system, especially the venous part
of it, and the circulation of the yolk-sack. It also contains an account of
two bodies which I shall call the suprarenal and interrenal bodies, which
are generally described as vascular glands.
_The heart._
The first trace of the heart becomes apparent during stage G, as a cavity
between the splanchnic mesoblast and the wall of the gut immediately behind
the region of the visceral clefts (Pl. 11, fig. 4, _ht._).
The body-cavity in the region of the heart is at first double, owing to the
two divisions of it not having coalesced; but even in the earliest
condition of the heart the layers of splanchnic mesoblast of the two sides
have united so as to form a complete wall below. The cavity of the heart is
circumscribed by a more or less complete epithelioid (endothelial) layer of
flattened cells, connected with the splanchnic wall of the heart by
protoplasmic processes. The origin of this lining layer I could not
certainly determine, but its connection with the splanchnic mesoblast
suggests that it is probably a derivative of this[314]. In front the cavity
of the heart is bounded by the approximation of the splanchnic mesoblast to
the wall of the throat, and behind by the stalk connecting the alimentary
canal with the yolk-sack.
Footnote 314: From observations on the development of the
heart in the Fowl, I have been able to satisfy myself that the
epithelioid lining of the heart is derived from the splanchnic
mesoblast. When the cavity of the heart is being formed by the
separation of the splanchnic mesoblast from the hypoblast, a
layer of the former remains close to the hypoblast, but
connected with the main mass of the splanchnic mesoblast by
protoplasmic processes. A second layer next becomes split from
the splanchnic mesoblast, connected with the first layer by the
above-mentioned protoplasmic processes. These two layers form
the epithelioid lining of the heart; between them is the cavity
of the heart, which soon loses the protoplasmic trabeculæ which
at first traverse it.
As development proceeds the ventral wall of the heart becomes bent inwards
on each side on a level with the wall of the gut (Plate 11, fig. 4), and
eventually becomes so folded in as to form for the heart a complete
muscular wall of splanchnic mesoblast. The growth inwards of the mesoblast
to form the dorsal wall of the heart does not, as might be expected, begin
in front and proceed backwards, but commences behind and is gradually
carried forwards.
From the above account it is clear that I have failed to find in
Elasmobranchii any traces of two distinct cavities coalescing to form the
heart, such as have been recently described in Mammals and Birds; and this,
as well as the other features of the formation of the heart in
Elasmobranchii, are in very close accordance with the careful description
given by Götte[315] of the formation of the heart in Bombinator. The
divergence which appears to be indicated in the formation of so important
an organ as the heart between Pisces and Amphibians on the one hand, and
Aves and Mammalia on the other, is certainly startling, and demands a
careful scrutiny. The most complete observations on the double formation of
the heart in Mammalia have been made by Hensen, Götte and Kölliker. These
observations lead to the conclusion (1) that the heart arises as two
independent splits between the splanchnic mesoblast and the hypoblast, each
with an epithelioid (endothelial) lining. (2) _That the heart is first
formed at a period when the folding in of the splanchnopleure to form the
throat has not commenced, and when therefore it would be impossible for it
to be formed as a single tube._
Footnote 315: Bischoff has recently stated,
_Historisch-kritische Bemerkungen ii. d. Entwicklung d.
Säugethiereier_, that Götte has found a double formation of the
heart in Bombinator. It may seem bold to question the accuracy
of Bischoff's interpretation of writings in his own language,
but I have certainly failed to gather this either from Dr
Götte's text or figures.
In Birds almost every investigator since von Baer has detected more or less
clearly the coalescence of two halves to form the unpaired heart[316]. Most
investigators have however believed that there was from the first an
unpaired anterior section of the heart, and that only the posterior part
was formed by the coalescence of two lateral halves. Professor Darlste His,
and more recently Kölliker, have stated that there is no such unpaired
anterior section of the heart. My own recent observations confirm their
conclusions as to the double formation of the heart, though I find that the
heart has from the first a Lambda-shaped form. At the apex of the Lambda
the two limbs are only separated by a median partition and are not
continuous with the aortic arches, which do not arise till a later
period[317]. In the Bird the heart arises just _behind_ the completed
throat, and a double formation of the heart appears, in fact, in all
instances to be _most distinctly correlated with the non-closure of the
throat_, a non-closure which it must be noted would render it impossible
for the heart to arise otherwise than as a double cavity.
Footnote 316: Vide _Elements of Embryology_, Foster and
Balfour, pp. 64-66.
Footnote 317: Professor Bischoff (_loc. cit._) throws doubts
upon the double formation of the heart, and supports his views
by Dr Foster's and my failure to find any trace of a double
formation of the heart in the chick. Professor Bischoff must, I
think, have misunderstood our description, which contains a
clear account of the double formation of the heart.
In the instances in which the heart arises as a double cavity _it is formed
before the complete closure of the throat_, and in those in which it arises
as a single cavity _it is formed subsequently to the complete formation of
the throat_. There is thus a double coincidence which renders the
conclusion almost certain, _that the formation of the heart as two cavities
is a secondary change which has been brought about by variations in the
period of the closing in of the wall of the throat_.
If the closing in of the throat were deferred and yet the primitive time of
formation of the heart retained, it is clear that such a condition as may
be observed in Birds and Mammals must occur, and that the two halves of the
heart must be formed widely apart, and only eventually united on the
folding in of the wall of the throat. We may then safely conclude that the
double formation of the heart has no morphological significance, and does
not, as might at first sight be supposed, imply that the ancestral
Vertebrate had two tubes in the place of the present unpaired heart. I have
spoken of this point at considerable length, on account of the
morphological importance which has been attached to the double formation of
the heart. But the views above enunciated are not expressed for the first
time. In the _Elements of Embryology_ we say, p. 64, "The exact mode of
development (of the heart) appears according to our present knowledge to be
very different in different cases; and it seems probable that the
differences are in fact the result of variations in the mode of formation
and time of closure of the alimentary canal." Götte again in his great
work[318] appears to maintain similar views, though I do not perfectly
understand all his statements. In my review of Kölliker's Embryology[319]
this point is still more distinctly enunciated in the following passage:
"The primitive wide separation and complete independence of the two halves
of the heart is certainly surprising; but we are inclined, provisionally at
least, to regard it as a secondary condition due to the late period at
which the closing of the throat takes place in Mammals."
Footnote 318: _Entwicklungsgeschichte d. Unke_, pp. 779, 780,
781.
Footnote 319: _Journal of Anatomy and Physiology_, Vol. X. p.
794.
_The general circulation._
The chief points of interest in connection with the general circulation
centre round the venous system. The arterial arches present no
peculiarities: the dorsal aorta, as in all other Vertebrates, is at first
double (Pl. 11, fig. 6, _ao_), and, generally speaking, the arrangement of
the arteries accords with what is already known in other forms. The
evolution of the venous system deserves more attention.
The cardinal veins are comparatively late developments. There is at first
one single primitive vein continuous in front with the heart and underlying
the alimentary canal through its præanal and postanal sections. This vein
is shewn in section in Pl. 11, fig. 8, _V_. It may be called either the
subintestinal or splanchnic vein. At the cloaca, where the gut enlarges and
comes in contact with the skin, this vein is compelled to bifurcate
(Pl. 18, fig. 6,_d_, _v.cau._), and usually the two branches into which it
divides are unequal in size. The two branches meet again behind the cloaca
and take their course ventral to the postanal section of the gut, and
terminate close to the end of the tail, Pl. 18, fig. 6,_c_, _v.cau._ In the
tail they form what is usually known as the caudal vein. The venous system
of Scyllium or Pristiurus, during the early parts of stage K, presents the
simple constitution just described.
Before proceeding to describe the subsequent changes which take place in
it, it appears to me worth pointing out the remarkable resemblance which
the vascular system of an Elasmobranch presents at this stage to that of an
ordinary Annelid and Amphioxus. It consists, as does the circulatory
system, in Annelids, of a neural vessel (the aorta) and an intestinal
vessel, the blood flowing backwards in the latter and forwards in the
former. The two in Elasmobranchii communicate posteriorly by a capillary
system, and in front by the arterial arches, connected like the similar
vessels in Annelids with the branchiæ. Striking as is this resemblance,
there is a still closer resemblance between the circulation of the Scyllium
embryo at stage K and that of Amphioxus. The two systems are in fact
identical except in very small details. The subintestinal vessel, absent or
only represented by the caudal vein and in part by the ductus venosus in
higher Vertebrates and adult Fish, forms the main and only posterior venous
trunk of Amphioxus and the embryo Scyllium. The only noteworthy point of
difference between Amphioxus and the embryo Scyllium is the presence of a
portal circulation in the former, absent at this stage in the latter; but
even this is acquired in Scyllium before the close of stage K, and does not
therefore represent a real difference between the two types.
The cardinal veins make their appearance before the close of stage K, and
very soon unite behind with the unpaired section of the caudal vein
(Pl. 11, fig. 9_b_, _p.cav._ and _v._). On this junction being effected
retrogressive changes take place in the original subintestinal vessel. It
breaks up in front into a number of smaller vessels; the lesser of the two
branches connecting it round the cloaca with the caudal vein first vanishes
(Pl. 11, fig. 9_a_, _v_), and then the larger; and the two cardinals are
left as the sole forward continuations of the caudal vein. This latter then
becomes prolonged forwards, and the two posterior cardinals open into it
some little distance in front of the hind end of the kidneys. By these
changes and by the disappearance of the postanal section of the gut the
caudal vein is made to appear as a superintestinal and not a subintestinal
vessel, and as the direct posterior continuation of the cardinal veins.
Embryology proves however that the caudal vein is a true subintestinal
vessel[320], and that its connection with the cardinals is entirely
secondary.
Footnote 320: The morphological importance of this point is
considerable. It proves, for instance, that the hæmal arches of
the vertebræ in the tail (vide pp. 373 and 374) potentially, at
any rate, encircle the gut and enclose the body-cavity as
completely as the ribs which meet in the median ventral line
may be said to do anteriorly.
The invariably late appearance of the cardinal veins in the embryo and
their absence in Amphioxus leads me to regard them as additions to the
circulatory system which appeared in the Vertebrata themselves, and were
not inherited from their ancestors. It would no doubt be easy to point to
vessels in existing Annelids which might be regarded as their equivalent,
but to do so would be in my opinion to follow an entirely false
morphological scent.
_The circulation of the yolk-sack._
The observations recorded on this subject are so far as I am acquainted
with them very imperfect, and in most cases the arteries and veins appear
to have been transposed.
Professor Wyman[321], however, gives a short description of the circulation
in Raja Batis, in which he rightly identifies the arteries, though he
regards the arterial ring which surrounds the vascular area as equivalent
to the venous sinus terminalis of the Bird.
Footnote 321: _Memoirs of the American Academy of Arts and
Sciences_, Vol. IX.
The general features of the circulation are clearly portrayed in the
somewhat diagrammatic figures on Pl. 9, in which the arteries are
represented red, and the veins blue[322].
Footnote 322: I may state that my determinations of the
arrangement of the circulation were made by actual observation
of the flow of the blood under the microscope.
I shall follow the figures on this plate in my descriptions.
Fig. 1 represents my earliest stage of the circulation of the yolk-sack. At
this stage there is visible a single aortic trunk passing forwards from the
embryo and dividing into two branches. No venous trunk could be detected
with the simple microscope, but probably venous channels were present in
the thickened edge of the blastoderm.
In fig. 2 the circulation was greatly advanced[323]. The blastoderm has now
nearly completely enveloped the yolk, and there remains only a small
circular space (_yk_) not enclosed by it. The arterial trunk is present as
before, and divides in front of the embryo into two branches which turn
backwards and nearly form a complete ring round the embryo. In general
appearance it resembles the sinus terminalis of the area vasculosa of the
Bird, but in reality bears quite a different relation to the circulation.
It gives off branches only on its inner side.
Footnote 323: My figure may be compared with that of Leydig,
_Rochen und Haie_, Plate III. fig. 6. Leydig calls the arterial
ring the sinus terminalis, and appears to regard it as venous,
but his description is so short that this point is not quite
clear.
A venous system of returning vessels is now fully developed, and its
relations are very remarkable. There is a main venous ring round the
thickened edge of the blastoderm, which is connected with the embryo by a
single stem which runs along the seam where the edges of the blastoderm
have coalesced. Since the venous trunks are only developed behind the
embryo, it is only the posterior part of the arterial ring which gives off
branches.
The succeeding stage, fig. 3, is also one of considerable interest. The
arterial ring has greatly extended, and now embraces nearly half the yolk,
and sends off trunks on its inner side along its whole circumference.
More important changes have taken place in the venous system. The
blastoderm has now completely enveloped the yolk, and as a result of this,
the venous ring no longer exists, but at the point where it vanished there
may be observed a number of smaller veins diverging in a brush-like fashion
from the termination of the unpaired trunk which originally connected the
venous ring with the heart. This point is indicated in the figure by the
letter _y_. The brush-like divergence of the veins is a still more marked
feature in a blastoderm of a succeeding stage (fig. 4).
The circulation in the succeeding stage (fig. 4) (projected in my figure)
only differs in details from that of the previous stage. The arterial ring
has become much larger, and the portion of the yolk not embraced (_x_) by
it is quite small. Instead of all the branches from the ring being of
nearly equal size, two of them are especially developed. The venous system
has undergone no important changes.
In fig. 5 the circulation is represented at a still later stage. The
arterial ring has come to embrace the whole yolk, and as a result of this,
has in its turn vanished as did the venous ring before it. At this stage of
the circulation there is present a single arterial and a single venous
trunk. The arterial trunk is a branch of the dorsal aorta, and the venous
trunk originally falls into the heart together with the subintestinal or
splanchnic vein, but on the formation of the liver enters this and breaks
up into capillaries in it. The venous trunk leaves the body on the right
side, and the arterial on the left.
The most interesting point to be noticed in connection with the yolk-sack
circulation of Scyllium is the fact of its being formed on a completely
different type to that of the Amniotic Vertebrates.
THE VASCULAR GLANDS.
There are in Scyllium two structures which have gone under the name of the
suprarenal body. The one of these is an unpaired rod-like body lying
between the dorsal aorta and the caudal vein in the region of the posterior
end of the kidneys. This body I propose to call _the interrenal body_. The
other is formed by a series of paired bodies situated dorsal to the
cardinal veins on branches of the aorta, and arranged segmentally. These
bodies I shall call _the suprarenal bodies_. I propose treating the
literature of these bodies together, since they have usually been dealt
with in this way, and indeed regarded as parts of the same system. As I
hope to shew in the sequel, the origin of these bodies is very different.
The interrenal body appears to be developed from the mesoblast; while my
researches on the suprarenal bodies confirm the brilliant investigations of
Leydig, shewing that they are formed out of the sympathetic ganglia.
The most important investigations on these bodies have been made by
Leydig[324]. In his first researches, _Rochen u. Haie_, pp. 71, 72, he
gives an account of the position and histology of what is probably my
interrenal body[325].
Footnote 324: _Rochen und Haie and Untersuchung. ü. Fische u.
Reptilien._
Footnote 325: I do not feel sure that Leydig's unpaired
suprarenal body is really my interrenal body, or at any rate it
alone. The point could no doubt easily be settled with fresh
specimens, but these I unfortunately cannot at present obtain.
My doubts rest partly on the fact that, in addition to my
interrenal body, other peculiar masses of tissue (which may be
called lymphoid in lieu of a better name) are certainly present
around some of the larger vessels of the kidneys which are not
identical in structure and development with my interrenal body,
and partly that Stannius' statements (to be alluded to
directly) rather indicate the existence of a second unpaired
body in connection with the kidneys, though I do not fully
understand his descriptions.
The position and relations of the interrenal body vary somewhat according
to Leydig in different cases. He makes the following statement about its
histology. "Fat molecules form the chief mass of the body, which causes its
white, or ochre-yellow colour, and one finds freely embedded in them clear
vesicular nuclei." He then proceeds to state that this structure is totally
dissimilar to that of the Mammalian suprarenal body, and gives it as his
opinion that it is not the same body as this. In his later researches[326]
he abandons this opinion, and adopts the view that the interrenal body is
part of the same system as the suprarenal bodies to be subsequently spoken
of. Leydig describes the suprarenal bodies as paired bodies segmentally
arranged along the ventral side of the spinal column situated on the
successive arteriæ axillares, and in close connection with one or more
sympathetic ganglia. He finds them formed of lobes, consisting of closed
vesicles full of nuclei and cells. Numerous nerve-fibres are also described
as present. With reference to the real meaning of these bodies he expresses
a distinct view. He says[327], "As the pituitary body is an integral part
of the brain, so are the suprarenal bodies part of the sympathetic system."
He re-affirms with still greater emphasis the same view in his _Fische u.
Reptilien_. Though these views have not obtained much acceptance, and the
accuracy of the histological data on which they are grounded has been
questioned, yet I hope to shew in the sequel not only that Leydig's
statements are in the main true, but that development proves his
conclusions to have been well founded.
Footnote 326: _Fische u. Reptilien_, p. 14.
Footnote 327: _Rochen u. Haie_, p. 18.
Stannius alludes[328] to both these bodies, and though he does not
contribute much to Leydig's previous statements, yet he accepts Leydig's
position with reference to the relation of the sympathetic and suprarenal
bodies[329].
Footnote 328: _Vergleichende Anatomie_, II. Auflage.
Footnote 329: Stannius' description is not quite intelligible,
but appears to point to the existence of a third kind of body
connected with the kidney. From my own observations (vide
above), I am inclined to regard it as probable that such a
third body exists.
The general text-books of Histology, Kölliker's work, and Eberth's article
in Stricker's _Histology_, do not give much information on this subject;
but Eberth, without apparently having examined the point, questions the
accuracy of Leydig's statements with reference to the anatomical relations
of the sympathetic ganglia and suprarenal bodies.
The last author who has dealt with this subject is Professor Semper[330].
He records observations both on the anatomy and development of these
organs. His anatomical observations are in the main confirmatory of those
of Leydig, but he shews still more clearly than did Leydig the segmental
arrangement of the suprarenal bodies. He definitely regards the interrenal
and suprarenal bodies as parts of the same system, and states that in many
forms they are continuous (p. 228):
Footnote 330: "Urogenitalsystem d. Plagiostomen." _Arb.
zool.-zoot. Inst. z. Würzburg_, Vol. II.
"Hier freilich gehen sie bei manchen Formen...in einen Körper über,
welcher zwischen den Enden d. beiden Nieren liegend dicht an der
einfachen Caudalvene sitzt."
With reference to their development he says: "They arise then also
completely independently of the kidneys, as isolated segmentally arranged
groups of mesoderm cells between the convolutions of the segmental organs;
only anteriorly do they stretch beyond them, and extend quite up to the
pericardium."
To Semper's statements I shall return, but now pass on to my own
observations. The paired suprarenal bodies are dealt with first.
_The suprarenal bodies._
My observations on these bodies in the adult Scyllium have only been made
with specimens hardened in chromic acid, and there are many points which
deserve a fuller investigation than I have been able to give them.
The general position and relations of the suprarenal bodies have been fully
given by Leydig and Semper, and I have nothing to add to their statements.
They are situated on branches of the aorta, segmentally arranged, and
extend on each side of the vertebral column from close behind the heart to
the posterior part of the body-cavity. The anterior pair are the largest,
and are formed apparently from the fusion of two bodies[331]. When these
bodies are examined microscopically, their connection with the sympathetic
ganglia becomes at once obvious. Bound up in the same sheath as the
anterior one is an especially large ganglion already alluded to by Leydig,
and sympathetic ganglia are more or less distinctly developed in connection
with all the others. There is however considerable irregularity in the
development and general arrangement of the sympathetic ganglia, which are
broken up into a number of small ganglionic swellings, on some of which an
occasional extra suprarenal body is at times developed. As a rule it may be
stated that there is a much smaller ganglionic development in connection
with the posterior suprarenal bodies than with the anterior.
Footnote 331: There is a very good figure of them in Semper's
paper, Pl. XXI. fig. 3.
The different suprarenal bodies exhibit variations in structure mainly
dependent on the ganglion cells and nerves in them, and their typical
structure is best exhibited in a posterior one, in which there is a
comparatively small development of nervous elements.
A portion of a section through one of these is represented on Pl. 19,
fig. 6, and presents the following features. Externally there is present a
fibrous capsule, which sends in the septa, imperfectly dividing up the body
into a series of alveoli or lobes. Penetrating and following the septa
there is a rich capillary network. The parenchyma of the body itself
exhibits a well-marked distinction in the majority of instances into a
cortical and medullary substance. The cortical substance is formed of
rather irregular columnar cells, for the most part one row deep, arranged
round the periphery of the body. Its cells measure on about an average
.03 Mm. in their longest diameter. The medullary substance is more or less
distinctly divided into alveoli, and is formed of irregularly polygonal
cells; and though it is difficult to give an estimate of their size on
account of their irregularity, .021 Mm. may be taken as probably about the
diameter of an average cell. The character of the cortical and medullary
cells is nearly the same, and the cells of the two strata appear rather to
differ in shape than in any other essential point. The protoplasm of both
has a markedly yellow tinge, giving to the suprarenal bodies a yellowish
brown colour. The nuclei are small compared to the size of the cells, being
about .009 Mm. in both cortical and medullary cells. In the anterior
suprarenal body there is a less marked distinction between the cortical and
the medullary layers, and a less pronounced yellow coloration of the whole,
than in the posterior bodies. The suprarenal bodies are often partially or
completely surrounded by a lymphoid tissue, which is alluded to in the
account of their development.
The most interesting features of my sections of the anterior bodies are the
relations they bring to light between the sympathetic ganglia and the
suprarenal bodies. In the case of one of the posterior suprarenal bodies, a
small ganglion is generally found attached to both ends of the body, and
invested in the same sheath; in addition to this a certain number of
ganglion cells (very conspicuous by their size and other characters) are to
be found scattered through the body. In the anterior suprarenal bodies the
development of ganglion cells is very much greater. If a section is taken
through the region where the large sympathetic ganglion (already mentioned)
is attached to the body, one half of the section is composed mainly of
sympathetic ganglion cells and nerve fibres, and the other of suprarenal
tissue, but the former spread in considerable numbers into the latter. A
transverse section through the suprarenal body in front of, or behind this
point, is still more instructive. One of these is represented in Pl. 19,
fig. 7. The suprarenal tissue is not inserted, but fills up the whole space
within the outline of the body. At one point a nerve (_n_) is seen to
enter. In connection with this are a number of ganglion cells, the exact
distribution of which has been reproduced. They are scattered irregularly
throughout the suprarenal body, but are more concentrated at the smaller
than at the large end. It is this small end which, in succeeding sections,
is entirely replaced by a sympathetic ganglion. Wavy fibres (which I take
to be nervous) are distributed through the suprarenal body in a manner
which, roughly speaking, is proportional to the number of ganglion cells.
At the large end of the body, where there are few nerve cells, the typical
suprarenal structure is more or less retained. Where the nerve fibres are
more numerous at the small end of the section, they give to the tissue a
somewhat peculiar appearance, though the individual suprarenal cells retain
their normal structure. In a section of this kind the ganglion and nerves
are clearly so intimately united with the suprarenal body as not to be
separable from it.
The question naturally arises as to whether there are cells of an
intermediate character between the ganglion cells and the cells of the
suprarenal body. I have not clearly detected any such, but my observations
are of too limited a character to settle the point in an adverse sense.
The embryological part of my researches on these bodies is in reality an
investigation of later development of the sympathetic ganglia. The earliest
stages in the development of these have already been given[332], and I take
them up here as they appear during stage L, and shall confine my
description to the changes they undergo in the anterior part of the trunk.
They form during stage L irregular masses of cells with very conspicuous
branches connecting them with the spinal nerves (Pl. 18, fig. 3). There may
be noticed at intervals solid rods of cells passing from the bodies to the
aorta, Pl. 18, fig. 2. These rods are the rudiments of the aortic branches
to which the suprarenal bodies are eventually attached.
Footnote 332: _Antea_, pp. 394-396.
In a stage between M and N the trunks connecting these bodies with the
spinal nerves are much smaller and less easy to see than during stage L. In
some cases moreover the nerves appear to attach themselves more definitely
to a central and inner part of the ganglia than to the whole of them. This
is shewn in Pl. 19, fig. 8, and I regard it as the first trace of a
division of the primitive ganglia into a suprarenal part and a ganglionic
part. The branches from the aorta have now a definite lumen, and take a
course through the centre of these bodies, as do the aortic branches in the
adult.
By stage O these bodies have acquired a distinct mesoblastic investment,
which penetrates into their interior, and divides it, especially in the
case of the anterior bodies, into a number of distinct alveoli. These
alveoli are far more distinct in some parts of the bodies than in others.
The nerve-trunks uniting the bodies with the spinal nerves are (at least in
specimens hardened in picric and chromic acids) very difficult to see, and
I have failed to detect that they are connected with special parts of the
bodies, or that the separate alveoli differ much as to the nature of their
constituent cells. The aortic branches to the bodies are larger than in the
previous stage, and the bodies themselves fairly vascular.
By stage Q (Pl. 19, fig. 9) two distinct varieties of cells are present in
these bodies. One of these is large, angular, and strikingly resembles the
ganglion cells of the spinal nerves at the same period. This variety is
found in separate lobules or alveoli on the inner border of the bodies. I
take them to be true ganglion cells, though I have not seen them in my
sections especially connected with the nerves. The cells of the second
variety are also aggregated in special lobules, and are very markedly
smaller than the ganglionic cells. They form, I imagine, the cells of the
true suprarenal tissue. At this and the earlier stage lymphoid tissue, like
that surrounding the suprarenal bodies in the adult, is found adjacent to
these bodies.
Stage Q forms my last embryonic stage, and it may perhaps be asked on what
grounds I regard these bodies as suprarenal bodies at all and not as simple
sympathetic ganglia.
My determination mainly rests on three grounds: (1) That a branch from the
aorta penetrates these bodies and maintains exactly the same relations to
them that the same branches of the aorta do in the adult to the true
suprarenal bodies. (2) That the bodies are highly vascular. (3) That in my
last stage they become divided into a ganglionic and a non-ganglionic part,
with the same relations as the ganglia and suprarenal tissue in the adult.
These grounds appear to me to afford ample justification for my
determinations, and the evidence adduced above appears to me to render it
almost certain that the suprarenal tissue is a product of the primitive
ganglion and not introduced from the mesoblast without, though it is not to
be denied that a more complete investigation of this point than it has been
possible for me to make would be very desirable.
Professor Semper states that he only made a very slight embryological
investigation of these bodies, and probably has only carefully studied
their later stages. He has accordingly overlooked the branches connecting
them with the spinal nerves, and has not therefore detected the fact that
they develop as parts of the sympathetic nervous system. I feel sure that
if he re-examines his sections of younger embryos he will not fail to
discover the nerve-branches described by me. His descriptions apart from
this point accord fairly well with my own. The credit of the discovery that
these bodies are really derivatives of the sympathetic nervous system is
entirely Leydig's: my observations do no more than confirm his remarkable
observations and well-founded conclusions.
_Interrenal body._
My investigations on the interrenal body in the adult are even less
complete than those on the suprarenal bodies. I find the body forming a
small rod elliptical in section in the posterior region of the kidney
between the dorsal aorta and unpaired caudal vein. Some little distance
behind its front end (and probably not at its thickest point) it measured
in one example, of which I have sections, a little less than a millimetre
in its longest diameter. Anteriorly it overlaps the suprarenal bodies, and
I failed to find any connection between them and it. On this point my
observations do not accord with those of Professor Semper. I have however
only been able to examine hardened specimens.
It is, vide Pl. 18, fig. 8, invested by a fairly thick tunica propria,
which sends in septa, dividing it into rather well-marked lobules or
alveoli. These are filled with polygonal cells, which form the true
parenchyma of the body. These cells are in my hardened specimens not
conspicuous by the number of oil-globules they contain, as might have been
expected from Leydig's description[333]. They are rather granular in
appearance, and are mainly peculiar from the somewhat large size of the
nucleus. The diameter of an average cell is about .015 Mm., and that of the
nucleus about .01 to .012. The nuclei are remarkably granular. The septa of
the body are provided with a fairly rich capillary network.
Footnote 333: Perhaps the body I am describing is not
identical with Leydig's posterior suprarenal body. I do not, as
mentioned above, feel satisfied that it is so from Leydig's
description.
At the first glance there is some resemblance in structure between the
tissues of the suprarenal and interrenal bodies, but on a closer inspection
this resemblance resolves itself into both bodies being divided up into
lobules by connective-tissue septa. There is in the interrenal body no
distinction between cortical and medullary layers as in the suprarenal. The
cells of the two bodies have very different characters, as is demonstrated
by a comparison of the relative diameters of the nuclei and the cells. The
cells of the suprarenal bodies are considerably larger than those of the
interrenal (.021 to .03 as compared to .015), yet the nuclei of the larger
cells of the former body do not equal in size those of the smaller cells of
the latter (.009 as compared to .01).
My observations both on the coarser anatomy and on the histology of the
interrenal body in the adult point to its being in no way connected with
the suprarenal bodies, and are thus in accordance with the earlier and not
the later views of Leydig.
The embryology of this body (under the title of suprarenal body) was first
described in my preliminary account of the development of the Elasmobranch
Fishes[334]. A short account of its embryonic structure was given, and I
stated that although I had not fully proved the point, yet I believed it to
be derived from the wall of the alimentary canal. As will be shewn in the
sequel this belief was ill-founded, and the organ in question is derived
from the mesoblast. Allusion has also been made to it by Professor Semper,
who figures it at an early stage of development, and implies that it arises
in the mesoblast and in connection with the suprarenal body. It appears at
stage K as a rod-like aggregate of mesoblast cells, rather more closely
packed than their neighbours, between the two kidneys near their hinder
ends (Plate 11, fig. 9_a_, _su_). The posterior and best marked part of it
does not extend further forwards than the front end of the large intestine,
and reaches backwards nearly as far as the hinder end of the kidneys. This
part of the body lies between the caudal vein and dorsal aorta.
Footnote 334: _Quarterly Journal of Microscopic Science_,
October, 1874. [This edition No. V.]
At about the point where the unpaired caudal vein divides into the two
cardinals, the interrenal body becomes less well marked off from the
surrounding tissue, though it may be traced forward for a considerable
distance in the region of the small intestine. It retains up to stage Q its
original extension, but the anterior part becomes quite definite though
still of a smaller calibre than the posterior. In one of my examples of
stage O the two divisions were separated by a small interval, and not as in
other cases continuous. I have not determined whether this was an
accidental peculiarity or a general feature. I have never seen any signs of
the interrenal body becoming continuous with the suprarenal bodies, though,
as in the adult, the two bodies overlap for a considerable distance.
The histology of the interrenal body in the embryonic periods is very
simple. At first it is formed of cells differing from those around in being
more circular and more closely packed. By stage L its cells have acquired a
character of their own. They are still spherical or oval, but have more
protoplasm than before, and their nucleus becomes very granular. At the
same time the whole body becomes invested by a tunic of spindle-shaped
mesoblast cells. By stage O it begins to be divided into a number of
separate areas or lobes by septa formed of nucleated fibres. These become
more distinct in the succeeding stages up to Q (Pl. 18, fig. 7), and in
them a fair number of capillaries are formed.
From the above description it is clear that embryology lends no more
countenance than does anatomy to the view that the interrenal bodies belong
to the same system as the suprarenal, and it becomes a question with which
(if of either) of these two bodies the suprarenal bodies of the higher
Vertebrata are homologous. This question I shall not attempt to answer in a
definite way. My own decided belief is that the suprarenal bodies of
Scyllium are homologous with the suprarenal bodies of Mammalia, and a good
many points both in their structure and position might be urged in favour
of this view. In the mean time, however, it appears to me better to wait
before expressing a definite opinion till the embryonic development of the
suprarenal bodies has been worked out in the higher Vertebrata.
EXPLANATION OF PLATE 19.
COMPLETE LIST OF REFERENCE LETTERS.
_Nervous System._
_n._ Nerve. _spn._ Spinal nerve. _syg._ Sympathetic ganglion.
_Alimentary Canal._
_cl._ Cloaca. _incl._ Cloacal involution. _oeep._ OEsophageal epithelium.
_pan._ Pancreas. _th._ Thyroid body.
_General._
_abp._ Abdominal pocket (pore). _aur._ Auricle. _cav._ Cardinal vein.
_cauv._ Caudal vein. _ly._ Lymphoid tissue. _mm._ Muscles. _od._ Oviduct.
_pc._ Pericardium. _pp._ body-cavity. _sr._ Suprarenal body. _u._ Ureter.
_vao._ Ventral aorta (anterior continuation of bulbus arteriosus). _ven._
Ventricle. _wd._ Wolffian duct.
Figs. 1_a_, 1_b_, 1_c_. Three sections through the cloacal region of an
embryo belonging to stage O. 1_a_ is the anterior of the three sections.
Zeiss A, ocul. 2. Reduced one-third.
1_a_ shews the cloacal involution at its deepest part abutting on the
cloacal section of the alimentary tract.
1_b_ is a section through a point somewhat behind this close to the opening
of the Wolffian ducts into the cloaca.
1_c_ shews the opening to the exterior in the posterior part of the cloaca,
and also the rudiments of the two abdominal pockets (_abp_).
Fig. 2. Section through the cloacal region of an embryo belonging to stage
P. Zeiss A, ocul. 2.
The figure shews the solid anterior extremity of the cloacal involution.
Fig. 3. Longitudinal vertical section through the thyroid body in a stage
between O and P. Zeiss a a, ocul. 1.
The figure shews the solid thyroid body (_th_) connected in front with
throat, and terminating below the bulbus arteriosus.
Fig. 4. Pancreas (_pan_) and adjoining part of the alimentary tract in
longitudinal section, from an embryo between stages L and M. Zeiss A, ocul.
2.
Fig. 5. Portion of liver network of stage L. Zeiss C, ocul. 2. The section
is intended to illustrate the fact that the tubules or cylinders of which
the liver is composed are hollow and not solid. Between the liver tubules
are seen blood spaces with distinct walls, and blood corpuscles in their
interior.
Fig. 6. Section through part of one of the suprarenal bodies of an adult
Scyllium hardened in chromic acid. Zeiss C, ocul. 2. The section shews the
columnar cells forming the cortex and the more polygonal cells of the
medulla.
Fig. 7. Transverse section through the anterior suprarenal body of an adult
Scyllium. Zeiss B, ocul. 2. Reduced one-third. The tissue of the suprarenal
body has not been filled in, but only the sympathetic ganglion cells which
are seen to be irregularly scattered through the substance of the body. The
entrance of the nerve (_n_) is shewn, and indications are given of the
distribution of the nerve-fibres.
Fig. 8. Section through the sympathetic ganglion of a Scyllium embryo
between stages M and N, shewing the connecting trunk between the suprarenal
body and the spinal nerve (_spn_), and the appearance of an indication in
the ganglion of a portion more directly connected with the nerve. Zeiss D,
ocul. 2.
Fig. 9. Section through one of the anterior sympathetic ganglia of an
embryo of stage Q, shewing its division into a true ganglionic portion
(_syg_), and a suprarenal body (_sr_). Zeiss C, ocul. 2.
CHAPTER XII.
THE ORGANS OF EXCRETION.
The earliest stages in the development of the excretory system have already
been described in a previous chapter[335] of this memoir, and up to the
present time no investigator, with the exception of Dr Alex. Schultz[336],
has gone over the same ground. Dr Schultz' descriptions are somewhat brief,
but differ from my own mainly in stating that the segmental duct arises
from an involution instead of as a solid knob. This discrepancy is, I
believe, due to Dr Schultz drawing his conclusions as to the development of
the segmental duct from its appearance at a comparatively late stage. He
appears to have been unacquainted with my earlier descriptions.
Footnote 335: Chapter VI. p. 345, _et seq._
Footnote 336: _Archiv f. Micr. Anat_. Bd. XI.
The adult anatomy and later stages in the development of the excretory
organs form the subject of the present chapter, and stand in marked
contrast to the earlier stages in that they have been dealt with in a
magnificent monograph[337] by Professor Semper, whose investigations have
converted this previously almost unknown field of vertebrate embryology
into one of the most fully explored parts of the whole subject. Reference
is frequently made to this monograph in the succeeding pages, but my
references, numerous as they are, give no adequate idea of the completeness
and thoroughness of Professor Semper's investigations. In Professor
Semper's monograph are embodied the results of a considerable number of
preliminary papers published by him in his _Arbeiten_ and in the
_Centralblatt_. The excretory organs of Elasmobranchii have also formed the
subject of some investigations by Dr Meyer[338] and by myself[339]. Their
older literature is fully given by Professor Semper. In addition to the
above-cited works, there is one other paper by Dr Spengel[340] on the
Urinogenital System of Amphibians, to which reference will frequently be
made in the sequel, and which, though only indirectly connected with the
subject of this chapter, deserves special mention both on account of the
accuracy of the investigations of which it forms the record, and of the
novel light which it throws on many of the problems of the constitution of
the urinogenital system of Vertebrates.
Footnote 337: "Urogenital System d. Plagiostomen," Semper,
_Arbeiten_, Vol. II.
Footnote 338: _Sitzungsberichte d. Naturfor. Ges. Leipzig_,
1875. No. 2.
Footnote 339: "Preliminary account of the development of
Elasmobranch Fishes," _Quarterly Journal of Microscopical
Science_, 1874. "Origin and History of the Urinogenital Organs
of Vertebrates," _Journal of Anat. and Physiol._ Vol. X.
Footnote 340: _Arbeiten_, Semper, Vol. III.
_Excretory organs and genital ducts in the adult._
The kidneys of Scyllium canicula are paired bodies in contact along the
median line. They are situated on the dorsal wall of the abdominal cavity,
and extend from close to the diaphragm to a point a short way behind the
anus. Externally, each appears as a single gland, but by the arrangement of
its ducts may be divided into two distinct parts, an anterior and a
posterior. The former will be spoken of as the Wolffian body, and the
latter as the kidney, from their respective homology with the glands so
named in higher Vertebrates. The grounds for these determinations have
already been fully dealt with both by Semper[341] and by myself.
Footnote 341: Though Professor Semper has come to the same
conclusion as myself with respect to these homologies, yet he
calls the Wolffian body Leydig's gland after its distinguished
discoverer, and its duct Leydig's duct.
Externally both the Wolffian body and the kidney are more or less clearly
divided into segments, and though the breadth of both glands as viewed from
the ventral surface is fairly uniform, yet the hinder part of the kidney is
very much thicker and bulkier than the anterior part and than the whole of
the Wolffian body. In both sexes the Wolffian body is rather longer than
the kidney proper. Thus in a male example, 33 centimetres long, the two
glands together measured 8-1/4 centimetres and the kidney proper only
3-1/2. In the male the Wolffian bodies extend somewhat further forwards
than in the female. Leaving the finer details of the glands for subsequent
treatment, I pass at once to their ducts. These differ slightly in the two
sexes, so that it will be more convenient to take the male and female
separately.
A partly diagrammatic representation of the kidney and Wolffian body of the
male is given on Pl. 20, fig. 1. The secretion of the Wolffian body is
carried off by a duct, _the Wolffian duct (w.d.)_, which lies on the
ventral surface of the gland, and receives a separate ductule from each
segment (Pl. 20, fig. 5). The main function of the Wolffian duct in the
male is, however, that of a vas deferens. The testicular products are
brought to it through the coils of the anterior segments of the Wolffian
body by a number of vasa efferentia, the arrangement of which is treated of
on pp. 487, 488. The section of the Wolffian duct which overlies the
Wolffian body is much contorted, and in adult individuals at the generative
period enormously so. The duct often presents one or two contortions beyond
the hind end of the Wolffian body, but in the normal condition takes a
straight course from this point to the unpaired urinogenital cloaca, into
which it falls independently of its fellow of the opposite side. It
receives no feeders from the kidney proper.
The excretion of the kidney proper is carried off not by a single duct, but
by a series of more or less independent ducts, which, in accordance with
Prof. Semper's nomenclature, will be spoken of as _ureters_. These are very
minute, and their investigation requires some care. I have reason, from my
examinations of this and other species of Elasmobranchii, to believe that
they are, moreover, subject to considerable variations, and the following
description applies to a definite individual. Nine or possibly ten distinct
ureters, whose arrangement is diagrammatically represented in fig. 1,
Pl. 20, were present on each side. It will be noticed that, whereas the
five hindermost are distinct till close to their openings into the
urinogenital cloaca, the four anterior ones appear to unite at once into a
single duct, but are probably only bound up in a common sheath. The ureters
fall into the common urinogenital cloaca, immediately behind the opening of
the Wolffian duct (so far as could be determined), by four apertures on
each side. In a section made through the part of the wall of the cloaca
containing the openings of the ureters of both sides, there were present on
the left side (where the section passed nearer to the surface than on the
right) four small openings posteriorly, viz. the openings of the ureters
and one larger one anteriorly, viz. the opening of the Wolffian duct. On
the other side of the section where the level was rather deeper, there were
five distinct ducts cut through, one of which was almost on the point of
dividing into two. This second section proves that, in this instance at
least, the two ureters did not unite till just before opening into the
urinogenital cloaca. The same section also appeared to shew that one of the
ureters fell not into the cloaca but into the Wolffian duct.
As stated above both the Wolffian duct and the ureters fall into an
unpaired urinogenital cloaca. This cloaca communicates at one end with the
general cloaca by a single aperture situated at the point of a somewhat
conspicuous papilla, just behind the anus (Pl. 20, fig. 1, _o_), and on the
other it opens freely into a pair of bladders, situated in close contact
with each other, on the ventral side of the kidney (Pl. 20, fig. 1, _sb_).
To these bladders Professor Semper has given the name _uterus masculinus_,
from having supposed them to correspond with the lower part of the oviducts
of the female. This homology he now admits to be erroneous, and it will
accordingly be better to drop the name uterus masculinus, for which may be
substituted _seminal bladder_--a name which suits their function, since
they are usually filled with semen at the generation season. The seminal
bladders communicate with the urinogenital cloaca by wide openings, and it
is on the borders of these openings that the mouths of the Wolffian duct
and ureters must be looked for. My embryological investigations, though
they have not been specially directed to this point, seem to shew that the
seminal bladders do not arise during embryonic life, and are still absent
in very young individuals. It seems probable that both the bladders and the
urinogenital cloaca are products of the lower extremities of the Wolffian
duct. The only other duct requiring any notice in the male is the
rudimentary oviduct. As was first shewn by Semper, rudiments of the upper
extremities of the oviducts, with their abdominal openings, are to be found
in the male in the same position as in the female, on the front surface of
the liver.
In the female the same ducts are present as in the male, viz. the Wolffian
duct and the ureters. The part of the Wolffian duct which receives the
secretion of the Wolffian body is not contorted, but is otherwise similar
to the homologous part of the Wolffian duct in the male. The Wolffian ducts
of the two sides fall independently into an unpaired urinal cloaca, but
their lower ends, instead of remaining simple as in the male, become
dilated into urinary bladders. Vide Pl. 20, fig. 2. There were nine ureters
in the example dissected, whose arrangement did not differ greatly from
that in the male--the hinder ones remaining distinct from each other, but a
certain amount of fusion, the extent of which could not be quite certainly
ascertained, taking place between the anterior ones. The arrangement of the
openings of these ducts is not quite the same as in the male. A somewhat
magnified representation of it is given in Pl. 20, fig. 3, _o.u._ The two
Wolffian ducts meet at so acute an angle that their hindermost extremities
are only separated by a septum. In the region of this septum on the inner
walls of the two Wolffian ducts were situated the openings of the ureters,
of which there were five on each side arranged linearly. In a second
example, also adult, I found four distinct openings on each side similarly
arranged to those in the specimen described. Professor Semper states that
all the ureters in the female unite into a _single duct_ before opening
into the Wolffian duct. It will certainly surprise me to find such great
variations in different individuals of this species as is implied by the
discrepancy between Professor Semper's description and my own.
The main difference between the ureters in the male and female consists in
their falling into the urinogenital cloaca in the former and into the
Wolffian duct in the latter. Since, however, the urinogenital cloaca is a
derivative of the Wolffian duct, this difference between the two sexes is
not a very important one. The urinary cloaca opens, in the female, into the
general cloaca by a median papilla of somewhat smaller dimensions than the
corresponding papilla in the male. Seminal bladders are absent in the
female, though possibly represented by the bladder-like dilatations of the
Wolffian duct. The oviducts, whose anatomy is too well known to need
description, open independently into the general cloaca.
Since the publication of Professor Semper's researches on the urinogenital
system of Elasmobranch fishes, it has been well known that, in most adult
Elasmobranchii, there are present a series of funnel-shaped openings,
leading from the perivisceral cavity, by the intermediation of a short
canal, into the glandular tubuli of the kidney. These openings are called
by Professor Semper, _Segmentaltrichter_, and by Dr Spengel, in his
valuable work on the urogenital system of Amphibia, _Nephrostomen_. In the
present work the openings will be spoken of as segmental openings, and the
tubes connected with them as segmental tubes. Of these openings there are a
considerable number in the adults of both sexes of Scy. canicula, situated
along the inner border of each kidney. The majority of them belong to the
Wolffian body, though absent in the extreme anterior part of this. In very
young examples a few certainly belong to the region of the kidney proper.
Where present, there is one for each segment[342]. It is not easy to make
certain of their exact number. In one male I counted thirteen. In the
female it is more difficult than in the male to make this out with
certainty, but in one young example, which had left the egg but a short
time, there appeared to be at least fourteen present. According to Semper
there are thirteen funnels in both sexes--a number which fairly well agrees
with my own results. In the male, rudiments of segmental tubes are present
in all the anterior segments of the Wolffian body behind the vasa
efferentia, but it is not till about the tenth segment that the first
complete one is present. In the female a somewhat smaller number of the
anterior segments, six or seven, are without segmental tubes, or only
possess them in a rudimentary condition.
Footnote 342: The term segment will be more accurately defined
below.
A typical segment of the Wolffian body or kidney, in the sense in which
this term has been used above, consists of a number of factors, each of
which will be considered in detail with reference to its variations. On
Pl. 20, fig. 5, is represented a portion of the Wolffian body with three
complete segments and part of a fourth. If one of these be selected, it
will be seen to commence with (1) a segmental opening, somewhat oval in
form (_st.o_) and leading directly into (2) a narrow tube, the segmental
tube, which takes a more or less oblique course backwards, and, passing
superficially to the Wolffian duct (_w.d_), opens into (3) a Malpighian
body (_p.mg_) at the anterior extremity of an isolated coil of glandular
tubuli. This coil forms the fourth section of each segment, and starts from
the Malpighian body. It consists of a considerable number of rather
definite convolutions, and after uniting with tubuli from one or two
(according to size of the segment) accessory Malpighian bodies (_a.mg_),
smaller than the one into which the segmental tube falls, eventually opens
by a (5) narrowish tube into the Wolffian duct at the posterior end of the
segment. Each segment is completely isolated (except for certain
rudimentary structures to be alluded to shortly) from the adjoining ones,
_and never has more than one segmental tube and one communication with the
Wolffian duct_.
The number and general arrangement of the segmental tubes have already been
spoken of. Their openings into the body-cavity are, in Scyllium, very
small, much more so than in the majority of Elasmobranchii. The general
appearance of a segmental tube and its opening is somewhat that of a spoon,
in which the handle represents the segmental tube, and the bowl the
segmental opening. Usually amongst Elasmobranchii the openings and tubes
are ciliated, but I have not determined whether this is the case in Scy.
canicula, and Semper does not speak definitely on this point. From the
segmental openings proceed the segmental tubes, which in the front segments
have nearly a transverse direction, but in the posterior ones are directed
more and more obliquely backwards. This statement applies to both sexes,
but the obliquity is greater in the female than in the male.
As has been said, each segmental tube normally opens into a Malpighian
body, from which again there proceeds the tubulus, the convolutions of
which form the main mass of each segment. This feature can be easily seen
in the case of the Malpighian bodies of the anterior part of the Wolffian
gland in young examples, and sometimes fairly well in old ones, of either
sex[343]. There is generally in each segment a second Malpighian body,
which forms the commencement of a tubulus joining that from the primary
Malpighian body, and, where the segments are larger, there are three, and
possibly in the hinder segments of the Wolffian gland and segments of the
kidney proper, more than three Malpighian bodies.
Footnote 343: My observations on this subject completely
disprove, if it is necessary to do so after Professor Semper's
investigations, the statement of Dr Meyer, that segmental tubes
in Scyllium open into lymph organs.
The accessory Malpighian bodies, or at any rate one of them, appear to have
curious relations to the segmental tubes. The necks of some of the anterior
segmental tubes (Pl. 20, fig. 5) close to their openings into the primary
Malpighian bodies are provided with a small knob of cells which points
towards the preceding segment and is usually connected with it by a fibrous
band. This knob is most conspicuous in the male, and in very young animals
or almost ripe embryos. In several instances in a ripe male embryo it
appeared to me to have a lumen, and to be continued directly forwards into
the accessory Malpighian body of the preceding segment. One such case is
figured in the middle segment on Pl. 20, fig. 5. In this embryo segmental
tubes were present in the segments immediately succeeding those connected
with the vasa efferentia, and at the same time these segments contained
ordinary and accessory Malpighian bodies. The segmental tubes of these
segments were not, however, connected with the Malpighian body of their
proper segment, but instead, turned forwards and entered the segment in
front of that to which they properly belonged. I failed to trace them quite
definitely to the accessory Malpighian body of the preceding segment, but,
in one instance at least, there appeared to me to be present a fibrous
connection, which is shewn in the figure already referred to, Pl. 20,
fig. 5, _r.st_. In any case it can hardly be doubted that this peculiarity
of the foremost segmental tubes is related to what would seem to be the
normal arrangement in the next few succeeding segments, where each
segmental tube is connected with a Malpighian body in its own segment, and
more or less distinctly with an accessory Malpighian body in the preceding
segment.
In the male the anterior segmental tubes, which even in the embryo exhibit
signs of atrophy, become in the adult completely aborted (as has been
already shewn by Semper), and remain as irregular tubes closed at both
ends, which for the most part do not extend beyond the Wolffian duct
(Pl. 20, fig. 4, _r.st_). In the adult, the first two or three segments
with these aborted tubes contain only accessory Malpighian bodies; the
remaining segments, with aborted segmental tubes, both secondary and
primary Malpighian bodies. In neither case are the Malpighian bodies
connected with the aborted tubes.
The Malpighian bodies in Scyllium present no special peculiarities. The
outer layer of their capsule is for the most part formed of flattened
cells; but, between the opening of the segmental tube and the efferent
tubulus of the kidney, their cells become columnar. Vide Pl. 20, fig. 5.
The convoluted tubuli continuous with them are, I believe, ciliated in
their proximal section, but I have not made careful investigations with
reference to their finer structure. Each segment is connected with the
Wolffian duct by a single tube at the hinder end of the segment. In the
kidney proper, these tubes become greatly prolonged, and form the ureters.
It has already been stated that the semen is carried by vasa efferentia
from the testes to the anterior segments of the Wolffian body, and thence
through the coils of the Wolffian body to the Wolffian duct. The nature of
the vasa will be discussed in the embryological section of this chapter: I
shall here confine myself to a simple description of their anatomical
relations. The consideration of their connections naturally falls under
three heads: (1) the vasa efferentia passing from the testes to the
Wolffian body, (2) the mode in which these are connected with the Wolffian
body, and (3) with the testis.
In Pl. 20, fig. 4, drawn for me from nature by my friend Mr Haddon, are
shewn the vasa efferentia and their junctions both with the testes and the
kidney. This figure illustrates better than any description the anatomy of
the various parts. Behind there are two simple vasa efferentia (_v.e._) and
in front a complicated network of vasa, which might be regarded as formed
of either two or four main vessels. It will be shewn in the sequel that it
is really formed of four distinct vessels. Professor Semper states that
there is but a single vas efferens in Scyllium canicula, a statement which
appears to me unquestionably erroneous. All the vasa efferentia fall into a
_longitudinal duct (l.c)_, which is connected in succession with the
several segments of the Wolffian body (one for each vas efferens) which
appertain to the testis. The hind end of the longitudinal duct is simple,
and ends blindly close to its junction with the last vas efferens; but in
front, where the vasa efferentia are complicated, the longitudinal duct
also has a complicated constitution, and forms a network rather than a
simple tube. It typically sends off a duct to join the coils of the
Wolffian body between each pair of vasa efferentia, and is usually swollen
where this duct parts from it. A duct similar to this has been described by
Semper as _Nierenrandcanal_ in several Elasmobranchii, but its existence is
expressly denied in the case of Scyllium! It is usually found in Amphibia,
as we know from Bidder and Spengel's researches. Spengel calls it
_Längscanal des Hoden_; the vessels from it into the kidney he calls _vasa
efferentia_, and the vessels to it, which I speak of as vasa efferentia, he
calls _Quercanale_.
The exact mode of junction of the separate vasa efferentia with the testis
is difficult to make out on account of the opacity of the basal portion of
the testis. My figure shews that there is a network of tubes (formed of
four main tubes connected by transverse branches) which is a continuation
of the anterior vasa efferentia, and joined by the two posterior ones.
These tubes receive the tubuli coming from the testicular ampullæ. The
whole network may be called, with Semper, the _testicular network_. While
its general relations are represented in my figure, the opacity of the
testes was too great to allow of all the details being with certainty
filled in.
The kidneys of Scyllium stellare, as might be expected, closely resemble
those of Scy. canicula. The ducts of the kidney proper, have, in the former
species, a larger number of distinct openings into the urinogenital cloaca.
In two male examples I counted seven distinct ureters, though it is not
impossible that there may have been one or two more present. In one of my
examples the ureters had seven distinct openings into the cloaca, in the
other five openings. In a female I counted eleven ureters opening into the
Wolffian duct by seven distinct openings. In the remaining parts of the
excretory organs the two species of Scyllium resemble each other very
closely.
As may be gathered from Prof. Semper's monograph, the excretory organs of
Scyllium canicula are fairly typical for Elasmobranchii generally. The
division into kidney and Wolffian body is universal. The segmental openings
may be more numerous and larger, _e.g._ Acanthias and Squatina, or absent
in the adult, _e.g._ Mustelus and Raja. Bladder-like swellings of the
Wolffian duct in the female appear to be exceptional, and seminal bladders
are not always present. The variations in the ureters and their openings
are considerable, and in some cases all the ureters are stated to fall into
a single duct, which may be spoken of as the ureter _par excellence_[344],
with the same relations to the kidneys as the Wolffian duct bears to the
Wolffian body. In some cases Malpighian corpuscles are completely absent in
the Wolffian body, _e.g._ Raja.
Footnote 344: I feel considerable hesitation in accepting
Semper's descriptions of the ureters and their openings. It has
been shewn above that for Scyllium his statements are probably
inaccurate, and in other instances, _e.g._ Raja, I cannot bring
my dissections to harmonise with his descriptions.
The vasa efferentia of the testes in Scyllium are very typical, but there
are some forms in which they are more numerous as well as others in which
they are less so. Perhaps the vasa efferentia are seen in their most
typical form in Centrina as described and figured (Pl. XXI) by Professor
Semper, or in Squatina vulgaris, as I find it, and have represented it on
Pl. 20, fig. 8. From my figure, representing the anterior part of the
Wolffian body of a nearly ripe embryo, it will be seen that there are five
vasa efferentia (_v.e_) connected on the one hand with a longitudinal canal
at the base of the testes (_n.t_) and on the other with a longitudinal
canal in the Wolffian body. Connected with the second longitudinal canal
are four Malpighian bodies, three of them stalked and one sessile; from
which again proceed tubes forming the commencements of the coils of the
anterior segments of the Wolffian body. These Malpighian bodies are clearly
my primary Malpighian bodies, but there are in Squatina, even in the
generative segments, secondary Malpighian bodies. What Semper has described
for Centrina and one or two other genera, closely correspond with what is
present in Squatina.
_Development of the Segmental Tubes._
On p. 345, _et seq._ an account was given of the first formation of the
segmental tubes and the segmental duct, and the history of these bodies was
carried on till nearly the period at which it is taken up in the exhaustive
Memoir of Professor Semper. Though the succeeding narration traverses to a
great extent the same ground as Semper's Memoir, yet many points are
treated somewhat differently, and others are dealt with which do not find a
place in the latter. In the majority of instances, attention is called to
points on which my results either agree with, or are opposed to, those of
Professor Semper.
From previous statements it has been rendered clear that _at first_ the
excretory organs of Elasmobranchii exhibit no division into Wolffian body
or kidney proper. Since this distinction is merely a question of the ducts,
and does not concern the glandular tubuli, no allusion is made to its
appearance in the present section, which deals only with the glandular part
of the kidneys and not with their ducts.
Up to the close of stage K the urinogenital organs consist of a segmental
duct opening in front into the body-cavity, and terminating blindly behind
in close contact with the cloaca, and of a series of segmental tubes, each
opening into the body-cavity on the inner side of the segmental duct, but
ending blindly at their opposite extremities. It is with these latter that
we have at present to deal. They are from the first directed obliquely
backwards, and coil close round the inner and dorsal sides of the segmental
duct. Where they are in contact (close to their openings into the
body-cavity) with the segmental duct, the lumen of the latter diminishes
and so comes to exhibit regular alternations of size. This is shewn in
Pl. 12, fig. 18, _s.d_. At the points where the segmental duct has a larger
lumen, it eventually unites with the segmental tubes.
The segmental tubes rapidly undergo a series of changes, the character of
which may be investigated, either by piecing together transverse sections,
or more easily from longitudinal and vertical sections. They acquire a
Lambda-shaped form with an anterior limb opening into the body-cavity and
posterior limb, resting on a dilated portion of the segmental duct. The
next important change which they undergo consists in a junction being
effected between their posterior limbs and the segmental duct. In the
anterior part of the body these junctions appear before the commencement of
stage L. A segmental tube at this stage is shewn in longitudinal section on
Pl. 21, fig. 7_a_, and in transverse section on Pl. 18, fig. 2. In the
former the actual openings into the body-cavity are not visible. In the
transverse section only one limb of the Lambda is met with on either side
of the section; the limb opening into the body-cavity is seen on the left
side, and that opening into the segmental duct on the right side. This
becomes quite intelligible from a comparison with the longitudinal section,
which demonstrates that it is clearly not possible to see more than a
single limb of the Lambda in any transverse section.
After the formation of their junctions with the segmental duct, other
changes soon take place in the segmental tubes. By the close of stage L
four distinct divisions may be noticed in each tube. Firstly, there is the
opening into the body-cavity, with a somewhat narrow stalk, to which the
name segmental tube will be strictly confined in the future, while the
whole products of the original segmental tube will be spoken of as a
segment of the kidney. This narrow stalk opens into a vesicle (Pl. 18,
fig. 2, and 21, fig. 6), which forms the second division. From the vesicle
proceeds a narrower section forming the third division, which during stage
L remains very short, though in later stages it grows with great rapidity.
It leads into the fourth division, which constitutes the posterior limb of
the Lambda, and has the form of a dilated tube with a narrow opening into
the segmental duct.
The subsequent changes of each segment do not for the most part call for
much attention. They consist mainly in the elongation of the third
division, and its conversion into a coiled tubulus, which then constitutes
the main mass of each segment of the kidney. There are, however, two points
of some interest, viz. (1) the formation of the Malpighian bodies, and (2)
the establishment of the connection between each segmental tube and the
tubulus of the preceding segment which was alluded to in the description on
p. 486. The development of the Malpighian body is intimately linked with
that of the secondary connection between two segments. They are both
products of the metamorphosis of the vesicle which forms the termination of
the segmental tube proper.
At about stage O this vesicle grows out in two directions (Pl. 21,
fig. 10), viz. towards the segment in front (_p.x_) and posteriorly into
the segment of which it properly forms a part (_mg_). That portion which
grows backward remains continuous with the third division of its proper
segment, and becomes converted into a Malpighian body. It assumes (Pl. 21,
figs. 6 and 10) a hemispherical form, while near one edge of it is the
opening from a segmental tube, and near the other the opening leading into
a tubulus of the kidney. The two-walled hemisphere soon grows into a nearly
closed sphere, with a central cavity into which projects a vascular tuft.
For this tuft the thickened inner wall of cells forms a lining, and at the
same time the outer wall becomes thinner, and formed of flattened cells,
except in the interval between the openings of the segmental tube and
kidney tubulus, where its cells remain columnar.
The above account of the formation of the Malpighian bodies agrees very
well with the description which Pye[345] has given of the formation of
these bodies in the embryonic Mammalian kidney. My statements also agree
with those of Semper, in attributing the formation of the Malpighian body
to a metamorphosis of part of the vesicle at the end of the segmental tube.
Semper does not however enter into full details on this subject.
Footnote 345: _Journal of Anatomy and Physiology_, Vol. IX.
The elucidation of the history of the second outgrowth from the original
vesicle towards the preceding segment is fraught with considerable
difficulties, which might no doubt be overcome by a patient investigation
of ample material, but which I have not succeeded in fully accomplishing.
The points which I believe myself to have determined are illustrated by
fig. 10, Pl. 21, a longitudinal vertical section through a portion of the
kidney between stages O and P. In this figure parts of three segments of
the kidney are represented. In the hindermost of the three--the one to the
right--there is a complete segmental tube (_s.t_) which opens at its upper
extremity into an irregular vesicle, prolonged _behind_ into a body which
is obviously a developing Malpighian body, _m.g_, and in _front_ into a
wide tube cut obliquely in the section and ending apparently blindly
(_p.x_). In the preceding segment there is also a segmental tube (_s.t_)
whose opening into the body-cavity passes out of the plane of the section,
but which is again connected with a vesicle dilating behind into a
Malpighian body (_m.g_) and in front into the irregular tube (_p.x_), as in
the succeeding segment, _but this tube is now connected_ (and this could be
still more completely seen in the segment in front of this) _with a vesicle
which opens into the thick-walled collecting tube (fourth division) of the
preceding segment_ close to the opening of the latter into the Wolffian
duct. The fact that the anterior prolongation of the vesicle ends blindly
in the hinder-most segment is due of course to its terminal part passing
out of the plane of the section. _Thus we have established between stages O
and P a connection between each segmental tube and the collecting tube of
the segment in front of that to which it properly belongs; and it further
appears that in consequence of this each segment of the kidney contains two
distinct coils of tubuli which only unite close to their common opening
into the Wolffian duct!_
This remarkable connection is not without morphological interest, but I am
unfortunately only able to give in a fragmentary manner its further
history. During the greater part of embryonic life a large amount of
interstitial tissue is present in the embryonic kidneys, and renders them
too opaque to be advantageously studied as a whole; and I have also, so
far, failed to prepare longitudinal sections suitable for the study of this
connection. It thus results that the next stage I have satisfactorily
investigated is that of a nearly ripe embryo already spoken of in
connection with the adult, and represented on Pl. 20, fig. 5. This figure
shews that each segmental tube, while distinctly connected with the
Malpighian body of its own segment, also sends out a branch towards the
secondary Malpighian body of the preceding segment. This branch in most
cases appeared to be rudimentary, and in the adult is certainly not
represented by more than a fibrous band, but I fancy that I have been able
to trace it (though not with the distinctness I could desire) in surface
views of the embryonic kidney of stage Q. _The condition of the Wolffian
body represented on Pl. 20, fig. 5 renders it probable that the accessory
Malpighian body in each segment is developed in connection with the
anterior growth from the original vesicle at the end of the segmental tube
of the succeeding segment._ How the third or fourth accessory Malpighian
bodies, when present, take their origin I have not made out. It is,
however, fairly certain that they form the commencement of two additional
coils which unite, like the coil connected with the first accessory
Malpighian body, with the collecting tube of the primitive coil close to
its opening into the Wolffian duct or ureter.
The connection above described between two successive kidney segments
appears to have escaped Professor Semper's notice, though I fancy that the
peculiar vesicle he describes, _loc. cit._ p. 303, as connected with the
end of each segmental tube, is in some way related to it. It seems possible
that the secondary connection between the segmental tube and the preceding
segment may explain a peculiar observation of Dr Spengel[346] on the kidney
of the tailless Amphibians. He finds that, in this group, the segmental
tubes do not open into Malpighian bodies, but into the fourth division of
the kidney tube. Is it not just possible that in this case the primitive
attachment of the segmental tubes may have become lost, and a secondary
attachment, equivalent to that above described, though without the
development of a secondary Malpighian body, have been developed? In my
embryos the secondary coil of the segmental tubes opens, as in the Anura,
into the fourth section of a kidney tubulus.
Footnote 346: _Loc. cit._ pp. 85-89.
_Development of the Müllerian and Wolffian ducts._
The formation of the Müllerian and Wolffian ducts out of the original
segmental duct has been dealt with in a masterly manner by Professor
Semper, but though I give my entire assent to his general conclusions, yet
there are a few points on which I differ from him. These are for the most
part of a secondary importance; but they have a certain bearing on the
homology between the Müllerian duct of higher Vertebrates and that of
Elasmobranchii. The following account refers to Scy. canicula, but so far
as my observations go, the changes in Scy. stellare are nearly identical in
character.
I propose treating the development of these ducts in the two sexes
separately, and begin with the female.
Shortly before stage N a horizontal split arises in the segmental
duct[347], commencing some little distance from its anterior extremity, and
extending backwards. This split divides the duct into a dorsal section and
a ventral one. The dorsal section forms the Wolffian duct, and receives the
openings of the segmental tubes, and the ventral one forms the Müllerian
duct or oviduct, and is continuous with the unsplit anterior part of the
primitive segmental duct, which opens into the body-cavity. The nature of
the splitting may be gathered from the woodcut, fig. 6, p. 511, where _x_
represents the line along which the segmental duct is divided. The
splitting of the primitive duct extends slowly backwards, and thus there is
for a considerable period a single duct behind, which bifurcates in front.
A series of transverse sections through the point of bifurcation always
exhibits the following features. Anteriorly two separate ducts are present,
next two ducts in close juxtaposition, and immediately behind this a single
duct. A series of sections through the junction of two ducts is represented
on Plate 21, figs. 1A, 1B, 1C, 1D.
Footnote 347: For the development of the segmental duct, vide
p. 345, _et seq._
In my youngest example, in which the splitting had commenced, there were
two separate ducts for only 14 sections, and in a slightly older one for
about 18. In the second of these embryos the part of the segmental duct
anterior to the front end of the Wolffian duct, which is converted directly
into the oviduct, extended through 48 sections. In the space included in
these 48 sections at least five, and I believe six, segmental tubes with
openings into the body-cavity were present. These segmental tubes did not
however unite with the oviduct, or at best, but one or two rudimentary
junctions were visible, and the evidence of my earlier embryos appears to
shew that the segmental tubes in front of the Wolffian duct never become in
the female united with the segmental duct. The anterior end of the Wolffian
duct is very much smaller than the oviduct adjoining it, and as the reverse
holds good in the male, an easy method is afforded of distinguishing the
two sexes even at the earliest period of the formation of the Wolffian
duct.
Hitherto merely the general features of the development of the oviduct and
Wolffian duct have been alluded to, but a careful inspection of any good
series of sections, shewing the junction of these two ducts, brings to
light some features worth noticing in the formation of the oviduct. It
might have been anticipated that, where the two ducts unite behind as the
segmental duct, their lumens would have nearly the same diameter, but
normally this appears to be far from the case.
To illustrate the formation of the oviduct I have represented a series of
sections through a junction in an embryo in which the splitting into two
ducts had only just commenced (Pl. 21, fig. 1), but I have found that the
features of this series of sections are exactly reproduced in other series
in which the splitting has extended as far back as the end of the small
intestine. In the series represented (Pl. 21) 1A is the foremost section,
and 1D the hindermost. In 1A the oviduct (_od_) is as large or slightly
larger than the Wolffian duct (_w.d_), and in the section in front of this
(which I have not represented) was considerably the larger of the two
ducts. In 1B the oviduct has become markedly smaller, but there is no
indication of its lumen becoming united with that of the Wolffian duct--the
two ducts, though in contact, are distinctly separate. In 1C the walls of
the two ducts have fused, and the oviduct appears merely as a ridge on the
under surface of the Wolffian duct, and its lumen, though extremely minute,
_shews no sign of becoming one with that of the Wolffian duct_. Finally, in
1D the oviduct can merely be recognised as a thickening on the under side
of the segmental duct, as we must now call the single duct, but a slight
bulging downwards of the lumen of the segmental duct appears to indicate
that the lumens of the two ducts may perhaps have actually united. But of
this I could not be by any means certain, and it seems quite possible that
the lumen of the oviduct never does open into that of the segmental duct.
The above series of sections goes far to prove that the posterior part of
the oviduct is developed as a nearly solid ridge split off from the under
side of the segmental duct, into which at the utmost a very small portion
of the lumen of the latter is continued. One instance has however occurred
amongst my sections which probably indicates that the lumen of the
segmental duct may sometimes, in the course of the formation of the oviduct
and Wolffian duct, become divided into two parts, of which that for the
oviduct, though considerably smaller than that for the Wolffian duct, is
not so markedly so as in normal cases (Pl. 21, fig. 2).
Professor Semper states that the lumen of the part of the oviduct split off
from the hindermost end of the segmental duct becomes continuously smaller,
till at last close to the cloaca it is split off as a solid rod of cells
without a lumen, and thus it comes about that the oviduct, when formed,
ends blindly, and does not open into the cloaca till the period of sexual
maturity. My own sections do not include a series shewing the formation of
a terminal part of the oviduct, but Semper's statements accord precisely
with what might probably take place if my account of the earlier stages in
the development of the oviduct is correct. The presence of a hymen in young
female Elasmobranchii was first made known by Putmann and Garman[348], and
subsequently discovered independently by Semper[349].
Footnote 348: "On the Male and Female Organs of Sharks and
Skates, with special reference to the use of the claspers,"
_Proceed. American Association for Advancement of Science_,
1874.
Footnote 349: _Loc. cit._
The Wolffian duct appears to receive its first segmental tube at its
anterior extremity.
In the male the changes of the original segmental duct have a somewhat
different character to those in the female, although there is a fundamental
agreement between the two sexes. As in the female, a horizontal split makes
its appearance a short way behind the front end of the segmental duct, and
divides this into a dorsal Wolffian duct and a ventral Müllerian duct, the
latter continuous with the anterior section of the segmental duct, which
carries the abdominal opening. The differences in development between the
two sexes are, in spite of a general similarity, very obvious. In the first
place, the ventral portion split off from the segmental duct, instead of
being as in the female larger in front than the Wolffian duct, is very much
smaller; while behind it does not form a continuous duct, but in some parts
a lumen is present, and in others again absent (Pl. 21, fig. 6). It does
not even form an unbroken cord, but is divided in disconnected portions.
Those parts with a lumen do not appear to open into the Wolffian duct.
The process of splitting extends gradually backwards, so that there is a
much longer rudimentary Müllerian duct by stage O than by stage N. By stage
P the posterior portions of the Müllerian ducts have vanished. The anterior
parts remain, as has been already stated, till adult life. A second
difference between the male and female depends on the fact that, in the
male, the splitting of the segmental duct into Müllerian duct and Wolffian
duct never extends beyond the hinder extremity of the small intestine. A
third and rather important point of difference consists in the splitting
commencing far nearer the front end of the segmental duct in the male than
in the female. In the female it was shewn that about 48 sections intervened
between the front end of the segmental duct and the point where this became
split, and that this region included five or six segmental tubes. In the
male the homologous space only occupies _about 7 to 12 sections, and does
not contain the rudiment of more than a single segmental tube_. Although my
sections have not an absolutely uniform thickness, yet the above figures
suffice to shew in a conclusive manner that the splitting of the segmental
duct commences far further forwards in the male than in the female. This
difference accounts for two facts which were mentioned in connection with
the excretory organs of the adult, viz. (1) the greater length of the
Wolffian body in the male than in the female, and (2) the fact that
although a nearly similar number of segmental tubes persist in the adults
of both sexes, yet that in the male there are five or six more segments in
front of the first fully developed segmental opening than in the female.
The above description of the formation of the Müllerian duct in the male
agrees very closely with that of Professor Semper for Acanthias. For
Scyllium however he denies, as it appears to me erroneously, the existence
of the posterior rudimentary parts of the Müllerian duct. He further
asserts that the portions of the Müllerian duct with a lumen open into the
Wolffian duct. The most important difference, however, between Professor
Semper's and my own description consists in his having failed to note that
the splitting of the segmental duct commences much further forwards in the
male than in the female.
I have attempted to shew that the oviduct in the female, with the exception
of the front extremity, is formed as a nearly solid cord split off from the
ventral surface of the segmental duct, and not by a simple splitting of the
segmental duct into two equal parts. If I am right on this point, it
appears to me far easier to understand the relationship between the oviduct
or Müllerian duct of Elasmobranchii and the Müllerian duct of Birds, than
if Professor Semper's account of the development of the oviduct is the
correct one. Both Professor Semper and myself have stated our belief in the
homology of the ducts in the two cases, but we have treated their
relationship in a very different way. Professor Semper[350] finds himself
compelled to reject, on theoretical grounds, the testimony of recent
observers on the development of the Müllerian duct in Birds, and to assert
that it is formed out of the Wolffian duct, or, according to my
nomenclature, 'the segmental duct.' In my account[351], the ordinary
statements with reference to the development of the Müllerian duct in Birds
are accepted; but it is suggested that the independent development of the
Müllerian duct may be explained by the function of this duct in the adult
having, as it were, more and more impressed itself upon the embryonic
development, till finally all connection, even during embryonic life,
between the oviduct and the segmental duct (Wolffian duct) became lost.
Footnote 350: _Loc. cit._ pp. 412, 413.
Footnote 351: "The Urinogenital Organs of Vertebrates,"
_Journal of Anatomy and Physiology_, Vol. X. p. 47. [This
edition, p. 164.]
Since finding what a small portion of the segmental duct became converted
into the Müllerian duct in Elasmobranchii, I have reexamined the
development of the Müllerian duct in the Fowl, in the hope of finding that
its posterior part might develop nearly in the same manner as in
Elasmobranchii, at the expense of a thickening of cells on the outer
surface of the Wolffian duct. I have satisfied myself, in conjunction with
Mr Sedgwick, that this is not the case, and that the general account is in
the main true; but at the same time we have obtained evidence which tends
to shew that the cells which form the Müllerian duct are in part derived
from the walls of the Wolffian duct. We propose giving a full account of
our observations on this point, so that I refrain from mentioning further
details here. It may however be well to point out that, apart from
observations on the actual development of the Müllerian duct in the Bird,
the fact of its abdominal opening being situated some way behind the front
end of the Wolffian duct, is of itself a sufficient proof that it cannot be
the metamorphosed front extremity of the Wolffian (= segmental) duct, in
the same way that the abdominal opening of the Müllerian duct is the front
extremity of the segmental duct in Elasmobranchii.
Although the evidence I can produce in the case of the Fowl of a direct
participation of the Wolffian duct in the formation of the Müllerian is not
of an absolutely conclusive kind, yet I am inclined to think that the
complete independence of the two ducts, if eventually established as a
fact, would not of itself be sufficient (as Semper is inclined to think) to
disprove the identity of the Müllerian duct in Birds and Elasmobranchii.
We have, no doubt, almost no knowledge of the magnitude of the changes
which can take place in the mode of development of the same organ in
different types, yet this would have to be placed at a very low figure
indeed in order to exclude the possibility of a change from the mode of
development of the Müllerian duct in Elasmobranchii to that in Birds. We
have, it appears to me, in the smallness of the portion of the segmental
duct which goes to form the Müllerian duct in Elasmobranchii, evidence that
a change has already appeared in this group in the direction of a
development of the Müllerian duct independent of the segmental duct, and
therefore of the Wolffian duct; and it has been in view of this
consideration, that I have devoted so much attention to the apparently
unimportant point of how much of the segmental duct was concerned in the
formation of the Müllerian duct. An analogous change, in a somewhat
different direction, would seem to be taking place in the development of
the rudimentary Müllerian duct in the male Elasmobranchii.
It is, perhaps, just worth pointing out, that the blindness of the oviduct
of female Elasmobranchii, and its mode of development from an imperfect
splitting of the segmental duct, may probably be brought into connection
with the blindness of the extremity of the Müllerian duct or oviduct which
so often occurs in both sexes of Sturgeons (Accipenser).
I may, perhaps, at this point, be permitted to say a few words about my
original account of the development of the Wolffian duct This account was
incorrect, and based upon a false interpretation of an imperfect series of
sections, and I took the opportunity, in a general account of the
urinogenital system of Vertebrates, to point out my mistake[352]. Professor
Semper has, however, subsequently done me the honour to discuss, at
considerable length, my original errors, and to attempt to explain them.
Since it appears to me improbable that the continuation of such a
discussion can be of much general interest, it will suffice to say now,
that both Professor Semper's and my own original statements on the
development of the Wolffian duct were erroneous; but that both of us have
now recognised our mistakes; and that the first morphologically correct
account of the development was given by him.
Footnote 352: _Journal of Anatomy and Physiology_, Vol X.
1875. [This edition, No. VII.]
* * * * *
With reference to the formation of the urinal cloaca there is not much to
say. The originally widely separated openings of the two Wolffian ducts
gradually approximate in both sexes. By stage O (Pl. 19, fig. 1_b_) they
are in close contact, and the lower ends of the two ducts actually coalesce
at a somewhat later period, and open by a single aperture into the common
cloaca. The papilla on which this is situated begins to make its appearance
considerably before the actual fusion of the lower extremities of the two
ducts.
_Formation of Wolffian Body and Kidney proper._
Between stages L and M the hindermost ten or eleven segments of the
primitive undivided excretory organ commence to undergo changes which
result in their separation from the anterior segments as a distinct gland,
which was spoken of in the description of the adult as the kidney proper,
while the unaltered preceding segments of the kidney were spoken of as the
Wolffian body.
It will be remembered that each segment of the embryonic kidney consists of
four divisions, the last or fourth of which opens into the Wolffian duct.
The changes which take place in the hindermost ten or eleven segments, and
cause them to become distinguished as the kidney proper, concern alone the
fourth division of each segment, which becomes prolonged backwards, and its
opening into the Wolffian duct proportionately shifted. These changes
affect the foremost segments of the kidney much more than the hindermost,
so that the fourth division in the foremost segments becomes very much
longer than in the hindermost, and at last all the prolongations of the
kidney segments come to open nearly on the same level, close to the cloacal
termination of the Wolffian duct (Pl. 21, fig. 8). The prolongations of the
fourth division of the kidney-segments have already (p. 481) been spoken of
in the description of the adult as ureters, and this name will be employed
for them in the present section.
The exact manner in which the changes, that have been briefly related, take
place is rather curious, and very difficult to unravel without the aid of
longitudinal sections. First of all, the junction between each segment of
the kidney and the Wolffian duct becomes so elongated as to occupy the
whole interval between the junctions of the two neighbouring segments. The
original opening of each tube into the Wolffian duct is situated at the
anterior end of this elongated attachment, the remaining part of the
attachment being formed solely of a ridge of cells on the dorsal side of
the Wolffian duct. The general character of this growth will be understood
by comparing figs. 7_a_ and 7_b_, Pl. 21--two longitudinal vertical
sections through part of the kidneys. Fig. 7 _a_ shews the normal junction
of a segmental tube with the Wolffian duct in the Wolffian body, while in
figure 7_b_ (_r.u_) is shewn the modified junction in the region of the
kidney proper in the same embryo. The latter of these figures (fig. 7_b_)
appears to me to prove that the elongation of the attachments between the
segmental tubes and Wolffian duct takes place _entirely at the expense of
the former_. Owing to the length of this attachment, every transverse
section through the kidney proper at this stage either presents a solid
ridge of cells closely adhering to the dorsal side of the Wolffian duct, or
else passes through one of the openings into the Wolffian duct.
During stage M the original openings of the segmental tubes into the
Wolffian duct appear to me to become obliterated, and at the same time the
lumen of each ureter is prolonged into the ridge of cells on the dorsal
wall of the duct.
Both of these changes are illustrated in my figures. The fact of the
obliteration of the original opening into the Wolffian duct is shewn in
longitudinal section in Pl. 21, fig. 9, _u_, but more conclusively in the
series of transverse sections represented on Pl. 21, figs. 3A, 3B, 3C. In
the hindermost of these (3C) is seen the solid terminal point of a ureter,
while the same ureter possesses a lumen in the two previous sections, but
exhibits no signs of opening into the Wolffian duct. Sections may however
be met with which appear to shew that in some instances the ureters still
continue to open into the Wolffian duct, but these I find to be rare and
inconclusive, and am inclined to regard them as abnormalities. The
prolongation of the lumen of the ureters takes place in a somewhat peculiar
fashion. The lumen is not, as might be expected, _completely_ circumscribed
by the wall of the ureter, but only _dorsally and to the sides_. Ventrally
it is closed in by the dorsal wall of the Wolffian duct. In other words,
each ureter is at first an incomplete tube. This peculiarity is clearly
shewn in the middle figure of the series on Pl. 21, fig. 3B.
During stages M and N the ureters elongate considerably, and, since the
foremost ones grow the most rapidly, they soon come to overlap those
behind. As each ureter grows in length it remains an incomplete tube, and
its lumen, though proportionately prolonged, continues to present the same
general relations as at first. It is circumscribed by its proper walls only
dorsally and laterally; its floor being formed in the case of the front
ureter by the Wolffian duct, and in the case of each succeeding ureter by
the dorsal wall of the ureter in front. This is most easily seen in
longitudinal sections, and is represented on Pl. 21, fig. 9, or on a larger
scale in fig. 9A. In the latter figure it is especially clear that while
the wall on the dorsal side of the lumen of each ureter is continuous with
the dorsal wall of the tubulus of its own segment, the wall on the ventral
side is continuous with the dorsal wall of the ureter of the preceding
segment. This feature in the ureters explains the appearance of transverse
sections in which the ureters are not separate from each other, but form
together a kind of ridge on the dorsal side of the Wolffian duct, in which
there are a series of perforations representing the separate lumens of the
ureters (Pl. 21, fig. 4). The peculiarities in the appearance of the dorsal
wall of the Wolffian duct in fig. 9A, and the difference between the cells
composing it and those of the ventral wall, become intelligible on
comparing this figure with the representation of transverse section in
figs. 3B and 3C, and especially in fig. 4. Most of the ureters continue to
end blindly at the close of stage N, and appear to have solid posterior
terminations like that of the Müllerian duct in Birds.
By stage O all the ureters have become prolonged up to the cloacal end of
the Wolffian duct, so that the anterior one has a length equal to that of
the whole kidney proper. For the most part they acquire independent
openings into the end section of the Wolffian duct, though some of them
unite together before reaching this. The general appearance of the
hindermost of them between stages N and O is shewn in longitudinal and
vertical section in Pl. 21, fig. 8, _u_.
They next commence to develop into complete and independent tubes by their
side walls growing inwards and meeting below so as to completely enclose
their lumen. This is seen already to have occurred in most of the posterior
ureters in Pl. 21, fig. 8.
Before stage P the ureters cease to be united into a continuous ridge, and
each becomes separated from its neighbours by a layer of indifferent
tissue: by this stage, in fact, the ureters have practically attained very
nearly their adult condition. The general features of a typical section
through them are shewn on Pl. 21, fig. 5. The figure represents the section
of a female embryo, not far from the cloaca. Below is the oviduct (_od_).
Above this again is the Wolffian duct (_w.d_), and still dorsal to this are
four ureters (_u_). In female embryos more than four ureters are not
usually to be seen in a single section. This is probably owing to the
persistence, in some instances, of the intimate connection between the
ureters found at an earlier stage of development, and results in a single
ureter coming to serve as the collecting duct for several segments. A
section through a male embryo of stage P would mainly differ from that
through a female in the absence of the oviduct, and in the presence of
probably six[353], instead of four, ureters.
Footnote 353: This at least holds good for one of my embryos
at this stage, which is labelled Scy. canicula, but which may
possibly be Scy. stellare.
The exact amount of fusion which takes place between the ureters, and the
exact number of the ureters, cannot easily be determined from sections, but
the study of sections is chiefly of value in shewing the general nature of
the changes which take place in the process of attaining the adult
condition.
It may be noticed, as a consequence of the above account, that the
formation of the ureters takes place by a growth of the original segmental
tubes, and not by a splitting off of parts of the wall of the Wolffian
duct.
The formation of ureters in Scyllium, which has been only very cursorily
alluded to by Professor Semper, appears to differ very considerably from
that in Acanthias as narrated by him.
_The Vasa Efferentia._
A comparison of the results of Professor Semper on Elasmobranchii, and Dr
Spengel on Amphibians, suggests several interesting questions with
reference to the development of the vasa efferentia, and the longitudinal
canal of the Wolffian body.
Professor Semper was the first to describe the adult anatomy and
development of vasa efferentia in Elasmobranchii, and the following
extracts will fully illustrate his views with reference to them.
"In[354] dem frühesten Stadium finden sich wie früher angegeben ungefahr 34
Trichter in der Leibeshöhle, von diesen gehen die 27 hintersten in die
persistirenden Segmentaltrichter über, von denen 4 beim erwachsenen Thiere
auf dem Mesorchium stehen. Die übrigen 7 schliessen sich vollständig ab zu
den erwähnten länglichen und später mannigfach auswachsenden varicösen
Trichterblasen; von diesen sind es wiederum 3-4 welche untereinander in der
Längsrichtung verwachsen und dadurch den in der Basis der Hodenfalte
verlaufenden Centralcanal des Hodens bilden. Ehe aber diese Verwachsung zu
einem mehr oder minder geschlängelten Centralcanal vollständig wird, hat
sich einmal das Lumen der Trichterblasen fast vollständig geschlossen und
ausserdem von ihnen aus durch Verwachsung und Knospung die erste Anlage des
rete vasculosum Halleri gebildet (Taf. XX. Figs. 1, 2_c_). Es erstreckt
sich nämlich mehr oder minder weit in die Genitalfalte hinein ein
unregelmässiges von kleinen Zellen begränztes Canalnetz welches zweifellos
mit dem noch nicht ganz vollständigen Centralcanale des Hodens (Taf. XX.
Fig. 2_c_) in Verbindung steht. Von diesem letzteren aus gehen in
regelmässigen Abständen die Segmentalgänge (Taf. XX. Fig. 2 _sg._) gegen
die Niere hin; da sie meist stark geneigt oder selbst geschlängelt (bei
6{ctm} langen Embryonen) gegen die Niere zu verlaufen, wo sie sich an die
primären _Malpighi_'schen Körperchen und deren Bildungsblasen ansetzen, so
kann ein verticaler Querschnitt auch nie einen solchen nun zum vas efferens
gewordenen Segmentalgang seiner ganzen Länge nach treffen. Gegen die
Trichterfurche zu aber steht namentlich am hinteren Theile der Genitalfalte
der Centralcanal häufig noch durch einen kurzen Zellstrang mit dem
Keimepithel der Trichterfurche in Verbindung; mitunter findet sich hier
sogar noch eine kleine Höhlung, Rest des ursprünglich hier vorhandenen
weiten Trichters" (Taf. XX. Fig. 3_c_).
Footnote 354: _Loc. cit._ p. 364.
And again: "Dieser[355] Gegensatz in der Umbildung der Segmentalgänge an
der Hodenbasis scheint nun mit einem anderen Hand in Hand zu gehen. Es
bildet sich nämlich am Innenrande der Niere durch Sprossung und Verwachsung
der Segmentalgänge vor ihrer Insertion an das primäre _Malpighi_'sche
Körperchen ein Canal beim Männchen aus, den ich als _Nierenrandcanal_ oben
bezeichnet habe. Ich habe denselben bei Acanthias Centrina (Taf. XXI.
Fig. 13) und Mustelus (Taf. XV. Fig. 8) gefunden. Bei Centrina ist er
ziemlich lang und vereinigt mindestens 7 Segmentalgänge, aber von diesen
letzteren stehen nur 5 mit dem Hodennetz in Verbindung. Dort nun wo diese
letzteren sich an den Nierenrandcanal ansetzen (Taf. XXI. Fig. 13
sg.1-sg.5) findet sich jedesmal ein typisch ausgebildetes _Malpighi_'sches
Körperchen, mit dem aber nun nicht mehr wie ursprünglich nur 2 Canäle
verbunden sind (Taf. XXI. Fig. 14) sondern 3. Einer dieser letzteren ist
derjenige Ast des Nierenrandcanals welcher die Verbindung mit dem nächst
folgenden Segmentalgang zu besorgen hat. An den Stellen aber wo sich an den
Nierenrandcanal die hinteren blind gegen den Hoden hin endenden
Segmentalgänge ansetzen fehlen diese _Malpighi_'schen Körperchen (Taf. XXI.
Fig. 13 _sg_7) vollständig. Auch bei Mustelus (Taf. XV. Figs. 8, 10) findet
genau dasselbe Verhältniss statt; da aber hier nur 2 (oder 3)
Segmentalgänge zu vasa efferentia umgewandelt werden, so stehen hier am
kurzen Randcanal der Niere auch nur 2 oder 3 _Malpighi_'sche Körperchen.
Diese aber sind typisch ausgebildet" (Taf. XV. Fig. 10).
Footnote 355: _Loc. cit._ p. 395.
From these two extracts it is clear that Semper regards both the vasa
efferentia, and central canal of the testis network, as well as the
longitudinal canal of the Wolffian body, as products of the anterior
segmental tubes.
The appearance of these various parts in the fully grown embryos or adults
of such genera as Acanthias and Squatina strongly favours this view, but
Semper appears to have worked out the development of these structures
somewhat partially and by means of sections, a method not, in Scyllium at
least, very suitable for this particular investigation. I myself at first
unhesitatingly accepted Semper's views, and it was not till after the study
of the paper of Dr Spengel on the Amphibian kidney that I came to have my
doubts as to their accuracy. The arrangement of the parts in most
Amphibians is strikingly similar to that in Elasmobranchii. From the testis
come transverse canals corresponding with my vasa efferentia; these fall
into a longitudinal canal of the kidneys, from which again, as in Squatina
(Pl. 20, fig. 8), Mustelus and Centrina, canals (the vasa efferentia of
Spengel) pass off to Malpighian bodies. So far there is no difficulty, but
Dr Spengel has made the extremely important discovery, that in young
Amphibians each Malpighian body in the region of the generative ducts, in
addition to receiving the vasa efferentia, is connected with a fully
developed segmental tube opening into the body-cavity. In Amphibians,
therefore, it is improbable that the vasa efferentia are products of the
open extremities of the segmental tubes, considering that these latter are
found in their unaltered condition at the same time as the vasa efferentia.
When it is borne in mind how strikingly similar in most respects is the
arrangement of the testicular ducts in Amphibia and Elasmobranchii, it will
not easily be credited that they develop in entirely different methods.
Since then we find in Amphibians fully developed segmental tubes in the
same segments as the vasa efferentia, it is difficult to believe that in
Elasmobranchii the same vasa efferentia have been developed out of the
segmental tubes by the obliteration of their openings.
I set myself to the solution of the origin of the vasa efferentia by means
of surface views, after the parts had been made transparent in creosote,
but I have met with great difficulties, and so far my researches have only
been partially successful. From what I have been able to see of Squatina
and Acanthias, I am inclined to think that the embryos of either of these
genera would form far more suitable objects for this research than
Scyllium. I have had a few embryos of Squatina which were unfortunately too
old for my purpose.
Very early the vasa efferentia are fully formed, and their arrangement in
an embryo eight centimetres long is shewn in Pl. 20, fig. 6, _v.e_. It is
there seen that there are six if not seven vasa efferentia connected with a
longitudinal canal along the base of the testes (Semper's central canal of
the testis), and passing down like the segmental tubes to spaces between
the successive segments of the Wolffian body. They were probably connected
by a longitudinal canal in the Wolffian body, but this could not be clearly
seen. In the segment immediately behind the last vas efferens was a fully
developed segmental tube. This embryo clearly throws no light on the
question at issue except that on the whole it supports Semper's views. I
further failed to make out anything from an examination of still younger
embryos.
In a somewhat older embryo there was connected with the anterior vas
efferens a peculiar structure represented on Pl. 20, fig. 7, _r.st_? which
strangely resembled the opening of an ordinary segmental tube, but as I
could not find it in the younger embryo, this suggestion as to its nature,
is, at the best, extremely hazardous. If, however, this body really is the
remnant of a segmental opening, it would be reasonable to conclude that the
vasa efferentia are buds from the segmental tubes as opposed to their
openings; a mode of origin which is not incompatible with the discoveries
of Dr Spengel. I have noticed a remnant, somewhat similar to that in the
Scyllium embryo, close to the hindermost vas efferens in an embryo Squatina
(Pl. 20, fig. 8, _r.st_?).
With reference to the development of the longitudinal canal of the Wolffian
body, I am without observations, but it appears to me to be probably a
further development of the outgrowths of the vesicles of each segmental
tube, which were described in connection with the development of the
segmental tubes, p. 492. Were an anterior outgrowth of one vesicle to meet
and coalesce with the posterior outgrowth of the preceding vesicle, a
longitudinal canal such as actually exists would be the result. The central
canal of the base of the testes and the network connected with it in the
adult (Pl. 20, fig. 4), appear to be derivatives of the vasa efferentia.
I am thus compelled to leave open the question of the real nature of the
vasa efferentia, but am inclined to regard them as outgrowths from the
anterior segmental tubes, though not from their open terminations.
* * * * *
My views upon the homologies of the various parts of the urinogenital
system, the development of which has been described in the present chapter,
have already been expressed in a paper on Urinogenital organs of
Vertebrates[356]. Although Kölliker's[357] discovery of the segmental tubes
in Aves, and the researches of Spengel[358], Gasser[359], Ewart[360] and
others, have rendered necessary a few corrections in my facts, I still
adhere in their entirety to the views expressed in that paper, and feel it
unnecessary to repeat them in this place. I conclude the chapter with a
résumé of the development of the urinogenital organs in Elasmobranchii from
their first appearance to their permanent condition.
Footnote 356: _Journal of Anatomy and Physiology_, Vol. X.
[This edition, No. VII.]
Footnote 357: _Entwicklungsgeschichte des Menschen u. der
höheren Thiere._
Footnote 358: _Loc. cit._
Footnote 359: _Beiträge zur Entwicklungsg. d. Allantois d.
Müller'schen Gänge u. d. Afters._
Footnote 360: "Abdominal Pores and Urogenital Sinus of
Lamprey," _Journal of Anatomy and Physiology_, Vol. X. p. 488.
* * * * *
_Résumé._--The first trace of the urinary system makes its appearance as a
knob springing from the intermediate cell-mass opposite the fifth
protovertebra (woodcut, fig. 5A, _p.d_). This knob is the rudiment of the
abdominal opening of the segmental duct, and from it there grows backwards
to the level of the anus a solid column of cells, which constitutes the
rudiment of the segmental duct itself (woodcut, fig. 5B, _p.d_). The knob
projects towards the epiblast, and the column connected with it lies
between the mesoblast and epiblast. The knob and column do not long remain
solid, but the former acquires an opening into the body-cavity continuous
with a lumen, which makes its appearance in the latter.
[Illustration: FIG. 5.
TWO SECTIONS OF A PRISTIURUS EMBRYO WITH THREE VISCERAL CLEFTS.
The sections illustrate the development of the segmental duct (_pd_) or
primitive duct of the kidneys. In _A_ (the anterior of the two sections)
this appears as a solid knob (_pd_) projecting towards the epiblast. In _B_
is seen a section of the column which has grown backwards from the knob in
_A_.
_spn._ rudiment of a spinal nerve; _mc._ medullary canal; _ch._ notochord;
_X._ string of cells below the notochord; _mp._ muscle-plate; _mp´._
specially developed portion of muscle-plate; _ao._ dorsal aorta; _pd._
segmental duct; _so._ somatopleure; _sp._ splanchnopleure; _pp._
pleuro-peritoneal or body-cavity; _ep._ epiblast; _al._ alimentary canal.]
While the lumen is gradually pushing its way backwards along the solid
rudiment of the segmental duct, the first traces of the segmental tubes, or
proper excretory organs, make their appearance in the form of solid
outgrowths of the intermediate cell-mass, which soon become hollow and open
into the body-cavity. Their blind ends curl obliquely backwards round the
inner and dorsal side of the segmental duct. One segmental tube makes its
appearance for each protovertebra, commencing with that immediately behind
the abdominal opening of the segmental duct, the last tube being situated a
short way behind the anus. Soon after their formation the blind ends of the
segmental tubes open into the segmental duct, and each of them becomes
divided into four parts. These are (woodcut 7) (1) a section carrying the
abdominal opening or segmental tube proper, (2) a dilated vesicle into
which this opens, (3) a coiled tubulus proceeding from (2) and terminating
in (4), a wider portion opening into the segmental duct. At the same time,
or shortly before this, each segmental duct unites with and opens into one
of the horns of the cloaca, and also retires from its primitive position
between the epiblast and mesoblast, and assumes a position close to the
epithelium lining the body-cavity. The general features of the excretory
organs at this period are diagrammatically represented on the woodcut,
fig. 6. In this fig. _p.d_ is the segmental duct and _o_ its abdominal
opening. _s.t_ points to the segmental tubes, the finer details of whose
structure are not represented in the diagram. The kidneys thus form at this
period an unbroken gland composed of a series of isolated coiled tubes, one
extremity of each of which opens into the body-cavity, and the other into
the segmental duct, which forms the only duct of the kidney, and
communicates at one end with the body-cavity, and at the other with the
cloaca.
[Illustration: FIG. 6.
DIAGRAM OF THE PRIMITIVE CONDITION OF THE KIDNEY IN AN ELASMOBRANCH EMBRYO.
_pd._ segmental duct. It opens at _o_ into the body-cavity and at its other
extremity into the cloaca; _x._ line along which the division appears which
separates the segmental duct into the Wolffian duct above and the Müllerian
duct below; _st._ segmental tubes. They open at one end into the
body-cavity, and at the other into the segmental duct.]
The next important change concerns the segmental duct, which becomes
longitudinally split into two complete ducts in the female, and one
complete duct and parts of a second in the male. The manner in which this
takes place is diagrammatically represented in woodcut 6 by the clear line
_x_, and in transverse section in woodcut 7. The resulting ducts are the
(1) Wolffian duct dorsally, which remains continuous with the excretory
tubules of the kidney, and ventrally (2) the oviduct or Müllerian duct in
the female, and the rudiments of this duct in the male. In the female the
formation of these ducts takes place by a nearly solid rod of cells, being
gradually split off from the ventral side of all but the foremost part of
the original segmental duct, with the short undivided anterior part of
which duct it is continuous in front. Into it a very small portion of the
lumen of the original segmental duct is perhaps continued (Pl. 21, fig. 1A,
etc.). The remainder of the segmental duct (after the loss of its anterior
section and the part split off from its ventral side) forms the Wolffian
duct. The process of formation of the ducts in the male chiefly differs
from that in the female in the fact of the anterior undivided part of the
segmental duct, which forms the front end of the Müllerian duct, being
shorter, and in the column of cells with which it is continuous being from
the first incomplete.
[Illustration: FIG. 7.
DIAGRAMMATIC REPRESENTATION OF A TRANSVERSE SECTION OF A SCYLLIUM EMBRYO
ILLUSTRATING THE FORMATION OF THE WOLFFIAN AND MÜLLERIAN DUCTS BY THE
LONGITUDINAL SPLITTING OF THE SEGMENTAL DUCT.
_mc._ medullary canal; _mp._ muscle-plate; _ch._ notochord; _ao._ aorta;
_cav._ cardinal vein; _st._ segmental tube. On the one side the section
passes through the opening of a segmental tube into the body-cavity. On the
other this opening is represented by dotted lines, and the opening of the
segmental tube into the Wolffian duct has been cut through; _w.d._ Wolffian
duct; _m.d._ Müllerian duct. The section is taken through the point where
the segmental duct and Wolffian duct have just become separate; _gr._ The
germinal ridge with the thickened germinal epithelium; _l._ liver; _i._
intestine with spiral valve.]
The tubuli of the primitive excretory organ undergo further important
changes. The vesicle at the termination of each segmental tube grows
forwards towards the preceding tubulus, and joins the fourth section of it
close to the opening into the Wolffian duct (Pl. 21, fig. 10). The
remainder of the vesicle becomes converted into a Malpighian body. By the
first of these changes a connection is established between the successive
segments of the kidney, and though this connection is certainly lost (or
only represented by fibrous bands) in the anterior part of the excretory
organs in the adult, and very probably in the hinder part, yet it seems
most probable that traces of it are to be found in the presence of the
secondary Malpighian bodies of the majority of segments, which are most
likely developed from it.
Up to this time there has been no distinction between the anterior and
posterior tubuli of the primitive excretory organ which alike open into the
Wolffian duct. The terminal division of the tubuli of a considerable number
of the hindermost of these (ten or eleven in Scyllium canicula), either in
some species elongate, overlap, and eventually open by apertures (not
usually so numerous as the separate tubes), on nearly the same level, into
the hindermost section of the Wolffian duct in the female, or into the
urinogenital cloaca, formed by the coalesced terminal parts of the Wolffian
ducts, in the male; or in other species become modified in such a manner as
to pour their secretion into a single duct on each side, which opens in a
position corresponding with the numerous ducts of the other type (woodcut,
fig. 8). It seems that both in Amphibians and Elasmobranchii the type with
a single duct, or approximations to it, are more often found in the females
than in the males. The subject requires however to be more worked out in
Elasmobranchii[361]. In both groups the modified posterior kidney-segments
are probably equivalent to the permanent kidney of the amniotic
Vertebrates, and for this reason the numerous ducts of the first group or
single duct of the second were spoken of as ureters. The anterior tubuli of
the primitive excretory organ retain their early relation to the Wolffian
duct, and form the Wolffian body.
Footnote 361: The reverse of the above rule is the case with
Raja, in the male of which a closer approximation to the
single-duct type is found than in the female.
The originally separate terminal extremities of the Wolffian ducts always
coalesce, and form a urinal cloaca, opening by a single aperture situated
at the extremity of a median papilla behind the anus. Some of the abdominal
openings of the segmental tubes in Scyllium, or in other cases all the
openings, become obliterated.
In the male the anterior segmental tubes undergo remarkable modifications.
There appear to grow from the first three or four or more of them (though
the point is still somewhat obscure) branches, which pass to the base of
the testis and there unite into a longitudinal canal, form a network, and
receive the secretion of the testicular ampullæ (woodcut 9, _nt_). These
ducts, the vasa efferentia, carry the semen to the Wolffian body, but
before opening into the tubuli of this they unite into the _longitudinal
canal of the Wolffian body (l.c)_, from which pass off ducts equal in
number to the vasa efferentia, each of which normally ends in a Malpighian
body. From the Malpighian body so connected start the convoluted tubuli of
what may be called the generative segments of the Wolffian body along which
the semen is conveyed to the Wolffian duct (_v.d_). The Wolffian duct
itself becomes much contorted and acts as vas deferens.
[Illustration: FIG. 8.
DIAGRAM OF THE ARRANGEMENT OF THE URINOGENITAL ORGANS IN AN ADULT FEMALE
ELASMOBRANCH.
_m.d._ Müllerian duct; _w.d._ Wolffian duct; _s.t._ glandular tubuli; five
of them are represented with openings into the body-cavity; _d._ duct of
the posterior segmental tubes; _ov._ ovary.]
In the woodcuts, figs. 8 and 9, are diagrammatically represented the chief
constituents of the adult urinogenital organs in the two sexes. In the
adult female, fig. 8, there are present the following parts:
(1) The oviduct or Müllerian duct (_m.d_) split off from the segmental duct
of the kidneys. Each oviduct opens at its anterior extremity into the
body-cavity, and behind the two oviducts have independent communications
with the general cloaca.
(2) The Wolffian ducts (_w.d_), the other product of the segmental ducts of
the kidneys. They end in front by becoming continuous with the tubulus of
the anterior segment of the Wolffian body on each side, and unite behind to
open by a common papilla into the cloaca. The Wolffian duct receives the
secretion of the anterior part of the primitive kidney which forms the
Wolffian body.
(3) The ureter (_d_) which carries off the secretion of the kidney proper.
It is represented in my diagram in its most rare and differentiated
condition as a single duct.
(4) The glandular tubuli (_s.t_), some of which retain their original
openings into the body-cavity, and others are without them. They are
divided into two groups, an anterior forming the Wolffian body, which pour
their secretion into the Wolffian duct, and a posterior group forming the
kidney proper, which are connected with the ureter.
[Illustration: FIG. 9.
DIAGRAM OF THE ARRANGEMENT OF THE URINOGENITAL ORGANS IN AN ADULT MALE
ELASMOBRANCH.
_m.d._ rudiment of Müllerian duct; _w.d._ Wolffian duct, marked _vd_ in
front and serving as vas deferens; _st._ glandular tubuli; two of them are
represented with openings into the body-cavity; _d._ ureter; _t._ testis;
_nt._ central canal at the base of the testis; _VE._ vasa efferentia; _lc._
longitudinal canal of the Wolffian body.]
In the male the following parts are present (woodcut 9):
(1) The Müllerian duct (_md_), consisting of a small rudiment attached to
the liver representing the foremost end of the oviduct of the female.
(2) The Wolffian duct (_w.d_) which precisely corresponds to the Wolffian
duct of the female, but, in addition to functioning as the duct of the
Wolffian body, also acts as a vas deferens (_vd_). In the adult male its
foremost part has a very tortuous course.
(3) The ureter (_d_), which has the same fundamental constitution as in the
female.
(4) The segmental tubes (_st_). The posterior of these have the same
arrangement in both sexes, but in the male modifications take place in
connection with the anterior ones to fit them to act as transporters of the
testicular products.
Connected with the anterior ones there are present (1) the vasa efferentia
(VE), united on the one hand with (2) the central canal in the base of the
testis (_nt_), and on the other with the longitudinal canal of the Wolffian
body (_l.c_). From the latter are seen passing off the successive tubuli of
the anterior segments of the Wolffian body in connection with which
Malpighian bodies are typically present, though not represented in my
diagram.
_Postscript._
It was my original intention to have given an account of the development of
the generative organs. In the course, however, of my work a number of novel
and unexpected points turned up, which have considerably protracted my
investigations, and it has appeared to me better no longer to delay the
appearance of this monograph, but to publish elsewhere my results on the
generative organs. In chapter VI. p. 349 _et seq._ the early stages of the
generative organs are described, but in contemplation of the completion of
the account no allusion was made to their literature, and more especially
to Professor Semper's important contributions. I may perhaps say that I
have been able to confirm the most important result to which he and other
anatomists have nearly simultaneously arrived with respect to Vertebrates,
viz. _that the primitive ova give rise to both the male and female
generative products_.
EXPLANATION OF PLATES 20 AND 21.
COMPLETE LIST OF REFERENCE LETTERS.
_amg._ Accessory Malpighian body. _cav._ Cardinal vein. _ge._ Germinal
epithelium. _k._ True kidney. _l.c._ Longitudinal canal of the Wolffian
body connected with vasa efferentia. _mg._ Malpighian body. _nt._ Network
and central canal at the base of the testis. _o._ External aperture of
urinal cloaca. _od._ Oviduct or Müllerian duct of the female. _od´._
Müllerian duct of the male. _ou._ Openings of ureters in Wolffian duct in
the female (fig. 3). _pmg._ Primary Malpighian body. _px._ Growth from
vesicle at the end of a segmental tube to join the collecting tube of the
preceding segment. _rst._ Rudimentary segmental tube. _ru._ Ureter
commencing to be formed. _sb._ Seminal bladder. _sd._ Segmental duct. _st._
Segmental tube. _sto._ Opening of segmental tube into body-cavity. _sur._
Suprarenal body. _t._ Testis. _u._ Ureters. _ve._ Vas efferens. _wb._
Wolffian body. _wd._ Wolffian duct.
PLATE 20.
Fig. 1. Diagrammatic representation of excretory organs on one side of a
male Scyllium canicula, natural size.
Fig. 2. Diagrammatic representation of the kidney proper on one side of a
female Scyllium canicula, natural size, shewing the ducts of the kidney and
the dilated portion of the Wolffian duct.
Fig. 3. Opening of the ureters into the Wolffian duct of a female Scyllium
canicula. The figure represents the Wolffian ducts (_wd_) with ventral
portion removed so as to expose their inner surface, and shews the junction
of the two W. ducts to form the common urinal cloaca, the single external
opening of this (_o_), and openings of ureters into one Wolffian duct
(_ou_).
Fig. 4. Anterior extremity of Wolffian body of a young male Scyllium
canicula shewing the vasa efferentia and their connection with the kidneys
and the testis. The vasa efferentia and longitudinal canal are coloured to
render them distinct. They are intended to be continuous with the
uncoloured coils of the Wolffian body, though this connection has not been
very successfully rendered by the artist.
Fig. 5. Part of the Wolffian body of a nearly ripe male embryo of Scyllium
canicula as a transparent object. Zeiss a a, ocul. 3. The figure shews two
segmental tubes opening into the body-cavity and connected with a primary
Malpighian body, and also, by a fibrous connection, with a secondary
Malpighian body of the preceding segment. It also shews one segmental tube
(_rst_) imperfectly connected with the accessory Malpighian body of the
preceding segment of the kidney. The coils of the kidney are represented
somewhat diagrammatically.
Fig. 6. Vasa efferentia of a male embryo of Scyllium canicula eight
centimetres in length. Zeiss a a, ocul. 2.
There are seen to be at the least six and possibly seven distinct vasa
going to as many segments of the Wolffian body and connected with a
longitudinal canal in the base of the testis. They were probably also
connected with a longitudinal canal in the Wolffian body, but this could
not be clearly made out.
Fig. 7. The anterior four vasa efferentia of a nearly ripe embryo.
Connected with the foremost one is seen a body which looks like the remnant
of a segmental tube and its opening (_rst?_).
Fig. 8. Testis and anterior part of Wolffian body of an embryo of Squatina
vulgaris.
The figure is intended to illustrate the arrangement of the vasa
efferentia. There are five of these connected with a longitudinal canal in
the base of the testis, and with another longitudinal canal in the Wolffian
body. From the second longitudinal canal there pass off four ducts to as
many Malpighian bodies. Through the Malpighian bodies these ducts are
continuous with the several coils of the Wolffian body, and so eventually
with the Wolffian duct. Close to the hindermost vas efferens is seen a body
which resembles a rudimentary segmental tube (_rst?_).
PLATE 21.
Figs. 1A, 1B, 1C, 1D. Four sections from a female Scyllium canicula of a
stage between M and N through the part where the segmental duct becomes
split into Wolffian duct and oviduct. Zeiss B, ocul. 2. 1A is the foremost
section.
The sections shew that the oviduct arises as a thickening on the under
surface of the segmental duct into which at the utmost a very narrow
prolongation of the lumen of the segmental duct is carried. The small size
of the lumen of the Wolffian duct in the foremost section is due to the
section passing through nearly its anterior blind extremity.
Fig. 2. Section close to the junction of the Wolffian duct and oviduct in a
female embryo of Scyllium canicula belonging to stage N. Zeiss B, ocul. 2.
The section represented shews that in some instances the formation of the
oviduct and Wolffian duct is accompanied by a division of the lumen of the
segmental duct into two not very unequal parts.
Figs. 3A, 3B, 3C. Three sections illustrating the formation of a ureter in
a female embryo belonging to stage N. Zeiss B, ocul. 2.
3A is the foremost section.
The figures shew that the lumen of the developing ureter is enclosed in
front by an independent wall (fig. 3A), but that further back the lumen is
partly shut in by the subjacent Wolffian duct, while behind no lumen is
present, but the ureter ends as a solid knob of cells without an opening
into the Wolffian duct.
Fig. 4. Section through the ureters of the same embryo as fig. 3, but
nearer the cloaca. Zeiss B, ocul. 2.
The figure shews the appearance of a transverse section through the wall of
cells above the Wolffian duct formed by the overlapping ureters, the lumens
of which appear as perforations in it. It should be compared with fig. 9A,
which represents a longitudinal section through a similar wall of cells.
Fig. 5. Section through the ureters, the Wolffian duct and the oviduct of a
female embryo of Scy. canicula belonging to stage P. Zeiss B, ocul. 2.
Fig. 6. Section of part of the Wolffian body of a male embryo of Scyllium
canicula belonging to stage O. Zeiss B, ocul. 2.
The section illustrates (1) the formation of a Malpighian body (_mg_) from
the dilatation at the end of a segmental tube, (2) the appearance of the
rudiment of the Müllerian duct in the male (_od´_).
Figs. 7_a_, 7_b_. Two longitudinal and vertical sections through part of
the kidney of an embryo between stages L and M. Zeiss B, ocul. 2.
7_a_ illustrates the parts of a single segment of the Wolffian body at this
stage, vide p. 491. The segmental tube and opening are not in the plane of
the section, but the dilated vesicle is shewn into which the segmental tube
opens.
7_b_ is taken from the region of the kidney proper. To the right is seen
the opening of a segmental tube into the body-cavity, and in the segment to
the left the commencing formation of a ureter, vide p. 502.
Fig. 8. Longitudinal and vertical section through the posterior part of the
kidney proper of an embryo of Scyllium canicula at a stage between N and O.
Zeiss A, ocul. 2.
The section shews the nearly completed ureters, developing Malpighian
bodies, &c.
Fig. 9. Longitudinal and vertical section through the anterior part of the
kidney proper of the same embryo as fig. 8. Zeiss A, ocul. 2.
The figure illustrates the mode of growth of the developing ureters.
9A. More highly magnified portion of the same section as fig. 9.
Compare with transverse section fig. 4.
Fig. 10. Longitudinal and vertical section through part of the Wolffian
body of an embryo of Scyllium canicula at a stage between O and P.
The section contains two examples of the budding out of the vesicle of a
segmental tube to form a Malpighian body in its own segment and to unite
with the tubulus of the preceding segment close to its opening into the
Wolffian duct.
XI. ON THE PHENOMENA ACCOMPANYING THE MATURATION
AND IMPREGNATION OF THE OVUM[362].
Footnote 362: From the _Quarterly Journal of Microscopical
Science_, April, 1878.
The brilliant discoveries of Strasburger and Auerbach have caused the
attention of a large number of biologists to be turned to the phenomena
accompanying the division of nuclei and the maturation and impregnation of
the ovum. The results of the recent investigations on the first of these
points formed the subject of an article by Mr Priestley in the sixteenth
volume of this Journal, and the object of the present article is to give
some account of what has so far been made out with reference to the second
of them. The matters to be treated of naturally fall under two heads: (1)
the changes attending the ripening of the ovum, _which are independent of
impregnation_; (2) the changes which are directly due to impregnation.
[Illustration: FIG. 1.--Unripe ovum of Toxopneustes lividus (copied from
Hertwig).]
Every ovum as it approaches maturity is found to be composed (Fig. 1) of
(1) a protoplasmic body or vitellus usually containing yolk-spherules in
suspension; (2) of a germinal vesicle or nucleus, containing (3) one or
more germinal spots or nucleoli. It is with the germinal vesicle and its
contents that we are especially concerned. This body at its full
development has a more or less spherical shape, and is enveloped by a
distinct membrane. Its contents are for the most part fluid, but may be
more or less granular. Their most characteristic component is, however, a
protoplasmic network which stretches from the germinal spot to the
investing membrane, but is especially concentrated round the former
(Fig. 1). The germinal spot forms a nearly homogeneous body, with
frequently one or more vacuoles. It occupies an often excentric position
within the germinal vesicle, and is usually rendered very conspicuous by
its high refrangibility. In many instances it has been shewn to be capable
of amoeboid movements (Auerbach, and Os. Hertwig), and is moreover more
solid and more strongly tinged by colouring reagents than the remaining
constituents of the germinal vesicle. These peculiarities have caused the
matter of which it is composed to be distinguished by Auerbach and Hertwig
as nuclear substance.
In many instances there is only one germinal spot, or one main spot, and
two or three accessory smaller spots. In other cases, _e.g._ Osseous Fish,
there are a large number of nearly equal germinal spots. The eggs which
have been most investigated with reference to the changes of germinal
vesicle are those with a single germinal spot, and it is with these that I
shall have more especially to deal in the sequel.
The germinal vesicle occupies in the first instance a central position in
the ovum, but at maturity is almost always found in close proximity to the
surface. Its change of position in a large number of instances is
accomplished during the growth of the ovum in the ovary, but in other cases
does not take place till the ovum has been laid.
The questions which many investigators have recently set themselves to
answer are the two following:--(1) What becomes of the germinal vesicle
when the ovum is ready to be impregnated? (2) Is any part of it present in
the ovum at the commencement of segmentation? According to their answers to
these questions the older embryologists roughly fall into two groups: (1)
By one set the germinal vesicle is stated to completely disappear and not
to be genetically connected with the subsequent nuclei of the embryo. (2)
According to the other set it remains in the ovum and by successive
divisions forms the parent nucleus of all the nuclei in the body of the
embryo. Though the second of these views has been supported by several very
distinguished names the first view was without doubt the one most generally
entertained, and Haeckel (though from his own observations he was
originally a supporter of the second view) has even enunciated the theory
that there exists an anuclear stage, after the disappearance of the
germinal vesicle, which he regards as an embryonic repetition of the monad
condition of the Protozoa.
While the supporters of the first view agree as to the disappearance of the
germinal vesicle they differ considerably as to the manner of this
occurrence. Some are of opinion that the vesicle simply vanishes, its
contents being absorbed in the ovum; others that it is ejected from the
ovum and appears as the _polar cell_ or _body_, or _Richtungskörper_ of the
Germans--a small body which is often found situated in the space between
the ovum and its membrane, and derives its name from retaining a constant
position in relation to the ovum, and thus serving as a guide in
determining the similar parts of the embryo through the different stages.
The researches of Oellacher (15)[363] in this direction deserve special
mention, as having in a sense formed the foundation of the modern views
upon this subject. By a series of careful observations upon the egg of the
trout and subsequently of the bird, he demonstrated that the germinal
vesicle of the ovum, while still in the ovary, underwent partial
degeneration and eventually became ejected. His observations were made to a
great extent by means of sections, and the general accuracy of his results
is fairly certain, but the nature of the eggs he worked on, as well as
other causes, prevented his obtaining so deep an insight into the phenomena
accompanying the ejection of the germinal vesicle as has since been
possible. Lovén, Flemming (6), and others have been led by their
investigations to adopt views similar in the main to Oellacher's. As a
rule, however, it is held by believers in the disappearance of the germinal
vesicle that it becomes simply absorbed, and many very accurate accounts,
so far as they go, have been given of the gradual atrophy of the germinal
vesicle. The description of Kleinenberg (14) for Hydra, and Götte for
Bombinator, may perhaps be selected as especially complete in this respect;
in both instances the germinal vesicle commences to atrophy at a relatively
early period.
Footnote 363: The numbers appended to authors' names refer to
the list of publications at the end of the paper.
Coming to the more modern period the researches of five workers, viz.
Bütschli, E. van Beneden, Fol, Hertwig, and Strasburger have especially
thrown light upon this difficult subject. It is now hardly open to doubt
that while part of the germinal vesicle is concerned in the formation of
the polar cell or cells, when such are present, and is therefore ejected
from the ovum, part also remains in the ovum and forms a nuclear body which
will be spoken of as the _female pronucleus_, the fate of which is recorded
in the second part of this paper. The researches of Bütschli and van
Beneden have been especially instrumental in demonstrating the relation
between the polar bodies and the germinal vesicle, and those of Hertwig and
Fol, in shewing that part of the germinal vesicle remained in the ovum. It
must not, however, be supposed that the results of these authors are fully
substantiated, or that all the questions connected with these phenomena are
settled. The statements we have are in many points opposed and
contradictory, and there is much that is still very obscure.
In the sequel an account is first given of the researches of the
above-named authors, followed by a statement of those results which appear
to me the most probable.
The researches of van Beneden (3 and 4) were made on the ovum of the rabbit
and of Asterias, and from his observations on both these widely separated
forms he has been led to conclude that the germinal vesicle is either
ejected or absorbed, but that it has in no case a genetic connection with
the first segmentation sphere. He gives the following description of the
changes in the rabbit's ovum. The germinal vesicle is enclosed by a
membrane, and contains one main germinal spot, and a few accessory ones,
together with a granular material which he calls _nucleoplasma_, which
affects, as is usual in nuclei, a reticular arrangement. The remaining
space in the vesicle is filled by a clear fluid. As the ovum approaches
maturity the germinal vesicle assumes an excentric position, and fuses with
the peripheral layer of the egg to constitute the _cicatricular lens_. The
germinal spot next travels to the surface of the cicatricular lens and
forms the _nuclear disc_: at the same time the membrane of the germinal
vesicle vanishes though it probably unites with the nuclear disc. The
nucleoplasma then collects into a definite mass and forms the nucleoplasmic
body. Finally the nuclear disc assumes an ellipsoidal form and becomes the
nuclear body. Nothing is now left of the original germinal vesicle but the
nuclear body and the nucleoplasmic body both still situated within the
ovum. In the next stage no trace of the germinal vesicle can be detected in
the ovum, but outside it, close to the point where the modified remnants of
the vesicle were previously situated, there is present a polar body which
is composed of two parts, one of which stains deeply and resembles the
nuclear body, and the other does not stain but is similar to the
nucleoplasmic body. Van Beneden concludes that the polar bodies are the two
ejected products of the germinal vesicle. In the case of Asterias, van
Beneden has not observed the mode of formation of the polar bodies, and
mainly gives an account of the atrophy of the germinal vesicle, but adds
very little to what was already known to us from Kleinenberg's (14) earlier
observations. He describes with precision the breaking up of the germinal
spot into fragments and its eventual disappearance.
Though there are reasons for doubting the accuracy of all the above details
on the ovum of the rabbit, nevertheless, the observations of van Beneden
taken as a whole afford strong grounds for concluding that the formation of
the polar cells is connected with the disappearance, partial or otherwise,
of the germinal vesicle. A very similar account of the apparent
disappearance of the germinal vesicle is given by Greeff (19) who states
that the apparent disappearance of the germinal spot precedes that of the
vesicle.
The observations of Bütschli are of still greater importance in this
direction. He has studied with a view to elucidating the fate of the
germinal vesicle, the eggs of Nephelis, Lymnæus, Cucullanus, and other
Nematodes; and Rotifers. In all of these, with the exception of Rotifers,
he finds polar bodies, and in this respect his observations are of value as
tending to shew the widespread existence of these structures. Negative
results with reference to the presence of the polar bodies have, it may be
remarked, only a very secondary value. Bütschli has made the very important
discovery that in perfectly ripe eggs of Nephelis, Lymnæus and Cucullanus
and allied genera a _spindle_, similar to that of ordinary nuclei in the
act of division, appears close to the surface of the egg. This spindle he
regards as the metamorphosed germinal vesicle, and has demonstrated that it
takes part in the formation of the polar cells. He states that the whole
spindle is ejected from the egg, and that after swelling up and forming a
somewhat spherical mass it divides into three parts.
In the Nematodes generally, Bütschli has been unable to find the spindle
modification of the germinal vesicle, but he states that the germinal
vesicle undergoes degeneration, its outline becoming indistinct and the
germinal spot vanishing. The position of the germinal vesicle continues to
be marked by a clear space which gradually approaches the surface of the
egg. When it is in contact with the surface a small spherical body, the
remnant of the germinal vesicle, comes into view, and eventually becomes
ejected. The clear space subsequently disappears. This description of
Bütschli resembles in some respects that given by van Beneden of the
changes in the rabbit's ovum, and not impossibly refers to a nearly
identical series of phenomena. The discovery by Bütschli of the spindle and
its relation to the polar body has been of very great value.
The publications of van Beneden, and more especially those of Bütschli,
taken by themselves lead to the conclusion that the whole germinal vesicle
is either ejected or absorbed. Nearly simultaneously with their
publications there appeared, however, a paper by Oscar Hertwig (11) on the
eggs of one of the common sea urchins (_Toxopneustes lividus_), in which he
attempted to shew that part of the germinal vesicle, at any rate, was
concerned in the formation of the first segmentation nucleus. He believed
(though he has himself now recognised that he was in error on the point)
that no polar cell was formed in Toxopneustes, and that the whole germinal
vesicle was absorbed, with the exception of the germinal spot which
remained in the egg as the female pronucleus.
The following is the summary which he gives of his results, pp. 357-8.
"At the time when the egg is mature the germinal vesicle undergoes a
retrogressive metamorphosis and becomes carried towards the surface of
the egg by the contraction of the protoplasm. Its membrane becomes
dissolved and its contents disintegrated and finally absorbed by the
yolk. The germinal spot appears, however, to remain unaltered and to
continue in the yolk and to become the permanent nucleus of the ripe
ovum capable of impregnation."
After the publication of Bütschli's monograph, O. Hertwig (12) continued
his researches on the ova of Leeches (_Hæmopis_ and _Nephelis_), and not
only added very largely to our knowledge of the history of the germinal
vesicle, but was able to make a very important rectification in Bütschli's
conclusions. The following is a summary of his results:--The germinal
vesicle, as in other cases, undergoes a form of degeneration, though
retaining its central position; and the germinal spot breaks up into
fragments. The stages in which this occurs are followed by one when, on a
superficial examination, the ovum appears to be absolutely without a
nucleus; but there can be demonstrated by means of reagents in the position
previously occupied by the germinal vesicle a spindle nucleus with the
usual suns at its poles, which Hertwig believes to be a product of the
fragments of the germinal spot. This spindle travels towards the periphery
of the ovum and then forms the spindle observed by Bütschli. At the point
where one of the apices of the spindle lies close to the surface a small
protuberance arises which is destined to form the first polar cell. As the
protuberance becomes more prominent one half of the spindle passes into it.
The spindle then divides in the normal manner for nuclei, one half
remaining in the protuberance, the other in the ovum, and finally the
protuberance becomes a rounded body united to the egg by a narrow stalk. It
is clear that if, as there is every reason to think, the above description
is correct, the polar cell is formed by a simple process of cell-division
and not, as Bütschli believed, by the forcible ejection of the spindle.
The portion of the spindle in the polar cell becomes a mass of granules,
and that in the ovum becomes converted without the occurrence of the usual
nuclear stage into a fresh spindle. A second polar cell is formed in the
same manner as the first one, and the first one subsequently divides into
two. The portion of the spindle which remains in the egg after the
formation of the second polar cell reconstitutes itself into a nucleus--the
female pronucleus--and travelling towards the centre of the egg undergoes a
fate which will be spoken of in the second part of this paper.
The most obscure part of Hertwig's work is that which concerns the
formation of the spindle on the atrophy of the germinal vesicle, and his
latest paper, though it gives further details on this head, does not appear
to me to clear up the mystery. Though Hertwig demonstrates clearly enough
that this spindle is a product of the metamorphoses of the germinal
vesicle, he does not appear to prove the thesis which he maintains, that it
is the metamorphosed germinal spot.
Fol, to whom we are indebted in his paper on the development of Geryonia
(7) for the best of the earlier descriptions of the phenomena which attend
the maturation of the egg, and later for valuable contributions somewhat
similar to those of Bütschli with reference to the development of the
Pteropod egg (8), has recently given us a very interesting account of what
takes place in the ripe egg of _Asterias glacialis_ (9). In reference to
the formation of the polar cells, his results accord closely with those of
Hertwig, but he differs considerably from this author with reference to the
preceding changes in the germinal vesicle. He believes that the germinal
spot atrophies more or less completely, but that in any case its
constituents remain behind in the egg, though he will not definitely assert
that it takes no share in the formation of the spindle at the expense of
which both the polar cells and the female pronucleus are formed. The
spindle with its terminal suns arises, according to him, from the contents
of the germinal vesicle, loses its spindle character, travels to the
surface, and reacquiring a spindle character is concerned in the formation
of the polar cells in the way described by Hertwig.
Giard (10) gives a somewhat different account of the behaviour of the
germinal vesicle in _Psammechinus miliaris_. At maturity the contents of
the germinal vesicle and spot mix together and form an amoeboid mass,
which, assuming a spindle form, divides into two parts, one of which
travels towards the centre of the egg and forms the female pronucleus, the
other remains at the surface and gives origin to two polar cells, both of
which are formed after the egg is laid. What Giard regards as the female
pronucleus is perhaps the lower of the two bodies which take the place of
the original germinal vesicle as described by Fol. Vide the account of
Fol's observations on p. 531.
Strasburger, from observations on _Phallusia_, accepts in the main
Hertwig's conclusion with reference to the formation of the polar bodies,
but does not share Hertwig's view that either the polar bodies or female
pronucleus are formed at the expense of the germinal spot alone. He has
further shewn that the so-called canal-cell of conifers is formed in the
same manner as the polar cells, and states his belief that an equivalent of
the polar cells is widely distributed in the vegetable subkingdom.
This sketch of the results of recent researches will, it is hoped, suffice
to bring into prominence the more important steps by which the problems of
this department of embryology have been solved. The present aspects of the
question may perhaps be most conveniently displayed by following the
history of a single ovum. For this purpose the eggs of _Asterias
glacialis_, which have recently formed the subject of a series of beautiful
researches by Fol (9), may conveniently be selected.
The ripe ovum (Fig. 2), when detached from the ovary, is formed of a
granular vitellus without a vitelline membrane, but enveloped in a
mucilaginous coat. It contains an excentrically situated germinal vesicle
and germinal spot. In the former is present the usual protoplasmic
reticulum. As soon as the ovum reaches the sea water the germinal vesicle
commences to undergo a peculiar metamorphosis. It exhibits frequent changes
of form, its membrane becomes gradually absorbed and its outline indented
and indistinct, and finally its contents become to a certain extent
confounded with the vitellus (Fig. 3).
The germinal spot at the same time loses its clearness of outline and
gradually disappears from view.
[Illustration: FIG. 2.--Ripe ovum of Asterias glacialis enveloped in a
mucilaginous envelope, and containing an excentric germinal vesicle and
germinal spot (copied from Fol).]
[Illustration: FIG. 3.--Two successive stages in the gradual metamorphosis
of the germinal vesicle and spot of the ovum of Asterias glacialis
immediately after it is laid (copied from Fol).]
[Illustration: FIG. 4.--Ovum of Asterias glacialis, shewing the clear
spaces in the place of the germinal vesicle. Fresh preparation (copied from
Fol).]
At a slightly later stage in the place of the original germinal vesicle
there may be observed in the fresh ovum two clear spaces (fig. 4), one
ovoid and nearer the surface, and the second more irregular in form and
situated rather deeper in the vitellus. By treatment with reagents the
first clear space is found to be formed of a spindle with two terminal suns
on the lower side of which is a somewhat irregular body (Fig. 5). The
second clear space by the same treatment is shewn to contain a round body.
Fol concludes that the spindle is formed out of part of the germinal
vesicle and not of the germinal spot, while he sees in the round body
present in the lower of the two clear spaces the metamorphosed germinal
spot. He will not, however, assert that no fragment of the germinal spot
enters into the formation of the spindle. It may be observed that Fol is
here obliged to fill up (so far at least as his present preliminary account
enables me to determine) a lacuna in his observations in a hypothetical
manner, and O. Hertwig's (13) most recent observations on the ovum of the
same or an allied species of Asterias tend to throw some doubt upon Fol's
interpretations.
[Illustration: FIG. 5.--Ovum of Asterias glacialis, at the same stage as
Fig. 4, treated with picric acid (copied from Fol).]
The following is Hertwig's account of the changes in the germinal vesicle.
A quarter of an hour after the egg is laid the protoplasm on the side of
the germinal vesicle towards the surface of the egg develops a prominence
which presses inwards the wall of the vesicle. At the same time the
germinal spot develops a large vacuole, in the interior of which is a body
consisting of nuclear substance, and formed of a firmer and more refractive
material than the remainder of the germinal spot. In the above-mentioned
prominence towards the germinal vesicle, first one sun is formed by radial
striæ of protoplasm, and then a second makes its appearance, while in the
living ovum the germinal spot appears to have vanished, the outline of the
germinal vesicle to have become indistinct, and its contents to have
mingled with the surrounding protoplasm. Treatment with reagents
demonstrates that in the process of disappearance of the germinal spot the
nuclear mass in the vacuole forms a rod-like body, the free end of which is
situated between the two suns which occupy the prominence of the germinal
vesicle. At a slightly later period granules may be seen at the end of the
rod and finally the rod itself vanishes. After these changes there may be
demonstrated by the aid of reagents a spindle between the two suns, which
Hertwig believes to grow in size as the last remnants of the germinal spot
gradually vanish, and he maintains, as before mentioned, that the spindle
is formed at the expense of the germinal spot. Without following Hertwig so
far as this[364] it may be permitted to suggest that his observations tend
to shew that the body noticed by Fol in the median line, on the inner side
of his spindle, is in reality a remnant of the germinal spot and not, as
Fol supposes, part of the germinal vesicle. Considering how conflicting is
the evidence before us it seems necessary to leave open for the present the
question as to what parts of the germinal vesicle are concerned in forming
the first spindle.
Footnote 364: Hertwig's full account of his observations, with
figures, in the 4th vol. of the _Morphologische Jahrbuch_, has
appeared since the above was written. The figures given
strongly support Hertwig's views.
[Illustration: FIG. 6.--Portion of the ovum of Asterias glacialis, shewing
the spindle formed from the metamorphosed germinal vesicle projecting into
a protoplasmic prominence of the surface of the egg. Picric acid
preparation (copied from Fol).]
[Illustration: FIG. 7.--Portion of the ovum of Asterias glacialis at the
moment of the detachment of the first polar body and the withdrawal of the
remaining part of the spindle within the ovum. Picric acid preparation
(copied from Fol).]
[Illustration: FIG. 8.--Portion of the ovum of Asterias glacialis, with the
first polar body as it appears when living (copied from Fol).]
[Illustration: FIG. 9.--Portion of the ovum of Asterias glacialis
immediately after the formation of the second polar body. Picric acid
preparation (copied from Fol).]
The spindle, however it be formed, has up to this time been situated with
its axis parallel to the surface of the egg, but not long after the stage
last described a spindle is found with one end projecting into a
protoplasmic prominence which makes its appearance on the surface of the
egg (Fig. 6). Hertwig believes that the spindle simply travels towards the
surface, and while doing so changes the direction of its axis. Fol finds,
however, that this is not the case, but that between the two conditions of
the spindle an intermediate one is found in which a spindle can no longer
be seen in the egg, but its place is taken by a compact rounded body. He
has not been able to arrive at a conclusion as to what meaning is to be
attached to this occurrence. In any case the spindle which projects into
the prominence on the surface of the egg divides it into two parts, one in
the prominence and one in the egg (Fig. 7). The prominence itself with the
enclosed portion of the spindle becomes partially constricted off from the
egg as the first polar body (Fig. 8). The part of the spindle which remains
in the egg becomes directly converted into a second spindle by the
elongation of its fibres without passing through a typical nuclear
condition. A second polar cell next becomes formed in the same manner as
the first (Fig. 9), and the portion of the spindle remaining in the egg
becomes converted into two or three clear vesicles (Fig. 10) which soon
unite to form a single nucleus, the female pronucleus (Fig. 11). The two
polar cells appear to be situated between two membranes, the outer of which
is very delicate and only distinct where it covers the polar cells, while
the inner one is thicker and becomes, after impregnation, more distinct and
then forms what Fol speaks of as the vitelline membrane. It is clear, as
Hertwig has pointed out, that the polar bodies originate by a regular cell
division and have the value of cells.
[Illustration: FIG. 10.--Portion of the ovum of Asterias glacialis after
the formation of the second polar cell, shewing the part of the spindle
remaining in the ovum becoming converted into two clear vesicles. Picric
acid preparation (copied from Fol).]
[Illustration: FIG. 11.--Ovum of Asterias glacialis with the two polar
bodies and the female pronucleus surrounded by radial striæ, as seen in the
living egg (copied from Fol).]
_General conclusions._
Considering how few ova have been adequately investigated with reference to
the behaviour of the germinal vesicle any general conclusions which may at
present be formed are to be regarded as provisional, and I trust that this
will be borne in mind by the reader in perusing the following paragraphs.
There is abundant evidence that at the time of maturation of the egg the
germinal vesicle undergoes peculiar changes, which are, in part at least,
of a retrogressive character. These changes may begin considerably before
the egg has reached the period of maturity, or may not take place till
after it has been laid. They consist in appearance of irregularity and
obscurity in the outline of the germinal vesicle, the absorption of its
membrane, the partial absorption of its contents in the yolk, and the
breaking up and disappearance of the germinal spot. The exact fate of the
single germinal spot, or the numerous spots where they are present, is
still obscure; and the observations of Oellacher on the trout, and to a
certain extent my own on the skate, tend to shew that the membrane of the
germinal vesicle may in some cases be ejected from the egg, but this
conclusion cannot be accepted without further confirmation.
The retrogressive metamorphosis of the germinal vesicle is followed in a
large number of instances by the conversion of what remains into a striated
spindle similar in character to a nucleus previous to division. This
spindle travels to the surface and undergoes division to form the polar
cell or cells in the manner above described. The part which remains in the
egg forms eventually the female pronucleus.
The germinal vesicle has up to the present time only been observed to
undergo the above series of changes in a certain number of instances,
which, however, include examples from several divisions of the
Coelenterata, the Echinodermata, and the Mollusca, and also some of the
Vermes (Nematodes, Hirudinea, Sagitta). It is very possible, not to say
probable, that it is universal in the animal kingdom, but the present state
of our knowledge does not justify us in saying so. It may be that in the
case of the rabbit, and many Nematodes as described by van Beneden and by
Bütschli, we have instances of a different mode of formation of the polar
cells.
The case of Amphibians, as described by Bambeke (2) and Hertwig (12) cannot
so far be brought into conformity with our type, though observations are so
difficult to make with such opaque eggs that not much reliance can be
placed upon the existing statements. In both of these types of possible
exceptions it is fairly clear that, whatever may be the case with reference
to the formation of the polar cells, part of the germinal vesicle remains
behind as the female pronucleus.
There are a large number of types, including the whole of the Rotifera[365]
and Arthropoda, with a few doubtful exceptions, in which the polar cells
cannot as yet be said to have been satisfactorily observed.
Footnote 365: Flemming (6) finds that, in the summer and
probably parthenogenetic eggs of _Lacinularia socialis_, the
germinal vesicle approaches the surface and becomes invisible,
and that subsequently a slight indentation in the outline of
the egg marks the point of its disappearance. In the hollow of
the indentation Flemming believes a polar cell to be situated,
though he has not definitely seen one.
Whatever may be the eventual result of more extended investigation, it is
clear that the formation of polar cells according to our type is a very
constant occurrence. Its importance is also very greatly increased by the
discovery by Strasburger of the existence of an analogous process amongst
plants. Two questions about it obviously present themselves for solution:
(1) What are the conditions of its occurrence with reference to
impregnation? (2) What meaning has it in the development of the ovum or the
embryo?
The answer to the first of these questions is not difficult to find. The
formation of the polar bodies is independent of impregnation, and is the
final act of the normal growth of the ovum. In a few types the polar cells
are formed while the ovum is still in the ovary, as, for instance, in some
species of Echini, Hydra, &c., but, according to our present knowledge, far
more usually after the ovum has been laid. In some of the instances the
budding off of the polar cells precedes, and in others follows
impregnation; but there is no evidence to shew that in the later cases the
process is influenced by the contact with the male element. In Asterias, as
has been shewn by O. Hertwig, the formation of the polar cells may
indifferently either precede or follow impregnation--a fact which affords a
clear demonstration of the independence of the two occurrences.
To the second of the two questions it does not unfortunately seem possible
at present to give an answer which can be regarded as satisfactory.
The retrogressive changes in the membrane of the germinal vesicle which
usher in the formation of the polar bodies may very probably be viewed as a
prelude to a renewed activity of the contents of the vesicle; and are
perhaps rendered the more necessary from the thickness of the membrane
which results from a protracted period of passive growth. This suggestion
does not, however, help us to explain the formation of polar cells by a
process identical with cell division. The ejection of part of the germinal
vesicle in the formation of the polar cells may probably be paralleled by
the ejection of part or the whole of the original nucleus which, if we may
trust the beautiful researches of Bütschli, takes place during conjugation
in Infusoria as a preliminary to the formation of a fresh nucleus. This
comparison is due to Bütschli, and according to it the formation of the
polar bodies would have to be regarded as assisting, in some as yet unknown
way, the process of regeneration of the germinal vesicle. Views analogous
to this are held by Strasburger and Hertwig, who regard the formation of
the polar bodies in the light of a process of excretion or removal of
useless material. Such hypotheses do not unfortunately carry us very far.
I would suggest that in the formation of the polar cells part of the
constituents of the germinal vesicle which are requisite for its functions
as a complete and independent nucleus are removed to make room for the
supply of the necessary parts to it again by the spermatic nucleus (vide p.
541). More light on this, as on other points, may probably be thrown by
further investigations on parthenogenesis and the presence or absence of a
polar cell in eggs which develop parthenogenetically. Curiously enough the
two groups in which parthenogenesis most frequently occurs in the ordinary
course of development (_Arthropoda_ and _Rotifera_) are also those in which
polar cells, with the possible exception mentioned above, of the
parthenogenetic eggs of Lacenularia, are stated to be absent. This curious
coincidence, should it be confirmed, may perhaps be explained on the
hypothesis, I have just suggested, viz. _that a more or less essential part
of the nucleus is removed in the formation of the polar cells; so that in
cases, e.g. Arthropoda and Rotifera, where polar cells are not formed, and
an essential part of the nucleus not therefore removed, parthenogenesis can
much more easily occur than when polar cells are formed_.
That the part removed in the formation of the polar cells is not absolutely
essential, seems at first sight to follow from the fact of parthenogenesis
being possible in instances where impregnation is the normal occurrence.
The genuineness of all the observations on this head is too long a subject
to enter into here[366], but after admitting, as we probably must, that
there are genuine cases of parthenogenesis, it cannot be taken for granted
without more extended observation that the occurrence of development in
these rare instances may not be due to the polar cells not having been
formed as usual, and that when the polar cells are formed the development
without impregnation is less possible.
Footnote 366: The instances quoted by Siebold from Hensen and
Oellacher are not quite satisfactory. In Hensen's case
impregnation would have been possible if we can suppose the
spermatozoa to be capable of passing into the body-cavity
through the open end of the uninjured oviduct; and though
Oellacher's instances are more valuable, yet sufficient care
seems hardly to have been taken, especially when it is not
certain for what length of time spermatozoa may be able to live
in the oviduct. For Oellacher's precautions, vide _Zeit. für
wiss. Zool._ Bd. XXII. p. 202.
The remarkable observations of Professor Greeff (19) on the parthenogenetic
development of the eggs of _Asterias rubens_ tell, however, very strongly
against this explanation. Greeff has found that under normal circumstances
the eggs of this species of starfish will develop without impregnation in
simple sea water. The development is quite regular and normal though much
slower than in the case of impregnated eggs. It is not definitely stated
that polar cells are formed, but there can be no doubt that this is
implied. Professor Greeff's account is so precise and circumstantial that
it is not easy to believe that any error can have crept in; but neither
Hertwig nor Fol have been able to repeat his experiments, and we may be
permitted to wait for further confirmation before absolutely accepting
them.
It is possible that the removal of part of the protoplasm of the egg in the
formation of the polar cells may be a secondary process due to an
attractive influence of the nucleus on the cell protoplasm, such as is
ordinarily observed in cell division.
_Impregnation of the Ovum._
A far greater amount of certainty appears to me to have been attained as to
the effects of impregnation than as to the changes of the germinal vesicle
which precede this, and there appears, moreover, to be a greater uniformity
in the series of resulting phenomena. For convenience I propose to reverse
the order hitherto adopted and to reserve the history of the literature and
my discussion of disputed points till after my general account. Fol's paper
on _Asterias glacialis_, is again my source of information. The part of the
germinal vesicle which remains in the egg, after the formation of the
second polar cell, becomes converted into a number of small vesicles
(Fig. 10), which aggregate themselves into a single clear nucleus which
gradually travels toward the centre of the egg and around which as a centre
the protoplasm becomes radiately striated (Fig. 11). This nucleus is known
as the _female pronucleus_[367]. In _Asterias glacialis_ the most
favourable period for fecundation is about an hour after the formation of
the female pronucleus. If at this time the spermatozoa are allowed to come
in contact with the egg, their heads soon become enveloped in the investing
mucilaginous coat. A prominence, pointing towards the nearest spermatozoon,
now arises from the superficial layer of protoplasm of the egg and grows
till it comes in contact with the spermatozoon (Figs. 12 and 13), Under
normal circumstances the spermatozoon, which meets the prominence, is the
only one concerned in the fertilisation, and it makes its way into the egg
by passing through the prominence. The tail of the spermatozoa, no longer
motile, remains visible for some time after the head has bored its way in,
but its place is soon taken by a pale conical body which is, however,
probably in part a product of the metamorphosis of the tail itself
(Fig. 14). This body vanishes in its turn.
Footnote 367: According to Hertwig's most recent statement a
nucleolus is present in this nucleus.
[Illustration: FIGS. 12 AND 13.--Small portion of the ovum of Asterias
glacialis. The spermatozoa are shewn enveloped in the mucilaginous coat. In
Fig. 12 a prominence is rising from the surface of the egg towards the
nearest spermatozoon; and in Fig. 13 the spermatozoon and prominence have
met. From living ovum (copied from Fol).]
At the moment of contact between the spermatozoon and the egg the outermost
layer of the protoplasm of the latter raises itself as distinct membrane,
which separates from the egg and prevents the entrance of any more
spermatozoa. At the point where the spermatozoon entered a crater-like
opening is left in the membrane (Fig. 14).
[Illustration: FIG. 14.--Portion of the ovum of Asterias glacialis after
the entrance of a spermatozoon into the ovum. It shows the prominence of
the ovum through which the spermatozoon has entered. A vitelline membrane
with a crater-like opening has become distinctly formed. From living ovum
(copied from Fol).]
The head of the spermatozoon when in the egg forms a nucleus for which the
name _male pronucleus_ may be conveniently adopted. It grows in size by
absorbing, it is said, material from the ovum, though this may be doubted,
and around it is formed a clear space free from yolk-spherules. Shortly
after its formation the protoplasm in its neighbourhood assumes a radiate
arrangement (Fig. 15). At whatever point of the egg the spermatozoon may
have entered, it gradually travels towards the female pronucleus. This
latter, around which the protoplasm no longer has a radial arrangement,
remains motionless till it comes in contact with the rays of the male
pronucleus, after which its condition of repose is exchanged for one of
activity, and it rapidly approaches the male pronucleus, and eventually
fuses with it (Fig. 16).
[Illustration: FIG. 15.--Ovum of Asterias glacialis, with male and female
pronucleus and a radial striation of the protoplasm around the former. From
living ovum (copied from Fol).]
[Illustration: FIG. 16.--Three successive stages in the coalescence of the
male and female pronucleus in Asterias glacialis. From the living ovum
(copied from Fol).]
The product of this fusion forms the first segmentation nucleus (Fig. 17),
which soon, however, divides into the two nuclei of the two first
segmentation spheres. While the two pronuclei are approaching one another
the protoplasm of the egg exhibits amoeboid movements.
Of the earlier observations on this subject there need perhaps only be
cited one of E. van Beneden, on the rabbit's ovum, shewing the presence of
two nuclei before the commencement of segmentation. Bütschli was the
earliest to state from observations on _Rhabditis dolichura_ that the first
segmentation nucleus arose from the fusion of two nuclei, and this was
subsequently shewn with greater detail for _Ascaris nigrovenosa_, by
Auerbach (1). Neither of these authors gave at first the correct
interpretation of their results. At a later period Bütschli (5) arrived at
the conclusion that in a large number of instances (_Lymnæus_, _Nephelis_,
_Cucullanus_, &c.), the nucleus in question was formed by the fusion of two
or more nuclei, and Strasburger at first made a similar statement for
_Phallusia_, though he has since withdrawn it. Though Bütschli's statements
depend, as it seems, upon a false interpretation of appearances, he
nevertheless arrived at a correct view with reference to what occurs in
impregnation. Van Beneden (3) described in the rabbit the formation of the
original segmentation nucleus from two nuclei, one peripheral and the other
central, and he gave it as his hypothetical view that the peripheral
nucleus was derived from the spermatic element. It was reserved for Oscar
Hertwig (11) to describe in _Echinus lividus_ the entrance of a
spermatozoon into the egg and the formation from it of the male pronucleus.
[Illustration: FIG. 17.--Ovum of Asterias glacialis, after the coalescence
of the male and female pronucleus (copied from Fol).]
Though there is a general agreement between the most recent observers,
Hertwig, Fol, Selenka, Strasburger, &c., as to the main facts connected
with the entrance of one spermatozoon into the egg, the formation of the
male pronucleus, and its fusion with the female pronucleus, there still
exist differences of detail in the different descriptions which partly, no
doubt, depend upon the difficulties of observation, but partly also upon
the observations not having all been made upon the same species. Hertwig
does not enter into details with reference to the actual entrance of the
spermatozoon into the egg, but in his latest paper points out that
considerable differences may be observed in occurrences which succeed
impregnation, according to the relative period at which this takes place.
When, in Asterias, the impregnation is effected about an hour after the egg
is laid and previously to the formation of the polar cells, the male
pronucleus appears at first to exert but little influence on the
protoplasm, but after the formation of the second polar cell, the radial
striæ around it become very marked, and the pronucleus rapidly grows in
size. When it finally unites with the female pronucleus it is equal in size
to the latter. In the case when the impregnation is deferred for four hours
the male pronucleus never becomes so large as the female pronucleus. With
reference to the effect of the time at which impregnation takes place,
Asterias would seem to serve as a type. Thus in _Hirudinea_, _Mollusca_,
and _Nematodes_ impregnation normally takes place before the formation of
the polar bodies is completed, and the male pronucleus is accordingly as
large as the female. In _Echinus_, on the other hand, where the polar
bodies are formed in the ovary, the male pronucleus is always small.
Selenka, who has investigated the formation of the male pronucleus in
_Toxopneustes variegatus_, differs in certain points from Fol. He finds
that usually, though not always, a single spermatozoon enters the egg, and
that though the entrance may be effected at any part of the surface, it
generally occurs at the point marked by a small prominence where the polar
cell was formed. The spermatozoon first makes its way through the mucous
envelope of the egg, within which it swims about, and then bores with its
head into the polar prominence. The head of the spermatozoon on entering
the egg becomes enveloped by the superficial protoplasm, and travels inward
with its envelope, while the tail remains outside. As Fol has described, a
delicate membrane becomes formed shortly after the entrance of the
spermatozoon. The head continues to make its way by means of rapid
oscillations, till it has traversed about one eighth of the diameter of the
egg, and then suddenly becomes still. The tail in the meantime vanishes,
while the neck swells up and forms the male pronucleus. The junction of the
male and female pronucleus is described by Fol and Selenka in nearly the
same manner.
Giard gives an account of impregnation which is not easily brought into
harmony with that of the other investigators. His observations were made on
_Psammechinus miliaris_. At one point is situated a polar body and usually
at the pole opposite to it a corresponding prominence. The spermatozoa on
gaining access to the egg attach themselves to it and give it a rotatory
movement, but according to Giard none of them penetrate the vitelline
membrane which, though formed at an earlier period, now retires from the
surface of the egg.
Giard believes that the prominence opposite the polar cells serves for the
entrance of the spermatic material, which probably passes in by a process
of diffusion. Thus, though he regards the male pronucleus as a product of
impregnation, he does not believe it to be the head of a spermatozoon.
Both Hertwig and Fol have made observations on the result of the entrance
into the egg of several spermatozoa. Fol finds that when the impregnation
has been too long delayed the vitelline membrane is formed with comparative
slowness and several spermatozoa are thus enabled to penetrate. Each
spermatozoon forms a separate pronucleus with a surrounding sun; and
several male pronuclei usually fuse with the female pronucleus. Each male
pronucleus appears to exercise a repulsive influence on other male
pronuclei, but to be attracted by the female pronucleus. When there are
several male pronuclei the segmentation is irregular and the resulting
larva a monstrosity. These statements of Fol and Hertwig are at first sight
in contradiction with the more recent results of Selenka. In _Toxopneustes
variegatus_ Selenka finds that though impregnation is usually effected by a
single spermatozoon yet that several may be concerned in the act. The
development continues, however, to be normal if three or even four
spermatozoa enter the egg almost simultaneously. Under such circumstances
each spermatozoon forms a separate pronucleus and sun.
It may be noticed that, while the observations of Fol and Hertwig were
admittedly made upon eggs in which the impregnation was delayed till they
no longer displayed their pristine activity, Selenka's were made upon quite
fresh eggs; and it seems not impossible that the pathological symptoms in
the embryos reared by the two former authors may have been due to the
imperfection of the egg and not to the entrance of more than one
spermatozoon. This, of course, is merely a suggestion which requires to be
tested by fresh observations. We have not as yet a sufficient body of
observations to enable us to decide whether impregnation is usually
effected by a single spermatozoon, though in spite of certain conflicting
evidence the balance would seem to incline towards the side of a single
spermatozoon[368].
Footnote 368: The recent researches of Calberla on the
impregnation of the ovum of _Petromyzon Planeri_ support this
conclusion.
The discovery of Hertwig as to the formation of the male pronucleus throws
a flood of light upon impregnation.
The act of impregnation is seen essentially to consist in the fusion of a
male and female nucleus; not only does this appear in the actual fusion of
the two pronuclei, but it is brought into still greater prominence by the
fact that the female pronucleus is a product of the nucleus of a primitive
ovum, and the male pronucleus is the metamorphosed _head_ of the
spermatozoon which is itself developed from the nucleus of a spermatic
cell[369]. The spermatic cells originate from cells (in the case of
Vertebrates at least) identical with the primitive ova, so that the fusion
which takes place is the fusion of morphologically similar parts in the two
sexes.
Footnote 369: This seems the most probable view with reference
to the nature of the head of the spermatozoon, though the point
is not perhaps yet definitely decided.
It must not, however, be forgotten, as Strasburger has pointed out, that
part of the protoplasm of the generative cells of the two sexes also fuse,
viz. the tail of the spermatozoon with the protoplasm of the egg. But there
is no evidence that the former is of importance for the act of
impregnation. The fact that impregnation mainly consists in the union of
two nuclei gives an importance to the nucleus which would probably not have
been accorded to it on other grounds.
Hertwig's discovery is in no way opposed to Mr Darwin's theory of
pangenesis and other similar theories, but does not afford any definite
proof of their accuracy, nor does it in the meantime supply any explanation
of the origin of two sexes or of the reasons for an embryo becoming male or
female.
_Summary._
In what may probably be regarded as a normal case the following series of
events accompanies the maturation and impregnation of an egg:--
(1) Transportation of the germinal vesicle to the surface of the egg.
(2) Absorption of the membrane of the germinal vesicle and metamorphosis of
the germinal spot.
(3) Assumption of a spindle character by the remains of germinal vesicle,
these remains being probably largely formed from the germinal spot.
(4) Entrance of one end of the spindle into a protoplasmic prominence at
the surface of the egg.
(5) Division of the spindle into two halves, one remaining in the egg, the
other in the prominence. The prominence becomes at the same time nearly
constricted off from the egg as a polar cell.
(6) Formation of a second polar cell in same manner as first, part of the
spindle still remaining in the egg.
(7) Conversion of the part of the spindle remaining in the egg after the
formation of the second polar cell into a nucleus--the female pronucleus.
(8) Transportation of the female pronucleus towards the centre of the egg.
(9) Entrance of one spermatozoon into the egg.
(10) Conversion of the head of the spermatozoon into a nucleus--the male
pronucleus.
(11) Appearance of radial striæ round the male pronucleus which gradually
travels towards the female pronucleus.
(12) Fusion of male and female pronuclei to form the first segmentation
nucleus.
_List of important recent Publications on the Maturation and
Impregnation of the Ovum._
1. Auerbach. _Organologische Studien_, Heft 2.
2. Bambeke. "Recherches s. Embryologie des Batraciens." _Bull. de l'Acad.
royale de Belgique_, 2me sér., t. LXI. 1876.
3. E. Van Beneden. "La Maturation de l'OEuf des Mammifères." _Bull. de
l'Acad. royale de Belgique_, 2me sér., t. XL, no. 12, 1875.
4. E. Van Beneden. "Contributions à l'Histoire de la Vésicule Germinative,
&c." _Bull. de l'Acad. royale de Belgique_, 2me sér., t. XLI, no. 1, 1876.
5. Bütschli. _Eizelle, Zelltheilung, und Conjugation der Infusorien._
6. Flemming. "Studien in d. Entwicklungsgeschichte der Najaden." _Sitz. d.
k. Akad. Wien_, B. LXXI. 1875.
7. Fol. "Die erste Entwicklung des Geryonideneies." _Jenaische
Zeitschrift_, Vol. VII.
8. Fol. "Sur le Développement des Pteropodes." _Archives de Zoologie
Expérimentale et Générale_, Vols. IV and V.
9. Fol. "Sur le Commencement de l'Hénogénie." _Archives des Sciences
Physiques et Naturelles_. Genève, 1877.
10. Giard. _Note sur les premiers phénomènes du développement de l'Oursin._
1877.
11. Hertwig, Oscar. "Beit. z. Kenntniss d. Bildung, &c., d. thier. Eies."
_Morphologisches Jahrbuch_, Bd. I.
12. Hertwig, Oscar. Ibid. _Morphologisches Jahrbuch_, Bd. III, Heft. 1.
13. Hertwig, Oscar. "Weitere Beiträge, &c." _Morphologisches Jahrbuch_,
Bd. III, Heft 3.
14. Kleinenberg. _Hydra_. Leipzig, 1872.
15. Oellacher, J. "Beiträge zur Geschichte des Keimbläschens im
Wirbelthiereie." _Archiv f. micr. Anat._, Bd. VIII.
16. Selenka. _Befruchtung u. Theilung des Eies von Toxopneustes variegatus_
(Vorläufige Mittheilung). Erlangen, 1877.
17. Strasburger. _Ueber Zellbildung u. Zelltheilung._ Jena, 1876.
18. Strasburger. _Ueber Befruchtung u. Zelltheilung._ Jena, 1878.
19. R. Greeff. "Ueb. d. Bau u. d. Entwicklung d. Echinodermen." _Sitzun.
der Gesellschaft z. Beförderung d. gesammten Naturwiss. z. Marburg_, No. 5.
1876.
_Postscript_.--Two important memoirs have appeared since this paper was in
type. One of these by Hertwig, _Morphologisches Jahrbuch_, Bd. IV, contains
a full account with illustrations of what was briefly narrated in his
previous paper (13); the other by Calberla, "Der Befruchtungsvorgang beim
Ei von _Petromyzon Planeri_," _Zeit. für wiss. Zool._, Bd. XXX, shews that
the superficial layer of the egg is formed by a coating of protoplasm free
from yolk-spheres, which at one part is continued inwards as a column, and
contains the germinal vesicle. The surface of this column is in contact
with a micropyle in the egg-membrane. Impregnation is effected by the
entrance of the head of a single spermatozoon (the tail remaining outside)
through the micropyle, and then along the column of clear protoplasm to the
female pronucleus.
XII. ON THE STRUCTURE AND DEVELOPMENT OF THE VERTEBRATE OVARY[370].
Footnote 370: From the _Quarterly Journal of Microscopical
Science_, Vol. 18, 1878.
(With Plates 24, 25, 26.)
The present paper records observations on the ovaries of but two types,
viz., Mammalia and Elasmobranchii. The main points dealt with are
three:--1. The relation of the germinal epithelium to the stroma. 2. The
connection between _primitive ova_ in Waldeyer's sense and the permanent
ova. 3. The homologies of the egg membranes.
The second of these points seems to call for special attention after
Semper's discovery that the primitive ova ought really to be regarded as
_primitive sexual cells_, in that they give rise to the generative elements
of both sexes.
THE DEVELOPMENT OF THE ELASMOBRANCH OVARY.
The development of the Elasmobranch ovary has recently formed the subject
of three investigations. The earliest of them, by H. Ludwig, is contained
in his important work, on the 'Formation of the Ovum in the Animal
Kingdom[371].' Ludwig arrives at the conclusion that the ovum and the
follicular epithelium are both derived from the germinal epithelium, and
enters into some detail as to their formation. Schultz[372], without
apparently being acquainted with Ludwig's observations, has come to very
similar results for Torpedo.
Footnote 371: _Arbeiten a. d. zool.-zoot. Institut Würzburg_,
Bd. I.
Footnote 372: _Archiv f. micr. Anat._ Vol. XI.
Semper[373], in his elaborate memoir on the urogenital system of
Elasmobranchii, has added very greatly to our knowledge on this subject. In
a general way he confirms Ludwig's statements, though he shews that the
formation of the ova is somewhat more complicated than Ludwig had imagined.
He more especially lays stress on the existence of nests of ova
(Ureiernester), derived from the division of a single primitive ovum, and
of certain peculiarly modified nuclei, which he compares to spindle nuclei
in the act of division.
Footnote 373: _Arbeiten a. d. zool.-zoot. Institut Würzburg_,
Bd. II.
My own results agree with those of previous investigators, in attributing
to the germinal epithelium the origin both of the follicular epithelium and
ova, but include a number of points which I believe to be new, and,
perhaps, of some little interest; they differ, moreover, in many important
particulars, both as to the structure and development of the ovary, from
the accounts of my predecessors.
The history of the female generative organs may conveniently be treated
under two heads, viz. (1) the history of the ovarian ridge itself, and (2)
the history of the ova situated in it. I propose dealing in the first place
with the ovarian ridge.
_The Ovarian ridge in Scyllium._--At the stage spoken of in my monograph on
Elasmobranch Fishes as stage L, the ovarian ridge has a very small
development, and its maximum height is about 0.1 mm. It exhibits in section
a somewhat rounded form, and is slightly constricted along the line of
attachment. It presents two surfaces, which are respectively outer and
inner, and is formed of a layer of somewhat thickened germinal epithelium
separated by a basement membrane from a central core of stroma. The
epithelium is far thicker on the outer surface than on the inner, and the
primitive ova are entirely confined to the former. The cells of the
germinal epithelium are irregularly scattered around the primitive ova, and
have not the definite arrangement usually characteristic of epithelial
cells. Each of them has a large nucleus, with a deeply staining small
nucleolus, and a very scanty protoplasm. In stage N the ovarian ridge has a
pointed edge and narrower attachment than in stage L. Its greatest height
is about 0.17 mm. There is more stroma, and the basement membrane is more
distinct than before; in other respects no changes worth recording have
taken place. By stage P a distinction is observable between the right and
left ovarian ridges; the right one has, in fact, grown more rapidly than
the left, and the difference in size between the two ridges becomes more
and more conspicuous during the succeeding stages, till the left one ceases
to grow any larger, though it remains for a great part of life as a small
rudiment.
The right ovarian ridge, which will henceforth alone engage our attention,
has grown very considerably. Its height is now about 0.4 mm. It has in
section (vide Pl. 24, fig. 1) a triangular form with constricted base, and
is covered by a flat epithelium, except for an area on the outer surface,
in length co-extensive with the ovarian ridge, and with a maximum breadth
of about 0.25 mm. This area will be spoken of as the ovarian area or
region, since the primitive ova are confined to it. The epithelium covering
it has a maximum thickness of about 0.05 mm., and thins off rather rapidly
on both borders, to become continuous with the general epithelium of the
ovarian ridge. Its cells have the same character as before, and are several
layers deep. Scattered irregularly amongst them are the primitive ova. The
germinal epithelium in the ovarian region is separated by a basement
membrane from the adjacent stroma.
In succeeding stages, till the embryo reaches a length of 7 centimetres, no
very important changes take place. The ovarian region grows somewhat in
breadth, though in this respect different embryos vary considerably. In two
embryos of nearly the same age, the breadth of the ovarian epithelium was
0.3 mm. in the one and 0.35 mm. in the other. In the former of these
embryos, the thickness of the epithelium was slightly greater than in the
latter, viz. 0.09 mm. as compared with 0.08. In both the epithelium was
sharply separated from the subjacent stroma. There were relatively more
epithelial cells in proportion to primitive ova than at the earlier date,
and the individual cells exhibited great variations in shape, some being
oval, some angular, others very elongated, and many of them applied to part
of an ovum and accommodating themselves to its shape. In some of the more
elongated cells very deeply stained nuclei were present, which (in a
favourable light and with high powers) exhibited the spindle modification
of Strasburger with great clearness, and must therefore be regarded as
undergoing division. The ovarian region is at this stage bounded on each
side by a groove.
In an embryo of seven centimetres (Pl. 24, fig. 2) the breadth of the
ovarian epithelium was 0.5, but its height only 0.06 mm. It was still
sharply separated from the subjacent stroma, though a membrane could only
be demonstrated in certain parts. The amount of stroma in the ovarian ridge
varies greatly in different individuals, and no reliance can be placed on
its amount as a test of the age of the embryo. In the base of the ovarian
ridge the cells were closely packed, elsewhere they were still embryonic.
My next stage (Pl. 24, fig. 3, and fig. 4), shortly before the time of the
hatching of the embryo, exhibits in many respects an advance on the
previous one. It is the stage during which a follicular covering derived
from the germinal epithelium is first distinctly formed round the ova, in a
manner which will be more particularly spoken of in the section devoted to
the development of the ovum itself. The breadth of the ovarian region is
0.56 mm., and its greatest height close to the central border, 0.12 mm.--a
great advance on the previous stage, mainly, however, due to the larger
size of the ova.
The ovarian epithelium is still in part separated from the subjacent stroma
by a membrane close to its dorsal and ventral borders, but elsewhere the
separation is not so distinct, it being occasionally difficult within a
cell or so to be sure of the boundary of the epithelium. The want of a
clear line between the stroma and the epithelium is rendered more obvious
by the fact that the surface of the latter is somewhat irregular, owing to
projections formed by specially large ova, into the bays between which are
processes of the stroma. In an ovary about this stage, hardened in osmic
acid, the epithelium stains very differently from the subjacent stroma, and
the line of separation between the two is quite sharp. A figure of the
whole ovarian ridge, shewing the relation between the two parts, is
represented on Pl. 24, fig. 5.
The layer of stroma in immediate contact with the epithelium is very
different from the remainder, and appears to be destined to accompany the
vascular growths into the epithelium, which will appear in the next stage.
The protoplasm of the cells composing it forms a loose reticulum with a
fair number of oval or rounded nuclei, with their long axis for the most
part parallel to the lower surface of the epithelium. It contains, even at
this stage, fully developed vascular channels.
The remainder of the stroma of the ovarian ridge has now acquired a
definite structure, which remains constant through life, and is eminently
characteristic of the genital ridge of both sexes. The bulk of it (Pl. 24,
fig. 3, _str_) consists of closely packed polygonal cells, of about
0.014 mm. with large nuclei of about 0.009. These cells appear to be
supported by a delicate reticulum. The whole tissue is highly vascular,
with the numerous capillaries; the nuclei in the walls of which stand out
in some preparations with great clearness.
In the next oldest ovary, of which I have sections, the breadth of the
ovarian epithelium is 0.7 mm. and its thickness 0.096. The ovary of this
age was preserved in osmic acid, which is the most favourable reagent, so
far as I have seen, for observing the relation of the stroma and
epithelium. On Pl. 24, fig. 6, is represented a transverse section through
the whole breadth of the ovary, slightly magnified to shew the general
relations of the parts, and on Pl. 24, fig. 7, a small portion of a section
more highly magnified. The inner surface of the ovarian epithelium is more
irregular than in the previous stage, and it may be observed that the
subjacent stroma is growing in amongst the ova. From the relation of the
two tissues it is fairly clear that the growth which is taking place is a
definite growth of the stroma into the epithelium, and not a mutual
intergrowth of the two tissues. The ingrowths of the stroma are, moreover,
directed towards individual ova, around which, outside the follicular
epithelium, they form a special vascular investment in the succeeding
stages. They are formed of a reticular tissue with comparatively few
nuclei.
By the next stage, in my series of ovaries of _Scy. canicula_, important
changes have taken place in the constitution of ovarian epithelium. Fig. 8,
Pl. 24, represents a portion of the ovarian epithelium, on the same scale
as figs. 1, 2, 3, &c., and fig. 9 a section through the whole ovarian ridge
slightly magnified. Its breadth is now 1.3 mm., and its thickness 0.3 mm.
The ova have grown very greatly, and it appears to me to be mainly owing to
their growth that the greater thickness of the epithelium is due, as well
as the irregularity of its inner surface (vide fig. 9).
The general relation of the epithelium to the surrounding parts is much the
same as in the earlier stage, but two new features have appeared--(1) The
outermost cells of the ovarian region have more or less clearly arranged
themselves as a kind of epithelial covering for the organ; and (2) the
stroma ingrowths of the previous stage have become definitely vascular, and
have penetrated through all parts of the epithelium.
The external layer of epithelium is by no means a very marked structure,
the character of its cells varies greatly in different regions, and it is
very imperfectly separated from the subjacent layer. I shall speak of it
for convenience as _pseudo-epithelium_.
The greater part of the germinal epithelium forms anastomosing columns,
separated by very thin tracts of stroma. The columns are, in the majority
of instances, continuous with the pseudo-epithelium at the surface, and
contain ova in all stages of development. Many of the cells composing them
naturally form the follicular epithelium for the separate ova; but the
majority have no such relation. They have in many instances assumed an
appearance somewhat different from that which they presented in the last
stage, mainly owing to the individual nuclei being more widely separated. A
careful examination with a high power shews that this is owing to an
increase in the amount of protoplasm of the individual cells, and it may be
noted that a similar increase in the size of the bodies of the cells has
taken place in the pseudo-epithelium and in the follicular epithelium of
the individual ova.
The stroma ingrowths form the most important feature of the stage. In most
instances they are very thin and delicate, and might easily be overlooked,
especially as many of the cells in them are hardly to be distinguished,
taken separately, from those of the germinal epithelium. These features
render the investigation of the exact relation of the stroma and epithelium
a matter of some difficulty. I have, however, been greatly assisted by the
investigation of the ovary of a young example of _Scyllium stellare_,
16-1/2 centimètres in length, a section of which is represented in Pl. 25,
fig. 26. In this ovary, although no other abnormalities were observable,
the stroma ingrowths were exceptionally wide; indeed, quite without a
parallel in my series of ovaries in this respect. The stroma most clearly
divides up the epithelium of the ovary into separate masses, or more
probably anastomosing columns, the equivalents of the egg-tubes of Pflüger.
These columns are formed of normal cells of the germinal epithelium, which
enclose ovarian nests and ova in all stages of development. A comparison of
the section I have represented, with those from previous stages, appears to
me to demonstrate that the relation of the epithelium and stroma has been
caused by an ingrowth or penetration of the stroma into the epithelium, and
not by a mutual intergrowth of the two tissues. Although the ovary, of
which fig. 26 represents a section was from _Scy. stellare_, and the
previous ovaries have been from _Scy. canicula_, yet the thickness of the
epithelium may still be appealed to in confirmation of this view. In the
previous stage the thickness was about 0.096 mm., in the present one it is
about 0.16 mm., a difference of thickness which can be easily accounted for
by the growth of the individual ova and the additional tracts of stroma. A
pseudo-epithelium is more or less clearly formed, but it is continuous with
the columns of epithelium. In the stroma many isolated cells are present,
which appear to me, from a careful comparison of a series of sections, to
belong to the germinal epithelium.
The thickness of the follicular epithelium on the inner side of the larger
ova deserves to be noted. Its meaning is discussed on p. 567.
Quite a different interpretation to that which I have given has been put by
Ludwig and Semper upon the parts of the ovary at this stage. My
_pseudo-epithelium_ is regarded by them as forming, together with the
_follicular epithelium_ of the ova, the sole remnant of the original
germinal epithelium; and the masses of cells below the pseudo-epithelium,
which I have attempted to shew are derived from the original germinal
epithelium, are regarded as parts of the ingrowths of the adjacent stroma.
Ludwig has assumed this interpretation without having had an opportunity of
working out the development of the parts, but Semper attempts to bring
forward embryological proofs in support of this position.
If the series of ovaries which I have represented be examined, it will not,
I think, be denied that the general appearances are very much in favour of
my view. The thickened patch of ovarian epithelium can apparently be traced
through the whole series of sections, and no indications of its sudden
reduction to the thin pseudo-epithelium are apparent. The most careful
examination that I have been able to make brings to light nothing tending
to shew that the general appearances are delusive. The important difference
between us refers to _our views of the nature of the tissue subjacent to
the pseudo-epithelium_. If my results be accepted, it is clear that the
whole ovarian region is an epithelium interpenetrated by connective tissue
ingrowths, so that the region below the pseudo-epithelium is a kind of
honeycomb or trabecular net-work of germinal epithelium, developing ova of
all stages and sizes, and composed of cells capable of forming follicular
epithelium for developing ova. Ludwig figures what he regards as the
formation of the follicular epithelium round primitive ova during their
passage into the stroma. It is quite clear to me, that his figures of the
later stages, 33 and 34, represent fully formed permanent ova surrounded by
a follicular epithelium, and that their situation in contact with the
pseudo-epithelium is, so to speak, an accident, and it is quite possible
that his figures 31 and 32 also represent fully formed ova; but I have
little hesitation in asserting that he has not understood the mode of
formation of the follicular epithelium, and that, though his statement that
it is derived from the germinal epithelium is quite correct, his account of
the process is completely misleading. The same criticism does not exactly
apply to Semper's statements. Semper has really observed the formation of
the follicular epithelium round young ova; but, nevertheless, he appears to
me to give an entirely wrong account of the relation of the stroma to the
germinal epithelium. The extent of the difference between Semper's and my
view may perhaps best be shewn by a quotation from Semper, _loc. cit._,
465:--"In females the nests of primitive ova sink in groups into the
stroma. In these groups one cell enlarges till it becomes the ovum, the
neighbouring cells increase and arrange themselves around the ova as
follicle cells."
Although the histological changes which take place in the succeeding stages
are not inconsiderable, they do not involve any fundamental change in the
constitution of the ovarian region, and may be described with greater
brevity than has been so far possible.
In a half-grown female, with an ovarian region of 3mm. in breadth, and
0.8mm. in thickness, the stroma of the ovarian region has assumed a far
more formed aspect than before. It consists (Pl. 24, fig. 10) of a basis in
most parts fibrous, but in some nearly homogeneous, with a fair number of
scattered cells. Immediately below the pseudo-epithelium, there is an
imperfectly developed fibrous layer, forming a kind of tunic, in which are
imbedded the relatively reduced epithelial trabeculæ of the previous
stages. They appear in sections as columns, either continuous with or
independent of the pseudo-epithelium, formed of normal cells of the
germinal epithelium, nests of ova, and permanent ova in various stages of
development. Below this there comes a layer of larger ova which are very
closely packed. A not inconsiderable number of the larger ova have,
however, a superficial situation, and lie in immediate contact with the
pseudo-epithelium. Some of the younger ova, enclosed amongst epithelial
cells continuous with the pseudo-epithelium, are very similar to those
figured by Ludwig. It is scarcely necessary to insist that this fact does
not afford any argument in favour of his interpretations. The ovarian
region is honeycombed by large vascular channels with distinct walls, and
other channels which are perhaps lymphatic.
The surface of the ovarian region is somewhat irregular and especially
marked by deep oblique transverse furrows. It is covered by a distinct,
though still irregular pseudo-epithelium, which is fairly columnar in the
furrows but flattened along the ridges. The cells of the pseudo-epithelium
have one peculiarity very unlike that of ordinary epithelial cells. Their
inner extremities (vide fig. 10) are prolonged into fibrous processes which
enter the subjacent tissue, and bending nearly parallel to the surface of
the ovary, assist in forming the tunic spoken of above. This peculiarity of
the pseudo-epithelial cells seems to indicate that they do not essentially
differ from cells which have the character of undoubted connective tissue
cells, and renders it possible that the greater part of the tunic, which
has apparently the structure of ordinary connective tissue, is in reality
derived from the original germinal epithelium, a view which tallies with
the fact that in some instances the cells of the tunic appear as if about
to assist in forming the follicular epithelium of some of the developing
ova. In Raja, the similarity of the pseudo-epithelium to the subjacent
tissue is very much more marked than in Scyllium. The pseudo-epithelium
appears merely as the superficial layer of the ovarian tunic somewhat
modified by its position on the surface. It is formed of columnar cells
with vertically arranged fibres which pass into the subjacent layers, and
chiefly differ from the ordinary fibres in that they still form parts of
the cell-protoplasm enclosing the nucleus. In Pl. 25, fig. 34, an attempt
is made to represent the relations of the pseudo-epithelium to the
subjacent tissue in Raja. Ludwig's figures of the pseudo-epithelium of the
ovary, in the regular form of its constituent cells, and its sharp
separation by a basement membrane from the tissue below, are quite unlike
anything which I have met with in my sections either of Raja or Scyllium.
Close to the dorsal border of the ovary the epithelial cells of the
non-ovarian region have very conspicuous tails, extending into a more or
less homogeneous substance below, which constitutes a peculiar form of
tunic for this part of the ovarian ridge.
In the full-grown female the stroma of the ovarian region is denser and has
a more fibrous aspect than in the younger animal. Below the
pseudo-epithelium it is arranged in two or three more or less definite
layers, in which the fibres run at right angles. It forms a definite
ovarian tunic. The pseudo-epithelium is much more distinct, and the tails
of its cells, so conspicuous in previous stages, can no longer be made out.
_Formation of the permanent ova and the follicular epithelium._--In my
monograph on the development of Elasmobranch Fishes an account was given of
the earliest stages in the development of the primitive ova, and I now take
up their development from the point at which it was left off in that work.
From their first formation till the stage spoken of in my monograph as P,
their size remains fairly constant. The larger examples have a diameter of
about 0.035 mm., and the medium-sized examples of about 0.03 mm. The larger
nuclei have a diameter of about 0.16 mm., but their variations in size are
considerable. If the above figures be compared with those on page 350 of my
monograph on Elasmobranch Fishes, it will be seen that the size of the
primitive ova during these stages is not greater than it was at the period
of their very first appearance.
The ova (Pl. 24, fig. 1) are usually aggregated in masses, which might have
resulted from division of a single ovum. The outlines of the individual ova
_are always distinct_. Their protoplasm is clear, and their nuclei, which
are somewhat passive towards staining reagents, are granular, with one to
three nucleoli. I have noticed, up to stage P, the occasional presence of
highly refractive spherules in the protoplasm of the primitive ova already
described in my monograph (pp. 353, 354, Pl. 12, fig. 15). They seem to
occur up to a later period than I at first imagined. Their want of
constancy probably indicates that they have no special importance.
Professor Semper has described similar appearances in the male primitive
ova of a later period.
As to the distribution of the primitive ova in the germinal epithelium,
Professor Semper's statement that the larger primitive ova are found in
masses in the centre, and that the smaller ova are more peripherally
situated is on the whole true, though I do not find this distribution
sufficiently constant to lay so much stress on it as he does.
The passive condition of the primitive ova becomes suddenly broken during
stage Q, and is succeeded by a period of remarkable changes. It has only
been by the expenditure of much care and trouble that I have been able to
elucidate to my own satisfaction what takes place, and there are still
points which I do not understand.
Very shortly after stage Q, in addition to primitive ova with a perfectly
normal nucleus, others may be seen in which the nucleus is apparently
replaced by a deeply stained irregular body, smaller than the ordinary
nuclei (Pl. 24, fig. 11, _d.n._). This body, by the use of high objectives,
is seen to be composed of a number of deeply stained granules, and around
it may be noticed a clear space, bounded by a very delicate membrane. The
granular body usually lies close to one side of this membrane, and
occasionally sends a few fine processes to the opposite side.
The whole body, _i.e._ all within the delicate membrane is, according to my
view, a modified nucleus; as appears to me very clearly to be shewn by the
fact that it occupies the normal position of a nucleus within a cell body.
Semper, on the other hand, regards the contained granular body as the
nucleus, which he compares with the spindles of Bütschli, Auerbach,
&c.[374]. This interpretation appears to me, however, to be negatived by
the position of these bodies. The manner in which Semper may, perhaps, have
been led to his views will be obvious when the later changes of the
primitive ova are described. The formation of these nuclei would seem to be
due to a segregation of the constituents of the original nuclei; the solid
parts becoming separated from the more fluid. As a rule, the modified
nuclei are slightly larger than the original ones. In stage Q the following
two tables shew the dimensions of the parts of three unmodified and of
three modified nuclei taken at random.
Footnote 374: _Loc. cit._ p. 361.
_Primitive ova with unmodified nuclei_--
Nuclei.
0.014 mm.
0.012 mm.
0.01 mm.
_Primitive ova with modified nuclei_--
Granular
Nuclei. Bodies in nuclei.
0.018 mm. 0.006 mm.
0.018 mm. 0.006 mm.
0.012 mm. 0.009 mm.
For a slightly older stage than Q, the two annexed tables also shew the
comparative size of the modified and unmodified nuclei:
_Unmodified nuclei of normal primitive ova--_
0.014 mm.
0.016 mm.
0.014 mm.
0.016 mm.
0.016 mm.
_Nuclei of primitive ova with modified nuclei--_
Granular
Nuclei. Bodies in Nuclei.
0.018 mm. 0.008 mm.
0.016 mm. 0.008 mm.
0.016 mm. 0.01 mm.
0.016 mm.
0.018 mm.
These figures bring out with clearness the following points: (1) that the
modified nuclei are slightly but decidedly larger on the average than the
unmodified nuclei; (2) that the contained granular bodies _are very
considerably_ smaller than ordinary nuclei.
Soon after the appearance of the modified nuclei, remarkable changes take
place in the cells containing them. Up to the time such nuclei first make
their appearance the outlines of the individual ova are very clearly
defined, but subsequently, although numerous ova with but slightly modified
nuclei are still to be seen, yet on the whole the outlines of all the
primitive ova are much less distinct than before; and this is especially
the case with the primitive ova containing modified nuclei.
From cases in which three or four ova are found in a mass with modified
nuclei, but in which the outline of each ovum is fairly distinct, it is
possible to pass by insensible gradations to other cases in which two or
three or more modified nuclei are found embedded in a mass of protoplasm in
which no division into separate cells can be made out (fig. 14). For these
masses I propose to employ the term nests. They correspond in part with the
_Ureiernester_ of Professor Semper.
Frequently they are found in hardened specimens to be enclosed in a
membrane-like tunic which appears to be of the nature of coagulated fluid.
These membranes closely resemble and sometimes are even continuous with
trabeculæ which traverse the germinal epithelium. Ovaries differ
considerably as to the time and completeness of the disappearance of the
outlines marking the separate cells, and although, so far as can be
gathered from my specimens, the rule is that the outlines of the primitive
ova with modified nuclei soon become indistinct, yet in one of my best
preserved ovaries very large nests with modified nuclei are present in
which the outline of each ovum is as distinct as during the period before
the nuclei undergo these peculiar changes (Pl. 24, fig. 12). In the same
ovary other nests are present in which the outlines of the individual ova
are no longer visible. The section represented on Pl. 24, fig. 2, is fairly
average as to the disappearance of the outlines of the individual ova.
It is clear from the above statements, that in the first instance the nests
are produced by the coalescence of several primitive ova into a single mass
or syncytium; though of course, the several separate ova of a nest may
originally, as Semper believes, have arisen from the division of a single
ovum. In any case there can be no doubt that the nests of separate ova
increase in size as development proceeds; a phenomenon which is more
reasonably explained on the view that the ova divide, than on the view that
they continue to be freshly formed. The same holds true for the nests of
nuclei and this, as well as other facts, appears to me to render it
probable that the nests grow by division of the nuclei without
corresponding division of the protoplasmic matrix. I cannot, however,
definitely prove this point owing to my having found nests, with distinct
outlines to the ova, as large as any without such outlines.
The nests are situated for the most part near the surface of the germinal
epithelium. The smaller ones are frequently spherical, but the larger are
irregular in form. The former are about 0.05 mm. in diameter; the latter
reach 0.1 mm. Scattered generally, and especially in the deeper layers, and
at the edges of the germinal epithelium, are still unmodified or only
slightly modified primitive ova. These unmodified primitive ova are
aggregated in masses, but in these masses the outlines of each ovum, though
perhaps less clear than in the earlier period, are still distinct.
When the embryo reaches a length of seven centimètres, and even in still
younger embryos, further changes are observable. In the first place many of
the modified nuclei acquire fresh characters, and it becomes necessary to
divide the modified nuclei into two categories. In both of these the outer
boundary of the nucleus is formed by a very delicate membrane, the space
within which is perfectly clear except for the granular body. In the
variety which now appears in considerable numbers the granular body has an
irregular star-like form. The rays of the star are formed of fibres
frequently knobbed at their extremities, and the centre of the star usually
occupies an eccentric position. Typical examples of this form of modified
nucleus, which may be spoken of as the stellate variety, are represented on
Pl. 25, fig. 17; between it and the older granular variety there is an
infinite series of gradations, many of which are represented on Pl. 24,
figs. 12, 14, 15, 16. Certain of the stellate nuclei exhibit two centres
instead of one, and in some cases, like that represented on Pl. 25,
fig. 19, the stellate body of two nuclei is found united. Both of these
forms are possibly modifications of the spindle-like form assumed by nuclei
in the act of dividing, and may be used in proving that the nests increase
in size by the division of the contained nuclei. In addition to the normal
primitive ova, a few of which are still present, there are to be found,
chiefly in the deeper layers of the germinal epithelium, larger ova
differing considerably from the primitive ova. They form the permanent ova
(Pl. 24, fig. 3, _o_). Their average diameter is 0.04 mm., compared with
0.03 mm., the diameter of original primitive ova. The protoplasm of which
they are composed is granular, but at first a membrane can hardly be
distinguished around them; their nucleus is relatively large, 0.02 -
0.027 mm. in diameter. It presents the characters ascribed by Eimer[375],
and many other recent authors[376], to typical nuclei (vide Pl. 24, fig. 3,
and Pl. 24, 25, figs. 13, 14, 15, 16, 17, 18). It is bounded by a distinct
membrane, within which is a more or less central nucleolus from which a
number of radial fibres which stain very deeply pass to the surface; here
they form immediately internal to the membrane a network with granules at
the nodal points. In some instances the regularity of the arrangement of
these fibres is very great, in other instances two central nucleoli are
present, in which case the regularity is considerably interfered with. The
points in which the youngest permanent ova differ from the primitive may be
summed up as follows:--
(1) The permanent ova are larger, the smallest of them being larger than
the average primitive ova in the proportion of four to three. (2) They have
less protoplasm as compared to the size of the nucleus. (3) Their
protoplasm is granular instead of being clear. (4) Their nucleus is clear
with exception of a network of fibres instead of being granular as in the
primitive ova. It thus appears that the primitive ova and permanent ova are
very different in constitution, though genetically related in a way to be
directly narrated.
Footnote 375: _Archiv f. micr. Anat._ Vol. XIV.
Footnote 376: Vide especially Klein, _Quart. Journ. of Mic.
Sci._ July 1878.
The formation of permanent ova is at its height in embryos of about seven
centimètres or slightly larger. The nests at this stage are for the most
part of a very considerable size and contain a large number of nuclei,
which have probably, as before insisted, originated from a division of the
smaller number of nuclei present in the nests at an earlier stage. Figs.
14-18 are representations of nests at this period. The diameter of the
nuclei is, on the whole, slightly greater than at an earlier stage. A
series of measurements gave the following results:--
0.016 mm.
0.016 mm.
0.018 mm.
0.02 mm.
0.02 mm.
Both varieties of modified nuclei are common enough, though the stellate
variety predominates. The nuclei are sometimes in very close contact, and
sometimes separated by protoplasm, which in many instances is very slightly
granular. In a large number of the nests nothing further is apparent than
what has just been described, but in a very considerable number one or more
nuclei are present, which exhibit a transitional character between the
ordinary stellate nuclei of my second category, and the nuclei of permanent
ova as above described; and in these nests the formation of permanent ova
is taking place. Permanent ova in the act of development are indicated in
my figures by the letters _do_. Many of the intermediate nuclei are more
definitely surrounded by granular protoplasm than the other nuclei of the
nests, and accordingly have their outlines more sharply defined. Between
nuclei of this kind, and others as large as those of the permanent ova,
there are numerous transitional forms. The larger ones frequently lie in a
mass of granular protoplasm projecting from the nest, and only united with
it by a neck (Pl. 24, figs. 14 and 16). For prominences of this kind to
become independent ova, it is only necessary for the neck to become broken
through. Nests in which such changes are taking place present various
characters. In some cases several nuclei belonging to a nest appear to be
undergoing conversion into permanent ova at the same time. Such a case is
figured on Pl. 25, figs. 17 and 18. In these cases the amount of granular
protoplasm in the nest and around each freshly formed ovum is small. In the
more usual cases only one or two permanent ova at the utmost are formed at
the same time, and in these instances a considerable amount of granular
protoplasm is present around the nucleus of the developing permanent ovum.
In such instances it frequently happens several of the nuclei not
undergoing conversion appear to be in the process of absorption, and give
to the part of the nest in which they are contained a very hazy and
indistinct aspect (Pl. 24, fig. 15). Their appearance leads me to adopt the
view _that while some of the nuclei of each nest are converted into the
nuclei of the permanent ova, others break down and are used as the pabulum,
at the expense of which the protoplasm of the young ovum grows_.
It should, however, be stated, that after the outlines of the permanent ova
have become definitely established, I have only observed in a single
instance the inclusion of a nucleus within an ovum (Pl. 25, fig. 24). In
many instances normal nuclei of the germinal epithelium may be so observed
within the ovum.
The nuclei which are becoming converted into the nuclei of permanent ova
gradually increase in size. The following table gives the diameter of four
such nuclei:--
0.022 mm.
0.022 mm.
0.024 mm.
0.032 mm.
These figures should be compared with those of the table on page 564.
The ova when first formed are situated either at the surface or in the
deeper layers of the germinal epithelium. Though to a great extent
surrounded by the ordinary cells of the germinal epithelium, they are not
at first enclosed in a definite follicular epithelium. The follicle is,
however, very early formed.
My observations lead me then to the conclusion that in a general way the
permanent ova are formed by the increase of protoplasm round some of the
nuclei of a nest, and the subsequent separation of the nuclei with their
protoplasm from the nest as distinct cells--a mode of formation exactly
comparable with that which so often takes place in invertebrate egg tubes.
Besides the mode of formation of permanent ova just described, a second one
also seems probably to occur. In ovaries just younger than those in which
permanent ova are distinctly formed, there are present primitive ova, with
modified nuclei of the stellate variety, or nuclei sometimes even
approaching in character those of permanent ova, which are quite isolated
and not enclosed in a definite nest. The body of these ova is formed of
granular protoplasm, but their outlines are very indistinct. Such ova are
considerably larger than the normal primitive ova. They may measure
0.04 mm. In a slightly later stage, when fully formed permanent ova are
present, isolated ones are not infrequent, and it seems natural to conclude
that these isolated ova are the direct descendants of the primitive ova of
the earlier stage. It seems a fair deduction that in some cases primitive
ova undergo a direct metamorphosis into permanent ova by a modification of
their nucleus, and the assumption of a granular character in their
protoplasm, without ever forming the constituent part of a nest.
It is not quite clear to me that in all nests the coalescence of the
protoplasm of the ova necessarily takes place, since some nests are to be
found at all stages in which the ova are distinct. Nevertheless, I am
inclined to believe that the fusion of the ova is the normal occurrence.
The mode of formation of the permanent ova may then, according to my
observations, take place in two ways:--1. By the formation of granular
protoplasm round the nucleus in a nest, and the separation of the nucleus
with its protoplasm as a distinct ovum. 2. By the direct metamorphosis of
an isolated primitive ovum into a permanent ovum. The difference between
these two modes of formation does not, from a morphological point of view,
appear to be of great importance.
The above results appear clearly to shew that _the primitive ova in the
female are not to be regarded as true ova, but as the parent sexual cells
which give rise to the ova_: a conclusion which completely fits in with the
fact that cells exactly similar to the primitive ova in the female give
rise to the spermatic cells in the male.
Slightly after the period of their first formation the permanent ova become
invested by a very distinct and well-marked, somewhat flattened, follicular
epithelium (Pl. 24, fig. 3). Where the ova lie in the deeper layers of the
germinal epithelium, the follicular epithelium soon becomes far more
columnar on the side turned inwards, than on that towards the surface,
especially when the inner side is in contact with the stroma (Pl. 24,
fig. 7, and Pl. 25, figs. 24 and 26). This is probably a special provision
for the growth and nutrition of the ovum.
There cannot be the smallest doubt that the follicular epithelium is
derived from the general cells of the germinal epithelium--a point on which
my results fully bear out the conclusions of Ludwig and Semper.
The larger ova themselves have a diameter of about 0.06 mm., and their
nucleus of about 0.04 mm. The vitellus is granular, and provided with a
distinct, though delicate membrane, which has every appearance of being a
product of the ovum itself rather than of the follicular epithelium. The
membrane would seem indeed to be formed in some instances even before the
ovum has a definite investment of follicle cells. The vitellus is
frequently vacuolated, but occasionally the vacuoles appear to be caused by
a shrinking due to the hardening reagent. The nucleus has the same peculiar
reticulate character as at first. Its large size, as compared with the
ovum, is very noticeable.
With this stage the embryonic development of the ova comes to a close,
though the formation of fresh ova continues till comparatively late in
life. I have, however, two series of sections of ovaries preserved in osmic
acid, from slightly larger embryos than the one last described, about which
it may be well to say a few words before proceeding to the further
development of the permanent ova.
The younger of these ovaries was from a Scyllium embryo 10 centimètres
long, preserved in osmic acid.
A considerable number of nests were present (Pl. 24, fig. 13), exhibiting,
on the whole, similar characters to those just described.
A series of measurements of the nuclei in them were made, leading to the
following results:--
0.014 mm.
0.014 mm.
0.016 mm.
0.016 mm.
0.018 mm.
0.018 mm.
Thus, if anything, the nuclei were slightly smaller than in the younger
embryo. It is very difficult in the osmic specimens to make out clearly the
exact outlines of the various structures, the nuclei in many instances
being hardly more deeply stained than in the protoplasm around them. The
network in the nuclei is also far less obvious than after treatment with
picric acid. The permanent ova were hardly so numerous as in the younger
ovary before described. A number of these were measured with the following
results:--
Ovum. Nucleus.
0.03 mm. 0.014 mm.
0.034 mm. 0.018 mm.
0.028 mm. 0.016 mm.
0.03 mm. 0.02 mm.
0.04 mm. 0.02 mm.
0.04 mm. 0.02 mm.
0.048 mm. 0.02 mm.
These figures shew that the nuclei of the permanent ova are smaller than in
the younger embryo, and it may therefore be safely concluded that, in spite
of the greater size of the embryo from which it is taken, the ovary now
being described is in a more embryonic condition than the one last dealt
with.
Though the permanent ova appeared to be formed from the nests in the manner
already described, it was fairly clear from the sections of this ovary that
many of the original primitive ova, after a metamorphosis of the nucleus
and without coalescing with other primitive ova to form nests, become
converted directly into the permanent ova. Many large masses of primitive
ova, or at least of ova with the individual outlines of each ovum distinct,
were present. The average size of ova composing these was however small,
the body measuring about 0.016 mm., and the nucleus 0.012 mm. Isolated ova
with metamorphosed nuclei could also be found measuring 0.022, and their
nuclei about 0.014 mm.
The second of the two ovaries, hardened in osmic acid, was somewhat more
advanced than the ovary in which the formation of permanent ova was at its
height. Fewer permanent ova were in the act of being formed, and many of
these present had reached a considerable size, measuring as much as
0.07 mm. Nests of the typical forms were present as before, but the nuclei
in them were more granular than at the earlier period, and on the average
slightly smaller. A series measured had the following diameters:--
0.01 mm.
0.012 mm.
0.014 mm.
0.016 mm.
One of these nests is represented on Pl. 25, fig. 20. Many nests with the
outlines of the individual ova distinct were also present.
On the whole it appeared to me, that the second mode of formation of
permanent ova, viz. that in which the nest does not come into the cycle of
development, preponderated to a greater extent than in the earlier
embryonic period.
POST-EMBRYONIC DEVELOPMENT OF THE OVA.--My investigations upon the
post-embryonic growth and development of the ova, have for the most part
been conducted upon preserved ova, and it has been impossible for me, on
this account, to work out, as completely as I should have wished, certain
points, more especially those connected with the development of the yolk.
Although my ovaries have been carefully preserved in a large number of
reagents, including osmic acid, picric acid, chromic acid, spirit,
bichromate of potash, and Müller's fluid, none of these have proved
universally successful, and bichromate of potash and Müller's fluid are
useless. Great difficulties have been experienced in distinguishing the
artificial products of these reagents. My investigations have led me to the
result, that in the gradual growth of the ova with the age of the
individual the changes are not quite identical with those during the rapid
growth which takes place at periods of sexual activity, after the adult
condition has been reached--a result to which His has also arrived, with
reference to the ova of Osseous Fish. I propose dealing separately with the
several constituents of the egg-follicle.
_Egg membranes._--A vitelline membrane has been described by Leydig[377] in
Raja, and an albuminous layer of the nature of a chorion[378] by
Gegenbaur[379] in Acanthias--the membranes described in these two ways
being no doubt equivalent.
Footnote 377: _Rochen u. Haie._
Footnote 378: By _chorion_ I mean, following E. van Beneden's
nomenclature, a membrane formed by the follicular epithelium,
and, by _vitelline membrane_, one formed by the vitellus or
body of the ovum.
Footnote 379: "Bau und Entwicklung d. Wirbelthiereier," &c.,
_Müll. Archiv_, 1861.
Dr Alex. Schultz[380] has more recently investigated a considerable variety
of genera and finds three conditions of the egg membranes. (1) In Torpedo,
a homogeneous membrane, which is of the nature of a chorion. (2) In Raja, a
homogeneous membrane which is, however, perforated. (3) In Squalidæ, a
thick homogeneous membrane, internal to which is a thinner perforated
membrane. He apparently regards the perforated inner membrane as a
specialised part of the simple membrane found in Torpedo, and states that
this membrane is of the nature of a chorion.
Footnote 380: "Zur Entwicklungsgeschichte d. Selachier,"
_Arch. f. mikr. Anat._ Vol. XI.
My own investigations have led me to the conclusion that though the
egg-membranes can probably be reduced to single type for Elasmobranchii,
yet that they vary with the stage of development of the ovum. Scyllium
(stellare and canicula) and Raja have formed the objects of my
investigation. I commence with the two former.
It has already been stated that in Scyllium, even before the follicular
epithelium becomes formed, a delicate membrane round the ovum can be
demonstrated, which appears to me to be derived from the vitellus or body
of the ovum, and is therefore of the nature of a vitelline membrane. It
becomes the vitelline membrane of Leydig, the albuminous membrane of
Gegenbaur, and homogeneous membrane of Schultz.
In a young fish (not long hatched) with ova of not more than 0.12 mm., this
membrane, though considerably thicker than in the embryo, is not thick
enough to be accurately measured. In ova of 0.5 mm. from a young female
(Pl. 25, fig. 21) the vitelline membrane has a thickness of 0.002 mm. and
is quite homogeneous[381]. Internally to it may be observed very faint
indications of the differentiation of the outermost layer of the vitellus
into the perforated or radially striated membrane of Schultz, which will be
spoken of as _zona radiata_.
Footnote 381: The apparent structure in the vitelline membrane
in my figure is merely intended to represent the dark colour
assumed by it on being stained. The zona radiata has been made
rather too thick by the artist.
In an ovum of 1 mm. from the nearly full grown though not sexually mature
female, the zona radiata has increased in thickness and definiteness, and
may measure as much as 0.004 mm. It is always very sharply separated from
the vitelline membrane, but appears to be more or less continuous on its
inner border with the body of the ovum, at the expense of which it no doubt
grows in thickness.
In ova above 1 mm. in diameter, both vitelline membrane and zona radiata,
but especially the latter, increase in thickness. The zona becomes marked
off from the yolk, and its radial striæ become easy to see even with
comparatively low powers. In many specimens it appears to be formed of a
number of small columns, as described by Gegenbaur and others. The stage of
about the greatest development of both the vitelline membrane and zona
radiata is represented on Pl. 25, fig. 22.
At this time the vitelline membrane appears frequently to exhibit a
distinct stratification, dividing it into two or more successive layers. It
is not, however, acted on in the same manner by all reagents, and with
absolute alcohol appears at times longitudinally striated.
From this stage onwards, both vitelline membrane and zona gradually
atrophy, simultaneously with a series of remarkable changes which take
place in the follicular epithelium. The zona is the first to disappear, and
the vitelline membrane next becomes gradually thinner. Finally, when the
egg is nearly ripe, the follicular epithelium is separated from the yolk by
an immeasurably thin membrane--the remnant of the vitelline membrane--only
visible in the most favourable sections (Pl. 25, fig. 23, _vt._). When the
egg becomes detached from the ovary even this membrane is no longer to be
seen.
Both the vitelline membrane and the zona radiata are found in Raja, but in
a much less developed condition than in Scyllium. The vitelline membrane is
for a long time the only membrane present, but is never very thick (Pl. 25,
fig. 31). The zona is not formed till a relatively much later period than
in Scyllium, and is always delicate and difficult to see (Pl. 25, fig. 32).
Both membranes atrophy before the egg is quite ripe; and an apparently
fluid layer between the follicular epithelium and the vitellus, which
coagulates in hardened specimens, is probably the last remnant of the
vitelline membrane. It is, however, much thicker than the corresponding
remnant in Scyllium.
Though I find the same membranes in Scyllium as Alexander Schultz did in
other Squalidæ, my results do not agree with his as to Raja. Torpedo I have
not investigated.
It appears to me probable that the ova in all Elasmobranch Fishes have at
some period of their development the two membranes described at length for
Scyllium. Of these the inner one, or zona radiata, will probably be
admitted on all hands to be a product of the peripheral protoplasm of the
egg.
The outer one corresponds with the membrane usually regarded in other
Vertebrates as a chorion or product of the follicular epithelium, but, by
tracing it back to its first origin, I have been led to reject this view of
its nature.
_The follicular epithelium._--The follicular epithelium in the eggs of Raja
and Acanthias has been described by Gegenbaur[382]. He finds it flat in
young eggs, but in the larger eggs of Acanthias more columnar, and with the
cells wedged in so as to form a double layer. These observations are
confirmed by Ludwig[383].
Footnote 382: _Loc. cit._
Footnote 383: _Loc. cit._
Alexander Schultz[384] states that in Torpedo, the eggs are at first
enclosed in a simple epithelium, but that in follicles of .008 mm. there
appear between the original large cells of the follicle (which he describes
as granulosa cells and derives from the germinal epithelium) a number of
peculiar small cells. He states that these are of the same nature as the
general stroma cells of the ovary, and believes that they originate in the
stroma. When the eggs have reached 0.1 - 0.15 mm., he finds that the small
and large cells have a very regular alternating arrangement.
Footnote 384: _Loc. cit._
Semper records but few observations on the follicular epithelium, but
describes in Raja the presence of a certain number of large cells amongst
smaller cells. He believes that they may develop into ova, and considers
them identical with the larger cells described by Schultz, whose
interpretations he does not, however, accept.
My own results accord to a great extent with those of Dr Schultz, as far as
the structure of the follicular epithelium is concerned, but I am at one
with Semper in rejecting Schultz's interpretations.
In Scyllium, as has already been mentioned, the follicular epithelium is at
first flat and formed of a single layer of uniform cells, each with a
considerable amount of clear protoplasm and a granular nucleus. It is
bounded externally by a delicate membrane--the membrana propria folliculi
of Waldeyer--and internally by the vitelline membrane. In the ovaries of
very young animals the cells of the follicular epithelium are more columnar
on the side towards the stroma than on the opposite side, but this
irregularity soon ceases to exist.
In many cases the nuclei of the cells of the follicular epithelium exhibit
a spindle modification, which shews that the growth of the follicular
epithelium takes place by the division of its cells. No changes of
importance are observable in the follicular epithelium till the egg has
reached a diameter of more than 1 mm.
It should here be stated that I have some doubts respecting the
completeness of the history of the epithelium recorded in the sequel.
Difficulties have been met with in completely elucidating the chronological
order of the occurrences, and it is possible that some points have escaped
my observation.
The first important change is the assumption of a palisade-like character
by the follicle cells, each cell becoming very narrow and columnar and the
nucleus oval (Pl. 25, fig. 28). In this condition the thickness of the
epithelium is about 0.025 mm. The epithelium does not, however, become
uniformly thick over the whole ovum, but in the neighbourhood of the
germinal vesicle it is very flat and formed of granular cells with
indistinct outlines, rather like the hypodermis cells of many Annelida.
Coincidently with this change in the follicular epithelium the commencement
of the atrophy of the membranes of the ovum, described in the last section,
becomes apparent.
The original membrana propria folliculi is still present round the
follicular epithelium, but is closely associated with a fibrous layer with
elongated nuclei. Outside this there is now a layer of cells, very much
like an ordinary epithelial layer, which may possibly be formed of cells of
the true germinal epithelium (fig. 28, _fe´_). This layer, which will be
spoken of as the secondary follicle layer, might easily be mistaken for the
follicular epithelium, and it is possible that it has actually been so
mistaken by Eimer, Clark, and Klebs, in Reptilia, and that the true
follicular epithelium (in a flattened condition) has been then spoken of as
the _Binnenepithel_.
In slightly older eggs the epithelial cells are no longer uniform or
arranged as a single layer. The general arrangement of these cells is shewn
in Pl. 25, fig. 29. A considerable number of them are more or less
flask-shaped, with bulky protoplasm prolonged into a thin stem directed
towards the vitelline membrane, with which, in many instances if not all,
it comes in contact. These larger cells are arranged in several tiers.
Intercalated between them are a number of elongated small cells with scanty
protoplasm and a deeply staining nucleus, not very dissimilar to, though
somewhat smaller than, the columnar cells of the previous stage. There is
present a complete series of cells intermediate between the larger cells
and those with a deeply stained nucleus, and were it not for the condition
of the epithelium in Raja, to be spoken of directly, I should not sharply
divide the cells into two categories. In surface views of the epithelium
the division into two kinds of cells would not be suspected. There can, it
appears to me, be no question that both varieties of cell are derived from
the primitive uniform follicle cells.
The fibrous layer bounding the membrana propria folliculi is thicker than
in the last stage, and the epithelial-like layer (_fe´_) which bounds it
externally is more conspicuous than before. Immediately adjoining it are
vascular and lymph sinuses. The thickness of the follicular epithelium at
this stage may reach as much as 0.04 mm., though I have found it sometimes
considerably flatter. The cells composing it are, however, so delicate that
it is not easy to feel certain that the peculiarities of any individual
ovum are not due to handling. The absence of the peculiar columnar
epithelium on the part of the surface adjoining the germinal vesicle is as
marked a feature as in the earlier stage. When the egg is nearly ripe, and
the vitelline membrane has been reduced to a mere remnant, the follicular
epithelium is still very columnar (Pl. 25, fig. 23). The thickness is
greater than in the last stage, being now about 0.045 mm., but the cells
appear only to form a single definite layer. From the character of their
nuclei, I feel inclined to regard them as belonging to the category of the
smaller cells of the previous stage, and feel confirmed in this view by
finding certain bodies in the epithelium, which have the appearance of
degenerating cells with granular nuclei, which I take to be the
flask-shaped cells which were present in the earlier stage.
I have not investigated the character of the follicular epithelium in the
perfectly ripe ovum ready to become detached from the ovary. Nor can I
state for the last-described stage anything about the character of the
follicular epithelium in the neighbourhood of the germinal vesicle.
As to the relation of the follicular epithelium to the vitelline membrane,
and the possible processes of its cells continued into the yolk, I can say
very little. I find in specimens teased out after treatment with osmic
acid, that the cells of the follicular epithelium are occasionally provided
with short processes, which might possibly have perforated the vitelline
membrane, but have met with nothing so clear as the teased out specimens
figured by Eimer. Nothing resembling the cells within the vitelline
membrane, as described by His[385] in Osseous Fish, and Lindgren in
Mammalia, has been met with[386].
Footnote 385: _Das Ei bei Knochenfischen._
Footnote 386: _Arch. f. Anat. Phys._ 1877.
My observations in Raja are not so full as those upon Scyllium, but they
serve to complete and reconcile the observations of Semper and Schultz, and
also to shew that the general mode of growth of the follicular epithelium
is fundamentally the same in my representatives of the two divisions of the
Elasmobranchii. In very young eggs, in conformity with the results of all
previous observers, I find the follicular epithelium approximately uniform.
The cells are flat, but extended so as to appear of an unexpected size in
views of the surface of the follicle. This condition does not, however,
last very long. A certain number of the cells enlarge considerably, others
remaining smaller and flat. The differences between the larger and the
smaller cells are more conspicuous in sections than in surface views, and
though the distribution of the cells is somewhat irregular, it may still be
predicted as an almost invariable rule that the smaller cells of the
follicle will line that part of the surface of the ovum, near to which the
germinal vesicle is situated. On Pl. 25, fig. 30, is shewn in section a
fairly average arrangement of the follicle cells. Semper considers the
larger cells of such a follicle to be probably primitive ova destined to
become permanent ova. This view I cannot accept: firstly, because these
cells only agree with primitive ova in being exceptionally large--the
character of their nucleus, with its large nucleolus, being not very like
that of a primitive ovum. Secondly, because they shade into ordinary cells
of the follicle; and thirdly, because no evidence of their becoming ova has
come before me, but rather the reverse, in that it seems probable that they
have a definite function connected with the nutrition of the egg. To this
point I shall return.
In the next stage the small cells have become still smaller. They are
columnar, and are wedged in between the larger ones. No great regularity in
distribution is as yet attained (Pl. 25, fig. 31). Such a regularity
appears in a later stage (Pl. 25, fig. 32), which clearly corresponds with
fig. 8 on Pl. 34 of Schultz's paper, and also with the stage of Scyllium in
Pl. 25, fig. 29, though the distinction between the two kinds of cells is
here far better marked than in Scyllium. The big cells have now become
flask-shaped like those in Scyllium, and send a process down to the
vitelline membrane. The smaller cells are arranged in two or three tiers,
but the larger cells in a single layer. The distribution of the larger and
smaller cells is in some instances very regular, as shewn in the surface
view on Pl. 25, fig. 33. There can, it appears to me, be no doubt that
Schultz's view of the smaller cells being lymph-cells which have migrated
into the follicle cannot be maintained.
The thickness of the epithelium at this stage is about 0.04 mm. In the
succeeding stages, during which the egg is rapidly growing to the colossal
size which it eventually attains, the follicular epithelium does not to any
great extent alter in constitution. It grows thicker on the whole, and as
the vitelline membrane gradually atrophies, its lower surface becomes
irregular, exhibiting somewhat flattened prominences, which project into
the yolk. At the greatest height of the prominences the epithelium may
reach a thickness of 0.06 mm., or even more. The arrangement of the tissues
external to the follicular epithelium is the same in Raja as in Scyllium.
The most interesting point connected with the follicle, both in Scyllium
and Raja and presumably in other Elasmobranchii is that its epithelium at
the time when the egg is rapidly approaching maturity is composed with more
or less of distinctness of two forms of cells. One of these is large
flask-shaped and rich in protoplasm, the other is small, consisting of a
mere film of protoplasm round a nucleus. Considering that the larger cells
appear at the time of rapid growth, it is natural to interpret their
presence as connected with the nutrition of the ovum. This view is
supported by the observations of Eimer and Braun, on the development of
Reptilian ova. In many Reptilian ova it appears from Eimer's[387]
observations, that the follicular epithelium becomes several layers thick,
and that a differentiation of the cells, similar to that in Elasmobranchii,
takes place. The flask-shaped cells eventually undergo peculiar changes,
becoming converted into a kind of beaker-cell, with prolongations through
the egg membranes, which take the place of canals leading to the interior
of the egg. Braun also expresses himself strongly in favour of the
flask-shaped cells functioning in the nutrition of the egg[388]. That these
cells in the Reptilian ova really correspond with those in Elasmobranchii
appears to me clear from Eimer's figures, but I have not myself studied any
Reptilian ovum. My reasons for dissenting from both Semper's and Schultz's
views on the nature of the two forms of follicular cells have already been
stated.
Footnote 387: _Archiv f. mikr. Anat._ Vol. VIII.
Footnote 388: Braun, "Urogenitalsystem d. Amphibien,"
_Arbeiten a. d. zool.-zoot. Institut Würzburg_, Bd. IV. He
says, in reference to the flask-shaped cell, p. 166, "Höchstens
würde ich die Funktion der grossen Follikelzellen als
_einzellige Drüsen_ mehr betonen."
_The Vitellus and the development of the yolk spherules._--Leydig,
Gegenbaur, and Schultz, have recorded important observations on this head.
Leydig[389] chiefly describes the peculiar characters of the yolk
spherules.
Footnote 389: _Loc. cit._
Gegenbaur[390] finds in the youngest eggs fine granules, which subsequently
develop into vesicles, in the interior of which the solid oval spheres, so
characteristic of Elasmobranchii, are developed.
Footnote 390: _Loc. cit._
Schultz describes in the youngest ova of Torpedo the minute yolk spherules
arranged in a semilunar form around the eccentric germinal vesicle. In
older ova they spread through the whole. He also gives a description of
their arrangement in the ripe ovum. Dr Schultz further finds in the body of
the ovum peculiar protoplastic striæ, arranged as a series of pyramids,
with the bases directed outwards. In the periphery of the ovum a
protoplastic network is also present, which is continuous with the
above-mentioned pyramidal structures.
My observations do not very greatly extend those of Gegenbaur and Schultz
with reference to the development of the yolk, and closely agree with what
Gegenbaur has given in the paper above quoted more fully for Aves and
Reptilia than for Elasmobranchii.
In very young ova the body of the ovum is simply granular, but when it has
reached about 0.5 mm. the granules are seen to be arranged in a kind of
network, or sponge-work (Pl. 25, fig. 21), already spoken of in my
monograph on Elasmobranch Fishes.
This network becomes more distinct in succeeding stages, especially in
chromic acid specimens (Pl. 25, fig. 22), probably in part owing to a
granular precipitation of the protoplasm. In the late stages, when the yolk
spherules are fully developed, it is difficult to observe this network,
but, as has been shewn in my monograph above quoted, it is still present
after the commencement of embryonic development. An arrangement of the
protoplasmic striæ like that described by Schultz has not come under my
notice.
The development of the yolk appears to me to present special difficulties,
owing to the fact pointed out by His[391] that the conditions of
development vary greatly according to whether the ovary is in a state of
repose or of active development. I do not feel satisfied with my results on
this subject, but believe there is still much to be made out. Observations
on the yolk spherules may be made either in living ova, in ova hardened in
osmic acid, or in ova hardened in picric or chromic acids. The two latter
reagents, as well as alcohol, are however unfavourable for the purpose of
this study, since by their action the yolk spherules appear frequently to
be broken up and otherwise altered. This has to some extent occurred in
Pl. 25, fig. 21, and the peculiar appearance of the yolk of this ovum is in
part due to the action of the reagent. On the whole I have found osmic acid
the most suitable reagent for the study of the yolk, since without breaking
up the developing spherules, it stains them of a deep black colour. The
yolk spherules commence to be formed in ova, of not more than 0.06 mm. in
the ovaries of moderately old females. In young females they are apparently
not formed in such small ova. They arise as extremely minute, highly
refracting particles, in a stratum of protoplasm _some little way below the
surface, and are always most numerous at the pole opposite the germinal
vesicle_. Their general arrangement is very much that figured and described
by Allen Thomson in Gasterosteus[392], and by Gegenbaur and Eimer in young
Reptilian ova. In section they naturally appear as a ring, their general
mode of distribution being fairly typically represented on Pl. 25, fig. 27.
The ovum represented in fig. 27 was 0.5 mm. in diameter, and the yolk
spherules were already largely developed; in smaller ova they are far less
numerous, though arranged in a similar fashion. The developing yolk
spherules are not uniformly distributed but are collected in peculiar
little masses or aggregations (Pl. 25, fig. 21). These resemble the
granular masses, figured by His (_loc. cit._ Pl. 4, fig. 33) in the Salmon,
and may be compared with the aggregations figured by Götte in his monograph
on _Bombinator igneus_ (Pl. 1, fig. 9). It deserves to be especially noted,
that when the yolk spherules are first formed, the _peripheral layer of the
ovum_ is entirely free from them, a feature which is however apt to be lost
in ova hardened in picric acid (Pl. 25, fig. 21). Two points about the
spherules appear clearly to point to their being developed in the
protoplasm of the ovum, and not in the follicular epithelium. (1) That they
do not make their appearance in the superficial stratum of the ovum. (2)
That no yolk spherules are present in the cells of the follicular
epithelium, in which they could not fail to be detected, owing to the deep
colour they assume on being treated with osmic acid.
Footnote 391: _Das Ei bei Knochenfischen._
Footnote 392: "Ovum" in Todd's _Encyclopædia_, fig. 69.
It need scarcely be said that the yolk spherules at this stage are not
cells, and have indeed no resemblance to cells. They would probably be
regarded by His as spherules of fatty material, unrelated to the true food
yolk.
As the ova become larger the granules of the peripheral layer before
mentioned gradually assume the character of the yolk spheres of the adult,
and at the same time spread towards the centre of the egg. Not having
worked at fresh specimens, I cannot give a full account of the growth of
the spherules; but am of opinion that Gegenbaur's account is probably
correct, according to which the spheres at first present gradually grow and
develop into vesicles, in the interior of which solid bodies (nuclei of
His?) appear and form the permanent yolk spheres. When the yolk spheres are
still very small they have the typical oblong form[393] of the ripe ovum,
and this form is acquired while the centre of the ovum is still free from
them.
Footnote 393: The peculiar oval, or at times slightly
rectangular and striated yolk spherules of Elasmobranchii are
mentioned by Leydig and Gegenbaur (Pl. 11, fig. 20), and
myself, _Preliminary Account of Development of Elasmobranch
Fishes_, and by Filippi and His in _Osseous Fishes_.
The growth of the yolk appears mainly due to the increase in size and
number of the individual yolk spheres. Even when the ovum is quite filled
with large yolk spheres, the granular protoplastic network of the earlier
stages is still present, and serves to hold together the constituents of
the yolk. In the cortical layer of nearly ripe ova, the yolk has a somewhat
different character to that which it exhibits in the deeper layers, chiefly
owing to the presence of certain delicate granular (in hardened specimens)
bodies, whose nature I do not understand, and to special yolk spheres
rather larger than the ordinary, provided with numerous smaller spherules
in their interior, which are probably destined in the course of time to
become free and to form ordinary yolk spheres.
The mode of formation of the yolk spheres above described appears to me to
be the normal, and possibly the only one. Certain peculiar structures have,
however, come under my notice, which may perhaps be connected with the
formation of the yolk. One of these resembles the bodies described by
Eimer[394] as "Dotterschorfe." I have only met these bodies in a single
instance in ova of 0.6 mm., from the ovary (in active growth) of a specimen
of _Scy. canicula_ 23 inches in length. In this instance they consisted of
homogeneous clear bodies (not bounded by any membrane) of somewhat
irregular shape, though usually more or less oval, and rarely more than
0.02 mm. in their longest diameter. They were very numerous in the
peripheral layer of the ovum, but quite absent in the centre, and also not
found outside the ovum (as they appear to be in Reptilia). Yolk granules
formed in the normal way, and staining deeply by osmic acid, were present,
but the "Dotterschorfe" presented a marked contrast to the remainder of the
ovum, in being absolutely unstained by osmic acid, and indeed they appeared
more like a modified form of vacuole than any definite body. Their general
appearance in Scyllium may be gathered from Eimer's figure 8, Pl. 11,
though they were much more numerous than represented in that figure, and
confined to the periphery of the ovum.
Footnote 394: "Untersuchung über die Eier d. Reptilien,"
_Archiv f. mikros. Anat._ Vol. VIII.
Dr Eimer describes a much earlier condition of these structures, in which
they form a clear shell enclosing a central dark nucleus. This stage I have
not met with, nor can I see any grounds for connecting these bodies with
the formation of the yolk, and the fact of their not staining with osmic
acid is strongly opposed to this view of their function. Dr Eimer does not
appear to me to bring forward any satisfactory proof that they are in any
way related to the formation of the yolk, but wishes to connect them with
the peculiar body, well known as the yolk nucleus, which is found in the
Amphibian ovum[395].
Footnote 395: Vide Allen Thomson, article "Ovum," Todd's
_Encyclopædia_, p. 95.
Another peculiar body found in the ova may be mentioned here, though it
more probably belongs to the germinal vesicle than to the yolk. It has only
been met with in the vitellus of some of the medium sized ova of a young
female. Examples of this body are represented on Pl. 25, fig. 25A, _x_. As
a rule there is only one in each of the ova in which they are present, but
there may be as many as four. They consist of small vesicles with a very
thick doubly contoured membrane, which are filled with numerous deeply
staining spherical granules. At times they contain a vacuole. Some of the
larger of them are not very much smaller than the germinal vesicle of their
ovum, while the smallest of them present a striking resemblance to the
nucleoli (fig. 25B), which makes me think that they may possibly be
nucleoli which have made their way out of the germinal vesicle. I have not
found them in the late stages or large ova.
The following measurements shew the size of some of these bodies in
relation to the germinal vesicle and ovum:--
Diameter of Germinal Diameter of Body in
Diameter of Ovum. Vesicle. Vitellus.
0.096 mm. 0.03 mm. 0.009 mm.
0.064 mm. 0.025 mm. 0.012 mm.
{0.019 mm.
0.096 mm. 0.03 mm {0.003 mm.
_Germinal vesicle._--Gegenbaur[396] finds the germinal vesicle completely
homogeneous and without the trace of a germinal spot. In Raja granules or
vesicles may appear as artificial products, and in Acanthias even in the
fresh condition isolated vesicles or masses of such may be present. To
these structures he attributes no importance.
Footnote 396: _Loc. cit._
Alexander Schultz[397] states that there is nothing remarkable in the
germinal vesicle of the Torpedo egg, but that till the egg reaches 0.5 mm.,
a single germinal spot is always present (measuring about 0.01 mm.), which
is absent in larger ova.
Footnote 397: _Loc. cit._
The bodies described by Gegenbaur are now generally recognised as germinal
spots, and will be described as such in the sequel. I have very rarely met
with the condition with the single nucleolus described by Schultz in
Torpedo.
My own observations are confined to Scyllium. In very young females, with
ova not larger than 0.09 mm., the germinal vesicle has the same characters
as during the embryonic periods. The contents are clear but traversed by a
very distinct and deeply staining reticulum of fibres connected with the
several nucleoli which are usually present and situated close to the
membrane.
In a somewhat older female in the largest ova of about 0.12 mm., the
germinal vesicle measures about 0.06 mm., and usually occupies an eccentric
position. It is provided with a distinct though delicate membrane. The
network, so conspicuous during the embryonic period, is not so clear as it
was, and has the appearance of being formed of lines of granules rather
than of fibres. The fluid contents of the nucleus remain as a rule, even in
the hardened specimens, perfectly clear, though they become in some
instances slightly granular. There are usually two, three, or more nucleoli
generally situated, as described by Eimer, close to the membrane of the
vesicle, the largest of which may measure as much as 0.006 mm. They are
highly refracting bodies, containing in most instances a vacuole, and very
frequently a smaller spherical body of a similar nature to themselves[398].
Granules are sometimes also present in the germinal vesicle, but are
probably only extremely minute nucleoli.
Footnote 398: Compare, with reference to several points, the
germinal vesicle at this stage with the germinal vesicle of the
frog's ovum figured by O. Hertwig, _Morphologisches Jahrbuch_,
Vol. III. pl. 4, fig. 1.
In ova of 0.5 mm. the germinal vesicle has a diameter of 0.12 mm. (Pl. 25,
fig. 21). It is usually shrunk in hardened specimens though nearly
spherical in the living ovum. Its contents are rendered granular by
reagents though quite clear when fresh, and the reticulum of the earlier
stages is sometimes with difficulty to be made out, though in other
instances fairly clear. In all cases the fibres composing it are very
granular. The membrane is thick. Peculiar highly refracting nucleoli,
usually enclosing a large vacuole, are present in considerable numbers, and
are either arranged in a circle round the periphery, or sometimes
aggregated towards one side of the vesicle; and in addition, numerous
deeply staining smaller granular aggregations, probably belonging to the
same category as the nucleoli (from which in the living ovum they can only
be distinguished by their size), are scattered close to the inner side of
the membrane over the whole or only a part of the surface of the germinal
vesicle. In a fair number of instances bodies like that figured on Pl. 25,
fig. 27, are to be found in the germinal vesicle. They appear to be
nucleoli in which a number of smaller nucleoli are originating by a process
of endogenous growth, analogous perhaps to endogenous cell-formation. The
nucleoli thus formed are, no doubt, destined to become free. The above mode
of increase for the nucleoli appears to be exceptional. The ordinary mode
is, no doubt, that by simple division into two, as was long ago shewn by
Auerbach.
Of the later stages of the germinal vesicle and its final fate, I can give
no account beyond the very fragmentary statements which have already
appeared in my monograph on Elasmobranch Fishes.
_Formation of fresh ova and ovarian nests in the post-embryonic
stages._--Ludwig[399] was the first to describe the formation of ova in the
post-embryonic periods. His views will be best explained by quoting the
following passage:--
"The follicle of Skates and Dog-fish, with the ovum it contains, is to
be considered as an aggregation of the cells of the single-layered
ovarian epithelium which have grown into the stroma, and of which one
cell has become the ovum and the others the follicular epithelium. The
follicle, however, draws in with it into the stroma a number of
additional epithelial cells in the form of a stalk connecting the
follicle with the superficial epithelium. At a later period the lower
part of the stalk at its junction with the follicle becomes
continuously narrowed, and at the same time a rupture takes place in
the cells which form it. In this manner the follicle becomes at last
constricted off from the stalk, and so from its place of origin in the
superficial epithelium, and subsequently lies freely in the stroma of
the ovary."
Footnote 399: _Loc. cit._
He further explains that the separation of the follicles from the
epithelium takes place much earlier in Acanthias than in Raja, and that the
sinkings of the epithelium into the stroma may have two or three branches
each with a follicle.
Semper gives very little information with reference to the post-embryonic
formation of ova. He expresses his agreement on the whole with Ludwig, but,
amongst points not mentioned by Ludwig, calls attention to peculiar
aggregations of primitive ova in the superficial epithelium, which he
regards as either rudimentary testicular follicles or as nests similar to
those in the embryo.
My observations on this subject do not agree very closely with those either
of Ludwig or Semper. The differences between us partly, though not
entirely, depend upon the fundamentally different views we hold about the
constitution of the ovary and the nature of the epithelium covering it
(vide pp. 555 and 556).
In very young ovaries (Pl. 24, fig. 8) nests of ova (in my sense of the
term) are very numerous, but though usually superficial in position are
also found in the deeper layers of the ovary. They are especially
concentrated in their old position, close to the dorsal edge of the organ.
In some instances they do not present quite the same appearance as in the
embryo, owing to the outlines of the ova composing them being distinct, and
to the presence between the ova of numerous interstitial cells derived from
the germinal epithelium, and destined to become follicular epithelium.
These latter cells at first form a much flatter follicular epithelium than
in the embryonic periods, so that the smaller adult ova have a much less
columnar investment than ova of the same size in the embryo. A few
primitive ova may still be found in a very superficial position, but
occasionally also in the deeper layers. I am inclined to agree with Semper
that some of these are freshly formed from the cells of the germinal
epithelium.
In the young female with ova of about 0.5 mm. nests of ova are still fairly
numerous. The nests are characteristic, and present the various remarkable
peculiarities already described in the embryo. In many instances they form
polynuclear masses, not divided into separate cells, generally, however,
the individual ova are distinct. The ova in these nests are on the average
rather smaller than during the embryonic periods. The nests are frequently
quite superficial and at times continuous with the pseudo-epithelium, and
individual ova also occasionally occupy a position in the superficial
epithelium. Some of the appearances presented by separate ova are not
unlike the figures of Ludwig, but a growth such as he describes has,
according to my observations, no existence. The columns which he believes
to have grown into the stroma are merely trabeculæ connecting the deeper
and more superficial parts of the germinal epithelium; and his whole view
about the formation of the follicular epithelium round separate ova
certainly does not apply, except in rare cases, to Scyllium. It is, indeed,
very easy to see that most freshly formed ova are derived from nests, as in
the embryo; and the formation of a follicular epithelium round these ova
takes place as they become separated from the nests. A few solitary ova,
which have never formed part of a nest, seem to be formed in this stage as
in the embryo; but they do not grow into the stroma surrounded by the cells
of the pseudo-epithelium, and only as they reach a not inconsiderable size
is a definite follicular epithelium formed around them. The follicular
epithelium, though not always formed from the pseudo-epithelium, is of
course always composed of cells derived from the germinal epithelium.
In all the ova formed at this stage the nucleus would seem to pass through
the same metamorphosis as in the embryo.
In the later stages, and even in the full-grown female of Scyllium, fresh
ova seemed to be formed and nests also to be present. In Raja I have not
found freshly formed ova or nests in the adult, and have had no opportunity
of studying the young forms.
_Summary of observations on the development of the ovary in Scyllium and
Raja._
(1) The ovary in the embryo is a ridge, triangular in section, attached
along the base. It is formed of a core of stroma and a covering of
epithelium. A special thickening of the epithelium on the outer side forms
the true germinal epithelium, to which the ova are confined (Pl. 24,
fig. 1). In the development of the ovary the stroma becomes differentiated
into an external vascular layer, especially developed in the neighbourhood
of the germinal epithelium, and an internal lymphatic portion, which forms
the main mass of the ovarian ridge (Pl. 24, figs. 2, 3, and 6).
(2) At first the thickened germinal epithelium is sharply separated by a
membrane from the subjacent stroma (Pl. 24, figs. 1, 2, and 3), but at
about the time when the follicular epithelium commences to be formed round
the ova, numerous strands of stroma grow into the epithelium, and form a
regular network of vascular channels throughout it, and partially isolate
individual ova (Pl. 24, figs. 7 and 8). At the same time the surface of the
epithelium turned towards the stroma becomes irregular (Pl. 24, fig. 9),
owing to the development of individual ova. In still later stages the
stroma ingrowths form a more or less definite tunic close to the surface of
the ovary. External to this tunic is the superficial layer of the germinal
epithelium, which forms what has been spoken of as the pseudo-epithelium.
In many instances the protoplasm of its cells is produced into peculiar
fibrous tails which pass into the tunic below.
(3) _Primitive ova._--Certain cells in the epithelium lining the dorsal
angle of the body-cavity become distinguished as primitive ova by their
abundant protoplasm and granular nuclei, at a very early period in
development, even before the formation of the genital ridges. Subsequently
on the formation of the genital ridges these ova become confined to the
thickened germinal epithelium on the outer aspect of the ridges (Pl. 24,
fig. 1).
(4) _Conversion of primitive ova into permanent ova._--Primitive ova may in
Scyllium become transformed into permanent ova in two ways--the difference
between the two ways being, however, of secondary importance.
(_a_) A nest of primitive ova makes its appearance, either by continued
division of a single primitive ovum or otherwise. The bodies of all the ova
of the nest fuse together, and a polynuclear mass is formed, which
increases in size concomitantly with the division of its nuclei. The
nuclei, moreover, pass through a series of transformations. They increase
in size and form delicate vesicles filled with a clear fluid, but contain
close to one side a granular mass which stains very deeply with colouring
reagents. The granular mass becomes somewhat stellate, and finally assumes
a reticulate form with one more highly refracting nucleoli at the nodal
points of the reticulum. When a nucleus has reached this condition the
protoplasm around it has become slightly granular, and with the enclosed
nucleus is segmented off from the nest as a special cell--a permanent ovum
(figs. 13, 14, 15, 16). Not all the nuclei in a nest undergo the whole of
the above changes; certain of them, on the contrary, stop short in their
development, atrophy, and become employed as a kind of pabulum for the
remainder. Thus it happens that out of a large nest perhaps only two or
three permanent ova become developed.
(_b_) In the second mode of development of ova the nuclei and protoplasm
undergo the same changes as in the first mode; but the ova either remain
isolated and never form part of a nest, or form part of a nest in which no
fusion of the protoplasm takes place, and all the primitive ova develop
into permanent ova. Both the above modes of the formation continue through
a great part of life.
(5) _The follicle._--The cells of the germinal epithelium arrange
themselves as a layer around each ovum, almost immediately after its
separation from a nest, and so constitute a follicle. They are at first
flat, but soon become more columnar. In Scyllium they remain for a long
time uniform, but in large eggs they become arranged in two or three
layers, while at the same time some of them become large and flask-shaped,
and others small and oval (fig. 29). The flask-shaped cells have probably
an important function in the nutrition of the egg, and are arranged in a
fairly regular order amongst the smaller cells. Before the egg is quite
ripe both kinds of follicle cells undergo retrogressive changes (Pl. 25,
fig. 23).
In Raja a great irregularity in the follicle cells is observable at an
early stage, but as the ovum grows larger the cells gradually assume a
regular arrangement more or less similar to that in Scyllium (Pl. 25, figs.
30-33).
(6) _The egg membranes._--Two membranes are probably always present in
Elasmobranchii during some period of their growth. The first formed and
outer of these arises in some instances before the formation of the
follicular epithelium, and would seem to be of the nature of a vitelline
membrane. The inner one is the zona radiata with a typical radiately
striated structure. It is formed from the vitellus at a much later period
than the proper vitelline membrane. It is more developed in Scyllium than
in Raja, but atrophies early in both genera. By the time the ovum is nearly
ripe both membranes are very much reduced, and when the egg (in Scyllium
and Pristiurus) is laid, no trace of any membrane is visible.
(7) _The vitellus._--The vitellus is at first faintly granular, but at a
later period exhibits a very distinct (protoplasmic) network of fibres,
which is still present after the ovum has been laid.
The yolk arises, in the manner described by Gegenbaur, in ova of about
0.06 mm. as a layer of fine granules, which stain deeply with osmic acid.
They are at first confined to a stratum of protoplasm slightly below the
surface of the ovum, and are most numerous at the pole furthest removed
from the germinal vesicle. They are not regularly distributed, but are
aggregated in small masses. They gradually grow into vesicles, in the
interior of which oval solid bodies are developed, which form the permanent
yolk-spheres. These oval bodies in the later stages exhibit a remarkable
segmentation into plates, which gives them a peculiar appearance of
transverse striation.
Certain bodies of unknown function are occasionally met with in the
vitellus, of which the most remarkable are those figured at _x_ on Pl. 25,
fig. 25A.
(8) _The germinal vesicle._--A reticulum is very conspicuous in the
germinal vesicle in the freshly formed ova, but becomes much less so in
older ova, and assumes, moreover, a granular appearance. At first one to
three nucleoli are present, but they gradually increase in number as the
germinal vesicle grows older, and are frequently situated in close
proximity to the membrane.
THE MAMMALIAN OVARY (Pl. 26).
The literature of the mammalian ovary has been so often dealt with that it
may be passed over with only a few words. The papers which especially call
for notice are those of Pflüger[400], Ed. van Beneden[401], and especially
Waldeyer[402], as inaugurating the newer view on the nature of the ovary,
and development of the ova; and of Foulis[403] and Kölliker[404], as
representing the most recent utterances on the subject. There are, of
course, many points in these papers which are touched on in the sequel, but
I may more especially here call attention to the fact that I have been able
to confirm van Beneden's statement as to the existence of polynuclear
protoplasmic masses. I have found them, however, by no means universal or
primitive; and I cannot agree in a general way with van Beneden's account
of their occurrence. I have found no trace of a germogene (Keimfache) in
the sense of Pflüger and Ed. van Beneden. My own results are most in
accordance with those of Waldeyer, with whom I agree in the fundamental
propositions that both ovum and follicular epithelium are derived from the
germinal epithelium, but I cannot accept his views of the relation of the
stroma to the germinal epithelium.
Footnote 400: _Die Eierstöcke d. Säugethiere u. d. Menschen_,
Leipzig, 1863.
Footnote 401: "Composition et Signification de l'oeuf," _Acad.
r. de Belgique_, 1868.
Footnote 402: _Eierstock u. Ei._ Leipzig, 1870.
Footnote 403: _Trans. of Royal Society, Edinburgh_, Vol. XXVII.
1875, and _Quarterly Journal of Microscopical Science_,
Vol. XVI.
Footnote 404: _Verhandlung d. Phys. Med. Gesellschaft_,
Würzburg, 1875, N. F. Bd. VIII.
In the very interesting paper of Foulis, the conclusion is arrived at, that
while the ova are derived from the germinal epithelium, the cells of the
follicle originate from the ordinary connective tissue cells of the stroma.
Foulis regards the zona pellucida as a product of the ovum and not of the
follicle. To both of these views I shall return, and hope to be able to
shew that Foulis has not traced back the formation of the follicle through
a sufficient number of the earlier stages. It thus comes about that though
I fully recognise the accuracy of his figures, I am unable to admit his
conclusions. Kölliker's statements are again very different from those of
Foulis. He finds certain cords of cells in the hilus of the ovary, which he
believes to be derived from the Wolffian body, and has satisfied himself
that they are continuous with Pflüger's egg-tubes, and that they supply the
follicular epithelium. To the general accuracy of Kölliker's statements
with reference to the relations of these cords in the hilus of the ovary I
can fully testify, but am of opinion that he is entirely mistaken as to
their giving rise to the follicular epithelium, or having anything to do
with the ova. I hope to be able to give a fuller account of their origin
than he or other observers have done.
My investigations on the mammalian ovary have been made almost entirely on
the rabbit--the type of which it is most easy to procure a continuous
series of successive stages; but in a general way my conclusions have been
controlled and confirmed by observations on the cat, the dog, and the
sheep. My observations commence with an embryo of eighteen days. A
transverse section, slightly magnified, through the ovary at this stage, is
represented on Pl. 26, fig. 35, and a more highly magnified portion of the
same in fig. 35A. The ovary is a cylindrical ridge on the inner side of the
Wolffian body, composed of a superficial epithelium, the germinal
epithelium (_g.e._), and of a tissue internal to this, which forms the main
mass of it. In the latter two constituents have to be distinguished--(1) an
epithelial-like tissue (_t_), coloured brown, which forms the most
important element, and (2) vascular and stroma elements in this.
The germinal epithelium is a layer about 0.03 - 0.04 mm. in thickness. It
is (vide fig. 35A, _g.e._) composed of two or three layers of cells, with
granular nuclei, of which the outermost layer is more columnar than the
remainder, and has elongated rather than rounded nuclei. Its cells, though
they vary slightly in size, are all provided with a fair amount of
protoplasm, and cannot be divided (as in the case of the germinal
epithelium of Birds, Elasmobranchii, &c.), into primitive ova, and normal
epithelial cells. Very occasionally, however, a specially large cell,
which, perhaps, deserves the appellation primitive ovum, may be seen. From
the subjacent tissue the germinal epithelium is in most parts separated by
a membrane-like structure (fluid coagulum); but this is sometimes absent,
and it is then very difficult to determine with exactness the inner border
of the epithelium. The tissue (_t_), which forms the greater mass of the
ovary at this stage, is formed of solid columns or trabeculæ of
epithelial-like cells, which present a very striking resemblance in size
and character to the cells of the germinal epithelium. The protoplasm of
these cells stains slightly more deeply with osmic acid than does that of
the cells of the germinal epithelium, so that it is rather easier to note a
difference between the two tissues in osmic acid than in picric acid
specimens. This tissue approaches very closely, and is in many parts in
actual contact with the germinal epithelium. Between the columns of it are
numerous vascular channels (shewn diagrammatically in my figures) and a few
normal stroma cells. This remarkable tissue continues visible through the
whole course of the development of the ovary, till comparatively late in
life, and during all the earlier stages might easily be supposed to be
about to play some part in the development of the ova, or even to be part
of the germinal epithelium. It really, however, has nothing to do with the
development of the ova, as is easily demonstrated when the true ova begin
to be formed. In the later stages, as will be mentioned in the description
of those stages, it is separated from the germinal epithelium by a layer of
stroma; though at the two sides of the ovary it is, even in later stages,
sometimes in contact with the germinal epithelium.
In most parts this tissue is definitely confined within the limits of the
ovary, and does not extend into the mesentery by which the ovary is
attached. It may, however, be traced _at the anterior end_ of the ovary
into connection with the walls of the Malpighian bodies, which lie on the
inner side of the Wolffian body (vide fig. 35B), and I have no doubt that
it grows out from the walls of these bodies into the ovary. In the male it
appears to me to assist in forming, together with cells derived from the
germinal epithelium, the seminiferous tubules, the development of which is
already fairly advanced by this stage. I shall speak of it in the sequel as
tubuliferous tissue. The points of interest in connection with it concern
the male sex, which I hope to deal with in a future paper, but I have no
hesitation in identifying it with the segmental cords (_segmentalstränge_)
discovered by Braun in Reptilia, and described at length in his valuable
memoir on their urogenital system[405]. According to Braun the segmental
cords in Reptilia are buds from the outer walls of the Malpighian bodies.
The bud from each Malpighian body grows into the genital ridge before the
period of sexual differentiation, and sends out processes backwards and
forwards, which unite with the buds from the other Malpighian bodies. There
is thus formed a kind of trabecular work of tissue in the stroma of the
ovary, which in the Lacertilia comes into connection with the germinal
epithelium in both sexes, but in Ophidia in the male only. In the female,
in all cases, it gradually atrophies and finally vanishes, but in the male
there pass into it the primitive ova, and it eventually forms, with the
enclosed primitive ova, the tubuli seminiferi. From my own observations in
Reptilia I can fully confirm Braun's statements as to the entrance of the
primitive ova into this tissue in the male, and the conversion of it into
the tubuli seminiferi. The chief difference between Reptilia and Mammalia,
in reference to this tissue, appears to be that in Mammalia it arises only
from a few of the Malpighian bodies at the anterior extremity of the ovary,
but in Reptilia from all the Malpighian bodies adjoining the genital ridge.
More extended observations on Mammalia will perhaps shew that even this
difference does not hold good.
Footnote 405: _Arbeiten a. d. Zool.-zoot. Institut Würzburg_,
Bd. IV.
It is hardly to be supposed that this tissue, which is so conspicuous in
all young ovaries, has not been noticed before; but the notices of it are
not so numerous as I should have anticipated. His[406] states that the
parenchyma of the sexual glands undoubtedly arises from the Wolffian
canals, and adds that while the cortical layer (Hulle) represents the
earlier covering of a part of the Wolffian body, the stroma of the hilus,
with its vessels, arises from a Malpighian body. In spite of these
statements of His, I still doubt very much whether he has really observed
either the tissue I allude to or its mode of development. In any case he
gives no recognisable description or figure of it.
Footnote 406: _Archiv f. mikros. Anat._ Vol. I. p. 160.
Waldeyer[407] notices this tissue in the dog, cat, and calf. The following
is a free translation of what he says, (p. 141):--"In a full grown but
young dog, with numerous ripe follicles, there were present in the vascular
zone of the ovary numerous branched elongated small columns (Schläuche) of
epithelial cells, between which ran blood-vessels. They were only separated
from the egg columns of the cortical layer by a row of large follicles.
There can be no doubt that we have here remains of the sexual part of the
Wolffian body--the canals of the parovarium--which in the female sex have
developed themselves to an extraordinary extent into the stroma of the
sexual gland, and perhaps are even to be regarded as _homologues of the
seminiferous tubules_ (the italics are my own). I have almost always found
the above condition in the dog, only in old animals these seminiferous
canals seem gradually to atrophy. Similar columns are present in the cat,
only they do not appear to grow so far into the stroma." Identical
structures are also described in the calf.
Footnote 407: _Loc. cit._
Romiti gives a very similar description to Waldeyer of these bodies in the
dog[408]. Born also describes this tissue in young and embryonic ovaries of
the horse as the _Keimlager_[409]. The columns described by Kölliker[410]
and believed by him to furnish the follicular epithelium, are undoubtedly
my tubuliferous tissue, and, as Kölliker himself points out, are formed of
the same tissue as that described by Waldeyer.
Footnote 408: _Archiv f. mikr. Anat._ Vol. X.
Footnote 409: _Archiv f. Anatomie, Physiologie, u. Wiss.
Medicin._ 1874.
Footnote 410: _Loc. cit._
Egli gives a very clear and accurate description of this tissue, though he
apparently denies its relation with the Wolffian body.
My own interpretation of the tissue accords with that of Waldeyer. In
addition to the rabbit, I have observed it in the dog, cat, and sheep. In
all these forms I find that close to the attachment of the ovary, and
sometimes well within it, a fair number of distinct canals with a large
lumen are present, which are probably to be distinguished from the solid
epithelial columns. Such large canals are not as a rule present in the
rabbit. In the dog solid columns are present in the embryo, but later they
appear frequently to acquire a tubular form, and a lumen. Probably there
are great variations in the development of the tissue, since in the cat
(not as Waldeyer did in the dog) I have found it most developed.
In the very young embryonic ovary of the cat the columns are very small and
much branched. In later embryonic stages they are frequently elongated,
sometimes convoluted, and are very similar to the embryonic tubuli
seminiferi. In the young stages these columns are so similar to the egg
tubes (which agree more closely with Pflüger's type in the cat than in
other forms I have worked at) that to any one who had not studied the
development of the tissue an embryo cat's ovary at certain stages would be
a very puzzling object. I have, however, met with nothing in the cat or any
other form which supports Kölliker's views.
My next stage is that of a twenty-two days' embryo. Of this stage I have
given two figures corresponding to those of the earlier stage (figs. 36 and
36A).
From these figures it is at once obvious that the germinal epithelium has
very much increased in bulk. It has a thickness 0.1 - 0.09 mm. as compared
to 0.03 mm. in the earlier stage. Its inner outline is somewhat irregular,
and it is imperfectly divided into lobes, which form the commencement of
structures nearly equivalent to the nests of the Elasmobranch ovary. The
lobes _are not_ separated from each other by connective tissue
prolongations; the epithelium being at this stage perfectly free from any
ingrowths of stroma. The cells constituting the germinal epithelium have
much the same character as in the previous stage. They form an outer row of
columnar cells internal to which the cells are more rounded. Amongst them a
few large cells with granular nuclei, which are clearly primitive ova, may
now be seen, but by far the majority of the cells are fairly uniform in
size, and measure from 0.01 - 0.02 mm. in diameter, and their nuclei from
0.004 - 0.006 mm. The nuclei of the columnar outer cells measure about
0.008 mm. They are what would ordinarily be called granular, though high
powers shew that they have the usual nuclear network. There is no special
nucleolus. The rapid growth of the germinal epithelium is due to the
division of its cells, and great masses of these may frequently be seen to
be undergoing division at the same time. Of the tissue of the ovary
internal to the germinal epithelium, it may be noticed that the
tubuliferous tissue derived from the Malpighian bodies is no longer in
contact with the germinal epithelium, but that a layer of vascular stroma
is to a great extent interposed between the two. The vascular stroma of the
hilus has, moreover, greatly increased in quantity.
My next stage is that of a twenty-six days' embryo, but the characters of
the ovary at this stage so closely correspond with those of the succeeding
one at twenty-eight days that, for the sake of brevity, I pass over this
stage in silence.
Figs. 37 and 37A are representative sections of the ovary of the
twenty-eighth day corresponding with those of the earlier stages.
Great changes have become apparent in the constitution of the germinal
epithelium. The vascular stroma of the ovary has grown into the germinal
epithelium precisely as in Elasmobranchii. It appears to me clear that the
change in the relations between the stroma and epithelium is not due to a
mutual growth, but entirely to the stroma, so that, as in the case of
Elasmobranchii, the result of the ingrowth is that the germinal epithelium
is honeycombed by vascular stroma. The vascular growths generally take the
paths of the lines which separated the nests in an earlier condition, and
cause these nests to become the egg tubes of Pflüger. It is obvious in
figure 37 that the vascular ingrowths are so arranged as imperfectly to
divide the germinal epithelium into two layers separated by a space with
connective tissue and blood-vessels. The outer part is relatively thin, and
formed of a superficial row of columnar cells, and one or two rows of more
rounded cells; the inner layer is much thicker, and formed of large masses
of rounded cells. The two layers are connected together by numerous
trabeculæ, the stroma between which eventually gives rise to the connective
tissue capsule, or tunica albuginea, of the adult ovary.
The germinal epithelium is now about 0.19 to 0.22 mm. in thickness. Its
cells have undergone considerable changes. A fair number of them (fig. 37A,
_p.o._), especially in the outer layer of the epithelium, have become
larger than the cells around them, from which they are distinguished, not
only by their size, but by their granular nucleus and abundant protoplasm.
They are in fact undoubted primitive ova with all the characters which
primitive ova present in Elasmobranchii, Aves, &c. In a fairly typical
primitive ovum of this stage the body measures 0.02 mm. and the nucleus
0.014 mm. In the inner part of the germinal epithelium there are very few
or no cells which can be distinguished by their size as primitive ova, and
the cells themselves are of a fairly uniform size, though in this respect
there is perhaps a greater variation than might be gathered from fig. 37A.
The cells are on the average about 0.016 mm. in diameter, and their nuclei
about 0.008 to 0.001 mm., considerably larger, in fact, than in the earlier
stage. The nuclei are moreover more granular, and make in this respect an
approach to the character of the nuclei of primitive ova.
The germinal epithelium is still rapidly increasing by the division of its
cells, and in fig. 37A there are shewn two or three nuclei in the act of
dividing. I have represented fairly accurately the appearance they present
when examined with a moderately high magnifying power. With reference to
the stroma of the ovary, internal to the germinal epithelium, it is only
necessary to refer to fig. 37 to observe that the tubuliferous tissue (_t_)
forms a relatively smaller part of the stroma than in the previous stage,
and is also further removed from the germinal epithelium.
My next stage is that of a young rabbit two days after birth, but to
economise space I pass on at once to the following stage five days after
birth. This stage is in many respects a critical one for the ovary, and
therefore of great interest. Figure 38 represents a transverse section
through the ovary (on rather a smaller scale than the previous figures) and
shews the general relations of the tissues.
The germinal epithelium is very much thicker than before--about 0.38 mm. as
compared with 0.22 mm. It is divided into three obvious layers: (1) an
outer epithelial layer which corresponds with the pseudo-epithelial layer
of the Elasmobranch ovary, average thickness 0.03 mm. (2) A middle layer of
small nests, which corresponds with the middle vascular layer of the
previous stage; average thickness 0.1 mm. (3) An inner layer of larger
nests; average thickness 0.23 mm.
The general appearance of the germinal epithelium at this stage certainly
appears to me to lend support to my view that the whole of it simply
constitutes a thickened epithelium interpenetrated with ingrowths of
stroma.
The cells of the germinal epithelium, which form the various layers, have
undergone important modifications. In the first place a large number of the
nuclei--at any rate of those cells which are about to become ova--have
undergone a change identical with that which takes place in the conversion
of the primitive into the permanent ova in Elasmobranchii. The greater part
of the contents of the nucleus becomes clear. The remaining contents
arrange themselves as a deeply staining granular mass on one side of the
membrane, and later on as a somewhat stellate figure: the two stages
forming what were spoken of as the granular and stellate varieties of
nucleus. To avoid further circumlocution I shall speak of the nucleus
undergoing the granular and the stellate modifications. At a still later
period the granular contents form a beautiful network in the nucleus.
The pseudo-epithelium (fig. 38A) is formed of several tiers of cells, the
outermost of which are very columnar and have less protoplasm than in an
earlier stage. In the lower tiers of cells there are many primitive ova
with granular nuclei, and others in which the nuclei have undergone the
granular modification. The primitive ova are almost all of the same size as
in the earlier stage. The pseudo-epithelium is separated from the middle
layer by a more or less complete stratum of connective tissue, which,
however, is traversed by trabeculæ connecting the two layers of the
epithelium. In the middle layer there are comparatively few modified
nuclei, and the cells still retain for the most part their earlier
characters. The diameter of the cells is about 0.012 mm., and that of the
nucleus about 0.008 mm. In the innermost layer (fig. 38B), which is not
sharply separated from the middle layer, the majority of the cells, which
in the previous stage were ordinary cells of the epithelium, have commenced
to acquire modified nuclei. This change, which first became apparent to a
small extent in the young two days after birth, is very conspicuous at this
stage. In some of the cells the nucleus is modified in the granular manner,
in others in the stellate, and in a certain number the nucleus has assumed
a reticular structure characteristic of the young permanent ovum.
In addition, however, to the cells which are becoming converted into ova, a
not inconsiderable number may be observed, if carefully looked for, which
are for the most part smaller than the others, generally somewhat oval, and
in which the nucleus retains its primitive characters. A fair number of
such cells are represented in fig. 38B. In the larger ones the nucleus will
perhaps eventually become modified; but the smaller cells clearly
correspond with the interstitial cells of the Elasmobranch germinal
epithelium, and are destined to become converted into the epithelium of the
Graafian follicle. In some few instances indeed (at this stage very few),
in the deeper part of the germinal epithelium, these cells commence to
arrange themselves round the just formed permanent ova as a follicular
epithelium. An instance of this kind is shewn in fig. 38B, _o_. The cells
with modified nuclei, which are becoming permanent ova, usually present one
point of contrast to the homologous cells in Elasmobranchii, in that they
are quite distinct from each other, and not fused into a polynuclear mass.
They have around them a dark contour line, which I can only interpret as
the commencement of the membrane (zona radiata?), which afterwards becomes
distinct, and which would thus seem, as Foulis has already insisted, to be
of the nature of a vitelline membrane.
In a certain number of instances the protoplasm of the cells which are
becoming permanent ova appears, however, actually to fuse, and polynuclear
masses identical with those in Elasmobranchii are thus formed (cf. E. van
Beneden[411]). These masses become slightly more numerous in the succeeding
stages. Indications of a fusion of this kind are shewn in fig. 38B. That
the polynuclear masses really arise from a fusion of primitively distinct
cells is clear from the description of the previous stages. The ova in the
deeper layers, with modified granular nuclei, measure about 0.016 -
0.02 mm., and their nuclei from 0.01 - 0.012 mm.
Footnote 411: _Loc. cit._
With reference to the tissue of the hilus of the ovary, it may be noticed
that the tubuliferous tissue (_t_) is relatively reduced in quantity. Its
cells retain precisely their previous characters.
The chief difference between the stage of five days and that of two days
after birth consists in the fact that during the earlier stage
comparatively few modified nuclei were present, but the nuclei then
presented the character of the nuclei of primitive ova.
I have ovaries both of the dog and cat of an equivalent stage, and in both
of these the cells of the nests or egg tubes may be divided into two
categories, destined respectively to become ova and follicle cells. Nothing
which has come under my notice tends to shew that the tubuliferous tissue
is in any way concerned in supplying the latter form of cell.
In a stage, seven days after birth, the same layers in the germinal
epithelium may be noticed as in the last described stage. The outermost
layer or pseudo-epithelium contains numerous developing ova, for the most
part with modified nuclei. It is separated by a well marked layer of
connective tissue from the middle layer of the germinal epithelium. The
outer part of the middle layer contains more connective tissue and smaller
nests than in the earlier stage, and most of the cells of this layer
contain modified nuclei. In a few nests the protoplasm of the developing
ova forms a continuous mass, not divided into distinct cells, but in the
majority of instances the outline of each ovum can be distinctly traced. In
addition to the cells destined to become ova, there are present in these
nests other cells, which will clearly form the follicular epithelium. A
typical nest from the middle layer is represented on Pl. 26, fig. 39A.
The nests or masses of ova in the innermost layer are for the most part
still very large, but, in addition to the nests, a few isolated ova,
enclosed in follicles, are to be seen.
A fairly typical nest, selected to shew the formation of the follicle, is
represented on Pl. 26, fig. 39B.
The nest contains (1) fully formed permanent ova, completely or wholly
enclosed in a follicle. (2) Smaller ova, not enclosed in a follicle. (3)
Smallish cells with modified nuclei of doubtful destination. (4) Small
cells obviously about to form follicular epithelium.
The inspection of a single such nest is to my mind a satisfactory proof
that the follicular epithelium takes its origin from the germinal
epithelium and not from the stroma or tubuliferous tissue. The several
categories of elements observable in such a nest deserve a careful
description.
(1) _The large ova in their follicles._--These ova have precisely the
character of the young ova in Elasmobranchii. They are provided with a
granular body invested by a delicate, though distinct membrane. Their
nucleus is large and clear, but traversed by the network so fully described
for Elasmobranchii. The cells of their follicular epithelium have obviously
the same character as many other small cells of the nest. Two points about
them deserve notice--(_a_) that many of them are fairly columnar. This is
characteristic only of the first formed follicles. In the later formed
follicles the cells are always flat and spindle-shaped in section. In this
difference between the early and late formed follicles Mammals agree with
Elasmobranchii. (_b_) The cells of the follicle are much more columnar
towards the inner side than towards the outer. This point also is common to
Mammals and Elasmobranchii.
Round the completed follicle a very delicate membrana propria folliculi
appears to be present[412].
Footnote 412: _Loc. cit._, Waldeyer, p. 23, denies the
existence of this membrane for Mammalia. It certainly is not so
conspicuous as in some other types, but appears to me
nevertheless to be always present.
The larger ova, with follicular epithelium, measure about 0.04 mm., and
their nucleus about 0.02 mm., the smaller ones about 0.022 mm., and their
nucleus about 0.014 mm.
(2) _Medium sized ova._--They are still without a trace of a follicular
epithelium, and present no special peculiarities.
(3) _The smaller cells with modified nuclei._--I have great doubt as to
what is the eventual fate of these cells. There appear to be three
possibilities.
(_a_) That they become cells of the follicular epithelium; (_b_) that they
develop into ova; (_c_) that they are absorbed as a kind of food by the
developing ova. I am inclined to think that some of these cells may have
each of the above-mentioned destinations.
(4) _The cells which form the follicle._--The only point to be noticed
about these is that they are smaller than the indifferent cells of the
germinal epithelium, from which they no doubt originate by division. This
fact has already been noticed by Waldeyer.
The isolated follicles at this stage are formed by ingrowths of connective
tissue cutting off fully formed follicles from a nest. They only occur at
the very innermost border of the germinal epithelium. This is in accordance
with what has so often been noticed about the mammalian ovary, viz. that
the more advanced ova are to be met with in passing from without inwards.
By the stage seven days after birth the ovary has reached a sufficiently
advanced stage to answer the more important question I set myself to solve,
nevertheless, partly to reconcile the apparent discrepancy between my
account and that of Dr Foulis, and partly to bring my description up to a
better known condition of the ovary, I shall make a few remarks about some
of the succeeding stages.
In a young rabbit about four weeks old the ovary is a very beautiful object
for the study of the nuclei, &c.
The pseudo-epithelium is now formed of a single layer of columnar cells,
with comparatively scanty protoplasm. In it there are present a not
inconsiderable number of developing ova.
A layer of connective tissue--the albuginea--is now present below the
pseudo-epithelium, which contains a few small nests with very young
permanent ova. The layer of medium sized nests internal to the albuginea
forms a very pretty object in well stained sections, hardened in
Kleinenberg's picric acid. The ova in it have all assumed the permanent
form, and are provided with beautiful reticulate nuclei, with, as a rule,
one more especially developed nucleolus, and smaller granular bodies. Their
diameter varies from about 0.028 to 0.04 mm. and that of their nucleus from
0.016 to 0.02 mm. The majority of these ova are not provided with a
follicular investment, but amongst them are numerous small cells, clearly
derived from the germinal epithelium, which are destined to form the
follicle (vide fig. 40Aand B). In a few cases the follicles are completed,
and are then formed of very flattened spindle-shaped (in section) cells. In
the majority of cases all the ova of each nest are quite distinct, and each
provided with a delicate vitelline membrane (fig. 40A) In other instances,
which, so far as I can judge, are more common than in the previous stages,
the protoplasm of two or more ova is fused together.
Examples of this are represented in Pl. 26, fig. 40A. In some of these the
nuclei in the undivided protoplasm are all of about the same size and
distinctness, and probably the protoplasm eventually becomes divided up
into as many ova as nuclei; in other cases, however, one or two nuclei
clearly preponderate over the others, and the smaller nuclei are indistinct
and hazy in outline. In these latter cases I have satisfied myself as
completely as in the case of Elasmobranchii, that only one or two ova
(according to the number of distinct nuclei) will develop out of the
polynuclear mass, and that the other nuclei atrophy, and the material of
which they were composed serves as the nutriment for the ova which complete
their development. This does not, of course, imply that the ova so formed
have a value other than that of a single cell, any more than the
development of a single embryo out of the many in one egg capsule implies
that the embryo so developing is a compound organism.
In the innermost layer of the germinal epithelium the outlines of the
original large nests are still visible, but many of the follicles have been
cut off by ingrowths of stroma. In the still intact nests the formation of
the follicles out of the cells of the germinal epithelium may be followed
with great advantage. The cells of the follicle, though less columnar than
was the case at an earlier period, are more so than in the case of
follicles formed in the succeeding stages. The previous inequality in the
cells of the follicles is no longer present.
The tubuliferous tissue in the zona vasculosa appears to me to have rather
increased in quantity than the reverse; and is formed of numerous solid
columns or oval masses of cells, separated by strands of connective tissue,
with typical spindle nuclei.
It is partially intelligible to me how Dr Foulis might from an examination
of the stages similar to this, conclude that the follicle cells were
derived from the stroma; but even at this stage the position of the cells
which will form the follicular epithelium, their passage by a series of
gradations into obvious cells of the germinal epithelium and the
peculiarities of their nuclei, so different from those of the stroma cells,
supply a sufficient series of characters to remove all doubt as to the
derivation of the follicle cells. Apart from these more obvious points, an
examination of the follicle cells from the surface, and not in section,
demonstrates that the general resemblance in shape of follicle cells to the
stroma cells is quite delusory. They are in fact flat, circular, or oval,
plates not really spindle-shaped, but only apparently so in section. While
I thus fundamentally differ from Foulis as to the nature of the follicle
cells, I am on this point in complete accordance with Waldeyer, and my own
results with reference to the follicle cannot be better stated than in his
own words (pp. 43, 44).
At six weeks after birth the ovary of the rabbit corresponds very much more
with the stages in the development of the ovary, which Foulis has more
especially studied, for the formation of the follicular epithelium, than
during the earlier stages. His figure (_Quart. Journ. Mic. Sci._,
Vol. XVI., Pl. 17, fig. 6) of the ovary of a seven and a half months' human
foetus is about the corresponding age. Different animals vary greatly in
respect to the relative development of the ovary. For example, the ovary of
a lamb at birth about corresponds with that of a rabbit six weeks after
birth. The points which may be noticed about the ovary at this age are
first that the surface of the ovary begins to be somewhat folded. The
appearances of these folds in section have given rise, as has already been
pointed out by Foulis, to the erroneous view that the germinal epithelium
(pseudo-epithelium) became involuted in the form of tubular open pits. The
folds appear to me to have no connection with the formation of ova, but to
be of the same nature as the somewhat similar folds in Elasmobranchii. A
follicular epithelium is present around the majority of the ova of the
middle layer, and around all those of the inner layer of the germinal
epithelium. The nests are, moreover, much more cut up by connective tissue
ingrowths than in the previous stages.
The follicle cells of the middle layers are very flat, and spindle-shaped
in section, and though they stain more deeply than the stroma cells, and
have other not easily characterised peculiarities, they nevertheless do
undoubtedly closely resemble the stroma cells when viewed (as is ordinarily
the case) in optical section.
In the innermost layer many of the follicles with the enclosed ova have
advanced considerably in development and are formed of columnar cells. The
somewhat heterodox view of these cells propounded by Foulis I cannot quite
agree to. He says (_Quart. J. Mic. Sci._, Vol. XVI., p. 210): "The
protoplasm which surrounds the vesicular nuclei acts as a sort of cement
substance, holding them together in the form of a capsular membrane round
the young ovum. This capsular membrane is the first appearance of the
membrana granulosa." I must admit that I find nothing similar to this, nor
have I met with any special peculiarities (as Foulis would seem to
indicate) in the cells of the germinal epithelium or other cells of the
ovary.
Figure 41 is a representation of an advanced follicle of a six weeks'
rabbit, containing two ova, which is obviously in the act of dividing into
two. Follicles of this kind with more than one ovum are not very uncommon.
It appears to me probable that follicles, such as that I have figured, were
originally formed of a single mass of protoplasm with two nuclei; but that
instead of one of the nuclei atrophying, both of them eventually developed
and the protoplasm subsequently divided into two masses. In other cases it
is quite possible that follicles with two ova should rather be regarded as
two follicles not separated by a septum of stroma.
On the later stages of development of the ovary I have no complete series
of observations. The yolk spherules I find to be first developed in a
peripheral layer of the vitellus. I have not been able definitely to decide
the relation of the zona radiata to the first formed vitelline membrane.
Externally to the zona radiata there may generally be observed a somewhat
granular structure, against which the follicle cells abut, and I cannot
agree with Waldeyer (_loc cit._, p. 40) that this structure is continuous
with the cells of the discus, or with the zona radiata. Is it the remains
of the first formed vitelline membrane? I have obtained some evidence in
favour of this view, but have not been successful in making observations to
satisfy me on the point, and must leave open the question whether my
vitelline membrane becomes the zona radiata or whether the zona is not a
later and independent formation, but am inclined myself to adopt the latter
view. The first formed membrane, whether or no it becomes the zona radiata,
is very similar to the vitelline membrane of Elasmobranchii and arises at a
corresponding stage.
_Summary of observations on the mammalian ovary._--The general results of
my observations on the mammalian ovary are the following:--
(1) The ovary in an eighteen days' embryo consists of a cylindrical ridge
attached along the inner side of the Wolffian body, which is formed of two
parts; (_a_) an external epithelium--two or three cells deep (the germinal
epithelium); (_b_) a hilus or part forming in the adult the vascular zone,
at this stage composed of branched masses of epithelial tissue
(tubuliferous tissue) derived from the walls of the anterior Malpighian
bodies, and numerous blood-vessels, and some stroma cells.
(2) The germinal epithelium gradually becomes thicker, and after a certain
stage (twenty-three days) there grow into it numerous stroma ingrowths,
accompanied by blood-vessels. The germinal epithelium thus becomes
honeycombed by strands of stroma. Part of the stroma eventually forms a
layer close below the surface, which becomes in the adult the tunica
albuginea. The part of the germinal epithelium external to this layer
becomes reduced to a single row of cells, and forms what has been spoken of
in this paper as the pseudo-epithelium of the ovary. The greater part of
the germinal epithelium is situated internal to the tunica albuginea, and
this part is at first divided up by strands of stroma into smaller
divisions externally, and larger ones internally. These masses of germinal
epithelium (probably sections of branched trabeculæ) may be spoken of as
nests. In the course of the development of the ova they are broken up by
stroma ingrowths, and each follicle with its enclosed ovum is eventually
isolated by a layer of stroma.
(3) The cells of the germinal epithelium give rise both to the permanent
ova and to the cells of the follicular epithelium. For a long time,
however, the cells remain indifferent, so that the stages, like those in
Elasmobranchii, Osseous Fish, Birds, Reptiles, &c., with numerous primitive
ova embedded amongst the small cells of the germinal epithelium, are not
found.
(4) The conversion of the cells of the germinal epithelium into permanent
ova commences in an embryo of about twenty-two days. All the cells of the
germinal epithelium appear to be capable of becoming ova: the following are
the stages in the process, which are almost identical with those in
Elasmobranchii:--
(_a_) The nucleus of the cells loses its more or less distinct network, and
becomes very granular, with a few specially large granules (nucleoli). The
protoplasm around it becomes clear and abundant--primitive ovum stage. It
may be noted that the largest primitive ova are very often situated in the
pseudo-epithelium. (_b_) A segregation takes place in the contents of the
nucleus within the membrane, and the granular contents pass to one side,
where they form an irregular mass, while the remaining space within the
membrane is perfectly clear. The granular mass gradually develops itself
into a beautiful reticulum, with two or three highly refracting nucleoli,
one of which eventually becomes the largest and forms the germinal spot
_par excellence_. At the same time the body of the ovum becomes slightly
granular. While the above changes, more especially those in the nucleus,
have been taking place, the protoplasm of two or more ova may fuse
together, and polynuclear masses be so formed. In some cases the whole of
such a polynuclear mass gives rise to only a single ovum, owing to the
atrophy of all the nuclei but one, in others it gives rise by subsequent
division to two or more ova, each with a single germinal vesicle.
(5) All the cells of a nest do not undergo the above changes, but some of
them become smaller (by division) than the indifferent cells of the
germinal epithelium, arrange themselves round the ova, and form the
follicular epithelium.
(6) The first membrane formed round the ovum arises in some cases even
before the appearance of the follicular epithelium, and is of the nature of
a vitelline membrane. It seems probable, although not definitely
established by observation, that the zona radiata is formed internally to
the vitelline membrane, and that the latter remains as a membrane, somewhat
irregular on its outer border, against which the ends of the follicle cells
abut.
GENERAL OBSERVATIONS ON THE STRUCTURE AND DEVELOPMENT OF THE OVARY.
In selecting Mammalia and Elasmobranchii as my two types for investigation,
I had in view the consideration that what held good for such dissimilar
forms might probably be accepted as true for all Vertebrata with the
exception of Amphioxus.
_The structure of the ovary._--From my study of these two types, I have
been led to a view of the structure of the ovary, which differs to a not
inconsiderable extent from that usually entertained. For both types the
conclusion has been arrived at that the whole egg-containing part of the
ovary is really _the thickened germinal epithelium_, and that it differs
from the original thickened patch or layer of germinal epithelium, mainly
in the fact that it is broken up into a kind of meshwork by growths of
vascular stroma. If the above view be accepted for Elasmobranchii and
Mammalia, it will hardly be disputed for the ovaries of Reptilia and Aves.
In the case also of Osseous Fish and Amphibia, this view of the ovary
appears to be very tenable, but the central core of stroma present in the
other types is nearly or quite absent, and the ovary is entirely formed of
the germinal epithelium with the usual strands of vascular stroma[413]. It
is obvious that according to the above view Pflüger's egg-tubes are merely
trabeculæ of germinal epithelium, and have no such importance as has been
attributed to them. They are present in a more or less modified form in all
types of ovaries. Even in the adult Amphibian ovary, columns of cells of
the germinal epithelium, some indifferent, others already converted into
ova, are present, and, as has been pointed out by Hertwig[414], represent
Pflüger's egg-tubes.
Footnote 413: My view of the structure of the ovary would seem
to be that held by Götte, _Entwicklungsgeschichte d. Unke_, pp.
14 and 15.
Footnote 414: _Loc. cit._ 36.
_The formation of the permanent ova._--The passage of primitive ova into
permanent ova is the part of my investigation to which the greatest
attention was paid, and the results arrived at for Mammalia and
Elasmobranchii are almost identical. Although there are no investigations
as to the changes undergone by the nucleus in other types, still it appears
to me safe to conclude that the results arrived at hold good for
Vertebrates generally[415]. As has already been pointed out the
transformation which the so-called primitive ova undergo is sufficient to
shew that _they are not to be regarded as ova but merely as embryonic
sexual cells_. A feature in the transformation, which appears to be fairly
constant in Scyllium, and not uncommon in the rabbit, is the fusion of the
protoplasm of several ova into a syncytium, the subsequent increase in the
number of nuclei in the syncytium, the atrophy and absorption of a portion
of the nuclei, and the development of the remainder into the germinal
vesicles of ova; the vitellus of each ovum being formed by a portion of the
protoplasm of the syncytium.
Footnote 415: Since writing the above I have made out that in
the Reptilia the formation of the permanent ova takes place in
the same fashion as in Elasmobranchii and Mammalia.
As to the occurrence of similar phenomena in the Vertebrata generally, it
has already been pointed out that Ed. van Beneden has described the
polynuclear masses in Mammalia, though he does not appear to me to have
given a complete account of their history. Götte[416] describes a fusion of
primitive ova in Amphibia, but he believes that the nuclei fuse as well as
the bodies of the ova, so that one ovum (according to his view no longer a
cell) is formed by the fusion of several primitive ova with their nuclei. I
have observed nothing which tends to support Götte's view about the fusion
of the nuclei, and regard it as very improbable. As regards the
interpretation to be placed upon the nests formed of fused primitive ova,
Ed. van Beneden maintains that they are to be compared with the upper ends
of the egg tubes of Insects, Nematodes, Trematodes, &c. There is no doubt a
certain analogy between the two, in that in both cases certain nuclei of a
polynuclear mass increase in size, and with the protoplasm around them
become segmented off from the remainder of the mass as ova, but the analogy
cannot be pressed. The primitive ova, or even the general germinal
epithelium, rather than these nests, must be regarded as giving origin to
the ova, and the nests should be looked on, in my opinion, as connected
more with the nutrition than with the origin of the ova. In favour of this
view is the fact that as a rule comparatively few ova are developed from
the many nuclei of a nest; while against the comparison with the egg tubes
of the Invertebrata it is to be borne in mind that many ova appear to
develop independently of the nests.
Footnote 416: _Entwicklungsgeschichte d. Unke._
In support of my view about the nests there may be cited many analogous
instances from the Invertebrata. In none of them, however, are the
phenomena exactly identical with those in Vertebrata. In the ovary of many
Hydrozoa (_e.g. Tubularia mesembryanthemum_), out of a large number of ova
which develop up to a certain point, a comparatively very small number
survive, and these regularly feed upon the other ova. During this process
the boundary between a large ovum and the smaller ova is indistinct: in the
outermost layer of a large ovum a number of small ova are embedded, the
outlines of the majority of which have become obscure, although they can
still be distinguished. Just beyond the edge of a large ovum the small ova
have begun to undergo retrogressive changes; while at a little distance
from the ovum they are quite normal. An analogous phenomenon has been very
fully described by Weismann[417] in the case of Leptodera, the ovary of
which consists of a germogene, in which the ova develop in groups of four.
Each group of four occupies a separate chamber of the ovary, but in summer
only one of the four eggs (the third from the germogene) develops into an
ovum, the other three are used as pabulum. In the case of the winter eggs
the process is carried still further, in that the contents of the alternate
chambers, instead of developing into ova, are entirely converted, by a
series of remarkable changes, into nutritive reservoirs. Fundamentally
similar occurrences to the above are also well known in Insects. Phenomena
of this nature are obviously in no way opposed to the view of the ovum
being a single cell.
Footnote 417: _Zeit. für wiss. Zool._ Bd. XXVII.
With reference to the origin of the primitive ova, it appears to me that
their mode of development in Mammals proves beyond a doubt that they are
modified cells of the germinal epithelium. In Elasmobranchii their very
early appearance, and the difficulty of finding transitional forms between
them and ordinary cells of the germinal epithelium, caused me at one time
to seek (unsuccessfully) for a different origin for them. Any such attempts
appear to me, however, out of the question in the case of Mammals.
_The egg membranes._--The homologies of the egg membranes in the Vertebrata
are still involved in some obscurity. In Elasmobranchii there are
undoubtedly two membranes present. (1) An outer and first formed
membrane--the albuminous membrane of Gegenbaur--which, in opposition to
previous observers, I have been led to regard as a vitelline membrane. (2)
An inner radiately striated membrane, formed as a differentiation of the
surface of the yolk at a later period. Both these membranes usually atrophy
before the ovum leaves the follicle. In Reptilia[418] precisely the same
arrangement is found as in Elasmobranchii, except that as a rule the zona
radiata is relatively more important. The vitelline membrane external to
this (or as it is usually named the chorion) is, as a rule, thin in
Reptilia; but in Crocodilia is thick (Gegenbaur), and approaches the
condition found in Scyllium and other Squalidæ. It appears, as in
Elasmobranchii, to be formed before the zona radiata. A special internal
differentiation of the zona radiata is apparently found (Eimer) in many
Reptilia. No satisfactory observations appear to be recorded with reference
to the behaviour of the two reptilian membranes as the egg approaches
maturity. In Birds[419] the same two membranes are again found. The first
formed and outer one is, according to Gegenbaur and E. van Beneden, a
vitelline membrane; and from the analogy of Elasmobranchii I feel inclined
to accept their view. The inner one is the zona radiata, which disappears
comparatively early, leaving the ovum enclosed only by the vitelline
membrane, when it leaves the follicle. All the large-yolked vertebrate ova
appear then to agree very well with Elasmobranchii in presenting during
some period of their development the two membranes above mentioned.
Footnote 418: Gegenbaur, _loc. cit._; Waldeyer, _loc. cit._;
Eimer, _loc. cit._; and Ludwig, _loc. cit._
Footnote 419: Gegenbaur, Waldeyer, E. van Beneden, Eimer.
Osseous fish have almost always a zona radiata, which it seems best to
assume to be equivalent to that in Elasmobranchii. Internal to this is a
thin membrane, the equivalent, according to Eimer, of the membrane found by
the same author within the zona in Reptilia. A membrane equivalent to the
thick vitelline membrane of Elasmobranchii would seem to be absent in most
instances, though a delicate membrane, external to the zona, has not
infrequently been described; Eimer more especially asserts that such a
membrane exists in the perch within the peculiar mucous covering of the egg
of that fish.
In Petromyzon, a zona radiata appears to be present[420], which is divided
in the adult into two layers, both of them perforated. The inner of the two
perhaps corresponds with the membrane internal to the zona radiata in other
types. In Amphibia the single late formed and radiately striated (Waldeyer)
membrane would appear to be a zona radiata. If the suggestion on page 605
turns out to be correct the ova of Mammalia possess both a vitelline
membrane and zona radiata. E. van Beneden[421] has, moreover, shewn that
they are also provided at a certain period with a delicate membrane within
the zona.
Footnote 420: Carlberla, _Zeit. f. wiss. Zool._ Bd. XXX.
Footnote 421: _Loc. cit._
_The reticulum of the germinal vesicle._--In the course of description of
the ovary it has been necessary for me to enter with some detail into the
structure of the nucleus, and I have had occasion to figure and describe a
reticulum identical with that recently described by so many observers. The
very interesting observations of Dr Klein in the last number of this
Journal[422] have induced me to say one or two words in defence of some
points in my description of the reticulum. Dr Klein says, on page 323, "I
have distinctly seen that when nucleoli are present--the instances are
fewer than is generally supposed; they are accumulations of the fibrils of
the network." I have no doubt that Klein is correct in asserting that
nucleoli are fewer than is generally supposed; and that in many of these
instances what are called nucleoli are accumulations, "natural or
artificial," of the fibrils of the network; but I cannot accept the
universality of the latter statement, which appears to me most certainly
not to hold good in the case of ova, in which nucleoli frequently exist in
the absence of the network.
Footnote 422: [_Quarterly Journal Microscopical Science_, July
1878.]
Again, I find that at the point of intersection of two or more fibrils
there is, as a rule, a distinct thickening of the matter of the fibrils,
and that many of the dots seen are not merely, as Dr Klein would maintain,
optical sections of fibrils.
It appears to me probable that both the network and the nucleoli are
composed of the same material--what Hertwig calls nuclear substance--and if
Dr Klein merely wishes to assert this identity in the passage above quoted,
I am at one with him.
Although a more or less distinct network is present in most nuclei (I have
found it in almost all embryonic nuclei) it is not universally so. In the
nuclei of primitive ova I have no doubt that it is absent, though present
in the unmodified nuclei of the germinal epithelium; and it is present only
in a very modified form in the nuclei of primitive ova undergoing a
transformation into permanent ova. The absence of the reticulum does not,
of course, mean that the substance capable of forming a reticulum is
absent, but merely that it does not assume a particular arrangement.
One of the most interesting points in Klein's paper, as well as in those of
Heitzmann and Eimer, is the demonstration of a connection between the
reticulum of the nucleus and fibres in the body of the cell. Such a
connection I have not found in ova, but may point out that it appears to
exist between the sub-germinal nuclei in Elasmobranchii and the
protoplasmic network in the yolk in which they lie. This point is called
attention to in my _Monograph on Elasmobranch Fishes_, page 39[423], where
it is stated that "the network in favourable cases may be observed to be in
connection with the nuclei just described. Its meshes are finer in the
vicinity of the nuclei, and the fibres in some cases appear almost to start
from them." The nuclei in the yolk are knobbed bodies divided by a sponge
work of septa into a number of areas each with a nucleolar body.
Footnote 423: [This Edition, p. 252.]
EXPLANATION OF PLATES 24, 25, 26.
PLATE 24.
LIST OF REFERENCE LETTERS.
_dn._. Modified nucleus of primitive ovum. _do._. Permanent ovum in the act
of being formed. _dv._. Developing blood-vessels. _dyk._ Developing yolk.
_ep._ Non-ovarian epithelium of ovarian ridge. _fe._ Follicular epithelium.
_gv._ Germinal vesicle. _lstr._ Lymphatic region of stroma. _nn._ Nests of
nuclei of ovarian region. _o._ Permanent ovum. _ovr._ Ovarian portion of
ovarian ridge. _po._ Primitive ovum. _pse._ Pseudo-epithelium of ovarian
ridge. _str._ Stroma ingrowths into ovarian epithelium. _v._ Blood-vessel.
_vstr._ Vascular region of stroma adjoining ovarian ridge. _vt._ Vitelline
membrane. _x._ Modified nucleus. _yk._ Yolk. _zn._ Zona radiata.
Fig. 1. Transverse section of the ovarian ridge of an embryo of _Scy.
canicula_, belonging to stage P, shewing the ovarian region with thickened
epithelium and numerous primitive ova. Zeiss C, ocul. 2. _Picric acid._
Fig. 2. Transverse section of the ovarian ridge of an embryo of _Scyllium
canicula_, considerably older than stage Q. Zeiss C, ocul. 2. _Picric
acid._ Several nests, some with distinct ova, and others with the ova fused
together, are present in the section (_nn_), and several examples of
modified nuclei in still distinct ova are also represented. One of these is
marked _x_. The stroma of the ovarian ridge is exceptionally scanty.
Fig. 3. Transverse section through part of the ovarian ridge, including the
ovarian region of an almost ripe embryo of _Scyllium canicula_. Zeiss C,
ocul. 2. _Picric acid._ Nuclear nests (_n.n._), developing ova (_d.o._),
and ova (_o._), with completely formed follicular epithelium, are now
present. The ovarian region is still well separated from the subjacent
stroma, and does not appear to contain any cells except those of the
original germinal epithelium.
Fig. 4. Section through ovarian ridge of the same embryo as fig. 3, to
illustrate the relation of the stroma (_str._) and ovarian region. Zeiss _a
a_, ocul. 2. _Picric acid._
Fig. 5. Section through the ovarian ridge of an embryo of _Scyllium
canicula_, 10 cm. long, in which the ovary was slightly less advanced than
in fig. 3. To illustrate the relation of the ovarian epithelium to the
subjacent vascular stroma. Zeiss A, ocul. 2. _Osmic acid._ _y_ points to a
small separated portion of the germinal epithelium.
Fig. 6. Section through the ovarian ridge of an embryo of _Scyllium
canicula_, slightly older than fig. 5. To illustrate the relation of the
ovarian epithelium to the subjacent vascular stroma. Zeiss A, ocul. 2.
_Osmic acid._
Fig. 7. More highly magnified portion of the same ovary as fig. 6. To
illustrate the same points. Zeiss C, ocul. 2. _Osmic acid._
Fig. 8. Section through the ovarian region (close to one extremity, where
it is very small) from a young female of _Scy. canicula_. Zeiss C, ocul. 2.
_Picric acid._ It shews the vascular ingrowths amongst the original
epithelial cells of the ovarian region.
Fig. 9. Section through the ovarian region of the same embryo as fig. 8, at
its point of maximum development. Zeiss A, ocul. 2. _Picric acid._
Fig. 10. Section through superficial part of the ovary of an embryo,
shewing the pseudo-epithelium; the cells of which are provided with tails
prolonged into the general tissue of the ovary. At _f.e._ is seen a surface
view of the follicular epithelium of an ovum. Zeiss C, ocul. 2. _Picric
acid._
Fig. 11. Section through part of an ovary of _Scyllium canicula_ of stage
Q, with three primitive ova, the most superficial one containing a modified
nucleus.
Fig. 12. Section through part of an ovary of an example of _Scyllium
canicula_, 8 cm. long. The section passes through a nest of ova with
modified nuclei, in which the outlines of the individual ova are quite
distinct. Zeiss E, ocul. 2. _Picric acid._
Fig. 13. Section through part of ovary of the same embryo as in fig. 5. The
section passes through a nest of nuclei, with at the least two developing
ova, and also through one already formed permanent ovum. Zeiss E, ocul. 2.
_Osmic acid._
Figs. 14, 15, 16, 17, 18 [Figs. 17 and 18 are on Pl. 25]. Sections through
parts of the ovary of the same embryo as fig. 3, with nests of nuclei and a
permanent ova in the act of formation. Fig. 14 is drawn with Zeiss D D,
ocul. 2. Figs. 15, 16, 17, with Zeiss E, ocul. 2. _Picric acid._
PLATE 25.
LIST OF REFERENCE LETTERS.
_do._ Permanent ovum in the act of being formed. _dyk._ Developing yolk.
_fe._ Follicular epithelium. _fe´._ Secondary follicular epithelium. _gv._
Germinal vesicle. _nn._ Nests of nuclei of ovarian region. _o._ Permanent
ovum. _pse._ Pseudo-epithelium. _str._ Stroma ingrowths into ovarian
epithelium. _vt._ Vitelline membrane. _x._ Modified nucleus. _yk._ Yolk
(vitellus). _zn._ Zona radiata.
[Figs. 17 and 18. Vide description of Plate 24.].
Fig. 19. Two nuclei from a nest which appear to be in the act of division.
From ovary of the same embryo as fig. 3.
Fig. 20. Section through part of an ovary of the same embryo as fig. 6,
containing a nest of nuclei. Zeiss F, ocul. 2. _Osmic acid._
Fig. 21. Ovum from the ovary of a half-grown female, containing isolated
deeply stained patches of developing yolk granules. Zeiss B, ocul. 2.
_Picric acid._
Fig. 22. Section through a small part of the ovum of an immature female of
_Scyllium canicula_, to shew the constitution of the yolk, the follicular
epithelium, and the egg membranes. Zeiss E, ocul. 2. _Chromic acid._
Fig. 23. Section through part of the periphery of a nearly ripe ovum of
_Scy. canicula_. Zeiss C, ocul. 2. It shews the remnant of the vitelline
membrane (_v.t._) separating the columnar but delicate cells of the
follicular epithelium (_f.e._) from the yolk (_yk._). In the yolk are seen
yolk-spherules in a protoplasmic network. The transverse markings in the
yolk-spherules have been made oblique by the artist.
Fig. 24. Fully formed ovum containing a second nucleus (_x_), probably
about to be employed as pabulum; from the same ovary as fig. 5. The
follicular epithelium is much thicker on the side adjoining the stroma than
on the upper side of the ovum. Zeiss F, ocul. 2. _Osmic acid._
Fig. 25. A. Ovum from the same ovary as fig. 21, containing in the yolk
three peculiar bodies, similar in appearance to the two small bodies in the
germinal vesicle. B. Germinal vesicle of a large ovum from the same ovary,
containing a body of a strikingly similar appearance to those in the body
of the ovum in A. Zeiss E, ocul. 2. _Picric acid._
Fig. 26. Section of the ovary of a young female of _Scyllium stellare_
16-1/2 centimetres in length. The ovary is exceptional, on account of the
large size of the stroma ingrowths into the epithelium. Zeiss C, ocul. 2.
_Osmic acid._
Fig. 27. Ovum of _Scyllium canicula_, 5 mm. in diameter, treated with osmic
acid. The figure illustrates the development of the yolk and a peculiar
mode of proliferation of the germinal spots. Zeiss A, ocul. 2.
Fig. 28. Small part of the follicular epithelium and egg membranes of a
somewhat larger ovum of _Scyllium canicul_a than fig. 22. Zeiss D D, ocul.
2.
Fig. 29. The same parts as in fig. 28, from a still larger ovum. Zeiss D D,
ocul. 2.
Fig. 30. Ovum of Raja with follicular epithelium. Zeiss C, ocul. 2.
Fig. 31. Small portion of a larger ovum of Raja than fig. 30. Zeiss D D,
ocul. 2.
Fig. 32. Follicular epithelium, &c., from an ovum of Raja still larger than
fig. 31. Zeiss D D, ocul. 2.
Fig. 33. Surface view of follicular epithelium from an ovum of Raja of
about the same age as fig. 33.
Fig. 34. Vertical section through the superficial part of an ovary of an
adult Raja to shew the relation of the pseudo-epithelium to the subjacent
stroma. Zeiss D D, ocul. 2.
PLATE 26.
COMPLETE LIST OF REFERENCE LETTERS.
_do._ Developing ovum. _fc._ Cells which will form the follicular
epithelium, _fe._ Follicular epithelium. _ge._ Germinal epithelium. _mg._
Malpighian body. _n._ Nest of cells of the germinal epithelium. _nd._
Nuclei in the act of dividing. _o._ Permanent ovum. _ov._ Ovary. _po._
Primitive ovum. _t._ Tubuliferous tissue, derived from Malpighian bodies.
Fig. 35. Transverse section through the ovary of an embryo rabbit of
eighteen days, hardened in osmic acid. The colours employed are intended to
render clear the distinction between the germinal epithelium (_ge._) and
the tubuliferous tissue (_t._), which has grown in from the Wolffian body,
and which gives rise in the male to parts of the tubuli seminiferi. Zeiss
A, ocul. 2.
Fig. 35A . Transverse section through a small part of the ovary of an
embryo from the same female as fig. 35, hardened in picric acid, shewing
the relation of the germinal epithelium to the subjacent tissue. Zeiss D D,
ocul. 2.
Fig. 35B. Longitudinal section through part of the Wolffian body and the
anterior end of the ovary of an eighteen days' embryo, to shew the
derivation of tubuliferous tissue (_t._) from the Malpighian bodies, close
to the anterior extremity of the ovary. Zeiss A, ocul. 1.
Fig. 36. Transverse section through the ovary of an embryo rabbit of
twenty-two days, hardened in osmic acid. It is coloured in the same manner
as fig. 35. Zeiss A, ocul. 2.
Fig. 36A. Transverse section through a small part of the ovary of an
embryo, from the same female as fig. 36, hardened in picric acid, shewing
the relation of the germinal epithelium to the stroma of the ovary. Zeiss D
D, ocul. 2.
Figs. 37 and 37A. The same parts of an ovary of a twenty-eight days' embryo
as figs. 36 and 36A of a twenty-two days' embryo.
Fig. 38. Ovary of a rabbit five days after birth, coloured in the same
manner as figs. 35, 36 and 37, but represented on a somewhat smaller scale.
_Picric acid._
Fig. 38A. Vertical section through a small part of the surface of the same
ovary as fig. 38. Zeiss D D, ocul. 2.
Fig. 38B. Small portion of the deeper layer of the germinal epithelium of
the same ovary as fig. 38. The figure shews the commencing differentiation
of the cells of the germinal epithelium into true ova and follicle cells.
Zeiss D D, ocul. 2.
Fig. 39A. Section through a small part of the middle region of the germinal
epithelium of a rabbit seven days after birth. Zeiss D D, ocul. 2.
Fig. 39B. Section through a small part of the innermost layer of the
germinal epithelium of a rabbit seven days after birth, shewing the
formation of Graafian follicles. Zeiss D D, ocul. 2.
Figs. 40A and 40B. Small portions of the middle region of the germinal
epithelium of a rabbit four weeks after birth. Zeiss D D, ocul. 2.
Fig. 41. Graafian follicle with two ova, about to divide into two
follicles, from a rabbit six weeks after birth. Zeiss D D, ocul. 2.
XIII. ON THE EXISTENCE OF A HEAD-KIDNEY IN THE EMBRYO CHICK, AND ON
CERTAIN POINTS IN THE DEVELOPMENT OF THE MÜLLERIAN DUCT[424].
BY F. M. BALFOUR AND A. SEDGWICK.
Footnote 424: From the _Quarterly Journal of Microscopical
Science_, Vol. XIX. 1879.
(With Plates 27 and 28.)
The following paper is divided into three sections. The first of these
records the existence of certain structures in the embryo chick, which
eventually become in part the abdominal opening of the Müllerian duct, and
which, we believe, correspond with the head-kidney, or "Vorniere" of German
authors. The second deals with the growth and development of the Müllerian
duct. With reference to this we have come to the conclusion that the
Müllerian duct does not develop entirely independently of the Wolffian
duct. The third section of our paper is of a more general character, and
contains a discussion of the rectifications in the views of the homologies
of the parts of the excretory system in Aves, necessitated by the results
of our investigations.
We have, as far as possible, avoided entering into the extended literature
of the excretory system, since this has been very fully given in three
general papers which have recently appeared by Semper[425], Fürbinger[426],
and by one of us[427].
Footnote 425: "Das Urogenital-System der Plagiostomen,"
_Arbeiten a. d. zool.-zoot. Institut. Würzburg_.
Footnote 426: "Zur vergl. Anat. u. Entwick. d.
Excretionsorgane d. Vertebraten," _Morphologisches Jahrbuch_,
Vol. IV.
Footnote 427: "On the Origin and History of the Urinogenital
Organs of Vertebrates," _Journal of Anat. and Phys._, Vol. X.
[This Edition No. VII.]
All recent observers, including Braun[428] for Reptilia, and Egli[429] for
Mammalia, have stated that the Müllerian duct develops as a groove in the
peritoneal epithelium, which is continued backward as a primitively solid
rod in the space between the Wolffian duct and peritoneal epithelium.
Footnote 428: _Arbeiten a. d. zool.-zoot. Institut. Würzburg_,
Vol. IV.
Footnote 429: _Beitr. zur Anat. u. Entwick. d.
Geschlechtsorgane_, Inaug. Diss., Zürich, 1876.
In our preliminary account we stated[430], in accordance with the general
view, that the Müllerian duct was formed as a groove, or elongated
involution of the peritoneal epithelium adjoining the Wolffian duct. We
have now reason to believe that this is not the case. In the earliest
condition of the Müllerian duct which we have been able to observe, it
consists of three successive open involutions of the peritoneal epithelium,
connected together by more or less well-defined ridge-like thickenings of
the epithelium. We believe, on grounds hereafter to be stated, that the
whole of this formation is equivalent to the head-kidney of the
Ichthyopsida. The head-kidney, as we shall continue to call it, takes its
origin from the layer of thickened epithelium situated near the dorsal
angle of the body-cavity, close to the Wolffian duct, which has been known
since the publication of Waldeyer's important researches as the germinal
epithelium. The anterior of the three open involutions or grooves is
situated some little distance behind the front end of the Wolffian duct. It
is simply a shallow groove in the thickest part of the germinal epithelium,
and forms a corresponding projection into the adjacent stroma. In front the
projection is separated by a considerable interval from the Wolffian duct;
but near its hindermost part it almost comes into contact with the Wolffian
duct. The groove extends in all for about five of our sections, and then
terminates by its walls becoming gradually continued into a slight
ridge-like thickening of the germinal epithelium. The groove arises as a
simple depression in a linear area of thickened germinal epithelium. The
linear area is, however, continued very considerably further forward than
the groove, and sometimes exhibits a slight central depression, which might
be regarded as a forward continuation of the groove. The passage from the
groove to the ridge may best be conceived by supposing the groove to be
suddenly filled up, so as to form a solid ridge pointing inwards towards
the Wolffian duct.
Footnote 430: _Proceedings of Royal Society_, 1878.
The ridge succeeding the first groove is continued for about six sections,
and is considerably more prominent at its posterior extremity than in
front. It is replaced by groove number two, which appears as if formed by
the reverse process to that by which the ridge arose, viz., by a hollowing
out of the ridge on the side towards the body-cavity. The wall of the
second groove is, after a few sections, continued into a second ridge or
thickening of the germinal epithelium, which, however, is so faintly marked
as to be hardly visible in its middle part. In its turn this ridge is
replaced by the third and last groove. This vanishes after one or two
sections, and behind the point of its disappearance we have failed to find
any further traces of the head-kidney. The whole formation extends through
about twenty-four of our sections and one and a half segments
(muscle-plates).
We have represented (Plate 27, Series A, Nos. 1-10) a fairly complete
series of sections through part of the head-kidney of an embryo slightly
older than that last described, containing the second and third grooves and
accessory parts. The connection between the grooves and the ridges is very
well illustrated in Nos. 3, 4, and 5 of this series. In No. 3 we have a
prominent ridge, in the interior of which there appears in No. 4 a groove,
which becomes gradually wider in Nos. 5 and 6. Both the grooves and ridges
are better marked in this than in the younger stage; but the chief
difference between the two stages consists in the third groove no longer
forming the hindermost limit of the head-kidney. Instead of this, the last
groove (No. 7) terminates by the upper part of its walls becoming
constricted off as a separate rod, which appears at first to contain a
lumen continuous with the open groove. This rod (Nos. 7, 8, 9, 10) situated
between the germinal epithelium and Wolffian duct is continued backward for
some sections. It finally terminates by a pointed extremity, composed of
not more than two cells abreast (Nos. 8-10).
Our third stage, sections of which are represented in series B (Plate 27),
is considerably advanced beyond that last described. The most important
change which has been effected concerns the ridges connecting the
successive grooves. A lumen has appeared in each of these, which seems to
open at both ends into the adjacent grooves. At the same time the cells,
which previously constituted the ridge, have become (except where they are
continuous with the walls of the grooves) partially constricted off from
the germinal epithelium. The ridges, in fact, now form ducts situated in
the stroma of the ovarian ridge, in the space between the Wolffian duct and
the germinal epithelium. The duct continuous with the last groove is
somewhat longer than before. In a general way, the head-kidney may now be
described as a duct opening into the body-cavity by three groove-like
apertures, and continuous behind with the rudiment of the true Müllerian
duct. Although the general constitution of the head-kidney at this stage is
fairly simple, there are a few features in our sections which we do not
fully understand, and a few points about the organ which deserve a rather
fuller description than we have given in this general sketch.
The anterior groove (Nos. 1-3, series B, Pl. 27) is at first somewhat
separated from the Wolffian duct, but approaches close to it in No. 3. In
Nos. 2 and 3 there appears a rod-like body on the outer side of the walls
of the groove. In No. 2 this body is disconnected with the walls of the
groove, and even appears as if formed by a second invagination of the
germinal epithelium. In No. 3 this body becomes partially continuous with
the walls of the groove, and finally in No. 4 it becomes completely
continuous with the walls of the groove, and its lumen communicates freely
with the groove[431].
Footnote 431: A deep focus of the rather thick section
represented in No. 3 shewed the body much more nearly in the
position it occupies in No. 4.
The last trace of this body is seen on the upper wall of the groove in No.
5. We believe that the body (_r_1) represents the ridge between the first
and second grooves of the earlier stage; so that in passing from No. 3 to
No. 5 we pass from the first to the second groove. The meaning of the
features of the body _r_1 in No. 2 we do not fully understand, but cannot
regard them as purely accidental, since we have met with more or less
similar features in other series of sections. The second groove becomes
gradually narrower, and finally is continued into the second ridge (No. 8).
The ridge contains a lumen, and is only connected with the germinal
epithelium by a narrow wall of cells. A narrow passage from the body-cavity
leads into that wall for a short distance in No. 8, but it is probably
merely the hinder end of the groove of No. 7. The third groove appears in
No. 11, and opens into the lumen of the second ridge (_r_2) in No. 12. In
No. 13 the groove is closed, and there is present in its place a duct
(_r_3) connected with the germinal epithelium by a wall of cells. This duct
is the further development of the third ridge of the last stage; its lumen
opens into the body-cavity through the third and last groove (_gr_3). In
the next section this duct (_r_3) is entirely separated from the germinal
epithelium, and it may be traced backwards through several sections until
it terminates by a solid point, very much as in the last stage.
In the figures of this series (B) there may be noticed on the outer side of
the Müllerian duct a fold of the germinal epithelium (_x_) forming a second
groove. It is especially conspicuous in the first six sections of the
series. This fold sometimes becomes much deeper, and then forms a groove,
the upper end of which is close to the grooves of the head-kidney. It is
very often much deeper than these are, and without careful study might
easily be mistaken for one of these grooves. Fig. C, taken from a series
slightly younger than B, shews this groove (_x_) in its most exaggerated
form.
The stage we have just described is that of the fullest development of the
head-kidney. In it, as in all the previous stages, there appear to be only
three main openings into the body-cavity; but we have met in some of our
sections with indications of the possible presence of one or two extra
rudimentary grooves.
In an embryo not very much older than the one last described the atrophy of
the head-kidney is nearly completed, and there is present but a single
groove opening into the body-cavity.
In series D (Pl. 28) are represented a number of sections from an embryo at
this stage. Nos. 1 and 2 are sections through the hind end of the single
groove now present. Its walls are widely separated from the Wolffian duct
in front, but approach close to it at the hinder termination of the groove
(No. 2). The features of the single groove present at this stage agree
closely with those of the anterior groove of the previous stages. The
groove is continued into a duct--the Müllerian duct (as it may now be
called, but in a previous stage the hollow ridge connecting the first and
second grooves of the head-kidney)--which, after becoming nearly separated
from the germinal epithelium, is again connected to it by a mass of cells
at two points (Nos. 5, 6, and 8). The germinal epithelium is slightly
grooved and is much reduced in thickness at these points of contact (_gr_2
and _gr_3), and we believe that they are the remnants of the posterior
grooves of the head-kidney present at an earlier stage.
The Müllerian duct has by this stage grown much further backwards, but the
peculiarities of this part of it are treated in a subsequent section.
We consider that, taking into account the rudiments we have just described,
as well as the fact that the features of the single groove at this stage
correspond with those of the anterior groove at an earlier stage, we are
fully justified in concluding that _the permanent abdominal opening of the
Müllerian duct corresponds with the anterior of our three grooves_.
Although we have, on account of their indefiniteness, avoided giving the
ages of the chicks in which the successive changes of the head-kidney may
be observed, we may, perhaps, state that all the changes we have described
are usually completed between the 90th and 120th hour of incubation.
_The Glomerulus of the Head-Kidney._
In connection with the head-kidney in Amphibians there is present, as is
well known, a peculiar vascular body usually described as the glomerulus of
the head-kidney. We have found in the chick a body so completely answering
to this glomerulus that we have hardly any hesitation in identifying it as
such.
In the chick the glomerulus is paired, and consists of a vascular outgrowth
or ridge projecting into the body-cavity on each side at the root of the
mesentery. It extends from the anterior end of the Wolffian body to the
point where the foremost opening of the head-kidney commences. We have
found it at a period slightly earlier than that of the first development of
the head-kidney. It is represented in figs. E and F, Pl. 28, _gl_, and is
seen to form a somewhat irregular projection into the body-cavity, covered
by a continuation of the peritoneal epithelium, and attached by a narrow
stalk to the insertion of the embryonic mesentery (_me_).
In the interior of this body is seen a stroma with numerous vascular
channels and blood corpuscles, and a vascular connection is apparently
becoming established, if it is not so already, between the glomerulus and
the aorta. We have reason to think that the corpuscles and vascular
channels in the glomerulus are developed _in situ_. The stalk connecting
the glomerulus with the attachment of the mesentery varies in thickness in
different sections, but we believe that the glomerulus is continued
unbroken throughout the very considerable region through which it extends.
This point is, however, difficult to make sure of owing to the facility
with which the glomerulus breaks away.
At the stage we are describing, no true Malpighian bodies are present in
the part of the Wolffian body on the same level with the anterior end of
the glomerulus, but the Wolffian body merely consists of the Wolffian duct.
At the level of the posterior part of the glomerulus this is no longer the
case, but here a regular series of primary Malpighian bodies is present
(using the term "primary" to denote the Malpighian bodies developed
directly out of part of the primary segmental tubes), and the glomerulus of
the head-kidney may frequently be seen in the same section as a Malpighian
body. In most sections the two bodies appear quite disconnected, but in
those sections in which the _glomerulus_ of the Malpighian body comes into
view it is seen to be derived from the same formation as the glomerulus of
the head-kidney (Pl. 28, fig. F). It would seem, in fact, that the vascular
tissue of the glomerulus of the head-kidney grows into the concavity of the
Malpighian bodies. Owing to the stage we are now describing, in which we
have found the glomerulus most fully developed, being prior to that in
which the head-kidney appears, it is not possible to determine with
certainty the position of the glomerulus in relation to the head-kidney.
After the development of the head-kidney it is found, however, as we have
already stated, that the glomerulus terminates at a point just in front of
the anterior opening of the head-kidney. It is less developed than before,
but is still present up to the period of the atrophy of the head-kidney. It
does not apparently alter in constitution, and we have not thought it worth
while giving any further representations of it during the later stages of
its existence.
_Summary of the development of the head-kidney and glomerulus._--The first
rudiment of the head-kidney arises as three successive grooves in the
thickened germinal epithelium, connected by ridges, and situated some way
behind the front end of the Wolffian duct. In the next stage the three
ridges connecting the grooves have become more marked, and in each of them
a lumen has appeared, opening at both extremities into the adjoining
grooves. Still later the ridges become more or less completely detached
from the peritoneal epithelium, and the whole head-kidney then consists of
a slightly convoluted duct, with, at the least, three peritoneal openings,
which is posteriorly continued into the Müllerian duct. Still later the
head-kidney atrophies, its two posterior openings vanishing, and its
anterior opening remaining as the permanent opening of the Müllerian duct.
The glomerulus arises as a vascular prominence at the root of the
mesentery, slightly prior in point of time to the head-kidney, and slightly
more forward than it in position. We have not traced its atrophy.
We stated in our preliminary paper that the peculiar structures we had
interpreted as the head-kidney had completely escaped the attention of
previous observers, though we called attention to a well-known figure of
Waldeyer's (copied in the _Elements of Embryology,_ fig. 51). In this
figure a connection between the germinal epithelium and the Müllerian duct
is drawn, which is probably part of the head-kidney, and may be compared
with our figures (Series B, No. 8, and Series D, No. 4). Since we made the
above statement, Dr Gasser has called our attention to a passage in his
valuable memoir on "The Development of the Allantois[432]," in which
certain structures are described which are, perhaps, identical with our
head-kidney. The following is a translation of the passage:--
"In the upper region of Müller's duct I have often observed small
canals, especially in the later stages of development, which appear as
a kind of doubling of the duct, and run for a short distance close to
Müller's duct and in the same direction, opening, however, into the
body-cavity posterior to the main duct. Further, one may often observe
diverticula from the extreme anterior end of the oviduct of the bird,
which form blind pouches and give one the impression of being
receptacula seminis. Both these appearances can quite well be
accounted for on the supposition that an abnormal communication is
effected between the germinal epithelium and Müller's duct at unusual
places; or else that an attempt at such a communication is made,
resulting, however, only in the formation of a diverticulum of the
wall of the oviduct."
Footnote 432: _Beiträge zur Entwicklungsgeschichte d.
Allantois der Müller'schen Gange u. des Afters._ Frankfurt,
1874.
The statement that these accessory canals are late in developing, prevents
us from feeling quite confident that they really correspond with our
head-kidney.
Before passing on to the other parts of this paper it is necessary to say a
few words in justification of the comparison we have made between the
modified abdominal extremity of the Müllerian duct in the chick and the
head-kidney of the Ichthyopsida.
For the fullest statement of what is known with reference to the anatomy
and development of the head-kidney in the lower types we may refer to
Spengel and Fürbringer[433]. We propose ourselves merely giving a
sufficient account of the head-kidney in Amphibia (which appears to be the
type in which the head-kidney can be most advantageously compared with that
in the bird) to bring out the grounds for our determination of the
homologies.
Footnote 433: _Loc. cit._
The development of the head-kidney in Amphibia has been fully elucidated by
the researches of W. Müller[434], Götte[435], and Fürbringer[436], while to
the latter we are indebted for a knowledge of the development of the
Müllerian duct in Amphibians. The first part of the urinogenital system to
develop is the segmental duct (_Vornieregang_ of Fürbringer), which is
formed by a groove-like invagination of the peritoneal epithelium. It
becomes constricted into a duct first of all in the middle, but soon in the
posterior part also. It then forms a duct, ending in front by a groove in
free communication with the body-cavity, and terminating blindly behind.
The open groove in front at first deepens, and then becomes partially
constricted into a duct, which elongates and becomes convoluted, but
remains in communication with the body-cavity by from two to four
(according to the species) separate openings. The manner in which the
primitive single opening is related to the secondary openings is not fully
understood. By these changes there is formed out of the primitive groove an
anterior glandular body, communicating with the body-cavity by several
apertures, and a posterior duct, which carries off the secretion of the
gland, and which, though blind at first, eventually opens into the cloaca.
In addition to these parts there is also formed on each side of the
mesentery, opposite the peritoneal openings, a very vascular projection
into this part of the body-cavity, which is known as the glomerulus of the
head-kidney, and which very closely resembles in structure and position the
body to which we have assigned the same name in the chick.
Footnote 434: _Jenaische Zeitschrift_, Vol. IX. 1875.
Footnote 435: _Entwicklungsgeschichte d. Unke._
Footnote 436: _Loc. cit._
The primitive segmental duct is at first only the duct for the head-kidney,
but on the formation of the posterior parts of the kidney (Wolffian body,
&c.) it becomes the duct for these also.
After the Wolffian bodies have attained to a considerable development, the
head-kidney undergoes atrophy, and its peritoneal openings become
successively closed from before backwards. At this period the formation of
the Müllerian duct takes place. It is a solid constriction of the ventral
or lateral wall of the segmental duct, which subsequently becomes hollow,
and acquires an opening into the body-cavity _quite independent of the
openings of the head-kidney_.
The similarity in development and structure between the head-kidney in
Amphibia and the body we have identified as such in Aves, is to our minds
too striking to be denied. Both consist of two parts--(1) a somewhat
convoluted longitudinal canal, with a certain number of peritoneal
openings; (2) a vascular prominence at the root of the mesentery, which
forms a glomerulus. As to the identity in position of the two organs we
hope to deal with that more fully in speaking of the general structure of
the excretory system, but may say that one of us[437] has already, on other
grounds, attempted to shew that the abdominal opening of the Müllerian duct
in the bird is the homologue of the abdominal opening of the segmental duct
in Amphibia, Elasmobranchii, &c., and that we believe that this homology
will be admitted by most anatomists. If this homology is admitted, the
identity in position of this organ in Aves and Amphibia necessarily
follows. The most striking difference between Aves and Amphibia in relation
to these structures is the fact that in Aves the anterior pore of the
head-kidney remains as the permanent opening of the Müllerian duct, while
in Amphibia, the pores of the head-kidney atrophy, and an entirely fresh
abdominal opening is formed for the Müllerian duct.
Footnote 437: Balfour, "Origin and History of Urinogenital
Organs of Vertebrates," _Journal of Anat. and Phys._ Vol. X.,
and _Monograph on Elasmobranch Fishes._ [This edition Nos. VII.
and X.]
II.
_The Growth of the Müllerian Duct._
Although a great variety of views have been expressed by different
observers on the growth of the Müllerian duct, it is now fairly generally
admitted that it grows in the space between a portion of the thickened
germinal epithelium and the Wolffian duct, but quite independently of both
of them. Both Braun and Egli, who have specially directed their attention
to this point, have for Reptilia and Mammalia fully confirmed the views of
previous observers. We were, nevertheless, induced, partly on account of
the _à priori_ difficulties of this view, and partly by certain peculiar
appearances which we observed, to undertake the re-examination of this
point, and have found ourselves unable altogether to accept the general
account. We propose first describing, in as matter-of-fact a way as
possible, the actual observations we have made, and then stating what
conclusions we think may be drawn from these observations.
We have found it necessary to distinguish three stages in the growth of the
Müllerian duct. Our first stage embraces the period prior to the
disappearance of the head-kidney. At this stage the structure we have
already spoken of as the rudiment of the Müllerian duct consists of a solid
rod of cells, continuous with the third groove of the head-kidney. It
extends through a very few sections, and terminates by a fine point of
about two cells, wedged in between the Wolffian duct and germinal
epithelium (described above, Nos. 7-10, series A, Plate 27).
In an embryo slightly older than the above, such as that from which series
B was taken, but still belonging to our first stage, a definite lumen
appears in the anterior part of the Müllerian duct, which vanishes after a
few sections. The duct terminates in a point which lies in a concavity of
the wall of the Wolffian duct (Plate 27, Nos. 1 and 2, series G). The
limits of the Wolffian wall and the pointed termination of the Müllerian
duct are in many instances quite distinct; but the outline of the Wolffian
duct appears to be carried round the Müllerian duct, and in some instances
the terminal point of the Müllerian duct seems almost to form an integral
part of the wall of the Wolffian duct.
The second of our stages corresponds with that in which the atrophy of the
head-kidney is nearly complete (series D and H, Plate 28).
The Müllerian duct has by this stage made a very marked progress in its
growth towards the cloaca, and, in contradistinction to the earlier stage,
a lumen is now continued close up to the terminal point of the duct. In the
two or three sections before it ends it appears as a distinct oval mass of
cells (No. 10, series D, and No. 1, series H), without a lumen, lying
between and touching the external wall of the Wolffian duct on the one
hand, and the germinal epithelium on the other. It may either lie on the
ventral side of the Wolffian duct (series D), or on the outer side (series
H), but in either case is opposite the maximum thickening of that part of
the germinal epithelium which always accompanies the Müllerian duct in its
backward growth.
In the last section in which any trace of the Müllerian duct can be made
out (series D, No. 11, and series H, No. 2), it has no longer an oval,
well-defined contour, but appears to have completely fused with the wall of
the Wolffian duct, which is accordingly very thick, and occupies the space
which in the previous section was filled by its own wall and the Müllerian
duct. In the following section the thickening in the wall of the Wolffian
duct has disappeared (Plate 28, series H, No. 3), and every trace of the
Müllerian duct has vanished from view. The Wolffian duct is on one side in
contact with the germinal epithelium.
The stage during which the condition above described lasts is not of long
duration, but is soon succeeded by our third stage, in which a fresh mode
of termination of the Müllerian duct is found. (Plate 28, series I.) This
last stage remains up to about the close of the sixth day, beyond which our
investigations do not extend.
A typical series of sections through the terminal part of the Müllerian
duct at this stage presents the following features:
A few sections before its termination the Müllerian duct appears as a
well-defined oval duct lying in contact with the wall of the Wolffian duct
on the one hand and the germinal epithelium on the other (series I, No. 1).
Gradually, however, as we pass backwards, the Müllerian duct dilates; the
external wall of the Wolffian duct adjoining it becomes greatly thickened
and pushed in in its middle part, so as almost to touch the opposite wall
of the duct, and so form a bay in which the Müllerian duct lies (Plate 28,
series I, Nos. 2 and 3). As soon as the Müllerian duct has come to lie in
this bay its walls lose their previous distinctness of outline, and the
cells composing them assume a curious vacuolated appearance. No
well-defined line of separation can any longer be traced between the walls
of the Wolffian duct and those of the Müllerian, but between the two is a
narrow clear space traversed by an irregular network of fibres, in some of
the meshes of which nuclei are present.
The Müllerian duct may be traced in this condition for a considerable
number of sections, the peculiar features above described becoming more and
more marked as its termination is approached. It continues to dilate and
attains a maximum size in the section or so before it disappears. A lumen
may be observed in it up to its very end, but is usually irregular in
outline and frequently traversed by strands of protoplasm. The Müllerian
duct finally terminates quite suddenly (Plate 28, series I, No. 4), and in
the section immediately behind its termination the Wolffian duct assumes
its normal appearance, and the part of its outer wall on the level of the
Müllerian duct comes into contact with the germinal epithelium (Plate 28,
series I, No. 5).
We have traced the growing point of the Müllerian duct with the above
features till not far from the cloaca, but we have not followed the last
phases of its growth and its final opening into the cloaca.
In some of our embryos we have noticed certain rather peculiar structures,
an example of which is represented at _y_ in fig. K, taken from an embryo
of 123 hours, in which all traces of the head-kidney had disappeared. It
consists of a cord of cells, connecting the Wolffian duct and the hind end
of the abdominal opening of the Müllerian duct. At the least one similar
cord was met with in the same embryo, situated just behind the abdominal
opening of the Müllerian duct. We have found similar structures in other
embryos of about the same age, though never so well marked as in the embryo
from which fig. K is taken. We have quite failed to make out the meaning,
if any, of them.
Our interpretation of the appearances we have described in connection with
the growth of the Müllerian duct can be stated in a very few words. Our
second stage, where the solid point of the Müllerian duct terminates by
fusing with the walls of the Wolffian duct, we interpret as meaning that
the Müllerian is growing backwards as a solid rod of cells, split off from
the outer wall of the Wolffian duct; in the same manner, in fact, as in
Amphibia and Elasmobranchii. The condition of the terminal part of the
Müllerian duct during our third stage cannot, we think, be interpreted in
the same way, but the peculiarities of the cells of both Müllerian and
Wolffian ducts, and the indistinctness of the outlines between them, appear
to indicate that the Müllerian duct grows by cells passing from the
Wolffian duct to it. In fact, although in a certain sense the growth of the
two ducts is independent, yet the actual cells which assist in the growth
of the Müllerian duct are, we believe, derived from the walls of the
Wolffian duct.
III.
_General considerations._
The excretory system of a typical Vertebrate consists of the following
parts:--
1. A head-kidney with the characters already described.
2. A duct for the head-kidney--the segmental duct.
3. A posterior kidney--(Wolffian body, permanent kidney, &c. The nature and
relation of these parts we leave out of consideration, as they have no
bearing upon our present investigations). The primitive duct for the
Wolffian body is the segmental duct.
4. The segmental duct may become split into (_a_) a dorsal or inner duct,
which serves as ureter (in the widest sense of the word); and (_b_) a
ventral or outer duct, which has an opening into the body-cavity, and
serves as the generative duct for the female, or for both sexes.
These parts exhibit considerable variations both in their structure and
development, into some of which it is necessary for us to enter.
The head-kidney[438] attains to its highest development in the
Marsipobranchii (Myxine, Bdellostoma). It consists of a longitudinal canal,
from the ventral side of which numerous tubules pass. These tubules, after
considerable subdivision, open by a large number of apertures into the
pericardial cavity. From the longitudinal canal a few dorsal diverticula,
provided with glomeruli, are given off. In the young the longitudinal canal
is continued into the segmental duct; but this connection becomes lost in
the adult. The head-kidney remains, however, through life. In Teleostei and
Ganoidei (?) the head-kidney is generally believed to remain through life,
as the dilated cephalic portion of the kidneys when such is present. In
Petromyzon and Amphibia the head-kidney atrophies. In Elasmobranchii the
head-kidney, so far as is known, is absent.
Footnote 438: I am inclined to give up the view I formerly
expressed with reference to the head-kidney and segmental duct,
viz. "that they were to be regarded as the most anterior
segmental tube, the peritoneal opening of which had become
divided, and which had become prolonged backwards so as to
serve as the duct for the posterior segmental tubes," and
_provisionally_ to accept the Gegenbaur-Fürbringer view which
has been fully worked out and ably argued for by Fürbringer
(_loc. cit._ p. 96). According to this view the head-kidney and
its duct are to be looked on as the primitive and unsegmented
part of the excretory system, more or less similar to the
excretory system of many Trematodes and unsegmented Vermes. The
segmental tubes I regard as a truly segmental part of the
excretory system acquired subsequently.--F. M. B.
The development of the segmental duct and head-kidney (when present) is
still more important for our purpose than their adult structure.
In Myxine the development of these structures is not known. In Amphibia and
Teleostei it takes place upon the same type, viz. by the conversion of a
groove-like invagination of the peritoneal epithelium into a canal open in
front. The head-kidney is developed from the anterior end of this canal,
the opening of which remains in Teleostei single and closes early in
embryonic life, but becomes in Amphibia divided into two, three, or four
openings. In Elasmobranchii the development is very different.
"The first trace of the urinary system makes its appearance as a knob
springing from the intermediate cell-mass opposite the fifth
protovertebra. This knob is the rudiment of the abdominal opening of
the segmental duct, and from it there grows backwards to the level of
the anus a solid column of cells, which constitutes the rudiment of
the segmental duct itself. The knob projects towards the epiblast, and
the column connected with it lies between the mesoblast and epiblast.
The knob and column do not long remain solid, but the former acquires
an opening into the body-cavity continuous with a lumen, which makes
its appearance in the latter."
The difference in the development of the segmental duct in the two types
(Amphibia and Elasmobranchii) is very important. In the one case a
continuous groove of the peritoneal epithelium becomes constricted into a
canal, in the other a solid knob of cells is continued into a rod, at first
solid, which grows backwards without any apparent relation to the
peritoneal epithelium[439].
Footnote 439: In a note on p. 50 of his memoir Fürbringer
criticises my description of the mode of growth of the
segmental duct. The following is a free translation of what he
says: "In Balfour's, as in other descriptions, an account is
given of a backward growth, which easily leads to the
supposition of a structure formed anteriorly forcing its way
through the tissues behind. This is, however, not the case,
since, to my knowledge, no author has ever detected a sharp
boundary between the growing point of the segmental duct (or
Müllerian duct) and the surrounding tissues." He goes on to say
that "the growth in these cases really takes place by a
differentiation of tissue along a line in the region of the
peritoneal cavity." Although I fully admit that it would be far
easier to homologise the development of the segmental duct in
Amphibia and Elasmobranchii according to this view, I must
nevertheless vindicate the accuracy of my original account. I
have looked over my specimens again, since the appearance of Dr
Fürbringer's paper, and can find no evidence of the end of the
duct becoming continuous with the adjoining mesoblastic
tissues. In the section, before its disappearance, the
segmental duct may, so far as I can make out, be seen as a very
small but distinct rod, which is much more closely connected
with the epiblast than with any other layer. From Gasser's
observations on the Wolffian duct in the bird, I am led to
conclude that it behaves in the same way as the segmental duct
in the Elasmobranchii. I will not deny that it is possible that
the growth of the duct takes place by wandering cells, but on
this point I have no evidence, and must therefore leave the
question an open one.--F. M. B.
The abdominal aperture of the segmental duct in Elasmobranchii, in that it
becomes the permanent abdominal opening of the oviduct, corresponds
physiologically rather with the abdominal opening of the Müllerian duct
than with that of the segmental duct of Amphibia, which, after becoming
divided up to form the pores of the head-kidney, undergoes atrophy.
Morphologically, however, it appears to correspond with the opening of the
segmental duct in Amphibia. We shall allude to this point more than once
again, and give our grounds for the above view on p. 640.
The development of the segmental duct in Elasmobranchii as a solid rod is,
we hope to shew, of special importance for the elucidation of the excretory
system of Aves.
The development of these parts of Petromyzon is not fully known, but from
W. Müller's account (_Jenaische Zeitschrift_, 1875) it would seem that an
anterior invagination of the peritoneal epithelium is continued backwards
as a duct (segmental duct), and that the anterior opening subsequently
becomes divided up into the various apertures of the head-kidney. If this
account is correct, Petromyzon presents a type intermediate between
Amphibia and Elasmobranchii. In certain types, viz. Marsipobranchii and
Teleostei, the segmental duct becomes the duct for the posterior kidney
(segmental tubes), but otherwise undergoes no further differentiation. In
the majority of types, however, the case is different. In Amphibia[440], as
has already been mentioned, a solid rod of cells is split off from its
ventral wall, which afterwards becomes hollow, acquires an opening into the
body-cavity, and forms the Müllerian duct.
Footnote 440: Fürbringer, _loc. cit._
In Elasmobranchii the segmental duct undergoes a more or less similar
division. "It becomes longitudinally split into two complete ducts in the
female, and one complete duct and parts of a second in the male. The
resulting ducts are (1) the Wolffian duct dorsally, which remains
continuous with the excretory tubules of the kidney, and ventrally (2) the
oviduct or Müllerian duct in the female, and the rudiments of this duct in
the male. In the female the formation of these ducts takes place by a
nearly solid rod of cells, being gradually split off from the ventral side
of all but the foremost part of the original segmental duct, with the short
undivided anterior part of which duct it is continuous in front. Into it a
very small portion of the lumen of the original segmental duct is perhaps
continued. The remainder of the segmental duct (after the loss of its
anterior section and the part split off from its ventral side) forms the
Wolffian duct. The process of formation of the ducts in the male chiefly
differs from that in the female, in the fact of the anterior undivided part
of the segmental duct, which forms the front end of the Müllerian duct,
being shorter, and in the column of cells with which it is continuous being
from the first incomplete."
It will be seen from the above that the Müllerian duct consists of two
distinct parts--an anterior part with the abdominal opening, and a
posterior part split off from the segmental duct. This double constitution
of the Müllerian duct is of great importance for a proper understanding of
what takes place in the Bird.
The Müllerian duct appears therefore to develop in nearly the same manner
in the Amphibian and Elasmobranch type, as a solid or nearly solid rod
split off from the ventral wall of the segmental duct. But there is one
important difference concerning the abdominal opening of the duct. In
Amphibia this is a new formation, but in Elasmobranchii it is the original
opening of the segmental duct. Although we admit that in a large number of
points, including the presence of a head-kidney, the urinogenital organs of
Amphibia are formed on a lower type than those of the Elasmobranchii, yet
it appears to us that this does not hold good for the development of the
Müllerian duct.
The above description will, we trust, be sufficient to render clear our
views upon the development of the excretory system in Aves.
In the bird the excretory system consists of the following parts (using the
ordinary nomenclature) which are developed in the order below.
1. Wolffian duct. 2. Wolffian body. 3. Head-kidney. 4. Müllerian duct. 5.
Permanent kidney and ureter.
About 2 and 5 we shall have nothing to say in the sequel.
We have already in the early part of the paper given an account of the
head-kidney and Müllerian duct, but it will be necessary for us to say a
few words about the development of the Wolffian duct (so called). Without
entering into the somewhat extended literature on the subject, we may state
that we consider that the recent paper of Dr Gasser[441] supplies us with
the best extant account of the development of the Wolffian duct.
Footnote 441: _Arch. für Mic. Anat._ Vol. XIV.
The first trace of it, which he finds, is visible in an embryo with eight
protovertebræ as a slight projection from the intermediate cell mass
towards the epiblast in the region of the three hindermost protovertebræ.
In the next stage, with eleven protovertebræ, the solid rudiment of the
duct extends from the fifth to the eleventh protovertebra, from the eighth
to the eleventh protovertebra it lies between the epiblast and mesoblast,
and is quite distinct from both, and Dr Gasser distinctly states that in
its growth backwards from the eighth protovertebra the Wolffian duct never
comes into continuity with the adjacent layers.
In the region of the fifth protovertebra, where the duct was originally
continuous with the mesoblast, it has now become free, but is still
attached in the region of the sixth and to the eighth protovertebra. In an
embryo with fourteen protovertebræ the duct extends from the fourth to the
fourteenth protovertebra, and is now free between epiblast and mesoblast
for its whole extent. It is still for the most part solid though perhaps a
small lumen is present in its middle part. In the succeeding stages the
lumen of the duct gradually extends backwards and forwards, the duct itself
also passes inwards till it acquires its final position close to the
peritoneal epithelium; at the same time its hind end elongates till it
comes into connection with the cloacal section of the hind-gut. It should
be noted that the duct in its backward growth does not appear to come into
continuity with the subjacent mesoblast, but behaves in this respect
exactly as does the segmental duct in Elasmobranchii (vide note on p. 634).
The question which we propose to ourselves is the following:--What are the
homologies of the parts of the Avian urinogenital system above enumerated?
The Wolffian duct appears to us morphologically to correspond _in part_ to
the segmental duct[442], or what Fürbringer would call the duct of the
head-kidney. This may seem a paradox, since in birds it never comes into
relation with the head-kidney. Nevertheless we consider that this homology
is morphologically established, for the following reasons:--
Footnote 442: The views here expressed about the Wolffian duct
are nearly though not exactly those which one of us previously
put forward ("Urinogenital Organs of Vertebrates," &c., pp.
45-46) [This edition, pp. 164, 165], and with which Fürbringer
appears exactly to agree. Possibly Dr Fürbringer would alter
his view on this point were he to accept the facts we believe
ourselves to have discovered. Semper's view also differs from
ours, in that he believes the Wolffian duct to correspond in
its entirety with the segmental duct.
(1) That the Wolffian duct gives rise (vide _supra_, p. 631) to the
Müllerian duct as well as to the duct of the Wolffian body. In this respect
it behaves precisely as does the segmental duct of Elasmobranchii and
Amphibia. That it serves as the duct for the Wolffian body, before the
Müllerian duct originates from it, is also in accordance with what takes
place in other types.
(2) That it develops in a strikingly similar manner to the segmental duct
of Elasmobranchii.
We stated expressly that the Wolffian duct corresponded only in part to the
segmental duct. It does not, in fact, in our opinion, correspond to the
whole segmental duct, but to the segmental duct minus the anterior
abdominal opening in Elasmobranchii, which becomes the head-kidney in other
types. In fact, we suppose that the segmental duct and head-kidney, which
in the Ichthyopsida develop as a single formation, develop in the Bird as
two distinct structures--one of these known as the Wolffian duct, and the
other the head-kidney. If our view about the head-kidney is accepted the
above position will hardly require to be disputed, but we may point out
that the only feature in which the Wolffian duct of the Bird differs in
development from the segmental duct of Elasmobranchii is in the absence of
the knob, which forms the commencement of the segmental duct, and in which
the abdominal opening is formed; so that the comparison of the development
of the duct in the two types confirms the view arrived at from other
considerations.
The head-kidney and Müllerian duct in the Bird must be considered together.
The parts which they eventually give rise to after the atrophy of the
head-kidney have almost universally been regarded as equivalent to the
Müllerian duct of the Ichthyopsida. By Braun[443], however, who from his
researches on the Lizard satisfied himself of the entire independence of
the Müllerian and Wolffian ducts in the Amniota, the Müllerian duct of
these forms is regarded as a completely new structure with no genetic
relations to the Müllerian duct of the Ichthyopsida. Semper[444], on the
other hand, though he accepts the homology of the Müllerian duct in the
Ichthyopsida and Amniota, is of opinion that the anterior part of the
Müllerian duct in the Amniota is really derived from the Wolffian duct,
though he apparently admits the independent growth of the posterior part of
the Müllerian duct. We have been led by our observations, as well as by our
theoretical deductions, to adopt a view exactly the reverse of that of
Professor Semper. We believe that the anterior part of the Müllerian duct
of Aves, which is at first the head-kidney, and subsequently becomes the
abdominal opening of the duct, is developed from the peritoneal epithelium
independently of all other parts of the excretory system; but that the
posterior part of the duct is more or less completely derived from the
walls of the Wolffian duct. This view is clearly in accordance with our
account of the facts of development in Aves, and it fits in very well with
the development of the Müllerian duct in Elasmobranchii. We have already
pointed out that in Elasmobranchii the Müllerian duct is formed of two
factors--(1) of the whole anterior extremity of the segmental duct,
including its abdominal opening; (2) of a rod split off from the ventral
side of the segmental duct. In Birds the anterior part (corresponding to
factor No. 1) of the Müllerian duct has a different origin from the
remainder; so that if the development of the posterior part of the duct
(factor No. 2) were to proceed in the same manner in Birds and
Elasmobranchii, it ought to be formed at the expense of the Wolffian
(_i.e._ segmental) duct, though in connection anteriorly with the
head-kidney. And this is what actually appears to take place.
Footnote 443: "Urogenital-System d. Reptilien," _Arb. aus d.
zool.-zoot. Inst. Würzburg_, Vol. IV.
Footnote 444: _Loc. cit._
So far the homologies of the avian excretory system are fairly clear; but
there are still some points which have to be dealt with in connection with
the permanent opening of the Müllerian duct, and the relatively posterior
position of the head-kidney. With reference to the first of these points
the facts of the case are the following:--
In Amphibia the permanent opening of the Müllerian duct is formed as an
independent opening after the atrophy of the head-kidney.
In Elasmobranchii the original opening of the segmental duct forms the
permanent opening of the Müllerian duct and no head-kidney appears to be
formed.
In Birds the anterior of the three openings of the head-kidney remains as
the permanent opening of the Müllerian duct.
With reference to the difficulties involved in there being apparently three
different modes in which the permanent opening of the Müllerian duct is
formed, we would suggest the following considerations:
The history of the development of the excretory system teaches us that
primitively the segmental duct must have served as efferent duct both for
the generative products and kidney secretion (just as the Wolffian duct
still does for the testicular products and secretion of the Wolffian body
in Elasmobranchii and Amphibia); and further, that at first the generative
products entered the segmental duct from the abdominal cavity by one or
more of the abdominal openings of the kidney (almost certainly of the
head-kidney). That the generative products did not enter the segmental duct
at first by an opening specially developed for them appears to us to follow
from Dohrn's principle of the transmutation of function
(_Functionswechsel_). As a consequence (by a process of natural selection)
of the segmental duct having both a generative and a urinary function, a
further differentiation took place, by which that duct became split into
two--a ventral Müllerian duct and dorsal Wolffian duct.
The Müllerian duct without doubt was continuous with the head-kidney, and
so with the abdominal opening or openings of the head-kidney which served
as generative pores. At first the segmental duct was probably split
longitudinally into two equal portions, but the generative function of the
Müllerian duct gradually impressed itself more and more upon the embryonic
development, so that, in the course of time, the Müllerian duct developed
less and less at the expense of the Wolffian duct. This process appears
partly to have taken place in Elasmobranchii, and still more in Amphibia;
the Amphibia offering in this respect a less primitive condition than
Elasmobranchii; while in Aves it has been carried even further. The
abdominal opening no doubt also became specialised. At first it is quite
possible that more than one abdominal pore may have served for the
generative products; one of which, no doubt, eventually came to function
alone. In Amphibia the specialisation of the opening appears to have gone
so far that it no longer has any relation to the head-kidney, and even
develops after the atrophy of the head-kidney. In Elasmobranchii, on the
other hand, the functional opening appears at a period when we should
expect the head-kidney to develop. This state is very possibly the result
of a differentiation (along a different line to that in Amphibia) by which
the head-kidney gradually ceased to become developed, but by which the
primitive opening (which in the development of the head-kidney used to be
divided into several pores leading into the body-cavity) remained undivided
and served as the abdominal aperture of the Müllerian duct. Aves, finally,
appear to have become differentiated along a third line; since in their
ancestors the anterior pore of the head-kidney appears to have become
specialised as the permanent opening of the Müllerian duct.
With reference to the posterior position of the head-kidney in Aves we have
only to remark, that a change in position of the head-kidney might easily
take place after it acquired an independent development. The fact that it
is slightly behind the glomerulus would seem to indicate, on the one hand,
that it has already ceased to be of any functional importance; and, on the
other, that the shifting has been due to its having a connection with the
Müllerian duct.
We have made a few observations on the development of the Müllerian duct in
_Lacerta muralis_, which have unfortunately led us to no decided
conclusions. In a fairly young stage in the development of the Müllerian
duct (the youngest we have met with), no trace of a head-kidney could be
observed, but the character of the abdominal opening of the Müllerian duct
was very similar to that figured by Braun[445]. As to the backward growth
of the Müllerian duct, we can only state that the solid point of the duct
in the young stages is in contact with the wall of the Wolffian duct, and
the relation between the two is rather like that figured by Fürbringer
(Pl. 1, figs. 14-15) in Amphibia.
Footnote 445: _Loc. cit._
DESCRIPTION OF PLATES 27 AND 28.
COMPLETE LIST OF REFERENCE LETTERS.
_ao._ Aorta. _cv._ Cardinal vein. _gl._ Glomerulus. _gr_1. First groove of
head-kidney. _gr_2. Second groove of head-kidney. _gr_3. Third groove of
head-kidney. _ge._ Germinal epithelium. _mrb._ Malpighian body. _me._
Mesentery. _md._ Müllerian duct. _r_1. First ridge of head-kidney. _r_2.
Second ridge of head-kidney. _r_3. Third ridge of head-kidney. _Wd._
Wolffian duct. _x._ Fold in germinal epithelium.
PLATE 27.
SERIES A. Sections through the head-kidney at our second stage. Zeiss 2,
ocul. 3 (reduced one-third). The second and third grooves are represented
with the ridge connecting them, and the rod of cells running backwards for
a short distance.
No. 1. Section through the second groove.
No. 2. Section through the ridge connecting the second and third grooves.
No. 3. Section passing through the same ridge at a point nearer the third
groove.
Nos. 4, 5, 6. Sections through the third groove.
No. 7. Section through the point where the third groove passes into the
solid rod of cells.
No. 8. Section through the rod when quite separated from the germinal
epithelium.
No. 9. Section very near the termination of the rod.
No. 10. Last section in which any trace of the rod is seen.
SERIES B. Sections passing through the head-kidney at our third stage.
Zeiss C, ocul. 2. Our figures are representations of the following sections
of the series, section 1 being the first which passes through the anterior
groove of the head-kidney.
No. 1 SECTION 3. No. 8 SECTION 13.
" 2 " 4. " 9 " 15.
" 3 " 5. " 10 " 16.
" 4 " 6. " 11 " 17.
" 5 " 8. " 12 " 18.
" 6 " 10. " 13 " 19.
" 7 " 11. " 14 " 20.
The Müllerian duct extends through eleven more sections.
The first groove (_gr_1.) extends to No. 3.
The second groove (_gr_2.) extends from No. 4 to No. 7.
The third groove (_gr_3.) extends from No. 11 to No. 13.
The first ridge (_r_1.) extends from No. 2 to No. 5.
The second ridge (_r_2.) extends from No. 8 to No. 11.
The third ridge (_r_3.) extends from No. 13 backwards through twelve
sections, when it terminates by a pointed extremity.
FIG. C. Section through the ridge connecting the second and third grooves
of the head-kidney of an embryo slightly younger than that from which
Series B was taken. Zeiss C, ocul. 3 (reduced one-third).
The fold of the germinal epithelium, which gives rise to a deep groove
(_x._) external to the head-kidney is well marked.
SERIES G. Sections through the rod of cells constituting the termination of
the Müllerian duct at a stage in which the head-kidney is still present.
Zeiss C, ocul. 2.
PLATE 28.
SERIES D. Sections chosen at intervals from a complete series traversing
the peritoneal opening of the Müllerian duct, the remnant of the
head-kidney, and the termination of the Müllerian duct. Zeiss C, ocul. 3
(reduced one-third).
Nos. 1 and 2. Sections through the persistent anterior opening of the
head-kidney (abdominal opening of Müllerian duct). The approach of the
Wolffian duct to the groove may be seen by a comparison of these two
figures. In the sections in front of these (not figured) the two are much
more widely separated than in No. 1.
No. 3. Section through the Müllerian duct, just posterior to the persistent
opening.
Nos. 4 and 5. Remains of the ridges, which at an earlier stage connected
the first and second grooves, are seen passing from the Müllerian duct to
the peritoneal epithelium.
No. 6. Rudiment of the second groove (_gr_2.) of the head-kidney.
Between 6 and 7 is a considerable interval.
No. 7. All traces of this groove (_gr_2.) have vanished, and the Müllerian
duct is quite disconnected from the epithelium.
No. 8. Rudiment of the third groove (_gr_3.).
No. 9. Müllerian duct quite free in the space between the peritoneal
epithelium and the Wolffian duct, in which condition it extends until near
its termination. Between Nos. 9 and 10 is an interval of eight sections.
No. 10. The penultimate section, in which the Müllerian duct is seen. A
lumen cannot be clearly made out.
No. 11. The last section in which any trace of the Müllerian duct is
visible. No line of demarcation can be seen separating the solid end of the
Müllerian duct from the ventral wall of the Wolffian duct.
FIGS. E. and F. Sections through the glomerulus of the head-kidney from an
embryo prior to the appearance of the head-kidney. Zeiss B, ocul. 2. A
comparison of the two figures shows the variation in the thickness of the
stalk of the glomerulus. E. Section anterior to the foremost Malpighian
body. F. Section through both the glomerulus of the head-kidney and that of
a Malpighian body. The two are seen to be connected.
SERIES H. Consecutive sections through the hind end of the Müllerian duct,
from an embryo in which the head-kidney was only represented by a rudiment.
(The embryo was, perhaps, very slightly older than that from which Series D
was taken.) Zeiss C, ocul. 3 (reduced one-third).
No. 1. Müllerian duct is without a lumen, and quite distinct from the
Wolffian wall.
No. 2. The solid end of the Müllerian duct is no longer distinct from the
internal wall of the Wolffian duct.
No. 3. All trace of the Müllerian duct has vanished.
SERIES I. Sections through the hinder end of the Müllerian duct from an
embryo of about the middle of the sixth day. Zeiss C, ocul. 2 (reduced
one-third).
No. 1. The Müllerian duct is distinct and small.
No. 2. Is posterior by twelve sections to No. 1. The Müllerian duct is
dilated, and its cells are vacuolated.
No. 3. Penultimate section, in which the Müllerian duct is visible; it is
separated by three sections from No. 2.
No. 4. Last section in which any trace of the Müllerian duct is visible;
the lumen, which was visible in the previous section, is now absent.
No. 5. No trace of Müllerian duct. Nos. 3, 4, and 5 are consecutive
sections.
FIG. K. Section through the hind end of the abdominal opening of the
Müllerian duct of a chick of 123 hours. Zeiss C, ocul. 2 (reduced
one-third). It illustrates the peculiar cord connecting the Müllerian and
Wolffian ducts.
XIV. ON THE EARLY DEVELOPMENT OF THE LACERTILIA, TOGETHER WITH SOME
OBSERVATIONS ON THE NATURE AND RELATIONS OF THE PRIMITIVE STREAK[446].
Footnote 446: From the _Quarterly Journal of Microscopical
Science_, Vol. XIX. 1879.
(With Plate 29.)
Till quite recently no observations were recorded on the early
developmental changes of the reptilian ovum. Not long ago Professors
Kupffer and Benecke published a preliminary note on the early development
of _Lacerta agilis_ and _Emys Europea_[447]. I have myself also been able
to make some observations on the embryo of _Lacerta muralis_. The number of
my embryos has been somewhat limited, and most of those which I have had
have been preserved in bichromate of potash, which has turned out a far
from satisfactory hardening reagent. In spite of these difficulties I have
been led on some points to very different results from those of the German
investigators, and to results which are more in accordance with what we
know of other Sauropsidan types. I commence with a short account of the
results of Kupffer and Benecke.
Footnote 447: _Die Erste Entwicklungsvorgänge am Ei der
Reptilien_, Königsberg, 1878.
Segmentation takes place exactly as in birds, and the resulting blastoderm,
which is thickened at its edge, spreads rapidly over the yolk. Shortly
before the yolk is half enclosed a small embryonic shield (area pellucida)
makes its appearance in the centre of the blastoderm, which has, in the
meantime, become divided into two layers. The upper of these is the
epiblast, and the lower the hypoblast. The embryonic shield is mainly
distinguished from the remainder of the blastoderm by the more columnar
character of its constituent epiblast cells. It is somewhat pyriform in
shape, the narrower end corresponding with the future posterior end of the
embryo. At the narrow end an invagination takes place, which gives rise to
an open sac, the blind end of which is directed forwards. The opening of
this sac is regarded by the authors as the blastopore. A linear thickening
of epiblast arises in front of the blastopore, along the median line of
which the medullary groove soon appears. In the caudal region the medullary
folds spread out and enclose between them the blastopore, behind which they
soon meet again. On the conversion of the medullary groove into a closed
canal the blastopore becomes obliterated. The mesoblast grows out from the
lip of the blastopore as four masses. Two of these are lateral: a third is
anterior and median, and, although at first independent of the epiblast,
soon attaches itself to it, and forms with it a kind of axis-cord. A fourth
mass applied itself to the walls of the sac formed by invagination.
With reference to the very first developmental phenomena my observations
are confined to two stages during the segmentation[448]. In the earliest of
these the segmentation was about half completed, in the later one it was
nearly over. My observations on these stages bear out generally the
statements of Kupffer and Benecke. In the second of them the blastoderm was
already imperfectly divided into two layers--a superficial epiblastic layer
formed of a single row of cells, and a layer below this several rows deep.
Below this layer fresh segments were obviously being added to the
blastoderm from the subjacent yolk.
Footnote 448: For these two specimens, which were hardened in
picric acid, I am indebted to Dr Kleinenberg.
Between the second of these blastoderms and my next stage there is a
considerable gap. The medullary plate is just established, and is marked by
a shallow groove which becomes deeper in front. A section through the
embryo is represented in Pl. 29, Series A, fig. 1. In this figure there may
be seen the thickened medullary plate with a shallow medullary groove,
below which are two independent plates of mesoblast (_me.p._), one on each
side of the middle line, very imperfectly divided into somatopleuric and
splanchnopleuric layers. Below the mesoblast is a continuous layer of
hypoblast (_hy._), which develops a rod-like thickening along the axial
line (_ch._). This rod becomes in the next stage the notochord. Although
this embryo is not well preserved I feel very confident in asserting the
continuity of the notochord with the hypoblast at this stage.
At the hind end of the embryo is placed a thickened ridge of tissue which
continues the embryonic axis. In this ridge all the layers coalesce, _and I
therefore take it to be equivalent to the primitive streak of the avian
blastoderm_. It is somewhat triangular in shape, with the apex directed
backward, the broad base placed in front.
At the junction between the primitive streak and the blastoderm is situated
a passage, open at both extremities, leading from the upper surface of the
blastoderm obliquely forwards to the lower.
The dorsal and anterior wall of this passage is formed of a distinct
epithelial layer, continuous at its upper extremity with the epiblast, and
at its lower with the notochordal plate, so that it forms a layer of cells
connecting together the epiblast and hypoblast. The hinder and lower wall
of the passage is formed by the cells of the primitive streak, which only
assume a columnar form near the dorsal opening of the passage (vide
fig. 4). This passage is clearly the blind sac of Kupffer and Benecke, who,
if I am not mistaken, have overlooked its lower opening. As I hope to show
in the sequel, it is also the equivalent of the neurenteric passage, which
connects the neural and alimentary canals in the Ichthyopsida, and
therefore represents the blastopore of Amphioxus, Amphibians, &c.
Series A, figs. 2, 3, 4, 5, illustrate the features of the passage and its
relation to the embryo.
Fig. 2 passes through the ventral opening of the passage. The notochordal
plate (_ch´._) is vaulted over the opening, and on the left side is
continuous with the mesoblast as well as the hypoblast. Figs. 3 and 4 are
taken through the middle part of the passage (_ne._), which is bounded
above by a continuation of the notochordal plate, and below by the tissue
of the primitive streak. The hypoblast (_hy._), in the middle line, is
imperfectly fused with the mesoblast of the primitive streak, which is now
continuous across the middle line. The medullary groove has disappeared,
but the medullary plate (_mp._) is quite distinct.
In fig. 5 is seen the dorsal opening of the passage (_ne._). If a section
behind this had been figured, as is done for the next series (B), it would
have passed through the primitive streak, and, as in the chick, all the
layers would have been fused together. The epiblast in the primitive streak
completely coalesces with the mesoblast; but the hypoblast, though attached
to the other layers in the middle line, can always be traced as a distinct
stratum.
Fig. B is a surface view of my next oldest embryo. The medullary groove has
become much deeper, especially in front. Behind it widens out to form a
space equivalent to the sinus rhomboidalis of the embryo bird. The amnion
forms a small fold covering over the cephalic extremity of the embryo,
which is deeply embedded in the yolk. Some somites (protovertebræ) were
probably present, but this could not be made out in the opaque embryo.
[Illustration: FIG. 1. Diagrammatic longitudinal section of an embryo of
Lacerta. _pp._ body-cavity. _am._ Amnion. _ne._ Neurenteric canal. _ch._
Notochord. _hy._ Hypoblast. _ep._ Epiblast. _pr._ Primitive streak.]
The woodcut (fig. 1) represents a diagrammatic longitudinal section through
this embryo, and the sections belonging to Series B illustrate the features
of the hind end of the embryo and of the primitive streak.
As is shown in fig. 1, the notochord (_ch._) has now throughout the region
of the embryo become separated from the subjacent hypoblast, and the
lateral plates of mesoblast are distinctly divided into somatic and
splanchnic layers. The medullary groove is continued as a deepish groove up
to the opening of the neurenteric passage, which thus forms a perforation
in the floor of the hinder end of the medullary groove (vide Series B,
figs. 2, 3, and 4).
The passage itself is somewhat shorter than in the previous stage, and the
whole of it is shown in a single section (fig. 4). This section must either
have been taken somewhat obliquely, or else the passage have been
exceptionally short in this embryo, since in an older embryo it could not
all be seen in one section.
The front wall of the passage is continuous with the notochord, which for
two sections or so in front remains attached to the hypoblast (figs. 2 and
3). Behind the perforation in the floor of the medullary groove is placed
the primitive streak (fig. 5), where all the layers become fused together,
as in the earlier stage. Into this part a narrow diverticulum from the end
of the medullary groove is continued for a very short distance (vide
fig. 5, _mc._).
The general features of the stage will best be understood by an examination
of the diagrammatic longitudinal section, represented in woodcut, fig. 1.
In front is shown the amnion (_am._), growing over the head of the embryo.
The notochord (_ch._) is seen as an independent cord for the greater part
of the length of the embryo, but falls into the hypoblast shortly in front
of the neurenteric passage. The neurenteric passage is shown at _ne._, and
behind it is shown the primitive streak.
In a still older stage, represented in surface view on Pl. 29, fig. C, the
medullary folds have nearly met above, but have not yet united. The
features of the passage from the neural groove to the hypoblast are
precisely the same in the embryo just described, although the lumen of the
passage has become somewhat narrower. There is still a short primitive
streak behind the embryo.
The neurenteric passage persists but a very short time after the complete
closure of the medullary canal. It is in no way connected with the
allantois, as conjectured by Kupffer and Benecke, but the allantois is
formed, as I have satisfied myself by longitudinal sections of a later
stage, in the manner already described by Dobrynin, Gasser, and Kölliker
for the bird and mammal.
The general results of Kupffer's and Benecke's observations, with the
modifications introduced by my own observations, are as follows:--After the
segmentation and the formation of the embryonic shield (area pellucida) the
blastoderm becomes distinctly divided into epiblast and hypoblast[449]. At
the hind end of the shield a somewhat triangular primitive streak is formed
by the fusion of the epiblast and hypoblast with a number of cells between
them, which are probably derived from the lower rows of the segmentation
cells. At the front end of the streak a passage arises, open at both
extremities, leading obliquely forwards through the epiblast to the space
below the hypoblast. The walls of the passage are formed of a layer of
columnar cells continuous both with epiblast and hypoblast. In front of the
primitive streak the body of the embryo becomes first differentiated by the
formation of a medullary plate, and at the same time there grows out from
the primitive streak a layer of mesoblast, which spreads out in all
directions between the epiblast and hypoblast. In the axis of the embryo
the mesoblast plate is stated by Kupffer and Benecke to be continuous
across the middle line, but this appears very improbable. In a slightly
later stage the medullary plate becomes marked by a shallow groove, and the
mesoblast of the embryo is then undoubtedly constituted of two lateral
plates, one on each side of the median line. In the median line the
notochord arises as a ridge-like thickening of the hypoblast, which becomes
very soon quite separated from the hypoblast, except at the hind end, where
it is continued into the front wall of the neurenteric passage. It is
interesting to notice the remarkable relation of the notochord to the walls
of the neurenteric passage. More or less similar relations are also well
marked in the case of the goose and the fowl (Gasser)[450], and support the
conclusion deducible from the lower forms of vertebrata, that the notochord
is essentially hypoblastic.
Footnote 449: This appears to me to take place before the
formation of the embryonic shield.
Footnote 450: Gasser, _Der Primitivstreifen bei
Vogelembryonen_, Marburg, 1878.
The passage at the front end of the primitive streak forms the posterior
boundary of the medullary plate, though the medullary groove is not at
first continued back to it. The anterior wall of this passage connects
together the medullary plate and the notochordal ridge of the hypoblast. In
the succeeding stages the medullary groove becomes continued back to the
opening of the passage, which then becomes enclosed in the medullary folds,
and forms a true neurenteric passage. It becomes narrowed as the medullary
folds finally unite to form the medullary canal, and eventually disappears.
I conclude this paper with a concise statement of what appears to me the
probable nature of the much-disputed organ, the primitive streak, and of
the arguments in support of my view.
In a paper on the primitive streak in the _Quart. Journ. of Mic. Sci._, in
1873 (p. 280) [This edition, p. 45], I made the following statement with
reference to this subject:--"It is clear, therefore, that the primitive
groove must be the rudiment of some ancestral feature.... It is just
possible that it is the last trace of that involution of the epiblast by
which the hypoblast is formed in most of the lower animals."
At a later period, in July, 1876, after studying the development of
Elasmobranch fishes, I enlarged the hypothesis in a review of the first
part of Prof. Kölliker's _Entwicklungsgeschichte_. The following is the
passage in which I speak of it[451]:
Footnote 451: _Journal of Anat. and Phys._, Vol. X. pp. 790
and 791. Compare also my _Monograph on Elasmobranch Fishes_,
note on p. 68 [This edition, p. 281].
"In treating of the exact relation of the primitive groove to the
formation of the embryo, Professor Kölliker gives it as his view that
though the head of the embryo is formed independently of the primitive
groove, and only secondarily unites with this, yet that the remainder
of the body is without doubt derived from the primitive groove. With
this conclusion we cannot agree, and the very descriptions of
Professor Kölliker appear to us to demonstrate the untenable nature of
his results. We believe that the front end of the primitive groove at
first occupies the position eventually filled by about the third pair
of protovertebræ, but that as the protovertebræ are successively
formed, and the body of the embryo grows in length, the primitive
groove is carried further and further back, so as always to be
situated immediately behind the embryo. As Professor Kölliker himself
has shewn it may still be seen in this position even later than the
fortieth hour of incubation.
"Throughout the whole period of its existence it retains a character
which at once distinguishes it in sections from the medullary groove.
"Beneath it the epiblast and mesoblast are _always fused_, though they
are always separate elsewhere; this fact, which was originally shewn
by ourselves, has been very clearly brought out by Professor
Kölliker's observations.
"The features of the primitive groove which throw special light on its
meaning are the following:--
"(1) It does not enter directly into the formation of the embryo.
"(2) The epiblast and mesoblast always become fused beneath it.
"(3) It is situated immediately behind the embryo.
"Professor Kölliker does not enter into any speculations as to the
meaning of the primitive groove, but the above-mentioned facts appear
to us clearly to prove that the primitive groove is a rudimentary
structure, the origin of which can only be completely elucidated by a
knowledge of the development of the Avian ancestors.
"In comparing the blastoderm of a bird with that of any anamniotic
vertebrate, we are met at the threshold of our investigations by a
remarkable difference between the two. Whereas in all the lower
vertebrates the embryo is situated at the _edge_ of the blastoderm, it
is in birds and mammals situated in the centre. This difference of
position at once suggests the view that the primitive groove may be in
some way connected with the change of position in the blastoderm which
the ancestors of birds must have undergone. If we carry our
investigations amongst the lower vertebrates a little further, we find
that the Elasmobranch embryo occupies at first the normal position at
the edge of the blastoderm, but that in the course of development the
blastoderm grows round the yolk far more slowly in the region of the
embryo than elsewhere. Owing to this, the embryo becomes left in a
bay, the two sides of which eventually meet and coalesce in a linear
fashion immediately behind the embryo, thus removing the embryo from
the edge of the blastoderm and forming behind it a linear streak not
unlike the primitive streak. We would suggest the hypothesis that the
primitive groove is a rudiment which gives the last indication of a
change made by the Avian ancestors in their position in the
blastoderm, like that made by Elasmobranch embryos when removed from
the edge of the blastoderm and placed in a central situation similar
to that of the embryo bird. On this hypothesis the situation of the
primitive groove immediately behind the embryo, as well as the fact of
its not becoming converted into any embryonic organ would be
explained. The central groove might probably also be viewed as the
groove naturally left between the coalescing edges of the blastoderm.
"Would the fusion of epiblast and mesoblast also receive its
explanation on this hypothesis? We are of opinion that it would. At
the edge of the blastoderm which represents the blastopore mouth of
Amphioxus all the layers become fused together in the anamniotic
vertebrates. So that if the primitive groove is in reality a rudiment
of the coalesced edges of the blastoderm, we might naturally expect
the layers to be fused there, and the difficulty presented by the
present condition of the primitive groove would rather be that the
hypoblast is not fused with the other layers than that the mesoblast
is indissolubly united with the epiblast. The fact that the hypoblast
is not fused with the other layers does not appear to us to be fatal
to our hypothesis, and in Mammalia, where the primitive and medullary
grooves present precisely the same relations as in birds, all three
layers are, according to Hensen's account, fused together. This,
however, is denied by Kölliker, who states that in Mammals, as in
Birds, only the epiblast and mesoblast fuse together. Our hypothesis
as to the origin of the primitive groove appears to explain in a
fairly satisfactory manner all the peculiarities of this very
enigmatical organ; it also relieves us from the necessity of accepting
Professor Kölliker's explanation of the development of the mesoblast,
though it does not, of course, render that explanation in any way
untenable."
At a somewhat later period Rauber arrived at a more or less similar
conclusion, which, however, he mixes up with a number of opinions from
which I am compelled altogether to dissent[452].
Footnote 452: "Primitivrinne u. Urmund," _Morphologisches
Jahrbuch_, Band II. p. 551.
The general correctness of my view, as explained in my second quotation,
appears to me completely established by Gasser's beautiful researches on
the early development of the chick and goose[453], and by my own
observations just recorded on the lizard. While at the same time the
parallel between the blastopore of Elasmobranchii and of the Sauropsida, is
rendered more complete by the discovery of the neurenteric passage in the
latter group, which was first of all made by Gasser.
Footnote 453: Gasser, _Der Primitivstreifen bei
Vogelembryonen_, Marburg, 1878.
The following paragraphs contain a detailed attempt to establish the above
view by a careful comparison of the primitive streak and its adjuncts in
the amniotic vertebrates with the blastopore in Elasmobranchii.
In Elasmobranchii the blastopore consists of the following parts:--(1), a
section at the end of the medullary plate, which becomes converted into the
neurenteric canal[454]; (2), a section forming what may be called the yolk
blastopore, which eventually constitutes a linear streak connecting the
embryo with the edge of the blastoderm (vide monograph on Elasmobranch
fishes, pp. 281 and 296). In order to establish my hypothesis on the nature
of the primitive streak, it is necessary to find the representatives of
both these parts in the primitive streak of the amniotic vertebrates. The
first section ought to appear as a passage from the neural to the enteric
side of the blastoderm at the posterior end of the medullary plate. At its
front edge the epiblast and hypoblast should be continuous, as they are at
the hind end of the embryo in Elasmobranchii, and, finally, the passage
should, on the closure of the medullary groove, become converted into the
_neurenteric canal_. All these conditions are exactly fulfilled by the
opening at the front end of the primitive streak of the lizard (vide
woodcut, fig. 1, p. 647). In the chick there is at first no such opening,
but, as I hope to shew in a future paper, it is replaced by the epiblast
and hypoblast falling into one another at the front end of the primitive
streak. At a later period, as has been shewn by Gasser[455], there is a
distinct rudiment of the neurenteric canal in the chick, and a complete
canal in the goose. Finally, in mammals, as has been shewn by Schäffer[456]
for the guinea-pig, there is at the front end of the primitive streak a
complete continuity between epiblast and hypoblast. The continuity of the
epiblast and hypoblast at the hind end of the embryo in the bird and the
mammal is a rudiment of the continuity of these layers at the dorsal lip of
the blastopore in Elasmobranchii, Amphibia, &c. The second section of the
blastopore in Elasmobranchii or yolk blastopore is, I believe, partly
represented by the primitive streak. The yolk blastopore in Elasmobranchii
is the part of the blastopore belonging to the yolk sac as opposed to that
belonging to the embryo, and it is clear that the primitive streak cannot
correspond to the whole of this, since the primitive streak is far removed
from the edge of the blastoderm long before the yolk is completely
enclosed. Leaving this out of consideration the primitive streak, in order
that the above comparison may hold good, should satisfy the following
conditions:
Footnote 454: I use this term for the canal connecting the
neural and alimentary tract, which was first discovered by
Kowalevsky.
Footnote 455: _Loc. cit._
Footnote 456: "A contribution to the history of the
development in the Guinea-pig," _Journal of Anat. and Phys._
Vol. XI. pp. 332-336.
1. It should connect the embryo with the edge of the blastoderm.
2. It should be constituted as if formed of the fused edges of the
blastoderm.
3. The epiblast of it should eventually not form part of the medullary
plate of the embryo, but be folded over on to the ventral side.
The first of these conditions is only partially fulfilled, but, considering
the rudimentary condition of the whole structure, no great stress can, it
seems to me, be laid on this fact.
The second condition seems to me very completely satisfied. Where the two
edges of the blastoderm become united we should expect to find a complete
fusion of the layers such as takes place in the primitive streak; and the
fact that in the primitive streak the hypoblast does not so distinctly
coalesce with the mesoblast as the mesoblast with the epiblast cannot be
urged as a serious argument against me.
The growth outwards of the mesoblast from the axis of the primitive streak
is probably a remnant of the invagination of the hypoblast and mesoblast
from the lip of the blastopore in Amphibia, &c.
The groove in the primitive streak may with great plausibility be regarded
as the indication of a depression which would naturally be found along the
line where the thickened edges of the blastoderm became united.
With reference to the third condition, I will make the following
observations. The neurenteric canal, as it is placed at the extreme end of
the embryo, must necessarily, with reference to the embryo, be the
hindermost section of the blastopore, and therefore the part of the
blastopore apparently behind this can only be so owing to the embryo not
being folded off from the yolk sac; and as the yolk sac is in reality a
specialised part of the ventral wall of the body, the yolk blastopore must
also be situated on the ventral side of the embryo.
Kölliker and other distinguished embryologists have believed that the
epiblast of the whole of the primitive streak became part of the neural
plate. If this view were correct, which is accepted even by Rauber, the
hypothesis I am attempting to establish would fall to the ground. I have,
however, no doubt that these embryologists are mistaken. The very careful
observations of Gasser shew that the part of the primitive streak adjoining
the embryo becomes converted into the tail-swelling, and that the posterior
part is folded in on the ventral side of the embryo, and, losing its
characteristic structure, forms part of the ventral wall of the body. On
this point my own observations confirm those of Gasser. In the lizard the
early appearance of the neurenteric canal at the front end of the primitive
streak clearly shews that here also the primitive streak can take no share
in forming the neural plate.
The above considerations appear to me sufficient to establish my hypothesis
with reference to the nature of the primitive streak, which has the merit
of explaining, not only the structural peculiarities of the primitive
streak, but also the otherwise inexplicable position of the embryo of the
amniotic vertebrates in the centre of the blastoderm.
DESCRIPTION OF PLATE 29.
COMPLETE LIST OF REFERENCE LETTERS.
_am._ Amnion. _ch._ Notochord. _ch´._ Notochordal thickening of hypoblast.
_ep._ Epiblast. _hy._ Hypoblast. _m.g._ Medullary groove. _me.p._
Mesoblastic plate. _ne._ Neurenteric canal (blastopore). _pr._ Primitive
streak.
SERIES A. Sections through an embryo shortly after the formation of the
medullary groove. x 120[457].
Footnote 457: The spaces between the layers in these sections
are due to the action of the hardening reagent.
Fig. 1. Section through the trunk of the embryo.
Figs. 2-5. Sections through the neurenteric canal.
Fig. B. Surface view of a somewhat older embryo than that from which Series
A is taken. x 30.
SERIES B. Sections through the embryo represented in Fig. B. x 120.
Fig. 1. Section through the trunk of the embryo.
Figs. 2, 3. Sections through the hind end of the medullary groove.
Fig. 4. Section through the neurenteric canal.
Fig. 5. Section through the primitive streak.
Fig. C. Surface view of a somewhat older embryo than that represented in
Fig. B. x 30.
XV. ON CERTAIN POINTS IN THE ANATOMY OF PERIPATUS CAPENSIS[458].
Footnote 458: From the _Proceedings of the Cambridge
Philosophical Society_, Vol. III. 1879.
The discovery by Mr Moseley[459] of a tracheal system in Peripatus must be
reckoned as one of the most interesting results obtained by the naturalists
of the "Challenger." The discovery clearly proves that the genus Peripatus,
which is widely distributed over the globe, is the persisting remnant of
what was probably a large group of forms, from which the present tracheate
Arthropoda are descended.
Footnote 459: "On the Structure and Development of _Peripatus
Capensis_," _Phil. Trans._, Vol. CLXIV. 1874.
The affinities of Peripatus render any further light on its anatomy a
matter of some interest; and through the kindness of Mr Moseley I have had
an opportunity of making investigations on some well preserved examples of
_Peripatus capensis_, a few of the results of which I propose to lay before
the Society.
I shall confine my observations to three organs. (1) The segmental organs,
(2) the nervous system, (3) the so-called fat bodies of Mr Moseley.
In all the segments of the body, with the exception of the first two or
three postoral ones, there are present glandular bodies, apparently
equivalent to the segmental organs of Annelids.
These organs have not completely escaped the attention of previous
observers. The anterior of them were noticed by Grube[460], but their
relations were not made out. By Saenger[461], as I gather from Leuckart's
_Bericht_ for the years 1868-9, these structures were also noticed, and
they were interpreted as segmental organs. Their external openings were
correctly identified. They are not mentioned by Moseley, and no notice of
them is to be found in the text-books. The observations of Grube and
Saenger seem, in fact, to have been completely forgotten.
Footnote 460: "Bau von _Perip. Edwardsii_," _Archiv f. Anat.
u. Phys._ 1853.
Footnote 461: _Moskauer Naturforscher Sammlung_, Abth. Zool.
1869.
The organs are placed at the bases of the feet in two lateral divisions of
the body-cavity shut off from the main central median division of the
body-cavity by longitudinal septa of transverse muscles.
Each fully developed organ consists of three parts:
(1) A dilated vesicle opening externally at the base of a foot.
(2) A coiled glandular tube connected with this and subdivided again into
several minor divisions.
(3) A short terminal portion opening at one extremity into the coiled tube
(2) and at the other, as I believe, into the body-cavity. This section
becomes very conspicuous in stained preparations by the intensity with
which the nuclei of its walls absorb the colouring matter.
The segmental organs of Peripatus, though formed on a type of their own,
more nearly resemble those of the Leech than of any other form with which I
am acquainted. The annelidan affinities shewn by their presence are of some
interest. Around the segmental organs in the feet are peculiar cells richly
supplied with tracheæ, which appear to me to be similar to the fat bodies
in insects. There are two glandular bodies in the feet in addition to the
segmental organs.
The more obvious features of the nervous system have been fully made out by
previous observers, who have shewn that it consists of large paired
supra-oesophageal ganglia connected with two widely separated ventral
cords--stated by them not to be ganglionated. Grube describes the two cords
as falling into one another behind the anus--a feature the presence of
which is erroneously denied by Saenger. The lateral cords are united by
numerous (5 or 6 for each segment) transverse cords.
The nervous system would appear at first sight to be very lowly organised,
but the new points I believe myself to have made out, as well as certain
previously known features in it appear to me to shew that this is not the
case.
The following is a summary of the fresh points I have observed in the
nervous system:
(1) Immediately underneath the oesophagus the oesophageal commissures
dilate and form a pair of ganglia equivalent to the annelidan and
arthropodan sub-oesophageal ganglia. These ganglia are closely approximated
and united by 5 or 6 commissures. They give off large nerves to the oral
papillæ.
(2) The ventral nerve cords are covered on their ventral side by a thick
ganglionic layer[462], and at each pair of feet they dilate into a small
but distinct _ganglionic swelling_. From each ganglionic swelling are given
off a pair of large nerves[463] to the feet; and the ganglionic swellings
of the two cords are connected together by _a pair of commissures
containing ganglion cells_[464]. The other commissures connecting the two
cords together do not contain ganglion cells.
Footnote 462: This was known to Grube, _loc. cit._
Footnote 463: These nerves were noticed by Milne-Edwards, but
Grube failed to observe that they were much larger than the
nerves given off between the feet.
Footnote 464: These commissures were perhaps observed by
Saenger, _loc. cit._
The chief feature in which Peripatus was supposed to differ from normal
Arthropoda and Annelida, viz. the absence of ganglia on the ventral cords,
does not really exist. In other particulars, as in the amount of nerve
cells in the ventral cords and the completeness of the commissural
connections between the two cords, &c., the organisation of the nervous
system of Peripatus ranks distinctly high. The nervous system lies within
the circular and longitudinal muscles, and is thus not in proximity with
the skin. In this respect also Peripatus shews no signs of a primitive
condition of the nervous system.
A median nerve is given off from the posterior border of the
supra-oesophageal ganglion to the oesophagus, which probably forms a
rudimentary sympathetic system. I believe also that I have found traces of
a paired sympathetic system.
The organ doubtfully spoken of by Mr Moseley as a fat body, and by Grube as
a lateral canal, is in reality a glandular tube, lined by beautiful
columnar cells containing secretion globules, which opens by means of a
non-glandular duct into the mouth. It lies close above the ventral nerve
cords in a lateral compartment of the body-cavity, and extends backwards
for a varying distance.
This organ may perhaps be best compared with the simple salivary gland of
Julus. It is not to be confused with the slime glands of Mr Moseley, which
have their opening in the oral papillæ. If I am correct in regarding it as
homologous with the salivary glands so widely distributed amongst the
Tracheata, its presence indicates a hitherto unnoticed arthropodan affinity
in Peripatus.
XVI. ON THE MORPHOLOGY AND SYSTEMATIC POSITION OF THE SPONGIDA[465].
Footnote 465: From the _Quarterly Journ. of Microscopical
Science_, Vol. XIX. 1879.
Professor Schulze's[466] last memoir on the development of Calcareous
Sponges, confirms and enlarges Metschnikoff's[467] earlier observations,
and gives us at last a fairly complete history of the development of one
form of Calcareous Sponge. The facts which have been thus established have
suggested to me a view of the morphology and systematic position of the
Spongida, somewhat different to that now usually entertained. In bringing
forward this view, I would have it understood that it does not claim to be
more than a mere suggestion, which if it serves no other function may,
perhaps, be of use in stimulating research.
Footnote 466: "Untersuchungen über d. Bau u. d. Entwicklung
der Spongien," _Zeit. f. wiss. Zool._ Bd. XXXI. 1878.
Footnote 467: "Zur Entwicklungsgeschichte der Kalkschwämme,"
_Zeit. f. wiss. Zool._ Bd. XXIV. 1874.
To render clear what I have to say, I commence with a very brief statement
of the facts which may be considered as established with reference to the
development of _Sycandra raphanus_, the form which was studied by both
Metschnikoff and Schulze. The segmentation of the ovum, though in many ways
remarkable, is of no importance for my present purpose, and I take up the
development at the close of the segmentation, while the embryo is still
encapsuled in the parental tissues. It is at this stage lens-shaped, with a
central segmentation cavity. An equatorial plane divides it into two parts,
which have equal shares in bounding the segmentation cavity. One of these
halves is formed of about thirty-two large, round, granular cells, the
other of a larger number of ciliated clear columnar cells. While the embryo
is still encapsuled a partial invagination of the granular cells takes
place, reducing the segmentation cavity to a mere slit; this invagination
is, however, quite temporary and unimportant, and on the embryo becoming
free, which shortly takes place, no trace of it is visible; but, on the
contrary, the segmentation cavity becomes larger, and the granular cells
project very much more prominently than in the encapsuled state.
[Illustration: FIG. 1.
Two free stages in the development of _Sycandra raphanus_ (copied from
Schulze).
A. Amphiblastula stage; B. a later stage after the ciliated cells have
commenced to become invaginated; _cs._ segmentation cavity; _ec._ granular
cells which will form the ectoderm; _en._ ciliated cells which become
invaginated to form the entoderm.]
The larva, after it has left the parental tissues, has an oval form and is
transversely divided into two areas (fig. 1, A). One of these areas is
formed of the elongated, clear, ciliated cells, with a small amount of
pigment near the inner ends (_en_), and the other and larger area of the
thirty-two granular cells already mentioned (_ec_). Fifteen or sixteen of
these are arranged as a special ring on the border of the clear cells. In
the centre of the embryo is a segmentation cavity (_cs_) which lies between
the granular and the clear cells, but is mainly bounded by the vaulted
inner surface of the latter. This stage is known as the amphiblastula
stage. After the larva has for some time enjoyed a free existence, a
remarkable series of changes takes place, which result in the invagination
of the half of it formed of the clear cells, and form a prelude to the
permanent attachment of the larva. The entire process of invagination is
completed in about half an hour. The whole embryo first becomes flattened,
but especially the ciliated half which gradually becomes less prominent
(fig. 1, B), and still later the cells composing it undergo a true process
of invagination. As a result of this invagination the segmentation cavity
is obliterated and the larva assumes a compressed plano-convex form with a
central gastrula cavity, and a blastopore in the middle of the flattened
surface. The two layers of the gastrula may now be spoken of as ectoderm
and entoderm. The blastopore becomes gradually narrowed by the growth over
it of the outer row of granular cells. When it has become very small the
attachment of the larva takes place by the flat surface where the
blastopore is situated. It is effected by protoplasmic processes of the
outer ring of ectoderm cells, which, together with the other ectoderm
cells, now become amoeboid. At the same time they become clearer and permit
a view of the interior of the gastrula. Between the ectoderm cells and the
entoderm cells which line the gastrula cavity there arises a hyaline
structureless layer, which is more closely attached to the ectoderm than to
the entoderm, and is probably derived from the former. A view of the
gastrula stage after the larva has become fixed is given in fig. 2.
[Illustration: FIG. 2.
Fixed Gastrula stage of _Sycandra raphanus_ (copied from Schulze).
The figure shews the amoeboid ectoderm cells (_ec_) derived from the
granular cells of the earlier stage, and the columnar entoderm cells,
lining the gastrula cavity, derived from the ciliated cells of the earlier
stage. The larva is fixed by the amoeboid cells on the side on which the
blastopore is situated.]
[Illustration: FIG. 3.
The young of _Sycandra raphanus_ shortly after the development of the
_spicula_ (copied from Schulze).
A. View from the side; B. view from the free extremity; _os._ osculum;
_ec._ ectoderm; _en._ entoderm composed of collared ciliated cells. The
terminal osculum and lateral pores are represented as oval white spaces.]
After invagination the cilia of the entoderm cells can no longer be seen,
and are probably absorbed, and their disappearance is nearly coincident
with the complete obliteration of the blastopore, an event which takes
place shortly after the attachment of the larva. After the formation of the
structureless layer between the ectoderm and entoderm, calcareous spicules
make their appearance in it as delicate unbranched rods pointed at both
extremities. The larva when once fixed rapidly grows in length and assumes
a cylindrical form (fig. 3, A). The sides of the cylinder are beset with
calcareous spicules which project beyond the surface, and in addition to
the unbranched forms, spicules are developed with three and four rays as
well as some with a blunt extremity and serrated edge. The extremity of the
cylinder opposite the attached surface is flattened, and though surrounded
by a ring of four-rayed spicules is itself free from them. At this
extremity a small perforation is formed leading into the gastric cavity
which rapidly increases in size and forms an exhalent osculum (_os_). A
series of inhalent apertures are also formed at the sides of the cylinder.
The relative times of appearance of the single osculum and smaller
apertures is not constant for the different larvæ. On the central gastrula
cavity of the sponge becoming placed in communication with the external
water, the entoderm cells lining it become ciliated afresh (fig. 3, B,
_en_) and develop the peculiar collar characteristic of the entoderm cells
of the Spongida. When this stage of development is reached we have a fully
developed sponge of the type made known by Haeckel as Olynthus.
Till the complete development of other forms of Spongida has been worked
out it is not possible to feel sure how far the phenomena observable in
Sycandra hold good in all cases. Quite recently the Russian embryologist,
M. Ganin[468], has given an account, without illustrations, of the
development of _Spongilla fluviatilis_, which does not appear reconcileable
with that of Sycandra. Considering the difficulties of observation it
appears better to assume for this and some other descriptions that the
observations are in error rather than that there is a fundamental want of
uniformity in development amongst the Spongida.
Footnote 468: "Zur Entwicklung d. Spongilla fluviatilis,"
_Zoologischer Anzeiger_, Vol. I. No. 9, 1878.
The first point in the development of Sycandra which deserves notice is the
character of the free swimming larva. The peculiar larval form, with one
half of the body composed of amoeboid granular cells and the other of clear
ciliated cells is nearly constant amongst the Calcispongiæ, and widely
distributed in a somewhat modified condition amongst the Fibrospongiæ and
Myxospongiæ. Does this larva retain the characters of an ancestral type of
the Spongida, and if so what does its form mean? It is, of course, possible
that it has no ancestral meaning but has been secondarily acquired; I
prefer myself to think that this is not the case, more especially as it
appears to me that the characters of the larva may be plausibly explained
by regarding it as a transitional form between the Protozoa and Metazoa.
According to this view the larva is to be considered as a colony of
Protozoa, one half of the individuals of which have become differentiated
into nutritive forms, and the other half into locomotor and respiratory
forms. The granular amoeboid cells represent the nutritive forms, and the
ciliated cells represent the locomotor and respiratory forms. That the
passage from the Protozoa to the Metazoa may have been effected by such a
differentiation is not improbable on _à priori_ grounds, and fits in very
well with the condition of the free swimming larva of Spongida, though
another and perhaps equally plausible suggestion as to this passage has
been put forward by my friend Professor Lankester[469].
Footnote 469: "Notes on Embryology and Classification."
_Quarterly Journal of Microscopical Science_, Vol. XVII. 1877.
It seems not impossible, if the speculations in this paper have
any foundation that while the views here put forward as to the
passage from the Protozoon to the Metazoon condition may hold
true for the Spongida, some other mode of passage may have
taken place in the case of the other Metazoa.
While the above view seems fairly satisfactory for the free swimming stage
of the larval Sponge there arises in the subsequent development a
difficulty which appears at first sight fatal to it. This difficulty is the
invagination of the ciliated cells instead of the granular ones. If the
granular cells represent the nutritive individuals of the colony, they and
not the ciliated cells ought most certainly to give rise to the lining of
the gastrula cavity, according to the generally accepted views of the
morphology of the Spongida. The suggestion which I would venture to put
forward in explanation of this paradox involves a completely new view of
the nature and functions of the germinal layers of adult Sponges.
It is as follows:--When the free swimming ancestor of the Spongida became
fixed, the ciliated cells by which its movements used to be effected must
have to a great extent become functionless. At the same time the amoeboid
nutritive cells would need to expose as large a surface as possible. In
these two considerations there may, perhaps, be found a sufficient
explanation of the invagination of the ciliated cells, and the growth of
the amoeboid cells over them. Though respiration was, no doubt, mainly
effected by the ciliated cells, it is improbable that it was completely
localised in them, but the continuation of their function was provided for
by the formation of an osculum and pores. The ciliated collared cells which
line the ciliated chambers, or in some cases the radial tubes, are
undoubtedly derived from the invaginated cells, and if there is any truth
in the above suggestion, the collared cells in the adult Sponge must be
mainly respiratory and not digestive in function, while the normal
epithelial cells which cover the surface of the sponge, and in most cases
line the greater part of the passages through its substance, must carry on
the digestion[470]. If the reverse is the case the whole theory falls to
the ground. It has not, so far as I know, been definitely made out where
the digestion is carried on. Lieberkühn would appear to hold the view that
the amoeboid lining cells of the passages are mainly concerned with
digestion, while Carter holds that digestion is carried on by the collared
cells of the ciliated chambers.
Footnote 470: That the flat cells which line the greater part
of the passages of most Sponges are really derived from
ectodermic invaginations appears to me clearly proved by
Schulze's and Barrois' observations on the young fixed stages
of Halisarea. Ganin appears, however, to maintain a contrary
view for Spongilla.
If it is eventually proved by actual experiments on the nutrition of
Sponges, that digestion is carried on by the general cells lining the
passages, and not by the ciliated cells, it is clear that neither the
ectoderm nor entoderm of Sponges will correspond with the similarly named
layers in the Coelenterata and the Metazoa. The invaginated entoderm will
be the respiratory layer and the ectoderm the digestive and sensory layer;
the sensory function being probably mainly localised in the epithelium on
the surface, and the digestive one in the epithelium lining the passages.
Such a fundamental difference in the germinal layers between the Spongida
and the other Metazoa, would necessarily involve the creation of a special
division of the Metazoa for the reception of the former group.
XVII. NOTES ON THE DEVELOPMENT OF THE ARANEINA[471].
Footnote 471: From the _Quarterly Journ. of Microscopical
Science_, Vol. XX. 1880.
(With Plates 30, 31, 32.)
The following observations do not profess to contain a complete history of
the development even of a single species of spider. They are the result of
investigations carried on at intervals during rather more than two years,
on the ova of _Agelena labyrinthica_; and I should not have published them
now, if I had any hope of being able to complete them before the appearance
of the work I am in the course of publishing on Comparative Embryology. It
appeared to me, however, desirable to publish in full such parts of my
observations as are completed before the appearance of my treatise, since
the account of the development of the Araneina is mainly founded upon them.
My investigations on the germinal layers and organs have been chiefly
conducted by means of sections. To prepare the embryos for sections, I
employed the valuable method first made known by Bobretzky. I hardened the
embryos in bichromate of potash, after placing them for a short time in
nearly boiling water. They were stained as a whole with hæmatoxylin after
the removal of the membranes, and embedded for cutting in coagulated
albumen.
The number of investigators who have studied the development of spiders is
inconsiderable. A list of them is given at the end of the paper.
The earliest writer on the subject is Herold (No. 4); he was followed after
a very considerable interval of time by Claparède (No. 3), whose memoir is
illustrated by a series of beautiful plates, and contains a very
satisfactory account of the external features of development.
Balbiani (No. 1) has gone with some detail into the history of the early
stages; and Ludwig (No. 5) has published some very important observations
on the development of the blastoderm. Finally, Barrois (No. 2) has quite
recently taken up the study of the group, and has added some valuable
observations on the development of the germinal layers.
In addition to these papers on the true spiders, important investigations
have been published by Metschnikoff on other groups of the Arachnida,
notably the scorpion. Metschnikoff's observations on the formation of the
germinal layers and organs accord in most points with my own.
The development of the Araneina may be divided into four periods: (1) the
segmentation; (2) the period from the close of the segmentation up to the
period when the segments commence to be formed; (3) the period from the
commencing formation of the segments to the development of the full number
of limbs; (4) the subsequent stages up to the attainment of the adult form.
In my earliest stage the segmentation was already completed, and the embryo
was formed of a single layer of large flattened cells enveloping a central
mass of polygonal yolk-segments.
Each yolk-segment is formed of a number of large clear somewhat oval
yolk-spherules. In hardened specimens the yolk-spherules become polygonal,
and in ova treated with hot water prior to preservation are not
unfrequently broken up. Amongst the yolk-segments are placed a fair number
of nucleated bodies of a very characteristic appearance. Each of them is
formed of (1) a large, often angular, nucleus, filled with deeply staining
bodies (nucleoli?); (2) a layer of protoplasm surrounding the nucleus,
prolonged into a protoplasmic reticulum. The exact relation of these
nucleated bodies to the yolk-segments is not very easy to make out, but the
general tendency of my observations is to shew (1) that each nucleated body
belongs to a yolk-sphere, and (2) that it is generally placed not at the
centre, but to one side of a yolk-sphere. If the above conclusions are
correct each complete yolk-segment is a cell, and each such cell consists
of a normal nucleus, protoplasm, and yolk-spherules. There is a special
layer of protoplasm surrounding the nucleus, while the remainder of the
protoplasm consists of a reticulum holding together the yolk-spherules.
Yolk-cells of this character are seen in Pls. 31 and 32, figs. 10-21.
The nuclei of the yolk-cells are probably derived by division from the
nuclei of the segmentation rosettes (vide Ludwig, No. 5), and it is
probable that they take their origin at the time when the superficial layer
of protoplasm separates from the yolk-columns below to form the blastoderm.
The protoplasm of the yolk-cells undergoes rapid division, as is shewn by
the fact that there are often two nucleated bodies close together, and
sometimes two nuclei in a single mass of protoplasm (fig. 10). It is
probable that in some cases the yolk-spheres divide at the same time as the
protoplasm belonging to them; the division of the nucleated bodies is,
however, in the main destined to give rise to fresh cells which enter the
blastoderm.
I have not elucidated to my complete satisfaction the next stage or two in
the development of the embryo; and have not succeeded in completely
reconciling the results of my own observations with those of Claparède and
Balbiani. In order to shew exactly where my difficulties lie it is
necessary briefly to state the results arrived at by the above authors.
According to Claparède the first differentiation in Pholcus consists in the
accumulation of the cells over a small area to form a protuberance, which
he calls the _primitive cumulus_. Owing to its smaller specific gravity the
part of the ovum with the cumulus always turns upwards, like the
blastodermic pole of a fowl's egg.
After a short time the cumulus elongates itself on one side, and becomes
connected by a streak with a white patch, which appears on the surface of
the egg, about 90° from the cumulus. This patch gradually enlarges, and
soon covers the whole surface of the ovum except the region where the
cumulus is placed. It becomes the ventral plate or germinal streak of the
embryo, its extremity adjoining the cumulus is the anal extremity, and its
opposite extremity the cephalic one. The cumulus itself is placed in a
depression on the dorsal surface of the ovum. Claparède compares the
cumulus to the dorsal organ of many Crustacea.
Balbiani (No. 1) describes the primitive cumulus in _Tegenaria domestica_,
_Epeira diadema_, and _Agelena labyrinthica_, as originating as a
protuberance at the centre of the ventral surface, surrounded by a
specialised portion of the blastoderm (p. 57), which I will call the
ventral plate. In _Tegenaria domestica_ he finds that it encloses the
so-called yolk-nucleus, p. 62. By an unequal growth of the ventral plate
the primitive cumulus comes to be placed at the cephalic pole of the
ventral plate. The cumulus now becomes less prominent, and in a few cases
disappears. In the next stage the central part of the ventral plate becomes
very prominent and forms the procephalic lobe, close to the anterior border
of which is usually placed the primitive cumulus (p. 67). The space between
the cumulus and the procephalic lobe grows larger, so that the latter
gradually travels towards the dorsal surface and finally vanishes. Behind
the procephalic lobe the first traces of the segments make their
appearance, as three transverse bands, before a distinct anal lobe becomes
apparent.
The points which require to be cleared up are, (1) what is the nature of
the primitive cumulus? (2) where is it situated in relation to the embryo?
Before attempting to answer these questions I will shortly describe the
development, so far as I have made it out, for the stages during which the
cumulus is visible.
The first change that I find in the embryo (when examined after it has been
hardened)[472] is the appearance of a small, whitish spot, which is at
first very indistinct. A section through such an ovum (Pl. 31, fig. 10)
shews that the cells of about one half of the ovum have become more
columnar than those of the other half, and that there is a point (_pr.c._)
near one end of the thickened half where the cells are more columnar, and
about two layers or so deep. It appears to me probable that this point is
the whitish spot visible in the hardened ovum. In a somewhat later stage
(Pl. 30, fig. 1) the whitish spot becomes more conspicuous (_pc._), and
appears as a distinct prominence, which is, without doubt, the primitive
cumulus, and from it there proceeds on one side a whitish streak. The
prominence, as noticed by Claparède and Balbiani, is situated on the
flatter side of the ovum. Sections at this stage shew the same features as
the previous stage, except that (1) the cells throughout are smaller, (2)
those of the thickened hemisphere of the ovum more columnar, and (3) the
cumulus is formed of several rows of cells, though not divided into
distinct layers. In the next stage the appearances from the surface are
rather more obscure, and in some of my best specimens a coagulum, derived
from the fluid surrounding the ovum, covers the most important part of the
blastoderm. In Pl. 30, fig. 2, I have attempted to represent, as truly as I
could, the appearances presented by the ovum. There is a well-marked
whitish side of the ovum, near one end of which is a prominence (_pc._),
which must, no doubt, be identified with the cumulus of the earlier stages.
Towards the opposite end, or perhaps rather nearer the centre of the white
side of the ovum, is an imperfectly marked triangular white area. There can
be no doubt that the line connecting the cumulus with the triangular area
is the future long axis of the embryo, and the white area is, without
doubt, the procephalic lobe of Balbiani.
Footnote 472: I was unfortunately too much engaged, at the
time when the eggs were collected, to study them in the fresh
condition; a fact which has added not a little to my
difficulties in elucidating the obscure points in the early
stages.
A section of the ovum at this stage is represented in Pl. 31, fig. 11. It
is not quite certain in what direction the section is taken, but I think it
probable it is somewhat oblique to the long axis. However this may be, the
section shews that the whitish hemisphere of the blastoderm is formed of
columnar cells, for the most part two or so layers deep, but that there is,
not very far from the middle line, a wedge-shaped internal thickening of
the blastoderm where the cells are several rows deep. With what part
visible in surface view this thickened portion corresponds is not clear. To
my mind it most probably corresponds to the larger white patch, in which
case I have not got a section through the terminal prominence. In the other
sections of the same embryo the wedge-shaped thickening was not so marked,
but it, nevertheless, extended through all the sections. It appears to me
probable that it constitutes a longitudinal thickened ridge of the
blastoderm. In any case, it is clear that the white hemisphere of the
blastoderm is a thickened portion of the blastoderm, and that the
thickening is in part due to the cells being more columnar, and, in part,
to their being more than one row deep, _though they have not become divided
into two distinct germinal layers_. It is further clear that the increase
in the number of cells in the thickened part of the blastoderm is, _in the
main, a result of the multiplication of the original single row of cells_,
while a careful examination of my sections proves that it is also partly
due to cells, derived from the yolk, having been added to the blastoderm.
In the following stage which I have obtained (which cannot be very much
older than the previous stage, because my specimens of it come from the
same batch of eggs), a distinct and fairly circumscribed thickening forming
the ventral surface of the embryo has become established. Though its
component parts are somewhat indistinct, it appears to consist of a
procephalic lobe, a less prominent caudal lobe, and an intermediate portion
divided into about three segments; but its constituents cannot be clearly
identified with the structures visible in the previous stage. I am
inclined, however, to identify the anterior thickened area of the previous
stage with the procephalic lobe, and a slight protuberance of the caudal
portion (visible from the surface) with the primitive cumulus. I have,
however, failed to meet with any trace of the cumulus in my sections.
To this stage, which forms the first of the second period of the larval
history, I shall return, but it is necessary now to go back to the
observations of Claparède and Balbiani.
There can, in the first place, be but little doubt that what I have called
the primitive cumulus in my description is the structure so named by
Claparède and Balbiani.
It is clear that Balbiani and Claparède have both failed to appreciate the
importance of the organ, which my observations shew to be the part of the
ventral thickening of the blastoderm where two rows of cells are first
established, and therefore the point where the first traces of the future
mesoblast becomes visible.
Though Claparède and Balbiani differ somewhat as to the position of the
organ, they both make it last longer than I do: I feel certainly inclined
to doubt whether Claparède is right in considering a body he figures after
six segments are present, to be the same as the dorsal organ of the embryo
before the formation of any segments, especially as all the stages between
the two appear to have escaped him. In Agelena there is undoubtedly no
organ in the position he gives when six segments are found.
Balbiani's observations accord fairly with my own up to the stage
represented in fig. 2. Beyond this stage my own observations are not
satisfactory, but I must state that I feel doubtful whether Balbiani is
correct in his description of the gradual separation of the procephalic
lobe and the cumulus, and the passage of the latter to the dorsal surface,
and think it possible that he may have made a mistake as to which side of
the procephalic lobe, in relation to the parts of the embryo, the cumulus
is placed.
Although there appear to be grounds for doubting whether either Balbiani
and Claparède are correct in the position they assign to the cumulus, my
observations scarcely warrant me in being very definite in my statements on
this head, but, as already mentioned, I am inclined to place the organ near
the posterior end (and therefore, as will be afterwards shewn, in a
somewhat dorsal situation) of the ventral embryonic thickening.
In my earliest stage of the third period there is present, as has already
been stated, a procephalic lobe, and an indistinct and not very prominent
caudal portion, and about three segments between the two. The definition of
the parts of the blastoderm at this stage is still very imperfect, but from
subsequent stages it appears to me probable that the first of the three
segments is that of the first pair of ambulatory limbs, and that the
segments of the cheliceræ and pedipalpi are formed later than those of the
first three ambulatory appendages.
Balbiani believes that the segment of the cheliceræ is formed later than
that of the six succeeding segments. He further concludes, from the fact
that this segment is cut off from the procephalic portion in front, that it
is really part of the procephalic lobe. I cannot accept the validity of
this argument; though I am glad to find myself in, at any rate, partial
harmony with the distinguished French embryologist as to the facts.
Balbiani denies for this stage the existence of a caudal lobe. There is
certainly, as is very well shewn in my longitudinal sections, a thickening
of the blastoderm in the caudal region, though it is not so prominent in
surface views as the procephalic lobe.
A transverse section through an embryo at this stage (Pl. 31, fig. 12)
shews that there is a ventral plate of somewhat columnar cells more than
one row deep, and a dorsal portion of the blastoderm formed of a single row
of flattened cells. Every section at this stage shews that the inner layer
of cells of the ventral plate is receiving accessions of cells from the
yolk, which has not to any appreciable extent altered its constitution. A
large cell, passing from the yolk to the blastoderm, is shewn in fig. 12 at
_y.c_.
_The cells of the ventral plate are now divided into two distinct layers._
The outer of these is the _epiblast_, the inner the _mesoblast_. The cells
of both layers are quite continuous across the median line, and exhibit no
trace of a bilateral arrangement.
This stage is an interesting one on account of the striking similarity
which (apart from the amnion) exists between a section through the
blastoderm of a spider and that of an insect immediately after the
formation of the mesoblast. The reader should compare Kowalevsky's (_Mém.
Acad. Pétersbourg_, Vol. XVI. 1871) fig. 26, Pl. IX. with my fig. 12. The
existence of a continuous ventral plate of mesoblast has been noticed by
Barrois (p. 532), who states that the two mesoblastic bands originate from
the longitudinal division of a primitive single band.
In a slightly later stage (Pl. 30, fig. 3_a_ and 3_b_) six distinct
segments are interpolated between the procephalic and the caudal lobes. The
two foremost, _ch_ and _pd_ (especially the first), of these are far less
distinct than the remainder, and the first segment is very indistinctly
separated from the procephalic lobe. From the indistinctness of the first
two somites, I conclude that they are later formations than the four
succeeding ones. The caudal and procephalic lobes are very similar in
appearance, but the procephalic lobe is slightly the wider of the two.
There is a slight protuberance on the caudal lobe, which is possibly the
remnant of the cumulus. The superficial appearance of segmentation is
produced by a series of transverse valleys, separating raised intermediate
portions which form the segments. The ventral thickening of the embryo now
occupies rather more than half the circumference of the ovum.
Transverse sections shew that considerable changes have been effected in
the constitution of the blastoderm. In the previous stage, the ventral
plate was formed of an uniform external layer of epiblast, and a continuous
internal layer of mesoblast. The mesoblast has now become divided along the
whole length of the embryo, except, perhaps, the procephalic lobes, into
two lateral bands which are not continuous across the middle line (Pl. 31,
fig. 13, _me_). It has, moreover, become a much more definite layer,
closely attached to the epiblast. Between each mesoblastic band and the
adjoining yolk there are placed a few scattered cells, which in a somewhat
later stage become the splanchnic mesoblast. These cells are derived from
the yolk-cells; and almost every section contains examples of such cells in
the act of joining the mesoblast.
The epiblast of the ventral plate has not, to any great extent, altered in
constitution. It is, perhaps, a shade thinner in the median line than it is
laterally. The division of the mesoblast plate into two bands, together,
perhaps, with the slight reduction of the epiblast in the median ventral
line, gives rise at this stage to an imperfectly marked median groove.
The dorsal epiblast is still formed of a single layer of flat cells. In the
neighbourhood of this layer the yolk nuclei are especially concentrated.
The yolk itself remains as before.
The segments continue to increase regularly, each fresh segment being added
in the usual way between the last formed segment and the unsegmented caudal
lobe. At the stage when about nine or ten segments have become established,
the first rudiments of appendages become visible. At this period (Pl. 30,
fig. 4) there is a distinct median ventral groove, extending through the
whole length of the embryo, which becomes, however, considerably shallower
behind. The procephalic region is distinctly bilobed. The first segment
(that of the cheliceræ) is better marked off from it than in the previous
stage, but is without a trace of an appendage, and exhibits therefore, in
respect to the development of its appendages, the same retardation that
characterised its first appearance. The next five segments, viz. those of
the pedipalpi and four ambulatory appendages, present a very well-marked
swelling at each extremity. These swellings are the earliest traces of the
appendages. Of the three succeeding segments, only the first is well
differentiated. The caudal lobe, though less broad than the procephalic
lobe, is still a widish structure. The most important internal changes
concern the mesoblast, which is now imperfectly though distinctly divided
into somites, corresponding with segments visible externally. Each
mesoblastic somite is formed of a distinct somatic layer closely attached
to the epiblast, and a thinner and less well-marked splanchnic layer. In
the appendage-bearing segments the somatic layer is continued up into the
appendages.
The epiblast is distinctly thinner in the median line than at the two
sides.
The next stage figured (Pl. 30, figs. 5 and 6) is an important one, as it
is characterized by the establishment of the full number of appendages. The
whole length of the ventral plate has greatly increased, so that it
embraces nearly the circumference of the ovum, and there is left uncovered
but a very small arc between the two extremities of the plate (Pl. 30,
fig. 6; Pl. 31, fig. 15). This arc is the future dorsal portion of the
embryo, which lags in its development immensely behind the ventral portion.
There is a very distinctly bilobed procephalic region (_pr.l_) well
separated from the segment with the cheliceræ (_ch_). It is marked by a
shallow groove opening behind into a circular depression (_st._)--the
earliest rudiment of the stomodæum. The six segments behind the procephalic
lobes are the six largest, and each of them bears two prominent appendages.
They constitute the six appendage-bearing segments of the adult. The four
future ambulatory appendages are equal in size: they are slightly larger
than the pedipalpi, and these again than the cheliceræ. Behind the six
somites with prominent appendages there are four well-marked somites, each
with a small protuberance. These four protuberances are provisional
appendages. They have been found in many other genera of Araneina
(Claparède, Barrois). The segments behind these are rudimentary and
difficult to count, but there are, at any rate, five, and at a slightly
later stage probably six, including the anal lobe. These fresh segments
have been formed by the continued segmentation of the anal lobe, which has
greatly altered its shape in the process. The ventral groove of the earlier
stage is still continued along the whole length of the ventral plate.
By the close of this stage the full number of post-cephalic segments has
become established. They are best seen in the longitudinal section (Pl. 31,
fig. 15). There are six anterior appendage-bearing segments, followed by
four with rudimentary appendages (not seen in this figure), and six without
appendages behind. There are, therefore, sixteen in all. This number
accords with the result arrived at by Barrois, but is higher by two than
that given by Claparède.
The germinal layers (vide Pl. 31, fig. 14) have by this stage undergone a
further development. The mesoblastic somites are more fully developed. The
general relations of these somites is shewn in longitudinal section in
Pl. 31, fig. 15, and in transverse section in Pl. 31, fig. 14. In the tail,
where they are simplest (shewn on the upper side in fig. 14), each
mesoblastic somite is formed of a somatic layer of more or less cubical
cells attached to the epiblast, and a splanchnic layer of flattened cells.
Between the two is placed a completely circumscribed cavity, which
constitutes part of the embryonic body-cavity. Between the yolk and the
splanchnic layer are placed a few scattered cells, which form the latest
derivatives of the yolk-cells, and are to be reckoned as part of the
splanchnic mesoblast. The mesoblastic somites do not extend outwards beyond
the edge of the ventral plate, and the corresponding mesoblastic somites of
the two sides do not nearly meet in the middle line. In the limb-bearing
somites the mesoblast has the same general characters as in the posterior
somites, but the _somatic_ layer is prolonged as a hollow papilliform
process into the limb, so that each limb has an axial cavity continuous
with the section of the body-cavity of its somite. The description given by
Metschnikoff of the formation of the mesoblastic somites in the scorpion,
and their continuation into the limbs, closely corresponds with the history
of these parts in spiders. In the region of each procephalic lobe the
mesoblast is present as a continuous layer underneath the epiblast, but in
the earlier part of the stage, at any rate, is not formed of two distinct
layers with a cavity between them.
The epiblast at this stage has also undergone important changes. Along the
median ventral groove it has become very thin. On each side of this groove
it exhibits in each appendage-bearing somite a well-marked thickening,
which gives in surface views the appearance of a slightly raised area
(Pl. 30, fig. 5), between each appendage and the median line. These
thickenings are the first rudiments of the ventral nerve ganglia. The
ventral nerve cord at this stage is formed of two ridge-like thickenings of
the epiblast, widely separated in the median line, each of which is
constituted of a series of raised divisions--the ganglia--united by
shorter, less prominent divisions (fig. 14, _vg_). The nerve cords are
formed from before backwards, and are not at this stage found in the hinder
segments. _There is a distinct ganglionic thickening for the cheliceræ
quite independent of the procephalic lobes._
In the procephalic lobes the epiblast is much thickened, and is formed of
several rows of cells. The greater part of it is destined to give rise to
the supra-oesophageal ganglia.
During the various changes which have been described the blastoderm cells
have been continually dividing, and, together with their nuclei, have
become considerably smaller than at first. The yolk cells have in the
meantime remained much as before, and are, therefore, considerably larger
than the nuclei of the blastoderm cells. They are more numerous than in the
earlier stages, but are still surrounded by a protoplasmic body, which is
continued into a protoplasmic reticulum. The yolk is still divided up into
polygonal segments, but from sections it would appear that the nuclei are
more numerous than the segments, though I have failed to arrive at quite
definite conclusions on this point.
As development proceeds the appendages grow longer, and gradually bend
inwards. They become very soon divided by a series of ring-like
constrictions which constitute the first indications of the future joints
(Pl. 30, fig. 6). The full number of joints are not at once reached, but in
the ambulatory appendages five only appear at first to be formed. There are
four joints in the pedipalpi, while the cheliceræ do not exhibit any signs
of becoming jointed till somewhat later. The primitive presence of only
five joints in the ambulatory appendages is interesting, as this number is
permanent in Insects and in Peripatus.
The next stage figured forms the last of the third period (Pl. 30, figs. 7
and 7_a_). The ventral plate is still rolled round the egg (fig. 7), and
the end of the tail and the procephalic lobes nearly meet dorsally, so that
there is but a very slight development of the dorsal region. There are the
same number of segments as before, and the chief differences in appearance
between the present and the previous stage depend upon the fact (1) that
the median ventral integument between the nerve ganglia has become wider,
and at the same time thinner; (2) that the limbs have become much more
developed; (3) that the stomodæum is definitely established; (4) that the
procephalic lobes have undergone considerable development.
Of these features, the three last require a fuller description. The limbs
of the two sides are directed towards each other, and nearly meet in the
ventral line. The cheliceræ are two-jointed, and terminate in what appear
like rudimentary chelæ, a fact which perhaps indicates that the spiders are
descended from ancestors with chelate cheliceræ. The four embryonic
post-ambulatory appendages are now at the height of their development.
The stomodæum (Pl. 30, fig. 7, and Pl. 31, fig. 17, _st_) is a deepish pit
between the two procephalic lobes, and distinctly in front of the segment
of the cheliceræ. It is bordered in front by a large, well-marked, bilobed
upper lip, and behind by a smaller lower lip. The large upper lip is a
temporary structure, to be compared, perhaps, with the gigantic upper lip
of the embryo of Chelifer (cf. Metschnikoff). On each side of and behind
the mouth two whitish masses are visible, which are the epiblastic
thickenings which constitute the ganglia of the cheliceræ (Pl. 30, fig. 7,
_ch.g_).
The procephalic lobes (_pr.l_) now form two distinct masses, and each of
them is marked by a semicircular groove, dividing them into a narrower
anterior and a broader posterior division.
In the region of the trunk the general arrangement of the germinal layers
has not altered to any great extent. The ventral ganglionic thickenings are
now developed in all the segments in the abdominal as well as in the
thoracic region. The individual thickenings themselves, though much more
conspicuous than in the previous stage (Pl. 31, fig. 16, _v.c_), are still
integral parts of the epiblast. They are more widely separated than before
in the middle line. The mesoblastic somites retain their earlier
constitution (Pl. 31, fig. 16). Beneath the procephalic lobes the mesoblast
has, in most respects, a constitution similar to that of a mesoblastic
somite in the trunk. It is formed of two bodies, one on each side, each
composed of a splanchnic and somatic layer (Pl. 31, fig. 17, _sp._ and
_so_), enclosing between them a section of the body-cavity. But the
cephalic somites, unlike those of the trunk, are united by a median bridge
of mesoblast, in which no division into two layers can be detected. This
bridge assists in forming a thick investment of mesoblast round the
stomodæum (_st_).
The existence of a section of the body-cavity in the præoral region is a
fact of some interest, especially when taken in connection with the
discovery, by Kleinenberg, of a similar structure in the head of Lumbricus.
The procephalic lobe represents the præoral lobe of Chætopod larvæ, but the
prolongation of the body-cavity into it does not, in my opinion,
necessarily imply that it is equivalent to a post-oral segment.
The epiblast of the procephalic lobes is a thick layer several cells deep,
but without any trace of a separation of the ganglionic portion from the
epidermis.
The nuclei of the yolk have increased in number, but the yolk, in other
respects, retains its earlier characters.
The next period in the development is that in which the body of the embryo
gradually acquires the adult form. The most important event which takes
place during this period is the development of the dorsal region of the
embryo, which, up to its commencement, is practically non-existent. As a
consequence of the development of the dorsal region, the embryo, which has
hitherto had what may be called a dorsal flexure, gradually unrolls itself,
and acquires a ventral flexure. This change in the flexure of the embryo is
in appearance a rather complicated phenomenon, and has been somewhat
differently described by the two naturalists who have studied it in recent
times.
For Claparède the prime cause of the change of flexure is the translation
dorsalwards of the limbs. He compares the dorsal region of the embryo to
the arc of a circle, the two ends of which are united by a cord formed by
the line of insertion of the limbs. He points out that if you bring the
middle of the cord, so stretched between the two ends of the arc, nearer to
the summit of the arc, you necessarily cause the two ends of the arc to
approach each other, or, in other words, if the insertion of the limbs is
drawn up dorsally, the head and tail must approach each other ventrally.
Barrois takes quite a different view to that of Claparède, which will
perhaps be best understood if I quote a translation of his own words. He
says: "At the period of the last stage of the embryonic band (the stage
represented in Pl. 31, fig. 7, in the present paper) this latter completely
encircles the egg, and its posterior extremity nearly approaches the
cephalic region. Finally, the germinal bands, where they unite at the anal
lobe (placed above on the dorsal surface), form between them a very acute
angle. During the following stages one observes the anal segment separate
further and further from the cephalic region, and approach nearer and
nearer to the ventral region. This displacement of the anal segment
determines, in its turn, a modification in the divergence of the anal
bands; the angle which they form at their junction tends to become more
obtuse. The same processes continue regularly till the anal segment comes
to occupy the opposite extremity to the cephalic region, a period at which
the two germinal bands are placed in the same plane and the two sides of
the obtuse angle end by meeting in a straight line. If we suppose a
continuation of the same phenomenon it is clear that the anal segment will
come to occupy a position on the ventral surface, and the germinal bands to
approach, but in the inverse way, so as to form an angle opposite to that
which they formed at first. This condition ends the process by which the
posterior extremity of the embryonic band, at first directed towards the
dorsal side, comes to bend in towards the ventral region."
Neither of the above explanations is to my mind perfectly satisfactory. The
whole phenomenon appears to me to be very simple, and to be caused by the
elongation of the dorsal region, _i.e._ the region on the dorsal surface
between the anal and procephalic lobes. Such an elongation necessarily
separates the anal and procephalic lobes; but, since the ventral plate does
not become shortened in the process, and the embryo cannot straighten
itself on account of the egg-shell, it necessarily becomes flexed, and such
flexure can only be what I have already called a ventral flexure. If there
were but little food yolk this flexure would cause the whole embryo to be
bent in, so as to have the ventral surface concave, but instead of this the
flexure is confined at first to the two bands which form the ventral plate.
These bands are bent in the natural way (Pl. 30, fig. 8_b_), but the yolk
forms a projection, a kind of yolk-sack as Barrois calls it, distending the
thin integument between the two ventral bands. This yolk-sack is shewn in
surface view in Pl. 30, fig. 8, and in section in Pl. 32, fig. 18. At a
later period, when the yolk has become largely absorbed in the formation of
various organs, the true nature of the ventral flexure becomes apparent,
and the abdomen of the young Spider is found to be bent over so as to press
against the ventral surface of the thorax (Pl. 30, fig. 9). This flexure is
shewn in section in Pl. 32, fig. 21.
At the earliest stage of this period of which I have examples, the dorsal
region has somewhat increased, though not very much. The limbs have grown
very considerably and _now cross in the middle line_.
The ventral ganglia, though not the supra-oesophageal, have become
separated from the epiblast.
The yolk nuclei, each surrounded by protoplasm as before, are much more
numerous.
In other respects there are no great changes in the internal features.
In my next stage, represented in Pl. 30, figs. 8_a_, and 8_b_, a very
considerable advance has become effected. In the first place the dorsal
surface has increased in length to rather more than one half the
circumference of the ovum. The dorsal region has, however, not only
increased in length, but also in definiteness, and a series of transverse
markings (figs. 8_a_ and _b_), which are very conspicuous in the case of
the four anterior abdominal segments (the segments with rudimentary
appendages), have appeared, indicating the limits of segments dorsally. The
terga of the somites may, in fact, be said to have become formed. The
posterior terga (fig. 8_a_) are very narrow compared to the anterior.
The caudal protuberance is more prominent than it was, and somewhat
bilobed; it is continued on each side into one of the bands, into which the
ventral plate is divided. These bands, as is best seen in side view
(fig. 8_b_), have a ventral curvature, or, perhaps more correctly, are
formed of two parts, which meet at a large angle open towards the ventral
surface. The posterior of these parts bears the four still very conspicuous
provisional appendages, and the anterior the six pairs of thoracic
appendages. The four ambulatory appendages are now seven-jointed, as in the
adult, but though longer than in the previous stage they do not any longer
_cross or even meet in the middle line_, but are, on the contrary,
separated by a very considerable interval. This is due to the great
distension by the yolk of the ventral part of the body, in the interval
between the two parts of the original ventral plate. The amount of this
yolk may be gathered from the section (Pl. 32, fig. 18). The pedipalpi
carry a blade on their basal joint. The cheliceræ no longer appear to
spring from an independent postoral segment.
There is a conspicuous lower lip, but the upper is less prominent than
before. Sections at this stage shew that the internal changes have been
nearly as considerable as the external.
The dorsal region is now formed of a (1) flattened layer of epiblast cells,
and a (2) fairly thick layer of large and rather characteristic cells which
any one who has studied sections of spider's embryos will recognize as
derivatives of the yolk. These cells are not, therefore, derived from
prolongations of the somatic and splanchnic layers of the already formed
somites, but are new formations derived from the yolk. They commenced to be
formed at a much earlier period, and some of them are shewn in the
longitudinal section (Pl. 31, fig. 15). In the next stage these cells
become differentiated into the somatic and splanchnic mesoblast layers of
the dorsal region of the embryo.
In the dorsal region of the abdomen the heart has already become
established. So far as I have been able to make out it is formed from a
solid cord of the cells of the dorsal region. The peripheral layer of this
cord gives rise to the walls of the heart, while the central cells become
converted into the corpuscles of the blood.
The rudiment of the heart is in contact with the epiblast above, and there
is no greater evidence of its being derived from the splanchnic than from
the somatic mesoblast; it is, in fact, formed before the dorsal mesoblast
has become differentiated into two layers.
In the abdomen three or four transverse septa, derived from the splanchnic
mesoblast, grow a short way into the yolk. They become more conspicuous
during the succeeding stage, and are spoken of in detail in the description
of that stage. In the anterior part of the thorax a longitudinal and
vertical septum is formed, which grows downwards from the median dorsal
line, and divides the yolk in this region into two parts. In this septum
there is formed at a later stage a vertical muscle attached to the
suctorial part of the stomodæum.
The mesoblastic somites of the earlier stage are but little modified; and
there are still prolongations of the body-cavity into the limbs (Pl. 32,
fig. 18).
The lateral parts of the ventral nerve cords are now at their maximum of
separation (Pl. 32, fig. 18, _v.g._). Considerable differentiation has
already set in in the constitution of the ganglia themselves, which are
composed of an outer mass of ganglion cells enclosing a kernel of nerve
fibres, which lie on the inner side and connect the successive ganglia.
There are still distinct thoracic and abdominal ganglia for each segment,
and there is also a pair of separate ganglion for the cheliceræ, which
assists, however, in forming the oesophageal commissures.
The thickenings of the præoral lobe which form the supra-oesophageal
ganglia are nearly though not quite separated from the epiblast. The
semicircular grooves of the earlier stages are now deeper than before, and
are well shewn in sections nearly parallel to the outer anterior surface of
the ganglion (Pl. 32, fig. 19). The supra-oesophageal ganglia are still
entirely formed of undifferentiated cells, and are without commissural
tissue like that present in the ventral ganglia.
The stomodæum has considerably increased in length, and the proctodæum has
become formed as a short, posteriorly directed involution of the epiblast.
I have seen traces of what I believe to be two outgrowths from it, which
form the Malpighian bodies.
The next stage constitutes (Pl. 30, fig. 9) the last which requires to be
dealt with so far as the external features are concerned. The yolk has now
mainly passed into the abdomen, and the constriction separating the thorax
and abdomen has begun to appear. The yolk-sack has become absorbed, so that
the two halves of the ventral plate in the thorax are no longer widely
divaricated. The limbs have to a large extent acquired their permanent
structure, and the rings of which they are formed in the earlier stages are
now replaced by definite joints. A delicate cuticle has become formed,
which is not figured in my sections. The four rudimentary appendages have
disappeared, unless, which seems to me in the highest degree improbable,
they remain as the spinning mammillæ, two pairs of which are now present.
Behind is the anal lobe, which is much smaller and less conspicuous than in
the previous stage. The spinnerets and anal lobe are shewn as five papillæ
in Pl. 30, fig. 9. Dorsally the heart is now very conspicuous, and in front
of the cheliceræ may be seen the supra-oesophageal ganglia.
The indifferent mesoblast has now to a great extent become converted into
the permanent tissues. On the dorsal surface there was present in the last
stage a great mass of unformed mesoblast cells. This mass of cells has now
become divided into a somatic and splanchnic layer (Pl. 32, fig. 22). It
has, moreover, in the abdominal region at any rate, become divided up into
somites. At the junction between the successive somites the splanchnic
mesoblast on each side of the abdomen dips down into the yolk and forms a
septum (Pl. 32, fig. 22, _s_). The septa so formed, which were first
described by Barrois, are not complete. The septa of the two sides do not,
in the first place, quite meet along the median dorsal or ventral lines,
and in the second place they only penetrate the yolk for a certain
distance. Internally they usually end in a thickened border.
Along the line of insertion of each of these septa there is developed a
considerable space between the somatic and splanchnic layers of mesoblast.
The parts of the body-cavity so established are transversely directed
channels passing from the heart outwards. They probably constitute the
venous spaces, and perhaps also contain the transverse aortic branches.
In the intervals between these venous spaces the somatic and splanchnic
layers of mesoblast are in contact with each other.
I have not been able to work out satisfactorily the later stages of
development of the septa, but I have found that they play an important part
in the subsequent development of the abdomen. In the first place they send
off lateral offshoots, which unite the various septa together, and divide
up the cavity of the abdomen into a number of partially separated
compartments. There appears, however, to be left a free axial space for the
alimentary tract, the mesoblastic walls of which are, I believe, formed
from the septa.
At the present stage the splanchnic mesoblast, apart from the septa, is a
delicate membrane of flattened cells (fig. 22, _sp_). The somatic mesoblast
is thicker, and is formed of scattered cells (_so_).
The somatic layer is in part converted, in the posterior region of the
abdomen, into a delicate layer of longitudinal muscles, the fibres of which
are not continuous for the whole length of the body, but are interrupted at
the lines of junction of the successive segments. They are not present in
the anterior part of the abdomen. The longitudinal direction of these
fibres, and their division with myotomes, is interesting, since both these
characters, which are preserved in Scorpions, are lost in the abdomen of
the adult Spider.
The original mesoblastic somites have undergone quite as important changes
as the dorsal mesoblast. In the abdominal region the somatic layer
constitutes two powerful bands of longitudinal muscles, inserted anteriorly
at the root of the fourth ambulatory appendage, and posteriorly at the
spinning mammillæ. Between these two bands are placed the nervous bands.
The relation of these parts are shewn in the section in Pl. 32, fig. 20_d_,
which cuts the abdomen horizontally and longitudinally. The mesoblastic
bands are seen at _m._, and the nervous bands within them at _ab.g_. In the
thoracic region the part of the somatic layer in each limb is converted
into muscles, which are continued into dorsal and ventral muscles in the
thorax (vide fig. 20_c_). There are, in addition to these, intrinsic
transverse fibres on the ventral side of the thorax. Besides these muscles
there are in the thorax, attached to the suctorial extremity of the
stomodæum, three powerful muscles, which I believe to be derived from the
somatic mesoblast. One of these passes vertically down from the dorsal
surface, in the septum the commencement of which was described in the last
stage. The two other muscles are lateral, one on each side (Pl. 31,
fig. 20_c_.).
The heart has now, in most respects, reached its full development. It is
formed of an outer muscular layer, within which is a doubly-contoured
lining, containing nuclei at intervals, which is probably of the nature of
an epithelioid lining (Pl. 32, fig. 22, _ht_). In its lumen are numerous
blood-corpuscles (not represented in my figure). The heart lies in a space
bound below by the splanchnic mesoblast, and to the sides by the somatic
mesoblast. This space forms a kind of pericardium (fig. 22, _pc_), but
dorsally the heart is in contact with the epiblast. The arterial trunks
connected with it are fully established.
The nervous system has undergone very important changes.
In the abdominal region the ganglia of each side have fused together into a
continuous cord (fig. 21, _ab.g_). In fig. 20, in which the abdomen is cut
horizontally and longitudinally, there are seen the two abdominal cords
(_ab.g_) united by two transverse commissures; and I believe that there are
at this stage three or four transverse commissures at any rate, which
remain as indications of the separate ganglia, from the coalescence of
which the abdominal cords are formed. The two abdominal cords are parallel
and in close contact.
In the thoracic region changes of not less importance have taken place. The
ganglia are still distinct. The two cords formed of these ganglia are no
longer widely separated in median line, but meet, in the usual way, in the
ventral line. Transverse commissures have become established (fig. 20_c_)
between the ganglia of the two sides. There is as little trace at this, as
at the previous stages, of an ingrowth of epiblast, to form a median
portion of the central nervous system. Such a median structure has been
described by Hatschek for Lepidoptera, and he states that it gives rise to
the transverse commissures between the ganglia. My observations shew that
for the spider, at any rate, nothing of the kind is present.
As shewn in the longitudinal section (Pl. 32, fig. 21), the ganglion of the
cheliceræ has now united with the supra-oesophageal ganglion. It forms, as
is shewn in fig. 20_b_ (_ch.g._), a part of the oesophageal commissure, and
there is no sub-oesophageal commissure uniting the ganglia of the
cheliceræ, but the oesophageal ring is completed below by the ganglia of
the pedipalpi (fig. 20_c_, _pd.g._).
The supra-oesophageal ganglia have become completely separated from the
epiblast.
I have unfortunately not studied their constitution in the adult, so that I
cannot satisfactorily identify the parts which can be made out at this
stage.
I distinguish, however, the following regions:
(1) A central region containing the commissural part, and continuous below
with the ganglia of the cheliceræ.
(2) A dorsal region formed of two hemispherical lobes.
(3) A ventral anterior region.
The central region contains in its interior the commissural portion,
forming a punctiform, rounded mass in each ganglion. A transverse
commissure connects the two (vide fig. 20_b_).
The dorsal hemispherical lobes are derived from the part which, at the
earlier stage, contained the semicircular grooves. When the
supra-oesophageal ganglia become separated from the epidermis the cells
lining these grooves become constricted off with them, and form part of
these ganglia. Two cavities are thus formed in this part of the
supra-oesophageal ganglia. These cavities become, for the most part,
obliterated, but persist at the outer side of the hemispherical lobes
(figs. 20_a_ and 21).
The ventral lobe of the brain is a large mass shewn in longitudinal section
in fig. 21. It lies immediately in front of and almost in contact with the
ganglia of the cheliceræ.
The two hemispherical lobes agree in position with the fungiform body
(_pilzhutförmige Körpern_), which has attracted so much the attention of
anatomists, in the supra-oesophageal ganglia of Insects and Crustacea; but
till the adult brain of Spiders has been more fully studied it is not
possible to state whether the hemispherical lobes become fungiform bodies.
Hatschek[473] has described a special epiblastic invagination in the
supra-oesophageal ganglion of Bombyx, which is probably identical with the
semicircular groove of Spiders and Scorpions, but in the figure he gives
the groove does not resemble that in the Arachnida. A similar groove is
found in Peripatus, and there forms, as I have found, a large part of the
supra-oesophageal ganglia. It is figured by Moseley, _Phil. Trans._,
Vol. CLXIV. pl. lxxv, fig. 9.
Footnote 473: "Beiträge z. Entwick. d. Lepidopteren,"
_Jenaische Zeit._, Vol. XI. p. 124.
The stomodæum is considerably larger than in the last stage, and is lined
by a cuticle; it is a blind tube, the blind end of which is the suctorial
pouch of the adult. To this pouch are attached the vertical dorsal, and two
lateral muscles spoken of above.
The proctodæum (_pr._) has also grown in length, and the two Malpighian
vessels which grow out from its blind extremity (fig. 20_e_, _mp.g._) have
become quite distinct. The part now formed is the rectum of the adult. The
proctodæum is surrounded by a great mass of splanchnic mesoblast. The
mesenteron has as yet hardly commenced to be developed. There is, however,
a short tube close to the proctodæum (fig. 20_e_, _mes_), which would seem
to be the commencement of it. It ends blindly on the side adjoining the
rectum, but is open anteriorly towards the yolk, and there can be very
little doubt that it owes its origin to cells derived from the yolk. On its
outer surface is a layer of mesoblast.
From the condition of the mesenteron at this stage there can be but little
doubt that it will be formed, not on the surface, _but in the interior of
the yolk_. I failed to find any trace of an anterior part of the mesenteron
adjoining the stomodæum. In the posterior part of the thorax (vide
fig. 20_d_), there is undoubtedly no trace of the alimentary tract.
The presence of this rudiment shews that Barrois is mistaken in supposing
that the alimentary canal is formed entirely from the stomodæum and
proctodæum, which are stated by him to grow towards each other, and to meet
at the junction of the thorax and abdomen. My own impression is that the
stomodæum and proctodæum have reached their full extension at the present
stage, and that both the stomach in the thorax and the intestine in the
abdomen are products of the mesenteron.
The yolk retains its earlier constitution, being divided into polygonal
segments, formed of large yolk vesicles. The nuclei are more numerous than
before. In the thorax the yolk is anteriorly divided into two lobes by the
vertical septum, which contains the vertical muscle of the suctorial pouch.
In the posterior part of the thorax it is undivided.
I have not yet been able clearly to make out the eventual fate of the yolk.
At a subsequent stage, when the cavity of the abdomen is cut up into a
series of compartments by the growth of the septa, described above, the
yolk fills these compartments, and there is undoubtedly a proliferation of
yolk cells round the walls of these compartments. It would not be
unreasonable to conclude from this that the compartments were destined to
form the hepatic cæca, each cæcum being enclosed in a layer of splanchnic
mesoblast, and its hypoblastic wall being derived from the yolk cells. I
think that this hypothesis is probably correct, but I have met with some
facts which made me think it possible that the thickenings at the ends of
the septa, visible in Pl. 32, fig. 22, were the commencing hepatic cæca.
I must, in fact, admit that I have hitherto failed to work out
satisfactorily the history of the mesenteron and its appendages. The firm
cuticle of young spiders is an obstacle both in the way of making sections
and of staining, which I have not yet overcome.
_General Conclusions._
Without attempting to compare at length the development of the spiders with
that of other Arthropoda, I propose to point out a few features in the
development of spiders, which appear to shew that the Arachnida are
undoubtedly more closely related to the other Tracheata than to the
Crustacea.
The whole history of the formation of the mesoblast is very similar to that
in insects. The mesoblast in both groups is formed by a thickening of the
median line of the ventral plate (germinal streak).
In insects there is usually formed a median groove, the walls of which
become converted into a plate of mesoblast. In spiders there is no such
groove, but a median keel-like thickening of the ventral plate (Pl. 31,
fig. 11), is very probably an homologous structure. The unpaired plate of
mesoblast formed in both insects and Arachnida is exactly similar, and
becomes divided, in both groups, into two bands, one on each side of the
middle line. Such differences as there are between Insects and Arachnida
sink into insignificance compared with the immense differences in the
origin of the mesoblast between either group, and that in the Isopoda, or,
still more, the Malacostraca and most Crustacea. In most Crustacea we find
that the mesoblast is budded off from the walls of an invagination, which
gives rise to the mesenteron.
In both spiders and Myriopoda, and probably insects, the mesoblast is
subsequently divided into somites, the lumen of which is continued into the
limbs. In Crustacea mesoblastic somites have not usually been found, though
they appear occasionally to occur, _e.g._ Mysis, but they are in no case
similar to those in the Tracheata.
In the formation of the alimentary tract, again, the differences between
the Crustacea and Tracheata are equally marked, and the Arachnida agree
with the Tracheata. There is generally in Crustacea an invagination, which
gives rise to the mesenteron. In Tracheata this never occurs. The
proctodæum is usually formed in Crustacea before or, at any rate, not later
than the stomodæum[474]. The reverse is true for the Tracheata. In
Crustacea the proctodæum and stomodæum, especially the former, are very
long, and usually give rise to the greater part of the alimentary tract,
while the mesenteron is usually short.
Footnote 474: If Grobben's account of the development of Moina
is correct this statement must be considered not to be
universally true.
In the Tracheata the mesenteron is always considerable, and the proctodæum
is always short. The derivation of the Malpighian bodies from the
proctodæum is common to most Tracheata. Such organs are not found in the
Crustacea.
With reference to other points in my investigations, the evidence which I
have got that the cheliceræ are true postoral appendages supplied in the
embryo from a distinct postoral ganglion, confirms the conclusions of most
previous investigators, and shews that these appendages are equivalent to
the mandibles, or possibly the first pair of maxillæ of other Tracheata.
The invagination, which I have found, of part of a groove of epiblast in
the formation of the supra-oesophageal ganglia is of interest, owing to the
wide extension of a similar occurrence amongst the Tracheata.
The wide divarication of the ventral nerve cords in the embryo renders it
easy to prove that there is no median invagination of epiblast between
them, and supports Kleinenberg's observations on Lumbricus as to the
absence of this invagination. I have further satisfied myself as to the
absence of such an invagination in Peripatus. It is probable that Hatschek
and other observers who have followed him are mistaken in affirming the
existence of such an invagination in either the Chætopoda or the
Arthropoda.
The observations recorded in this paper on the yolk cells and their
derivations are, on the whole, in close harmony with the observations of
Dohrn, Bobretzky, and Graber, on Insects. They shew, however, that the
first formed mesoblastic plate does not give rise to the whole of the
mesoblast, but that during the whole of embryonic life the mesoblast
continues to receive accessions of cells derived from the cells of the
yolk.
_Araneina._
1. Balbiani, "Mémoire sur le Développement des Araneides," _Ann. Sci.
Nat._, series v, Vol. XVII. 1873.
2. J. Barrois, "Recherches s. l. Développement des Araignées," _Journal de
l'Anat. et de la Physiol._, 1878.
3. E. Claparède, _Recherches s. l'Evolution des Araignées_, Utrecht, 1860.
4. Herold, _De Generatione Araniorum in Ovo_, Marburg, 1824.
5. H. Ludwig, "Ueb. d. Bildung des Blastoderm bei d. Spinnen," _Zeit. f.
wiss. Zool._, Vol. XXVI. 1876.
EXPLANATION OF PLATES 30, 31, AND 32.
PLATE 30.
COMPLETE LIST OF REFERENCE LETTERS.
_ch._ Cheliceræ. _ch.g._ Ganglion of cheliceræ. _c.l._ Caudal lobe. _p.c._
Primitive cumulus. _pd._ Pedipalpi. _pr.l._ Præoral lobe. _pp_{1}. _pp_{2}.
_etc._ Provisional appendages. _sp._ Spinnerets. _st._ Stomodæum.
I-IV. Ambulatory appendages. 1-16. Postoral segments.
Fig. 1. Ovum, with primitive cumulus and streak proceeding from it.
Fig. 2. Somewhat later stage, in which the primitive cumulus is still
visible. Near the opposite end of the blastoderm is a white area, which is
probably the rudiment of the procephalic lobe.
Fig. 3_a_ and 3_b_. View of an embryo from the ventral surface and from the
side when six segments have become established.
Fig. 4. View of an embryo, ideally unrolled, when the first rudiments of
the appendages become visible.
Fig. 5. Embryo ideally unrolled at the stage when all the appendages have
become established.
Fig. 6. Somewhat older stage, when the limbs begin to be jointed. Viewed
from the side.
Fig. 7. Later stage, viewed from the side.
Fig. 7_a_. Same embryo as fig. 7, ideally unrolled.
Figs. 8_a_ and 8_b_. View from the ventral surface and from the side of an
embryo, after the ventral flexure has considerably advanced.
Fig. 9. Somewhat older embryo, viewed from the ventral surface.
PLATES 31 AND 32.
COMPLETE LIST OF REFERENCE LETTERS.
_ao._ Aorta. _ab.g._ Abdominal nerve cord. _ch._ Cheliceræ. _ch.g._
Ganglion of cheliceræ. _ep._ Epiblast. _hs._ Hemispherical lobe of
supra-oesophageal ganglion. _ht._ Heart. _l.l._ Lower lip. _m._ Muscles.
_me._ Mesoblast. _mes._ Mesenteron. _mp.g._ Malpighian tube. _ms._
Mesoblastic somite. _oe._ OEsophagus. _p.c._ Pericardium. _pd._ Pedipalpi.
_pd.g._ Ganglion of pedipalpi. _pr._ Proctodæum (rectum). _pr.c._ Primitive
cumulus. _s._ Septum in abdomen. _so._ Somatopleure. _sp._ Splanchnopleure.
_st._ Stomodæum. _su._ Suctorial apparatus. _su.g._ Supra-oesophageal
ganglion. _th. g._ Thoracic ganglion. _v.g._ Ventral nerve cord. _y.c._
Cells derived from yolk. _yk._ Yolk. _y.n._ Nuclei of yolk cells.
I_g_-IV_g_. Ganglia of ambulatory limbs. 1-16. Postoral segments.
Fig. 10. Section through an ovum, slightly younger than fig. 1. Shewing the
primitive cumulus and the columnar character of the cells of one half of
the blastoderm.
Fig. 11. Section through an embryo of the same age as fig. 2. Shewing the
median thickening of the blastoderm.
Fig. 12. Transverse section through the ventral plate of a somewhat older
embryo. Shewing the division of the ventral plate into epiblast and
mesoblast.
Fig. 13. Section through the ventral plate of an embryo of the same age as
fig. 3, shewing the division of the mesoblast of the ventral plate into two
mesoblastic bands.
Fig. 14. Transverse section through an embryo of the same age as fig. 5,
passing through an abdominal segment above and a thoracic segment below.
Fig. 15. Longitudinal section slightly to one side of the middle line
through an embryo of the same age.
Fig. 16. Transverse section through the ventral plate in the thoracic
region of an embryo of the same age as fig. 7.
Fig. 17. Transverse section through the procephalic lobes of an embryo of
the same age. _gr._ Section of hemicircular groove in procephalic lobe.
Fig. 18. Transverse section through the thoracic region of an embryo of the
same age as fig. 8.
Fig. 19. Section through the procephalic lobes of an embryo of the same
age.
Fig. 20_a_, _b_, _c_, _d_, _e_. Five sections through an embryo of the same
age as fig. 9. _a_ and _b_ are sections through the procephalic lobes, _c_
through the front part of the thorax. _d_ cuts transversely the posterior
parts of the thorax, and longitudinally and horizontally the ventral
surface of the abdomen. _e_ cuts the posterior part of the abdomen
longitudinally and horizontally, and shews the commencement of the
mesenteron.
Fig. 21. Longitudinal and vertical section of an embryo of the same age.
The section passes somewhat to one side of the middle line, and shews the
structure of the nervous system.
Fig. 22. Transverse section through the dorsal part of the abdomen of an
embryo of the same stage as fig. 9.
XVIII. ON THE SPINAL NERVES OF AMPHIOXUS[475].
Footnote 475: From the _Quarterly Journal of Microscopical
Science_, Vol. XX. 1880.
In an interesting memoir devoted to the elucidation of a series of points
in the anatomy and development of the Vertebrata, Schneider[476] has
described what he believes to be motor nerves in Amphioxus, which spring
from the anterior side of the spinal cord. According to Schneider these
nerves have been overlooked by all previous observers except Stieda.
Footnote 476: _Beiträge z. Anat. u. Entwick. d. Wirbelthiere_,
Berlin, 1879.
I[477] myself attempted to shew some time ago that anterior roots were
absent in Amphioxus; and in some speculations on the cranial nerves, I
employed this peculiarity of the nervous system of Amphioxus to support a
view that Vertebrata were primitively provided only with nerves of mixed
function springing from the posterior side of the spinal cord. Under these
circumstances, Schneider's statement naturally attracted my attention, and
I have made some efforts to satisfy myself as to its accuracy. The nerves,
as he describes them, are very peculiar. They arise from a number of
distinct roots in the hinder third of each segment. They form a flat
bundle, of which part passes upwards and part downwards. When they meet the
muscles they bend backwards, and fuse with the free borders of the
muscle-plates. The fibres, which at first sight appear to form the nerve,
are, however, transversely striated, and are regarded by Schneider as
muscles; and he holds that each muscle-plate sends a process to the edge of
the spinal cord, which there receives its innervation. A considerable body
of evidence is requisite to justify a belief in the existence of such very
extraordinary and unparalleled motor nerves; and for my part I cannot say
that Schneider's observations are convincing to me. I have attempted to
repeat his observations, employing the methods he describes.
Footnote 477: "On the Spinal Nerves of Amphioxus," _Journ. of
Anat. and Phys._ Vol. X. 1876. [This edition, No. IX. p. 197.]
In the first place, he states that by isolating the spinal cord by boiling
in acetic acid, the anterior roots may be brought into view as numerous
conical processes of the spinal cord in each segment. I find by treating
the spinal cord in this way, that processes more or less similar, but more
irregular than those which he figures, are occasionally present; but I
cannot persuade myself that they are anything but parts of the sheath of
the spinal cord which is not completely dissolved by treatment with acetic
acid. By treatment with nitric acid _no such processes are to be seen_,
though the whole length and very finest branches of the posterior nerves
are preserved.
By treating with nitric acid and clarifying by oil of cloves, and
subsequently removing one half of the body so as to expose the spinal cord
_in sitû_, the origin and distribution of the posterior nerves is very
clearly exhibited. But I have failed to detect any trace of the anterior
nerve-roots. Horizontal section, which ought also to bring them clearly
into view, failed to shew me anything which I could interpret as such. I
agree with Schneider that a process of each muscle-plate is prolonged up to
the anterior border of the spinal cord, but I can find no trace of a
connection between it and the cord.
Schneider has represented a transverse section in which the anterior nerves
are figured. I am very familiar with an appearance in section such as that
represented in his figure, but I satisfied myself when I previously studied
the nerves in Amphioxus, that the body supposed to be a nerve by Schneider
was nothing else than part of the intermuscular septum, and after
re-examining my sections I see no reason to alter my view.
A very satisfactory proof that the ventral nerves do not exist would be
found, if it could be established that the dorsal nerves contained both
motor and sensory fibres. So far I have not succeeded in proving this; I
have not, however, had fresh specimens to assist me in the investigation.
Langerhans[478], whose careful observations appear to me to have been
undervalued by Schneider, figures a branch distributed to the muscles,
which passes off from the dorsal roots. Till the inaccuracy of this
observation is demonstrated, the balance of evidence appears to me to be
opposed to Schneider's view.
Footnote 478: _Archiv f. Mikros. Anatomie_, Vol. XII.
XIX. ADDRESS TO THE DEPARTMENT OF ANATOMY AND PHYSIOLOGY OF THE BRITISH
ASSOCIATION, 1880.
In the spring of the present year, Professor Huxley delivered an address at
the Royal Institution, to which he gave the felicitous title of '_The
coming of age of the origin of species_.' It is, as he pointed out,
twenty-one years since Mr Darwin's great work was published, and the
present occasion is an appropriate one to review the effect which it has
had on the progress of biological knowledge.
There is, I may venture to say, no department of biology the growth of
which has not been profoundly influenced by the Darwinian theory. When
Messrs Darwin and Wallace first enunciated their views to the scientific
world, the facts they brought forward seemed to many naturalists
insufficient to substantiate their far-reaching conclusions. Since that
time an overwhelming mass of evidence has, however, been rapidly
accumulating in their favour. Facts which at first appeared to be opposed
to their theories have one by one been shewn to afford striking proofs of
their truth. There are at the present time but few naturalists who do not
accept in the main the Darwinian theory, and even some of those who reject
many of Darwin's explanations still accept the fundamental position that
all animals are descended from a common stock.
To attempt in the brief time which I have at my disposal to trace the
influence of the Darwinian theory on all the branches of anatomy and
physiology would be wholly impossible, and I shall confine myself to an
attempt to do so for a small section only. There is perhaps no department
of Biology which has been so revolutionised, if I may use the term, by the
theory of animal evolution, as that of Development or Embryology. The
reason of this is not far to seek. According to the Darwinian theory, the
present order of the organic world has been caused by the action of two
laws, known as the laws of heredity and of variation. The law of heredity
is familiarly exemplified by the well-known fact that offspring resemble
their parents. Not only, however, do the offspring belong to the same
species as their parents, but they inherit the individual peculiarities of
their parents. It is on this that the breeders of cattle depend, and it is
a fact of every-day experience amongst ourselves. A further point with
reference to heredity to which I must call your attention is the fact that
the characters, which display themselves at some special period in the life
of the parent, are acquired by the offspring at a corresponding period.
Thus, in many birds the males have a special plumage in the adult state.
The male offspring is not, however, born with the adult plumage, but only
acquires it when it becomes adult.
The law of variation is in a certain sense opposed to the law of heredity.
It asserts that the resemblance which offspring bear to their parents is
never exact. The contradiction between the two laws is only apparent. All
variations and modifications in an organism are directly or indirectly due
to its environments; that is to say, they are either produced by some
direct influence acting upon the organism itself, or by some more subtle
and mysterious action on its parents; and the law of heredity really
asserts that the offspring and parent would resemble each other if their
environments were the same. Since, however, this is never the case, the
offspring always differ to some extent from the parents. Now, according to
the law of heredity, every acquired variation tends to be inherited, so
that, by a summation of small changes, the animals may come to differ from
their parent stock to an indefinite extent.
We are now in a position to follow out the consequences of these two laws
in their bearing on development. Their application will best be made
apparent by taking a concrete example. Let us suppose a spot on the surface
of some very simple organism to become, at a certain period of life,
pigmented, and therefore to be especially sensitive to light. In the
offspring of this form, the pigment-spot will reappear at a corresponding
period; and there will therefore be a period in the life of the offspring
during which there is no pigment-spot, and a second period in which there
is one. If a naturalist were to study the life-history, or, in other words,
the embryology of this form, this fact about the pigment-spot would come to
his notice, and he would be justified, from the laws of heredity, in
concluding that the species was descended from an ancestor without a
pigment-spot, because a pigment-spot was absent in the young. Now, we may
suppose the transparent layer of skin above the pigment-spot to become
thickened, so as gradually to form a kind of lens, which would throw an
image of external objects on the pigment-spot. In this way a rudimentary
eye might be evolved out of the pigment-spot. A naturalist studying the
embryology of the form with this eye would find that the pigment-spot was
formed before the lens, and he would be justified in concluding, by the
same process of reasoning as before, that the ancestors of the form he was
studying first acquired a pigment-spot and then a lens. We may picture to
ourselves a series of steps by which the simple eye, the origin of which I
have traced, might become more complicated; and it is easy to see how an
embryologist studying the actual development of this complicated eye would
be able to unravel the process of its evolution.
The general nature of the methods of reasoning employed by embryologists,
who accept the Darwinian theory, is exemplified by the instance just given.
If this method is a legitimate one, and there is no reason to doubt it, we
ought to find that animals, in the course of their development, pass
through a series of stages, in each of which they resemble one of their
remote ancestors; but it is to be remembered that, in accordance with the
law of variation, there is a continual tendency to change, and that the
longer this tendency acts the greater will be the total effect. Owing to
this tendency, we should not expect to find a perfect resemblance between
an animal, at different stages of its growth, and its ancestors; and the
remoter the ancestors, the less close ought the resemblance to be. In
spite, however, of this limitation, it may be laid down as one of the
consequences of the law of inheritance that every animal ought, in the
course of its individual development, to repeat with more or less fidelity
the history of its ancestral evolution.
A direct verification of this proposition is scarcely possible. There is
ample ground for concluding that the forms from which existing animals are
descended have in most instances perished; and although there is no reason
why they should not have been preserved in a fossil state, yet, owing to
the imperfection of the geological record, palæontology is not so often of
service as might have been hoped.
While, for the reasons just stated, it is not generally possible to prove
by direct observation that existing forms in their embryonic state repeat
the characters of their ancestors, there is another method by which the
truth of this proposition can be approximately verified.
A comparison of recent and fossil forms shews that there are actually
living at the present day representatives of a considerable proportion of
the groups which have in previous times existed on the globe, and there are
therefore forms allied to the ancestors of those living at the present day,
though not actually the same species. If therefore it can be shewn that the
embryos of existing forms pass through stages in which they have the
characters of more primitive groups, a sufficient proof of our proposition
will have been given.
That such is often the case is a well-known fact, and was even known before
the publication of Darwin's works. Von Baer, the greatest embryologist of
the century, who died at an advanced age but a few years ago, discussed the
proposition at considerable length in a work published between the years
1830 and 1840. He came to the conclusion that the embryos of higher forms
never actually resemble lower forms, but only the embryos of lower forms;
and he further maintained that such resemblances did not hold at all, or
only to a very small extent, beyond the limits of the larger groups. Thus
he believed that, though the embryos of Vertebrates might agree amongst
themselves, there was no resemblance between them and the embryos of any
invertebrate group. We now know that these limitations of Von Baer do not
hold good, but it is to be remembered that the meaning _now_ attached by
embryologists to such resemblances was quite unknown to him.
These preliminary remarks will, I trust, be sufficient to demonstrate how
completely modern embryological reasoning is dependent on the two laws of
inheritance and variation, which constitute the keystones of the Darwinian
theory.
Before the appearance of the _Origin of Species_ many very valuable
embryological investigations were made, but the facts discovered were to
their authors merely so many ultimate facts, which admitted of being
classified, but could not be explained. No explanation could be offered of
why it is that animals, instead of developing in a simple and
straightforward way, undergo in the course of their growth a series of
complicated changes, during which they often acquire organs which have no
function, and which, after remaining visible for a short time, disappear
without leaving a trace.
No explanation, for instance, could be offered of why it is that a frog in
the course of its growth has a stage in which it breathes like a fish, and
then why it is like a newt with a long tail, which gradually becomes
absorbed, and finally disappears. To the Darwinian the explanation of such
facts is obvious. The stage when the tadpole breathes by gills is a
repetition of the stage when the ancestors of the frog had not advanced in
the scale of development beyond a fish, while the newt-like stage implies
that the ancestors of the frog were at one time organized very much like
the newts of to-day. The explanation of such facts has opened out to the
embryologist quite a new series of problems. These problems may be divided
into two main groups, technically known as those of phylogeny and those of
organogeny. The problems of phylogeny deal with the genealogy of the animal
kingdom. A complete genealogy would form what is known as a natural
classification. To attempt to form such a classification has long been the
aim of a large number of naturalists, and it has frequently been attempted
without the aid of embryology. The statements made in the earlier part of
my address clearly shew how great an assistance embryology is capable of
giving in phylogeny; and as a matter of fact embryology has been during the
last few years very widely employed in all phylogenetic questions, and the
results which have been arrived at have in many cases been very striking.
To deal with these results in detail would lead me into too technical a
department of my subject; but I may point out that amongst the more
striking of the results obtained _entirely_ by embryological methods is the
demonstration that the Vertebrata are not, as was nearly universally
believed by older naturalists, separated by a wide gulf from the
Invertebrata, but that there is a group of animals, known as the Ascidians,
formerly united with the Invertebrata, which are now universally placed
with the Vertebrata.
The discoveries recently made in organogeny, or the genesis of organs, have
been quite as striking, and in many respects even more interesting, than
those in phylogeny, and I propose devoting the remainder of my address to a
history of results which have been arrived at with reference to the origin
of the nervous system.
To render clear the nature of these results I must say a few words as to
the structure of the animal body. The body is always built of certain
pieces of protoplasm, which are technically known to biologists as cells.
The simplest organisms are composed either of a single piece of this kind,
or of several similar pieces loosely aggregated together. Each of these
pieces or cells is capable of digesting and assimilating food, and of
respiring; it can execute movements, and is sensitive to external stimuli,
and can reproduce itself. All the functions of higher animals can, in fact,
be carried on in this single cell. Such lowly organized forms are known to
naturalists as the Protozoa. All other animals are also composed of cells,
but these cells are no longer complete organisms in themselves. They
exhibit a division of labour: some carrying on the work of digestion; some,
which we call nerve-cells, receiving and conducting stimuli; some, which we
call muscle-cells, altering their form--in fact, contracting in one
direction--under the action of the stimuli brought to them by the
nerve-cells. In most cases a number of cells with the same function are
united together, and thus constitute a tissue. Thus the cells which carry
on the work of digestion form a lining membrane to a tube or sack, and
constitute a tissue known as a secretory epithelium. The whole of the
animals with bodies composed of definite tissues of this kind are known as
the Metazoa.
A considerable number of early developmental processes are common to the
whole of the Metazoa.
In the first place every Metazoon commences its existence as a simple cell,
in the sense above defined; this cell is known as the ovum. The first
developmental process which takes place consists in the division or
segmentation of the single cell into a number of smaller cells. The cells
then arrange themselves into two groups or layers known to embryologists as
the _primary germinal layers_. These two layers are usually placed one
within the other round a central cavity. The inner of the two is called the
hypoblast, the outer the epiblast. The existence of these two layers in the
embryos of vertebrated animals was made out early in the present century by
Pander, and his observations were greatly extended by Von Baer and Remak.
But it was supposed that these layers were confined to vertebrated animals.
In the year 1849, and at greater length in 1859, Huxley demonstrated that
the bodies of all the polype tribe or Coelenterata--that is to say of the
group to which the common polype, jelly-fish and the sea-anemone
belong--were composed of two layers of cells, and stated that in his
opinion these two layers were homologous with the epiblast and hypoblast of
vertebrate embryos. This very brilliant discovery came before its time. It
fell upon barren ground, and for a long time bore no fruit. In the year
1866 a young Russian naturalist named Kowalevsky began to study by special
histological methods the development of a number of invertebrated forms of
animals, and discovered that at an early stage of development the bodies of
all these animals were divided into germinal layers like those in
vertebrates. Biologists were not long in recognizing the importance of
these discoveries, and they formed the basis of two remarkable essays, one
by our own countryman, Professor Lankester, and the other by a
distinguished German naturalist, Professor Haeckel, of Jena.
In these essays the attempt was made to shew that the stage in development
already spoken of, in which the cells are arranged in the form of two
layers enclosing a central cavity has an ancestral meaning, and that it is
to be interpreted to signify that all the Metazoa are descended from an
ancestor which had a more or less oval form, with a central digestive
cavity provided with a single opening, serving both for the introduction of
food and for the ejection of indigestible substances. The body of this
ancestor was supposed to have been a double-walled sack formed of an inner
layer, the hypoblast, lining the digestive cavity, and an outer layer, the
epiblast. To this form Haeckel gave the name of gastræa or gastrula.
There is every reason to think that Lankester and Haeckel were quite
justified in concluding that a form more or less like that just described
was the ancestor of the Metazoa; but the further speculations contained in
their essays as to the origin of this form from the Protozoa can only be
regarded as suggestive feelers, which, however, have been of great
importance in stimulating and directing embryological research. It is,
moreover, very doubtful whether there are to be found in the developmental
histories of most animals any traces of this gastræa ancestor, other than
the fact of their passing through a stage in which the cells are divided
into two germinal layers.
The key to the nature of the two germinal layers is to be found in Huxley's
comparison between them, and the two layers in the fresh-water polype and
the sea-anemone. The epiblast is the primitive skin, and the hypoblast is
the primitive epithelial wall of the alimentary tract.
In the whole of the polype group, or Coelenterata, the body remains through
life composed of the two layers, which Huxley recognized as homologous with
the epiblast and hypoblast of the Vertebrata; but in all the higher Metazoa
a third germinal layer, known as the mesoblast, early makes its appearance
between the two primary layers. The mesoblast originates as a
differentiation of one or of both the primary germinal layers; but although
the different views which have been held as to its mode of origin form an
important section of the history of recent embryological investigations, I
must for the moment confine myself to saying that from this layer there
take their origin--the whole of the muscular system, of the vascular
system, and of that connective-tissue system which forms the internal
skeleton, tendons, and other parts.
We have seen that the epiblast represents the skin or epidermis of the
simple sack-like ancestor common to all the Metazoa. In all the higher
Metazoa it gives rise, as might be expected, to the epidermis, but it gives
rise at the same time to a number of other organs; and, in accordance with
the principles laid down in the earlier part of my address, it is to be
concluded that _the organs so derived have been formed as differentiations
of the primitive epidermis_. One of the most interesting of recent
embryological discoveries is the fact that the nervous system is, in all
but a very few doubtful cases, derived from the epiblast. This fact was
made out for vertebrate animals by the great embryologist Von Baer; and the
Russian naturalist Kowalevsky, to whose researches I have already alluded,
shewed that this was true for a large number of invertebrate animals. The
derivation of the nervous system from the epiblast has since been made out
for a sufficient number of forms satisfactorily to establish the
generalization that it is all but universally derived from the epiblast.
In any animal in which there is no distinct nervous system, it is obvious
that the general surface of the body must be sensitive to the action of its
surroundings, or to what are technically called stimuli. We know
experimentally that this is so in the case of the Protozoa, and of some
very simple Metazoa, such as the freshwater Polype or Hydra, where there is
no distinct nervous system. The skin or epidermis of the ancestor of the
Metazoa was no doubt similarly sensitive; and the fact of the nervous
system being derived from the epiblast implies that the functions of the
central nervous system, which were originally taken by the whole skin,
became gradually concentrated in a special part of the skin which was step
by step removed from the surface, and finally became a well-defined organ
in the interior of the body.
What were the steps by which this remarkable process took place? How has it
come about that there are nerves passing from the central nervous system to
all parts of the skin, and also to the muscles? How have the arrangements
for reflex actions arisen by which stimuli received on the surface of the
body are carried to the central part of the nervous system, and are thence
transmitted to the appropriate muscles, and cause them to contract? All
these questions require to be answered before we can be said to possess a
satisfactory knowledge of the origin of the nervous system. As yet,
however, the knowledge of these points derived from embryology is
imperfect, although there is every hope that further investigation will
render it less so. Fortunately, however, a study of comparative anatomy,
especially that of the Coelenterata, fills up some of the gaps left from
our study of embryology.
From embryology we learn that the ganglion-cells of the central part of the
nervous system are originally derived from the simple undifferentiated
epithelial cells of the surface of the body. We further learn that the
nerves are out-growths of the central nervous system. It was supposed till
quite recently that the nerves in Vertebrates were derived from parts of
the middle germinal layer or mesoblast, and that they only became
secondarily connected with the central nervous system. This is now known
not to be the case, but the nerves are formed as processes growing out from
the central part of the nervous system.
Another important fact shewn by embryology is that the central nervous
system, and percipient portion of the organs of special sense, are often
formed from the same part of the primitive epidermis. Thus, in ourselves
and in other vertebrate animals the sensitive part of the eye, known as the
retina, is formed from two lateral lobes of the front part of the primitive
brain. The crystalline lens and cornea of the eye are, however,
subsequently formed from the skin.
The same is true for the peculiar compound eyes of crabs or Crustacea. The
most important part of the central nervous system of these animals is the
supra-oesophageal ganglia, often known as the brain, and these are formed
in the embryo from two thickened patches of the skin at the front end of
the body. These thickened patches become gradually detached from the
surface, remaining covered over by a layer of skin. They then constitute
the supra-oesophageal ganglia; but they form not only the ganglia, but also
the rhabdons or retinal elements of the eye--the parts in fact which
correspond to the rods and cones in our own retina. The layer of epidermis
or skin which lies immediately above the supra-oesophageal ganglia becomes
gradually converted into the refractive media of the crustacean eye. A
cuticle which lies on its surface forms the peculiar facets on the surface
of the eye, which are known as the corneal lenses, while the cells of the
epidermis give rise to lens-like bodies known as the crystalline cones.
It would be easy to quote further instances of the same kind, but I trust
that the two which I have given will be sufficient to shew the kind of
relation which often exists between the organs of special sense, especially
those of vision, and the central nervous system. It might have been
anticipated _à priori_ that organs of special sense would only appear in
animals provided with a well-developed central nervous system. This,
however, is not the case. Special cells, with long delicate hairs, which
are undoubtedly highly sensitive structures, are present in animals in
which as yet nothing has been found which could be called a central nervous
system; and there is every reason to think that the organs of special sense
originated _pari passu_ with the central nervous system. It is probable
that in the simplest organisms the whole body is sensitive to light, but
that with the appearance of pigment-cells in certain parts of the body, the
sensitiveness to light became localised to the areas where the
pigment-cells were present. Since, however, it was necessary that stimuli
received by such organs should be communicated to other parts of the body,
some of the epidermic cells in the neighbourhood of the pigment-spots,
which were at first only sensitive, in the same manner as other cells of
the epidermis, became gradually differentiated into special nerve-cells. As
to the details of this differentiation, embryology does not as yet throw
any great light; but from the study of comparative anatomy there are
grounds for thinking that it was somewhat as follows:--Cells placed on the
surface sent protoplasmic processes of a nervous nature inwards, which came
into connection with nervous processes from similar cells placed in other
parts of the body. The cells with such processes then became removed from
the surface, forming a deeper layer of the epidermis below the sensitive
cells of the organ of vision. With these cells they remained connected by
protoplasmic filaments, and thus they came to form a thickening of the
epidermis underneath the organ of vision, the cells of which received their
stimuli from those of the organ of vision, and transmitted the stimuli so
received to other parts of the body. Such a thickening would obviously be
the rudiment of a central nervous system, and it is easy to see by what
steps it might become gradually larger and more important, and might
gradually travel inwards, remaining connected with the sense organ at the
surface by protoplasmic filaments, which would then constitute nerves. The
rudimentary eye would at first merely consist partly of cells sensitive to
light, and partly of optical structures constituting the lens, which would
throw an image of external objects upon it, and so convert the whole
structure into a true organ of vision. It has thus come about that, in the
development of the individual, the retina or sensitive part of the eye is
first formed in connection with the central nervous system, while the
lenses of the eye are independently evolved from the epidermis at a later
period.
The general features of the origin of the nervous system which have so far
been made out by means of the study of embryology are the following:--
(1) That the nervous system of the higher Metazoa has been developed in the
course of a long series of generations by a gradual process of
differentiation of parts of the epidermis.
(2) That part of the central nervous system of many forms arose as a local
collection of nerve-cells in the epidermis, in the neighbourhood of
rudimentary organs of vision.
(3) That ganglion cells have been evolved from simple epithelial cells of
the epidermis.
(4) That the primitive nerves were outgrowths of the original ganglion
cells; and that the nerves of the higher forms are formed as outgrowths of
the central nervous system.
The points on which embryology has not yet thrown a satisfactory light
are:--
(1) The steps by which the protoplasmic processes, from the primitive
epidermic cells, became united together so as to form a network of
nerve-fibres, placing the various parts of the body in nervous
communication.
(2) The process by which nerves became connected with muscles, so that a
stimulus received by a nerve-cell could be communicated to and cause a
contraction in a muscle.
Recent investigations on the anatomy of the Coelenterata, especially of
jelly-fish and sea-anemones, have thrown some light on these points,
although there is left much that is still obscure.
In our own country Mr Romaines has conducted some interesting physiological
experiments on these forms; and Professor Schäfer has made some important
histological investigations upon them. In Germany a series of interesting
researches have also been made on them by Professors Kleinenberg, Claus and
Eimer, and more especially by the brothers Hertwig, of Jena. Careful
histological investigations, especially those of the last-named authors,
have made us acquainted with the forms of some very primitive types of
nervous system. In the common sea-anemones there are, for instance, no
organs of special sense, and no definite central nervous system. There are,
however, scattered throughout the skin, and also throughout the lining of
the digestive tract, a number of specially modified epithelial cells, which
are no doubt delicate organs of sense. They are provided at their free
extremity with a long hair, and are prolonged on their inner side into a
fine process which penetrates the deeper part of the epithelial layer of
the skin or digestive wall. They eventually join a fine network of
protoplasmic fibres which forms a special layer immediately within the
epithelium. The fibres of this network are no doubt essentially nervous. In
addition to fibres there are, moreover, present in the network cells of the
same character as the multipolar ganglion-cells in the nervous system of
Vertebrates, and some of these cells are characterized by sending a process
into the superjacent epithelium. Such cells are obviously epithelial cells
in the act of becoming nerve-cells; and it is probable that the nerve-cells
are, in fact, sense-cells which have travelled inwards and lost their
epithelial character.
There is every reason to think that the network just described is not only
continuous with the sense-cells in the epithelium, but that it is also
continuous with epithelial cells which are provided with muscular
prolongations. The nervous system thus consists of a network of
protoplasmic fibres, continuous on the one hand with sense-cells in the
epithelium, and on the other with muscular cells. The nervous network is
generally distributed both beneath the epithelium of the skin and that of
the digestive tract, but is especially concentrated in the disc-like region
between the mouth and tentacles. The above observations have thrown a very
clear light on the characters of the nervous system at an early stage of
its evolution, but they leave unanswered the questions (1) how the nervous
network first arose, and (2) how its fibres became continuous with muscles.
It is probable that the nervous network took its origin from processes of
the sense-cells. The processes of the different cells probably first met
and then fused together, and, becoming more arborescent, finally gave rise
to a complicated network.
The connection between this network and the muscular cells also probably
took place by a process of contact and fusion.
Epithelial cells with muscular processes were discovered by Kleinenberg
before epithelial cells with nervous processes were known, and he suggested
that the epithelial part of such cells was a sense-organ, and that the
connecting part between this and the contractile processes was a
rudimentary nerve. This ingenious theory explained completely the fact of
nerves being continuous with muscles; but on the further discoveries being
made which I have just described, it became obvious that this theory would
have to be abandoned, and that some other explanation would have to be
given of the continuity between nerves and muscles. The hypothetical
explanation just offered is that of fusion.
It seems very probable that many of the epithelial cells were originally
provided with processes the protoplasm of which, like that of the Protozoa,
carried on the functions of nerves and muscles at the same time, and that
these processes united amongst themselves into a network. By a process of
differentiation parts of this network may have become specially
contractile, and other parts may have lost their contractility and become
solely nervous. In this way the connection between nerves and muscles might
be explained, and this hypothesis fits in very well with the condition of
the neuro-muscular system as we find it in the Coelenterata.
The nervous system of the higher Metazoa appears then to have originated
from a differentiation of some of the superficial epithelial cells of the
body, though it is possible that some parts of the system may have been
formed by a differentiation of the alimentary epithelium. The cells of the
epithelium were most likely at the same time contractile and sensory, and
the differentiation of the nervous system may very probably have commenced,
in the first instance, from a specialization in the function of part of a
network formed of neuro-muscular prolongations of epithelial cells. A
simultaneous differentiation of other parts of the network into muscular
fibres may have led to the continuity at present obtaining between nerves
and muscles.
Local differentiations of the nervous network, which was no doubt
distributed over the whole body, took place on the formation of organs of
special sense, and such differentiations gave rise to the formation of a
central nervous system. The central nervous system was at first continuous
with the epidermis, but became separated from it and travelled inwards.
Ganglion-cells took their origin from sensory epithelial cells, provided
with prolongations, continuous with the nervous network. Such epithelial
cells gradually lost their epithelial character, and finally became
completely detached from the epidermis.
Nerves, such as we find them in the higher types, originated from special
differentiations of the nervous network, radiating from the parts of the
central nervous system.
Such, briefly, is the present state of our knowledge as to the genesis of
the nervous system. I ought not, however, to leave this subject without
saying a few words as to the hypothetical views which the distinguished
evolutionist Mr Herbert Spencer has put forward on this subject in his work
on Psychology.
For Herbert Spencer nerves have originated, not as processes of epithelial
cells, but from the passage of motion along the lines of least resistance.
The nerves would seem, according to this view, to have been formed in any
tissue from the continuous passage of nervous impulses through it. "A wave
of molecular disturbance," he says, "passing along a tract of mingled
colloids closely allied in composition, and isomerically transforming the
molecules of one of them, will be apt at the same time to form some new
molecules of the same type," and thus a nerve becomes established.
A nervous centre is formed, according to Herbert Spencer, at the point in
the colloid in which nerves are generated, where a single nervous wave
breaks up, and its parts diverge along various lines of least resistance.
At such points some of the nerve-colloid will remain in an amorphous state,
and as the wave of molecular motion will there be checked, it will tend to
cause decompositions amongst the unarranged molecules. The decompositions
must, he says, cause "additional molecular motion to be disengaged; so that
along the outgoing lines there will be discharged an augmented wave. Thus
there will arise at this point something having the character of a ganglion
corpuscle."
These hypotheses of Herbert Spencer, which have been widely adopted in this
country, are, it appears to me, not borne out by the discoveries to which I
have called your attention to-day. The discovery that nerves have been
developed from processes of epithelial cells, gives a very different
conception of their genesis to that of Herbert Spencer, which makes them
originate from the passage of nervous impulses through a tract of mingled
colloids; while the demonstration that ganglion-cells arose as epithelial
cells of special sense, which have travelled inwards from the surface,
admits still less of a reconciliation with Herbert Spencer's view on the
same subject.
Although the present state of our knowledge on the genesis of the nervous
system is a great advance on that of a few years ago, there is still much
remaining to be done to make it complete.
The subject is well worth the attention of the morphologist, the
physiologist, or even of the psychologist, and we must not remain satisfied
by filling up the gaps in our knowledge by such hypotheses as I have been
compelled to frame. New methods of research will probably be required to
grapple with the problems that are still unsolved; but when we look back
and survey what has been done in the past, there can be no reason for
mistrusting our advance in the future.
XX. ON THE DEVELOPMENT OF THE SKELETON OF THE PAIRED FINS OF
ELASMOBRANCHII, CONSIDERED IN RELATION TO ITS BEARINGS ON THE NATURE OF
THE LIMBS OF THE VERTEBRATA[479].
Footnote 479: From the _Proceedings of the Zoological Society
of London_, 1881.
(With Plate 33.)
Some years ago the study of the development of the soft parts of the fins
in several Elasmobranch types, more especially in _Torpedo,_ led me to the
conclusion that the vertebrate limbs were remnants of two continuous
lateral fins[480]. More or less similar views (which I was not at that time
acquainted with) had been previously held by Maclise, Humphrey, and other
anatomists; these views had not, however, met with much acceptance, and
diverge in very important points from those put forward by me. Shortly
after the appearance of my paper, J. Thacker published two interesting
memoirs comparing the skeletal parts of the paired and unpaired fins[481].
Footnote 480: "Monograph on the Development of Elasmobranch
Fishes," pp. 319, 320.
Footnote 481: J. K. Thacker, "Median and Paired Fins; a
Contribution to the History of the Vertebrate Limbs," _Trans.
of the Connecticut Acad._ Vol. III. 1877. "Ventral Fins of
Ganoids," _Trans. of the Connecticut Acad._ Vol. IV. 1877.
In these memoirs Thacker arrives at conclusions as to the nature of the
fins in the main similar to mine, but on entirely independent grounds. He
attempts to shew that the structure of the skeleton of the paired fins is
essentially the same as that of the unpaired fins, and in this comparison
lays special stress on the very simple skeleton of the pelvic fin in the
cartilaginous Ganoids, more especially in _Acipenser_ and _Polyodon_. He
points out that the skeleton of the pelvic fin of _Polyodon_ consists
essentially of a series of nearly isolated rays, which have a strikingly
similar arrangement to that of the rays of the skeleton in many unpaired
fins. He sums up his views in the following way[482]:--
Footnote 482: _Loc. cit._ p. 298.
"As the dorsal and anal fins were specializations of the median folds
of _Amphioxus,_ so the paired fins were specializations of the two
lateral folds which are supplementary to the median in completing the
circuit of the body. These lateral folds, then, are the homologues of
Wolffian ridges, in embryos of higher forms. Here, as in the median
fins, there were formed chondroid and finally cartilaginous rods.
These became at least twice segmented. The orad ones, with more or
less concrescence proximally, were prolonged inwards. The cartilages
spreading met in the middle line; and a later extension of the
cartilages dorsad completed the limb-girdle.
"The limbs of the Protognathostomi consisted of a series of parallel
articulated cartilaginous rays. They may have coalesced somewhat
proximally and orad. In the ventral pair they had extended themselves
mesiad until they had nearly or quite met and formed the hip-girdle;
they had not here extended themselves dorsad. In the pectoral limb the
same state of things prevailed, but was carried a step further,
namely, by the dorsal extension of the cartilage constituting the
scapular portion, thus more nearly forming a ring or girdle."
The most important point in Thacker's theories which I cannot accept is the
derivation of the folds, of which the paired fins of the Vertebrata are
supposed to be specializations, from the lateral folds of _Amphioxus;_ and
Thacker himself recognizes that this part of his theory stands on quite a
different footing to the remainder.
Not long after the publication of Thacker's paper, an important memoir was
published by Mivart in the _Transactions_ of this Society[483]. The object
of the researches recorded in this paper was, as Mivart explains, to test
how far the hard parts of the limbs and of the azygos fins may have arisen
through centripetal chondrifications or calcifications, and so be
genetically exoskeletal[484].
Footnote 483: St George Mivart, "On the Fins of
Elasmobranchii," _Zoological Trans._ Vol. X.
Footnote 484: Mivart used the term exoskeletal in an unusual
and (as it appears to me) inconvenient manner. The term is
usually applied to dermal skeletal structures; but the skeleton
of the limbs, with which we are here concerned, is undoubtedly
not of this nature.
Mivart's investigations and the majority of his views were independent of
Thacker's memoir; but he acknowledges that he has derived from Thacker the
view that pelvic and pectoral girdles, as well as the skeleton of the
limbs, may have arisen independently of the axial skeleton.
The descriptive part of Mivart's paper contains an account of the structure
of a great variety of interesting and undescribed types of paired and
unpaired fins, mainly of Elasmobranchii. The following is the summary given
by Mivart of the conclusions at which he has arrived[485]:--
Footnote 485: _Loc. cit._ p. 480.
"1. Two continuous lateral longitudinal folds were developed, similar
to dorsal and ventral median longitudinal folds.
"2. Separate narrow solid supports (radials), in longitudinal series,
and with their long axes directed more or less outwards at right
angles with the long axis of the body, were developed in varying
extents in all these four longitudinal folds.
"3. The longitudinal folds became interrupted variously, but so as to
form two prominences on each side, _i.e._ the primitive paired limbs.
"4. Each anterior paired limb increased in size more rapidly than the
posterior limb.
"5. The bases of the cartilaginous supports coalesced as was needed,
according to the respective practical needs of the different separate
portions of the longitudinal folds, _i.e._ the respective needs of the
several fins.
"6. Occasionally the dorsal radials coalesced (as in _Notidanus_, &c.)
and sought centripetally (_Pristis_, &c.) adherence to the skeletal
axis.
"7. The radials of the hinder paired limb did so more constantly, and
ultimately prolonged themselves inwards by mesiad growth from their
coalesced base, till the piscine pelvic structure arose, as, _e.g._,
in _Squatina_.
"8. The pectoral radials with increasing development also coalesced
proximally, and thence prolonging themselves inwards to seek a _point
d'appui_, shot dorsad and ventrad to obtain a firm support, and at the
same time to avoid the visceral cavity. Thus they came to abut
dorsally against the axial skeleton, and to meet ventrally together in
the middle line below.
"9. The lateral fins, as they were applied to support the body on the
ground, became elongated, segmented, and narrowed, so that probably
the line of the propterygium, or possibly that of the mesopterygium,
became the cheiropterygial axis.
"10. The distal end of the incipient cheiropterygium either preserved
and enlarged preexisting cartilages or developed fresh ones to serve
fresh needs, and so grew into the developed cheiropterygium; but there
is not yet enough evidence to determine what was the precise course of
this transformation.
"11. The pelvic limb acquired a solid connection with the axial
skeleton (a pelvic girdle) through its need of a _point d'appui_ as a
locomotive organ on land.
"12. The pelvic limb became also elongated; and when its function was
quite similar to that of the pectoral limb, its structure became also
quite similar (_e.g. Ichthyosaurus_, _Plesiosaurus_, _Chelydra_, &c.);
but for the ordinary quadrupedal mode of progression it became
segmented and inflected in a way generally parallel with, but (from
its mode of use) in part inversely to, the inflections of the pectoral
limb."
Günther[486] has propounded a theory on the primitive character of the
fins, which, on the whole, fits in with the view that the paired fins are
structures of the same nature as the unpaired fins. The interest of
Günther's views on the nature of the skeleton of the fins more especially
depends upon the fact that he attempts to evolve the fin of _Ceratodus_
from the typical Selachian type of pectoral fin. His own statement on this
subject is as follows[487]:--
Footnote 486: "Description of _Ceratodus_," _Phil. Trans._
1871.
Footnote 487: _Loc. cit._ p. 534.
"On further inquiry into the more distant relations of the
_Ceratodus_-limb, we may perhaps be justified in recognizing in it a
modification of the typical form of the Selachian pectoral fin.
Leaving aside the usual treble division of the carpal cartilage
(which, indeed, is sometimes simple), we find that this shovel-like
carpal forms the base for a great number of phalanges, which are
arranged in more or less regular transverse rows (zones) and in
longitudinal rows (series). The number of phalanges of the zones and
series varies according to the species and the form of the fin; in
_Cestracion philippi_ the greater number of phalanges is found in the
proximal zones and middle series, all the phalanges decreasing in size
from the base of the fin towards the margins. In a Selachian with a
long, pointed, scythe-shaped pectoral fin, like that of _Ceratodus_,
we may, from analogy, presume that the arrangement of the cartilages
might be somewhat like that shewn in the accompanying diagram, which I
have divided into nine zones and fifteen series.
"When we now detach the outermost phalanx from each side of the first
horizontal zone, and with it the other phalanges of the same series,
when we allow the remaining phalanges of this zone to coalesce into
one piece (as, in nature, we find coalesced the carpals of _Ceratodus_
and many phalanges in Selachian fins), and when we repeat this same
process with the following zones and outer series, we arrive at an
arrangement identical with what we actually find in _Ceratodus_."
While the researches of Thacker and Mivart are strongly confirmatory of the
view at which I had arrived with reference to the nature of the paired
fins, other hypotheses as to the nature of the skeleton of the fins have
been enunciated, both before and after the publication of my memoir, which
are either directly or indirectly opposed to my view.
Huxley in his memoir on _Ceratodus_, which throws light on so many
important morphological problems, has dealt with the nature of paired
fins[488].
Footnote 488: T. H. Huxley, "On _Ceratodus Fosteri_, with some
Observations on the Classification of Fishes," _Proc. Zool.
Soc._ 1876.
He holds, in accordance with a view previously adopted by Gegenbaur, that
the limb of _Ceratodus_ "presents us with the nearest known approximation
to the fundamental form of vertebrate limb or archipterygium," and is of
opinion that in a still more archaic fish than _Ceratodus_ the skeleton of
the fin "would be made up of homologous segments, which might be termed
pteromeres, each of which would consist of a mesomere with a preaxial and a
postaxial paramere." He considers that the pectoral fins of Elasmobranchii,
more especially the fin of _Notidanus_, which he holds to be the most
primitive form of Elasmobranch fin, "results in the simplest possible
manner from the shortening of the axis of such a fin-skeleton as that of
_Ceratodus_, and the coalescence of some of its elements." Huxley does not
enter into the question of the origin of the skeleton of the pelvic fin of
Elasmobranchii.
It will be seen that Huxley's idea of the primitive structure of the
archipterygium is not easily reconcilable with the view that the paired
fins are parts of a once continuous lateral fin, in that the skeleton of
such a lateral fin, if it has existed, must necessarily have consisted of a
series of parallel rays.
Gegenbaur[489] has done more than any other living anatomist to elucidate
the nature of the fins; and his views on this subject have undergone
considerable changes in the course of his investigations. After Günther had
worked out the structure of the fin of _Ceratodus_, Gegenbaur suggested
that it constituted the most primitive _persisting_ type of fin, and has
moreover formed a theory as to the origin of the fins founded on this view,
to the effect that the fins, together with their respective girdles, are to
be derived from visceral arches with their rays.
Footnote 489: C. Gegenbaur, _Untersuchungen z. vergleich.
Anat. d. Wirbelthiere_ (Leipzig 1864-5): erstes Heft, "Carpus
u. Tarsus;" zweites Heft, "Brustflosse d. Fische." "Ueb. d.
Skelet d. Gliedmaassen d. Wirbelthiere im Allgemeinen u. d.
Hintergliedmaassen d. Selachier insbesondere," _Jenaische
Zeitschrift_, Vol. V. 1870. "Ueb. d. Archipterygium,"
_Jenaische Zeitschrift_, Vol. VII. 1873. "Zur Morphologie d.
Gliedmaassen d. Wirbelthiere," _Morphologisches Jahrbuch_, Vol. II.
1876.
His views on this subject are clearly explained in the subjoined passages
quoted from the English translation of his _Elements of Comparative
Anatomy_, pp. 473 and 477.
"The skeleton of the free appendage is attached to the extremity of
the girdle. When simplest, this is made up of cartilaginous rods
(rays), which differ in their size, segmentation, and relation to one
another. One of these rays is larger than the rest, and has a number
of other rays attached to its sides. I have given the name of
_archipterygium_ to the ground-form of the skeleton which extends from
the limb-bearing girdle into the free appendage. The primary ray is
the stem of this archipterygium, the characters of which enable us to
follow out the lines of development of the skeleton of the appendage.
Cartilaginous arches beset with the rays form the branchial skeleton.
The form of skeleton of the appendages may be compared with them; and
we are led to the conclusion that it is possible that they may have
been derived from such forms. In the branchial skeleton of the
Selachii the cartilaginous bars are beset with simple rays. In many a
median one is developed to a greater size. As the surrounding rays
become smaller, and approach the larger one, we get an intermediate
step towards that arrangement in which the larger median ray carries a
few smaller ones. This differentiation of one ray, which is thereby
raised to a higher grade, may be connected with the primitive form of
the appendicular skeleton; and as we compare the girdle with a
branchial arch, so we may compare the median ray and its secondary
investment of rays with the skeleton of the free appendage.
"All the varied forms which the skeleton of the free appendages
exhibits may be derived from a ground-form which persists in a few
cases only, and which represents the first, and consequently the
lowest, stage of the skeleton in the fin--the _archipterygium_. This
is made up of a stem which consists of jointed pieces of cartilage,
which is articulated to the shoulder-girdle and is beset on either
side with rays which are likewise jointed. In addition to the rays of
the stem there are others which are directly attached to the
limb-girdle.
"_Ceratodus_ has a fin-skeleton of this form; in it there is a stem
beset with two rows of rays. But there are no rays in the
shoulder-girdle. This biserial investment of rays on the stem of the
fin may also undergo various kinds of modifications. Among the Dipnoi,
_Protopterus_ retains the medial row of rays only, which have the form
of fine rods of cartilage; in the Selachii, on the other hand, the
lateral rays are considerably developed. The remains of the medial row
are ordinarily quite small, but they are always sufficiently distinct
to justify us in supposing that in higher forms the two sets of rays
might be better developed. Rays are still attached to the stem and are
connected with the shoulder-girdle by means of larger plates. The
joints of the rays are sometimes broken up into polygonal plates which
may further fuse with one another; concrescence of this kind may also
affect the pieces which form the base of the fin. By regarding the
free rays, which are attached to these basal pieces, as belonging to
these basal portions, we are able to divide the entire skeleton of the
fin into three segments--pro-, meso-, and metapterygium.
"The metapterygium represents the stem of the archipterygium and the
rays on it. The propterygium and the mesopterygium are evidently
derived from the rays which still remain attached to the
shoulder-girdle."
Since the publication of the memoirs of Thacker, Mivart, and myself, a
pupil of Gegenbaur's, M. v. Davidoff[490], has made a series of very
valuable observations, in part directed towards demonstrating the
incorrectness of our theoretical views, more especially Thacker's and
Mivart's view of the genesis of the skeleton of the limbs. Gegenbaur[491]
has also written a short paper in connection with Davidoff's memoir, in
support of his own as against our views.
Footnote 490: M. v. Davidoff, "Beiträge z. vergleich. Anat. d.
hinteren Gliedmaassen d. Fische, I.," _Morphol. Jahrbuch_,
Vol. V. 1879.
Footnote 491: "Zur Gliedmaassenfrage. An die Untersuchungen
von Davidoff's angeknüpfte Bemerkungen," _Morphol. Jahrbuch_,
Vol. V. 1879.
It would not be possible here to give an adequate account of Davidoff's
observations on the skeleton, muscular system, and nerves of the pelvic
fins. His main argument against the view that the paired fins are the
remains of a continuous lateral fin is based on the fact that a variable
but often considerable number of the spinal nerves in front of the pelvic
fin are united by a longitudinal commissure with the true plexus of the
nerves supplying the fin. From this he concludes that the pelvic fin has
shifted its position, and that it may once therefore have been situated
close behind the visceral arches. Granting, however, that Davidoff's
deduction from the character of the pelvic plexus is correct, there is, so
far as I see, no reason in the nature of the lateral-fin theory why the
pelvic fins should not have shifted; and, on the other hand, the
longitudinal cord connecting some of the ventral roots in front of the
pelvic fin may have another explanation. It may, for instance, be a remnant
of the time when the pelvic fin had a more elongated form than at present,
and accordingly extended further forwards.
In any case our knowledge of the nature and origin of nervous plexuses is
far too imperfect to found upon their characters such conclusions as those
of Davidoff.
Gegenbaur, in his paper above quoted, further urges against Thacker and
Mivart's views the fact that there is no proof that the fin of _Polyodon_
is a primitive type; and also suggests that the epithelial line which I
have found connecting the embryonic pelvic and pectoral fins in _Torpedo_
may be a rudiment indicating a migration backwards of the pelvic fin.
With reference to the development of the pectoral fin in the Teleostei
there are some observations of 'Swirski[492], which unfortunately do not
throw very much light upon the nature of the limb.
Footnote 492: G. 'Swirski, _Untersuch. üb. d. Entwick. d.
Schultergürtels u. d. Skelets d. Brustflosse d. Hechts._ Inaug.
Diss. Dorpat, 1880.
'Swirski finds that in the Pike the skeleton of the limb is formed of a
plate of cartilage continuous with the pectoral girdle, which soon becomes
divided into a proximal and a distal portion. The former is subsequently
segmented into five basal rays, and the latter into twelve parts, the
number of which subsequently becomes reduced.
* * * * *
The observations which I have to lay before the Society were made with the
object of determining how far the development of the skeleton of the limbs
throws light on the points on which the anatomists whose opinions have just
been quoted are at variance.
They were made, in the first instance, to complete a chapter in my work on
comparative embryology; and, partly owing to the press of other
engagements, but still more to the difficulty of procuring material, my
observations are confined to the two British species of the genus
_Scyllium_, viz. _Sc. stellare_ and _Sc. canicula_; yet I venture to
believe that the results at which I have arrived are not wholly without
interest.
Before dealing with the development of the skeleton of the fin, it will be
convenient to describe with great brevity the structure of the pectoral and
pelvic fins of the adult. The pectoral fins consist of broad plates
inserted horizontally on the sides of the body; so that in each there may
be distinguished a dorsal and a ventral surface, and an anterior and a
posterior border. Their shape may best be gathered from the woodcut
(fig. 1); and it is to be especially noted that the narrowest part of the
fin is the base, where it is attached to the side of the body. The
cartilaginous skeleton only occupies a small zone at the base of the fin,
the remainder being formed of a fringe supported by radiately arranged
horny fibres[493].
Footnote 493: The horny fibres are mesoblastic products; they
are formed, in the first instance, as extremely delicate
fibrils on the inner side of the membrane separating the
epiblast from the mesoblast.
[Illustration: FIG. 1.
Pectoral fins and girdle of an adult of _Scyllium canicula_ (natural size,
seen from behind and above).
_co._ Coracoid. _sc._ scapula. _pp._ propterygium. _mep._ mesopterygium.
_mp._ metapterygium. _fn._ part of fin supported by horny fibre.]
[Illustration: FIG. 2.
Right pelvic fin and part of pelvic girdle of an adult female of _Scyllium
canicula_ (natural size).
_il._ iliac process. _pn._ pubic process, cut across below. _bp._
basipterygium. _af._ anterior cartilaginous fin-ray articulated to pelvic
girdle. _fn._ part of fin supported by horny fibres.]
The true skeleton consists of three basal pieces articulating with the
pectoral girdle; on the outer side of which there is a series of more or
less segmented cartilaginous fin-rays. Of the basal cartilages one (_pp_)
is anterior, a second (_mep_) is placed in the middle, and a third is
posterior (_mp_). They have been named by Gegenbaur the _propterygium_, the
_mesopterygium_, and the _metapterygium_; and these names are now generally
adopted.
The metapterygium is by far the most important of the three, and in
_Scyllium canicula_ supports 12 or 13 rays[494]. It forms a large part of
the posterior boundary of the fin, and bears rays only on its _anterior_
border.
Footnote 494: In one example where the metapterygium had 13
rays the mesopterygium had only 2 rays.
The mesopterygium supports 2 or 3 rays, in the basal parts of which the
segmentation into distinct rays is imperfect; and the propterygium supports
only a single ray.
The pelvic fins are horizontally placed, like the pectoral fins, but differ
from the latter in nearly meeting each other along the median ventral line
of the body. They also differ from the pectoral fins in having a relatively
much broader base of attachment to the sides of the body. Their
cartilaginous skeleton (woodcut, fig. 2) consists of a basal bar, placed
parallel to the base of the fin, and articulated in front with the pelvic
girdle.
On its outer border it articulates with a series of cartilaginous fin-rays.
I shall call the basal bar the basipterygium. The rays which it bears are
most of them less segmented than those of the pectoral fin, being only
divided into two; and the posterior ray, which is placed in the free
posterior border of the fin, continues the axis of the basipterygium. In
the male it is modified in connection with the so-called clasper.
The anterior fin-ray of the pelvic fin, which is broader than the other
rays, articulates directly with the pelvic girdle, instead of with the
basipterygium. This ray, in the female of _Scyllium canicula_ and in the
male of _Scyllium catulus_ (Gegenbaur), is peculiar in the fact that its
distal segment is longitudinally divided into two or more pieces, instead
of being single as is the case with the remaining rays. It is probably
equivalent to two of the posterior rays.
_Development of the paired Fins._--The first rudiments of the limbs appear
in _Scyllium_, as in other fishes, as slight longitudinal ridge-like
thickenings of the epiblast, which closely resemble the first rudiments of
the unpaired fins.
These ridges are two in number on each side--an anterior immediately behind
the last visceral fold, and a posterior on the level of the cloaca. In most
Fishes they are in no way connected; but in some Elasmobranch embryos, more
especially in that of _Torpedo_, they are connected together at their first
development by a line of columnar epiblast cells. This connecting line of
columnar epiblast, however, is a very transitory structure. The rudimentary
fins soon become more prominent, consisting of a projecting ridge both of
epiblast and mesoblast, at the outer edge of which is a fold of epiblast
only, which soon reaches considerable dimensions. At a later stage the
mesoblast penetrates into this fold, and the fin becomes a simple ridge of
mesoblast covered by epiblast. The pectoral fins are at first considerably
ahead of the pelvic fins in development.
The direction of the original epithelial line which connected the two fins
of each side is nearly, though not quite, longitudinal, sloping somewhat
obliquely ventralwards. It thus comes about that the attachment of each
pair of limbs is somewhat on a slant, and that the pelvic pair nearly meet
each other in the median ventral line shortly behind the anus.
The embryonic muscle-plates, as I have elsewhere shewn, grow into the bases
of the fins; and the cells derived from these ingrowths, which are placed
on the dorsal and ventral surfaces in immediate contact with the epiblast,
probably give rise to the dorsal and ventral muscular layers of the limb,
which are shewn in section in Plate 33, fig. 1, _m_, and in Plate 33,
fig. 7, _m_.
The cartilaginous skeleton of the limbs is developed in the indifferent
mesoblast cells between the two layers of muscles. Its early development in
both the pectoral and the pelvic fins is very similar. When first visible
it differs histologically from the adjacent mesoblast simply in the fact of
its cells being more concentrated; while its boundary is not sharply
marked.
At this stage it can only be studied by means of sections. It arises
simultaneously and continuously with the pectoral and pelvic girdles, and
consists, in both fins, of a bar springing at right angles from the
posterior side of the pectoral or pelvic girdle, and running parallel to
the long axis of the body along the base of the fin. The outer side of this
bar is continued into a thin plate, which extends into the fin.
The structure of the skeleton of the fin slightly after its first
differentiation will be best understood from Plate 33, fig. 1, and Plate
33, fig. 7. These figures represent transverse sections through the pelvic
and pectoral fins of the same embryo on the same scale. The basal bar is
seen at _bp_, and the plate at this stage (which is considerably later than
the first differentiation) already partially segmented into rays at _br_.
Outside the region of the cartilaginous plate is seen the fringe with the
horny fibres (_h.f._); and dorsally and ventrally to the cartilaginous
skeleton are seen the already well-differentiated muscles (_m_).
The pectoral fin is shewn in horizontal section in Plate 33, fig. 6, at a
somewhat earlier stage than that to which the transverse sections belong.
The pectoral girdle (_p.g._) is cut transversely, and is seen to be
perfectly continuous with the basal bar (_vp_) of the fin. A similar
continuity between the basal bar of the pelvic fin and the pelvic girdle is
shewn in Plate 33, fig. 2, at a somewhat later stage. The plate continuous
with the basal bar of the fin is at first, to a considerable extent in the
pectoral, and to some extent in the pelvic fin, a continuous lamina, which
subsequently segments into rays. In the parts of the plate which eventually
form distinct rays, however, almost from the first the cells are more
concentrated than in those parts which will form the tissue between the
rays; and I am not inclined to lay any stress whatever upon the fact of the
cartilaginous fin-rays being primitively part of a continuous lamina, but
regard it as a secondary phenomenon, dependent on the mode of conversion of
embryonic mesoblast cells into cartilage. In all cases the separation into
distinct rays is to a large extent completed before the tissue of which the
plates are formed is sufficiently differentiated to be called cartilage by
an histologist.
The general position of the fins in relation to the body, and their
relative sizes, may be gathered from Plate 33, figs. 4 and 5, which
represent transverse sections of the same embryo as that from which the
transverse sections shewing the fin on a larger scale were taken.
During the first stage of its development the skeleton of both fins may
thus be described as consisting of _a longitudinal bar running along the
base of the fin, and giving off at right angles series of rays which pass
into the fin_. The longitudinal bar may be called the basipterygium; and it
is continuous in front with the pectoral or pelvic girdle, as the case may
be.
The further development of the primitive skeleton is different in the case
of the two fins.
_The Pelvic Fin._--The changes in the pelvic fin are comparatively slight.
Plate 33, fig. 2, is a representation of the fin and its skeleton in a
female of _Scyllium stellare_ shortly after the primitive tissue is
converted into cartilage, but while it is still so soft as to require the
very greatest care in dissection. The fin itself forms a simple projection
of the side of the body. The skeleton consists of a basipterygium (_bp_),
continuous in front with the pelvic girdle. To the outer side of the
basipterygium a series of cartilaginous fin-rays are attached--the
posterior ray forming a direct prolongation of the basipterygium, while the
anterior ray is united rather with the pelvic girdle than with the
basipterygium. All the cartilaginous fin-rays except the first are
completely continuous with the basipterygium, their structure in section
being hardly different from that shewn in Plate 33, fig. 1.
The external form of the fin does not change very greatly in the course of
the further development; but the hinder part of the attached border is, to
some extent, separated off from the wall of the body, and becomes the
posterior border of the adult fin. With the exception of a certain amount
of segmentation in the rays, the character of the skeleton remains almost
as in the embryo. The changes which take place are illustrated by Plate 33,
fig. 3, shewing the fin of a young male of _Scyllium stellare_. The
basipterygium has become somewhat thicker, but is still continuous in front
with the pelvic girdle, and otherwise retains its earlier characters. The
cartilaginous fin-rays have now become segmented off from it and from the
pelvic girdle, the posterior end of the basipterygial bar being segmented
off as the terminal ray.
The anterior ray is directly articulated with the pelvic girdle, and the
remaining rays continue articulated with the basipterygium. Some of the
latter are partially segmented.
As may be gathered by comparing the figure of the fin at the stage just
described with that of the adult fin (woodcut, fig. 2), the remaining
changes are very slight. The most important is the segmentation of the
basipterygial bar from the pelvic girdle.
The pelvic fin thus retains in all essential points its primitive
structure.
_The Pectoral Fin._--The earliest stage of the pectoral fin differs, as I
have shewn, from that of the pelvic fin only in minor points (Pl. 33,
fig. 6). There is the same longitudinal or basipterygial bar (_bp_), to
which the fin-rays are attached, which is continuous in front with the
pectoral girdle (_pg_). The changes which take place in the course of the
further development, however, are very much more considerable in the case
of the pectoral than in that of the pelvic fin.
The most important change in the external form of the fin is caused by a
reduction in the length of its attachment to the body. At first (Pl. 33,
fig. 6), the base of the fin is as long as the greatest breadth of the fin;
but it gradually becomes shortened by being constricted off from the body
at its hinder end. In connection with this process the posterior end of the
basipterygial bar is gradually rotated outwards, its anterior end remaining
attached to the pectoral girdle. In this way this bar comes to form the
posterior border of the skeleton of the fin (Pl. 33, figs. 8 and 9),
constituting the metapterygium (_mp_). It becomes eventually segmented off
from the pectoral girdle, simply articulating with its hinder edge.
The plate of cartilage, which is continued outwards from the basipterygium,
or, as we may now call it, the metapterygium, into the fin, is not nearly
so completely divided up into fin-rays as the homologous part of the pelvic
fin; and this is especially the case with the basal part of the plate. This
basal part becomes, in fact, at first only divided into two parts (Pl. 33,
fig. 8)--a small anterior part at the front end (_me.p_), and a larger
posterior along the base of the metapterygium (_mp_); and these two parts
are not completely segmented from each other. The anterior part directly
joins the pectoral girdle at its base, resembling in this respect the
anterior fin-ray of the pelvic girdle. It constitutes the (at this stage
undivided) rudiment of the mesopterygium and propterygium of Gegenbaur. It
bears in my specimen of this age four fin-rays at its extremity, the
anterior not being well marked. The remaining fin-rays are prolongations
outwards of the edge of the plate continuous with the metapterygium. These
rays are at the stage figured more or less transversely segmented; but at
their outer edge they are united together by a nearly continuous rim of
cartilage. The spaces between the fin-rays are relatively considerably
larger than in the adult.
The further changes in the cartilages of the pectoral limb are,
morphologically speaking, not important, and are easily understood by
reference to Pl. 33, fig. 9 (representing the skeleton of the limb of a
nearly ripe embryo). The front end of the anterior basal cartilage becomes
segmented off as a propterygium (_pp_), bearing a single fin-ray, leaving
the remainder of the cartilage as a mesopterygium (_mes_). The remainder of
the now considerably segmented fin-rays are borne by the metapterygium.
* * * * *
_General Conclusions._--From the above observations, conclusions of a
positive kind may be drawn as to the primitive structure of the skeleton;
and the observations have also, it appears to me, important bearings on the
theories of my predecessors in this line of investigation.
The most obvious of the positive conclusions is to the effect that the
embryonic skeleton of the paired fins consists of a series of parallel rays
similar to those of the unpaired fins. These rays support the soft parts of
the fins, which have the form of a longitudinal ridge; and they are
continuous at their base with a longitudinal bar. This bar, from its
position at the base of the fin, can clearly never have been a median axis
with the rays on both sides. It becomes the basipterygium in the pelvic
fin, which retains its embryonic structure much more completely than the
pectoral fin; and the metapterygium in the pectoral fin. The metapterygium
of the pectoral fin is thus clearly homologous with the basipterygium of
the pelvic fin, as originally supposed by Gegenbaur, and as has since been
maintained by Mivart. The propterygium and mesopterygium are obviously
relatively _unimportant_ parts of the skeleton as compared with the
metapterygium.
My observations on the development of the skeleton of the fins certainly do
not of themselves demonstrate that the paired fins are remnants of a once
continuous lateral fin; but they support this view in that they shew the
primitive skeleton of the fins to have exactly the character which might
have been anticipated if the paired fins had originated from a continuous
lateral fin. The longitudinal bar of the paired fins is believed by both
Thacker and Mivart to be due to the coalescence of the bases of the
primitively independent rays of which they believe the fin to have been
originally composed. This view is probable enough in itself, and is
rendered more so by the fact, pointed out by Mivart, that a longitudinal
bar supporting the cartilaginous rays of unpaired fins is occasionally
formed; but there is no trace in the embryo Scylliums of the bar in
question being formed by the coalescence of rays, though the fact of its
being perfectly continuous with the bases of the fin-rays is somewhat in
favour of such coalescence.
Thacker and Mivart both hold that the pectoral and pelvic girdles are
developed by ventral and dorsal growths of the anterior end of the
longitudinal bar supporting the fin-rays.
There is, so far as I see, no theoretical objection to be taken to this
view; and the fact of the pectoral and pelvic girdles originating
continuously and long remaining united with the longitudinal bars of their
respective fins is in favour of it rather than the reverse. The same may be
said of the fact that the first part of each girdle to be formed is that in
the neighbourhood of the longitudinal bar (basipterygium) of the fin, the
dorsal and ventral prolongations being subsequent growths.
On the whole my observations do not throw much light on the theories of
Thacker and Mivart as to the genesis of the skeleton of the paired fin;
but, so far as they bear on the subject, they are distinctly favourable to
those theories.
The main results of my observations appear to me to be decidedly adverse to
the views recently put forward on the structure of the fin by Gegenbaur and
Huxley, both of whom, as stated above, consider the primitive type of fin
to be most nearly retained in _Ceratodus_, and to consist of a central
multisegmented axis with numerous lateral rays.
Gegenbaur derives the Elasmobranch pectoral fin from a form which he calls
the archipterygium, nearly like that of _Ceratodus_, with a median axis and
two rows of rays--but holds that in addition to the rays attached to the
median axis, which are alone found in _Ceratodus_, there were other rays
directly articulated to the shoulder-girdle. He considers that in the
Elasmobranch fin the majority of the lateral rays on the posterior (or
median according to his view of the position of the limb) side have become
aborted, and that the central axis is represented by the metapterygium;
while the pro- and mesopterygium and their rays are, he believes, derived
from those rays of the archipterygium which originally articulated directly
with the shoulder-girdle.
This view appears to me to be absolutely negatived by the facts of
development of the pectoral fin in _Scyllium_--not so much because the
pectoral fin in this form is necessarily to be regarded as primitive, but
because what Gegenbaur holds to be the primitive axis of the biserial fin
is demonstrated to be really the base, and it is only in the adult that it
is conceivable that a second set of lateral rays could have existed on the
posterior side of the metapterygium. If Gegenbaur's view were correct, we
should expect to find in the embryo, if anywhere, traces of the second set
of lateral rays; but the fact is that, as may easily be seen by an
inspection of figs. 6 and 7, such a second set of lateral rays could not
possibly have existed in a type of fin like that found in the embryo. With
this view of Gegenbaur's it appears to me that the theory held by this
anatomist to the effect that the limbs are modified gill-arches also falls,
in that his method of deriving the limbs from gill-arches ceases to be
admissible, while it is not easy to see how a limb, formed on the type of
the embryonic limb of Elasmobranchii, could be derived from a gill-arch
with its branchial rays.
Gegenbaur's older view, that the Elasmobranch fin retains a primitive
uniserial type, appears to me to be nearer the truth than his more recent
view on this subject; though I hold the fundamental point established by
the development of these parts in _Scyllium_ to be that the posterior
border of the adult Elasmobranch pectoral fin is the primitive
base-line,_i.e._line of attachment of the fin to the side of the body.
Huxley holds that the mesopterygium is the proximal piece of the axial
skeleton of the limb of _Ceratodus_, and derives the Elasmobranch fin from
that of _Ceratodus_ by the shortening of its axis and the coalescence of
some of its elements. The entirely secondary character of the
mesopterygium, and its total absence in the young embryo _Scyllium_, appear
to me as conclusive against Huxley's view as the character of the embryonic
fin is against that of Gegenbaur; and I should be much more inclined to
hold that the fin of _Ceratodus_ has been derived from a fin like that of
the Elasmobranchii by a series of steps similar to those which Huxley
supposes to have led to the establishment of the Elasmobranch fin, but in
exactly the reverse order.
There is one statement of Davidoff's which I cannot allow to pass without
challenge. In comparing the skeletons of the paired and unpaired fins he is
anxious to prove that the former are independent of the axial skeleton in
their origin and that the latter have been segmented from the axial
skeleton, and thus to shew that an homology between the two is impossible.
In support of his view he states[495] that he has satisfied himself, from
embryos of _Acanthias_ and _Scyllium_, that the rays of the unpaired fins
_are undoubtedly products of the segmentation of the dorsal and ventral
spinous processes_.
Footnote 495: _Loc. cit._ p. 514.
This statement is wholly unintelligible to me. From my examination of the
development of the first dorsal and the anal fins of _Scyllium_ I find that
their rays develop at a considerable distance from, and quite independently
of, the neural and hæmal arches, and that they are at an early stage of
development distinctly in a more advanced state of histological
differentiation than the neural and hæmal arches of the same region. I have
also found exactly the same in the embryos of _Lepidosteus_.
I have, in fact, no doubt that the skeleton of both the paired and the
unpaired fins of Elasmobranchii and _Lepidosteus_ is in its development
independent of the axial skeleton. The phylogenetic mode of origin of the
skeleton both of the paired and of the unpaired fins cannot, however, be
made out without further investigation.
EXPLANATION OF PLATE 33.[496]
Footnote 496: I employ here the same letters to indicate the
stages as in my "Monograph on Elasmobranch Fishes."
Fig. 1. Transverse section through the pelvic fin of an embryo of
_Scyllium_ belonging to stage P{1}, magnified 50 diameters. _bp._
basipterygium. _br._ fin ray. _m._ muscle. _hf._ horny fibres supporting
the peripheral part of the fin.
Fig. 2. Pelvic fin of a very young female embryo of _Scyllium stellare_,
magnified 16 diameters. _bp._ basipterygium. _pu._ pubic process of pelvic
girdle (cut across below). _il._ iliac process of pelvic girdle. _fo._
foramen.
Fig. 3. Pelvic fin of a young male embryo of _Scyllium stellare_, magnified
16 diameters. _bp._ basipterygium. _mo._ process of basipterygium continued
into clasper. _il._ iliac process of pelvic girdle. _pu._ pubic section of
pelvic girdle.
Fig. 4. Transverse section through the ventral part of the trunk of an
embryo _Scyllium_ of stage P, in the region of the pectoral fins, to shew
how the fins are attached to the body, magnified 18 diameters. _br._
cartilaginous fin-ray. _bp._ basipterygium. _m._ muscle of fin. _mp._
muscle-plate.
Fig. 5. Transverse section through the ventral part of the trunk of an
embryo _Scyllium_ of stage P, in the region of the pelvic fin, on the same
scale as fig. 4. _bp._ basipterygium. _br._ cartilaginous fin-rays. _m._
muscle of the fins. _mp._ muscle-plate.
Fig. 6. Pectoral fin of an embryo of _Scyllium canicula_, of a stage
between O and P, in longitudinal and horizontal section (the skeleton of
the fin was still in the condition of embryonic cartilage), magnified 36
diameters. _bp._ basipterygium (eventual metapterygium). _fr._
cartilaginous fin-rays. _pg._ pectoral girdle in transverse section. _fo._
foramen in pectoral girdle. _pe._ epithelium of peritoneal cavity.
Fig. 7. Transverse section through the pectoral fin of a _Scyllium_ embryo
of stage P, magnified 50 diameters. _bp._ basipterygium. _br._
cartilaginous fin-ray. _m._ muscle. _hf._ horny fibres.
Fig. 8. Pectoral fin of an embryo of _Scyllium stellare_, magnified 16
diameters. _mp._ metapterygium (basipterygium of earlier stage). _me.p._
rudiment of future pro- and mesopterygium. _sc._ cut surface of a scapular
process. _cr._ coracoid process. _fr._ foramen. _hf._ horny fibres.
Fig. 9. Skeleton of the pectoral fin and part of pectoral girdle of a
nearly ripe embryo of _Scyllium stellare_, magnified 10 diameters. _mp._
metapterygium. _mes._ mesopterygium. _pp._ propterygium. _cr._ coracoid
process.
XXI. ON THE EVOLUTION OF THE PLACENTA, AND ON THE POSSIBILITY OF EMPLOYING
THE CHARACTERS OF THE PLACENTA IN THE CLASSIFICATION OF THE MAMMALIA[497].
Footnote 497: From the _Proceedings of the Zoological Society
of London_, 1881.
From Owen's observations on the Marsupials it is clear that the yolk-sack
in this group plays an important (if not the most important) part, in
absorbing the maternal nutriment destined for the foetus. The fact that in
Marsupials both the yolk-sack and the allantois are concerned in rendering
the chorion vascular, makes it _à priori_ probable that this was also the
case in the primitive types of the Placentalia; and this deduction is
supported by the fact that in the Rodentia, Insectivora, and Cheiroptera
this peculiarity of the foetal membranes is actually found. In the
primitive Placentalia it is also probable that from the discoidal allantoic
region of the chorion simple foetal villi, like those of the Pig, projected
into uterine crypts; but it is not certain how far the umbilical region of
the chorion, which was no doubt vascular, may also have been villous. From
such a primitive type of foetal membranes divergencies in various
directions have given rise to the types of foetal membranes found at the
present day.
In a general way it may be laid down that variations in any direction which
tended to increase the absorbing capacities of the chorion would be
advantageous. There are two obvious ways in which this might be done, viz.
(1) by increasing the complexity of the foetal villi and maternal crypts
over a limited area, (2) by increasing the area of the part of the chorion
covered by the placental villi. Various combinations of the two processes
would also, of course, be advantageous.
The most fundamental change which has taken place in all the existing
Placentalia is the exclusion of the umbilical vesicle from any important
function in the nutrition of the foetus.
The arrangement of the foetal parts in the Rodentia, Insectivora, and
Cheiroptera may be directly derived from the primitive form by supposing
the villi of the discoidal placental area to have become more complex, so
as to form a deciduate discoidal placenta, while the yolk-sack still plays
a part, though physiologically an unimportant part, in rendering the
chorion vascular.
In the Carnivora, again, we have to start from the discoidal placenta, as
evinced by the fact that in the growth of the placenta the allantoic region
of the placenta is at first _discoidal_, and only becomes zonary at a later
stage. A zonary deciduate placenta indicates an increase both in area and
in complexity. The relative diminution of the breadth of the placental zone
in late foetal life in the zonary placenta of the Carnivora is probably due
to its being on the whole advantageous to secure the nutrition of the
foetus by insuring a more intimate relation between the foetal and maternal
parts, than by increasing their area of contact. The reason of this is not
obvious, but, as shewn below, there are other cases where it is clear that
a diminution in the area of the placenta has taken place, accompanied by an
increase in the complexity of its villi.
The second type of differentiation from the primitive form of placenta is
illustrated by the Lemuridæ, the Suidæ, and _Manis_. In all these cases the
area of the placental villi appears to have increased so as to cover nearly
the whole subzonal membrane, without the villi increasing to any great
extent in complexity. From the diffused placenta covering the whole surface
of the chorion, differentiations appear to have taken place in various
directions. The placenta of Man and Apes, from its mode of ontogeny, is
clearly derived from a diffused placenta (very probably similar to that of
Lemurs) by a concentration of the foetal villi, which are originally spread
over the whole chorion, to a disk-shaped area, and by an increase in their
arborescence. Thus the discoidal placenta of Man has no connexion with, and
ought not to be placed in, the same class as those of the Rodentia,
Cheiroptera, and Insectivora.
The polycotyledonary forms of placenta are due to similar concentrations of
the foetal villi of an originally diffused placenta.
In the Edentata we have a group with very varying types of placenta. Very
probably these may all be differentiations within the group itself from a
diffused placenta such as that found in _Manis_. The zonary placenta of
_Orycteropus_ is capable of being easily derived from that of _Manis_ by
the disappearance of the foetal villi at the two poles of the ovum. The
small size of the umbilical vesicle in _Orycteropus_ indicates that its
discoidal placenta is not, like that of the Carnivora, directly derived
from a type with both allantoic and umbilical vascularization of the
chorion. The discoidal and dome-shaped placentæ of the Armadillos,
_Myrmecophaga_, and the Sloths may easily have been formed from a diffused
placenta, just as the discoidal placenta of the Simiidæ and Hominidæ
appears to have been formed from a diffused placenta like that of the
Lemuridæ.
The presence of zonary placenta in _Hyrax_ and _Elephas_ does not
necessarily afford any proof of affinity of these types with the Carnivora.
A zonary placenta may be quite as easily derived from a diffused placenta
as from a discoidal placenta; and the presence of two villous patches at
the poles of the chorion in _Elephas_ very probably indicates that its
placenta has been evolved from a diffused placenta.
Although it would not be wise to attempt to found a classification upon the
placental characters alone, it may be worth while to make a few suggestions
as to the affinities of the orders of Mammalia indicated by the structure
of the placenta. We clearly, of course, have to start with forms which
could not be grouped with any of the existing orders, but which might be
called the Protoplacentalia. They probably had the primitive type of
placenta described above: the nearest living representatives of the group
are the Rodentia, Insectivora, and Cheiroptera. Before, however, these
three groups had become distinctly differentiated, there must have branched
off from the primitive stock the ancestors of the Lemuridæ, the Ungulata,
and the Edentata.
It is obvious on general anatomical grounds that the Monkeys and Man are to
be derived from a primitive Lemurian type; and with this conclusion the
form of the placenta completely tallies. The primitive Edentata and
Ungulata had no doubt a diffused placenta which was probably not very
different from that of the primitive Lemurs; but how far these groups arose
quite independently from the primitive stock, or whether they may have had
a nearer common ancestor, cannot be decided from the structure of the
placenta. The Carnivora were certainly an offshoot from the primitive
placental type which was quite independent of the three groups just
mentioned; but the character of the placenta of the Carnivora does not
indicate at what stage in the evolution of the placental Mammalia a
primitive type of Carnivora was first differentiated.
No important light is thrown by the placenta on the affinities of the
Proboscidea, the Cetacea, or the Sirenia; but the character of the placenta
in the latter group favours the view of their being related to the
Ungulata.
XXII. ON THE STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS[498].
By F. M. BALFOUR and W. N. PARKER.
Footnote 498: From the _Philosophical Transactions of the
Royal Society_, 1882.
(With Plates 34-42.)
TABLE OF CONTENTS.
PAGE
INTRODUCTION 739
GENERAL DEVELOPMENT 740
BRAIN--
Adult brain 759
Development of the brain 764
Comparison of the larval and adult brain of
_Lepidosteus_, together with some observations on
the systematic value of the characters of the
Ganoid brain 767
SENSE ORGANS--
Olfactory organ 771
Anatomy of the eye _ib._
Development of the eye 772
SUCTORIAL DISC 774
MUSCULAR SYSTEM 775
SKELETON--
Vertebral column and ribs of the adult 776
Development of the vertebral column and ribs. 778
Comparison of the vertebral column of _Lepidosteus_
with that of other forms 792
The ribs of Fishes 793
The skeleton of the ventral lobe of the tail fin, and
its bearing on the nature of the tail fin of the
various types of Pisces 801
EXCRETORY AND GENERATIVE ORGANS--
Anatomy of the excretory and generative organs of the
female 810
Anatomy of the excretory and generative organs of the
male 813
Development of the excretory and generative organs 815
Theoretical considerations 822
THE ALIMENTARY CANAL AND ITS APPENDAGES--
Topographical anatomy of the alimentary canal 828
Development of the alimentary canal and its appendages 831
THE GILL ON THE HYOID ARCH 835
THE SYSTEMATIC POSITION OF LEPIDOSTEUS 836
LIST OF MEMOIRS ON THE ANATOMY AND DEVELOPMENT OF
LEPIDOSTEUS 840
LIST OF REFERENCE LETTERS 841
EXPLANATION OF PLATES 842
INTRODUCTION.
The following paper is the outcome of the very valuable gift of a series of
embryos and larvæ of _Lepidosteus_ by Professor Alex. Agassiz, to whom we
take this opportunity of expressing our most sincere thanks. The skull of
these embryos and larvæ has been studied by Professor Parker, and forms the
subject of a memoir already presented to the Royal Society.
Considering that _Lepidosteus_ is one of the most interesting of existing
Ganoids, and that it is very closely related to species of Ganoids which
flourished during the Triassic period, we naturally felt keenly anxious to
make the most of the opportunity of working at its development offered to
us by Professor Agassiz' gift. Professor Agassiz, moreover, most kindly
furnished us with four examples of the adult Fish, which have enabled us to
make this paper a study of the adult anatomy as well as of the development.
The first part of our paper is devoted to the segmentation, formation of
the germinal layers, and general development of the embryo and larva. The
next part consists of a series of sections on the organs, in which both
their structure in the adult and their development are dealt with. This
part is not, however, in any sense a monograph, and where already known,
the anatomy is described with the greatest possible brevity. In this part
of the paper considerable space is devoted to a comparison of the organs of
_Lepidosteus_ with those of other Fishes, and to a statement of the
conclusions which follow from such comparison.
The last part of the paper deals with the systematic position of
_Lepidosteus_ and of the Ganoids generally.
GENERAL DEVELOPMENT.
The spawning of _Lepidosteus_ takes place in the neighbourhood of New York
about May 20th. Agassiz (No. 1)[499] gives an account of the process from
Mr S. W. Garman's notes, which we venture to quote in full.
Footnote 499: The numbers refer to the list of memoirs of the
anatomy and development given at the end of this memoir.
"Black Lake is well stocked with Bill-fish. When they appear, they are
said to come in countless numbers. This is only for a few days in the
spring, in the spawning season, between the 15th of May and the 8th of
June. During the balance of the season they are seldom seen. They
remain in the deeper parts of the lake, away from the shore, and,
probably, are more or less nocturnal in habits. Out of season, an
occasional one is caught on a hook baited with a minnow. Commencing
with the 20th of April, until the 14th of May we were unable to find
the Fish, or to find persons who had seen them during this time. Then
a fisherman reported having seen one rise to the surface. Later,
others were seen. On the afternoon of the 18th, a few were found on
the _points_, depositing the spawn. The temperature at the time was
68° to 69° on the shoals, while out in the lake the mercury stood at
62° to 63°. The _points_ on which the eggs were laid were of naked
granite, which had been broken by the frost and heat into angular
blocks of 3 to 8 inches in diameter. The blocks were tumbled upon each
other like loose heaps of brick-bats, and upon and between them the
eggs were dropped. The _points_ are the extremities of small capes
that make out into the lake. The eggs were laid in water varying in
depth from 2 to 14 inches. At the time of approaching the shoals, the
Fish might be seen to rise quite often to the surface to take air.
This they did by thrusting the bill out of the water as far as the
corners of the mouth, which was then opened widely and closed with a
snap. After taking the air, they seemed more able to remain at the
surface. Out in the lake they are very timid, but once buried upon the
shoals they become quite reckless as to what is going on about them. A
few moments after being driven off, one or more of the males would
return as if scouting. If frightened, he would retire for some time;
then another scout would appear. If all promised well, the females,
with the attendant males, would come back. Each female was accompanied
by from one to four males. Most often, a male rested against each
side, with their bills reaching up toward the back of her head.
Closely crowded together, the little party would pass back and forth
over the rocky bed they had selected, sometimes passing the same spot
half-a-dozen times without dropping an egg, then suddenly would
indulge in an orgasm; and, lashing and plashing the water in all
directions with their convulsive movements, would scatter at the same
instant the eggs and the sperm. This ended, another season of moving
slowly back and forth was observed, to be in turn followed by another
of excitement. The eggs were excessively sticky. To whatever they
happened to touch, they stuck, and so tenaciously that it was next to
impossible to release them without tearing away a portion of their
envelopes. It is doubtful whether the eggs would hatch if removed. As
far as could be seen at the time, upon or under the rocks to which the
eggs were fastened there was an utter absence of anything that might
serve as food for the young Fishes.
"Other Fishes, Bull-heads, &c., are said to follow the Bill-fish to
eat the spawn. It may be so. It was not verified. Certainly the points
under observations were unmolested. During the afternoon of the 18th
of May a few eggs were scattered on several of the beds. On the 19th
there were more. With the spear and the snare, several dozens of both
sexes of the Fish were taken. Taking one out did not seem greatly to
startle the others. They returned very soon. The males are much
smaller than the average size of the females; and, judging from those
taken, would seem to have as adults greater uniformity in size. The
largest taken was a female, of 4 feet 1-1/2 inch in length. Others of
2 feet 6 inches contained ripe ova. With the 19th of May all
disappeared, and for a time--the weather being meanwhile cold and
stormy--there were no signs of their continued existence to be met
with. Nearly two weeks later, on the 31st of May, as stated by Mr
Henry J. Perry, they again came up, not in small detachments on
scattered points as before, but in multitudes, on every shoal at all
according with their ideas of spawning beds. They remained but two
days. During the summer it happens now and then that one is seen to
come up for his mouthful of air; beyond this there will be nothing to
suggest the ravenous masses hidden by the darkness of the waters."
_Egg membranes._--The ova of _Lepidosteus_ are spherical bodies of about 3
millims. in diameter. They have a double investment consisting of (1) an
outer covering formed of elongated, highly refractive bodies, somewhat
pyriform at their outer ends (Plate 34, fig. 17, _f.e._), which are
probably metamorphosed follicular cells[500], and (2) of an inner membrane,
divided into two zones, viz.: an outer and thicker zone, which is radially
striated, and constitutes the _zona radiata (z.r.)_, and an inner and
narrow homogeneous zone (_z.r´._).
Footnote 500: We have examined the structure of the ovarian
ova in order to throw light on the nature of these peculiar
pyriform bodies. Unfortunately, the ovaries of our adult
examples of _Lepidosteus_ were so badly preserved, that we
could not ascertain anything on this subject. The ripe ova in
the ovary have an investment of pyriform bodies similar to
those of the just laid ova. With reference to the structure of
the ovarian ova we may state that the germinal vesicles are
provided with numerous nucleoli arranged in close proximity
with the membrane of the vesicle.
_Segmentation._--We have observed several stages in the segmentation, which
shew that it is complete, but that it approaches the meroblastic type more
nearly than in the case of any other known holoblastic ovum.
Our earliest stage shewed a vertical furrow at the upper or animal pole,
extending through about one-fifth of the circumference (Plate 34, fig. 1),
and in a slightly later stage we found a second similar furrow at right
angles to the first (Plate 34, fig. 2). We have not been fortunate enough
to observe the next phases of the segmentation, but on the second day after
impregnation (Plate 34, fig. 3), the animal pole is completely divided into
small segments, which form a disc, homologous to the blastoderm of
meroblastic ova; while the vegetative pole, which subsequently forms a
large yolk-sack, is divided by a few vertical furrows, four of which nearly
meet at the pole opposite the blastoderm (Plate 34, fig. 4). The majority
of the vertical furrows extend only a short way from the edge of the small
spheres, and are partially intercepted by imperfect equatorial furrows.
_Development of the embryo._--We have not been able to work out the stages
immediately following the segmentation, owing to want of material; and in
the next stage satisfactorily observed, on the third day after
impregnation, the body of the embryo is distinctly differentiated. The
lower pole of the ovum is then formed of a mass in which no traces of the
previous segments or segmentation furrows could any longer be detected.
Some of the dates of the specimens sent to us appear to have been
transposed; so that our statements as to ages must only be taken as
_approximately_ correct.
_Third day after impregnation._--In this stage the embryo is about 3.5
millims. in length, and has a somewhat dumb-bell shaped outline (Plate 34,
fig. 5). It consists of (1) an outer area (_p.z_) with some resemblance to
the area pellucida of the Avian embryo, forming the parietal part of the
body; and (2) a central portion consisting of the vertebral and medullary
plates and the axial portions of the embryo. In hardened specimens the
peripheral part forms a shallow depression surrounding the central part of
the embryo.
The central part constitutes a somewhat prominent ridge, the axial part of
it being the medullary plate. Along the anterior half of this part a dark
line could be observed in all our specimens, which we at first imagined to
be caused by a shallow groove. We have, however, failed to find in our
sections a groove in this situation except in a single instance (Plate 35,
fig. 20, _x_), and are inclined to attribute the appearance above-mentioned
to the presence of somewhat irregular ridges of the outer layer of the
epiblast, which have probably been artificially produced in the process of
hardening.
The anterior end of the central part is slightly dilated to form the brain
(_b_); and there is present a pair of lateral swellings near the anterior
end of the brain which we believe to be the commencing optic vesicles. We
could not trace any other clear indications of the differentiation of the
brain into distinct lobes.
At the hinder end of the central part of the embryo a very distinct
dilatation may also be observed, which is probably homologous with the tail
swelling of Teleostei. Its structure is more particularly dealt with in the
description of our sections of this stage.
After the removal of the egg-membranes described above we find that there
remains a delicate membrane closely attached, to the epiblast. This
membrane can be isolated in distinct portions, and appears to be too
definite to be regarded as an artificial product.
We have been able to prepare several more or less complete series of
sections of embryos of this stage (Plate 35, figs. 18-22). These sections
present as a whole a most striking resemblance to those of Teleostean
embryos at a corresponding stage of development.
Three germinal layers are already fully established. The epiblast (_ep._)
is formed of the same parts as in Teleostei, viz.:--of an outer epidermic
and an inner nervous or mucous stratum. In the parietal region of the
embryo these strata are each formed of a single row of cells only. The
cells of both strata are somewhat flattened, but those of the epidermic
stratum are decidedly the more flattened of the two.
Along the axial line there is placed, as we have stated above, the
medullary plate. The epidermic stratum passes over this plate without
undergoing any change of character, and the plate is _entirely constituted
of the nervous stratum of the epidermis_.
The medullary plate has, roughly speaking, the form of a solid keel,
projecting inwards towards the yolk. There is no trace, at this stage at
any rate, of a medullary groove; and as, we shall afterwards shew, the
central canal of the cerebro-spinal cord is formed in the middle of the
solid keel. The shape of this keel varies according to the region of the
body. In the head (Plate 35, fig. 18, _m.c._), it is very prominent, and
forming, as it does, the major part of the axial tissue of the body,
impresses its own shape on the other parts of the head and gives rise to a
marked ridge on the surface of the head directed towards the yolk. In the
trunk (Plate 35, figs. 19, 20) the keel is much less prominent, but still
projects sufficiently to give a convex form to the surface of the body
turned towards the yolk.
In the head, and also near the hind end of the trunk, the nervous layer of
the epiblast continuous with the keel on each side is considerably thicker
than the lateral parts of the layer. The thickening of the nervous layer in
the head gives rise to what has been called by Götte[501] "the special
sense plate," owing to its being subsequently concerned in the formation of
parts of the organs of special sense. We cannot agree with Götte in
regarding it as part of the brain.
Footnote 501: "Ueb. d. Entwick. d. Central Nerven Systems d.
Teleostier," _Archiv für mikr. Anat._ Vol. XV. 1878.
In the keel itself two parts may be distinguished, viz.: a superficial
part, best marked in the region of the brain, formed of more or less
irregularly arranged polygonal cells, and a deeper part of horizontally
placed flatter cells. The upper part is mainly concerned in the formation
of the cranial nerves, and of the dorsal roots of the spinal nerves.
The mesoblast (_ms._) in the trunk consists of a pair of independent plates
which are continued forwards into the head, and in the prechordal region of
the latter, unite below the medullary keel.
The mesoblastic plates of the trunk are imperfectly divided into vertebral
and lateral regions. Neither longitudinal sections nor surface views shew
at this stage any trace of a division of the mesoblast into somites. The
mesoblast cells are polygonal, and no indication is as yet present of a
division into splanchnic and somatic layers.
The notochord (_nc._) is well established, so that its origin could not be
made out. It is, however, much more sharply separated from the mesoblastic
plates than from the hypoblast, though the ventral and inner corners of the
mesoblastic plates which run in underneath it on either side, are often
imperfectly separated from it. It is formed of polygonal cells, of which
between 40 and 50 may as a rule be seen in a single section. No sheath is
present around it. It has the usual extension in front.
The hypoblast (_hy._) has the form of a membrane, composed of a single row
of oval cells, bounding the embryo on the side adjoining the yolk.
In the region of the caudal swelling the relations of the germinal layers
undergo some changes. This region may, from the analogy of other
Vertebrates, be assumed to constitute the lip of the blastopore. We find
accordingly that the layers become more or less fused. In the anterior part
of the tail swelling, the boundary between the notochord and hypoblast
becomes indistinct. A short way behind this point (Plate 35, fig. 21), the
notochord unites with the medullary keel, and a neurenteric cord,
homologous with the neurenteric canal of other Ichthyopsida, is thus
established. In the same region the boundary between the lateral plates of
mesoblast and the notochord, and further back (Plate 35, fig. 22), that
between the mesoblast and the medullary keel, becomes obliterated.
_Fifth day after impregnation._--Between the stage last described and the
next stage of which we have specimens, a considerable progress has been
made. The embryo (Plate 34, figs. 6 and 7) has grown markedly in length and
embraces more than half the circumference of the ovum. Its general
appearance is, however, much the same as in the earlier stage, but in the
cephalic region the medullary plate is divided by constrictions into three
distinct lobes, constituting the regions of the fore-brain, the mid-brain,
and the hind-brain. The fore-brain (Plate 34, fig. 6, _f.b._) is
considerably the largest of the three lobes, and a pair of lateral
projections forming the optic vesicles are decidedly more conspicuous than
in the previous stage. The mid-brain (_m.b._) is the smallest of the three
lobes, while the hind-brain (_h.b._) is decidedly longer, and passes
insensibly into the spinal cord behind.
The medullary keel, though retaining to a great extent the shape it had in
the last stage, is no longer completely solid. Throughout the whole region
of the brain and in the anterior part of the trunk (Plate 35, figs. 23, 24,
25) a slit-like lumen has become formed. We are inclined to hold that this
is due to the appearance of a space between the cells, and not, as supposed
by Oellacher for Teleostei, to an actual absorption of cells, though we
must admit that our sections are hardly sufficiently well preserved to be
conclusive in settling this point. Various stages in its growth may be
observed in different regions of the cerebro-spinal cord. When first
formed, it is a very imperfectly defined cavity, and a few cells may be
seen passing right across from one side of it to the other. It gradually
becomes more definite, and its wall then acquires a regular outline.
The optic vesicles are now to be seen in section (Plate 35, fig. 23, _op._)
as flattish outgrowths of the wall of the fore-brain, into which the lumen
of the third ventricle is prolonged for a short distance.
The brain has become to some extent separate from the superjacent epiblast,
but the exact mode in which this is effected is not clear to us. In some
sections it appears that the separation takes place in such a way that the
nervous keel is only covered above by the epidermic layer of the epiblast,
and that the nervous layer, subsequently interposed between the two, grows
in from the two sides. Such a section is represented in Plate 35, fig. 24.
Other sections again favour the view that in the isolation of the nervous
keel, a superficial layer of it remains attached to the nervous layer of
the epidermis at the two sides, and so, from the first, forms a continuous
layer between the nervous keel and the epidermic layer of the epiblast
(Plate 35, fig. 25). In the absence of a better series of sections we do
not feel able to determine this point. The posterior part of the nervous
keel retains the characters of the previous stage.
At the sides of the hind-brain very distinct commencements of the auditory
vesicles are apparent. They form shallow pits (Plate 35, fig. 24, _au._) of
the thickened part of the nervous layer adjoining the brain in this region.
Each pit is covered over by the epidermic layer above, which has no share
in its formation.
In many parts of the lateral regions of the body the nervous layer of the
epidermis is more than one cell deep.
The mesoblastic plates are now divided in the anterior part of the trunk
into a somatic and a splanchnic layer (Plate 35, fig. 25, _so._, _sp._),
though no distinct cavity is as yet present between these two layers. Their
vertebral extremities are somewhat wedge-shaped in section, the base of the
wedge being placed at the sides of the medullary keel. The wedge-shaped
portions are formed of a superficial layer of palisade-like cells and an
inner kernel of polygonal cells. The superficial layer on the dorsal side
is continuous with the somatic mesoblast, while the remainder pertains to
the splanchnic layer.
The diameter of the notochord has diminished, and the cells have assumed a
flattened form, the protoplasm being confined to an axial region. In
consequence of this, the peripheral layer appears clear in transverse
sections. A delicate cuticular sheath is formed around it. This sheath is
probably the commencement of the permanent sheath of later stages, but at
this stage it cannot be distinguished in structure from a delicate cuticle
which surrounds the greater part of the medullary cord.
The hypoblast has undergone no changes of importance.
The layers at the posterior end of the embryo retain the characters of the
last stage.
_Sixth day after impregnation._--At this stage (Plate 34, fig. 8) the
embryo is considerably more advanced than at the last stage. The trunk has
decidedly increased in length, and the head forms a relatively smaller
portion of the whole. The regions of the brain are more distinct. The optic
vesicles (_op._) have grown outwards so as to nearly reach the edges of the
area which forms the parietal part of the body. The fore-brain projects
slightly in front, and the mid-brain is seen as a distinct rounded
prominence. Behind the latter is placed the hind-brain, which passes
insensibly into the spinal cord. On either side of the mid- and hind-brain
a small region is slightly marked off from the rest of the parietal part,
and on this are seen two more or less transversely directed streaks, which,
by comparison with the Sturgeon[502], we are inclined to regard as the two
first visceral clefts (_br.c._). We have, however, failed to make them out
in sections, and owing to the insufficiency of our material, we have not
even studied them in surface views as completely as we could have wished.
Footnote 502: Salensky, "Recherches s. le Développement du
Sterlet." _Archives de Biol._ Vol. II. 1881, pl. XVII.
fig. 27.
The body is now laterally compressed, and more decidedly raised from the
yolk than in the previous stages. In the lateral regions of the trunk the
two segmental or archinephric ducts (_sg._) are visible in surface views:
the front end of each is placed at the level of the hinder border of the
head, and is marked by a flexure inwards towards the middle line. The
remainder of each duct is straight, and extends backwards for about half
the length of the embryo. The tail has much the same appearance as in the
last stage.
The vertebral regions of the mesoblastic plates are now segmented for the
greater part of the length of the trunk, and the somites of which they are
composed (Plate 36, fig. 30, _pr._) are very conspicuous in surface views.
Our sections of this stage are not so complete as could be desired: they
shew, however, several points of interest.
The central canal of the nervous system is large, with well-defined walls,
and in hardened specimens is filled with a coagulum. It extends nearly to
the region of the tail.
The optic vesicles, which are so conspicuous in surface views, appear in
section (Plate 35, fig. 26, _op._) as knob-like outgrowths of the
fore-brain, and very closely resemble the figures given by Oellacher of
these vesicles in Teleostei[503].
Footnote 503: "Beiträge zur Entwick. d. Knochenfische," _Zeit.
f. wiss. Zool._ Vol. XXIII. 1873, taf. III. fig. IX. 2.
From the analogy of the previous stage, we are inclined to think that they
have a lumen continuous with that of the fore-brain. In our only section
through them, however, they are solid, but this is probably due to the
section merely passing through them to one side.
The auditory pits (Plate 35, fig. 27, _au._) are now well marked, and have
the form of somewhat elongated grooves, the walls of which are formed of a
single layer of columnar cells belonging to the nervous layer of the
epidermis, and extending inwards so as nearly to touch the brain.
In an earlier stage it was pointed out that the dorsal part of the
medullary keel was different in its structure from the remainder, and that
it was destined to give rise to the nerves. The process of differentiation
is now to a great extent completed, and may best be seen in the auditory
region (Plate 35, fig. 27, VIII.). In this region there was present during
the last stage a great rhomboidal mass of cells at the dorsal region of the
brain (Plate 35, fig. 24, VIII.). In the present stage, this, which is the
rudiment of the seventh and auditory nerves, is seen growing down on each
side from the roof of the hind-brain, between the brain and the auditory
involution, and abutting against the wall of the latter.
Rudiments of the spinal nerves are also seen at intervals as projections
from the dorsal angles of the spinal cord (Plate 36, fig. 29, _sp.n._).
They extend only for a short distance outwards, gradually tapering off to a
point, and situated between the epiblast and the dorsal angles of the
mesoblastic somites.
The process of formation of the cranial nerves and dorsal roots of the
spinal nerves is, it will be seen, essentially the same as that already
known in the case of Elasmobranchii, Aves, &c. The nerves arise as
outgrowths of a special crest of cells, the _neural crest_ of Marshall,
which is placed along the dorsal angle of the cord. The peculiar position
of the dorsal roots of the spinal nerves is also very similar to what has
been met with in the early stages of these structures by Marshall in
Birds[504], and by one of us in Elasmobranchii[505].
Footnote 504: _Journal of Anat. and Physiol._ Vol. XI. p. 491,
plates XX. and XXI.
Footnote 505: "Elasmobranch Fishes," p. 156, plates 10 and 13.
[This edition, p. 378, pl. 11, 14.]
In the parietal region a cavity has now appeared in part of the trunk
between the splanchnic and somatic layers of the mesoblast (Plate 36,
fig. 29, _b.c._), the somatic layer (_so._) consisting of a single row of
columnar cells on the dorsal side, while the remainder of each somite is
formed of the splanchnic layer (_sp._). In many of the sections the somatic
layer is separated by a considerable interval from the epiblast.
We have been able to some extent to follow the development of the segmental
duct. The imperfect preservation of our specimens has, as in other
instances, rendered the study of the point somewhat difficult, but we
believe that the figure representing the development of the duct some way
behind its front end (Plate 36, fig. 29) is an accurate representation of
what may be seen in a good many of our sections.
It appears from these sections that the duct (Plate 36, fig. 29, _sg._) is
developed as a hollow ridge-like outgrowth of the somatic layer of
mesoblast, directed towards the epiblast, in which it causes a slight
bulging. The cavity of the ridge freely communicates with the body-cavity.
The anterior part of this ridge appears to be formed first. Very soon, in
fact, in an older embryo belonging to this stage, the greater part of the
groove becomes segmented off as a duct lying between the epiblast and
somatic mesoblast (Plate 36, fig. 28, _sg._), while the front end still
remains, as we believe, in communication with the body-cavity by an
anterior pore.
This mode of development corresponds in every particular with that observed
in Teleostei by Rosenberg and Oellacher.
The structure of the notochord (_nc._) at this stage is very similar to
that observed by one of us in Elasmobranchii[506]. The cord is formed of
transversely arranged flattened cells, the outer parts of which are
vacuolated, while the inner parts are granular, and contain the nuclei.
This structure gives rise to the appearance in transverse sections of an
axial darker area and a peripheral lighter portion.
Footnote 506: "Elasmobranch Fishes," p. 136, plate 11,
fig. 10. [This edition, p. 354, pl. 12.]
The hypoblast retains for the most part its earlier constitution, but
underneath the notochord, in the trunk, it is somewhat thickened, and the
cells at the two sides spread in to some extent under the thickened portion
(Plate 36, fig. 29, _s.nc._). This thickening, as is shewn in transverse
sections at the stage when the segmental duct becomes separated from the
somatic mesoblast (Plate 36, fig. 28, _s.nc._), is the commencement of the
subnotochordal rod.
The tail end of the embryo still retains its earlier characters.
_Seventh day after impregnation._--Our series of specimens of this stage is
very imperfect, and we are only able to call attention to the development
of a certain number of organs.
Our sections clearly establish the fact that the optic vesicles are now
hollow processes of the fore-brain. Their outer ends are dilated, and are
in contact with the external skin. The formation of the optic cup has not,
however, commenced. The nervous layer of the skin adjoining the outer wall
of the optic cup is very slightly thickened, constituting the earliest
rudiment of the lens.
In one of our embryos of this day the developing auditory vesicle still has
the form of a pit, but in the other it is a closed vesicle, already
constricted off from the nervous layer of the epidermis.
With reference to the development of the excretory duct we cannot add much
to what we have already stated in describing the last stage.
The duct is considerably dilated anteriorly (Plate 36, fig. 31, _sg._); but
our sections throw no light on the nature of the abdominal pore. The
posterior part of the duct has still the form of a hollow ridge united with
somatic mesoblast (Plate 36, fig. 32, _sg._).
During this stage, the embryo becomes to a small extent folded off from the
yolk-sack both in front and behind, and in the course of this process the
anterior and posterior extremities of the alimentary tract become
definitely established.
We have not got as clear a view of the process of formation of these two
sections of the alimentary tract as we could desire, but our observations
appear to shew that the process is in many respects similar to that which
takes place in the formation of the anterior part of the alimentary tract
in Elasmobranchii[507]. One of us has shewn that in Elasmobranchii the
ventral wall of the throat is formed _not_ by a process of folding in of
the hypoblastic sheet as in Birds, but by a growth of the ventral face of
the hypoblastic sheet on each side of and at some little distance from the
middle line. Each growth is directed inwards, and the two eventually meet
and unite, thus forming a complete ventral wall for the gut. Exactly the
same process would seem to take place in _Lepidosteus_, and after the lumen
of the gut is in this way established, a process of mesoblast on each side
also makes its appearance, forming a mesoblastic investment on the ventral
side of the alimentary tract. Some time after the alimentary tract has been
thus formed, the epiblast becomes folded in, in exactly the same manner as
in the Chick, the embryo becoming thereby partially constricted off from
the yolk (Plate 36, figs. 33, 34).
Footnote 507: F. M. Balfour, "Monograph on the Development of
Elasmobranch Fishes," p. 87, plate 9, fig. 2. [This edition, p.
303, pl. 10.]
The form of the lumen of the alimentary tract differs somewhat in front and
behind. In front, the hypoblastic sheet remains perfectly flat during the
formation of the throat, and thus the lumen of the latter has merely the
form of a slit. The lumen of the posterior end of the alimentary tract is,
however, narrower and deeper (Plate 36, figs. 33, 34, _al._). Both in front
and behind, the lateral parts of the hypoblastic sheet become separated
from the true alimentary tract as soon as the lumen of the latter is
established.
It is quite possible that at the extreme posterior end of the embryo a
modification of the above process may take place, for in this region the
hypoblast appears to us to have the form of a solid cord.
We could detect no true neurenteric canal, although a more or less complete
fusion of the germinal layers at the tail end of the embryo may still be
traced.
During this stage the protoplasm of the notochordal cells, which in the
last stage formed a kind of axial rod in the centre of the notochord,
begins to spread outwards toward the sheath of the notochord.
_Eighth day after impregnation._--The external form of the embryo (Plate
34, fig. 9) shews a great advance upon the stage last figured. Both head
and body are much more compressed laterally and raised from the yolk, and
the head end is folded off for some distance. The optic vesicles are much
less prominent externally. A commencing opercular fold is distinctly seen.
Our figure of this stage is not, however, so satisfactory as we could wish.
A thickening of the nervous layer of the external epiblast which will form
the lens (Plate 36, fig. 35, _l._) is more marked than in the last stage,
and presses against the slightly concave exterior wall of the optic vesicle
(_op._). The latter has now a large cavity, and its stalk is considerably
narrowed.
The auditory vesicles (Plate 36, fig. 36, _au._) are closed, appearing as
hollow sacks one on each side of the brain, and are no longer attached to
the epiblast.
The anterior opening of the segmental duct can be plainly seen close behind
the head. The lumen of the duct is considerably larger.
The two vertebral portions of the mesoblast are now separated by a
considerable space from the epiblast on one side and from the notochord on
the other, and the cells composing them have become considerably elongated
from side to side (Plate 36, fig. 37, _ms_).
In some sections the aorta can be seen (Plate 36, fig. 37, _ao_) lying
close under the subnotochordal rod, between it and the hypoblast, and on
either side of it a slightly larger cardinal vein (_cd.v._).
The protoplasm of the notochord has now again retreated towards the centre,
shewing a clear space all round. This is most marked in the region of the
trunk (Plate 36, fig. 37). The subnotochordal rod (_s.nc._) lies close
under it.
A completely closed fore-gut, lined by thickened hypoblast, extends about
as far back as the auditory sacks (Plate 36, figs. 35 and 36, _al._). In
the trunk the hypoblast, which will form the walls of the alimentary tract,
is separated from the notochord by a considerable interval.
_Ninth day after impregnation: External characters._--Very considerable
changes have taken place in the external characters of the embryo. It is
about 8 millims. in length, and has assumed a completely piscine form. The
tail especially has grown in length, and is greatly flattened from side to
side: it is wholly detached from the yolk, and bends round towards the
head, usually with its left side in contact with the yolk. It is provided
with well-developed dorsal and ventral fin-folds, which meet each other
round the end of the tail, the tail fin so formed being nearly symmetrical.
The head is not nearly so much folded off from the yolk as the tail. At its
front end is placed a disc with numerous papillæ, of which we shall say
more hereafter. This disc is somewhat bifid, and is marked in the centre by
a deep depression.
Dorsal to it, on the top of the head, are two widely separated nasal pits.
On the surface of the yolk, in front of the head, is to be seen the heart,
just as in Sturgeon embryos. Immediately below the suctorial disc is a
slit-like space, forming the mouth. It is bounded below by the two
mandibular arches, which meet ventrally in the median line. A shallow but
well-marked depression on each side of the head indicates the posterior
boundary of the mandibular arch. Behind this is placed the very conspicuous
hyoid arch with its rudimentary opercular flap; and in the depression,
partly covered over by the latter, may be seen a ridge, the external
indication of the first branchial arch.
_Eleventh day after impregnation: External characters._--The embryo (Plate
34, fig. 10) is now about 10 millims. in length, and in several features
exhibits an advance upon the embryo of the previous stage.
The tail fin is now obviously not quite symmetrical, and the dorsal
fin-fold is continued for nearly the whole length of the trunk. The
suctorial disc (Plate 34, fig. 11, _s.d._) is much more prominent, and the
papillæ (about 30 in number) covering it are more conspicuous from the
surface. It is not obviously composed of two symmetrical halves. The
opercular flap is larger, and the branchial arches behind it (two of which
may be made out without dissection) are more prominent.
The anterior pair of limbs is now visible in the form of two _longitudinal_
folds projecting in a vertical direction from the surface of the yolk-sack
at the sides of the body.
The stages subsequent to hatching have been investigated with reference to
the external features and to the habits by Agassiz, and we shall enrich our
own account by copious quotations from his memoir.
He states that the first batch were hatched on the eighth[508] day after
being laid. "The young Fish possessed a gigantic yolk-bag, and the
posterior part of the body presented nothing specially different from the
general appearance of a Teleostean embryo, with the exception of the great
size of the chorda. The anterior part, however, was most remarkable; and at
first, on seeing the head of this young _Lepidosteus_, with its huge
mouth-cavity extending nearly to the gill-opening, and surmounted by a
hoof-shaped depression edged with a row of protuberances acting as suckers,
I could not help comparing this remarkable structure, so utterly unlike
anything in Fishes or Ganoids, to the Cyclostomes, with which it has a
striking analogy. This organ is also used by _Lepidosteus_ as a sucker, and
the moment the young Fish is hatched he attaches himself to the sides of
the disc, and there remains hanging immovable; so firmly attached, indeed,
that it requires considerable commotion in the water to make him loose his
hold. Aërating the water by pouring it from a height did not always produce
sufficient disturbance to loosen the young Fishes. The eye, in this stage,
is rather less advanced than in corresponding stages in bony Fishes; the
brain is also comparatively smaller, the otolith ellipsoidal, placed
obliquely in the rear above the gill-opening.... Usually the gill-cover is
pressed closely against the sides of the body, but in breathing an opening
is seen through which water is constantly passing, a strong current being
made by the rapid movement of the pectorals, against the base of which the
extremity of the gill-cover is closely pressed. The large yolk-bag is
opaque, of a bluish-gray colour. The body of the young _Lepidosteus_ is
quite colourless and transparent. The embryonic fin is narrow, the dorsal
part commencing above the posterior end of the yolk-bag; the tail is
slightly rounded, the anal opening nearer the extremity of the tail than
the bag. The intestine is narrow, and the embryonic fin extending from the
vent to the yolk-bag is quite narrow. In a somewhat more advanced
stage,--hatched a few hours earlier,--the upper edge of the yolk-bag is
covered with black pigment cells, and minute black pigment cells appear on
the surface of the alimentary canal. There are no traces of embryonic
fin-rays either in this stage or the one preceding; the structure of the
embryonic fin is as in bony Fishes--previous to the appearance of these
embryonic fin-rays--finely granular. Seen in profile, the yolk-bag is
ovoid; as seen from above, it is flattened, rectangular in front, with
rounded corners, tapering to a rounded point towards the posterior
extremity, with re-entering sides."
Footnote 508: This statement of Agassiz does not correspond
with the dates on the specimens sent to us--a fact no doubt due
to the hatching not taking place at the same time for all the
larvæ.
We have figured an embryo of 11 millims. in length, shortly after hatching
(Plate 34, fig. 12), the most important characters of which are as
follows:--The yolk-sack, which has now become much reduced, forms an
appendage attached to the ventral surface of the body, and has a very
elongated form as compared with its shape just before hatching. The mouth,
as also noticed by Agassiz, has a very open form. It is (Plate 34, fig. 13,
_m._) more or less rhomboidal, and is bounded behind by the mandibular arch
(_mn._) and laterally by the superior maxillary processes (_s.mx_). In
front of the mouth is placed the suctorial disc (_s.d._), the central
papillæ of which are arranged in groups. The opercular fold (_h.op._) is
very large, covering the arches behind. A well-marked groove is present
between the mandibular and opercular arches, but so far as we can make out
it is not a remnant of the hyomandibular cleft.
The pectoral fins (Plate 34, fig. 12, _pc.f._) are very prominent
longitudinal ridges, which, owing to their being placed on the surface of
the yolk-sack, project in a nearly vertical direction: a feature which is
also found in many Teleostean embryos with large yolk-sacks.
No traces of the pelvic fins have yet become developed.
The positions of the permanent dorsal, anal, and caudal fins, as pointed
out by Agassiz, are now indicated by a deposit of pigment in the embryonic
fin.
In an embryo on the sixth day after hatching, of about 15 millims. in
length, of which we have also given a figure (Plate 34, fig. 14), the
following fresh features deserve special notice.
In the region of the head there is a considerable elongation of the
pre-oral part, forming a short snout, at the end of which is placed the
suctorial disc. At the sides of the snout are placed the nasal pits, which
have become somewhat elongated anteriorly.
The mouth has lost its open rhomboidal shape, and has become greatly
narrowed in an antero-posterior direction, so that its opening is reduced
to a slit. The mandibles and maxillary processes are nearly parallel,
though both of them are very much shorter than in the adult. The operculum
is now a very large flap, and has extended so far backwards as to cover the
insertion of the pectoral fin. The two opercular folds nearly meet
ventrally.
The yolk-sack is still more reduced in size, one important consequence of
which is that the pectoral fins (_pc.f._) appear to spring out more or less
horizontally from the sides of the body, and at the same time their
primitive line of attachment to the body becomes transformed from a
longitudinal to a more or less transverse one.
The first traces of the pelvic fins are now visible as slight longitudinal
projections near the hinder end of the yolk-sack (_pl.f._).
The pigmentation marking the regions of the permanent fins has become more
pronounced, and it is to be specially noted that the ventral part of the
caudal fin (the permanent caudal) is considerably more prominent than the
dorsal fin opposite to it.
The next changes, as Agassiz points out, "are mainly in the lengthening of
the snout; the increase in length both of the lower and upper jaw; the
concentration of the sucker of the sucking disc; and the adoption of the
general colouring of somewhat older Fish. The lobe of the pectoral has
become specially prominent, and the outline of the fins is now indicated by
a fine milky granulation. Seen from above, the gill-cover is seen to leave
a large circular opening leading to the gill-arches, into which a current
of water is constantly passing, by the lateral expansion and contraction of
the gill-cover; the outer extremity of the gill-cover covers the base of
the pectorals. In a somewhat older stage the snout has become more
elongated, the sucker more concentrated, and the disproportionate size of
the terminal sucking-disc is reduced; the head, when seen from above,
becoming slightly elongated and pointed."
In a larva of about 18 days old and 21 millims. in length, of which we have
not given a figure, the snout has grown greatly in length, carrying with it
the nasal organs, the openings of which now appear to be divided into two
parts. The suctorial disc is still a prominent structure at the end of the
snout. The lower jaw has elongated correspondingly with the upper, so that
the gape is very considerable, though still very much less than in the
adult.
The opercular flaps overlap ventrally, the left being superficial. They
still cover the bases of the pectoral fins. The latter are described by
Agassiz as being "kept in constant rapid motion, so that the fleshy edge is
invisible, and the vibration seems almost involuntary, producing a constant
current round the opening leading into the cavity of the gills."
The pelvic fins are somewhat more prominent.
The yolk-sack, as pointed out by Agassiz, has now disappeared as an
external appendage.
After the stage last described the young Fish rapidly approaches the adult
form. To shew the changes effected we have figured the head of a larva of
about a month old and 23 millims. in length (Plate 34, fig. 15). The
suctorial disc, though much reduced, is still prominent at the end of the
snout. Eventually, as shewn by Agassiz, it forms the fleshy globular
termination of the upper jaw.
The most notable feature in which the larva now differs in its external
form from the adult is in the presence of an externally heterocercal tail,
caused by the persistence of the primitive caudal fin as an elongated
filament projecting beyond the permanent caudal (Plate 41, fig. 68).
Delicate dermal fin-rays are now conspicuous in the peripheral parts of all
the permanent fins. These rays closely resemble the horny fin-rays in the
fins of embryo Elasmobranchii in their development and structure. They
appear gradually to enlarge to form the permanent rays, and we have
followed out some of the stages of their growth, which is in many respects
interesting. Our observations are not, however, complete enough to publish,
and we can only say here that their early development and structure proves
their homology with the horny fibres or rays in fins of Elasmobranchii. The
skin is still, however, entirely naked, and without a trace of its future
armour of enamelled scales.
The tail of a much older larva, 11 centims. in length, in which the scales
have begun to be formed, is shewn in Plate 34, fig. 16.
We complete this section of our memoir by quoting the following passages
from Agassiz as to the habits of the young fish at the stages last
described:--
"In the stages intervening between plate iii, fig. 19, and plate iii,
fig. 30, the young _Lepidosteus_ frequently swim about, and become
readily separated from their point of attachment. In the stage of
plate iii, fig. 30, they remain often perfectly quiet close to the
surface of the water; but, when disturbed, move very rapidly about
through the water.... The young already have also the peculiar habit
of the adult of coming to the surface to swallow air. When they go
through the process under water of discharging air again they open
their jaws wide, and spread their gill-covers, and swallow as if they
were choking, making violent efforts, until a minute bubble of air has
become liberated, when they remain quiet again. The resemblance to a
Sturgeon in the general appearance of this stage of the young
_Lepidosteus_ is quite marked."
BRAIN.
I. _Anatomy._
The brain of _Lepidosteus_ has been figured by Busch (whose figure has been
copied by Miklucho-Maclay, and apparently by Huxley), by Owen and by Wilder
(No. 15). The figure of the latter author, representing a longitudinal
section through the brain, is the most satisfactory, the other figures
being in many respects inaccurate; but even Wilder's figure and
description, though taken from the fresh object, appear to us in some
respects inadequate. He offers, moreover, fresh interpretations of certain
parts of the brain which we shall discuss in the sequel.
We have examined two brains which, though extremely soft, were,
nevertheless, sufficiently well preserved to enable us to study the
external form. We have, moreover, made a complete series of transverse
sections through one of the brains, and our sections, though utterly
valueless from a histological point of view, have thrown some light on the
topographical anatomy of the brain.
Plate 38, figs. 47A, B, and C, represent three views of the brain, viz.:
from the side, from above, and from below. We will follow in our
description the usual division of the brain into fore-brain, mid-brain, and
hind-brain.
The fore-brain consists of an anterior portion forming the cerebrum, and a
posterior portion constituting the thalamencephalon.
The cerebrum at first sight appears to be composed of (_a_) a pair of
posterior and somewhat dorsal lobes, forming what have usually been
regarded as the true cerebral hemispheres, but called by Wilder the
prothalami, and (_b_) a pair of anterior and ventral lobes, usually
regarded as the olfactory lobes, from which the olfactory nerves spring.
Mainly from a comparison with our embryonic brains described in the sequel,
we are inclined to think that the usual interpretations are not wholly
correct, but that the true olfactory lobes are to be sought for in small
enlargements (Plate 38. figs. 47A, B, and C, _olf._) at the front end of
the brain[509] from which the olfactory nerves spring. The cerebrum proper
would then consist of a pair of anterior and ventral lobes (_ce._), and of
a pair of posterior lobes (_ce´._), both pairs uniting to form a basal
portion behind.
Footnote 509: The homologies of the olfactory lobes throughout
the group of Fishes require further investigation.
The two pairs of lobes probably correspond with the two parts of the
cerebrum of the Frog, the anterior of which, like that of _Lepidosteus_,
was held to be the olfactory lobe, till Götte's researches shewed that this
view was not tenable.
The anterior lobes of the cerebrum have a conical form, tapering
anteriorly, and are completely separated from each other. The posterior
lobes, as is best shewn in side views, have a semicircular form. Viewed
from above they appear as rounded prominences, and their dorsal surface is
marked by two conspicuous furrows (Plate 38, fig. 47B, _ce´._), which have
been noticed by Wilder, and are similar to those present in many Teleostei.
Their front ends overhang the base of the anterior cerebral lobes. The
basal portion of the cerebrum is an undivided lobe, the anterior wall of
which forms the lamina terminalis.
What we have above described as the posterior cerebral lobes have been
described by Wilder as constituting the everted dorsal border of the basal
portion of the cerebrum.
The portion of the cerebro-spinal canal within the cerebrum presents
certain primitive characters, which are in some respects dissimilar to
those of higher types, and have led Wilder to hold the posterior cerebral
lobes, together with what we have called the basal portion of the cerebrum,
to be structures peculiar to Fishes, for which he has proposed the name
"prothalami."
In the basal portion of the cerebrum there is an unpaired slit-shaped
ventricle, the outer walls of which are very thick. It is provided with a
floor formed of nervous matter, in part of which, judging from Wilder's
description, a well-marked commissure is placed. We have found in the larva
a large commissure in this situation (Plate 37, figs. 44 and 45, _a.c._);
and it may be regarded as the homologue of the anterior commissure of
higher types. This part of the ventricle is stated by Wilder to be without
a roof. This appears to us highly improbable. We could not, however,
determine the nature of the roof from our badly preserved specimens, but if
present, there is no doubt that it is extremely thin, as indeed it is in
the larva (Plate 37, fig. 46B). In a dorsal direction the unpaired
ventricle extends so as to separate the two posterior cerebral lobes.
Anteriorly the ventricle is prolonged into two horns, which penetrate for a
short distance, as _the lateral ventricles_, into the base of the anterior
cerebral lobes. The front part of each anterior cerebral lobe, as well as
of the whole of the posterior lobes, appears solid in our sections; but
Wilder describes the anterior horns of the ventricle as being prolonged for
the whole length of the anterior lobes.
In the embryos of all Vertebrates the cerebrum is not at first divided into
two lobes, so that the fact of the posterior part of the cerebrum in
_Lepidosteus_ and probably other Ganoids remaining permanently in the
undivided condition does not appear to us a sufficient ground for giving to
the lobes of this part of the cerebrum the special name of prothalami, as
proposed by Wilder, or for regarding them as a section of the brain
peculiar to Fishes.
The thalamencephalon (_th._) contains the usual parts, but is in some
respects peculiar. Its lateral walls, forming the optic thalami, are thick,
and are not sharply separated in front from the basal part of the cerebrum;
between them is placed the third ventricle. The thalami are of considerable
extent, though partially covered by the optic lobes and the posterior lobes
of the cerebrum. They are not, however, relatively so large as in other
Ganoid forms, more especially the Chondrostei and _Polypterus_.
On the roof of the thalamencephalon is placed a large thin-walled vesicle
(Plate 38, figs. 47A and B, _v.th._), which undoubtedly forms the most
characteristic structure connected with this part of the brain. Owing to
the wretched state of preservation of the specimens, we have found it
impossible to determine the exact relations of this body to the remainder
of the thalamencephalon; but it appears to be attached to the roof of the
thalamencephalon by a narrow stalk only. It extends forwards so as to
overlap part of the cerebrum in front, and is closely invested by a highly
vascular layer of the pia mater.
No mention is made by Wilder of this body; nor is it represented in his
figures or in those of the other anatomists who have given drawings of the
brain of _Lepidosteus_. It might at first be interpreted as a
highly-developed pineal gland, but a comparison with the brain of the larva
(vide p. 764) shews that this is not the case, but that the body in
question is represented in the larva by a special outgrowth of the roof of
the thalamencephalon. The vesicle of the roof of the thalamencephalon is
therefore to be regarded as a peculiar development of the tela choroidea of
the third ventricle.
How far this vesicle has a homologue in the brains of other Ganoids is not
certain, since negative evidence on this subject is all but valueless. It
is possible that a vesicular sack covering over the third ventricle of the
Sturgeon described by Stannius[510], and stated by him to be wholly formed
of the membranes of the brain, is really the homologue of our vesicle.
Footnote 510: "Ueb. d. Gehirn des Störs," Müller's _Archiv_,
1843, and _Lehrbuch d. vergl. Anat. d. Wirbelthiere_. Cattie,
_Archives de Biologie_, Vol. III. 1882, has recently described
in _Acipenser sturio_ a vesicle on the roof of the
thalamencephalon, whose cavity is continuous with the third
ventricle. This vesicle is clearly homologous with that in
_Lepidosteus_. (June 28, 1882.)
Wiedersheim[511] has recently described in _Protopterus_ a body which is
undoubtedly homologous with our vesicle, which he describes in the
following way:--
"Dorsalwärts ist das Zwischenhirn durch ein tiefes, von Hirnschlitz
eingenommenes Thal von Vorderhirn abgesetzt; dasselbe ist jedoch durch
eine häutige, mit der Pia mater zusammenhängende Kuppel oder Kapsel
überbrückt."
Footnote 511: R. Wiedersheim, _Morphol. Studien_, 1880, p.
71.
This "Kuppel" has precisely the same relations and a very similar
appearance to our vesicle. The true pineal gland is placed behind it. It
appears to us possible that the body found by Huxley[512] in _Ceratodus_,
which he holds to be the pineal gland, is in reality this vesicle. It is
moreover possible that what has usually been regarded as the pineal gland
in _Petromyzon_ may in reality be the homologue of the vesicle we have
found in _Lepidosteus_.
Footnote 512: "On _Ceratodus Forsteri_," &c., _Proc. Zool.
Soc._ 1876.
We have no observations on the pineal gland of the adult, but must refer
the reader for the structure and relations of this body to the
embryological section.
The infundibulum (Plate 38, fig. 47A, _in._) is very elongated. Immediately
in front of it is placed the optic chiasma (Plate 38, figs. 47A and C,
_op.ch._) from which the optic fibres can be traced passing along the sides
of the optic thalami and to the optic lobes, very much as in Müller's
figure of the brain of _Polypterus_.
On the sides of the infundibulum are placed two prominent bodies, the lobi
inferiores (_l.in._), each of which contains a cavity continuous with the
prolongation of the third ventricle into the infundibulum. The apex of the
infundibulum is enlarged, and to it is attached a pituitary body (_pt._).
The mid-brain is of considerable size, and consists of a basal portion
connecting the optic thalami with the medulla, and a pair of large optic
lobes (_op.l._). The iter a tertio ad quartum ventriculum, which forms the
ventricle of this part of the brain, is prolonged into each optic lobe, and
the floor of each prolongation is taken up by a dome-shaped projection, the
homologue of the torus semicircularis of Teleostei.
The hind-brain consists of the usual parts, the medulla oblongata and the
cerebellum. The medulla presents no peculiar features. The sides of the
fourth ventricle are thickened and everted, and marked with peculiar folds
(Plate 38, figs. 47A and B, _m.o._).
The cerebellum is much larger than in the majority of Ganoids, and
resembles in all essential features the cerebellum of Teleostei. In side
views it has a somewhat S-shaped form, from the presence of a peculiar
lateral sulcus (Plate 38, fig. 47A, _cb._). As shewn by Wilder, its wall
actually has in longitudinal section this form of curvature, owing to its
anterior part projecting forwards into the cavity of the iter[513]. This
forward projection is not, however, so conspicuous as in most Teleostei.
The cerebellum contains a large unpaired prolongation of the fourth
ventricle.
Footnote 513: In Wilder's figure the walls of the cerebellum
are represented as much too thin.
II. _Development._
The early development of the brain has already been described; and,
although we do not propose to give any detailed account of the later stages
of its growth, we have thought it worth while calling attention to certain
developmental features which may probably be regarded as to some extent
characteristic of the Ganoids. With this view we have figured (Plate 37,
figs. 44, 45) longitudinal sections of the brain at two stages, viz.: of
larvæ of 15 and 26 millims., and transverse sections (Plate 37, figs.
46A-G) of the brain of a larva at about the latter stage (25 millims.).
The original embryonic fore-brain is divided in both embryos into a
cerebrum (_ce._) in front and a thalamencephalon (_th_) behind. In the
younger embryo the cerebrum is a single lobe, as it is in the brains of all
Vertebrate embryos; but in the older larva it is anteriorly (Plate 37,
fig. 46A) completely divided into two hemispheres. The roof of the
undivided posterior part of the cerebrum is extremely thin (Plate 37, fig.
46B). Near the posterior border of the base of the cerebrum there is a
great development of nervous fibres, which may probably be regarded as in
part equivalent to the anterior commissure (Plate 37, figs. 44, 45 _a.c._).
Even in the oldest of the two brains the olfactory lobes are very slightly
developed, constituting, however, small lateral and ventral prominences of
the front end of the hemispheres. From each of them there springs a long
olfactory nerve, extending for the whole length of the rostrum to the
olfactory sack.
The thalamencephalon presents a very curious structure, and is relatively a
more important part of the brain than in the embryo of any other form which
we know of. Its roof, instead of being, as usual, compressed
antero-posteriorly[514], so as to be almost concealed between the cerebral
hemispheres and the optic lobes (mid-brain), projects on the surface for a
length quite equal to that of the cerebral hemispheres (Plate 37, figs. 44
and 45, _th._). In the median line the roof of the thalamencephalon is thin
and folded; at its posterior border is placed the opening of the small
pineal gland. This body is a papilliform process of the nervous matter of
the roof of this part of the brain, and instead of being directed forwards,
as in most Vertebrate types, tends somewhat backwards, and rests on the
mid-brain behind (Plate 37, figs. 44, 45, and 46C and D, _pn._). The roof
of the thalamencephalon immediately in front of the pineal gland forms a
sort of vesicle, the sides of which extend laterally as a pair of lobes,
shewn in transverse sections in Plate 37, figs. 46C and D, as _th.l._ This
vesicle becomes, we cannot doubt, the vesicle on the roof of the
thalamencephalon which we have described in the adult brain. Immediately in
front of the pineal gland the roof of the thalamencephalon contains a
transverse commissure (Plate 37, fig. 46C, _z._), which is the homologue of
a similarly situated commissure present in the Elasmobranch brain[515],
while behind the pineal gland is placed the posterior commissure. The sides
of the thalamencephalon are greatly thickened, forming the optic thalami
(Plate 37, figs. 46C and D, _op.th._), which are continuous in front with
the thickened outer walls of the hemispheres. Below, the thalamencephalon
is produced into a very elongated infundibulum (Plate 37, figs. 44, 45,
46E, _in._), the apex of which is trilobed as in Elasmobranchii and
Teleostei. The sides of the infundibulum exhibit two lobes, the lobi
inferiores (Plate 37, fig. 46E, _l.in._), which are continued posteriorly
into the crura cerebri.
Footnote 514: Vide F. M. Balfour, _Comparative Embryology_,
Vol. II. figs. 248 and 250.
Footnote 515: Vide F. M. Balfour, _Comparative Embryology_,
Vol. II. pp. 355-6 [the original edition], where it is
suggested that this commissure is the homologue of the grey
commissure of higher types.
The pituitary body[516] (Plate 37, figs. 44, 45, 46E, _pt._) is small, not
divided into lobes, and provided with a very minute lumen.
Footnote 516: We have not been able to work out the early
development of the pituitary body as satisfactorily as we could
have wished. In Plate 37, fig. 40, there is shewn an
invagination of the oral epithelium to form it; in Plate 37,
figs. 41 and 42, it is represented in transverse section in two
consecutive sections. Anteriorly it is still connected with the
oral epithelium (fig. 41), while posteriorly it is free. It is
possible that an earlier stage of it is shewn in Plate 36,
fig. 35. Were it not for the evidence in other types of its being
derived from the epiblast we should be inclined to regard it as
hypoblastic in origin.
In front of the infundibulum is the optic chiasma (Plate 37, fig. 46D,
_op.ch._), which is developed very early. It is, as stated by Müller, a
true chiasma.
The mid-brain (Plate 37, figs. 44 and 45, _m.b._) is large, and consists in
both stages of (1) a thickened floor forming the crura cerebri, the central
canal of which constitutes the iter a tertio ad quartum ventriculum; and
(2) the optic lobes (Plate 37, figs. 46E, F, G, _op.l._) above, each of
which is provided with a cavity continuous with the median iter. The optic
lobes are separated dorsally and in front by a well-marked median
longitudinal groove. Posteriorly they largely overlap the cerebellum. In
the anterior part of the optic lobes, at the point where the iter joins the
third ventricle, there may be seen slight projections of the floor into the
lumen of the optic lobes (Plate 37, fig. 46E). These masses probably become
in the adult the more conspicuous prominences of the floor of the
ventricles of the optic lobes, which we regard as homologous with the tori
semicirculares of the brain of the Teleostei.
The hind-brain is formed of the usual divisions, viz.: cerebellum and
medulla oblongata (Plate 37, figs. 44 and 45, _cb._, _md._). The former
constitutes a bilobed projection of the roof of the hind-brain. Only a
small portion of it is during these stages left uncovered by the optic
lobes, but the major part extends forwards for a considerable distance
under the optic lobes, as shewn in the transverse sections (Plate 37, figs.
46F and G, _cb._); and its two lobes, each with a prolongation of its
cavity, are continued forwards beyond the opening of the iter into the
fourth ventricle.
It is probable that the anterior horns of the cerebellum are equivalent to
the prolongations of the cerebellum into the central cavity of the optic
lobes of Teleostei, which are continuous with the so-called fornix of
Göttsche.
III. _Comparison of the larval and adult brain of Lepidosteus,
together with some observations on the systematic value
of the characters of the Ganoid brain._
The brain of the older of the two larvæ, which we have described,
sufficiently resembles in most of its features that of the adult to render
material assistance in the interpretation of certain of the parts of the
latter. It will be remembered that in the adult brain the parts usually
held to be olfactory lobes were described as the anterior cerebral lobes.
The grounds for this will be apparent by a comparison of the cerebrum of
the larva and adult. In the larva the cerebrum is formed of (1) an unpaired
basal portion with a thin roof, and (2) of a pair of anterior lobes, with
small olfactory bulbs at their free extremities.
The basal portion in the larva clearly corresponds in the adult with the
basal portion, together with the two posterior cerebral lobes, which are
merely special outgrowths of the dorsal edge of the primitive basal
portion. The pair of anterior lobes have exactly the same relations in the
larva as in the adult, except that in the former the ventricles are
prolonged for their whole length instead of being confined to their
proximal portions. If, therefore, our identifications of the larval parts
of the brain are correct, there can hardly be a question as to our
identifications of the parts in the adult. As concerns these
identifications, the comparison of the brain of our two larvæ appears
conclusive in favour of regarding the anterior lobes as parts of the
cerebrum, as distinguished from the olfactory lobes, in that they are
clearly derived from the undivided anterior portion of the cerebrum of the
younger larva.
The comparison of the larval brain with that of the adult again appears to
us to leave no doubt that the vesicle attached to the roof of the
thalamencephalon in the adult is the same structure as the bilobed
outgrowth of this roof in the larva; and since there is in addition a
well-developed pineal gland in the larva with the usual relations, there
can be no ground for identifying the vesicle in the adult with the pineal
gland.
Müller, in his often quoted memoir (No. 13), states that the brains of
Ganoids are peculiar and distinct from those both of Teleostei and
Elasmobranchii; but in addition to pointing out that the optic nerves form
a chiasma he does not particularly mention the features, to which he
alludes in general terms. More recently Wilder (No. 15) has returned to
this subject; and though, as we have already had occasion to point out, we
cannot accept all his identifications of the parts of the Ganoid brain, yet
he has called attention to certain characteristic features of the cerebrum
which have an undoubted systematic value.
The distinctive characters of the Ganoid brain are, in our opinion, (1) the
great elongation of the region of the thalamencephalon; and (2) the
unpaired condition of the posterior part of the cerebrum, and the presence
of so thin a roof to the ventricle of this part as to cause it to appear
open above.
The immense length of the region of the thalamencephalon is a feature in
the Ganoid brain which must at once strike any one who examines figures of
the brains of Chondrostei, _Polypterus_, or _Amia_. It is less striking in
the adult _Lepidosteus_, though here also we have shewn that the
thalamencephalon is really very greatly developed; but in the larva of
_Lepidosteus_ this feature is still better marked, so that the brain of the
larva may be described as being more characteristically Ganoid than that of
the adult.
The presence of a largely developed thalamencephalon at once distinguishes
a Ganoid brain from that of a Teleostean Fish, in which the optic thalami
are very much reduced; but _Lepidosteus_ shews its Teleostean affinities by
a commencing reduction of this part of the brain.
The large size of the thalamencephalon is also characteristic of the Ganoid
brain in comparison with the brain of the Dipnoi; but is not however so
very much more marked in the Ganoids than it is in some Elasmobranchii.
On the whole, we may consider the retention of a large thalamencephalon as
a primitive character.
The second feature which we have given as characteristic of the Ganoid
brain is essentially that which has been insisted upon by Wilder, though
somewhat differently expressed by him.
The simplest condition of the cerebrum is that found in the larva of
_Lepidosteus_, where there is an anterior pair of lobes, and an undivided
posterior portion with a simple prolongation of the third ventricle, and a
very thin roof. The dorsal edges of the posterior portion, adjoining the
thin roof, usually become somewhat everted (cf. Wilder), and in
_Lepidosteus_ these edges have in the adult a very great development, and
form (vide Plate 38, fig. 47A-C, _ce´._) two prominent lobes, which we have
spoken of as the posterior cerebral lobes.
These characters of the cerebrum are perhaps even more distinctive than
those of the thalamencephalon.
In Teleostei the cerebrum appears to be completely divided into two
hemispheres, which are, however, all but solid, the lateral ventricles
being only prolonged into their bases. In Dipnoi again there is either
(_Protopterus_, Wiedersheim[517]) a completely separated pair of oval
hemispheres, not unlike those of the lower Amphibia, or the oval
hemispheres are not completely separated from each other (_Ceratodus_,
Huxley[518], _Lepidosiren_, Hyrtl[519]); in either case the hemispheres are
traversed for the whole length by lateral ventricles which are either
completely or nearly completely separated from each other.
Footnote 517: _Morphol. Studien_, III. Jena, 1880.
Footnote 518: "On _Ceratodus Forsteri_," _Proc. Zool. Soc._
1876.
Footnote 519: _Lepidosiren paradoxa._ Prag. 1845.
In Elasmobranchii the cerebrum is an unpaired though bilobed body, but
traversed by two completely separated lateral ventricles, and without a
trace of the peculiar membranous roof found in Ganoids.
Not less interesting than the distinguishing characters of the Ganoid brain
are those cerebral characters which indicate affinities between
_Lepidosteus_ and other groups. The most striking of these are, as might
have been anticipated, in the direction of the Teleostei.
Although the foremost division of the brain is very dissimilar in the two
groups, yet the hind-brain in many Ganoids and the mid-brain also in
_Lepidosteus_ approaches closely to the Teleostean type. The most essential
feature of the cerebellum in Teleostei is its prolongation forwards into
the ventricles of the optic vesicles as the valvula cerebelli. We have
already seen that there is a homologous part of the cerebellum in
_Lepidosteus_; Stannius also describes this part in the Sturgeon, but no
such part is represented in Müller's figure of the brain of _Polypterus_,
or described by him in the text.
The cerebellum is in most Ganoids relatively smaller, and this is even the
case with _Amia_; but the cerebellum of _Lepidosteus_ is hardly less bulky
than that of most Teleostei.
The presence of tori semicirculares on the floor of the mid-brain of
_Lepidosteus_ again undoubtedly indicates its affinities with the
Teleostei, and such processes are stated by Stannius to be absent in the
Sturgeon, and have not, so far as we are aware, been described in other
Ganoids. Lastly we may point to the presence of well-developed lobi
inferiores in the brain of _Lepidosteus_ as an undoubted Teleostean
character.
On the whole, the brain of _Lepidosteus_, though preserving its true Ganoid
characters, approaches more closely to the brain of the Teleostei than that
of any other Ganoid, including even _Amia_.
It is not easy to point elsewhere to such marked resemblances of the Ganoid
brain, as to the brain of the Teleostei.
The division of the cerebrum into anterior and posterior lobes, which is
found in _Lepidosteus_, probably reappears again, as already indicated, in
the higher Amphibia. The presence of the peculiar vesicle attached to the
roof of the thalamencephalon has its parallel in the brain of
_Protopterus_, and as pointing in the same direction a general similarity
in the appearance of the brain of _Polypterus_ to that of the Dipnoi may be
mentioned.
There appears to us to be in no points a close resemblance between the
brain of Ganoids and that of Elasmobranchii.
SENSE ORGANS.
_Olfactory organ._
_Development._--The nasal sacks first arise during the late embryonic
period in the form of a pair of thickened patches of the nervous layer of
the epiblast on the dorsal surface of the front end of the head (Plate 37,
fig. 39, _ol._). The patches very soon become partially invaginated; and a
small cavity is developed between them and the epidermic layer of the
epiblast (Plate 37, figs. 42 and 43, _ol._). Subsequently, the roof of this
space, formed by the epidermic layer of the epiblast, is either broken
through or absorbed; and thus open pits, _lined entirely by the nervous
layer of the epidermis_, are formed.
We are not acquainted with any description of an exactly similar mode of
origin of the olfactory pits, though the process is almost identical with
that of the other sense organs.
We have not worked out in detail the mode of formation of the double
openings of the olfactory pits, but there can be but little doubt that it
is caused by the division of the single opening into two.
The olfactory nerve is formed very early (Plate 37, fig. 39, I), and, as
Marshall has found in Aves and Elasmobranchii, it arises at a stage prior
to the first differentiation of an olfactory bulb as a special lobe of the
brain.
_The Eye._
_Anatomy._--We have not made a careful histological examination of the eye
of _Lepidosteus_, which in our specimens was not sufficiently well
preserved for such a purpose; but we have found a vascular membrane
enveloping the vitreous humour on its retinal aspect, which, so far as we
know, is unlike anything which has so far been met with in the eye of any
other adult Vertebrate.
The membrane itself is placed immediately outside the hyaloid membrane,
_i.e._ on the side of the hyaloid membrane bounding the vitreous humour. It
is easily removed from the retina, to which it is only adherent at the
entrance of the optic nerve. In both the eyes we examined it also adhered,
at one point, to the capsule of the lens, but we could not make out whether
this adhesion was natural, or artificially produced by the coagulation of a
thin layer of albuminous matter. In one instance, at any rate, the adhesion
appeared firmer than could easily be produced artificially.
The arrangement of the vessels in the membrane is shewn diagrammatically in
Plate 38, fig. 49, while the characteristic form of the capillary plexus is
represented in Plate 38, fig. 50.
The arterial supply appears to be derived from a vessel perforating the
retina close to the optic nerve, and obviously homologous with the artery
of the processus falciformis and pecten of Teleostei and Birds, and with
the arteria centralis retinæ of Mammals. From this vessel branches diverge
and pursue a course towards the periphery. They give off numerous branches,
the blood from which enters a capillary plexus (Plate 38, figs. 49 and 50)
and is collected again by veins, which pass outwards and finally bend over
and fall into (Plate 38, fig. 49) a circular vein (_cr.v._) placed at the
outer edge of the retina along the insertion of the iris (_ir_). The
terminal branches of some of the main arteries appear also to fall directly
into this vein.
The membrane supporting the vessels just described is composed of a
transparent matrix, in which numerous cells are embedded (Plate 38,
fig. 50).
_Development._--In the account of the first stages of development of
_Lepidosteus_, the mode of formation of the optic cup, the lens, &c., have
been described (vide Plates 35 and 36, figs. 23, 26, 35). With reference to
the later stages in the development of the eye, the only subject with which
we propose to deal is the growth of the mesoblastic processes which enter
the cavity of the vitreous humour through the choroid slit.
_Lepidosteus_ is very remarkable for the great number of mesoblast cells
which thus enter the cavity of the vitreous humour, and for the fact that
these cells are _at first unaccompanied by any vascular structures_ (Plate
37, fig. 43, _v.h_). The mesoblast cells are scattered through the
vitreous humour, and there can be no doubt that during early larval life,
at a period however when the larva is certainly able to see, every
histologist would consider the vitreous humour to be a tissue formed of
scattered cells, with a large amount of intercellular substance; and the
fact that it is so appears to us to demonstrate that Kessler's view of the
vitreous humour being a mere transudation is not tenable.
In the larva five or six days after hatching, and about 15 millims. in
length, the choroid slit is open for its whole length. The edges of the
slit near the lens are folded, so as to form a ridge projecting into the
cavity of the vitreous humour, while nearer the insertion of the optic
nerve they cease to exhibit any such structure. The mesoblast, though it
projects between the lips of the ridge near the lens, only extends through
the choroid slit into the cavity of the vitreous humour in the
neighbourhood of the optic nerve. Here it forms a lamina with a thickened
edge, from which scattered cells in the cavity of the vitreous humour seem
to radiate.
At a slightly later stage than that just described, blood-vessels become
developed within the cavity of the vitreous humour, and form the vascular
membrane already described in the adult, placed close to the layer of
nerve-fibres of the retina, but separated from this layer by the hyaloid
membrane (Plate 38, fig. 48, _v.sh._). The artery bringing the blood to the
above vascular membrane is bound up in the same sheath as the optic nerve,
and passes through the choroid slit very close to the optic nerve. Its
entrance into the cavity of the vitreous humour is shewn in Plate 38,
fig. 48 (_vs._); its relation to the optic nerve in Plate 37, fig. 46, C
and D (_vs._).
The above sheath has, so far as we know, its nearest analogue in the eye of
_Alytes_, where, however, it is only found in the larva.
The reader who will take the trouble to refer to the account of the
imperfectly-developed processus falciformis of the Elasmobranch eye in the
treatise _On Comparative Embryology_, by one of us[520], will not fail to
recognize that the folds of the retina at the sides of the choroid slit,
and the mesoblastic process passing through this slit, are strikingly
similar in _Lepidosteus_ and Elasmobranchii; and that, if we are justified
in holding them to be an imperfectly-developed processus falciformis in the
one case, we are equally so in the other.
Footnote 520: Vol. II. p. 414 [the original edition].
Johannes Müller mentions the absence of a processus falciformis as one of
the features distinguishing Ganoids and Teleostei. So far as the systematic
separation of the two groups is concerned, he is probably perfectly
justified in this course; but it is interesting to notice that both in
Ganoids and Elasmobranchii we have traces of a structure which undergoes a
very special development in the Teleostei, and that the processus
falciformis of Teleostei is therefore to be regarded, not as an organ
peculiar to them, but as the peculiar modification within the group of a
primitive Vertebrate organ.
SUCTORIAL DISC.
One of the most remarkable organs of the larval _Lepidosteus_ is the
suctorial disc, placed at the front end of the head, to which we have made
numerous allusions in the first section of this memoir.
The external features of the disc have been fully dealt with by Agassiz,
and he also explained its function by observations on the habits of the
larva. We have already quoted (p. 755) a passage from Agassiz' memoir
shewing how the young Fishes use the disc to attach themselves firmly to
any convenient object. The discs appear in fact to be highly efficient
organs of attachment, in that the young Fish can remain suspended by them
to the sides of the jar, even after the water has been lowered below the
level at which they are attached.
The disc is formed two or three days before hatching, and from Agassiz'
statements, it appears to come into use immediately the young Fish is
liberated from the egg membranes.
We have examined the histological structure of the disc at various ages of
its growth, and may refer the reader to Plate 34, figs. 11 and 13, and
Plate 37, figs. 40 and 44. The result of our examination has been to shew
that the disc is provided with a series of papillæ often exhibiting a
bilateral arrangement. The papillæ are mainly constituted of highly
modified cells of the mucous layer of the epidermis. These cells have the
form of elongated columns, the nucleus being placed at the base, and the
main mass of the cells being filled with a protoplasmic reticulum. They may
probably be regarded as modified mucous cells. In the mesoblast adjoining
the suctorial disc there are numerous sinus-like vascular channels.
It does not appear probable that the disc has a true sucking action. It is
unprovided with muscular elements, and there appears to be no mechanism by
which it could act as a sucking organ. We must suppose, therefore, that its
adhesive power depends upon the capacity of the cells composing its papillæ
to pour out a sticky secretion.
MUSCULAR SYSTEM.
There is a peculiarity in the muscular system of _Lepidosteus_, which so
far as we know has not been previously noticed. It is that the lateral
muscles of each side are not divided, either in the region of the trunk or
of the tail, into a dorso-lateral and ventro-lateral division.
This peculiarity is equally characteristic of the older larvæ as of the
adult, and is shewn in Plate 41, figs. 67, 72, and 73, and Plate 42, figs.
74-76. In the Cyclostomata the lateral muscles are not divided into dorsal
and ventral sections; but except in this group such a division has been
hitherto considered as invariable amongst Fishes.
This character must, without doubt, be held to be the indication of a very
primitive arrangement of the muscular system. In the embryos of all Fishes
with the usual type of the lateral muscles, the undivided condition of the
muscles precedes the divided condition; and in primitive forms such as the
Cyclostomata and Amphioxus the embryonic condition is retained, as it is in
_Lepidosteus_.
SKELETON.
PART I.--_Vertebral column and ribs of the adult._
A typical vertebra from the trunk of _Lepidosteus_ has the following
characters (Plate 42, figs. 80 and 81).
The centrum is slightly narrower in the middle than at its two extremities.
It articulates with adjacent vertebræ by a convex face in front and a
concave face behind, being thus, according to Owen's nomenclature,
opisthocoelous. It presents on its under surface a well-marked longitudinal
ridge, which in many vertebræ is only united at its two extremities with
the main body of the vertebra.
From the lateral borders of the centrum there project, at a point slightly
nearer the front than the hind end, a pair of prominent hæmal processes
(_h.a._), to the ends of which are articulated the ribs. These processes
have a nearly horizontal direction in the greater part of the trunk, though
bent downwards in the tail.
The neural arches (_n.a._) have a somewhat complicated form. They are
mainly composed of two vertical plates, the breadth of the basal parts of
which is nearly as great as the length of the vertebræ, so that
comparatively narrow spaces are left between the neural arches of
successive vertebræ for the passage of the spinal nerves. Some little way
from its dorsal extremity each neural arch sends a horizontal process
inwards, which meets its fellow and so forms a roof for the spinal canal.
These processes appear to be confined to the posterior parts of the
vertebræ, so that at the front ends of the vertebræ, and in the spaces
between them, the neural canal is without an osseous roof. Above the level
of this osseous roof there is a narrow passage, bounded laterally by the
dorsal extremities of the neural plates. This passage is mainly filled up
by a series of cartilaginous elements (Plate 42, figs. 80 and 81, _i.c._)
(probably fibro-cartilage), which rest upon the roof of the neural canal.
Each element is situated _intervertebrally_, its anterior end being wedged
in between the two dorsal processes of the neural arch of the vertebra in
front, and its posterior end extending for some distance over the vertebra
behind. The successive elements are connected by fibrous tissue, and are
continuous dorsally with a fibrous band, known as the ligamentum
longitudinale superius (Plate 42, figs. 80 and 81, _l.l._), characteristic
of Fishes generally, and running continuously for the whole length of the
vertebral column. Each of the cartilaginous elements is, as will be
afterwards shewn, developed as two independent pieces of cartilage, and
might be compared with the dorsal element which usually forms the keystone
of the neural arch in Elasmobranchii, were not the latter vertebral instead
of intervertebral in position. More or less similar elements are described
by Götte in the neural arches of many Teleostei, which also, however,
appear to be vertebrally placed, and he has compared them and the
corresponding elements in the Sturgeon with the Elasmobranch cartilages
forming the keystone of the neural arch. Götte does not, however, appear to
have distinguished between the cartilaginous elements, and the osseous
elements forming the roof of the spinal canal, which are true membrane
bones; it is probable that the two are not so clearly separated in other
types as in _Lepidosteus_.
The posterior ends of the neural plates of the neural arches are continued
into the dorsal processes directed obliquely upwards and backwards, which
have been somewhat unfortunately described by Stannius as rib-like
projections of the neural arch. The dorsal processes of the two sides do
not meet, but between them is placed a median free spinous element, also
directed obliquely upwards and backwards, which forms a kind of roof for
the groove in which the cartilaginous elements and the ligamentum
longitudinale are placed.
The vertebræ are wholly formed of a very cellular osseous tissue, in which
a distinction between the bases of the neural and hæmal processes and the
remainder of the vertebra is not recognizable. The bodies of the vertebræ
are, moreover, directly continuous with the neural and hæmal arches.
The ribs in the region of the trunk are articulated to the ends of the long
hæmal processes. They envelop the body-cavity, their proximal parts being
placed immediately outside the peritoneal membrane, along the bases of the
intermuscular septa. Their distal ends do not, however, remain close to the
peritoneal membrane, _but pass outwards along the intermuscular septa till
their free ends come into very close proximity with the skin_. This
peculiarity, which holds good in the adult for all the free ribs, is shewn
in one of the anterior ribs of an advanced larva in Plate 41, fig. 72
(_rb._). We are not aware that this has been previously noticed, but it
appears to us to be a point not without interest in all questions which
concern the homology of rib-like structures occupying different positions
in relation to the muscles. Its bearings are fully dealt with in the
section of this paper devoted to the consideration of the homologies of the
ribs in Fishes.
As regards the behaviour of the ribs in the transitional region between the
trunk and the tail, we cannot do better than translate the description
given by Gegenbaur of this region (No. 6, p. 411):--"Up to the 34th
vertebra the ribs borne by the laterally and posteriorly directed processes
present nothing remarkable, though they have gradually become shorter. The
ribs of the 35th vertebra exhibit a slight curvature outwards of their free
ends, a peculiarity still more marked in the 36th. The last named pair of
ribs converge somewhat in their descent backwards so that both ribs
decidedly approach before bending outwards. The 37th vertebra is no longer
provided with freely terminating ribs, but on the contrary, the same pair
of processes which in front was provided with ribs, bears a short forked
process as the hæmal arch. _The two, up to this point separated ribs, have
here formed a hæmal arch by the fusion of their lower ends, which arch is
movable just like the ribs, and, like them, is attached to the vertebral
column._"
In the region of the tail-fin the hæmal arches supporting the caudal
fin-rays are very much enlarged.
PART II.--_Development of the vertebral column and ribs._
The first development and early histological changes of the notochord have
already been given, and we may take up the history of the vertebral column
at a period when the notochord forms a large circular rod, whose cells are
already highly vacuolated, while the septa between the vacuoles form a
delicate wide-meshed reticulum. Surrounding the notochord is the usual
cuticular sheath, which is still thin.
The first indications of the future vertebral column are to be found in the
formation of a distinct mesoblastic investment of the notochord. On the
dorsal aspect of the notochord, the mesoblast forms two ridges, one on each
side, which are prolonged upwards so as to meet above the neural canal, for
which they form a kind of sheath. On the ventral side of the notochord
there are also two ridges, which are, however, except on the tail, much
less prominent than the dorsal ridges.
The changes which next ensue are practically identical with those which
take place in Teleostei. Around the cuticular sheath of the notochord there
is formed an elastic membrane--the membrana elastica externa. At the same
time the basal parts of the dorsal, or as we may perhaps more conveniently
call them, the neural ridges of the notochord become enlarged at each
intermuscular septum, and the tissue of these enlargements soon becomes
converted into cartilage, thus forming a series of independent paired
neural processes riding on the membrana elastica externa surrounding the
notochord, and extending about two-thirds of the way up the sides of the
medullary cord. They are shewn in transverse section in Plate 41, fig. 67
(_n.a._), and in a side view in fig. 68 (_n.a._).
Simultaneously with the neural arches, the hæmal arches also become
established, and arise by the formation of similar enlargements of the
ventral or hæmal ridges. In the trunk they are very small, but in the
region of the tail their condition is very different. At the front end of
the anal fin the paired hæmal arches suddenly enlarge and extend
ventralwards (Plate 41, fig. 67, _h.a._).
Each succeeding pair of arches becomes larger than the one in front, and
the two elements of each arch first nearly meet below the caudal vein
(Plate 41, fig. 67) and finally actually do so, forming in this way a
completely closed hæmal canal. At the point where they first meet the
permanent caudal fin commences, and here (Plate 41, fig. 68) we find that
not only do the hæmal arches meet and coalesce below the caudal vein, but
they are actually produced into long spines supporting the fin-rays of the
caudal fin, which thus differs from the other fins in being supported by
parts of the true vertebral column and not by independently formed elements
of the skeleton.
Each of the large caudal hæmal arches, including the spine, forms a
continuous whole, and arises at an earlier period of larval life than any
other part of the vertebral column. We noticed the first indications of the
neural arches in the larva of about a week old, while they are converted
into fully formed cartilage in the larva of three weeks.
The neural and hæmal arches, resting on the membrana elastica externa, do
not at this early stage in the least constrict the notochord. They grow
gradually more definite, till the larva is five or six weeks old and about
26 millims. in length, but otherwise for a long time undergo no important
changes. During the same period, however, the true sheath of the notochord
greatly increases in thickness, and the membrana elastica externa becomes
more definite. So far it would be impossible to distinguish the development
of the vertebral column of _Lepidosteus_ from that of a Teleostean Fish.
Of the stages immediately following we have unfortunately had no examples,
but we have been fortunate enough to obtain some young specimens of
_Lepidosteus_[521], which have enabled us to work out with tolerable
completeness the remainder of the developmental history of the vertebral
column. In the next oldest larva, of about 5.5 centims., the changes which
have taken place are already sufficient to differentiate the vertebral
column of _Lepidosteus_ from that of a Teleostean, and to shew how certain
of the characteristic features of the adult take their origin.
Footnote 521: These specimens were given to us by Professor W.
K. Parker, who received them from Professor Burt G. Wilder.
In the notochord the most important and striking change consists in the
appearance of a series of very well marked vertebral constrictions
_opposite the insertions of the neural and hæmal arches_. The first
constrictions of the notochord are thus, as in other Fishes, vertebral; and
although, owing to the growth of the intervertebral cartilage, the
vertebral constrictions are subsequently replaced by intervertebral
constrictions, yet at the same time the primitive occurrence of vertebral
constrictions demonstrates that the vertebral column of _Lepidosteus_ is a
modification of a type of vertebral column with biconcave vertebræ.
The structure of the gelatinous body of the notochord has undergone no
important change. The sheath, however, exhibits certain features which
deserve careful description. In the first place the attention of the
observer is at once struck by the fact that, in the vertebral regions, the
sheath is much thicker (.014 millim.) than in the intervertebral (.005
millim.), and a careful examination of the sheath in longitudinal sections
shews that the thickening is due to the special differentiation of a
superficial part (Plate 41, fig. 69, _sh._) of the sheath in each vertebral
region. This part is somewhat granular as compared to the remainder,
especially in longitudinal sections. It forms a cylinder (the wall of which
is about .01 millim. thick) in each vertebral region, immediately within
the membrana elastica externa. Between it and the gelatinous tissue of the
notochord within there is a very thin unmodified portion of the sheath,
which is continuous with the thinner intervertebral parts of the sheath.
This part of the sheath is faintly, but at the same time distinctly,
concentrically striated--a probable indication of concentric fibres. The
inner unmodified layer of the sheath has the appearance in transverse
sections through the vertebral regions of an inner membrane, and may
perhaps be Kölliker's "membrana elastica interna."
We are not aware that any similar modification of the sheath has been
described in other forms.
The whole sheath is still invested by a very distinct membrana elastica
externa (_m.el_).
The changes which have taken place in the parts which form the permanent
vertebræ will be best understood from Plate 41, figs. 69-71. From the
transverse section (fig. 70) it will be seen that there are still neural
and hæmal arches resting upon the membrana elastica externa; but
longitudinal sections (fig. 69) shew that laterally these arches join a
cartilaginous tube, embracing the intervertebral regions of the notochord,
and continuous from one vertebra to the next.
It will be convenient to treat separately the neural arches, the hæmal
arches with their appendages, and the intervertebral cartilaginous rings.
The neural arches, except in the fact of embracing a relatively smaller
part of the neural tube than in the earlier stage, do not at first sight
appear to have undergone any changes. Viewed from the side, however, in
dissected specimens, they are seen to be prolonged upwards so as to unite
above with bars of cartilage directed obliquely backwards. An explanation
of this appearance is easily found in the sections. The cartilaginous
neural arches are invested by a delicate layer of homogeneous bone,
developed in the perichondrium, and this bone is prolonged beyond the
cartilage and joins a similar osseous investment of the dorsal bars above
mentioned. The whole of these parts may, it appears to us, be certainly
reckoned as parts of the neural arches, so that at this stage each neural
arch consists of: (1) a pair of basal portions resting on the notochord
consisting of cartilage invested by bone, (2) of a pair of dorsal
cartilaginous bars invested in bone (_n.a´._), and (3) of osseous bars
connecting (1) and (2).
Though, in the absence of the immediately preceding stages, it is not
perfectly certain that the dorsal pieces of cartilage are developed
independently of the ventral, there appears to us every probability that
this is so; and thus the cartilage of each neural arch is developed
discontinuously, while the permanent bony neural arch, which commences as a
deposit of bone partly in the perichondrium and partly in the intervening
membrane, forms a continuous structure.
Analogous occurrences have been described by Götte in Teleostei.
The dorsal portion of each neural arch becomes what we have called the
dorsal process of the adult arch.
Between the dorsal processes of the two sides there is placed a median rod
of cartilage (Plate 41, fig. 70, _i.s._), which in its development is
wholly independent of the true neural arches, and which constitutes the
median spinous element of the adult. In tracing these backwards it becomes
obvious that they are homologous with the interspinous elements supporting
the dorsal fin, in that they are replaced by these interspinous elements in
the region of the dorsal fin, and that the interspinous bones occupy the
same position as the median spinous processes. This homology was first
pointed out by Götte in the case of the Teleostei.
Immediately beneath this rod is placed the longitudinal ligament (Plate 41,
fig. 70, _l.l._), but there is as yet no trace of a junction between the
neural arches of the two sides in the space between the longitudinal
ligament and the spinal cord.
The basal parts of the neural arches of the two sides are united dorsally
by a thin cartilaginous layer resting on the sheath of the notochord, but
they are not united ventrally with the hæmal arches.
The hæmal processes in the trunk are much more prominent than in the
preceding stage, and their bases are united ventrally by a tolerably thick
layer of cartilage. In the trunk they are continuous with the so-called
ribs of the adult (Plate 41, fig. 70); but in order to study the nature of
these ribs it is necessary to trace the modifications undergone by the
hæmal arches in passing from the tail to the trunk.
It will be remembered that at an earlier stage the hæmal arches in the
region of the tail-fin were fully formed, and that through the anterior
part of the caudal region the hæmal processes were far advanced in
development, and just in front of the caudal fin had actually met below the
caudal vein.
The mode of development of the hæmal arches in the tail as _unjointed_
cartilaginous bars investing the caudal arteries and veins is so similar to
that of the caudal hæmal arches of Elasmobranchii, that it appears to us
impossible to doubt their identity in the two groups[522].
Footnote 522: Gegenbaur (No. 6) takes a different view on this
subject, as is clear from the following passage in this memoir
(pp. 369-370):--"Each vertebra of _Lepidosteus_ thus consists
of a section of the notochord, and of the cartilaginous tissue
surrounding its sheath, which gives origin to the upper arches
for the whole length of the vertebral column, and in the caudal
region to that of the lower arches also. _The latter do not
however complete the enclosure of a lower canal, but this is
effected by special independent elements_, which are to be
interpreted as homologues of the ribs." (The italics are ours.)
While we fully accept the homology between the ribs and the
lower elements of the hæmal arches of the tail, the view
expressed in the italicised section, to the effect that the
lower parts of the caudal arches are not true hæmal arches but
are independently formed elements, is entirely opposed to our
observations, and has we believe only arisen from the fact that
Gegenbaur had not the young larvæ to work with by which alone
this question could be settled.
The changes which have taken place by this stage with reference to the
hæmal arches of the tail are not very considerable.
In the case of a few more vertebræ the hæmal processes have united into an
arch, and the spinous processes of the arches in the region of the caudal
fin have grown considerably in length. A more important change is perhaps
the commencement of a segmentation of the distal parts of the hæmal arches
from the proximal. This process has not, however, as yet resulted in a
complete separation of the two, such as we find in the adult.
If the hæmal processes are traced forwards (Plate 42, figs. 75 and 76) from
the anterior segment where they meet ventrally, it will be found that each
hæmal process consists of a basal portion, adjoining the notochord, and a
peripheral portion. These two parts are completely continuous, but the line
of a future separation is indicated by the structure of the cartilage,
though not shewn in our figures. As the true body-cavity of the trunk
replaces the obliterated body-cavity of the caudal region, no break of
continuity will be found in the structure of the hæmal processes (Plates 41
and 42, figs. 73 and 74), but while the basal portions grow somewhat
larger, the peripheral portions gradually elongate and take the form of
delicate rods of cartilage extending ventralwards, on each side of the
body-cavity, immediately outside the peritoneal membrane, and along the
lines of insertion of the intermuscular septa. These rods obviously become
the ribs of the adult.
As one travels forwards the ribs become continually longer and more
important, and though they are at this stage united with the hæmal
processes in every part of the trunk, yet they are much more completely
separated from these processes in front than behind (Plate 41, fig. 72).
In front (Plate 41, fig. 72), each rib (_rb._), after continuing its
ventral course for some distance, immediately outside the peritoneal
membrane, turns outwards, and passes along one of the intermuscular septa
till it reaches the epidermis. This feature in the position of the ribs is,
as has been already pointed out in the anatomical part of this section,
characteristic of all the ribs of the adult.
It is unfortunate that we have had no specimens shewing the ribs at an
earlier stage of development; but it appears hardly open to doubt that _the
ribs are originally continuous with the hæmal processes_, and that the
indications of a separation between those two parts at this stage are not
due to a secondary fusion, but to a commencing segmentation.
It further appears, as Müller, Gegenbaur and others have stated, that the
ribs and hæmal processes of the tail are serially homologous structures;
but that the view maintained by Götte in his very valuable memoirs on the
Vertebrate skeleton is also correct to the effect that _the hæmal arches of
the tail are homologous throughout the series of Fishes_.
To this subject we shall return again at the end of the section.
Before leaving the hæmal arches it may be mentioned that behind the region
of the ventral caudal fin the two hæmal processes merge into one, and form
an unpaired knob resting on the ventral side of the notochord, and not
perforated by a canal.
There are now present well-developed intervertebral rings of cartilage,
each of which eventually becomes divided into two parts, and converted into
the adjacent faces of the contiguous vertebræ. These rings are united with
the neural and hæmal arches of the vertebræ in front and behind.
Each ring, as shewn by the transverse section (Plate 41, fig. 71), is not
uniformly thick, but exhibits four projections, two dorsal and two ventral.
These four projections are continuous with the bases of the neural and
hæmal arches of the adjacent vertebræ, and afford presumptive evidence of
the derivation of the intervertebral rings from the neural and hæmal
arches; in that had they so originated, it would be natural to anticipate
the presence of four thickenings indicating the four points from which the
cartilage had spread, while if the rings had originated independently, it
would not be easy to give any explanation of the presence of such
thickenings. Gegenbaur (No. 6), from the investigation of a much older
larva than that we are now describing, also arrived at the conclusion that
the intervertebral cartilages were derived from the neural and hæmal
arches; but as doubts have been thrown upon this conclusion by Götte, and
as it obviously required further confirmation, we have considered it
important to attempt to settle this point. From the description given
above, it is clear that we have not, however, been able absolutely to trace
the origin of this cartilage, but at the same time we think that we have
adduced weighty evidence in corroboration of Gegenbaur's view.
As shewn in longitudinal section (Plate 41, fig. 69, _iv.r._), the
intervertebral rings are thicker in the middle than at the two ends. In
this thickened middle part the division of the cartilage into two parts to
form the ends of two contiguous vertebræ is subsequently effected. The
curved line which this segmentation will follow is, however, already marked
out, and from surface views it might be supposed that this division had
actually occurred.
The histological structure of the intervertebral cartilage is very distinct
from that of the cartilage of the bases of the arches, the nuclei being
much more closely packed. In parts, indeed, the intervertebral cartilage
has almost the character of fibro-cartilage. On each side of the line of
division separating two vertebræ it is invested by a superficial osseous
deposit.
The next oldest larva we have had was 11 centims. in length. The
filamentous dorsal lobe of the caudal fin still projected far beyond the
permanent caudal fin (Plate 34, fig. 16).
The vertebral column was considerably less advanced in development than
that dissected by Gegenbaur, though it shews a great advance on the
previous stage. Its features are illustrated by two transverse sections,
one through the median plane of a vertebral region (Plate 42, fig. 78) and
the other through that of an intervertebral region (Plate 42, fig. 79), and
by a horizontal section (Plate 42, fig. 77).
In the last stage the notochord was only constricted vertebrally. Now,
however, by the great growth of intervertebral cartilage there have
appeared (Plate 42, fig. 77) very well-marked _intervertebral_
constrictions, by the completion of which the vertebræ of _Lepidosteus_
acquire their unique character amongst Fishes.
These constrictions still, however, coexist with the earlier, though at
this stage relatively less conspicuous, vertebral constrictions.
The gelatinous body of the notochord retains its earlier condition. The
sheath has, however, undergone some changes. In the vertebral regions there
is present in any section of the sheath--(1) externally, the membrana
elastica externa (_m.el._); then (2) the external layer of the sheath
(_sh._), which is, however, less thick than before, and exhibits a very
faint form of radial striation; and (3) internally, a fairly thick and
concentrically striated layer. The whole thickness is, on an average, 0.18
millim.
In the intervertebral regions the membrana elastica externa is still
present in most parts, but has become absorbed at the posterior border of
each vertebra, as shewn in longitudinal section in Plate 42, fig. 77. It is
considerably puckered transversely. The sheath of the notochord within the
membrana elastica externa is formed of a concentrically striated layer,
continuous with the innermost layer of the sheath in the vertebral regions.
It is puckered longitudinally. Thus, curiously enough, the membrana
elastica externa and the sheath of the notochord in the intervertebral
regions are folded in different directions, the folds of the one being only
visible in transverse sections (Plate 42, fig. 79), and those of the other
in longitudinal sections (Plate 42, fig. 77).
The osseous and cartilaginous structures investing the notochord may
conveniently be dealt with in the same order as before, viz.: the neural
arches, the hæmal arches, and the intervertebral cartilages.
The cartilaginous portions of the neural arches are still unossified, and
form (Plate 42, fig. 78, _n.a._) small wedge-shaped masses resting on the
sheath of the notochord. They are invested by a thick layer of bone
prolonged upwards to meet the dorsal processes (_n.a´._), which are still
formed of cartilage invested by bone.
It will be remembered that in the last stage there was no key-stone closing
in the neural arch above. This deficiency is now however supplied, and
consists of (1) two bars of cartilage repeated for each vertebra, but
intervertebrally placed, which are directly differentiated from the
ligamentum longitudinale superius, into which they merge above; and (2) two
osseous plates placed on the outer sides of these cartilages, which are
continuous with the lateral osseous bars of the neural arch. The former of
these elements gives rise to the cartilaginous elements above the osseous
bridge of the neural arch in the adult. The two osseous plates supporting
these cartilages clearly form what we have called in our description of the
adult the osseous roof of the spinal canal.
A comparison of the neural arch at this stage with the arch in the adult,
and in the stage last described, shews that the greater part of the neural
arch of the adult is formed of membrane-bone, there being preformed in
cartilage only a small basal part, a dorsal process, and paired key-stones
below the ligamentum longitudinale superius.
The hæmal arches (Plate 42, fig. 78) are still largely cartilaginous, and
rest upon the sheath of the notochord. They are invested by a thick layer
of bone. The bony layer investing the neural and hæmal arches is prolonged
to form a continuous investment round the vertebral portions of the
notochord (Plate 42, fig. 78). This investment is at the sides prolonged
outwards into irregular processes (Plate 42, fig. 78), which form the
commencement of the outer part of the thick but cellular osseous cylinder
forming the middle part of the vertebral body.
The intervertebral cartilages are much larger than in the earlier stage
(Plate 42, figs. 77 and 79), and it is by their growth that the
intervertebral constrictions of the notochord are produced. They have
ceased to be continuous with the cartilage of the arches, the intervening
portion of the vertebral body between the two being only formed of bone.
They are not yet divided into two masses to form the contiguous ends of
adjacent vertebræ.
Externally, the part of each cartilage which will form the hinder end of a
vertebral body is covered by a tube of bone, having the form of a truncated
funnel, shewn in longitudinal section in Plate 42, fig. 77, and in
transverse section in Plate 42, fig. 79.
At each end, the intervertebral cartilages are becoming penetrated and
replaced by beautiful branched processes from the homogeneous bone which
was first of all formed in the perichondrium (Plate 42, fig. 77).
This constitutes the latest stage which we have had.
Gegenbaur (No. 6) has described the vertebral column in a somewhat older
larva of 18 centims.
The chief points in which the vertebral column of this larva differed from
ours are: (1) the disappearance of all trace of the primitive vertebral
constriction of the notochord; (2) the nearly completed constriction of the
notochord in the intervertebral regions; (3) the complete ossification of
the vertebral portions of the bodies of the vertebræ, the terminal
so-called intervertebral portions alone remaining cartilaginous; (4) the
complete ossification of the basal portions of the hæmal and neural
processes included within the bodies of the vertebræ, so that in the case
of the neural arch all trace of the fact that the greater part was
originally not formed in cartilage had become lost. The cartilage of the
dorsal spinous processes was, however, still persistent.
The only points which remain obscure in the later history of the vertebral
column are the history of the notochord and of its sheath. We do not know
how far these are either simply absorbed or partially or wholly ossified.
Götte in his memoir on the formation of the vertebral bodies of the
Teleostei attempts to prove (1) that the so-called membrana elastica
externa of the Teleostei is not a homogeneous elastica, but is formed of
cells, and (2) that in the vertebral regions ossification first occurs in
it.
In _Lepidosteus_ we have met with no indication that the membrana elastica
externa is composed of cells; though it is fair to Götte to state that we
have not examined such isolated portions of it as he states are necessary
in order to make out its structure. But further than this we have satisfied
ourselves that during the earlier stage of ossification this membrane is
not ossified, and indeed in part becomes absorbed in proximity to the
intervertebral cartilages; and Gegenbaur met with no ossification of this
membrane in the later stage described by him.
_Summary of the development of the vertebral column and ribs._
A mesoblastic investment is early formed round the notochord, which is
produced into two dorsal and two ventral ridges, the former uniting above
the neural canal. Around the cuticular sheath of the notochord an elastic
membrane, the membrana elastica externa, is next developed. The neural
ridges become enlarged at each inter-muscular septum, and these
enlargements soon become converted into cartilage, thus forming a series of
neural processes riding on the membrana elastica externa, and extending
about two-thirds of the way up the sides of the neural canal. The hæmal
processes arise simultaneously with, and in the same manner as, the neural.
They are small in the trunk, but at the front end of the anal fin they
suddenly enlarge and extend ventralwards. Each succeeding pair of hæmal
arches becomes larger than the one in front, each arch finally meeting its
fellow below the caudal vein, thus forming a completely closed hæmal canal.
These arches are moreover produced into long spines supporting the fin-rays
of the caudal fin, which thus differs from the other unpaired fins in being
supported by parts of the vertebral column, and not by separately formed
skeletal elements.
In the next stage which we have had the opportunity of studying (larva of
5-1/2 centims.), a series of very well-marked _vertebral_ constrictions are
to be seen in the notochord. The sheath is now much thicker in the
vertebral than in the intervertebral regions: this is due to a special
differentiation of a superficial part of the sheath, which appears more
granular than the remainder. This granular part of the sheath thus forms a
cylinder in each vertebral region. Between it and the gelatinous tissue of
the notochord there remains a thin unmodified portion of the sheath, which
is continuous with the intervertebral parts of the sheath. The neural and
hæmal arches are seen to be continuous with a cartilaginous tube embracing
the intervertebral regions of the notochord, and continuous from one
vertebra to the next. A delicate layer of bone, developed in the
perichondrium, invests the cartilaginous neural arches, and this bone grows
upwards so as to unite above with the osseous investment of separately
developed bars of cartilage, which are directed obliquely backwards. These
bars, or dorsal processes, may be reckoned as parts of the neural arches.
Between the dorsal processes of the two sides is placed a median rod of
cartilage, which is developed separately from the true neural arches, and
which constitutes the median spinous element of the adult. Immediately
below this rod is placed the ligamentum longitudinale superius. There is
now a commencement of separation between the dorsal and ventral parts of
the hæmal arches, not only in the tail, but also in the trunk, where they
pass ventralwards on each side of the body-cavity, immediately outside the
peritoneal membrane, along the lines of insertion of the intermuscular
septa. These are obviously the ribs of the adult, and there is no break of
continuity of structure between the hæmal processes of the tail and the
ribs. In the anterior part of the trunk the ribs pass outwards along the
intermuscular septa till they reach the epidermis. Thus the ribs are
originally continuous with the hæmal processes. Behind the region of the
ventral caudal fin the two hæmal processes merge into one, which is not
perforated by a canal.
Each of the intervertebral rings of cartilage becomes eventually divided
into two parts, and converted into the adjacent faces of contiguous
vertebræ, the curved line where this will be effected being plainly marked
out. These rings are united with the neural and hæmal arches of the
vertebræ next in front and behind. As these rings are formed originally by
the spreading of the cartilage from the primitive neural and hæmal
processes, the intervertebral cartilages are clearly derived from the
neural and hæmal arches. The intervertebral cartilages are thicker in the
middle than at their two ends.
In our latest stage (11 centims.), the vertebral constrictions of the
notochord are rendered much less conspicuous by the growth of the
intervertebral cartilages giving rise to marked intervertebral
constrictions. In the intervertebral regions the membrana elastica externa
has become aborted at the posterior border of each vertebra, and the
remaining part is considerably puckered transversely. The inner sheath of
the notochord is puckered longitudinally in the intervertebral regions. The
granular external layer of the sheath in the vertebral regions is less
thick than in the last stage, and exhibits faint radial striations.
Two closely approximated cartilaginous elements now form a key-stone to the
neural arch above: these are directly differentiated from the ligamentum
longitudinale superius, into which they merge above. An osseous plate is
formed on the outer side of each of these cartilages. These plates are
continuous with the lateral osseous bars of the neural arches, and also
give rise to the osseous roof of the spinal canal of the adult.
Thus the greater part of the neural arches is formed of membrane bone. The
hæmal arches are invested by a thick layer of bone, and there is also a
continuous osseous investment round the vertebral portions of the
notochord. The intervertebral cartilages become penetrated by branched
processes of bone.
_Comparison of the vertebral column of Lepidosteus with that of
other forms._
The peculiar form of the articulatory faces of the vertebræ of
_Lepidosteus_ caused L. Agassiz (No. 2) to compare them with the vertebræ
of Reptiles, and subsequent anatomists have suggested that they more nearly
resemble the vertebræ of some Urodelous Amphibia than those of any other
form.
If, however, Götte's account of the formation of the amphibian vertebræ is
correct, there are serious objections to a comparison between the vertebræ
of _Lepidosteus_ and Amphibia on developmental grounds. The essential point
of similarity supposed to exist between them consists in the fact that in
both there is a great development of intervertebral cartilage which
constricts the notochord intervertebrally, and forms the articular faces of
contiguous vertebræ.
In _Lepidosteus_ this cartilage is, as we have seen, derived from the bases
of the arches; but in Amphibia it is held by Götte to be formed by a
special thickening of a cellular sheath round the notochord which is
probably homologous with the cartilaginous sheath of the notochord of
Elasmobranchii, and therefore with part of the notochordal sheath placed
within the membrana elastica externa.
If the above statements with reference to the origin of the intervertebral
cartilage in the two types are true, it is clear that no homology can exist
between structures so differently developed. Provisionally, therefore, we
must look elsewhere than in _Lepidosteus_ for the origin of the amphibian
type of vertebræ.
The researches which we have recorded demonstrate, however, in a very
conclusive manner that the vertebræ of _Lepidosteus_ have very close
affinities with those of Teleostei.
In support of this statement we may point: (1) To the structure of the
sheath of the notochord; (2) to the formation of the greater part of the
bodies of the vertebræ from ossification in membrane around the notochord;
(3) to the early biconcave form of the vertebræ, only masked at a later
period by the development of intervertebral cartilages; (4) to the
character of the neural arches.
This latter feature will be made very clear if the reader will compare our
figures of the sections of later vertebræ (Plate 42, fig. 78) with
Götte's[523] figure of the section of the vertebra of a Pike (Plate 7,
fig. 1). In Götte's figure there are shewn similar intercalated pieces of
cartilage to those which we have found, and similar cartilaginous dorsal
processes of the vertebræ. Thus we are justified in holding that whether or
no the opisthocoelous form of the vertebræ of _Lepidosteus_ is a
commencement of a type of vertebræ inherited by the higher forms, yet in
any case the vertebræ are essentially built on the type which has become
inherited by the Teleostei from the bony Ganoids.
Footnote 523: "Beiträge zur vergl. Morphol. d. Skeletsystems
d. Wirbelthiere." _Archiv f. Mikr. Anat._ Vol. XVI. 1879.
PART III.--_The ribs of Fishes._
The nature and homologies of the ribs of Fishes have long been a matter of
controversy; but the subject has recently been brought forward in the
important memoirs of Götte[524] on the Vertebrate skeleton. The
alternatives usually adopted are, roughly speaking, these:--Either the
hæmal arches of the tail are homologous throughout the piscine series,
while the ribs of Ganoids and Teleostei are not homologous with those of
Elasmobranchii; or the ribs are homologous in all the piscine groups, and
the hæmal arches in the tail are differently formed in the different types.
Götte has brought forward a great body of evidence in favour of the first
view; while Gegenbaur[525] may be regarded as more especially the champion
of the second view.
Footnote 524: "Beiträge z. vergl. Morph. d. Skeletsystems d.
Wirbelthiere. II. Die Wirbelsäule u. ihre Anhänge." _Archiv f.
Mikr. Anat._, Vol. XV., 1878, and Vol. XVI., 1879.
Footnote 525: "Ueb. d. Entwick. d. Wirbelsäule d. Lepidosteus,
mit. vergl. Anat. Bemerkungen." _Jenaische Zeitschrift_,
Bd. III., 1863.
One of us held in a recent publication[526] that the question was not yet
settled, though the view that the ribs are homologous throughout the series
was provisionally accepted.
Footnote 526: _Comparative Embryology_, Vol. II., pp. 462, 463
[the original edition].
It is admitted by both Gegenbaur and Götte that in _Lepidosteus_ the ribs,
in the transition from the trunk to the tail, bend inwards, and finally
unite in the region of the tail to form the ventral parts of the hæmal
arches, and our researches have abundantly confirmed this conclusion.
Are the hæmal arches, the ventral parts of which are thus formed by the
coalescence of the ribs, homologous with the hæmal arches in
Elasmobranchii? The researches recorded in the preceding pages appear to us
to demonstrate in a conclusive manner that they are so.
The development of the hæmal arches in the tail in these two groups is
practically identical; they are formed in both as simple elongations of the
primitive hæmal processes, which meet below the caudal vein. In the adult
there is an apparent difference between them, arising from the fact that in
_Lepidosteus_ the peripheral parts of the hæmal processes are only
articulated with the basal portions, and not, as in Elasmobranchii,
continuous with them. This difference does not, however, exist in the early
larva, since in the larval _Lepidosteus_ the hæmal arches of the tail are
unsegmented cartilaginous arches, as they permanently are in
Elasmobranchii. If, however, the homology between the hæmal arches of the
two types should still be doubted, the fact that in both types the hæmal
arches are similarly modified to support the fin-rays of the ventral lobe
of the caudal fin, while in neither type are they modified to support the
anal fin, may be pointed out as a very strong argument in confirmation of
their homology.
The demonstration of the homology of the hæmal arches of the tail in
_Lepidosteus_ and Elasmobranchii might at first sight be taken as a
conclusive argument in favour of Götte's view, that the ribs of
Elasmobranchii are not homologous with those of Ganoidei. This view is
mainly supported by two facts:--
(1) In the first place, the ribs in Elasmobranchii do not at first sight
appear to be serially homologous with the ventral parts of the hæmal arches
of the tail, but would rather seem to be lateral offshoots of the hæmal
processes, while the hæmal arches of the tail appear to be completed by the
coalescence of independent ventral prolongations of the hæmal processes.
(2) In the second place, the position of the ribs is different in the two
groups. In Elasmobranchii they are situated between the dorso-lateral and
ventro-lateral muscles (woodcut, fig. 1, _rb._), while in _Lepidosteus_ and
other Ganoids they immediately girth the body-cavity.
[Illustration: FIG. 1.
Diagrammatic section through the trunk of an advanced embryo of _Scyllium_,
to shew the position of the ribs.
_ao._, aorta; _c.sh._, cartilaginous notochordal sheath; _cv._, cardinal
vein; _hp._, hæmal process; _k._, kidney; _l.s._, ligamentum longitudinale
superius; _m.el._, membrana elastica externa; _na._, neural arch; _no._,
notochord; _ll._, lateral line; _rb._, rib; _sp.c._, spinal cord.]
There is much, therefore, to be said in favour of Götte's view. At the same
time, there is another possible interpretation of the facts which would
admit the homology of the ribs as well as of the hæmal arches throughout
the Pisces.
Let us suppose, to start with, that the primitive arrangement of the parts
is more or less nearly that found in _Lepidosteus_, where we have
well-developed ribs in the region of the trunk, girthing the body-cavity,
and uniting in the caudal region to form the ventral parts of the hæmal
arches. It is easy to conceive that the ribs in the trunk might somewhat
alter their position by passing into the muscles, along the inter-muscular
septa, till they come to lie between the dorso-lateral and ventro-lateral
muscles, as in Elasmobranchii. _Lepidosteus_ itself affords a proof that
such a change in the position of the ribs is not impossible, in that it
differs from other Ganoids and from Teleostei in the fact that the free
ends of the ribs leave the neighbourhood of the body-cavity and penetrate
into the muscles.
If it be granted that the mere difference in position between the ribs of
Ganoids and Elasmobranchii is not of itself sufficient to disprove their
homology, let us attempt to picture what would take place at the junction
of the trunk and tail in a type in which the ribs had undergone the above
change in position. On nearing the tail it may be supposed that the ribs
would gradually become shorter, and at the same time alter their position,
till finally they shaded off into ordinary hæmal processes. If, however,
the hæmal canal became prolonged forwards by the formation of some
additional complete or nearly complete hæmal arches, an alteration in the
relation of the parts would necessarily take place. Owing to the position
of the ribs, these structures could hardly assist in the new formation of
the anterior part of the hæmal canal, but the continuation forwards of the
canal would be effected by prolongations of the hæmal processes supporting
the ribs. The new arches so formed would naturally be held to be homologous
with the hæmal arches of the tail, though really not so, while the true
nature of the ribs would also be liable to be misinterpreted, in that the
ribs would appear to be lateral outgrowths of the hæmal processes of a
wholly different nature to the ventral parts of the hæmal arches of the
tail.
In some Elasmobranchii, as shewn in the accompanying woodcut (fig. 2), in
the transitional vertebræ between the trunk and the tail, the ribs are
supported by lateral outgrowths of the hæmal processes, while the wholly
independent prolongations of the hæmal processes appear to be about to give
rise to the hæmal arches of the tail.
This peculiar state of things led Götte, and subsequently one of us, to
deny for Elasmobranchii all homology between the ribs and any part of the
hæmal arches of the tail; but in view of the explanation just suggested,
this denial was perhaps too hasty.
[Illustration: FIG. 2.
Transverse section through the ventral part of the notochord, and adjoining
structures of an advanced _Scyllium_ embryo at the root of the tail.
_Vb._, cartilaginous sheath of the notochord; _ha._, hæmal process; _r.p._,
process to which the rib is articulated; _m.el._, membrana elastica
externa; _ch._, notochord; _ao._, aorta; _V.cau._, caudal vein.]
We are the more inclined to take this view because the researches of Götte
appear to shew that an occurrence, in many respects analogous, has taken
place in some Teleostei.
In Teleostei, Johannes Müller, and following him Gegenbaur, do not admit
that the hæmal arches of the tail are in any part formed by the ribs.
Gegenbaur (_Elements of Comp. Anat._, translation, p. 431) says, "In the
Teleostei, the costiferous transverse processes" (what we have called the
hæmal processes) "gradually converge in the caudal region, and form
inferior arches, which are not homologous with those of Selachii and
Ganoidei, although they also form spinous processes."
The opposite view, that the hæmal arches of the tail in Teleostei contain
parts serially homologous with the basal parts of the hæmal processes as
well as with the ribs, has been also maintained by many anatomists, _e.g._,
Meckel, Aug. Müller, &c., and has recently found a powerful ally in Götte.
In many cases, the relations of the parts appear to be fundamentally those
found in _Lepidosteus_ and _Amia_, and Götte has shewn by his careful
embryological investigations on _Esox_ and _Anguilla_, that in these two
forms there is practically conclusive evidence that the ribs as well as the
hæmal costiferous processes of Gegenbaur, which support them, enter into
the formation of the hæmal arches of the tail.
In a great number of Teleostei, _e.g._, the Salmon and most Cyprinoids,
&c., the hæmal arches in the region of transition from the trunk to the
tail have a structure which at first sight appears to support Johannes
Müller's and Gegenbaur's view. The hæmal processes grow larger and meet
each other ventrally; while the ribs articulated to them gradually grow
smaller and disappear.
The Salmon is typical in this respect, and has been carefully studied by
Götte, who attempts to shew (with, in our opinion, complete success) that
the anterior hæmal arches are really not entirely homologous with the true
hæmal arches behind, but that in the latter, the closure of the arch below
is effected by the hæmal spine, which is serially homologous with a pair of
coalesced ribs, while in the anterior hæmal arches, _i.e._, those of the
trunk, the closure of the arch is effected by a bridge of bone uniting the
hæmal processes.
The arrangement of the parts just described, as well as the view of Götte
with reference to them, will be best understood from the accompanying
woodcut (fig. 3), copied from Götte's memoir.
Götte sums up his own results on this point in the following words (p.
138): "It follows from this, that the half rings, forming the hæmal canal
in the hindermost trunk vertebræ of the Salmon, are not (with the exception
of the last) completely homologous with those of the tail, but are formed
by a connecting piece between the basal stumps (hæmal processes), which
originates as a paired median process of these stumps."
The incomplete homology between the anterior hæmal arches and the true
caudal hæmal arches which follow them is exactly what we suggest may be the
case in Elasmobranchii, and if it be admitted in the one case, we see no
reason why it should not also be admitted in the other.
[Illustration: FIG. 3.
Semi-diagrammatic transverse sections through the first caudal vertebra
(A), the last trunk vertebra (B), and the two trunk vertebræ in front (C
and D), of a Salmon embryo of 2-3 centims. (From Götte.)
_ub._, hæmal arch; _ub´._, hæmal process; _ub´´._, rib; _c._, notochord;
_a._, aorta; _v._, vein; _h._, connecting pieces between hæmal processes;
_u._, kidney; _d._, intestine; _sp´._, hæmal spine; _m´._, muscles.]
If this admission is made, the only ground for not regarding the ribs of
Elasmobranchii as homologous with those of Ganoids is their different
position, and we have already attempted to prove that this is not a
fundamental point.
The results of our researches appear to us, then, to leave two alternatives
as to the ribs of Fishes. One of these, which may be called Götte's view,
may be thus stated:--The hæmal arches are homologous throughout the Pisces:
in Teleostei, Ganoidei, and Dipnoi[527], the ribs, placed on the inner face
of the body-wall, are serially homologous with the ventral parts of the
hæmal arches of the tail; in Elasmobranchii, on the other hand, the ribs
are neither serially homologous with the hæmal arches of the tail nor
homologous with the ribs of Teleostei and Ganoidei, but are outgrowths of
the hæmal processes into the space between the dorso-lateral and
ventro-lateral muscles, which may perhaps have their homologues in
Teleostei and Ganoids in certain accessory processes of the vertebræ.
Footnote 527: We find the serial homology of the ribs and
ventral parts of the hæmal arches to be very clear in
_Ceratodus_. Wiedersheim states that it is not clear in
_Protopterus_, although he holds that the facts are in favour
of this view.
The other view, which we are inclined to adopt, and the arguments for which
have been stated in the preceding pages, is as follows:--The Teleostei,
Ganoidei, Dipnoi, and Elasmobranchii are provided with homologous hæmal
arches, which are formed by the coalescence below the caudal vein of simple
prolongations of the primitive hæmal processes of the embryo. The canal
enclosed by the hæmal arches can be demonstrated embryologically to be the
aborted body-cavity.
In the region of the trunk the hæmal processes and their prolongations
behave somewhat differently in the different types.
In Ganoids and Dipnoi, in which the most primitive arrangement is probably
retained, the ribs are attached to the hæmal processes, and are placed
immediately without the peritoneal membrane at the insertions of the
intermuscular septa. These ribs are in many instances (_Lepidosteus_,
_Acipenser_), and very probably in all, developed continuously with the
hæmal processes, and become subsequently segmented from them. They are
serially homologous with the ventral parts of the hæmal arches of the tail,
which, like them, are in many instances (_Ceratodus_, _Lepidosteus_,
_Polypterus_, and to some extent in _Amia_) segmented off from the basal
parts of the hæmal arches.
In Teleostei the ribs have the same position and relations as those in
Ganoids and Dipnoi, but their serial homology with the ventral parts of the
hæmal processes of the tail, is often (_e.g._, the Salmon) obscured by some
of the anterior hæmal arches in the posterior part of the trunk being
completed, not by the ribs, but by independent outgrowths of the basal
parts of the hæmal processes.
In Elasmobranchii a still further divergence from the primitive arrangement
is present. The ribs appear to have passed outwards along the intermuscular
septa into the muscles, and are placed between the dorso-lateral and
ventro-lateral muscles (a change of position of the ribs of the same
nature, but affecting only their ends, is observable in _Lepidosteus_).
This change of position, combined probably with the secondary formation of
a certain number of anterior hæmal arches similar to those in the Salmon,
renders their serial homology with the ventral parts of the hæmal processes
of the tail far less clear than in other types, and further proof is
required before such homology can be considered as definitely established.
This is not the place to enter into the obscure question as to how far the
ribs of the Amphibia and Amniota are homologous with those of Fishes. It is
to be remarked, however, that the ribs of the Urodela (1) occupy the same
position in relation to the muscles as the Elasmobranch ribs, (2) that they
are connected with the neural arches, and (3) that they coexist in the tail
with the hæmal arches, and seem, therefore, to be as different as possible
from the ribs of the Dipnoi.
PART IV.--_The skeleton of the ventral lobe of the tail fin, and its
bearing on the nature of the tail fin of the various types of Pisces._
In the embryos or larvæ of all the Elasmobranchii, Ganoidei, and Teleostei
which have up to this time been studied, the unpaired fins arise as median
longitudinal folds of the integument on the dorsal and ventral sides of the
body, which meet at the apex of the tail. The tail at first is symmetrical,
having a form which has been called diphycercal or protocercal. At a later
stage, usually, though not always, parts of these fins atrophy, while other
parts undergo a special development and constitute the permanent unpaired
fins.
Since the majority of existing as well as extinct Fishes are provided with
discontinuous fins, those forms, such as the Eel (_Anguilla_), in which the
fins are continuous, have probably reverted to an embryonic condition: an
evolutional process which is of more frequent occurrence than has usually
been admitted.
In the caudal region there is almost always developed in the larvæ of the
above groups a special ventral lobe of the embryonic fin a short distance
from the end of the tail. In Elasmobranchii and Chondrostean Ganoids the
portion of the embryonic tail behind this lobe persists through life, and a
special type of caudal fin, which is usually called heterocercal, is thus
produced. This type of caudal fin appears to have been the most usual in
the earlier geological periods.
Simultaneously with the formation of the ventral lobe of the heterocercal
caudal fin, the notochord with the vertebral tissues surrounding it,
becomes bent somewhat dorsalwards, and thus the primitive caudal fin forms
a dorsally directed lobe of the heterocercal tail. We shall call this part
the dorsal lobe of the tail-fin, and the secondarily formed lobe the
ventral lobe.
_Lepidosteus_ and _Amia_ (Wilder, No. 15) amongst the bony Ganoids, and, as
has recently been shewn by A. Agassiz[528], most Teleostei acquire at an
early stage of their development heterocercal caudal fins, like those of
Elasmobranchii and the Chondrostean Ganoids; but in the course of their
further growth the dorsal lobe partly atrophies, and partly disappears as
such, owing to the great prominence acquired by the ventral lobe. A portion
of the dorsally flexed notochord and of the cartilage or bone replacing or
investing it remains, however, as an indication of the original dorsal
lobe, though it does not project backwards beyond the level of the end of
the ventral lobe, which in these types forms the terminal caudal fin.
Footnote 528: "On the Young Stages of some Osseous Fishes.--I.
The Development of the Tail," _Proc. of the American Academy of
Arts and Sciences_, Vol. XIII., 1877.
The true significance of the dorsally flexed portion of the vertebral axis
was first clearly stated by Huxley[529], but as A. Agassiz has fairly
pointed out in the paper already quoted, this fact does not in any way
militate against the view put forward by L. Agassiz that there is a
complete parallelism between the embryonic development of the tail in these
Fishes and the palæontological development of this organ. We think that it
is moreover convenient to retain the term homocercal for those types of
caudal fin in which the dorsal lobe has atrophied so far as not to project
beyond the ventral lobe.
Footnote 529: "Observations on the Development of some Parts
of the Skeleton of Fishes," _Quart. Journ. of Micr. Science_,
Vol. VII., 1859.
We have stated these now well-known facts to enable the reader to follow us
in dealing with the comparison between the skeleton supporting the fin-rays
of the ventral lobe of the caudal fin, and that supporting the fin-rays of
the remaining unpaired fins.
It has been shewn that in _Lepidosteus_ the unpaired fins fall into two
categories, according to the nature of the skeletal parts supporting them.
The fin-rays of the true ventral lobe of the caudal fin are supported by
the spinous processes of certain of the hæmal arches. The remaining
unpaired fins, including the anal fin, are supported by the so-called
interspinous bones, which are developed independently of the vertebral
column and its arches.
The question which first presents itself is, how far does this distinction
hold good for other Fishes? This question, though interesting, does not
appear to have been greatly discussed by anatomists. Not unfrequently the
skeletal supports of the ventral lobe of the caudal fin are assumed to be
the same as those of the other fins.
Davidoff[530], for instance, in speaking of the unpaired fins of
Elasmobranch embryos, says (p. 514): "The cartilaginous rays of the dorsal
fins agreed not only in number with the spinous processes (as indeed is
also found in the caudal fin of the full-grown Dog-fish)," &c.
Footnote 530: "Beiträge z. vergl. Anat. d. hinteren
Gliedmassen d. Fische," _Morph. Jahrbuch_, Vol. V., 1879.
Thacker[531], again, in his memoir on the Median and Paired Fins, states at
p. 284: "We shall here consider the skeleton of the dorsal and anal fins
alone. That of the caudal fin has undergone peculiar modifications by the
union of fin-rays with hæmal spines."
Footnote 531: _Trans. of the Connecticut Acad._, Vol. III.,
1877.
Mivart[532] goes into the question more fully. He points out (p. 471) that
there is an essential difference between the dorsal and ventral parts of
the caudal fin in Elasmobranchii, in that in the former the radials are
more numerous than the vertebræ and unconformable to them, while in the
latter they are equal in number to the vertebræ and continuous with them.
"This," he goes on to say, "seems to point to a difference in nature
between the dorsal and ventral portions of the caudal fin, in at least most
Elasmobranchii." He further points out that _Polyodon_ resembles
Elasmobranchii. As to Teleostei, he does not express himself decidedly
except in the case of _Muræna_, to which we shall return.
Footnote 532: St George Mivart, "Fins of Elasmobranchii,"
_Zool. Trans._, Vol. X.
Mivart expresses himself as very doubtful as to the nature of the supports
of the caudal fin, and thinks "that the caudal fin of different kinds of
Fishes may have arisen in different ways in different cases."
An examination of the ventral part of the caudal fin in various Ganoids,
Teleostei, and Elasmobranchii appears to us to shew that there can be but
little doubt that, in the majority of the members of these groups at any
rate, and we believe in all, the same distinction between the ventral lobe
of the caudal fin and the remaining unpaired fins is found as in
_Lepidosteus_.
In the case of most Elasmobranchii, a simple inspection of the caudal fin
suffices to prove this, and the anatomical features involved in this fact
have usually been recognized; though, in the absence of embryological
evidence, the legitimate conclusion has not always been drawn from them.
The difference between the ventral lobe of the caudal fin and the other
fins in the mode in which the fin-rays are supported is as obvious in
Chondrostean Ganoids as it is in Elasmobranchii; it would appear also to
hold good for _Amia_. _Polypterus_ we have had no opportunity of examining,
but if, as there is no reason to doubt, the figure of its skeleton given by
Agassiz (_Poissons Fossiles_) is correct, there can be no question that the
ventral lobe of the caudal fin is supported by the hæmal arches, and not by
interspinous bones. In _Calamoicthys_, the tail of which we have had an
opportunity of dissecting through the kindness of Professor Parker, the
fin-rays of the ventral lobe of the true caudal fin are undoubtedly
supported by true hæmal arches.
There is no unanimity of opinion as to the nature of the elements
supporting the fin-rays of the caudal fin of Teleostei.
Huxley[533] in his paper on the development of the caudal fin of the
Stickleback, holds that these elements are of the nature of interhæmal
bones. He says (p. 39): "The last of these rings lay just where the
notochord began to bend up. It was slightly longer than the bony ring which
preceded it, and instead of having its posterior margin parallel with the
anterior, it sloped from above downwards and backwards. Two short osseous
plates, attached to the anterior part of the inferior surface of the
penultimate ring, or rudimentary vertebral centrum, passed downwards and a
little backwards, and abutted against a slender elongated mass of
cartilage. Similar cartilaginous bodies occupy the same relation to
corresponding plates of bone in the anterior vertebræ in the region of the
anal fin; and it is here seen, that while the bony plates coalesce and form
the inferior arches of the caudal vertebræ, the cartilaginous elements at
their extremities become the interhæmal bones. The cartilage connected with
the inferior arch of the penultimate centrum is therefore an "interhæmal"
cartilage. The anterior part of the inferior surface of the terminal
ossification likewise has its osseous inferior arch, but the direction of
this is nearly vertical, and though it is connected below with an element
which corresponds in position with the interhæmal cartilage, this cartilage
is five or six times as large, and constitutes a broad vertical plate,
longer than it is deep, and having its longest axis inclined downwards and
backwards....
"Immediately behind and above this anterior hypural apophysis (as it
may be termed) is another very much smaller vertical cartilaginous
plate, which may be called the posterior hypural apophysis."
Footnote 533: "Observations on the Development of some parts
of the Skeleton of Fishes," _Quart. Journ. Micr. Science_,
Vol. VII., 1859.
We have seen that Mivart expresses himself doubtful on the subject.
Gegenbaur[534] appears to regard them as hæmal arches.
Footnote 534: _Elements of Comparative Anatomy._
(Translation), p. 431.
The latter view appears to us without doubt the correct one. An examination
of the tail of normal Teleostei shews that the fin-rays of that part of the
caudal fin which is derived from the ventral lobe of the larva are
supported by elements serially homologous with the hæmal arches, but in no
way homologous with the interspinous bones of the anal fin. The elements in
question formed of cartilage in the larva, become ossified in the adult,
and are known as the hypural bones. They may appear in the form of a series
of separate hæmal arches, corresponding in number with the primitive
somites of this region, which usually, however, atrophy in the adult, or
more often are from the first imperfectly segmented, and have in the adult
the form of two or three or even of a single broad bony plate. The
transitional forms between this state of things and that, for instance, in
_Lepidosteus_ are so numerous, that there can be no doubt that even the
most peculiar forms of the hypural bones of Teleostei are simply modified
hæmal arches.
This view of the hypural bones is, moreover, supported by embryological
evidence, since Aug. Müller[535] (p. 205) describes their development in a
manner which, if his statements are to be trusted, leaves no doubt on this
point.
Footnote 535: "Beobachtungen zur vergl. Anat. d. Wirbelsäule,"
Müller's _Archiv_, 1853.
There are a considerable number of Fishes which are not provided with an
obvious caudal fin as distinct from the remaining unpaired fins, _i.e._
Chimæra, Eels, and various Eel-like forms amongst Teleostei, and the
Dipnoi. Gegenbaur appears to hold that these Fishes ought to be classed
together in relation to the structure of the caudal portion of their
vertebral column, as he says on p. 431 of his _Comparative Anatomy_
(English Translation): "In the Chimæræ, Dipnoi, and many Teleostei, the
caudal portion of the vertebral column ends by gradually diminishing in
size, but in most Fishes, &c."
For our purpose it will, however, be advisable to treat them separately.
The tail of Chimæra appears to us to be simply a peculiar modification of
the typical Elasmobranch heterocercal tail, in which the true ventral lobe
of the caudal fin may be recognized in the fin-fold immediately in front of
the filamentous portion of the tail. In the allied genus _Callorhynchus_
this feature is more distinct. The filamentous portion of the tail of
Chimæra constitutes, according to the nomenclature adopted above, the true
dorsal lobe, and may be partially paralleled in the filamentous dorsal lobe
of the tail of the larval _Lepidosteus_ (Plate 34, fig. 16).
The tail of the eel-like Teleostei is again undoubtedly a modification of
the normal form of tail characteristic of the Teleostei, in which, however,
the caudal fin has become very much reduced and merged into the
prolongations of the anal and dorsal fins.
This can be very clearly seen in Siluroid forms with an Eel-like tail, such
as _Cnidoglanis_. Although the dorsal and ventral fins appear to be
continuous round the end of the tail, and there is superficially no
distinct caudal fin, yet an examination of the skeleton of _Cnidoglanis_
shews that the end of the vertebral column is modified in the usual
Teleostean fashion, and that the hæmal arches of the modified portion of
the vertebral column support a small number of fin-rays; the adjoining
ventral fin-rays being supported by independent osseous fin-supports
(interspinous bones).
In the case of the Eel (_Anguilla anguilla_) Huxley (_loc. cit._) long ago
pointed out that the terminal portion of the vertebral column was modified
in an analogous fashion to that of other Teleostei, and we have found that
the modified hæmal arches of this part support a few fin-rays, though a
still smaller number than in _Cnidoglanis_. The fin-rays so supported
clearly constitute an aborted ventral lobe of the caudal fin.
Under these circumstances we think that the following statement by Mivart
(_Zool. Trans._ Vol. X., p. 471) is somewhat misleading:--
"As to the condition of this part (_i.e._ the ventral lobe of the
tail-fin) in Teleosteans generally, I will not venture as yet to say
anything generally, _except that it is plain that in such forms as
Muræna, the dorsal and ventral parts of the caudal fin are similar in
nature and homotypal with ordinary dorsal and anal fins_[536]."
Footnote 536: The italics are ours.
The italicized portion of this sentence is only true in respect to that
part of the fringe of fin surrounding the end of the body, which is not
only homotypal with, but actually part of, the dorsal and anal fins.
Having settled, then, that the tails of Chimæra and of Eel-like Teleostei
are simply special modifications of the typical form of tail of the group
of Fishes to which they respectively belong, we come to the consideration
of the Dipnoi, in which the tail-fin presents problems of more interest and
greater difficulty than those we have so far had to deal with.
The undoubtedly very ancient and primitive character of the Dipnoi has led
to the view, implicitly if not definitely stated in most text-books, that
their tail-fin retains the character of the piscine tail prior to the
formation of the ventral caudal lobe, a stage which is repeated
embryologically in the pre-heterocercal condition of the tail in ordinary
Fishes.
Through the want of embryological data, and in the absence of really
careful histological examination of the tail of any of the Dipnoi, we are
not willing to speak with very great confidence as to its nature; we are
nevertheless of the opinion that the facts we can bring forward on this
head are sufficient to shew that the tail of the existing Dipnoi is largely
aborted, so that it is more or less comparable with that of the Eel.
We have had opportunities of examining the structure of the tail of
_Ceratodus_ and _Protopterus_ in dissected specimens in the Cambridge
Museum. The vertebral axis runs to the ends of the tail without shewing any
signs of becoming dorsally flexed. At some distance from the end of the
tail the fin-rays are supported by what are apparently segmented spinous
prolongations of the neural and hæmal arches. The dorsal elements are
placed above the longitudinal dorsal cord, and occupy therefore the same
position as the independent elements of the neural arches of _Lepidosteus_.
They are therefore to be regarded as homologous with the dorsal
fin-supports or interspinous bones of other types. The corresponding
ventral elements are therefore also to be regarded as interspinous bones.
In view of the fact that the fin-supports, whenever their development has
been observed, are found to be formed independently of the neural and hæmal
arches, we may fairly assume that this is also true for what we have
identified as the interspinous elements in the Dipnoi.
The interspinous elements become gradually shorter as the end of the tail
is approached, and it is very difficult from a simple examination of
dissected specimens to make out how far any of the posterior fin-rays are
supported by the hæmal arches only. To this question we shall return, but
we may remark that, although there is a prolongation backwards of the
vertebral axis beyond the last interspinous elements, composed it would
seem of the coalesced neural and hæmal arches but without the notochord,
yet by far the majority of the fin-rays which constitute the apparent
caudal fin are supported by interspinous elements.
The grounds on which we hold that the tail of the Dipnoi is to be regarded
as a degenerate rather than primitive type of tail are the following:--
(1) If it be granted that a diphycercal or protocercal form of tail must
have preceded a heterocercal form, it is also clear that the ventral
fin-rays of such a tail must have been supported, as in _Polypterus_ and
_Calamoicthys_, by hæmal arches, and not by interspinous elements;
otherwise, a special ventral lobe, giving a heterocercal character to the
tail, and provided with fin-rays supported only by hæmal arches, could
never have become evolved from the protocercal tail-fin. Since the ventral
fin-rays of the tail of the Dipnoi are supported by interspinous elements
and not by hæmal arches, this tail-fin cannot claim to have the character
of _that_ primitive type of diphycercal or protocercal tail from which the
heterocercal tail must be supposed to have been evolved.
(2) Since the nearest allies of the Dipnoi are to be found in _Polypterus_
and the Crossopterygidæ of Huxley, and since in these forms (as evinced by
the structure of the tail-fin of _Polypterus_, and the transitional type
between a heterocercal and diphycercal form of fin observable in fossil
Crossopterygidæ) the ventral fin-rays of the caudal fin were clearly
supported by hæmal arches and not by interspinous elements, it is rendered
highly probable that the absence of fin-rays so supported in the Dipnoi is
a result of degeneration of the posterior part of the tail.
[We use this argument without offering any opinion as to whether the
diphycercal character of the tail of many Crossopterygidæ is primary or
secondary.]
(3) The argument just used is supported by the degenerate and variable
state of the end of the vertebral axis in the Dipnoi--a condition most
easily explained by assuming that the terminal part of the tail has become
aborted.
(4) We believe that in _Ceratodus_ we have been able to trace a small
number of the ventral fin-rays supported by hæmal arches only, but these
rays are so short as not to extend so far back as some of the rays attached
to the interspinous elements in front. These rays may probably be
interpreted, like the more or less corresponding rays in the tail of the
Eel, as the last remnant of a true caudal fin.
The above considerations appear to us to shew with very considerable
probability that the true caudal fin of the Dipnoi has become all but
aborted like that of various Teleostei; and that the apparent caudal fin is
formed by the anal and dorsal fins meeting round the end of the stump of
the tail.
From the adult forms of Dipnoi we are, however, of opinion that no
conclusion can be drawn as to whether their ancestors were provided with a
diphycercal or a heterocercal form of caudal fin.
The general conclusions with reference to the tail-fin at which we have
arrived are the following:--
(1) The ventral lobe of the tail-fin of Pisces differs from the other
unpaired fins in the fact that its fin-rays are directly supported by
spinous processes of certain of the hæmal arches instead of independently
developed interspinous bones.
(2) The presence or absence of fin-rays in the tail-fin supported by hæmal
arches may be used in deciding whether apparently diphycercal tail-fins are
aborted or primitive.
EXCRETORY AND GENERATIVE ORGANS.
I.--_Anatomy._
The excretory organs of _Lepidosteus_ have been described by Müller (No.
13) and Hyrtl (No. 11). These anatomists have given a fairly adequate
account of the generative ducts in the female, and Hyrtl has also described
the male generative ducts and the kidney and its duct, but his description
is contradicted by our observations in some of the most fundamental points.
In the female example of 100.5 centims. which we dissected, the kidney
forms a paired gland, consisting of a narrow strip of glandular matter
placed on each side of the vertebral column, on the dorsal aspect of the
body-cavity. It is covered on its ventral aspect by the oviduct and by its
own duct, but is separated from both of these by a layer of the tough
peritoneal membrane, through which the collecting tubes pass. It extends
forwards from the anus for about three-fifths of the length of the
body-cavity, and in our example had a total length of about 28 centims.
(Plate 39, fig. 60, _k_). Anteriorly the two kidneys are separated by a
short interval in the median line, but posteriorly they come into contact,
and are so intimately united as almost to constitute a single gland.
A superficial examination might lead to the supposition that the kidney
extended forwards for the whole length of the body-cavity up to the region
of the branchial arches, and Hyrtl appears to have fallen into this error;
but what appears to be its anterior continuation is really a form of
lymphatic tissue, something like that of the spleen, filled with numerous
cells. This matter (Plate 39, fig. 60, _ly._) continues from the kidney
forwards without any break, and has a colour so similar to that of the
kidney as to be hardly distinguishable from it with the naked eye. The true
anterior end of the kidney is placed about 3 centims. in front on the left
side, and on the same level on the right side as the wide anterior end of
the generative duct (Plate 39, fig. 60, _od._). It is not obviously divided
into segments, and is richly supplied with malpighian bodies.
It is clear from the above description that there is no trace of
head-kidney or pronephros visible in the adult. To this subject we shall,
however, again return.
As will appear from the embryological section, the ducts of the kidneys are
probably simply the archinephric ducts, but to avoid the use of terms
involving a theory, we propose in the anatomical part of our work to call
them kidney ducts. They are thin-walled widish tubes coextensive with the
kidneys. If cut open there may be seen on their inner aspect the numerous
openings of the collecting tubes of the kidneys. They are placed ventrally
to and on the outer border of the kidneys (Plate 39, fig. 60, _s.g._).
Posteriorly they gradually enlarge, and approaching each other in the
median line, coalesce, forming an unpaired vesicle or bladder
(_bl._)--about 6 centims. long in our example--opening by a median pore on
a more or less prominent papilla (_u.g._) behind the anus. The dilated
portions of the two ducts are called by Hyrtl the horns of the bladder.
The sides of the bladder and its so-called horns are provided with lateral
pockets into which the collecting tubes of the kidney open. These pockets,
which we have found in two female examples, are much larger in the horns of
the bladder than in the bladder itself. Similar pockets, but larger than
those we have found, have been described by Hyrtl in the male, but are
stated by him to be absent in the female. It is clear from our examples
that this is by no means always the case.
Hyrtl states that the wide kidney ducts, of which his description differs
in no material point from our own, suddenly narrow in front, and,
perforating the peritoneal lining, are continued forwards to supply the
anterior part of the kidney. We have already shewn that the anterior part
of the kidney has no existence, and the kidney ducts supplying it are,
according to our investigations, equally imaginary.
It was first shewn by Müller, whose observations on this point have been
confirmed by Hyrtl, &c., that the ovaries of _Lepidosteus_ are continuous
with their ducts, forming in this respect an exception to other Ganoids.
In our example of _Lepidosteus_ the ovaries (Plate 39, fig. 60, _ov._) were
about 18 centims. in length. They have the form of simple sacks, filled
with ova, and attached about their middle to their generative duct, and
continued both backwards and forwards from their attachment into a blind
process.
With reference to these sacks Müller has pointed out--and the importance of
this observation will become apparent when we deal with the
development--that the ova are formed in the thickness of the inner wall of
the sack. We hope to shew that the inner wall of the sack is alone
equivalent to the genital ridge of, for instance, the ovary of _Scyllium_.
The outer aspect of this wall--_i.e._, that turned towards the interior of
the sack--is equivalent to the outer aspect of the Elasmobranch genital
ridge, on which alone the ova are developed[537]. The sack into which the
ova fall is, as we shall shew in the embryological section, a special
section of the body-cavity shut off from the remainder, and the dehiscence
of the ova into this cavity is equivalent to their discharge into the
body-cavity in other forms.
Footnote 537: _Treatise on Comparative Embryology_, Vol. I.,
p. 43 [the original edition].
The oviduct (Plate 39, fig. 60, _od._) is a thin-walled duct of about 21
centims. in length in the example we are describing, continuous in front
with the ovarian sack, and gradually tapering behind, till it ends (_od´._)
by opening into the dilated terminal section of the kidney duct on the
inner side, a short distance before the latter unites with its fellow. It
is throughout closely attached to the ureter and placed on its inner, and
to some extent on its ventral, aspect. The hindermost part of the oviduct
which runs beside the enlarged portion of the kidney duct--that portion
called by Hyrtl the horn of the urinary bladder--is so completely enveloped
by the wall of the horn of the urinary bladder as to appear like a
projection into the lumen of the latter structure, and the somewhat
peculiar appearance which it presents in Hyrtl's figure is due to this
fact. In our examples the oviduct was provided with a simple opening into
the kidney duct, on a slight papilla; the peculiar dilatations and
processes of the terminal parts of the oviduct, which have been described
by Hyrtl, not being present.
The results we have arrived at with reference to the male organs are very
different indeed from those of our predecessor, in that we find _the
testicular products to be carried off by a series of vasa efferentia, which
traverse the mesorchium, and are continuous with the uriniferous tubuli; so
that the semen passes through the uriniferous tubuli into the kidney duct
and so to the exterior. We have moreover been unable to find in the male a
duct homologous with the oviduct of the female._
This mode of transportation outwards of the semen has not hitherto been
known to occur in Ganoids, though found in all Elasmobranchii, Amphibia,
and Amniota. It is not, however, impossible that it exists in other
Ganoids, but has hitherto been overlooked.
Our male example of Lepidosteus was about 60 centims. in length, and was no
doubt mature. It was smaller than any of our female examples, but this
according to Garman (vide, p. 361) is usual. The testes (Plate 39,
fig. 58A., _t._) occupied a similar position to the ovaries, and were about
21 centims. long. They were, as is frequently the case with piscine testes,
divided into a series of lobes (10-12), and were suspended by a delicate
mesentery (mesorchium) from the dorsal wall of the abdomen on each side of
the dorsal aorta. Hyrtl (No. 11) states that air or quicksilver injected
between the limbs of the mesentery, passed into a vas deferens homologous
with the oviduct which joins the ureter. We have been unable to find such a
vas deferens; but we have found in the mesorchium a number of tubes of a
yellow colour, the colour being due to a granular substance quite unlike
coagulated blood, but which appeared to us from microscopic examination to
be the remains of spermatozoa[538]. These tubes to the number of 40-50
constitute, we believe, the vasa efferentia. Along the line of suspension
of the testis on its inner border these tubes unite to form an elaborate
network of tubes placed on the inner face of the testis--an arrangement
very similar to that often found in Elasmobranchii (vide F. M. Balfour,
_Monograph on the Development of Elasmobranch Fishes_, plate 20, figs. 4
and 8).
Footnote 538: The females we examined, which were no doubt
procured at the same time as the male, had their oviducts
filled with ova: and it is therefore not surprising that the
vasa efferentia should be naturally injected with sperm.
We have figured this network on the posterior lobe of the testi
(fig. 58B), and have represented a section through it (fig. 59A, _n.v.e._),
and through one of the vasa efferentia (_v.e._) in the mesorchium. Such a
section conclusively demonstrates the real nature of these passages: they
are filled with sperm like that in the body of the testis, and are, as may
be seen from the section figured, continuous with the seminal tubes of the
testis itself.
At the attached base of the mesorchium the vasa efferentia unite into a
longitudinal canal, placed on the inner side of the kidney duct (Plate 39,
fig. 58A, _l.c._, also shewn in section in Plate 39, fig. 59B, _l.c._).
From this canal tubules pass off which are continuous with the tubuli
uriniferi, as may be seen from fig. 59B, but the exact course of these
tubuli through the kidney could not be made out in the preparations we were
able to make of the badly conserved kidney. Hyrtl describes the arrangement
of the vascular trunks in the mesorchium in the following way (No. 11, p.
6): "The mesorchium contains vascular trunks, viz., veins, which through
their numerous anastomoses form a plexus at the hilus of the testis, whose
efferent trunks, 13 in number, again unite into a plexus on the vertebral
column, which is continuous with the cardinal veins." The arrangement
(though not the number) of Hyrtl's vessels is very similar to that of our
vasa efferentia, and we cannot help thinking that a confusion of the two
may have taken place; which, in badly conserved specimens, not injected
with semen, would be very easy.
We have, as already stated, been unable to find in our dissections any
trace of a duct homologous with the oviduct of the female, and our sections
through the kidney and its ducts equally fail to bring to light such a
duct. The kidney ducts are about 19 centims. in length, measured from the
genital aperture to their front end. These ducts are generally similar to
those in the female; they unite about 2 centims. from the genital pore to
form an unpaired vesicle. Their posterior parts are considerably enlarged,
forming what Hyrtl calls the horns of the urinary bladder. In these
enlarged portions, and in the wall of the unpaired urinary bladder,
numerous transverse partitions are present, as correctly described by
Hyrtl, which are similar to those in the female, but more numerous. They
give rise to a series of pits, at the blind ends of which are placed the
openings of the kidney tubules. The kidney duct without doubt serves as vas
deferens, and we have found in it masses of yellowish colour similar to the
substance in the vasa efferentia identified by us as remains of
spermatozoa.
II.--_Development._
In the general account of the development we have already called attention
to the earliest stages of the excretory system.
We may remind the reader that the first part of the system to be formed is
the segmental or archinephric duct (Plate 36, figs. 28 and 29, _sg._). This
duct arises, as in Teleostei and Amphibia, by the constriction of a hollow
ridge of the somatic mesoblast into a canal, which is placed in contiguity
with the epiblast, along the line of junction between the mesoblastic
somites and the lateral plates of mesoblast. Anteriorly the duct does not
become shut off from the body-cavity, and also bends inwards towards the
middle line. The inflected part of the duct is the first rudiment of the
pronephros, and very soon becomes considerably dilated relatively to the
posterior part of the duct.
The posterior part of each segmental duct acquires an opening into the
cloacal section of the alimentary tract. Apart from this change, the whole
of the ducts, except their pronephric sections, remain for a long time
unaltered, and the next changes we have to speak of concern the definite
establishment of the pronephros.
The dilated incurved portion of each segmental duct soon becomes
convoluted, and by the time the embryo is about 10 millims. in length, but
before the period of hatching, an important change is effected in the
relations of their peritoneal openings[539].
Footnote 539: The change is probably effected somewhat earlier
than would appear from our description, but our specimens were
not sufficiently well preserved to enable us to speak
definitely as to the exact period.
Instead of leading into the body-cavity, they open into an isolated chamber
on each side (Plate 38, fig. 51, _pr.c._), which we will call the
_pronephric chamber_. The pronephric chamber is not, however, so far as we
can judge, completely isolated from the body-cavity. We have not, it is
true, detected with certainty at this stage a communication between the
two; but in later stages, in larvæ of from 11 to 26 millims., we have found
a richly ciliated passage leading from the body-cavity into the pronephros
on each side (Plate 38, fig. 52, _p.f.p._). We have not succeeded in
determining with absolute certainty the exact relations between this
passage and the tube of the pronephros, but we are inclined to believe that
it opens directly into the pronephric chamber just spoken of.
As we hope to shew, this chamber soon becomes largely filled by a vascular
glomerulus. On the accomplishment of these changes, the pronephros is
essentially provided with all the parts typically present in a segment of
the mesonephros (woodcut, fig. 4). There is a peritoneal tube (_f_)[540],
opening into a vesicle (_v_); from near the neck of the peritoneal tube
there comes off a convoluted tube (_pr.n._), forming the main mass of the
pronephros, and ending in the segmental duct (_sd._).
Footnote 540: We feel fairly confident that there is only one
pronephric opening on each side, though we have no single
series of sections sufficiently complete to demonstrate this
fact with absolute certainty.
[Illustration: FIG. 4.
Diagrammatic views of the pronephros of _Lepidosteus_.
A, pronephros supposed to be isolated and seen from the side; B, section
through the vesicle of the pronephros and the ciliated peritoneal funnel
leading into it; _pr.n._, coiled tube of pronephros; _sd._, segmental or
archinephric duct; _f._, peritoneal funnel; _v._, vesicle of pronephros;
_bv._, blood vessel of glomerulus; _gl._, glomerulus.]
The different parts do not, however, appear to have the same morphological
significance as those in the mesonephros.
Judging from the analogy of Teleostei, the embryonic structure of whose
pronephros is strikingly similar to that of _Lepidosteus_, the two
pronephric chambers into which the segmental ducts open are constricted off
sections of the body-cavity.
With the formation of the convoluted duct opening into the isolated section
of the body-cavity we may speak of a definite pronephros as having become
established. The pronephros is placed, as can be made out in later stages,
on the level of the opening of the air-bladder into the throat.
The pronephros increases in size, so far as could be determined, by the
further convolution of the duct of which it is mainly formed; and the next
change of importance which we have noticed is the formation of a vascular
projection into the pronephric chamber, forming the glomerulus already
spoken of (vide woodcut, fig. 4, _gl._), which is similar to that of the
pronephros of Teleostei. We first detected these glomeruli in an embryo of
about 15 millims., some days after hatching (Plate 38, fig. 52, _gl._), but
it is quite possible that they may be formed considerably earlier.
In the same embryo in which the glomeruli were found we also detected for
the first time a _mesonephros_ consisting of a series of isolated segmental
or nephridial tubes, placed posteriorly to the pronephros along the dorsal
wall of the abdomen.
These were so far advanced at this stage that we are not in a position to
give any account of their mode of origin. They are, however, formed
independently of the segmental ducts, and in the establishment of the
junction between the two structures, there is no outgrowth from the
segmental duct to meet the segmental tubes. We could not at this stage find
peritoneal funnels of the segmental tubes, though we have met with them at
a later stage (Plate 38, fig. 53, _p.f._), and our failure to find them at
this stage is not to be regarded as conclusive against their existence.
A very considerable space exists between the pronephros and the foremost
segmental tube of the mesonephros. The anterior mesonephric tubes are,
moreover, formed earlier than the posterior.
In the course of further development, the mesonephric tubules increase in
size, so that there ceases to be an interval between them, the mesonephros
thus becoming a continuous gland. In an embryo of 26 millims. there was no
indication of the formation of segmental tubes to fill up the space between
the pronephros and mesonephros.
The two segmental ducts have united behind into an unpaired structure in an
embryo of 11 millims. This structure is no doubt the future unpaired
urinogenital chamber (Plate 39, figs. 58A, and 60, _bl._). Somewhat later,
the hypoblastic cloaca becomes split into two sections, the hinder one
receiving the coalesced segmental ducts, and the anterior remaining
continuous with the alimentary tract. The opening of the hinder one forms
the urinogenital opening, and that of the anterior the anus.
In an older larva of about 5.5 centims. the pronephros did not exhibit any
marked signs of atrophy, though the duct between it and the mesonephros was
somewhat reduced and surrounded by the trabecular tissue spoken of in
connection with the adult. In the region between the pronephros and the
front end of the fully developed part of the mesonephros very rudimentary
tubules had become established.
The latest stage of the excretory system which we have studied is in a
young Fish of about 11 centims. in length. The special interest of this
stage depends upon the fact that the ovary is already developed, and not
only so, but the formation of the oviducts has commenced, and their
condition at this stage throws considerable light on the obscure problem of
their nature in the Ganoids.
Unfortunately, the head of the young Fish had been removed before it was
put into our hands, so that it was impossible for us to determine whether
the pronephros was still present; but as we shall subsequently shew, the
section of the segmental duct, originally present between the pronephros
and the front end of the permanent kidney or mesonephros, has in any case
disappeared.
In addition to an examination of the excretory organs _in situ_, which
shewed little except the presence of the generative ridges, we made a
complete series of sections through the excretory organs for their whole
length (Plate 39, figs. 54-57).
Posteriorly these sections shewed nothing worthy of note, the excretory
organs and their ducts differing in no important particular from these
organs as we have described them in the adult, except in the fact that the
segmental ducts are not joined by the oviducts.
Some little way in front of the point where the two segmental ducts
coalesce to form the urinary bladder, the genital ridge comes into view.
For its whole extent, except near its anterior part (of which more
hereafter) this ridge projects freely into the body-cavity, and in this
respect the young Fish differs entirely from the adult. As shewn in Plate
39, figs. 56 and 57 (_g.r._), it is attached to the abdominal wall on the
ventral side of, and near the inner border of each kidney. The genital
ridge itself has a structure very similar to that which is characteristic
of young Elasmobranchii, and it may be presumed of young Fishes generally.
The free edge of the ridge is swollen, and this part constitutes the true
generative region of the ridge, while its dorsal portion forms the
supporting mesentery. The ridge itself is formed of a central stroma and a
germinal epithelium covering it. The epithelium is thin on the whole of the
inner aspect of the ridge, but, just as in Elasmobranchii, it becomes
greatly thickened for a band-like strip on the outer aspect. Here, the
epithelium is several layers deep, and contains numerous primitive germinal
cells (_p.o._).
Though the generative organs were not sufficiently advanced for us to
decide the point with certainty, the structure of the organ is in favour of
the view that this specimen was a female, and, as will be shewn directly,
there can on other grounds be no doubt that this is so. The large size of
the primitive germinal cells (primitive ova) reminded us of these bodies in
Elasmobranchii.
In the region between the insertion of the genital ridge (or ovary, as we
may more conveniently call it) and the segmental duct we detected the
openings of a series of peritoneal funnels of the excretory tubes (Plate
39, fig. 57, _p.f._), which clearly therefore persist till the young Fish
has reached a very considerable size.
As we have already said, the ovary projects freely into the body-cavity for
the greater part of its length. Anteriorly, however, we found that a lamina
extended from the free ventral edge of the ovary to the dorsal wall of the
body-cavity, to which it was attached on the level of the outer side of the
segmental duct. A somewhat triangular channel was thus constituted, the
inner wall of which was formed by the ovary, the outer by the lamina just
spoken of, and the roof by the strip of the peritoneum of the abdominal
wall covering that part of the ventral surface of the kidney in which the
openings of the peritoneal funnels of the excretory tubes are placed. The
structure of this canal will be at once understood by the section of it
shewn in Plate 39, fig. 55.
There can be no doubt that this canal is the commencing ovarian sack. On
tracing it backwards we found that the lamina forming its outer wall arises
as a fold growing upwards from the free edge of the genital ridge meeting a
downward growth of the peritoneal membrane from the dorsal wall of the
abdomen; and in Plate 39, fig. 56, these two laminæ may be seen before they
have met. Anteriorly the canal becomes gradually smaller and smaller in
correlation with the reduced size of the ovarian ridge, and ends blindly
nearly on a level with the front end of the excretory organs.
It should be noted that, owing to the mode of formation of the ovarian
sack, the outer side of the ovary with the band of thickened germinal
epithelium is turned towards the lumen of the sack; and thus the fact of
the ova being formed on the inner wall of the genital sack in the adult is
explained, and the comparison which we instituted in our description of the
adult between the inner wall of the genital sack and the free genital ridge
of Elasmobranchii receives its justification.
It is further to be noticed that, from the mode of formation of the ovarian
sack, the openings of the peritoneal funnels of the excretory organs ought
to open into its lumen; and if these openings persist in the adult, they
will no doubt be found in this situation.
Before entering on further theoretical considerations with reference to the
oviduct, it will be convenient to complete our description of the excretory
organs at this stage.
When we dissected the excretory organs out, and removed them from the body
of the young Fish, we were under the impression that they extended for the
whole length of the body-cavity. Great was our astonishment to find that
slightly in front of the end of the ovary both excretory organs and
segmental ducts grew rapidly smaller and finally vanished, and that what we
had taken to be the front part of the kidney was nothing else but a linear
streak of tissue formed of cells with peculiar granular contents supported
in a trabecular work (Plate 39, fig. 54). This discovery first led us to
investigate histologically what we, in common with previous observers, had
supposed to be the anterior end of the kidneys in the adult, and to shew
that they were nothing else but trabecular tissue with cells like that of
lymphatic glands. The interruption of the segmental duct at the
commencement of this tissue demonstrates that if any rudiment of the
pronephros still persists, it is quite functionless, in that it is not
provided with a duct.
III.--_Theoretical considerations._
There are three points in our observations on the urinogenital system which
appear to call for special remark. The first of these concerns the
structure and fate of the pronephros, the second the nature of the oviduct,
and the third the presence of vasa efferentia in the male.
Although the history we have been able to give of the pronephros is not
complete, we have nevertheless shewn that in most points it is essentially
similar to the pronephros of Teleostei. In an early stage we find the
pronephros provided with a peritoneal funnel opening into the body-cavity.
At a later stage we find that there is connected with the pronephros on
each side, a cavity--the pronephric cavity--into which a glomerulus
projects. This cavity is in communication on the one hand with the lumen of
the coiled tube which forms the main mass of the pronephros, and on the
other hand with the body-cavity by means of a richly ciliated canal
(woodcut, fig. 4, p. 817).
In Teleostei the pronephros has precisely the same characters, except that
the cavity in which the glomerulus is placed is without a peritoneal canal.
The questions which naturally arise in connection with the pronephros are:
(1) what is the origin of the above cavity with its glomerulus; and (2)
what is the meaning of the ciliated canal connecting this cavity with the
peritoneal cavity?
We have not from our researches been able to answer the first of these
questions. In Teleostei, however, the origin of this cavity has been
studied by Rosenberg[541] and Götte[542]. According to the account of the
latter, which we have not ourselves confirmed but which has usually been
accepted, the front end of the segmental duct, instead of becoming folded
off from the body-cavity, becomes included in a kind of diverticulum of the
body-cavity, which only communicates with the remainder of the body-cavity
by a narrow opening. On the inner wall of this diverticulum a projection is
formed which becomes a glomerulus. At this stage in the development of the
pronephros we have essentially the same parts as in the fully formed
pronephros of _Lepidosteus_, the only difference being that the passage
connecting the diverticulum containing the glomerulus with the remainder of
the body-cavity is short in Teleostei, and in _Lepidosteus_ forms a longish
ciliated canal. In Teleostei the opening into the body-cavity becomes soon
closed. If the above comparison is justified, and if the development of
these parts in _Lepidosteus_ takes place as it is described as doing in
Teleostei, there can, we think, be no doubt that the ciliated canal of
_Lepidosteus_, which connects the pronephric cavity with the body-cavity,
is a persisting communication between this cavity and the body-cavity; and
that _Lepidosteus_ presents in this respect a more primitive type of
pronephros than Teleostei.
Footnote 541: Rosenberg, _Untersuch. ueb. d. Entwick. d.
Teleostierniere_, Dorpat, 1867.
Footnote 542: Götte, _Entwick. d. Unke_, p. 826.
It may be noted that in _Lepidosteus_ the whole pronephros has exactly the
character of a single segmental tube of the mesonephros. The pronephric
cavity with its glomerulus is identical in structure with a malpighian
body. The ciliated canal is similar in its relations to the peritoneal
canal of such a segmental tube, and the coiled portion of the pronephros
resembles the secreting part of the ordinary segmental tube. This
comparison is no doubt an indication that the pronephros is physiologically
very similar to the mesonephros, and so far justifies Sedgwick's[543]
comparison between the two, but it does not appear to us to justify the
morphological conclusions at which he has arrived, or to necessitate any
modification in the views on this subject expressed by one of us[544].
Footnote 543: Sedgwick, "Early Development of the Wolffian
Duct and anterior Wolffian Tubules in the Chick; with some
Remarks on the Vertebrate Excretory System," _Quart. Journ. of
Micros. Science_, Vol. XXI., 1881.
Footnote 544: F. M. Balfour, _Comparative Embryology_,
Vol. II., pp. 600-603 [the original edition].
The genital ducts of Ganoids and Teleostei have for some time been a source
of great difficulty to morphologists; and any contributions with reference
to the ontogeny of these structures are of interest.
The essential point which we have made out is that the anterior part of the
oviduct of _Lepidosteus_ arises by a fold of the peritoneum attaching
itself to the free edge of the genital ridge. We have not, unfortunately,
had specimens old enough to decide how the posterior part of the oviduct is
formed; and although in the absence of such stages it would be rash in the
extreme to speak with confidence as to the nature of this part of the duct,
it may be well to consider the possibilities of the case in relation to
other Ganoids and Teleostei.
The simplest supposition would be that the posterior part of the genital
duct had the same origin as the anterior, _i.e._, that it was formed for
its whole length by the concrescence of a peritoneal fold with the genital
ridge, and that the duct so formed opened into the segmental duct.
The other possible supposition is that a true Müllerian duct--_i.e._, a
product of the splitting of the segmental duct--is subsequently developed,
and that the open end of this duct coalesces with the duct which has
already begun to be formed in our oldest larva.
In attempting to estimate the relative probability of these two views, one
important element is the relation of the oviducts of _Lepidosteus_ to those
of other Ganoids.
In all other Ganoids (vide Hyrtl, No. II) there are stated to be genital
ducts in both sexes which are provided at their anterior extremities with a
funnel-shaped mouth open to the abdominal cavity. At first sight,
therefore, it might be supposed that they had no morphological relationship
with the oviducts of _Lepidosteus_, but, apart from the presence of a
funnel-shaped mouth, the oviducts of _Lepidosteus_ are very similar to
those of Chondrostean Ganoids, being thin-walled tubes opening on a
projecting papilla into the dilated kidney ducts (horns of the urinary
bladder, Hyrtl). These relations seem to prove beyond a doubt that the
oviduct of _Lepidosteus_ is for its major part homologous with the genital
ducts of other Ganoids.
The relationship of the genital ducts to the kidney ducts in _Amia_ and
_Polypterus_ is somewhat different from that in the Chondrostei and
_Lepidosteus_. In _Amia_ the ureters are so small that they may be
described rather as joining the coalesced genital ducts than _vice versâ_,
although the apparent coalesced portion of the genital ducts is shewn to be
really part of the kidney ducts by receiving the secretion of a number of
mesonephric tubuli. In _Polypterus_ the two ureters are stated to unite,
and open by a common orifice into a sinus formed by the junction of the two
genital ducts, which has not been described as receiving directly the
secretion of any part of the mesonephros.
It has been usual to assume that the genital ducts of Ganoids are true
Müllerian ducts in the sense above defined, on the ground that they are
provided with a peritoneal opening and that they are united behind with the
kidney ducts. In the absence of ontological evidence this identification is
necessarily provisional. On the assumption that it is correct we should
have to accept the second of the two alternatives above suggested as to the
development of the posterior parts of the oviduct in _Lepidosteus_.
There appear to us, however, to be sufficiently serious objections to this
view to render it necessary for us to suspend our judgment with reference
to this point. In the first place, if the view that the genital ducts are
Müllerian ducts is correct, the true genital ducts of _Lepidosteus_ must
necessarily be developed at a later period than the secondary attachment
between their open mouths and the genital folds, which would, to say the
least of it, be a remarkable inversion of the natural order of development.
Secondly, the condition of our oldest larva shews that the Müllerian duct,
if developed later, is only split off from quite the posterior part of the
segmental duct; yet in all types in which the development of the Müllerian
duct has been followed, its anterior extremity, with the abdominal opening,
is split off from either the foremost or nearly the foremost part of the
segmental duct.
Judging from the structure of the adult genital ducts of other Ganoids they
must also be developed only from the posterior part of the segmental duct,
and this peculiarity so struck one of us that in a previous paper[545] the
suggestion was put forward that the true Ganoid genital ducts were perhaps
not Müllerian ducts, but enlarged segmental tubes with persisting abdominal
funnels belonging to the mesonephros.
Footnote 545: F. M. Balfour, "On the Origin and History of the
Urinogenital Organs of Vertebrates," _Journ. of Anat. and
Phys._, Vol. X., 1876 [This edition, No. VII].
If the possibility of the oviduct of _Lepidosteus_ not being a Müllerian
duct is admitted, a similar doubt must also exist as to the genital ducts
of other Ganoids, and we must be prepared to shew that there is a
reasonable ground for scepticism on this point. We would in this connexion
point out that the second of the two arguments urged against the view that
the genital duct of _Lepidosteus_ is not a Müllerian duct applies with
equal force to the case of all other Ganoids.
The short funnel-shaped genital duct of the Chondrostei is also very unlike
undoubted Müllerian ducts, and could moreover easily be conceived as
originating by a fold of the peritoneum, a slight extension of which would
give rise to a genital duct like that of _Lepidosteus_.
The main difficulty of the view that the genital ducts of Ganoids are not
Müllerian ducts lies in the fact that they open into the segmental duct.
While it is easy to understand the genesis of a duct from a folding of the
peritoneum, and also easy to understand how such a duct might lead to the
exterior by coalescing, for instance, with an abdominal pore, it is not
easy to see how such a duct could acquire a communication with the
segmental duct.
We do not under these circumstances wish to speak dogmatically, either in
favour of or against the view that the genital ducts of Ganoids are
Müllerian ducts. Their ontogeny would be conclusive on this matter, and we
trust that some of the anatomists who have the opportunity of studying the
development of the Sturgeon will soon let us know the facts of the case. If
there are persisting funnels of the mesonephric segmental tubes in adult
Sturgeons, some of them ought to be situated within the genital ducts, if
the latter are not Müllerian ducts; and naturalists who have the
opportunity ought also to look out for such openings.
The mode of origin of the anterior part of the genital duct of
_Lepidosteus_ appears to us to tell strongly in favour of the view, already
regarded as probable by one of us[546], that the Teleostean genital ducts
are derived from those of Ganoids; and if, as appears to us indubitable,
the most primitive type of Ganoid genital ducts is found in the
Chondrostei, it is interesting to notice that the remaining Ganoids present
in various ways approximations to the arrangement typically found in
Teleostei. _Lepidosteus_ obviously approaches Teleostei in the fact of the
ovarian ridge forming part of the wall of the oviduct, but differs from the
Teleostei in the fact of the oviduct opening into the kidney ducts, instead
of each pair of ducts having an independent opening in the cloaca, and in
the fact that the male genital products are not carried to the exterior by
a duct homologous with the oviduct. _Amia_ is closer to the Teleostei in
the arrangement of the posterior part of the genital ducts, in that the two
genital ducts coalesce posteriorly; while _Polypterus_ approaches still
nearer to the Teleostei in the fact that the two genital ducts and the two
kidney ducts unite with each other before they join; and in order to
convert this arrangement into that characteristic of the Teleostei we have
only to conceive the coalesced ducts of the kidneys acquiring an
independent opening into the cloaca behind the genital opening.
Footnote 546: F. M. Balfour, _Comparative Embryology_,
Vol. II., p. 605 [the original edition].
_The male genital ducts._--The discovery of the vasa efferentia in
_Lepidosteus_, carrying off the semen from the testis, and transporting it
to the mesonephros, and thence through the mesonephric tubes to the
segmental duct, must be regarded as the most important of our results on
the excretory system.
It proves in the first place that the transportation outwards of the
genital products of both sexes by homologous ducts, which has been hitherto
held to be universal in Ganoids, and which, in the absence of evidence to
the contrary, must still be assumed to be true for all Ganoids except
_Lepidosteus_, is a secondary arrangement. This conclusion follows from the
fact that in Elasmobranchii, &c., which are not descendants of the Ganoids,
the same arrangement of seminal ducts is found as in _Lepidosteus_, and it
must therefore have been inherited from an ancestor common to the two
groups.
If, therefore, the current statements about the generative ducts of Ganoids
are true, the males must have lost their vasa efferentia, and the function
of vas deferens must have been taken by the homologue of the oviduct,
presumably present in the male. The Teleostei must, moreover, have sprung
from Ganoidei in which the vasa efferentia had become aborted.
Considerable phylogenetic difficulties as to the relationships of Ganoidei
and Elasmobranchii are removed by the discovery that Ganoids were
originally provided with a system of vasa efferentia like that of
Elasmobranchii.
THE ALIMENTARY CANAL AND ITS APPENDAGES.
I.--_Anatomy._
Agassiz (No. 2) gives a short description with a figure of the viscera of
_Lepidosteus_ as a whole. Van der Hoeven has also given a figure of them in
his memoir on the air-bladder of this form (No. 8), and Johannes Müller
first detected the spiral valve and gave a short account of it in his
memoir (No. 13). Stannius, again, makes several references to the viscera
of _Lepidosteus_ in his anatomy of the Vertebrata, and throws some doubt on
Müller's determination of the spiral valve.
The following description refers to a female _Lepidosteus_ of 100.5
centims. (Plate 40, fig. 66).
With reference to the mouth and pharynx, we have nothing special to remark.
Immediately behind the pharynx there comes an elongated tube, which is not
divisible into stomach and oesophagus, and may be called the stomach
(_st._). It is about 44.6 centims. long, and gradually narrows from the
middle towards the hinder or pyloric extremity. It runs straight backwards
for the greater part of its length, the last 3.8 centims., however, taking
a sudden bend forwards. For about half its length the walls are thin, and
the mucous membrane is smooth; in the posterior half the walls are thick,
and the mucous membrane is raised into numerous longitudinal ridges. The
peculiar glandular structure of the epithelium of this part in the embryo
is shewn in Plate 40, fig. 62 (_st._). Its opening into the duodenum is
provided with a very distinct pyloric valve (_py._). This valve projects
into a kind of chamber, freely communicating with the duodenum, and
containing four large pits (_c´_), into each of which a group of pyloric
cæca opens. These cæca form a fairly compact gland (_c._) about 6.5
centims. long, which overlaps the stomach anteriorly, and the duodenum
posteriorly.
Close to the pyloric valve, on its right side, is a small papilla, on the
apex of which the bile duct opens (_b.d´_).
A small, apparently glandular, mass closely connected with the bile duct,
in the position in which we have seen the pancreas in the larva (Plate 40,
figs. 62 and 63, _p._), is almost certainly a rudimentary pancreas, like
that of many Teleostei; but its preservation was too bad for histological
examination. We believe that the pancreas of _Lepidosteus_ has hitherto
been overlooked.
The small intestine passes straight backwards for about 8 centims., and
then presents three compact coils. From the end of these a section, about 5
centims. long, the walls of which are much thicker, runs forwards. The
intestine then again turns backwards, making one spiral coil. This spiral
part passes directly, without any sharp line of demarcation, into a short
and straight tube, which tapers slightly from before backwards, and ends at
the anus. The mucous membrane of the intestine for about the first 3.5
centims. is smooth, and the muscular walls thin: the rest of the small
intestine has thick walls, and the mucous membrane is reticulated.
A short spiral valve (_sp.v._), with a very rudimentary epithelial fold,
making nearly two turns, begins in about the posterior half of the spiral
coil of the intestine, extending backwards for slightly less than half the
straight terminal portion of the intestine, and ending 4 centims. in front
of the anus. Its total length in one example was about 4.5 centims.
The termination of the spiral valve is marked by a slight constriction, and
we may call the straight portion of the intestine behind it the rectum
(_rc._).
The posterior part of the intestine, from the beginning of the spiral valve
to the anus, _is connected with the ventral wall of the abdomen by a
mesentery_.
The air-bladder (_a.b._) is 45 centims. long, and opens into the alimentary
canal by a slit-like aperture (_a.b´._) on the median dorsal line,
immediately behind the epipharyngeal teeth. Each lip of this aperture is
largely formed by a muscular cushion, thickest at its posterior end, and
extending about 6 millims. behind the aperture itself. A narrow passage is
bounded by these muscular walls, which opens dorsally into the air-bladder.
The air-bladder is provided with two short anterior cornua, and tapers to a
point behind: it shews no indication of any separation into two parts. A
strong band of connective tissue runs along the inner aspect of its whole
dorsal region, from which there are given off on each side--at intervals of
about 12 millims. anteriorly, gradually increasing to 18 millims.
posteriorly--bands of muscle, which pass outwards towards its side walls,
and then spread out into the numerous reticulations with which the
air-bladder is lined throughout. By the contraction of these muscles the
cavity of the air-bladder can doubtless be very much diminished.
The main muscular bands circumscribe a series of more or less complete
chambers, which were about twenty-seven in number on each side in our
example. The chambers are confined to the sides, so that there is a
continuous cavity running through the central part of the organ. The whole
organ has the characteristic structure of a simple lung.
The liver (_lr._) consists of a single elongated lobe, about 32 centims.
long, tapering anteriorly and posteriorly, the anterior half being on the
average twice as thick as the posterior half. The gall-bladder (_g.b._)
lies at its posterior end, and is of considerable size, tapering gradually
so as to pass insensibly into the bile duct. The hepatic duct (_hp.d._)
opens into the gall-bladder at its anterior end.
The spleen (_s._) is a large, compact, double gland, one lobe lying in the
turn of the intestine immediately above the spiral valve, and the other on
the opposite side of the intestine, so that the intestine is nearly
embraced between the two lobes.
II.--_Development._
We have already described in detail the first formation of the alimentary
tract so far as we have been able to work it out, and we need only say here
that the anterior and posterior ends of the canal become first formed, and
that these two parts gradually elongate, so as to approach each other; the
growth of the posterior part is, however, the most rapid. The junction of
the two parts takes place a very short distance behind the opening of the
bile duct into the intestine.
For some time after the two parts of the alimentary tract have nearly met,
the ventral wall of the canal at this point is not closed; so that there is
left a passage between the alimentary canal and the yolk-sack, which forms
a vitelline duct.
After the yolk-sack has ceased to be visible as an external appendage it
still persists within the abdominal cavity. It has, however, by this stage
ceased to communicate with the gut, so that the eventual absorption of the
yolk is no doubt entirely effected by the vitelline vessels. At these later
stages of development we have noticed that numerous yolk nuclei, like those
met with in Teleostei and Elasmobranchii[547], are still to be found in the
yolk.
Footnote 547: For a history of similar nuclei, vide _Comp.
Embryol._, Vol. II., chapters III. and IV.
It will be convenient to treat the history of sections of the alimentary
tract in front of and behind the vitelline duct separately. The former
gives rise to the pharyngeal region, the oesophagus, the stomach, and the
duodenum.
The pharyngeal region, immediately after it has become established, gives
rise to a series of paired pouches. These may be called the branchial
pouches, and are placed between the successive branchial arches. The first
or hyomandibular pouch, placed between the mandibular and hyoid arches, has
rather the character of a double layer of hypoblast than of a true pouch,
though in parts a slight space is developed between its two walls. It is
shewn in section in Plate 37, fig. 43 (_h.m._), from an embryo of about 10
millims., shortly before hatching. It does not appear to undergo any
further development, and, so far as we can make out, disappears shortly
after the embryo is hatched, without acquiring an opening to the exterior.
It is important to notice that this cleft, which in the cartilaginous
Ganoids and _Polypterus_ remains permanently open as the spiracle, is
rudimentary even in the embryo of _Lepidosteus_.
The second pouch is the hyobranchial pouch: its outer end meets the
epiblast before the larva is hatched, and a perforation is effected at the
junction of the two layers, converting the pouch into a visceral cleft.
Behind the hyobranchial pouch there are four branchial pouches, which
become perforated and converted into branchial clefts shortly after
hatching.
The region of the oesophagus following the pharynx is not separated from
the stomach, unless a glandular posterior region (vide description of
adult) be regarded as the stomach, a non-glandular anterior region forming
the oesophagus. The lumen of this part appears to be all but obliterated in
the stages immediately before hatching, giving rise for a short period to a
solid oesophagus like that of Elasmobranchii and Teleostei[548].
Footnote 548: Vide _Comp. Embryol._, Vol. II., pp. 50-63 [the
original edition].
From the anterior part of the region immediately behind the pharynx the
air-bladder arises as a dorsal unpaired diverticulum. From the very first
it has an elongated slit-like mouth (Plate 40, fig. 64, _a.b´._), and is
placed in the mesenteric attachment of the part of the throat from which it
springs.
We have first noticed it in the stages immediately after hatching. At first
very short and narrow, it grows in succeeding stages longer and wider,
making its way backwards in the mesentery of the alimentary tract (Plate
40, fig. 65, _a.b._). In the larva of a month and a half old (26 millims.)
it has still a perfectly simple form, and is without traces of its adult
lung-like structure; but in the larva of 11 centims. it has the typical
adult structure.
The stomach is at first quite straight, but shortly after the larva is
hatched its posterior end becomes bent ventralwards and forwards, so that
the flexure of its posterior end (present in the adult) is very early
established. The stomach is continuous behind with the duodenum, the
commencement of which is indicated by the opening of the bile duct.
The liver is the first-formed alimentary gland, and is already a compact
body before the larva is hatched. We have nothing to say with reference to
its development, except that it exhibits the same simple structure in the
embryo that it does in the adult.
A more interesting glandular body is the pancreas. It has already been
stated that in the adult we have recognized a small body which we believe
to be the pancreas, but that we were unable to study its histological
characters.
In the embryo there is a well-developed pancreas which arises in the same
position and the same manner as in those Vertebrata in which the pancreas
is an important gland in the adult.
We have first noticed the pancreas in a stage shortly after hatching (Plate
40, fig. 61, _p._). It then has the form of a funnel-shaped diverticulum of
the _dorsal_ wall of the duodenum, immediately behind the level of the
opening of the bile duct. From the apex of this funnel numerous small
glandular tubuli soon sprout out.
The similarity in the development of the pancreas in _Lepidosteus_ to that
of the same gland in Elasmobranchii is very striking[549].
Footnote 549: Vide F. M. Balfour, "Monograph on Development of
Elasmobranch Fishes," p. 226 [This edition, No. X., p. 454].
The pancreas at a later stage is placed immediately behind the end of the
liver in a loop formed by the pyloric section of the stomach (Plate 40,
fig. 62, _p._). During larval life it constitutes a considerable gland, the
anterior end of which partly envelopes the bile duct (Plate 40, fig. 63,
_p._).
Considering the undoubted affinities between _Lepidosteus_ and the
Teleostei, the facts just recorded with reference to the pancreas appear to
us to demonstrate that the small size and occasional absence (?) of this
gland in Teleostei is a result of the degeneration of this gland; and it
seems probable that the pancreas will be found in the larvæ of most
Teleostei. These conclusions render intelligible, moreover, the great
development of the pancreas in the Elasmobranchii.
We have first noticed the pyloric cæca arising as outgrowths of the
duodenum in larvæ of about three weeks old, and they become rapidly longer
and more prominent (Plate 40, fig. 62, _c._).
The portion of the intestine behind the vitelline duct is, as in all the
Vertebrata, at first straight. In Elasmobranchii the lumen of the part of
the intestine in which a spiral valve is present in the adult, very early
acquires a more or less semilunar form by the appearance of a fold which
winds in a long spiral. In _Lepidosteus_ there is a fold similar in every
respect (Plate 38, fig. 53, _sp.v._), forming an open spiral round the
intestine. This fold is the first indication of the spiral valve, but it is
relatively very much later in its appearance than in Elasmobranchii, not
being formed till about three weeks after hatching. It is, moreover, in
correlation with the small extent of the spiral valve of the adult,
confined to a much smaller portion of the intestine than in Elasmobranchii,
although owing to the relative straightness of the anterior part of the
intestine it is proportionately longer in the embryo than in the adult.
The similarity of the embryonic spiral valve of _Lepidosteus_ to that of
Elasmobranchii shews that Stannius' hesitation in accepting Müller's
discovery of the spiral valve in _Lepidosteus_ is not justified.
J. Müller (_Bau u. Entwick. d. Myxinoiden_) holds that the so-called bursa
entiana of Elasmobranchii (_i.e._, the chamber placed between the part of
the intestine with the spiral valve and the end of the pylorus) is the
homologue of the more elongated portion of the small intestine which
occupies a similar position in the Sturgeon. This portion of the small
intestine is no doubt homologous with the still more elongated and coiled
portion of the small intestine in _Lepidosteus_ placed between the chamber
into which the pyloric cæca, &c., open and the region of the spiral valve.
The fact that the vitelline duct in the embryo _Lepidosteus_ is placed
close to the pyloric end of the stomach, and that the greater portion of
the small intestine is derived from part of the alimentary canal behind
this, shews that Müller is mistaken in attempting to homologise the bursa
entiana of Elasmobranchii, which is placed in front of the vitelline duct,
with the coiled part of the small intestine of the above forms. The latter
is either derived from an elongation of the very short portion of the
intestine between the vitelline duct and the primitive spiral valve, or
more probably by the conversion of the anterior part of the intestine,
originally provided with a spiral valve into a coiled small intestine not
so provided.
We have already called attention to the peculiar mesentery present in the
adult attaching the posterior straight part of the intestine to the ventral
wall of the body. This mesentery, which together with the dorsal mesentery
divides the hinder section of the body-cavity into two lateral compartments
is, we believe, a persisting portion of the ventral mesentery which, as
pointed out by one of us[550], is primitively present for the whole length
of the body-cavity. The persistence of such a large section of it as that
found in the adult _Lepidosteus_ is, so far as we know, quite exceptional.
This mesentery is shewn in section in the embryo in Plate 38, fig. 53
(_v.mt._). The small vessel in it appears to be the remnant of the
subintestinal vein.
Footnote 550: _Comparative Embryology_, Vol. II. p. 514 [the
original edition].
THE GILL ON THE HYOID ARCH.
It is well known that _Lepidosteus_ is provided with a gill on the hyoid
arch, divided on each side into two parts. An excellent figure of this gill
is given by Müller (No. 13, plate 5, fig. 6), who holds from a
consideration of the vascular supply that the two parts of this gill
represent respectively the hyoid gill and the mandibular gill (called by
Müller pseudobranch). Müller's views on this subject have not usually been
accepted, but it is the fashion to regard the whole of the gill as the
hyoid gill divided into two parts. It appeared to us not improbable that
embryology might throw some light on the history of this gill, and
accordingly we kept a look out in our embryos for traces of gills on the
hyoid and mandibular arches. The results we have arrived at are purely
negative, but are not the less surprising for this fact. The hyomandibular
cleft as shewn above, is never fully developed, and early undergoes a
complete atrophy--a fact which is, on the whole, against Müller's view; but
what astonished us most in connection with the gill in question is that we
have been unable to find any trace of it even in the oldest larva whose
head we have had (26 millims.), and at a period when the gills on the
hinder arches have reached their full development.
We imagined the gill in question to be the remnant of a gill fully formed
in extinct Ganoid types, and therefore expected to find it better developed
in the larva than in the adult. That the contrary is the fact appears to us
fairly certain, although we cannot at present offer any explanation of it.
SYSTEMATIC POSITION OF LEPIDOSTEUS.
A. Agassiz concludes his memoir on the development of _Lepidosteus_ by
pointing out that in spite of certain affinities in other directions this
form is "not so far removed from the bony Fishes as has been supposed." Our
own observations go far to confirm Agassiz' opinion.
Apart from the complete segmentation, the general development of
_Lepidosteus_ is strikingly Teleostean. In addition to the general
Teleostean features of the embryo and larva, which can only be appreciated
by those who have had an opportunity of practically working at the subject,
we may point to the following developmental features[551] as indicative of
Teleostean affinities:--
Footnote 551: The features enumerated above are not in all
cases confined to _Lepidosteus_ and Teleostei, but are always
eminently characteristic of the latter.
(1) The formation of the nervous system as a solid keel of the epiblast.
(2) The division of the epiblast into a nervous and epidermic stratum.
(3) The mode of development of the gut (vide pp. 752-754).
(4) The mode of development of the pronephros; though, as shewn on p. 822,
the pronephros of _Lepidosteus_ has primitive characters not retained by
Teleostei.
(5) The early stages in the development of the vertebral column (vide p.
779).
In addition to these, so to speak, purely embryonic characters there are
not a few important adult characters:--
(1) The continuity of the oviducts with the genital glands.
(2) The small size of the pancreas, and the presence of numerous so-called
pancreatic cæca.
(3) The somewhat coiled small intestine.
(4) Certain characters of the brain, _e.g._, the large size of the
cerebellum; the presence of the so-called lobi inferiores on the
infundibulum; and of tori semicirculares in the mid-brain.
In spite of the undoubtedly important list of features to which we have
just called attention, a list containing not less important characters,
both embryological and adult, separating _Lepidosteus_ from the Teleostei,
can be drawn up:--
(1) The character of the truncus arteriosus.
(2) The fact of the genital ducts joining the ureters.
(3) The presence of vasa efferentia in the male carrying the semen from the
testes to the kidney, and through the tubules of the latter into the kidney
duct.
(4) The presence of a well-developed opercular gill.
(5) The presence of a spiral valve; though this character may possibly
break down with the extension of our knowledge.
(6) The typical Ganoid characters of the thalamencephalon and the cerebral
hemispheres (vide pp. 769 and 770).
(7) The chiasma of the optic nerves.
(8) The absence of a pecten, and presence of a vascular membrane between
the vitreous humour and the retina.
(9) The opisthocoelous form of the vertebræ.
(10) The articulation of the ventral parts of the hæmal arches of the tail
with processes of the vertebral column.
(11) The absence of a division of the muscles into dorso-lateral and
ventro-lateral divisions.
(12) The complete segmentation of the ovum.
The list just given appears to us sufficient to demonstrate that
_Lepidosteus_ cannot be classed with the Teleostei; and we hold that
Müller's view is correct, according to which _Lepidosteus_ is a true
Ganoid.
The existence of the Ganoids as a distinct group has, however, recently
been challenged by so distinguished an Ichthyologist as Günther, and it may
therefore be well to consider how far the group as defined by Müller is a
natural one for living forms[552], and how far recent researches enable us
to improve upon Müller's definitions. In his classical memoir (No. 13) the
characters of the Ganoids are thus shortly stated:--
"These Fishes are either provided with plate-like angular or rounded
cement-covered scales, or they bear osseous plates, or are quite
naked. The fins are often, but not always, beset with a double or
single row of spinous plates or splints. The caudal fin occasionally
embraces in its upper lobe the end of the vertebral column, which may
be prolonged to the end of the upper lobe. Their double nasal openings
resemble those of Teleostei. The gills are free, and lie in a
branchial cavity under an operculum, like those of Teleostei. Many of
them have an accessory organ of respiration, in the form of an
opercular gill, which is distinct from the pseudobranch, and can be
present together with the latter; many also have spiracles like
Elasmobranchii. They have many valves in the stem of the aorta like
the latter, also a muscular coat in the stem of the aorta. Their ova
are transported from the abdominal cavity by oviducts. Their optic
nerves do not cross each other. The intestine is often provided with a
spiral valve, like Elasmobranchii. They have a swimming-bladder with a
duct, like many Teleostei. Their pelvic fins are abdominal.
"If we include in a definition only those characters which are
invariable, the Ganoids may be shortly defined as being those Fish
with numerous valves to the stem of the aorta, which is also provided
with a muscular coat; with free gills and an operculum, and with
abdominal pelvic fins."
Footnote 552: We do not profess to be able to discuss this
question for extinct forms of Fish, though of course it is a
necessary consequence of the theory of descent that the various
groups should merge into each other as we go back in geological
time.
To these distinctive characters, he adds in an appendix to his paper, the
presence of the spiral valve, and the absence of a processus falciformis
and a choroid gland.
To the distinctive set of characters given by Müller we may probably add
the following:--
(1) Oviducts and urinary ducts always unite, and open by a common
urinogenital aperture behind the anus.
(2) Skull hyostylic.
(3) Segmentation complete in the types so far investigated, though perhaps
_Amia_ may be found to resemble the Teleostei in this particular.
(4) A pronephros of the Teleostean type present in the larva.
(5) Thalamencephalon very large and well developed.
(6) The ventricle in the posterior part of the cerebrum is not divided
behind into lateral halves, the roof of the undivided part being extremely
thin.
(7) Abdominal pores always present.
The great number of characters just given are amply sufficient to
differentiate the Ganoids as a group; but, curiously enough, the only
characters amongst the whole series which have been given, which can be
regarded as peculiar to the Ganoids, are (1) the characters of the brain,
and (2) the fact of the oviducts and kidney ducts uniting together and
opening by a common pore to the exterior.
This absence of characters peculiar to the Ganoids is an indication of how
widely separated in organization are the different members of this great
group.
At the same time, the only group with which existing Ganoids have close
affinities is the Teleostei. The points they have in common with the
Elasmobranchii are merely such as are due to the fact that both retain
numerous primitive Vertebrate characters[553], and the gulf which really
separates them is very wide.
Footnote 553: As instances of this we may cite (1) the spiral
valve; (2) the frequent presence of a spiracle; (3) the
frequent presence of a communication between the pericardium
and the body-cavity; (4) the heterocercal tail.
There is again no indication of any close affinity between the Dipnoi and,
at any rate, existing Ganoids.
Like the Ganoids, the Dipnoi are no doubt remnants of a very primitive
stock; but in the conversion of the air-bladder into a true lung, the
highly specialized character of their limbs[554], their peculiar autostylic
skulls, the fact of their ventral nasal openings leading directly into the
mouth, their multisegmented bars (interspinous bars), directly prolonged
from the neural and hæmal arches and supporting the fin-rays of the
unpaired dorsal and ventral fins, and their well-developed cerebral
hemispheres, very unlike those of Ganoids and approaching the Amphibian
type, they form a very well-defined group, and one very distinctly
separated from the Ganoids.
Footnote 554: Vide F. M. Balfour, "On the Development of the
Skeleton of the Paired Fins of Elasmobranchii," _Proc. Zool.
Soc._, 1881 [This edition, No. XX.].
No doubt the Chondrostean Ganoids are nearly as far removed from the
Teleostei as from the Dipnoi, but the links uniting these Ganoids with the
Teleostei have been so fully preserved in the existing fauna of the globe,
that the two groups almost run into each other. If, in fact, we were
anxious to make any radical change in the ordinary classification of
Fishes, it would be by uniting the Teleostei and Ganoids, or rather
constituting the Teleostei into one of the sub-groups of the Ganoids,
equivalent to the Chondrostei. We do not recommend such an arrangement,
which in view of the great preponderance of the Teleostei amongst living
Fishes would be highly inconvenient, but the step from _Amia_ to the
Teleostei is certainly not so great as that from the Chondrostei to _Amia_,
and is undoubtedly less than that from the Selachii to the Holocephali.
LIST OF MEMOIRS ON THE ANATOMY AND DEVELOPMENT OF LEPIDOSTEUS.
1. Agassiz, A. "The Development of _Lepidosteus_." Part 1., _Proc. Amer.
Acad. Arts and Sciences_, Vol. XIV. 1879.
2. Agassiz, L. _Recherches s. l. Poissons Fossiles._ Neuchatel. 1833-45.
3. Boas, J. E. "Ueber Herz u. Arterienbogen bei _Ceradotus_ u.
_Protopterus_," _Morphol. Jahrbuch_, Vol. VI. 1880.
4. Davidoff, M. von. "Beiträge z. vergleich. Anat. d. hinteren Gliedmassen
d. Fische," _Morphol. Jahrbuch_, Vol. VI. 1880.
5. Gegenbaur, C. _Untersuch. z. vergleich. Anat. d. Wirbelthiere_, Heft
II., _Schultergürtel d. Wirbelthiere. Brustflosse der Fische_. Leipzig,
1865.
6. Gegenbaur, C. "Zur Entwick. d. Wirbelsäule d. _Lepidosteus_, &c."
_Jenaische Zeitschrift_, Vol. III. 1867.
7. Hertwig, O. "Ueber d. Hautskelet d. Fische (_Lepidosteus_ u.
_Polypterus_)," _Morphol. Jahrbuch_, Vol. V. 1879.
8. Hoeven, Van der. "Ueber d. zellige Schwimmblase d. _Lepidosteus_."
Müller's _Archiv_, 1841.
9. Hyrtl, J. "Ueber d. Schwimmblase von _Lepidosteus osseus_," _Sitz. d.
Wiener Akad._ Vol. VIII. 1852.
10. Hyrtl, J. "Ueber d. Pori abdominales, d. Kiemen-Arterien, u. d.
Glandula thyroidea d. Ganoiden," _Sitz. d. Wiener Akad._ Vol. VIII. 1852.
11. Hyrtl, J. _Ueber d. Zusammenhang d. Geschlechts u. Harnwerkzeuge bei d.
Ganoiden_, Wien, 1855.
12. Kölliker, A. _Ueber d. Ende d. Wirbelsäule b. Ganoiden_, Leipzig, 1860.
13. Müller, J. "Ueber d. Bau u. d. Grenzen d. Ganoiden," _Berlin Akad._
1844.
14. Schneider, H. "Ueber d. Augenmuskelnerven d. Ganoiden," _Jenaische
Zeitschrift_, Vol. XV. 1881.
15. Wilder, Burt G. "Notes on the North American Ganoids, _Amia_,
_Lepidosteus_, _Acipenser_, and _Polyodon_." _Proc. Amer. Assoc. for the
Advancement of Science_, 1875.
LIST OF REFERENCE LETTERS.
_a._ Anus. _ab._ Air-bladder. _ab´._ Aperture of air-bladder into throat.
_ac._ Anterior commissure. _af._ Anal fin. _al._ Alimentary canal. _ao._
Aorta. _ar._ Artery. _au._ Auditory pit. _b._ Brain. _bc._ Body-cavity.
_bd._ Bile duct. _bd´._ Aperture of bile duct into duodenum. _bl._
Coalesced portion of segmental ducts, forming urinogenital bladder. _bra._
Branchial arches. _brc._ Branchial clefts. _c._ Pyloric caæca. _c´._
Apertures of caæca into duodenum. _cb._ Cerebellum. _cdv._ Cardinal vein.
_ce._ Cerebrum: in figs. 47A and B, anterior lobe of cerebrum. _ce´._
Posterior lobe of cerebrum. _cf._ Caudal fin. _cn._ Centrum. _ch._
Choroidal fissure. _crv._ Circular vein of vascular membrane of eye. _csh._
Cuticular sheath of notochord. _cv._ Caudal vein. _d._ Duodenum. _dc._
Dorsal cartilage of neural arch. _df._ Dermal fin-rays. _dl._ Dorsal lobe
of caudal fin. _dlf._ Dorsal fin. _e._ Eye. _ed._ Epidermis. _ep._
Epiblast. _fb._ Fore-brain. _fe._ Pyriform bodies surrounding the zona
radiata of the ovum, probably the remains of epithelial cells. _gb._
Gall-bladder. _gd._ Genital duct. _gl._ Glomerulus. _gr._ Genital ridge.
_h._ Heart. _ha._ Hæmal arch. _hb._ Hind-brain. _hc._ Head-cavity. _hpd._
Hepatic duct. _hm._ Hyomandibular cleft. _hop._ Operculum. _hy._ Hypoblast;
in fig. 10, hyoid arch. _hyl._ Hyaloid membrane. _ic._ Intercalated
cartilaginous elements of the neural arches. _in._ Infundibulum. _ir._
Iris. _is._ Interspinous cartilage or bones. _iv._ subintestinal vein.
_ivr._ Intervertebral ring of cartilage. _k._ Kidney. _l._ Lens. _lc._
Longitudinal canal, formed by union of the vasa efferentia. _lin._ Lobi
inferiores. _ll._ Ligamentum longitudinale superius. _lr._ Liver. _lt._
Lateral line. _ly._ Lymphatic body in front of kidney. _m._ Mouth. _mb._
Mid-brain. _mc._ Medullary cord. _mel._ Membrana elastica externa. _mes._
Mesorchium. _mn._ Mandible. _md._ and _mo._ Medulla oblongata. _ms._
Mesoblast. _na._ Neural arch. _na´._ Dorsal element of neural arch. _nc._
Notochord. _nve._ Network formed by vasa efferentia on inner face of
testis. _od._ Oviduct. _od´._ Aperture of oviduct into bladder. _ol._ Nasal
pit or aperture. _olf._ Olfactory lobe. _op._ Optic vesicle. _op ch._ Optic
chiasma. _opl._ Optic lobes. _op th._ Optic thalami. _or ep._ Oral
epithelium. _ov._ Ovary. _p._ Pancreas. _pc._ Pericardium. _pcf._ Pectoral
fin. _pch._ Pigmented layer of choroid. _pf._ Peritoneal funnel of
segmental tube of mesonephros. _pfp._ Peritoneal funnel leading into
pronephric chamber. _pg._ Pectoral girdle. _plf._ Pelvic fin. _pn._ Pineal
gland. _po._ Primitive germinal cells. _pr._ Mesoblastic somite. _prc._
Pronephric chamber. _prn._ Pronephros. _pr n´._ Opening of pronephros into
pronephric chamber. _pt._ Pituitary body. _py._ Pyloric valve. _pz._
Parietal zone of blastoderm. _r._ Rostrum. _rb._ Rib. _rc._ Rectum. _s._
Spleen. _sc._ Seminal vessels passing from the longitudinal canal into the
kidney. _sd._ Suctorial disc. _sg._ Segmental or archinephric duct. _sgt._
Segmental tubules. _sh._ Granular outer portion of the sheath of the
notochord in the vertebral regions. _smx._ Superior maxillary process.
_snc._ subnotochordal rod. _so._ Somatic mesoblast. _sp._ Splanchnic
mesoblast. _spn._ Spinal nerve. _spv._ Spiral valve. _st._ Stomach. _st._
Seminal tubes of the testis. _sup._ Suctorial papillæ. _t._ Testis. _th._
Thalamencephalon. _thl._ Lobes of the roof of the thalamencephalon. _tr._
Trabeculæ. _ug._ Urinogenital aperture. _v._ Ventricle. _ve._ Vasa
efferentia. _vh._ Vitreous humour. _vl._ Ventral lobe of the caudal fin.
_vmt._ Ventral mesentery. _vn._ Vein. _vs._ Blood-vessel. _vsh._ Vascular
sheath between the hyaloid membrane and the vitreous humour. _vth._ Vesicle
of the thalamencephalon. _x._ Groove in epiblast, probably formed in
process of hardening. _y._ Yolk. _z._ Commissure in front of pineal gland.
_zr._ Outer striated portion of investing membrane (zona radiata) of ovum.
_zr´._ Inner non-striated portion of investing membrane of ovum. I.
Olfactory nerve. II. Optic nerve. III. Oculomotor nerve. V. Trigeminal
nerve. VIII. Facial and auditory nerves.
EXPLANATION OF PLATES 34-42.
PLATE 34.
Figs. 1-4. Different stages in the segmentation of the ovum.
Fig. 1. Ovum with a single vertical furrow, from above.
Fig. 2. Ovum with two vertical furrows, from above.
Fig. 3. Side view of an ovum with a completely formed blastodermic
disc.
Fig. 4. The same ovum as fig. 3, from below, shewing four vertical
furrows nearly meeting at the vegetative pole.
Figs. 5-10. External views of embryos up to time of hatching.
Fig. 5. Embryo, 3.5 millims. long, third day after impregnation.
Fig. 6. Embryo on the fifth day after impregnation.
Fig. 7. Posterior part of same embryo as fig. 6, shewing tail
swelling.
Fig. 8. Embryo on the sixth day after impregnation.
Fig. 9. Embryo on the seventh day after impregnation.
Fig. 10. Embryo on the eleventh day after impregnation (shortly before
hatching).
Fig. 11. Head of embryo about the same age as fig. 10, ventral aspect.
Fig. 12. Side view of a larva about 11 millims. in length, shortly after
hatching.
Fig. 13. Head of a larva about the same age as fig. 12, ventral aspect.
Fig. 14. Side view of a larva about 15 millims. long, five days after
hatching.
Fig. 15. Head of a larva 23 millims. in length.
Fig. 16. Tail of a larva 11 centims. in length.
Fig. 17. Transverse section through the egg-membranes of a just-laid ovum.
We are indebted to Professor W. K. Parker for figs. 12, 14 and 15.
PLATE 35.
Figs. 18-22. Transverse sections of embryo on the third day after
impregnation.
Fig. 18. Through head, shewing the medullary keel.
Fig. 19. Through anterior part of trunk.
Fig. 20. Through same region as fig. 19, shewing a groove (_x_) in the
epiblast, probably artificially formed in the process of hardening.
Fig. 21. Through anterior part of tail region, shewing partial fusion
of layers.
Fig. 22. Through posterior part of tail region, shewing more complete
fusion of layers than fig. 21.
Figs. 23-25. Transverse sections of an embryo on the fifth day after
impregnation.
Fig. 23. Through fore-brain and optic vesicles.
Fig. 24. Through hind-brain and auditory pits.
Fig. 25. Through anterior part of trunk.
Figs. 26-27. Transverse sections of the head of an embryo on the sixth day
after impregnation.
Fig. 26. Through fore-brain and optic vesicles.
Fig. 27. Through hind-brain and auditory pits.
PLATE 36.
Figs. 28-29. Transverse sections of the trunk of an embryo on the sixth day
after impregnation.
Fig. 28. Through anterior part of trunk (from a slightly older embryo
than the other sections of this stage).
Fig. 29. Slightly posterior to fig. 28, shewing formation of segmental
duct as a fold of the somatic mesoblast.
Fig. 30. Longitudinal horizontal section of embryo on the sixth day after
impregnation, passing through the mesoblastic somites, notochord, and
medullary canal.
Figs. 31-34. Transverse sections through an embryo on the seventh day after
impregnation.
Fig. 31. Through anterior part of trunk.
Fig. 32. Through the trunk somewhat behind fig. 31.
Fig. 33. Through tail region.
Fig. 34. Further back than fig. 33, shewing constriction of tail from
the yolk.
Figs. 35-37. Transverse sections through an embryo on the eighth day after
impregnation.
Fig. 35. Through fore-brain and optic vesicles.
Fig. 36. Through hind-brain, shewing closed auditory pits, &c.
Fig. 37. Through anterior part of trunk.
Fig. 38. Section through tail of an embryo on the ninth day after
impregnation.
PLATE 37.
Fig. 39. Section through the olfactory involution and part of fore-brain of
a larva on the ninth day after impregnation, shewing olfactory nerve.
Fig. 40. Section through the anterior part of the head of the same larva,
shewing pituitary involution.
Figs. 41-43. Transverse sections through an embryo on the eleventh day
after impregnation.
Fig. 41. Through fore-part of head, shewing the pituitary body still
connected with the oral epithelium.
Fig. 42. Slightly further back than fig. 41, shewing the pituitary
body constricted off from the oral epithelium.
Fig. 43. Slightly posterior to fig. 42, to shew olfactory involution,
eye, and hyomandibular cleft.
Fig. 44. Longitudinal section of the head of an embryo of 15 millims. in
length, a few days after hatching, shewing the structure of the brain.
Fig. 45. Longitudinal section of the head of an embryo, about five weeks
after hatching, 26 millims. in length, shewing the structure of the brain.
In the front part of the brain the section passes slightly to one side of
the median line.
Figs. 46A to 46G. Transverse sections through the brain of an embryo 25
millims. in length, about a month after hatching.
Fig. 46A. Through anterior lobes of cerebrum.
Fig. 46B. Through posterior lobes of cerebrum.
Fig. 46C. Through thalamencephalon.
Fig. 46D. Through optic thalami and optic chiasma.
Fig. 46E. Through optic lobes and infundibulum.
Fig. 46F. Through optic lobes and cerebellum.
Fig. 46G. Through optic lobes and cerebellum, slightly in front of
fig. 46F.
PLATE 38.
Figs. 47A, B, C. Figures of adult brain.
Fig. 47A. From the side.
Fig. 47B. From above.
Fig. 47C. From below.
Fig. 48. Longitudinal vertical section through the eye of an embryo, about
a week after hatching, shewing the vascular membrane surrounding the
vitreous humour.
Fig. 49. Diagram shewing the arrangement of the vessels in the vascular
membrane of the vitreous humour of adult eye.
Fig. 50. Capillaries of the same vascular membrane.
Fig. 51. Transverse section through anterior part of trunk of an embryo on
the ninth day after impregnation, shewing the pronephros and pronephric
chamber.
Fig. 52. Transverse section through the region of the stomach of an embryo
15 millims. in length, shortly after hatching, to shew the glomerulus and
peritoneal funnel of pronephros.
Fig. 53. Transverse section through posterior part of the body of an
embryo, about a month after hatching, shewing the structure of the
mesonephros, the spiral valve, &c.
PLATE 39.
Figs. 54, 55, 56, and 57 are a series of transverse sections through the
genital ridge and mesonephros of one side from a larva of 11 centims.
Fig. 54. Section of the lymphatic organ which lies in front of the
mesonephros.
Fig. 55. Section near the anterior end of the mesonephros, where the
genital sack is completely formed.
Fig. 56. Section somewhat further back, shewing the mode of formation
of the genital sack.
Fig. 57. Section posterior to the above, the formation of the genital
sack not having commenced, and the genital ridge with primitive
germinal cells projecting freely into the body-cavity.
Fig. 58A. View of the testis, mesorchium, and duct of the kidney of the
left side of an adult male example of _Lepidosteus_, 60 centims. in length,
shewing the vasa efferentia and the longitudinal canal at the base of the
mesorchium. The kidney ducts have been cut open posteriorly to shew the
structure of the interior.
Fig. 58B. Inner aspect of the posterior lobe of the testis from the same
example, to shew the vasa efferentia forming a network on the face of the
testis.
Figs. 59A and B. Two sections shewing the structure and relations of the
efferent ducts of the testis in the same example.
Fig. 59A. Section through the inner aspect of a portion of the testis
and mesorchium, to shew the network of the vasa efferentia (_nve_)
becoming continuous with the seminal tubes (_st_). The granular matter
nearly filling the vasa efferentia and the seminal tubes represent the
spermatozoa.
Fig. 59B. Section through part of the kidney and its duct and the
longitudinal canal (_lc_) at the base of the mesorchium. Canals (_sc_)
are seen passing off from the latter, which enter the kidney and join
the uriniferous tubuli. Some of the latter (as well as the seminal
tubes) are seen to be filled with granular matter, which we believe to
be the remains of spermatozoa.
Fig. 60. Diagram of the urinogenital organs of the left side of an adult
female example of _Lepidosteus_ 100 centims. in length. This figure shews
the oviduct (_od_) continuous with the investment of the ovary, opening at
_od´_ into the dilated part of the kidney duct (segmental duct). It also
shews the segmental duct and the junction of the latter with its fellow of
the right side to form the so-called bladder, this part being represented
as cut open. The kidney (_k_) and lymphatic organ (_ly_) in front of it are
also shewn.
PLATE 40.
Fig. 61. Transverse section through the developing pancreas (_p_) of a
larva 11 millims. in length.
Fig. 62. Longitudinal section through portions of the stomach, liver, and
duodenum of an embryo about a month after hatching, to shew the relations
of the pancreas (_p_) to the surrounding parts.
Fig. 63. External view of portions of the liver, stomach, duodenum, &c., of
a young Fish, 11 centims. in length, to shew the pancreas (_p_).
Fig. 64. Transverse section through the anterior part of the trunk of an
embryo, about a month after hatching, shewing the connection of the
air-bladder with the throat (_ab´_).
Fig. 65. Transverse section through the same embryo as fig. 64 further
back, shewing the posterior part of the air-bladder (_ab_).
Fig. 66. Viscera of an adult female, 100 centims. in length, shewing the
alimentary canal with its appended glands in natural position, and the
air-bladder with its aperture into the throat (_ab´_). The proximal part of
the duodenum and the terminal part of the intestine are represented as cut
open, the former to shew the pyloric valve and the apertures of the pyloric
cæca and bile duct, and the latter to shew the spiral valve.
This figure was drawn for us by Professor A. C. Haddon.
PLATE 41.
Fig. 67. Transverse section through the tail of an advanced larva, shewing
the neural and hæmal processes, the independently developed interneural and
interhæmal elements (_is_), and the commencing dermal fin-rays (_df_).
Fig. 68. Side view of the tail of a larva, 21 minims. in length, dissected
so as to shew the structure of the skeleton.
Fig. 69. Longitudinal horizontal section through the vertebral column of a
larva, 5.5 centims. in length, on the level of the hæmal arches, shewing
the intervertebral rings of cartilage continuous with the arches, the
vertebral constriction of the notochord, &c.
Figs. 70 and 71. Transverse sections through the vertebral column of a
larva of 5.5 centims. The red represents bone, and the blue cartilage.
Fig. 70. Through the vertebral region, shewing the neural and hæmal
arches, the notochordal sheath, &c.
Fig. 71. Through the intervertebral region, shewing the intervertebral
cartilage.
Figs. 72 and 73. Transverse sections through the trunk of a larva of 5.5
centims. to shew the structure of the ribs and hæmal arches.
Fig. 72. Through the anterior part of the trunk.
Fig. 73. Through the posterior part of the trunk.
PLATE 42.
Figs. 74-76. Transverse sections through the trunk of the same larva as
figs. 72 and 73.
Fig. 74. Through the posterior part of the trunk (rather further back
than fig. 73).
Fig. 75. Through the anterior part of the tail.
Fig. 76. Rather further back than fig. 75.
Fig. 77. Longitudinal horizontal section through the vertebral column of a
larva of 11 centims., passing through the level of the hæmal arches, and
shewing the intervertebral constriction of the notochord, the ossification
of the cartilage, &c.
Fig. 78. Transverse section through a vertebral region of the vertebral
column of a larva 11 centims. in length.
Fig. 79. Transverse section through an intervertebral region of the same
larva as fig. 78.
Fig. 80. Side view of two trunk vertebræ of an adult _Lepidosteus_.
Fig. 81. Front view of a trunk vertebra of adult.
In figures 80 and 81 the red does not represent bone as in the other
figures, but simply the ligamentum longitudinale superius.
XXIII. ON THE NATURE OF THE ORGAN IN ADULT TELEOSTEANS AND
GANOIDS, WHICH IS USUALLY REGARDED AS THE HEAD-KIDNEY
OR PRONEPHROS[555].
Footnote 555: From the _Quarterly Journal of Microscopical
Science_, Vol. XXII., 1882.
While working at the anatomy of _Lepidosteus_ I was led to doubt the
accuracy of the accepted accounts of the anterior part of the kidneys in
this[556] and in allied species of Fishes. In order to test my doubts I
first examined the structure of the kidneys in the Sturgeon (Acipenser), of
which I fortunately had a well-preserved specimen.
Footnote 556: I am about to publish, in conjunction with Mr
Parker, a full account of the anatomy and development of
Lepidosteus [No. XXII. of this edition], and shall therefore in
this paper make no further allusion to it.
The bodies usually described as the kidneys consist of two elongated bands,
attached to the dorsal wall of the abdomen, and extending for the greater
part of the length of the abdominal cavity. In front each of these bands
first becomes considerably narrowed, and then expands and terminates in a
great dilatation, which is usually called the head-kidney. Along the outer
border of the hinder part of each kidney is placed a wide ureter, which
ends suddenly in the narrow part of the body, some little way behind the
head-kidney. To the naked eye there is no distinction in structure between
the part of the so-called kidney in front of the ureter and that in the
region of the ureter. Any section through the kidney in the region of the
ureter suffices to shew that in this part the kidney is really formed of
uriniferous tubuli with numerous Malpighian bodies. Just in front, however,
of the point where the ureter ends the true kidney substance rapidly thins
out, and its place is taken by a peculiar tissue formed of a trabecular
work filled with cells, which I shall in future call lymphatic tissue.
_Thus the whole of that part of the apparent kidney in front of the ureter,
including the whole of the so-called head-kidney, is simply a great mass of
lymphatic tissue, and does not contain a single uriniferous tubule or
Malpighian body._
The difference in structure between the anterior and posterior parts of the
so-called kidney, although not alluded to in most modern works on the
kidneys, appears to have been known to Stannius, at least I so interpret a
note of his in the second edition of his _Comparative Anatomy_, p. 263,
where he describes the kidney of the Sturgeon as being composed of two
separate parts, viz. a spongy vascular substance (no doubt the so-called
head-kidney) and a true secretory substance.
After arriving at the above results with reference to the Sturgeon I
proceeded to the examination of the structure of the so-called head-kidney
in Teleostei.
I have as yet only examined four forms, viz. the Pike (_Esox lucius_), the
Smelt (_Osmerus eperlanus_), the Eel (_Anguilla anguilla_), and the Angler
(_Lophius piscatorius_).
The external features of the apparent kidney of the Pike have been
accurately described by Hyrtl[557]. He says: "The kidneys extend from the
second trunk vertebra to the end of the abdominal cavity. Their anterior
extremities, which have the form of transversely placed coffee beans, are
united together, and lie on the anterior end of the swimming bladder. The
continuation of the kidney backwards forms two small bands, separated from
each other by the whole breadth of the vertebral column. They gradually,
however, increase in breadth, so that about the middle of the vertebral
column they unite together and form a single symmetrical, keel-shaped
body," &c.
Footnote 557: "Das Uropoëtische System der Knochenfische,"
_Sitz. d. Wien. Akad._, 1830.
The Pike I examined was a large specimen of about 58 centimètres in length,
and with an apparent kidney of about 25-1/2 centimètres. The relations of
lymphatic tissue and kidney tissue were much as in the Sturgeon. The whole
of the anterior swelling, forming the so-called head-kidney, together with
a considerable portion of the part immediately behind, forming not far
short of half the whole length of the apparent kidney, was entirely formed
of lymphatic tissue. The posterior part of the kidney was composed of true
kidney substance, but even at 16 centimètres from the front end of the
kidney the lymphatic tissue formed a large portion of the whole.
A rudiment of the duct of the kidney extended forwards for a short way into
the lymphatic substance beyond the front part of the functional kidney.
In the Smelt (_Osmerus eperlanus_) the kidney had the typical Teleostean
form, consisting of two linear bands stretching for the whole length of the
body-cavity, and expanding into a great swelling in front on the level of
the ductus Cuvieri, forming the so-called head-kidney. The histological
examination of these bodies shewed generally the same features as in the
case of the Sturgeon and Pike. The posterior part was formed of the usual
uriniferous tubuli and Malpighian bodies. The anterior swollen part of
these bodies, and the part immediately following, were almost wholly formed
of a highly vascular lymphatic tissue; but in a varying amount in different
examples portions of uriniferous tubules were present, mainly, however, in
the region behind the anterior swelling. In some cases I could find no
tubules in the lymphatic tissue, and in all cases the number of them beyond
the region of the well-developed part of the kidney was so slight, that
there can be little doubt that they are functionless remnants of the
anterior part of the larval kidney. Their continuation into the anterior
swelling, when present, consisted of a single tube only.
In the Eel (_Anguilla anguilla_), which, however, I have not examined with
the same care as the Smelt, the true excretory part of the kidney appears
to be confined to the posterior portion, and to the portion immediately in
front of the anus, the whole of the anterior part of each apparent kidney,
which is not swollen in front, being composed of lymphatic tissue.
_Lophius piscatorius_ is one of the forms which, according to Hyrtl[558],
is provided with a head-kidney only, _i.e._ with that part of the kidney
which corresponds with the anterior swelling of the kidney of other types.
For this reason I was particularly anxious to investigate the structure of
its kidneys.
Footnote 558: "Das Uropoëtische System der Knochenfische,"
_Sitz. d. Wien. Akad._, 1830.
Each of these bodies forms a compact oval mass, with the ureter springing
from its hinder extremity, situated in a forward position in the
body-cavity. Sections through the kidneys shewed that they were throughout
penetrated by uriniferous tubules, but owing to the bad state of
preservation of my specimens I could not come to a decision as to the
presence of Malpighian bodies. The uriniferous tubules were embedded in
lymphatic tissue, similar to that which forms the anterior part of the
apparent kidneys in other Teleostean types.
With reference to the structure of the Teleostean kidneys, the account
given by Stannius is decidedly more correct than that of most subsequent
writers. In the note already quoted he gives it as his opinion that there
is a division of the kidney into the same two parts as in the Sturgeon,
viz. into a spongy vascular part and a true secreting part; and on a
subsequent page he points out the absence or poverty of the uriniferous
tubules in the anterior part of the kidney in many of our native Fishes.
Prior to the discovery that the larvæ of Teleosteans and Ganoids were
provided with two very distinct excretory organs, viz. a pronephros or
head-kidney, and a mesonephros or Wolffian body, which are usually
separated from each other by a more or less considerable interval, it was a
matter of no very great importance to know whether the anterior part of the
so-called kidney was a true excretory organ. In the present state of our
knowledge the question is, however, one of considerable interest.
In the Cyclostomata and Amphibia the pronephros is a purely larval organ,
which either disappears or ceases to be functionally active in the adult
state.
Rosenberg, to whom the earliest satisfactory investigations on the
development of the Teleostean pronephros are due, stated that he had traced
in the Pike (_Esox lucius_) the larval organ into the adult part of the
kidney, called by Hyrtl the pronephros; and subsequent investigators have
usually assumed that the so-called head-kidney of adult Teleosteans and
Ganoids is the persisting larval pronephros.
We have already seen that Rosenberg was entirely mistaken on this point, in
that the so-called head-kidney of the adult is not part of the true kidney.
From my own studies on young Fishes I do not believe that the oldest larvæ
investigated by Rosenberg were sufficiently advanced to settle the point in
question; and, moreover, as Rosenberg had no reason for doubting that the
so-called head-kidney of the adult was part of the excretory organ, he does
not appear to have studied the histological structure of the organ which he
identified with the embryonic pronephros in his oldest larva.
The facts to which I have called attention in this paper demonstrate that
in the Sturgeon the larval pronephros undoubtedly undergoes atrophy before
the adult stage is reached. The same is true for _Lepidosteus_, and may
probably be stated for Ganoids generally.
My observations on Teleostei are clearly not sufficiently extensive to
_prove_ that the larval pronephros _never_ persists in this group. They
appear to me, however, to shew that in the normal types of Teleostei the
organ usually held to be the pronephros is actually nothing of the kind.
A different interpretation might no doubt be placed upon my observations on
_Lophius piscatorius_, but the position of the kidney in this species
appears to me to be far from affording a conclusive proof that it is
homologous with the anterior swelling of the kidney of more normal
Teleostei.
When, moreover, we consider that Lophius, and the other forms mentioned by
Hyrtl as being provided with a head-kidney only, are all of them peculiarly
modified and specialized types of Teleostei, it appears to me far more
natural to hold that their kidney is merely the ordinary Teleostean kidney,
which, like many of their other organs, has become shifted in position,
than to maintain that the ordinary excretory organ present in other
Teleostei has been lost, and that a larval organ has been retained, which
undergoes atrophy in less specialized Teleostei.
As the question at present stands, it appears to me that the probabilities
are in favour of there being no functionally active remains of the
pronephros in adult Teleostei, and that in any case the burden of proof
rests with those who maintain that such remnants are to be found.
The general result of my investigations is thus to render it probable _that
the pronephros, though found in the larvæ or embryos of almost all the
Ichthyopsida, except the Elasmobranchii, is always a purely larval organ,
which never constitutes an active part of the excretory system in the adult
state_.
This conclusion appears to me to add probability to the view of Gegenbaur
that the pronephros is the primitive excretory gland of the Chordata; and
that the mesonephros or Wolffian body, by which it is replaced in existing
Ichthyopsida, is phylogenetically a more recent organ.
In the preceding pages I have had frequent occasion to allude to the
lymphatic tissue which has been usually mistaken for part of the excretory
organ. This tissue is formed of trabecular work, like that of lymphatic
glands, in the meshes of which an immense number of cells are placed, which
may fairly be compared with the similarly placed cells of lymphatic glands.
In the Sturgeon a considerable number of cells are found with peculiar
granular nuclei, which are not found in the Teleostei. In both groups, but
especially in the Teleostei, the tissue is highly vascular, and is
penetrated throughout by a regular plexus of very large capillaries, which
appear to have distinct walls, and which pour their blood into the
posterior cardinal vein as it passes through the organ. The relation of
this tissue to the lymphatic system I have not made out.
The function of the tissue is far from clear. Its great abundance, highly
vascular character, and presence before the atrophy of the pronephros,
appear to me to shew that it cannot be merely the non-absorbed remnant of
the latter organ. From its size and vascularity it probably has an
important function; and from its structure this must either be the
formation of lymph corpuscles or of blood corpuscles.
In structure it most resembles a lymphatic gland, though, till it has been
shewn to have some relation to the lymphatic system, this can go for very
little.
On the whole, I am provisionally inclined to regard it as a form of
lymphatic gland, these bodies being not otherwise represented in fishes.
XXIV.--A RENEWED STUDY OF THE GERMINAL LAYERS OF THE CHICK.
BY F. M. BALFOUR AND F. DEIGHTON[559].
Footnote 559: From the _Quarterly Journal of Microscopical
Science_, Vol. XXII. N. S. 1882.
(With Plates 43, 44, 45.)
The formation of the germinal layers in the chick has been so often and so
fully dealt with in recent years, that we consider some explanation to be
required of the reasons which have induced us to add to the long list of
memoirs on this subject. Our reasons are twofold. In the first place the
principal results we have to record have already been briefly put forward
in a _Treatise on Comparative Embryology_ by one of us; and it seemed
desirable that the data on which the conclusions there stated rest should
be recorded with greater detail than was possible in such a treatise. In
the second place, our observations differ from those of most other
investigators, in that they were primarily made with the object of testing
a theory as to the nature of the primitive streak. As such they form a
contribution to comparative embryology; since our object has been to
investigate how far the phenomena of the formation of the germinal layers
in the chick admit of being compared with those of lower and less modified
vertebrate types.
We do not propose to weary the reader by giving a new version of the often
told history of the views of various writers on the germinal layers in the
chick, but our references to other investigators will be in the main
confined to a comparison of our results with those of two embryologists who
have published their memoirs since our observations were made. One of them
is L. Gerlach, who published a short memoir[560] in April last, and the
other is C. Koller, who has published his memoir[561] still more recently.
Both of them cover part of the ground of our investigations, and their
results are in many, though not in all points, in harmony with our own.
Both of them, moreover, lay stress on certain features in the development
which have escaped our attention. We desired to work over these points
again, but various circumstances have prevented our doing so, and we have
accordingly thought it best to publish our observations as they stand, in
spite of their incompleteness, merely indicating where the most important
gaps occur.
Footnote 560: "Ueb. d. entodermale Entstehungsweise d. Chorda
dorsalis," _Biol. Centralblatt_, Vol. 1. Nos. 1 and 2.
Footnote 561: "Untersuch. üb. d. Blätterbildung im
Hühnerkeim," _Archiv f. mikr. Anat._ Vol. XX. 1881.
Our observations commence at a stage a few hours after hatching, but before
the appearance of the primitive streak.
The area pellucida is at this stage nearly spherical. In it there is a
large oval opaque patch, which is continued to the hinder border of the
area. This opaque patch has received the name of the embryonic shield--a
somewhat inappropriate name, since the structure in question has no very
definite connection with the formation of the embryo.
Koller describes, at this stage, in addition to the so-called embryonic
shield, a sickle-shaped opaque appearance at the hinder border of the area
pellucida.
We have not made any fresh investigations for the purpose of testing
Koller's statements on this subject.
Embryologists are in the main agreed as to the structure of the blastoderm
at this stage. There is (Pl. 43, Ser. A, 1 and 2) the epiblast above,
forming a continuous layer, extending over the whole of the area opaca and
area pellucida. In the former its cells are arranged as a single row, and
are cubical or slightly flattened. In the latter the cells are more
columnar, and form, in the centre especially, more or less clearly, a
double row; many of them, however, extend through the whole thickness of
the layer.
We have obtained evidence at this stage which tends to shew that at its
outer border the epiblast grows not merely by the division of its own
cells, but also by the addition of cells derived from the yolk below. The
epiblast has been observed to extend itself over the yolk by a similar
process in many invertebrate forms.
Below the epiblast there is placed, in the peripheral part of the area
opaca, simply white yolk; while in a ring immediately outside and
concentric with the area pellucida, there is a closely-packed layer of
cells, known as the _germinal wall_. The constituent cells of this wall are
in part relatively small, of a spherical shape, with a distinct nucleus,
and a granular and not very abundant protoplasm; and in part large and
spherical, filled up with highly refracting yolk particles of variable
size, which usually render the nucleus (which is probably present)
invisible (A, 1 and 2). This mass of cell rests, on its outer side, on a
layer of white yolk.
The sickle-shaped structure, visible in surface veins, is stated by Koller
to be due to a special thickening of the germinal wall. We have not found
this to be a very distinctly marked structure in our sections.
In the region of the area pellucida there is placed below the epiblast a
more or less irregular layer of cells. This layer is continuous,
peripherally, with the germinal wall; and is composed of cells, which are
distinguished both by their flattened or oval shape and more granular
protoplasm from the epiblast-cells above, to which, moreover, they are by
no means closely attached. Amongst these cells a few larger cells are
usually present, similar to those we have already described as forming an
important constituent of the germinal wall.
We have figured two sections of a blastoderm of this age (Ser. A, 1 and 2)
mainly to shew the arrangement of these cells. A large portion of them,
considerably more flattened than the remainder, form a continuous membrane
over the whole of the area pellucida, except usually for a small area in
front, where the membrane is more or less interrupted. This layer is the
hypoblast (_hy._). The remaining cells are interposed between this layer
and the epiblast. In front of the embryonic shield there are either
comparatively few or none of these cells present (Ser. A, 1), but in the
region of the embryonic shield they are very numerous (Ser. A, 2), and are,
without doubt, the main cause of the opacity of this part of the area
pellucida. These cells may be regarded as not yet completely differentiated
segmentation spheres.
In many blastoderms, not easily distinguishable in surface views from those
which have the characters just described, the hypoblastic sheet is often
much less completely differentiated, and we have met with other
blastoderms, again, in which the hypoblastic sheet was completely
established, except at the hinder part of the embryonic shield; where, in
place of it and of the cells between it and the epiblast, there was only to
be found a thickish layer of rounded cells, continuous behind with the
germinal wall.
In the next stage, of which we have examined surface views and sections,
there is already a well-formed primitive streak.
The area pellucida is still nearly spherical, the embryonic shield has
either disappeared or become much less obvious, but there is present a dark
linear streak, extending from the posterior border of the area pellucida
towards the centre, its total length being about one third, or even less,
of the diameter of the area. This streak is the _primitive streak_. It
enlarges considerably behind, where it joins the germinal wall. By Koller
and Gerlach it is described as joining the sickle-shaped structure already
spoken of. We have in some instances found the posterior end of the
primitive streak extending laterally in the form of two wings (Pl. 45,
fig. L). These extensions are, no doubt, the sickle; but the figures given
by Koller appear to us somewhat diagrammatic. One or two of the figures of
early primitive streaks in the sparrow, given by Kupffer and Benecke[562],
correspond more closely with what we have found, except that in these
figures the primitive streak does not reach the end of the area pellucida,
which it certainly usually does at this early stage in the chick.
Footnote 562: "Photogramme d. Ontogenie d. Vogel." Nova Acta.
K. Leop. Carol, _Deutschen Akad. d. Naturfor_. Bd. X. 41,
1879.
Sections through the area pellucida (Pl. 43, Ser. B and C) give the
following results as to the structure of its constituent parts.
The epiblast cells have undergone division to a considerable extent, and in
the middle part, especially, are decidedly more columnar than at an earlier
stage, and distinctly divided into two rows, the nuclei of which form two
more or less distinct layers.
In the region in front of the primitive streak the cells of the lower part
of the blastoderm have arranged themselves as a definite layer, the cells
of which are not so flat as is the case with the hypoblast cells of the
posterior part of the blastoderm, and in the older specimens of this stage
they are very decidedly more columnar than in the younger specimens.
The primitive streak is however the most interesting structure in the area
pellucida at this stage.
The feature which most obviously strikes the observer in transverse
sections through it is the fact, proved by Kölliker, that it is mainly due
to a proliferation of the epiblast cells along an axial streak, which,
roughly speaking, corresponds with the dark line visible in surface views.
In the youngest specimens and at the front end of the primitive streak, the
proliferated cells do not extend laterally beyond the region of their
origin, but in the older specimens they have a considerable lateral
extension.
The hypoblast can, in most instances, be traced as a distinct layer
underneath the primitive streak, although it is usually less easy to follow
it in that region than elsewhere, and in some cases it can hardly be
distinctly separated from the superjacent cells.
The cells, undoubtedly formed by a proliferation of the epiblast, form a
compact mass extending downwards towards the hypoblast; but between this
mass and the hypoblast there are almost always present along the whole
length of the primitive streak a number of cells, more or less loosely
arranged, and decidedly more granular than the proliferated cells. Amongst
these loosely arranged cells there are to be found a certain number of
large spherical cells filled with yolk granules. Sometimes these cells are
entirely confined to the region of the primitive streak, at other times
they are continuous laterally with cells irregularly scattered between the
hypoblast and epiblast (Ser. C, 2), which are clearly the remnants of the
undifferentiated cells of the embryonic shield. The junction between these
cells and the cells of the primitive streak derived from the epiblast is
often obscure, the two sets of cells becoming partially intermingled. The
facility with which the cells we have just spoken of can be recognized
varies moreover greatly in different instances. In some cases they are very
obvious (Ser. C), while in other cases they can only be distinguished by a
careful examination of good sections.
The cells of the primitive streak between the epiblast and the hypoblast
are without doubt mesoblastic, and constitute the first portion of the
mesoblast which is established. The section of these cells attached to the
epiblast, in our opinion, clearly originates from the epiblast; while the
looser cells adjoining the hypoblast must, it appears to us, be admitted to
have their origin in the indifferent cells of the embryonic shield, placed
between the epiblast and the hypoblast, and also very probably in a
distinct proliferation from the hypoblast below the primitive streak.
Posteriorly the breadth of the streak of epiblast which buds off the cells
of the primitive streak widens considerably, and in the case of the
blastoderm with the earliest primitive streaks extends into the region of
the area opaca. The widening of the primitive streak behind is shewn in
Ser. B, 3; Ser. C, 2; and Ser. E, 4. Where very marked it gives rise to the
sickle-shaped appearance upon which so much stress has been laid by Koller
and Gerlach. In the case of one of the youngest of our blastoderms of this
stage in which we found in surface views (Pl. 45, fig. L) a very
well-marked sickle-shaped appearance at the hind end of the primitive
streak, the appearance was caused, as is clearly brought out by our
sections, by a thickening of the hypoblast of the germinal wall.
There is a short gap in our observations between the stage with a young
primitive streak and the first described stage in which no such structure
is present. This gap has been filled up both by Gerlach and Koller.
Gerlach states that during this period a small portion of the epiblast,
within the region of the area opaca, but close to the posterior border of
the area pellucida, becomes thickened by a proliferation of its cells. This
portion gradually grows outwards laterally, forming in this way a
sickle-shaped structure. From the middle of this sickle a process next
grows forward into the area pellucida. This process is the primitive
streak, and it is formed, like the sickle, of proliferating epiblast cells.
Koller[563] described the sickle and the growth forwards from it of the
primitive streak in surface views somewhat before Gerlach; and in his later
memoir has entered with considerable detail into the part played by the
various layers in the formation of this structure.
Footnote 563: "Beitr. z. Kenntuiss d. Hühmerkeims im Beginne
d. Bebrütung," _Sitz. d. k. Akad. Wiss._ IV. Abth. 1879.
He believes, as already mentioned, that the sickle-shaped structure, which
appears according to him at an earlier stage than is admitted by Gerlach,
is in the first instance due to a thickening of the hypoblast. At a later
stage he finds that the epiblast in the centre of the sickle becomes
thickened, and that a groove makes its appearance in this thickening which
he calls the "Sichel-rinne." This groove is identical with that first
described by Kupffer and Benecke[564] in the sparrow and fowl. We have
never, however, found very clear indications of it in our sections.
Footnote 564: _Die erste Entwick. an Eier d. Reptilien._
Königsberg. 1878.
In the next stage, Koller states that, in the region immediately in front
of the "Sichel-rinne," a prominence appears which he calls the Sichelknopf,
and from this a process grows forwards which constitutes the primitive
streak. This structure is in main derived from a proliferation of epiblast
cells, but Koller admits that some of the cells just above the hypoblast in
the region of the Sichelknopf are probably derived from the hypoblast.
Since these cells form part of the mesoblast it is obvious that Koller's
views on the origin of the mesoblast of the primitive streak closely
approach those which we have put forward.
The primitive streak starting, as we have seen, at the hinder border of the
area pellucida, soon elongates till it eventually occupies at least
two-thirds of the length of the area. As Koller (_loc. cit._) has stated,
this can only be supposed to happen in one of two ways, viz. either by a
progression forward of the region of epiblast budding off mesoblast, or by
an interstitial growth of the area of budding epiblast. Koller adopts the
second of these alternatives, but we cannot follow him in doing so. The
simplest method of testing the point is by measuring the distance between
the front end of the primitive streak and the front border of the area
pellucida at different stages of growth of the primitive streak. If this
distance diminishes with the elongation of the primitive streak then
clearly the second of the two alternatives is out of the question.
We have made measurements to test this point, and find that the diminution
of the space between the front end of the primitive streak and the anterior
border of the area pellucida is very marked up to the period in which the
medullary plate first becomes established. We can further point in support
of our view to the fact that the extent of the growth lateralwards of the
mesoblast from the sides of the primitive streak is always less in front
than behind; which would seem to indicate that the front part of the streak
is the part formed latest. Our view as to the elongation of the primitive
streak appears to be that adopted by Gerlach.
Our next stage includes roughly the period commencing slightly before the
first formation of a groove along the primitive streak, known as the
primitive groove, and terminating immediately before the first trace of the
notochord makes its appearance. After the close of the last stage the
primitive streak gradually elongates, till it occupies fully two-thirds of
the diameter of the area pellucida. The latter structure also soon changes
its form from a circular to an oval, and finally becomes pyriform with the
narrow end behind, while the primitive streak occupying two-thirds of its
long axis becomes in most instances marked by a light linear band along the
centre, which constitutes the primitive groove.
In surface views the primitive streak often appears to stop short of the
hinder border of the area pellucida.
During the period in which the external changes, which we have thus briefly
described, take place in the area pellucida, great modifications are
effected in the characters of the germinal layers. The most important of
these concern the region in front of the primitive streak; but they will be
better understood if we commence our description with the changes in the
primitive streak itself.
In the older embryos belonging to our last stage we pointed out that the
mesoblast of the primitive streak was commencing to extend outwards from
the median line in the form of two lateral sheets. This growth of the
mesoblast is continued rapidly during the present stage, so that during the
latter part of it any section through the primitive streak has
approximately the characters of Ser. I, 5.
The mesoblast is attached in the median line to the epiblast. Laterally it
extends outwards to the edge of the area pellucida, and in older embryos
may even form a thickening beyond the edge (fig. G). Beneath the denser
part of the mesoblast, and attached to the epiblast, a portion composed of
stellate cells may in the majority of instances be recognized, especially
in the front part of the primitive streak. We believe these stellate cells
to be in the main directly derived from the more granular cells of the
previous stage. The hypoblast forms a sheet of flattened cells, which can
be distinctly traced for the whole breadth of the area pellucida, though
closely attached to the mesoblast above.
In sections we find that the primitive streak extends back to the border of
the area pellucida, and even for some distance beyond. The attachment to
the epiblast is wider behind; but the thickness of the mesoblast is not
usually greater in the median line than it is laterally, and for this
reason probably the posterior part of the streak fails to shew up in
surface views. The thinning out of the median portion of the mesoblast of
the primitive streak is shewn in a longitudinal section of a duck's
blastoderm of this stage (fig. D). The same figure also shews that the
hypoblastic sheet becomes somewhat thicker behind, and more independent of
the parts above.
A careful study of the peripheral part of the area pellucida, in the region
of the primitive streak, in older embryos of this stage, shews that the
hypoblast is here thickened, and that its upper part, _i.e._ that adjoining
the mesoblast, is often formed of stellate cells, many of which give the
impression of being in the act of passing into the mesoblast above. At a
later stage the mesoblast of the vascular area undoubtedly receives
accessions of cells from the yolk below; so that we see no grounds for
mistrusting the appearances just spoken of, or for doubting that they are
to be interpreted in the sense suggested.
We have already stated that during the greater part of the present stage a
groove, known as the primitive groove, is to be found along the dorsal
median line of the primitive streak.
The extent to which this groove is developed appears to be subject to very
great variation. On the average it is, perhaps, slightly deeper than it is
represented in Ser. I, 5. In some cases it is very much deeper. One of the
latter is represented in fig. G. It has here the appearance of a narrow
slit, and sections of it give the impression of the mesoblast originating
from the lips of a fold; in fact, the whole structure appears like a linear
blastopore, from the sides of which the mesoblast is growing out; and this
as we conceive actually to be the true interpretation of the structure.
Other cases occur in which the primitive groove is wholly deficient, or at
the utmost represented by a shallow depression along the median axial line
of a short posterior part of the primitive streak.
We may now pass to the consideration of the part of the area pellucida in
front of the primitive streak.
We called attention to a change in the character of the hypoblast cells of
this region as taking place at the end of the last stage. During the very
early part of this stage the change in the character of these cells becomes
very pronounced.
What we consider to be our earliest stage in this change we have only so
far met with in the duck, and we have figured a longitudinal and median
section to shew it (Pl. 43, fig. D). The hypoblast (_hy_) has become a
thick layer of somewhat cubical cells several rows deep. These cells,
especially in front, are characterized by their numerous yolk spherules,
and give the impression that part of the area pellucida has been, so to
speak, reclaimed from the area opaca. _Posteriorly, at the front end of the
primitive streak, the thick layer of hypoblast, instead of being continuous
with the flattened hypoblast under the primitive streak, falls, in the
axial line, into the mesoblast of the primitive streak_ (Pl. 43, fig. D).
In a slightly later stage, of which we have specimens both of the duck and
chick, but have only figured selected sections of a chick series, still
further changes have been effected in the constitution of the hypoblast
(Pl. 44, Ser. H, 1 and 2).
Near the front border of the area pellucida (1) it has the general
characters of the hypoblast of the duck's blastoderm just described.
Slightly further back the cells of the hypoblast have become differentiated
into stellate cells several rows deep, _which can hardly be resolved in the
axial line into hypoblast and mesoblast_, though one can fancy that in
places, especially laterally, they are partially differentiated into two
layers. The axial sheet of stellate cells is continuous laterally with
cubical hypoblast cells.
As the primitive streak is approached an axial prolongation forwards of the
rounded and closely-packed mesoblastic elements of the primitive streak is
next met with; and at the front end of the primitive streak, where this
prolongation unites with the epiblast, it also becomes continuous with the
stellate cells just spoken of. In fact, close to the end of the primitive
streak it becomes difficult to say which mesoblast cells are directly
derived from the primitive layer of hypoblast in front of the primitive
streak, and which from the forward growth of the mesoblast of the primitive
streak. There is, in fact, as in the earlier stage, a fusion of the layers
at this point.
Sections of a slightly older chick blastoderm are represented in Pl. 45,
Ser. I, 1, 2, 3, 4 and 5.
Nearly the whole of the hypoblast in front of the primitive streak has now
undergone a differentiation into stellate cells. In the second section the
products of the differentiation of this layer form a distinct mesoblast and
hypoblast laterally, while in the median line they can hardly be divided
into two distinct layers.
In a section slightly further back the same is true, except that we have
here, in the axial line above the stellate cells, rounded elements derived
from a forward prolongation of the cells of the primitive streak. In the
next section figured, passing through the front end of the primitive
streak, the axial cells have become continuous with the axial mesoblast of
the primitive streak, while below there is an independent sheet of
flattened hypoblast cells.
The general result of our observations on the part of the blastoderm in
front of the primitive streak during this stage is to shew that the
primitive hypoblast of this region undergoes considerable changes,
including a multiplication of its cells; and that these changes result in
its becoming differentiated on each side of the middle line, with more or
less distinctness, into (1) a hypoblastic sheet below, formed of a single
row of flattened cells, and (2) a mesoblast plate above formed of stellate
cells, while in the middle line there is a strip of stellate cells in which
there is no distinct differentiation into two layers.
Since the region in which these changes take place is that in which the
medullary plate becomes subsequently formed, the lateral parts of the
mesoblast plate are clearly the permanent lateral plates of the trunk, from
which the mesoblastic somites, &c., become subsequently formed; _so that
the main part of the mesoblast of the trunk is not directly derived from
the primitive streak_.
Before leaving this stage we would call attention to the presence, in one
of our blastoderms of this stage, of a deep pit at the junction of the
primitive streak with the region in front of it (Pl. 44, Ser. F, 1 and 2).
Such a pit is unusual, but we think it may be regarded as an exceptionally
early commencement of that most variable structure in the chick, the
neurenteric canal.
The next and last stage we have to deal with is that during which the first
trace of the notochord and of the medullary plate make their appearance.
In surface views this stage is marked by the appearance of a faint dark
line, extending forwards, from the front end of the primitive streak, to a
fold, which has in the mean time made its appearance near the front end of
the area pellucida, and constitutes the head fold.
Pl. 45, Ser. K, represents a series of sections through a blastoderm of
this stage, which have been selected to illustrate the mode of formation of
the notochord.
In a section immediately behind the head fold the median part of the
epiblast is thicker than the lateral parts, forming the first indication of
a medullary plate (Ser. K, 1). Below the median line of the epiblast is a
small cord of cells, not divided into two layers, but continuous laterally,
both with the hypoblast and mesoblast, which are still more distinctly
separated than in the previous stage.
A section or so further back (Ser. K, 2) the axial cord, which we need
scarcely say is the rudiment of the notochord, is thicker, and causes a
slight projection in the epiblast above. It is, as before, continuous
laterally, both with the mesoblast and with the hypoblast. The medullary
plate is more distinct, and a shallow but unmistakable medullary groove has
made its appearance.
As we approach the front end of the primitive streak the notochord becomes
(Ser. K, 3) very much more prominent, though retaining the same relation to
the germinal layers as in front.
In the section immediately behind (Ser. K, 4) the convex upper surface of
the notochord has become continuous with the epiblast for a very small
region. The section, in fact, traverses the front end of the primitive
streak.
In the next section the attachment between the epiblast and the cells below
becomes considerably wider. It will be noticed that this part of the
primitive streak is placed on the floor of the wide medullary groove, and
there forms a prominence known as the anterior swelling of the primitive
streak.
It will further be noticed that in the two sections passing through the
primitive streak, the hypoblast, instead of simply becoming continuous with
the axial thickening of the cells, as in front, forms a more or less
imperfect layer underneath it. This layer becomes in the sections following
still more definite, and forms part of the continuous layer of hypoblast
present in the region of the primitive streak.
A comparison of this stage with the previous one shews very clearly that
the notochord is formed out of the median plate of cells of the earlier
stage, which was not divided into mesoblast and hypoblast, together with
the short column of cells which grew forwards from the primitive streak.
The notochord, from its mode of origin, is necessarily continuous behind
with the axial cells of the primitive streak.
The sections immediately behind the last we have represented shew a
rudiment of the neurenteric canal of the same form as that first figured by
Gasser, viz. a pit perforating the epiblast with a great mass of rounded
cells projecting upwards through it.
* * * * *
The observations just recorded practically deal with two much disputed
points in the ontogeny of birds, viz. the origin of the mesoblast and the
origin of the notochord.
With reference to the first of these our results are briefly as follows:
The first part of the mesoblast to be formed is that which arises in
connection with the primitive streak. This part is in the main formed by a
proliferation from an axial strip of the epiblast along the line of the
primitive streak, but in part also from a simultaneous differentiation of
hypoblast cells also along the axial line of the primitive streak. The two
parts of the mesoblast so formed become subsequently indistinguishable. The
second part of the mesoblast to be formed is that which gives rise to the
lateral plates of mesoblast of the head and trunk of the embryo. This part
appears as two plates--one on each side of the middle line--which arise by
direct differentiation from the hypoblast in front of the primitive streak.
They are continuous behind with the lateral wings of mesoblast which grow
out from the primitive streak, and on their inner side are also at first
continuous with the cells which form the notochord.
In addition to the parts of mesoblast, formed as just described, the
mesoblast of the vascular area is in a large measure developed by a direct
formation of cells round the nuclei of the germinal wall.
The mesoblast formed in connection with the primitive streak gives rise in
part to the mesoblast of the allantois, and ventral part of the tail of the
embryo (?), and in part to the vascular structures found in the area
pellucida.
With reference to the formation of the mesoblast of the primitive streak,
our conclusions are practically in harmony with those of Koller; except
that Koller is inclined to minimise the share taken by the hypoblast in the
formation of the mesoblast of the primitive streak.
Gerlach, with reference to the formation of this part of the mesoblast,
adopts the now generally accepted view of Kölliker, according to which the
whole of the mesoblast of the primitive streak is derived from the
epiblast.
As to the derivation of the lateral plates of mesoblast of the trunk from
the hypoblast of the anterior part of the primitive streak, our general
result is in complete harmony with Gerlach's results, although in our
accounts of the details of the process we differ in some not unimportant
particulars.
As to the origin of the notochord, our main result is that this structure
is formed as an actual thickening of the primitive hypoblast of the
anterior part of the area pellucida. We find that it unites posteriorly
with a forward growth of the axial tissue of the primitive streak, while it
is laterally continuous, at first, both with the mesoblast of the lateral
plates and with the hypoblast. At a later period its connection with the
mesoblast is severed, while the hypoblast becomes differentiated as a
continuous layer below it.
As to the hypoblastic origin of the notochord, we are again in complete
accord with Gerlach; but we differ from him in admitting that the notochord
is continuous posteriorly with the axial tissue of the primitive streak,
and also at first continuous with the lateral plates of mesoblast.
The account we have given of the formation of the mesoblast may appear to
the reader somewhat fantastic, and on that account not very credible. We
believe, however, that if the view which has been elsewhere urged by one of
us, that the primitive streak is the homologue of the blastopore of the
lower vertebrates is accepted, the features we have described receive an
adequate explanation.
The growth outwards of part of the mesoblast from the axial line of the
primitive streak is a repetition of the well-known growth from the lips of
the blastopore. It might have been anticipated that all the layers would
fuse along the line of the primitive streak, and that the hypoblast as well
as part of the mesoblast would grow out from it. There is, however, clearly
a precocious formation of the hypoblast; but the formation of the mesoblast
of the primitive streak, partly from the epiblast and partly from the
hypoblast, is satisfactorily explained by regarding the whole structure as
the blastopore. The two parts of the mesoblast subsequently become
indistinguishable, and their difference in origin is, on the above view, to
be regarded as simply due to a difference of position, and not as having a
deeper significance.
The differentiation of the lateral plates of mesoblast of the trunk
directly from the hypoblast is again a fundamental feature of vertebrate
embryology, occurring in all types from Amphioxus upwards, the meaning of
which has been fully dealt with in the _Treatise on Comparative Embryology_
by one of us. Lastly, the formation of the notochord from the hypoblast is
the typical vertebrate mode of formation of this organ, while the fusion of
the layers at the front end of the primitive streak is the universal fusion
of the layers at the dorsal lip of the blastopore, which is so well known
in the lower vertebrate types.
EXPLANATION OF PLATES 43-45.
N. B. The series of sections are in all cases numbered from before
backwards.
LIST OF REFERENCE LETTERS.
_a.p._ Area pellucida. _ep._ Epiblast. _ch._ Notochord. _gr._ Germinal
wall. _hy._ Hypoblast. _m._ Mesoblast. _o.p._ Area opaca. _pr.g._ Primitive
groove. _pvs._ Primitive streak. _yk._ Yolk of germinal wall.
PLATE 43.
SERIES A, 1 and 2. Sections through the blastoderm before the appearance of
primitive streak.
1. Section through anterior part of area pellucida in front of embryonic
shield. The hypoblast here forms an imperfect layer. The figure represents
about half the section. 2. Section through same blastoderm, in the region
of the embryonic shield. Between the epiblast and hypoblast are a number of
undifferentiated cells. The figure represents considerably more than half
the section.
SERIES B, 1, 2 and 3. Sections through a blastoderm with a very young
primitive streak.
1. Section through the anterior part of the area pellucida in front of the
primitive streak. 2. Section through about the middle of the primitive
streak. 3. Section through the posterior part of the primitive streak.
SERIES C, 1 and 2. Sections through a blastoderm with a young primitive
streak.
1. Section through the front end of the primitive streak. 2. Section
through the primitive streak, somewhat behind 1. Both figures shew very
clearly the difference in character between the cells of the epiblastic
mesoblast of the primitive streak, and the more granular cells of the
mesoblast derived from the hypoblast.
FIG. D. Longitudinal section through the axial line of the primitive
streak, and the part of the blastoderm in front of it, of an embryo duck
with a well-developed primitive streak.
PLATE 44.
SERIES E, 1, 2, 3 and 4. Sections through blastoderm with a primitive
streak, towards the end of the first stage.
1. Section through the anterior part of the area pellucida. 2. Section a
little way behind 1 shewing a forward growth of mesoblast from the
primitive streak. 3. Section through primitive streak. 4. Section through
posterior part of primitive streak, shewing the great widening of primitive
streak behind.
SERIES F, 1 and 2. Sections through a blastoderm with primitive groove.
1. Section shewing a deep pit in front of primitive streak, probably an
early indication of the neurenteric canal. 2. Section immediately following
1.
FIG. G. Section through blastoderm with well-developed primitive streak,
shewing an exceptionally deep slit-like primitive groove.
SERIES H, 1 and 2. Sections through a blastoderm with a fully-developed
primitive streak.
1. Section through the anterior part of area pellucida, shewing the cubical
granular hypoblast cells in this region. 2. Section slightly behind 1,
shewing the primitive hypoblast cells differentiated into stellate cells,
which can hardly be resolved in the middle line into hypoblast and
mesoblast.
PLATE 45.
SERIES I, 1, 2, 3, 4 and 5. Sections through blastoderm somewhat older than
Series H.
1. Section through area pellucida well in front of primitive streak. 2.
Section through area pellucida just in front of primitive streak. 3.
Section through the front end of primitive streak. 4. Section slightly
behind 3. 5. Section slightly behind 4.
SERIES K, 1, 2, 3, 4 and 5. Sections through a blastoderm in which the
first traces of notochord and medullary groove have made their appearance.
Rather more than half the section is represented in each figure, but the
right half is represented in 1 and 3, and the left in 2 and 4.
1. Section through notochord immediately behind the head fold. 2. Section
shewing medullary groove a little behind 1. 3. Section just in front of the
primitive streak. 4 and 5. Sections through the front end of the primitive
streak.
FIG. L. Surface view of blastoderm with a very young primitive streak.
XXV. THE ANATOMY AND DEVELOPMENT OF PERIPATUS CAPENSIS[565].
Footnote 565: From the _Quarterly Journal of Microscopical
Science_, April, 1883.
(With Plates 46-53.)
INTRODUCTION.
The late Professor Balfour was engaged just before his death in
investigating the structure and embryology of _Peripatus capensis_, with
the view of publishing a complete monograph of the genus. He left numerous
drawings intended to serve as illustrations to the monograph, together with
a series of notes and descriptions of a large part of the anatomy of
_Peripatus capensis_. Of this manuscript some portions were ready for
publication, others were more or less imperfect; while of the figures many
were without references, and others were provided with only a few words of
explanation.
It was obviously necessary that Professor Balfour's work--embodying as it
did much important discovery--should be published without delay; and the
task of preparing his material for the press was confided to us. We have
printed all his notes and descriptions without alteration[566].
Explanations which appeared to be necessary, and additions to the text in
cases in which he had prepared figures without writing descriptions,
together with full descriptions of all the plates, have been added by us,
and are distinguished by enclosure in square brackets[567].
Footnote 566: Excepting in an unimportant matter of change of
nomenclature used with regard to the buccal cavity.
Footnote 567: The account of the external characters,
generative organs, and development, has been written by the
editors.
We have to thank Miss Balfour, Professor Balfour's sister, for the
important service which she has rendered by preparing a large part of the
beautiful drawings with which the monograph is illustrated. Many of these
had been executed by her under Professor Balfour's personal supervision;
and the knowledge of his work which she then acquired has been of the
greatest assistance to us in preparing the MSS. and drawings for
publication.
Since his death she has spared no pains in studying the structure of
_Peripatus_, so as to enable us to bring out the first part of the
monograph in as complete a state as possible. It is due to her skill that
the first really serviceable and accurate representation of the legs of any
species of _Peripatus_ available for scientific purposes are issued with
the present memoir[568].
Footnote 568: The drawings on Pl. 47, figs. 9 and 10 on Pl. 48,
and the drawings of the embryos (except fig. 37), have been
made by Miss Balfour since Professor Balfour's death.
We have purposely refrained from introducing comments on the general
bearing of the new and important results set forth in this memoir, and have
confined ourselves to what was strictly necessary for the presentation of
Mr Balfour's discoveries in a form in which they could be fully
comprehended.
Mr Balfour had at his disposal numerous specimens of _Peripatus novæ
zealandiæ_, collected for him by Professor Jeffrey Parker, of Christchurch,
New Zealand; also specimens from the Cape of Good Hope collected by Mr
Lloyd Morgan, and brought to England by Mr Roland Trimen in 1881; and
others given to him by Mr Wood Mason, together with all the material
collected by Mr Moseley during the "Challenger" voyage.
A preliminary account of the discoveries as to the embryology of
_Peripatus_ has already been communicated to the Royal Society[569]. It is
intended that the present memoir shall be followed by others, comprising a
complete account of all the species of the genus _Peripatus_.
H. M. MOSELEY.
A. SEDGWICK.
Footnote 569: _Proc. Royal Soc._ 1883.
PART I.
DESCRIPTION OF THE SPECIES.
_Peripatus capensis_ (fig. 1).
[The body is elongated, and slightly flattened dorso-ventrally. The dorsal
surface is arched, and darkly pigmented; while the ventral surface is
nearly flat, and of a lighter colour.
The mouth is placed at the anterior end of the body, on the ventral
surface.
The anus is posterior and terminal.
The generative opening is single and median, and placed in both sexes on
the ventral surface, immediately in front of the anus.
There are a pair of ringed antennæ projecting from the anterior end of the
head, and a pair of simple eyes, placed on the dorsal surface at the roots
of the antennæ.
The appendages of the body behind the antennæ are disposed in twenty pairs.
1. The single pair of jaws placed within the buccal cavity in front of the
true mouth opening, and consisting each of a papilla, armed at its
termination with two cutting blades.
2. The oral papillæ placed on each side of the mouth. At their apices the
ducts of the slime glands open.
3. The seventeen pairs of ambulatory appendages, each provided with a pair
of chitinous claws at its extremity.
4. The anal papillæ placed on each side of the generative opening.
_Colour._--The following statements on this head are derived from
observations of spirit specimens. The colour varies in different
individuals. It always consists of a groundwork of green and bluish grey,
with a greater or less admixture of brown. The chief variations in the
appearance of the animal, so far as colour is concerned, depend on the
shade of the green. In some it is dark, as in the specimen figured
(fig. 1); in others it is of a lighter shade.
There is present in most specimens a fairly broad light band on each side
of the body, immediately dorsal to the attachment of the legs. This band is
more prominent in the lighter coloured varieties than in the dark, and is
especially conspicuous in large individuals. It is due to a diminution in
the green pigment, and an increase in the brown.
There is a dark line running down the middle of the dorsal surface, in the
middle of which is a fine whitish line.
The ventral surface is almost entirely free from the green pigment, but
possesses a certain amount of light brown. This brown pigment is more
conspicuous and of a darker shade on the spinous pads of the foot.
In parts of the body where the pigment is scarce, it is seen to be confined
to the papillæ. This is especially evident round the mouth, where the
sparse green pigment is entirely confined to the papillæ.
In some specimens a number of white papillæ, or perhaps light brown, are
scattered over the dorsal surface; and sometimes there is a scattering of
green papillæ all over the ventral surface. These two peculiarities are
more especially noticeable in small specimens.
_Ridges and Papillæ of the Skin._--The skin is thrown into a number of
transverse ridges, along which the primary wart-like papillæ are placed.
The papillæ, which are found everywhere, are specially developed on the
dorsal surface, less so on the ventral. The papillæ round the lips differ
from the remaining papillæ of the ventral surface in containing a green
pigment. Each papilla bears at its extremity a well-marked spine.
The ridges of the skin are not continued across the dorsal middle line,
being interrupted by the whitish line already mentioned. Those which lie in
the same transverse line as the legs are not continued on to the latter,
but stop at the junction of the latter with the body. All the others pass
round to the ventral surface and are continued across the middle line; they
do not, however, become continuous with the ridges of the other side, but
passing between them gradually thin off and vanish.
The ridges on the legs are directed transversely to their long axes, _i.e._
are at right angles to the ridges of the rest of the body.
The antennæ are ringed and taper slightly till near their termination,
where they present a slight enlargement in spirit specimens, which in its
turn tapers to its termination.
The rings consist essentially of a number of coalesced primary papillæ, and
are, therefore, beset by a number of spines like those of the primary
papillæ (described below). They are more deeply pigmented than the rest of
the antenna.
The free end of the antenna is covered by a cap of tissue like that of the
rings. It is followed by four or more rings placed close together on the
terminal enlargement. There appears to be about thirty rings on the antennæ
of all adults of this species. But they are difficult to count, and a
number of small rings occur between them, which are not included in the
thirty.
The antennæ are prolongations of the dorso-lateral parts of the anterior
end of the body.
The eyes are paired and are situated at the roots of the antennæ on the
dorso-lateral parts of the head. Each is placed on the side of a
protuberance which is continued as the antenna, and presents the appearance
of a small circular crystalline ball inserted on the skin in this region.
The rings of papillæ on that part of the head from which the antennæ arise
lose their transverse arrangement. They are arranged concentrically to the
antennal rings, and have a straight course forwards between the antennæ.
The oral papillæ are placed at the side of the head. They are attached
ventro-laterally on each side of the lips. The duct of the slime gland
opens through their free end. They possess two main rings of projecting
tissue, which are especially pigmented on the dorsal side; and their
extremities are covered by papillæ irregularly arranged.
The buccal cavity, jaws, and lips are described below.
_The Ambulatory Appendages._--The claw-bearing legs are usually seventeen
in number; but in two cases of small females we have observed that the anal
papillæ bear claws, and present all the essential features of the
ambulatory appendages. In one small female specimen there were twenty pairs
of claw-bearing appendages, the last being like the claw-bearing anal
papillæ last mentioned, and the generative opening being placed between
them.
The ambulatory appendages, with the exception of the fourth and fifth pairs
in both sexes, and the last pair (seventeenth) in the male, all resemble
each other fairly closely. A typical appendage (figs. 2 and 3) will first
be described, and the small variations found in the appendages just
mentioned will then be pointed out. Each consists of two main divisions, a
larger proximal portion, the leg, and a narrow distal claw-bearing portion,
the foot.
The leg has the form of a truncated cone, the broad end of which is
attached to the ventro-lateral body-wall, of which it appears to be, and
is, a prolongation. It is marked by a number of rings of primary papillæ,
placed transversely to the long axis of the leg, the dorsal of which
contain a green and the ventral a brown pigment. These rings of papillæ, at
the attachment of the leg, gradually change their direction and merge into
the body rings. At the narrow end of the cone there are three ventrally
placed pads, in which the brown pigment is dark, and which are covered by a
number of spines precisely resembling the spines of the primary papillæ.
These spinous pads are continued dorsally, each into a ring of papillæ.
The papillæ of the ventral row next the proximal of these spinous pads are
intermediate in character between the primary papillæ and the spinous pads.
Each of these papillæ is larger than a normal papilla, and bears several
spines (fig. 2). This character of the papilla of this row is even more
marked in some of the anterior legs than in the one figured; it seems
probable that the pads have been formed by the coalescence of several rows
of papillæ on the ventral surface of the legs. On the outer and inner sides
of these pads the spines are absent, and secondary papillæ only are
present.
In the centre of the basal part of the ventral surface of the foot there
are present a group of larger papillæ, which are of a slightly paler colour
than the others. They are arranged so as to form a groove, directed
transversely to the long axis of the body, and separated at its internal
extremity by a median papilla from a deep pit which is placed at the point
of junction of the body and leg. The whole structure has the appearance,
when viewed with the naked eye, of a transverse slit placed at the base of
the leg. The segmental organs open by the deep pit placed at the internal
end of this structure. The exact arrangement of the papillæ round the outer
part of the slit does not appear to be constant.
The foot is attached to the distal end of the leg. It is slightly narrower
at its attached extremity than at its free end, which bears the two claws.
The integument of the foot is covered with secondary papillæ, but spines
and primary papillæ are absent, except at the points now to be described.
On each side of the middle ventral line of the proximal end of the foot is
placed an elliptical elevation of the integument covered with spines.
Attached to the proximal and lateral end of this is a primary papilla. At
the distal end of the ventral side of the foot on each side of the middle
line is a group of inconspicuous pale elevations, bearing spines.
On the front side of the distal end of the foot, close to the socket in
which the claws are placed, are two primary papillæ, one dorsal and the
other ventral.
On the posterior side of the foot the dorsal of these only is present. The
claws are sickle-shaped, and placed on papillæ on the terminal portion of
the foot. The part of the foot on which they are placed is especially
retractile, and is generally found more or less telescoped into the
proximal part (as in the figure).
The fourth and fifth pairs of legs exactly resemble the others, except in
the fact that the proximal pad is broken up into three, a small central and
two larger lateral. The enlarged segmental organs of these legs open on the
small central division.
The last (17) leg of the male (Pl. 47, fig. 4) is characterized by
possessing a well-marked white papilla on the ventral surface. This
papilla, which presents a slit-like opening at its apex, is placed on the
second row of papillæ counting from the innermost pad, and slightly
posterior to the axial line of the leg.
The anal papillæ, or as they should be called, generative papillæ, are
placed one on each side of the generative aperture. They are most marked in
small and least so in large specimens. That they are rudimentary ambulatory
appendages is shewn by the fact that they are sometimes provided with
claws, and resemble closely the anterior appendages.]
PART II.
ALIMENTARY CANAL.
The alimentary canal of _Peripatus capensis_ forms, in the extended
condition of the animal, a nearly straight tube, slightly longer than the
body, the general characters of which are shewn in figs. 6 and 7.
For the purposes of description, it may conveniently be divided into five
regions, viz. (1) the buccal cavity with the tongue, jaws, and salivary
glands, (2) pharynx, (3) the oesophagus, (4) the stomach, (5) the rectum.
_The Buccal Cavity._--The buccal cavity has the form of a fairly deep pit,
of a longitudinal oval form, placed on the ventral surface of the head, and
surrounded by a tumid lip.
[The buccal cavity has been shewn by Moseley to be formed in the embryo by
the fusion of a series of processes surrounding the true mouth-opening, and
enclosing in their fusion the jaws.]
The lip is covered by a soft skin, in which are numerous organs of touch,
similar to those in other parts of the skin having their projecting
portions enclosed in delicate spines formed by the cuticle. The skin of the
lips differs, however, from the remainder of the skin, in the absence of
tubercles, and in the great reduction of the thickness of the dermis. It is
raised into a series of papilliform ridges, whose general form is shewn in
fig. 5; of these there is one unpaired and median behind, and a pair,
differing somewhat in character from the remainder, in front, and there
are, in addition, seven on each side.
The structures within the buccal cavity are shewn as they appear in surface
views in figs. 5 and 7, but their real nature is best seen in sections, and
is illustrated by Pl. 49, figs. 11 and 12, representing the oral cavity in
transverse section, and by Pl. 49, figs. 17 and 18, representing it in
horizontal longitudinal sections. In the median line of the buccal cavity
in front is placed a thick muscular protuberance, which may perhaps
conveniently be called the tongue, though attached to the dorsal instead of
the ventral wall of the mouth. It has the form of an elongated ridge, which
ends rather abruptly behind, becoming continuous with the dorsal wall of
the pharynx. Its projecting edge is armed by a series of small teeth, which
are thickenings of the chitinous covering, prolonged from the surface of
the body over the buccal cavity. Where the ridge becomes flatter behind,
the row of teeth divides into two, with a shallow groove between them
(Pl. 48, fig. 7).
The surface of the tongue is covered by the oral epithelium, in parts of
which are organs of special sense, similar to those in the skin; but its
interior is wholly formed of powerful muscles. The muscles form two groups,
intermingled amongst each other. There are a series of fibres inserted in
the free edge of the tongue, which diverge, more or less obliquely, towards
the skin at the front of the head anteriorly, and towards the pharynx
behind. The latter set of fibres are directly continuous with the radial
fibres of the pharynx. The muscular fibres just described are clearly
adapted to give a sawing motion to the tongue, whose movements may thus, to
a certain extent, be compared to those of the odontophore of a mollusc.
In addition to the above set of muscles, there are also transverse muscles,
forming laminæ between the fibres just described. They pass from side to
side across the tongue, and their action is clearly to narrow it, and so
cause it to project outwards from the buccal cavity.
On each side of the tongue are placed the jaws, which are, no doubt, a pair
of appendages, modified in the characteristic arthropodan manner, to
subserve mastication. Their structure has never been satisfactorily
described, and is very complicated. They are essentially short papillæ,
moved by an elaborate and powerful system of muscles, and armed at their
free extremities by a pair of cutting blades or claws. The latter
structures are, in all essential points, similar to the claws borne by the
feet, and, like these, are formed as thickenings of the cuticle. They have
therefore essentially the characters of the claws and jaws of the
Arthropoda, and are wholly dissimilar to the setæ of Chætopoda. The claws
are sickle-shaped and, as shewn in Pl. 47, fig. 5, have their convex edge
directed nearly straight forwards, and their concave or cutting edge
pointed backwards. Their form differs somewhat in the different species,
and, as will be shewn in the systematic part of this memoir[570], forms a
good specific character. In _Peripatus capensis_ (Pl. 48, fig. 10) the
cutting surface of the outer blade is smooth and without teeth, while that
of the inner blade (fig. 9), which is the larger of the two, is provided
with five or six small teeth, in addition to the main point. A more
important difference between the two blades than that in the character of
the cutting edge just spoken of, is to be found in their relation to the
muscles which move them. The anterior parts of both blades are placed on
two epithelial ridges, which are moved by muscles common to both blades
(Pl. 49, fig. 11). Posteriorly, however, the behaviour of the two blades is
very different. The epithelial ridge bearing the outer blade is continued
back for a short distance behind the blade, but the cuticle covering it
becomes very thin, and it forms a simple epithelial ridge placed parallel
to the inner blade. The cuticle covering the epithelial ridge of the inner
blade is, on the contrary, prolonged behind the blade itself as a thick
rod, which, penetrating backwards along a deep pocket of the buccal
epithelium, behind the main part of the buccal cavity for the whole length
of the pharynx, forms a very powerful lever, on which a great part of the
muscles connected with the jaws find their insertion. The relations of the
epithelial pocket bearing this lever are somewhat peculiar.
Footnote 570: Some material for this memoir was left by Prof.
Balfour, which will be published separately.
The part of the epithelial ridge bearing the proximal part of this lever is
bounded on both its outer and inner aspect by a deep groove. The wall of
the outer groove is formed by the epithelial ridge of the outer blade, and
that of the inner by a special epithelial ridge at the side of the tongue.
Close to the hinder border of the buccal cavity (as shewn in Pl. 49,
fig. 12, on the right hand side), the outer walls of these two grooves meet
over the lever, so as completely to enclose it in an epithelial tube, and
almost immediately behind this point the epithelial tube is detached from
the oral epithelium, and appears in section as a tube with a chitinous rod
in its interior, lying freely in the body-cavity (shewn in Pl. 49, figs.
13-16, _le_). This apparent tube is the section of the deep pit already
spoken of. It may be traced back even beyond the end of the pharynx, and
serves along its whole length for the attachment of muscles.
The greater part of the buccal cavity is filled with the tongue and jaws
just described. It opens dorsally and behind by the mouth into the pharynx,
there being no sharp line of demarcation between the buccal cavity and the
pharynx. Behind the opening into the pharynx there is a continuation of the
buccal cavity shewn in transverse section in fig. 13, and in longitudinal
and horizontal section in fig. 17, into which there opens the common
junction of the two salivary glands. This diverticulum is wide at first and
opens by a somewhat constricted mouth into the pharynx above (Pl. 49,
fig. 13, also shewn in longitudinal and horizontal section in fig. 17).
Behind it narrows, passing insensibly into what may most conveniently be
regarded as a common duct for the two salivary glands (Pl. 49, fig. 17).
_The Salivary Glands._--These two bodies were originally described by
Grube, by whom their nature was not made out, and subsequently by Moseley,
who regarded them as fat bodies. They are placed in the lateral
compartments of the body-cavity immediately dorsal to the ventral nerve
cords, and extend for a very variable distance, sometimes not more than
half the length of the body, and in other instances extending for nearly
its whole length. Their average length is perhaps about two-thirds that of
the body. Their middle portion is thickest, and they thin off very much
behind and to a slight extent in front. Immediately behind the mouth and in
front of the first pair of legs, they bend inwards and downwards, and fall
(fig. 7) one on each side into the hind end of the narrow section of the
oral diverticulum just spoken of as the common duct for the two salivary
glands. The glandular part of these organs is that extending back from the
point where they bend inwards. This part (fig. 16) is formed of very
elongated cells supported by a delicate membrana propria. The section of
this part is somewhat triangular, and the cells are so long as to leave a
comparatively small lumen. The nuclei of the cells are placed close to the
supporting membrane, and the remainder of the cells are filled with very
closely packed secretory globules, which have a high index of refraction.
It was the presence of these globules which probably led Moseley to regard
the salivary glands as fat bodies. The part of each gland which bends
inwards must be regarded as the duct.
The cells lining the ducts are considerably less columnar than those of the
gland proper. Their nuclei (fig. 14) are situated at the free extremities
instead of at the base of the cells, and they are without secretory
globules. The cells lining the ducts of the salivary glands pass, without
any sharp line of demarcation, into those of the oral epithelium, which are
flatter and have their nuclei placed in the middle.
_The Pharynx._--The Pharynx is a highly muscular tube (fig. 7) with a
triangular lumen (figs. 14, 15), which extends from the mouth to about half
way between the first and second pair of legs. It is lined by a flattish
epithelium bounded by a cuticle continuous with that of the mouth. On the
dorsal side is a ridge projecting into the lumen of the pharynx. This ridge
may be traced forwards (Pl. 49, figs. 11-14) into the tongue, and the two
grooves at the side of this ridge, forming the two upper angles of the
triangular lumen, may be followed into those at the sides of the tongue.
The muscles of the pharynx are very highly developed, consisting of an
intrinsic and an extrinsic set. The former consists, as is best seen in
longitudinal sections, of (Pl. 51, fig. 23) radial fibres, arranged in
somewhat wedge-shaped laminæ, between which are rings of circular fibres.
The latter are thicker externally than internally, and so also appear
wedge-shaped in longitudinal sections. Very characteristic of the pharynx
are the two sympathetic nerves placed close to the two dorsal angles of the
triangular lumen (fig. 14, _sy_).
The pharynx of Peripatus is interesting in that it is unlike, so far as I
know, the pharynx of any true Arthropod, in all of which the region
corresponding with the pharynx of Peripatus is provided with relatively
very thin walls.
The pharynx of Peripatus has, on the other hand, a very close and obvious
resemblance to that of many of the Chætopoda, a resemblance which is
greatly increased by the characteristic course of the sympathetic nerves.
The form of the lumen, as already pointed out by Grube, resembles that of
the Nematoda.
_The OEsophagus._--Behind the pharynx there follows a narrow oesophagus
(fig. 7, _oe_) shewn in section in fig. 16. It has somewhat folded and
fairly thick walls, and lies freely in the central division of the
body-cavity without any mesenteric support. Its walls are formed of five
layers, viz. from without inwards.
(1) A peritoneal investment.
(2) A layer of longitudinal fibres.
(3) A layer of circular fibres, amongst which are numerous nuclei.
(4) A connective-tissue layer supporting (5) a layer of fairly columnar
hyaline epithelium, bounded on its inner aspect by a cuticle continued from
that of the pharynx. In front it passes insensibly into the pharynx, and
beyond the region where the dorsal walls of the pharynx have clearly
commenced, the ventral walls still retain the characters of the oesophageal
walls. The oesophagus is vertically oval in front, but more nearly circular
behind. Characteristic of the oesophagus is the junction of the two
sympathetic nerves on its dorsal wall (fig. 16). These nerves cannot be
traced far beyond their point of junction.
_The Stomach._--The next section of the alimentary tract is the stomach or
mesenteron (fig. 6). It is by far the largest part of the alimentary tract,
commencing at about the second pair of legs and extending nearly to the
hind end of the body. It tapers both in front and behind, and is narrowest
in the middle, and is marked off sharply both from the oesophagus in front
and the rectum behind, and is distinguished from both of these by its
somewhat pinker hue. In the retracted condition of the animal it is, as
pointed out by Moseley, folded in a single short dorsal loop, at about the
junction of its first with its second third, and also, according to my
observations, at its junction with the rectum; but in the extended
condition it is nearly straight, though usually the posterior fold at the
junction of the rectum is not completely removed. Its walls are always
marked by plications which, as both Moseley and Grube have stated, do not
in any way correspond with the segmentation of the body. In its interior I
have frequently found the chitinous remains of the skins of insects, so
that we are not justified in considering that the diet is purely vegetable.
It lies free, and is, like the remainder of the alimentary tract, without a
mesentery. The structure of the walls of the stomach has not hitherto been
very satisfactorily described.
The connective tissue and muscular coats are extremely thin. There is
present everywhere a peritoneal covering, and in front a fairly well-marked
though very thin layer of muscles formed of an external circular and an
internal longitudinal layer. In the middle and posterior parts, however, I
was unable to recognize these two layers in section; although in surface
view Grube found an inner layer of circular fibres and an outer layer
formed of bands of longitudinal fibres, which he regards as muscular.
The layer supporting the epithelium is reduced to a basement membrane. The
epithelial part of the wall of the stomach is by far the thickest
(fig. 20), and is mainly composed of enormously elongated, fibre-like
cells, which in the middle part of the stomach, where they are longest, are
nearly half a millimètre in length, and only about .006 mm. in breadth.
Their nuclei, as seen in fig. 20, are very elongated, and are placed about
a quarter of the length from the base.
The cells are mainly filled with an immense number of highly refracting
spherules, probably secretory globules, but held by Grube, from the fact of
their dissolving in ether, to be fat. The epithelial cells are raised into
numerous blunt processes projecting into the lumen of the stomach.
In addition to the cells just described there are present in the anterior
part of the stomach a fair sprinkling of mucous cells. There are also
everywhere present around the bases of the columnar cells short cells with
spherical nuclei, which are somewhat irregularly scattered in the middle
and posterior parts of the stomach, but form in the front part a definite
layer. I have not been able to isolate these cells, and can give no account
of their function.
The rectum extends from the end of the stomach to the anus. The region of
junction between the stomach and the rectum is somewhat folded. The usual
arrangement of the parts is shewn in fig. 6, where the hind end of the
stomach is seen to be bent upon itself in a U-shaped fashion, and the
rectum extending forwards under this bent portion and joining the front end
of the dorsal limb of the U. The structure of the walls of the rectum is
entirely different to that of the stomach, and the transition between the
two is perfectly sudden. Within the peritoneal investment comes a
well-developed muscular layer with a somewhat unusual arrangement of its
layers, there being an external circular layer and an internal layer formed
of isolated longitudinal bands. The epithelium is fairly columnar, formed
of granular cells with large nuclei, and is lined by a prolongation of the
external cuticle. It is raised into numerous longitudinal folds, which are
visible from the surface, and give a very characteristic appearance to this
part of the alimentary tract. The muscular layers do not penetrate into the
epithelial folds, which are supported by a connective tissue layer.
NERVOUS SYSTEM.
The central nervous system consists of a pair of supra-oesophageal ganglia
united in the middle line, and of a pair of widely divaricated ventral
cords, continuous in front with the supra-oesophageal ganglia.
It will be convenient in the first instance to deal with the general
anatomy of the nervous system and then with the histology.
_Ventral Cords._--The ventral cords at first sight appear to be without
ganglionic thickenings, but on more careful examination they are found to
be enlarged at each pair of legs (Pl. 48, fig. 8). These enlargements may
be regarded as imperfect ganglia. There are, therefore, seventeen such
pairs of ganglia corresponding to the seventeen pairs of legs. There is in
addition a ganglionic enlargement at the commencement of the oesophageal
commissures, where the nerves to the oral papillæ are given off (Pl. 51,
fig. 22, _or.g._), and the region of junction between the oesophageal
commissures with the supra-oesophageal ganglia, where another pair of
nerves are given off to the jaws (Pl. 51, fig. 22, _jn_), may be regarded
as the anterior ganglion of the ventral cords. There are, therefore,
according to the above reckoning, nineteen pairs of ganglia connected with
the ventral cords.
The ventral cords are placed each in the lateral compartments of the
body-cavity, immediately within the longitudinal layer of muscles.
They are connected with each other, rather like the pedal nerves of Chiton
and the lower Prosobranchiata, by a number of commissures. These
commissures exhibit a fairly regular arrangement from the region included
between the first and the last pair of true feet. There are nine or ten of
them between each pair of feet (Pl. 52, fig. 26). They pass along the
ventral wall of the body, perforating the ventral mass of longitudinal
muscles. On their way they give off nerves which innervate the skin.
In _Peripatus novæ zealandiæ_, and probably also in _P. capensis_, two of
these nerves, coming off from each pair of ganglia, are distinguished from
the remainder by the fact that they are provided with numerous nerve-cells,
instead of being composed of nerve-fibres only, like the remaining
commissures (Pl. 52, fig. 26 _gco_). In correlation with the nerves given
off from them to the skin the commissures are smaller in the middle than at
the two ends.
Posteriorly the two nerve-cords nearly meet immediately in front of the
generative aperture, and between this aperture and the last pair of feet
there are about six commissures passing between them (Pl. 48, fig. 8).
Behind the generative aperture the two cords bend upwards, and, as is shewn
in fig. 8, fall into each other dorsally to the rectum. The section of the
two cords placed dorsally to the rectum is solely formed of nerve-fibres;
the nerve-cells, present elsewhere, being here absent.
In front of the ganglion of the first foot the commissures have a more
dorsal situation than in the remainder of the body. The median longitudinal
ventral muscle here gradually thins out and comes to an end, while the
commissures pass immediately below the wall of the pharynx (Pl. 49, figs.
14, 15). The ventral cords themselves at first approach very close to each
other in this region, separating again, however, to envelope between them
the pharynx (Pl. 51, fig. 22).
There are eleven commissures in front of the first pair of legs (Pl. 51,
fig. 22). The three foremost of these are very close together, the middle
one arising in a more ventral position than the other two, and joining in
the median ventral line a peculiar mass of cells placed in contact with the
oral epithelium (fig. 14). It is probably an organ of special sense.
The ventral cords give off a series of nerves from their outer borders,
which present throughout the trunk a fairly regular arrangement. From each
ganglion two large nerves (figs. 8, 22, 26) are given off, which, diverging
somewhat from each other, pass into the feet, and, giving off branches on
their way, may be traced for a considerable distance within the feet along
their anterior and posterior borders.
In front of each of the pair of pedal nerves a fairly large nerve may be
seen passing outwards towards the side of the body (fig. 22). In addition
to this nerve there are a number of smaller nerves passing off from the
main trunk, which do not appear to be quite constant in number, but which
are usually about seven or eight. Similar nerves to those behind are given
off from the region in front of the first pair of legs, while at the point
where the two ventral cords pass into the oesophageal commissures two large
nerves (fig. 22), similar to the pairs of pedal nerves, take their origin.
These nerves may be traced forwards into the oral papillæ, and are
therefore to be regarded as the nerves of these appendages. On the ventral
side of the cords, where they approach most closely, between the oral
papillæ and the first pair of legs, a number of small nerves are given off
to the skin, whose distribution appears to be to the same region of the
skin as that of the branches from the commissures behind the first pair of
legs.
From the oesophageal commissures, close to their junction with the
supra-oesophageal ganglia, a nerve arises on each side which passes to the
jaws, and a little in front of this, apparently from the supra-oesophageal
ganglion itself, a second nerve to the jaws also takes its origin (Pl. 51,
fig. 22, _jn_). These two nerves I take to be homologous with a pair of
pedal nerves.
Between the nerves to the jaws and those to the oral papillæ a number of
small nerves take their origin. Three of these on each side pass in a
dorsal direction and one or two in a ventral one.
_The Supra-oesophageal Ganglia._--The supra-oesophageal ganglia (figs. 8
and 22) are large, somewhat oval masses, broader in front than behind,
completely fused in the middle, but free at their extremities. Each of them
is prolonged anteriorly into an antennary nerve, and is continuous behind
with one of the oesophageal commissures. On the ventral surface of each,
rather behind the level of the eye, is placed a very peculiar protuberance
(fig. 22, _d_), of which I shall say more in dealing with the histology of
the nervous system.
A number of nerves arise from the supra-oesophageal ganglia, mainly from
their dorsal surface.
In front are the immense antennary nerves extending along the whole length
of each antenna, and giving off numerous lateral twigs to the sense organs.
Near the origin of the antennary nerves, and rather on the dorsal surface,
there spring a few small twigs, which pass to the skin, and are presumably
sensory. The largest of them is shewn in Pl. 50, fig. 19A. About one-third
of the way back the two large optic nerves take their origin, also arising
laterally, but rather from the dorsal surface (Pl. 50, fig. 19D and E).
Each of them joins a large ganglionic mass placed immediately behind the
retina. Nearly on a level with the optic nerves and slightly nearer the
middle dorsal line a pair of small nerves (fig. 19D) spring from the brain
and pass upwards, while nearly in the same line with the optic nerves and a
little behind them a larger pair of nerves take their origin.
Behind all these nerves there arises from the line of suture between the
two supra-oesophageal ganglia a large median nerve which appears to supply
the integument of the dorsal part of the head (Pl. 48, fig. 8; Pl. 49,
figs. 11-14, _dn_).
_Sympathetic System._--In addition to the nerves just described there are
two very important nerves which arise near the median ventral line, close
to the hind end of the supra-oesophageal ganglia. The origin of these two
nerves is shewn in the surface view (fig. 22, _sy_, and in section in
fig. 11). They at first tend somewhat forwards and pass into the muscles
near the epithelium lining the groove on each side of the tongue. Here they
suddenly bend backwards again and follow the grooves into the pharynx.
The two grooves are continuous with the two dorsal angles of the pharynx;
and embedded in the muscles of the pharynx, in juxtaposition with the
epithelium, these two nerves may easily be traced in sections. They pass
backwards the whole length of the pharynx till the latter joins the
oesophagus. Here they at once approach and shortly meet in the median
dorsal line (fig. 16). They can only be traced for a very short distance
beyond their meeting point. These nerves are, without doubt, the homologues
of the sympathetic system of Chætopods, occupying as they do the exact
position which Semper has shewn to be characteristic of the sympathetic
nerves in that group, and arising from an almost identical part of the
brain[571].
Footnote 571: Vide Spengel, "Oligognathus Bonelliæ." _Naples
Mittheilungen_, Bd. III. pl. IV. fig. 52.
_Histology of the Nervous System._
_Ventral Cords._--The histology of the ventral cords and oesophageal
commissures is very simple and uniform. They consist of a cord almost
wholly formed of nerve-fibres, placed dorsally, and a ventral layer of
ganglion cells (figs. 16 and 20).
The fibrous portion of the cord has the usual structure, being formed
mainly of longitudinal fibres, each probably being a bundle of fibres of
various sizes, enveloped in a sponge-work of connective tissue. The larger
bundles of fibres are placed near the inner borders of the cords. In this
part of the cord there are placed a very small number of ganglion cells.
The layer of ganglion cells is somewhat crescent-shaped in section, and, as
shewn in figs. 16 and 20, envelopes the whole ventral aspect of the fibrous
parts of the cord, and even creeps up slightly on to the dorsal side. It is
thicker on the inner than on the outer side, and increases considerably in
bulk at each ganglionic enlargement. The cells of which it is composed are
for the most part of a nearly uniform size, but at the border of the
fibrous matter a fair sprinkling of larger cells is found.
The tracheal vessels supplying the nervous system are placed amongst the
larger cells, at the boundary between the ganglionic and fibrous regions of
the cords.
With reference to the peripheral nerve-stems there is not much to be said.
They have for the most part a similar structure to the fibrous parts of the
main cord, but are provided with a somewhat larger number of cells.
_Sheath of the Ventral Cords._--The ventral cords are enveloped by a double
sheath, the two layers of which are often in contact, while in other cases
they may be somewhat widely separated from each other. The inner layer is
extremely thin and always very closely envelopes the nerve-cords. The outer
layer is thick and fibrous, and contains a fair sprinkling of nuclei.
_Supra-oesophageal Ganglia._--In the present state of our knowledge a very
detailed description of the histology of the supra-oesophageal ganglia
would be quite superfluous, and I shall confine myself to a description of
the more obvious features in the arrangement of the ganglionic and fibrous
portions (Pl. 50, fig. 19A-G).
The ganglion cells are in the first place confined, for the most part, to
the surface. Along the under side of each ganglion there is a very thick
layer of cells, continuous behind, with the layer of ganglion cells which
is placed on the under surface of the oesophageal commissures. These cells
have, moreover, an arrangement very similar to that in the ventral cords,
so that a section through the supra-oesophageal ganglia has an obvious
resemblance to what would be the appearance of a section through the united
ventral cords. On the outer borders of the ganglia the cells extend
upwards, but they end on about the level of the optic nerve (fig. 19D).
Immediately dorsal to this point the fibrous matter of the brain is exposed
freely on the surface (fig. 19A, B, &C., _a_). I shall call the region of
fibrous matter so exposed the dorso-lateral horn of white matter.
Where the two ganglia separate in front the ganglion cells spread up the
inner side, and arch over so as to cover part of the dorsal side. Thus, in
the anterior part, where the two ganglia are separate, there is a complete
covering of ganglionic substance, except for a narrow strip, where the
dorso-lateral lobe of white matter is exposed on the surface (fig. 19A).
From the point where the two ganglia meet in front the nerve-cells extend
backwards as a median strip on the dorsal surface (fig. 19D and E). This
strip, becoming gradually smaller behind, reaches nearly, though not quite,
the posterior limit of the junction of the ganglia. Behind it there is,
however, a region where the whole dorsal surface of the ganglia is without
any covering of nerve-cells.
This tongue of ganglion cells sends in, slightly behind the level of the
eyes, a transverse vertical prolongation inwards into the white matter of
the brain, which is shewn in the series of transverse sections in fig. 19E,
and also in the vertical longitudinal section (Pl. 51, fig. 21), and in
horizontal section in Pl. 51, fig. 22.
On the ventral aspect of each lobe of the brain there is present a very
peculiar, bluntly conical protuberance of ganglion cells (Pl. 51, fig. 22),
which was first detected by Grube (No. 10), and described by him as "a
white thick body of a regular tetrahedral form, and exhibiting an oval dark
spot in the middle of two of the faces." He further states that it is
united by a delicate nerve to the supra-oesophageal ganglion, and regards
it as an organ of hearing.
In _Peripatus capensis_ the organ in question can hardly be described as
tetrahedral. It is rather of a flattened oval form, and consists, as shewn
in sections (Pl. 50, fig. 19C and D, _d_), mainly of ganglion cells. In its
interior is a cavity with a distinct bounding membrane: the cells of which
it is composed vary somewhat in size, being smallest near the point of
attachment. At its free end is placed a highly refractive, somewhat oval
body, probably forming what Grube describes as a dark spot, half embedded
in its substance, and kept in place by the sheath of nervous matter
surrounding it. This body appears to have fallen out in my sections. The
whole structure is attached to the under surface of the brain by a very
short stalk formed of a bundle of cells and nervous fibres.
It is difficult to offer any interpretation of the nature of this body. It
is removed considerably from the surface of the animal, and is not,
therefore, so far as I can see, adapted to serve as an organ of hearing.
The distribution of the white or fibrous matter of the ganglia is not very
easy to describe.
There is a central lobe of white matter (fig. 19E), which is continuous
from ganglion to ganglion, where the two are united. It is smaller behind
than in front. On its ventral side it exhibits fairly well-marked
transverse commissural fibres, connecting the two halves of the ganglion.
Laterally and somewhat ventrally it is prolonged into a horn (fig. 19D, E,
_b_), which I propose calling the ventro-lateral horn. In front it is
placed in a distinct protuberance of the brain, which is placed ventrally
to and nearly in the same vertical plane as the optic nerve. This
protuberance is best shewn in the view of the brain from below given in
Pl. 51, fig. 22. This part of the horn is characterized by the presence of
large vertically-directed bundles of nerve-fibres, shewn in transverse
section in fig. 19 D. Posteriorly the diameter of this horn is larger than
in front (fig. 19E, F, G), but does not give rise to a protuberance on the
surface of the brain owing to the smaller development of the median lobe
behind.
The median lobe of the brain is also prolonged into a dorso-lateral lobe
(fig. 19, _a_), which, as already mentioned, is freely exposed on the
surface. On its ventral border there springs the optic nerve, and several
pairs of sensory nerves already described (fig. 19D, E), while from its
dorsal border a pair of sensory nerves also spring, nearly in the same
vertical plane as the optic nerves.
Posteriorly where the dorsal surface of the brain is not covered in with
ganglion cells the dorso-lateral horn and median lobe of the brain become
indistinguishable.
In the front part of the brain the median lobe of white matter extends
dorsalwards to the dorsal strip of ganglion cells, but behind the region of
the transverse prolongation of these cells, into the white matter already
described (p. 890), there is a more or less distinctly defined lobe of
white matter on the dorsal surface, which I propose calling the
postero-dorsal lobe of white matter. It is shewn in the transverse sections
(fig. 19F and G, _c_). It gradually thins away and disappears behind. It is
mainly characterized by the presence on the ventral border of definite
transverse commissural fibres.
THE SKIN.
The skin is formed of three layers.
1. The cuticle.
2. The epidermis or hypodermis.
3. The dermis.
The cuticle is a layer of about 0.002 mm. in thickness. Its surface is not,
however, smooth, but is everywhere, with the exception of the perioral
region, raised into minute secondary papillæ, the base of which varies
somewhat in diameter, but is usually not far from 0.02 mm. On the ventral
surface of the body these papillæ are for the most part somewhat blunt, but
on the dorsal surface they are more or less sharply pointed. In most
instances they bear at their free extremity a somewhat prominent spine. The
whole surface of each of the secondary papillæ just described is in its
turn covered by numerous minute spinous tubercles. In the perioral region,
where the cuticle is smooth, it is obviously formed of two layers which
easily separate from each other, and there is I believe a similar division
elsewhere, though it is not so easy to see. It is to be presumed that the
cuticle is regularly shed.
The epidermis, placed immediately within the cuticle, is composed of a
single row of cells, which vary, however, a good deal in size in different
regions of the body. The cells excrete the cuticle, and, as shewn in
fig. 32, they stand in a very remarkable relation to the secondary papillæ
of the cuticle just described. Each epidermis cell is in fact placed within
one of these secondary papillæ, so that the cuticle of each secondary
papilla is the product of a single epidermis cell. This relation is easily
seen in section, while it may also be beautifully shewn by taking a part of
the skin which is not too much pigmented, and, after staining it, examining
from the surface.
In fig. 32 a region of the epidermis is figured, in which the cells are
exceptionally columnar. The cuticle has, moreover, in the process of
cutting the section, been somewhat raised and carried away from the
subjacent cells. The cells of the epidermis are provided with large oval
nuclei, which contain a well-developed reticulum, giving with low powers a
very granular appearance to the nuclei. The protoplasm of the cells is also
somewhat granular, and the granules are frequently so disposed as to
produce a very well-marked appearance of striation on the inner end of the
cells. The pigment which gives the characteristic colour to the skin is
deposited in the protoplasm of the outer ends of the cells in the form of
small granules. An attempt is made to shew this in fig. 32.
At the apex of most, if not all, the primary wart-like papillæ there are
present oval aggregations, or masses of epidermis cells, each such mass
being enclosed in a thickish capsule (fig. 31). The cells of these masses
appear to form the wall of a cavity which leads into the hollow interior of
a long spine. These spines when carefully examined with high objectives
present a rather peculiar structure. The base of the spine is enveloped by
the normal cuticle, but the spine itself, which terminates in a very fine
point, appears, as shewn in fig. 31, to be continuous with the inner layer
of the cuticle. In the perioral region the outer layer of the cuticle, as
well as the inner, appear to be continued to the end of the spines. Within
the base of the spine there is visible a finely striated substance which
may often be traced into the cavity enclosed by the cells, and appears to
be continuous with the cells. Attached to the inner ends of most of the
capsules of these organs a delicate fibrillated cord may be observed, and
although I have not in any instance succeeded in tracing this cord into one
of the nerve-stems, yet in the antennæ, where the nerve-stems are of an
enormous size, I have satisfied myself that the minute nerves leaving the
main nerve-stems and passing out towards the skin are histologically not to
be distinguished from these fibrillated cords. I have therefore but little
hesitation in regarding these cords as nerves.
In certain regions of the body the oval aggregations of cells are extremely
numerous; more especially is this the case in the antennæ, lips, and oral
papillæ. On the ventral surface of the peripheral rings of the thicker
sections of the feet they are also very thick set (fig. 20, P). They here
form a kind of pad, and have a more elongated form than in other regions.
In the antennæ they are thickly set side by side on the rings of skin which
give such an Arthropod appearance to these organs in Peripatus.
The arrangement of the cells in the bodies just described led me at first
to look upon them as glands, but a further investigation induced me to
regard them as a form of tactile organ. The arguments for this view are
both of a positive and a negative kind.
The positive arguments are the following:
(1) The organs are supplied with large nerves, which is distinctly in
favour of their being sense organs rather than glands.
(2) The peculiar striæ at the base of the spines appear to me like the
imperfectly preserved remains of sense hairs.
(3) The distribution of these organs favours the view that they are tactile
organs. They are most numerous on the antennæ, where such organs would
naturally be present, especially in a case like that of Peripatus, where
the nerve passing to the antennæ is simply gigantic. On the other hand, the
antennæ would not be a natural place to look for an enormous development of
dermal glands.
The lips, oral papillæ, and under surface of the legs, where these bodies
are also very numerous, are situations where tactile organs would be of
great use.
Under the head of negative arguments must be classed those which tell
against these organs being glandular. The most important of these is the
fact that they have no obvious orifice. Their cavities open no doubt into
the spines, but the spines terminate in such extremely fine points that the
existence of an orifice at their apex is hardly credible.
Another argument, from the distribution of these organs over the body is
practically the converse of that already used. The distribution being as
unfavourable to the view that they are glands, as it is favourable to that
of their being sense organs.
THE TRACHEAL SYSTEM.
The apertures of the tracheal system are placed in the depressions between
the papillæ or ridges of the skin. Each of them leads into a tube, which I
shall call the tracheal pit (fig. 30), the walls of which are formed of
epithelial cells bounded towards the lumen of the pit by a very delicate
cuticular membrane continuous with the cuticle covering the surface of the
body. The pits vary somewhat in depth; the pit figured was about 0.09 mm.
It perforates the dermis and terminates in the subjacent muscular layer.
The investigation of the inner end of the pit gave me some little trouble.
Transverse sections (fig. 30) through the trunk containing a tracheal
opening shew that the walls of the pit expanded internally in a
mushroom-like fashion, the narrow part being, however, often excentric in
relation to the centre of the expanded part.
Although it was clear that the tracheæ started from the expanded region of
the walls of the pit, I could not find that the lumen of the pit dilated
into a large vesicle in this part, and further investigation proved that
the tracheæ actually started from the slightly swollen inner extremity of
the narrow part of the pit, the expanded walls of the pit forming an
umbrella-like covering for the diverging bundles of tracheæ.
I have, in fig. 30, attempted to make clear this relation between the
expanded walls of the tracheal pits and the tracheæ. In longitudinal
sections of the trunk the tracheal pits do not exhibit the lateral
expansion which I have just described, which proves that the divergence of
the bundles of tracheæ only takes place laterally and not in an
antero-posterior direction. Cells similar in general character to those of
the walls of the tracheal pits are placed between the branches of tracheæ,
and somewhat similar cells, though generally with more elongated nuclei,
accompany the bundles of tracheæ as far as they can be followed in my
sections. The structure of these parts in the adult would, in fact, lead
one to suppose that the tracheæ had originated at the expense of the cells
of pits of the epidermis, and that the cells accompanying the bundles of
tracheæ were the remains of cords of cells which sprouted out from the
blind ends of the epidermis pits and gave rise in the first instance to the
tracheæ.
The tracheæ themselves are extremely minute, unbranched (so far as I could
follow them) tubes. Each opening by a separate aperture into the base of
the tracheal pit, and measuring about 0.002 mm. in diameter. They exhibit a
faint transverse striation, which I take to be the indication of a spiral
fibre. [Moseley (_Phil. Trans._, 1874, Pl. 73, fig. 1) states that the
tracheæ branch, but only exceptionally.]
_Situation of the tracheal apertures._--Moseley states (No. 13) that the
tracheæ arise from the skin all over the surface of the body, but are
especially developed in certain regions. He finds "a row of minute oval
openings on the ventral surface of the body," the openings being "situate
with tolerable regularity in the centres of the interspaces between the
pairs of members, but additional ones occurring at irregular intervals.
Other similar openings occur in depressions on the inner side of the
conical foot protuberance." It is difficult in preserved specimens to make
out the exact distributions of the tracheal apertures, but I have been able
to make out certain points about them.
There is a double row of apertures on each side of the median dorsal line,
forming two sub-dorsal rows of apertures. The apertures are considerably
more numerous than the legs. There is also a double row of openings, again
more numerous than the legs, on each side of the median ventral line
between the insertions of the legs. Moseley speaks of a median row in this
position. I think this must be a mistake.
Posteriorly the two inner rows approach very close to each other in the
median ventral line, but I have never seen them in my section opening quite
in the middle line. Both the dorsal and ventral rows are very irregular.
I have not found openings on the ventral or dorsal side of the feet but
there are openings at the anterior and posterior aspects of the feet. There
are, moreover, a considerable number of openings around the base of the
feet.
The dorsal rows of tracheal apertures are continued into the head and give
rise in this situation to enormous bundles of tracheæ.
In front of the mouth there is a very large median ventral tracheal pit,
which gives off tracheæ to the ventral part of the nervous system, and
still more in front a large number of such pits close together. The tracheæ
to the central nervous system in many instances enter the nervous system
bound up in the same sheath as the nerves.
THE MUSCULAR SYSTEM.
The general muscular system consists of--(1) the general wall of the body;
(2) the muscles connected with the mouth, pharynx, and jaws; (3) the
muscles of the feet; (4) the muscles of the alimentary tract.
The muscular wall of the body is formed of--(1) an external layer of
circular fibres; (2) an internal layer of longitudinal muscles; (3) a layer
of transverse fibres.
The layer which I have spoken of as formed of circular fibres is formed of
two strata of fibres which girth the body somewhat obliquely (Pl. 51,
fig. 25). In the outer stratum the rings are arranged so that their ventral
parts are behind, while the ventral parts of the rings of the inner stratum
are most forward. Both in the median dorsal and ventral lines the layer of
circular fibres become somewhat thinner, and where the legs are attached
the regularity of both strata is somewhat interfered with, and they become
continuous with a set of fibres inserted in the wall of the foot.
The longitudinal muscles are arranged as five bands (vide fig. 16), viz.
two dorsal, two lateral, and three ventral. The three ventral may be spoken
of as the latero-ventral and medio-ventral bands.
The transverse fibres consist of (1) a continuous sheet on each side
inserted dorsally in the cutis, along a line opposite the space between the
dorsal bands of longitudinal fibres, and ventrally between the
ventro-median and ventro-lateral bands. Each sheet at its insertion
slightly breaks up into separate bands. They divide the body-cavity into
three regions--a median, containing the alimentary tract, slime glands,
&c., and two lateral, which are less well developed, and contain the
nervous system, salivary glands, segmental organs, &c.
(2) Inserted a little dorsal to the transverse band just described is a
second band which immediately crosses the first, and then passes on the
outer side of the nervous cord and salivary gland, where such is present,
and is inserted ventrally in the space between the ventro-lateral and
lateral longitudinal band.
Where the feet are given off the second transverse band becomes continuous
with the main retractor muscular fibres in the foot, which are inserted
both on to the dorsal side and ventral side.
_Muscular system of the feet._--This consists of the retractors of the feet
connected with the outer transverse muscle and the circular layer of
muscles. In addition to these muscles there are intrinsic transverse
muscles which cross the cavity of the feet in various directions (Pl. 51,
fig. 20). There is no special circular layer of fibres.
_Histology of the muscle._--The main muscles of the body are unstriated and
divided into fibres, each invested by a delicate membrane. Between the
membrane and muscle are scattered nuclei, which are never found inside the
muscle fibres. The muscles attached to the jaws form an exception in that
they are distinctly transversely striated.
THE BODY-CAVITY AND VASCULAR SYSTEM.
The body-cavity, as already indicated, is formed of three compartments--one
central and two lateral. The former is by far the largest, and contains the
alimentary tract, the generative organs, and the mucous glands. It is lined
by a delicate endothelial layer, and is not divided into compartments nor
traversed by muscular fibres.
The lateral divisions are much smaller than the central, and are shut off
from it by the inner transverse band of muscles. They are almost entirely
filled with the nerve-cord and salivary gland in front and with the
nerve-cord alone behind, and their lumen is broken up by muscular bands.
They further contain the segmental organs which open into them. They are
prolonged into the feet, as is the embryonic body-cavity of most
Arthropoda.
The vascular system is usually stated to consist of a dorsal heart. I find
between the dorsal bands of longitudinal fibres a vessel in a space shut
off from the body-cavity by a continuation of the endothelial lining of the
latter (fig. 16). The vessel has definite walls and an endothelial lining,
but I could not make out whether the walls were muscular. The ventral part
of it is surrounded by a peculiar cellular tissue, probably, as suggested
by Moseley, equivalent to the fat bodies of insects. It is continued from
close to the hind end of the body to the head, and is at its maximum
behind. In addition to this vessel there is present a very delicate ventral
vessel, by no means easy to see, situated between the cutis and the outer
layer of circular muscles.
SEGMENTAL ORGANS.
A series of glandular organs are found in Peripatus which have their
external openings situated on the ventral surface of a certain number of
the legs, and which, to the best of my belief, end internally by opening
into the lateral compartments of the body-cavity. These organs are probably
of an excretory nature, and I consider them homologous with the nephridia
or segmental organs of the Chætopoda.
In _Peripatus capensis_ they are present in all the legs. In all of them
(except the first three) the following parts may be recognized:
(1) A vesicular portion opening to the exterior by a narrow passage.
(2) A coiled portion, which is again subdivided into several sections.
(3) A terminal section ending by a somewhat enlarged opening into the
lateral compartment of the body-cavity.
The last twelve pairs of these organs are all constructed in a very similar
manner, while the two pairs situated in the fourth and fifth pairs of legs
are considerably larger than those behind, and are in some respects very
differently constituted.
It will be convenient to commence with one of the hinder nephridia. Such a
nephridium from the ninth pair of legs is represented in fig. 28. The
external opening is placed at the outer end of a transverse groove placed
at the base of one of the feet, while the main portion of the organ lies in
the body-cavity in the base of the leg, and extends into the trunk to about
the level of the outer edge of the nerve-cord of its side. The external
opening (_os_) leads into a narrow tube (_sd_), which gradually dilates
into a large sack (_s_).
The narrow part is lined by small epithelial cells, which are directly
continuous with and perfectly similar to those of the epidermis (fig. 20).
It is provided with a superficial coating of longitudinal muscular fibres,
which thins out where it passes over the sack, along which it only extends
for a short distance.
The sack itself, which forms a kind of bladder or collecting vesicle for
the organ, is provided with an extremely thin wall, lined with very large
flattened cells. These cells are formed of granular protoplasm, and each of
them is provided with a large nucleus, which causes a considerable
projection into the lumen of the sack (figs. 20, 29, _s_). The epithelial
wall of the sack is supported by a membrana propria, over which a delicate
layer of the peritoneal epithelium is reflected.
The coiled tube forming the second section of the nephridium varies in
length, and by the character of the epithelium lining it may be divided
into four regions. It commences with a region lined by a fairly columnar
epithelium with smallish nuclei (fig. 28, _sc_1). The boundaries of the
cells of this epithelium are usually very indistinct, and the protoplasm
contains numerous minute granules, which are usually arranged in such a
manner as to give to optical or real sections of the wall of this part of
the tube a transversely striated appearance. These granules are very
probably minute balls of excretory matter.
The nuclei of the cells are placed near their free extremities, contrary to
what might have been anticipated, and the inner ends of the cells project
for very different lengths into the interior, so causing the inner boundary
of the epithelium of this part of the tube to have a very ragged
appearance. This portion of the coiled tube is continuous at its outer end
with the thin-walled vesicle. At its inner end it is continuous with region
No. 2 of the coiled tube (fig. 28, _sc_2), which is lined by small
closely-packed columnar cells. This portion is followed by region No. 3,
which has a very characteristic structure (fig. 28 _sc_3). The cells lining
this part are very large and flat, and contain large disc-shaped nuclei,
which are usually provided with large nucleoli, and often exhibit a
beautiful reticulum. They may frequently be observed in a state of
division. The protoplasm of this region is provided with similar granules
to that in the first region, and the boundaries of the cells are usually
very indistinct. The fourth region is very short (fig. 28, _sc_4), and is
formed of small columnar cells. It gradually narrows till it opens suddenly
into the terminal section (_sot_), which ends by opening into the
body-cavity, and constitutes the most distinct portion of the whole organ.
Its walls are formed of columnar cells almost filled by oval nuclei, which
absorb colouring matters with very great avidity, and thus renders this
part extremely conspicuous. The nuclei are arranged in several rows.
The study of the internal opening of this part gave me some trouble. No
specimens ever shew it as rounded off in the characteristic fashion of
tubes ending in a cul-de-sac. It is usually somewhat ragged and apparently
open. In the best preserved specimens it expands into a short funnel-shaped
mouth, the free edge of which is turned back. Sections confirm the results
of dissections. Those passing longitudinally through the opening prove its
edges are turned back, forming a kind of rudimentary funnel. This is
represented in fig. 29, from the last leg of a female. I have observed
remains of what I consider to be cilia in this section of the organ. The
fourth region of the organ is always placed close to the thin-walled
collecting vesicle (figs. 28 and 29). In the whole of the coiled tube just
described the epithelium is supported by a membrana propria, which in its
turn is invested by a delicate layer of peritoneal epithelium.
The fourth and fifth pairs are very considerably larger than those behind,
and are in other respects peculiar. The great mass of each organ is placed
behind the leg, on which the external opening is placed, immediately
outside one of the lateral nerve-cords. Its position is shewn in fig. 8.
The external opening, instead of being placed near the base of the leg, is
placed on the ventral side of the third ring (counting from the outer end)
of the thicker portion of the leg. It leads (fig. 27) into a portion which
clearly corresponds with the collecting vesicle of the hinder nephridia.
This part is not, however, dilated into a vesicle in the same sort of way,
and the cells which form the lining epithelium have not the same
characteristic structure, but are much smaller. Close to the point where
the vesicle joins the coiled section of the nephridium the former has a
peculiar nick or bend in it. At this nick it is firmly attached to the
ventral side of the foot by muscles and tracheæ, and when cut away from its
attachment the muscles and tracheæ cannot easily be detached from it. The
main part of the coils are formed by region No. 1, and the epithelial cells
lining this part present very characteristically the striated appearance
which has already been spoken of. The large-celled region of the coiled
tube (fig. 27) is also of considerable dimensions, and the terminal portion
is wedged in between this and the commencing part of the coiled tube. The
terminal portion with its internal opening is in its histological
characters exactly similar to the homologous region in the hinder
nephridia.
The three pairs of nephridia in the three foremost pairs of legs are very
rudimentary, consisting, so far as I have been able to make out, solely of
the collecting vesicle and the duct leading from them to the exterior. The
external opening is placed on the ventral side of the base of the feet, in
the same situation as that of the posterior nephridia, but the histological
characters of the vesicle are similar to those of the fourth and fifth
pairs.
GENERATIVE ORGANS.
[The sexes are distinct, and the average size of the females appears to be
greater than that of the males.
The only outward characteristic by which the males can be distinguished
from the females is the presence in the former of a small white papilla on
the ventral side of the 17th pair of legs (Pl. 47, fig. 4). At the
extremity of this papilla the modified crural gland of the last leg opens
by a slit-like aperture.
The generative orifice in both sexes is placed on the ventral surface of
the body, close to the anus, and between the two anal papillæ, which are
much more marked in small specimens than in large ones, and in two cases
(of females) were observed to bear rudimentary claws.
1. _The Male Organs._ Pl. 53, fig. 43.
The male organs consist of a pair of testes (_te_), a pair of prostrates
(_pr_) and vasa deferentia (_vd_) and accessory glandular tubules (_f_).
All the above parts lie in the central compartment of the body-cavity. In
addition, the accessory glandular bodies or crural glands of the last
(17th) pair of legs are enlarged and prolonged into an elongated tube
placed in the lateral compartment of the body-cavity (_ag_).
The arrangement of these parts represented in the figure appears
essentially that which Moseley has already described for this species. The
dilatations on the vasa deferentia, which he calls vesiculæ seminales, is
not so marked; nor can the peculiar spiral twisting of this part of the vas
deferens which he figures (No. 13) be made out in this specimen. The testes
are placed at different levels in the median compartment of the
body-cavity, and both lie on the same side of the intestine (right side).
The arrangement of the terminal portions of the vas deferens is precisely
that described by Moseley. The right vas deferens passes under both
nerve-cords to join the left, and from the enlarged tube (_p_), which,
passing beneath the nerve-cord of its side, runs to the external orifice.
The enlarged terminal portion possesses thick muscular walls, and possibly
constitutes a spermatophore maker, as has been shewn to be the case in P.
N. Zealandiæ, by Moseley.
In some specimens a different arrangement obtains, in that the left vas
deferens passes under both nerve-cords to join the right.
In addition to the above structures, which are all described by Moseley,
there are a pair of small glandular tubes (_f_), which open with the
unpaired terminal portion of the vas deferens at the generative orifice.
2. _Female Organs._ Pl. 52, fig. 33.
The female organs consist of a median unpaired ovary and a pair of
oviducts, which are dilated for a great part of their course to perform a
uterine function, and which open behind into a common vestibule
communicating directly with the exterior.
_Ovary._--In the specimen figured the following is the arrangement:
The ovary lies rather to the dorsal side in the central compartment of the
body-cavity, and is attached to one of the longitudinal septa separating
this from the lateral compartment. It lies between the penultimate and
antepenultimate pair of legs.
The oviducts cross before opening to the exterior. The right oviduct passes
under the rectum, and the left over the rectum. They meet by opening into a
common vestibule, which in its turn opens to the exterior immediately
ventral to the anus. It has not been ascertained how far this arrangement,
which differs from that observed by Moseley, is a normal one. The young
undergo nearly the whole of their development within the uterus. They
possess at birth the full number of appendages, and differ from the parent
only in size and colour.]
NOTES ON ADDITIONAL GLANDULAR BODIES IN THE LEGS
[CRURAL GLANDS].
1. They are present in all except the first.
2. They open externally to the nephridia (Pl. 51, fig. 20), except in the
fourth and fifth pairs of legs, in which they are internal.
3. A muscular layer covers the whole gland, consisting, I believe, of an
oblique circular layer.
4. The accessory gland in the male (fig. 43, _ag_) is probably a
modification of one of these organs.
[The structure and relations of these glands may be best understood by
reference to Pl. 51, fig. 20. Each consists of a dilated vesicular portion
(_fgl_) placed in the lateral compartment of the body-cavity in the foot,
and of a narrow duct leading to the exterior, and opening on the ventral
surface amongst the papillæ of the second row (counting from the internal
of the three foot pads--fig. 20, P).
The vesicular portion is lined by columnar cells, with very large oval
nuclei, while the duct is lined by cells similar to the epidermic cells,
with which they are continuous at the opening.
In the last (17th) leg of the males of this species, this gland (vide
above, note 4) possesses a slit-like opening placed at the apex of a
well-developed white papilla (Pl. 47, fig. 4). It is enormously enlarged,
and is prolonged forward as a long tubular gland, the structure of which
resembles that of the vesicles of the crural glands in the other legs. This
gland lies in the lateral compartment of the body-cavity, and extends
forward to the level of the 9th leg (Pl. 48, fig. 8, and Pl. 53, fig. 43).
It is described by Professor Balfour as the accessory gland of the male,
and is seen in section lying immediately dorsal to the nerve-cord in
fig. 20, _ag_.]
PART III.
THE DEVELOPMENT OF PERIPATUS CAPENSIS.
[The remarkable discoveries about the early development of Peripatus, which
Balfour made in June last, shortly before starting for Switzerland, have
already been the subject of a short communication to the Royal Society
(_Proc. Roy. Soc._ No. 222, 1882). They relate (1) to the blastopore, (2)
to the origin of the mesoblast.
Balfour left no manuscript account or notes of his discovery in connection
with the drawings which he prepared in order to illustrate it, but he spoke
about it to Professor Ray Lankester and also to us, and he further gave a
short account of the matter in a private letter to Professor Kleinenberg.
In this letter, which by the courtesy of Professor Kleinenberg we have been
permitted to see, he describes the blastopore as an elongated slit-like
structure extending along nearly the whole ventral surface; and further
states, as the result of his examination of the few and ill-preserved
embryos in his possession, that the mesoblast appears to originate as
paired outgrowths from the lips of the blastopore.
The drawings left by Balfour in connection with the discoveries are four in
number: one of the entire embryo, shewing the slit-like blastopore and the
mesoblastic somites, the other three depicting the transverse sections of
the same embryo.
The first drawing (fig. 37), viz. that of the whole embryo, shews an embryo
of an oval shape, possessing six somites, whilst along the middle of its
ventral surface there are two slit-like openings, lying parallel to the
long axis of the body, and placed one behind the other. The mesoblastic
somites are arranged bilaterally in pairs, six on either side of these
slits. The following note in his handwriting is attached to this drawing:
"Young larva of _Peripatus capensis_.--I could not make out for certain
which was the anterior end. Length 1.34 millimetres."
Balfour's three remaining drawings (figs. 40-42) are, as already stated,
representations of transverse sections of the embryo figured by him as a
whole. They tend to shew, as he stated in the letter referred to above,
that the mesoblast originates as paired outgrowths from the hypoblast, and
that these outgrowths are formed near the junction of the hypoblast with
the epiblast at the lips of the blastopore.
In fig. 42 the walls of the mesoblastic somites appear continuous with
those of the mesenteron near the blastopore.
In fig. 40, which is from a section a little in front of fig. 42, the walls
of the mesoblastic somites are independent of those of the mesenteron.
Fig. 41 is from a section made in front of the region of the blastopore.
In all the sections the epiblast lying over the somites is thickened, while
elsewhere it is formed of only one layer of cells; and this thickening
subsequently appears to give rise to the nervous system. Balfour in his
earlier investigations on the present subject found in more advanced stages
of the embryo the nerve-cords still scarcely separated from the
epiblast[572].
Footnote 572: _Comparative Embryology_; original edition,
Vol. I. p. 318. [This edition, Vol. II. p. 385.]
We have since found, in Balfour's material, embryos of a slightly different
age to that just described. Of these, three (figs. 34, 35, 36) are younger,
while one (fig. 38) is older than Balfour's embryo.
Stage A.--The youngest (fig. 34) is of a slightly oval form, and its
greatest length is .48 mm. It possesses a blastopore, which is elongated in
the direction of the long axis of the embryo, and is slightly narrower in
its middle than at either end. From one end of the blastopore there is
continued an opaque band. This we consider to be the posterior end of the
blastopore of the embryo. The blastopore leads into the archenteron.
Stage B.--In the next stage (fig. 35) the embryo is elongate-oval in form.
Its length is .7 mm. The blastopore is elongated and slightly narrowed in
the middle. At the posterior end of the embryo there is a mass of opaque
tissue. On each side of the blastopore are three mesoblastic somites. The
length of the blastopore is .45 mm.
Stage C.--In the next stage (fig. 36) the features are much the same as in
the preceding. The length of the whole embryo is .9 mm.
The following were the measurements of an embryo of this stage with five
somites, but slightly younger than that from which fig. 36 was drawn.
Length of embryo .74 mm.
" blastopore .46 "
Distance between hind end of blastopore and hind end
of body .22 "
Distance between front end of body and front end of
blastopore .06 "
The somites have increased to five, and there are indications of a sixth
being budded off from the posterior mass of opaque tissue. The median parts
of the lips of the blastopore have come together preparatory to the
complete fusion by which the blastopore becomes divided into two parts.
Stage D.--The next stage is Balfour's stage, and has been already
described.
The length is 1.34.
It will be observed, on comparing it with the preceding embryos, that while
the anterior pair of somites in figs. 35 and 36 lie at a considerable
distance from what we have called the anterior end of the embryo (_a_), in
the embryo now under consideration they are placed at the anterior end of
the body, one on each side of the middle line. We cannot speak positively
as to how they come there, whether by a pushing forward of the anterior
somites of the previous stage, or by the formation of new somites
anteriorly to those of the previous stage.
In the next stage it is obvious that this anterior pair of somites has been
converted into the præoral lobes.
The anterior of the two openings to which the blastopore gives rise is
placed between the second pair of somites; we shall call it the embryonic
mouth. The posterior opening formed from the blastopore is elongated, being
dilated in front and continued back as a narrow slit (?) to very near the
hind end of the embryo, where it presents a second slight dilatation. The
anterior dilatation of the posterior open region of the blastopore we shall
call the embryonic anus.
Lately, but too late to be figured with this memoir, we have been fortunate
enough to find an embryo of apparently precisely the same stage as fig. 37.
We are able, therefore, to give a few more details about the stage.
The measurements of this embryo were:
Length of whole embryo 1.32 mm.
Distance from front end of body to front end of mouth .32 "
Distance from embryonic mouth to hind end of embryonic
anus .52 "
Distance from hind end of embryonic anus to hind end
of body .45 "
Length of embryonic anus .2 "
" part of blastopore behind embryonic anus .2 "
Greatest width of embryo .64 "
Stage E.--In the next stage (figs. 38 and 39) the flexure of the hind end
of the body has considerably increased. The anterior opening of the
blastopore, the embryonic mouth, has increased remarkably in size. It is
circular, and is placed between the second pair of mesoblastic somites. The
anterior dilatation of the posterior opening of the blastopore, the
embryonic anus, has, like the anterior opening, become much enlarged. It is
circular, and is placed on the concavity of the ventral flexure. From its
hind end there is continued to the hind end of the body a groove (shewn in
fig. 39 as a dotted line), which we take to be the remains of the posterior
slit-like part of the posterior opening of the blastopore of the preceding
stage. The posterior dilatation has disappeared. The embryo has apparently
about thirteen somites, which are still quite distinct from one another,
and apparently do not communicate at this stage with the mesenteron.
The epiblast lying immediately over the somites is, as in the, earlier
stages, thickened, and the thickenings of the two sides join each other in
front of the embryonic mouth, where the anterior pair of mesoblastic
somites (the præoral lobes) are almost in contact.
The median ventral epiblast, _i.e._ the epiblast in the area, bounded by
the embryonic mouth and anus before and behind and by the developing
nerve-cords laterally, is extremely thin, and consists of one layer of very
flat cells. Over the dorsal surface of the body the epiblast cells are
cubical, and arranged in one layer.
Measurements of Embryo of Stage E.
Length of embryo 1.12 mm.
Greatest width .64 "
Distance from front end of embryonic mouth to hind
end of embryonic anus .48 "
Greatest length of embryonic mouth .16 "
Length between hind end of embryonic mouth and
front end of embryonic anus .29 "
These measurements were made with a micrometer eyepiece, with the embryo
lying on its back in the position of fig. 38, so that they simply indicate
the length of the straight line connecting the respective points.
This is the last embryo of our series of young stages. The next and oldest
embryo was 3.2 mm. in length. It had ringed antennæ, seventeen (?) pairs of
legs, and was completely doubled upon itself, as in Moseley's figure.
The pits into the cerebral ganglia and a mouth and anus were present. There
can be no doubt that the mouth and anus of this embryo become the mouth and
anus of the adult.
The important question as to the connection between the adult mouth and
anus, and the embryonic mouth and anus of the Stage E, must, considering
the great gap between Stage E and the next oldest embryo, be left open.
Meanwhile, we may point out that the embryonic mouth of Stage E has exactly
the same position as that of the adult; but that the anus is considerably
in front of the hind end of the body in Stage E, while it is terminal in
the adult.
If the embryonic mouth and anus do become the adult mouth and anus, there
would appear to be an entire absence of stomodæum and proctodæum in
_Peripatus_, unless the buccal cavity represents the stomodæum. The latter
is formed, as has been shewn by Moseley, by a series of outgrowths round
the simple mouth-opening of the embryo, which enclosing the jaws give rise
to the tumid lips of the adult.
For our determination of the posterior and anterior ends of each of these
embryos, Stage A to E, we depend upon the opaque tissue seen in each case
at one end of the blastopore.
In Stage A it has the form of a band, extending backwards from the
blastopore.
In Stages B-D, it has the form of an opaque mass of tissue occupying the
whole hind end of the embryo, and extending a short distance on either side
of the posterior end of the blastopore.
This opacity is due in each case to a proliferation of cells of the
hypoblast, and, perhaps, of the epiblast (?).
There can be no doubt that the mesoblast so formed gives rise to the great
majority of the mesoblastic somites.
This posterior opacity is marked in Stage C by a slight longitudinal groove
extending backwards from the hind end of the blastopore. This is difficult
to see in surface views, and has not been represented in the figure, but is
easily seen in sections.
But in Stage D this groove has become very strongly marked in surface
views, and looks like a part of the original blastopore of Stage C.
Sections shew that it does not lead into the archenteron, but only into the
mass of mesoblast which forms the posterior opacity. It presents an
extraordinary resemblance to the primitive streak of vertebrates, and the
ventral groove of insect embryos.
We think that there can be but little doubt that it is a part of the
original blastopore, which, on account of its late appearance (this being
due to the late development of the posterior part of the body to which it
belongs), does not acquire the normal relations of a blastopore, but
presents only those rudimentary features (deep groove connected with origin
of mesoblast) which the whole blastopore of other tracheates presents.
We think it probable that the larval anus eventually shifts to the hind end
of the body, and gives rise to the adult anus. We reserve the account of
the internal structure of these embryos (Stages A-E) and of the later
stages for a subsequent memoir.
We may briefly summarise the more important facts of the early development
of _Peripatus capensis_, detailed in the preceding account.
1. The greater part of the mesoblast is developed from the walls of the
archenteron.
2. The embryonic mouth and anus are derived from the respective ends of the
original blastopore, the middle part of the blastopore closing up.
3. The embryonic mouth almost certainly becomes the adult mouth, _i.e._ the
aperture leading from the buccal cavity into the pharynx, the two being in
the same position. The embryonic anus is in front of the position of the
adult anus, but in all probability shifts back, and persists as the adult
anus.
4. The anterior pair of mesoblastic somites gives rise to the swellings of
the præoral lobes, and to the mesoblast of the head[573].
Footnote 573: We have seen nothing in any of our sections
which we can identify as of so-called mesenchymatous origin.
There is no need for us to enlarge upon the importance of these facts.
Their close bearing upon some of the most important problems of morphology
will be apparent to all, and we may with advantage quote here some passages
from Balfour's _Comparative Embryology_, which shew that he himself long
ago had anticipated and in a sense predicted their discovery.
"Although the mesoblastic groove of insects is not a gastrula, it is quite
possible that it is the rudiment of a blastopore, the gastrula
corresponding to which has now vanished from development." (_Comparative
Embryology_, Vol. I. p. 378, the original edition[574].)
Footnote 574: This edition, Vol. II. p. 457.
"TRACHEATA.--Insecta. It (the mesoblast) grows inwards from the lips of the
germinal groove, which probably represents the remains of a blastopore."
(_Comparative Embryology_, Vol. II. p. 291, the original edition[575].)
Footnote 575: This edition, Vol. III. p. 352.
"It is, therefore, highly probable that the paired ingrowths of the
mesoblast from the lips of the blastopore may have been, in the first
instance, derived from a pair of archenteric diverticula." (_Comparative
Embryology_, Vol. II. p. 294, the original edition[576].)
Footnote 576: This edition, Vol. III. p. 356.
The facts now recorded were discovered in June last, only a short time
before Balfour started for Switzerland; we know but little of the new ideas
which they called up in his mind. We can only point to passages in his
published works which seem to indicate the direction which his speculations
would have taken.
After speculating as to the probability of a genetic connection between the
circumoral nervous system of the Coelenterata, and the nervous system of
Echinodermata, Platyhelminthes, Chætopoda, Mollusca, &c., he goes on to
say:
"A circumoral nerve-ring, if longitudinally extended, might give rise
to a pair of nerve-cords united in front and behind--exactly such a
nervous system, in fact, as is present in many Nemertines (the Enopla
and Pelagonemertes), in _Peripatus_ and in primitive molluscan types
(Chiton, Fissurella, &c.). From the lateral parts of this ring it
would be easy to derive the ventral cord of the Chætopoda and
Arthropoda. It is especially deserving of notice, in connection with
the nervous system of the above mentioned Nemertines and Peripatus,
that the commissure connecting the two nerve-cords behind is placed on
the dorsal side of the intestines. As is at once obvious, by referring
to the diagram (fig. 231 B), this is the position this commissure
ought, undoubtedly, to occupy if derived from part of a nerve-ring
which originally followed more or less closely the ciliated edge of
the body of the supposed radiate ancestor." (_Comparative Embryology_,
Vol. II. pp. 311, 312, the original edition[577].)
Footnote 577: This edition, Vol. III. pp. 378, 379.
The facts of development here recorded give a strong additional support to
this latter view, and seem to render possible a considerable extension of
it along the same lines.]
LIST OF MEMOIRS ON PERIPATUS.
1. M. Lansdown Guilding. "An Account of a New Genus of Mollusca,"
_Zoological Journal_, Vol. II. p. 443, 1826.
2. M. Andouin and Milne-Edwards. "Classific. des Annélides et description
de celles qui habitent les côtes de France," p. 411, _Ann. Scien. Nat._
ser. I. Vol. XXX. 1833.
3. M. Gervais. "Études p. servir à l'histoire naturelle des Myriapodes,"
_Ann. Scien. Nat._ ser. II. Vol. VII. 1837, p. 38.
4. Wiegmann. Wiegmann's _Archiv_, 1837.
5. H. Milne-Edwards. "Note sur le _Peripate juluforme_," _Ann. Scien. Nat._
ser. II. Vol. XVIII. 1842.
6. Blanchard. "Sur l'organisation des Vers," chap. IV. pp. 137-141, _Ann.
Scien. Nat._ ser. III. Vol. VIII. 1847.
7. Quatrefages. "Anat. des Hermelles, note on," p. 57, _Ann. Scien. Nat._
ser. III. Vol. X. 1848.
8. Quatrefages. _Hist. Nat. des Annelés_, 1865, Appendix, pp. 675-6.
9. De Blainville. _Suppl. au Dict. des Sc. Nat._ Vol. I.
10. Ed. Grube. "Untersuchungen üb. d. Bau von _Peripatus Edwardsii_,"
_Archiv für Anat. und Physiol._ 1853.
11. Saenger. "Moskauer Naturforscher Sammlung," _Abth. Zool._ 1869.
12. H. N. Moseley. "On the Structure and Development of _Peripatus
capensis_," _Proc. Roy. Soc._ No. 153, 1874.
13. H. N. Moseley. "On the Structure and Development of _Peripatus
capensis_," _Phil. Trans._ Vol. CLXIV. 1874.
14. H. N. Moseley. "Remarks on Observations by Captain Hutton, Director of
the Otago Museum, on _Peripatus novæ zealandiæ_," _Ann. and Mag. of Nat.
History_, Jan. 1877.
15. Captain Hutton. "Observations on _Peripatus novæ zealandiæ_," _Ann. and
Mag. of Nat. History_, Nov. 1876.
16. F. M. Balfour. "On Certain Points in the Anatomy of _Peripatus
capensis_," _Quart. Journ. of Micr. Science_, Vol. XIX. 1879.
17. A. Ernst. _Nature_, March 10th, 1881.
EXPLANATION OF PLATES 46-53[578].
Footnote 578: The explanations of the figures printed within
inverted commas are by Professor Balfour, the rest are by the
Editors.
COMPLETE LIST OF REFERENCE LETTERS.
A. Anus. _a._ Dorso-lateral horn of white matter in brain. _a.g._ Accessory
gland of male (modified accessory leg gland). _at._ Antenna. _at.n._
Antennary nerve. _b._ Ventro-lateral horn of white matter of brain. _b.c._
Body-cavity. _bl._ Blastopore. C. Cutis. _c._ Postero-dorsal lobe of white
matter of brain. _c.g._ Supra-oesophageal ganglia. _cl._ Claw. _c.m._
Circular layer of muscles. _co._ Commissures between the ventral
nerve-cords. _co.2._ Second commissure between the ventral nerve-cords.
_co_{1}. 2. Mass of cells developed on second commissure. _cor._ Cornea.
_c.s.d._ Common duct for the two salivary glands. _cu._ Cuticle. _d._
Ventral protuberance of brain. _d.l.m._ Dorsal longitudinal muscle of
pharynx. _d.n._ Median dorsal nerve to integument from supra-oesophageal
ganglia. _d.o._ Muscular bands passing from the ventro-lateral wall of the
pharynx at the region of its opening into the buccal cavity. E. Eye. E.
Central lobe of white matter of brain. _e.n._ Nerves passing outwards from
the ventral cords. _ep._ Epidermis. _ep.c._ Epidermis cells. F.1, F.2,
_&c._ First and second pair of feet, &c. _f._ Small accessory glandular
tubes of the male generative apparatus. F._g._ Ganglionic enlargement on
ventral nerve-cord, from which a pair of nerves to foot pass off. _f.gl._
Accessory foot-gland. F._n._ Nerves to feet. _g.co._ Commissures between
the ventral nerve-cords containing ganglion cells. _g.o._ Generative
orifice. H. Heart. _h._ Cells in lateral division of body-cavity. _hy._
Hypoblast. _i.j._ Inner jaw. _j._ Jaw. _j.n._ Nerves to jaws. L. Lips. _l._
Lens. _l.b.c._ Lateral compartment of body-cavity. _le._ Jaw lever
(cuticular prolongation of inner jaw lying in a backwardly projecting
diverticulum of the buccal cavity). _l.m._ Bands of longitudinal muscles.
M. Buccal cavity. M{1}. Median backward diverticulum of mouth or common
salivary duct which receives the salivary ducts. _me._ Mesenteron. _mes._
Mesoblastic somite. _m.l._ Muscles of jaw lever. _m.s._ Sheets of muscle
passing round the side walls of pharynx to dorsal body-wall. _od._ Oviduct.
_oe._ OEsophagus. _oes.co._ OEsophageal commissures. _o.f.g._ Orifice of
duct of foot-gland. _o.j._ Outer jaw. _op._ Optic ganglion. _op.n._ Optic
nerve. _or.g._ Ganglionic enlargements for oral papillæ. _or.n._ Nerves to
oral papillæ. _or.p._ Oral papillæ. _o.s._ Orifice of duct of segmental
organ. _ov._ Ovary. P. Pads on ventral side of foot. _p._ Common duct into
which the vasa deferentia open. _p.c._ Posterior lobe of brain. _p.d.c._
Posterior commissure passing dorsal to rectum. _p.f._ Internal opening of
nephridium into body-cavity. _ph._ Pharynx. _pi._ Pigment in outer ends of
epidermic cells. _pi.r._ Retinal pigment. _p.n._ Nerves to feet. _p.p._
Primary papilla. _pr._ Prostate. R. Rectum. _Re._ Retinal rods. R. _m._
Muscle of claw. _s._ Vesicle of nephridium. _s_{1}. Part of 4th or 5th
nephridium which corresponds to vesicle of other nephridia. _s.c._1. Region
No. 1 of coiled tube of nephridium. _s.c._2. Region No. 2 of ditto.
_s.c._3. Region No. 3 of ditto. _s.c._4. Region No. 4 of ditto. _s.d._
Salivary duct. _s.g._ Salivary gland. _sl.d._ Reservoir of slime gland.
_sl.g._ Tubules of slime gland. _s.o._1, 2, 3, _&c._ Nephridia of 1st, 2nd,
&c., feet. _s.o.f._ Terminal portion of nephridium. _s.p._ Secondary
papilla. _st._ Stomach. _st.e._ Epithelium of stomach. _sy._ Sympathetic
nerve running in muscles of tongue and pharynx. _sy´_. Origin of pharyngeal
sympathetic nerves. T. Tongue. _t._ Teeth on tongue. _te._ Testis. _tr._
Tracheæ. _tr.c._ Cells found along the course of the tracheæ. _tr.o._
Tracheal stigma. _tr.p._ Tracheal pit. _ut._ Uterus. _v.c._ Ventral nerve
cord. _v.d._ Vas deferens. _v.g._ Imperfect ganglia of ventral cord.
PLATE 46.
Fig. 1. _Peripatus capensis_, x 4; viewed from the dorsal surface. (From a
drawing by Miss Balfour.)
PLATE 47.
Fig. 2. A left leg of _Peripatus capensis_, viewed from the ventral
surface; x 30. (From a drawing by Miss Balfour.)
Fig. 3. A right leg of _Peripatus capensis_, viewed from the front side.
(From a drawing by Miss Balfour.)
Fig. 4. The last left (17th) leg of a male _Peripatus capensis_, viewed
from the ventral side to shew the papilla at the apex of which the
accessory gland of the male, or enlarged crural gland, opens to the
exterior. (From a drawing by Miss Balfour.) Prof. Balfour left a rough
drawing (not reproduced) shewing the papilla, to which is appended the
following note. "Figure shewing the accessory genital gland of male, which
opens on the last pair of legs by a papilla on the ventral side. The
papilla has got a slit-like aperture at its extremity."
Fig. 5. Ventral view of head and oral region of _Peripatus capensis_. (From
a drawing by Miss Balfour.)
PLATE 48.
Figs. 6 and 7 are from one drawing.
Fig. 6. _Peripatus capensis_ dissected so as to shew the alimentary canal,
slime glands, and salivary glands; x 3. (From a drawing by Miss Balfour.)
Fig. 7. The anterior end of Fig. 6 enlarged; x 6. (From a drawing by Miss
Balfour.) The dissection is viewed from the ventral side, and the lips, L.,
have been cut through in the middle line behind and pulled outwards, so as
to expose the jaws, _j._, which have been turned outwards, and the tongue,
T., bearing a median row of chitinous teeth, which branches behind into
two. The junction of the salivary ducts, _s.d._, and the opening of the
median duct so formed into the buccal cavity is also shewn. The muscular
pharynx, extending back into the space between the 1st and 2nd pairs of
legs, is followed by a short tubular oesophagus. The latter opens into the
large stomach with plicated walls, extending almost to the hind end of the
animal. The stomach at its point of junction with the rectum presents an
S-shaped ventro-dorsal curve.
A. Anus. _at._ Antenna. F.1, F.2. First and second feet. _j._ Jaws. L.
Lips. _oe._ OEsophagus. _or.p._ Oral papilla. _ph._ Pharynx. R. Rectum.
_s.d._ Salivary duct. _s.g._ Salivary gland. _sl.d._ Slime reservoir.
_sl.g._ Portion of tubules of slime gland. _st._ Stomach. T. Tongue in roof
of mouth.
Fig. 8. _Peripatus capensis_, x 4; male. (From a drawing by Miss Balfour.)
Dissected so as to shew the nervous system, slime glands, ducts of the
latter passing into the oral papilla, accessory glands opening on the last
pair of legs (enlarged crural glands), and segmental organs, viewed from
dorsal surface. The first three pairs of segmental organs consist only of
the vesicle and duct leading to the exterior. The fourth and fifth pairs
are larger than the succeeding, and open externally to the crural glands.
The ventral nerve-cords unite behind dorsal to the rectum.
A. Anus. _a.g._ Accessory generative gland, or enlarged crural gland of the
17th leg. _at._ Antenna. _c.g._ Supra-oesophageal ganglia with eyes. _co._
Commissures between the ventral nerve-cords. _d.n._ Large median nerve to
dorsal integument from hinder part of brain. F.1, 2, &c. Feet. _g.o._
Generative orifice. _oe._ OEsophagus. _oes.co._ OEsophageal commissures.
_or.p._ Oral papilla. _p.d.c._ Posterior dorsal commissure between the
ventral nerve-cords. _ph._ Pharynx. _p.n._ Nerves to feet, one pair from
each ganglionic enlargement. _sl.d._ Reservoir of slime gland. _sl.g._
Tubules of slime gland. _s.o._1, 2, 3, _&c._ Segmental organs. _v.c._
Ventral nerve-cords. _v.g._ Imperfect ganglia of ventral cords.
Figs. 9 and 10. Left jaw of _Peripatus capensis_ (male), shewing reserve
jaws. (From a drawing by Miss Balfour.)
Fig. 9. Inner jaw.
Fig. 10. Outer jaw.
PLATE 49.
Figs. 11-16. A series of six transverse sections through the head of
_Peripatus capensis._
Fig. 11. The section is taken immediately behind the junction of the
supra-oesophageal ganglia, _c.g._, and passes through the buccal cavity,
M., and jaws, _o.j._ and _i.j._
Fig. 12. The section is taken through the hinder part of the buccal cavity
at the level of the opening of the mouth into the pharynx and behind the
jaws. The cuticular rod-like continuation (_le._) of the inner jaw lying in
a backwardly directed pit of the buccal cavity is shewn; on the right hand
side the section passes through the opening of this pit.
Fig. 13. The section passes through the front part of the pharynx, and
shews the opening into the latter of the median backward diverticulum of
the mouth (M{1}), which receives the salivary ducts. It also shews the
commencement of the ventral nerve-cords, and the backwardly projecting
lobes of the brain.
Fig. 14. The section passes through the anterior part of the pharynx at the
level of the second commissure (_co._ 2), between the ventral nerve-trunks,
and shews the mass of cells developed on this commissure, which is in
contact with the epithelium of the backward continuation of the buccal
cavity (M{1}).
Fig. 15. Section through the point of junction of the salivary ducts with
the median oral diverticulum.
Fig. 16. Section behind the pharynx through the oesophagus.
_b.c._ Body-cavity. C. Cutis. _c.b.c._ Central compartment of body-cavity.
_c.g._ Supra-oesophageal ganglia. _c.m._ Layer of circular muscles. _co._
Commissure between ventral nerve-cords. _co._ 2. Second commissure between
the ventral nerve-cords. _co{1}._ 2. Mass of cells developed on second
commissure (probably sensory). _c.s.d._ Common duct for the two salivary
glands. _d.l.m._ Dorsal longitudinal muscles of pharynx. _d.o._ Muscles
serving to dilate the opening of the pharynx. _Ep._ Epidermis. _e.n._ Nerve
passing outwards from ventral nerve-cord. H. Heart. _i.j._ Inner jaw.
_j.p._ Jaw papillæ. _L._ Lips of buccal cavity. _l.b.c._ Lateral
compartment of body-cavity. _le._ Rod-like cuticular continuation of inner
jaw, lying in a pit of the buccal cavity. _l.m._ Bands of longitudinal
muscles. M. Buccal cavity. M{1}. Median backward continuation of buccal
cavity. _m.l._ Muscles of jaw lever. _m.s._ Muscular sheets passing from
side walls of pharynx to dorsal body-wall. _oe._ OEsophagus. _oes.co._
OEsophageal commissures. _o.j._ Outer jaw. _ph._ Pharynx. _s.d._ Salivary
duct. _s.g._ Salivary gland. _sl.d._ Reservoir of slime gland. _sy._
Sympathetic nerves running in muscles of tongue or pharynx. _sy{1}._ Origin
of sympathetic nerves to pharynx. T. Tongue. _v.c._ Ventral nerve-cords.
Figs. 17, 18. Two longitudinal horizontal sections through the head of
_Peripatus capensis_. Fig. 17 is the most ventral. They are both taken
ventral to the cerebral ganglia. In Fig. 17 dorsal tracheal pits are shewn
with tracheæ passing off from them. (Zeiss a a, Hartnack's camera.) C.
Cutis. _c.s.d._ Common salivary duct. _ep._ Epidermis. _i.j._ Inner jaw. M.
Buccal cavity. M{1}. Median backward diverticulum of mouth. _o.j._ Outer
jaw. _s.d._ Salivary ducts. T. Tongue. _t._ Teeth on tongue. _tr._ Tracheæ.
_tr.p._ Tracheal pits.
PLATE 50.
Fig. 19. "A, B, C, D, E, F, G." Seven transverse sections illustrating the
structure of the supra-oesophageal ganglia. (Zeiss A, Hartnack's camera.)
_a._ Dorso-lateral horn of white matter. _b._ Ventro-lateral horn of white
matter. _c._ Postero-dorsal lobe of white matter. _d._ Ventral protuberance
of brain. _e._ Central lobe of white matter. _o.p._ Optic ganglion.
"A. Section through anterior portions of ganglia close to the origin of the
antennary nerve. B. Section a little in front of the point where the two
ganglia unite. C. Section close to anterior junction of two ganglia. D.
Section through origin of optic nerve on the right side. E. Section shewing
origin of the optic nerve on the left side. F. Section through the
dorso-median lobe of white matter. G. Section near the termination of the
dorsal tongue of ganglion cells."
PLATE 51.
Fig. 20. Portion of a transverse section through the hinder part of
_Peripatus capensis_ (male). The section passes through a leg, and shews
the opening of the segmental organ (_o.s._), and of a crural gland,
_o.f.g._, and the forward continuation of the enlarged crural gland of the
17th leg (_f.gl._). (Zeiss a a, Hartnack's camera.) _a.g._ accessory gland
of male (modified crural gland of last leg). C. Cutis. _cl._ Claw. _cu._
Cuticle. _ep._ Epidermis. _f.gl._ Crural gland. _h._ Cells in lateral
compartment of body-cavity. _o.f.g._ Orifice of accessory foot gland.
_o.s._ Opening of segmental organ. P. Three spinous pads on ventral surface
of foot. _pr._ Prostate. R.M. Retractor muscle of claw. _s._ Vesicle of
nephridium. _s.c.i._ Region No. 1 of coiled part of nephridium. _sl.g._
Tubule of slime gland. _s.o.t._ Terminal portion of nephridium. _st._
Stomach. _st.e._ Epithelium of stomach. _v.c._ Ventral nerve-cord. _v.d._
Vas deferens.
Fig. 21. "Longitudinal vertical section through the supra-oesophageal
ganglion and oesophageal commissures of _Peripatus capensis_. (Zeiss a a,
Hartnack.)" _at._ Antenna. _e._ Central lobe of white matter. _j._ Part of
jaw. _s.g._ Salivary gland.
Fig. 22: drawn by Miss Balfour. Brain and anterior part of the ventral
nerve-cords of _Peripatus capensis_ enlarged and viewed from the ventral
surface. The paired appendages (_d_) of the ventral surface of the brain
are seen, and the pair of sympathetic nerves (_sy_{1}) arising from the
ventral surface of the hinder part.
From the commencement of the oesophageal commissures (_oes.co._) pass off
on each side a pair of nerves to the jaws (_j.n._).
The three anterior commissures between the ventral nerve-cords are placed
close together; immediately behind them the nerve-cords are swollen, to
form the ganglionic enlargements from which pass off to the oral papillæ a
pair of large nerves on each side (_or.n._).
Behind this the cords present a series of enlargements, one pair for each
pair of feet, from which a pair of large nerves pass off on each side to
the feet (_p.n_). _at.n._ Antennary nerves. _co._ Commissures between
ventral cords. _d._ Ventral appendages of brain. E. Eye. _e.n._ Nerves
passing outwards from ventral cord. _F.g._ Ganglionic enlargements from
which nerves to feet pass off. _j.n._ Nerves to jaws. _or.g._ Ganglionic
enlargement from which nerves to oral papillæ pass off. _or.n._ Nerves to
oral papillæ. _p.c._ Posterior lobe of brain. _p.n._ Nerves to feet. _s.y._
Sympathetic nerves.
Fig. 23. "Longitudinal horizontal section through the head of _Peripatus
capensis_, shewing the structure of the brain, the antennary and optic
nerves, &c. (Zeiss a a, Hartnack's camera.)" _at._ Antenna. _at.n._
Antennary nerve. _cor._ Cornea. _e._ Central mass of white matter. _l._
Lens. _op.n._ Optic nerve. _ph._ Pharynx. _p.p._ Primary papilla covered
with secondary papillæ and terminating in a long spine. _sy._ Pharyngeal
sympathetic nerves.
Fig. 24. "Eye of _Peripatus capensis_, as shewn in a longitudinal
horizontal section through the head. The figure is so far diagrammatic that
the lens is represented as filling up the whole space between the rods and
the cornea. In the actual section there is a considerable space between the
parts, but this space is probably artificial, being in part caused by the
shrinkage of the lens and in part by the action of the razor. (Zeiss C,
Hartnack's camera.)" (It appears that the ganglionic region of the eye is
covered by a thin capsule, which is omitted in the figure.)
_cor._ Cornea. _l._ Lens. _op._ Optic ganglion. _op.n._ Optic nerve.
_pi.r._ Pigment. _Re._ rods. _s.p._ Secondary papillæ.
Fig. 25. Longitudinal horizontal section through the dorsal skin, shewing
the peculiar arrangement of the circular muscular fibres. (Zeiss A,
Hartnack's camera.)
PLATE 52.
Fig. 26. Portion of ventral cord of _Peripatus capensis_ enlarged, shewing
two ganglionic enlargements and the origin of the nerves and commissures.
(From a drawing by Miss Balfour.)
_co._ Commissures. E._n._ Nerves passing out from ventral cords. F._n._
Nerves to feet. _g.co._ Commissures between the ventral cords containing
ganglion cells. _v.g._ Ganglionic enlargements.
Fig. 27. Segmental organ from the 5th pair of legs of _Peripatus capensis_.
This nephridium resembles those of the 4th legs, and differs from all the
others in its large size and in the absence of any dilatation giving rise
to a collecting vesicle on its external portion (enlarged). The terminal
portion has the same histological characters as in the case of the hinder
segmental organs. (From a drawing by Miss Balfour.)
Fig. 28. Segmental organ or nephridium from the 9th pair of legs of
_Peripatus capensis_, shewing the external opening, the vesicle, the coiled
portion and the terminal portion with internal opening (enlarged). (From a
drawing by Miss Balfour.)
_o.s._ External opening of segmental organ. _p.f._ Internal opening of
nephridium into the body-cavity (lateral compartment). _s._ Vesicle of
segmental organ. _s_{1}. Portion of segmental organ of 4th and 5th legs,
corresponding to vesicle of the other nephridia. _s.c._1. First or external
portion of coiled tube of nephridium, lined by columnar epithelium with
small nuclei; the cells project for very different distances, giving the
inner boundary of this region a ragged appearance. _s.c._2. Region No. 2 of
coiled tube of nephridium, lined by small closely-packed columnar cells.
_s.c._3. Region No. 3 of coiled tube of segmental organ, lined by large
flat cells with large disc-shaped nuclei. _s.c._4. Region No. 4 of coiled
tube of nephridium; this region is very short and lined by small columnar
cells. _s.o.t._ Terminal portion of nephridium.
Fig. 29. "Portion of nephridium of the hindermost leg of _Peripatus
capensis_, seen in longitudinal and vertical section. The figure is given
to shew the peritoneal funnel of the nephridium. Portions of the collecting
sack (_s._) and other parts are also represented. (Zeiss B, Hartnack's
camera.)"
_p.f._ Peritoneal funnel. _s._ Vesicle. _s.c.1_, _s.c.2_, _s.c.3._ Portions
of coiled tube.
Fig. 30. "Section through a tracheal pit and diverging bundles of tracheal
tubes" taken transversely to the long axis of the body. (Zeiss E, oc. 2.)
(From a rough drawing by Prof. Balfour.)
_tr._ _Tracheæ_, shewing rudimentary spiral fibre. _tr.c._ Cells resembling
those lining the tracheal pits, which occur at intervals along the course
of the tracheæ. _tr.s._ Tracheal stigma. _tr.p._ Tracheal pit.
Fig. 31. "Sense organs and nerves attached from antenna of _Peripatus
capensis_ (Zeiss, immersion 2, oc. 2.)" (From a rough drawing by Prof.
Balfour.) The figure shews the arrangement of the epidermis cells round the
base of the spine. The spine is seen to be continuous with the inner layer
of the cuticle.
Fig. 32. Section through the skin of _Peripatus capensis_; it shews the
secondary papillæ covered with minute spinous tubercles and the relation of
the epidermis to them. (The cuticle in the process of cutting has been torn
away from the subjacent cells.) The cells of the epidermis are provided
with large oval nuclei, and there is a deposit of pigment in the outer ends
of the cells. The granules in the protoplasm of the inner ends of the cells
are arranged in lines, so as to give a streaked appearance. (Zeiss E, oc.
2.) (From a rough drawing by Prof. Balfour.)
_c._ Dermis. _cu._ Cuticle. _ep.c._ Epidermis cells. _pi._ Deposit of
pigment in outer ends of epidermis cells. _s.p._ Secondary papillæ.
Fig. 33. Female generative organs of _Peripatus capensis_, × 5. (From a
rough drawing by Prof. Balfour.) The following note was appended to this
drawing: "Ovary rather to dorsal side, lying in a central compartment of
body-cavity and attached to one of the longitudinal septa, dividing this
from the lateral compartment between the penultimate pair of legs and that
next in front. The oviducts cross before opening to the exterior, the right
oviduct passing under the rectum and the left over it. They meet by opening
into a common vestibule, which in its turn opens below the anus. On each
side of it are a pair of short papillæ (aborted feet?)."
F. 16, 17. Last two pairs of legs. _od._ Oviduct. _ov._ Ovary. _ut._
Uterus. _v.c._ Nerve-cord.
PLATE 53.
Figs. 34-39. Five young embryos of _Peripatus capensis_; ventral view. All,
excepting Fig. 37, from drawings by Miss Balfour. In figures 34 to 38_a_
denotes what is probably the anterior extremity.
Fig. 34, Stage A. Youngest embryo found, with slightly elongated
blastopore.
Fig. 35, Stage B. Embryo with three mesoblastic somites and elongated
blastopore. The external boundaries of the somites are not distinct.
Fig. 36, Stage C. Embryo with five somites. The blastopore is closing in
its middle portion.
Fig. 37, Stage D. The blastopore has completely closed in its middle
portion, and given rise to two openings, the future mouth and anus. (From a
rough drawing left by Professor Balfour.) (Zeiss A, Camera Oberhaus. on
level of stage.)
The following note was appended to this drawing in his handwriting: "Young
larva of _Peripatus capensis_. I could not tell for certain which was the
anterior end. Length, 1.34 mm."
Fig. 38, Stage E. Embryo with about thirteen mesoblastic somites in which
the flexure of the hind part of the body has commenced. The remains of the
original blastopore are present as the mouth, placed between the second
pair of mesoblastic somites, and the anus placed on the concavity of the
commencing flexure of the hind part of the body.
Fig. 39. Side view of same embryo.
Figs. 40-42. Drawings by Professor Balfour of three transverse sections
through the embryo from which fig. 36 was taken. (Zeiss c, Camera.) Figs.
40 and 42 pass through the region of the blastopore.
_bl._ Blastopore. _ep._ Epiblast. _hy._ Hypoblast. _me._ Mesenteron. _mes._
Mesoblastic somite.
Fig. 43. Male generative organs of _Peripatus capensis_, viewed from the
dorsal surface. (From a drawing by Miss Balfour.)
_a.g._ Enlarged crural glands of last pair of legs. F.16, 17. Last pairs of
legs. _f._ Small accessory glandular tubes. _p._ Common duct into which
vasa deferentia open. _p.r._ Prostate. _te._ Testes. _v.c._ Nerve-cord.
_v.d._ Vas deferens.
CAMBRIDGE: PRINTED BY C. J. CLAY, M.A., AND SON, AT THE UNIVERSITY PRESS.
TRANSCRIBER'S NOTES:
Underscores surround text in italics, _like this_.
Hyphens were spaced in ranges of small numbers to ease readability, e.g.,
"1/2000-1/3000 of an inch" was changed to "1/2000 - 1/3000 of an inch".
Raised dots in numbers were converted to decimals. Superscript letters
are enclosed in braces, e.g. P{1}.
The Greek letter, Lambda, is spelled out.
Use of periods and commas in the abbreviations within and referring to
illustrations is inconsistent. Often punctuation marks do not match the
illustrations to which they refer. Periods were retained; commas
were added to separate figure numbers from abbreviations within the figure.
Spacing within the abbreviations was standardized.
Footnotes were renumbered sequentially, indented, and moved to follow the
paragraph in which the anchor occurs. There is no anchor for footnote 496;
anchor was placed at the spot the transcriber deemed it likely belonged.
Changes for consistency within the text of the book:
body cavity to body-cavity
body wall to body-wall
choroid-slit to choroid slit
develope(s) to develop(s)
dog fish to dog-fish
Elasmobranchs to Elasmobranchii
Entwickelung to Entwicklung
head-fold to head fold
inter-renal to interrenal
juxta-position to juxtaposition
lenslike to lens-like
re-agent(s) to reagent(s)
omphalo-meseraic to omphalomeseraic
pleuroperitoneal to pleuro-peritoneal
proto-vertebra(æ) to protovertebra(æ)
re-appear to reappear
semi-lunar to semilunar
side-fold to side fold
spongework to sponge-work
subgerminal to sub-germinal
sub-intestinal to subintestinal
sub-kingdom to subkingdom
sub-notochordal to subnotochordal
suboesophageal to sub-oesophageal
supraoesophageal to supra-oesophageal
urino-genital to urinogenital
Urogenital-system to Urogenitalsystem, except where cited as a title of
a work.
Verwandschaft to Verwandtschaft
widespread to wide-spread
wood-cut(s) to woodcut(s)
zool. zoot. to zool.-zoot.
italics removed from eight instances of 'vide'
italics, where missing, were added to 'loc. cit', 'i.e.' and 'e.g.'
Other changes:
'reremainder' to 'remainder' ... as compared with the remainder of ...
'on' to 'or' ... one or two words ...
'splachnopleure' to 'splanchnopleure' ... where the somatopleure and
splanchnopleure unite,...
'Sitzen.' to 'Sitzun.' (Footnote - abbreviation for 'Sitzungsberichte')
'diffiulty' to 'difficulty' ... as a serious difficulty....
'it' to 'is' ... is still very difficult to observe....
'primive' to 'primitive' ... That such a condition could be a primitive
one seemed scarcely possible....
'opthalmicus' to 'ophthalmicus'
... to form ramus ophthalmicus superficialis ...
... as the _ramus ophthalmicus superficialis of the fifth nerve_ ...
'Ureierernester' to 'Ureiernester'
... nests of ova (Ureiernester),...
'vascula' to 'vascular' ... the subjacent vascular stroma ...
'Metozoa' to 'Metazoa' ... Coelenterata and the Metazoa....
duplicate word 'of' removed ...'(2) Of a layer of protoplasm' changed to
'(2) a layer of protoplasm' ...
'protodæum' to 'proctodæum' ... The proctodæum (_pr._) has also grown ...
'is it' to 'it is' ... where it is attach to the side of the body ...
'is is' to 'is in' ... but is in some respects peculiar....
'continous' to 'continuous' ... forms a continuous whole,...
'Zussammenhang' to 'Zusammenhang' ... Ueber d. Zusammenhang d. ...
'Tranverse' to 'Transverse' ... Transverse sections of the head ...
'odontophor' to 'odontophore' ... of the odontophore of a mollusc....
'lens' to 'legs' ... the last (17th) pair of legs are enlarged ...
'Platyelminthes' to 'Platyhelminthes' ...the nervous system of
Echinodermata, Platyhelminthes,...
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