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THE WORKS
OB'
FRANCIS MAITLAND BALFOUR
VOL. I.
SEPARATE MEMOIRS.
Uottiron :
MACMILLAN AND CO.
1885
THE WORKS
OF
FRANCIS MAITLAND BALFOUR.
VOL. I.
jttemorfal Oftu'ttom
PRINTED BY C. J. CLAY, M.A. AND SON,
AT THE UNIVERSITY PRESS.
Memorial (Station,
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.
MACMILLAN AND CO.
1885
[The Right of Translation is reserved.]
5\2
v. I
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 meet-
ing 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.
B. b
M345578
PREFACE.
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 pre-
fixed 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. I. 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 wood-cuts illustrating
memoir no. xx. of Vol. i.
PREFACE. iii
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 Hilde-
brand of Florence has executed a posthumous bust in
bronze*. The portrait which forms the frontispiece of
Vol. i. 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 com-
plete success his features and expression, we would ven-
ture to ask them to bear in mind the acknowledged
difficulties of posthumous portraiture.
* 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 i
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 blasto-
derm. With Plate i 29
III. On the disappearance of the Primitive Groove in the
Embryo Chick. With Plate I 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 Elasmo-
branch 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
VI
TABLE OF CONTENTS.
1876
IX. On the spinal nerves of Amphioxus .
1876—78
X. A Monograph on the development of Elasmobranch
Fishes. With Plates 6—21
1878
XI. On the phenomena accompanying the maturation and
impregnation of the ovum ......
XII. On the structure and development of the vertebrate ovary.
With Plates 24, 25, 26
1879
XIII. On the existence of a Head-kidney in the Embryo Chick,
and on certain points in the development of the
Miillerian duct. By F. M. BALFOUR and A. SEDGWICK.
With Plates 27 and 28
XIV. On the early development of the Lacertilia, together with
some observations on the nature and relations of the
primitive Streak. With Plate 29 ....
XV. On certain points in the Anatomy of Peripatus Capensis .
XVI. On the morphology and systematic position of the
Spongida
1880
XVII. Notes on the development of the Araneina. With Plates
30, 3i, 32
XVIII. On the spinal nerves of Amphioxus
XIX. Address to the Department of Anatomy and Physiology
of the British Association for the Advancement of
Science
PAGE
197
203
521
549
618
644
657
661
668
696
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 classi-
fication of the Mammalia 734
TABLE OF CONTENTS. Vll
PAGE
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 loth 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 chil-
dren 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 Whitting-
hame 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 be-
came 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
B. I
INTRODUCTION.
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 pre-
serving skins, succeeded in making a very considerable collec-
tion. 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 some-
what 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
INTRODUCTION.
same time warm-hearted and affectionate ; full of strong im-
pulses, 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, some-
what 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 1 86 1 he was sent to the Rev. C. G. Chittenden's prepara-
tory school at Hoddesden in Hertfordshire, and here the quali-
ties 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
shew 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
I — 2
INTRODUCTION.
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 obser-
vation 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 micro-
scope) "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 develope 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 concern-
ing 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
INTRODUCTION. 5
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 con-
stituted 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 scrupu-
lous 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 resi-
dence, and his influence in wisely directing Balfour's studies had
a most beneficial effect on the latter's progress.
INTRODUCTION.
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 Praelector,
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 com-
petitors.
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
INTRODUCTION.
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 investi-
gation 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 un-
satisfactory 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 overwork-
ing himself, he obviously grew stronger. He rejoiced exceed-
ingly 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
INTRODUCTION.
that he should never be able to make satisfactory microscopic
sections ; as to his being able to make drawings of his dissec-
tions 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
INTRODUCTION.
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 in-
terest 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 phe-
nomena 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
10 INTRODUCTION.
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 gentle-
man 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 hesi-
tate for a moment to neglect altogether the formal written
answers (and indeed the papers of questions were only intro-
duced as a safeguard, or as a resource in case evidence of
original power should be wanted) and unanimously recom-
mended 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 Elas-
mobranch 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 Microscopi-
cal Science a preliminary account of his Elasmobranch re-
searches.
He and his friends thought that after these almost inces-
sant labours, and . the excitement necessarily contingent upon
the fellowship election, he needed rest and change. Ac-
cordingly on the 1 7th 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.
I875-
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.
INTRODUCTION. 1 1
On his return to Cambridge, he still continued working on
the Elasmobranchs, 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 Phi-
losophical 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 "Obser-
vations 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 tra-
velling, 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
12 INTRODUCTION.
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 arrange-
ment 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 en-
thusiasm 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 develop-
ment 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 com-
plete 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 begin-
nings 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,
INTRODUCTION. 13
having meanwhile left Cambridge. Indeed, from this time on-
ward, 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 eTerfient-
ary 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 dis-
secting 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
one1, 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
1 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.
14 INTRODUCTION.
enthusiasm. His class, at first slowly, but afterwards more
rapidly, increased in numbers, and, what is of more import-
ance, 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.
Even this new accommodation soon became insufficient,
and in the spring of 1 882 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
INTRODUCTION. 15
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 them-
selves, 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 Sec-
tion with charge of the Department of Anatomy and Physio-
logy. 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 inter-
esting 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 there-
fore 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 investi-
gation.
During these years of travail with the Comparative Em-
bryology the amount of work which he got through was a
marvel to his friends, for besides his lectures, and the re-
searches, and the writing of the book, new labours were de-
manded 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
16 INTRODUCTION.
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 im-
proving in health after his first year at Cambridge, he was not
robust, and from time to time he seemed on the point of break-
ing 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
INTRODUCTION.
brother Gerald, and spent some weeks near Zermatt in systematic
climbing, ascending, among other mountains, the Matterhorn and
the Weisshorn. In the following summer, 1 88 1, he and his brother
Gerald again visited the Alps, dividing their time between the
Chamonix district and the Bernese Oberland. On this occa-
sion 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 diffi-
culties, 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. More-
over 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 pur-
sued 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, 1 88 1, 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, Presi-
dent of the Philosophical Society, and in the December of that
B. 2
1 8 INTRODUCTION.
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 re-
mained a Lecturer of Trinity College, giving lectures in a Uni-
versity 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 1 88 1 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 Cam-
bridge. 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
1 88 1 — 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 develope 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
INTRODUCTION. 1 9
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 prepara-
tion 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 com-
plained of being unwell, and in due time distinct symptoms of
typhoid fever made their appearance. The attack at first pro-
mised 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
2 — 2
20 INTRODUCTION.
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 Pro-
fessor 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, en-
gaged 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
Geant, 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
INTRODUCTION. 21
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 £i$o. 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 Cour-
mayeur. 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 sepa-
rates 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
22 INTRODUCTION.
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 precipi-
tated 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 I9th. 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 Eus-
tace, 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 in-
clined 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
INTRODUCTION. 23
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 Iiis
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 judg-
ment 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 fol-
lowing 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
24 INTRODUCTION.
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 \
By G. W. and F. M. BALFOUR, Trinity College, Cambridge.
THE interesting relation between the Porphyrite of Whit-
berry 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 Geologi-
cal Siirvey 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 inter-
section 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 con-
siderably 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
1 From the Geological Magazine, Vol. ix. No. 4. April, 1872.
26
GEOLOGY OF THE EAST LOTHIAN COAST.
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 in-
creasing 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.
FIG. I.
FIG. i. 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 be-
neath, 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
GEOLOGY OF THE EAST LOTHIAN COAST. 27
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 county1, adopts a view on this subject which is somewhat
different from that which is suggested in this paper. He con-
siders 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.
LEVEL OF
SHORE
FIG. 2
FIG. i. VERTICAL SECTION THROUGH CC. DIAGRAM (Fio. i).
A. Orifice by which the lava ascended. B. Sandstone Beds. B'. Hypothetical
extension of ditto. C. Sheet of lava spread over the sandstones /?. C. Hypo-
thetical extension of ditto.
He admits that the inclination of the sandstone beds towards
the igneous mass in the centre is a phenomenon that is some-
what difficult to explain, and suggests that a subsequent contrac-
tion 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 orifice2."
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
1 Memoirs of Geological Survey of Scotland, sheet 33, pp. 40, 41.
2 Note on p. 41 of Mem. Geol. Survey of East Lothian.
28 GEOLOGY OF THE EAST LOTHIAN COAST.
*
strata are bent down so as to kdip 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 verti-
cal, 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. In-
deed, 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 him-
self has suggested, that the high angle at which the strata dip is
difficult to account for. But, in fact, this steep inclination con-
stitutes 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 BLASTODERM1.
With Plate I. figs, i — 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 embryo-
logists, but is nevertheless of the greatest interest, both in refer-
ence 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 out-
lines 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
1 From the Quarterly Journal of Microscopical Science, Vol. xin., 1873.
30 DEVELOPMENT AND GROWTH OF
Keimblatter im Hiihnerei," Sitzungsberichte der K. Akademie der
Wissenscliaften in Wien, 1868. Oellacher, " Untersuchung uber
die Furchung und Blatterbildung im Hiihnerei," Studien aus dem
Institut filr Experim, PatJwlogie in Wien, 1870 (pp. 54 — 74), and
Dr Klein, Ixiii. Bande der Sitz. der K. Acadamie der Wiss. in
Wien, 1871.
The unincubated blastoderm (PI. I, fig. i) 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
(PI. I. fig. 6) of the cells. The diameter of the cells when
viewed from above is from ^Vo — FcW °f an mcn- 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 appear-
ance, 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
THE LAYERS OF THE BLASTODERM. 31
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 ^J^ — Y^ of an inch. The largest of the formative
cells come up to ^ 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 seg-
mentation— 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 consider-
ably 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 //) 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,
32 DEVELOPMENT AND GROWTH OF
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 be-
tween 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 (PI. I, 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 PI. I, 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 im-
portance, 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
THE LAYERS OF THE BLASTODERM. 33
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, ist. That the mesoblast
and hypoblast are formed nearly synchronously, and except at
the centre a fairly even sprinkling of lower layer cells isTrom
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 fiir wissenschaftliche
Zoologie, 1873, " Beitrage zur Entwick. Gesch. der Knochen-
fische") 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,
fur 1869) has given a different account of the origin of the
layers. There is no doubt, however, in opposition to his stat.e-
' ments and drawings, that from the very first the hypoblast is
distinct from the mesoblast, which is, indeed, most conspicu-
ously shewn in good sections ; and his drawings of the deriva-
tion 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 (PI. I, 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
B- 3
34 DEVELOPMENT AND GROWTH OF
silver nitrate shew that they are much expanded horizontally,
but very irregular as to size, varying even within a small area
from ffaq — ffa 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 ¥^OT of an inch in diameter
over the centre of the pellucid area, and increase to -^^ 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
THE LAYERS OF THE BLASTODERM. 35
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 ac.tual 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 succeed-
ing paper), it cannot be considered of any importance in reference
to the possible origin of the Wolfftan 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.
3—2
36 DEVELOPMENT AND GROWTH OF
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 PI. I, 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 PI. I, 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
THE LAYERS OF THE BLASTODERM. 37
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, arid there super-
venes a complete and unbroken continuity between the hypo-
blast 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 proto-vertebrae, are at the eighteenth hour consider-
ably 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
38 DEVELOPMENT AND GROWTH OF
to consist of a nucleus surrounded simply by granular proto-
plasm.
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
(PI. I, fig. 10). This regularity, however, is much more marked
in some specimens than in others. These cells are about 4oVotn
of an inch in breadth, and y^^th in length. On each side of the
embryo immediately external to the proto-vertebrae 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 ^y^th 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
THE LAYERS OF THE BLASTODERM. 39
in size towards the edge of the pellucid area. Here they are
about jtj^th 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 (PI. I, 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, ^oijth inch, rising to ^oVtfth 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 -^^ to ^Vutn
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 any-
where else in the epiblast, being here about y^^th 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 y^Vrrth to aoVoth mcn ^n diameter, but at the periphery
of the opaque area they are smaller again, being about the
•jniVoth 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.
4O DEVELOPMENT AND GROWTH OF THE BLASTODERM.
EXPLANATION OF PLATE I. Figs. 1—5 and 9—12.
Fig. i. 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 (6).
Fig. 2. Section through the periphery of an eight hours' blastoderm, shewing the
epiblast (/), 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 (//) 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 com-
pletely 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. n. 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 *.
With Plate I, figs. 6—8 and 13—19.
THE investigations of Dursy (Der Primitivstreif des Hiihn-
chciis, 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 corro-
borating 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 thicken-
ing 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.
1 From the Quarterly Journal of Microscopical Science, Vol. xm, 1873.
42 PRIMITIVE GROOVE IN THE EMBRYO CHICK.
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 PI. I, 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
PRIMITIVE GROOVE IN THE EMBRYO CHICK. 43
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. More-
over, 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 ex-
tremity 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 me-
dullary streak is the medullary groove, which subsequently forms
the cavity of the medullary or neural canal.
Everything which I have described above can without diffi-
culty 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 PI. I, 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 I, figs. 7, 9, 17) all sections through the primitive groove
44 PRIMITIVE GROOVE IN THE EMBRYO CHICK.
shew most clearly an adhesion between the epiblast and meso-
blast. 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 back-
wards by the growth of the medullary groove.
The specimen figured in PL I, fig. 18, magnified about ten
diameters, shews the appearance presented by an embryo of
twenty-three hours. The medullary groove (me) 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 corre-
sponding numbers in fig. 18. Section I (fig. 13) passes through
the middle of the medullary canal.
In it the following points are to be noted, (i) That the
epiblast becomes very much thinner where it lines the me-
dullary canal (me), 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
distinct1.
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 I. In
the third section (fig. 15) the notochord is still more expanded;
1 In the figure the notochord has been made too distinct.
PRIMITIVE GROOVE IN THE EMBRYO CHICK. 4$
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 proto-vertebrae
begin to be formed along the sides of the medullary groove (PI.
I, fig. 19, pv). Each new proto-vertebra (of those which are
formed from before backwards) arises just in front of the an-
terior 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 di-
rectly 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
46 PRIMITIVE GROOVE IN THE EMBRYO CHICK.
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 I. 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 (nid),
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 meso-
blast. Headfold (//).
Figs. 13 — 17 are sections through the blastoderm, drawn in fig. 18 through the
lines i, 2, 3, 4, 5 respectively.
The first section (fig. 13) passes through the true medullary groove (me); 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 me-
dullary 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, Proto-vertebrse ; 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 CHICK1.
With Plate II.
THE development of the first blood-vessels of the yolk-sac
of the chick has been investigated by a large number of ob-
servers, but with very discordant results. A good historical
resume of the subject will be found in a paper of Dr Klein
(liii. Band der K. Akad. der Wissensch. Wien], its last in-
vestigator.
The subject is an important one in reference to the homo-
logies 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
1 From the Quarterly Journal of Microscopical Science^ Vol. XIII, 1873.
48 DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK.
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 (i) 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 proto-vertebrae on each side.
Fig. i shews the appearance at this time. Immediately
above the hypoblast there are certain cells whose protoplasm
sends out numerous processes. These processes vary consider-
ably 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
DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK. 49
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 proto-vertebrae.
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 be-
ginning 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
B. 4
5O DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK.
see them distinctly), have a more jagged and irregular appear-
ance 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 forma-
tion 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
PI. 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
DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK. 51
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 areai that the chief formation of blood-corpuscles
takes place.
The part of the pellucid area intermediate in position be-
tween 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 capil-
laries 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 con-
nect 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 sur-
round 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
4—2
52 DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK.
the protoplasmic network, a large number of the connecting
processes in this network have become filled with blood-cor-
puscles. The appearances presented by the network at a
slightly later stage than this is shewn in PI. 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 proto-vertebrae, 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 an-
terior 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 de-
velopment has reached the stage described, very little is re-
quired 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 invest-
ment 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
DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK. 53
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 ac-
count of this formation. It results from the cells of the meso-
blast 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 PI. 2.
fig- 9) i° tne opaque area, joining the somatopleure and the
54 DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK.
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 appear-
ances of the capillaries in the vascular area are similar to the
appearances in the pellucid area, from which it is fair to con-
clude 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 aortae 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 refer-
ence 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 ; pro-
bably they come from the walls of the capillaries.
DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK. 55
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 movementsjn
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 proto-
plasm 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 observa-
tions are not quite complete. It is, however, easy to prove
from sections (vide figs. 10 and II, 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 thick-
ened mass of mesoblast is, as can easily be seen from figs. 10
and 11, PI. 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 n. 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
56 DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK.
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 h z, 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 splanch-
nopleure, 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 to-
gether. 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 pro-
cess 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 (Bulletin de
rAcadem. Impe'riale de St Petersb., torn, 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
DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK. 57
which separated at first the two halves of the heart became
absorbed, the endothelium lining of each of the originally sepa-
rate vessels would remain complete, dividing the cavity of the
heart into two parts. The partition in the central line is, Jiow-
ever, 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 PI. 2, figs. 10 and 11, explain what I have just said
about the origin of the heart. Immediately around the noto-
chord 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 sec-
tions are taken. The latter (sp) forms with the hypoblast (liy}
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. n, 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 meso-
blast 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
58 DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK.
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. i is taken from the anterior part of the pellucid area of a thirty hours' chick,
with four proto-vertebrse. 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 proto-vertebras. In fig. 3 the nuclei are seen to have considerably in-
creased 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 con-
taining 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 sec-
tion, 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, i — 5 are drawn with an ^ 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' em-
bryo ; 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 invest-
ment of Klein ; /, e, pellucid area ; o, p, 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. Alimen-
tary canal ; hb, hind brain ; nc, notochord ; e, epiblast ; s, o, mesoblast of the soma-
topleure ; sp, mesoblast of the splanchnopleure ; hy, hypoblast ; hz, cavity of the
heart.
DEVELOPMENT OF THE BLOOD-VESSELS OF THE CHICK. 59
Fig. ii.— Section through the same embryo as fig. 10, and passing through the
orifice of the omphalo-meseraic vein, of, Omphalo-meseraic 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— meso-
blast which has turned to assume its normal direction after being folded in to form
the muscular wall of the alimentary canal. In fig. 1 1 the cavities so formed on each
side have not yet united, but in fig. 10 they have united. When the folding be-
comes more complete the cavities (of, of) in fig. 1 1 will unite, and in this way the
origin of the omphalo-meseraic veins will be carried further backwards. In the sec-
tion immediately behind section 1 1 the mesoblast had become thickened, but had not
split.
V. A PRELIMINARY ACCOUNT OF THE DEVELOPMENT OF
THE ELASMOBRANCH FiSHES1.
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 Scy Ilium
stellare in a more advanced condition than I ever had at Naples,
which have enabled me to fill up some lacunae in my observa-
tions.
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 Elas-
mobranchii. 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
1 From the Quarterly Journal of Microscopical Science, Vol. xiv. 1874.
Read in Section D, at the Meeting of the British Association at Belfast.
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 6l
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 ex-
amined 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
chalazae.
The Yolk.
The yolk is not enclosed in any membrane comparable to
the vitelline membrane of Birds, but lies freely in a viscid albu-
men 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 striae 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 striae are normal, or produced
by the action of water I have not determined.
Position of the Blastoderm. .
The blastoderm is always situated, immediately after impreg-
nation, 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 circu-
62 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
lar 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 distinc-
tion 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 be-
tween 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 blasto-
derm was not defined by a true furrow, and the segmentation
furrows still ended below without meeting any horizontal fur-
rows, 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
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 63
this particular the segmentation in these animals differs materi-
ally from that in the Bird, where the horizontal furrows appear
very early.
In each segment a nucleus was generally to be seen in sec-
tions. 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 de-
scribed 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 tJie Yolk.
Intimately connected with the segmentation is the appear-
ance 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
64 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
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 PI. 3, fig. i, 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 struc-
ture. This is shewn in PI. 3, figs. I and 2, ;/.
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 PI. 3,
fig. I.
. These nuclei colour red with haematoxylin 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 PI. 3, fig. i, 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.
(i) We have, then, nuclei of this very peculiar character
scattered through the subgerminal 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
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 65
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 PI. 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 disap-
peared partly or entirely, leaving only this fine network with
the nuclei in it.
A specimen of this kind is represented in PI. 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 lines1 (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
1 The interpretation of this network is entirely due to Dr Kleinenberg, who sug-
gested it to me on my shewing him a number of specimens exhibiting the nuclei and
network.
B. 5
66 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
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.
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 pro-
bable. 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 for-
mation ? 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 PI. 3, fig. I. 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 ob-
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 67
served that the nucleus of a sphere first divides1, 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 Neplielis
(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.
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 dis-
tinct 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 speci-
mens of this age which shew the formation of these new cells
with great clearness. This is most distinctly to be seen imme-
diately 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 cer-
tain of this.
1 Kowalevsky (" Beitrage zur Entwickelungsgeschichte der Holothurien, " Mt-
moirs de fAc. 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.
5—2
68 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
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 con-
cerned 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 ap-
pear and increase either by division or by a process of in-
dependent formation, and a great number of these subse-
quently 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 ob-
servers. Kupffer (Archiv. fur Micr. Anat., Bd. IV. 1868) and
Owsjannikow ('' Entwickelung der Coregonus," Bulletin der
Akad. St Petersburg^ Vol. XIX.) in osseous fishes1, Ray Lan-
kester (Annals and Mag. of Nat. Hist. Vol. XI. 1873, p. 81) in
Cephalopoda, Gotte (Archiv. fur 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 ap-
pearance.
1 Gotte, at the end of a paper on "The Development of the Layers in the Chick "
(Archiv. Jiir Micr. Anat., Vol. X. 1873, P- J96). 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.
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 69
Formation of tJie Layers.
Leaving these nuclei, I will now pass on to the formation
of the layers.
At the close of segmentation the surface of the blasto-
derm is composed of cells of a uniform size, which, however,
are too small to be seen by the aid of the simple micro-
scope.
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 blas-
toderm 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 subse-
quently appear.
This very early appearance of distinction in the blasto-
derm 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 fur Wiss. Zoo-
logie, Vol. XXXIII. 1873) has shewn, and, though differing from
him on many other points, on this point Gotte (Arch, fur 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
7O DEVELOPMENT OF THE ELASMOBRANCH FISHES.
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 other-
wise 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 re-
lations 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, s g}. In
the next and third stage (PI. 3, fig. 4, s g] 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.
DEVELOPMENT OF THE ELASMOBRANCH FISHES. /I
The segmentation cavity of the Dog-fish most nearly agrees
with that of Osseous fishes in its mode of formation and re-
lation to the embryo.
Dog-fish resemble Osseous fish in the fact that their em-
bryos 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 Gotte, Archiv. fur
Micr. Anat. Bd. IX. are correct) in the floor of the segmen-
tation cavity being formed at one period by yolk. Toge-
ther 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 Gotte 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 differ-
ence, 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,
72 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
forming the lower layer, are of a fairly uniform size, and poly-
gonal 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 conspi-
cuous in the next and second stage (PI. 3, fig. 3).
In the second stage the chief points of progress, in addi-
tion 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 seg-
mentation 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 pro-
jecting 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 ap-
pear. But its most remarkable feature is that at the outer
edge of the " embryonic rim" (e r) it turns round and becomes
continuous with the lower layer cells. This feature is most im-
portant, and involves some peculiar modifications in the develop-
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 73
ment. I will, however, reserve a discussion of its meaning till
the next stage.
The only other important feature of this stage is the ap-
pearance 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 cer-
tainty. The following facts, however, make me believe that
the newly formed cells do play an important part in the forma-
tion of this layer.
(1) The presence at an earlier date of almost a row of nuclei
under the floor of the segmentation cavity (PI. 3, fig. i).
(2) The presence on the floor of the cavity of such large cells
as those represented in fig. i, b d, cells which are very different,
as far as the size and granules are concerned, from the remain-
der 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 cor-
responds with what Kupffer (loc. tit.} 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 sym-
metry between the embryonic end of the germ and the opposite
end first appears.
74 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
I described in the last stage the appearance of the " embry-
onic 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, be-
tween them, a flat broadish ridge, "tfie embryo" (PI. 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, m g) —
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.
Oh 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 differ-
entiated into hypoblast and mesoblast, and remain continu-
ous 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 dif-
ferentiation 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 primi-
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 75
tive, 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 un-
doubtedly a very early condition of the mesoblast. The con-
dition 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 Lunibricus. 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 " Wurmern u. Arthropoden " ; Me"m. de I'Acad.
Imp. St Peter sbourg, 1871).
From longitudinal sections I have found that the segmen-
tation 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 vas-
cular 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 ceHs somewhat
resembling the epiblast-cells, and an upper one of more flat-
tened cells (PI. 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, re-
mains 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 meso-
blast in this way I have assumed that they are formed out
of the large mass of lower layer cells which underlie the epi-
blast at the embryonic end of the blastoderm. But there
is another and, in some ways, rather a tempting view, viz.
76 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
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 em-
ployed 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 conti-
nuous 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 involu-
tion, 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 ne-
cessary 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 koloblastic
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 "Stur-
geon," and " Batrachians."
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 77
The second class are those with meroblastic ova and no anus
of Rusconi, and with an alimentary canal formed by the infold-
ing of the sheet of hypoblast, the digestive canal remaining in
communication with the food-yolk for the greater part of em-
bryonic 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 de-
velopment of the alimentary canal took place.
In all the members of the first class, viz. " A mphioxus" 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 Store "), communicates freely at its ex-
treme 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 other1.
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 Dog-
1 This has been already made out by Kowalevsky, " Wurmern u. Arthropoden, "
lot. cit.
78 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
fish 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 involu-
tion. 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 indirect 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 em-
bryonic 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 hypo-
thetically to trace the steps by which the involution gradually
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 79
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 Ampkioxus'&oA. the Dog-
fishes, since in them the yolk becomes divided during segmen-
tation into lower layer cells and epiblast, but a modified invo-
lution 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— (i)
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 pouits
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 con-
verted 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
So DEVELOPMENT OF THE ELASMOBRANCH FISHES.
in Osseous fishes is the true medullary groove ; although Oel-
lacher 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 ad-
dition 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 epi-
dermic layer, as has been supposed to be the case by Strieker
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 under-
going other important changes, with the exception of the ap-
pearance of two swellings, one on each side of its tail.
These swellings, which I will call the Caudal lobes (figs. 8
and 9, t s), 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 develop-
ment of the Dog-fish, and are still more marked in the Torpedo
(PI. 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 hypo-
blast appears (PI. 3, figs, ^a and jb, 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
DKVKLOPMKXT OF THE EI.ASMOBRAXCH FISHKS. 8l
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 for-
mation will be quite clear without further description from
an inspection of PI. 3, figs, "a and jb, cli and ell . Both are
taken from one embryo. In fig. 7^, the most anterior of the
two, the notochord has become quite separated from the hypo-
blast. 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. 6a and 6b, that
there is no sign of a thickening of the hypoblast. My numerous
sections (all made from embryos hardened in osmic acid) shew-
ing 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 llic
hypoblast, one on e"ach 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.
H. 6
82 DEVELOPMENT OF THE- ELASMOBRANCH FISHES.
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 :
(i) 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 meso-
blast, 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 imsegmentcd portion of the axial skeleton.
Whether the strong a priori difficulties of the hypoblastic
origin of the notochord are sufficient to counterbalance the
O
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 illus-
trating 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
DKVKI.OI'MF.XT OF THK ELASMO6RANCH FISIIKS. 8}
origin would become lost ; while if, on the other hand, it is
primitively a hypoblastic structure, we see from higher verte-
brates 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 ei 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 modifi-
cations 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 arc derived, important conse-
quences must follow.
It will, for instance, by no means be sufficient evidence of
6—2
84 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
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 dis-
cussion 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 PI. 3, figs. 6a, 66,
jb, 11. 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, how-
ever, another point in reference to it which is still more inter-
esting. The cells to form the ingrowth from the bottom (ven-
tral) 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. 6b, 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
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 85
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
protovertebrae.
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 con-
siderably later period, the mesoblast is not split into somato-
pleure and splanchnopleure, and it is not divided into vertebral
and lateral plates. The transverse lines of division of the proto-
vertebras do not, however, extend to the outer edge of the
undivided lateral plates.
The differences between this mode of formation of the pro-
tovertebrae 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 protovertebras of the Dog-fish.
I will only now say that I have had in the early stages
to investigate the formation of the protovertebras entirely by
means of sections, the objects being too opaque to be other-
wise 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 (PI. 3, fig. 8).
In the region of the head the medullary groove is at first
totally absent (vide section, PI. 3, fig. 8. a),
Indeed, as can be seen from fig. 8 b, the laminae dorsales, so
86 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
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 Stur-
geons ; 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, / s). They are very conspicuous
objects, and, together with the spatula-like head, give the whole
embryo an alm6st comical appearance. The medullary canal
has by this time become completely closed in the region of the
tail (figs. 8 and 8 U].
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 groove1 between the two caudal lobes must not be con-
fused (as may easily be done) with the medullary groove, which
by the time the former groove has become conspicuous is a
completely closed canal.
The vertebral plates are not divided (vide fig. 7) into a
somatopleuric and splanchnoplcuric layer by this stage, except
in the region of the head (vide fig. 8 £, //), 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 subse-
quent history I shall say a few words when I come to speak of
the later stages.
1 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.
DEVELOPMENT OF THE ELASMOBKANCH FISHES. 8/
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 insig-
nificant. 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 divi-
sion 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 proto-
vertebrae, of which about twenty are present, can noiv 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 em-
bryo, I have followed in my description a chronological order.
I shall now cease to do so, since it would be too long for a pre-
liminary notice of this kind, but shall confine myself to the
history of a few organs whose development is either more im-
portant or more peculiar than that of the others.
The Protovertebra.
I have thought it worth while to give a short history of
the development of the protovertebrae, firstly, because it is
very easy to follow this in the Dog-fish, and, secondly, because
DEVELOPMENT OF THE ELASMOBKANCH FISHES.
I believe that the Dog-fish have more nearly retained the pri-
mitive condition of the protovertebrae 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 (PI. 3, fig. 8 a, v p), but which had be-
come cut by transverse lines (not, indeed, extending to the
outer limit of the sheet, but as yet not cut off by longitudi-
nal lines of cleavage) into segments, which I called proto-
vertebrae.
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 (PI. 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 protovertebrae 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 protovertebrae, because at this time no separa-
tion 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 protovertebrae. From this it is clear that
the pleuro-peritoneal cavity extends primitively quite up to the
top of the protovertebrae ; 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 mus-
cular system of. the digestive tract.
The pleuro-peritoneal cavity is first distinctly formed at a
DEVELOPMENT OF THK ELASMOBRANCH FISHES. 89
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 protovertebrae (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 be-
comes deeply stained by reagents (PI. 4, fig. \\,mp'}. Coin-
cidently 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, n,
12, 13, by the letters mp'. Its early appearance is most pro-
bably 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 protovertebrae, and closely
applied to the upper and outer corners of the involuted epiblast
of the neural canal (PI. 4, fig. ntspn}. 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, suf-
ficient evidence at present to enable me to say with any cer-
tainty 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.
90 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
In any case, it is clear that the condition in the Bird, where
the spinal nerves are derived from tissue of the protovertebrae,
is not the primitive one. Of this, however, I will speak again
when I have concluded my account, of the development of the
protovertebrae.
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 (M tiller's duct) is formed
(PL 4, fig. 11,0V).
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. u, nip), split up by transverse partitions into
protovertebrae, 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 cor-
responds with the intermediate cell-mass of Birds (vide Waldeyer,
Eierstock tmd Ei).
At the same time, in the upper of these two sheets (the pro-
tovertebrae), the splanchnic layer sends a growth of cells in-
wards 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 ad-
joining this.
This mass of cells is at first quite continuous with the
splanchnic layer of the protovertebrae, 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. II and \2a; and
from these it will also be clear, especially from fig. 1 1 a, that
DEVKLOPMKXT OF THE ELASMOBRANCH FISHES. QI
the outermost layer of this mass of cells, which was the primi-
tive splanchnic layer of the protovertebrae, 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 splanch-
nic 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 protovertebrae are formed, the two together form an inde-
pendent mass (fig. 12, in p\ 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,
in /') which I spoke of before.
The section represented in fig. 12 is from a very considerably
later embryo than that represented in fig. II, so that the skele-
ton-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 noto-
chord and neural canal forms the cartilaginous centra and arches
of the vertebrse, 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) com-
posed 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 (?«/').
Each of these plates now grows both upwards and down-
wards ; 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
92 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
downwards, the cells of which they are composed commence to
become elongated and soon acquire an unmistakably muscular
character (PI. 4, fig. 13, ;///).
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, ;«/).
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 in-
vestigated) are derived from the muscle-plates which grow up-
wards 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 develop-
mental changes.
They become more elongated and fibrous, their main attach-
ment 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 protovertebrae are —
(i) That at the time when the mesoblast becomes split
horizontally into somatopleure and splanchnopleure the verte-
bral 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.
DEVELOPMENT OK THE EEASMOBRANTH FISHES. 93
(2) That the following parts are respectively formed by the
vertebral and lateral plates :
(#) 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 nnd 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.
(<:) 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
protovertebrae, so that the protovertebrae of the Elasmobranchii
do not appear to be of such a complicated structure as the proto-
vertebrae of Birds.
TJie Digestive Canal.
I do not intend to enter into the whole history of the di-
gestive 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 be-
tween 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 di-
gestive canal.
94 DEVELOPMENT OF THK ELASMOBKANCH FISHES.
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
larsrer bore than the remainder of the canal. Its diameter be-
o
comes, 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 tfme its
calibre continually becomes smaller as compared with the re-
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 :
DEVELOPMENT OF THE EEASMOHRAXCII EISHI.S. 95
(1) The terminal vesicle.
(2) The disappearance of a large and well-developed por-
tion 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 (Arclriv. fiir Micro. Ana/. Vol. II. pi. 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 com-
mencing 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 under-
stand 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 secon-
dary significance. It corresponds with the point of closing of
96 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
the primitive involution. If it was not for this peculiarity of the
vertebrate anus we would naturally suppose, from the disap-
pearance 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 Gotte (" Untersuchung iiber die
Entwickelung der Bombinator igneus," ArcJiiv. fur 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 noto-
chord, and in contact with it (vide PL 3, fig. 10; 4, 11 and I2,;r),
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 ofif from the
alimentary canal a small rod-like body close under the noto-
chord 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
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 97
It was first seen by Gotte (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 de-_
velopment of this body with sufficient care to be in a position
to judge of the correctness of Gotte'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 de-
velopment 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, s u, 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 supra-
renal organ, which in the Dog-fish forms a yellowish elongated
body lying between the two kidneys.
The development of tlic Wolffian Duct and Body and of t/ie
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.
B. 7
98 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
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 embryo-
logy has hitherto supplied, and at the same time renders easier
the task of understanding the differences in the modes of de-
velopment 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 (PI. 4, fig. 1 1 b, o v\ and from
this knob a solid rod of cells grows backwards towards the
tail (fig. nc, o i>) very closely applied to the epiblast. This
description will be rendered clear by referring to figs, lib and c.
Fig. 1 1 b is a section at the level of the knob, and fig. 1 1 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 Mutter 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-
DEVELOPMENT OF THE KI.ASMO15RANCH FISIIKS. 99
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, o v). 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 for-
mation, 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 invo-
lution, 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.
7—2
100 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
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 for-
mation), at numerous points with the pleuro-peritoneal cavity.
It is very probable that there is one involution to each seg-
ment of the body between the front and hind ends of the
Oviduct. This duct is the Wolffian duct, which thus, toge-
ther 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 diverti-
cula, 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.
DEVELOPMENT OF THE ELASMOBRANCH FISHES. IOI
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. i^^piud.
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 appendages1. 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.
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 develop-
ment 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 preli-
minary point.
From their development the Oviduct and Wolffian body
appear to stand to each other in the relation of the Wolffian
1 Fur the specimens of this age I am indebted to Profes-ior Huxley.
IO2 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
duct being the equivalent to a series, so to speak, of Ovi-
ducts.
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 t 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 epiblast1, instead of as an
involution.
If the above explanation about the Oviduct be correct, then
it is clear that similar causes have produced a similar modifica-
tion in development (only with a different organ) in Birds ; while,
at the same time, the primitive mode of origin of the Oviduct
(Miiller's duct) has been retained by them.
The Oviduct, then, may be considered as arising by an invo-
lution 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.
1 If Roiniti's observations (Archives fiir J///v. Anatoin. 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 protovertebne will have to be abandoned.
DEVELOPMENT OF THE ELASMOBRANCH FISH1 -. 103
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 coa-
lescence 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. Gegen-
baur looks upon the whole urino-genital system as homolo-
gous 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 urino-genital system is homologous. The
first of these have become modified so as to form the Ovi-
ducts, 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 invo-
lution, or, what is equivalent to it, the other involutions having
disappeared. This even appears to be the case in the Mar-
sipobranchii. In the adult Lamprey the Wolffian duct ter-
minates 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 open-
ings1. The Oviduct, when present, arises in other vertebrates
1 While correcting the proofs of this paper I have come across a memoir of W.
Miiller (" Ueber die Persistenz der Urniere bei Myxine Glutinosa," Jcnaische Zeit-
schrift, Vol. vn. 1873), in which he mentions that in Myxine the upper end of the
104 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
as a single involution, strongly supporting the view that its
mode of formation in the Dog-fish is fundamentally merely an
involution.
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 develop-
ment 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 on two words
about the development of the Ovary. In both sexes the ger-
minal 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 epithe-
lium on the knob grows more and more conspicuous, and de-
velops 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 con-
taining 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 be-
come the Ovaries.
Wolffian duct communicates by numerous openings with the pleuro-peritoneal cavity ;
this gives to the suggestion in the text a foundation of fact.
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 105
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 cor-
respondingly 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 Plenro-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 (PI. 3, fig. 8 a, pp'} ; this be-
comes 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 appear-
ance 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 neces-
sarily 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, //. 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.
106 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
TJie 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 Gotte (Archiv. filr 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 embry-
onic 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, g I), the nerves to the other arches become the bran-
chial branches of the vagus nerve (fig. 14, v g). 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, Vll). Its mode of distribution to
DEVELOPMENT OF THE ELASMOBRANCH FISHES. IO/
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 to-
wards 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 inter-
pretation 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 mor-
phology 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.
IO8 DEVELOPMENT OF THE ELASMOBRANCH FISHES.
LIST OF WORKS REFERRED TO.
Gegenbaur. Anat. der Wirbelthiere, III Heft, Leipzig, 1873.
A. Gotte. Archiv. fur Micr. Anat., Vol. x. 1873. "Der Keim der Forelleneies,"
Archiv.filr. Micr. Anat., Vol. IX. 1873. " Untersuchung liber die Entwickelung
der Bombinator igneus," Archiv. filr Micr. Anat., Vol. V. 1869. " Kurze Mit-
theilungen aus der Entwickelungsgeschichte der Unke," Archiv. fur Micr. Anat.,
Vol. IX. 1873.
Kupffer. Archiv. fur Micr. Anat., Vol. n. 1866, p. 473. Ibid. Vol. IV. 1868,
p. 209.
Kowalevsky. " Entwickelungsgeschichte der Holothurien," Memoirs de fAcad.
Imper. des Sciences de St Petersboiirg, vii ser. Vol. xi. 1867.
Kowalevsky, Owsjannikow, uncl Wagner. "Entwickelung der Store," Bulletin der
K. Acad. St Petersbourg, Vol. XIV. 1873.
Kowalevsky. " Embryologische Studien an Wurmern und Arthropoden," Memoirs
de rAcad. Imper. des Sciences de St Petersbourg, Vol. xvi. 1871.
E. Ray Lankester. Annals and Mag. of Nat. History, Vol. xi. 1873, P- 81.
W. Mliller. " Ueber die Persistenz der Urniere bei Myxine Glutinosa," Jenaische
Zeitschrift, Vol. vii. 1873.
Oellacher. Zeitschrift fur IViss. Zoologie, Vol. XXIII. 1873.
Owsjannikow. "Entwickelung der Coregonus," Eul. der K. Akad. St Petersbourg,
Vol. xix.
Romiti. Archiv. filr Micr. Anat., Vol. IX. 1873,
Waldeyer. EierstocR u. Eie.
EXPLANATION OF PLATES 3 AND 4.
COMPLETE LIST OF REFERENCE LETTERS.
a I. Alimentary canal, a o. Dorsal aorta, an v. Auditory vesicle, b d. Forma-
tive cell probably derived from the yolk, ca v. Cardinal vein, c h. Notochord.
c H . Thickening of hypoblast to form the notochord. e b. Line indicating the edge
of the blastoderm, e p. Epiblast. e p' . Epidermis, e r. Embryonic rim. e s. Em-
bryonic swelling, g I. Glosso-pharyngeal nerve, h. Head. ///. Heart, h y. Hypo-
blast. //. Lower layer cells. I y. Line of separation between the blastoderm and
the yolk. m. Mesoblast. m c. Medullary canal, m g. Medullary groove, m p.
Muscle-plate, m p'. Early formed mass of muscles, n. Peculiar nuclei formed in
the yolk. «'. Similar nuclei in the cells of the blastoderm, n a. Cells which help
to close in the alimentary canal, and which are derived from the yolk, n y. Network
of lines present in the food-yolk, o I. Olfactory pit. op. Eye. ov. Oviduct, p n.
Pineal gland, p ov. Projection which becomes the ovary. //. Pleuro-peritoneal
cavity. //'• Remains of pleuro-peritoneal cavity in the head, pr v. Protovertebrse.
p wd. Primary points of involution from the pleuro-peritoneal cavity by the coalesc-
ence of which the Wolffian duct is formed, s g. Segmentation cavity, j o. Somato-
pleure. so s. Stalk connecting embryo with yolk-sac, s p. Splanchnopleure. sp n.
DEVELOPMENT OF THE ELASMOBRANCH FISHES. 109
Spinal nerve, su r. Supra-renal body, t s. Caudal lobes, v. Blood-vessel, v g.
Vagus nerve, v. Fifth nerve, vn. Seventh nerve, v c , 1,2, 3, £c. ist, 2nd and
3rd &c. visceral clefts, v p. Vertebral plates, iv d. Wolffian duct. x. Peculiar body
underlying the notochord derived from the hypoblast. y k. Yolk spherules.
All the figures were drawn with the Camera Lucida.
Plate 3.
Fig. i. Section parallel with the long axis of the embryo through a blastoderm,
in which the floor of the segmentation cavity (s g) 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 («) in the yolk under the blasto-
derm. 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 pro-
bably 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 («) and the network in the yolk
between them ; this network is seen to be closer around the nuclei than in the inter-
vening 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 (i) the characters of the epiblast, (2) the embryonic swelling (e s),
(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 appear-
ance of the embryonic rim, and before the formation of the medullary groove.
(Magnified 45 diam.)
It illustrates (i) 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 me-
dullary 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 (i) 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 (n a) derived from the yolk.
b. Section in the region of the head where the medullary groove is deficient,
other points as above.
IIO DEVELOPMENT OF THE ELASMOBRANCH FISHES.
Fig. 7 a and K. 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 (chr).
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 (i) the
flattened head (k) 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 (i) the absence of the medullary groove in the head
and the medullary folds turning dovvn at this time instead of upwards; (2) the pre-
sence of the pleuro-peritoneal cavity in the head (//); (3) the completely closed
alimentary canal (a /).
Fig. 8 b. Transverse section of fig. 8, through the line b. (Magnified 90 diam.)
It shews (i) 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 t s.
The front end of the notochord became indistinct, and I could not see its exact
termination. The epithelium of the alimentary canal (a 1} is seen closely underlying
the notochord and becoming continuous with the epiblast at the hind end of the
notochord.
The first visceral cleft (i v c] 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 (i) the formation by a pinching off from the top of the alimentary canal of
a peculiar body which underlies the notochord (x)\ (i) the primitive extension of the
pleuro-peritoneal cavity up to the top of the vertebral plates.
Plate 4.
Fig. 1 1 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. (Mag-
nified 96 diam.) In all of these the muscle-plates are shewn at in p. 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 (m p').
The figures further shew (i) the formation of the spinal nerves (sp n) 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 /' and c are given
more especially to shew the mode of formation of the oviduct (ov).
DEVELOPMENT OF THE ELASMOBRANCH FISHES. I I I
In b it is seen as a solid knob (ov), arising from the point where the somatopleure
and splachnopleure unite, and in c (the section behind l>) as a solid rod (ov) closely ap-
plied 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. 120 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 (p w d), while b is a section
from the space between two involutions from the pleuro-peritoneal cavity, so that the
Wolffian duct (at first solid) (w d) 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 (a I).
(2) The supra- renal body (si/ >•).
(3) The oviduct (ov), which has acquired a lumen.
(4) The increase in length of the muscle-plates, the spinal nerve1:, &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 (w d).
(2) One of the still continuing connections (primitive involutions) between
the Wolffian duct and the pleuro-peritoneal cavity (/ w d).
(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.
(?) The formation of an outgrowth on each side of the mesentery (/ ov), which
will become the ovary.
(6) The spiral valve (a /).
Fig. 14. Transparent view of the head of an embryo shortly before the appear-
ance 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 (g /) and vagus (v g) are united.
(2) The remnants of the pleuro-peritoneal cavity in the head (p p).
(3) The eye (of). 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 DE-
VELOPMENT OF VERTEBRATES1.
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
a 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 be-
come 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 ex-
ception. In Elasmobranchs, 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 an-
cestral and which secondary. For this purpose it is requisite
1 From the Quarterly Journal of Microscopical Science, Vol. xv. 1875.
EARLY STAGES IN DEVELOPMENT OF VERTEBRATES. 113
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 verte-
brates, 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 BischofFs 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 Elasmobranchs.
With reference to Reptiles we have no satisfactory investi-
gations.
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 an-
cestor 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 segmenta-
tion 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.
u. 8
114 KARLY STAGES IN THE
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 vesicle1.
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 in, is that of the com-
mencing 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 de-
velopment, 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 (Entwickelungeschichte 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.
1 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.
DEVELOPMENT OF VERTEBRATES. 115
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 em-
ployed, 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-spheruies 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
8—2
Il6 EARLY STAGES IN THE
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 dia-
grammatic 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 l).
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 com-
menced ; this involution is (i) 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 por-
tion ; 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 ill, the involution has become nearly completed and the
opening to the exterior or blastopore quite constricted.
The segmentation cavity has been entirely obliterated, as
DEVELOPMENT OF VERTEBRATES.
would have been found to be the case with Amphioxus had the
stage a little older than that on Plate 5, A ill, been represented.
The cavity marked (#/), as was the case with Amphioxus, is that
of the alimentary canal.
The similarities between the mode of formation of the hypo-
blast 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 epi-
thelium. 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 re-
mainder 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 epi-
blast 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 n, 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
Il8 EARLY STAGES IN THE
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 develop-
ment 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 de-
velopment.
In the next stage (c li) we find that the involution to form
the alimentary canal has commenced (#/), 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 l) 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 hypo-
blast, 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 com-
DEVELOPMENT OF VERTEBRATES. I 19
pleted, 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 epiblasl 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 l). 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 rela-
tion 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 ali-
mentary 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 epi-
thelium 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, cm, 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 nar-
rowed, it does not become the anus of the adult. It may be
noticed that at the front end of the embryo the primitive dorsal
120 EARLY STAGES IN THE
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.
DEVELOPMENT OF VERTEBRATES. 121
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 seg-
mentation 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 invo-
lution, are to be found in (i) 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 cer-
tainly 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 : — (i) 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 con-
spicuous 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 ali-
mentary canal by a split and not by an involution is exactly
what Bambeke finds in Pelobates.
The next stage, D ill, 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
122 EARLY STAGES IN THE
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 com-
pletely vanished, and the epiblast with its accompanying meso-
blast 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 funda-
mental agreement between the two, and between this mode of
development and that of the Selachians we shall find the agree-
ment 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 seg-
ments of the previous eggs is proved (i) by its containing a
number of nuclei (E I, ;/), 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 invo-
lution 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 blasto-
derm take a share except that part where the epiblast and hypo-
blast 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
DEVELOPMENT OF VERTEBRATES. 123
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 ill, is in many ways identical with Jthe
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 Sela-
chians and Batrachians. The neural canal (n c] is by the stage
figured E ill, 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 con-
tinuous at the point x), the two canals, viz. the neural and ali-
mentary, 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 blasto-
derm rests like a disc on the yolk and grows over it on all sides,
except at the point where the epiblast and hypoblast are con-
tinuous (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
124 EARLY STAGES IN THE
tail of the embryo) as well as everywhere else. It thus comes
about that the final point where the various parts of the blasto-
derm meet and completely enclose the yolk mass does not cor-
respond 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 («) 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 conse-
quence 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 be-
comes very narrow and forms the duct of the so-called umbilical
cord which places the yolk-sac in communication with the ali-
mentary 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 verte-
brates, 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, " De-
velopment of Selachians1," Journal of Microscopical Science, Oct.,
1874).
1 Paper No. V, p. 82 el set/, in this edition.
DEVELOPMENT OF VERTEBRATES. 12$
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 l) is very similar in -many
respects to the corresponding stage in the Selachian. The seg-
mentation 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 Gotte'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 Sela-
chian'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 blasto-
derm. A necessary consequence of this is, that the epiblast does
not, as in the previous cases, become continuous with the hypo-
blast 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 blasto-
pore 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.
126 EARLY STAGES IN THE
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 be-
coming 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 ob-
servers, but has been disputed by several, and recently by
Kolliker. 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 continua-
tions of what took place in the last stage.
DEVELOPMENT OF VERTEBRATES. 12;
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 ihe
Selachian, it is not very difficult to do so directly from Amphi-
oxus. 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 develope on the type
we now find.
The careful investigation of the development of some Rep-
tiles 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
128 EARLY STAGES 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 seg-
mentation 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 ma-
terial ; 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 pro-
bable that the eggs of Osseous fish are fundamentally simplified
Selachian eggs ; in which case we already know that the dimi-
nution of food material has affected but very slightly the funda-
mental 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 meso-
blast 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 invo-
lution 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
DEVELOPMENT OF VERTEBRATES.
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 investi-
gations of Kowalevsky seem to shew that in Lumbricus the
mesoblast is derived from the hypoblast.
Amongst Crustaceans, Bobretsky's1 observations on Oniscus
(Zeitsclirift fur wiss. Zoologie, 1874) lead to the same con-
clusion.
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 Poduridae, 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
vertebrates2, the derivation of mesoblast from hypoblast is with-
out doubt.
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 differentia-
tion, 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 ?
1 He says, p. 182 : " Bevor aber die Halfte der Eioberflache von den Embryonal-
zellen bedeckt 1st, kommt die erste gemeinsame Anlage des mittleren imd unteren
Keimblattes zum Vorschein."
- Anton Dohrn, Der Ursprung des Wirbclthieres. Leipzig, 1875.
I!. 9
130 EARLY STAGES IN THE
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. y. 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 di-
gestive tract.
I put this forward merely as a suggestion, in the truth of
which I feel no confidence, but which may perhaps induce em-
bryologists 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 be-
come 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 mus-
cular 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 mus-
cular 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 (i) subse-
DEVELOPMENT OF VERTEBRATES. 131
quently 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 tcL their
being better nourished as they would necessarily be, and to
their possibly easier adaptability to some new form of move-
ment of the animal, the muscle-cells of the alimentary canal
might become developed exclusively whilst the original mus-
cular system atrophied.
I only hold this view provisionally till some better explana-
tion 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 Elasmo-
branch Fishes1,' Quart. Journ. of Micro. Science for Oct., 1874.
Plate XV, fig. n a, 1 1 b, 12 a, ;///.) 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.
It is very possible that the formation of the mesoblast as two
masses, one on each side of the middle line as occurs in Sela-
chians, 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 ali-
mentary canal. This would also explain the fact that in Sela-
chians the body cavity consists at first of two separate portions,
one on each side of the alimentary canal, which only subse-
1 I'apui XD. V, p. 60 ft -vty. of tliis edition, pi. 4. lijjs. 1 1 <i, 1 1 A, 1 1 a, ////>.
C — 2
132 EARLY STAGES IN THE
quently become united below and converted into a single cavity
(vide loc. cit.\ Plate XIV, fig. 8 b, //).
In the Echinoderms we find instances where the body cavity
and water-vascular system arise as an outgrowth from the ali-
mentary 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 blasto-
pore 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 never-
theless 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 king-
dom it sometimes forms the mouth and sometimes the anus :
thus for instance in Lumbricus it is the mouth (according to
Kowalevsky), in Palaemon (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
1 PI. 3 of this edition, fig. 8 /-. />/>.
DEVELOPMENT OF VEKTKHKATES. 133
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 blasto-
pore 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.
134 EARLY STAGES IN DEVELOPMENT OF VERTEBRATES.
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. / /. Lower layer cells. ;//.
Mesoblast. «. Nuclei of yolk of Selachian egg. n c. Neural canal, s g. Segmenta-
tion 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 ill. Diagrammatic sections of Amphioxus in its early stages (founded
upon Kowalevsky's observations).
B I, B n, 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 Gotte's observations). In c in the neural canal is com-
pleted, which was not the case in B in. The epiblast in c ill has been diagram-
matically represented as a single layer.
D I, D II, D in. 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 11, F in. Diagrammatic longitudinal sections of a Bird in its early stages.
VII. ON THE ORIGIN AND HISTORY OF THE URINOGENITAL
ORGANS OF VERTEBRATES1.
RECENT discoveries2 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.
1 From the Journal of Anatomy and Physiology, Vol. X. 1875.
2 The more important of these are: —
Semper — Ueber die Stammverwandtschaft der Wirbelthiere u. Anneliden. Cen-
tralblatt f. Med. Wiss. 1874, No. 35.
Semper— Segmentalorgane bei ausgewachsenen Haien. Centralblatt f. Med.
Wiss. 1874, No. 52.
Semper — Das Urogenitalsystem der hoheren Wirbelthiere. Centralblatt /". Med.
Wiss. 1874, No. 59.
Semper — Stammesverwandschaft d. Wirbelthiere u. \Virbellosen. Arbeiten ans
Zool. Zootom. Inst. Wiirzburg. II Band.
Semper — Bildung u. Wachstum der Keimdriisen bei den Plagiostomen. Central-
blatt f. Med. Wiss. 1875, No. 12.
Semper — Entw. d. Wolf. u. Miill. 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. Natnr-
for. 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. Miiller — Persistenz der Urniere bei Myxine glutinosa. Jenaische Zeitschrijt,
1873-
W. Miiller Urogenitalsystem d. Amphioxus u. d. Cyclostomen. Jatmscke Zeit-
schrift, 1875.
Alex. Gotte Entwickelnngsgeschichtf d.-r l'nk<- (Rinnbinator igncns}.
136 THE URINOGENITAL ORGANS OF VERTEBRATES.
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 observa-
tions alone, but have had recourse to all the Memoirs with which
I am acquainted, and to which I have access. I have com-
menced 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 original1 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.
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 protovertebrae. 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. i, pd.}.
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 be-
coming hollow acquires a wide opening into the pleuroperitoneal
or body cavity, and the column a lumen ; so that by the time
that five visceral clefts have appeared, the two together form a
1 These organs were discovered independently by Professor Semper and myself.
Professor Semper's preliminary account appeared prior to my own which was pub-
lished (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.
THE URINOGENITAL ORGANS OF VERTEBRATES.
137
spa
FlG. I. TWO SECTIONS OF A PRISTIURUS EMBRYO WITH THREE VISCERAL
CLEFTS.
The sections are to shew the development of the segmental duct (pd) or primi-
tive 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 ; me. medullary canal ; ch. notochord ; X.
string of cells below the notochord ; mp. muscle-plate ; nip', specially developed
portion of muscle-plate ; ao. dorsal aorta ; pd. segmental duct. so. somatopleura ;
sp. splanchnopleura ; //. pleuroperitoneal or body cavity ; ep. epiblast ; al. ali-
mentary canal.
duct closed behind, but communicating in front by a wide
opening with the pleuroperitoneal cavity.
Before these changes are accomplished, a series of solid?
outgrowths of elements of the 'intermediate cell- mass' appear
at the uppermost corner of the body-cavity. These soon be-
come hollow and appear as involutions from the body-cavity,
curling round the inner and dorsal side of the previously formed
duct.
One involution of this kind makes its appearance for each
protovertebra, and the first belongs to the protovertebra im-
mediately behind the anterior end of the duct whose develop-
ment 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.
1 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.
138 THE URINOGENTTAL ORGANS OF VERTEBRATES.
The duct is the primitive duct of the kidney1; I shall call it
in future the segmental duct ; and the involutions are the com-
mencements of the segmental tubes which constitute the body
of the kidney. I shall call them in future segmental tubes
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 seg-
mental 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.
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 seg-
mental duct into the Wolffian duct above and the Miillerian duct below ; st. seg-
mental 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 (p) into the body-cavity, and behind into the cloaca, and
there are a series of convoluted segmental tubes (sf), 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 Miiller's duct,
or the oviduct, and the duct of the Wolffian bodies or Leydig's
duct. The splitting2 is effected by the growth of a wall of cells
, * This duct is often called either Miiller's duct, the oviduct, or the duct of the
primitive kidneys ' Urnierengang.' None of these terms are very suitable. A justifi-
cation 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.
• 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
THE UKINOCKXITAI. ORGANS ()K VERTEBRATES. 139
which divides the duct into two parts (fig. 3, ^Lvd. 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, .r).
The dorsal portion also forms an independent duct, and into
it the segmental tubes continue to open. Such at least is the
tn-p
FIG. 3. TRANSVERSE SECTION OF A SELACHIAN EMBRYO ILLUSTRATING THE
FORMATION OF THE WOLFFIAN AND MiJLLERIAN DUCTS BY THE LONGI-
TUDINAL SPLITTING OF THE SEGMENTAL DUCT.
me. medullary canal ; mp. muscle-plate; c/i. notochord; ao. aorta; cav. car-
dinal 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. Miillerian duct. The Miil-
lerian duct and the Wolffian duct together constitute the primitive segmental duct ;
jfr. The germinal ridge with the thickened germinal epithelium : /. liver ; /. intes-
tine with spiral valve.
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.
140 THE URTNOGENITAL ORGANS OF VERTEBRATES.
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
Miillerian duct, or oviduct, and in the male portions only of
such a duct.
The next change which takes place is the formation of an-
other 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 fur Med. Wiss. 1874, No. 59), but they are of no
fundamental importance.
These constitute the main changes undergone by the seg-
mental 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 Meyer1 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 open-
ings of the segmental tubes in the adult merely lead into lymph
organs and not into the gland of the kidneys.
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 fluid2. The spermatozoa have therefore to
1 Sitzen. der Naturfor. Gesellschaft, Leipzig, 30 April, 1875.
2 We owe to Professor Semper the discovery of the arrangement of the seminal
ducts. Centralblatt f. Med. Wiss. 1875, No. \i.
THE URINOGENITAL ORGANS OF VERTEBRATES. 141
pass through a glandular portion of the kidneys before they
enter the Wolffian duct, by which they are finally carried away
to the exterior.
In the adult female, then, there are the following parts of
the urinogenital system (fig. 4) :
(i) The oviduct, or M tiller'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 ovi-
ducts serve simply to carry to the exterior the ova, and have no
communication with the glandular portion of the kidneys.
s.f
FIG. 4. DIAGRAM OF THE ARRANGEMENT OF THE URINOGENITAL ORGANS IN
AN ADULT FEMALE SELACHIAN.
Hid. Mullerian 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 kidneys1, that is to say, of all the anterior segmental tubes.
(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
1 This upper portion of the kidneys is called Leydig's gland by Semper. It would
be letter to call it the Wolftian body, for I shall attempt to shew that it is homologous
with the gland so named in Saumpsida and Mammalia.
142
THE URINOGENITAL ORGANS OF VERTEBRATES.
into two parts, according to the duct by which their secretion is
carried off.
In the male the following parts are present :
(1) The Miillerian 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 corre-
sponds to the Wolffian duct of the female, except that, in ad-
dition 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).
FIG. 5. DIAGRAM OF THE ARRANGEMENT OF THE URINOGENITAL ORGANS IN
AN ADULT MALE SELACHIAN.
md. rudiment of Miillerian duct ; ivd. 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 kid-
neys, which has the same relations as in the female.
(4) The segmental tubes (fig. 5. .$•/.) . 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 seg-
mental tubes developc primitively as completely independent
THE URINOGENITAL ORGANS OF VERTEBRATES. 143
organs1, 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 verte-
brates possessed a series of independent and segmental ex-
cretory organs.
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 inde-
pendent 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.
1 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 demon-
strable manner.
144 THE URINOGENITAL ORGANS OF VERTEBRATES.
In favour of this view are the following anatomical and em-
bryological facts, (i) It developes 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, Cyclos-
tomes 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 seg-
mental 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, Func-
tionsweclisel, 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 sup-
pose 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 a posteriori proof of its
being a metamorphosed segmental tube. The development in
insects of a longitudinal tracheal duct by the coalescence of a
THE URTNOGEXITAL ORGANS OF VERTEBRATES. 145
series of transverse tracheal tubes affords a parallel to the forma-
tion 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 open-
ing 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
Gunther, Trans, of Royal Society, 1871), and the majority of
Ganoids (Hyrtl, Dcnkschriften Wien, Vol. VIII.). In the majo-
rity 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
B. 10
146 THE URINOGENITAL ORGANS OF VERTEBRATES.
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 per-
manent 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 con-
veniently 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. M tiller Myxinoid fislies,
and Wilhelm Miiller, Jenaische Zeitschrift, 1875, Das Urogenital-
system des Amphioxus u. d. Cyclostomcn} there is a pair of ducts
which communicate posteriorly by a common opening with
the abdominal pore. From these ducts spring a series of trans-
verse 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. Muller (loc. cit.} has given a short but interesting account
of the development of the urinary system of Petromyzon. He
THE URINOGENITAL ORGANS OF VERTEBRATES. 147
finds that the segmental ducts develop first of all as simple
involutions from the body-cavity. The anterior end of each
then developes 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. Muller 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 seg-
mental 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 Muller, 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 Muller (JenaiscJie
Zeitschrift, 1873). The large development of this glandular
mass in the Cyclostome and Osseous fishes and in embryo Am-
phibians, 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 seg-
mental organ.
The remainder of the kidney in Cyclostomes is equivalent to
the kidney of Selachians. Its development from segmental in-
volutions has not been recognized. If these segmental involu-
tions 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 con-
dition.
IO — 2
148 THE URINOGENITAL ORGANS OF VERTEBRATES.
In Osseous fishes the segmental duct of the kidneys developes,
as the observations of Rosenberg1 (" Teleostierniere," Liang.
Disser. Dorpat, 1867) and Oellacher (Zeitschrift fur 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.
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 inde-
pendent 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
1 I am unfortunately only acquainted with Dr Rosenberg's paper from an ab-
stract.
THE URINOGENITAL ORGANS OF VERTEBRATES. 149
common opening. For further details vide Hyrtl, Denk. der k.
Akad. Wicn, 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 (Mullerian 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 (Mullerian 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 Mullerian 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
Mullerian duct was normal.
In the Sturgeon (vide J. Miiller, Ban u. Grenzen d. Ganoiden,
Berlin Akad. 1844; Leydig, Fisclicn u. kept Hie n, and Hyrtl,
Ganoiden} the same parts are found as in Spatularia.
150 THE URINOGENITAL ORGANS OF VERTEBRATES.
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 Miillerian 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 Mu'ller makes the same statement
for both sexes. It was open on both sides in a female specimen
I examined1, and Hyrtl found it invariably so in both sexes in
all the specimens he examined.
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 ob-
servers 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 Mullerian duct
is in favour of the view that these ducts of Rathke are really
present.
In Polypterus (vide Hyrtl, Ganoideii) there is, as in other
Ganoids, a pair of Mullerian 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 Mullerian ducts and ureters, has an opening to the exterior
immediately behind the anus.
In Amia (vide Hyrtl) there is a pair of Mullerian ducts
which, as well as the ureters, open into a dilated vesicle. This
vesicle appears as a continuation of the Mullerian ducts, but
receives a number of the efferent ductules of the kidneys. There
is a single genito-urinary pore behind the anus.
In Ceratodus (Giinther, 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
1 For this specimen I am indebted to Ur Giinther.
THE URINOGENITAL ORGANS OF VERTEBRATES. 151
the length of the abdominal cavity. In both male and female
there is a long Mullerian 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 Mullerian duct
has a wide opening near the anterior extremity of the body-
cavity. The ureters coalesce and open together into the urino-
genital cloaca dorsal to the Mullerian ducts. It is not abso-
lutely certain that the semen is transported to the exterior
by the Mullerian duct of the male, which is perhaps merely a
rudiment as in Amphibia. Dr Giinther failed however to find
any other means by which it could be carried away.
The genital ducts of Lepidosteus differ in important par-
ticulars from those of the other Ganoids (vide M tiller, loc. cit.
and Hyrtl, loc. cit.}.
In both sexes the genital ducts are continuous with the in-
vestments 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 asym-
metry 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 convolu-
tions. 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 Mullerian duct in the male is function-
less, 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. Gunther's (loc. cit.} injection ex-
periments on Ccratodus militate against this view, but I do
not think they can be considered as conclusive as long as the
152 THE URINOGENITAL ORGANS OF VERTEBRATES.
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 Miillerian 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 re-
present 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 satisfac-
tory 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 tubes1, and which also receives the ducts of the
kidneys.
Gegenbaur suggests that these are to be looked upon as
Mullerian 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 pores2. In the Greenland Shark (L&margus Borcalis]
1 According to M tiller (Myxinoidcn, 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.
- My own rough examination of preserved specimens was hardly sufficient to
THE URINOGENITAL ORGANS OF VERTEBRATES. 153
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 Scyl-
lium, or, as is commonly stated, open into the body-cavity,
there can be no question that they are homologous with true
abdominal powers.
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 Cyclo-
stomes, and also occur in addition to true Miillerian ducts, speak
strongly against the view that the abdominal pores have any
relation to Mullerian 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 Mullerian ducts.
We next come to the question which I reserved while speak-
ing 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 gen-
erative 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 organs1 and
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.
1 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 Jluvialis). The walls of the duct are in the Perch con-
tinuous 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
154 TI*E URINOGENITAL ORGANS OF VERTEBRATES.
have generally, though not always, an opening or openings inde-
pendent 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.
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 Pappehheim (loc. cit.) have already insisted, as a
case of degeneration than of a primitive condition. The pre-
sence of genital ducts in the near allies of the Salmonidae, and
even in the male salmon, are conclusive proofs of this. If we
admit that the presence of an abdominal pore in Salmonidae 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 dcr k. Akad. Wien, Vol I.) 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 Se-
lachians. It must be admitted, with Gegenbaur, that embry-
ology 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 genera-
tive bodies, unite with the ureters, and in this differ from the
generative ducts of Osseous fishes. The relation, indeed, of the
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.
THE URIXOGEXITAL ORGANS OF VERTEBRATES. 155
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 anus1, makes it most proba-
ble that its generative ducts are true Mullerian ducts.
In the Amphibians the urinary system is again more primi-
tive than in the Selachians. .
The segmental duct of the kidneys is formed2 by an elon-
gated fold arising from the outer wall of the body-cavity, in
the same position as in Selachians. This fold becomes con-
stricted 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 portion3 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.
After the formation of the gland just described the remainder
of the kidney is formed.
1 This is mentioned by Muller (Ganoid fishes, Berlin Akad. 1844), Hyrtl (loc. fit.),
and Giinther (loc. cit.), and through the courtesy of Dr Giinther I have had an oppor-
tunity of confirming the fact of the presence of the abdominal pores on two specimens
of Lepidosteus in the British Museum.
2 My account of the development of these parts in Amphibians is derived for the
most part from Gotte, Die Entwickdungsgeschichte dcr Unkc.
3 It is called Kopfniere (head-kidney), or Urniere (primitive kidney), by German
authors. Leydig correctly looks upon it as together with the permanent kidney con-
stituting the Urniere of Amphibians. The term Urniere is one which lias arisen in
my opinion from a misconception ; but certainly the Kopfniere has no greater right t<>
the appellation thau the remainder of the kidney.
156 THE URINOGENITAL ORGANS OF VERTEBRATES.
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 primi-
tive 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
Gotte. Their openings are ciliated, and, as Spengel (loc, cit.) and
Meyer (loc. «'/.) 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 Mul-
lerian 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 en-
trance 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 Mullerian duct near its posterior ex-
THE URINOGENITAL ORGANS OF VERTEBRATES. 157
tremity. This process is not always carried out with equal
completeness. In the tailless Amphibians, however, the process
is generally1 completed, and the ureters (Wolffian ducts) are of
considerable length. . Bufo cinereus, in the male of which the
Mullerian ducts are very conspicuous, serves as an excellent
example of this.
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 Amphi-
bians. 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 Mulle-
rian duct and a ureter is quite complete. The Newt (Triton)
also serves as an excellent example of the formation of distinct
Mullerian 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 Mullerian duct near its termination, but in the male
the anterior segrnental tubes, including those which, as will be
afterwards seen, serve as vasa efferentia of the testis, enter the
Mullerian duct directly, while the posterior unite as in the
female into a common duct before joining the Mullerian duct.
For further details as to the variations exhibited in the Amphi-
bians, the reader is referred to Leydig, Anat. Untersuclinng,
Fischen u. Reptilien. Ditto, Lehrbuch der Histologie, Menschen
u. TJtiere. Von Wittich, Siebold n. Kolliker, Zeitschriff, 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 Mullerian and Wolffian
1 In Bombinator igneus, Von Wittich stated that the embryonic condition was
retained. Leydig, Anatom. d. Amphib. u. Kcptilien, shewed that this is not the case,
but that in the male the Mullerian duct is very small, though distinct.
158 THE URINOGENITAL ORGANS OF VERTEBRATES.
duct is probably to be looked upon as an embryonic abbre-
viation of the process by which these two ducts are formed in
Amphibians. The fact that this separation into Miillerian and
Wolffian ducts proceeds further in the females of most Amphi-
bians than in the males, strikingly shews that it is the oviductal
function of the Miillerian duct which is the indirect cause of its
separation from the Wolffian duct. The Miillerian 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 gene-
rally 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 incon-
spicuous 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 effe-
rentia 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 con-
sists of the following parts (Fig. 6) :
(1) Rudimentary Miillerian ducts, opening anteriorly into
the body-cavity, which sometimes carry aborted Kopfiiicren.
(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.
THE URINOGKNITAL ORGANS OF VERTEBRATES.
159
(4) The united lower parts of Wolffian and Miillerian ducts
which are really the lower unsplit part of the segmental ducts of
the kidneys.
m.tl
V /
FIG. 6. DIAGRAM OF THE URINOGENITAL ORGANS OF A MALE SALAMANDER.
(Copied from Ley dig's Histologic des Menschen u. der Thiere.}
md. Miiller'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 Miillerian ducts which function as the oviducts.
(2) The Wolffian ducts.
(3)
(4)
male.
The kidneys.
The united Miillerian and Wolffian ducts as in the
m.d
DIAGRAM OF THE URINOGENITAL ORGANS OF A FEMALE SALAMANDER.
(Copied from Ley Jig's Histologie des Menschen u. der Thiere}
Aid. Miiller's duct or oviduct ; IVd. 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
l6o THE URINOGENITAL ORGANS OF VERTEBRATES.
ova are carried off in both by a specialized oviduct. The
Wolffian duct, or ureter, is found both in Selachians and Am-
phibians, 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 Amphi-
bian 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 Se-
lachian.
(2) The division of the primitive duct of the kidney into
the Miillerian 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 Se-
lachians.
(4) The Miillerian duct persists in its entirety in male Am-
phibians, 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 rela-
tionship 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,
THE URTNOGENITAL ORGANS OF VERTEBRA IKS. l6l
there are no essential variations except in the later periods
of development throughout the division. These later varia-
tions, 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 conve-
nient 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.cT). As in Selachians, the in-
termediate cell-mass is a group of cells between the outer edge
of the protovertebrae 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 Miillerian duct to speak of the relations between the
Selachian duct and that of the bird.
Romiti (ArcJiiv f. Micr. Anat. Vol. X.) has recently stated
that the Wolffian duct developes 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 protovertebrae 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
B. II
162 THE URINOGENITAL ORGANS OF VERTEBRATES.
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. Pro-
tovertebrae ; W.d. Wolffian duct ; So. Somatopleure ; Sp. Splanchnopleure ; //.
pleuroperitoneal cavity ; ch. note-chord ; ao. dorsal aorta ; v. blood-vessels.
THE URINOGENITAL ORGANS OF VERTEBRATES. 163
series of ducts and Malpighian tufts which form the mass of the
Wolffian body1.
The Mullerian 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 8oth and looth hour of incubaticn the ducts
of the permanent kidneys begin to make their appearance.
Near its posterior extremity each Wolffian duct becomes ex-
panded, 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 im-
mediately after the formation of the permanent kidneys is
strikingly similar to its permanent condition in adult Sela-
chians. There is the Mullerian 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 perma-
nent 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.
1 This account of the origin of the Wolffian body differs from that given by Wal-
deyer, 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.
II — 2
164 THE URINOGENITAL ORGANS OF VERTEBRATES.
The subsequent changes of these parts are different in the
two sexes.
In the female the Miillerian ducts1 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 Sau-
ropsida 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 extre-
mity 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.
In the male the Miillerian 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 epi-
didymis. 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 por-
tion of the primitive uriniferous system which persists in the
adult.
In considering the relations between the modes of develop-
ment of the urinogenital organs of the bird and of the Se-
lachians, the first important point to notice is, that whereas in
the Selachians the segmental duct of the kidneys is first de-
veloped and subsequently becomes split into the Mullerian and
Wolffian ducts ; in the bird these two ducts develope inde-
pendently. This difference in development would be accurately
described by saying that in birds the segmental duct of the kid-
neys developes as in Selachians, but that the Mullerian duct
developes independently of it.
Since in Selachians the Wolffian duct is equivalent to the
segmental duct of the kidneys with the Mullerian removed from
it, when in birds the Mullerian duct developes independently of
the segmental kidney duct, the latter becomes the same as the
Wolffian duct.
1 The right oviduct atrophies in birds, and the left alone persists in the adult.
THE URINOGENITAL ORGANS OF VERTEBRATES. 165
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
Miillcrian and not at the same time, as one might expect ac-
cording 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 develope ; and not impro-
bably the development of the Miillerian 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 de-
velopment 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
Miillerian duct became more and more confirmed we might ex-
pect that the adult condition would impress itself more and
more upon the embryonic development, till finally the Miil-
lerian 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 be-
tween the Miillerian 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 (Eier-
stock 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 por-
tion of the kidneys of Selachians. The identity of the ana-
tomical 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
166 THE URINOGENITAL ORGANS OF VERTEBRATES.
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 develope as segmental involutions in point of time
anteriorly to their duct, while in birds they develope 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 diffiulty.
The further points of comparison between the Selachian and
the bird are very simple. The Miillerian 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 inde-
pendent 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 inde-
pendent 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 anatomi-
cal, are the abdominal pores of fishes, the generative ducts of
Ganoids, especially Lepidosteus, and the generative ducts of
Osseous fishes.
THE URINOGENITAL ORGANS OF VERTEBRATES. 167
The only further point which requires discussion is the em-
bryonic 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 in-
vestigators have attempted to prove that these organs are
derived from the epiblast. The proof they give is the fol-
lowing : 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 for-
mation 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 urino-
genital system is derived ! Whatever may have been the primi-
tive origin of the system, its mesoblastic origin in vertebrates
cannot in my opinion be denied.
Kowalewsky (Embryo. Stud, an Vermen it. Arthropoda, Mem.
Akad. St Petersbourg, 1871) finds that the segmental tubes of
Annelids develope 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 \
.
With Plates 22 and 23.
IN the course of an inquiry into the development of Elasmo-
branch 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 investiga-
tions embryos of Scyllium canicula, Scyllium stcllare, 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 conclu-
sions 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 lacunae 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 Pristiitrns.
In a Pristiurus-embryo, at the time when two visceral
clefts become visible from the exterior (though there are as yet
1 [From the Philosophical Transactions of the Royal Society of London, Vol.
CLXVI. Pt. i. Received October 5, Read December 16, 1875.]
DEVELOPMENT OF THE SPINAL NERVES, &C. 169
no openings from without into the throat), a transverse section
through the dorsal region exhibits the following features (PI.
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 y^ 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 pre-
pared 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 ^m inch, or about two-thirds of that of the cell.
The nuclei are granular, and very often contain several espe-
cially 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
haematoxylin 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 neu-
ral tube. The membrane is at this stage perfectly continuous
round the whole exterior of the neural tube as well on tJie dorsal
surface as on tJie 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
I/O DEVELOPMENT OF THE SPINAL NERVES
canal and tube become more nearly circular in section. Im-
mediately beneath the neural tube is situated the notochord (cJi).
It exhibits at this stage a central area rich in protoplasm, and a
peripheral layer very poor in protoplasm ; externally it is in-
vested by a distinct cuticular membrane.
Beneath the notochord is a peculiar rod of cells, constricted
from the top of the alimentary canal1. On each side and below
this are the two aortae, just commencing to be formed, and
ventral to these is the alimentary canal.
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, Bill, which are representa-
tions 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 PI. 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 aortas
1 Vide Balfour, " Preliminary account of the Development of Elasinobranch
Fishes," Quart. Journ. of Microsc. Scn-nce, Oct. 1874, p. 33. [This edition, p. 96.]
IN ELASMOBRANCH FISHES.
The upper ends of the muscle-plates have grovyn no further
round the neural canal than in fig. A, and no scattered meso-
blastic connective-tissue cells are visible.
In fig. A the dorsal surface of the neural canal was as com-
pletely 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. Bll,/r). 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 (PI. 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 dis-
tinguish 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
DEVELOPMENT OF THE SPINAL NERVES
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, accord-
ing 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 (PI. 23, fig. L)
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 struc-
tures to which I would call attention occurs at about the time
when three to five visceral clefts are present. The disappear-
ance 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 dif-
ficult to study.
Fortunately, however, in Torpedo these peculiar features
IX ELASMOBRANCH FISHES.
are not present to nearly the same extent as in Pristiurus and
Scyllimn.
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 pro-
ceeding 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 Pristinrus and Scylliiun.
TJie 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 duct1 is just appearing, but the cells of the
notochord have not become completely vacuolated. The rudi-
ments 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
(PI. 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.
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 distin-
guishing 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 (PI. 22,
1 Vide Balfour, " Origin and History of Urinogenital Organs of Vertebrates,"
Journal of Anatomy and Physiology, Oct. 1875. [This edition, No. vn.]
1/4 DEVELOPMENT OF THE SPINAL NERVES
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 indis-
tinct 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 vacuo-
lated ; 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 pro-
bably 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. Db), 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
IN ELASMOBRANCH FISHES. 175
the last stage (PI. 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 interpre-
tations in the previous stages of the Pristiurus-zmbryo.
It might be urged that the two masses which I have called
nerve-rudiments are nothing else than mesoblastic connective
tissue commencing to develope 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 promi-
nence, 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 (PI. 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 pos-
terior rudiments have made considerable steps in develop-
ment.
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 junc-
tion 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
DEVELOPMENT OF THE SPINAL NERVES
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 down-
ward 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 con-
siderable 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 com-
plete 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 under-
gone 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
IN ELASMOBRANCH FISHES. 177
anterior root are not less important than those in the posterior.
The anterior root now forms a very conspicuous cellular promi-
nence 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 down-
wards at an open angle : this, however, is not represented in the
specimen figured. The cells of which it is composed each con-
tain 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 sec-
tions 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 iij 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 (PI. 22, fig. Dd).
If the figure representing a transverse section of the em-
bryo (fig. D c) be examined, or better still the figure of a section
of the slightly older 6V/////7;//-embryo (PI. 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 (PI. 22, fig.
D d). In this figure pr points to the posterior roots and x to
the commissures uniting them.
B. 12
1/8 DEVELOPMENT OF THE SPINAL NERVES
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 (PI. 23, fig. L) in each case by a proto-
plasmic commissure with imbedded nuclei1. Near its dorsal
extremity each posterior root dilates, and from the dilated por-
tion is given off on each side the commissure uniting it with the
adjoining roots.
Considering the clearness of this formation in this embryo,
as well as in the embryo belonging to the stage under descrip-
tion, 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 Pristiums.
In the youngest of these (PI. 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 com-
menced to be visible.
In the previous stage the two nerve-rudiments met above the
1 This commissure is not satisfactorily represented in the figure. Vide Explana-
tion of Plate 2.
IN ELASMOBRANCH FISHES.
summit of the spinal cord and were broadly attached to it
there; now their points of attachment have glided a short dis-
tance down the sides of the spinal cord1.
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 visi-
ble. This appears, precisely as in Torpedo, in the form of a
small projection from the ventral corner of the spinal cord
(fig. E b, <7/-).
The second step in this stage (PI. 22, fig. F) is comparable,
as far as the connective-tissue is concerned, with the section of
Torpedo (PI. 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 ex-
tent by mesoblastic tissue, which, as in the case of the Torpedo,
takes its origin from two sources, (i) 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.
1 [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 enun-
ciated 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.]
l8o DEVELOPMENT OF THE SPINAL NERVES
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: — (i) 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 -^-^ x ^^ to
unnr x W<nr mcn> those of the vertebral rudiment y^ XTI|L^ 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 PI. 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. F1.
The cells forming the nerve-rudiments have undergone slight
modifications ; they are for the most part more distinctly elon-
gated 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 haematoxylin 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
1 The artist has not been very successful in rendering this figure.
TN ELASMOBRANCH FISHES. l8l
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
haematoxylin, and thus an apparent space is left between the
nerve-root and the spinal cord. This space by careful examina-
tion 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 PI. 22, figs. G I, G 2, and G 3.
The sections are approximately horizontal and longitudinal.
G i 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.
1 82 DEVELOPMENT OF THE SPINAL NERVES
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. G I and G 2).
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. G I and G 2) ; 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. G 2 and G 3).
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 op-
posite the median line of the muscle-plates, and do not appear
to join the posterior roots (vide fig. G 3, ar).
At the end of this period or second stage the main cha-
racters 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 undif-
ferentiated 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 com-
missures.
(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 differen-
tiations of the nerve-rudiments commence. Owing to the
IN ELASMOBRANCH FISHES. 183
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 (PI. 23, fig. H i).
Surrounding nearly the whole structure there is present a
delicate investment similar to that which I mentioned as sur-
rounding the neural canal and other organs ; it is quite struc-
tureless, 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 proxi-
mal portion of the posterior root, but vanishes near its distal
extremity.
The nerve-rudiment itself may be divided into three distinct
portions: — (i) 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 remark-
ably enough, not by its extremity, but by its side, to the spinal
cord. The dorsal extremities of the posterior nerves are there-
fore 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 uni-
form 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
184 DEVELOPMENT OF THE SPINAL NERVES
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, it 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 cor-
responding to x (PI. 23, fig. H l). 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 dis-
tinct 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 com-
posed 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 por-
tion of the nerve-rudiment : each of them possesses a large and
distinct nucleus.
The remainder of the nerve rudiment forms the commence-
ment 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-rudi-
IN ELASMOBRANCH FISHES. 185
msnt 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. 1 1, pr) consists, as before, of nearly
circular cells, each containing a nucleus, very large in propor-
tion to the size of the cell. The cells have a diameter of about
3oW °f an mcn- This mass forms not only the junction
between the ganglion and the spinal canal, but is also con-
tinued 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 elon-
gated 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
1 86 DEVELOPMENT OF THE SPINAL NERVES
both ends. The processes of the cells are at this stage very
difficult to observe : figs. la, I b, I c represent three cells pro-
vided with them and placed in the positions they occupied in
the ganglion.
The relatively very small amount of protoplasm in com-
parison 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 elon-
gated shape seems to imply this. In the next stage special
bundles of nerve-fibres become very conspicuous in the gan-
glion. The long diameter of an average ganglion-cell is about
Ysm °f 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 haematoxylin 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 PI. 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 sec-
tion to lie nearly opposite the anterior extremity of a muscle-
plate.
In a more ventral plane (fig. K 11) 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 mem-
brane 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 constitu-
tion 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
IN ELASMOBRANCH FISHES. 1 87
are cut through as they are proceeding, in a more or less hori-
zontal 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, jn 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 haematoxylin 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 consider-
able distance below the cord : this is shewn in PI. 23, fig. L.
Still later the portion of the roqt 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 Bill.
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
1 88 DEVELOPMENT OF THE SPINAL NERVES
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 ll), still in the region of the ear,
has no trace of a nerve, and thus serves to shew the early dis-
continuity 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 nerves1. The similarity in development be-
tween 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.
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 through-
out their whole length, soon cease to be so, and remain in con-
nexion 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 rudi-
ments. 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
1 [May 18, 1876. — Subsequent observations have led me to the conclusion that no
anterior nerve-roots are to be found- in the brain.]
IN ELASMOBRANCH FISHES. 189
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 pos-
terior 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 protovertebrae. His
alone, so far as I know, takes a different view.
His's1 observations lead him to the conclusion that the pos-
terior roots are developed as ingrowths from the external epiblast
into the space between the protovertebrae and the neural canal.
These subsequently become constricted off, unite with the neural
canal and form spinal nerves.
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 observations2.
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 con-
siderable light is the primitive origin of nerves.
So long as it was admitted that the spinal and cerebral nerves
1 Erste Anlage des Wirbclthier-Leibes.
2 [May 1 8, 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 re-
sembling 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.]
1 90 DEVELOPMENT OF THE SPINAL NERVES
developed in the embryo independently of the central nervous
system, their mode of origin always presented to my mind con-
siderable 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 peri-
phery), ultimately brought the two into connexion.
That such a condition could be a primive 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 com-
pletely 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 Elasmo-
branchs.
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 indepen-
dently of the spinal cord, and only subsequently become united
with it.
I have already insisted that this cannot be the primary con-
dition ; 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 mesoblast1.
1 [May 1 8, 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.]
IN ELASMOBRANCH FISHES. 19 1
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 un-
acquainted 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 stage1.
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 pneu-
mogastric is not a secondary state, but the remnant of a primary
one, in which all the spinal nerves were united, as they embryo-
nically are in Elasmobranchs.
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 ordi-
nary 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
1 Balfour, "A Preliminary Account of the Development of Elasmobranch Fishes,"
Q. y. Micros. Sc. 1874, plate xv. fig. 14, r.g. [This edition, PI. 4, fig. 14, v.g.}.
1 92 DEVELOPMENT OF THE SPINAL NERVES
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 comparison1, a transverse sec-
tion of which is represented by Leydig2 and Claparede. In this
we find that on the ventral surface (the Annelidan ventral
surface) of the nervous cord the ganglion-cells (grey matter) (/£)
are situated, and on the dorsal side the nerve-fibres or white
matter (//). 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.
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 Elasmobranchs 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 rem-
nant of the ciliation of the external skin now found amongst
many of the lower Annelids.
1 The nervous cords of other Annelids resemble that of Lumbricus in the relations
of the ganglion-cells of the nerve-fibres.
2 Tafeln zur vcrgleichenden Anatomic, Taf. iii. fig. 8.
IN ELASMOBRANCI1 FISHKS.
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 a priori possibility of
the formation of a spinal canal and the a 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 PLATES1.
PLATE it.
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 in. 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. i. )
In B in 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 rudi-
ments of the posterior nerve-roots.
In B I the rudiments of the posterior roots are of considerable length.
1 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.
B. I3
194 DEVELOPMENT OF THE SPINAL NERVES
pr. rudiment of posterior roots, nc. neural canal, mp. muscle-plate, ch. noto-
chord. x. subnotochordal rod. ao. dorsal aorta, so. somatopleure. sp. splanchno-
pleure. 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
Da. Camera. (Zeiss CC ocul. 2.) The posterior nerve-rudiment is considerably
longer than in fig. D a, 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 E a. 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.
IN KI.ASMoIiRANCH F1SHF.S. 195
Figs. G i, G i, 03. Three longitudinal and horizontal sections of an embryo some-
what older than F. The embryo from which these sections were taken was hardened
in osmic acid, but the sections have been represented without tinting. G i is most
dorsal of the three sections. Camera. (Zeiss CC ocul. i.)
nc. neural canal, sp.c. spinal cord. pr. rudiment of posterior root. ar. rudiment
of anterior root. nip. muscle- plate, t. 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 (sfl.g), and nerve («), 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. i.)
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 n. Two sections of a Fristiitrus-embryo somewhat older than H.
Camera. (Zeiss CC ocul. i.)
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 n. 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. i.)
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, nip. muscle-plate, nip '. first-formed muscles.
Fig. L. Longitudinal and vertical section through the trunk of a Scyllium-emhryo
after the external gills have attained their full development. . Camera. (Zeiss CC
ocul. i.)
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 unfortu-
nately 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 con-
13—2
196 DEVELOPMENT OF THE SPINAL NERVES, &C.
spicuous 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. Mi, 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 ex-
hibiting an outgrowth to form the first visceral cleft.
IX. ON THE SPINAL NERVES OF AMPHIOXUSI.
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 Elasmobranchs, 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 cor-
roborated by subsequent observers.
Stieda2, 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 alter-
nately 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.
Langerhans3 apparently agrees with Stieda as to the facts
about the alternation of dorsal and ventral roots, but differs
1 From the Journal of Anatomy and Physiology, Vol. X. 1876.
- Mem. Acad. Pctersbour^, Vol. XIX.
3 Archiv f, mikr. Anatomic, Vol. xii.
198 THE SPINAL NERVES OF AMPHIOXUS.
from him as to the conclusions to be drawn from those facts.
He does not, for two reasons, believe that two nerves of Amphi-
oxus can be equivalent to a single nerve in higher vertebrates :
(i) Because he finds no connecting branch between two suc-
ceeding 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 equiva-
lent to those which in higher vertebrates supply a single myo-
tome only.
Although the agreement as to facts between Langerhans
and Stieda is apparently a complete one, yet a critical exami-
nation of the statements of these two authors proves that their
results, on one important point at least, are absolutely contra-
dictory. 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 sup-
plied 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 counter-
balance 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 Langerhans1. On
examining specimens so obtained it appeared that, for the
greater length of the cord, the nerves arose alternately on the
1 Lot. at.
THE SPINAL NERVES OF AMPHIOXUS. IQ9
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.
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 investiga-
tion 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 Amphi-
oxus 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 diffi-
cult 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 con-
tact 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.
2OO THE SPINAL NERVES OF AMPHIOXUS.
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 ven-
tricle 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 l.
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 be-
hind 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 con-
stant, 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
<•. cil.
THE SPINAL NERVES OF AMPHIOXUS. 2OI
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 ger-
minal vesicle and on the division of nuclei. I may also call
attention to the valuable papers of Prof. His1 on the formation
of the layers in Elasmobranchs, and of Prof. Kowalevsky2 on
the development of Amphioxus, to both of which I would
certainly have referred, had it been possible for me to do so.
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 con-
firmation of the views expressed in chapter VI. on the develop-
1 Zeitschrift f. Anat. u. Entwicklungsgeschichte, Bd. II.
2 Archivf. Micr. Anat. Bd. xm.
206 PREFACE.
ment 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 His1 and
Gotte2, 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 explana-
tions 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 establish-
ment 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.
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 con-
ception 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 embryo-
logical 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 con-
clusions in reference to the relations of the sympathetic system
and the suprarenal body, and to the development of the meso-
1 Erste A nlage des \Virbclthierldbes.
2 Enhvicklungsgeschichte dcr Unkc.
PREFACE. 207
blast, 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
Elasmobranchs 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 expen-
diture of time on the part of any writer, who is capable of some-
thing 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 for-
warded 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 de-
mands on their liberality.
To my friend and former teacher Dr Michael Foster I
tender my sincerest thanks for the neverfailing 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. Gotte'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 seg-
mentation.
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 Elasmobranchs 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.
B. 14
210 TABLE OF CONTENTS.
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 me-
dullary canal. The mesoblast. — Its division into somatic and splanchnic layers.
Formation of protovertebr£e. 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. — Con-
stitution of lateral plates of mesoblast. Their splanchnic and somatic layers.
Body-cavity constituting space between them. Their division into lateral and ver-
tebral plates. Continuation of body-cavity into vertebral plates. Protovertebrae.
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. Com-
munication of pericardial and peritoneal cavities. Somatopleure and splanchnopleure.
Resume. General considerations on development of mesoblast. Probability of
lateral plates of mesoblast in Elasmobranchs 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 noto-
chord.— 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 Gotte's
view of lateral nerve. Muscle-plates. — Their growth. Conversion of both layers into
TABLE OF CONTENTS. 211
muscles. Division into dorso-lateral and ventro-lateral sections. Derivation of limb-
muscles from muscle-plates. Vertebral column and notochord. — Previous investi-
gations. Formation of arches. Formation of cartilaginous sheath of notochord and
membrana elastica externa. Differentiation of neural arches. Differentiation of
hrcmal 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 develop-
ment 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. Gotte. Calberla. Relations between
Annelidan and Vertebrate nervous systems. Spinal canal. Dr Dohrn's views.
Their difficulties. Hypothesis of dorsal coalescence of lateral nerve cords. Sympa-
thetic 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 mem-
brane. 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 devel-
opment of 5th, 7th, 8th, Qth and roth 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. — Separa-
tion of single rudiment into seventh and auditory. Forking of seventh nerve over
hyomandibular cleft. Formation of anterior branch to form ramus opthalmicus super-
ficialis of adult. General view of morphology of branches of seventh nerve. Glosso-
pharyngeal 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 my otomes 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 (i) cranial nerves, (2) visceral clefts, (3) head-cavities.
Comparison of results obtained.
212 TABLE OF CONTENTS.
CHAPTER X.
THE ALIMENTARY CANAL, pp. 446 — 459.
The solid (esophagus. — OZsophagus 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. Pre-
vious 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 XL
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 veiri. The circulation of the yolk-sack. — Previous obser-
vations. Various stages. Difference of type in amniotic Vertebrates. The vascular
glands. — Supra-renal and inter-renal bodies. Previous investigations. The supra-
renal bodies. — Their structure in the adult. Their development from the sympathetic
ganglia. The inter-renal body. — Its structure in the adult. Its independence of supra-
renal 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 Elasmobranchs. 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 Miillerian and Wolffian ducts. In female — General account. Formation of ovi-
duct as nearly solid cord. Hymen. In male — Rudimentary Miillerian duct. —
Comparison of development of Miillerian duct in Birds and Elasmobranchs. 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. Resume, 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 pro-
tecting 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 im-
perfect.
The bulk of the ovum is composed of yolk spherules,
imbedded in a protoplasmic matrix. Dr Alexander Schultz1,
who has studied with great care the constitution of the yolk,
finds, near the centre of the ovum, a kernel of small yolk sphe-
rules, 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.
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 observa-
tions on this subject'2. Dr Schultz's confirmation is the more
important, since he appears to be unacquainted with my pre-
vious investigations. In my paper (loc. cit.\ after giving a
description of the network I make the following statement as to
its distribution.
1 Archiv fur Micro. Anat. Vol. XI. 1875.
'2 Quart. Journ. Micro- Science, Oct. 1874. [This edition, No. V.]
214 THE DEVELOPMENT OF ELASMOBRANCH FISHES.
"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 represent-
ing 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.]
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 demon-
strates 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 PI. 6, fig. i) 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 PI. 6, fig. I. 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. i). 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
THE RIPE OVARIAN OVUM. 21$
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 displace-
ment. In the germinal vesicle figured the contents are some-
what 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 pecu-
liar 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 regu-
larity 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,
2l6 THE DEVELOPMENT OF ELASMOBRANCH FISHES.
(i) 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 follow-
ing features of my sections :
(i) The rupture of the membrane of the germinal vesicle on
its lower surface. (2) The position of the contents almost com-
pletely below the membrane of the vesicle and surrounded by yolk.
In connection with this subject, Oellacher's valuable observa-
tions upon the behaviour of the germinal vesicle in Osseous
Fishes and in Birds at once suggest themselves1. 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 aggre-
gated 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."
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.
1 Archiv fiir Micr. Anat. Vol. vm. p. i.
RIPE OVARIAN OVUM. 2 1/
While, then, there are on the one hand Oellacher's observa-
tions on a single animal, hitherto unconfirmed, there are on the
other very definite observations tending to shew that the ger-
minal vesicle has in many cases an altogether different fate.
Gotte1, 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.
Gotte 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 lenslike 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 Gotte 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 Beneden2 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 Gotte, but it is difficult to believe that an
1 Entwicklungsgcschichte der Unke.
J Rechcrches sur la Composition et la Signification de FCEuf.
B. I5
2l8 DEVELOPMENT OF ELASMOBRANCH FISHES.
extrusion of the vesicle in the way described by Oellacher would
have escaped his notice.
Passing from Vertebrates to Invertebrates, we find that
almost every careful investigator has observed the disappear-
ance, apparent or otherwise, of the germinal vesicle, but that
very few have watched with care the steps of the process.
The so-called Richtungskorper 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
Flemming1.
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, accord-
ing to his observations, disappeared before the appearance of the
Richtungskorper.
Kleinenberg2, 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 con-
toured membrane, and equally distributed granular contents, in which the
germinal spot had appeared The germinal vesicle reaches o-o6mm. 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.
1 " Studien in der Entwicklungsgeschichte der Najaden," Silz. d. k. Akad. Wien,
Bd. LXXI. 1875. 2 Hydra. Leipzig, 1872.
RIPE OVARIAN OVUM. 219
"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."
Kleinenberg clearly finds that the germinal vesicle disappears
completely before the appearance of the Richtungskorper, in
which he states a pseudocell or yolk-sphere is usually found.
The connection between the Richtungskorper and the germi-
nal 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 Richtungskorper 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 Richtungskorper.
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 Schenk1. 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.
If we suppose, and this is not contradicted by observation,
that the Richtungskorper 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
1 " Die Eier von Raja quadrimaculata," Si'/z. d?r k. Akad. Wien, Bel. LXVIII.
15—2
220 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 imme-
diately 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 Richtungskorper. 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.
(i) Oellacher (Bird, Osseous Fish). (2) Gotte (Bombinator
igneus). (3) Kupffer (Ascidia canina). (4) Strasburger
(Phallusia mamillata). (5) Kleinenberg (Hydra). (6) Metsch-
nikoff (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. Asterocanthion1, 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
1 Agassiz, Embryology of the Star-Fish.
RIPE OVARIAN OVUM. 221
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 nigro-
venosa), Fol (Geryonia), Kupffer (Ascidia canina), Strasburger
(Phallusia mamillata), Flemming (Anodon), Gotte (Bombinator
igneus)], which is generally stated to vanish before the appear-
ance of the first furrow ; but in some cases (Kupffer and Gotte,
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.
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 seg-
ments.
The external appearance of the blastoderm, which remains
nearly constant during segmentation, has been already well
described by Leydig1.
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, i|m. in diameter. Its colour renders it
very conspicuous, a feature which is further increased by its
being surrounded by a narrow dark line (PI. 6, fig. 2), the indica-
tion 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. «'/.), and
as Leydig (loc. «Y.) 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
1 Rochen mid Haie.
SEGMENTATION. 223
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 im-
mediately surrounding the germinal disc. The innermost band
is formed by the germinal disc itself and is composed of sphe-
rules 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 men-
tioned 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.
224 DEVELOPMENT OF ELASMOBRANCH FISHES.
In the next youngest of the eggs1 examined the germinal
disc was already divided into twenty-one segments. When
viewed from the surface (PI. 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.
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 (PI. 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
1 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.
SEGMENTATION. 22 5
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 PI. 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 ap-
pearance 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 seg-
mentation furrows.
Lining the two sides of the segmentation furrows there is
present in sections a layer which stains deeply with colouring
re-agents; 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 vacuo-
lar 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 satis-
factory observations on the behaviour of the nucleus. I find
226 DEVELOPMENT OF ELASMOBRANCH FISHES.'
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 con-
tinued, would have passed. The connection (if any exists) be-
tween 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 PI. 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 seg-
ments completely circumscribed on all sides. The peripheral
SEGMENTATION. 22J
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 seg-
ments 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 (PI. 6, fig. 7 /); 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 sur-
rounded 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 com-
mencing to be distinguished from the remainder as a separate
layer which becomes progressively more distinct as segmenta-
tion proceeds.
The largest segments in this section measure about the
Ti^th of an inch in diameter, and the smallest about ^hjth of
an inch.
The nuclei at this stage present points of rather a special in-
terest. In the first place, though visible in many, and certainly
present in all the segments1, 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,
1 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, clue to the yolk-spherules and in part to the
thinness of the section as compared witli the diameter of a segmentation sphere.
228 DEVELOPMENT OF ELASMOBRANCH FISHES.
but are also to be seen in places where there are no traces of
fresh segments.
This fact, especially when taken in connection with the for-
mation of fresh segments outside the germinal disc and with
other facts which I shall mention hereafter, is of great morpho-
logical 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 be-
haviour 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 striae. 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
striae, 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 striae diverging outwards from the apices of the cones
must be carefully distinguished from the striae of the cones
themselves. The cones are bodies quite as distinctly differ-
entiated from the protoplasm of the cell as nuclei, while the
striae which diverge from their apices are merely structures in
the general protoplasm of the cell.
SEGMENTATION. 229
In some cells, which contain these bodies, no trace of a com-
mencing 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 de-
termine 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 PI. 6, figs. 8 a, 8 b, 8 c. In all
of these there can be traced out the two cones, which are how-
ever 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.
230 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 de-
scribed by me in a preliminary paper1, and I feel satisfied that
there is in some cases an actual connection between the net-
work and the nuclei. This network I shall describe more fully
hereafter.
Further points about these figures and the nuclei of this
stage I should like to have been able to observe more com-
pletely than I have done, but they are so small that with the
highest powers I possess (Zeiss, Immersion No. 2 = Ty n.) 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 (PI. 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
PI. 7). In some cases it appears to me that several of these
are in close juxta-position, 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 re-
markable 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 increas-
ing rapidly, such figures are not to be met with.
1 Loc. dt.
SEGMENTATION. 231
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 c'ell.
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 I 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 com-
pletely 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
232 DEVELOPMENT OF ELASMOBRANCH FISHES.
evidence is quite conclusive are not very numerous. Recently
F. E. Schultze1 appears to have observed it in the case of an
Amoeba in an altogether satisfactory manner. The instance is
quoted by Flemming2. 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 Amceba, which occu-
pied eight minutes. Amongst vegetable cells the division of the
nucleus seems to be still rarer than with animal cells. Sachs3
admits the division of the nucleus in the case of the paren-
chyma cells of certain Dicotyledons (Sambucus, Helianthus,
Lysimachia, Polygonum, Silene) on the authority of Hanstein.
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
Fol4, Flemming5, Auerbach6 and possibly also Oellacher7 as well
as other observers.
These figures8 are possibly due to the streaming out of the
1 Archivf. Micr. Anat. xi. p. 592.
2 "EntwicklungsgeschictederNajaden,"LXXl.Bd.der5zV2.^r£.^<ra</. Wim, 1875.
3 Text-Book of Botany, English trans, p. 19.
4 "Entw. d. Geryonideneies." Jenaische Zcitschrift, Bd. VII.
6 Loc. cit.
6 Organologische Studien, Zweites Heft.
7 "Beitrage z. Entwicklungsgeschichte der Knochenfischen." Zeit. fiir Wiss.
Zoologie. Bd. xxn. 1872.
8 The memoirs of Auerbach and Strasburger (Zellbildung a. Zelltheilung) have
unfortunately come into my hands too late for me to take advantage of them. Especi-
ally 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 striae of the proto-
plasm, 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
SKCMKNTATION. 233
protoplasm of the nucleus into that of the cell1. The appear-
ance 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 fey the
stream will leave behind it a slack area where there is no move-
ment 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", even the larger yolk-
spherules are arranged in this fashion.
On the supposition that the striation of these figures is
due to the outflow from the nucleus, the appearances presented
in Elasmobranchs 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 striae in the body con-
verging 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
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 strire ; and in some respects they
support Strasburger's views against those of other observers, since they demonstrate
that in Elasmobranchs the modified nucleus does actually divide.
1 This is the view which has been taken by Auerbach (Organologische Studien).
• Loc. fit.
H. 1 6
234 DEVELOPMENT OF ELASMOBRANCH FISHES.
vesicle of an ovum. The whole of the contents of the germinal
vesicle become at its disappearance mingled with the proto-
plasm 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 proto-
plasm of the cell necessarily has a share in forming the new
nuclei.
Although, in instances where the nucleus vanishes, an abso-
lute 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 nu-
clear formation, I wish to shew that my results in Elasmobranchs
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 dissolu-
tion ; but though a portion of the nucleus may stream out into
the yolk, I think it impossible that the whole of it does1.
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 extremi-
ties were less marked than in the earlier stage.
1 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.
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. Gotte1 has
figured structures somewhat similar to these bodies, but I~haTdly
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, Gotte gives a very different explanation of
them from my own2.
A second of my results, which points to a series of inter-
mediate 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. Hertwig3 on the gemmation of Podo-
plirya geuimipara, 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.
From the peculiar arrangement of the net-work of lines of
the yolk around these knobbed nuclei, it is reasonable to con-
clude that interchange of material between the protoplasm of
1 Entwickelungsgeschite dcr Unke, PI. i. fig. 18.
2 As I before mentioned, Strasburger (Zellbildung u. Zelltheilung) has represented
bodies precisely similar to those I have described, which appear during the seg-
mentation in the egg of Phalltisia mammillata as well as similar figures observed by
Butschli in eggs of Cucitllanus elegans and Blatla Gcrmanica, The figures in this
monograph are the only ones I have seen, which are identical with my own.
3 Morphologischcs Jahrbiich, Bd. i. pp. 46, 47.
1 6 — 2
236 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Elasmobranchs 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 protoplasm1. If the lobate nuclei are also
nuclei undergoing division, we have in the egg of an Elasmo-
branch examples of all the known forms of nuclear increase
unaccompanied by cell division.
The next stage in the segmentation does not present so
many features of interest as the last one. The segments are
1 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.
SEGMENTATION. 237
now so small, as to be barely visible from the surface with a
simple lens. A section of an embryo of this stage is repre-
sented in PI. 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 seg-
ments composing it are markedly smaller than the remainder
of the cells of the germinal disc, but possess nuclei of an abso-
lutely 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 ^^ 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 -^^ 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 «').
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 seg-
mentation, the cells of the whole blastoderm have become
smaller (PI. 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.
238 DEVELOPMENT OF ELASMOBRANCH FISHES.
Instead of being but indistinctly separated from the sur-
rounding 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 at-
tached 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.
SEGMENTATION. 239
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. Oellacher1 and Gotte2 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 Elasmobranchs 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.
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 seg-
mentation 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 Elasmobranchs the first two furrows are formed in a per-
fectly 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 hori-
zontal furrow of the Batrachian egg formed. This furrow
appears to be represented in the Elasmobranch segmentation
1 Zeitschrift fiir Wiss. Zotlogie, Bd. xxm. 1873.
2 Archivfur MUr. An at. Bd. IX. 1873.
240 DEVELOPMENT OF ELASMOBKANCH FISHES.
by the irregular circumscription of a body of central smaller
spheres from a ring of peripheral larger ones (vide PI. 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 disc1.
From Oellacher's2 account of the segmentation in the fowl3 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 PI. 6, fig. 6). Segmentation in the Elasmo-
branch 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.
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
Oellacher4 and Klein8). 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.
In Oellacher's6 figures, PI. 23, figs. 19 — 21, peculiar headings
1 Vide Elements of Embryology, p. 23.
2 Strieker's Studien, 1869, Pt. i, PI. II. fig. 4.
3 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.
4 Z-eitschrift fur Wiss. Zool. Bd. xxn. -1871.
5 Mo nthly Microscopical Journal, .March, 1872. K Loc. at.
SEGMENTATION. 24!
of the sides of the earlier formed furrows are distinctly shewn.
No mention of these is made in the text, but they are un-
questionably similar to those I have described in the Elasmo-
branch furrows. In the case of Elasmobranchs 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.
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
Oellacher1 describes as crossing the commencing segmentation
furrows. I have also failed to discover any signs of a concentra-
tion 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.
With reference to the nuclei which Oellacher2 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.
He3 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.
1 Loc. cit. - Liu. tit. '* Loc. cit. pp. 410, 411, &c.
242 DEVELOPMENT OF ELASMOBRANCH FISHES.
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.
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 paper1.
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
1 Loc. cit. p. 415. [This Edition, p. 64.]
SEGMENTATION. 243
from the lower parts of the germinal disc which in Osseous Fish
is more distinctly marked off from the food-yolk than in Elasmo-
branchs.
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 Leydig1. To his description of the
germinal disc, I have already done full justice.
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*. 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.
Schenk3 has also made important investigations on the sub-
ject. 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 Leydig4 in denying its existence.
Schenk further found that after impregnation, but before seg-
mentation, 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
1 Rochen u. Haie. It is here mentioned that Coste observed the segmentation in
these fishes.
3 "Recherches sur la segmentation des products adventifs de 1'ceuf des Plagios-
tomes et particulierement des Raies." Robin, jfoitrnal de r Anatomic et de la Phy-
siologie, p. 609, 1872.
3 "Die Eier von Raja quadrimaculata innerhalb der Eileiter." Silz. der k. Akad.
Wien. Vol. LXXlll. 1873.
4 Loc. cit. My denial of the existence of this membrane naturally applies only to
the egg after impregnation, and to the genera Scyllium and Prisliurus.
244 . DEVELOPMENT OF ELASMOBRANCH FISHES.
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 segmen-
tation, which were caused by the non-penetration of my harden-
ing reagent beyond a certain point.
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 im-
pregnation, the germinal disc presents towards the yolk a
strongly convex surface, and that at a later period, but still be-
fore 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
Fishes1. In this a large number of the facts here described in
full are briefly alluded to.
The last author who has investigated the segmentation in
Elasmobranchs, is Dr Alexander Schultz2. He merely states
that he has observed the segmentation, and confirms Professor
Schenk's statements about the amoeboid movements of the
germinal disc.
EXPLANATION OF PLATE 6.
Fig. i. 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 segmen-
tation.
1 Loc. cit.
2 "Die Embryonal Anlage der Selachier. Vorlaufige Mittheilung," Centralblatt f.
Med. IViss. No. 33, 1875.
SEGMENTATION. 245
Fig. 6. Section through the germinal disc represented in fig 3. «. 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 6b. Two furrows of the same germinal disc more highly magnified.
Fig. 6c. 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 ; /. furrow
appearing in the yolk around the germinal disc.
Figs. 7 a, fi>, ic. Three segments with modified nuclei from the same germinal
disc.
Fig. 8. Section through a somewhat older germinal disc. ep. epiblast ; »'. nuclei
of yolk.
Figs. 8 a, 8i>, Sc. 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 segmenta-
tion cavity, or cavity of von Baer, which arises as a small space
in the midst of the blastoderm, near its non-embryonic end
(PI. 7, % i).
This condition of the segmentation cavity, though already1
described, has nevertheless been met with in one case only.
The circumstance of my having so rarely met with this con-
dition 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 Schultz2 does not mention having found
any stage of this kind.
The position of the cavity in question, and its general ap-
pearance, incline me to the view that it is the segmentation
cavity3. If this is the true view of its nature the fact should be
1 Qy. Journal of Microsc. Science, Oct. 1874. [This Edition, No. V.]
2 Ctntr. f. Med. Wiss. No. 38, 1875.
3 Professor Bambeke (" Poissons Osseux," Mem. Acad. Belgique 1875) describes a
cavity in the blastoderm of Leuciscus rutilus, which he regards as the true seg-
mentation cavity, but not as identical with the segmentation cavity of Osseous Fishes,
FORMATION OF THE LAYERS. 247
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 de-
velopment.
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 epi-
blast, and a lower one consisting of the remaining cells of the
blastoderm.
An average cell of the lower layer has a diameter of about
T^U 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 Schultz1 for cells: there can however be
no question that they are true nuclei.
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 (PI. 8, fig. A) the blastoderm
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.
1 Loc. cit.
248 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 blasto-
derm, 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 never-
theless not absolute, and it is doubtful whether there is any
period in which the floor of the cavity is quite without cells.
Dr Schultz supposes1 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 PI. 13, fig. i, of
1 Loc. cit.
FORMATION OF THE LAYERS. 249
my preliminary paper1, an illustration which is repeated on PL
7, fig. 2.
The number of cells on the floor of the cavity differs con-
siderably 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 (PI. 7, fig. 2, b d\ In my preliminary paper2
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.
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
Schultz3, but in all cases the cells simply rested upon it.
Passing from the segmentation cavity to the blastoderm
itself, the first feature to be noticed is the more decided differ-
entiation 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 blasto-
derm. In my specimens this layer was never more than one
cell deep, but Dr Schultz4 states that, in the Elasmobranch
embryos investigated by him, the epiblast was composed of
more than a single row of cells.
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 PI. 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
1 Loc. cit.
- Qy. Journal of Micros. Science, Oct. 1874. [This Edition, No. V.]
3 Loc. cit. Probably Dr Schultz, here as in other cases,"has mistaken nuclei for
cells.
4 Loc. cit.
B. 17
250 DEVELOPMENT OF ELASMOBRANCH FISHES.
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
(PI. 7, fig. 4). In these it is very easy to see that the epiblast
simply thins out at the edge of the blastoderm without exhibit-
ing the slightest tendency to become continuous with the lower
layer cells1.
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
1 Prof. Haeckel ("Die Gastrula u. die Eifurchung d. Thiere," Jenaische Zeit-
schrift, 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.
FORMATION OF THE LAYERS. 251
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 com-
posed 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 PI. 7, fig. 2 a. An
average cell measures about ^ to -^ of an inch, but some of
the larger ones on the floor attain to the -^ 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 y^- 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.
17—2
252 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 -gfo to -^ 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 (PI. 7, figs. 2 a and
2c and 3), which vary from simple knobs to projections of such a
size as to cause the nucleus to present an appearance of com-
mencing 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 con-
dition is represented in PL J, 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 de-
scribed. Its meshes are finer in the vicinity of the nuclei, and
its fibres in some cases almost appear to start from them (PI. 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
(PI. 7, fig. 12). In other specimens hardened in osmic acid
(PI. 7, fig. 11), and in all hardened in chromic acid (PI. 7, fig. 2a
and 2c), 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 else-
where or completely absent, vide PI. 7, fig. 2b.
FORMATION OF THE LAYERS. 253
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
Flemming1, Hertwig2 and Van Beneden8. The latter view ap-
pears to me to be the more probable one.
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 nu-
clei 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 de-
duction 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.
1 "Entwicklungsgeschichte der Najaden," Sitz. d. k. Akad. IVien, 1875.
2 Morphologische Jahrbuch, Vol. I. Heft 3.
3 " Developpement des Mammiferes," Bui. de r Acad.de Relgiqnc, \\.. No. 12, 1875.
254 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Elasmo-
branchs 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 be-
comes 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 pro-
jection I propose calling, as in my preliminary paper1, the em-
bryonic rim.
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
PI. 7, fig. 4, is represented in PI. 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 (i)
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
1 Qy. Journal Microsc. Science, Oct. 1874. [This Edition, No. V.]
FORMATION OF THE LAYERS. 255
precisely similar but more partial change in the constitution of
the floor takes place in Osseous Fishes1.
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 in-
wards 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 com-
bined 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 PI. 7, fig. 5) Towards the
1 Gotte, "Der Keim d. Forelleneies, " Arch. f. Mikr. Anat. Vol. ix.; Haeckel,
"Die Gastrula u. die Eifurchung d. Thiere," Jenaische Zeitschrift, Bd. ix.
256 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 be-
comes 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#, 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. Ad-
joining 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 com-
mencement 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 be-
FORMATION OF THE LAYERS. 257
tween the columnar cells and the typical rounded lower layer
cells1.
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 struc-
ture has become visible.
A surface view of a blastoderm of this age, with the embryo,
is represented on PI. 8, fig. B ; and I shall, for the sake of con-
venience, 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 blasto-
derm, 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 figured2 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.
A fresh feature of great importance is the complete dis-
appearance 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 oblite-
ration 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.
1 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.
a Owing to the small size of the plates this section has been drawn on a con-
siderably smaller scale than that represented in fig. 5.
258 DEVELOPMENT OF ELASMOBRANCII FISHES.
Its earliest appearance is involved in some obscurity, though
it probably arises as a simple cavity in the midst of the lower
layer cells (PI. 7, fig. i). 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 (PI. 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 Elasmobranchs 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 seg-
mentation 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 Vertebrates1."
It was there pointed out, that as the food material in the ovum
increases, the bulk of the lower layer cells necessarily also in-
creases ; 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.
All the most recent observations2 on Osseous Fishes tend
1 Quart. Journ.of Microscop. Science, July, 1875. [This Edition, No. VI.]
2 Oellacher, Zeit. f. Wiss. Zoologie, Bd. xxin. Gotte, Archiv f. Mikr. Anat.
Vol. ix. Haeckel, loc. cit.
FORMATION OF THE LAYERS. 259
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 blasto-
derms of these animals, I still hesitate to accept as conclusive
the testimony on this point.
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 Fish1. Upon this feature
great stress is laid both by Dr Gotte2 and Prof. Haeckel3 : but I
am unable to agree with the interpretation of it offered by them.
Both Dr Gotte 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
Elasmobranchs by a structure quite separate from the ingrowth
of cells to form the floor of the segmentation cavity.
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 embry-
onic 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 Oellacher4 and Gotte6.
Its meaning becomes at once intelligible by referring to the
diagrams in my paper6 on the Early Stages in the Development
of Vertebrates. It in fact arises from the asymmetrical character
1 This floor appears in most Osseous Fish to be only partially formed. Vide
Gotte, loc. at.
8 Loc. cit. s Loc. cit. * Loc. cit.
b Loc. cit. 6 Loc. cit.
2<5<D DEVELOPMENT OF ELASMOBRANCH FISHES.
of the primitive alimentary involution in all anamniotic verte-
brates with the exception of Amphioxus.
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 PI. 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 PI. 7, fig. 8 a, 8&
and 8^.
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 qf 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 else-
where (compare fig. 6 and fig. 7 and 7«), yet that this gain in
size is not produced by an outgrowth of the embryo beyond
FORMATION OF THE LAYERS. 26 1
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<r) 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, how-
ever, 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 (PI. 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 ex-
ternal 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 alimen-
tary 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 Elasmobranchs by the
262 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 (PI. 7, fig. 8*:). 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
PI. 7, fig. 8b, n. al. The cells constituting this mass eventually
become converted into the lateral and ventral walls of the alimen-
tary 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 com-
mencing mesoblast.
Thus much of the mode of formation of the mesoblast can
be easily made out in longitudinal sections, but transverse sec-
tions 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 embryo1. In my
1 Professor Lieberkiihn (Gesellschaft zu Marburg, Jan. 1876) finds in Mammalia a
bilateral arrangement of the mesoblast, which he compares with that described by me
in Elasmobranchs. 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 Elasmobranchs though overlooked by me. I can definitely state
that, whatever may be the condition of the mesoblast in Mammalia, in Elasmobranchs
at any rate no such layer exists.
FORMATION OF THE LAYERS. 263
preliminary account1 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 meso-
blast arises as two distinct lateral masses, one on each side~of the
axial line.
In the embryo from which the sections PL 7, fig. 8 a, 86,
8c were taken, the mesoblast had, in most parts, not yet become
separated from the hypoblast. It still formed with this a con-
tinuous layer, though the mesoblast cells were distinguishable by
their shape from the hypoblast. In only one section (&} 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. 8b] ; but no continuous layer
of it is present In the foremost of the three sections (fig. 8^)
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 maybe 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 forma-
tion 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 fea-
tures 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
1 Loc. fit.
264 DEVELOPMENT OF ELASMOBRANCH FISHES.
direction. The growth of the blastoderm has continued to be
very rapid.
In the region of the embryo (PI. 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 (PI. 7,
fig- 9)> while the two plates of mesoblast are isolated and dis-
connected from any other masses of cells.
The alimentary cavity is best studied in transverse sections.
(Vide PI. 7, fig. ioa, lob and loc, 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 sepa-
rated 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 (PI. 7, fig. ioa
and iob], 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 develop-
ment of the mesoblast, it is clear that in Elasmobranchs this
layer is derived from the same mass of cells as the hypoblast,
FORMATION OF THE LAYERS. 265
and receives none of its elements from the epiblast. In connec-
tion with its development, as two independent lateral masses,
I may observe, as I have previously done1, that in this respect
it bears a close resemblance to mesoblast in Euaxes, as de-
scribed by Kowalevsky2. This resemblance is of some interest,
as bearing on a probable Annelid origin of Vertebrata. Kow-
alevsky has also shewn3 that the mesoblast in Ascidians is
similarly formed as two independent masses, one on each side
of the middle line.
It ought, however, to be pointed out that a similar bilateral
origin of the mesoblast had been recently met with in Lym-
naeus by Carl Rabl4. A fact which somewhat diminishes the
genealogical value of this feature in the mesoblast in Elasmo-
branchs.
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 some-
times be seen without any yolk-spherule whatever.
On PI. 7, fig. ja, and figs. II 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 PI. 7,
1 Quart. Journ. of Micro sc. Science, Oct., 1874. [This Edition, No. V.]
2 "Embryologische Studien an Wiirmern u. Arthropoden." Mtmoires de r Acad,
S. Pctersbourg. Vol. xiv. 1873.
3 Archivfur Mikr. Anat. Vol. vii.
4 Jenaische Zeitschrift, Vol. ix. 1875. A bilateral development of mesoblast,
according to Professor Haeckel (loc. cit.), occurs in some Osseous Fish. Hensen,
Zcit.fiir Anat. u. Ent-w. Vol. i., has recently described the mesoblast in Mammalia
as consisting of independent lateral masses.
B. 18
266 DEVELOPMENT OF ELASMOBRANCH FISHES.
fig. 14. In full-sized ovarian eggs, according to Schultz1, it
forms, as was mentioned in the first chapter, radiating striae,
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.
I have already (p. 252) touched upon the relation of this
network to the nuclei of the yolk2.
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 PI. 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 (PI. 7, fig. 13). Although it would
be possible for cells in the living state to pass from the blasto-
derm 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, (i) That the cells
1 Archivfiir Mikr. Anat. Vol. XI.
2 A protoplasmic network resembling in its essential features the one just de-
scribed 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. (JenaischeZeitschrift, Vol. vn.) Metschnikoff (Zeitschrift f. Wiss. Zoologie,
1874) nas demonstrated its presence in the ova of many Siphonophorire and Medusae.
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 fur Mikr.
Anat., Vol. Vlll.) 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.
FORMATION OF THE LAYERS. 267
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 (PI. 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
haematoxylin, 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 some-
what 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, con-
sisting 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 parti}- from the formation of cells around the
nuclei of the yolk.
1 8— 2
268 DEVELOPMENT OF ELASMOBRANCH FISHES.
Shortly after the floor of cells has appeared, the whole seg-
mentation cavity becomes obliterated.
When the embryonic rim has attained to some importance,
the position of the embryo becomes marked out by the appear-
ance of the medullary groove at its most projecting part. The
embryo extends from the edge of the blastoderm inwards to-
wards 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 hypo-
blast 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 hypo-
blast, 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 Gegenbaur1 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 His2 and to a very
modified extent by Waldeyer3, and has recently been attacked
from an entirely new standpoint by Gotte4; but, to my mind,
the objections of these authors do not upset the well founded
conclusions of previous observations.
1 "Wirbelthiereier mit partieller Dottertheilung." Miiller's Arch. 1861.
'2 Erste Anlage des Wirbelthierleibes .
3 Eierstock u. Ei.
4 Entwicklungsgeschichte der Unke. The important researches of Gotte on the
development of the ovum, though meriting the most careful attention, do not admit of
discussion in this place.
FORMATION OF THE LAYERS. 269
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 rrratvner
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 Cephalopoda1, and of
Dr Gotte2 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.
The observations of Dr Gotte 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 develop-
ment of Elasmobranchs3, 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 develop-
ment of the Elasmobranch ovum ; and then to discuss how far
the facts of the growth of the blastoderm in Elasmobranchs
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.
Taking for granted that the ripe ovum is a single cell, the
1 Annals and Magaz. of Natural History, Vol. xi. 1873, p. 81.
2 Archivf. Mikr. Anat. Vol. X.
3 Quart. Journ. of Micr. Science, Oct. 1874.
270 DEVELOPMENT OF ELASMOBRANCH FISHES.
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, com-
posed 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 holoblas-
tic 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 con-
stituents.
My own observations in conjunction with the specially inte-
resting observations of Dr Schultz1 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 through-
out the whole yolk, is present both before and after impregna-
tion.
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 Elasmobranchs 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 Elasmobranchs, must be considered
as a proof of the homology of the yolk cells in the first case
1 Archivf. Mikr. Anat. Vol. xxi.
FORMATION OF THE LAYERS. 2/1
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 proto-
plasm than they do in the Amphibian ovum. As I have suggested
elsewhere1, 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, seg-
mentation becomes slower, and the resulting segments larger
and larger.
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 paper2 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.
In the wood-cut, fig. I A, B, C3, are represented three dia-
grammatic 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 wood-cuts 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. i 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
1 "Comparison," &c., Quart. Journ. Micr. Science, July, 1875. [This Edition,
No. VI.]
- Loc. cit.
'•' This figure, together with figs. 2 and 3, are reproduced from my paper upon the
comparison of the early stages of development in vertebrates.
2/2
DEVELOPMENT OF ELASMOBRANCH FISHES.
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
FIG. i.
Diagrammatic longitudinal sections of an Elnsmobranch 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 dis-
tinctly 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.
FORMATION OF THE LAYERS.
273
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. «. nuclei of the yolk.
The stages A , B and C are the same as in figure .
274 DEVELOPMENT OF ELASMOBRANCH FISHES.
FIG. 3.
Diagrammatic longitudinal sections of Bombinator igneus. Reproduced with modi-
fications from Gotte.
Epiblast without shading. Mesoblast black with clear outlines to the cells. Lower
layer cells and hypoblast with simple shading.
ep, epiblast. /./. 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 Gotte'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.
FORMATION OF THE LAYERS. 275
enclosed by smaller cells (in the diagram) which correspond
exactly in function and position with the lower layer cells of the
Elasmobranch blastoderm.
The relation of the yolk to the blastoderm in theJElasmo-
branch 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. I and 2 B and
PI. 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 hypo-
blast 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 Elasmo-
branch 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 (Elasmo-
branch) are nearly identical with those of the yolk cells to the
blastoderm in the other (Amphibian). The mam features in
which'the two embryos differ, during the stage under considera-
tion, arise from the same cause as the solitary point of differ-
ence during the preceding stage.
2/6 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Elasmobranchs, 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 segmenta-
tion, 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 invagi-
nation 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: — (i) 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 hypo-
blast, which gradually extends backwards towards the segmenta-
tion 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 Cyclo-
stomes, Amphibians, Elasmobranchs 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 invagi-
nation, 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,
FORMATION OF THE LAYERS. 277
which have been worked out in some detail in my paper already
quoted1.
Prof. Haeckel, in a paper recently published2, appears to
imply that because I do not find absolute invagination in
Elasmobranchs, I therefore look upon Elasmobranchs~as~ mili-
tating against his Gastraea theory. I cannot help thinking that
Prof. Haeckel must have somewhat misunderstood my meaning.
The importance of the Gastraea 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
meanings3 — 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.
Professor Haeckel4 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 own5 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.
The following is Professor Haeckel's own statement of the
scheme or type, which he regards as characteristic of mero-
blastic eggs, pp. 98 and 99.
Jetzt folgt der hochst wichtige und interessante Vorgang, den ich als
Einstiilpung der Blastula auffasse und der zur Bildung der Gastrula
fiihrt (Fig. 63, 64) 6. Es schlagt sich niimlich der verdickte Saum der Keim-
scheibe, der " Randwulst " oder das Properistom, nach innen um und eine
diinne Zellenschicht wachst als directe Fortsetzung desselben, wie ein immer
1 Quart. Journ. of Micr. Science, July, 1875. [This Edition, No. VI.]
2 " Die Gastrula u. Eifurchung d. Thiere," Jenaische Zeitschrift, Vol. IX.
3 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.
4 IM. fit. 5 Loc. clt.
6 The references in this quotation are to the figures in the original.
2/8 DEVELOPMENT OF ELASMOBRANCH FISHES.
enger werdendes Diaphragma, in die Keimhohle hinein. Diese Zellen-
schicht ist das entstehende Entoderm (Fig. 64 z, 74 z). Die Zellen, welche
dieselbe zusammensetzen und aus dem innern Theile des Randwulstes her-
vorwachsen, sind viel grosser aber flacher als die Zellen der Keimhohlen-
decke und zeigen ein dunkleres grobkorniges Protoplasma. Auf dem Boden
der Keimhohle, d. h. also auf der Eiweisskugel des Nahrungsdotters, liegen
sie unmittelbar auf und riicken hier durch centripetale Wanderung
gegen dessen Mitte vor, bis sie dieselbe zuletzt erreichen und nunmehr eine
zusammenhangende einschichtige Zellenlage auf dem ganzen Keimhohlen-
boden bilden. Diese ist die erste vollstandige Anlage des Darmblatts,
Entoderms oder " Hypoblasts", und von nun an konnen wir, im Gegen-
satz dazu den gesammten iibrigen Theil des Blastoderms, namlich die
mehrschichtige Wand der Keimhohlendecke als Hautblatt, Exoderm
oder " Epiblast " bezeichnen. Der verdickte Randwulst (Fig. 64 w, 74 w],
in welchem beide primare Keimblatter in einander iibergehen, besteht in
seinem oberen und ausseren Theile aus Exodermzellen, in seinem unteren
und inneren Theile aus Entodermzellen.
In diesem Stadium entspricht unser Fischkeim einer Amphiblastula,
welche mitten in der Invagination begrififen ist, und bei welcher die
entstehende Urdarmhohle eine grosse Dotterkugel aufgenommen hat. Die
Invagination wird nunmehr dadurch vervollstandigt und die Gastrula-
bildung dadurch abgeschlossen, dass die Keimhohle verschwindet. Das
wachsende Entoderm, dem die Dotterkugel innig anhangt, wolbt sich in
die letztere hinein und nahert sich so dem Exoderm. Die klare Fliissigkeit
in der Keimhohle wird resorbirt und schliesslich legt sich die obere convexe
Flache 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
gefiittertes Miitzchen fast die ganze obere Hemisphere der hyalinen Dot-
terkugel eng anliegend bedeckt (Fig. 65). Der Ueberzug des Miitzchens
entspricht dem Exoderm (*>), sein Futter dem Entoderm (z). Ersteres
besteht aus drei Schichten von kleineren Zellen, letzteres aus einer einzigen
Schicht von grosseren Zellen. Die Exodermzellen (Fig. 77) messen 0,006 —
0,009 Mm., und haben ein klares, sehr feinkorniges Protoplasma. Die
Entodermzellen (Fig. 78) messen 0,02 — 0,03 Mm. und ihr Protoplasma ist
mehr grobkornig und triiber. Letztere bilden auch den grossten Theil des
Randwulstes, den wir nunmehr als Urmundrand der Gastrula, als
" Properistoma " oder auch als " RuscbNl'schen After" bezeichnen kon-
nen. Der letztere umfasst die Dotterkugel, welche die ganze Urdarm-
hohle ausfullt und weit aus der dadurch verstopften Urmund-Oeffnung
vorragt.
My objections to the view so lucidly explained in the passage
just quoted, fall under two heads.
FORMATION OF THE LAYERS. 279
(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 Ihese
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 Elasmobranchs the hypoblast cells occupy, even
before the close of segmentation, the position which, on Pro-
fessor Haeckel's view, they ought only eventually to take up
after being involuted from the whole periphery of the blasto-
derm.
(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 segmenta-
tion 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 asym-
metry of the blastoderm ; an asymmetry which is unquestion-
ably 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 Pro-
fessor Haeckel rests his views, are too much disputed, for their
280 DEVELOPMENT OF ELASMOBRANCH FISHES.
discussion in this place to be profitable1. 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 dis-
tinguish 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 ancestors2. This dis-
appearance 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.
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
Gotte, or the views of Professor Haeckel3.
Apart from disputed points of development, it appears to me
that a comparative account of the development of the meroblastic
1 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 Elasmobranchs. Kowalevsky says,
Arch. f. Mikr, Anat. Vol. vn. 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.
2 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.
3 I find myself unable without figures to understand Dr Rauber's (Centralblatt
fur 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 tfnckened 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.
FORMATION OF THE LAYERS. 28 1
vertebrate ova ought to take into consideration the essential differ-
ences 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 second1.
This difference entails important modifications in develop-
ment, 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 Elasmobranchs and Osseous
Fishes a true anus of Rusconi, or primitive opening into the
alimentary canal, which is absent in Birds. Yet in neither
Elasmobranchs2 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 Birds3.
Owing also to the respective situations of the embryo in the
1 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 PI. 9, fig. i, 2). Assuming this to be the real expla-
nation 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 struc-
ture 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 formations 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 Elasmobranchs. 1
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.
3 Vide p. 296 and Plate 9, fig. r and 2, and Self, "Comparison," &c., loc. cit.
3 The relation of the anus of Rusconi and blastopore in Elasmobranchs 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.
B. IQ
282 DEVELOPMENT OF ELASMOBRANCH FISHES.
blastoderm, the alimentary and neural canals communicate
posteriorly in Elasmobranchs 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 Gotte's researches in Mammalia is completely cut
away by the recent discoveries of Van Beneden1 and Hensen2.
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 ' segmenta-
tion3. 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 inva-
gination, 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.
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 holo-
blastic ova, and thus destroy one of the most important results
of the Gastraea 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 unseg-
mented food-yolk a fresh element is added to the ovum, it
1 " Developpement Embryonnaire des Mammiferes, " Bulletin de I 'A cad. r. d.
Belgique, 1875.
2 Loc. cit.
3 For an explanation of these terms, vide Prof. Haeckel's original paper or the
abstract in Quart. Journ. of Micr. Science for January, 1876.
FORMATION OF THE LAYERS. 283
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 imagination
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 Gastraea 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 Gastrasa theory in its general bearings.
Observations upon the formation of the layers in Elasmo-
branchs have hitherto been very few in number. Those published
in my preliminary account of these fishes are, I believe, the
earliest1.
Since then there has been published a short notice on the
subject by Dr Alex. Schultz2. 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.
1 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.
2 Centralblatt f. Med. Wiss. No. 33, 1875.
IQ — 2
284 DEVELOPMENT OF ELASMOBRANCH FISHES.
EXPLANATION OF PLATE 7.
COMPLETE LIST OF REFERENCE LETTERS.
c. Cells formed in the yolk around the nuclei of the yolk. ep. Epiblast. er. Em-
bryonic ring. es. Embryo swelling, hy. Hypoblast. //. Lower layer cells, ly. Line
separating the yolk from the blastoderm, m. Mesoblast. mg. Medullary groove.
;/'. Nuclei of yolk. na. Cells to form ventral wall of alimentary canal which have
been derived from the yolk, n al. 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. r. Longitudinal section of a blastoderm at the first appearance of the seg-
mentation cavity.
Fig. i. 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. i 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 (i) 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 appear-
ance 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 PI. 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 PI. 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.
FORMATION OF THE LAYERS. 285
Figs. 8 a, Sl>, 8r. Three sections of the same embryo. Inserted mainly to illus-
trate 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 l>, from the anterior part of the embryo, the main mass oLmegpblast
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^ and 8c 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, loa, lob, loc. 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.
ic-tf. The most posterior of the three sections. It shews the posterior flatness
of the medullary groove and the two isolated vertebral plates.
lob. 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.
\oc shews the disappearance of the medullary groove and the thinning out of
the mesoblast plates in the region of the head.
Fig. ii. Small portion of the blastoderm and the subjacent yolk of an embryo at
the time of the first appearance of the medullary groove x 300. It shews two large
nuclei of the yolk (») 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. ii. 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 forma-
tion of cells around the nuclei of the yolk.
Fig. 14. Section through part of a young Scyllium egg, about tVtn of an inch in
diameter.
«/. Protoplasmic network in yolk. zp. Zona pellucida. eh. Structureless
chorion. fcp. 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. Un-
fortunately 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 here-
after 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
GENERAL FEATURES. 287
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 formsjpart 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 liead fold, and
those at the sides the side folds. There is in Elasmobranchs
no tail fold, owing to the position of the embryo at the peri-
phery 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 indica-
tion 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 develop-
ment, and consist of two large aggregations of mesoblast cells.
288 DEVELOPMENT OF ELASMOBRANCH FISHES.
In accordance with the nomenclature adopted in my preliminary
paper1, 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.
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
1 Quart. Jour it. Micr. Science, Oct. 1874. [This Edition, No. V.]
GENERAL FEATURES. 289
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 dis-
appearance 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 protovertebrae 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
2QO DEVELOPMENT OF ELASMOBRANCH FISHES.
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 («/.) 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 repre-
sented 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 (pp^) 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 (/;/.).
GENERAL FEATURES. 2QI
The fore and hind guts are now longer than they were. A
slight pushing in from the exterior to form the mouth has
appeared (/«.), 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 move-
ments 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-brain1 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.
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
1 The part of the brain which I have here called mid-brain, and which unquestion-
ably 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.
2Q2 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 in-
creased. 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 trans-
parent 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, com-
paratively 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 com-
pletely 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
GENERAL FEATURES. 293
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 meso-
blast 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 never-
theless 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
294 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 com-
menced 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 mandi-
bular 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 Elasmobranchs but even of the
genus Scyllium.
GENERAL FEATURES. 295
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 distinct-
ness 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
296 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 con-
spicuous feature (PI. 9, fig. i). 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 PI. 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. Through-
out 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 (PI. 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 Elasmobranchs is the fact of its not corresponding in position
with the opening of the anus of Rusconi. We thus have in
Elasmobranchs 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 Elas-
mobranchs coincide in position. It is the blastopore of Elasmo-
branchs 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 situation1.
1 For a fuller discussion of this question vide Self, " A comparison of the early
stages of development in vertebrates." Quart. Journ. of Micr. Science, ]u\y, 1875.
[This Edition, No. VI.]
GENERAL FEATURES. 297
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.
au v. Auditory vesicle, bl. Blastoderm, ch. Notochord. es. Embryo-swelling, h.
Head. ht. Heart. ;«. Mouth, mg. Medullary groove, mp. Muscle-plate or proto-
vertebra. op. Eye. s c. Segmentation cavity, so s. Somatic stalk, is. Tail-swelling.
v. Veins of yolk sac (blue), vc. Visceral cleft. I.vc. ist 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. i . 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 thick-
ened 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.
Eig- 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.
B. 20
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 medul-
lary 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 inter-
mediate between B and C, the epiblast is composed of a single
layer of cells. (PI. 10, fig. i.)
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 con-
dition 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 un-
dergo any important change, with the exception of the layer
STAGES B TO G. MEDULLARY GROOVE. 299
becoming much thickened, and its cells two or three deep in the
anterior parts of the embryo. (PI. 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 arrange-
ment, 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 epi-
blast 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. (PI. 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. (PI. 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, PI.
10, figs. 3^, 3*?, 3/; but the anterior flattened area in the last
stage has grown into a round flat plate which may be called the
cephalic plate, PI. 8, D and PI. IO, 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
20 — 2
300 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 PI. 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
(PI. 8, fig. F), while the groove is still widely open elsewhere1.
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.
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 PI. 10, fig. 6, a section taken
through the posterior part of the cephalic plate), and the en-
larged 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 ob-
served in other groups.
The medullary canal in Elasmobranchs 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
1 Vide Preliminary Account, etc. Q. Jl. Micros. Science, Oct. 1874, PI. 14, 8 a.
[This Edition, No. V. PI. 3, 8a.] 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.
STAGES B TO G. MESOBLAST. 301
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 how-
ever 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 (PI. 10, fig. 3), a splanchnic layer adjoining the
hypoblast (sp), and a somatic layer adjoining the epiblast1 (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.
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 con-
tinuous 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.
1 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.
302 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 pro-
tovertebrae. 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
protovertebra, 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 protovertebrae 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 PI. 8, figs. D, F, and PI. 10, fig. 3/and fig. 4 ts.
These masses of mesoblast are neither divided into proto-
vertebrae, nor do they exhibit any trace of a commencing dif-
ferentiation 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
protovertebrse. 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 considera-
tions with reference to it I propose reserving till I have described
the changes which it undergoes in the subsequent periods.
PI. 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
STAGES B TO G. ALIMENTARY CANAL. 303
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 U) 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 Oellacher1 for the Trout : but he believes that
the cavity in this part is solely related to the formation of the
pericardial space.
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 (PI. 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 protovertebrae are present
both in Pristiurus and Torpedo embryos.
The A limentary 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
(PI- 7, %. 7).
1 Zeitschrift f. iviss. Zoologie, 1873.
304 DEVELOPMENT OF ELASMOBRANCH FISHES.
The cavity anteriorly has a more or less definite form, having
lateral walls, as well as a roof and floor (P.I. 7, figs. iQb and ioc\
Posteriorly it is not nearly so definitely enclosed (PL 7, fig. io«).
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 (PI. 10, figs. 2b and 2c}. 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 (PI. 10, fig. 2) ; and, finally, in front, it forms a definite space
completely closed in on all sides by cells (PL 10, fig. 2.0). 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
STAGES B TO G. ALIMENTARY CANAL. 305
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 Elasmobranchs.
The fact of this feature being common to the yolk-cells of
Amphibians and the yolk of Elasmobranchs, supplies a strong
argument in favour of the homology of the yolk-cells in the one
case with the yolk in the other1.
1 Nearly simultaneously with Chapter III. of the present monograph on the
Development of Elasmobranchs, which dealt in a fairly complete manner with the
genesis of cells outside the blastoderm, there appeared two important papers dealing
wilh the same subject for Teleostei. One of these, by Professor Bambeke, " Em-
bryologie des Poissons Osseux," Mem. Cour. Acad. Belgique, 1875, which appeared
some little time before my paper, and a second by Dr Klein, Quart, your, 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 observa-
tions 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 Elasmobranchs, 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 (i) that in Osseous Fish there is a
gradation between the two substances, while (2) in Elasmobranchs 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 pheno-
menon 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
3O6 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 (PI. 10,
fig. 3«). 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
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 ex-
tending 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, PI. ro, 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 pro-
duced 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.
STAGES B TO G. ALIMENTARY CANAL. 307
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 PI.
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 Elasmobranchs, 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 Goette1 in Amphibians and by Kowalevsky, Owsjannikow
and Wagner2 in the Sturgeon (Acipenser). The same arrange-
ment is also stated by Kowalevsky8 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 Marsipo-
branchii.
The Reptilia, Aves, and Mammalia have usually been dis-
tinguished 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
1 Eniwicklungsgeschichte der Unke.
- Melanges Biologiques de F Acadhnie Ptiersbourg, Tome vil.
3 Archiv. f. mikros. Anat. Vol. vn. p. 114. In the passage on this point
Kowalevsky states that in Elasmobranchs the neural and alimentary canals com-
municate. This I believe to be the first notice published of this peculiar arrangement.
308 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 abbre-
viation the embryo Bird occupies from the first a central position
in the blastoderm1.
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.
1 Vide Note on p. 281, also p. 295, and PI. 9, Figs, i 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 em-
bryo, and the Note on p. 281 con tains- 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 blas-
toderm 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.
STAGES B TO G. THE NOTOCHORD. 309
The Notochord.
One of the most interesting features in the Elasmobranch
development is the formation of the notochord from the 4iypo-
blast. 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 (PI. 10, fig. I c, ch') a slight thickening is
to be observed in the hypoblast, immediately below the medul-
lary 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 (PI. 10,
fig. i 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
(PI. 10, fig. i a), and in some cases is barely visible except with
high powers.
From the series of sections represented, it is clear that the
3IO DEVELOPMENT OF ELASMOBRANCH FISHES.
notochord commences to be separated from the hypoblast an-
teriorly, 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 hsematoxylin. I conclude from its subsequent history,
that it is to be regarded as a product of the cells of the noto-
chord, 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 longi-
tudinal 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 ' on the development of the Elasmobranch fishes.
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 develop-
ment 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
1 Loc. tit.
STAGES B TO G. THE NOTOCHORD. 3 1 I
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 state-
ments 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 ob-
jections as the view that the notochord has only apparently a
hypoblastic source in Elasmobranchs, and, provisionally at least,
the first of them ought to be accepted. The reasons for ac-
cepting 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 Hensen1,
on the development of the notochord in Mammalia, render it
very probable that, in this group, the notochord is developed
from the hypoblast.
Hensen finds that in Mammalia, as in Elasmobranchs, the
mesoblast forms two independent lateral masses, one on each
side of the medullary canal.
After the commencing formation of the protovertebrse the
hypoblast becomes considerably thickened beneath the medul-
1 Zeitschrift f. Anat. u. Entwicklun&geschichte, Vol. I. p. 366.
312 DEVELOPMENT OF ELASMOBRANCH FISHES.
lary groove ; and, though he has not followed out all the steps of
the process by which this thickening is converted into the noto-
chord, 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 Lieberkuhn \ 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.
Lieberkuhn gives no further statements or figures, and it is
clear that, even if there is present the delicate layer of meso-
blast, which he fancies he has detected, yet this cannot in any
way invalidate such a section as that represented on PI. X. fig.
40, of Hensen's paper.
In this figure of Hensen's, the hypoblast cells become dis-
tinctly more columnar, and the whole layer much thicker im-
mediately below the medullary canal than elsewhere, and this
independently of any possible layer of mesoblast.
It appears to me reasonable to conclude that Lieberkiihn'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 2.
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
1 Sits, der Gesell. zu Marburg, Jan. 1876.
a 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.
STAGES B TO G. THE NOTOCHORD. 313
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.
a/. Alimentary canal, ch. Chorda dorsalis or notochord. ch'. Ridge of hypoblast,
which will become separated off as the notochord. ep. Epiblast. Ay. Hypoblast.
//. Coalesced lateral and vertebral plate of mesoblast. m g. Medullary groove.
«. Nucleus of yolk. n a. Cells formed around the nuclei of the yolk to enter into the
ventral wall of the alimentary canal, n c. Neural or medullary canal. / v. Proto-
vertebra. so. Somatopleure. sp. Splanchnopleure. t s. Mesoblast of tail-swelling.
yk. Yolk-spherules.
Figs, i a, i b, i c. Three sections from the same embryo belonging to a stage
intermediate between B and C, of which fig. i a is the most anterior, x 96 diameters.
The sections illustrate (i) The different characters of the medullary groove in the
different regions of the embryo. (2) The structure of the coalesced lateral and verte-
bral 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 (i 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, ib, ic. 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.
x 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, $f. Sections of the same embryo as fig. 3 ( x 60 dia-
meters). Fig. 3 belongs to part of the embryo intermediate between figs. 3^ and %f.
The sections shew the features of various parts of the embryo. Figs. 30, 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/to the tail.
Fig. 4. Section through the region of the tail at the commencement of stage F.
x 60 diameters.
The section shews the character of the tail-swellings and the commencing closure
of the medullary groove.
B. 21
3 14 DEVELOPMENT OF ELASMOBRANCH FISHES.
Fig. 5. Transverse section through the anterior part of the head of an embryo
belonging to stage F ( x 60 diameters). It shews (i) 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. x 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 proto-
vertebrse 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 develop-
ment ; 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 differentia-
tion 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 arrange-
ment 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 epiblast1 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 differentia-
tion into nervous and epidermic layers. (PL 11, figs, i — 5.)
1 Unless the contrary is stated, the facts recorded in this chapter apply only to
the genera Scyllium and Pristiurus.
21 — 2
316 DEVELOPMENT OF EL AS MOB RANCH FISHES.
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. (PI. n, 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. (PI. 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.
STAGES G TO K. THE EXTERNAL EPIBLAST. 317
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 cells1.
The history of the epiblast in Elasmobranchs 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
Elasmobranchs present the strongest contrast in the develop-
ment 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 Strieker 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 distinguished2, 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
together3, 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
1 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 Uebcr attgcmrine Bedeckungen der Amphibien, p. 20. Bonn,
.1876.
2 Vide Leydig, loc. at.
:t Vide Gotte, Entwicklungsgeschichte der Unke,
3l8 DEVELOPMENT OF ELASMOBRANCH FISHES.
of the epidermis, while this layer also has the greater share in
forming the olfactory sac.
In Elasmobranchs 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 Amphi-
bians. 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 equiva-
lent parts of the epidermis in Elasmobranchs 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
Elasmobranchs, 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: (i) 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 develop-
ment, and then to re-appear 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
STAGES G TO K. THE FINS. 319
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 it1.
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 consider-
ably, 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 un-
paired fins.
Similar thickenings to those in Elasmobranchs are found at
the ends of the limbs in the embryos of both Birds and Mammals,
in the form of caps of columnar epiblast2.
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
1 Vide Self, "Development of Spinal Nerves in Elasmobranchs." Phil. Transact.
1876. [This Edition, No. VIII.]
2 For Birds, vide Elements of Embryology, Foster and Balfour, pp. 144, 145, and
for Mammals, Kolliker, Entwicklungsgesehichte, p. 283.
320 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 (PI. n, 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
STAGES G TO K. THE PAIRED FINS. 321
to that of the dorsal fins. There appears a lateral linear thick-
ening of epiblast, which however does not, like the similar
thickening of the fins, grow into a distinct fold. Its develop-
ment 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 Elasmo-
branchs, 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 adopted1.
My researches throw no light on the nature of the skeletal
parts of the limb, but the suggestion which has been made by
Giinther* 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.
Dr Dohrn8 in speaking of the limbs, points out the difficulties
1 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.
2 Philosophical Transactions, 1871.
8 Ursprung d. Wirbelthierc and Functionnvechsels.
322 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Gegenbaur1.
Dr Dohrn has not as yet given the grounds for his determina-
tion, so that any judgment on his views is premature.
None of my observations on Elasmobranchs lends any sup-
port 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 Dohrn2, cannot be used
as an argument against limbs having existed in still more
primitive Vertebrates.
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 be-
tween them a space which constitutes the commencement of the
body-cavity (PI. 10, fig. i). From the very first this cavity is
more or less clearly divided into two distinct parts ; one of them
1 Grundriss d. Vergleichenden Anat. p. 494.
2 Loc. cit.
STAGES G TO K. THE MESOBLAST. 323
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 verte-
bral 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 (proto-
vertebras), 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 protovertebrae. The cavity
in each of the protovertebrae is formed of a narrowed dorsal and
a dilated ventral segment, the latter on the level of the dorsal
aorta (PI. n, 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.
Protovertebrce. Each protovertebra1 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 protovertebrae 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 proto-
plasm.
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, under-
1 No attempt has been made to describe in detail the different appearances
presented by the protovertebrae in the various parts of the body, but in each stage a
protovertebra from the dorsal region is taken as typical.
324 DEVELOPMENT OF ELASMOBRANCH FISHES.
going peculiar changes. These changes are indicated in trans-
verse 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
(PI. 12, fig. 10) that the cells in this situation have become elong-
ated 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 (PI.
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 re-
maining cells of the protovertebrae. 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 protovertebra are at first per
fectly 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 (PI. n, 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
STAGES G TO K. THE PROTOVERTEBR^E. 325
seen both in transverse and longitudinal sections, and form the
commencing vertebral bodies (PI. u, fig. 6, and PI. 12, figs. IO
and 1 1 Vr}.
At first the vertebral bodies have the same segmentation as
the protovertebrae 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 protoverte-
brae. They have therefore at their first appearance a segmentation
completely different from that which they eventually acquire
(PI. 12, fig. ii).
After the separation of the vertebral bodies from the proto-
vertebrae, the remaining parts of the protovertebrae 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 PI. 12, fig. 17 nip.
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 (PI. u, figs.
7 and 8).
Between stages I and K the bodies of the vertebrae rapidly
326 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 how-
ever 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 PI. 12, fig. 12 pr.
Intermediate Cell-mass. At about the period when the
muscle-plates become completely free, a fusion takes place be-
tween the somatopleure and splanchnopleure immediately above
the dorsal extremity of the true body-cavity (PL n, 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 urino-genital 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 (i) 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
STAGES G TO K. THE BODY-CAVITY. 327
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 alimen-
tary 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 (PI. n, 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 (PI. 11, fig. i). At the caudal swelling the meso-
blast plates cease to be distinctly divided into somatopleure and
splanchnopleure, and more or less fuse with the hypoblast of the
caudal vesicle (PI. n, 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 every-
where, is formed of two independent lateral halves (PI. 1 1, fig. 90).
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 (PI. n, fig. 8) suspended by a very
short mesentery.
328 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 PI. n, 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 exami-
nation of longitudinal horizontal sections from an embryo be-
longing 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 (PI. 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
STAGES G TO K. THE MESOBLAST. 329
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
(PI. u, fig. 8). Towards the end of stage K, however, there
appears between the two a network of mesoblastic cells connect-
ing 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 hypo-
blastic epithelium of the alimentary tract are fairly numerous
(PI. 1 1, fig. 8), and by the close of this period become concentric-
ally 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 (PI. u, figs, gc, Qd\
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 protovertebrae and body-cavity ap-
plies 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 proto-
vertebrae 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
B. 22
33O DEVELOPMENT OF ELASMOBRANCH FISHES.
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 splanch-
nic 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 (tnp'} 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 pre-
cisely 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 connect-
ing 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.
Resumt. 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 proto-
vertebrae 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 separa-
tion 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 com-
posed 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 rudi-
STAGES G TO K. RESUME. 33 l
ments of the vertebral bodies which are originally segmented
in the same planes as the protovertebrae. The plates themselves
remain as the muscle-plates and develop a special layer of
muscle (mp1) 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 Elasmobranchs and in other Vertebrates, in order
to distinguish as far as possible the primitive and the secondary
characters present in the various groups.
22 — 2
332 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Hensen1, present numerous
remarkable approximations to the Elasmobranchs. We find ac-
cordingly2 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 Elasmo-
branchs.
In Birds3 the horizontal splitting of the mesoblast into
somatic and splanchnic layers appears, as in Mammals, to extend
at first to the summit of the protovertebrae, 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 protovertebrae is
continuous with the somatic layer of the lateral plates, and the
inner layer and kernel of the protovertebrae with the splanchnic
layer of the lateral plates4. After the isolation of the proto-
vertebrae the primitive position of the split which separated
their somatic and splanchnic layers becomes obscured, but when
1 Zeitschriftf. Anat. Ent-wicklungsgeschichte, Vol. I.
8 Hensen loc. cit.
3 For the history of protovertebrae 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.
4 Vide Elements of Embryology, p. 56.
STAGES G TO K. GENERAL CONSIDERATIONS. 333
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 Dar- .
winian 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 Elasmo-
branchs. The two layers of the muscle-plate also correspond
with the two layers present in Elasmobranchs, the one belonging
to the somatic, the other to the splanchnic layer of mesoblast.
The remainder of the protovertebrae internal to the muscle-plates
is very large in Birds, and is the equivalent of that portion of the
protovertebrae which in Elasmobranchs is split off to form the
vertebral bodies1 (PI. 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 Elasmobranchs, 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 Elasmobranchs.
According to the statements of Bambeke and Gotte, the
Amphibians present rather remarkable peculiarities in the develop-
ment 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 (protovertebrae) 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
1 Dr Gbtte, Enlwicklungsgeschichte der Unke, p. 534, gives a different account of
the development of the protovertebrse from that in the text. He states that the
muscle-plates do not give rise to the main dorso-lateral muscles, hut only to some
superficial ventral muscles, while the dorso-lateral muscles are according to him formed
from part of the kernel of the protovertebrae 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 Kolliker, Entiuicklungsgeschichte, 1876.
334 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Elasmo-
branchs. 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 Gotte appears to think that the vertebral plates in Am-
phibians present a perfectly normal development very similar
to that of other Vertebrates. The divergences between Am-
phibians and other Vertebrates appear, however, to myself, to be
very great, and although the very careful account given by Dr
Gotte 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, Elasmo-
branchs and Mammals. In the subsequent development, how-
ever, a great difference between the types becomes apparent, for
whereas in Elasmobranchs 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 Elas-
mobranchs, converted into the special early formed band of
muscles (m.p'.}, rather than, as their development seems to
indicate, with the whole Elasmobranch muscle-plates1.
1 The type of development of the muscle-plates of Amphibians would become
identical with that of Elasmobranchs if their first-formed mass of muscle corresponded
with the early-formed muscles of Elasmobranchs, and the remaining cells of both
layers of the protovertebrse became in the course of development converted into
muscle-cells indistinguishable from those formed at first. Is it possible that, owing
(o the distinctness of the first-formed mass of muscle, Dr Gotte can have overlooked
DERIVATION OF THE MESOBLAST. 335
Osseous Fishes are stated to agree with Amphibians in the
development of their protovertebrae and muscular system1, but
further observations on this point are required.
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
sub-kingdom, yet the comparison which has been instituted
between Elasmobranchs 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 in-
herited from the ancestors of Vertebrates. These features are
(i) 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 primi-
tively only two embryonic layers were present — the epiblast
and the hypoblast — and that the mesoblast subsequently ap-
peared as a distinct layer, after a certain complexity of organiza-
tion 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 meso-
blast. 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,
the fact that its subsequent growth is carried on at the expense of the adjacent cells
of the somatic layer ?
1 Ehrlich, "Ueber den peripher. Theil d. Urwirbel." Archiv f. Mic. Anat,
Vol. XI.
336 DEVELOPMENT OF ELASMOBRANCH FISHES.
(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 Ccelenterata, and we might almost
say by that of this group only1.
Amongst the Ccelenterata 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 d 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 embry-
ologist as Professor Haeckel, and it must be admitted, that on
d 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 The most important other instances in addition to that of the Ccelenterata 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 Kblliker 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,
DERIVATION OF THE MESOBLAST. 337
(1) From the fact that some investigators derive the meso-
blast 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 deriva-
tion of the mesoblast in Amphioxus from .both epiblast and
hypoblast. Kowalevsky's account (on which apparently Prof.
Haeckel's1 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.
(3) Professor Haeckel's own observations on the develop-
ment 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 primi-
tive streak has, however, according to my views, quite another
significance to that attributed to it by Professor Haeckel2; but
in any case Professor Kolliker'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.
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
1 Vide Anthropogenie, p. 197.
* Vide Self, " Development of Elasmobranch Fishes," Journal of Anat. and Phys.
Vol. X. note on p. 682, and also Review of Professor Kolliker's " Entwicklungs-
geschichte des Menschen u. d. hoheren Thiere," Journal of Anat. and Phys. Vol. x.
338 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Elasmobranchs
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 origin1.
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 dis-
crepancy 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
1 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.
TAiere), 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.
DERIVATION OF THE MESOBLAST. 339
it is very difficult to understand how there could be formed from
it a part of the voluntary muscular system of the body in-
distinguishably 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 .mus-
cular system is formed from the splanchnic layer of the meso-
blast, 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 a 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 Ver-
tebrates1" a short resume 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, Gotte),
Nematodes (Blitschli), Sagitta (Kowalevsky, Biitschli), Lum-
bricus and probably other Annelids (Kowalevsky), Brachiopoda
(Kowalevsky), Crustaceans (Bobretzky), Insects (Kowalevsky,
Ulianin, Dohrn), Myriapods (Metschnikoff), Tunicates (Kowa-
levsky, Kuppfer), Petromyzon (Owsjanikoff), Osseous fishes
(Oellacher, Gotte, Kowalevsky), Elasmobranchs (Self), Amphi-
bians (Remak, Strieker, Gotte).
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 Ccelenterates has been already explained
and my grounds for regarding the Amniotic Vertebrates as
1 Quart. JL of Micros. Science, July, 1875. [This Edition, No. vi.J
340 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Rabl1, who seems recently to have studied the develop-
ment of Lymnseus 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 Lankester2 and Dr
Fol3 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 Bobretzky4. 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.
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 Con-
sideration. The most important of these are the Echinoderms,
Brachiopods and Sagitta.
In the Echinoderms the mesoblast is in part formed by cells
budded ofif 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 skeleton5. The diverticula
1 Jcnaische Zeitschrift, Vol. IX.
2 Quart. Jl. of Micros. Science, Vol. xxv. 1874, and Phil. Trans. 1875.
1 Archives de Zoologie, Vol. IV.
4 Archiv f. Micr. Anat. Vol. xm.
5 The recent researches of Selenka, Zeitschrift f. Wiss. Zoologie, Vol. xxvn. 1876,
demonstrate that in Echjnoderrns the muscles are derived from the cells first split off
DERIVATION OF THE MESOBLAST. 34!
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
epWtelium of the alimentary tract. Though this fundamental
arrangement would seem to be universal amongst Echinoderms,
considerable variations of it are exhibited in different groups.
There is one outgrowth from the alimentary tract in Sy-
napta; two in Echinoids, Asteroids and Ophiura; three in
Comatula, and four (?) in Amphiura. The cavity of the out-
growth 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 Sagitta1 the formation of the mesoblast and the ali-
mentary 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 tfie mesoblast
of the somatopleure. The central division of the primitive
gastraea cavity remains as the alimentary tract of the adult.
The remarkable observations of Kowalevsky* on the devel-
opment of the Brachiopoda have brought to light the unexpected
fact that in two genera at least (Argiope and Terebratula) the
mesoblast and body-cavity develope as paired constrictions from
from the hypoblast, and that the diverticula only form the water-vascular system and
the epithelial lining of the body-cavity.
1 Kowalevsky, " Wiirmer u. Arthropoden," Mem. Acad. Petersbourg, 1871.
* "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, Jahres-
btricht f. 1873.
342 DEVELOPMENT OF ELASMOBRANCH FISHES.
the alimentary tract in a manner almost identically the same as
in Sagitta.
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 suggested1 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 con-
tractile 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 ali-
mentary 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.
An attempt has been already made to shew that the meso-
blast in Elasmobranchs is formed in a very primitive fashion,
and for this reason the Elasmobranchs appear to be especially
adapted for determining whether any signs are exhibited of a
derivation of the mesoblast as paired diverticula of the ali-
mentary 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.
1 Comparison of Early Stages, Quart. Jl. Micros. Science, July, 1875. [This
Edition, No. vi.]
DERIVATION OF THE MESOBLAST. 343
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 tlie mtiscle- 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 splanchno-
pleure 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
Elasmobranchs, which favour the view of its having originally
formed the walls of the alimentary diverticula. Against this
view of its nature are the facts (i) 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 Elasmobranchs 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.
344 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Elasmo-
branchs, 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 a 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
THE URINOGENITAL SYSTEM. 345
flexure of the vertebral column are clearly that each muscle-
segment shall be capable of acting on two vertebrae; and this
condition can only be fulfilled when the muscle-segments are
opposite the intervals between the vertebrae. Owing to this
necessity, when the vertebral segments became formed^ thnir
centres corresponded, not with the centres of the muscle-plates,
but with the inter-muscular septa.
These considerations fully explain the secondary segmen-
tation of the vertebrae 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 unsegmerited 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 (PI. 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,/^). This knob consists at
first of 20 — 30 cells, which agree in character with the neigh-
bouring 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 hinder-
most 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
B. 23
346
DEVELOPMENT OF ELASMOBRANCH FISHES.
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 elsewhere1 called the segmental
duct.
FlG. 4. TWO SECTIONS OF A PRISTIURUS EMBRYO WITH THREE VISCERAL CLEFTS.
spn
spn
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 ; me. 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. splanch-
nopleura ; pp. pleuroperitoneal 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 PI. 1 1, fig. 7, sd.
At a stage somewhat older than I, the condition of the
segmental duct has not very materially altered. It has in-
creased considerably in length, and the knob at its front end
is both absolutely smaller, and also consists of fewer cells than
before (PI. 1 1, fig. J,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
1 " Urinogenital Organs of Vertebrates," Journ. of Anat. and Phys. Vol. x.
[This Edition, No. vn.]
THE URINOGEN1TAL SYSTEM. 347
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 com-
mencing separation of the muscle-plate from the remainder of
the mesoblast, begins to pass inwards and approach the plcuro-
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. (PI.
u, fig. 9, sd.) The lumen is formed by the columnar cells
spoken of in the last stage, acquiring a radiating arrange-
ment 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 (PI. u, fig. 8 and PI. 12, fig.
\^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
23—2
348 DEVELOPMENT OF ELASMOBRANCH FISHES.
of them ; the first of them arising in the segment immediately
behind the front end of the oviduct (PI. 12, fig. 17, sf), and two
of them being formed in segments just posterior to the hinder
extremity of the oviduct.
PI. 12, figs. 16 and 1 8 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. 140), 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 involu-
tions, 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 n, fig. 9, sd}. It pos-
sesses a lumen along its whole length up to the extreme hind
end (PI. n, fig. 9«). 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 begin-
ning 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 u, fig. 9^). 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 (PI. TI.
figs- 9 ^> 9 ^ and 9 d).
THE URINOGENITAL SYSTEM. 349
Primitive Ova. The true generative products make their
first appearance as tin& 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. 140).
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. 140).
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. 140 and 14 b}.
They are formed of a nucleus which stains deeply, invested
by a very delicate layer of protoplasm. At the junction of somato-
pleure and splanchnopleure they are more rounded than else-
where. Very few loose connective-tissue cells are present. The
cells just described vary from '008 Mm. to 'Oi 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.
350 DEVELOPMENT OF ELASMOBRANCH FISHES.
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.
TO 8
13 8
13 *
H 7
i5 •' 7
13 • 7i-
ii 8
16 Si
12 7
10 7
iS 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^; in another case 10 : 8, the nucleus has
only a slightly smaller diameter than the cell. The irration-
ality 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 haema-
toxylin. They usually contain a single deeply stained nucleolus,
but in many cases, especially where large (and this independently
THE URINOGENITAL SYSTEM. 351
of the size of the cell), they contain two nucleoli (PI. 12, figs. 14^
and 14^), 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 Gotte1, 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.
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 Gotte, 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 PI. 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 de-
veloping primitive ova from ordinary cells. Except with the
1 Entvricklungsgeschichte der Unke, PI. i, fig. 8.
352 DEVELOPMENT OF ELASMOBRANCH FISHES.
very thinnest sections a small extra quantity of protoplasm
around a nucleus might easily escape detection, and the de-
veloping 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 metamor-
phosis of adjoining cells, or may not be introduced from else-
where. 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 Verte-
brates. 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 Elasmobranchs
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 suffi-
ciently well marked features for a certain determination of their
true nature.
THE URINOGENITAL SYSTEM. 353
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 dif-
ferentiated 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.
O
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 ha^matoxylin these bodies are stained of a
deep purple colour, but the nucleus can in most cases be dis-
tinctly seen. In addition to the instances in which the proto-
plasm of the ova is quite filled with these bodies, there are
others in which they only occupy a small area adjoining the
nucleus (PI. 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
354 DEVELOPMENT OF ELASMOBRANCH FISHES.
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, consider-
ing 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 ex-
pressly stated. Only the development of the parts of the noto-
chord 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 longi-
tudinal 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 pro-
toplasm frequently vacuolated and containing in suspension
numerous yolk-spherules. It is difficult to determine whether
THE NOTOCHORD. 355
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 (PI. n, 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 mem-
brane1; the cells themselves have a flattened form, and each ex-
tends from the edge to the centre of the notochord, the long axis
of each being rather greater than half the diameter of the cord.
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 haema-
toxylin. Their long diameter in Scyllium is about O'O2 Mm.
The diameter of the whole notochord in Pristiurus during
stage I is about OT Mm. in the region of the back, and about
o-o8 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 (PI. 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.
1 This membrane is better looked upon, as is done by Gegenbaur and Gottef as
intercellular matter.
356 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 PI. 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 PI. 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. n it is in the
anterior part of the body of Pristiurus about O'li Mm. At the
age of fig. 12 it is in the same species O'I2 Mm., while in Scyl-
lium stellare it reaches about O'lj Mm.
During stage K (PI. 1 1, 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 pro-
toplasm may be found in an occasional corner.
THE NOTOCHORD. 357
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 noto-
chord 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
•QI2 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 O'2i 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 struc-
ture 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
358 DEVELOPMENT OF ELASMOBRANCH FISHES.
of Pristiurus, is the absence of any signs of nuclei or pro-
toplasm 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 n 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. /. Liver, mp. Muscle-plate, mp' . Early formed
band of muscles from the splanchnic layer of the muscle-plates, nc. Neural canal.
/. Protoplasm from yolk in the alimentary tract, pc. Pericardial cavity, po. Primi-
tive ovum. //. 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. sp c. Spinal cord. sp. v. Spiral valve, sr. Inter-
renal 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. i . Section from the caudal region of a Pristiurus embryo belonging to stage
H. Zeiss C, ocul. i. Osmic acid specimen.
It shews (i) the constriction of the subnotpchordal 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. i 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. i.
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. i. 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^. Section from the caudal region of an embryo slightly younger than 30.
Zeiss C, ocul. i. Osmic acid specimen.
PLATES II AND 12. 359
Fig. 4. Section from the cardiac region of a Pristiurus embryo belonging to stage
H. Zeiss C, ocul. i. Osmic acid specimen.
It shews the formation of the heart (fit) 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. i. Osmic acid specimen.
It shews the general features of an embryo of stage H, more especially the rela-
tions 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 cesophageal region of Scyllium embryo belonging to
stage I. Zeiss C, ocul. i. 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. i, reduced \. Osmic acid specimen.
It shews (i) 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. i. 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. i.
It shews (i) the solid oesophagus. (2) The narrow passage connecting the peri-
cardial (pc) and body cavities (//).
Fig. 9. Section of a Pristiurus embryo belonging to stage K. Zeiss A, ocul. i .
Osmic acid specimen.
It shews the formation of the liver (/), the structure'of the anterior fins (/>), and the
anterior opening of the segmental duct into the body-cavity (sd).
Figs. 9 a, 96, gc, gd. Four sections through the anterior region of the same
embryo as 9. Osmic acid specimens.
The sections shew (i) the atrophy of the post-anal section of the alimentary tract
(gb, gc, gd). (2) The existence of the segmental tubes behind the anus (9^, gc, gd).
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 gc but reappears in gd. (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. i. Reduced by \. Picric acid specimen.
It shews (i) the structure of the notochord ; (2) the appearance of the early formed
band of muscles (inp1) in the splanchnic layer of the protovertebra.
Fig. ii. Longitudinal and horizontal sections of an embryo belonging to stage I.
Zeiss C, ocul. i. 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.
360 DEVELOPMENT OF ELASMOBRANCH FISHES.
Fig. I2.1 Longitudinal and horizontal section of an embryo belonging to the
stage intermediate between I and K. Zeiss C, ocul. i. Osmic acid specimen
illustrating the same points as the previous section.
Fig. 13. Longitudinal and horizontal section of an embryo belonging to stage K.
Zeiss C, ocul. i, and illustrating same points as previous section.
Figs. i4#, 14^, 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^ are portions of transverse sections. Zeiss C, ocul. 3 reduced \.
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. i, ocul. i. The protoplasm of the ova is seen to be nearly filled with
bodies resembling yolk-spherules : and one ovum is apparently undergoing division.
Fig. 1 5 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. i. 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 trans-
parent 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. 1 8. Vertical longitudinal section of a Scyllium embryo "belonging to stage K.
Zeiss A, ocul. i. 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.
1 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.
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, (i) 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 (PI. 13, fig. 8), unquestionably pertaining to the
epiblast. This layer is especially thickened in the terminal
parts of the paired fins (PI. 13, fig. i). 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,
B. 24
362 DEVELOPMENT OF ELASMOBRANCH FISHES.
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. Hertwig1, 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.
Lateral line.
The lateral line and the nervous structures appended to it
have been recently studied from an embryological point of view
by Gotte* in Amphibians and by Semper3 in Elasmobranchs.
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 accord-
ance 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 appear-
ance, at a stage slightly subsequent to K, in the form of a
1 Jenaische Zeitschrift, Vol. vili.
2 Ent-wicklungsgeschichte d. Unke.
:t Urogenital-system d. Selachier. Semper's Arbeiten, Bd. II.
THE LATERAL LINE. 363
linear thickening of the inner row of cells of the external epi-
blast, 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 O'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 PI. 1 3,
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 ad-
joining nervous structures or traces of stick.
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^, ;/./). 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
24 — 2
364 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 (PI. 13, figs, ^b,
and 3^). In this position the nerve though small is still very
distinct in all good sections, and is formed of a rod of pro-
toplasm, 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 pre-
senting 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 incon-
siderable 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 O'i7 Mm. broad. At a point not far from this
it was O'OQ 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 (PI. 13 fig.
3«). 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^). Nearer the hind end of the trunk a space appears in it
between its columnar cells and the flattened cells of the outer-
most layer of the skin (PI. 13, fig. y], and this space becomes
posteriorly invested by a very definite layer of cells. The space
(Pi. 13, fig. 3<aO or lumen has a slit-like section, and is not
formed by the closing in of an originally open groove, but by
THE LATERAL LINE. 365
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 PI. 13, fig. 4. The lateral
line forms a canal situated completely below the skin, but at
intervals (corresponding with segments) sends upwards and .out-
wards 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 Elasmobranchs; 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 nume-
366 DEVELOPMENT OF ELASMOBRANCH FISHES.
rous 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 ampullae 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 ampullae and the nerves not so clear. In the case of the
head, there can for Elasmobranchs 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 peri-
pheral 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 Semper1, with whom as dealing with Elasmobranchs
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
1 Loc. cit. p. 398.
DERIVATION OF THE LATERAL NERVE. 367
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:
(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 observa-
tion 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
way1, affords a strong argument in favour of the lateral line
receiving an ordinary nerve-supply.
Considering all these facts, I am led to the conclusion that
the lateral nerve in Elasmobranchs 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 Elasmobranchs 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
1 Gotte 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 Elasrno-
branchs are concerned, nearly conclusive against such a derivation of the nerves in the
head.
368 DEVELOPMENT OF ELASMOBRANCH FISHES.
mucous canals are the only sense-organs which originate subse-
quently to the distinct differentiation of the epiblast into mu-
cous and horny layers, goes far to prove1 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.
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 com-
posed 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 (PI. 11, fig. 8 m. /), 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 conver-
sion 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 (PI. 13, fig. i). At the same time
the connective-tissue cells, which by this process become situ-
ated 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
1 I believe that Gotte, amongst his very numerous valuable remarks in the
Enhvickhmgsgeschichte der Unke, has put forward a view similar to this, though I
cannot put my hand on the reference.
THE MUSCLE-PLATES. 369
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 mecluttary
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 PI. 13, figs, i 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 PI. 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 protovertebrae, 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
PI. 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 somatic1.
1 The difference between Dr Gbtte's account of the development of the muscles
and my own consists mainly in my attributing to the somatic layer of the muscle-plates
3/O DEVELOPMENT OF ELASMOBRANCH FISHES.
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 undiffer-
entiated columnar cells. The peculiar outlines of the inter-
muscular septa gradually appear during the later stages of
development, causing the well-known appearances of the mus-
cles in transverse sections, but require no special notice here.
With reference to the histological features of the develop-
ment 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 fibrilla:. 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 Elasmobranchs, 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
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 Gotte's having
taken the highly differentiated Bombinator as his type instead of the less differentiated
Elasmobranch,
THE VERTEBRAL COLUMN. 371
(PL 1 8, fig. i). Small portions of several muscle-plates come in
this way to be situated in the limbs, and are very soon seg-
mented off from the remainder of the muscle-plates. The por-
tions 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 down-
wards, and by stage L cease to shew any trace of what has
occurred (PL 13, fig. i). This fact, coupled with the late develop-
ment of the muscles of the limbs (stage O), caused me to fall
into my original error.
T/te 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 vertebrae.
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 re-
searches of Gegenbaur1 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 Gotte's2 account
of the development of the haemal arches, and may add that
Cartier3 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.
At their first appearance the cells destined to form the per-
manent vertebrae present the same segmentation as the muscle-
1 Das Kopfskelet d. Selachier, p. 123.
3 Entivicklungsgeschichte d. Unke, pp. 433 — 4.
3 Zeitschrift f. Wiss. Anat. Bd. XXV., Supplement.
372 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 ob-
served, which is not however very distinctly marked1.
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 haemal 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 distinct-
ness in the succeeding stages, and by stage N have unques-
tionably 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 haematoxylin, and with the highest power may be observed
to contain flattened nuclei. It is barely thicker than the ad-
joining sheath, but is nevertheless the rudiment of the vertebral
bodies. PI. 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. Observa-
tions on the base of the brain afford fairly conclusive evidence
that the homologous tissue present there has this origin. Gegen-
baur apparently answers the question of the origin of this layer
in the way suggested above, and gives a figure in support of his
conclusion (PI. XXII. fig. 3)*.
1 Vide pp. 356, 357.
* 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
THE NEURAL AND H.EMAL ARCHES. 373
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 PI. XXII. fig. 4, a distinct
membrane (Kolliker's Membrana Elastica Externa) may easily
be recognized surrounding it and separating it from the adjoin-
ing 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 con-
stitutes a uniform unsegmented investment for the notochord
(vide PI. 13, fig. 10).
The neural and hsemal 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 (i) a series of arches encircling the spinal cord,
and 1.2) 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 it1.
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 haemal 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
figures alluded to. Gotte's very valuable researches with reference to the origin of
this layer in Amphibians tend to confirm the view advocated in the text.
1 In the adult Scyllium it is well known that the posterior root pierces the inter-
calated cartilage and the anterior root the true neural arch. This however does not
seem to be the case in the embryo at stage 1'.
374 DEVELOPMENT OF ELASMOBRANCH FISHES.
centres of the vertebrae. 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 haemal 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 PI. 13,
fig. 10), a fact which shews (i) 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 haemal pro-
cesses 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
arches1. 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 (PI. 13, fig. 11).
The innermost layer adjoining the notochord retains its primitive
1 A good representation of a longitudinal section at this stage is given by Cartier
(Zeitschrift f. Wiss. Zoologie, Bd. xxv., Supplement PI. iv. fig. i), who also gives a
fair description of the succeeding changes of the vertebral column.
THE NOTOCHORD. 375
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. 1 1), an external ring of hyaline cartilage invested by "-the
membrana elastica externa " (m.el), followed by a ring of calcify-
ing cartilage, and internal to this a ring of fibrous cartilage,
which adjoins the now slightly constricted notochord. A trans-
verse 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.
The constriction of the notochord proceeds till in the centre
of the vertebrae 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 verte-
bral 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 (PI. 13, fig. 11), but I have failed
to detect it in the adult, so that I cannot there clearly dis-
tinguish the arches from the body of the vertebrae. 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 vertebrae.
The changes in the notochord itself during the stages sub-
sequent 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
3/6 DEVELOPMENT OF ELASMOBRANCH FISHES.
fused, and are probably rightly regarded by Gegenbaur and
Gotte 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 (PI. 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 assumes1 a
radiating arrangement, giving to sections of the notochord the
appearance of a number of lines radiating from the centre to the
periphery (PI. 13, fig. n).
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 Miiller1 and Gegenbaur2, and re-
garded 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. Miiller3 (though not by Gegenbaur) as Kolliker's " mem-
brana 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 detect4.
EXPLANATION OF PLATE 13.
COMPLETE LIST OF REFERENCE LETTERS.
al. Alimentary tract, ao. Aorta, c. Connective tissue, ca v. Cardinal vein.
ch. Notochord. ep. Epiblast ha. Haemal arch. /. Liver. //. Lateral line, m c.
Mucous canal of the head. mel. Membrana elastica externa. nip. Muscle-plate.
mp'. Muscles of muscle-plate, na. Neural arch. nl. Nervus lateralis. rp. Rib
process, s d. Segmental duct. sh. Sheath of notochord. spc. Spinal cord, sp g.
Spinal ganglion, syg. Sympathetic ganglion, um. Ductus choledochus. v. Blood-
1 Jenaische Zeitschrift, Vol. VI. 2 Loc. cit. * Loc. cit.
4 Gegenbaur makes the reserve statement with reference to the sheath of the noto-
chord. For my own sections the statement in the text certainly holds good. For-
tunately the point is one of no importance.
PLATE I3. 377
vessel, var. Vertebral arch. vb. Vertebral body, vcati. Caudal vein. vin. In-
testinal branch of the vagus, v op. Ramus ophthalmicus of the fifth nerve, x. Sub-
notochordal rod.
Fig. i. Section through the anterior part of an embryo of Scy ilium 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. i.
Fig. 2. Section through the lateral line at the time of its first formation.
The cells marked « / were not sufficiently distinct to make it quite certain that
they really formed part of the lateral nerve. Zeiss B, ocul. 2.
Figs. 3«, 3<$, ^c, 3</. Four sections of the lateral line from an embryo belonging
to stage L. 30 is the most anterior. In ^a the lateral nerve («/) 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^ (46), $c (64), 3 b (84), 30 (93). The figures all drawn on the same
scale, but 3« 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 inner-
most part deserve to be noticed. Zeiss D, ocul. i.
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 aa, ocul. i.
Fig- 7- Junction of a nerve and mucous canal. Stage P. Zeiss D, ocul. T..
Fig. 8. Longitudinal and horizontal section through the muscle-plates and adjoin-
ing 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 haemal arches in the first few sections behind the
point where the latter appear. Zeiss C, ocul. i .
Fig. 1 1 . Transverse section through the centre of a caudal vertebra of an embryo
somewhat older than Q. It shews (i) 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 externa1 (met). It shews also the differentiation of
three layers in the vertebral centrum : vide p. 374.
1 The slight difference observable between these two tissues in the arrangement of their nuclei has
been much exaggerated by the engraver.
B. 25
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*, 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 sub-
ject are discussed.
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 pro-
liferate, and the uniform outline of the cord becomes broken
(PI. 14, fig. 3). There is formed in this way a small prominence
of cells springing from the summit of the spinal cord, and con-
stituting 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 PI. 14, fig. 2, and the rudiments may there be seen
1 Phil. Trans. Vol. 166, p. 175. [This Edition, No. vni.]
THE SPINAL NERVES. 379
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 PI. 14,
fig. i, and PI. u, figs. 6 and 7), but soon meet with and become
partially enclosed in the mesoblastic tissue (PI. u, 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 (PI. 14, fig. 4 a. r.) arises as a very small but dis-
tinct 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 con-
siderable 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
25 — 2
380 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 out-
growth 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 be-
comes 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 connect-
ing 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 PI. 12,
fig. 1 8, com. What it has been possible for me to make out of its
eventual fate is mentioned subsequently1.
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 pos-
terior roots spring from the spinal cord in the position normal
for Vertebrates.
This apparent migration caused me at first great perplexity,
1 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.
THE SPINAL NERVES. 381
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 (PI. 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 tlie 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 con-
tinuous 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
382 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 pos-
terior 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 alter-
nately with the dorsal roots, a condition which persists in the
adult.
Although I have made some efforts to determine the even-
tual 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 pro-
toplasm 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 origi-
nally 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 ex-
treme 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.
THE SPINAL NERVES. 383
These are the rudiments of the posterior nerve-roots. The
outgrowths, though at first attached to the spinal cord through-
out 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 Mam-
malia1.'
Mr Marshall2 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
Elasmobranchs 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 unprofit-
able, and I proceed at once to certain considerations suggested
by the above observations.
1 Zeit. f. Anat. u. Enhvicklungsgeschichtc, Vol. I.
- Journal of Anatomy and Physiology, Vol. xi. April, 18771
384 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 ap-
peared 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 Elasmobranchs.
It is possible to suppose that in their primitive differentia-
tion contractile and sensory systems may, as in Hydra1, 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 in-
creasing 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
1 Kleinenberg Hydra.
ORIGIN OF NERVES. 385
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-celhtxrthe
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.
As the descendants of the animal in which the rupture
occurred became progressively more complicated, the two ter-
minal 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 ' 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
1 Virchow's Archiv, Vol. XXXI. 1864.
386 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 shewn1
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.
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 Elasmobranchs 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. Gotte2,
whose account of the development of the spinal ganglia is com-
pletely in accordance with the ordinary views, yet states3 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 pre-
ceding chapter of the manner in which the nerves become con-
nected 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.
On the other hand, Calberla4 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 ad-
mits 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.
1 Phil. Trans., 1876. [This Edition, No. vm.]
2 Entwicklungsgeschichte der Unke. 3 Loc. cit. p. 516.
4 Archiv fiir Micros. Anat. Vol. xi. 1875.
VERTEBRATE AND ANNELIDAN NERVOUS SYSTEMS. 387
The obvious difficulty, already alluded to, of understanding
how it is, according to the generally accepted mode of develop-
ment 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
388 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Elasmobranchs1 arise, in the exact manner which might have
been anticipated, were the spinal canal due to such a folding as
I have suggested.
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 ex-
plained 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 rela-
tion between the two, as to shew the a priori possibility of the
formation of a spinal cord, and the a 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.
1 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.
DR DOHRN'S HYPOTHESIS. 389
Professor Gegenbaur1 looks upon the central nervous system of
Vertebrates as equivalent to the superior cesophageal ganglia
of Annelids and Arthropods only, while Professors Leydig2 and
Semper3 and Dr Dohrn4 compare it with the whole Annelidan
nervous system.
The first of these two views is only possible on the suppo-
sition that Vertebrates are descended from unsegmented an-
cestors, 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 ex-
isting 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 cesophageal ganglia. Dr Dohrn5, who has specu-
lated 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 de-
scended, 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 cesophageal nervous ring, the latter structure
ceased to be visible as such, and no part of the alimentary
1 Grundriss d. vergleichenden Anat. p. 264.
2 Bmi des thierischen Korpers.
* Stammesvenuandschaft d. Wirbelthiere u. Wirbellosen and Die Venvandschafts-
beziehungen 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 observa-
tions on Spinal Nerves above recorded.
4 Ursprung d. Wirbelthiere u. Princip des Functionswechsds.
5 Loc. at.
39O DEVELOPMENT OF ELASMOBRANCH FISHES.
canal was any longer enclosed by a commissure of the central
nervous system. With the change of mouth Dr Dohrn also sup-
poses that there took place a change, which would for a swim-
ming 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.
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 forma-
tion 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 be-
fore the atrophy of the primitive mouth, the folding to form it
must necessarily have ceased behind the mouth ; and, on the
supposition of the cesophageal 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 cesophageal 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
HOMOLOGIES OF THE VERTEBRATE NERVOUS SYSTEM. 39!
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 expla-
nation 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 a 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
392 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 canal1.
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 sub-
sequent 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 cesophageal
ring, fresh mouth2, and of the change of the ventral to the dorsal
1 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.
2 Professor Semper ("Die Verwandtschaftsbeziehungen d. gegliederten Thiere,"
Arbeiten aus d. Zool.-zoot. Institut, Wiirzburg, 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 Turbel-
larians and Nemertines. He comes to the conclusion that there was a primitive
mouth on the cardiac side of the supra-resophageal ganglion, which is the existing
mouth of Turbellarians and Vertebrates and the opening of the proboscis of Nemer-
tines, 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 subse-
quent to the Annelidan mouth. Under these circumstances this fresh hypothesis does
ORIGIN OF THE VERTEBRATE NERVOUS SYSTEM. 393
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. Thw 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.
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-cesophageal
ganglia, from which two main nervous stems extended back-
wards, one on each side of the body. Such a nervous system in
fact as is possessed by existing Nemertines or Turbellarians1.
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 cord2.
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 cesophageal nerve-ring3.
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 satis-
factory 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 pro-
vided with a separate opening and perhaps carried with it the so-called vagus of
Professors Semper and Leydig.
1 It is not of course to be supposed that the primitive nervous system was pierced
by a proboscis like that of the Nemertines.
2 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.
3 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 Poly-
gordius.
B. 26
394 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 seg-
mented 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
Chaetopodous Annelids and the Hirudinea. If the latter is an
isolated branch, it is especially interesting from having inde-
pendently developed a series of segmental organs like those of
Chaetopodous 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. i, 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
SYMPATHETIC NERVOUS SYSTEM. 395
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 com-
missure. 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 com-
missural 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 PI. 13,
% l> sy- S- a»d in PL 1 8, 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 1 8, 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 development1. My obser-
vations 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 developes
a ganglion, and the ganglia become connected by a longitudinal
commissure. On this view a typical spinal nerve has the follow-
ing parts: two roots, a dorsal and ventral, the dorsal one
ganglionated, and three main branches, (i) 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
1 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.
26 — 2
396 DEVELOPMENT OF ELASMOBRANCII FISHES.
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, how-
ever, 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.
EXPLANATION OF PLATE 14.
This Plate illustrates the Formation of the Spinal Nerves.
COMPLETE LIST OF REFERENCE LETTERS.
a r. Anterior root of a spinal nerve, ch. Notochord. com. Commissure connect-
ing the posterior roots of the spinal nerves, i. Mesoblastic investment of spinal cord.
m p. 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 rudi-
ment, w. White matter of spinal cord. y. Point where the spinal cord became
segmented off from the superjacent epiblast.
Figs, i , 2, and 3. Three sections of a Pristiurus embryo belonging to stage 1.
Fig. i 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. r 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 (a r).
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 elonga-
ted 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. r.) 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 (PI. 8, fig. G),and is in tact 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
398 DEVELOPMENT OF ELASMOBRANCH FISHES.
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^ and 4^).
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 (PI. 15, figs. I, 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 PI. 16, figs, la, 5 and /«.
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 hemi-
spheres have grown directly forwards, and if figures la and
5 in PI. 1 6 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 thala-
mencephalon. The thalamencephalon in fig. \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 hemi-
spheres that the angle between the trabeculae 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
THE FORE-BRAIN. 399
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 (PI. 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 (PI. 15, fig. !,/«)• 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 (PI. 15, fig. 2 and fig. i6#), 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 (PI. 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 (PI. 15,
figs, ga, 12, 1 6, 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 (PI. 15, fig. 1 1, op. «).
During stage L the infundibulum becomes much produced,
and forms a wide sack in contact with the pituitary body, and
4OO DEVELOPMENT OF ELASMOBRANCH FISHES.
its cavity communicates with that of the third ventricle by an
elongated slit-like aperture. This may be seen by comparing
PI. 16, figs. \a and ic. In fig. ic taken along the middle line,
there is present a long opening into the infundibulum (/;/), which
is shewn to be very narrow by being no longer present in fig. \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. ib,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 im-
portant of these are illustrated by a section of stage O, PI. 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 longi-
tudinal and vertical section through the brain (PI. 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
THE CEREBRAL HEMISPHERES. 401
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 (PI. 16, fig. 3, x), destined to form a
vertical septum dividing it into two hemispheres, and secondly,
lateral outgrowths (vide PI. 16, fig. 2, ol. I), 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 con-
stitution to any other cranial nerve makes its appearance (PI. 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 pro-
nounced (vide PI. 1 6, figs. 40 and 4^ ol.l). The root of the
olfactory nerve is now very thick, and the ganglion cells it con-
tains 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
4O2 DEVELOPMENT OF ELASiMOBRANCH FISHES.
development of the brain. Its structure is represented for this
stage in general view in PI. 16, figs. 6a, 6b, 6c, in longitudinal
section in PI. 16, figs, ja, jb, and in transverse section PL 16,
figs. 8a — d. The transverse sections are taken from a some-
what older embryo than the longitudinal. In the thalamence-
phalon there is no fresh point of great importance to be noticed.
The pineal gland remains as before, and has become, if any-
thing, 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. Sa, pn],
and does not extend outside the skull, as it appears to do,
according to Gotte's investigations, in Amphibians. Gotte1
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 Umbildungs-
produkt 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 vas-
culosi are perhaps indicated at this stage in the two lateral
divisions of the trilobed ventricle of the infundibulum (fig. 8c).
The lateral ventricles (fig. 8a) 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. Sa,
oU), and contain, as before, prolongations of the lateral ventricles.
The so called optic chiasma is very distinct (fig. 8b, op.ii), 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 PI. 16, fig. 4$, mb,
in which the distinctness of this character is by no means
exaggerated). During stage Q it becomes really bilobed through
1 Ent. d. Unite, p. 304.
THE HIND-BRAIN. 4° 3
the formation in its roof of a shallow median furrow (PI. 16, fig.
8£). 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. "ja]. It exhibits in surface-views of the hardened
brain of stages P and Q the appearance of a median con-
striction, and the portion of the ventricle contained in it is
prolonged into two lateral outgrowths (PI. 16, figs. Sc and
84 cb\
The posterior section of the hind-brain which forms the me-
dulla 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
(PI. 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 (PI. 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 (PI. 15, fig. 50). 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 (PI. 15, fig. 6), and
this latter becomes completely obliterated in the later stages.
The dorsal pair, while approximating, also become more promi-
nent, and stretch into the dorsal moiety of the fourth ventricle
(PI. 15, fig. 6). They are still very prominent at stage Q (PI. 16,
404 DEVELOPMENT OF ELASMOBRANCH FISHES.
fig. %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 (PI. 16, fig. 7ft).
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 (PI. 16, fig. 7 a,
rt}, which are regarded by Miklucho-Maclay1 as representing the
true cerebellum.
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
(PI. 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 con-
nected 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 (PI. 16, fig. ja, tv).
The development of the brain in Elasmobranchs 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
1 Das Gehirn d. Selachier, Leipzig, 1870.
THE VIEWS OF MIKLUCHO-MACLAY. 405
on Ceratodus1. 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.
" 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 (acts of develop-
ment."
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 develop-
ment, 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
Elasmobranchs, 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
1 Proceedings of the Zoological Society, 1876, Pt. I. pp. 30 and 31.
406 DEVELOPMENT OF ELASMOBRANCH FISHES.
importance, and may not improbably be regarded as a real
ancestral feature. Some observations have recently been pub-
lished by Professor B. G. Wilder * 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 hemi-
spheres 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 con-
clusions 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.'"
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 (i) the olfactory lobes (crura and bulbs) are direct
outgrowths from the cerebral rudiment, and develope quite in-
dependently 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
1 "Anterior brain-mass with Sharks and Skates," American Journal of Science
and Arts, Vol. xil. 1876.
THE OLFACTORY ORGAN. 407
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.
T/te olfactory organ. The olfactory pit is the latest formed
of the three organs of special sense. It appears during a stage
intermediate between / 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
(PI. 15, figs, i and 2, ol).
The epiblast cells which form this thickening are very co-
lumnar, 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 (PI. 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 (PI. 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 con-
striction 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 (PI. 15, fig.
130, 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.
408 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 (PI. 15,
fig- 7> 0- 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 Gotte1 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 c^^p.
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 (PI. 15, fig. I3«)2. They form the rudi-
ments 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 circum-
ference of the walls except the point of entrance of the optic
nerve (PL 15, fig. 13^), where no growth takes place; here accord-
ingly 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. 1 30). No further differentiations arise
before the close of stage K.
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
1 Entwicklungsgeschichte d. Unke.
2 The engraver has not been very successful in rendering these membranes.
THE PROCESSUS FALCIFORMIS. 409
wall becomes very thin, and its posterior wall thick, and doubly
convex (fig. 1 3#). 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 tJie optic cup round its edge, ~bttt 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. 1 3#, cli). 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 com-
prising 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 pro-
cessus falciformis. The development of these parts in Elasmo-
branchs has recently been dealt with by Dr Bergmeister1, and
his observations with reference to the vitreous humour and
processus falciformis, the discovery of which in embryo Elas-
mobranchs is due to him, are very complete. I cannot, however,
accept his view that the hyaloid membrane is a mesoblastic pro-
duct. 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 PI. 17, fig. 6, /. fal. ; it
1 "Emhryologie d. Coloboms," Sitz. d. k. Akad. IVien, Bd. LXXi. 1875.
B. 27
4IO DEVELOPMENT OF ELASMOBRANCH FISHES.
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 pro-
cess 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 PI. 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.
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 (PI. 15, fig. 13^), 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 C> 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 (PI. 17, fig. 6, ky. 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 attach-
ment 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 de-
scribed 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 ap-
pears at a period subsequent to the latest one investigated by
THE VITREOUS HUMOUR. 411
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 epi-
blastic 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 PI. 15, fig. 130. 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 Kolliker
and others in preference to the more modern ones of Lieberkuhn
and Arnold. It would take me too far from my subject to
discuss the arguments used by the later investigators' to main-
tain their view that the hyaloid membrane and lens capsule are
mesoblastic products ; but it will suffice to say that the con-
tinuity 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 mem-
branes, 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 Lieberkuhn 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 capsjilo-pupillaris) is said to be in part
formed. Lieberkuhn 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, con-
form 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 de-
pendent 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. Per-
haps the mode of formation of the vitreous humour in Mammalia
may be correlated with the early closing of the choroid-slit.
27 — 2
412 DEVELOPMENT OF ELASMOBRANCH FISHES.
Auditory Organ. With reference to the development of the
organ of hearing I have very little to say. Opposite the in-
terval between the seventh and the glosso-pharyngeal nerves
the external epiblast becomes thickened, and eventually in-
voluted 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 (PI. 15, fig. 2).
As has been already pointed out, the epiblast of Elasmo-
branchs during the early periods of development exhibits no
division into an epidermic and a nervous layer, and in accord-
ance 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 de-
rived 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 con-
veniently 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 pos-
terior surface by the front wall of the alimentary tract, and on
its anterior by the base of the fore-brain.
THE PITUITARY BODY. 413
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 cor-
rectness 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 Elas-
mobranch development1 ; and has also been shewn to be the
case in Amphibians by Gotte2 ; and in Birds by Mihalkowics3.
The fact is of considerable importance with reference to specula-
tions as to the meaning of this body.
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 hori-
zontally, 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 ter-
mination of the throat, which a little way back opens to the
exterior by the first visceral cleft (l. 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 con-
firmed 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 PI. 15, fig. i6a, and PI. 16, figs, i a,
i 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 nar-
1 Quarterly Journal of Microscopic Science, Oct. 1874.
'2 Ent-wicklungsgeschichte der Unke. Gotte was the first to draw attention to this
fact. His observations were then shewn to hold true for Elasmobranchs by myself,
and subsequently for Birds by Mihalkowics.
:! Arch. f. mift: Anat. Vol. XI.
4H DEVELOPMENT OF ELASMOBRANCH FISHES.
rower and narrower, and is finally reduced to a solid cord,
which in its turn disappears. The remaining vesicle then be-
comes divided into lobes, and connects itself closely with the
infundibulum (PL 16, figs. 5 and 6 pt}. The later stages for
Elasmobranchs are fully described by W. Miiller in his im-
portant memoir on the Comparative Anatomy and development
of this organ1.
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 tJie 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 tnet 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 inde-
pendently of it, opposite the anterior end of the thickening of
the epiblast to form the auditory involution. It arises precisely
1 W. Miiller, "Ueber Entwicklung und Bau d. Hypophysis u. d. Processus in-
fundibuli cerebri," Jenaische Zeitschrift, Bd. vi.
FIRST FORMATION OF CRANIAL NERVES. 415
like the fifth, from the extreme dorsal summit of the neural axis
(PI. 15, fig. 4«, vn). 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 more-
over continuous with that for the spinal nerves1. The outgrowth
of the vagus and glosso-pharyngeal nerves is not continuous
with that of the seventh nerve. This is shewn by PI. 15, figs. 4#
and 4& The outgrowth of the seventh nerve though present in
40 is completely absent in 4^ which represents a section just
behind 4^.
Thus, by the end of stage I, there have appeared the rudi-
ments of the 5th, 7th, 8th, Qth and loth cranial nerves, all of
which spring from the hind-brain. These nerves all develope
precisely as do the posterior roots of the spinal nerves, and it is
a remarkable fact tliat 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*.
1 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 Gbtte and myself with reference to the vagus
nerve. Gotte regards the vagus as a single nerve, from its originating as an undivided
rudiment ; but it is clear from my researches that, for Elasmobranchs 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 pro-
cesses from a continuous outgrowth from the brain !
- The conclusion here arrived at with reference to the anterior roots, is opposed
to the observations of both Gegenbaur on Hexanchus, Jenaisckc Zeifsc/irift, Vol. VI.,
416 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 con-
sideration shews that it is not seriously opposed to the facts
which we know. In the first place it has been shewn by myself1
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 develope 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.
Subsequent Changes of the Nerves. — To simplify my descrip-
tion of the subsequent growth of the cranial nerves, I have
inserted a short description of their distribution in the adult.
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 im-
possible 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 be-
longing to spinal nerves. This point is more fully spoken of at p. 428.
1 Journal of Anatomy and Physiology, Vol. x. [This Edition, No. ix.]
CRANIAL NERVES IN THE ADULT. 417
This is taken from a dissection of Scyllium stellare, which like
other species has some individualities of its own not found in
the other Elasmobranchs. 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
Stannius1 for Carcharias, Spinax, Raja, Chimaera, &c. ; Gegen-
oaur2 for Hexanchus ; Jackson and Clarke3 for Echinorhinus.
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 roots4: (i) an anterior more
or less ventral root; (2) a root slightly behind, but close to the former5,
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 dis-
tance 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 con-
nection 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 ophthal-
micus profundus is given off from the first of them.
The fifth nerve, according to the usual nomenclature, has three main
divisions. The first of these is the ophthalmic. It is formed by the coales-
cence of two entirely independent branches of the fifth, which unite on
leaving the orbit. The dorsalmost of these, or ramus ophthalmicus super-
ficialis, 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 ophthal-
micus prof undiis. 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 Elasmobranchs)
1 Neruensystem d. Fische, Rostock, 1849.
- Jenaische Zeitschrifl, Vol. vi.
3 Journal of Anatomy and Physiology, Vol. X.
4 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.
5 The root of the seventh nerve cannot properly be distinguished from this root.
41 8 DEVELOPMENT OF ELASMOBRANCH FISHES.
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
superficial, 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 maxillae 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 maxillae superioris, it
passes outwards along the line separating the musculus adductor mandibulas
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 Elasmobranchs. 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 mem-
brane 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 tv/o 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 super-
ficialis. The main stem of the facial is mixed motor and sensory. I have
DEVELOPMENT OF THE FIFTH NERVE. 419
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 back-
wards 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 an-
terior 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 pos-
terior 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 Elasmobranchs
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.
TJie FiftJi 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 men-
tioned, 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
420 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 con-
dition.
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, PI. 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 for-
wards, PI. 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, PI. 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 (PI. 17, fig. 4 b, V op. th.},
SEVENTH AND AUDITORY NERVES. 42!
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 pro-
fundus, 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), PI. 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 in-
ferior, 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. i.
Seventh and A uditory 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 pur-
sues a straight course to the hyoid arch (PL 15, fig. 10, VII.), the
second of the two (PL 15, fig. 10, ait* «.), which is clearly the
rudiment of the auditory nerve, developes a ganglionic enlarge-
ment and, turning backward, closely hugs the ventral wall of the
auditory involution.
The observation just recorded appears to lead to the fol-
lowing 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
422 DEVELOPMENT OF ELASMOBRANCH FISHES.
becomes split into two parts, an anterior to form the seventh
nerve, and a posterior to form the auditory nerve. The gan-
glionic part of the auditory nerve is derived from the primitive
outgrowths from the brain, and not from the auditory involu-
tion. 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 con-
sequence 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 gan-
glionic 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 PI. 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 termi-
RAMUS OPHTHALMICUS SUPERFICIALIS. 423
nating in branches to the skin in front of the eye (PI. 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 ob-
liqueness), 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 opthal-
micus 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, how-
ever, 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 cer-
tainly has the distribution in question in tJie embryo, and that
there is no reason why it should not retain it in the adult.
424 DEVELOPMENT OF ELASMOBRANCH FISHES.
Finally, the junction of the two rami ophthalmici, most re-
markable 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 succeed-
ing 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 (prae-spira-
cular 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 Clarke1 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
1 Loc. tit.
THE GLOSSOPHARYNGEAL AND VAGUS NERVES. 425
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 Tvhich
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 seventh1. 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 accompany-
ing 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.
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 con-
nected 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 (PI. 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 Gegenbaur2, equivalent
to four independent nerves, but form, together with the glosso-
pharyngeal, a compound nerve, which we may briefly call the
vagus.
1 Hexanchus, Gegenbaur, Jenaische Zeitschrift, Vol. VI. - Loc. cit.
B. 28
426 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 repre-
sented on the diagram, PI. 17, fig. I. 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 brain1. 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.
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 1 5,
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, i 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
1 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 ROOTS OF THE VAGUS NERVE. 427
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, coin. 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 glossopharyn-
geal 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 Gegenbaur1. 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 ex-
planation of their variability, since in the case of all organs
which are on the way to disappear variability is a precursor of
disappearance.
A second interesting point is the presence of the two connect-
ing 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
1 Loc. cit.
28—2
428 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 glosso-
pharyngeal nerve alone becomes eventually separated from the
succeeding branches. Stannius and Gegenbaur have, as was
mentioned above, detected in adult Elasmobranchs 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
embryologrcal 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 vagus1.
The similar relations of the apparently homologous branch or
branches in many Osseous Fish may also be used as an argument
for my view.
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 embryo-
logical 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.
1 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.
MYOTOMES OF THE HEAD. 429
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 PI. 10, figs. 3 b and 6//.) These cavities
end in front opposite the blind anterior extremity of the alimen-
tary 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 PI. 15, figs. 4 a and ^b pp.); and
during stage H it becomes, owing to the formation of a second
cleft, divided into three sections: (i) 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 inter-
vention 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 suc-
cessive sections, there being one section for each arch. Thus
the whole head-cavity becomes on each side divided into (i) 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
430 DEVELOPMENT OF ELASMOBRANCH FISHES.
is situated close to the eye, and presents a rounded or sometimes
triangular figure in sections (PL 15, figs. 7, 9 b and \6b, I 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 (PI. 15, fig. 8. i //.). 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 con-
sidered 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, PI. 15, fig. I //. 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, PI. 15, fig. 7. To-
wards 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 splanch-
nic 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
MYOTOMES OF THE HEAD. 431
like those in its anterior part, though at rather a later period.
Their walls however persist, and become more columnar. In
PI. 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 -en- the
outer side of the aortic trunk of its arch as does the cavity in
the mandibular arch (PI. 15, fig. 7, 2pp). 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 tJieir 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 interbranchialis1 ; and pro-
bably also musculus levator mandibuli and other muscles of the
front part of the head.
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 develope 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 sub-
sequent 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
1 Vide Vetter, " Die Kiemen und Kiefermusculatw d. Fische." Jenaische Zeit-
schrift, Vol. VI I.
432 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 pro-
duced 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 Surgeons1, and
will be published in full in the Transactions of the Zoological
Society.
All my efforts have hitherto failed to demonstrate any seg-
mentation in the mesoblast of the head, other than that in-
dicated 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 longi-
tudinal muscles, forming about three or four muscle-plates, the
ventral part of which is wanting. I have not the means of de-
ciding 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 PI. 15, fig. 15 b, and in PI. 17, fig. 2.
1 A report of the lectures appeared in Nature,
THE GILL-SLITS. 433
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 meso-
blast 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 retro-
gressive metamorphosis. It also becomes bent upon itself in a
ventral direction through an angle of 180°; vide PL 15, figs. 90
and 1 6 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 ali-
mentary 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 dis-
solution 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
434 DEVELOPMENT OF ELASMOBRANCH FISHES.
that the walls lining the clefts are entirely formed of hypoblast.
The clefts are formed successively1, 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.
In stage K, four if not five are open to the exterior, and the
rudiments of six, the full number, have appeared2. 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 mesoblast3.
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 alimen-
tary 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 regarded4 as homologous with the ex-
ternal gills of Annelids ; but, if derived from the hypoblast, this
view becomes, to say the least, very much less probable.
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
1 Vide Plate 8.
2 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.
3 Vide on the development of the gills, Schenk, Sitz. d. k. Akad. IVien, Vol.
LXXI. 1875.
4 Vide Dohrn, Ur sprung d. Wirbelthiere.
SEGMENTATION OF THE HEAD. 435
that, of a series of homodynamous segments1. While the
researches of Huxley, Parker, Gegenbaur, Gotte, 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 under-
gone, 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 con-
sideration 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: — (i) The
cranial nerves ; (2) the visceral clefts ; (3) the divisions of the
head-cavity.
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 Elasmobranchs.
The development of the cranial nerves has recently been
studied with great care by Dr Gotte, 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, amount-
ing 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
1 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.
436 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 (i) 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 seg-
ment. A comparison of the post-auditory nerves of Scyllium
and other typical Elasmobranchs 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 (PI. 17, fig. I, VII.) is
SEGMENTATION OF THE HEAD. 437
formed by the junction of three conspicuous branches, (i) 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 (vn. m?t): 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 inspec-
tion of the diagram of the nerves on PI. 17, fig. I, V., or from an
examination of the sections representing these nerves (PI. 17,
figs. 3 and 4). It divides like the seventh nerve into three main
branches : (i) 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. maxillae inferioris) ; and (3) an anterior
branch to the palatine arcade (r. maxillae superioris). I was at
first inclined to regard the anterior branch of the fifth (ophthal-
mic) 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 the1
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 supply-
ing the mandibular arch, and not, as has been usually thought, a
DEVELOPMENT OF ELASMOBRANCH FISHES.
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 morpho-
logical speculations of Professor Huxley1.
From this enumeration of the nerves the optic nerve is ex-
cluded for obvious reasons, and although it has been shewn
above that the olfactory nerve developes 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 seg-
mental cranial nerves.
The nerves then give us indications of seven cranial seg-
ments, 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 seg-
mentation 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 seg-
ments of the mandibular arch, hyoid arch, and of the five
branchial arches. If, following the views of Dr Dohrn2, 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 praeoral 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.
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
1 Preliminary note upon the brain and skull of Amphioxus, Proc. of the Royal
Society, Vol. xxir.
8 Ursprung d. Wirbelthiere.
SEGMENTATION OF THE HEAD.
439
of the body-cavity develope into muscles and resemble the
muscle-plates of the trunk, and with these they must be identi-
fied, 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 seg-
ments, the first of them praeoral. 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 sub-
joined table represented in a form in which they can be com-
pared : —
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
PicEoral i
Postoral -2
3rd and 4th and ? 6th
nerves (perhaps repre-
senting more than one
segment)
5th nerve
7th nerve
Glossopharyngeal nerve
ist branch of vagus
2nd branch of vagus
3rd branch of vagus
4th branch of vagus
(?)
Mandibular
Hyoid
ist branchial arch
2nd branchial arch
3rd branchial arch
4th branchial arch
5th branchial arch
ist head-cavity
(in my figures i //.)
2nd head-cavity
(in my figures 2 pp.)
3rd head-cavity
4th head-cavity
5th head-cavity
6th head-cavity
7th head-cavity
8th head-cavity
3
' 4
5
- f\
7
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
44O DEVELOPMENT OF ELASMOBRANCH FISHES.
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 seg-
ment 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.
i aa, iaa, etc. * ist, 2d, etc. aortic arch. acv. Anterior cardinal vein. al. Ali-
mentary canal, ao. Aorta. an. 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, i, 2, 3 etc.
eg. External gills, ep. External epiblast. fb. Fore-brain, gl. Glossopharyngeal
nerve, h b. Hind-brain, ht. Heart, hy. Hyaloid membrane. In. Infundibulum.
/. Lens. M. Mouth involution, m. Mesoblast at the base of the brain, m b. 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. V ' c. Visceral cleft. Vg. Vagus, vii. Seventh or facial nerve.
Fig. i. Head of a Pristiurus embryo of stage K viewed as a transparent object.
The points which deserve special attention are: (i) 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.
EXPLANATION OF PLATE 15. 44!
The notochord cannot be traced in the living embryo so far forward as it is repre-
sented. 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 sevchtll
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 (i) 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 ^b. Two sections through the head of a Pristiurus embryo of
stage I. They shew (i) 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. i.
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 (ffi) 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. i.
The section shews (i) 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. i.
The section illustrates (i) the formation of the pituitary body (//) from the mouth
involution (;«), 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 (i//, 2//). (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
('//)•
Figs. 9 a and gb. Two longitudinal sections through the brain of a Pristiurus
embryo belonging to a stage intermediate between I and K. Zeiss A, ocul. i.
9 a is taken through the median line, but is reconstructed from two sections. It
shews (i) 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.
B. 29
442 DEVELOPMENT OF ELASMOBRANCH FISHES.
gb is a section to one side of the same brain. It shews (i) The divisions of the
brain. (2) The point of outgrowth of the optic nerves (ppri). (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. n. 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 (i) the condition of the end of the notochord; (2) the relation of the
mouth involution to the infundibulum.
Fig. 130. Longitudinal and horizontal section through part of the head of a
Pristiurus embryo rather older than K. Zeiss A, ocul. i.
The figure contains the eye cut through in the plane of the choroid slit. Thus the
optic nerve (op n) 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^. Transverse section through the last arch but one of the same embryo
as 130. Zeiss A, ocul. i.
The figure shews ( i ) The mode of formation of a visceral cleft without any involu-
tion 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, con-
siderably 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. i5« and 15 3. Two longitudinal and vertical sections through the head of a
Pristiurus embryo belonging to stage K. Zeiss a, ocul. 3.
15 « 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 £ mainly illustrates the dorsal commissure of the vagus nerve (com) continuous
with the dorsal commissures of the posterior root of the spinal nerves.
Fig. 1 6. Two longitudinal and vertical sections of the head of a Pristiurus
embryo belonging to the end of stage K. Zeiss a, ocul. i.
i6a 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.
\6b is a more superficial section shewing the head-cavities// i, 2, 3, and the
lower vagus commissure.
EXPLANATION OF PLATE 1 6. 443
PLATE 16.
COMPLETE LIST OF REFERENCE LETTERS.
au v. Auditory vesicle, cb. Cerebellum, cer. Cerebral hemispheres, ch, Notcv
chord, cin. Internal carotid, ft. Fasciculi teretes. in, Infundibulum. Iv.
Lateral ventricle, m b. Mid-brain, or optic lobes, md. Medulla oblongata. mn,
Mandible. ol. Olfactory pit. oil. Olfactory lobe, op. Eye. opn. Optic nerve.
opth. Optic thalamus. pc. Posterior commissure, pel. Posterior clinoid. pn,
Pineal gland, pt. Pituitary body, r t, Restiform tracts, t v. Tela vasculosa of the
roof of the fourth ventricle, iv. v. Fourth ventricle, vii. Seventh nerve, x. Rudi-
ment of septum which will grow backwards and divide the unpaired cerebral rudiment
into the two hemispheres.
Figs, i a, i b, ic. Longitudinal sections of the brain of a Scyllium embryo
belonging to stage L. Zeiss a, ocul I.
i 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 (ft).
i b is through the median line of the pineal gland.
i 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 (i) 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^, \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 ( i ) 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 1>, 6c, Views from the side, from above, and from below, of a brain
of Scyllium stellare during a slightly later stage than Q.
29 — 2
444 DEVELOPMENT OF ELASMOBRANCH FISHES.
Figs. 7 a and 7 b. Two longitudinal sections through the brain of a Scyllium
embryo during stage Q. Zeiss a, ocul. i.
•ja cuts the hind part of the brain nearly through the middle line ; while ib cuts
the cerebral hemispheres and pineal gland through the middle.
In 7« the infundibulum (i), 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 (i), 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. i .
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 (fn).
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, a r. Anterior root of spinal nerve.
auv. Auditory vesicle, cer. Cerebrum, ch. Notochord. eh. Epithelial layer of
choroid membrane, gl. Glossopharyngeal nerve, vii. hy. Hyoid branch of seventh
nerve, hym. Hyaloid membrane. //. Lateral line. v. mn. Ramus mandibularis
of fifth nerve, vii. mn. Mandibular (spiracular) branch of seventh nerve, v. mx.
Ramus maxillae superioris of fifth nerve, n I. Nervus lateralis. ol. Olfactory pit.
op. Eye. v. op th. Ramus ophthalmicus of fifth nerve. / ch. Parachordal cartilage.
pfal. Processus falciformis. pp. Head cavity, pr. Posterior root of spinal nerve.
rt. Retina, sp. Spiracle, v. Fifth nerve, vii. Seventh nerve, v c. Visceral cleft.
•vg. Vagus nerve, vgbr. 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, v h. Vitreous humour.
Fig. i. 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.
EXPLANATION OF PLATE I/.
445
Fig. 2. Section through the hinder part of the medulla oblongata, stage between
K and L. Zeiss A, ocul. 2.
It shews (i) the vagus commissure with branches on one side from the medulla :
(i) 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. o th).
Figs. 4 a and 4^. Two horizontal and longitudinal sections through the head of a
Scyllium embryo belonging to stage O. Zeiss a, ocul. i.
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 glosso-
pharyngeal 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 (i) the rudimentary processus falciformis (pfal) giving origin to
the vitreous humour; and (2) the hyaloid membrane (Ay m) 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 em-
bryonic 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
POSTANAL SECTION OF ALIMENTARY CANAL. 447
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 PI. n, 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 (PI. 18, fig. 4, s ces.}.
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 in-
teresting, 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 says1 :
The two germinal layers, epiblast and hypoblast, are continuous with
each other at the border of the germinal disc. The primitive groove or
1 Archiv f. Mic. Anat. Vol. XIII. pp. 194, 195.
448 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 for-
mation 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 per-
sists there for a long time in the form of a large thin-walled vesicle.
The last part of the description beginning at " The con-
nection 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 section1 the history of the alimentary tract was
completed up to stage G.
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 PI. 8, figs. H and /, 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 develope a
terminal dilatation or vesicle, connected with the remainder of
the canal by a narrower stalk. The relation in diameter be-
tween the vesicle and the stalk may be gathered by a com-
parison of figs. 30 and 3^, PI. n. The diameter of the vesicle
represented in section in PI. n, fig. 3, is O'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 (PI. n, fig. $a) with the neural canal, and
behind is continued into two horns (PI. 11, fig. 2, al.) cor-
responding 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 con-
tinuous 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 alimen-
tary tract, without however altering in any of its essential
characters.
1 P- 3°3 et secl-
POSTANAL SECTION OF ALIMENTARY CANAL. 449
Its features at stage K are illustrated by an optical section
of the tail of an embryo (PI. 18, fig. 5) and by a series of trans-
verse sections through the tail of another embryo in PL 18,
figs. 6a, 6b, 6c, 6d. 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. 6a, 6b,
6c, and 6d} out of a fairly-complete series of about one hundred
and twenty.
Posteriorly (fig. 6a) 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. 6b}. Its average diameter is
about '084 Mm. Overlying its front end is the subnotochordal
rod (fig. 6b, 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 1 8, 6c, 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. &/).
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
4SO DEVELOPMENT OF ELASMOBRANCH FISHES.
(PI. 1 1, fig. <)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.
Elasmobranchs 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
PI. 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.
CLOACA AND ANUS. 451
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 PI. n, fig. ga. During the same stage the
segmental ducts grow downwards to the cloaca, and open into it
in the succeeding stage (PI. n, fig. gb). Up to stage" K the
cloaca is connected with the prseanal section of the alimentary
canal in front, and the postanal section behind ; the latter, how-
ever, 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, (i) 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
PI. 19, figs, i a, ib, ic.
The mouth of the cloaca is formed by an involution of the
skin, which is deepest in front and becomes very shallow behind
(PI. 19, figs. I a, ib). 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 (PI. 19, fig. ic) and forming its external opening. Else-
where 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 (PI. 19, fig.
ic, ab.p.} of the skin, which resembles the median cloacal involu-
tion, 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
452 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 for-
wards, 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 elsewhere1, 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.
In Elasmobranchs, 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 Elasmobranchs agree with other Vertebrata,
notably the Fowl2. The abdominal pockets, as might be anti-
cipated from their structure in the adult, are simple involutions
of the epiblast.
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
1 This Edition, No. vn. p. 152.
3 Vide Gasser, Entwicklungsgeschichte der Allantois, etc.
THE THYROID BODY. 453
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 (PI. 15, fig. $a, T/i.}, 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 (PI. 15, fig. $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 ven-
tral 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 PI. 19, fig. 3, th., in longitu-
dinal 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
454 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 MUller1, 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 discon-
nected 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.
In the Bird Dr Muller's figures shew that the thyroid body
developes in the region of the hyoid arch, whereas, in Elasmo-
branchs, it developes in the region of the mandibular arch.
Dr Gotte's2 account of this body in Bombinator accords very
completely with my own, both with reference to the region in
which it developes, and its mode of development.
The pancreas.
The pancreas arises towards the close of stage K as a some-
what 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. i), 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 out-
growth 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 some-
what 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
1 Jenaische Zeitsckrift, Vol. vi.
2 Entwicklungsgeschichte d. Unke.
THE LIVER. 455
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 recep-
tacle 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 contrary1, appear to me seriously
open to doubt.
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 developes 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 n, 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 con-
structed a regular network. As the cylinders increase in length
their lumen becomes very small, but appears never to vanish
(PL 19, ng. 5).
The mode of formation of the liver parenchyma by hollow
and not solid outgrowths agrees with the suggestion made in
1 Lehrbuch d. vergleichenden Embryologie.
DEVELOPMENT OF ELASMOBRANCH FISHES.
the Elements of Embryology, p. 133, and also with the results
of Gotte 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 (PI. II, fig. 9, u. v.) which unites with the sub-
intestinal or splanchnic vein (PL n, 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 Gotte 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 duc-
tus choledochus opens on the ventral side of the intestine im-
mediately in front of the commencement of the spiral valve.
It may be noted that the liver and pancreas are correspond-
ing 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 Gotte1, who not only demonstrated its
existence, but also gave a correct account of its development.
Its presence in Elasmobranchs and mode of development were
mentioned by myself in my preliminary account of the devel-
opment of these fishes2, and it has been independently ob-
served and described by Professor Semper3. 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
1 Archiv fur Micros. Anatomic, Bd. V., and Entwicklungsgeschichte d. Unke.
2 Quarterly Journal of Microscopic Science, Oct, 1874. [This Edition, No. V.]
3 " Stammverwandschaft d. Wirbelthiere u. Wirbellosen " and " Das Urogenital-
system d. Plagiostomen," Arb. Zool. Zoot. Institut. z. Wiirzburg, Bd. 11.
THE SUBNOTOCHORDAL ROD. 457
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.
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 develope. It arises
during stage H in the manner illustrated in PI. 1 1, figs. I and la.
The wall of the alimentary canal becomes thickened (PI. 11,
fig. i) 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 con-
trary, 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 an-
terior 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 develope in the
same way as in the trunk, and the splitting off from the throat
proceeds from before backwards (PL 15, fig. 40 x).
In Torpedo, this rod developes very much later in the Head
than in the trunk ; and indeed my conclusion that it developes
in the head at all is only based on grounds of analogy, since in
B. 30
458 DEVELOPMENT OF ELASMOBRANCH FISHES.
my oldest Torpedo embryo (just younger than K) there is no
trace of it present. In a Torpedo embryo of stage I the sub-
notochordal 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 in-
terposed 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 noto-
chord ; 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 (PI. 18, fig. 6bx). In stage L it is still
fairly large in the tail, though it has begun to atrophy an-
teriorly. We may therefore conclude that its atrophy, like its
development, takes place from before backwards. In the suc-
ceeding stages I have failed to find any trace of it, and con-
clude, as does Professor Semper, that it disappears completely.
Gotte1 is of opinion that the subnotochordal rod is con-
verted 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 men-
tioned, 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.
1 Entwicklungsgeschichte d. Unke, p. 775.
EXPLANATION OF PLATE 1 8. 459
EXPLANATION OF PLATE 18.
COMPLETE LIST OF REFERENCE LETTERS.
Nervous System.
a r. Anterior root of spinal nerve, n c. Neural canal. / r. Posterior root of
spinal nerve, sp n. Spinal nerve, sy g. Sympathetic ganglion.
Alimentary Canal.
al. Alimentary canal, al v. Caudal vesicle of the postanal gut. d al. Cloacal
section of alimentary canal, du. Duodenum, hpd. Ductus choledochus. pan.
pancreas, sees. Solid oesophagus, spv. Intestine with rudiment of spiral valve.
urn c. Umbilical canal.
General.
ao. Dorsal aorta, aur. Auricle of heart, ca v. Cardinal vein. ch. Notochord.
eppp. Epithelial lining of the body-cavity, ir. Interreual body. me. Mesentery.
mp. Muscle-plate, m p I. Muscle-plate sending a prolongation into the limb, p o.
Primitive ovum. pp. Body-cavity, s d. Segmental duct. st. Segmental tube.
ts. Tail swelling, v cau. Caudal vein. x. Subnotochordal rod.
Fig. i. 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. i.
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. i.
30—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, es-
pecially 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,^.).
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 com-
plete 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 pro-
toplasmic 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 this1. In
1 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
THE HEART. 461
front the cavity of the heart is bounded by the approximation
of the splanchnic mesoblast to the wall of the throat, and be-
hind by the stalk connecting the alimentary canal with the
yolk-sack.
As development proceeds the ventral wall of the heart~be-
comes bent inwards on each side on a level with the wall of the
gut (Plate ii, 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 Elasmobranchs any traces of two distinct cavities co-
alescing to form the heart, such as have been recently de-
scribed in Mammals and Birds ; and this, as well as the other
features of the formation of the heart in Elasmobranchs, are in
very close accordance with the careful description given by
Gb'tte1 of the formation of the heart in Bombinator. The di-
vergence which appears to be indicated in the formation of so
important an organ as the heart between Pisces and Amphi-
bians on the one hand, and Aves and Mammalia on the other,
is certainly startling, and demands a careful scrutiny. The
most complete observations 6n the double formation of the
heart in Mammalia have been made by Hensen, Gotte and
Kolliker. These observations lead to the conclusion (i) that
the heart arises as two independent splits between the splanchnic
mesoblast and the hypoblast, each with an epithelioid (endo-
thelial) lining. (2) That the heart is first formed at a period
when the folding in of the splanchnopleure to form tJw throat has
protoplasmic processes. A second layer next becomes split from the splanchnic
mesoblast, connected with the first layer by the above-mentioned protoplasmic pro-
cesses. These two layers form the epithelioid lining of the heart ; between them is
the cavity of the heart, which soon loses the protoplasmic trabeculae which at first
traverse it.
1 Bischoff has recently stated, Historisch-kritische Bemerkungen il.d. Entwickelung
d. Satigethiereier, that Gb'tte 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 Gotte's text
or figures.
462 DEVELOPMENT OF ELASMOBRANCH FISHES.
not commenced, and when therefore it would be impossible for it
to be formed as a single tube.
In Birds almost every investigator since von Baer has de-
tected more or less clearly the coalescence of two halves to
form the unpaired heart1. Most investigators have however
believed that there was from the first an unpaired anterior sec-
tion of the heart, and that only the posterior part was formed
by the coalescence of two lateral halves. Professor Darlste His,
and more recently Kolliker, have stated that there is no such
unpaired anterior section of the heart. My own recent ob-
servations confirm their conclusions as to the double formation
of the heart, though I find that the heart has from the first a
A-shaped form. At the apex of the A 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'2. 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.
In the instances in which the heart arises as a double cavity
it is formed before the complete closttre 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
1 Vide Elements of Embryology, Foster and Balfour, pp. 64-66.
2 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.
THE HEART. 463
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." Gotte again in his great work1 appears to maintain
similar views, though I do not perfectly understand all his state-
ments. In my review of Kolliker's Embryology2 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."
•
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 Ver-
tebrates, is at first double (PI. II, fig. 6 ad), 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
pfaeanal and postanal sections. This vein is shewn in section in
PI. 11, fig. 8, V. It may be called either the subintestinal or
1 Entwicklungsgeschichte d. Unite, pp. 779, 780, 781.
- Journal of Anatomy and Physiology, Vol. X. p. 794.
464 DEVELOPMENT OF ELASMOBRANCH FISHES.
splanchnic vein. At the cloaca, where the gut enlarges and
comes in contact with the skin, this vein is compelled to bi-
furcate (PI. 1 8, 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, PI. 18, fig. 6 c, v. can. In the tail they form what is
usually known as the caudal vein. The venous system of Scyl-
lium 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 re-
markable resemblance which the vascular system of an Elas-
mobranch 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 Elasmobranchs communicate posteriorly
by a capillary system, and in front by the arterial arches, con-
nected like the similar vessels in Annelids with the branchiae.
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 ex-
cept 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 (PI. 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 con-
THE VENOUS SYSTEM. 465
necting it round the cloaca with the caudal vein first vanishes
(PI. n, 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 pos-
terior cardinals open into it some little distance in fronForthe
hind end of the kidneys. By these changes and by the dis-
appearance 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 vessel1, and that its connection with the car-
dinals is entirely secondary.
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 circti/ation 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 Wyman2, 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.
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 blue3.
1 The morphological importance of this point is considerable. It proves, for
instance, that the haemal arches of the vertebrae 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.
2 Memoirs of the American Academy of Arts and Sciences, Vol. ix.
3 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.
466 DEVELOPMENT OF ELASMOBRANCH FISHES.
I shall follow the figures on this plate in my descriptions.
Fig. i 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 advanced1. The blasto-
derm 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 circula-
tion. It gives off branches only on its inner side.
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
1 My figure may be compared with that of Leydig, Rochen und Haie, Plate in.
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.
THE CIRCULATION OF THE YOLK-SACK. 467
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 under-
gone 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 Verte-
brates.
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
468 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Leydig1. In his first researches, RocJien u. Haie, pp.
71, 72, he gives an account of the position and histology of what
is probably my interrenal body2.
The position and relations of the interrenal body vary some-
what according to Leydig in different cases. He makes the fol-
lowing 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 researches3 he abandons this opinion, and adopts the view
that the interrenal body is part of the same system as the supra-
renal 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 arteriae 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
says4, " 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
1 Rochen und Haie and Untersuchung. u. Fische u. Reptilien.
2 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 con-
nection with the kidneys, though I do not fully understand his descriptions.
3 Fische u. Reptilien, p. 14.
4 Rochen u. ffaie, p. 18.
THE VASCULAR GLAND. 469
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.
Stannius alludes1 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 bodies2.
The general text-books of Histology, Kolliker's work, and
Eberth's article in Strieker's Histology, do not give much in-
formation on this subject; but Eberth, without apparently having
examined the point, questions the accuracy of Leydig's state-
ments with reference to the anatomical relations of the sympa-
thetic ganglia and suprarenal bodies.
The last author who has dealt with this subject is Professor
Semper8. 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) :
" Hier freilich gehen sie bei manchen Formen...in einen
Korper iiber, 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 con-
volutions 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.
1 Vergleichende Anatomie, II. Auflage.
2 Stannius' description is not quite intelligible, but appears to point to the ex-
istence 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.
:i " Urogenitalsystem d. Plagiostomen." Arb. zool. zoot. fnst. z. lViirzburg,Vo\.\\.
470 DEVELOPMENT OF ELASMOBRANCH FISHES.
The siiprarenal 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 bodies1. 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 develop-
ment 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.
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, im-
perfectly 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-
1 There is a very good figure of them in Semper's paper, PI. xxi. fig. 3.
THE SUPRARENAL BODIES. 4/1
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, 'O2i 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 sympa-
thetic 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 sympa-
thetic 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 PI. 19, fig. 7. The suprarenal tissue is not
4/2 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 dis-
tributed 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 struc-
ture. 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 sym-
pathetic ganglia. The earliest stages in the development of
these have already been given1, 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 con-
spicuous branches connecting them with the spinal nerves (PI.
1 8, fig. 3). There may be noticed at intervals solid rods of cells
passing from the bodies to the aorta, PI. 18, fig. 2. These rods
are the rudiments of the aortic branches to which the suprarenal
bodies are eventually attached.
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
1 Antea, pp. 394 — 396.
THE SUPRARENAL BODIES. 473
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 PI. 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 them-
selves fairly vascular.
By stage Q (PI. 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 supra-
renal 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: (i) 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
B. 3I
474 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 justifica-
tion 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 develope 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 observa-
tions 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. Lfind
the body forming a small rod elliptical in section in the poste-
rior 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 PI. 18, fig. 8, invested by a fairly thick tunica
propria, which sends in septa, dividing it into rather well-marked
THE INTERRENAL BODY. 475
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
description1. 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 'Oi to -012. The nuclei are remarkably
granular. The septa of the body are provided with a fairly rich
capillary network.
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 2. 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
1 Perhaps the body I am describing is not identical with Leydig's posterior supra-
renal body. I do not, as mentioned above, feel satisfied that it is so from Leydig's
description.
2 Quarterly Journal of Microscopic Science, October, 1874. [This edition No. V.]
31—2
476 DEVELOPMENT OF ELASMOBRANCH FISHES.
by Professor Semper, who figures it at an early stage of develop-
ment, 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 n, fig. ga, sit). 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.
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 (PI. 1 8, 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
EXPLANATION OF PLATE 19. 477
bodies the suprarenal bodies of the higher Vertebrata are homo-
logous. 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, how-
ever, 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, sy g. Sympathetic ganglion.
Alimentary Canal.
d. Cloaca. in cl. Cloacal involution, ce ep. OZsophageal epithelium, pan.
Pancreas, th. Thyroid body.
General.
abp. Abdominal pocket (pore), anr. Auricle. ca v. Cardinal vein. cauv.
Caudal vein. ly. Lymphoid tissue, mm. Muscles, od. Oviduct, pc. Pericardium.
pp. Body cavity, s r. Suprarenal body. it. Ureter, v ao. Ventral aorta (anterior
continuation of bulbus arteriosus). ven. Ventricle, wd. Wolffian duct.
Figs, i a, 1 1>, ic. Three sections through the cloacal region of an embryo belong-
ing to stage O. i a is the anterior of the three sections. Zeiss A, ocul. 2. Reduced
one-third.
i a shews the cloacal involution at its deepest part abutting on the cloacal section
of the alimentary tract.
i d is a section through a point somewhat behind this close to the opening of the
Wolffian ducts into the cloaca.
i 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 aa, ocul. i.
The figure shews the solid thyroid body (th) connected in front with throat, and
terminating below the bulbus arteriosus.
478 DEVELOPMENT OF ELASMOBRANCH FISHES.
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. i. 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. i. 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 (sf n), and the appearance of an indication in the ganglion of a portion
more directly connected with the nerve. Zeiss D, ocul. 2.
Fig. o,. Section through one of the anterior sympathetic ganglia of an embryo of
stage Q, shewing its division into a true ganglionic portion (sy g), 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 chapter1 of this
memoir, and up to the present time no investigator, with the
exception of Dr Alex. Schultz2, 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 unac-
quainted with my earlier descriptions.
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 monograph3 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 in-
vestigations. In Professor Semper's monograph are embodied
the results of a considerable number of preliminary papers pub-
lished by him in his Arbeiten and in the Centralblatt. The
excretory organs of Elasmobranchs have also formed the sub-
1 Chapter vi. p. 345, et set/.
2 Archiv f. Micr. Anat. Bd. XI.
* " Urogenital System d. Plagiostomen," Semper, Arbeiten, Vol. n.
480 DEVELOPMENT OF ELASMOBRANCH FISHES.
ject of some investigations by Dr Meyer1 and by myself2. Their
older literature is fully given by Professor Semper. In addition
to the above-cited works, there is one other paper by Dr Spengel3
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 investi-
gations 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.
Excretory organs and genital ducts in the adult.
The kidneys of Scyllium canicula are paired bodies in con-
tact along the *nedian 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 Semper4 and by myself. .
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
1 Sitzungsberichte d. Natiirfor. Gas. Leipzig, 1875. No. i.
2 " Preliminary account of the development of Elasmobranch Fishes," Qiiarterly
Journal of Microscopical Science, 1874. " Origin and History of the Urinogenital
Organs of Vertebrates," Journal of Anat. and Physiol. Vol. x.
8 Arbeiten, Semper, Vol. in.
* 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.
EXCRETORY ORGANS IN THE ADULT. 481
long, the two glands together measured 8£ centimetres and the
kidney proper only 3^. In the male the Wolffian bodies ex-
tend 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 twg~scxes,
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 PI. 20, fig. I. The se-
cretion 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 (PI. 20, fig. 5).
The main function of the Wolffian duct in the male is, how-
ever, 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 in-
vestigation requires some care. I have reason, from my ex-
aminations of this and other species of Elasmobranchs, to be-
lieve 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. I, PI. 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,
482 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 con-
taining 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 dis-
tinct ducts cut through, one of which was almost on the point of
dividing into two. This second section proves that, in this in-
stance 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 (PI. 20, fig. i, 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 (PI. 20, fig. I, sb). To these
bladders Professor Semper has given the name uterus mascu-
linus, 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
URINARY DUCTS OF THE FEMALE. 483
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 ascer-
tained, taking place between the anterior ones. The arrange-
ment 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 de-
scribed. 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 dis-
crepancy 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 im-
portant one. The urinary cloaca opens, in the female, into the
general cloaca by a median papilla of somewhat smaller di-
mensions than the corresponding papilla in the male. Seminal
484 DEVELOPMENT OF ELASMOBRANCH FISHES.
bladders are absent in the female, though possibly represented
by the bladder-like dilatations of the Wolffian duct. The ovi-
ducts, 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 Elasmobranchs, 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 segment1. 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 cer-
tainty, but in one young example, which had left the egg but a
short time, there appeared to be at least fourteen present. Ac-
cording 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 an-
terior 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.
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
1 The term segment will be more accurately defined below.
SEGMENTAL TUBES. 485
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 (i) a segmental opening, somewhat oval in .
form (st. o) and leading directly into (2) a narrow tube, the seg-
mental tube, which takes a more or less oblique course back-
wards, and, passing superficially to the Wolffian duct (w.d],
opens into (3) a Malpighian body (/. mg) at the anterior ex-
tremity of an isolated coil of glandular tubuli. This coil forms
the fourth section of each segment, and starts from the Mal-
pighian 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 seg-
ment 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 Elasmobranchs. 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 Elasmobranchs 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
486 DEVELOPMENT OF ELASMOBRANCH FISHES.
examples, and sometimes fairly well in old ones, of either sex1.
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.
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 PI. 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. how-
ever, connected with the Malpighian body of their proper seg-
ment, 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, PI. 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.
1 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 VASA EFFERENTIA. 487
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 (PI. 20, fig. 4, r. str}. - 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 PI. 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 refer-
ence 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 Wolf-
fian 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: (i) 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 PI. 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.
488 DEVELOPMENT OF ELASMOBRANCH FISHES.
Professor Semper states that there is but a single vas efferens in
Scyllium canicula, a statement which appears to me unquestion-
ably erroneous. All the vasa efferentia fall into a longitudinal
duct (I. 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 Elasmobranchs, 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 Langscanal 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 ampullae.
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
THE VASA EFFERENTIA.
In the remaining parts of the excretory organs the two species
of Scyllium resemble each other very closely.
As may be gathered from Prof. Samper's monograph, the
excretory organs of Scyllium canicula are fairly typical for Elas-
mobranchs generally. The division into kidney and Wolrrian
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
Wolrrian 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^, 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.
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 (PI. XXI) by Professor Semper, or in Squatina
vulgaris, as I find it, and have represented it on PI. 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 (y. e) connected on the one hand with a longitudinal
canal at the base of the testes (n. t) and orj 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.
1 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.
B. 32
490 DEVELOPMENT OF ELASMOBRANCH FISHES.
Development of tfie 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 Elasmobranchs 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 open-
ings 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 PI. 12, fig. 18^. 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 A -shaped form with an anterior limb
opening into the body-cavity and posterior limb, resting on a
THE SEGMENTAL TUBES. 49 1
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 4s
shewn in longitudinal section on PI. 21, fig. ja, and in transverse
section on PI. 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 A 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 A 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 pro-
ducts of the original segmental tube will be spoken of as a seg-
ment of the kidney. This narrow stalk opens into a vesicle
(PL 1 8, 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 A,
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. (i) 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
32 2
492 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 con-
verted 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 in-
terval 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 Pye1 has
given of the formation of these bodies in the embryonic Mam-
malian 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 seg-
mental tube. Semper does not however enter into full details
on this subject.
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 over-
come 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 repre-
sented. In the hindermost of the three — the one to the right —
1 Journal of Anatomy and Physiology, Vol. IX.
THE MALPIGHIAN BODIES. 493
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 tJie thick-walled collecting
tnbe (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 betwem
stages O and P a connection between each segmental tube and
the collecting tube of tJie 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 whicli 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 frag-
mentary 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 PI. 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 Mal-
pighian 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
494 DEVELOPMENT OF ELASMOBRANCH FISHES.
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
groivth from tJie original vesicle at the end of the segmental tube of
the sitcceeding segment. How the third or fourth accessory Mal-
pighian bodies, when present, take their origin I have not made
out. It is, however, fairly certain that they form the com-
mencement 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 pre-
ceding segment may explain a peculiar observation of Dr
Spengel1 on the kidney of the tailless Amphibians. He finds
that, in this group, the segmental tubes do not open into Mal-
pighian 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 seg-
mental tubes opens, as in the Anura, into the fourth section of a
kidney tubulus.
Development of the Mullerian and Wolffian ducts.
The formation of the Mullerian and Wolfnan 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
1 Loc. cit. pp. 85-89.
MULLERIAN AND WOLFFIAN DUCTS. 495
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 Miillerian duct of higher Vertebrates
and that of Elasmobranchs. 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 seg-
mental duct1, 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 seg-
mental tubes, and the ventral one forms the Mullerian 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 s£g-
mental 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 immedi-
ately behind this a single duct. A series of sections through
the junction of two ducts is represented on Plate 21, figs. I A,
i B, i C, i D.
In my youngest example, in which the splitting had com-
menced, 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 evi-
dence of my earlier embryos appears to shew that the segmental
1 For the development of the segmental duct, vide p. 345, et seq.
496 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 seg-
mental 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 (PI. 21,
fig. i), 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 intes-
tine. In the series represented (PI. 21) I A is the foremost
section, and I D the hindermost. In I A the oviduct (o d) 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 con-
siderably the larger of the two ducts. In i B 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 i C 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 i D 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.
MULLERIAN AND WOLFFIAN DUCTS. 497
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 (PI. 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 Elasmobranchs was
first made known by Putmann and Garman1, and subsequently
discovered independently by Semper2.
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 Miillerian duct, the latter
continuous with the anterior section of the segmental duct,
which carries the abdominal opening. The differences in deve-
lopment between the two sexes are, in spite of a general similarity,
1 "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,
1X74-
2 Loc. cit.
498 DEVELOPMENT OF ELASMOBRANCH FISHES.
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- (PI. 2 1 , fig. 6).
It does not even form an unbroken cord, but is divided in dis-
connected 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 Mullerian duct by stage O
than by stage N. By stage P the posterior portions of the
Mullerian 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 Mullerian 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 tJian 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. (i) 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 Mullerian duct
in the male agrees very closely with that of Professor Semper
for Acanthias. For Scyllium however he denies, as it appears to
MULLERIAN DUCT IN BIRDS. 499
me erroneously, the existence of the posterior rudimentary parts
of the Mullerian duct. He further asserts that the portions of
the Mullerian 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 Mullerian duct of Elasmobranchs and the Mullerian duct of
Birds, than if Professor Semper's account of the development of
the oviduct is the correct one. Both Professor Semper and my-
self 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 Semper1 finds himself compelled to
reject, on theoretical grounds, the testimony of recent observers
on the development of the Mullerian 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 account2, the ordinary
statements with reference to the development of the Mullerian
duct in Birds are accepted ; but it is suggested that the indepen-
dent development of the Mullerian 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.
Since finding what a small portion of the segmental duct
became converted into the Mullerian duct in Elasmobranchs, I
have reexamined the development of the Mullerian duct in the
Fowl, in the hope of finding that its posterior part might develope
nearly in the same manner as in Elasmobranchs, at the expense
of a thickening of cells on the outer surface of the Wolffian duct.
1 Loc. cit. pp. 412, 413.
4 " The Urinogenital Organs of Vertebrates," Journal of Anatomy and Physiology*
Vol. X. p. 47. [This edition, p. 164.]
5<DO DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Mullerian 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 Miillerian 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 Mullerian duct is the front extremity of the segmental
duct in Elasmobranchs.
Although the evidence I can produce in the case of the
Fowl of a direct participation of the Wolffian duct in the for-
mation of the Mullerian 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 Mullerian duct in Birds and Elasmobranchs.
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 Mullerian
duct in Elasmobranchs 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 Mullerian duct in Elasmobranchs, evidence
that a change has already appeared in this group in the direction
of a development of the Mullerian 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
Mullerian duct. An analogous change, in a somewhat different
direction, would seem to be taking place in the development
of the rudimentary Mullerian duct in the male Elasmobranchs.
URINAL CLOACA. 50 1
It is, perhaps, just worth pointing out, that the blindness of
the oviduct of female Elasmobranchs, and its mode of develop-
ment from an imperfect splitting of the segmental duct, may
probably be brought into connection with the blindness of the
extremity of the Mullerian 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 mistake1. Professor Semper
has, however, subsequently done me the honour to discuss, at
considerable length, my original errors, and to attempt to ex-
plain them. Since it appears to me improbable that the con-
tinuation 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.
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 (PI. 19, fig. I 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 seg-
ments of the primitive undivided excretory organ commence to
undergo changes which result in their separation from the
1 Journal of Anatomy and Physiology, Vol. X. 1875. [This edition, No. VII.]
502 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 back-
wards, 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 (PI. 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 seg-
ments. The original opening of each tube into the Wolffian
duct is situated at the anterior end of this elongated attach-
ment, 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 com-
paring figs. 7 a and 7 b, PI. 21 — two longitudinal vertical sec-
tions 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
THE URETERS. 503
and Wolffian duct takes place entirely at the expense of the
former. Owing to the length of this attachment, every trans-
verse 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 PI. 21, fig. 9, u, but
more conclusively in the series of transverse sections represented
on PI. 21, figs. 3 A, 3 B, 3 C. In the hindermost of these (3 C)
is seen the solid terminal point of a ureter, while the same
ureter possesses a lumen in the two previous sections, but ex-
hibits 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 in-
clined 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 in-
complete tube. This peculiarity is clearly shewn in the middle
figure of the series on PI. 21, fig. 3 B.
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 pro-
portionately 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 repre-
504 DEVELOPMENT OF ELASMOBRANCH FISHES.
sented on PL 21, fig. 9, or on a larger scale in fig. 9 A. 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
(PI. 21, fig. 4). The peculiarities in the appearance of the
dorsal wall of the Wolffian duct in fig. 9 A, and the difference
between the cells composing it and those of the ventral wall,
become intelligible on comparing this figure with the repre-
sentation of transverse section in figs. 3 B and 3 C, 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 Miillerian 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 PI. 21, fig. 8, u.
They next commence to develope into complete and in-
dependent tubes by their side walls growing inwards and meet-
ing below so as to completely enclose their lumen. This is seen
already to have occurred in most of the posterior ureters in
PI. 21, fig. 8.
Before stage P the ureters cease to be united into a con-
tinuous 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}t
Above this again is the Wolffian duct (w. d), and still dorsal to
THE VASA EFFERENTIA. 505
this are four ureters (#). 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 six1, instead of four, ureters.
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 Elasmo-
branchs, 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 Elasmobranchs, and
the following extracts will fully illustrate his views with reference
to them.
" In2 dem friihesten Stadium finden sich wie friiher angegeben
ungefahr 34 Trichter in der Leibeshohle, von diesen gehen die
27 hintersten in die persistirenden Segmentaltrichter u'ber, von
denen 4 beim erwachsenen Thiere auf dem Mesorchium stehen.
1 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.
'-' I.oc. cit. p. 364.
B. 33
5O6 DEVELOPMENT OF ELASMOBRANCH FISHES.
Die tibrigen 7 schliessen sich vollstandig ab zu den erwahnten
langlichen und spater mannigfach auswachsenden varicosen
Trichterblasen ; von diesen sind es wiederum 3 — 4 welche unter-
einander in der Langsrichtung verwachsen und dadurch den in
der Basis der Hodenfalte verlaufenden Centralcanal des Hodens
bilden. Ehe aber diese Verwachsung zu einem mehr oder
minder geschlangelten Centralcanal vollstandig wird, hat sich
einmal das Lumen der Trichterblasen fast vollstandig geschlossen
und ausserdem von ihnen aus durch Verwachsung und Knospung
die erste Anlage des rete vasculosum Halleri gebildet (Taf. XX.
Figs, i, 2 c). Es erstreckt sich namlich mehr oder minder weit
in die Genitalfalte hinein ein unregelmassiges von kleinen Zellen
begranztes Canalnetz welches zweifellos mit dem noch nicht
ganz vollstandigen Centralcanale des Hodens (Taf. XX. Fig. 2 c]
in Verbindung steht. Von diesem letzteren aus gehen in regel-
massigen Abstanden die Segmentalgange (Taf. XX. Fig. 2 sg.}
gegen die Niere hin ; da sie meist stark geneigt oder selbst
geschlangelt (bei 6ctm langen Embryonen) gegen die Niere zu
verlaufen, wo sie sich an die primaren Mafyighi'schen Korper-
chen und deren Bildungsblasen ansetzen, so kann ein verticaler
Querschnitt auch nie einen solchen nun zum vas efferens gewor-
denen Segmentalgang seiner ganzen Lange nach treffen. Gegen
die Trichterfurche zu aber steht namentlich am hinteren Theile
der Genitalfalte der Centralcanal haufig noch durch einen kurzen
Zellstrang mit dem Keimepithel der Trichterfurche in Ver-
bindung; mitunter findet sich hier sogar noch eine kleine
Hohlung, Rest des ursprunglich hier vorhandenen weiten
Trichters" (Taf. XX. Fig. 3^).
And again : " Dieser1 Gegensatz in der Umbildung der Seg-
mentalgange an der Hodenbasis scheint nun mit einem anderen
Hand in Hand zu gehen. Es bildet sich namlich am Innenrande
der Niere durch Sprossung und Verwachsung der Segmentalgange
vor ihrer Insertion an das primare Malpighi'sche Korperchen
ein Canal beim Mannchen 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
Segmentalgange, aber von diesen letzteren stehen nur 5 mit dem
1 Loc. cit. p. 395.
THE VASA EFFERENTIA. $°7
Hodennetz in Verbindung. Dort nun wo diese letzteren sich an
den Niercnrandcanal ansetzen (Taf. XXI. Fig. 13 sg.t — sg.6) findet
sich jedesmal ein typisch ausgebildetes Malpightsc\\es Korper-
chen, mit dem aber nun nicht mehr wie ursprtinglich nur 2 Canale
verbunden sind (Taf. XXI. Fig. 14) sondern 3. Einer dieser
letzteren ist derjenige Ast des Nierenrandcanals welcher die Ver-
bindung mit dem nachst folgenden Segmentalgang zu besorgen
hat. An den Stellen aber wo sich an den Nierenrandcanal die
hinteren blind gegen den Hoden hin endenden Segmentalgange
ansetzen fehlen diese Malpighischen Korperchen (Taf. XXI. Fig.
13 sg7] vollstandig. Auch bei Mustelus (Taf. XV. Figs. 8, 10) findet
genau dasselbe Verhaltniss statt; da aber hier nur 2 (oder 3)
Segmentalgange zu vasa efferentia umgewandelt werden, so
stehen hier am kurzen Randcanal der Niere auch nur 2 oder 3
Malpighi'schz Korperchen. Diese aber sind typisch ausgebildet"
(Taf. xv. Fig. 10).
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 Elasmobranchs. 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
33—2
508 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 Elasmobranchs, it will not easily be credited that
they develope 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 Elasmobranchs 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 effe-
rentia 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 PI. 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 PI. 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,
THE VASA EFFERENTIA. 509
extremely hazardous. If, however, this body really is the
remnant of a segmental opening, it would be reasonable to con-
clude 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
(PI. 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 longi-
tudinal 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 (PI. 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 Vertebrates1. Although Kolliker's2
discovery of the segmental tubes in Aves, and the researches of
Spengel3, Gasser4, Ewart6 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
1 Journal of Anatomy and Physiology, Vol. X. [This edition, No. vn.]
2 Entwicklungsgeschichte des Menschen u. der hoheren Thiere.
3 Loc. cit.
4 Beitrage zur Entwicklungsg. d. Allantois d. Muller 'schen Gange u. d. Afters.
6 "Abdominal Pores and Urogenital Sinus of Lam prey, "Journal of Anatomy and
Physiology, Vol. X. p. 488.
5io
DEVELOPMENT OF ELASMOBRANCH FISHES.
repeat them in this place. I conclude the chapter with a resume
of the development of the urinogenital organs in Elasmobranchs
from their first appearance to their permanent condition.
Resume. — 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. $A.,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. 5 B, p. d]. The knob projects
FIG. 5.
Two SECTIONS OF A PRISTIURUS EMBRYO WITH THREE VISCERAL CLEFTS.
spn
spn
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; me. 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. splanchno-
pleure; pp. pleuroperitoneal or body-cavity; ep. epiblast; al. alimentary canal.
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.
While the lumen is gradually pushing its way backwards
along the solid rudiment of the segmental duct, the first traces
RESUME OF URINOGENITAL SYSTEM. 511
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) (i)
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 dia-
grammatically represented on the woodcut, fig. 6. In this fig.
FIG. 6.
DIAGRAM OK 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 Mullerian duct below; st.
segmental tubes. They open at one end into the body-cavity, and at the other into
the segmental duct.
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
512
DEVELOPMENT OF ELASMOBRANCH FISHES.
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.
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 (i) Wolffian
duct dorsally, which remains continuous with the excretory
FIG. 7.
DIAGRAMMATIC REPRESENTATION OF A TRANSVERSE SECTION OF A SCYLLIUM
EMBRYO ILLUSTRATING THE FORMATION OF THE WOLFFIAN AND MULLERIAN
DUCTS BY THE LONGITUDINAL SPLITTING OF THE SEGMENTAL DUCT.
me. medullary canal; mp. muscle-plate; ch. notochord ; ao. aorta; ca v.
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. Miillerian 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 ; /. liver ; i. intestine with spiral valve.
RESUME OF URINOGENITAL SYSTEM. 513
tubules of the kidney, and ventrally (2) the oviduct or Mullerian
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 (PI. 21, fig. I A, 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 Mullerian duct, being shorter, and in the
column of cells with which it is continuous being from the first
incomplete.
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 (PI. 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 hindermostof 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
514 DEVELOPMENT OF ELASMOBRANCH FISHES.
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 correspond-
ing with the numerous ducts of the other type (woodcut, fig. 8).
It seems that both in Amphibians and Elasmobranchs 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 Elasmobranchs1. 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.
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 remark-
able 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 ampullae (woodcut 9, nf). 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.
1 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.
RESUME OF URINOGENITAL SYSTEM.
515
FIG. 8.
DIAGRAM OF THE ARRANGEMENT OF THE URINOGENITAL ORGANS IN AN ADULT
FEMALE ELASMOBRANCH.
in. d. Mullerian duct; iv. 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 repre-
sented 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 Mullerian duct (m.d] split off from the
segmental duct of the kidneys. Each oviduct opens at its an-
terior extremity into the body-cavity, and behind the two ovi-
ducts have independent communications with the general cloaca.
(2) The Wolffian ducts (w. d}, the other product of the seg-
mental ducts of the kidneys. They end in front by becoming
continuous with the tubulus of the anterior segment of the
Wolman body on each side, and unite behind to open by a com-
mon 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. /), 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
5i6
DEVELOPMENT OF ELASMOBRANCH FISHES.
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.
FIG. 9.
DIAGRAM OF THE ARRANGEMENT OF THE URINOGENITAL ORGANS IN AN ADULT
MALE ELASMOBRANCH.
tc
m. d. rudiment of Miillerian duct; w. d. Wolffian duct, marked vd in front
and serving as vas deferens ; 5/. 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; Ic. longitudinal canal of the
Wolffian body.
In the male the following parts are present (woodcut 9) :
(1) The Miillerian duct (md), consisting of a small rudi-
ment 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 consti-
tution as in the female.
(4) The segmental tubes (st). The posterior of these have
the same arrangement in both sexes, but in the male modifica-
tions 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 (i) 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
POSTSCRIPT. 517
longitudinal canal of the Wolffian body (l.c}. From the latter
are seen passing off the successive tubuli of the anterior seg-
ments 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, how-
ever, of my work a number of novel and unexpected points
turned up, which have considerably protracted my investiga-
tions, 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.
5l8 DEVELOPMENT OF ELASMOBRANCH FISHES.
EXPLANATION OF PLATES 20 AND 21.
COMPLETE LIST OF REFERENCE LETTERS.
a mg. Accessory Malpighian body. cav. Cardinal vein. ge. Germinal epithelium.
k. True kidney. /. 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 Miillerian duct
of the female, od' . Miillerian 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, r st. Rudimentary segmental tube. tu. Ureter commencing to be formed.
s b. Seminal bladder, s d. Segmental duct, s t. Segmental tube, st o. Opening of
segmental tube into body-cavity, sur. Suprarenal body. t. Testis. it. Ureters.
ve. Vas efferens. w b. Wolffian body, w d. Wolffian duct.
PLATE 20.
Fig. r. 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 por-
tion 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 (w d) 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 (r st) 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 iri
the Wolffian body, but this could not be clearly made out.
EXPLANATION OF PLATES 2O AND 21. 519
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 (r st ?).
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. Tliere
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 Mal-
pighian bodies these ducts are continuous with the several coils of the Wolfnan 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, i A, i B, i C, i D. 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. r A 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. 3 A, 3 B, 3 C. Three sections illustrating the formation of a ureter in a
female embryo belonging to stage N. Zeiss B, ocul. 2.
3 A is the foremost section.
The figures shew that the lumen of the developing ureter is enclosed in front by
an independent wall (fig. 3 A), 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 Wblffian duct formed by the overlapping ureters, the lumens of which
appear as perforations in it. It should be compared with fig. 9 A, 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.
520 DEVELOPMENT OF ELASMOBRANCH FISHES.
The section illustrates (i) the formation of a Malpighian body (nig) from the
dilatation at the end of a segmental tube, (2) the appearance of the rudiment of the
Miillerian duct in the male (od1).
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. i.
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 commenc-
ing 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 Scy Ilium 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.
9 A. 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 OvuM1.
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 sub-
ject 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: (i) the changes attending the ripening of the
ovum, wJiich are independent of impregnation ; (2) the changes
which are directly due to impregnation.
Every ovum as it approaches maturity is found to be composed
(Fig. i) of (i) a protoplasmic body or vitellus usually containing
yolk-spherules in suspension; (2) of a germinal vesicle or nucleus,
FIG. i.— Unripe ovum of Toxopneustes lividus (copied from Hertwig).
1 From the Quarterly Journal of Microscopical Science, April, 1878.
. 34
522 MATURATION AND IMPREGNATION OF THE OVUM.
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. i). The germinal spot forms a nearly homo-
geneous 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 peculiari-
ties 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: — (i) 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 : (i) By
one set the germinal vesicle is stated to completely disappear
and not to be genetically connected with the subsequent nuclei
MATURATION AND IMPREGNATION OF THE OVUM. 523
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 dis-
appearance 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 RicJitungskorper 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 (I5)1 in this direction
deserve special mention, as having in a sense formed the founda-
tion 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. Loven, 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
1 The numbers appended to authors' names refer to the list of publications at the
end of the paper.
34—2
524 MATURATION AND IMPREGNATION OF THE OVUM.
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 Gotte 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.
Coming to the more modern period the researches of five
workers, viz. Biitschli, E. van Beneden, Fol, Hertwig, and
Strasburger have especially thrown light upon this difficult sub-
ject. 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 \ho. female pronudeus , the fate of which
is recorded in the second part of this paper. The researches of
Biitschli and van Beneden have been especially instrumental in
demonstrating the relation between the polar bodies and the ger-
minal 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 con-
clude 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
MATURATION AND IMPREGNATION OF THE OVUM. 525
vesicle assumes an excentric position, and fuses with the peri-
pheral 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 nucleo-
plasmic 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 dis-
appearance.
Though there are reasons for doubting the accuracy of all the
above details on the ovum of the rabbit, nevertheless, the obser-
vations 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 Butschli 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 Ncphelis, Lymnaeus,
Cucullanus,and other Nematodes; and Rotifers. In all of these,
with the exception of Rotifers, he finds polar bodies, and in this
526 MATURATION AND IMPREGNATION OF THE OVUM.
respect his observations are of value as tending to shew the
wide-spread existence of these structures. Negative results with
reference to the presence of the polar bodies have, it may be re-
marked, only a very secondary value. Biitschli has made the
very important discovery that in perfectly ripe eggs of Nephelis,
Lymnaeus 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 meta-
morphosed 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. Biitschli has been unable to find
the spindle modification of the germinal vesicle, but he states
that the germinal vesicle undergoes degeneration, its outline be-
coming 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 de-
scription of Biitschli resembles in some respects that given by
van Beneden of the changes in the rabbit's ovum, and not im-
possibly refers to a nearly identical series of phenomena. The
discovery by Biitschli 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 Biitschli, 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 (n) on the eggs of one of the com-
mon sea urchins (Toxopneustes lividus), in which he attempted to
shew that part of the germinal vesicle, at any rate, was con-
cerned 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 Toxop-
neustes, and that the whole germinal vesicle was absorbed, with
the exception of the germinal spot which remained in the egg as
the female pronucleus.
MATURATION AND IMPREGNATION OF THE OVUM. 527
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 proto-
plasm. Its membrane becomes dissolved and its contents dis-
integrated 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 Butschli's monograph, O. Hertwig (12)
continued his researches on the ova of Leeches (Hcemopis and
Ncphelis), 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 Butschli'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 frag-
ments. 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 Butschli. At
the point where one of tlie 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 pro-
tuberance, 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 pro-
cess of cell-division and not, as Butschli 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
528 MATURATION AND IMPREGNATION OF THE OVUM.
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 un-
dergoes 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 con-
cerns 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 develop-
ment 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
Biitschli 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 con-
cerned in the formation of the polar cells in the way described
by Hertwig.
Giard (10) gives a somewhat different account of the be-
haviour of the germinal vesicle in Psammechinus miliaris. At
maturity the contents of the germinal vesicle and spot mix
MATURATION AND IMPREGNATION OF THE OVUM. 529
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 de-
scribed by Fol. Vide the account of Fol's observations on p. 531.
Strasburger, from observations on Phallnsia, 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 un-
dergo a peculiar metamorphosis. It exhibits frequent changes
of form, its membrane becomes gradually absorbed and its out-
line 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.
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
53O MATURATION AND IMPREGNATION OF THE OVUM.
FIG. 2. — Ripe ovum of Asterias glacialis enveloped in a mucilaginous envelope, and
containing an excentric germinal vesicle and germinal spot (copied from Fol).
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).
FIG. 4. — Ovum of Asterias glacialis, shewing the clear spaces in the place of the
germinal vesicle. Fresh preparation (copied from Fol).
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.
MATURATION AND IMPREGNATION OF THE OVUM. 531
FIG. 5. — Ovum of Asterias glacialis, at the same stage as Fig. 4, treated with picric
acid (copied from Fol).
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.
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 con-
sisting 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 striae 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
532 MATURATION AND IMPREGNATION OF THE OVUM.
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 this1 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.
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
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).
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
1 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.
MATURATION AND IMPREGNATION OF THE OVUM. 533
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 com-
pact rounded body. He has not been able to arrive at a conclu-
sion 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
FK;. 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).
enclosed portion of the spindle becomes partially constricted off
from the egg as the first polar body (Fig. 8). The part of the
FIG. 8. — Portion of the ovum of Asterias glacialis, with the first polar body as it
appears when living (copied from Fol).
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
FIG. 9. — Portion of the ovum of Asterias glacialis immediately after the formation of
the second polar body. Picric acid preparation (copied from Fol).
534 MATURATION AND IMPREGNATION OF THE OVUM.
the portion of the spindle remaining in the egg becomes con-
verted into two or three clear vesicles (Fig. 10) which soon
unite to form a single nucleus, the female pronucleus (Fig. n).
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).
FIG. u. — Ovum of Asterias glacialis with the two polar bodies and the female
pronucleus surrounded by radial striae, as seen in the living egg (copied from Fol).
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.
MATURATION AND IMPREGNATION OF THE OVUM. 535
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 break-
ing 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 Oellacheron
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 uni-
versal in the animal kingdom, but the present state of our know-
ledge 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
536 MATURATION AND IMPREGNATION OF THE OVUM.
and by Biitschli, we have instances of a different mode of for-
mation 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 exist-
ing 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 J and Arthropoda, with a few doubtful exceptions, in
which the polar cells cannot as yet be said to have been satis-
factorily observed.
Whatever may be the eventual result of more extended inves-
tigation, 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 : (i) 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
1 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.
MATURATION AND IMPREGNATION OF THE OVUM. 537
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 neces-
sary 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 pro-
cess 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 Biit-
schli, takes place during conjugation in Infusoria as a preliminary
to the formation of a fresh nucleus. This comparison is due to
Butschli, 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 develope parthenogenetically.
Curiously enough the two groups in which parthenogenesis most
frequently occurs in the ordinary course of development (Arthro-
poda 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,
B- 35
538 MATURATION AND IMPREGNATION OF THE OVUM.
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 tJie polar cells ;
so that in cases, e.g. Arthropoda and Rotifera, wJiere polar cells are
not formed, and an essential part of the nucleus not therefore
removed, parthenogenesis can much more easily occur titan 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 impreg-
nation is the normal occurrence. The genuineness of all the
observations on this head is too long a subject to enter into
here1, 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.
The remarkable observations of Professor Greeff (19) on the
parthenogenetic development of the eggs of Asterias rubens tell,
however, very strongly against this explanation. Greefif has
found that under normal circumstances the eggs of this species
of starfish will develope 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 Greeffs 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 per-
mitted to wait for further confirmation before absolutely accepting
them.
1 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. fiir iviss. Zool, Bd. xxn. p. 202.
MATURATION AND IMPREGNATION OF THE OVUM. 539
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 Astcrias glacialis, is again my source of informa-
tion. 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 them-
selves 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
\.\\Q female pronudeus*. 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 pro-
minence, 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.
1 According to Hert wig's most recent statement a nucleolus is present in this
nucleus
35—2
540 MATURATION AND IMPREGNATION OF THE OVUM.
FIG. 12.
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).
FIG. 14. — Portion of the ovum of Asterias glacialis after the entrance of a spermato-
zoon 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 forma-
MATURATION AND IMPREGNATION OF THE OVUM. 54!
tion the protoplasm in its neighbourhood assumes a radiate
arrangement (Fig. 15). At whatever point of the egg the
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).
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).
FIG. 16. — Three successive stages in the coalescence of the male and female pronu-
cleus 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,
542 MATURATION AND IMPREGNATION OF THE OVUM.
FIG. 17. — Ovum of Asterias glacialis, after the coalescence of the male and female
pronucleus (copied from Fol).
shewing the presence of two nuclei before the commencement
of segmentation. Biitschli was the earliest to state from ob-
servations on Rliabditis dolicJiura that the first segmentation
nucleus arose from the fusion of two nuclei, and this was sub-
sequently shewn with greater detail for A scans nigrovenosa, by
Auerbach (i). Neither of these authors gave at first the correct
interpretation of their results. At a later period Biitschli (5)
arrived at the conclusion that in a large number of instances
(Lymtuzus, 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 P/iallusia, though he has
since withdrawn it. Though Biitschli's statements depend, as
it seems, upon a false interpretation of appearances, he never-
theless 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 sperma-
tozoon into the egg and the formation from it of the male
pronucleus.
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
MATURATION AND IMPREGNATION OF THE OVUM. 543
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 observa-
tions not having all been made upon the same species. HeTtwig
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 striae 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 Ncmatodes impregna-
tion 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 Toxopmustes 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
544 MATURATION AND IMPREGNATION OF THE OVUM.
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 pronu-
cleus 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 sper-
matozoon forms a separate pronucleus with a surrounding sun ;
and several male pronuclei usually fuse with the female pro-
nucleus. 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 con-
tradiction with the more recent results of Selenka. In Toxo-
pneustes 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 sperma-
tozoon forms a separate pronucleus and sun.
MATURATION AND IMPREGNATION OF THE OVUM. 545
It may be noticed that, while the observations of Fol and
Hertwig were admittedly made upon eggs in which the impreg-
nation 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 spermato-
zoon, though in spite of certain conflicting evidence the balance
would seem to incline towards the side of a single spermato-
zoon1.
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 cell2.
The spermatic cells originate from cells (in the case of Verte-
brates 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.
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.
1 The recent researches of Calberla on the impregnation of the ovum of Petromyzon
Planeri support this conclusion.
8 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.
546 MATURATION AND IMPREGNATION OF THE OVUM.
•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 im-
pregnation 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.
(u) Appearance of radial striae round the male pronucleus
which gradually travels towards the female pronucleus.
(12) Fusion of male and female pronuclei to form the first
segmentation nucleus.
MATURATION AND IMPREGNATION OF THE OVUM. 547
List of important recent Publications on tJie Maturation and
Impregnation of t/ie Ovum.
1. Auerbach. Organologische Studien, Heft 2.
2. Bambeke. " Recherches s. Embryologie des Batraciens." Bull,
de I'Acad. royale de Belgiquc, 2me se*r., t. LXI, 1876.
3. E. Van Beneden. "La Maturation de 1'CEuf des Mammiferes."
Bull, de I'Acad. royale de Belgique, 2me se"r., t. XL, no. 12, 1875.
4. E. Van Beneden. " Contributions a PHistoire de la Vdsicule Ger-
minative, &c." Bull, de I'Acad. royale de Belgique, 2me seV., t. XLI, no. i,
1876.
5. Biitschli. Eiselle, Zelltheilung, und Conjugation der Infusorien.
6. Flemming. "Studien in d. Entwickelungsgeschichte der Najaden."
Sitz. d. k. Akad. Wien, B. LXXI, 1875.
7. Fol. "Die erste Entwickelung des Geryonideneies." Jenaische
Zcitschrift, Vol. VII.
8. Fol. "Sur le DeVeloppement des Pteropodes." Archives de
Zoologie Experimental et Gendrale, Vols. IV and v.
9. Fol. "Sur le Commencement de I'Hdnoge'nie." Archives des .
Sciences Physiques et Naturelle*. Geneve, 1877.
10. Giard. Note sur les premiers phtnomenes du developpement de
rOursin. 1877.
11. Hertwig, Oscar. "Beit. z. Kenntniss d. Bildung, &c., d. thier.
Eies." MorphologiscJies Jahrbuch, Bd. I.
12. Hertwig, Oscar. Ibid. Morphologisches Jahrbuch, Bd. in, Heft. i.
13. Hertwig, Oscar. "Weitere Beitrage, &c." Morphologisches
Jahrbuch, Bd. ill, Heft 3.
14. Klein enberg. Hydra. Leipzig, 1872.
15. Oellacher, J. " Beitrjige zur Geschichte des Keimblaschens im
Wirbelthiereie." Archiv f. micr. Anat., Bd. vin.
1 6. Selenka. Befruchtung u. Theihing des Eies von Toxopneustes
variegatus (Vorliiufige Mittheilung). Erlangen, 1877.
17. Strasburger. Ueber Zellbildung u. Zelltheilung. Jena, 1876.
1 8. Strasburger. Uebcr Befruchtung u. Zelltheilung. Jena, 1878.
19. R. Greeff. " Ucb. d. Bau u. d. Entwickelung d. Echinodermen."
Sitzitn. der Gesellschaft 2. Befbrderung d. gesammten Naturiviss, z.
Marburg, No. 5. 1876.
548 MATURATION AND IMPREGNATION OF THE OVUM.
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. fur 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*.
(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 : — i. 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. Ludvvig, is contained in his important work, on the
' Formation of the Ovum in the Animal Kingdom V Ludwig
arrives at the conclusion that the ovum and the follicular epithe-
lium are both derived from the germinal epithelium, and enters
into some detail as to their formation. Schultz 3, without appa-
rently being acquainted with Ludwig's observations, has come to
very similar results for Torpedo.
1 From the Quarterly Journal of Microscopical Science, Vol. 18, 1878.
- Arbeit en a. d. zool.-zoot. Instil ut Wiirzburg, Bd. I.
3 Archivf. micr, Anat. Vol. xi.
550 THE STRUCTURE AND DEVELOPMENT
Semper 1, in his elaborate memoir on the urogenital system of
Elasmobranchs, 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 (Ureierernester),
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.
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. (i) the history of the ovarian
ridge itself, and (2) the history of the ova situated in it. I pro-
pose dealing in the first place with the ovarian ridge.
TJie 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
O'l 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 mem-
brane is more distinct than before ; in other respects no changes
1 Arbeiten a. d. zool.-zoot. Institut Wiirzburg, Bel. II.
OF THE VERTEBRATE OVARY. 551
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 differ-
ence 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 PI. 24, fig. i) 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 O'O5 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 ovariaTi
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 em-
bryos, the thickness of the epithelium was slightly greater than
in the latter, viz. 0*09 mm. as compared with o-o8. 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
552 THE STRUCTURE AND DEVELOPMENT
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 (PI. 24, fig. 2) the breadth
of the ovarian epithelium was O'5, but its height only o-o6 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 (PI. 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, O'I2 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 pro-
jections 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
OF THE VERTEBRATE OVARY. 553
will appear in the next stage. The protoplasm of the cells com-
posing 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 (PI. 24, fig. 3, sfr) 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 07 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 PI. 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 PI. 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. canicnla,
important changes have taken place in the constitution of
ovarian epithelium. Fig. 8, PI. 24, represents a portion of the
ovarian epithelium, on the same scale as figs. I, 2, 3, &c, and
fig. 9 a section through the whole ovarian ridge slightly magni-
fied. Its breadth is now 1*3 mm., and its thickness 03 mm.
B. 36
554 THE STRUCTURE AND DEVELOPMENT
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 — (i) 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-
epitlielium.
The greater part of the germinal epithelium forms anasto-
mosing 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 THE VERTEBRATE OVARY. 555
of Scylliuni stellare, i6£ centimetres in length, a section of
which is represented in PI. 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 Pfluger. 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. stellarc, 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 O'(X)6 mm., in the present one it
is about o-i6 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-epWielium 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, aie
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
36—2
556 THE STRUCTURE AND DEVELOPMENT
Semper attempts to bring forward embryological proofs in
support of this position.
If the series of ovaries which I have represented be ex-
amined, it will not, I think, be denied that the general appear-
ances 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
OF THE VERTEBRATE OVARY. 557
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 3 mm. in
breadth, and O'8 mm. in thickness, the stroma of the ovarian
region has assumed a far more formed aspect than before. It
consists (PI. 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 im-
perfectly developed fibrous layer, forming a kind of tunic, in
which are imbedded the relatively reduced epithelial trabeculae
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. Tire ovarian region is honey-
combed 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 ex-
tremities (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
558 THE STRUCTURE AND DEVELOPMENT
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-proto-
plasm 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 con-
stitutes 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
OF THE VERTEBRATE OVARY. 559
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 O'O3 mm. The larger nuclei have a diameter of ftbout
O'i6 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 (PI. 24, fig. i) 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 proto-
plasm 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, PI. 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 de-
scribed 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 primi-
tive 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 remark-
able 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 (PI. 24, fig. 11, d. ;/.).
560 THE STRUCTURE AND DEVELOPMENT
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 mem-
brane, 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 /act 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 BUtschli, Auerbach, &c.\ 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 nvuclei 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 fol-
lowing two tables shew the dimensions of the parts of three
unmodified and of three modified nuclei taken at random.
Primitive ova with unmodified nuclei —
Nuclei
o'oi 4 mm.
o-oi 2 mm.
o'oi mm.
Primitive ova tvitk modified nuclei —
Granular
Nuclei. Bodies in Nuclei.
O'oi 8 mm O'oo6 mm.
o'oiS mm 0-006 mm.
O'oi 2 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 :
1 Loc. cit. p. 361.
OF THE VERTEBRATE OVARY. 561
Unmodified nuclei of normal primitive ova —
o'oi 4 mm.
o'oi 6 mm.
o-oi4 mm.
o'oi6 mm.
o'oi 6 mm.
Nuclei of primitive ova ivitJi modified nuclei —
Granular
Nuclei. Bodies in Nuclei.
o'oiS mm o'ooS mm.
ox>i6 mm O'ooS mm.
o'oi 6 mm o'oi mm.
ox>i6 mm. ......
o'oi 8 mm
These figures bring out with clearness the following points :
(i) 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 Ureierncster 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 trabeculae which tra-
verse the germinal epithelium. Ovaries differ considerably as
562 THE STRUCTURE AND DEVELOPMENT
to the time and completeness of the disappearance, of the out-
lines 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 (PI. 24, fig. 12). In the same
ovary other nests are present in which the outlines of the indi-
vidual ova are no longer visible. The section represented on
PI. 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 in-
stance 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 in-
crease 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. 1 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 O'O5 mm. in diameter; the latter reach O'l mm. Scat-
tered 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 centimetres, and
even in still younger embryos, further changes are observable.
OF THE VERTEBRATE OVARY. 563
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 extremi-
ties, 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 PI. 25, fig. 17; between it and the older granular variety
there is an infinite series of gradations, many of which are repre-
sented on PI. 24, figs. 12, 14, 15, 1 6. Certain of the stellate
nuclei exhibit two centres instead of one, and in some cases,
like that represented on PI. 25, fig. 19, the stellate body of two
nuclei is found united. Both of these forms are possibly modi-
fications 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 (PI. 24, fig. 3 o}. Their
average diameter is 0x34 mm., compared with 003 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 rela-
tively large, O'O2 — 0x327 mm. in diameter. It presents the
characters ascribed by Eimer1, and many other recent authors2,
to typical nuclei (vide PI. 24, fig. 3, and PI. 24, 25, figs. 13, 14, 15,
1 6, 17, 1 8). 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 in-
1 Archiv f. micr. Anat. Vol. xiv.
" Vide especially Klein. Quart. Joiir/i. of Mic. S<i. July 1878.
564 THE STRUCTURE AND DEVELOPMENT
stances two central nucleoli are present, in which case the regu-
larity is considerably interfered with. The points in which the
youngest permanent ova differ from the primitive may be
summed up as follows : —
(i) 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.
The formation of permanent ova is at its height in embryos
of about seven centimetres 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 : —
o-oi6 mm.
ox>i6 mm.
o'oiS mm.
ox>2 mm.
o'O2 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. Perma-
nent ova in the act of development are indicated in my figures
by the letters d o. Many of the intermediate nuclei are more
OF THE VERTEBRATE OVARY. 565
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 transi-
tional forms. The larger ones frequently lie in a mass ~of
granular protoplasm projecting from the nest, and only united
with it by a neck (PI. 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 PI. 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 proto-
plasm is present around the nucleus of the developing perma-
nent 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 (PI. 24, fig. 15).
Their appearance leads me to adopt the view that ivhile some
of the nuclei of each nest are converted into the nuclei of t/ie
permanent ova, others break down and are used as the pabti-
!um, 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 (PI. 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.
ox>22 mm.
0-024 mm.
0*032 mm.
566 THE STRUCTURE AND DEVELOPMENT
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 subse-
quent 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 de-
scribed, 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 con-
stituent 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 : — I. By
the formation of granular protoplasm round the nucleus in a
OF THE VERTEBRATE OVARY. 567
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, some-
what flattened, follicular epithelium (PI. 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 (PI. 24, fig. 7,
and PI. 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 epithe-
lium 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 O'o6 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 com-
paratively late in life. I have, however, two series of sections of
ovaries preserved in osmic acid, from slightly larger embryos
568 THE STRUCTURE AND DEVELOPMENT
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
centimetres long, preserved in osmic acid.
A considerable number of nests were present (PI. 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.
o-oi6 mm.
o'oi6 mm.
o'oiS mm.
o'oiS mm.
Thus, if anything, the nuclei were slightly smaller than in the
younger embryo, ft 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.
ox>3 mm 0*014 mm-
ox>34 mm o'oiS mm.
0-028 mm o%oi6 mm.
ox>3 mm o'o2 mm.
0-04 mm o'02 mm.
0*04 mm 0-02 mm.
ox>48 mm ox>2 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
OF THE VERTEBRATE OVARY. 569
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 how-
ever small, the body measuring about o-oi6 mm., and the nucleus
O'OI2 mm. Isolated ova with metamorphosed nuclei could
also be found measuring O'O22, 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 O'O/ 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 : —
o'oi mm.
o'oi2 mm.
0*014 mm.
O'oi6 mm.
One of these nests is represented on PI. 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 investi-
gations 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 Miiller's fluid, none of
these have proved universally successful, and bichromate of potash
B. 37
570 THE STRUCTURE AND DEVELOPMENT
and Muller's fluid are useless. Great difficulties have been ex-
perienced 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 Leydig1 in Raja, and an albuminous layer of the nature of a
chorion * by Gegenbaur3 in Acanthias — the membranes described
in these two ways being no doubt equivalent.
Dr Alex. Schultz4 has more recently investigated a consider-
able variety of genera and finds three conditions of the egg
membranes, (i) 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 Squalidae, 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.
My own investigations have led me to the conclusion that
though the egg-membranes can probably be reduced to single
type for Elasmobranchs, 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
1 Rochen u. Haie.
• 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.
3 "Ban und Entwicklung d. Wirbelthiereier," &c., Mull. Archiv, i86r.
4 " Zur Entwicklungsgeschichte d. Selachier," Arrh. f. mikr. Anat. Vol. XI.
OF TIIK VKRTEHKATK OVAI<\. 571
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
O'I2 mm., this membrane, though considerably thicker than in
the embryo, is not thick enough to be accurately measured. In
ova of o-5 mm. from a young female (PI. 25, fig. 21) the vitelline
membrane has a thickness of O'OO2 mm. and is quite -homo-
geneous1. 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.
In an ovum of I mm. from the nearly full grown though not
sexually mature female, the zona radiata has increased in thick-
ness 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 I 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 striae
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 PI. 25, fig. 22.
At this time the vitelline membrane appears frequently to
exhibit a distinct stratification, dividing it into two or more suc-
cessive layers. It is not, however, acted on in the same manner
by all reagents, and with absolute alcohol appears at times longi-
tudinally striated.
From this stage onwards, both vitelline membrane and zona
gradually atrophy, simultaneously with a series of remarkable
1 The apparent structure in the vitelline membrane in my figure is merely in-
tended to represent the dark colour assumed by it on being stained. The zona
radiata has been made rather too thick by the artist.
37—2
5/2 THE STRUCTURE AND DEVELOPMENT
changes which take place in the follicular epithelium. The zona
is the first to disappear, and the vitelline membrane next be-
comes gradually thinner. Finally, when the egg is nearly ripe,
the follicular epithelium is separated from the yolk by an im-
measurably thin membrane — the remnant of the vitelline
membrane — only visible in the most favourable sections (PI. 25,
fig. 23 v /.). 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 (PI. 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 (PI. 25, fig. 32). Both
membranes atrophy before the egg is quite ripe ; and an ap-
parently 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 Squalidae, 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 mem-
branes 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 Gegenbaur1.
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 Ludwig2.
Alexander Schultz3 states that in Torpedo, the eggs are at
first enclosed in a simple epithelium, but that in follicles of
1 Loc. n't. * Loc. at. 3 Loc. cit.
OF THE VERTEBRATE OVARY. 573
•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 err — 0^5 mm., he finds that the
small and large cells have a very regular alternating arrange-
ment.
Semper records but few observations on the follicular epithe-
lium, but describes in Raja the presence of a certain number of
large cells amongst smaller cells. He believes that they may
develope 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 mem-
brane— the membrana propria folliculi of Waldeyer — and in-
ternally 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 epithe-
lium 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 epithe-
lium till the egg has reached a diameter of more than i 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 eluci-
dating 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
5/4 TFiE STRUCTURE AND DEVELOPMENT
and columnar and the nucleus oval (PI. 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, ft''). This layer, which will be spoken of as the secondary
follicle layer, might easily be mistaken for the follicular epithe-
lium, 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 uni-
form or arranged as a single layer. The general arrangement of
these cells is shewn in PI. 25, fig. 29. A considerable number of
them are more or less flask-shaped, with bulky protoplasm pro-
longed 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 epithe-
lium 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.
OF THE VERTEBRATE OVARY. 575
The fibrous layer bounding the membrana propria folliculi is
thicker than in the last stage, and the epithelial-like layer (/<?')
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 consider-
ably 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 adjoin-
ing 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 (PI. 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 epithe-
lium 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 neighbour-
hood 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 His1 in Osseous Fish, and Lindgren
in Mammalia, has been met with2.
1 Das Ei bei Knochcnfischcn.
3 Airk.f. Anal. Pliys. 1877.
5/6 THE STRUCTURE AND DEVELOPMENT
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 PI. 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 con-
nected 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 (PI. 25,
fig- 31)- Such a regularity appears in a later stage (PI. 25, fig.
32), which clearly corresponds with fig. 8 on PI. 34 of Schultz's
paper, and also with the stage of Scyllium in PI. 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 be-
come flask-shaped like those in Scyllium, and send a process
down to the vitelline membrane. The smaller cells are arranged
OF THE VERTEBRATE OVARY. 577
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 PI. 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 grow-
ing to the colossal size which it eventually attains, the follicular
epithelium does not to any great extent alter in constitution.
It gro\vs thicker on the whole, and as the vitelline membrane
gradually atrophies, its lower surface becomes irregular, exhibit-
ing somewhat flattened prominences, which project into the
yolk. At the greatest height of the prominences the epithelium
may reach a thickness of ox)6 mm., or even more. The arrange-
ment 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 Elasmobranchs
is that its epithelium at the time when the egg is rapidly ap-
proaching 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's1 observations, that the follicular epi-
thelium becomes several layers thick, and that a differentiation
of the cells, similar to that in Elasmobranchs, 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 egg3. That these cells in the Reptilian ova really corrc-
1 Archir f. inikr. Anal. Vol. vni.
- I'.iaun, " Urogeuitalsystem d. Amphibien," Arbciten a. d. zool.-zoot. [nstilitt
5/8 THE STRUCTURE AND DEVELOPMENT
spond with those in Elasmobranchs 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.
The Vitellus and the development of the yolk spherules. —
Leydig, Gegenbaur, and Schultz, have recorded important ob-
servations on this head. Leydig1 chiefly describes the peculiar
characters of the yolk spherules.
Gegenbaur2 finds in the youngest eggs fine granules, which
subsequently develop into vesicles, in the interior of which the
solid oval spheres, so characteristic of Elasmobranchs, are de-
veloped.
Schultz describes in the youngest ova of Torpedo the minute
yolk spherules arranged in a semi-lunar form around the ec-
centric 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 striae, 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 Gegen-
baur 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 Elasmo-
branchii.
In very young ova the body of the ovum is simply granular,
but when it has reached about O'5 mm. the granules are seen to be
arranged in a kind of network, or spongework (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
Witrzburg, Bd. iv. He says, in reference to the flask-shaped cell, p. 166, " Hochstens
wiirde ich die P'unktion der grossen Follikelzellen als eiuzellige Driisen mehr be-
tonen."
1 Loc. cit. '2 Loc. cit.
OF THE VERTEBRATE OVARY. 579
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 commence-
ment of embryonic development. An arrangement of the proto-
plasmic striae like that described by Schultz has not come" under
my notice.
The development of the yolk appears to me to present spe-
cial difficulties, owing to the fact pointed out by His1 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 PI. 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 bclou1 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 Gaster-
osteus2, 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 PI. 25, fig. 27.
The ovum represented in fig. 27 was o-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 dis-
1 Das Ei bd Knochenfischen.
z "Ovum" in Todd's Encyclopedia, fig. 69.
580 THE STRUCTURE AND DEVELOPMENT
tributed but are collected in peculiar little masses or aggrega-
tions (PI. 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 Gotte in his mono-
graph on Bombinator igneus (PI. I, fig. 9). It deserves to be
especially noted, that when the yolk spherules are first formed,
the peripheral layer of tlie 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, (i) 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.
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 mate-
rial, 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 1 of the ripe ovum, and this form is acquired while
the centre of the ovum is still free from them.
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
1 The peculiar oval, or at times slightly rectangular and striated yolk spherules of
Klasmobranchs are mentioned by Leydig and Gegenbaur"(Pl. u, fig. 20), and myself,
Preliminary Account of Dci'dopinent of Elasmobranch Fishes, and by Filippi and His
in Osseous Fishes. •
OF THE VERTEBRATE OVARY. 581
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 differ-
ent 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 Eimer1 as
" Dotterschorfe." I have only met these bodies in a single
instance in ova of O'6 mm., from the ovary (in active growth)
of a specimen of Scy. canicnla 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 o-O2 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, PI. H, though they were much more numerous
than represented in that figure, and confined to the periphery of
the ovum.
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
1 " Untersuchung viher die Eier d. Rcptilien," Archiv f. mikros. Anat. Vol. vin.
582 THE STRUCTURE AND DEVELOPMENT
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 ovum1.
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. 25 A, 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. 25 'B), 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. . . O'O3 mm. . . o'oog mm.
0*064 mm' • • 0-025 mm- • • 0*012 mm.
fo-oio mm.
o'oo6 mm. . . 0*03 mm. . . \
(p'oo3 mm.
Germinal vesicle. — Gegenbaur2 finds the germinal vesicle
completely homogeneous and without the trace of a germinal
spot. In Raja granules or vesicles may appear as artificial pro-
ducts, and in Acanthias even in the fresh condition isolated
vesicles or masses of such may be present. To these structures
he attributes no importance.
Alexander Schultz3 states that there is nothing remarkable
in the germinal vesicle of the Torpedo egg, but that till the egg
1 Vide Allen Thomson, article "Ovum," Todd's Encyclopedia, p. 95.
'2 Loc. cit. 3 Loc. cit.
OF THE VERTEBRATE OVARY. 583
reaches O'5 mm., a single germinal spot is always present-(mea-
suring about O'oi mm.), which is absent in larger ova.
The bodies described by Gegenbaur are now generally recog-
nised 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 OT2
mm., the germinal vesicle measures about O'o6 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 themselves1.
Granules are sometimes also present in the germinal vesicle, but
are probably only extremely minute nucleoli.
In ova of o-5 mm. the germinal vesicle has a diameter of 0*12
mm. (PI. 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
1 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. in. pi. 4, fig. r.
584 THE STRUCTURE AND DEVELOPMENT
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 aggre-
gated towards one side of the vesicle ; and in addition, numerous
deeply staining smaller granular aggregations, probably belong-
ing 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 PI. 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. — Ludwig1 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 con-
tains, 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
1 I.oc. cit.
OF THE VERTEBRATE OVARY. 585
off from the stalk, and so from its place of origin in the super-
ficial epithelium, and subsequently lies freely in the stroma of
the ovary."
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 view 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 (PI. 24, fig. 8) nests of ova (in my
sense of the term) are very numerous, but though usually super-
ficial 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 O'5 mm. nests of ova
are still fairly numerous. The nests are characteristic, and
present the various remarkable peculiarities already described
B. 38
586 THE STRUCTURE AND DEVELOPMENT
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 trabeculae connecting
the deeper and more superficial parts of the germinal epithelium ;
and his whole view about the formation of the follicular epithe-
lium 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 epi-
thelium, 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.
(i) The ovary in the embryo is a ridge, triangular in sec-
tion, attached along the base. It is formed of a core of stroma
and a covering of epithelium. A special thickening of the epi-
OF THE VERTEBRATE OVARY. 587
thelium on the outer side forms the true germinal epithelium, to
which the ova are confined (PI. 24, fig. i). 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 (PI. 24, figs. 2, 3, and 6).
(2) At first the thickened germinal epithelium is sharply
separated by a membrane from the subjacent stroma (PI. 24,
figs, i, 2, and 3), but at about the time when the follicular epi-
thelium 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 (PI. 24, figs. 7 and 8). At the same time the
surface of the epithelium turned towards the stroma becomes
irregular (PI. 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 forma-
tion 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. i).
(4) Conversion of primitive ova into permanent ova.—
Primitive ova may in Scyllium become transformed into perma-
nent 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 deli-
38-2
588 THE STRUCTURE AND DEVELOPMENT
cate 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 imme-
diately after its separation from a nest, and so constitute a fol-
licle. 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 (PI. 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 (PI. 25, figs. 30 — 33).
(6) The egg membranes. — Two membranes are probably
always present in Klasmobranchs during some period of their
OF THE VERTEBRATE OVARY. 589
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 o-o6 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 inte-
rior 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 PI. 25, fig. 25 A.
(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.
59O THE STRUCTURE AND DEVELOPMENT
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 Pfliiger1,
Ed. van Beneden2, and especially Waldeyer3, as inaugurating the
newer view on the nature of the ovary, and development of the
ova ; and of Foulis4 and Kolliker5, 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, how-
ever, 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 Pfluger 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 epithe-
lium are derived from the germinal epithelium, but I cannot
accept his views of the relation of the stroma to the germinal
epithelium.
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. Kolliker's statements
1 Die Eierstocke d. Siiugethiere u. d. Menschen, Leipzig, 1863.
2 "Composition et Signification de 1'oeuf," Acad. r. de Belgique, 1868.
3 Eierstock u. Ei. Leipzig, 1870.
4 Trans, of Royal Society^ Edinburgh, Vol. XXVII. 1875, and Quarterly Journal
of Microscopical Science ) Vol. xvi.
~° Vcrhandliing d. Phys. Med. Gesellschaft, Wiirzburg, 1875, N. F. Bel. vm.
OF THE VERTEBRATE OVARY. 591
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 Wolman body, and has satisfied himself that
they are continuous with Pfliiger's egg-tubes, and that they
supply the follicular epithelium. To the general accuracy of
Kolliker'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 PI. 26, fig. 35, and a more highly
magnified portion of the same in fig. 35 A. The ovary is a cylin-
drical 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 —
(i) an epithelial-like tissue ((), coloured brown, which forms
the most important element, and (2) vascular and stroma ele-
ments in this.
The germinal epithelium is a layer about 0*03 — 0*04 mm. in
thickness. It is (vide fig. 35 A, 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 epithe-
lium is in most parts separated by a membrane-like structure
592 THE STRUCTURE AND DEVELOPMENT
(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 trabe-
culae of epithelial-like cells, which present a very striking re-
semblance 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 diagram-
matically 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. 35 B), 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
OF THE VERTEBRATE OVARY. 593
hesitation in identifying it with the segmental cords (segwent-
alstrdnge] discovered by Braun in Reptilia, and described at
length in his valuable memoir on their urogenital system *. Ac-
cording 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 Mal-
pighian 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.
It is hardly to be supposed that this tissue, which is so con-
spicuous in all young ovaries, has not been noticed before ; but
the notices of it are not so numerous as I should have antici-
pated. His2 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.
1 Arbeitcn a. d. Zool.-zoot. Tnstitiit Wurzburg, Bd. iv.
a Archivf. mikros. Anat. Vol. I. p. 160.
594 THE STRUCTURE AND DEVELOPMENT
Waldeyer1 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 (Schlauche) 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 homolognes 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.
Romiti gives a very similar description to Waldeyer of these
bodies in the dog 2. Born also describes this tissue in young
and embryonic ovaries of the horse as the Keimlager*. The
columns described by Kolliker4 and believed by him to furnish
the follicular epithelium, are undoubtedly my tubuliferous tissue,
and, as Kolliker himself points out, are formed of the same
tissue as that described by Waldeyer.
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
1 Loc. cit.
- Archivf. mikr. Anat. Vol. x.
3 Archivf. Anatomic, Pliysiologie, u. Ifiss. Median. 1874.
4 Loc. cit.
OF THE VERTEBRATE OVARY. 595
dog solid columns are present in the embryo, but later they
appear frequently to acquire a tubular form, and a lumen. Pro-
bably 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 Pfltiger'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
Kolliker'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 36 A).
From these figures it is at once obvious that the germinal
epithelium has very much increased in bulk. It has a thickness
O'l — oxx) 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 arc 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 ger-
minal 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 O'Oi — O'O2 mm. in diameter,
and their nuclei from 0004 — o-oo6 mm. The nuclei of the
columnar outer cells measure about o-oo8 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
596 THE STRUCTURE AND DEVELOPMENT
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.
Fig8- 37 and 37 A 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 Elasmobranchs.
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 Elasmobranchs,
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 Pfliager. 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 trabeculas, 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 — o-22 mm. in
thickness. Its cells have undergone considerable changes. A
fair number of them (fig. 37 A, />.#.), especially in the outer layer
of the epithelium, have become larger than the cells around
OF THE VERTEBRATE OVARY. 597
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 Elasmobranchs, Aves, &c. In a fairly
typical primitive ovum of this stage the body measures O'O2 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 dis-
tinguished by their size as primitive ova, and the cells them-
selves are of a fairly uniform size, though in this respect there is
perhaps a greater variation than might be gathered from fig. 3/A.
The cells are on the average about O'Oi6 mm. in diameter, and
their nuclei about o-oo8 — 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 37 A 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 (/)
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 O'22 mm. It is divided
into three obvious layers: (i) an outer epithelial layer which
corresponds with the pseudo-epithelial layer of the Elasmobranch
ovary, average thickness 0x33 mm. (2) A middle layer of small
nests, which corresponds with the middle vascular layer of the
previous stage; average thickness O'l mm. (3) An inner layer
of larger nests; average thickness 0^23 mm.
598 THE STRUCTURE AND DEVELOPMENT
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 inter-
penetrated 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 Elasmobranchs. 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 under-
going 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. 38 A) 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 trabeculae 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 O'OI2 mm., and that of the nucleus about O'ooS mm.
In the innermost layer (fig. 38 B), 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 com-
menced 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
OF THE VERTEBRATE OVARY. 599
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 con-
verted 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. 3811 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. 38 B, o. The cells with
modified nuclei, which are becoming permanent ova, usually
present one point of contrast to the homologous cells in Elas-
mobranchs, 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 after-
wards becomes distinct, and which would thus seem, as Foulis
has already insisted, to be of the nature of a vitelline mem-
brane.
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 Elasmo-
branchs are thus formed (cf. E. van Beneden 1). These masses
become slightly more numerous in the succeeding stages. In-
dications of a fusion of this kind are shewn in fig. 38 B. 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 O'Oi6 — cx>2 mm., and their nuclei from O'Oi—
o-oi2 mm.
With reference to the tissue of the hilus of the ovary, it
may be noticed that the tubuliferous tissue (t} is relatively
1 /<><-. tit.
6OO THE STRUCTURE AND DEVELOPMENT
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 nu-
merous 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 dis-
tinct 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 PI. 26, fig. 39 A.
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 PI. 26, fig. 39 B.
The nest contains (i) fully formed permanent ova, com-
pletely 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 satis-
OF THE VERTEBRATE OVARY. 6OI
factory 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 Elasmobranchs.
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 Elasmo-
branchs. 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
Elasmobranchs. (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 Elasmobranchs.
Round the completed follicle a very delicate membrana pro-
pria folliculi appears to be present1.
The larger ova, with follicular epithelium, measure about
0*04 mm., and their nucleus about O'O2 mm., the smaller ones
about o-O22 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 ap-
pear to be three possibilities.
(a) That they become cells of the follicular epithelium ; (ft)
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 des-
tinations.
(4) The cells which form the follicle. — The only point to be
noticed about these is that they are smaller than the indifferent
1 Loc. cit., Waldeyer, p. 23, denies the existence of this membrane for Mam-
malia. It certainly is not so conspicuous as in some other types, but appears to me
nevertheless to be always present.
!'•• 39
6O2 THE STRUCTURE AND DEVELOPMENT
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 ad-
vanced 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 espe-
cially developed nucleolus, and smaller granular bodies. Their
diameter varies from about 0*028 to 0*04 mm. and that of their
nucleus from o-oi6 to o-O2 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 epithe-
lium, which are destined to form the follicle (vide fig. 40 A and B).
In a few cases the follicles are completed, and are then formed
of very flattened spindle-shaped (in section) cells. In the ma-
jority of cases all the ova of each nest are quite distinct, and
each provided with a delicate vitelline membrane (fig. 40 A).
OF THE VERTEBRATE OVARY. 603
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 PI. 26, fig. 40 A. In
some of these the nuclei in the undivided protoplasm are all of
about the same size and distinctness, and probably the proto-
plasm eventually becomes divided up into as many ova as
nuclei ; in other cases, however, one or two nuclei clearly pre-
ponderate over the others, and the smaller nuclei are indistinct
and hazy in outline. In these latter cases I have satisfied my-
self as completely as in the case of Elasmobranchs, 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 out-
lines 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 epi-
thelium, their passage by a series of gradations into obvious
39—2
604 THE STRUCTURE AND DEVELOPMENT
cells of the germinal epithelium and the peculiarities of their
nuclei, so different from those of the stroma cells, supply a suffi-
cient series of characters to remove all doubt as to the deriva-
tion 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 forma-
tion of the follicular epithelium, than during the earlier stages.
His figure (Quart. Journ. Mic. Set., 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
Elasmobranchs. 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, more-
over, 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
OF THE VERTEBRATE OVARY. 605
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. Sd., Vol. xvi., p. 210): "The protoplasm which sur-
rounds 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 de-
veloped 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 con-
tinuous 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 mem-
brane becomes the zona radiata or whether the zona is not a
606 THE STRUCTURE AND DEVELOPMENT
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 Elasmobranchs 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); (&) 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 be-
comes 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 trabeculae) 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 Elasmobranchs, Osseous Fish, Birds,
Reptiles, &c., with numerous primitive ova embedded amongst
the small cells of the germinal epithelium, are not found.
OF THE VERTEBRATE OVARY. 607
(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 Elasmo-
branchs : —
(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 reticu-
lum, 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 indif-
ferent 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 epithe-
lium, 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 mem-
brane, and that the latter remains as a membrane, somewhat
irregular on its outer border, against which the ends of the follicle
cells abut.
608 THE STRUCTURE AND DEVELOPMENT
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 Am-
phioxus.
The strticture 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 Elasmo-
branchii 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 stroma1.
It is obvious that according to the above view Pfliiger's egg-
tubes are merely trabeculae 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 Hertwig2,
represent Pfliiger's egg-tubes.
The formation of the permanent ova. — The passage of primi-
tive 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. Al-
1 My view of the structure of the ovary would seem to be that held by Gotte,
Ent-wicklungsgeschichte d. Unke, pp. 14 and 15.
2 Loc. cit. 36.
OF THE VERTEBRATE OVARY 609
though there are no investigations as to the changes undergone
by the nucleus in other types, still it appears to me safe to con-
clude that the results arrived at hold good for Vertebrates
generally1. 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 syncy-
tium, 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.
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. Gotte2 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 Gotte's
view about the fusion of the nuclei, and regard it as very im-
probable. 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 con-
1 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 Mam-
malia.
" EntwickltatgtgticMckU d. L «Xv.
6 10 THE STRUCTURE AND DEVELOPMENT
nected 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 inde-
pendently of the nests.
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 Weismann1 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.
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
1 Zeit. fiir wiss. Zool. Bd. xxvn.
OF THE VERTEBRATE OVARY. 6ll
of finding transitional forms between them and ordinary "CeHs of
the germinal epithelium, caused me at one time to seek (un-
successfully) 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.
(i) An outer and first formed membrane — the albuminous
membrane of Gegenbaur — which, in opposition to previous ob-
servers, 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 mem-
branes usually atrophy before the ovum leaves the follicle. In
Reptilia1 precisely the same arrangement is found as in Elasmo-
branchii, 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 Squalidae. It appears, as
in Elasmobranchs, 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 Birds2
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 Elasmobranchs in presenting during
some period of their development the two membranes above
mentioned.
Osseous fish have almost always a zona radiata, which it
seems best to assume to be equivalent to that in Elasmobranchs.
1 Gegenbaur, loc. cit.; Waldeyer, loc. tit.; Eimer, loc. cit.; and Ludwig, loc. fit.
- Gegenbaur, Waldeyer, E. van JJeiieden. Eimer.
6l2 THE STRUCTURE AND DEVELOPMENT
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 present1, 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 Beneden2 has,
moreover, shewn that they are also provided at a certain period
with a delicate membrane within the zona.
TJu reticuhtm 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 interest-
ing observations of Dr Klein in the last number of this Journal 3
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.
Again, I find that at the point of intersection of two or more
1 Carlberla, Zeit. /. wiss. Zoo/. Bd. xxx. a Loc. dt.
3 [Quarterly Journal Microscopical Science, July 1878.]
OF THE VERTEBRATE OVARY. 613
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 reti-
culum 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
subgerminal nuclei in Elasmobranchs and the protoplasmic net-
work in the yolk in which they lie. This point is called attention
to in my Monograph on Elasmobranch Fishes, page 39 1, 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.
1 [This Edition, p. 252.]
614 THE STRUCTURE AND DEVELOPMENT
EXPLANATION OF PLATES 24, 25, 26.
PLATE 24.
LIST OF REFERENCE LETTERS.
d n. Modified nucleus of primitive ovum, d o. Permanent ovum in the act of
being formed, dv. Developing blood-vessels, d yk. Developing yolk, e p. Non-
ovarian epithelium of ovarian ridge, f e. Follicular epithelium, g v. Germinal
vesicle. / sir. Lymphatic region of stroma. n n. Nests of nuclei of ovarian region.
o. Permanent ovum. ov r. Ovarian portion of ovarian ridge. / o. Primitive ovum.
ps e. Pseudo-epithelium of ovarian ridge, sir. Stroma ingrowths into ovarian epithe-
lium, v. Blood-vessel, v sir. Vascular region of stroma adjoining ovarian ridge.
vt. Vitelline membrane, x. Modified nucleus, yk. Yolk, z n. Zona radiata.
Fig. r. 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. i. Transverse section of the ovarian ridge of an embryo of Scyllitim cani-
cula, considerably older than stage Q. Zeiss C, ocul. 2. Picric add. Several nests,
some with distinct ova, and others with the ova fused together, are present in the sec-
tion (n. n.), and several examples of modified nuclei in still distinct ova are also repre-
sented. 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 Scy Ilium 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 (sir.) and ovarian region. Zeiss a a, ocul. 2. Picric acid.
Fig. 5. Section through the ovarian ridge of an embryo of Scy Ilium canicula,
to cm. long, in which the ovary was slightly less advanced than in fig. 3. To illus-
trate the relation of the ovarian epithelium to the subjacent vascula stroma. Zeiss A,
ocul. 2. Osmic acid. y. points to a small separated portion of the germinal epithe-
lium.
Fig. 6. Section through the ovarian ridge of an embryo of Scyllinm 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.
OF THE VERTEBRATE OVARY. 615
Fig. 8. Section through the ovarian region (close to one extremity, where it is
very small) from a young female of Scy. caniaila. 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/, e. is seen a surface view of the follicular epithelium
of an ovum. Zeiss C, ocul. 2. Picric acid.
Fig. it. Section through part of an ovary of Scy 'Ilium 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 Scyllmm 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. \j). 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 PI. 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, j e.
Follicular epithelium, fe'. Secondary follicular epithelium, g v. 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). z n. 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, contain-
ing 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.
canicida. Zeiss C, ocul. 2. It shews the remnant of the vitelline membrane (v. t.)
separating the columnar but delicate cells of the follicular epithelium (/ 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.
6l6 THE STRUCTURE AND DEVELOPMENT
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 163 centime-
tres 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 prolifera-
tion of the germinal spots. Zeiss A, ocul. 2.
Fig. 28. Small part of the follicular epithelium and egg membranes of a some-
what larger ovum of Scyllium canicula than fig. 22. Zeiss D D, ocul. i.
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, f c. Cells which will form the follicular epithelium, f e.
Follicular epithelium, g e. Germinal epithelium, mg. Malpighian body. «. Nest of
cells of the germinal epithelium, n d. Nuclei in the act of dividing, o. Permanent
ovum, o v. Ovary, p o. Primitive ovum. f. Tubuliferous tissue, derived from Mal-
pighian 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 (g e.) and the tubuliferous tissue (/.),
which has grown in from the Wolfnan body, and which gives rise in the male to parts
of the tubuli seminiferi. Zeiss A, ocul. 2.
OF THE VERTEBRATE OVARY. 617
Fig- 35 A. 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- 35 B. Longitudinal section through part of the Wolffian body and the ante-
rior end of the ovary of an eighteen days' embryo, to shew the derivation of tubu-
liferous tissue (/.) from the Malpighian bodies, close to the anterior extremity of the
ovary. Zeiss A, ocul. i.
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. 36 A. 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 37 A. The same parts of an ovary of a twenty-eight days' embryo as
figs. 36 and 36 A 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. 38 A. Vertical section through a small part of the surface of the same ovary
as fig. 38. Zeiss D D, ocul. 2.
Fig. 38 B. 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- 39 A. 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- 39 B. 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 folli-
cles. Zeiss D D, ocul. 2.
Figs. 40 A and 40 B. Small portions of the middle region of the germinal epithe-
lium 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.
B. 40
XIII. ON THE EXISTENCE OF A HEAD-KIDNEY IN THE
EMBRYO CHICK, AND ON CERTAIN POINTS IN THE DE-
VELOPMENT OF THE MtJLLERIAN 'DUCT \ By F. M. BAL-
FOUR and A. SEDGWICK.
(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 Miillerian duct, and which, we believe, corre-
spond with the head-kidney, or " Vorniere " of German authors.
The second deals with the growth and development of the Miil-
lerian duct. With reference to this we have come to the con-
clusion that the Miillerian 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 ex-
tended literature of the excretory system, since this has been
very fully given in three general papers which have recently
appeared by Semper2, Fiirbinger3, and by one of us4.
All recent observers, including Braun5 for Reptilia, and Egli6
for Mammalia, have stated that the Miillerian duct develops as
1 From the Quarterly Journal of Microscopical Science, Vol. xix. 1879.
2 "Das Urogenital-System der Plagiostomen," Arbeiten a. d. zool.-zoot. Institut.
Wiirzburg.
3 " Zur vergl. Anat. u. Entwick. d. Excretionsorgane d. Vertebraten," Morpho-
logisches Jahrbuch, Vol. IV.
4 " On the Origin and History of the Urinogenital Organs of Vertebrates,"
Journal of Anat. and Pkys., Vol. x. [This Edition No. vn.]
5 Arbeiten a. d. zool.-zoot. Institut. Wiirzburg, Vol. IV.
6 Beitr. zur Anat. u. Entwick. d, Geschlechtsorgane, Inaug. Diss., Zurich, 1876.
EXISTENCE OF A HEAD-KIDNEY. 619
a groove in the peritoneal epithelium, which is continuecLback-
ward as a primitively solid rod in the space between the Wolf-
fian duct and peritoneal epithelium.
In our preliminary account we stated1, in accordance with
the general view, that the Miillerian 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 Miillerian duct
which we have been able to observe, it consists of three succes-
sive 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 ad-
jacent stroma. In front the projection is separated by a con-
siderable interval from the Wolffian duct ; but near its hinder-
most 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 thick-
ened germinal epithelium. The linear area is, however, con-
tinued 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 sup-
posing the groove to be suddenly filled up, so as to form a solid
ridge pointing inwards towards the Wolffian duct.
The ridge succeeding the first groove is continued for about
six sections, and is considerably more prominent at its posterior
1 /'i-ore citings of Royal Society, 1878.
40 — 2
620 EXISTENCE OF A HEAD-KIDNEY
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. I — 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 connec-
tion 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 pro-
minent 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 hinder-
most limit of the head-kidney. Instead of this, the last groove
(No. 7) terminates by the upper part of its walls becoming con-
stricted off as a separate rod, which appears at first to contain
a lumen continuous with the open groove. This rod (Nos. 7, 8,
9, I o) situated between the germinal epithelium and Wolffian
duct is continued backward for some sections. It finally termi-
nates 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
IN THE EMBRYO CHICK. 621
they are continuous with the walls of the grooves) partially con-
stricted 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 epithe-
lium. 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 Miillerian 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. i — 3, series B, PI. 27) is at first
somewhat separated from the Woiffian 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 groove1.
The last trace of this body is seen on the upper wall of the
groove in No. 5. We believe that the body (rj 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 rt
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,
1 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.
622 EXISTENCE OF A HEAD-KIDNEY
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 (rs) 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^). In the next section this duct
(r3) is entirely separated from the germinal epithelium, and it
may be traced backwards through several sections until it term-
inates 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 Mullerian duct a fold of the germinal epithe-
lium (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 de-
velopment 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 rudi-
mentary grooves.
In an embryo not very much older than the one last de-
scribed 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. I 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 Mullerian 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)
IN THE EMBRYO CHICK. 623
—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^ and gr^), and we believe that they are the remnants
of the posterior grooves of the head-kidney present at an earlier
stage.
The Mullerian 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 Mullerian 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 QOth and i2oth 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 de-
scribed 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 vas-
cular 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 open-
ing 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, PI. 28 gl, and is
seen to form a somewhat irregular projection into the body-
cavity, covered by a continuation of the peritoneal epithelium,
624 EXISTENCE OF A HEAD-KIDNEY
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 connec-
tion 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 glome-
rulus are developed in situ. The stalk connecting the glome-
rulus 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 pos-
terior 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 (PI. 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 glome-
rulus most fully developed, being prior to that in which the
head-kidney appears, it is not possible to determine with cer-
tainty 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 termi-
nates at a point just in front of the anterior opening of the
head-kidney. It is less developed than before, but is still pre-
sent up to the period of the atrophy of the head-kidney. It
IN THE EMBRYO CHICK. 625
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 tJie head-kidney and glome-
rulus. — The first rudiment of the head-kidney arises as three
successive grooves in the thickened germinal epithelium, con-
nected by ridges, and situated some way behind the front end
of the Wolffian duct. In the next stage the three ridges con-
necting 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 pos-
teriorly continued into the Mullerian duct. Still later the head-
kidney atrophies, its two posterior openings vanishing, and its
anterior opening remaining as the permanent opening of the
Mullerian 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 struc-
tures 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 Mullerian 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 Develop-
ment of the Allantois1," in which certain structures are described
which are, perhaps, identical with our head-kidney. The fol-
lowing is a translation of the passage : —
"In the upper region of M tiller'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
1 Beitrdge zur Entwickclnngsgeschichte d. Allantois dcr Mitllcr'schen Gange H. dcs
Afters. Frankfurt, 1874.
626 EXISTENCE OF A HEAD-KIDNEY
distance close to Miiller's duct and in the same direction, open-
ing, 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 suppo-
sition that an abnormal communication is effected between the
germinal epithelium and Miiller'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."
The statement that these accessory canals are late in de-
veloping, 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 neces-
sary to say a few words in justification of the comparison we
have made between the modified abdominal extremity of the
Mullerian duct in the chick and the head-kidney of the Ichthy-
opsida.
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 Furbringer1. We propose our-
selves 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.
The development of the head-kidney in Amphibia has been
fully elucidated by the researches of W. Miiller2, Gotte3, and
Fiirbringer4, while to the latter we are indebted for a knowledge
of the development of the Mullerian duct in Amphibians. The
first part of the urino-genital system to develop is the segmental
duct ( Vornieregang of Furbringer), which is formed by a groove-
like invagination of the peritoneal epithelium. It becomes con-
stricted into a duct first of all in the middle, but soon in the
1 Loc, cit.
2 Jenaische Zeitschrift, Vol. ix. 1875.
'A Entwickelungsgeschichte d. Unkt.
4 Loc. at.
IN THE EMBRYO CHICK. 627
posterior part also. It then forms a duct, ending in frorrhby a
groove in free communication with the body-cavity, and term-
inating 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 com-
munication 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.
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 peri-
toneal openings become successively closed from before back-
wards. At this period the formation of the Miillerian 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 — (i) a somewhat convoluted longitudinal
canal, with a certain number of peritoneal openings; (2) a vascu-
lar 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
628 EXISTENCE OF A HEAD-KIDNEY
structure of the excretory system, but may say that one of
us1 has already, on other grounds, attempted to shew that the
abdominal opening of the Mullerian 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 homo-
logy 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 Mullerian duct, while
in Amphibia, the pores of the head-kidney atrophy, and an
entirely fresh abdominal opening is formed for the Mullerian
duct.
II.
The Growth of the Mullerian Duct.
Although a great variety of views have been expressed by
different observers on the growth of the Mullerian 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 a 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 un-
able 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 Mullerian duct. Our first stage embraces the
1 Balfour, "Origin and History of Urinogenital Organs of Vertebrates," Journal
of Anat. and Phys. Vol. x., and Monograph on Elasmobranch Fishes. [This edition
Nos. vn. and x.]
IN THE EMBRYO CHICK. 629
period prior to the disappearance of the head-kidney. At this
stage the structure we have already spoken of as the rudiment
of the Mullerian 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 epithe-
lium (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
Mullerian 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. I and 2, series G). The limits of
the Wolffian wall and the pointed termination of the Mullerian
duct are in many instances quite distinct ; but the outline of the
Wolffian duct appears to be carried round the Mullerian duct,
and in some instances the terminal point of the Mullerian 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 Mullerian duct has by this stage made a very marked
progress in its growth towards the cloaca, and, in contradistinc-
tion 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. I, 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 Mullerian duct in its backward growth.
In the last section in which any trace of the Mullerian duct
can be made out (series D, No. 1 1, and series H, No. 2), it has no
longer an oval, well-defined contour, but appears to have com-
pletely fused with the wall of the Wolffian duct, which is accord-
ingly very thick, and occupies the space which in the previous
630 EXISTENCE OF A HEAD-KIDNEY
section was filled by its own wall and the Miillerian 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 Miillerian 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 Mullerian 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
MUllerian duct at this stage presents the following features:
A few sections before its termination the Mullerian 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. i). Gradually, however,
as we pass backwards, the Mullerian cluct 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
Mullerian duct lies (Plate 28, series I, Nos. 2 and 3). As soon
as the Mullerian 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 MUllerian, 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 Mullerian 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 ob-
served in it up to its very end, but is usually irregular in outline
and frequently traversed by strands of protoplasm. The MUller-
ian 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
IN THE EMBRYO CHICK. 631
its outer wall on the level of the Mtillerian duct comes into con-
tact with the germinal epithelium (Plate 28, series I, No. 5).
We have traced the growing point of the Miillerian 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 pecu-
liar 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 Miillerian duct. At the least one similar cord
was met with in the same embryo, situated just behind the
abdominal opening of the Miillerian duct. We have found simi-
lar 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 Miillerian duct can be stated
in a very few words. Our second stage, where the solid point
of the Miillerian duct terminates by fusing with the walls of the
Wolflfian duct, we interpret as meaning that the Miillerian 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 Miillerian duct during our third stage cannot, we
think, be interpreted in the same way, but the peculiarities of the
cells of both Miillerian and Wolffian ducts, and the indistinctness
of the outlines between them, appear to indicate that the Miiller-
ian 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 Mullerian duct are, we believe, derived from the walls of the
Wolffian duct.
632 EXISTENCE OF A HEAD-KIDNEY
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 con-
sideration, as they have no bearing upon our present investiga-
tions). 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 (ft) 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-kidney1 attains to its highest development in the
Marsipobranchii (Myxine, Bdellostoma). It consists of a longi-
tudinal 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
1 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-Fiirbringer view which
has been fully worked out and ably argued for by Fiirbringer (loc. cit. p. 96).
According to this view the head-kidney and its duct are to be looked on as the pri-
mitive 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 subse-
quently.— F. M. B.
IN THE EMBRYO CHICK. 633
lost in the adult. The head-kid ne}^ 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 Amphi-
bia the head-kidney atrophies. In Elasmobranchii the head-
kidney, so far as is known, is absent.
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 peri-
toneal 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 proto-vertebra. This knob is the rudiment of the abdominal
opening of the segmental duct, and from it there grows back-
wards 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 im-
portant. 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 epi-
thelium1.
1 In a note on p. 50 of his memoir Fiirbringer criticises my description of the
mode of growth of the segmental duct. The following is a free translation of what
he says : "In Halfour's, as in other descriptions, an account is given of a backward
B. A\
634 EXISTENCE OF A HEAD-KIDNEY
The abdominal aperture of the segmental duct in Elasmo-
branchii, in that it becomes the permanent abdominal opening
of the oviduct, corresponds physiologically rather with the
abdominal opening of the Miillerian 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. Mor-
phologically, 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. Miiller's account (Jcnaische Zeitschrift,
1875) it would seem that an anterior invagination of the peri-
toneal 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,
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 Miillerian 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 appear-
ance of Dr Furbringer'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 there-
fore leave the question an open one. — F. M. B.
IN THE EMBRYO CHICK. 635
however, the case is different. In Amphibia1, 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 Mullerian duct.
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 (i) the Wolf-
fian duct dorsally, which remains continuous with the excretory
tubules of the kidney, and ventrally (2) the oviduct or Mullerian
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 con-
tinuous in front. Into it a very small portion of the lumen of
the original segmental duct is perhaps continued. The re-
mainder 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 Mullerian duct, being shorter, and in the column
of cells with which it is continuous being from the first incom-
plete."
It will be seen from the above that the Mullerian duct con-
sists 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 Mullerian duct is of great im-
portance for a proper understanding of what takes place in the
Bird.
The Mullerian 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 concern-
ing 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
1 Fiirbringer, loc. fit.
41—2
636 EXISTENCE OF A HEAD-KIDNEY
number of points, including the presence of a head-kidney, the
urino-genital 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 Miillerian 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.
I. Wolffian duct. 2. Wolffian body. 3. Head-kidney. 4.
Miillerian 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 Miillerian 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 Gasser1 supplies us with
the best extant account of the development of the Wolffian duct.
The first trace of it, which he finds, is visible in an embryo
with eight proto-vertebrae as a slight projection from the inter-
mediate cell mass towards the epiblast in the region of the three
hindermost proto-vertebrse. In the next stage, with eleven
proto-vertebrae, the solid rudiment of the duct extends from
the fifth to the eleventh proto-vertebra, from the eighth to the
eleventh proto-vertebra it lies between the epiblast and meso-
blast, and is quite distinct from both, and Dr Gasser distinctly
states that in its growth backwards from the eighth proto-
vertebra the Wolffian duct never comes into continuity with the
adjacent layers.
In the region of the fifth proto-vertebra, 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 proto-vertebra. In an embryo with fourteen proto-ver-
tebrae the duct extends from the fourth to the fourteenth proto-
vertebra, and is now free between epiblast and mesoblast for its
whole extent. It is still for the most part solid though perhaps
1 Arch, filr Mic. Anat. Vol. Xiv.
IN THE EMBRYO CHICK. 637
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 con-
tinuity 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 follow-
ing : — What are the homologies of the parts of the Avian urino-
genital system above enumerated ? The Wolffian duct appears
to us morphologically to correspond in part to the segmental
duct1, or what Furbringer 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 : —
(1) That the Wolffian duct gives rise (vide supra, p. 631) to
the Mullerian 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 Mullerian 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 Elas-
mobranchii, which becomes the head-kidney in other types. In
fact, we suppose that the segmental duct and head-kidney, which
1 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 Fiirb ringer appears exactly
to agree. Possibly Dr Furbringer 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.
638 EXISTENCE OF A HEAD-KIDNEY
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 de-
velopment 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 Mullerian 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 Mullerian duct of the Ichthy-
opsida. By Braun1, however, who from his researches on the
Lizard satisfied himself of the entire independence of the Mul-
lerian and Wolffian ducts in the Amniota, the Mullerian duct of
these forms is regarded as a completely new structure with no
genetic relations to the Mullerian duct of the Ichthyopsida.
Semper2, on the other hand, though he accepts the homology
of the Mullerian duct in the Ichthyopsida and Amniota, is of
opinion that the anterior part of the Mullerian duct in the
Amniota is really derived from the Wolfifian duct, though he
apparently admits the independent growth of the posterior part
of the Mullerian 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 Mullerian 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 inde-
pendently 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 Mullerian
1 " Urogcnital-System d. Reptilien," .-/;•/>. cms d. zool.-zoot, Inst. Wiirzburg,
Vol. iv.
2 Lot: fit..
IN THE EMBRYO CHICK. 639
duct in Elasmobranchii. We have already pointed out that jn
Elasmobranchii the Mullerian duct is formed of two factors —
(i) of the whole anterior extremity of the segmental duct, in-
cluding 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. i) of the Mullerian 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.
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
Mullerian 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 Mullerian 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 Mullerian 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 Mullerian duct.
With reference to the difficulties involved in there being
apparently three different modes in which the permanent opening
of the Mullerian 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 cer-
tainly of the head-kidney). That the generative products did
640 EXISTENCE OF A HEAD-KIDNEY
not enter the segmental duct at first by an opening specially
developed for them appears to us to follow from Dohrn's princi-
ple of the transmutation of function (FunctionswecJisel}. 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 Miillerian duct and dorsal Wolffian duct.
The Miillerian 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 Miillerian duct gra-
dually impressed itself more and more upon the embryonic
development, so that, in the course of time, the Mullerian duct
developed less and less at the expense of the Wolffian duct.
This process appears partly to have taken place in Elasmo-
branchii, 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 open-
ing 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 Am-
phibia) 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 Mullerian 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 Mullerian duct.
With reference to the posterior position of the head-kidney
IN THE EMBRYO CHICK. 641
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 connec-
tion with the Mullerian duct.
We have made a few observations on the development of the
Mullerian duct in Lacerta muralis, which have unfortunately
led us to no decided conclusions. In a fairly young stage in
the development of the Miillerian 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 Mullerian duct Was
very similar to that figured by Braun1. As to the backward
growth of the Mullerian 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 Fiirbringer (PI. I, figs. 14 — 15) in
Amphibia.
DESCRIPTION OF PLATES 27 AND 28.
COMPLETE LIST OF REFERENCE LETTERS.
ao. Aorta, c v. Cardinal vein. gl. Glomerulus. grr First groove of head-
kidney, gr^ Second groove of head-kidney. gry Third groove of head-kidney.
ge. Germinal epithelium, mrb. Malpighian body. me. Mesentery, md. Mullerian
duct. rr First ridge of head-kidney, r^. Second ridge of head-kidney. ry Third
ridge of head-kidney. W ' d. 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. r. 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.
1 /<><., //.
642 EXISTENCE OF HEAD-KIDNEY IN EMBRYO-CHICK.
No. 8. Section through the rod when quite separated from the germinal epi-
thelium.
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
i being the first which passes through the anterior groove of the head-kidney.
No. i SECTION
2
3
4
5
3-
4-
5-
6.
8.
IO.
n.
No. 8 SECTION 13.
15-
16.
17-
18.
19.
20.
The Miillerian duct extends through eleven more sections.
The first groove (gr^.) extends to No. 3.
The second groove (gr^.) extends from No. 4 to No, 7.
The third groove (gr3.) extends from No. 11 to No. 13.
The first ridge (rr) extends from No. 2 to No. 5.
The second ridge (r2.) extends from No. 8 to No. n.
The third ridge (ry) extends from No. 13 backwards through twelve sections,
when it terminates by a pointed extremity.
FlG. 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
Miillerian 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 Miillerian duct, the remnant of the head-kidney, and the
termination of the Miillerian duct. Zeiss C, ocul. 3 (reduced one-third).
Nos. i and 2. Sections through the persistent anterior opening of the head-
kidney (abdominal opening of Miillerian 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. i.
No. 3. Section through the Miillerian 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 Miillerian duct to the peritoneal
epithelium.
No. 6. Rudiment of the second groove (grz.) of the head-kidney.
Between 6 and 7 is a considerable interval.
No. 7. All traces of this groove (grv) have vanished, and the Miillerian duct is
quite disconnected from the epithelium.
DESCRIPTION OF PLATES 27 AND 28. 643
No. 8. Rudiment of the third groove (gr a.).
No. 9. Miillerian 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 Miillerian duct is seen. A lumen
cannot be clearly made out.
No. n. The last section in which any trace of the Miillerian duct is visible. No
line of demarcation can be seen separating the solid end of the Miillerian 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. i. 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 Miillerian 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. i. Miillerian duct is without a lumen, and quite distinct from the Wolffian
wall.
No. 2. The solid end of the Miillerian duct is no longer distinct from the internal
wall of the Wolffian duct.
No. 3. All trace of the Miillerian duct has vanished.
SERIES i. Sections through the hinder end of the Miillerian duct from an embryo
of about the middle of the sixth day. Zeiss C, ocul. 2 (reduced one-third).
No. i. The Miillerian duct is distinct and small.
No. 2. Is posterior by twelve sections to No. i. The Miillerian duct is dilated,
and its cells are vacuolated.
No. 3. Penultimate section, in which the Miillerian duct is visible ; it is separated
by three sections from No. 2.
No. 4. Last section in which any trace of the Miillerian duct is visible ; the
lumen, which was visible in the previous section, is now absent.
No. 5. No trace of Miillerian duct. Nos. 3, 4, and 5 are consecutive sections.
FIG. K. Section through the hind end of the abdominal opening of the Miillerian
duct of a chick of 123 hours. Zeiss C, ocul. i (reduced one-third). It illustrates the
peculiar cord connecting the Miillerian and Wolffian ducts.
XIV. ON THE EARLY DEVELOPMENT OF THE LACERTILIA,
TOGETHER WITH SOME OBSERVATIONS ON THE NATURE
AND RELATIONS OF THE PRIMITIVE STREAK*.
(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?. I have myself also been able to make some observa-
tions on the embryo of Lacerta mnralis. 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.
Segmentation takes place exactly as in birds, and the result-
ing 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 dis-
tinguished from the remainder of the blastoderm by the more
columnar character of its constituent epiblast cells. It is some-
what pyriform in shape, the narrower end corresponding with
1 From the Quarterly Journal of Microscopical Science, Vol. xix. 1879.
z Die Erste Enlwickluiigsvorgd/igc am Eider Rcplilien, Konigsberg, 1878.
EARLY DEVELOPMENT OF THE LACERTILIA. 645
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 segmenta-
tion1. 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.
Between the second of these blastoderms and my next stage
there is a considerable gap. The medullary plate is just estab-
lished, 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. I. 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 somato-
pleuric and splanchnopleuric layers. Below the mesoblast is a
continuous layer of hypoblast (/ty.\ which -develops a rod-like
thickening along the axial line (c/i.}. This rod becomes in the
next stage the notochord. Although this embryo is not well
1 For these two specimens, which were hardened in picric acid, I am indebted to
Dr Kleinenberg.
646 EARLY DEVELOPMENT OF THE LACERTILIA.
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 triangu-
lar in shape, with the apex directed backward, the broad base
placed in front.
At the junction between the primitive streak and the blasto-
derm 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 colum-
nar 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 blasto-
pore 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 (cJi^] 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 (/y.)> 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 (in p.) is quite distinct.
In fig. 5 is seen the dorsal opening of the passage (tie.). If
a section behind this had been figured, as is done for the next
EARLY DEVELOPMENT OF THE LACERTILIA. 647
series (B), it would have passed through the primitive streak,
and, as in the chick, all the layers would have been fused to-
gether. The epiblast in the primitive streak completely coales-
ces 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 (protovertebrae)
were probably present, but this could not be made out in the
opaque embryo.
The woodcut (fig. i) represents a diagrammatic longitudinal
section through this embryo, and the sections belonging to
FIG. i. 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.
Series B illustrate the features of the hind end of the embryo
and of the primitive streak.
As is shown in fig. i, the notochord (c/i.) 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,
648 EARLY DEVELOPMENT OF THE LACERTILIA.
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 noto-
chord, 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, me.).
The general features of the stage will best be understood by
an examination of the diagrammatic longitudinal section, repre-
sented in woodcut, fig. I. In front is shown the amnion (<7w.),
growing over the head of the embryo. The notochord (c/i.) 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 nar-
rower. 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 Kolliker 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 dis-
tinctly divided into epiblast and hypoblast1. At the hind end of
the shield a somewhat triangular primitive streak is formed by
1 This appears to me to take place before the formation of the embryonic shield.
EARLY DEVELOPMENT OF THE LACERTILIA. 649
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 for-
wards 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 meso-
blast 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 un-
doubtedly 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 pas-
sage. 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)1, and support the conclusion deducible
from the lower forms of vertebrata, that the notochord is essenti-
ally hypoblastic.
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 noto-
chordal 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.
1 Gasser, Der Primitivstreifen bd Vogelembryonen, Marburg, 1878.
B. 42
650 EARLY DEVELOPMENT OF THE LACERTILIA.
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 develop-
ment of Elasmobranch fishes. I enlarged the hypothesis in a
review of the first part of Prof. Kolliker's Entwicklungs-
geschicJite. The following is the passage in which I speak
of it1:
" In treating of the exact relation of the primitive groove to
the formation of the embryo, Professor Kolliker 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 Kolliker appear to
us to demonstrate the untenable nature of his results. We be-
lieve that the front end of the primitive groove at first occupies
the position eventually filled by about the third pair of proto-
vertebrae, but that as the protovertebne 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 Kolliker 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
1 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].
EARLY DEVELOPMENT OF THE LACERTILIA. 651
originally shewn by ourselves, has been very clearly brought out
by Professor Kolliker's observations.
" The features of the primitive groove which throw special
light on its meaning are the following : —
"(i) It does not enter directly into the formation of the
embryo.
" (2) The epiblast and mesoblast always become fused be-
neath it.
" (3) It is situated immediately behind the embryo.
" Professor Kolliker 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 com-
pletely 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 in-
vestigations 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 develop-
ment 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 blasto-
derm and forming behind it a linear streak not unlike the primi-
tive 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
42 — 2
652 EARLY DEVELOPMENT OF THE LACERTILIA.
situation of the primitive groove immediately behind the em-
bryo, 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 indis-
solubly 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 Kolliker, who states "that
in Mamrfials, 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 Kolliker'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 dissent1.
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 goose2, 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
1 " Primitivrinne u. Urmund," Morphologisches Jahrbuch, Band n. p. 551.
2 Gasser, Der Primitivstreifen bei Vogelembryonen, Marburg, 1878.
EARLY DEVELOPMENT OF THE LACERTILIA. 653
more complete by the discovery of the neurenteric passage^in
the latter group, which was first of all made by Gasser.
The following paragraphs contain a detailed attempt to
establish the above view by a careful comparison of the primi-
tive streak and its adjuncts in the amniotic vertebrates with the
blastopore in Elasmobranchii.
In Elasmobranchii the blastopore consists of the following
parts: — (i), a section at the end of the medullary plate, which
becomes converted into the neurenteric canal1 ; (2), a section
forming what may be called the yolk blastopore, which even-
tually 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 con-
ditions are exactly fulfilled by the opening at the front end of
the primitive streak of the lizard (vide woodcut, fig. I, 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 hypo-
blast falling into one another at the front end of the primitive
streak. At a later period, as has been shewn by Gasser2, 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 Schaffer3 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
1 I use this term for the canal connecting the neural and alimentary tract, which
was first discovered by Kowalevsky.
2 Loc. cit.
3 "A contribution to the history of the development in the Guinea-pig," Journal
of Anat. and Phys. Vol. XI. pp. 332 — 336.
654 EARLY DEVELOPMENT OF THE LACERTILIA.
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 cor-
respond 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 :
1. It should connect the embryo with the edge of the blasto-
derm.
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 me-
soblast 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 Am-
phibia, &c.
The groove in the primitive streak may with great plausi-
bility 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 follow-
ing observations. The neurenteric canal, as it is placed at the
EARLY DEVELOPMENT OF THE LACERTILTA. 655
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.
Kolliker 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 ob-
servations 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 inex-
plicable position of the embryo of the amniotic vertebrates in
the centre of the blastoderm.
656 EARLY DEVELOPMENT OF THE LACERTILIA.
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 medul-
lary groove. X I2O1.
Fig. i. 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. i. 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.
1 The spaces between the layers in these sections are due to the action of the
hardening re-agent.
XV. ON CERTAIN POINTS IN THE ANATOMY OF
PERIPATUS CAPENSIS'.
THE discovery by Mr Moseley2 of a tracheal system in Peri-
patus 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 dis-
tributed over the globe, is the persisting remnant of what was
probably a large group of forms, from which the present tracheate
Arthropoda are descended.
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 investiga-
tions 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, (i) 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 An-
nelids.
These organs have not completely escaped the attention of
previous observers. The anterior of them were noticed by
Grube3, but their relations were not made out. By Saenger4, as
I gather from Leuckart's Bericht for the years 1868 — 9, these
structures were also noticed, and they were interpreted as seg-
1 From the Proceedings of the Cambridge Philosophical Society, Vol. III. 1879.
2 "On the Structure and Development of Peripatus Capensis," Phil. Trans..
Vol. CLXIV. 1874.
3 "Bau von Perip. Edwardsii" Archiv f. Aiiat. it. Phys. 1853.
4 Moskaner Naturforsclu-r Saniviliing, Abth. Zool. 1869.
658 POINTS IN THE ANATOMY OF PERIPATUS CAPENSIS.
mental organs. Their external openings were correctly identi-
fied. 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 for-
gotten.
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 subdi-
vided 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 tracheae, which appear to me to be similar to the fat bodies
in insects. There are two glandular bodies in the feet in addi-
tion 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 supraoesophageal 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.
POINTS IN THE ANATOMY OF PERIPATUS CAPENSIS. 659
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 suboesophageal ganglia. These
ganglia are closely approximated and united by 5 or 6 com-
missures. They give off large nerves to the oral papillae.
(2) The ventral nerve cords are covered on their ventral
side by a thick ganglionic layer1, 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 nerves2 to the
feet; and the ganglionic swellings of the two cords are connected
together by a pair of commissures containing ganglion cells*.
The other commissures connecting the two cords together do
not contain ganglion cells.
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
supracesophageal 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 com-
1 This was known to Grube, loc. cit.
2 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.
3 These commissures were perhaps observed by Saenger, loc. cit.
66o POINTS IN THE ANATOMY OF PERIPATUS CAPENSIS.
partment 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
papillae. 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 SPONGIDA1.
PROFESSOR SCHULZE'S* last memoir on the development
of Calcareous Sponges, confirms and enlarges MetschnikoflTs8
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.
To render clear what I have to say, I commence with a very
brief statement of the facts which may be considered as estab-
lished with reference to the development of Sycandra raphamts,
the form which was studied by both Metschnikoff and Schulze.
The segmentation of the ovum, though in many ways remark-
able, 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
1 From the Quarterly Journ. of Microscopical Science, Vol. xix, 1879.
2 " Untersuchungen iiber d. Bau u. d. Entwickelung der Spongien," Zeit. f. wiss.
Zool. Bd. xxxi. 1878.
3 " Zur Entwickelungsgeschichte der Kalkschwamme," Zeit. f. wiss. Zool. Bd.
xxiv. 1874.
662
MORPHOLOGY AND SYSTEMATIC
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.
FIG. i.
en
en\
e.g.
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. I, 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 amphi-
blastula 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
POSITION OF THE SPONGIDA.
663
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 promi-
nent (fig. i, 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.
FIG. 2.
ec
Fixed Gastrula stage of Sycandra raphanns (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.
664
MORPHOLOGY AND SYSTEMATIC
After imagination the cilia of the entoderm cells can no
longer be seen, and are probably absorbed, and their disap-
pearance 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
The young of Sycandra raphanus shortly after the development of the spictila
(copied from Schulze).
A. View from the side ; B, view from the free extremity ; os. osculum ; cc. ectoderm ;
en. entoderm composed of collared ciliated cells. The terminal osculum and
lateral pores are represented as oval white spaces.
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
POSITION OF THE SPONGIDA. 665
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 larvae. On the central gastrula cavity
of the sponge becoming placed in communication with the ex-
ternal 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 develop-
ment 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. Ganin1, 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.
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 con-
stant amongst the Calcispongise, and widely distributed in a
somewhat modified condition amongst the Fibrospongiae and
Myxospongiae. 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
1 " Zur Entwickclung d. Spongilla fluviatilis," Zoologischer Anzeiger, Vol. 'l.
No. 9, 1878.
B. 43
666 MORPHOLOGY AND SYSTEMATIC
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 a 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 Lankester1.
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 move-
ments 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 im-
probable that it was completely localised in them, but the
continuation of their function was provided for by the formation
1 " Notes on P'mbryology and Classification." Quarterly Journal of Microscopical
Science, Vol. xvtl. 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.
POSITION OF THE SPONGIDA. 667
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 digestion1. 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. Lieberkuhn 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.
If it is eventually proved by actual experiments on the nutri-
tion 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 Ccelenterata and the
Metozoa. 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.
1 That the flat cells which line the greater part of the passages of most Sponges
are really derived from ectodcnnic invaginations appears to me clearly proved by
Schulze's and Rarrois' observations on the young fixed stages of Halisarca. Ganin
appears, however, to maintain a contrary view for Spongilla.
43—2
XVII. NOTES ON THE DEVELOPMENT OF THE ARANEINA*.
(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 bichro-
mate of potash, after placing them for a short time in nearly
boiling water. They were stained as a whole with haematoxylin
after the removal of the membranes, and embedded for cutting
in coagulated albumen.
The number of investigators who have studied the develop-
ment 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 Claparede
1 From the Quarterly Journ. of Microscopical Science^ Vol. xx. 1880.
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 669
(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. i) has gone with some detail into the history
of the early stages; and Ludvvig (No. 5) has published some
very important observations on the development of the blasto-
derm. 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 : (i) 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
(i) a large, often angular, nucleus, filled with deeply staining
bodies (nucleoli ?). (2) Of 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 (i) 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
6/O NOTES ON THE DEVELOPMENT OF THE ARANEINA.
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 Pis. 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 blasto-
derm.
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 Claparede 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 Claparede 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.
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 6/1
Claparede compares the cumulus to the dorsal organ of many
Crustacea.
Balbiani (No. i) describes the primitive cumulus in Tegenaria
domestica, Epcira diadcnia, 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, (i) 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)1 is the appearance of a small, whitish
spot, which is at first very indistinct. A section through such an
ovum (PI. 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 thick-
ened 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 (PI. 30, fig. i) the whitish spot becomes more con-
1 T 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.
6/2 NOTES ON THE DEVELOPMENT OF THE ARANETNA.
spicuous (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
Claparede 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 (i) 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 (/>£•.), 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.
A section of the ovum at this stage is represented in PL 31,
fig. ii. 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 corre-
sponds 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 thick-
ened ridge of the blastoderm. In any case, it is clear that the
white hemisphere of the blastoderm is a thickened portion of the
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 673
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 tlie original single roiv 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 speci-
mens 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 proce-
phalic 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 Claparede 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 struc-
ture so named by Claparede and Balbiani.
It is clear that Balbiani and Claparede 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 Claparede 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 Claparede is right in
considering a body he figures after six segments are present, to
674 NOTES ON THE DEVELOPMENT OF THE ARANEINA.
be the same as the dorsal organ of the embryo before the form-
ation of any segments, especially as all the stages between the
two appear to have escaped him. In Agelena there is undoubt-
edly 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 observa-
tions 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 pro-
cephalic 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 Claparede 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 chelicerai and pedipalpi are formed later than those of
the first three ambulatory appendages.
Balbiani believes that the segment of the chelicerje 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 pro-
cephalic 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
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 675
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 (PI. 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 blasto-
derm 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 tivo distinct
layers. The outer of these is the epiblast, the inner the mcso-
blast. 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 sec-
tion through the blastoderm of a spider and that of an insect
immediately after the formation of the mesoblast. The reader
should compare Kowalevsky's (Mhn. Acad. Pttersbonrg, Vol.
XVI. 1871) fig. 26, PI. 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^ and 3 b} six distinct
segments are interpolated between the procephalic and the
caudal lobes. The two foremost, c/i 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 seg-
mentation is produced by a series of transverse valleys, sepa-
rating raised intermediate portions which form the segments.
6/6 NOTES ON THE DEVELOPMENT OF THE ARANEINA.
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 ex-
ternal layer of epiblast, and a continuous internal layer of meso-
blast. 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 (PI. 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 reduc-
tion 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 seg-
ment 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 (PI.
30, fig. 4) there is a distinct median ventral groove, extending
through the whole length of the embryo, which becomes, how-
ever, considerably shallower behind. The procephalic region is
distinctly bilobed. The first segment (that of the chelicerae) is
better marked off from it than in the previous stage, but is with-
out 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
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 6/7
a very well-marked swelling at each extremity. These swejlings
are the earliest traces of the appendages. Of the three succeed-
ing 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 con-
cern the mesoblast, which is now imperfectly though distinctly
divided into somites, corresponding with segments visible ex-
ternally. 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 (PI. 30, figs. 5 and 6) is an important
one, as it is characterized by the establishment of the full num-
ber 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 (PI. 30, fig. 6; PI. 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. 1}
well separated from the segment with the chelicerae (c/i). It is
marked by a shallow groove opening behind into a circular
depression (st.) — -the earliest rudiment of the stomodaeum. The
six segments behind the procephalic lobes are the six largest,
and each of them bears two prominent appendages. They con-
stitute 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
chelicerae. Behind the six somites with prominent appendages
there are four well-marked somites, each with a small protuber-
ance. These four protuberances are provisional appendages.
They have been found in many other genera of Araneina (Clapa-
rede, 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
678 NOTES ON THE DEVELOPMENT OF THE ARANEINA.
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 (PI. 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 Claparede.
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 trans-
verse 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 meso-
blastic 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.
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 6/9
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 append-
age-bearing somite a well-marked thickening, which gives in
surface views the appearance of a slightly raised area (PI. 30,
fig. 5), between each appendage and the median line. These
thickenings are the first rudiments of the ventral nerve gang-
lia. 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 divi-
sions (fig. 14, vg}. The nerve cords are formed from before
backwards, and are not at this stage found in the hinder seg-
ments. There is a distinct ganglionic thickening for tJie chelicercs
quite independent of the proccpJialic 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-cesophageal 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 seg-
ments, though I have failed to arrive at quite definite conclu-
sions 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 indi-
cations of the future joints (PI. 30, fig. 6). The full number of
joints are not at once reached, but in the ambulatory ap-
pendages five only appear at first to be formed. There are four
joints in the pedipalpi, while the chelicerae do not exhibit any
signs of becoming jointed till somewhat later. The primitive
presence of only five joints in the ambulatory appendages
68o NOTES ON THE DEVELOPMENT OF THE ARANEINA.
is interesting, as this number is permanent in Insects and in
Peripatus.
The next stage figured forms the last of the third period
(PI. 30, figs. 7 and yd). 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 develop-
ment of the dorsal region. There are the same number of
segments as before, and the chief differences in appearance be-
tween the present and the previous stage depend upon the fact
(i) 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 stomodaeum is definitely established; (4) that the pro-
cephalic 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 chelicerae are two-jointed,
and terminate in what appear like rudimentary chelae, a fact
which perhaps indicates that the spiders are descended from
ancestors with chelate chelicerae. The four embryonic post-
ambulatory appendages are now at the height of their develop-
ment.
The stomodaeum (PI. 30, fig. 7, and PI. 31, fig. 17, sf) is a
deepish pit between the two procephalic lobes, and distinctly in
front of the segment of the cheliceran. 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 chelicerae (PI. 30,
fig- 7> ch. g).
The procephalic lobes (pr. /) 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 ven-
tral ganglionic thickenings are now developed in all the segments
in the abdominal as well as in the thoracic region. The individ-
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 68 1
ual thickenings themselves, though much more conspicuous than
in the previous stage (PI. 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 (PI. 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 (PI. 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 stomodaeum (st).
The existence of a section of the body-cavity in the praeoral
region is a fact of some interest, especially when taken in con-
nection with the discovery, by Kleinenberg, of a similar structure
in the head of Lumbricus. The procephalic lobe represents the
praeoral lobe of Chaetopod larvae, 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 ganglio-
nic 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 con-
sequence 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.
!<\>r Claparedc the prime cause of the change of flexure is
B. 44
682 NOTES ON THE DEVELOPMENT OF THE ARANEINA.
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 ap-
proach each other ventrally.
Barrois takes quite a different view to that of Claparede,
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 PI. 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 em-
bryonic 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 pro-
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 683
cephalic 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 be-
comes 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, Bv,
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 ex-
amples, 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-cesophageal, 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 definite-
ness, 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.
44—2
684 NOTES ON THE DEVELOPMENT OF THE ARANEINA.
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 &), 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 append-
ages. 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 chelicerae 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 ex-
ternal.
The dorsal region is now formed of a (i) 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 com-
menced 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 mesdblast 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.
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 685
The peripheral layer of this cord gives rise to the walls of— the
heart, while the central cells become converted into the cor-
puscles 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 stomodaeum.
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 (PI. 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 chelicerae,
which assists, however, in forming the oesophageal commissures.
The thickenings of the praeoral lobe which form the supra-
cesophageal 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 (PI. 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 stomodaeum has considerably increased in length, and
the proctodaium has become formed as a short, posteriorly
686 NOTES ON THE DEVELOPMENT OF THE ARANEINA.
directed involution of the epiblast I have seen traces of what
I believe to be two outgrowths from it, which form the Mal-
pighian bodies.
The next stage constitutes (PL 30, fig. 9) the last which
requires to be dealt with so far as the external features are con-
cerned. 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 dis-
appeared, unless, which seerns to me in the highest degree im-
probable, they remain as the spinning mammillae, 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 papillae in PL 30, fig. 9.
Dorsally the heart is now very conspicuous, and in front of the
chelicerae may be seen the supra-cesophageal 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 splanch-
nic layers of mesoblast. The parts of the body-cavity so estab-
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 68/
lished are transversely directed channels passing from the Jieart
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 off-
shoots, which unite the various septa together, and divide up
the cavity of the abdomen into a number of partially sepa-
rated 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 junc-
tion 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
mammillae. 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 ;«., 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
688 NOTES ON THE DEVELOPMENT OF THE ARANEINA.
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 stomodaeum, 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 (PI.
31, fig. 20 c.).
The heart has now, in most respects, reached its full de-
velopment. It is formed of an outer muscular layer, within
which is a doubly-contoured lining, containing nuclei at inter-
vals, which is probably of the nature of an epithelioid lining
(PI. 32, fig. 22 hf}. 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 epi-
blast. 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 trans-
verse 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) be-
tween 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 Lepi-
doptera, and he states that it gives rise to the transverse com-
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 689
missures 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 (PI. 32, fig. 21), the
ganglion of the chelicerae has now united with the supra-ceso-
phageal ganglion. It forms, as is shewn in fig. 20 b (ch. g.},
a part of the oesophageal commissure, and there is no sub-
cesophageal commissure uniting the ganglia of the chelicerae,
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 sepa-
rated 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 chelicerae.
(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 chelicerae.
The two hemispherical lobes agree in position with the fungi-
form body (pilshittformige Korpeni), 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.
690 NOTES ON THE DEVELOPMENT OF THE ARANEINA.
Hatschek1 has described a special epiblastic invagination in
the supra-cesophageal 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 Peripat i<--, and
there forms, as I have found, a large part of the supra-ceso-
phageal ganglia. It is figured by Moseley, Phil. Trans., Vol.
CLXIV. pi. Ixxv, fig. 9.
The stomodseum 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 protodaeum (/r.) has also grown in length, and the two
Malpighian vessels which grow out from its blind extremity
(fig. 20 e. nip. g.} have become quite distinct. The part now
formed is the rectum of the adult. The proctodasum is sur-
rounded by a great mass of splanchnic mesoblast. The mesen-
teron has as yet hardly commenced to be developed. There
is, however, a short tube close to the proctodaeum (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 an-
teriorly 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 stomodaeum. In
the posterior part of the thorax (vide fig. 20 d], there is un-
doubtedly no trace of the alimentary tract.
The presence of this rudiment shews that Barrois is mis-
taken in supposing that the alimentary canal is formed entirely
from the stomodaeum and proctodaeum, 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 stomo-
daeum and proctodaeum have reached their full extension at the
1 " Bcitragc z. Entwick. d. Lepidopteren," Jenaische Zeit., Vol. XI. p. 124.
NOTES ON THE DEVELOPMENT OF THE ARANEINA. 69!
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 caeca, each caecum 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 caeca.
I must, in fact, admit that I have hitherto failed to work
out satisfactorily the history of the mesenteron and its append-
ages. 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 re-
lated 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).
692 NOTES ON THE DEVELOPMENT OF THE ARANEINA.
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 (PI. 31, fig. u), 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 Arach-
nida sink into insignificance compared with the immense differ-
ences 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 occa-
sionally 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 differ-
ences between the Crustacea and Tracheata are equally marked,
and the Arachnida agree with the Tracheata. There is gene-
rally in Crustacea an invagination, which gives rise' to the
mesenteron. In Tracheata this never occurs. The proctodaeum
is usually formed in Crustacea before or, at any rate, not later
than the stomodaeum1. The reverse is true for the Tracheata.
In Crustacea the proctodaeum and stomodaeum, especially the
former, are very long, and usually give rise to the greater part
of the alimentary tract, while the mesenteron is usually short.
In the Tracheata the mesenteron is always considerable, and
the proctodaeum is always short. The derivation of the Mal-
pighian bodies from the proctodaeum is common to most Tra-
cheata. Such organs are not found in the Crustacea.
With reference to other points in my investigations, the
evidence which I have got that the chelicerae are true postoral
appendages supplied in the embryo from a distinct postoral
1 If Grohben's account of the development of Moina is correct this statement must
be considered not to be universally true.
NOTES ON THE DEVELOPMENT OE THE ARANEINA. 693
ganglion, confirms the conclusions of most previous investi-
gators, and shews that these appendages are equivalent to the
mandibles, or possibly the first pair of maxillae of other Tra-
cheata. The invagination, which I have found, of part of a
groove of epiblast in the formation of the supra-cesophageal
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 em-
bryo renders it easy to prove that there is no median invagina-
tion of epiblast between them, and supports Kleinenberg's
observations on Lumbricus as to the absence of this invagina-
tion. 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 Chaetopoda
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, " Mdmoire sur le DeVeloppement des Araneides," Ann.
Set. Nat., series v, Vol. xvn. 1873.
2. J. Barrois, " Recherches s. 1. DeVeloppement des Araigne"es," Journal
de PAnat. et de la Physiol., 1878.
3. E. Claparede, Recherches s. V Evolution des Aratgn&s, Utrecht,
1860.
4. Her old, De Generations Araniorum in Ovo, Marburg, 1824.
5. H. Ludwig, "Ueb. d. Bildung des Blastoderm bei d. Spinnen,"
Zeit.f. iviss.Zool., Vol. XXVI. 1876.
694 NOTES ON THE DEVELOPMENT OF THE ARANEINA.
EXPLANATION OF PLATES 30, 31, AND 32.
PLATE 30.
COMPLETE LIST OF REFERENCE LETTERS.
ch. Chelicerse. ch. g. Ganglion of chelicerae. c. 1. Caudal lobe. p. c. Primitive
cumulus, pd. Pedipalpi. pr. I. Praeoral lobe. pp1. //2. etc. Provisional ap-
pendages, sp. Spinnerets, st. Stomodaeum.
I — IV. Ambulatory appendages, i — 16. Postoral segments.
Fig. i. 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. 30 and 3^. 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. la. 'Same embryo as fig. 7, ideally unrolled.
Figs. 8a and 8/>. 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. Chelicerae. ch. g. Ganglion of
chelicerse. ep. Epiblast. hs. Hemispherical lobe of supra-cesophageal ganglion.
At. Heart. /. /. Lower lip. m. Muscles, me. Mesoblast. mes. Mesenteron. mfi.g.
Malpighian tube. ms. Mesoblastic somite, a. CEsophagus. p. c. Pericardium.
pd. Pedipalpi. pd. g. Ganglion of pedipalpi. pr. Proctodwum (rectum), pr. c.
Primitive cumulus, s. Septum in abdomen, so. Somatopleure. sp. Splanchnopleure.
EXPLANATION OF PLATES 30, 31, 32. 695
sf. Stomodaeum. su. Suctorial apparatus. su. g. Supra-cesophageal ganglion.
t&. g. Thoracic ganglion, v. g. Ventral nerve cord. y. c. Cells derived fromTyolk.
yk. Yolk. y. n. Nuclei of yolk cells.
I ^ — IV^-. Ganglia of ambulatory limbs, i — 16. Postoral segments.
Fig. 10. Section through an ovum, slightly younger than fig. i. Shewing
the primitive cumulus and the columnar character of the cells of one half of the
blastoderm.
Fig. n. 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. 1 6. 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. 1 8. 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 '.
IN an interesting memoir devoted to the elucidation of a
series of points in the anatomy and development of the Ver-
tebrata, Schneider2 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.
I3 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 circum-
stances, 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 up-
wards 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 innerva-
tion. A considerable body of evidence is requisite to justify a
belief in the existence of such very extraordinary and un-
paralleled 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.
1 From the Quarterly Journal of Microscopical Science, Vol. XX. 1880.
2 Beitriige z. Anat. u. Entivick. d. Wirbdthiere, Berlin, 1879.
3 " On the Spinal Nerves of Amphioxus," Journ. of Anat. and Phys. Vol. X. 1876.
[This edition, No. IX. p. 197.]
THE SPINAL NERVES OF AMPIIIOXDS. 697
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 sit A, 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 an-
terior border of the spinal cord, but I can find no trace of a con-
nection between it and the cord.
Schneider has represented a transverse section in which the
anterior nerves are figured. I am very familiar with an ap-
pearance in section such as that represented in his figure, but I
satisfied myself when I previously studied the nerves in Amphi-
oxus, 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. Langerhans1, 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.
1 Arehiv f. Alikros. Anatoiiiif, Vol. XII.
B. 45
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 felici-
tous 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 sub-
stantiate their far-reaching conclusions. Since that time an
overwhelming mass of evidence has, however, been rapidly accu-
mulating 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 ani-
mals 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
ADDRESS TO THE BRITISH ASSOCIATION. 699
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 atten-
tion 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 ac-
quired 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 applica-
tion will best be made apparent by taking a concrete example.
Let us suppose a spot on the surface of some very simple organ-
ism to become, at a certain period of life, pigmented, and there-
fore 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
45—2
/OO ADDRESS TO THE DEPARTMENT OF ANATOMY
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 pro-
cess 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 com-
plicated ; 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 exempli-
fied 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
AND PHYSIOLOGY OF THE BRITISH ASSOCIATION. 70 1
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, palaeontology 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 em-
bryonic 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 con-
siderable 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 em-
bryos 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 pro-
position 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 main-
tained 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 em-
bryologists to such resemblances was quite unknown to him.
These preliminary remarks will, I trust, be sufficient to de-
monstrate how completely modern embryological reasoning is
dependent on the two laws of inheritance and variation, which
constitute the keystones of the Darwinian theory.
702 ADDRESS TO THE DEPARTMENT OF ANATOMY
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, in-
stead of developing in a simple and straightforward way, un-
dergo 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, dis-
appear 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 ge-
nealogy 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
AND PHYSIOLOGY OF THE BRITISH ASSOCIATION. 703
naturalists, separated by a wide gulf from the Invertebrate, 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 com-
posed 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 ex-
ternal 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 epi-
thelium. 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
704 ADDRESS TO THE DEPARTMENT OF ANATOMY
place consists in the division or segmentation of the single cell
into a number of smaller cells. The cells then arrange them-
selves 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 ex-
istence 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 ver-
tebrated animals. In the year 1849, ar>d at greater length in
1859, Huxley demonstrated that the bodies of all the polype
tribe or Ccelenterata — 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 hypo-
blast 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 develop-
ment the bodies of all these animals were divided into eer-
o
minal 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 pro-
vided 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
AND PHYSIOLOGY OF THE BRITISH ASSOCIATION. 70$
cavity, and an outer layer, the epiblast. To this form H-aeckel
gave the name of gastrsa 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 stimu-
lating and directing embryological research. It is, moreover,
very doubtful whether there are to be found in the develop-
mental histories of most animals any traces of this gastraea
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 Ccelenterata, 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 epider-
mis 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 Jinrc been formed as differentiations of
706 ADDRESS TO THE DEPARTMENT OF ANATOMY
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, whiah 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 know-
ledge 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.
AND PHYSIOLOGY OF THE BRITISH ASSOCIATION. 707
From embryology we learn that the ganglion-cells _of jthe
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-cesophageal 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 im-
mediately above the supra-cesophageal 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
708 ADDRESS TO THE DEPARTMENT OF ANATOMY
of special sense, especially those of vision, and the central
nervous system. It might have been anticipated a 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 part passn 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 pro-
cesses 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 thick-
ening 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 con-
sist partly of cells sensitive to light, and partly of optical structures
AND PHYSIOLOGY OF THE BRITISH ASSOCIATION. 709
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 develop-
ment 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 satis-
factory 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 Ccelenterata,
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 in-
teresting physiological experiments on these forms; and Professor
Schafer 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
7IO ADDRESS TO THE DEPARTMENT OF ANATOMY
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 pro-
longed 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 (i)
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
AND PHYSIOLOGY OF THE BRITISH ASSOCIATION. 711
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 expla-
nation 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 differentia-
tion 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 Ccelenterata.
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 differ-
entiation of the nervous system may very probably have com-
menced, 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.
712 ADDRESS TO THE DEPARTMENT OF ANATOMY
Local differentiations of the nervous network, which was no
doubt distributed over the whole body, took place on the forma-
tion 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 pro-
cesses 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 con-
tinuous 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 de-
compositions 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."
AND PHYSIOLOGY OF THE BRITISH ASSOCIATION. 713
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 com-
plete.
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 pro-
blems 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.
B. 46
XX. ON THE DEVELOPMENT OF THE SKELETON OF THE
PAIRED FINS OF ELASMOBRANCHII, CONSIDERED IN RE-
LATION TO ITS BEARINGS ON THE NATURE OF THE
LIMBS OF THE VERTEBRATA1.
(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 fins2. More or less
similar views (which I was not at that time acquainted with) had
been previously held by Maclise, Humphrey, and other anato-
mists ; 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 pub-
lished two interesting memoirs comparing the skeletal parts of
the paired and unpaired fins8.
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 essen-
tially of a series of nearly isolated rays, which have a strikingly
similar arrangement to that of the rays of the skeleton in
1 From the Proceedings of the Zoological Society of London, 1881.
2 "Monograph on the Development of Elasmobranch Fishes," pp. 319, 320.
3 J. K. Thacker, "Median and Paired Fins; a Contribution to the History of
the Vertebrate Limbs," Trans, of the Connecticut Acad. Vol. ill. 1877. "Ventral
Fins of Ganoids," Trans, of the Connecticut Acad. Vol. iv. 1877.
SKELETON OF THE PAIRED FINS OF ELASMOBRANCHS. 715
many unpaired fins. He sums up his views in the following
way ' : —
"As the dorsal and anal fins were specializations of the
median folds of Amp/iioxus, so the paired fins were specializa-
tions 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 con-
crescence 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 them-
selves 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 can-
not 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 im-
portant memoir was published by Mivart in the Transactions
of this Society2. 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 cen-
tripetal chondrifications or calcifications, and so be genetically
exoskeletal3.
1 Loc. cit. p. 298.
2 St George Mivart, "On the Fins of Elasmobranchii," Zoological Trans. Vol. x.
3 Mivart used the term exoskeletal in an unusual and (as it appears to me) incon-
venient manner. The term is usually applied to dermal skeletal structures ; but the
46 — 2
716 DEVELOPMENT OF THE SKELETON
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 conclu-
sions at which he has arrived1 : —
" i. Two continuous lateral longitudinal folds were deve-
loped, 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 primi-
tive 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 Noti-
danus, &c.) and sought centripetally (Pristis, &c.) adherence to
the skeletal axis.
"7. The radials of the hinder paired limb did so more con-
stantly, 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.
skeleton of the limbs, with which we are here concerned, is undoubtedly not of this
nature.
1 Loc. cit. p. 480.
OF THE PAIRED FINS OF ELASMOBRANCHS. 717
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 cheir-
opterygium ; but there is not yet enough evidence to determine
what was the precise course of this transformation.
" 1 1. 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 struc-
ture became also quite similar (e.g. Ichthyosaurus, Plesiosaurus,
CJielydra, &c.) ; but for the ordinary quadrupedal mode of pro-
gression 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."
Giinther1 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 Giinther'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 Sela-
chian type of pectoral fin. His own statement on this subject
is as follows2 : —
" On further inquiry into the more distant relations of the
Ceratodns-\\mb, 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
1 " Description of Ceratodus" Phil. Trans. 1871.
- Loc. cit. p. 534.
7l8 DEVELOPMENT OF THE SKELETON
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, pre-
sume 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 fins1.
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 ver-
tebrate 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 Noti-
danus, which he holds to be the most primitive form of Elasmo-
branch fin, " results in the simplest possible manner from the
1 T. H. Huxley, "On Ceratodus Fosteri, with some Observations on the Classifi-
cation of Fishes," Proc. Zool. Soc. 1876.
OF THE PAIRED FINS OF ELASMOBRANCHS. 719
shortening of the axis of such a fin-skeleton as that of Cerajodus,
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.
Gegenbaur1 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 in-
vestigations. After Giinther 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.
His views on this subject are clearly explained in the sub-
joined 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 car-
tilaginous 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 archip-
terygium, the characters of which enable us to follow out the
lines of development of the skeleton of the appendage. Carti-
laginous arches beset with the rays form the branchial skeleton.
The form of skeleton of the appendages may be compared with
1 C. Gegenbaur, Untersuchungen z. vergldch. Anat. d. Wirbeithierc (Leipzig
1864-5): erstes Heft, "Carpus u. Tarsus;" zweites Heft, " Brustflosse d. Fische."
" Ueb. d. Skelet d. Gliedmaassen d. Wirbelthiere im Allgemeinen u. d. Hinterglied-
maassen d. Selachier insbesondere," Jenaische Zeitschrift, Vol. V. 1870. "Ueb. d.
Archipterygium," Jtnaische Zeitschrift, Vol. vn. 1873. "Zur Morphologic d. Glied-
maassen d. Wirbelthiere," Morphologisches Jahrbuch, Vol. II. 1876.
720 DEVELOPMENT OF THE SKELETON
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 arrange-
ment 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 ap-
pendages 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
OF THE PAIRED FINS OF F.LASMOBRANCHS. /2I
divide the entire skeleton of the fin into three segments— pro-,
meso-, and metapterygium.
"The metapterygium represents the stem of the archiptery-
gium and the rays on it. The propterygium and the mesop-
terygium 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. Davidoff1, 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 2 has also written a short
paper in connection with Davidoff's memoir, in support of his
own as against our views.
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.
1 M. v. Davidoff, " Beitrage z. vergleich. Anat. d. hinteren Gliedmaassen d.
Fische, I.," Morphol. Jahrbuch, Vol. V. 1879.
3 " Zur Gliedmaassenfrage. An die Untersuchungen von Davidoff's angekniipfte
Bemerkungen," JMorphol, Jahrbuch, Vol. v. 1879.
722 DEVELOPMENT OF THE SKELETON
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 maybe 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 'Swirski1, which
unfortunately do not throw very much light upon the nature of
the limb.
'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 develop-
ment 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.
caniciila; 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. i) ; and it is to be especially noted that the narrowest part
1 G. 'Swirski, Untersuch. ul>. d. Entwick. d. Schultergiirtels u. d. Skelets d.
Brustflosse d. Hechts, Inaug. Diss. Dorpat, 1 880.
OF THE PAIRED FINS OF ELASMOBRANCHS.
723
of the fin is the base, where is it 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 fibres1.
FIG. i.
Pectoral fins and girdle of an adult of Scyllium canicula (natural size,
seen from behind and above).
co, Coracoid. sc. scapula. //. propterygium. me p. mesopterygium. mp. metap-
terygium. fn. part of fin supported by horny fibre.
FIG. 2.
Right pelvic fin and part of pelvic girdle of an adult female of Scyllium
canicula (natural size).
il. iliac process. /«. pubic process, cut across below, bp. basipterygiiun.
af. anterior cartilaginous fin-ray articulated to pelvic girdle, fn. part of fin supported
by horny fibres.
1 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.
724 DEVELOPMENT OF THE SKELETON
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 (//) is anterior, a second (mep] is placed
in the middle, and a third is posterior (mp). They have
been named by Gegenbaur the propterygiwn, 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 Scy Ilium canicula supports 12 or 13 rays1. It forms a
large part of the posterior boundary of the fin, and bears rays
only on its anterior border.
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 attach-
ment 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, con-
tinues 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 Scy Ilium
canicula and in the male of Scy Ilium 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.
1 In one example where the metapterygium had 13 rays the mesopterygium had
only i rays.
OF THE PAIRED FINS OF ELASMOBRANCHS. 725
Development of the paired Fins. — The first rudiments- of the
limbs appear in Scy Ilium, 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 con-
nected ; but in some Elasmobranch embryos, more especially in
that of Torpedo, they are connected together at their first develop-
ment 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 con-
siderable 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. i 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
726 DEVELOPMENT OF THE SKELETON
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. I, 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
(Ji. f.} ; and dorsally and ventrally to the cartilaginous skeleton
are seen the already well-differentiated muscles (ra).
The pectoral fin is shewn in horizontal section in Plate 33,
fig. 6, at a somewhat earlier stage than that to which the trans-
verse sections belong. The pectoral girdle (p. g} is cut trans-
versely, 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 sepa-
ration into distinct rays is to a large extent completed before
the tissue of which the plates are formed is sufficiently differ-
entiated 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.
OF THE PAIRED FINS OF ELASMOBRANCHS. 727
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 tJie 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 compara-
tively slight. Plate 33, fig. 2, is a representation of the fin and
its skeleton in a female of Scy Ilium stellarc 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. i.
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 Scy Ilium 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.
728 DEVELOPMENT OF THE SKELETON
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 dif-
fers, as I have shewn, from that of the pelvic fin only in minor
points (PI. 33, fig. 6). There is the same longitudinal or basip-
terygial bar (bp], to which the fin-rays are attached, which is
continuous in front with the pectoral girdle (p g). The changes
which take place in the course of the further development, how-
ever, 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 (PI. 33, fig. 6), the base of the fin is as long as the great-
est breadth of the fin ; but it gradually becomes shortened by
being constricted off from the body at its hinder end. In con-
nection 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 (PI. 33, figs.
8 and 9), constituting the metapterygium (inp). It becomes
eventually segmented off from the pectoral girdle, simply articu-
lating 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 be-
comes, in fact, at first only divided into two parts (PI. 33, fig. 8) —
a small anterior part at the front end (me. p\ and a larger pos-
terior 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, re-
sembling in this respect the anterior fin-ray of the pelvic girdle.
It constitutes the (at this stage undivided) rudiment of the meso-
OF THE PAIRED FINS OF ELASMOBRANCHS. 729
pterygium and propterygium of Gcgenbaur. 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 prolonga-
tions 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 under-
stood by reference to PI. 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 (//),
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, conclu-
sions 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 pre-
decessors 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.
B. 47
730 DEVELOPMENT OF THE SKELETON
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 sup-
port this view in that they shew the primitive skeleton of the
fins to have exactly the character which might have been an-
ticipated 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 cartilagin-
ous 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 ante-
rior 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 sub-
ject, 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 struc-
ture 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.
OF THE PAIRED FINS OF ELASMOBRANCHS. 731
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 poste-
rior (or median according to his view of the position of the limb)
side have become aborted, and that the central axis is repre-
sented by the metapterygium ; while ( the pro- and mesoptery-
gium 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 Elasmobranchs, 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 pf the body.
47—2
732 DEVELOPMENT OF FINS OF ELASMOBRANCHS.
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 en-
tirely secondary character of the mesopterygium, and its total
absence in the young embryo Scyllium, appear to me as con-
clusive 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 Elasmobranchs 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 states1 that he has satisfied himself,
from embryos of Acanthias and Scy Ilium, that the rays of the
unpaired fins are undoubtedly products of the segmentation of tJie
dorsal and ventral spinous processes.
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 haemal
arches, and that they are at an early stage of development dis-
tinctly in a more advanced state of histological differentiation
than the neural and haemal arches of the same region. I have
also found exactly the same in the embryos of Lepidostetis.
I have, in fact, no doubt that the skeleton of both the paired
and the unpaired fins of Elasmobranchs and Lepidosteus is in
its development independent of the axial skeleton. The phylo-
genetic mode of origin of the skeleton both of the paired and of
the unpaired fins cannot, however, be made out without further
investigation.
1 Loc. cit. p. 514.
EXPLANATION OF PLATE 33. 733
EXPLANATION OF PLATE 33.
Fig. i. Transverse section through the pelvic fin of an embryo of Scy Ilium
belonging to stage P1, magnified 50 diameters, bp. basipterygium. br. fin ray.
///. muscle, hf. horny fibres supporting the peripheral part of the fin.
Fig. 2. Pelvic fin of a very young female embryo of Scy Ilium stellare, magnified
1 6 diameters, bp. basipterygium. pit. 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 Scy Ilium stellare, magnified 16
diameters, bp. basipterygium. mo. process of basipterygium continued into clasper.
il. iliac process of pelvic girdle, pit. 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. basi-
pterygium. m. muscle of fin. nip. 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 condi-
tion 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.
h f. 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 Scyllittm stellare, magnified 10 diameters, mp. metapterygium. t/ies.
mesopterygium. //. propterygium. cr. coracoid process.
1 I employ here the same letters to indicate the stages as in my "Monograph on
Elasmobranch Fishes."
XXI. ON THE EVOLUTION OF THE PLACENTA, AND ON THE
POSSIBILITY OF EMPLOYING THE CHARACTERS OF THE
PLACENTA IN THE CLASSIFICATION OF THE MAMMALIA'.
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 a priori probable that this was also the case in the
primitive types of the Placentalia ; and this deduction is sup-
ported by the fact that in the Rodentia, Insectivora, and Cheiro-
ptera this peculiarity of the fcetal membranes is actually found.
In the primitive Placentalia it is also probable that from the
discoidal allantoic region of the chorion simple fcetal 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 fcetal 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. (i) by increasing the
complexity of the fetal 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 pro-
cesses would also, of course, be advantageous.
1 From the Proceedings of the Zoological Society of London, 1881.
THE EVOLUTION OF THE PLACENTA. 735
The most fundamental change which has taken place Jn jail
the existing Placentalia is the exclusion of the umbilical vesicle
from any important function in the nutrition of the foetus.
The arrangement of the fcetal parts in the Rodentia, In-
sectivora, 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 pla-
centa 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 fcetal life in the zonary placenta of the Carnivora is probably
due to its being on the whole advantageous to secure the nutri-
tion of the foetus by insuring a more intimate relation between
the fcetal 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 Lemuridae, the Suidae, 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
fcetal 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 Ro-
dentia, Cheiroptera, and Insectivora.
736 THE EVOLUTION OF THE PLACENTA.
The polycotyledonary forms of placenta are due to similar
concentrations of the fcetal villi of an originally diffused pla-
centa. .
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
fcetal villi at the two poles of the ovum. The small size of the
umbilical vesicle in Orycteropus indicates that its discoidal pla-
centa 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 placentae of the
Armadillos, Myrmecophaga, and the Sloths may easily have been
formed from a diffused placenta, just as the discoidal placenta of
the Simiidae and Hominidae appears to have been formed from a
diffused placenta like that of the Lemuridae.
The presence of zonary placentae 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 de-
rived 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 classi-
fication 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 repre-
sentatives of the group are the Rodentia, Insectivora, and Chei-
roptera. Before, however, these three groups had become dis-
tinctly differentiated, there must have branched off from the
.primitive stock the ancestors of the Lemuridae, 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
THE EVOLUTION OF THE PLACENTA. 737
with this conclusion the form of the placenta completely _tal]ies.
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 in-
dependently 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 in-
dependent 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 LEPI-
DOSTEUS1. By F. M. BALFOUR and W. N. PARKER.
(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 Lepidosteiis, 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 . . . 80 1
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
1 From the Philosophical Transactions of the Royal Society, 1882.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 739
Tin, ALIMENTARY CANAL AND ITS APPENDAGES — PAGE
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 OK 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 larvae of Lepidosteus by Professor Alex.
Agassiz, to whom we take this opportunity of expressing our
most sincere thanks. The skull of these embryos and larvae 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 develop-
ment.
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 state-
ment 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.
740 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
GENERAL DEVELOPMENT.
The spawning of Lepidosteus takes place in the neighbour-
hood of New York about May 2Oth. Agassiz (No. i)1 gives an
account of the process from Mr S. W. Carman's notes, which we
venture to quote in full.
" 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 1 5th 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 2Oth
of April, until the I4th 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 i8th, 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
1 The numbers refer to the list of memoirs of the anatomy and development given
at the end of this memoir.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 74!
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 atten-
dant 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 excite-
ment. 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 i8th of May a few eggs were scattered on
several of the beds. On the igth 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 ii inch in length.
Others of 2 feet 6 inches contained ripe ova. With the iQth of
May all disappeared, and for a time — the weather being mean-
while cold and stormy — there were no signs of their continued
existence to be met with. Nearly two weeks later, on the 3ist
of May, as stated by Mr Henry J. Perry, they again came up,
not in small detachments on scattered points as before, but in
742 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 (i) 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
cells1, 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 (2. r.}, and an inner and narrow
homogeneous zone (z. r'.\
Segmentation. — We have observed several stages in the seg-
mentation, 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 circum-
ference (Plate 34, fig. i), 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.
1 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 any-
thing 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.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 743
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.
TJiird 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 (i) an outer area (/. 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 speci-
mens, 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 homo-
logous with the tail swelling of Teleostei. Its structure is more
particularly dealt with in the description of our sections of this
stage.
744 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 uervojts stratum of tlie
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
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 745
what has been called by Gotte l " 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 Gotte in
regarding it as part of the brain.
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 (uis.} in the trunk consists of a pair of inde-
pendent 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 (///.) 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 be-
come more or less fused. In the anterior part of the tail
1 " Ueh. d. Entwick. d. Central Nerven Systems <1. Teleostier," Archiv fiir mikr.
Auat. Vol. xv. 1878.
H. 48
746 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 boun-
dary 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 de-
scribed and the next stage of which we have specimens, a con-
siderable 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 (/z.£.) 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 pre-
served 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» °P-} as flattish outgrowths of the wall of the fore-brain,
STRUCTURE: AND DKYKI.OI-MKNT OK LKITDOSTKUS. 747
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, an.} 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
48—2
748 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
is formed around it. This sheath is probably the commence-
ment 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 promi-
nence. 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 trans-
versely directed streaks, which, by comparison with the Sturgeon1.
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.
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 seg-
mented for the greater part of the length of the trunk, and the
1 Salensky, " Recherches s. le Developpement du Sterlet." Archives de Biol.
Vol. II. 1881, pi. xvn. fig. 27.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 749
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 coagu-
lum. 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 Teleostei1.
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 re-
mainder, and that it was destined to give rise to the nerves.
The process of differentiation is now to a great extent com-
pleted, 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.1t.}. They extend only for a short distance
outwards, gradually tapering off to a point, and situated
1 " Beitrii^e zur Enlwick. <1. Knociuinfische,'' Zcit.f. li'iss. Zool. Vol. xxiil. 1873,
taf. m. tig. ix. 2.
750 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 Birds1, and
by one of us in Elasmobranchs2.
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.) consist-
ing 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 develop-
ment 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 represent-
ing 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,
.jg-.) 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 com-
municates 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.
1 Journal of A 'tint and Pliysiol. Vol. xi. p. 491, plates xx. and xxi.
2 "Elasmobranch Fishes/' p. 156, plates 10 and 13. [This edition, p. 378,
pi. 11, 14-]
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 751
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 Elasmobranchii1. 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 appear-
ance in transverse sections of an axial darker area and a periphe-
ral lighter portion.
The hypoblast retains for the most part its earlier constitution,
but underneath the notochord, in the trunk, it is somewhat thick-
ened, and the cells at the two sides spread in to some extent
under the thickened portion (Plate 36, fig. 29, s.nc.). This thick-
ening, 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 subnoto-
chordal 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 ab-
dominal pore. The posterior part of the duct has still the form
1 " Elasmobranch Fishes," p. 136, plate u, fig. 10. [This edition, p. 354, pi. 12.]
752 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
of a hollow ridge united with somatic mesoblast (Plate 36, fig.
32, s&).
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 Elasmobranchii1.
One of us has shewn that in Elasmobranchs the ventral wall of
the throat is formed not by a process of folding in of the hypo-
blastic 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 Lcpidosteus, 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 ali-
mentary 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).
The form of the lumen of the alimentary tract differs some-
what 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, «/.). 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
1 F. M. Balfour, "Monograph on the Development of Elasmobranch Fishes,"
p. 87, plate 9, fig. 2. [This edition, p. 303, pi. 10.]
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 753
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 em-
bryo (Plate 34, fig. 9) shews a great advance upon the stage last
figured. Both head and body are much more compressed later-
ally 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, /.) 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, an.} are closed, ap-
pearing 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 consider-
ably larger.
The two vertebral portions of the mesoblast are now sepa-
rated 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. »""•)•
In some sections the aorta can be seen (Plate 36, fig. 37, ao.)
lying close under the sub- notochordal 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
754 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
most marked in the region of the trunk (Plate 36, fig. 37). The
sub-notochordal 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, a!.). 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 pro-
vided 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 papillae, of which we shall say more here-
after. 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 de-
pression on each side of the head indicates the posterior boundary
of the mandibular arch. Behind this is placed the very con-
spicuous 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. 1 1, s.d.} is much more
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 755
prominent, and the papillae (about 30 in number) covering it are
more conspicuous from the surface. It is not obviously com-
posed 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 quota-
tions from his memoir.
He states that the first batch were hatched on the eighth1
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. Aerating 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
1 This statement of Agassi/ tides not correspond with the dates on the specimens
>ent to us — a fact no doubt due In the hatching not taking place at the same time for
all the larva.-.
756 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 trans-
parent. 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 extend-
ing from the vent to the yolk-bag is quite narrow. In a some-
what 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, rect-
angular in front, with rounded corners, tapering to a rounded
point towards the posterior extremity, with re-entering sides."
We have figured an embryo of 1 1 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, ?;z.)
more or less rhomboidal, and is bounded behind by the mandi-
bular arch (;;z«.) and laterally by the superior maxillary processes
(s. mx). In front of the mouth is placed the suctorial 'disc (s. d.}, the
central papillae of which are arranged in groups. The opercular
fold (Ji. 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, /<:./) 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.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 757
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 max-
illary 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
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
758 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 some-
what 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 super-
ficial. 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 dis-
appeared as an external appendage.
After the stage last described the young Fish rapidly ap-
proaches 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 ex-
ternally heterocercal tail, caused by the persistence of the primi-
tive caudal fin as an elongated filament projecting beyond the
permanent caudal (Plate 41, fig. 68).
Delicate dermal fin-rays are now conspicuous in the peri-
pheral parts of all the permanent fins. These rays closely
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 759
resemble the horny fin-rays in the fins of embryo Elasrno-
branchs 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, 1 1 centims. in length, in
which the scales have begun to be formed, is shewn in Plate 34,
fig. 1 6.
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
Lcpidostcus is quite marked."
BRAIN.
I. Anatomy.
The brain of Lepidostcus 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
760 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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. 47 A, P, 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 thalamen-
cephalon.
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 enlarge-
ments (Plate 38. figs. 47 A, B, and C, off.) at the front end of the
brain1 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.
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 Gotte's
researches shewed that this view was not tenable.
1 The homoiogies of the olfactory lobes throughout the group of Fishes require
further investigation.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 761
The anterior lobes of the cerebrum have a conical fornv taper-
ing 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 con-
spicuous furrows (Plate 38, fig. 47 B, 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 " pro-
thalami."
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 ot nervous matter, in part of
which, judging from Wilder's description, a well-marked com-
missure is placed. We have found in the larva a large com-
missure 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.
46 B). 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
B. 49
762 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 pro-
posed by Wilder, or for regarding them as a section of the
brain peculiar to Fishes.
The thalamencephalon (///.) contains the usual parts, but is
is 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
Polyptertis.
On the roof of the thalamencephalon is placed a large thin-
walled vesicle (Plate 38, figs. 47 A 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 thalamen-
cephalon; 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 repre-
sented 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 thalamen-
cephalon. 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.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 763
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 Stannius1,
and stated by him to be wholly formed of the membranes of the
brain, is really the homologue of our vesicle.
Wiedersheim 2 has recently described in Protopterus a body
which is undoubtedly homologous with our vesicle, which he
describes in the following way : —
" Dorsalwarts ist das Zwischenhirn durch ein tiefes, von
Hirnschlitz eingenommenes Thai von Vorderhirn abgesetzt ;
dasselbe ist jedoch durch eine hautige, mit der Pia mater zusam-
menhangende Kuppel oder Kapsel uberbruckt."
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 Huxley3 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.
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. 47 A, in.} is very elongated.
Immediately in front of it is placed the optic chiasma (Plate 38,
figs. 47 A and C, op.c/i.} 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 Muller's figure of the brain of Po-
lypterus.
On the sides of the infundibulum are placed two promi-
nent bodies, the lobi inferiores (/.#/.), each of which contains a
cavity continuous with the prolongation of the third ventricle
1 " Ueb. d. Gehirn des Stors," Muller's Archii\ 1843, and Lehrbuch d. z-ergl. Anat.
d. Wirbdthiere. Cattie, Archives tie Biologic, Vol. in. 1882, has recently described
in Acipcnscr 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
Lepidostetis. (June 28, 1882.)
2 R. Wiedersheim, Morphol. SfuJitn, 1880, p. 71.
a " On Certitihtm h'orstirij' kc., /'roc. tool. Soc. ^76.
49—2
764 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 (<?/./.). 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 prolon-
gation 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. 47 A
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. 47 A,
cb.}. As shewn by Wilder, its wall actually has in longitudinal
section this form of curvature, owing to its anterior part pro-
jecting forwards into the cavity of the iter1. This forward pro-
jection is not, however, so conspicuous as in most Teleostei.
The cerebellum contains a large unpaired prolongation of the
fourth ventricle.
II. Development.
The early development of the brain has already been de-
scribed ; 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 larvae of 15 and 26 millims., and transverse sections (Plate 37,
figs. 46 A — G) of the brain of a larva at about the latter stage
(25 millims.).
1 In Wilder'* figure the walls of the cerebellum are represented as much too thin.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 765
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. 46 A) completely divided into
two hemispheres. The roof of the undivided posterior part of
the cerebrum is extremely thin (Plate 37, fig. 46 B). 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-posteriorly1, 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, ///.).
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 46 C and D, /«.). 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. 46 C and
D, as tli.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
1 Vide F. M. Balfour, Comparative Embryology, Vol. n. figs. 248 and 250.
766 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
(Plate 37, fig. 46 C, z.}, which is the homologue of a similarly-
situated commissure present in the Elasmobranch brain1, 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. 46 C and D, op.th^, which are
continuous in front with the thickened outer walls of the hemi-
spheres. Below, the thalamencephalon is produced into a very
elongated infundibulum (Plate 37, figs. 44, 45, 46 E, in.}, the
apex of which is trilobed as in Elasmobranchii and Teleostei.
The sides of the infundibulum exhibit two lobes, the lobi infe-
riores (Plate 37, fig. 46 E, l.in.}, which are continued posteriorly
into the crura cerebri.
The pituitary body2 (Plate 37, figs. 44, 45, 46 E, pt} is small,
not divided into lobes, and provided with a very minute lumen.
In front of the infundibulum is the optic chiasma (Plate 37,
fig. 46 D, op. c/i.}, which is developed very early. It isA as stated
by Miiller, a true chiasma.
The mid-brain (Plate 37, figs. 44 and 45, m. b.} is large, and
consists in both stages of (i) 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. 46
E, F, G, op. /.) 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. 46 E).
These masses probably become in the adult the more conspicuous
1 Vide F. M. Balfour, Comparative Embryology, Vol. n. pp. 355 — 6 [the original
edition], where it is suggested that this commissure is the homologue of the grey
commissure of higher types.
2 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 repre-
sented in transverse section in two consecutive sections. Anteriorly it is still con-
nected 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.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 767
prominences of the floor of the ventricles of the optic_Jo_bes,
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. : cere-
bellum 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. 46 F and G, cb.) ; and
its two lobes, each with a prolongation of its cavity, are con-
tinued 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 Gottsche.
III. Comparison of the larval and adult brain of Lepidosteus,
togetJier with some observations on tJie systematic value of the
characters of the Ganoid brain.
The brain of the older of the two larvae, 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 (i) 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
768 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 larvae 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 identify-
ing the vesicle in the adult with the pineal gland.
Muller, 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, (i) the great elongation of the region of the thalamen-
cephalon ; 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.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 769
The presence of a largely developed thalamencephajpn 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 some-
what everted (cf. Wilder), and in Lepidosteus these edges have in
the adult a very great development, and form (vide Plate 38, fig.
47 A — C, £•/.) 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 (Protoptcrus, Wiedersheim1) 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 (Ccratodus, Huxley2, Lepidosiren, Hyrtl3) ; 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.
l. Stiidicn, in. Jena, 1880.
2 "On Ceratodns Forsleri," Proc. Zool. Soc. 1876.
;| Ltpidosireit paradexa. Prag. 1845.
770 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 M tiller'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 Lepi-
dosteus 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
A mia.
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
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 771
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 em-
bryonic 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 tlie nervous
layer of tlic 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 open-
ing 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 examin-
ation of the eye of Lcpidostcns, which in our specimens was not
sufficiently well preserved for such a purpose ; but we have
772 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 hya-
loid membrane, i.e. on the side of the hyaloid membrane bound-
ing 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 per-
forating the retina close to the optic nerve, and obviously homo-
logous with the artery of the processus falciformis and pecten
of Teleostei and Birds, and with the arteria centralis retinae 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 (z>). 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 com-
posed of a transparent matrix, in which numerous cells are
embedded (Plate 38, fig. 50).
Development. — In the account of the first stages of develop-
ment of Lepidosteus, the mode of formation of the optic cup, the
lens, Sec., 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.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 773
—
Lepidosteus is very remarkable for the great number of meso-
blast 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, vJt). 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 con-
sider 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 ex-
hibit 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 Elas-
774 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
mobranch eye in the treatise On Comparative Embryology, by
one of us1, 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.
Johannes Mliller mentions the absence of a processus falci-
formis as one of the features distinguishing Ganoids and Te-
leostei. 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 Elasmo-
branchii 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 imme-
diately 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,
1 Vol. ii. p. 414 [the original edition].
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 775
figs. 1 1 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 papillae often exhibiting a bilateral arrangement.
The papillae 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 reti-
culum. 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 papillae to
pour out a sticky secretion.
MUSCULAR SYSTEM.
There is a peculiarity in the muscular system of Lcpidostens,
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 larvae
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 indica-
tion 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 Cyclosto-
mata and Amphioxus the embryonic condition is retained, as it
is in Lepidostcus.
776 STRUCTURE AND DEVELOPMENT OF 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 vertebrae by a
convex face in front and a concave face behind, being thus,
according to Owen's nomenclature, opisthoccelous. It presents
on its under surface a well-marked longitudinal ridge, which in
many vertebrae 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 pro-
minent haemal processes (h.a.}, to the ends of which are articu-
lated the ribs. These processes have a nearly horizontal direc-
tion 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 vertebrae, so that comparatively narrow spaces are left be-
tween the neural arches of successive vertebrae 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 pro-
cesses appear to be confined to the posterior parts of the ver-
tebrae, so that at the front ends of the vertebrae, 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.e.) (probably
fibre-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
. STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 777
distance over the vertebra behind. The successive elements arc
connected by fibrous tissue, and are continuous dorsally with
a fibrous band, known as the ligamentum longitudinale superius
(Plate 42, figs. 80 and 81, /./.), characteristic of Fishes generally,
and running continuously for the whole length of the vertebral
column. Each of the cartilaginous elements is, as will be after-
wards 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 Elasmobranchs, were
not the latter vertebral instead of intervertebral in position.
More or less similar elements are described by Gotte in the
neural arches of many Teleostei, which also, however, appear to
be vertebral ly placed, and he has compared them and the corre-
sponding elements in the Sturgeon with the Elasmobranch
cartilages forming the keystone of the neural arch. Gotte does
not, however, appear to have distinguished between the carti-
laginous 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
Lcpidosteus.
The posterior ends of the neural plates of the neural arches
are continued into the dorsal processes directed obliquely up-
wards 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 liga-
mentum longitudinale are placed.
The vertebrae are wholly formed of a very cellular osseous
tissue, in which a distinction between the bases of the neural
and haemal processes and the remainder of the vertebra is not
recognizable. The bodies of the vertebrae are, moreover, directly
continuous with the neural and haemal arches.
The ribs in the region of the trunk arc articulated to the
ends of the long haemal 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
B. 50
7/8 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. ,
peritoneal membrane, but pass outzvards 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 trans-
late the description given by Gegenbaur of this region (No. 6,
p. 411): — "Up to the 34th vertebra the ribs borne by the late-
rally and posteriorly directed processes present nothing remark-
able, 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 back-
wards so that both ribs decidedly approach before bending out-
wards. 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 haemal arch. The two, up to this point separated
ribs, have here formed a hcemal 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 haemal 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 vacuo-
latcd, while the septa between the vacuoles form a delicate
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 779
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 pro-
longed upwards so as to meet above the neural canal, for which
they form a kind of sheath. On the ventral side of the noto-
chord 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 haemal arches
also become established, and arise by the formation of similar
enlargements of the ventral or haemal 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
haemal arches suddenly enlarge and extend ventralwards (Plate
41, fig. 67, /i.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 haemal canal. At
the point where they first meet the permanent caudal fin com-
mences, and here (Plate 41, fig. 68) we find that not only do the
haemal 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
50 — 2
780 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
supported by parts of the true vertebral column and not by
independently formed elements of the skeleton.
Each of the large caudal haemal arches, including the spine,
forms a continous 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 haemal 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. Dur-
ing the same period, however, the true sheath of the notochord
greatly increases in thickness, and the membrana elastica ex-
terna becomes more definite. So far it would be impossible to
distinguish the development of the vertebral column of Lepidos-
teus 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 Lepidosteus1, which have enabled us to
work out with tolerable completeness the remainder of the de-
velopmental 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.
In the notochord the most important and striking change
consists in the appearance of a series of very well marked verte-
bral constrictions opposite the insertions of the neural and hcemal
arches. The first constrictions of the notochord are thus, as in
other Fishes, vertebral; and although, owing to the growth of
the -inter vertebral cartilage, the vertebral constrictions are subse-
quently replaced by intervertebral constrictions, yet at the same
time the primitive occurrence of vertebral constrictions demon-
strates that the vertebral column of Lepidosteus is a modification
of a type of vertebral column with biconcave vertebrae.
1 These specimens were given to us by Professor W. K. Parker, who received
them from Professor Hurt G. Wilder.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 781
The structure of the gelatinous body of the notochorct 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 (PJate 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 -oi 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, concentri-
cally 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 Kolliker'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 mem-
brana elastica externa (m.e/).
The changes which have taken place in the parts which form
the permanent vertebrae 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 haemal arches resting upon
the membrana elastica externa ; but longitudinal sections (fig. 69)
shew that laterally these arches join a cartilaginous tube, embrac-
ing 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 haemal 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
782 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 appear-
ance 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:
(i) 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
(i) 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 Gotte 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 Gotte in the case of the
Teleostei.
Immediately beneath this rod is placed the longitudinal
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 783
ligament (Plate 41, fig. 70, /./.), 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 haemal arches.
The haemal 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 haemal arches in pass-
ing from the tail to the trunk.
It will be remembered that at an earlier stage the haemal
arches in the region of the tail-fin were fully formed, and that
through the anterior part of the caudal region the haemal pro-
cesses 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 haemal arches in the tail as
uiijointed cartilaginous bars investing the caudal arteries and
veins is so similar to that of the caudal haemal arches of
Elasmobranchii, that it appears to us impossible to doubt their
identity in the two groups1.
The changes which have taken place by this stage with
reference to the haemal arches of the tail are not very con-
siderable.
In the case of a few more vertebrae the haemal processes
1 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 Lepidostens
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 haemal 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 haemal 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 larvae to work
with by which alone this question could be settled.
784 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 commence-
ment of a segmentation of the distal parts of the haemal arches
from the proximal. This process has not, however, as yet re-
sulted in a complete separation of the two, such as we find in
the adult.
If the haemal processes are traced forwards (Plate 42, figs.
75 and 76) from the anterior segment where they meet ventrally,
it will be found that each haemal 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 haemal processes (Plates 41 and 42, figs. 73 and 74), but
while the basal portions graw 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 haemal 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 peri-
toneal 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 ivith the
hcstnal processes, and that the indications of a separation between
STRUCTURE AND DEVELOPMENT OF LEPTDOSTEUS. 785
those two parts at this stage are not due to a secondary fusion,
but to a commencing segmentation.
It further appears, as Mtiller, Gegenbaur and others have
stated, that the ribs and haemal processes of the tail are serially
homologous structures ; but that the view maintained by Gotte
in his very valuable memoirs on the Vertebrate skeleton is also
correct to the effect that the Jicemal arches of tlie tail are Jwmo-
logous throughout the series of FisJies.
To this subject we shall return again at the end of the
section.
Before leaving the haemal arches it may be mentioned that
behind the region of the ventral caudal fin the two haemal pro-
cesses 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
vertebrae. These rings are united with the neural and haemal
arches of the vertebrae 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 haemal arches of the adjacent
vertebrae, and afford presumptive evidence of the derivation of
the intervertebral rings from the neural and haemal 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 describ-
ing, also arrived at the conclusion that the intervertebral carti-
lages were derived from the neural and haemal arches ; but as
doubts have been thrown upon this conclusion by Gotte, 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
786 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
time we think that we have adduced weighty evidence in corrobo-
ration 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 vertebrae 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
fibre-cartilage. On each side of the line of division separating
two vertebrae it is invested by a superficial osseous deposit.
The next oldest larva we have had was 1 1 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 deve-
lopment 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 verte-
brally. 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
vertebras of Lepidosteus acquire their unique character amongst
Fishes.
These constrictions still, however, coexist with the earlier,
though at this stage relatively less conspicuous, vertebral con-
strictions.
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 — (i) externally, the membrana elastica externa (m.el.) ;
STRUCTURE ANJ) DEVELOPMENT OF LEPIDOSTEUS. 787
i
then (2) the external layer of the sheath (s/i.)>, 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, O'i8
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 noto-
chord may conveniently be dealt with in the same order as
before, viz. : the neural arches, the haemal 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 in-
vested 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 (i) two bars of cartilage
repeated for each vertebra, but intervertebral ly placed, which are
directly differentiated from the ligamentum longitudinale supe-
rius, 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
788 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 mem-
brane-bone, there being preformed in cartilage only a small basal
part, a dorsal process, and paired key-stones below the ligamen-
tum longitudinale superius.
The haemal arches (Plate 42, fig. 78) are still largely carti-
laginous, and rest upon the sheath of the notochord. They are
invested by a thick layer of bone. The bony layer investing
the neural and haemal 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 com-
mencement 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 pro-
duced. 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
vertebrae.
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,
ng- 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 peri-
chondrium (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: (i) the disappearance of all trace of the
STRUCTURE AND DEVELOPMENT OF I.EPIDOSTEUS. 789
primitive vertebral constriction of the notochord ; (2) the-ne-arly
completed constriction of the notochord in the intervertebral
regions ; (3) the complete ossification of the vertebral portions
of the bodies of the vertebrae, the terminal so-called intervertebral
portions alone remaining cartilaginous ; (4) the complete ossifi-
cation of the basal portions of the haemal and neural processes
included within the bodies of the vertebrae, 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.
Gotte in his memoir on the formation of the vertebral bodies
of the Teleostei attempts to prove (i) that the so-called mem-
brana 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 Lepidostcus we have met with no indication that the mem-
brana elastica externa is composed of cells ; though it is fair to
Gotte 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 inter-
vertebral cartilages ; and Gcgenbaur 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 noto-
chord, 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
790 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 haemal 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 haemal arches
becomes larger than the one in front, each arch finally meeting its
fellow below the caudal vein, thus forming a completely closed
haemal 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 study-
ing (larva of 5^ 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 haemal 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 back-
wards. 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 haemal arches, not only in the tail, but also
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 791
in the trunk, where they pass ventralwards on each side-oil 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 con-
tinuity of structure between the haemal processes of the tail and
the ribs. In the anterior part of the trunk the ribs pass out-
wards along the intermuscular septa till they reach the epidermis.
Thus the ribs are originally continuous with the haemal pro-
cesses. Behind the region of the ventral caudal fin the two
haemal 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 vertebrae, the curved line where this will be effected
being plainly marked out. These rings are united with the
neural and haemal arches of the vertebrae next in front and
behind. As these rings are formed originally by the spreading
of the cartilage from the primitive neural and haemal processes,
the intervertebral cartilages are clearly derived from the neural
and haemal arches. The intervertebral cartilages are thicker in
the middle than at their two ends.
In our latest stage (u 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 differen-
tiated 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.
792 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
Thus the greater part of the neural arches is formed of mem-
brane bone. The haemal 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 vertebrae of
Lepidosteus caused L. Agassiz (No. 2) to compare them with the
vertebrae of Reptiles, and subsequent anatomists have suggested
that they more nearly resemble the vertebras of some Urodelous
Amphibia than those of any other form.
If, however, Gotte's account of the formation of the am-
phibian vertebrae is correct, there are serious objections to a
comparison between the vertebrae 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 vertebrae.
In Lepidosteus this cartilage is, as we have seen, derived from
the bases of the arches ; but in Amphibia it is held by Gotte 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 de-
veloped. Provisionally, therefore, we must look elsewhere
than in Lepidosteus for the origin of the amphibian type of
vertebrae.
The researches which we have recorded demonstrate, how-
ever, in a very conclusive manner that the vertebras of Lepi-
dosteus have very close affinities with those of Teleostei.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 793
In support of this statement we may point: (i) To the
structure of the sheath of the notochord ; (2) to the formation of
the greater part of the bodies of the vertebrae from ossification
in membrane around the notochord ; (3) to the early biconcave
form of the vertebras, only masked at a later period by the de-
velopment of intcrvertebral 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 vertebrae (Plate 42,
fig. 78) with Gotte's1 figure of the section of the vertebra of a
Pike (Plate 7, fig. i). In Gotte's figure there are shewn similar
intercalated pieces of cartilage to those which we have found,
and similar cartilaginous dorsal processes of the vertebrae. Thus
we are justified in holding that whether or no the opisthoccelous
form of the vertebrae of Lepidosteus is a commencement of a
type of vertebrae inherited by the higher forms, yet in any case
the vertebrae are essentially built on the type which has become
inherited by the Teleostei from the bony Ganoids.
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 Gotte'2 on the
Vertebrate skeleton. The alternatives usually adopted are,
roughly speaking, these : — Either the haemal 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 haemal arches in the tail are differently formed
in the different types. Gotte has brought forward a great body
of evidence in favour of the first view; while Gegenbaur3 may
1 "Beitrage zur vergl. Morphol. d. Skeletsystems d. Wirbelthiere." Archiv /.
Mikr. Anat. Vol. XVI. 1879.
- " Beitrage z. vergl. Morph. d. Skeletsystems d. Wirbelthiere. II. Die Wir-
belsaule u. ihre Anhange." Archiv f. Mikr. Anat., Vol. xv., 1878, and Vol. xvi.,
1879.
3 " Ueb. d. Entwick. d. Wirbelsiiule d. Lepidosteus, mil. vergl. Anat. Bemer-
kungen. " Jcnaisc/ic Zeilschrift, Bd. in., 1863.
B. 5I
794 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
be regarded as more especially the champion of the second
view.
One of us held in a recent publication1 that the question was
not yet settled, though the view that the ribs are homologous
throughout the series was provisionally accepted.
It is admitted by both Gegenbaur and Gotte that in Lepido-
stens 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 haemal arches, and our researches have
abundantly confirmed this conclusion.
Are the haemal arches, the ventral parts of which are thus
formed by the coalescence of the ribs, homologous with the
haemal 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 haemal arches in the tail in these two
groups is practically identical ; they are formed in both as simple
elongations of the primitive haemal 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 haemal 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 haemal arches of the tail
are unsegmented cartilaginous arches, as they permanently are
in Elasmobranchii. If, however, the homology between the
haemal arches of the two types should still be doubted, the fact
that in both types the haemal 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 haemal arches of
the tail in Lepidosteus and Elasmobranchii might at first sight be
taken as a conclusive argument in favour of Gotte's view, that
the ribs of Elasmobranchii are not homologous with those of
Ganoidei. This view is mainly supported by two facts : —
1 Comparative Embryology, Vol. II., pp. 462, 463 [the original edition].
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 795
(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 haemal arches of the tail, but would rather seem to
be lateral offshoots of the haemal processes, while the haemal
arches of the tail appear to be completed by the coalescence of
independent ventral prolongations of the haemal 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. I, rb.},
FIG. i.
II,
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., hremal
process; k., kidney; l.s., ligamentum longitudinale superius ; m.el9 membrana
elastica externa ; na., neural arch; no., notochord ; //., lateral line; rb., rib;
sp.c., spinal cord.
while in Lepidosteus and other Ganoids they immediately girth
the body-cavity.
There is much, therefore, to be said in favour of Gottc'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 haemal arches throughout the Pisces.
51—2
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 haemal arches. It is easy to con-
ceive 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 haemal processes. If, how-
ever, the haemal canal became prolonged forwards by the forma-
tion of some additional complete or nearly complete haemal
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 haemal canal, but the continuation forwards of the canal
would be effected by prolongations of the haemal processes
supporting the ribs. The new arches so formed would naturally
be held to be homologous with the haemal 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 haemal processes of a wholly
different nature to the ventral parts of the haemal arches of the
tail.
In some Elasmobranchii, as shewn in the accompanying
woodcut (fig. 2), in the transitional vertebrae between the trunk
and the tail, the ribs are supported by lateral outgrowths of the
haemal processes, while the wholly independent prolongations of
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 797
the haemal processes appear to be about to give rise tcr the
haemal arches of the tail.
This peculiar state of things led Gotte, and subsequently one
of us, to deny for Elasmobranchs all homology between the ribs
and any part of the haemal arches of the tail ; but in view of the
explanation just suggested, this denial was perhaps too hasty.
FIG. 2.
r.p -
. .V. COLXL*.
Transverse segtion 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., haemal process ; ;-./., process to
which the rib is articulated ; m.el., membrana elastica externa ; ck., notochord ;
ao., aorta; V.cau., caudal vein.
We are the more inclined to take this view because the re-
searches of Gotte appear to shew that an occurrence, in many
respects analogous, has taken place in some Teleostei.
In Teleostei, Johannes Muller, and following him Gegenbaur,
do not admit that the haemal arches of the tail are in any part
formed by the ribs. Gegenbaur (Elements of Comp. Anat., trans-
lation, p. 431) says, "In the Teleostei, the costiferous transverse
processes" (what we have called the haemal processes) "gradually
798 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 haemal arches of the tail in Tele-
ostei contain parts serially homologous with the basal parts of
the haemal processes as well as with the ribs, has been also
maintained by many anatomists, e.g., Meckel, Aug. Muller, &c.,
and has recently found a powerful ally in Gotte.
In many cases, the relations of the parts appear to be funda-
mentally those found in Lepidosteus and Amia, and Gotte 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 haemal costiferous pro-
cesses of Gegenbaur, which support them, enter into the forma-
tion of the haemal arches of the tail.
In a great number of Teleostei, e.g., the Salmon and most
Cyprinoids, &c., the haemal arches in the region of transition
from the trunk to the tail have a structure which at first sight
appears to support Johannes Muller's and Gegenbaur's view.
The hsemal 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 Gotte, who attempts to shew (with, in our opinion,
complete success) that the anterior haemal arches are really not
entirely homologous with the true haemal arches behind, but
that in the latter, the closure of the arch below is effected by the
haemal spine, which is serially homologous with a pair of coal-
esced ribs, while in the anterior haemal arches, i.e., those of the
trunk, the closure of the arch is effected by a bridge of bone
uniting the haemal processes.
The arrangement of the parts just described, as well as the
view of Gotte with reference to them, will be best understood
from the accompanying woodcut (fig. 3), copied from Gotte's
memoir.
Gotte sums up his own results on this point in the following
words (p. 138): "It follows from this, that the half rings, forming
the haemal canal in the hindermost trunk vertebrae of the Sal-
mon, are not (with the exception of the last) completely homo-
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 799
logous with those of the tail, but are formed by a connecting
piece between the basal stumps (haemal processes), which origi-
nates as a paired median process of these stumps."
The incomplete homology between the anterior haemal arches
and the true caudal haemal 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.
• If this admission is made, the only ground for not regarding
the ribs of Elasmobranchii as homologous with those of Ganoids
FIG. 3.
Semi -diagrammatic transverse sections through the first caudal vertebra (A), the last
trunk vertebra (B), and the two trunk vertebra- in front (C and D), of a Salmon
embryo of 2-3 centims. (From Gbtte.)
ttb., hremal arch; ul>'., haemal process; ui>"., rib; c., notochord ; a., aorta; v., vein;
h., connecting pieces between haemal processes ; u., kidney ; </., intestine ;
sp'., hnemal spine ; m'. , muscles.
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 Gotte's view, may be thus stated: — The haemal arches
80O STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
are homologous throughout the Pisces : in Teleostei, Ganoidei,
and Dipnoi1, the ribs, placed on the inner face of the body-wall,
are serially homologous with the ventral parts of the haemal
arches of the tail; in Elasmobranchii, on the other hand, the ribs
are neither serially homologous with the haemal arches of the
tail nor homologous with the ribs of Teleostei and Ganoidei, but
are outgrowths of the haemal 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 vertebrae.
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 Elasmobran-
chii are provided with homologous haemal arches, which are
formed by the coalescence below the caudal vein of simple pro-
longations of the primitive haemal processes of the embryo. The
canal enclosed by the haemal arches can be demonstrated em-
bryologically to be the aborted body-cavity.
In the region of the trunk the haemal processes and their
prolongations behave somewhat differently in the different types.
In Ganoids and Dipnoi, in which the most primitive arrange-
ment is probably retained, the ribs are attached to the haemal
processes,and are placed immediately without the peritoneal mem-
brane at the insertions of the intermuscular septa. These ribs are
in many instances (Lepidosteus, Acipenser}, and very probably in
all, developed continuously with the haemal processes, and be-
come subsequently segmented from them. They are serially
homologous with the ventral parts of the haemal arches of the
tail, which, like them, are in many instances (Ceratodus, Lepidos-
teus, Polypterus, and to some extent in Amia] segmented off
from the basal parts of the haemal 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 hsemal processes of the tail, is often (e.g., the
S Imon) obscured by some of the anterior haemal arches in the
I "erior part of the trunk being completed, not by the ribs, but
1 We find the serial homology of the ribs and ventral parts of the hsemal arches to
be very clear in Ceratodtis. Wiedersheim states that it is not clear in Protopterus,
although he holds that the facts are in favour of this view.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 8oi
by independent outgrowths of the basal parts of the haemal pro-
cesses.
In Elasmobranchii a still further divergence from the primi-
tive 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 haemal arches similar to those in the
Salmon, renders their serial homology with the ventral parts of
the haemal processes of the tail far less clear than in other types,
and further proof is required before such homology can be con-
sidered 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 (i) occupy the same position in relation to
the muscles as the Elasmobranch ribs, (2) that they are con-
nected with the neural arches, and (3) that they coexist in the
tail with the haemal arches, and seem, therefore, to be as differ-
ent as possible from the ribs of the Dipnoi.
PART IV. — The skeleton of the ventral lobe of the tail fin, and its
bearing on tlie nature of the tail fin of tlie various types of Pisces.
In the embryos or larvae of all the Elasmobranchii, Ganoidei,
and Teleostei which have up to this time been studied, the un-
paired 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 constit! e
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
(Angtiilla), in which the fins are continuous, have probably re-
802 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
verted 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
larvae of the above groups a special ventral lobe of the em-
bryonic fin a short distance from the end of the tail. In Elasmo-
branchii and Chondrostean Ganoids the portion of the em-
bryonic 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. Agassiz1, most
Teleostei acquire at an early stage of their development hetero-
cercal caudal fins, like those of Elasmobranchii and the Chondro-
stean 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.
The true significance of the dorsally flexed portion of the
vertebral axis was first clearly stated by Huxley2, 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 be-
tween the embryonic development of the tail in these Fishes
and the palseontological development of this organ. We think
1 " On the Young Stages of some Osseous Fishes. — I. The Development of the
Tail," Proc. of the American Academy of Arts and Sciences^ Vol. XIIL, 1877.
2 "Observations on the Development of some Parts of the Skeleton of Fishes,"
Quart. Journ. of Micr. Science, Vol. VII., 1859.
STRUCTURE AND DEVELOPMENT OF LEl'IDOSTKUS. 803
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.
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 haemal 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 arid
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.
Davidofif1, 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.
Thacker2, 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
luemal spines."
Mivart3 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 Elasmobranchs, in that in
1 " Beitrage z. vergl. Anat. d. hinteren Gliedmassen d. Fische," Morph. Jahrbuch,
Vol. v., 1879.
* J^rans. of the Connecticut Accui., Vol. III., 1877.
:l St George Mivart, "Fins of Elasmobranchs," Zool. Trans., Vol. X.
804 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
the former the radials are more numerous than the vertebrae and
unconformable to them, while in the latter they are equal in
number to the vertebrae and continuous with them. " This," he
goes on to say, "seems to point to a difference in nature be-
tween the dorsal and ventral portions of the caudal fin, in at
least most Elasmobranchs." He further points out that Polyodon
resembles Elasmobranchs. As to Teleostei, he does not express
himself decidedly except in the case of Murcena, to which we
shall return.
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 haemal 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 haemal
arches.
There is no unanimity of opinion as to the nature of the
elements supporting the fin-rays of the caudal fin of Teleostei.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 805
Huxley1 in his paper on the development of the caudal fin of
the Stickleback, holds that these elements are of the nature of
interhaemal 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 down-
wards 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
vertebrae 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 vertebrae, the cartilaginous elements at their ex-
tremities become the interhsemal bones. The cartilage connected
with the inferior arch of the penultimate centrum is therefore an
" interhaemal " 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 con-
nected below with an element which corresponds in position
with the interhaemal 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 back-
wards. . . .
" Immediately behind and above this anterior hypural apo-
physis (as it may be termed) is another very much smaller vertical
cartilaginous plate, which may be called the posterior hypural
apophysis."
We have seen that Mivart expresses himself doubtful on the
subject. Gegcnbaur2 appears to regard them as haemal arches.
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 haemal arches, but in no way homologous
1 "Observations on the Development of some parts of the Skeleton of Fishes,"
Quart. Journ. Micr. Science, Vol. VII., 1859.
- Elements of Comparative Anatomy. (Translation), p. 43 r.
806 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 haemal 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 haemal arches.
This view of the hypural bones is, moreover, supported by
embryological evidence, since Aug. Miiller1 (p. 205) describes
their development in a manner which, if his statements are to be
trusted, leaves no doubt on this point.
There are a considerable number of Fishes which are not
provided with an obvious caudal fin as distinct from the remain-
ing unpaired fins, i.e. Chimaera, 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 A natomy (English Translation):
" In the Chimaerae, 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 Chimaera 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 Chimaera con-
stitutes, 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).
1 " Beobachtungen zur vergl. Anat. d. Wirbelsaule," Miiller's Archiv, 1853.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 807
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
haemal 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 (inter-
spinous 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 haemal arches of
this part support a few fin-rays, though a still smaller number
than in Cnidoglanis. The fin-rays so supported clearly consti-
tute an aborted ventral lobe of the caudal fin.
Under these circumstances we think that the following state-
ment by Mivart (Zool. Trans. Vol. X., p. 471) is somewhat mis-
leading : —
"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 snch forms
as Murcsna, the dorsal and ventral parts of the caudal fin are
similar in nature and homotypal with ordinary dorsal and anal
fins\"
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 Chimaera and of Eel-
like Teleostei arc simply special modifications of the typical
form of tail of the group of Fishes to which they respectively
1 The italics arc ours.
808 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 confi-
dence 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 sup-
ported by what are apparently segmented spinous prolongations
of the neural and haemal 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 Lepidosteiis. They are therefore to be regarded as
homologous with the dorsal fin-supports or interspinous bones
of other types. The corresponding ventral elements are there-
fore 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 inde-
pendently of the neural and haemal arches, we may fairly assume
that this is also true for what we have identified as the inter-
spinous 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 haemal arches
only. To this question we shall return, but we may remark
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 809
that, although there is a prolongation backwards of the-verte-
bral axis beyond the last interspinous elements, composed it
would seem of the coalesced neural and haemal arches but
without the notochord, yet by far the majority of the fin-rays
which constitute the apparent caudal fin are supported by inter-
spinous 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 haemal 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 haemal 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 haemal arches, this tail-fin cannot claim to have the
character of t/iat 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 Crossopterygidae of Huxley, and since in
these forms (as evinced by the structure of the tail-fin of Polyp-
terus, and the transitional type between a heterocercal and
diphycercal form of fin observable in fossil Crossopterygidae) the
ventral fin-rays of the caudal fin were clearly supported by
haemal 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 Crossop-
terygidae 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.
B. 52
8 10 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
(4) We believe that in Ceratodus we have been able to trace
a small number of the ventral fin-rays supported by haemal
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 haemal arches
instead of independently developed interspinous bones.
(2) The presence or absence of fin-rays in the tail-fin
supported by haemal 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
Muller (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 ioo'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
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 8ll
the dorsal aspect of the body-cavity. It is covered ^>n- its
ventral aspect by the oviduct and by its own duct, but is sepa-
rated 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 poste-
riorly 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 with-
out 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
52 — 2
8l2 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 pro-
vided 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 de-
scription differs in no material point from our own, suddenly
narrow in front, and, perforating the peritoneal lining, are con-
tinued 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 Miiller, 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 Muller 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 developed1. 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,
1 Treatise on Comparative Embryology, Vol. i., p. 43 [the original edition].
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 813
and the dehiscence of the ova into this cavity is equivalent to
their discharge into the body-cavity in other forms.
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 cffercntia, which traverse tlte mesorchium, and are con-
tinuous with tlie nriniferous tubuli ; so tJiat tJie semen passes
througJi tlic uriniferous tubuli into the kidney duct and so to the
exterior. We have moreover been unable to find in tJu 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 Lepidostcns 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. 58 A. t.} occupied
a similar position to the ovaries, and were about 21 centims.
long. They were, as is frequently the case with piscine testes,
8 14 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 spermatozoa1. These tubes to the number of 40 — 50 con-
stitute, we believe, the vasa efferentia. Along the line of suspen-
sion 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 Elas-
mobranchii (vide F. M. Balfour, Monograph on the Development of
Elasmobranch Fislies, plate 20, figs. 4 and 8).
We have figured this network on the posterior lobe of the
testis (fig. 58 B), and have represented a- section through it
(fig. 59 A, 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. 58 A, I.e., also shewn in section in
Plate 39, fig. 59 B, I.e.). From this canal tubules pass off which
are continuous with the tubuli uriniferi, as may be seen from
fig. 59 B, 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 vas-
cular trunks, viz., veins, which through their numerous anasto-
1 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.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 815
moses 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 dis-
sections 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
8l6 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 openings1.
Instead of leading into the body-cavity, they open into an
isolated chamber on each side (Plate 38, fig. $i,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 larvae of from 1 1 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 (/)2, opening into
a vesicle (v) ; from near the neck of the peritoneal tube there
1 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.
2 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.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 817
comes off a convoluted tube (pr.n.}, forming the main mass of
the pronephros, and ending in the segmental duct (sd.\
FIG.
Diagrammatic views of the pronephros of Lepidostetis.
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; s</., segmental or archinephric duct ; /, peri-
toneal funnel ; v., vesicle of pronephros ; &v., blood vessel of glomerulus ;
£•/., 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.
8l8 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 pro-
nephric chamber, forming the glomerulus already spoken of
(vide woodcut, fig. 4, £"/.), 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. $2.,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 mesonepkros 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, //.), 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 forma-
tion of segmental tubes to fill up the space between the pronephros
and mesonephros.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
The two segmental ducts have united behind into an unpaired
structure in an embryo of 1 1 millims. This structure is no doubt
the future unpaired urinogenital chamber (Plate 39, figs. 58 A,
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 1 1 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 dis-
appeared.
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 excre-
tory 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
82O STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 Elasmo-
branchii.
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, /./), which clearly there-
fore 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, how-
ever, 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
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 821
of the abdominal wall covering that part of the ventral mirface
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 laminae 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 Elasmobranchs 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 im-
pression 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 seg-
mental 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
822 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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
o
that if any rudiment of the pronephros still persists, it is quite
functionless, in that it is not provided with a duct.
Ill . — Theoretical considerations.
There are three points in our observations on the urino-
genital 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 prone-
phros 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 peri-
toneal 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 charac-
ters, 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: (i) 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
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 823
cavity has been studied by Rosenberg1 and Gotte2. According
to the account of the latter, which we have not ourselves con-
firmed but which has usually been accepted, the front end of the
scgmental 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 con-
necting the diverticulum containing the glomerulus with the
remainder of the body-cavity is short in Teleostei, and in Lepi-
dosteus forms a longish ciliated canal. In Teleostei the opening
into the body-cavity becomes soon closed. If the above com-
parison is justified, and if the development of these parts in
Lepidosteus takes place as it is described as doing in Tele-
ostei, 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.
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 re-
sembles 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's3 comparison between the two, but it does
not appear to us to justify the morphological conclusions at
1 Rosenberg, Untersuch, ueb. d. Entwick. d. Teleoslierniere, Dorpat, 1867.
2 Gotte, Ent-wick. d. Unke, p. 826.
3 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.
824 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
which he has arrived, or to necessitate any modification in the
views on this subject expressed by one of us1.
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 ante-
rior 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 peri-
toneal fold with the genital ridge, and that the duct so formed
opened into the segmental duct.
The other possible supposition is that a true Miillerian duct
—i.e., a product of the splitting of the segmental duct — is sub-
sequently 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. 1 1) there are stated to
be genital ducts in both sexes which are provided at their ante-
rior extremities with a funnel-shaped mouth open to the abdo-
minal 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 (ho'rns of the
1 F. M. Balfour, Comparative Embryology, Vol. n., pp. 600—603 [the original
edition].
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 825
urinary bladder, Hyrtl). These relations seem to prove beyond
a doubt that the oviduct of Lepidostens 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 Lcpidosteus. In Amia the ureters are so small
that they may be described rather as joining the coalesced
genital ducts than vice versa, 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 meso-
nephric 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 meso-
nephros.
It has been usual to assume that the genital ducts of Ganoids
are true Miillerian 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 sug-
gested as to the development of the posterior parts of the oviduct
in Lepidostens.
There appear to us, however, to be sufficiently serious objec-
tions 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 Mullerian 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 develop-
ment. Secondly, the condition of our oldest larva shews that
the Mullerian 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 Mullerian 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 seg-
mental duct.
B- 53
826 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 paper1 the suggestion was put forward that
the true Ganoid genital ducts were perhaps not Mullerian ducts,
but enlarged segmental tubes with persisting abdominal funnels
belonging to the mesonephros.
If the possibility of the oviduct of Lepidostcus not being
a Mullerian 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 Mullerian 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 Mullerian 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 Mullerian 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 dog-
matically, either in favour of or against the view that the genital
ducts of Ganoids are Mullerian ducts. Their ontogeny would
be conclusive on this matter, and we trust that some of the
anatomists who have the opportunity of studying the develop-
ment 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 Mullerian ducts ;
1 F. M. Balfour, "On the Origin and History of the Urinogenital Organs of
Vertebrates," Journ. of Anat. and P/iys., Vol. X., 1876 [This edition, No. VII].
STRUCTURK AND DEVELOPMENT OF LEPIDOSTEUS. 827
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 Lepidostcus appears to us to tell strongly in favour of the
view, already regarded as probable by one of us1, 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 independ-
ent 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. Aviia is closer to the Teleostei in the arrange-
ment 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 charac-
teristic 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.
The male genital ducts. — The discovery of the vasa efferentia
in Lepidosteus, carrying off the semen from the testis, and trans-
porting it to the mesonephros, and thence through the mesone-
phric 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 Elasmobranchs, &c., which are not descendants of
1 F. M. Balfour, Comparative Embryology, Vol. II., p. 605 [the original edition].
53—2
828 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 Hceven has also
given a figure of them in his memoir on the air-bladder of this
form (No. 8), and Johannes Miiller first detected the spiral valve
and gave a short account of it in his memoir (No. 13). Stan-
nius, again, makes several references to the viscera of Lepi-
dosteus in his anatomy of the Vertebrata, and throws some doubt
on Miiller'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 cesophagus, and may be called the stomach (st\ It is about
44-6 centims. long, and gradually narrows from the middle to-
wards the hinder or pyloric extremity. It runs straight back-
wards 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 ;
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 829
in the posterior half the walls are thick, and the mucous~mem-
brane 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 duo-
denum is provided with a very distinct pyloric valve (/J.).
This valve projects into a kind of chamber, freely communi-
cating with the duodenum, and containing four large pits (c'},
into each of which a group of pyloric caeca opens. These caeca
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, /.), is almost certainly a
rudimentary pancreas, like that of many Teleostei ; but its
preservation was too bad for histological examination. We be-
lieve that the pancreas of Lepidosteus has hitherto been over-
looked.
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 rudimentaiy 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 in-
testine, 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 in-
testine behind it the rectum (re.}.
830 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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.fr.) 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. pos-
teriorly— 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 con-
fined 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 con-
siderable 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.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 831
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 de-
velopment we have noticed that numerous yolk nuclei, like
those met with in Teleostei and Elasmobranchii1, are still to be
found in the yolk.
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 (//.;«.), from
an embryo of about 10 millims., shortly before hatching. It
1 For a history of similar nuclei, vide Co»if>. Eml»yol., Vol. II., chapters III.
and iv.
832 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 cartila-
ginous 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 cesophagus 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 cesophagus. The lumen
of this part appears to be all but obliterated in the stages im-
mediately before hatching, giving rise for a short period to a
solid cesophagus like that of Elasmobranchii and Teleostei1.
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 1 1 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 be-
1 Vide Comf, Embryol., Vol. 11., pp. 50—63 [the original edition].
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 833
hind 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. 6i,/.). It then has the form of a funnel-
shaped diverticulum of the dorsal wall of the duodenum, imme-
diately 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 Lepi-
dosteus to that of the same gland in Elasmobranchii is very
striking1.
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,/.). During larval life it constitutes a
considerable gland, the anterior end of which partly envelopes
the bile duct (Plate 40, fig. 63,^.).
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 larvae of most Teleostei. These
conclusions render intelligible, moreover, the great development
of the pancreas in the Elasmobranchii.
1 Vide F. M. Balfour, "Monograph on Development of Elasmobranch Fishes,"
p. 226 [This edition, No. X., p. 454].
834 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
We have first noticed the pyloric caeca arising as outgrowths
of the duodenum in larvae 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 Elasmobranchs 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 Lepi-
dostens 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 Elasmobranchs, 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 accept-
ing Miiller's discovery of the spiral valve in Lepidosteus is not
justified.
J. Muller (Ban u. Entwick. d. Myxinoideii) 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 caeca, &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 Muller 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 cither derived from an elongation of the very short
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 835
portion of the intestine between the vitelline duct and the" primi-
tive 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 us1, 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 Lepidostens is, so far as we know, quite
exceptional. This mesentery is shewn in section in the embryo
in Plate 38, fig. 53 (?>.;///.). The small vessel in it appears to be
the remnant of the subintestinal vein.
THE GILL ON THE HYOID ARCH.
It is well known that Lepidostens 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 Muller (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 Muller pseudobranch). Miiller'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 embryo-
logy 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 Miiller's view ; but what astonished us
most in connection with the gill in question is that we have been
1 Comparative Embryology, Vol. II. p. 514 [the original edition].
836 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 can-
not 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 develop-
ment 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 features1 as indicative of Teleostean affinities : —
(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 :
(i) The continuity of the oviducts with the genital glands.
1 The features enumerated above are not in all cases confined to Lepidosteus and
Teleostei, but are always eminently characteristic of the latter.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 837
(2) The small size of the pancreas, and the presence of
numerous so-called pancreatic caeca.
(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 mem-
brane between the vitreous humour and the retina.
(9) The opisthoccelous form of the vertebrae.
(10) The articulation of the ventral parts of the haemal 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 Muller's view is correct, according to which Lepidosteus
is a true Ganoid.
The existence of the Ganoids as a distinct group has, how-
ever, recently been challenged by so distinguished an Ichthyolo-
gist as Giinther, and it may therefore be well to consider how
far the group as defined by Mliller is a natural one for living
838 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
forms1, and how far recent researches enable us to improve upon
Muller's definitions. In his classical memoir (No. 13) the charac-
ters 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 ver-
tebral 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 oper-
culum, 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 swim-
ming-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."
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 Miiller 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.
1 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.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 839
(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 (i)
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 indi-
cation 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 charac-
ters1, and the gulf which really separates them is very wide.
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 limbs2,
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
haemal arches and supporting the fin-rays of the unpaired dorsal
and ventral fins, and their well-developed cerebral hemispheres,
1 As instances of this we may cite (i) 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.
2 Vide F. M. Balfour, " On the Development of the Skeleton of the Paired Fins
of Elasmobranchs," Proc. Zool. Soc., 1881 [This edition, No. XX.].
840 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
very unlike those of Ganoids and approaching the Amphibian
type, they form a very well-defined group, and one very dis-
tinctly separated from the Ganoids.
No doubt the Chondrostean Ganoids are nearly as far re-
moved from the Teleostei as from the Dipnoi, but the links
uniting these Ganoids with the Teleostei have been so fully pre-
served 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 con-
stituting 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 I., Proc.
Amer. A cad. Arts and Sciences, Vol. xiv. 1879.
2. Agassiz, L. Recherches s. I. Poissons Fossiles. Neuchatel. 1833
—45.
3. Boas, J. E. " Ueber Herz u. Arterienbogen bei Ceradotus u. Protop-
terus," Morphol. Jahrbuch, Vol. VI. 1880.
4. Davidoff, M. von. " Beitrage z. vergleich. Anat. d. hinteren Glied-
massen d. Fische," Morphol. Jahrbuch, Vol. vi. 1880.
5. Gegenbaur, C. Uutersuch. z. vergleich. Anat. d. Wirbelthiere,
Heft II., Schnltergiirtel d. Wirbelthiere. Brustflosse der Fische. Leipzig,
1865.
6. Gegenbaur, C. " Zur Entwick. d. Wirbelsaule d. Lepidosteus, &c."
Jenaische Zeitschrift, Vol. ill. 1867.
7. Hertwig, O. "Ueber d. Hautskelet d. Fische (Lepidosteus u.
Polypterus)? Morphol. Jahrbuch, Vol. v. 1879.
8. Hceven, Van der. " Ueber d. zellige Schwimmblase d. Lepidostens?
M tiller's Archiv, 1841.
STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS. 84!
9. Hyrtl, J. " Ueber d. Schwimmblase von Lepidosteus osseus" *>'//-.
d. Wiener Akad. Vol. vill. 1852.
10. Hyrtl, J. "Ueber d. Pori abdominales, d. Kiemen-Arterien, u. d.
Glandula thyroidea d. Ganoiden," Sitz. d. Wiener Akad. Vol. vm. 1852.
u. H y r 1 1, J . Ueber d. Zussammenhang d. Geschlechts u. Harnwerkzeuge
bei d. Ganoiden, Wien, 1855.
12. Kolliker, A. Ueber d. Ende d. Wirhelsaule b. Ganoiden, Leipzig,
1860.
13. Miille r, J. "Ueber d. Ban 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 Ganoi Is, Amia,
Lepidosteus, Acipenser, and Polyodon? Proc. Amer. Assoc.for the Advance-
ment of Science, 1875.
LIST OK REFERENCE LETTERS.
a. Anus, a b. Air-bladder, a b'. Aperture of air-bladder into throat, ac. An-
terior commissure, af. Anal fin. al. Alimentary canal, ao. Aorta, ar. Artery.
au. Auditory pit. b. Brain, be. Body-cavity, bd. Bile duct. bit. Aperture of
bile duct into duodenum, bl. Coalesced portion of segmental ducts, forming urino-
genital bladder. bra. Branchial arches, br c. Branchial clefts, c. Pyloric casca.
c'. Apertures of caeca into duodenum. cb. Cerebellum. c>fv. Cardinal vein.
ce. Cerebrum : in figs. 47 A and B, anterior lobe of cerebrum, ce'. Posterior lobe of
cerebrum, cf. Caudal fin. en. Centrum, ch. Choroidal fissure, crv. Circular
vein of vascular membrane of eye. csh. Cuticular sheath of notochord. cv. Caudal
vein. d. Duodenum, d c. Dorsal cartilage of neural arch. df. Dermal fin-rays.
dl. Dorsal lobe of caudal fin. dlf. Dorsal fin. e. Eye. ed. Epidermis, ep. Epi-
blast. 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. Haemal arch. hb. Hind-
brain, he. Head-cavity, hpd. Hepatic duct, h m. 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. Sub-intestinal vein. ivr. Intervertebral
ring of cartilage, k. Kidney. /. Lens. le. Longitudinal canal, formed by union of
the vasa efierentia. I in. Lobi inferiores. //. Ligamentiun longitudinale supcrius.
Ir. Liver. It. Lateral line. ly. Lymphatic body in front of kidney, m. Mouth.
mb. Mid-brain. me. Medullary cord. met. Membrana elastica externa. mes.
Mesorchium. /««. Mandible, md. and mo. Medulla oblongata. nis. Mesoblast.
n a. Neural arch. na'. Dorsal element of neural arch. nc. Notochord. nve. Net-
work formed by vasa efferentia on inner face of testis. od. Oviduct, oif. Aperture
of oviduct into bladder, ol. Nasal pit or aperture, olf. Olfactory lobe. op. Optic
vesicle, opch. Optic chiasma. of> I. Optic lobes, oplh. Optic thalami. or ef>.
B. 54
842 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
Oral epithelium, ov. Ovary. />. Pancreas, pc. Pericardium, pcf. Pectoral fin.
p ck. Pigmented layer of choroid. pf. Peritoneal funnel of segmental tube of meso-
nephros. pfp~ Peritoneal funnel leading into pronephric chamber, p g. Pectoral
girdle. /// Pelvic fin. pn. Pineal gland, po. Primitive germinal cells, pr.
Mesoblastic somite, prc. Pronephric chamber, prn. Pronephros. prri. Opening
of pronephros into pronephric chamber. //. Pituitary body. py. Pyloric valve.
/ z. Parietal zone of blastoderm, r. Rostrum. rb. Rib. re. Rectum, s. Spleen.
s c. Seminal vessels passing from the longitudinal canal into the kidney, sd. Suc-
torial disc. sg. Segmental or archinephric duct. j§ t. Segmental tubules, sh.
Granular outer portion of the sheath of the notochord in the vertebral regions, s mx.
Superior maxillary process. s nc. Sub-notochordal rod. so. Somatic mesoblast.
sp. Splanchnic mesoblast. sp n. Spinal nerve, sp v. Spiral valve, st. Stomach.
s t. Seminal tubes of the testis. sup. Suctorial papillae, t. Testis. th. Thalamen-
cephalon. thl. Lobes of the roof of the thalamencephalon. tr. Trabeculse. tig.
Urinogenital aperture, v. Ventricle, v e. Vasa efferentia. v h. Vitreous humour.
v 1. Ventral lobe of the caudal fin. v mt. Ventral mesentery, v n. Vein. vs. Blood-
vessel, v sh. Vascular sheath between the hyaloid membrane and the vitreous
humour, v th. Vesicle of the thalamencephalon. x. Groove in epiblast, probably
formed in process of hardening, y. Yolk. z. Commissure in front of pineal gland.
z r. 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
EXPLANATION OF PLATES 34—42.
PLATE 34.
Figs. 1—4. Different stages in the segmentation of the ovum.
Fig. i. 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.
Fig5- 5 — ro- 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. ir. Head of embryo about the same age as fig. 10, ventral aspect.
Fig. 12. Side view of a larva about u millims. in length, shortly after hatching.
Fig. 13. Head of a larva about the same age as fig. 12, ventral aspect.
EXPLANATION OF PLATES 35, 36. 843
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 ir 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 harden-
ing.
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 impregna-
tion.
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. Tranverse 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 auditoiy 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 impreg-
nation, 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.
F'g- 34- Further back than fig. 33, shewing constriction of tail from the
yolk.
54—2
844 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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 con-
nected 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. 46 A to 46 G. Transverse sections through the brain of an embryo 25
millims. in length, about a month after hatching.
Fig. 46 A. Through anterior lobes of cerebrum.
Fig. 46 B. Through posterior lobes of cerebrum.
Fig. 46 C. Through thalamencephalon.
Fig. 46 D. Through optic thalami and optic chiasma.
Fig. 46 E. Through optic lobes and infundibulum.
Fig. 46 F. Through optic lobes and cerebellum.
Fig. 46 G. Through optic lobes and cerebellum, slightly in front of fig. 46 F.
PLATE 38.
Figs. 47 A, B, C. Figures of adult brain.
Fig. 47 A. From the side.
Fig. 47 B. From above.
Fig. 47 C. 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.
EXPLANATION OF PLATES 38, 39. 845
Fig. 49. Diagram shewing the arrangement of the vessels in the vascular mem-
brane 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 rr centims.
Fig. 54. Section of the lymphatic organ which lies in front of the mesone-
phros.
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 ger-
minal cells projecting freely into the body-cavity.
Fig. 58 A. 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. 58 B. 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. 59 A and B. Two sections shewing the structure and relations of the
efferent ducts of the testis in the same example.
Fig. 59 A. Section through the inner aspect of a portion of the testis and
mesorchium, to shew the network of the vasa efferentia (n ve)
becoming continuous with the seminal tubes (st). The granu-
lar matter nearly filling the vasa efferentia and the seminal
tubes represent the spermatozoa.
Fig. 59 B. Section through part of the kidney and its duct and the longitu-
dinal canal (Ic) at the base of the mesorchium. Canals (s c)
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.
846 STRUCTURE AND DEVELOPMENT OF LEPIDOSTEUS.
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. 6 1. Transverse section through the developing pancreas (p) of a larva n
millims. in length.
Fig. 62. Longitudinal section through portions of the stomach, liver, and duode-
num of an embryo about a month after hatching, to shew the relations of the pancreas
(/) to the surrounding parts.
•Fig- 63. External view of portions of the liver, stomach, duodenum. &c., of a
young Fish, n centims. in length, to shew the pancreas (/).
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 (a b').
Fig. 65. Transverse section through the same embryo as fig. 64 further back,
shewing the posterior part of the air-bladder (a b).
Fig. 66. Viscera of an adult female, 100 centims. in length, shewing the alimen-
tary canal with its appended glands in natural position, and the air-bladder with its
aperture into the throat (a b'). 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 caeca 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 haemal processes, the independently developed interneural and interhsemal
elements (i s), and the commencing dermal fin-rays (df).
Fig. 68. Side view of the tail of a larva, 21 millims. 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 haemal arches, shewing the intervertebral
rings of cartilage continuous with the arches, the vertebral constriction of the noto-
chord, &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 haemal
arches, the notochordal sheath, &c.
Fig. 71. Through the intervertebral region, shewing the intervertebral car-
tilage.
EXPLANATION OF PLATES 41, 42. 847
Figs. 72 and 73. Transverse sections through the trunk of a larva of 5*5 centims.
to shew the structure of the ribs and haemal 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
% 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 1 1 centims., passing through the level of the haemal arches, and shewing the inter-
vertebral 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 1 1 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 vertebrae of an adult Lepidosteus.
Fig. 8 r. 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 TE-
LEOSTEANS AND GANOIDS, WHICH IS USUALLY RE-
GARDED AS THE HEAD-KIDNEY OR PRONEPHROs1.
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* 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.
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 abdo-
minal cavity. In front each of these bands first becomes con-
siderably 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,
1 From the Quarterly Journal of Microscopical Science, Vol. XXII., 1882.
2 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.
I II. AD-KIDNEY IN ADULT TELEOSTEANS AND GANOIDS. 849
which I shall in future call lymphatic tissue. Thus tJiejwhole
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
lympJiatic tissue, and does not contain a single urinifcrous tubule
or Malpigldan 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 edi-
tion 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
Indus), the Smelt (Osmerus eperlanus], the Eel (Anguilla an-
guilld], and the Angler (LopJiius piscatorius).
The external features of the apparent kidney of the Pike
have been accurately described by Hyrtl1. 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 con-
tinuation of the kidney backwards forms two small bands, sepa-
rated 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.
The Pike I examined was a large specimen of about 58
centimetres in length, and with an apparent kidney of about 25^
centimetres. The relations of lymphatic tissue and kidney
tissue were much as in the Sturgeon. The whole of the ante-
rior 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,
1 "Das UropoctUche System der Knochenfische," .v/':. <l. /r/V//. Aka<l., isuo.
850 HEAD-KIDNEY IN ADULT TELEOSTEANS AND GANOIDS.
was entirely formed of lymphatic tissue. The posterior part of
the kidney was composed of true kidney substance, but even at
1 6 centimetres 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 follow-
ing, 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, con-
sisted 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 por-
tion, 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
Hyrtl1, 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.
1 "Das Uropoetische System der Knochenfische," Sitz. d. Wien. Akad., 1850.
HEAD-KIDNEY IN ADULT TELEOSTEANS AND GANOIDS. 851
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 speci-
mens 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 larvae of Teleosteans and
Ganoids were provided with two very distinct excretory organs,
viz. a pronephros or head-kidney, and a mesonephros or Wolf-
fian 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 Indus} 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
852 HEAD-KIDNEY IN ADULT TELEOSTEANS AND GANOIDS.
not part of the true kidney. From my own studies on young
Fishes I do not believe that the oldest larvae investigated by
Rosenberg were sufficiently advanced to settle the point in
question ; and, moreover, as Rosenberg had no reason for doubt-
ing that the so-called head-kidney of the adult was part of the
excretory organ, he does not appear to have studied the histo-
logical structure of the organ which he identified with the em-
bryonic pronephros in his oldest larva.
The facts to which I have called attention in this paper
demonstrate that in the Sturgeon the larval pronephros un-
doubtedly 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 ex-
tensive 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 larva or em-
HEAD-KIDNEY IN ADULT TELEOSTEANS AND GANOIDS. 853
bryos of almost all the IchtJiyopsida, except the 'Elasmobmnehii, is
always a ptirely 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 phylo-
genetically 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 tra-
becular 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 repre-
sented in fishes.
XXIV.— A RENEWED STUDY OF THE GERMINAL LAYERS OF
THE CHICK. BY F. M. BALFOUR AND F. DEiGHTON1.
(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 in-
duced 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 pri-
marily 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 in-
vestigate 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 memoir2 in April last, and
1 From the Quarterly Journal of Microscopical Science, Vol. xxn. N. S. 1882.
- " Ueb. d. entodermale Entstehungs\veise d. Chorda dorsalis," Biol. Centralblait,
Vol. I. Nos. i and 2.
RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK. 855
the other is C. Koller, who has published his memoir1 still- more
recently. Both of them cover part of the ground of our in-
vestigations, 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 worjc 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.
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 Roller's statements on this subject.
Embryologists are in the main agreed as to the structure of
the blastoderm at this stage. There is (PI. 43, Ser. A, I 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.
1 " Untersuch. lib. d. Blatterbildung im Hiihnerkeim," Arfhiv f. niikr. Anat.
Vol. xx. i88r.
856 RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK.
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 con-
stituent 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, I 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 Roller 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 com-
posed 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, i 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 (fry.). 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, i), 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 seg-
mentation spheres.
In many blastoderms, not easily distinguishable in surface
RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK. 857
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 pos-
terior 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 con-
siderably behind, where it joins the germinal wall. By Roller
and Gerlach it is described as joining the sickle-shaped struc-
ture already spoken of. We have in some instances found the
posterior end of the primitive streak extending laterally in the
form of two wings (PI. 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 Benecke1,
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.
Sections through the area pellucida (PI. 43, Sen 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
1 " Photogramme d. Ontogenie d. Vogcl." Nova Acts. K. Leop. Carol, Dciits-
chen A had. d. Naturj\>r. Bd. X. 41, 1879.
B. 55
858 RENEWED STUDY OF -GERMINAL LAYERS OF THE CHICK.
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 Kolliker, 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 views0 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 epi-
blast, 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. Some-
times these cells are entirely confined to the region of the primi-
tive 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 inter-
mingled. The facility with which the cells we have just spoken
of can be recognized varies moreover greatly in different in-
stances. In some cases they are very obvious (Sen c), while in
other cases they can only be distinguished by a careful ex-
amination of good sections.
RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK. 859
The cells of the primitive streak between the epibTast 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 Roller
and Gerlach. In the case of one of the youngest of our blasto-
derms of this stage in which we found in surface views (PI. 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 hypo-
blast 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 out-
wards 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.
Koller1 described the sickle and the growth forwards from it
of the primitive streak in surface views somewhat before Gerlach;
1 " Beitr. z. Kenntniss d. Hiihnerkeims im Beginne d. Bebriitung," Sffs. d. k.
Akad. Wiss. \\. Abth. 1879.
55—2
860 RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK.
and in his later memoir has entered with considerable detail
into the part played by the various layers in the formation of
this structure.
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 Benecke1 in the sparrow and fowl.
We have never, however, found very clear indications of it in
our sections.
In the next stage, Koller states that, in the region immedi-
ately 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 Keller'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.
1 Die erstt Entvriek. an Eier d. Reptilim. Konigsbcrg, 1878.
RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK. 86l
We have made measurements to test this point, and~find that
the diminution of the space between the front end of the primi-
tive streak and the anterior border of the area pellucida is very
marked up to the period in which the medullary plate first be-
comes 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 primi-
tive 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 primi-
tive 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.
862 RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK.
The mesoblast is attached in the median line to the epiblast.
Laterally it extends outwards to the edge of the area pellu-
cida, 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
RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK. 863
it is very much deeper. One of the latter is represented in
fig. G. It has here the appearance of a narrow slit, and sec-
tions 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 repre-
sented 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 hypo-
blast 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 (PI. 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
(PI. 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 con-
stitution of the hypoblast (PI. 44, Ser. H, I and 2).
Near the front border of the area pellucida (i) 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 t/ie axial line into hypoblast and meso-
blast, though one can fancy that in places, especially laterally,
they are partially differentiated into two layers. The axial
864 RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK.
sheet of stellate cells is continuous laterally with cubical hypo-
blast cells.
As the primitive streak is approached an axial prolongation
forwards of the rounded and closely-packed mesoblastic ele-
ments 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 PI. 45, Ser. I, i, 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, pass-
ing through the front end of the primitive streak, the axial cells
have become continuous with the axial mesoblast of the primi-
tive 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 (i) 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 lavers.
RENEWED STUDY OF GERMINAL LAYERS .OF THE CHICK. 865
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 pre-
sence, 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
(PI. 44, Ser. F, I 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 consti-
tutes the head fold.
PI. 45, Ser. K, represents a series of sections through a blas-
toderm 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, i). Below the
median line of the epiblast is a small cord of cells, not divided
into two layers, but continuous laterally, both with the hypo-
blast 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 ap-
pearance.
866 RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK.
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 con-
tinuous 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
RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK. 867
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 differentia-
tion 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 de-
scribed, 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 Roller ; except that Koller is inclined to mini-
mise 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 Kolliker,
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
868 RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK.
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 con-
tinuous 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 ac-
count 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 ver-
tebrates 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 re-
garding 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 Am-
phioxus 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
EXPLANATION OF PLATES. 869
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 verte-
brate 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. pv s.
Primitive streak, yk. Yolk of germinal wall.
PLATE 43.
SERIES A, i and 2. Sections through the blastoderm before the appearance of
primitive streak.
i. 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 embry-
onic shield. Between the epiblast and hypoblast are a number of undifferentiated
cells. The figure represents considerably more than half the section.
SERIES B, i, 2 and 3. Sections through a blastoderm with a very young primi-
tive streak.
i. Section through the anterior part of the area pellucida in front of the
primitive streak, i. Section through about the middle of the primitive streak.
3. Section through the posterior part of the primitive streak.
SERIES C, i and 2. Sections through a blastoderm with a young primitive streak,
i. Section through the front end of the primitive streak. 2. Section through
the primitive streak, somewhat behind r. Both figures shew very clearly the differ-
ence 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.
i. Section through the anterior part of the area pellucida. 2. Section a little
way behind i 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.
87© RENEWED STUDY OF GERMINAL LAYERS OF THE CHICK.
SERIES F, i and 2. Sections, through a blastoderm with primitive groove.
i. Section shewing a deep pit in front of primitive streak, probably an early
indication of the neurenteric canal. 2. Section immediately following i.
FIG. G. Section through blastoderm with well-developed primitive streak, shew-
ing an exceptionally deep slit-like primitive groove.
SERIES H, i and i. Sections through a blastoderm with a fully-developed primi-
tive streak.
i. Section through the anterior part of area pellucida, shewing the cubical
granular hypoblast cells in this region. 2. Section slightly behind i, 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, i, 2, 3, 4 and 5. Sections through blastoderm somewhat older than
Series H.
i. 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
i and 3, and the left in 2 and 4.
i. Section through notochord immediately behind the head-fold. 2. Section
shewing medullary groove a little behind i. 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
CAPENSIS1.
(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 pub-
lished 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 alteration2. Explanations which
appeared to be necessary, and additions to the text in cases in
which he had prepared figures without writing descriptions, to-
gether with full descriptions of all the plates, have been added
by us, and are distinguished by enclosure in square brackets*.
We have to thank Miss Balfour, Professor Balfour's sister,
for the important service which she has rendered by preparing
1 From the Quarterly Journal of Microscopical Science, April, 1883.
2 Excepting in an unimportant matter of change of nomenclature used with regard
to the buccal cavity.
3 The account of the external characters, generative organs, and development, has
been written by the editors.
872 ANATOMY AND DEVELOPMENT
a large part of the beautiful drawings with which the mono-
graph is illustrated. Many of these had been executed by her
under Professor Balfour's personal supervision ; and the know-
ledge 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 memoir1.
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 novcz zealaudicz, 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 em-
bryology of Peripatus has already been communicated to the
Royal Society2. 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.
1 The drawings on PI. 47, figs. 9 and 10 on PI. 48, and the drawings of the
embryos (except fig. 37), have been made by Miss Balfour since Professor Balfour's
death.
4 Proc. Royal Soc. 1883.
OF PERIPATUS CAPENSIS. 873
PART I.
DESCRIPTION OF THE SPECIES.
Peripatus capensis (fig. i).
[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 antennae projecting from the an-
terior end of the head, and a pair of simple eyes, placed on the
dorsal surface at the roots of the antennae.
The appendages of the body behind the antennae are dis-
posed 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 papillae 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 pro-
vided with a pair of chitinous claws at its extremity.
4. The anal papillae 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. I) ; 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
B. 56
8/4 ANATOMY AND DEVELOPMENT
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 papillae. This is especially evident round
the mouth, where the sparse green pigment is entirely confined
to the papillae.
In some specimens a number of white papillae, or perhaps
light brown, are scattered over the dorsal surface ; and some-
times there is a scattering of green papillae all over the ventral
surface. These two peculiarities are more especially noticeable
in small specimens.
Ridges and Papilla of the Skin. — The skin is thrown into
a number of transverse ridges, along which the primary wart-
like papillae are placed.
The papillae, which are found everywhere, are specially de-
veloped on the dorsal surface, less so on the ventral. The
papillae round the lips differ from the remaining papillae 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.
OF PERIPATUS CAPENSIS. 8/5
The antennae 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
papillae, and are, therefore, beset by a number of spines like
those of the primary papillae (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 antennae 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 antennae 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
antennae on the dorso-lateral parts of the head. Each is placed
on the side of a protuberance which is continued as the an-
tenna, and presents the appearance of a small circular crystal-
line ball inserted on the skin in this region.
The rings of papillae on that part of the head from which
the antennae arise lose their transverse arrangement. They
are arranged concentrically to the antennal rings, and have a
straight course forwards between the antennae.
The oral papillae are placed at the side of the head. They
are attached ventro-laterally on each side of the lips. The
duct of the slirne 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 papillae 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 papillae bear claws, and pre-
sent 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
papillae last mentioned, and the generative opening being placed
between them.
56-2
876 ANATOMY AND DEVELOPMENT
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 ap-
pendage (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 papillae, 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 papillae, 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 papillae. These spinous pads are con-
timaed dorsally, each into a ring of papillae.
"The papillae of the ventral row next the proximal of these
spinous pads are intermediate in character between the primary
papillae and the spinous pads. Each of these papillae 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 papillae on the ventral surface of the legs. On
the outer and inner sides of these pads the spines are absent,
and secondary papillae only are present.
In the centre of the basal part of the ventral surface of the
foot there are present a group of larger papillae, 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
OF FERIPATUS CAPENSIS. 877
at the internal end of this structure. The exact arrangement of
the papillae 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 seco'ndary papillae, but spines and primary pa-
pilla? 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 in-
conspicuous 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 papillae,
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 papillae
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 di-
vision.
The last (17) leg of the male (PI. 47, fig. 4) is character-
ized by possessing a \vell-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 papillae counting from the
innermost pad, and slightly posterior to the axial line of the leg.
The anal papillae, or as they should be called, generative
papillae, 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 resem-
ble closely the anterior appendages.]
8/8 ANATOMY AND DEVELOPMENT
PART II.
ALIMENTARY CANAL.
The alimentary canal of Peripatns 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 di-
vided into five regions, viz. (i) 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 re-
mainder 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 PI. 49, figs, n and 12,
representing the oral cavity in transverse section, and by PL 49,
figs. 17 and 1 8, 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
OF PERIPATUS CAPENSIS. 879
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 (PI. 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 com-
pared to those of the odontophor of a mollusc.
In addition to the above set of muscles, there are also trans-
verse muscles, forming laminae 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 papillae, moved by an elaborate
and powerful system of muscles, and armed at their free ex-
tremities by a pair of cutting blades or claws. The latter struc-
tures 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 setae of
Chaetopoda. The claws are sickle-shaped and, as shewn in PI.
47, fig. 5, have their convex edge directed nearly straight for-
wards, and their concave or cutting edge pointed backwards.
Their form differs somewhat in the different species, and, as will
880 ANATOMY AND DEVELOPMENT
be shewn in the systematic part of this memoir1, forms a good
specific character. In Peripatns capensis (PI. 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 (PI.
49, fig. 1 1). 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 epithe-
lium, 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.
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 epithe-
lial 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 PI. 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 PI. 49, figs. 13 — 16 /«?). This apparent
tube is the section of the deep pit already spoken of. It may
1 Some material for this memoir was left by Prof. Balfour, which will be published
separately-
OF PEKIPATUS CAPENSIS. 88 1
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 demarca-
tion 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. 1 6) is formed of very elongated cells supported by
a delicate membrana propria. The section of this part is some-
what triangular, and the cells are so long as to leave a compara-
tively 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
882 ANATOMY AND DEVELOPMENT
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 (PI. 49, figs. 1 1 — 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 (PI. 51, fig. 23) radial fibres, arranged in somewhat wedge-
shaped laminae, 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 Chaeto-
poda, a resemblance which is greatly increased by the character-
istic course of the sympathetic nerves.
The form of the lumen, as already pointed out by Grube,
resembles that of the Nematoda.
T/ie (Esophagus. — Behind the pharynx there follows a narrow
oesophagus (fig. 7, o e] shewn in section in fig. 16. It has some-
OF PERIPATUS CAPENSIS. 883
what 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 cesophageal 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.
Tlie Stomach. — The next section of the alimentary tract is
the stomach or rnesenteron (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 th«
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.
884 ANATOMY AND DEVELOPMENT
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 un-
able 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 base-
ment membrane. The epithelial part of the wall of the stomach
is by far the thickest (fig. 20), and is mainly composed of enor-
mously elongated, fibre-like cells, which in the middle part of
the stomach, where they are longest, are nearly half a millimetre
in length, and only about -006 mm. in breadth. Their nuclei, as
seen in fig. 20, are very elongated, and are placed about a quar-
ter 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 pro-
cesses 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 ac-
count 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 joinino-
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.
OF PERIPATUS CAPENSIS. 885
Within the peritoneal investment comes a well-developed mus-
cular 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-ceso-
phageal ganglia united in the middle line, and of a pair of
widely divaricated ventral cords, continuous in front with the
supra-cesophageal 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 examina-
tion they are found to be enlarged at each pair of legs (PI. 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 addi-
tion a ganglionic enlargement at the commencement of the
cesophageal commissures, where the nerves to the oral papillae
are given off (PI. 51, fig. 22 or. g.), and the region of junction
between the cesophageal commissures with the supra-cesophageal
ganglia, where another pair of nerves are given off to the jaws
(PI. 51, fig. 227 ri), 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 compart-
ments of the body-cavity, immediately within the longitudinal
layer of muscles.
886 ANATOMY AND DEVELOPMENT
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 (PI. 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 nova zealandia, and probably also in P. capen-
sis, 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 (PI. 52, fig.
26 g cd). 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 (PI. 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 imme-
diately below the wall of the pharynx (PI. 49, figs. 14, 15). The
ventral cords themselves at first approach very close to each
other in this region, separating again, however, to envelope be-
tween them the pharynx (PI. 51, fig. 22).
There are eleven commissures in front of the first pair of legs
(PI. 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.
OF PERIPATUS CAPENSIS. 887
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 cesophageal
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 papillae, 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
papillae 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 cesophageal commissures, close to their junction
with the supra-cesophageal ganglia, a nerve arises on each side
which passes to the jaws, and a little in front of this, apparently
from the supra-cesophageal ganglion itself, a second nerve to the
jaws also takes its origin (PI. 51, fig. 22 j ri). 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 papillae
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.
TJie Supra-cesopJiagcal Ganglia. — The supra-cesophageal gan-
glia (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
888 ANATOMY AND DEVELOPMENT
cesophageal commissures. On the ventral surface of each, rather
behind the level of the eye, is placed a very peculiar pro-
tuberance (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-cesophageal 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 an-
tennary 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. 19 A.
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. 19 D 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. 19 D) 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-cesophageal 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. 1 1 — 14 dn}.
Sympathetic System. — In addition to the nerves just de-
scribed there are two very important nerves which arise near
the median ventral line, close to the hind end of the supra-
cesophageal 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.
OF PERIPATUS CAPEXSIS. 889
Here they at once approach and shortly meet in the~rrredian
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 Chaetopods,
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 brain1.
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 com-
posed 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 struc-
ture to the fibrous parts of the main cord, but are provided with
a somewhat larger number of cells.
1 Vide Spengel, " Oligognatluis Ronelliac." Naph-s Mittht-ihiti^-tt, IJd. in. pi. iv.
fur. 5:.
B. 57
890 ANATOMY AND DEVELOPMENT
Sheath of the Ventral Cords. — The ventral cords are en-
veloped 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-cesophageal Ganglia. — In the present state of our know-
ledge 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 (PI. 50,
fig. 19 A— G).
The ganglion cells are in the first place confined, for the
most part, to the surface. Along the under side of each gan-
glion 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 cesophageal commissures. These cells have,
moreover, an arrangement very similar to that in the ventral
cords, so that a section through the supra-cesophageal 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. 19 D). Immediately
dorsal to this point the fibrous matter of the brain is exposed
freely on the surface (fig. 19 A, 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. 19 A). From
the point where the two ganglia meet in front the nerve-cells
extend backwards as a median strip on the dorsal surface (fig.
19 D and E). This strip, becoming gradually smaller behind,
reaches nearly, though not quite, the posterior limit of the junc-
tion of the ganglia. Behind it there is, however, a region where
OF PERIPATUS CAPENSIS. 89!
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. 19 E, and also in the vertical longi-
tudinal section (PI. 51, fig. 21), and in horizontal section in
PI. 51, fig. 22.
On the ventral aspect of each lobe of the brain there is pre-
sent a very peculiar, bluntly conical protuberance of ganglion
cells (PI. 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-cesophageal ganglion, and regards it
as an organ of hearing.
In Pcripatus 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 (PI. 50, fig. 19 C and D, d\
mainly of ganglion cells. In its interior is a cayity 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. 19 E), 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, con-
57—2
892 ANATOMY AND DEVELOPMENT
necting the two halves of the ganglion. Laterally and some-
what ventrally it is prolonged into a horn (fig. 19 D, 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 PI. 51, fig. 22. This part of the horn is charac-
terized by the presence of large vertically-directed bundles of
nerve-fibres, shewn in transverse section in fig. 190. Posteriorly
the diameter of this horn is larger than in front (fig. 19, E, 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 de-
scribed (fig. 19 D, 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. 19 F 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.
OF PERIPATUS CAPENSIS. 893
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 O'CO2 mm. in thickness. Its
surface is not, however, smooth, but is everywhere, with the
exception of the perioral region, raised into minute secondary
papillae, the base of which varies somewhat in diameter, but is
usually not far from O'O2 mm. On the ventral surface of the
body these papillae 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
papillas 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 re-
markable relation to the secondary papillae of the cuticle just
described. Each epidermis cell is in fact placed within one of
these secondary papillae, 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 cwticle has, moreover,
in the process of cutting the section, been somewhat raised and
carried away from the subjacent cells. The cells of the epi-
dermis are provided with large oval nuclei, which contain a well-
894 ANATOMY AND DEVELOPMENT
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 charac-
teristic colour to the skin is deposited in the protoplasm of the
outer ends of the cells in the form of small granules. An at-
tempt is made to shew this in fig. 32.
At the apex of most, if not all, the primary wart-like papillae
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 antennae, 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
antennae, lips, and oral papillae. On the ventral surface of the
peripheral rings of Jhe 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
antennae they are thickly set side by side on the rings of skin
OF PERIPATUS CAPENSIS. 895
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 inves-
tigation induced me to regard them as a form of tactile organ.
The arguments for this view are both of a positive and a nega-
tive kind.
The positive arguments are the following :
(1) The organs are supplied with large nerves, which is dis-
tinctly in favour of their being sense organs rather than glands.
(2) The peculiar striae at the base of the spines appear to me
like the imperfectly preserved remains of sense hairs.
(3) The distribution of the.se organs favours the view that
they are tactile organs. They are most numerous on the an-
tennas, where such organs would naturally be present, especially
in a case like that of Peripatus, where the nerve passing to
the antennae is simply gigantic. On the other hand, the an-
tennae would not be a natural place to look for an enormous
development of dermal glands.
The lips, oral papillae, 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 im-
portant 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 de-
pressions between the papillae 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
896 ANATOMY AND DEVELOPMENT
towards the lumen of the pit by a very delicate cuticular mem-
brane continuous with the cuticle covering the surface of the
body. The pits vary somewhat in depth; the pit figured was
about O'OQ 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 inter-
nally in a mushroom-like fashion, the narrow part being, how-
ever, often excentric in relation to the centre of the expanded
part.
Although it was clear that the tracheae started from the ex-
panded 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 tracheae 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 tracheae.
I have, in fig. 30, attempted to make clear this relation be-
tween the expanded walls of the tracheal pits and the tracheae.
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 tracheae 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 tracheae, and somewhat
similar cells, though generally with more elongated nuclei, ac-
company the bundles of tracheae 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 tracheae had originated at
the expense of the cells of pits of the epidermis, and that the
cells accompanying the bundles of tracheae 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 tracheae.
The tracheae themselves are extremely minute, unbranched
(so far as I could follow them) tubes. Each opening by a sepa-
rate 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.
OF PERIPATUS CAPENSIS. 897
[Moseley (Phil. Trans., 1874, PL 73, fig. i) states that the
tracheae branch, but only exceptionally.]
Situation of the tracJieal apertures. — Moseley states (No. 13)
that the tracheae 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 num-
ber 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
tracheae.
In front of the mouth there is a very large median ventral
tracheal pit, which gives off tracheae to the ventral part of the
nervous system, and still more in front a large number of such
pits close together. The tracheae to the central nervous system
in many instances enter the nervous system bound up in the
same sheath as the nerves.
898 ANATOMY AND DEVELOPMENT
THE MUSCULAR SYSTEM.
The general muscular system consists of— (i) 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 fhe alimentary tract.
The muscular wall of the body is formed of— (i) 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 (PI. 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. 1 6), 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 (i) 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 nerv-
ous system, salivary glands, segmental organs, &c.
(2) Inserted a little dorsal to the transverse band just de-
scribed 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.
OF PERIPATUS CAPENSIS. 899
Where the feet are given off the second transverse band be-
comes 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 (PI. 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 endo-
thelial 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 pro-
longed 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 con-
tinuation 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
ANATOMY AND DEVELOPMENT
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 seg-
mental organs of the Chaetopoda.
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 open-
ing 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 ex-
ternal opening (p s) leads into a narrow tube (s d], which
gradually dilates into a large sack (s).
OF PERIPATUS CAPENSIS. QOI
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 .$•). 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 s c i). 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 inte-
rior, so causing the inner boundary of the epithelium of this
part of the tube to have a very ragged appearance. This por-
tion 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 s c 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 s c 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
902 ANATOMY AND DEVELOPMENT
very indistinct. The fourth region is very short (fig. 28 s c 4),
and is formed of small columnar cells. It gradually narrows
till it opens suddenly into the terminal section (s o t\ 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 de-
scribed 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 ex-
ternal 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 (count-
ing 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 charac-
teristic structure, but are much smaller. Close to the point
where the vesicle joins the coiled section of the nephridium the
OF PERIPATUS CAPENSIS. 903
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 tracheae,
and when cut away from its attachment the muscles and trachese
cannot easily be detached from it. The main part of the coils
are formed by region No. i, 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 I7th pair of legs
(PI. 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
papillae, which are much more marked in small specimens than
in large ones, and in two cases (of females) were observed to
bear rudimentary claws.
i. The Male Organs. PI. 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 (/).
904 ANATOMY AND DEVELOPMENT
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 (i/th) pair of lens are enlarged and
prolonged into an elongated tube placed in the lateral com-
partment of the body-cavity (a g}.
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 vesiculse 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 (/), 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 sper-
matophore maker, as has been shewn to be the case in P. N.
Zealandiae, 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 (/),
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 arrange-
ment :
The ovary lies rather to the dorsal side in the central com-
partment of the bodj'-cavity, and is attached to one of the
OF PERIPATUS CAPENSIS. 905
longitudinal septa separating this from the lateral compart-
ment. 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 arrange-
ment, which differs from that observed by Moseley, is a normal
one. The young undergo nearly the whole of their develop-
ment 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 (PI. 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 PI. 51, fig. 20. Each consists of a
dilated vesicular portion (fgl] placed in the lateral compart-
ment of the body cavity in the foot, and of a narrow duct
leading to the exterior, and opening on the ventral surface
amongst the papillae of the second row (counting from the in-
ternal 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 (i/th) leg of the males of this species, this gland
(i'ittc above, note 4) possesses a slit-like opening placed at the
906 ANATOMY AND DEVELOPMENT
apex of a well-developed white papilla (PI. 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 Qth leg (PI. 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 (i) 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 examin-
ation 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 dis-
coveries 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.
OF PERIPATUS CAPENSIS. 907
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 ar-
ranged bilaterally in pairs, six on either side of these slits. The
following note in his handwriting is attached to this drawing:
"Young larva of Pcripatus capcnsis. — I could not make out
for certain which was the anterior end. Length r34 milli-
metres."
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 sfated 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 con-
tinuous 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 em-
bryo the nerve-cords still scarcely separated from the epiblast1.
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) arc 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,
1 Comparative Embryology, original edition, Vol. I. p. 318. [This edition, Vol. II.
P. 385-]
58—2
ANATOMY AND DEVELOPMENT
which is elongated in the direction of the long axis of the em-
bryo, 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 blasto-
pore 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 i'34.
It will be observed, on comparing it with the preceding em-
bryos, 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 con-
sideration 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
OF PERIPATUS CAPENSIS. 909
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 prasoral 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 . . . . . i -32 mm.
Distance from front end of body to front end of mouth '32 „
Distance from embryonic mouth to hind end of em-
bryonic 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 em-
bryonic 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 pre-
ceding stage. The posterior dilatation has disappeared. The
ANATOMY AND DEVELOPMENT
embryo has apparently about thirteen somites, which are still
quite distinct from one another, and apparently do not com-
municate 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 praeoral 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 connect-
ing 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
antennae, 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
OF PERIPATUS CAPENSIS. 911
same position as that of the adult ; but that the anus is consider-
ably 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 stomo-
dasum and proctodseum in Peripatus, unless the buccal cavity
represents the stomodaeum. 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 blas-
topore.
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 pri-
mitive 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 appear-
ance (this being due to the late development of the posterior
912 ANATOMY AND DEVELOPMENT
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 em-
bryos (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 praeoral lobes, and to the mesoblast of the
head1.
There is no need for us to enlarge upon the importance of
these facts. Their close bearing upon some of the most im-
portant problems of morphology will be apparent to all, and
we may with advantage quote here some passages from Bal-
four's Comparative Embryology, which shew that he himself
long ago had anticipated and in a sense predicted their dis-
covery.
"Although the mesoblastic groove of insects is not a gas-
trula, it is quite possible that it is the rudiment of a blasto-
pore, the gastrula corresponding to which has now vanished
1 We have seen nothing in any of our sections which we can identify as of so-
called mesenchymatous origin.
OF PERIPATUS CAPENSIS. 913
from development." (Comparative Embryology, Vol. I.— p.- 378,
the original edition1.)
"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 edition2.)
" 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 diver-
ticula." (Comparative Embryology, Vol. n. p. 294, the original
edition3.)
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 connec-
tion between the circumoral nervous system of the Ccelenterata,
and the nervous system of Echinodermata, Platyelminthes, Chae-
topoda, 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
Ncmertines (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 Chaitopoda and Arthropoda. It is especially de-
serving of notice, in connection with the nervous system of the
above-mentioned Nemertines and Peripatus, that the commis-
sure 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 6r less closely the ciliated
edge of the body of the supposed radiate ancestor." (Compara-
tive Embryology, Vol. II. pp. 311, 312, the original edition4.)
1 This edition, Vol. n. p. 457. * This edition, Vol. III. p. 352.
3 This edition, Vol. in. p. 356. 4 This edition, Vol. ill. pp. 378, 379.
ANATOMY AND DEVELOPMENT OF PER1PATUS CAPENSIS.
The facts of development here recorded give a strong addi-
tional 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. ll. p. 443, 1826.
2. M. Andouin and Milne-Edwards. " Classific. des Annelides et
description de celles qui habitent les cotes de France," p. 411, Ann. Scien.
Nat. ser. I. Vol. xxx. 1833.
3. M. Gervais. "Etudes p. servir a 1'histoire naturelle des Myria-
podes," Ann. Scien. Nat. ser. n. Vol. vn. 1837, p. 38.
4. Wiegmann. Wiegmann's Archiv, 1837.
5. H. Milne-Edwards. "Note sur le Peripate juluforme? Ann.
Scien. Nat. ser. n. Vol. xvm. 1842.
6. Blanchard. "Sur 1'organisation des Vers/' chap. IV. pp. 137 — 141,
Ann. Scien. Nat. ser. ill. Vol. VI 1 1. 1847.
7. Quatrefages. "Anat. des Hermelles, note on," p. 57, Ann. Scien.
Nat. ser. in. Vol. x. 1848.
8. Quatrefages. Hist. Nat. des Annele's, 1865, Appendix, pp. 675—6.
9. De Blainville. SiippL an Diet, des Sc. Nat. Vol. I.
10. Ed. Grube. " Untersuchungen lib. d. Bau von Peripatus Ed-
wardsii" Archiv filr 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 nova; zealandicc," Ann. and
Mag. of Nat. History, Jan. 1877.
15. Captain Hutton. " Observations on Peripatiis nova: sealandice"
Ann. and Mag. of Nat. History, Nov. 1876.
16. F. M. Balfour. "On Certain Points in the Anatomy of Peripatns
capensis,'" Quart. Journ. of Micr. Science, Vol. xix. 1879.
17. A. Ernst. Nature, March loth, 1881.
EXPLANATION OF PLATES. 915
EXPLANATION OF PLATES 46— 53 ».
COMPLETE LIST OF REFERENCE LETTERS.
A. Anus. a. Dorso-lateral horn of white matter in brain, a.g. Accessory gland
of male (modified accessoiy 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. e.g. Supraoesophageal
ganglia, cl. Claw. c. m. Circular layer of muscles, co. Commissures between the
ventral nerve-cords, co. i. Second commissure between the ventral nerve-cords.
co1. 2. Mass of cells developed on second commissure, cor. Cornea, c. s. d. Com-
mon duct for the two salivary glands, at. Cuticle, d. Ventral protuberance of
brain. d.l.m. Dorsal longitudinal muscle of pharynx. d. «. Median dorsal nerve
to integument from supraoesophageal 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. i, F. 2,&c. First and
second pair of feet, &c. f. Small accessory glandular tubes of the male generative
apparatus. F.^. Ganglionic enlargement on ventral nerve-cord, from which a pair of
nerves to foot pass off. /. gl. Accessory foot-gland, v. n. Nerves to feet. g. co.
Commissures between the ventral nerve-cords containing ganglion cells, g. o. Gene-
rative orifice. H. Heart, h. Cells in lateral division of body-cavity. hy. Hypo-
blast, i.j. Inner jaw. j. Jaw. j. n. Nerves to jaws. L. Lips. /. Lens. /. 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). /. m. Bands
of longitudinal muscles. M. Buccal cavity. M1. Median backward diverticulum of
mouth or common salivary duct which receives the salivary ducts, me. Mesenteron.
tnes. Mesoblaslic somite. ;//./. Muscles of jaw lever, m. s. Sheets of muscle passing
round the side walls of pharynx to dorsal body wall. od. Oviduct. <K. Oesophagus.
a's. co. GZsophageal 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 papillae, or. n. Nerves to oral papillae, or. p. Oral papilla:, o. s. Orifice of
duct of segmental organ, ov. Ovary. P. Pads on ventral side of foot. /. Common
duct into which the vasa deferentia open. /. c. Posterior lobe of brain, p. d. c.
Posterior commissure passing dorsal to rectum. /./. 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. /./. Primary papilla, pr. Prostate. R.
Rectum. Re. Retinal rods. R. ;//. Muscle of claw. s. Vesicle of nephridium. j1.
Part of 4th or 5th nephridium which corresponds to vesicle of other nephridia.
1 The explanations of the figures printed within inverted commas are by Professor
Balfour, the rest are by the Editors.
gi6 EXPLANATION OF PLATES.
s. c. i. Region No. i 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, si. d. Reservoir of slime gland, sl.g. Tubules of slime gland.
s. o. i, i, 3, &c. Nephridia of ist, 2nd, &c., feet. s. o.f. Terminal portion of nephri-
dium. s.p. Secondary papilla, st. Stomach, st. e. Epithelium of stomach, sy.
Sympathetic nerve running in muscles of tongue and pharynx, sy1. Origin of pharyn-
geal sympathetic nerves. T. Tongue, t. Teeth on tongue, te. Testis. tr. Tracheae.
tr. c. Cells found along the course of the tracheae. tr. o. Tracheal stigma. tr. p.
Tracheal pit. ut. Uterus. v. c. Ventral nerve cord. v. d. Vas deferens. z/. g.
Imperfect ganglia of ventral cord.
PLATE 46.
Fig. i. 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 (i;th) leg of a male Peripatns 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,
/., 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 ist and
•2nd pairs of legs, is followed by a short tubular oesophagus. The latter opens into
the large slomach 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.
EXPLANATION OF PLATES. 917
A. Anus. at. Antenna. F. i, K. 2. First and second feet. j. Jaws.~~ r. Lips.
a. (Esophagus. or. p. Oral papilla. ph. Pharynx. R. Rectum. s. d. Salivary
duct. s. g. Salivary gland, si. d. Slime reservoir, si. 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
scgmental 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 lyth
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. i, 2, &c. Feet. g. o. Generative orifice, ee. Oesophagus.
as. co. QEsophageal commissures, or. p. Oral papilla, p.d.c. Posterior dorsal com-
missure between the ventral nerve-cords, ph. Pharynx, p. n. Nerves to feet, one
pair from each ganglionic enlargement. si. d. Reservoir of slime gland. si. g.
Tubules of slime gland. s. o. i, 2, 3, &^. 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. ro. Outer jaw.
PLATE 49.
Figs, ii — 16. A series of six transverse sections through the head of Peripatus
capensis.
Fig. ir. The section is taken immediately behind the junction of the supra-
oesophageal ganglia, e.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 cuti-
cular 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 (M1),
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 (M1).
91 8 EXPLANATION OF PLATES.
Fig. 15. Section through the point of junction of the salivary ducts with the
median oral diverticulum.
Fig. 1 6. Section behind the pharynx through the oesophagus.
b. c. Body-cavity, c. Cutis. c. b. c. Central compartment of body-cavity, c. g.
Supra-cesophageal ganglia, c. m. Layer of circular muscles, co. Commissure between
ventral nerve-cords. co. i. Second commissure between the ventral nerve-cords.
co1. 2. Mass of cells developed on second commissure (probably sensory), c. s. d.
Common duct for the two salivary glands, d. I. m. Dorsal longitudinal muscles of
pharynx, d. o. Muscles serving to dilate the opening of the pharynx. Ep. Epider-
mis, e. n. Nerve passing outwards from ventral nerve-cord. H. Heart, i.j. Inner
jaw. j.p. Jaw papillae. L. Lips of buccal cavity. /. b. c. Lateral compartment of
body-cavity, le. Rod-like cuticular continuation of inner jaw, lying in a pit of the
buccal cavity. /. m. Bands of longitudinal muscles. M. Buccal cavity. M1. 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. ft'. Oesophagus.
a's. co. OZsophageal commissures. o.j. Outer jaw. ph. Pharynx. s. d. Salivary
duct. s. g. Salivary gland, si. d. Reservoir of slime gland, sy. Sympathetic nerves
running in muscles of tongue or pharynx, sy1. Origin of sympathetic nerves to
pharynx. T. Tongue, v. c. Ventral nerve-cords.
Figs. 17, 1 8. Two longitudinal horizontal sections through the head of Peripattis
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 tracheae 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. M1. Median backward diverti-
culum of mouth, o.j. Outer jaw. s. d. Salivary ducts. T. Tongue. /. Teeth on
tongue, tr. Tracheae, 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-latefral 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 anten-
nary 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 termi-
nation of the dorsal tongue of ganglion cells."
PLATE 51.
Fig. 20. Portion of a transverse section through the hinder part of Peripatm
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
EXPLANATION OF PLATES. 919
the enlarged crural gland of the lyth leg (f. gl.). (Zeiss a a, Hartnack's carmrn.} a-g.
accessory gland of male (modified crural gland of last leg). C. Cutis. cl. Claw.
eu. 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. i of coiled
part of nephridium. si. g. Tubule of slime gland, s. o. t. Terminal portion of nephri-
dium. st. Stomach, st. e. Epithelium of stomach, v. c. Ventral nerve-cord, v. d.
Vas deferens.
Fig. 21. "Longitudinal vertical section through the supra-cesophageal ganglion
and cesophageal commissures of Peripatus capensis. (Zeiss a a, Hartnack.)" at. An-
tenna, e. Central lobe of white matter. /. 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 (sy1) arising from the ventral surface of the hinder part.
From the commencement of the cesophageal commissures (as. co. ) pass off on each
side a pair of nerves to the jaws (/. ».).
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 papilla; a pair of large nerves on each
side (or. n.)
FiL-hind 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. Gan-
glionic enlargements from which nerves to feet pass off. j. n. Nerves to jaws. or. g.
Ganglionic enlargement from which nerves to oral papilla; pass off. or. n. Nerves to
oral papillae.' p.c. Posterior lobe of brain, p. n. Nerves to feet. s.y. Sympathetic
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. /. Lens. op. n. Optic nerve, ph. Pharynx. /./.
Primary papilla covered with secondary papillae 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. /. Lens. op. Optic ganglion, op. n. Optic nerve. //'. r. Pigment.
Re. rods. s. p. Secondary papillae.
920 EXPLANATION OF PLATES.
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 Pcripatus 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 gth 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. .?. External opening of segmental organ, p.f. Internal opening of nephridium
into the body-cavity (lateral compartment). s. Vesicle of segmental organ. j1.
Portion of segmental organ of 4th and 5th. legs, corresponding to vesicle of the other
nephridia. s. c. i. 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 Peripattis 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 repre-
sented. (Zeiss B, Hartnack's camera.)"
/./. Peritoneal funnel, s. Vesicle, s. c. i, s. c . i, s.c.$. 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. Tracheae, shewing rudimentary spiral fibre, tr. c. Cells resembling those
lining the tracheal pits, which occur at intervals along the course of the trachece.
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.
EXPLANATION OF PLATE 53. 92 1
Fig- 32. Section through the skin of Peripatus capensis ; it shews the secondary
papillae 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 papillae.
Fig- 33- Female generative organs of Peripatus capensis, x 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 papillae (aborted feet ?)."
F. 16, 17. Last two pairs of legs, od. Oviduct, .ov. Ovary, itt. 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 blasto-
pore. 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.
B. 59
922 EXPLANATION OF PLATE 53.
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. Meso-
blastic 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.
/. 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.
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