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Title: The works of Francis Maitland Balfour, Volume 2 (of 4)
A treatise on comparative embryology: Invertebrata

Author: Francis M. Balfour

Editor: Sir M. Foster
Adam Sedgwick

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*** START OF THE PROJECT GUTENBERG EBOOK THE WORKS OF
FRANCIS MAITLAND BALFOUR, VOLUME 2 (OF 4) ***

THE WORKS
OF

FRANCIS MAITLAND
BALFOUR.
VOL. II.

Memorial Edition.

Cambridge:
PRINTED BY C. J. CLAY, M.A. AND SON,
AT THE UNIVERSITY PRESS.

Memorial Edition.

THE WORKS
OF
FRANCIS MAITLAND BALFOUR,
M.A., LL.D., F.R.S.,
FELLOW OF TRINITY COLLEGE,
AND PROFESSOR OF ANIMAL MORPHOLOGY IN THE UNIVERSITY OF
CAMBRIDGE.

EDITED BY

M. FOSTER, F.R.S.,
PROFESSOR OF PHYSIOLOGY IN THE UNIVERSITY OF CAMBRIDGE;

AND

ADAM SEDGWICK, M.A.,
FELLOW AND LECTURER OF TRINITY COLLEGE, CAMBRIDGE.

VOL. II.
A TREATISE ON COMPARATIVE EMBRYOLOGY.
Vol. I. Invertebrata.

London:
MACMILLAN AND CO.
1885

[The Right of Translation is reserved.]

PREFACE.

My aim in writing this work has been to give such an account of the
development of animal forms as may prove useful both to students and to
those engaged in embryological research. The present volume, save in the
introductory chapters, is limited to a description of the development of the
Invertebrata: the second and concluding volume will deal with the
Vertebrata, and with the special histories of the several organs.
Since the work is, I believe, with the exception of a small but useful volume
by Packard, the first attempt to deal in a complete manner with the whole
science of Embryology in its recent aspects, and since a large portion of the
matter contained in it is not to be found in the ordinary text books, it
appeared desirable to give unusually ample references to original sources. I
have accordingly placed at the end of each chapter, or in some cases of each
section of a chapter, a list of the more important papers referring to the
subject dealt with. The papers in each list are numbered continuously, and
are referred to in the text by their numbers. These lists are reprinted as an
appendix at the end of each volume. It will of course be understood that
they do not profess to form a complete bibliography of the subject.
In order to facilitate the use of the work by students I have employed two
types. The more general parts of the work are printed in large type; while a
smaller type is used for much of the theoretical matter, for the details of
various special modes of development, for the histories of the less
important forms, and for controversial matter generally. The student,
especially when commencing his studies in Embryology, may
advantageously confine his attention to the matter in the larger type; it is of
course assumed that he already possesses a competent knowledge of
Comparative Anatomy.
Since the theory of evolution became accepted as an established doctrine,
the important bearings of Embryology on all morphological views have

been universally recognised: but the very vigour with which this department
of science has been pursued during the last few years has led to the
appearance of a large number of incomplete and contradictory observations
and theories; and to arrange these into anything like an orderly and
systematic exposition has been no easy task. Many Embryologists will
indeed probably hold that any attempt to do so at the present time is
premature, and therefore doomed to failure. I must leave it to others to
decide how far my effort has been justified. That what I have written
contains errors and shortcomings is I fear only too certain, but I trust that
those who are most capable of detecting them will also be most charitable
in excusing them.
The work is fully illustrated, and most of the figures have been especially
engraved from original memoirs or from my own papers or drawings by Mr
Collings, who has spared no pains to render the woodcuts as clear and
intelligible as possible. I trust my readers will not be disappointed with the
results. The sources from which the woodcuts are taken have been in all
cases acknowledged, and in the cases where no source is given the
illustrations are my own.
I take this opportunity of acknowledging my great obligations to Professors
Agassiz, Huxley, Gegenbaur, Lankester, Turner, Kölliker, and Claus, to Sir
John Lubbock, Mr Moseley, and Mr P. H. Carpenter, for the use of
electrotypes of woodcuts from their works.
I am also under great obligations to numerous friends who have helped me
in various ways in the course of my labour. Professor Kleinenberg, of
Messina, has read through the whole of the proofs, and has made numerous
valuable criticisms. My friend and former pupil, Mr Adam Sedgwick, has
been of the greatest assistance to me in correcting the proofs. I have had the
benefit of many useful suggestions by Professor Lankester especially in the
chapter on the Mollusca, and Mr P. H. Carpenter has kindly revised the
chapter on the Echinodermata.
I am also much indebted to Dr Michael Foster, Mr Moseley, and Mr Dew-
Smith for aid and advice.

CONTENTS OF VOLUME I.

Introduction. Pp. 1‑16.

Chapter I. The Ovum and Spermatozoon.
General history of the Ovum, pp. 17‑25. Special history of the Ovum in
different types, pp. 26‑65. The Spermatozoon, pp. 65‑67.

Chapter II. The Maturation and Impregnation of the Ovum.
Maturation of the Ovum, and formation of the polar bodies, pp. 68‑79.
Impregnation of the Ovum, pp. 79‑86. Summary, p. 86.

Chapter III. The Segmentation of the Ovum.
Internal phenomena of Segmentation, pp. 88‑92. External features of
Segmentation, pp. 92‑122.

Introduction to Systematic Embryology. Pp. 125‑130.

Chapter IV. Dicyemidæ and Orthonectidæ. Pp. 131‑137.

Chapter V. Porifera. Pp. 138‑151.

Chapter VI. Cœlenterata.
Hydrozoa, pp. 152‑167. Actinozoa, pp. 167‑173. Ctenophora,
pp. 173‑178. Summary, etc., pp. 178‑182. Alternations of generations,
pp. 182‑187.

Chapter VII. Platyelminthes.
Turbellaria, pp. 189‑196. Nemertea, pp. 196‑204. Trematoda,
pp. 205‑210. Cestoda, pp. 210‑218.

Chapter VIII. Rotifera. Pp. 221‑224.

Chapter IX. Mollusca.
Formation of the layers and larval characters, pp. 225‑273. Gasteropoda
and Pteropoda, pp. 225‑242. Cephalopoda, pp. 242‑254.
Polyplacophora, pp. 254‑257. Scaphopoda, pp. 257, 258.
Lamellibranchiata, pp. 258‑269. General review of Molluscan Larvæ,
pp. 270‑273. Development of organs, pp. 273‑288.

Chapter X. Polyzoa.
Entoprocta, pp. 292‑297. Ectoprocta, pp. 297‑305. Summary and
general considerations, pp. 305‑308.

Chapter XI. Brachiopoda.
Development of the layers, pp. 311‑313. The history of the larva,
pp. 313‑317. Development of organs, p. 317. General observations on
the affinities of the Brachiopoda, pp. 317, 318.

Chapter XII. Chætopoda.
Formation of the germinal layers, pp. 319‑325. The larval form,
pp. 325‑338. Formation of organs, pp. 338‑342. Alternations of
generations, pp. 342, 343.

Chapter XIII. Discophora.
Formation of layers, pp. 347‑350. History of larva, pp. 351‑354.

Chapter XIV. Gephyrea.
Gephyrea nuda, pp. 355‑361. Gephyrea tubicola, pp. 361‑364. General
considerations, p. 364.

Chapter XV.
Chætognatha, pp. 366‑369. Myzostomea, pp. 369, 370. Gastrotricha,
p. 370.

Chapter XVI.
Nematelminthes, pp. 370‑379. Acanthocephala, pp. 379‑381.

Chapter XVII. Tracheata.
Prototracheata, pp. 382‑387. Myriapoda, pp. 387‑395. Insecta,
pp. 395‑429. Embryonic membranes and the formation of the layers,
pp. 400‑406. Formation of the organs, pp. 406‑417. Special types of
larvæ, pp. 417‑419. Metamorphosis and heterogamy, pp. 420‑429.
Arachnida, pp. 431‑455. Formation of the layers and general
development, pp. 431‑446. Formation of the organs, pp. 446‑455.
Formation of the layers and embryonic envelopes in the Tracheata,
pp. 456‑458.

Chapter XVIII. Crustacea.
History of larval forms, pp. 459‑511. Branchiopoda, pp. 459‑465.
Malacostraca, pp. 465‑487. Copepoda, pp. 487‑492. Cirripedia,
pp. 492‑500. Ostracoda, pp. 500‑502. Phylogeny of the Crustacea,
pp. 502‑511. The formation of the germinal layers, pp. 511‑521.
Comparative development of organs, pp. 521‑529.

Chapter XIX.

Pœcilopoda, pp. 534‑538. Pycnogonida, pp. 538, 539. Pentastomida,
pp. 539‑541. Tardigrada, p. 541. Summary of Arthropodan
Development, pp. 541‑543.

Chapter XX. Echinodermata.
Development of the germinal layers, pp. 544‑553. Development of the
larval appendages and metamorphosis, pp. 553‑573. Summary and
general considerations, pp. 573‑576.

Chapter XXI. Enteropneusta. Pp. 579‑583.

Index. Pp. 584‑590.

Appendix.

EMBRYOLOGY.

INTRODUCTION.

Embryology forms a large and important department of Biology. Strictly
interpreted according to the meaning of the word, it ought to deal with the
growth and structure of organisms during their development within the egg
membranes, before they are capable of leading an independent existence.
Modern investigations have however shewn that such a limitation of the
science would have a purely artificial character, and the term Embryology is
now employed to cover the anatomy and physiology of the organism during
the whole period included between its first coming into being and its
attainment of the adult state.
The subject-matter of the science of Embryology admits of a twofold
classification. It may be placed under a series of heads, each dealing either
with a special group of organisms, or with a special department of the
whole science. If classified in the first of these ways the science will
naturally be divided into an Embryology of Plants, and an Embryology of
Animals; each of which admits of further subdivision. In the second way
the subject falls under two primary heads; viz. Physiological Embryology
and Anatomical Embryology.
The present treatise deals only with the Embryology of Animals, and is
further confined to those animals known as Metazoa. The science is
moreover treated from the morphological or anatomical, rather than from
the physiological side.
The marvellous phenomenon of the evolution of a highly complicated
living being from a simple undifferentiated germ in which it needs the aid
of the most modern microscopical appliances to detect any visible signs of
life, has not unnaturally attracted the attention of biologists from the very

earliest periods. Before the establishment of the cell theory the origin of the
organism from the germ was not known to be an occurrence of the same
nature as the growth of the fully formed individual, and Embryological
investigations were mixed up with irrelevant speculations on the origin of
life[1].
The difficulties of understanding the formation of the individual from the
structureless germ led anatomists at one time to accept the view “according
to which the embryo preexisted, even though invisible, in the ovum, and the
changes which took place during incubation consisted not in a formation of
parts, but in a growth, i.e. in an expansion with concomitant changes of the
already existing germ.”
Great as is the interest attaching to the simple and isolated life histories of
individual organisms, this interest has been increased tenfold by the
generalizations of Mr Charles Darwin.
It has long been recognized that the embryos and larvæ of the higher forms
of each group pass, in the course of their development, through a series of
stages in which they more or less completely resemble the lower forms of
the group[2]. This remarkable phenomenon receives its explanation on Mr
Darwin’s theory of descent. There are, according to this theory, two
guiding, and in a certain sense antagonistic principles which have rendered
possible the present order of the organic world. These are known as the
laws of heredity and variation. The first of these laws asserts that the
characters of an organism at all stages of its existence are reproduced in its
descendants at corresponding stages. The second of these laws asserts that
offspring never exactly resemble their parents. By the common action of
these two principles continuous variation from a parent type becomes a
possibility, since every acquired variation has a tendency to be inherited.
The remarkable law of development enunciated above, which has been
extended, especially by the researches of Huxley[3] and Kowalevsky, beyond
the limits of the more or less artificial groups created by naturalists, to the
whole animal kingdom, is a special case of the law of heredity. This law,
interpreted in accordance with the theory of descent, asserts that each
organism in the course of its individual ontogeny repeats the history of its
ancestral development. It may be stated in another way so as to bring out its

intimate connection with the laws of inheritance and variation. Each
organism reproduces the variations inherited from all its ancestors at
successive stages in its individual ontogeny which correspond with those at
which the variations appeared in its ancestors. This mode of stating the law
shews that it is a necessary consequence of the law of inheritance. The
above considerations clearly bring out the fact that Comparative
Embryology has important bearings on Phylogeny, or the history of the race
or group, which constitutes one of the most important branches of Zoology.
Were it indeed the case that each organism contained in its development a
full record of its origin, the problems of Phylogeny would be in a fair way
towards solution. As it is, however, the law above enunciated is, like all
physical laws, the statement of what would occur without interfering
conditions. Such a state of things is not found in nature, but development as
it actually occurs is the resultant of a series of influences of which that of
heredity is only one. As a consequence of this, the embryological record, as
it is usually presented to us, is both imperfect and misleading. It may be
compared to an ancient manuscript with many of the sheets lost, others
displaced, and with spurious passages interpolated by a later hand. The
embryological record is almost always abbreviated in accordance with the
tendency of nature (to be explained on the principle of survival of the
fittest) to attain her ends by the easiest means. The time and sequence of the
development of parts is often modified, and finally, secondary structural
features make their appearance to fit the embryo or larva for special
conditions of existence. When the life history of a form is fully known, the
most difficult part of his task is still before the scientific embryologist. Like
the scholar with his manuscript, the embryologist has by a process of
careful and critical examination to determine where the gaps are present, to
detect the later insertions, and to place in order what has been misplaced.
The aims of Comparative Embryology as restricted in the present work are
two-fold: (1) to form a basis for Phylogeny, and (2) to form a basis for
Organogeny or the origin and evolution of organs. The justification for
employing the results of Comparative Embryology in the solution of the
problems in these two departments of science is to be found in the law
above enunciated, but the results have to be employed with the
qualifications already hinted at; and in both cases a knowledge of
Comparative Anatomy is a necessary prelude to their application.

In accordance with the above objects Comparative Embryology may be
divided into two departments.
The scientific method employed in both of these departments is that of
comparison, and is in fact fundamentally the same as the method of
Comparative Anatomy. By this method it becomes possible with greater or
less certainty to distinguish the secondary from the primary or ancestral
embryonic characters, to determine the relative value to be attached to the
results of isolated observations, and generally to construct a science out of
the rough mass of collected facts. It moreover enables each observer to
know to what points it is important to direct his attention, and so prevents
that simple accumulation of disconnected facts which is too apt to clog and
hinder the advance of the science it is intended to promote.
In the department of Phylogeny the following are the more important points
aimed at.
(1) To test how far Comparative Embryology brings to light ancestral forms
common to the whole of the Metazoa. Examples of such forms have been
identified by various embryologists in the ovum itself, supposed to
represent the unicellular ancestral form of the Metazoa: in the ovum at the
close of segmentation regarded as the polycellular Protozoon parent form:
in the two-layered gastrula, etc., regarded by Haeckel as the ancestral form
of all the Metazoa[4].
(2) How far some special embryonic larval form is constantly reproduced in
the ontogeny of the members of one or more groups of the animal kingdom;
and how far such larval forms may be interpreted as the ancestral type for
those groups.
As examples of such forms may be cited the six-limbed Nauplius supposed
by Fritz Müller to be the ancestral form of the Crustacea; the trochosphere
larva of Lankester, which he considers to be common to the Mollusca,
Vermes, and Echinodermata; the planula of the Cœlenterata, etc.
(3) How far such forms agree with living or fossil forms in the adult state;
such an agreement being held to imply that the living or fossil form in
question is closely related to the parent stock of the group in which the
larval form occurs. It is not easy to cite examples of a very close agreement

of this kind between the larval forms of one group and the existing or fossil
forms of another. The larvæ of some of the Chætopoda with long
provisional setæ resemble fossil Chætopods. The Rotifers have many points
of resemblance to the trochosphere, especially to that form of trochosphere
characteristic of the Mollusca. The Turbellarians have some features in
common with the Cœlenterate planula. Some of the Gephyrea in the
presence of a præoral lobe resemble certain trochosphere types. The larva of
the Tunicata has the characters of a simple type of the Chordata.
Within the limits of a single group agreements of this kind are fairly
numerous. In the Craniata the tadpole of the Anura has its living
representative in the Pisces and perhaps especially in the Myxinoids. The
larval forms of the Insecta approach Peripatus. The stalked larva of
Comatula is reproduced by the living Pentacrinus and Rhizocrinus etc.
Numerous examples of the same phenomenon are found amongst the
Crustacea.
(4) How far organs appear in the embryo or larva which either atrophy or
become functionless in the adult state, and which persist permanently in
members of some other group or in lower members of the same group.
Cases of this kind are of the most constant occurrence, and it is only
necessary to cite such examples as the gill slits and Wolffian body in the
embryos of higher Craniata to illustrate the kind of instance alluded to. The
same conclusions may be drawn from them as from the cases under the
previous heading.
(5) How far organs pass in the course of their development through a
condition permanent in some lower form. Phylogenetic conclusions may be
drawn from instances of this character, though they have a more important
bearing on Organology than on Phylogeny.
The considerations which were used to shew that the ancestral history is
reproduced in the ontogeny of the individual apply with equal force to the
evolution of organs. The special questions in Organology, on which
Comparative Embryology throws light, may be classified under the
following heads.
(1) The origin and homologies of what are known as the germinal layers; or
the layers into which the embryo becomes divided immediately after the

segmentation.
(2) The origin of primary tissues, epithelial, nervous, muscular, connective,
etc., and their relation to the germinal layers.
(3) The origin of organs. The origin of the primitive organs is intimately
connected with that of the germinal layers. The first differentiation of the
segmented ovum results in the cells of the embryo becoming arranged as
two layers, an outer one known as the epiblast and an inner one as the
hypoblast. The outer of these forms a primitive sensory organ, and the inner
a primitive digestive organ.
(4) The gradual evolution of the more complicated organs and systems of
organs.
This part of the subject, even more than that dealing with questions of
Phylogeny, is intimately bound up with Comparative Anatomy; without
which indeed it becomes quite meaningless.

Reproduction.
A study of reproduction logically precedes that of Embryology.
Reproduction essentially consists in the separation of a portion of an
organism which has the capacity of developing into a form similar to that
which gave it origin. The simplest modes of reproduction are those which
occur amongst the Protozoa.
In this group, reproduction may take place in a great variety of ways. These
may be classified in three groups: (1) fission, (2) budding or gemmation, (3)
spore formation.
Reproduction in all these ways may take place either subsequently to and
apparently in consequence of a very important process known as
conjugation, which consists in the temporary or permanent fusion of two or
more individuals, or spontaneously, i.e. independently of any such previous
conjugation.
Reproduction by fission consists simply in the division of the organism into
two similar parts, the nucleus when present becoming divided

simultaneously with the cell body. This mode of reproduction is the
simplest conceivable, and is not followed by a development, since the two
organisms produced are exactly similar, except in size, to the parent form.
Besides single fission, a process of multiple fission may take place, as
amongst the Flagellata, where Drysdale and Dallinger have shewn that an
individual enclosed within a structureless cyst may divide first into two,
then into four, and so on.
The process of budding differs mainly from that of simple fission in the fact
that the two organisms produced are dissimilar in size, and also that the
separation of the smaller organism from the larger is preceded by a process
of growth in the latter, so that in the separation of the bud no essential part
of the parent form is removed. This mode of reproduction is found amongst
the Infusoria, Acineta, &c. An interesting variation in it is the internal
gemmation of many of the Acineta, where a portion of the internal
protoplasm with part of the nucleus is separated off to form a fresh
individual. This mode of gemmation is connected by a series of gradations
with the normal external gemmation. The organisms produced by
gemmation are not always similar at birth to the parent; e.g. Acineta.
Both fission and gemmation when incomplete lead to the formation of
colonies.
The third mode of reproduction, by spore formation, does not essentially
differ from that by multiple fission. It consists in the breaking up of the
organisms into a number (usually very considerable) of portions; each of
which eventually develops into an organism like the parent form. All
gradations between a simultaneous division of the organism into such
spores and simple multiple fission are to be found, but this process of
reproduction may be sometimes distinguished from that by such fission by
the fact that the two processes may coexist in a single form, e.g. the
biflagellate monad of Drysdale and Dallinger. In the majority of cases the
spores produced differ at first from the parent organism not only in size but
in other points, such as the possession of a flagellum, etc. They may even
be without a nucleus when the parent organism is nucleated, as in the
Gregarinidæ.

The encystment, which in many cases precedes reproduction by any of the
above processes, and more especially by spores, is not an essential
condition of their occurrence; and is probably in the first instance a
protective arrangement which has become secondarily adapted to and
connected with reproduction.
As has been already stated, all the above modes of reproduction take place
in some of the Protozoa without any anterior process which can be regarded
as of a sexual nature; but very often they are preceded by the temporary or
permanent fusion of two or more individuals, such fusion being known as
conjugation.
In most cases reproduction by spores is the consequence of conjugation, but
in the Infusoria etc. where the fusion at conjugation is temporary (except
Vorticella), there is probably merely a renewed activity—a rejuvenescence
—which most likely results in active fission or budding. In the Gregarinidæ
reproduction by spores usually follows conjugation, but may also take place
without it. In some Flagellata reproduction by spores follows the
conjugation of two individuals in a different stage of development. Thus in
the springing Monad, described by Drysdale and Dallinger, a form
produced by the fission of a monad in an amœboid condition fuses with an
ordinary monad to produce an individual, which then breaks up into spores.
Another instance of the fusion of dissimilar individuals is afforded by
Vorticella, where a free-swimming individual conjugates and is
permanently united with a fixed one (Engelmann, Bütschli). Conjugation
often consists in the fusion of more than two individuals. In conjugation
where the fusion is permanent, the nuclei of the conjugating forms usually
unite before the product breaks up into spores and where temporary fusion
occurs in the Infusoria a division of the paranuclei and often of the nuclei
takes place, followed by the ejection of parts of them, and a reproduction of
new paranuclei and nuclei from the remainder of the original structures.
In order to understand the meaning of conjugation in connection with
reproduction, it is important to understand how the two became in the first
instance related. For the solution of this question the fact that many
Protozoa have the capacity of temporarily or permanently fusing together
without an immediate act of reproduction is of great importance. A good
example of such fusion is supplied by Actinophrys. We must suppose in fact

that the simple coalescence of two or more individuals gives a sufficient
amount of extra vigour to their product, to compensate the race for the loss
in number of individuals so caused. This extra vigour probably first
exhibited itself especially by increased activity in reproduction, till finally
the two processes, viz. that of conjugation and that of reproduction, came to
be inseparably connected together.
The reproduction of the forms above the Protozoa, which are known as the
Metazoa, takes place by two methods, viz. a sexual and an asexual one. The
sexual process, which occurs in every known Metazoon[5], consists
essentially, as is shewn in the second chapter of this work, in the fusion of
two cells budded off from the parent organism, viz. the female cell or ovum,
and the male cell or spermatozoon, and of the subsequent division of the
compound cell so produced into a number of parts which build themselves
up into an organism resembling one of the parents. The sexual process has
obviously at first sight a very close resemblance to the process of
conjugation. Since it is a question of fundamental importance to determine
how sexual reproduction originated, it becomes necessary to examine how
far this apparent resemblance is a real one, and how far sexual reproduction
can be derived from reproduction following upon conjugation.
In spite of the general similarity between the two processes there is an
obvious difficulty in comparing them, in that the result of conjugation is
usually the breaking up of the individual formed by the fusion of two other
individuals into a number of new organisms, while the result of the fusion
which takes place in sexual reproduction is the formation of a single new
organism. This difference between the two processes, great as it is, is
perhaps apparent rather than real. It must be remembered that a single
individual Metazoon is equivalent to a number of Protozoa coalesced to
form a single organism in a higher state of aggregation. It results from this
that the segmentation of the ovum which follows the sexual act may be
compared to the breaking up of the product of conjugation into spores, the
difference between the two processes consisting in the fact that in the one
case the spores separate each to form an independent organism, while in the
other they remain united and give rise to a single compound organism.
If the above considerations are well founded it seems permissible to accept
the general view according to which sexual reproduction is derived from

conjugation. It is necessary to suppose that, in a colony of Protozoa in the
course of becoming a Metazoon, the capacity of reproduction by spores
became localized in certain definite cells, and although the formation of
spores from these cells may have been possible without previous
conjugation, yet that conjugation gradually became established as the rule.
The differentiation of primitively similar conjugating cells into male and
female cells was probably a very early occurrence, since indications of an
analogous differentiation, as has already been mentioned, are found in
certain existing Protozoa (Monads, Vorticella, etc.). I have attempted to
shew in the second chapter that the breaking up of the cell into spores
without previous conjugation is perhaps provided against in the extrusion of
the so-called ‘directive body’.
With the differentiation of special germinal cells, to take the place of the
whole individual in the act of conjugation, the possibility of each act of
conjugation resulting in the production of only a single organism became
introduced. Germinal cells can be indefinitely produced, and the
reproductive capacity of a single individual is therefore unlimited; while if
two whole individuals conjugated and only produced one from the process,
the result would be a diminution instead of an increase in the race[6].
It must be admitted that, in the present state of our knowledge, the passage
from reproduction by spores following conjugation, to true sexual
reproduction, can only be traced in a very speculative manner, and that a
further advance in our knowledge may prove that the steps which I have
attempted to sketch out are far from representing the true origin of sexual
differentiation. The peculiar conjugation and fusion of two individuals to
form Diplozoon paradoxum may be alluded to in this connection. This
fusion merely results in the attainment of sexual maturity by the two
conjugating individuals. It does not appear to me probable that this
conjugation is in any way connected with the conjugation of the Protozoa,
but the reverse must be borne in mind as a possibility.
It is not easy to decide whether the hermaphrodite or the diœcious state is
the primitive one, or in other words whether the two conjugating cells, from
which I have supposed the sexual products to originate, were derived in the
first instance from one or from two colonies of Protozoa. On purely a priori
grounds it seems probable that they were originally formed in one colony,

and that their derivation from two colonies or individuals was inaugurated
when the spermatozoon became motile. There can be no doubt that the
diœcious state is a very early one, and that the majority of existing cases of
hermaphroditism are secondary.
The above considerations with reference to the male and female cells
appear to indicate that they were primitively homodynamous; a conclusion
which is on the whole borne out by the history of their development.
Although the modes of reproduction amongst the Metazoa have been
divided into the classes sexual and asexual, there is nevertheless one mode
of asexual reproduction which ought to be classified with the sexual rather
than with the asexual modes. I mean parthenogenesis, which consists
essentially in the development of the ovum into a fresh individual without
previous coalescence with the male element. This mode of reproduction,
which has a very limited range in the animal kingdom, being confined to
the Arthropoda and Rotifera, is undoubtedly secondarily derived from
sexual reproduction. The conditions of its occurrence are discussed in the
second chapter.
It is remarkable that in certain cases the absence of fertilization causes the
production of males (Bees, a Saw-fly, Nematus ventricosus, etc.); more
usually it results in the production of females only, and there are very often
in the Arthropoda a series of successive generations of females all
producing ova which develop parthenogenetically into females; eventually
however, usually in direct or indirect connection with a change of food or
temperature, or other conditions, ova are formed which give rise without
fertilization both to males and females.
The true asexual modes of reproduction amongst the Metazoa consist of
fission and gemmation. Gemmation is by far the most widely disseminated
of the two. Various as are the methods in which it takes place, it seems
nevertheless that cells derived from all the germinal layers, and very
frequently from all the important organs of the adult, assist in forming the
bud. Into the details of the process, which require in many points a fuller
elucidation, it is not my purpose to enter.
Gemmation is a far commoner occurrence amongst the simpler than
amongst the more highly organised forms. It appears to have been

superadded to the sexual mode of reproduction quite independently in a
number of different instances.
While there is no difficulty in understanding how gemmation may have
started in such simple types as the Cœlenterata, the manner in which it first
originated in certain highly organised forms, as for instance the Ascidians,
is somewhat obscure, but it seems probable that it began with the division
of the developing germ into two or more embryos, at a very early stage of
growth.
Such a division of the germ is, as has been shewn by Kleinenberg, normal
in Lumbricus trapezoides[7] and Haeckel has shewn that an artificial division
of the germ in the Siphonophora leads to the development of two
individuals. It has been pointed out by various naturalists that the
production of double monsters is often a phenomenon of the same nature.
While it is next to impossible to understand how production of a bud could
commence for the first time in the adult of a highly organised form, it is not
difficult to form a picture of the steps by which the fission of the germ
might eventually lead to the formation of buds in the adult state.
The coexistence of sexual reproduction with normal asexual multiplication,
or with parthenogenesis, has led to a remarkable phenomenon in the animal
kingdom known as alternations of generations[8].
For the details of the various types of alternations of generations, and their
origin, the reader is referred to the body of the work; but a few general
remarks on the nature and origin of the process, and on its nomenclature,
may conveniently be introduced in this place. The simplest cases are those
in which an individual which produces by sexual means gives origin to
asexual individuals differently organised to itself, which produce by
budding the original sexual form, and so complete a cycle. Instances of this
kind are supplied by the Hydrozoa, Annelida and Tunicata. In the case of
the Tunicata (Doliolum) two different asexual generations may be
interpolated between the sexual generations. In all these cases the origin of
the phenomenon is easily understood. It appears, as is most clearly shewn in
the case of the Annelida, that the ancestors of the species which now exhibit
alternations of generations originally reproduced themselves at the same
time both sexually and by budding, though probably the two modes of

reproduction did not take place at the same season. Gradually a
differentiation became established, by which sexual reproduction was
confined to certain individuals, which in most instances did not also
reproduce asexually. After the two modes of reproduction became confined
to separate individuals, the dissimilarity in habits of life necessitated by
their diverse functions caused a difference in their organization; and thus a
complete alternation of generations became established. The above is no
merely speculative history, since all gradations between complete
alternations of generations and simple budding combined with sexual
reproduction can be traced in actually existing forms.
The alternation of generations as it is found amongst the Entoparasitic
Trematodes and most Cestodes, is to be explained in a slightly different
way.
It appears that in these parasitic forms a complicated metamorphosis first
arose from the parasite having to accommodate itself to the different hosts it
was compelled to inhabit, owing to the liability of its primitive and
subsequent hosts to be devoured[9]. A capacity for asexual multiplication—
obviously of immense advantage to a parasite—appears to have been
acquired in some of the stages of this metamorphosis, and an alternation of
generations thus established.
A nearly parallel series to that exhibiting alternations of sexual generations
with generations which produce by budding is supplied by the cases where
sexual generations alternate with parthenogenetic ones, or in some instances
even with larvæ which reproduce sexually or else parthenogenetically.
The best known examples of this form of alternations of generations are
found amongst the Insecta[10]. A simple case is that of the Aphides. The ova
deposited by impregnated females give rise to forms differently organised
to the parents but provided with an ovary[11]. The eggs from the ovary
develop parthenogenetically within the oviduct, and so long as there is
plenty of food and warmth the generations produced are always
parthenogenetic forms. The failure of warmth and nutriment causes the
production of true males and females, and so the cycle is completed. We
must suppose that the capacity possessed by so many female insects of
producing eggs capable of developing without the influence of the male

element, has been, so to speak, taken hold of by natural selection, and has
led to the production of viviparous parthenogenetic forms, by which, so
long as food is abundant, a clear economy in reproduction is effected. The
continuance of the species during winter is secured by the production of
males and females, the females laying eggs in autumn which are hatched in
the spring.
In Chermes there is less modification of the primitive condition in that the
parthenogenetic generations lay their eggs like the impregnated females. In
the gall-flies (Cynipidæ), there is frequently an alternation of generations of
the same kind as in Chermes; there being no viviparous forms. The
individuals of the different generations differ from each other to some
extent in all these cases.
A second type of alternations of parthenogenetic and sexual generations is
exemplified by the cases of Chironomus and Cecidomyia, where the larvæ
which develop from the eggs of the fertilized female produce
parthenogenetically, by means of true ova, forms which eventually after
several generations (Cecidomyia) of larval reproduction give rise to sexual
forms. The explanation is here practically the same as in the case of Aphis,
and is paralleled in the gemmiparous series by the production of buds in the
larval forms of Trematodes, etc. A very similar occurrence takes place in
Ascaris nigrovenosa (vide chapter on Nematoidea), except that larval forms,
which carry on reproduction and then perish without developing farther, do
so by a true sexual process. Thus there is an alternation of generations of
adult and larval sexual forms. The Axolotl is an intermittent example of the
same phenomenon.
As might be anticipated from the mode in which alternations of generations
have become established, incomplete approximations to it are not
uncommon. Such approximations are especially found in the Arthropoda,
where alternations of sexual and parthenogenetic generations frequently
take place, in which the individuals of different generations are similarly
organised (Psychidæ, Apus, &c.). Another approximation is afforded by the
parthenogenetic winter eggs of Leptodora amongst the Phyllopods, which
give rise to Nauplius larvæ, while the young hatched from the summer eggs
do not pass through a metamorphosis. Numerous transitional cases are also

found amongst the forms in which there is an alternation of sexual and
gemmiparous generations.
The whole of the cases to which allusion has been made in this section may
be conveniently classed under the term alternations of generations, but the
cases of alternation of two sexual generations, and of sexual and
parthenogenetic generations, are classified by Leuckart, Claus, etc. as cases
of heterogeny, which they oppose to the other form of alternation of
generations. If special terms are to be adopted for the two kinds of
alternation of generations, it would be perhaps convenient to classify the
cases of alternations of sexual and gemmiparous generations under the term
m e t a g e n e s i s , and to employ the term h e t e r o g a m y for the cases
of alternation of sexual and parthenogenetic generations.
The term Nurse (German Amme), employed for the asexual generations in
metagenesis, may advantageously be dropped altogether.

[1] To this general statement Wolff forms a remarkable exception, for though
without any clear knowledge of what we call cells he had very distinct notions on
the relations of growth and development.
[2] Von Baer who is often stated to have established the above generalization really
maintained a somewhat different view. He held (Ueber Entwickelungsgeschichte d.
Thiere, p. 224) that the embryos of higher forms never resembled the adult stages of
lower forms but merely the embryos of such forms. Von Baer was mistaken in thus
absolutely limiting the generalization, but his statement is much more nearly true
than a definite statement of the exact similarity of the embryos of higher forms to
the adults of lower ones.
[3] Huxley was the first to shew that the body of the Cœlenterata was formed of two
layers, and to identify these with the two primary germinal layers of the Vertebrata.
[4] The value of these identifications as well as of those below is discussed in its
appropriate place in the body of the work. Their citation here is not to be regarded
as necessarily implying my acceptance of them.
[5] Dicyema, if it is a true Metazoon, would seem to form an exception to this rule.

[6] In the vegetable kingdom there are numerous types of Thallophytes, which throw
a considerable amount of light on the relation between sexual reproduction and
conjugation. Subjoined are a few of the more striking cases. In Pandorina at the
time of sexual reproduction the cells which constitute a colony divide each into
sixteen, and the products of their division are set free. Pairs of them then conjugate
and permanently fuse. After a resting stage the protoplasm is set free from its
envelope after division into two or four parts. Each of these then divides into

sixteen coherent cells and constitutes a new Pandorina colony. In Œdogonium the
fertilization is effected by a spermatozoon fusing with an oosphere (ovum). The
fertilized oosphere (oospore) then undergoes segmentation like the ovum of an
animal; but the segments, instead of uniting to form a single organism, separate
from each other, and each of them gives rise to a fresh individual (swarm-spore)
which grows into a perfect Œdogonium. In Coleochæte the impregnation and
segmentation take place nearly as in Œdogonium, but the segments remain united
together, acquire definite cell walls, and form a single embryo. There is in fact in
Coleochæte a true sexual reproduction of the ordinary type. (Vide S. H. Vines “On
alternation of generation in the Thallophytes.” Journal of Botany, Nov., 1879.)
[7] The case of Pyrosoma, which might be cited in this connection, is probably
secondary.
[8] For an excellent account of this subject, vide Allen Thompson’s article Ovum in
Todd’s Cyclopædia. The metamorphosis of the Echinoderms included under this
head in Thompson’s article is now known not to be a proper case of alternations of
generations.
[9] The appearance of Vertebrata on the globe as the forms which most frequently
preyed on Invertebrate forms, and were themselves not so liable to be devoured, has
no doubt had a great influence on the metamorphosis of internal parasites, and has
amongst other things resulted in these parasites usually reaching their sexual state in
a vertebrate host.
[10] For details vide Chapter on Insecta.

[11] The distinction drawn by Huxley between ova and pseudova does not appear to
me a convenient one in practice.

CHAPTER I.

THE OVUM AND SPERMATOZOON.

The Ovum.
The complete developmental history of any being constitutes a cycle. It is
therefore permissible in treating of this history to begin at any point. As a
matter of convenience the ovum appears to be the most suitable point of
departure. The question as to the germinal layer from which it is ultimately
derived is dealt with in a subsequent part of the work; the present chapter
deals with its origin and growth.

General History of the Ovum.
Every young ovum (fig. 1) has the character of a simple cell. It is formed of
a mass of naked protoplasm (a), containing in its interior a nucleus (b),
within which there is a nucleolus (c). The nucleus and nucleolus are usually
known as the germinal vesicle and germinal spot.

Fig. 1. Diagram Of the Ovum. (From Gegenbaur.)
a. Granular protoplasm. b. Nucleus (germinal vesicle). c. Nucleolus (germinal spot).

The ovum so constituted is developed either (1) from one cell out of an
aggregation or layer of cells all of which have the capacity of becoming

ova; or (2) from one of a number of cells segmented off from a polynuclear
mass of protoplasm, not divided into separate cells. In both cases the cells
which have the capacity of becoming ova may be spoken of as germinal
cells, and in the case where the ova are ultimately developed from a
polynuclear mass of protoplasm the latter structure may be called a
germogen.
In some cases the whole of the germinal cells eventually become ova, but as
a rule only a small proportion of them have this fate, the remainder
undergoing various changes to be spoken of in the sequel.
Extended investigations have shewn that the distinction between germinal
cells which are independent cells from the first, or derived from a germogen
in which the nucleated protoplasm is not divided into cells, is an
unimportant one; and closely allied forms may differ in this respect. It is
moreover probable that a germogen of nucleated protoplasm is less
common than is often supposed: it being a matter of great difficulty to
determine the structure of the organs usually so described. A germogen is
stated to be found in most Platyelminthes, Nematoidea, Discophora,
Insecta, and Crustacea.
A more important distinction in the origin of the germinal cells is that
afforded by their position. In this respect three groups may be distinguished.
(1) The germinal cells may form the lining of a sack or tube, having the
form of a syncytium or of an epithelium of separate cells (Platyelminthes,
Mollusca, Rotifera, Echinodermata, Nematoidea, Arthropoda). (2) Or they
may form a specialized part of the epithelium lining the general body cavity
(Chætopoda, Gephyrea, Vertebrata). (3) Or they may form a mass placed
between the two elsewhere contiguous primitive germinal layers
(Cœlenterata[12]).
Types of transition between the first and second group are not uncommon.
Such types, properly belonging to the second group, originate by a special
membranous sack continuous with the oviduct being formed round the
primitively free patch of germinal cells. Examples of this are afforded by
the Discophora, the Teleostei, etc. It is very probable that all the cases
which fall under the first heading may have been derived from types which
belonged to the second group.

The mode of conversion of the germinal cells into ova is somewhat diverse.
Before the change takes place the germinal cells frequently multiply by
division. The change itself usually involves a considerable enlargement of
the germinal cell, and generally a change in the character of the germinal
vesicle, which in most young ova (fig. 2) is very large as compared to the
body of the ovum. The most complicated history of this kind is that of the
ovum of the Craniata. (Vide pp. 56, 57.)

Fig. 2. Ovum Of Carmarina (Geryonia) hastata. (Copied from Haeckel.)
gd. Body of ovum. gv. Germinal vesicle. gm. Germinal spot.

The ovum in its young condition is obviously nothing but a simple cell; and
such it remains till the period when it attains maturity.
Nevertheless the changes which it undergoes in the course of its growth are
of a very peculiar kind, and, consisting as they do in many instances of the
absorption of other cells, have led various biologists to hold that the ovum
is a compound structure. It becomes therefore necessary to consider the
processes by which the growth and nutrition of the ovum is effected before
dealing with the structure of the ovum at all periods of its history.

Fig. 3. Female gonophore of Tubularia Mesembryanthemum. Containing One Large
Ovum (ov) and a number of germinal cells (g.c.).
ep. Epiblast (Ectoderm). hy. Hypoblast (Entoderm). ov. Ovum. g.c. Germinal cells.

The ovum is of course nourished like every other cell by the nutritive fluids
in which it is surrounded, and special provisions are made for this, in that
the ovary is very frequently placed in contiguity with vascular channels.
But in addition to such nutrition a further nutrition, the details of which are
given in the special part of this chapter, is provided for in the germinal cells
which do not become ova.
In the simplest case, as in many Hydrozoa (fig. 3), the germinal cells which
do become ova are assimilated by the ovum much in the manner of an
Amœba.
In other cases the ovum becomes invested by a special layer of cells, which
then constitutes what is known as a follicle. The cells which form the
follicle are often germinal cells, e.g. Holothuria, Insecta (fig. 17), Vertebrata
(fig. 19). In other cases they seem rather to be adjoining connective-tissue
or epithelioid cells, though it is sometimes difficult to draw the line between
such cells and germinal cells. Examples of follicles formed of ordinary

connective-tissue cells, are supplied by Asterias, Bonellia (fig. 16),
Cephalopoda (fig. 14), etc.
A membrane enclosing the ovum without a lining of cells, as in many Arachnida, vide p. 51, has no
true analogy with a follicle and does not deserve the same name.

The function of the follicle cells appears to be, to elaborate nutriment for
the growth of the ovum. The follicle cells are not as a rule directly absorbed
into the body of the ovum, though in some instances, as in Sepia (vide
p. 40), they are eventually assimilated in this way.
In many cases some of the germinal cells form a follicle, while other
germinal cells form a mass within the follicle destined eventually to be used
as pabulum. Insects supply the best known examples of this, but Piscicola,
Bonellia (?) may also be cited as examples of the same character. In the
Craniata (pp. 56‑58) some of the germinal cells which advance a certain
distance on the road towards becoming ova, are eventually used as
pabulum, before the formation of the follicle; while other germinal cells
form at a later period the follicular epithelium. A peculiar case is that of the
Platyelminthes (fig. 9), where a kind of follicle is constituted by the cells of
a specially differentiated part of the ovary, known as the yolk-gland. The
cells of this follicle may either remain distinct, and continue to surround the
ovum after its development has commenced, and so be used as food by the
embryo; or they may secrete yolk particles, which enter directly into the
protoplasm of the ovum.
For further variations in the mode of nutrition the reader is referred to the
special part of this chapter. Suffice it to say that none of the known modes
of nutrition indicate that the ovum becomes a compound body any more
than the fact of an Amœba feeding on another Amœba would imply that the
first Amœba ceased thereby to be a unicellular organism.
The constitution of the ovum may be considered under three heads:—
(1) The body of the ovum.
(2) The nucleus or germinal vesicle.
(3) The investing membranes.
The body of the ovum. The essential constituent of the body of the ovum is
an active living protoplasm. As a rule there are present certain extraneous

matters in addition, which have not the vital properties of protoplasm. The
most important of these is known as food-yolk, which appears to be
generally composed of an albuminoid matter.
The body of the ovum is at first very small compared with the germinal
vesicle, but continually increases as the ovum approaches towards maturity.
It is at first comparatively free from food-yolk; but, except in the rare
instances where it is almost absent, food-yolk becomes deposited in the
form of granules, or highly refracting spheres, by the inherent activity of the
protoplasm during the later stages in the ripening of the ovum. In many
instances the protoplasm of the ovum assumes a sponge-like or reticulate
arrangement, a fluid yolk substance being placed in the meshes of the
reticulum. The character of the food-yolk varies greatly. Many of its chief
modifications are described below. There is not unfrequently present in the
vitellus a peculiar body known as the yolk nucleus, which is very possibly
connected with the formation of the food-yolk. It is found in many
Arachnida, Myriapoda, Amphibia, etc.[13]

Fig. 4. A. Ovum of Hydra in the amœboid state, with yolk-spherules (pseudocells) and
Chlorophyll Granules. (After Kleinenberg.)
gv. Germinal vesicle.
B. Single pseudocell of Hydra.

More important for the subsequent development than the variation in the
character of the food-yolk is its amount and distribution. In a large number
of forms it is distributed unsymmetrically, the yolk being especially
concentrated at one pole of the ovum, the germinal vesicle, surrounded by a
special layer of protoplasm comparatively free from food-yolk, being
placed at the opposite pole. In the Arthropoda it has in most instances a
symmetrical distribution. Further details on this subject are given in
connection with the segmentation; the character of which is greatly
influenced by the distribution of food-yolk.
The body of the ovum is usually spherical, but during a period in its
development it not unfrequently exhibits a very irregular amœboid form,
e.g. Hydra (fig. 4), Halisarca.

Fig. 5. Unripe ovum of Toxopneustes lividus. (Copied from Hertwig.)

The germinal vesicle. The germinal vesicle exhibits all the essential
characters of a nucleus. It has a more or less spherical shape, and is
enveloped by a distinct membrane which seems, however, in the living state
to be very often of a viscous semi-fluid nature and only to be hardened into
a membrane by the action of reagents (Fol). The contents of the germinal
vesicle are for the most part fluid, but may be more or less granular. Their
most characteristic components are, however, a protoplasmic network and
the germinal spots[14]. The protoplasmic network stretches from the
germinal spots to the investing membrane, but is especially concentrated

round the former. (Fig. 5.) The germinal spot forms a nearly homogeneous
body, with frequently one or more vacuoles. It often occupies an eccentric
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 amœboid movements (Hertwig, Eimer), and is moreover
more solid and more strongly tinged by colouring reagents than the
remaining constituents of the germinal vesicle.
In many instances there is only one germinal spot, or else one main spot and
two or three accessory smaller spots. In other cases, e.g. Osseous Fishes,
Echinaster fallax, Eucope polystyla, there are a large number of nearly
equal germinal spots which appear to result from the division or
endogenous proliferation of the original spot. Sometimes the germinal spots
are placed immediately within the membrane of the germinal vesicle
(Elasmobranchii and Sagitta). In many Lamellibranchiata, in the
earthworm, and in many Chætopoda the components of the germinal spot
become separated into two nearly spherical masses (fig. 12), which remain
in contiguity along a small part of their circumference, and are firmly united
together. The smaller of the two parts is more highly refractive than the
larger. Hertwig has shewn that the germinal spot is often composed of two
constituents as in the above cases, but that the more highly refractive
material is generally completely enclosed by the less dense substance. By
Fol the germinal spot is stated to be absent in a species of Sagitta, but this
must be regarded as doubtful. In young ova the relative size of the germinal
vesicle is very considerable. It 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.
As the ovum attains maturity, important changes take place in the
constitution of the germinal vesicle, which are described in the next chapter.
The egg membranes. A certain number of ova when ready to be fertilized
are naked cells devoid of any form of protecting covering, but as a rule the
ovum is invested by some form of membrane. Such coverings present great
variety in their character and origin, and may be conveniently (Ludwig, No.
4) divided into two great groups, viz. (1) those derived from the protoplasm

of the ovum itself or from its follicle, which may be called p r i m a r y
e g g m e m b r a n e s ; and (2) those formed by the wall of the oviduct or
otherwise, such as the egg-shell of a bird, which may be called
secondary egg membranes.

Fig. 6. Ovum of Toxopneustes variegatus with the pseudopodia-like processes of the
protoplasm penetrating the zona radiata (zr). (After Selenka.)

The primary egg membranes may again be divided into two groups (Ed. van
Beneden, No. 1), viz., (1) those formed by the protoplasm of the ovum, to
which the name v i t e l l i n e m e m b r a n e s will be applied; and (2)
those formed by the cells of the follicle, to which the name c h o r i o n
will be applied.
The secondary egg membranes will be dealt with in connection with the
systematic account of the development of the various groups. They coexist
as a rule with primary membranes, though in some types (Cephalophorous
Mollusca, many Platyelminthes, etc.), they constitute the only protecting
coverings of the ovum.
The vitelline membranes are either simple structureless membranes or
present numerous radial pores. Membranes with the latter structure are very
widely distributed, Echinodermata, Gephyrea, Vertebrata, etc. (Vide figs. 5
and 7.) The function of the pores appears to be a nutritive one. They either
serve for the emission of pseudopodia-like processes of the protoplasm of

the ovum, as has been very beautifully shown in the case of Toxopneustes
by Selenka (fig. 6), or they admit (?) processes of the follicular epithelial
cells (Vertebrata). Their presence is in fact probably caused by the existence
of such processes, which prevent the continuous deposition of the
membrane. The term z o n a r a d i a t a will be applied to perforated
membranes of this kind. Two vitelline membranes, one perforated and the
other homogeneous, may coexist at the same time, e.g. Sipunculida,
Vertebrata. (Fig. 7.)

Fig. 7. Section through a small part of the surface of an ovum of an immature female
of Scyllium Canicula.

fe. Follicular epithelium. vt. Vitelline membrane. Zn. Zona radiata. yk. Yolk with protoplasmic
network.

The chorion is often ornamented with various processes, etc. It is in many
cases doubtful whether a particular membrane is a chorion or a vitelline
membrane.
All the membranes which surround the ovum may be provided with a
special aperture known as the micropyle. A micropyle is by no means found
in the majority of types, and there is no homology between the various
apertures so named. Micropyles have two functions, either to assist in the
nutrition of the ovum during its development, or (2) to permit the entrance
of the spermatozoa. The two functions may in some cases coexist.
Micropyles of the first class are developed at the point of attachment of the
ovum to the wall of the ovary or to its follicle. Good examples of this kind
of micropyle are afforded by the Lamellibranchiata (fig. 12), Holothuria,

and many Annelida (Polynoe, etc.). The micropyle of the Lamellibranchiata
(p. 37) probably serves also to admit the spermatozoa. The second type of
micropyle is found in many Insecta, Teleostei, etc.

General Bibliography of the Ovum.
(1) Ed. van Beneden. “Recherches sur la composition et la signification de l’œuf,” etc. Mém. cour. d.
l’Acad. roy. des Sciences de Belgique, Vol. XXXIV. 1870.
(2) R. Leuckart. Artikel “Zeugung,” R. Wagner’s Handwörterbuch d. Physiologie, Vol. IV. 1853.
(3) Fr. Leydig. “Die Dotterfurchung nach ihrem Vorkommen in d. Thierwelt u. n. ihrer Bedeutung.”
Oken, Isis, 1848.
(4) Ludwig. “Ueber d. Eibildung im Thierreiche.” Arbeiten a. d. zool.-zoot. Institut Würzburg, Vol. I.
1874[15].
(5) Allen Thomson. Article “Ovum” in Todd’s Cyclopædia of Anatomy and Physiology, Vol. V. 1859.
(6) W. Waldeyer. Eierstock u. Ei. Leipzig, 1870.

Special History of the Ovum in different types.
Cœlenterata.
(7) Ed. van Beneden. “De la distinction originelle d. testicule et de l’ovaire.” Bull. Acad. roy.
Belgique, 3e série, Vol. XXXVII. 1874.
(8) R. and O. Hertwig. Der Organismus d. Medusen. Jena, 1878.
(9) N. Kleinenberg. Hydra. Leipzig, 1872.

Amongst the Cœlenterata the ova are developed in imperfectly specialized
organs, which are situated in various parts of the body, for the most part in
the space between the epiblast and the hypoblast.
In Hydra the locality where the ova are developed only becomes specialized
at the time when an ovum is about to be formed. At one or more points the
interstitial cells of the epiblast increase in number and form a protuberance
of germinal cells, which may be called the ovary. In this ovary a single
ovum is formed by the special growth of one cell. (Kleinenberg, No. 9.) In
the free and attached gonophores of Hydrozoa, the ova appear either around
the walls of the stomach, or the radial canals, or around other parts of the
gastro-vascular canals.

Fig. 8. Ripe Ovum Of Epibulia aurantiaca. The Germinal Vesicle has become invisible
without reagents.

Copied from Metschnikoff, “Entwicklung der Siphonophoren.” Zeitschrift f. wiss. Zool., Vol.
XXIV. 1874.

p.d. Peripheral layer of denser protoplasm. p.m. Central area consisting of a protoplasmic
meshwork.

Their close relations to the gastrovascular canals are probably determined
by the greater nutritive facilities thereby afforded. (Hertwig, No. 8.)
In the permanent Medusa forms the ova have similar relations to the gastro-
vascular system. Amongst the Actinozoa the ova are usually developed
between the epiblast and the hypoblast in the walls of the gastric
mesenteries. Amongst the Ctenophora the ova are situated in close relation
with the peripheral canals of the gastro-vascular system, which run along
the bases of the ciliated bands. There are many examples amongst the
Cœlenterata of ova which retain in their mature state the very simple
constitution which has been described as characteristic of all young ova;
and which are, when laid, absolutely without any trace of a vitelline
membrane or chorion. In many other cases both amongst the Medusæ, the
Siphonophora, and the Ctenophora, the ripe egg exhibits a distinction into
two parts. The outer part is composed of a dense protoplasm, while the
interior is composed of a network or more properly a spongework of
protoplasm enclosing in its meshes a more fluid substance. (Fig. 8.)

In some cases the ovum while still retaining the constitution last described becomes invested by a
very delicate membrane. Such is the constitution of the ripe ovum of Hippopodius gleba amongst the
Siphonophora[16] and of the eggs of Geryonia amongst the permanent Medusæ[17]. The ripe eggs of
the Ctenophora usually present a similar structure[18]. After being laid they are found to be invested
by a delicate membrane separated by a space filled with fluid from the body of the ovum. The latter
is composed of two layers, an outer one of finely granular protoplasm and an inner layer consisting of
a protoplasmic spongework containing in its meshes irregular spheres. These latter are stated by
Agassiz to be of a fatty nature, and it is probable that in most cases where a protoplasmic network is
present, this alone constitutes the active protoplasm and that the substance which fills up its meshes
is to be looked on as a form of food-yolk or deutoplasm, though it appears sometimes to have the
power of assimilating the firmer yolk particles.

The membrane which invests the ovum of many of the Cœlenterata is
probably a vitelline membrane.
The ova of the Hydrozoa take their origin, in most groups at any rate[19],
from the deeper layer of the epiblast (interstitial layer of Kleinenberg). The
interstitial cells in the ovarian region form primary germinal cells, and by
an excess of nutrition certain of them outstrip their fellows and become
young ova. Such ova differ from the full-grown ova already described,
mainly in the fact that they have a proportionately smaller amount of
protoplasm round the germinal vesicle. They grow to a considerable extent
at the expense of germinal cells which do not become converted into ova.
The ova of many Cœlenterata undergo changes of a more complicated kind
before attaining their full development. Of these ova that of Hydra may be
taken as the type. The ovary of Hydra (Kleinenberg, No. 9) is constituted of
angular flattish germinal cells of which no single one can be at first
distinguished from the remainder. As growth proceeds one of the cells
occupying a central position becomes distinguished from the remaining
cells by its greater size, and wedge-like shape. It constitutes the single
ovum of the ovary. After it has become prominent it grows rapidly in size,
and throws out irregular processes. The germinal vesicle, which for a
considerable time remains unaltered, also at length begins to grow; and the
sharply defined germinal spot which it contains after reaching a certain size
completely vanishes. After the atrophy of the germinal spot, there appears
in the middle of the ovum a number of roundish yolk granules.
The shape of the ovum becomes more irregular, and chlorophyll granules,
in addition to the yolk granules, make their appearance in it. A fresh
germinal spot of circular form also arises in the germinal vesicle.

Protoplasmic processes are next thrown out in all directions, giving to the
ovum a marvellous amœboid character. (Fig. 4.) The amœboid form of the
ovum serves no doubt to give it a larger surface for nutrition. Coincidently
with the assumption of an amœboid form there appear in the ovum a great
number of peculiar bodies. They are vesicles with a thick wall bearing a
conical projection into the interior which is filled with fluid. (Fig. 4B.)
These bodies are formed directly from the protoplasm of the ovum, and are
to be compared both morphologically and physiologically with the yolk-
spherules of such an ovum as that of the Bird. They are called pseudocells
by Kleinenberg, and are found with slightly varying characters in many ova
of the Hydrozoa.
They first appear as small highly refracting granules; in these a cavity is formed which is at first
central but is eventually pushed to one side by the formation of a conical projection from the wall of
the vesicle.

After the growth of the ovum is completed the amœboid processes
gradually withdraw themselves, and the ovum assumes a spherical form;
still however continuing to be invested by the remaining cells of the ovary.
It is important to notice that the egg of Hydra retains throughout its whole
development the characters of a single cell, and that the pseudocells and
other structures which make their appearance in it are not derived from
without, and supply not the slightest ground for regarding the ovum as a
structure compounded of more than one cell.
The development of the ova of the Tubularidæ, which has been supposed by
many investigators to present very special peculiarities, takes place on
essentially the same type as that of Hydra, but the germinal vesicle remains
permanently very small and difficult to observe. The mode of nutrition of
the ovum may be very instructively studied in this type. The process is one
of actual feeding, much as an Amœba might feed on other organisms.
Adjoining one of the large ova of the ovary there may be seen a number of
small germinal cells. (Fig. 3.) The boundary between these cells and the
ovum is indistinct. Just beyond the edge of the ovum the small cells have
begun to undergo retrogressive changes; while at a little distance from the
ovum they are quite normal (g.c.)[20].

Platyelminthes.

(10) P. Hallez. Contributions à l’Histoire naturelle des Turbellariés. Lille, 1879.
(11) S. Max Schultze. Beiträge z. Naturgeschichte d. Turbellarien. Greifswald, 1851.
(12) C. Th. von Siebold. “Helminthologische Beiträge.” Müller’s Archiv, 1836.
(13) C. Th. von Siebold. Lehrbuch d. vergleich. Anat. d. wirbellosen Thiere. Berlin, 1848.
(14) E. Zeller. “Weitere Beiträge z. Kenntniss d. Polystomen.” Zeit. f. wiss. Zool., Bd. XXVII. 1876.
[Vide also Ed. van Beneden] (No. 1).

This group, under which I include the Trematodes, Cestodes, Turbellarians
and Nemertines, has played an important part in all controversies relating to
the nature and composition of the ovum. The peculiarity in the development
of the ovum in most members of this group consists in the fact that two
organs assist in forming what is usually spoken of as the ovum. One of
these is known as the ovary proper, and the other as the vitellarium or yolk-
gland. In the sequel the term ovum will be restricted to the product of the
first of these organs. In Trematodes the ovary forms an unpaired organ
directly continuous with an oviduct into which there open the ducts from
paired yolk-glands.
The ovary has a sack-like form and contains in some instances a central
lumen (Polystomum integerrimum). At the blind end of the organ is placed
the germinal tissue. This part is, according to the accounts of the majority of
investigators, formed of a polynuclear mass of protoplasm not divided into
distinct cells. Whether it is really formed of undivided protoplasm or not, it
is quite certain that a little lower down in the organ distinct cells are found,
which have been segmented off from the above mass, and are formed of a
large nucleus and nucleolus, surrounded by a delicate layer of protoplasm.
These cells are the young ova. They usually assume a more or less angular
form from mutual pressure, and, in the cases where the ovary has a lumen,
constitute a kind of epithelial lining for the ovarian tube. They become
successively larger in passing down the ovary, and, though in most cases
naked, are in some instances (Polystomum integerrimum) invested by a
delicate vitelline membrane. Eventually the ova pass into the oviduct and
become free and at the same time assume a spherical form.
In the oviduct the ovum receives somewhat remarkable investing structures,
derived from the organ before spoken of as the yolk-gland. The yolk-gland
consists of a number of small vesicles, each provided with a special duct,
connected with the main duct of the gland. Each vesicle is lined by an
epithelium of cells provided with doubly contoured membranes, and
containing nuclei.

As the yolk cells grow older refracting spherules become deposited in their
protoplasm, which either completely hide the nucleus, or render it very
difficult to see. In the majority of cases the entire cells forming the lining of
the vesicles constitute the secretion of the yolk-gland. They invest the
ovum, and around them is formed a shell or membrane. In some cases (e.g.
Polystomum integerrimum) the yolk cells retain their cellular character and
vitality till the embryo is far developed. In other cases they lose their
membrane and nucleus shortly after the formation of the egg-shell, and
break up into a fluid, holding in suspension a number of yolk granules. A
partial disorganisation of the yolk cells can also take place before they
surround the ovum; while in some species of Distomum they completely
break up before leaving the yolk-gland.

Fig. 9. Generative system of Vortex viridis. (From Gegenbaur, after Max Schultze.)
t. Testis. v.d. Vasa differentia. v.s. Seminal vesicle. p. Penis. u. Uterus. o. Ovary. v. Vagina. g.v.
Yolk-glands. r.s. Receptaculum seminis.

There is thus a complete series of gradations between the investment of the
ovum by a number of distinct cells, and its investment by a layer of fluid
containing yolk-spherules in suspension. In neither the one case nor the
other do the investing structures take any share in the direct formation of
the embryo from the ovum. Physiologically speaking they play the same
part as the white in the fowl’s egg.
The egg-shell, which is usually formed by a secretion of a special shell-gland opening into the
oviduct, exhibits one or two peculiarities in the different species of Trematodes. In Amphistomum
subclavatum it presents at one extremity a thickened area, which is pierced by a narrow micropyle. In
other cases one extremity of the egg-shell is produced into a long process, and sometimes even both
extremities are armed in this way. Opercula and other types of armature are also found in different
forms.
The mode of development of the ovum in Cestodes is very nearly the same as in Trematodes.
The ovum becomes enveloped in the usual secretion of the yolk-gland; and an egg-shell is always
formed by the secretion of a special shell-gland.

Amongst the Turbellarians and Nemertines, there are greater variations in
the arrangement of the female generative glands, than in the preceding
types. In most of the Rhabdocœla and fresh-water Dendrocœla these organs
resemble in their fundamental characters those of the Trematodes and
Cestodes. There are present a paired or single ovary and a paired yolk-
gland. The general arrangement of the organs is shewn in fig. 9.
The blind end of the ovaries is usually (Ed. van Beneden, etc.) stated to be
formed of a polynuclear protoplasmic basis, but Hallez (No. 10) has
recently insisted that, even at the extreme end of the ovary, the germinal
cells are quite distinct, and not confounded together.
With one or two exceptions the yolk cells secreted by the vitellarium retain
their vitality till they are swallowed by the embryo, after the development
of its mouth. The few not so swallowed become disintegrated. They are
granular nucleated cells, and, as was first shewn by von Siebold, are
remarkable for exhibiting spontaneous amœboid movements.
Very important light on the nature of the vitellarium is afforded by the
structure of the generative organs in Prorhyncus and Macrostomum.
In Prorhyncus there is no separate vitellarium, but the lower part of the
ovarian tube functionally and morphologically replaces it. The ovum
becomes surrounded by yolk cells, which according to Hallez (No. 10)

retain their vitality for a long time. According to Ed. van Beneden yolk-
spherules are formed in the protoplasm of the ovum itself, in addition to and
independently of the surrounding yolk cells. In Convoluta paradoxa a
special vitellarium is stated to be absent; though a deposit of yolk is formed
round the ovum (Claparède).
In Macrostomum again the yolk-glands are at most represented by a lower
specialized part of the ovarian tube. The ova in passing down become filled
with yolk-spherules. According to Ed. van Beneden these spherules are
formed in the protoplasm of the ovum itself; but this is explicitly denied by
Hallez, who finds that they are formed from the lining cells of the ovarian
tube, which, instead of retaining their vitality as in Prorhyncus, break up
and form a granular mass which is absorbed by the protoplasm of the ovum.
In Prostomum caledonicum (Ed. van Beneden) the generative organs are
formed on the same plan as in other Rhabdocœla, but the cells which form
the yolk-gland give rise to yolk particles which enter the ovum, instead of
to a layer of yolk cells surrounding the ovum.
Amongst the marine dendrocœlous Turbellarians the ova are formed in separate sacks widely
distributed in the parenchyma of the body between the alimentary diverticula. In these the ova
undergo their complete development, without the intervention of yolk-glands.
The ovaries of the Nemertines more nearly resemble those of the marine Dendrocœla than those of
the Rhabdocœla. They consist of a series of sacks situated on the two sides of the body between the
prolongations of the digestive canal. The eggs are developed in these sacks in a perfectly normal
manner, and in many cases become filled with yolk-spherules which arise as differentiations of the
protoplasm of the ovum. The protecting membranes of the ova have not been accurately studied. In
some cases[21] two membranes are present, an internal and an external. The former, immediately
investing the vitellus, is very delicate: the external one is thicker and hyaline.

The constitution of the female generative organs of the Trematodes was first
clearly ascertained by von Siebold (No. 12). He originally, though not very
confidently, propounded the view that the germinal vesicles alone were
formed in the ovary and that the protoplasm of the ovum was supplied by
the yolk-gland. This view has long been abandoned, and von Siebold (No.
13) himself was the first to recognize that true ova with a protoplasmic
body containing a germinal vesicle and germinal spot were formed in the
ovary. The Trematodes have however not ceased to play an important part
in forming the current views upon the development of ova, and have quite

recently served Ed. van Beneden as his type in exposing his general view
upon this subject.
His view consists fundamentally in regarding the secretion of the yolk-glands, which in most cases
merely invests the ovum, as homologous with the yolk-spherules which fill the protoplasm of many
eggs; and he considers the part of the ovary where in most forms the ova receive their supply of yolk
particles, as equivalent to the vitellarium of the Platyelminthes. He further appears to regard the
primitive state as that exemplified in Trematodes, Cestodes, etc., and holds that the ovarian types
characteristic of other forms are secondarily derived from this, by the coalescence of the primitively
distinct vitellarium with the ovary proper.
This appears to me a case of putting the cart before the horse. To my mind the vitellarium is to be
regarded, as has already been suggested by Gegenbaur, Hallez, etc. as a special differentiation of the
primitively simple ovarian tube, and the instances Of Macrostomum and Prorhyncus just cited appear
to me to indicate some of the steps in this differentiation. In Macrostomum the cells of the lower part
of the oviduct simply supply a kind of nutriment to the ovum in the form of granular yolk particles,
while in Prorhyncus the yolk cells of the lower part of the ovarian tube form a complete investment
of independent cells for the ovum. If this lower part of the ovarian tube were to grow out as a special
diverticulum we should have produced a normal vitellarium. But even with the above modification
the theory of van Beneden appears to me not completely satisfactory. The view that the yolk-
spherules are of the same nature as the yolk cells is mainly supported by the case of Prostomum
caledonicum, where the vitellarium produces the yolk particles which fill the ovum. The cases Of
Prorhyncus and Macrostomum give a different complexion to that of Prostomum caledonicum. From
the first of these especially it appears that, even when normal yolk cells surround the ovum, yolk
particles can be deposited independently in the protoplasm of the ovum.

The most probable view of the nature of the vitellarium is that of
Gegenbaur, Hallez, etc., according to which it is to be regarded as a
specially modified part of the ovarian tube. On this view the nature and
function of the yolk cells admit of a fairly simple explanation. They are to
be regarded as primary germinal cells like those in the ovaries of Hydra,
Tubularia, etc., which do not become converted into ova. Like these cells
they may in some instances, Macrostomum, Prostomum, etc., serve directly
in the nutrition of the ovum. In other cases they retain their independence
and serve for the late nutrition of the embryo. In both instances they retain
the faculty, normally possessed by ova, of forming yolk particles in their
protoplasm.

Echinodermata.
(15) C. K. Hoffmann. “Zur Anatomie d. Echiniden u. Spatangen.” Niederländisch. Archiv f.
Zoologie, Vol. I. 1871.
(16) C. K. Hoffmann. “Zur Anatomie d. Asteriden.” Niederländisch. Archiv f. Zoologie, Vol. II.
1873.
(17) H. Ludwig. “Beiträge zur Anat. d. Crinoiden.” Zeit. f. wiss. Zool., Vol. XXVIII. 1877.

(18) Joh. Müller. “Ueber d. Canal in d. Eiern d. Holothurien.” Müller’s Archiv, 1854.
(19) C. Semper. Holothurien. Leipzig, 1868.
(20) E. Selenka. Befruchtung d. Eies v. Toxopneustes variegatus, 1878.
[Vide also Ludwig (No. 4), etc.]

The eggs of the Echinodermata present in their development certain points
of interest.
The ovaries themselves are usually surrounded by a special vascular
dilatation. In the Asteroidea, the Echinoidea, and the Holothuroidea the
organs have the form of sacks; specially surrounded in the two former
groups, and probably the latter, by a vascular sinus formed as a dilatation of
one of the generative vessels. In the Crinoids they have the form of a
hollow rachis completely surrounded by a blood-vessel. (Fig. 11, b.) The
proximity of the ovaries (generative organs) to the vascular system in these
forms has clearly the same physiological significance as the proximity of
the ovaries (generative organs) to the radial vessels in the Cœlenterata.
In the Asteroidea, the Echinoidea and the Holothuroidea the ovaries have
the form of sacks lined by an epithelium of germinal cells, and the ova are
formed by the enlargement of these cells, which, when they have reached a
certain size, become detached from the walls, and fall into the cavity of the
ovarian sack. In Toxopneustes (Selenka) and very probably in other forms
only a few of the epithelial cells undergo conversion into ova: the remainder
undergo repeated division, and, as in so many other cases, are eventually
employed in the nutrition of the true ova. In the nearly ripe ova of Asterias
Fol has described a flattened follicular epithelium the origin of which is
unknown.

Fig. 10. Ovum of Toxopneustes variegatus with the pseudopodia-like projections of the
protoplasm penetrating the zona radiata (zr). (After Selenka.)

In Holothuria (Semper) a further differentiation of the germinal cells, not
destined to become ova, takes place. They surround the enlarged cell which
forms the true ovum, for which they constitute a kind of follicular capsule.
This capsule is attached by a stalk to the walls of the ovary, and the ovum
lies freely in it except for an area nearly opposite its (the capsule’s) point of
attachment, where the ovum adheres to the wall of the capsule.
Subsequently the follicle cells which form the capsule fuse together, and
form a definite membrane in which only the nuclei remain distinct. Within
the membranous capsule there is formed for the ovum an albuminous zona
radiata. At the point where the ovum is attached to its capsule this
membrane cannot be developed, and therefore remains incomplete. The
perforation so formed, becomes the micropyle of the Holothurian egg,
which was first discovered by Joh. Müller. The albuminous membrane just
described for Holothurians is also found in Asteroids (fig. 5) and Echinoids.
In these groups there is no proper micropyle, though in Ophiothrix a
nutritive passage perforates the membrane at the attachment of the ovum
before the period when the ovum becomes free (Ludwig). The formation of
the zona radiata has been studied by Selenka. It is secreted by the
protoplasm of the ovum, and has a gelatinous consistency, and after it is
formed the peripheral layer of the protoplasm of the ovum sends out
through it pseudopodia-like processes to absorb nutriment from without.
These processes are at first large and irregular, but soon become finer and

finer (fig. 10), and acquire a regular radiating arrangement. They are
withdrawn when the ovum is ripe, but they nevertheless give rise to the
finely radiated appearance of the membrane, the radii being in reality
delicate pores.

Fig. 11. Transverse section through the pinna of a sexually mature Comatula. (From
Gegenbaur, after Ludwig.)
p. Tentacle. g. Lumen of genital rachis. w. Water-vascular vessel. n. Nerve cord. b. Blood-
vessel on nerve cord and round genital rachis. cg. Genital canal. cd. Dorsal section of the body
cavity. cv. Ventral section of body cavity.

In the Crinoids the generative rachis consists of a tube, the epithelium of
which is formed of the primary germinal cells. (Fig. 11.) While some of
these cells enlarge and become ova, the remainder supply the elements for a
follicular epithelium, which is established round the ova, exactly as in
Holothurians.

Mollusca.

Lamellibranchiata.
(21) H. Lacaze-Duthiers. “Organes génitaux des Acéphales Lamellibranches.” Ann. Sci. Nat., 4me
série, Vol. II. 1854.
(22) W. Flemming. “Ueb. d. er. Entwick. am Ei d. Teichmuschel.” Archiv f. mikr. Anat., Vol. X. 1874.
(23) W. Flemming. “Studien üb. d. Entwick. d. Najaden.” Sitz. d. k. Akad. Wiss. Wien, Vol. LXXI.
1875.
(24) Th. von Hessling. “Einige Bemerkungen, etc.” Zeit. f. wiss. Zool., Bd. V. 1854.
(25) H. von Jhering. “Zur Kenntniss d. Eibildung bei d. Muscheln.” Zeit. f. wiss. Zool., Vol. XXIX.
1877.
(26) Keber. De Introitu Spermatozoorum in ovula, etc. Königsberg, 1853.
(27) Fr. Leydig. “Kleinere Mittheilung etc.” Müller’s Archiv, 1854.

Gasteropoda.
(28) C. Semper. “Beiträge z. Anat. u. Physiol. d. Pulmonaten.” Zeit. f. wiss. Zool., Vol. VIII. 1857.
(29) H. Eisig. “Beiträge z. Anat. u. Entwick. d. Pulmonaten.” Zeit. f. wiss. Zool., Vol. XIX. 1869.
(30) Fr. Leydig. “Ueb. Paludina vivipara.” Zeit. f. wiss. Zool., Vol. II. 1850.

Cephalopoda.
(31) Al. Kölliker. Entwicklungsgeschichte d. Cephalopoden. Zurich, 1844.
(32) E. R. Lankester. “On the developmental History of the Mollusca.” Phil. Trans., 1875.

Lamellibranchiata.
The ova of the Lamellibranchiata present several points of interest. They are
developed in pouches of the ovary which are lined by a flattened germinal
epithelium, or sometimes (?) a syncytium. Some of the cells of this
epithelium enlarge and become ova, but remain attached to the walls of
their pouches by protoplasmic stalks. Round the ovum there appears in
some forms (Anodon, Unio) a delicate vitelline membrane, which is
incomplete at the protoplasmic stalk, and is therefore perforated by an
aperture which forms the micropyle. (Fig. 12.) As the ovum becomes ripe a
large space filled with albuminous fluid becomes established between the
ovum and its membrane, but the ovum remains attached to the membrane at
the micropyle. In Scrobicularia (von Jhering, No. 25) the membrane round

the ovum appears from the first as an albuminous layer, the outermost
stratum of which becomes subsequently hardened as the vitelline
membrane. In this form also the protoplasmic stalk becomes, in pouches
largely filled with ova, extremely long. The ova become eventually
detached by the stalk rupturing, and the portion of it which remains attached
to the vitelline membrane falling off. The function of the stalk and of the
micropyle during the development of the ovum is undoubtedly a nutritive
one.
In Anodon and Unio yolk granules similar to those deposited in the
protoplasm of the ovum are also found in the epithelial cells of the ovarian
pouches (Flemming, 22), and there can be but little doubt that they are
directly transported from these cells into the ovum. These cells would seem
therefore to play much the same part as the yolk-glands of some
Turbellarians (Prostomum caledonicum). In Scrobicularia yolk granules are
not found in the epithelium of the pouches, but are contained in the dilated
disc by which the ovum is attached to the wall of its pouch, as well as in the
ovum itself.

Fig. 12. Medium-sized ovum of Anodonta complanata. (After Flemming.)
mp. micropyle. gs. germinal spot.

On the ovum becoming detached the micropyle still remains as an aperture,
which probably has the function of admitting the spermatozoa.

The shape and form of the micropyle vary greatly. In Anodon and Unio it is a projecting trumpet-
shaped structure, which after fertilization becomes shortened and reduced to a mere aperture which is
finally stopped up. (Fig. 12.)
In other forms it is simply a perforation in the vitelline membrane which is sometimes very large. In
a species of Arca, which I had an opportunity of observing at Valparaizo, it was equal to nearly the
circumference of the ovum.

The eggs of the Lamellibranchiata are not only remarkable in the possession
of a micropyle, but in certain peculiarities of the yolk and of the germinal
vesicle.
In the fresh-water mussels there is usually found in young and medium-
sized ova a peculiar lens-shaped body—Keber’s corpuscle—which is
placed immediately internal to the micropyle. It is probably in some way
connected with the nutrition of the ovum, though the fact that it is not
always present shews that it cannot be of great importance.
A dark body found by von Jhering in the neighbourhood of the germinal
vesicle in the ripe ovum of Scrobicularia is probably of a similar nature to
Keber’s corpuscle. Both bodies may be placed in the same category as the
so-called yolk nucleus of the spider’s and frog’s ova.
In all except the youngest ova of Anodon and Unio the germinal spot is
composed of two nearly complete spheres united together for a small part of
their circumference. (Fig. 12, gs.) The smaller of these has a higher
refractive index than the larger, and often contains a vacuole: the two parts
together appear to be the separated components (though not by simple
division) of the primitive nucleolus. A nucleolus of this character is not
universal amongst Lamellibranchiata, but a similar separation of the
constituents of the germinal spot has been found by Flemming in
Tichogonia, in which however the more highly refracting body envelopes
part of the less highly refracting body in a cap-like fashion.

Gasteropoda.
The ova of the Gasteropoda are developed, like those of the
Lamellibranchiata, from the epithelial cells of the ovarian acini or pouches.
In the hermaphrodite forms both ova and spermatozoa are produced in the
same pouches (fig. 13), some of the epithelial cells becoming ova and

others spermatozoa. The ova are usually formed in the wall of the pouch,
and the spermatozoa internally (Pulmonata) (fig. 13 A), or a further
differentiation of parts may take place (fig.13 B). The ova of Gasteropods
are exceptional in the fact that a vitelline membrane is rarely or never
developed around them. The ovum in its passage to the exterior becomes
enclosed in a secretion of the albuminous gland, which hardens externally
to form a special membrane.

Fig. 13. Follicles of the hermaphrodite glands of Gasteropoda.
(From Gegenbaur.)
A. Of Helix hortensis. The ova (aa) are developed on the wall of the follicle, and the seminal
masses (b) internally.
B. Of Aeolidia. The seminal portion of a follicle is beset peripherally by ovarian saccules (a).
c. Common afferent duct.

Cephalopoda.
Lankester (No. 32) has brought out some very interesting points with
reference to the nutrition of the eggs of Sepia during their growth. The eggs
develop in connective-tissue pouches which early give rise to a double
pedunculated capsule of connective tissue. The cells of the inner layer of
this capsule soon assume an epithelial character, and become a definite
follicular epithelium, while between the two layers there penetrates a
network of vascular channels. The follicular epithelium becomes after the
establishment of these vascular channels folded in a most remarkable
manner. The folds, which are shewn in section in fig. 14, ic, project into and
nearly completely fill up the body of the ovum. An enormous increase is

thus effected in the nutritive surface exposed by the epithelium. Each fold is
thoroughly supplied with blood-vessels. The plications of the follicular
epithelium give rise to a basket-work tracery on the surface of the ovum.
During the stage when the follicular epithelium has the above structure, its
cells have a character similar to that of the goblet-cells of a mucous
membrane, and pour out their metamorphosed protoplasm into the body of
the ovum.

Fig. 14. Transverse section through an ovarian egg of Sepia. (Copied from Lankester.)
o.c. outer capsular membrane. i.c. inner capsular membrane with follicular epithelium. b.v.
blood-vessels in section between the outer and inner capsular membranes. c. vitellus.
The section shews the folds of the inner capsule with their epithelium, which penetrate into
the substance of the ovum for the purpose of supplying it with nourishment.

After the above mode of nutrition has gone on for a certain time a change
takes place, and the ridges gradually disappear. This is caused by the
epithelial cells passing off from the ridges into the protoplasm of the ovum;
and becoming assimilated, after retaining their individuality for a longer or
shorter period. When the absorption of the ridges is completed the surface
of the ovum assumes a perfectly regular outline. The capsule of the ovum
then bursts at the opposite pole to the peduncle, and the ovum falls into the
oviduct.

The ova of the Cephalopoda, like those of the Gasteropoda, are quite naked,
being without a vitelline membrane or chorion. The egg-capsule which is
formed for them in their passage down the oviduct is perforated in Sepia by
a micropylar aperture.

Chætopoda.
(33) Ed. Claparède. “Les Annelides Chætopodes d. Golfe de Naples.” Mém. d. l. Sociét. phys. et
d’hist. nat. de Genève 1868‑9 and 1870.
(34) E. Ehlers. Die Borstenwürmer nach system. und anat. Untersuchungen. Leipzig, 1864‑68.
(35) E. Selenka. “Das Gefäss-System d. Aphrodite aculeata.” Niederländisches Archiv f. Zool., Vol.
II. 1873.

The ova of the Chætopoda are in most cases developed from the special
tracts of the epithelial cells lining parts of the body cavity, which constitute
a germinal epithelium (fig. 15). Very frequently (Aphrodite, Arenicola), as
is so common in other types, these tracts of germinal cells surround the
blood-vessels. In some cases the germinal epithelium thickens to form a
compact organ, for which the outermost cells may form a more or less
definite membranous covering (Oligochæta, etc.). The ova are formed by
the enlargement, accompanied by other changes, of these germinal cells.
During their early development the ova are frequently surrounded by a
special capsule, which is often stalked, and provided at its attachment with
a large micropylar aperture. In Aphrodite and Polynoe this arrangement,
which is clearly connected with the nutrition of the ovum, is very easily
seen. The ovum is dehisced into the body cavity by the bursting of its
capsule or the rupture of the stalk. The capsule is always eventually thrown
off; but a vitelline membrane is frequently developed after the detachment
of the ovum into the body cavity. The vitelline membrane of Spio and other
Polychæta is provided with an equatorial ring of ampulliform vesicles.

Fig. 15. A Parapodium of Tomopteris.
(From Gegenbaur.)
o. Collection of germinal epithelial cells lining the body cavity.

Discophora.
(36) H. Dorner. “Ueber d. Gattung Branchiobdella.” Zeit. f. wiss. Zool., Vol. XV. 1865.
(37) R. Leuckart. Die menschlichen Parasiten.
(38) Fr. Leydig. “Zur Anatomie v. Piscicola geometrica, etc.” Zeit. f. wiss. Zool., Vol. I. 1849.
(39) C. O. Whitman. “Embryology of Clepsine.” Quart. J. of Micr. Sci., Vol. XVIII. 1878.

The ovary of the Discophora is formed of a mass of cells enveloped in a
membranous sack. In Branchiobdella there is placed in the central axis of
these cells a column of nucleated protoplasm from which the cells
themselves are budded off. The development of the ovum takes place by the
enlargement, etc. of one of the peripheral cells, which eventually bursts the
wall of the sack and is freely dehisced into the body cavity.
In most other Leeches (except Piscicola and its allies) there is found a more
specialized arrangement of the same nature as in Branchiobdella. There are
one or more coiled egg-strings which lie freely in a delicate sack continuous
with the oviduct. Each egg-string is formed of a central rachis and of a
peripheral layer of cells[22]. The ova are formed by the enlargement of the
peripheral cells accompanied by a deposition of food-yolk. Food-yolk
appears to be formed in the rachis even more energetically than in the
protoplasm of the ova. When ripe the ova fall into the ovarian sack.
In Piscicola the development of the ovum is somewhat peculiar but
resembles in certain respects that of Bonellia (p. 45). The ova are developed
from the primitive germinal cells which fill up the ovarian sack. The nuclei

in these cells increase in number, and a nucleated peripheral layer of each
cell becomes separated from the central part, which also contains nuclei.
This latter part next divides into numerous cells, of which one eventually
forms the ovum, and the remainder constitute a mass of cells adjoining it as
in Bonellia (fig. 16). This mass of cells eventually disappears, and is
probably employed in the nutrition of the ovum.
The ovaries of the Leech appear to belong to the tubular type in that the ova
are not formed from part of the epithelium lining the body cavity; but if, as
seems probable, the true affinities of the Leeches are with the Chætopoda,
the investment of the ovaries must be of a secondary nature. It should be
noted that the ova are not, as in the ordinary tubular ovary, developed from
the epithelium lining the ovarian tube.

Gephyrea.
(40) Keferstein u. Ehlers. Zoologische Beiträge. Leipzig, 1861.
(41) C. Semper. Holothurien, 1868, p. 145.
(42) J. W. Spengel. “Beiträge z. Kenntniss d. Gephyreen.” Beiträge a. d. zool. Station z. Neapel, Vol.
I. 1879.
(43) J. W. Spengel. “Anatomische Mittheilungen üb. Gephyreen.” Tagebl. d. Naturf. Vers. München,
1877.

In the Gephyrea, as in the Chætopoda, the ova are developed from the
lining cells of the peritoneum and frequently from the cells surrounding
parts of the vascular system (Bonellia, Thalassema). In many cases
(Sipunculus, Phascolosoma, Echiurus) the main growth of the ovum takes
place after it has been dehisced into the body cavity.
In Sipunculus the ova in the body cavity are surrounded by a follicle which
is thrown off before they become ripe.
Brandt denies the existence of this follicle or rather its cellular nature. Spengel’s (43) observations
are conclusive in favour of the correctness of the original interpretation Of Keferstein and Ehlers.
The follicles would seem to be formed after the ova have become free. In Phascolosoma there is no
follicle (Semper, Spengel).

In both Phascolosoma and Sipunculus a vitelline membrane with radial
pores—zona radiata—is formed, and in Phascolosoma the external part of
this is separated off as a structureless vitelline membrane. The formation of

both these membranes from the protoplasm of the ovum is rendered certain
in the latter case by the absence of a follicular epithelium.
Some interesting observations on the growth and origin of the ovum in
Bonellia have been made by Spengel.

Fig. 16. Follicle Of Bonellia at a medium stage of development. (After Spengel.)
ov. ovum. fe. flattened follicular epithelium.

The ova originate from certain cells (germinal cells) in the peritoneal
investment of the ventral vessel, overlying the nervous cord. These cells,
which are well marked off from the surrounding flattened peritoneal
elements, increase in number by division, and form small masses
surrounded by a follicle of peritoneal cells, and attached by a stalk to the
peritoneum. The central cell of each mass grows larger than the rest, which
arrange themselves in a columnar fashion round it; it is not, however,
destined to become the ovum. On the contrary certain of the other cells
adjoining the stalk grow larger, and finally one of these becomes
distinguished as the ovum by its greater size and the character of its
nucleus. The remainder of the larger cells become of the same size as their
neighbours. The ovum now becomes more or less separate from the mass of
germinal cells, rapidly grows in size, and soon forms the most considerable
constituent of the follicle (fig. 16, ov). The remaining germinal cells are
quite passive, and though, with the exception of the central cell, they do not
appear to atrophy, they soon constitute a relatively small prominence on the
surface of the ovum. By the rupture of the stalk the whole follicle becomes
eventually detached, and the further development of the ovum takes place
in the body cavity. A vitelline membrane is formed, and eventually the

ovum is taken into the oviduct (segmental organ). At this time or slightly
before, the follicle cells together with the germinal mass, which throughout
exhibits no signs of atrophy, become thrown off, and the ovum is left
invested in its vitelline membrane.

Nematoda.
(44) Ed. Claparède. De la formation et de la fécondation des œufs chez les Vers Nématodes. Genève,
1859.
(45) R. Leuckart. Die menschlichen Parasiten.
(46) H. Munk. “Ueb. Ei- u. Samenbildung u. Befruchtung b. d. Nematoden.” Zeit. f. wiss. Zool., Vol.
IX. 1858.
(47) H. Nelson. “On the reproduction of Ascaris mystax, etc.” Phil. Trans. 1852.
(48) A. Schneider. Monographie d. Nematoden. Berlin, 1866.

The female organs consist as a rule of two cæcal tubes which unite before
opening to the exterior. Each of these is divided into a vagina, uterus,
oviduct, and ovary. The ovary constitutes the blind end of the tube, and is
formed of a common protoplasmic column, holding a number of nuclei in
suspension. The protoplasm becomes cleft around the nuclei in the
uppermost part of the tube; the circumscription of the ova proceeds,
however, very gradually, and since it commences at the periphery of the
column the ova remain attached by stalks to a central axis with one end
free. In this way there is formed a rod-like structure known as the rachis,
which consists of a central axis with a series of half circumscribed ova
radiately arranged round it. In the lowest part of the ovary the ova become
completely isolated and form separate cells.
The protoplasm of the ova, which is clear in the terminal division of the
ovary, becomes in most forms filled lower down with yolk-spherules
secreted in the body of the ova. These commence to appear at the
uppermost extremity of the rachis.
In some instances, e.g. Cucullanus elegans, yolk-spherules are not formed. In the Oxyuridæ the ova
are directly segmented off from the terminal syncytium of protoplasm without the intervention of a
rachis; and are therefore formed in the same way as amongst Trematodes, etc.
The origin of the membrane around the ova of the Nematoda has been much disputed.
At the time when the ovum is detached from the rachis no membrane is present, but it nevertheless
appears from Schneider’s observations that the region at which it is detached is softer than other
parts, so that a kind of micropyle is here formed which disappears after impregnation. A delicate
vitelline membrane then appears, around which there is subsequently established an egg-shell, which

is usually stated to be formed as a secretion of the walls of the uterus; but Schneider and Leuckart
have given strong grounds for believing that it is really a further differentiation of the vitelline
membrane due to the activity of the protoplasm of the ovum. The originally single membrane
becomes as it thickens split into two layers. The outer of these forms the true egg-shell, and the
fertilization of the ovum appears to be a necessary prelude to its production. Round the egg-shell the
walls of the uterus often secrete a special albuminous covering.
The egg-shell exhibits in many cases peculiar sculpturings as well as terminal prolongations.

Insecta.
(49) A. Brandt. Ueber das Ei u. seine Bildungsstätte. Leipzig, 1878.
(50) T. H. Huxley. “On the agamic reproduction and morphology of Aphis.” Linnean Trans., Vol.
XXII. 1858. Vide also Manual of Invertebrated Animals, 1877.
(51) R. Leuckart. “Ueber die Micropyle u. den feinern Bau d. Schalenhaut bei den Insecteneiern.”
Müller’s Archiv, 1855.
(52) Fr. Leydig. Der Eierstock u. die Samentasche d. Insecten. Dresden, 1866.
(53) Lubbock. “The ova and pseudova of Insects.” Phil. Trans. 1859.
(54) Stein. Die weiblichen Geschlechtsorgane d. Käfer. Berlin, 1847.
[Conf. also Claus, Landois, Weismann, Ludwig (No. 4).]

The ovum of Insects has formed the subject of numerous investigations, and
has played an important part in the controversies on the nature of the ovum.
The ovaries are paired organs, rarely directly connected, each consisting of
more or fewer ovarian tubes which open into a common oviduct. The
oviducts unite into a vagina, usually provided with a spermatheca and
accessory glands, which need not be further alluded to. Each ovary is
invested by a peritoneal covering, which assumes various characters, and
either forms a loose network covering the whole or a special tunic round
each egg-tube. It is continuous with the general peritoneal investment. Each
ovarian tube (fig. 17) consists of three sections: (1) a terminal thread, (2)
the terminal chamber or germogen, (3) the egg-tube proper.

Fig. 17. A. Ovarian tube of the Flea, Pulex irritans. (From Gegenbaur, after Lubbock.)
o. ovum. g. germinal vesicle.
B. Ovarian tube of a Beetle, Carabus violaceus. (After Lubbock.)
o. ovarian segment, formed of an ovum a, and a mass of yolk cells, b.

The whole egg-tube is invested in a structureless tunica propria.
The terminal threads are fine prolongations of the ends of the egg-tubes usually continued close up to
the heart. At their extremities they frequently anastomose, or even unite into a common thread. In
some cases they are absent. They form either direct continuations of the germogen and have the same
histological structure, or in other cases are simply prolongations of the tunica propria, and serve as
ligaments.

The germogen usually consists of two parts: an upper, filled with nuclei
imbedded in protoplasm, and a lower, in which distinct cells have become
differentiated.
The lower part of the egg-tubes is filled with ova which advance in
development towards the oviduct, and lie in chambers more or less
distinctly constricted from each other. In these chambers there are in most
forms in addition to the true ova a certain number of nutritive cells. The true
egg-tubes are moreover lined by an epithelial layer which passes in and
forms more or less complete septa between the successive chambers. The
points which have been especially controverted are (1) the relation of the
ovum to the germogen, and (2) the relation of the nutritive or yolk cells to
the ovum. To the controversies on these points it will only be possible to
give a passing allusion.
As has been already hinted there are two distinct types of ovaries, viz. those
without the so-called nutritive or yolk cells and those with them[23].
The formation of the ovum is most simple in the type without yolk cells,
which will for that reason be first considered (fig. 17 A).
The germogen is constituted of a number of nuclei imbedded in a scanty
cementing protoplasm. In the lower part of the germogen the nuclei are
larger, and become separated off from the nucleated protoplasm above, as
distinct cells with a thin layer of protoplasm round the germinal vesicle.
These cells are the ova. As they pass down the egg-tube their protoplasm
increases in bulk, and they become isolated by ingrowths of the epithelial
cells the origin of which is still uncertain, which form round each ovum a
special follicle, so that the egg-tube is filled by a single row of ova each in
an epithelial follicle (fig. 17 A). The larger the ova the more columnar is the
epithelium of the follicle. As the oviductal extremity of the egg-tube is
approached the ova increase in size, and their protoplasm is more and more
filled with yolk particles.
In the lower part of the egg-tube the epithelium gives rise to a chorion.
The epithelium around each ovum has been spoken of as forming a follicle, and it is implied that the
epithelium round each ovum travels down the egg-tube with the ovum. It is however by no means
clear from the observations of the majority of writers that this is the case, and in fact the epithelium is

generally spoken of as if it were simply the epithelium of the egg-tube. In favour of the view here
adopted the following considerations may be urged.
Firstly, there is considerable evidence that the superficial layer of the germogen gives rise to the
epithelial cells, simultaneously with the formation of the ova from the deeper layers.
Secondly, the fact that the epithelium grows in between the separate ova appears to render it almost
certain that this part of the epithelium must travel down the egg-tubes with the ova.
Thirdly, the epithelium no doubt gives rise to the chorion, and considering the peculiar structure of
the chorion, this seems possible only on the view that the epithelium travels down the egg-tube with
the ova.
Fourthly, when, or even before, the egg is laid the epithelium undergoes atrophy, and the remains of it
have been compared to the corpora lutea.
If the view about the epithelium here adopted is correct, the epithelium without doubt corresponds to
the follicular epithelium of other ova, and has the same origin as the ova themselves.

The ovaries with yolk cells differ in appearance from those without, mainly
in each ovarian chamber of an egg-tube containing two elements, usually
more or less distinctly separated. These two elements are (1) at the lower
end of the chamber, the ovum, and (2) at the upper, large cells which
gradually disappear as the ovum grows larger (fig. 17 B).
The uppermost part of the egg-tube is formed, as in the previous type, by a
mass of nucleated protoplasm, but the germinal cells formed from it do not
all become ova. The germinal cells leave the germogen in batches, and in
each batch one of the cells may usually be distinguished from the very first
as the ovum; the remainder forming the nutritive cells. In the uppermost
part of the egg-tube the whole mass of each batch is very small, and the
successive batches are very imperfectly constricted from each other.
Gradually however both the nutritive cells and the ovum grow in size, and
then as a rule, the Diptera forming a marked exception, the chamber
containing a batch becomes constricted into an upper section with the
nutritive cells and a lower one with the ovum. The ovum in passing down
the tube becomes gradually invested by a layer of epithelial cells, which in
many cases pass in and partially separate the ovum from the nutritive cells.
The epithelium appears not unfrequently to be continued as a flat layer
between the nutritive cells and the wall of the egg-tube.
As was first shewn by Huxley and Lubbock, the protoplasm of the ovum is often continued up as a
solid cord, which terminates freely between the nutritive cells, and serves to bring to the ovum the
material elaborated by them. It is present in its most primitive form in the somewhat aberrant ovary
of Coccus. In this ovary the terminal chamber is filled with cells which are united to a central rachis,

as in Nematodes, and the prolongation from the ovum is continuous with this rachis. This cord is
known as the yolk-duct (Dottergang) by German writers. Although it is not generally present in a
distinct form, there is always a passage connecting the ovum and yolk cells, even when the follicular
epithelium grows in and nearly separates them.

The number of nutritive cells varies from two (one ?) to several dozen.
After they have reached a maximum they gradually atrophy, and are finally
absorbed without apparently fusing directly with the ovum. The two types
of insect ovaries appear fundamentally to differ in this. In the one type all
the germinal cells develop into ova; in the other the quantity is, so to speak,
sacrificed to the quality, and the majority of germinal cells are modified so
as to subserve the nutrition of the few. It is still undecided whether the yolk
cells absolutely elaborate yolk particles, or are merely conveyers of
nutriment to the ovum.
The egg membranes of Insects present many points of interest, which are
however for the most part beyond the scope of this work. There is always a
chorion formed as a cuticular deposit of the follicle cells, which is
frequently sculptured, finely perforated, etc., and is in many instances
provided with a micropyle, developed, according to Leydig, at the upper
end of the ovum.
Its development at this point appears to be due to the fact that the follicle is
here incomplete; so that the cuticular membrane deposited by it is also
incomplete.
A true vitelline membrane can in many instances be demonstrated (Donacia,
etc.).

Araneina.
(55) Victor Carus. “Ueb. d. Entwick. d. Spinneneies.” Zeit. f. wiss. Zool., Vol. II. 1850.
(56) v. Wittich. “Die Entstehung d. Arachnideneies im Eierstock, etc.” Müller’s Archiv. 1849.
[Conf. Leydig, Balbiani, Ludwig (No. 4), etc.]

The ova of many Araneina are remarkable for the presence in the ovum of
the so-called yolk-nucleus. The ova develop from the epithelial cells lining
the ovarian sack. Certain of these cells grow large and project outwards,
invested by the structureless membrane of the ovarian wall. The stalks of
projections so formed are turned towards the lumen of the ovary, and are

plugged with the epithelial cells which line the ovarian sack. When ripe, the
ova pass from their sacks into the cavity of the ovary. The yolk-nucleus,
which appears very early, is a solid body present in the protoplasm of the
ovum. It is not found in all genera of Araneina. At its full development it
exhibits in the fresh condition a granular structure, but very soon shews an
irregularly concentric stratification which becomes more marked on the
addition of reagents. According to Balbiani this stratification is confined to
the superficial layers, while internally there is a body with all the characters
of a cell. The yolk-nucleus is still found in the nearly ripe ovum, though it
always disappears before development commences. It is probably
connected with the nutrition of the ovum, though nothing is certainly
known about its function.

Crustacea.
(57) Aug. Weismann. “Ueb. d. Bildung von Wintereiern bei Leptodora hyalina.” Zeit. f. wiss. Zool.,
Vol. XXVII. 1876.
[For general literature vide Ludwig No. 4 and Ed. van Beneden, No. 1.]

Amongst the many interesting observations on the Crustacean ova I will
only allude to those of Weismann on the ova of Leptodora, a well-known
Cladoceran form.
The phenomena of the development of the ova in this form present a close
analogy with those in Insects.
The ovary is formed of (1) a germogen containing at its upper end nucleated
protoplasm and lower down germinal cells in groups of four; (2) of a
portion formed of successive chambers in each of which there is a row of
four germinal cells. Of the four cells only the third develops into an ovum;
the remainder are used as pabulum. This is the mode of development in the
summer. In the winter the sacrifice of a larger number of germinal cells is
required for the development of the ova; and an ovum is produced only in
the alternate chambers. In the chambers where an ovum will not be formed
an epithelial investment becomes first established round the four germinal
cells. The four cells then coalesce, and form a spherical ball of protoplasm
from which portions are budded off and absorbed by the investing epithelial
cells, which at the same time lose their nuclei. When the whole of the
central ball is thus absorbed by the epithelial cells, the latter become used

by the winter ovum as food. The winter ovum at its full development is
formed of a central mass of food-yolk and superficial layer of protoplasm.

Chordata.
Urochorda. (Tunicata.)
(58) A. Kowalevsky. “Weitere Studien ü. d. Entwicklung d. Ascidien.” Archiv f. mikr. Anat., Vol. VII.
1871.
(59) A. Kowalevsky. “Ueber Entwicklungsgeschichte d. Pyrosoma.” Arch. f. mikr. Anat., Vol. XI.
1875.
(60) Kupffer. “Stammverwandtschaft zwischen Ascidien u. Wirbelthieren.” Arch. f. mikr. Anat., Vol.
VI. 1870.
(61) Giard. “Études critiques des travaux, etc.” Archives Zool. expériment., Vol. I. 1872.
(62) C. Semper. “Ueber die Entstehung, etc.” Arbeiten a. d. zool.-zoot. Institut Würzburg, Bd. II.
1875.

Cephalochorda.
(63) P. Langerhans. “Z. Anatomie d. Amphioxus lanceolatus,” pp. 330‑3. Archiv f. mikr. Anat., Vol.
XII. 1876.

Craniata.
(64) F. M. Balfour. “On the structure and development of the Vertebrate Ovary.” Quart. J. of Micr.
Science, Vol. XVIII. 1878.
(65) Th. Eimer. “Untersuchungen ü. d. Eier d. Reptilien.” Archiv f. mikr. Anat., Vol. VIII. 1872.
(66) Pflüger. Die Eierstöcke d. Säugethiere u. d. Menschen. Leipzig, 1863.
(67) J. Foulis. “On the development of the ova and structure of the ovary in Man and other
Mammalia.” Quart. J. of Micr. Science, Vol. XVI. 1876.
(68) J. Foulis. “The development of the ova, etc.” Journal of Anat. and Phys., Vol. XIII. 1878‑9.
(69) C. Gegenbaur. “Ueb. d. Bau u. d. Entwicklung d. Wirbelthiereier mit partieller Dottertheilung.”
Müller’s Archiv, 1861.
(70) Alex. Götte. Entwicklungsgeschichte d. Unke. Leipzig, 1875.
(71) W. His. Untersuchungen üb. d. Ei u. d. Eientwicklung bei Knochenfischen. Leipzig, 1873.
(72) A. Kölliker. Entwicklungsgeschichte d. Menschen u. höherer Thiere. Leipzig, 1878.
(73) J. Müller. “Ueber d. zahlreichen Porenkanäle in d. Eikapsel d. Fische.” Müller’s Archiv, 1854.
(74) W. H. Ransom. “On the impregnation of the ovum in the Stickleback.” Pro. R. Society, Vol. VII.
1854.
(75) C. Semper. “Das Urogenitalsystem d. Plagiostomen, etc.” Arbeiten a. d. zool.-zoot. Instit.
Würzburg, Vol. II. 1875.
[Cf. Ludwig, No. 4, Ed. van Beneden, No. 1, Waldeyer, No. 6, &c. ]

There are some very obscure points connected with the growth of the ovum
of the Tunicata. When quite young the ovum is a naked cell with a central
nucleus containing a single large nucleolus. Around it is a flat follicular

epithelium enclosed in a m e m b r a n a p r o p r i a f o l l i c u l i . The
follicle cells soon become larger and give rise to an envelope round the egg
of the nature of a chorion. At the same time they frequently become cubical
or even columnar, and filled with numerous vacuoles.
During or after the completion of the above changes a number of bodies
usually spoken of as test-cells make their appearance in the superficial
protoplasm of the egg, which by the time the egg is ripe arrange themselves
in many species as a definite layer round the periphery of the ovum. These
bodies have received their name from the opinion, now known to be
erroneous (Hertwig and Semper), that they eventually migrated into the test
or mantle of the embryo which becomes developed round the ovum. By
Kowalevsky (No. 58) these bodies are regarded as true cells, and are
believed to be formed by some of the cells of the original follicular
epithelium making their way into the vitellus of the ovum and multiplying
there. By Kupffer (No. 60), and Giard (No. 61), and Fol, they are also
regarded as true cells but are believed to originate spontaneously in the
vitellus. Finally by Semper they are believed not to be cells, but to be
amœboid protoplasmic bodies which are pressed out from the vitellus under
the stimulus of the sea-water or otherwise.
They do not according to this author naturally appear till the ovum is quite ripe, though they can be
artificially produced at an earlier period by the action of reagents or sea-water. When produced in the
natural course of things the vitellus undergoes a contraction. They are without any apparent function,
and play no part in the embryonic development. Semper’s results are very peculiar, but owing to the
careful study which his paper displays they no doubt deserve attention. Further investigations are
however very desirable. Kowalevsky from his researches on Pyrosoma (No. 59) adheres to his first
opinion, though he abandons the view that these cells are connected with the formation of the test.

In the passage of the egg through the oviduct the vacuolated follicle cells
grow out into very peculiar long processes or villi. In Ascidia canina these
processes become as long as the whole diameter of the vitellus (Kupffer,
No. 60).
In Amphioxus and the Craniata the ova are developed as in the Chætopoda,
Gephyrea, etc., from specialized germinal cells of the peritoneal epithelium.
In Amphioxus the germinal epithelium which constitutes the essential part
of the ovary is divided into a number of distinct segments: in the Craniata
no such division is observable.

In young examples of Amphioxus the generative organs are in an indifferent
condition, and the two sexes cannot be distinguished. They form isolated
horse-shoe shaped masses of cells, which occupy a position at the base of
the myotomes, in the intervals between the successive segments; and extend
from the hinder end of the respiratory sack to the abdominal pore. They are
situated in the proper body cavity, and are surrounded by the peritoneal
membrane. Each generative mass is at first solid, and is formed of an outer
layer of more flattened cells and an inner mass of large rounded or
polygonal cells. In its interior there appears at a somewhat later period a
central cavity. After the cavity has appeared the sexes can be distinguished
by the different behaviour of the cells.
In all the Craniata, the ovary forms a paired ridge (unless single by abortion
or fusion) attached by a mesentery to the dorsal wall of a more or less
extended region of the abdominal cavity. This ridge is at first identical in
the two sexes, and arises at an early period of embryonic life. It is
essentially formed of a thickening of the peritoneal epithelium, and in
Osseous Fish, Ganoids (?) and Amphibia the ovary remains during
embryonic life nearly in this condition, though a small prominence of the
adjacent stroma also becomes formed. In other Craniata the ridge, though at
first in this condition, very soon becomes much more prominent, and is
formed of a central core of stroma enclosed in the germinal epithelium (fig.
18).

Fig. 18. Transverse section through the ovary of a young embryo of Scyllium canicula,
to shew the primitive germinal cells (po) lying in the germinal epithelium on the outer
side of the ovarian ridge.

The thickened germinal epithelium gives rise (in the case of the female) to
the ova and the follicular epithelium. Whether the genital ridge is provided
with a core of stroma or no, the germinal epithelium is always in contact on
one side with the stroma, from which it is at first separated by a well-
marked boundary line; but after a certain time there appear numerous
vascular ingrowths from the stroma, which penetrate through all parts of the
germinal epithelium, and break it up into a sponge-like structure formed of
trabeculæ of germinal epithelium interpenetrated by vascular strands of
stroma. The trabeculæ of the germinal epithelium form the egg-tubes of
Pflüger.
With reference to the distribution of the stroma in the germinal epithelium,
it may be said in a general way that there is a special layer close to the
surface of the ovary, which, after the formation of fresh ova has nearly
ceased, completely isolates a superficial layer of the germinal epithelium
from the deeper and major part of it. The superficial layer is frequently (but
erroneously) regarded as constituting the whole of the germinal epithelium.
The layer of stroma below the superficial epithelium forms in the
mammalian ovary the tunica albuginea. As the follicles are formed. in the
trabeculæ of germinal epithelium the stroma grows in around them, and
forms for each one of them a special tunic.
The adult ovaries differ in a corresponding manner to the embryonic genital
ridges as to the presence of a core of stroma. The ovaries which are without
such a core in the embryo, are also without it in the adult, and are formed of
a double layer of tissue entirely derived from the germinal epithelium with
its ingrowths of stroma, and composed, for the most part, of ova in all
stages of development. In the case of the other ovaries there is a hilus of
stroma—the zona vasculosa—internal to the egg-bearing region.
In Mammalia, proportionately to the ovary, the zona vasculosa is at a maximum, and in Birds and
Reptiles it is relatively far less developed. In these forms the germinal epithelium covers the whole
surface of the ovary. In Elasmobranchii the structure of the ovary is somewhat different, owing to the
presence in the ovarian ridge of a large quantity of a peculiar lymphatic tissue, which has no
homologue in the other ovaries; and still more to the fact that the true germinal epithelium is in most

forms entirely confined to the outer surface of the ovary, on which it forms a layer of thickened
epithelium in the embryo (fig. 17), and of ovigerous tissue in the adult.
In the ovary of Mammalia and Reptilia and possibly other forms there are present in the zona
vasculosa during embryonic life cords of epithelial tissue derived from the Malpighian bodies; these
cords have no function in the female, but in the male assist in forming the seminiferous tubules.

In considering the development of the ova it is again convenient to
distinguish between Amphioxus and the Craniata.
In Amphioxus the germinal cells destined to become ova are first
distinguished by the larger size of their germinal vesicles and by the
presence of certain refracting granules in their protoplasm. They
subsequently rapidly enlarge and form protuberances on the surface of the
ovary, which are enveloped for three-quarters of their circumference by the
flattened epithelioid cells of the peritoneal membrane, which thus form a
kind of follicle. As the ova become ripe yolk granules are deposited in their
protoplasm, first in the superficial layer and subsequently throughout. The
germinal vesicle also passes from the centre to the surface. A vitelline
membrane is formed when the ova are mature.
In the Craniata the ova are developed from the cells of the germinal
epithelium. In the types with larger ova (Teleostei, Elasmobranchii,
Amphibia, Reptilia, Aves), at a very early period, sometimes
(Elasmobranchii) even before the formation of the genital ridge, certain of
the cells which are destined to form ova become distinguished by their
greater size, and by the possession of an abundant clear protoplasm and a
large spherical granular nucleus. (Fig. 18, po.) Such special cells form
primitive germinal cells, and are common to both sexes.
For a considerable period after their first formation these cells remain
stationary in their development; but their number increases, partly, it
appears, by an addition of fresh ones, and partly by division. Owing to the
latter process the germinal cells come to form small masses or nests. The
following description of the further changes of these cells in the female
refers in the first instance to Elasmobranchii, but holds good in most
respects for other types as well.
It is convenient to distinguish two modes in which the primitive germinal
cells may become converted into permanent ova, though the morphological
difference between the two modes is of no great importance.

Fig. 19. Section through part of the germinal epithelium of the ovary of Scyllium at
the time when the primitive germinal cells are becoming converted into ova.

nn. Nests formed of agglomerated germinal cells. The nuclei of these cells are imbedded in
undivided protoplasm. do. developing ova. o. ovum with follicle. po. primitive germinal cell. dv.
blood-vessels.

In the first mode the protoplasm of all the cells forming a nest unites into a
single mass containing the nuclei of the previously independent ova (fig.
19, nn). The nuclei in the nest increase in number, probably by division, and
at the same time the nest itself increases in size. The nuclei while increasing
in number also undergo important changes. A segregation of their contents
takes place, and the granular part (nuclear substance) forms a mass close to
one side of the membrane of the nucleus, while the remainder of the
nucleus is filled with a clear fluid. The whole nucleus at the same time
increases somewhat in size. The granular mass gradually assumes a stellate
form, and finally becomes a beautiful reticulum, of the character so well
known in nuclei (fig. 19, do). Two or three special nucleoli are present, and
form the nodal points of the reticulum, while its meshes are filled up with
the clear fluid constituents of the nucleus. Not all the nuclei undergo the
above changes; but some of them stop short in their development, undergo
atrophy, and appear finally to be absorbed as pabulum by the protoplasm of
the nest. Such nuclei in a state of degeneration are shewn in fig. 19. Thus
only a few nuclei out of a nest undergo a complete development. At first the
protoplasm of the nest is clear and transparent, but as the nuclei undergo
their changes the protoplasm becomes more granular, and a specially large

quantity of granular protoplasm is generally present around the most
developed nuclei, and these with their protoplasm gradually become
constricted off from the nest, and constitute the permanent ova (fig. 19, do).
The relative number of ova which may develop from a single nest is subject
to great variation. The object of the whole occurrence of the fusion of
primitive ova and the subsequent atrophy of some of them is to ensure the
adequate nutrition of a certain number of them.
In the second and rarer mode of development of permanent ova from
primitive germinal cells, the nuclei and protoplasm undergo the same
changes as in the first mode, but the cells either remain isolated, and never
form part of a nest, or form part of a nest in which no fusion of protoplasm
takes place, and in which all the cells develop into permanent ova.
The isolated ova and nests are situated, during the whole of the above
changes, amongst the general undifferentiated cells of the germinal
epithelium, but as soon as a permanent ovum becomes formed the cells
adjoining it arrange themselves around it as a special layer, and so give rise
to the epithelium of the follicle (fig. 19, o). The growths of stroma into the
germinal epithelium appear shortly after the formation of the earlier
follicles.
Mammalia. The development of the ovary in Mammalia differs mainly
from that just described in that the formation of primitive germinal cells
from the indifferent cells of the germinal epithelium takes place at a
relatively much later period.
The stroma grows into the germinal epithelium while it is still formed of
rounded indifferent cells, and divides it into trabeculæ as described above.
At a later period a number of the cells in the deeper layer of the epithelium,
as well as certain cells in the superficial part, become primitive germinal
cells, while the remainder of the cells become smaller and are destined to
form the follicle cells.
The most conspicuous primitive germinal cells are situated in the
superficial layer of epithelium; and the primitive germinal cells in the
deeper layers of the germinal epithelium are not nearly so marked as in
most Craniata, so that it is difficult in some cases to be sure of their

destination till their nucleus commences to undergo its characteristic
metamorphosis.
The change of the primitive ova into permanent ova takes place in the same
manner in Mammals as in Elasmobranchii, except that the fusion of the
primitive ova into polynuclear masses is much rarer. The formation of the at
first quite simple follicles takes place while the ova are still aggregated in
large masses; and the first follicles are formed in the innermost part of the
germinal epithelium. Soon after their formation the follicles become
isolated by connective-tissue growths.

Post-embryonic development of the ova.
The ova of the Vertebrata differ greatly in size and structure. The
differences in size depend upon the quantity of the food-yolk. In the
Amphioxus and Mammalia, in which the ova are smallest, the
comparatively insignificant amount of food-yolk is distributed uniformly
through the ovum. A larger quantity of it is present in the ova of Amphibia,
Marsipobranchii and Teleostei, and it attains an immense development in
the ova of Elasmobranchii, Reptilia, and Aves.
The food-yolk originates from a differentiation of the protoplasm of the
egg. It arises as a number of small highly refracting particles in a stratum
slightly below the surface.
In the Mammalian ovum these particles spread through the protoplasm of the egg, but do not attain
any considerable development. In other forms the case is different. In Elasmobranch Fishes the
refracting particles appear to develop into vesicles, in the interior of which there arise solid oval or
even rectangular highly refracting bodies, in the substance of which a stratification may usually be
observed, which gives them an appearance not unlike that of striated muscle. In Teleostei the yolk
assumes very different characters in different cases. It is often formed of larger or smaller vesicles
containing in their interior other bodies. Stratified plates like those of Elasmobranchii are also not
uncommon. In the ripe ovum of Teleostei the food-yolk usually resolves itself into a large vitelline
sphere, which occupies the greater part of the ovum, and is formed of a highly refracting fluid
material which coagulates on the addition of water. It contains in many instances one or more highly
refracting bodies known as oil globules, and is invested by a granular protoplasmic layer continuous
with the germinal disc, in which a number of normal yolk-spherules are frequently present. In the
ovum of the Herring[24] no distinct investing protoplasmic layer or germinal disc is present till after
impregnation, but the ovum is formed of a superficial layer with minute yolk-spherules, and of a
central portion with larger yolk-spheres.
In Amphibia the yolk very often appears in the form of oval or quadrilateral plates. In Reptilia the
yolk-spherules are vesicles, somewhat similar to the white yolk-spheres of Aves, but as a rule without

the highly refracting spheres in their interior. The peculiar and complicated arrangement and structure
of the white and yellow yolk in Birds is fully described in the “Elements Of Embryology,” and it
need only be said that the yolk develops in Birds in the same manner as in other types, and that at
first all the yolk-spherules appear in the form of white yolk. The yellow yolk-spheres are a peculiar
modification of white yolk-spheres, formed comparatively late in the development of the egg (fig.
20).

Fig. 20. Yolk elements from the egg of the fowl.
A. Yellow yolk. B. White yolk.

In the eggs of many Amphibia a dark granular mass known as the yolk nucleus makes its appearance;
and is supposed, without any very clear evidence, to be related to the formation of the yolk.
A body in the form of a shell enclosing a dark nucleus, which is perhaps of the same nature, has been
described by Eimer in the Reptilian egg: it eventually resolves itself into a number Of angular
fragments. In Elasmobranchii a similar body is perhaps present.

The food-yolk just described is imbedded in the active protoplasmic portion
of the body of the ovum. In the case of the mammalian ovum the food-yolk
is fairly uniformly distributed, but in the case of all other craniate ova the
protoplasm of the ovum is especially concentrated at one pole, which is
known as the upper or animal pole, and the food-yolk is more especially
concentrated at the opposite pole. The Herring’s ovum forms an apparent
exception to this statement, in that the concentration of the protoplasm to
form the germinal disc does not take place till after impregnation. In
Amphibia the animal pole is mainly marked by the smaller size of the yolk-
spherules, but in most other forms a small portion of the ovum in the region
of the germinal vesicle is nearly free from yolk-spherules, and then forms a
more or less specialized part known as the germinal disc. In Aves, Reptilia,
and Elasmobranchii the germinal disc shades off insensibly into the yolk;
but in Teleostei it is more sharply marked off, and is continued more or less
completely round the periphery of the ovum. In ova with true germinal
discs it is the germinal disc alone which undergoes segmentation. The
protoplasm of vertebrate ova frequently exhibits a reticulate or sponge-like

structure (fig. 21) and the reticulum in many cases, e.g. Elasmobranchii and
Reptilia, serves to hold the yolk-spheres together. In the Tench it has been
observed by Bambeke to penetrate into the vitelline sphere.
In the ova of the Craniata the germinal vesicle is generally polynucleolar. In
Amphioxus and Petromyzon there is however but a single nucleolus, and in
Mammalia there is usually one special nucleolus and two or three accessory
ones. The opposite extreme is reached in many osseous fish where the
nucleoli are extremely numerous. The protoplasmic reticulum of the
embryonic germinal vesicle may in some instances be retained till the ovum
is nearly ripe, but usually assumes a very granular form. It is at first
connected with the nucleoli which form nodal points in it, but this relation
cannot always be detected in the later stages. A membrane, which in the
case of the larger ova becomes very thick, is always present round the
germinal vesicle. It is said to be perforated in some Reptilian ova (Eimer).
As to the position of the germinal vesicle, it is at first situated in the centre
of the ovum, but always eventually travels to the animal pole, and as the
egg becomes ripe undergoes changes which will be more especially detailed
in the next chapter. In the ova with a large amount of food-yolk it assumes
an eccentric position very early.
The homologies of the primary egg membranes of Craniata are still
involved in some obscurity. There seem to be three membranes, which may
all coexist, and of which one or more are almost always present. These
membranes are—
(1) An outermost usually homogeneous non-perforated membrane, which is
by most authors regarded as a chorion, but is probably a vitelline membrane
—by which name I shall speak of it.
(2) A radiately striated membrane (internal to the former when the two
coexist) which can be broken up into a series of separate columns. These
give to the membrane its radiate striation, but it is probable that between the
columns there are pores sufficiently large to admit of the passage of
protoplasmic filaments. This membrane will be spoken of as the zona
radiata. It is a differentiation of the outermost layer of the yolk.
(3) Within the zona radiata a third and delicate membrane is occasionally
found, especially when the ovum is approaching maturity.

Fig. 21. Section through a small part of the surface of an ovum of an immature female
of Scyllium canicula.

fe. follicular epithelium. vt. vitelline membrane. Zn. zona radiata. yk. yolk with protoplasmic
network.

In Elasmobranchii the first membrane to be formed is the vitelline
membrane, which appears in some instances before the formation of the
follicle—a fact which appears to shew that it is really formed as a
differentiation of the protoplasm of the egg. In most Elasmobranchii this
membrane attains a very considerable development. A zona radiata is
generally (if not always) present in Elasmobranchii, but arises at a later
period than the vitelline membrane (fig. 21, Zn). The zona radiata always
disappears long before the ovum is ripe. The vitelline membrane also
gradually atrophies, though it lasts much longer than the zona radiata. When
the egg is taken up by the oviduct all trace of both membranes has vanished.
In Reptilia precisely the same arrangements of the membranes are found as
in Elasmobranchii, except that as a rule the zona radiata is relatively more
important. The vitelline membrane is thin except in the Crocodilia. The
third innermost membrane is found according to Eimer in many Reptilia. In
birds both vitelline membrane and zona radiata are present, but the latter
atrophies early, leaving the former as the sole membrane when the egg is
ripe.
In osseous fish the vitelline membrane is usually either absent or may
perhaps in some instances, e.g. the Perch, be imperfectly represented. In the
ripe ovum of the Herring there is a distinctly developed membrane external

to the zona radiata which is probably the vitelline membrane. The zona
radiata attains a very great development, and is generally provided with
knobs of various shapes on its outer surface. A delicate membrane internal
to this—my third membrane—has often been described, but there is still
some doubt about its existence. In some cases an external less granular
layer of the ovum itself has been described as a special membrane. In the
Perch a peculiar mucous capsule, penetrated by irregular branched
prolongations of the follicle cells, is present in addition to the ordinary
membranes. In Petromyzon a zona radiata appears to be present, which in
the adult is divided into two layers, both of them radiately striated
according to Calberla, but according to Kupffer and Benecke the outer one
is not perforated, and would appear therefore to be a vitelline membrane as
defined above. A delicate membrane is formed at a comparatively late
period around the ova of the Amphibia, and is stated (Waldeyer, No. 6, and
Kolessnikow) to have a delicate radial striation. It probably corresponds
with the zona radiata.
In Mammalia a radiately striated membrane—the zona radiata—is generally
described as being present, and internal to it, in the nearly ripe egg, a
delicate membrane has been shewn by E. van Beneden to exist. Externally
to the zona radiata there may be observed a granular membrane irregular on
its outer surface on which the cells of the discus are supported. This
membrane is more or less distinctly separated from the zona radiata; and by
tracing back its development it appears very probable that it is the remnant
of the first-formed membrane in the very young ovum, and therefore the
vitelline membrane.
A micropyle (first discovered by Ransom, No. 74) is present in a large
number of osseous fish and in Petromyzon (Calberla). Doubts have been
thrown on its existence in the latter form by Kupffer and Benecke; and at
any rate it would only seem to perforate the zona radiata. In the osseous fish
in which it has been detected, Salmonidæ, Percidæ (Gasterosteus),
Clupeidæe, etc., it forms a minute perforation of the zona radiata at the
animal pole, just large enough to admit a single spermatozoon. Its
characters differ slightly in different cases, but there is usually a shallow
depression, in the centre of which it is situated.

The eggs of all Craniata (except Petromyzon (?)) appear to be enclosed in a
cellular envelope known as the follicle. The cells which form this are, as
has been already explained, derived from the germinal epithelium[25], and
frequently arrange themselves around the ovum before the appearance of
the growths of stroma into the epithelium. All young follicles are nearly
alike, but as they grow older they exhibit various modifications in the
different groups. They retain their simplest condition as a flat epithelial
layer in most osseous fish and Amphibia. In most other forms the cells
become at some period columnar, and are generally arranged in two or more
layers. There is formed externally to the epithelium a delicate membrane—
the membrana propria folliculi—which is in its turn enclosed in a vascular
connective-tissue sheath.
In Elasmobranchii and many Reptilia (Lacertilia, Ophidia) some of the
cells become much larger than the others, and assume a funnel-shaped form
with the narrow end in contact with the egg membrane. These large cells,
which have a regular arrangement in the epithelium, are probably in some
way connected with the nutrition. They have only been noticed in large-
yolked ova. Many observers have described prolongations of the follicle
cells through the pores of the zona radiata in Aves, Reptilia and Teleostei.
The most remarkable modification of the follicle is that which is found in
Mammalia. At first the follicle is similar to that of other Vertebrata, and is
formed of flat cells derived from the germinal cells adjoining the ovum.
These cells next become columnar and then one or two layers deep. Later
they become thicker on one side than on the other, and there appears in the
thickened mass a cavity, which gradually becomes more distended and is
filled with an albuminous fluid. As the cavity enlarges, the ovum with
several layers of cells around it forms a prominence projecting into it. The
whole structure with its tunic is known as the G r a a f i a n f o l l i c l e .
The follicle cells are known as the m e m b r a n a g r a n u l o s a , and the
projection, in which the ovum lies, as the d i s c u s or c u m u l u s
p r o l i g e r u s . The cells of the discus in immediate contiguity to the
ovum usually form a more or less specialized layer and are somewhat more
columnar than the adjoining cells.

The Spermatozoon.

Although there is no doubt that the spermatozoon in most instances plays as
important a part as the ovum in influencing the characters of the organism
which is evolved from the coalesced product of the ovum and
spermatozoon, yet the actual form of the spermatozoon has not, like the
form of the ovum, a secondary influence on the early phases of
development. A comparative history of the spermatozoon is therefore of less
importance for my purpose than that of the ovum; and I shall confine
myself to a few remarks on its general structure, and mode of growth. The
primary origin of the male germinal cells, and their relation to the sperm-
forming cells, is dealt with in the second part of the treatise.
Although the minute size of most spermatozoa places great difficulties in
the way of a satisfactory investigation of them, yet there can be but little
doubt that they always have the value of cells. In the vast majority of
instances the spermatic cell or spermatozoon is composed of (1) a spherical
or oval portion known as the head, formed of a nucleus enveloped in an
extremely delicate layer of protoplasm, and (2) of a motile protoplasmic
flagellum known as the tail; which together with the investing layer of the
head forms the body of the cell.
As might be anticipated, the proportion, size, and relations of the parts of
the spermatozoon are subject to great variations. The head is often
extremely elongated; and it is in many cases rather on theoretical grounds,
than as a result of actual observation, that a protoplasmic layer is stated to
be continued round the nucleus which forms the main constituent of the
head. In some of the elongated forms of spermatozoa, e.g. in Insecta, there
is no marked distinction, except in the character of the protoplasm, between
the head and the tail. A connecting element is frequently interposed between
the head and tail, which appears however to be constituted of the same
material as the tail, and sometimes forms a thickening on the tail close
below the head (Amphioxus). A very remarkable modification of the tail is
found in many Amphibia, Reptilia and Mammalia. In these types there is
attached to what appears to be a normal tail a delicate membrane, the outer
edge of which is thickened to form a kind of secondary filament. In the
living spermatozoon this filament is in a state of constant movement. The
membrane winds spirally round the tail.

In the majority of forms the tail of the living spermatozoon exhibits sinuous
cilia-like movements. In two groups the movements are however of an
amœboid character. These groups are the Nematoda and the Crustacea; and
the spermatozoa in both of them frequently present very abnormal forms. In
Nematoda they are pear-shaped, cylindrical, spine-shaped, etc., and are
mainly formed of protoplasm with a highly refracting nucleus. In the
Crustacea the variations of form are still greater. In the Malacostraca they
are sometimes simply spherical (Squilla), while in Astacus and a large
number of Decapoda they are composed of a nucleated body with stellate
rays. In Paludina amongst the Mollusca there are two forms of completely
developed spermatozoa existing side by side in the same individual.
The spermatozoa are formed by the breaking up of the male germinal cells,
or of cells secondarily derived from them by division. The cells which
directly give rise by division to the spermatozoa may be called
s p e r m o s p o r e s and are equivalent to the ova or oospores.
Amongst the Sponges (Halisarca, Schultze, No. 141) a germinal cell,
similar to that which in the female becomes an ovum, repeatedly divides
and eventually gives rise to a ball of cells (a s p e r m o s p h e r e or
s p e r m - m o r u l a ), each constituent cell of which becomes converted
into a spermatozoon, and may be designated by the special term
‘ s p e r m o b l a s t ’.
In most Hydrozoa the subepithelial epiblastic cells become converted into
germinal cells (spermospores), and then break up to form spermoblasts,
each of which becomes a spermatozoon.
In most higher Metazoa the spermospores usually form the epithelium of an
ampulla or tube, though more rarely (many Chætopoda, Gephyrea, etc.)
they may be derived from cells lining the body cavity, as in the case of ova.
The spermatozoa are formed either by the direct division of the
spermospores into a number of cells, spermoblasts, each of which grows
into a spermatozoon; or by the nucleus of the spermospore becoming
subdivided within the cell body, the latter differentiating itself into the tails
of the spermatozoa while the segments of the nucleus give rise to the main
part of the heads.

In many instances interstitial cells which do not give rise to spermatozoa, are intermingled with the
spermospores.

In a good many cases, as first pointed out by Blomfield[26], the whole of each spermospore does not
become converted into spermatozoa, but part, either with or without a segment of the original
nucleus, remains passive, and carrying as it does the off-budded spermoblasts may be called the
‘ s p e r m - b l a s t o p h o r .’ This passive portion of protoplasm is not employed in the regeneration
of the spermoblast. This very singular phenomenon has been observed in Elasmobranchii, the Frog,
the Earthworm, Helix, etc.[27], and probably has a much wider extension. In Elasmobranchii
(Semper) the passive portions of protoplasm are nucleated, and are placed on the outer side of the
columnar spermospores which line the testicular ampullæ; they are not distinctly differentiated till
the nuclei, segmented from the nucleus of the primitive spermospore to form the heads of the
spermatozoa, have become fairly numerous. In the Frog the passive blastophor also occurs as a
nucleated mass of protoplasm on the outer side of the spermospore. In the Earthworm the blastophor
forms a central non-nucleated portion of the spermospore; and the whole periphery of each
spermospore becomes converted into spermoblasts.

It has been already stated in the introduction that the male and female
generative products are homodynamous, but the consideration of the
development of the products in the two sexes shews that a single
spermatozoon is not equivalent to an ovum, but rather that the whole of the
spermatozoa derived from a spermospore are together equivalent to one
ovum.

[12] In all the Metazoa the generative organs are placed between the primitive
germinal layers; and the peculiarity of their position in the Cœlenterata depends on
the absence of a body cavity and of a distinct mesoblast.
[13] For details on the yolk nucleus vide Balbiani, Leçons s. l. Génération d.
Vertébrés. Paris, 1879. In this work the author maintains very peculiar views on the
nature and function of the yolk nucleus, which do not appear to me well founded.
[14] In the germinal vesicles of very young ova the reticulum is often absent.

[15] A very complete and critical account of the literature is contained in this paper.

[16] M e t s c h n i k o f f . Zeitschrift f. wiss. Zoologie, Vol. XXIV. 1874.

[17] H e r m a n F o l . Jenaische Zeitschrift, Vol. VII.
[18] K o w a l e v s k y . “Entwicklungsgeschichte d. Rippenquallen.” Mémoire de
l’Acad. Pétersbourg, 1866. And A l e x . A g a s s i z . “Embryology of the
Ctenophoræ.” Amer. Acad. of Science and Arts, Vol. X. No. 111.
[19] The view of van Beneden, according to which the ova have an endodermal
(hypoblastic) origin, has been shewn to be at any rate confined to certain groups.
The whole question of the origin of the generative products from the germinal
layers in the Cœlenterata is still involved in great obscurity.

[20] The above description of the ova of the Tubularidæ is founded on sections of
the gonophores of Tubularia mesembryanthemum. Dr Kleinenberg informs me
however that the absence of a distinct boundary between the germinal cells and the
ovum is not usual.

[21] Amphiporus lactiflorius and Nemertes gracilis. McIntosh. Monograph on
British Nemertines. Ray Society.
[22] The rachis is stated by Whitman (No. 39), and other observers to be formed of
nucleated protoplasm, but further investigations on this point are still required.
[23] For a list of the genera with and without nutritive cells, vide Brandt, pp. 47 and
48.
[24] Kupffer, Laichen u. Entwicklung des Ostsee-Härings. Berlin, 1878.

[25] For the different views maintained by Foulis, Kölliker, etc. the reader is referred
to the writings of these authors. The grounds for the view here adopted will be
found in my paper (No. 64).
[26] Quart. Journ. of Micro. Science, Vol. XX. 1880.

[27] Blomfield, loc. cit., p. 83, states that he has observed this fact in Lumbricus,
Tubifer, Hirudo, Helix, Arion, Paludina, Rana, Salamandra, and Mus.

CHAPTER II.

THE MATURATION AND IMPREGNATION OF THE OVUM.

Maturation of the ovum and formation of the polar bodies.
In the preceding chapter the changes in the ovum were described nearly up
to the period when it became ripe, and ready to be impregnated. Preparatory
to the act of impregnation there take place however a series of remarkable
changes, which more especially concern the germinal vesicle.
The attention of a large number of investigators has recently been directed to these changes as well as
to the phenomena of impregnation. The results of their investigations will be described in the present
chapter; but for an historical account of these investigations, as well as for a determination of the
delicate questions of priority, the reader is referred to Fol’s memoir (No. 87), and to a paper by the
author (No. 81).

Fig. 22. Ripe ovum of Asterias glacialis enveloped in a mucilaginous envelope, and
containing an eccentric germinal vesicle and germinal spot (copied from Fol).

The nature of the changes which take place in the maturation of the ovum
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 (87),
may be selected.

The ripe ovum (fig. 22), when detached from the ovary is formed of a
granular vitellus enveloped in a mucilaginous coat, the zona radiata. It
contains an eccentrically-situated germinal vesicle and a germinal spot. In
the former is present the usual protoplasmic reticulum. As soon as the ovum
reaches the sea-water the germinal vesicle commences to undergo a peculiar
metamorphosis. It exhibits frequent changes of form, the reticulum
vanishes, its membrane becomes gradually absorbed, its outline indented
and indistinct, and finally its contents become to a certain extent
confounded with the vitellus (fig. 23).

Fig. 23. 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).

The germinal spot at the same time loses its clearness of outline and
gradually disappears from view.
At this stage, and between it and the stage represented in fig. 26, the action
of reagents brings to light certain appearances the nature of which is not yet
fully cleared up for Asterias, which have been described somewhat
differently by Fol for Ast. glacialis and Hertwig for Asteracanthion.

Fig. 24. Ovum of Asterias glacialis shewing the clear spaces in the place of the
germinal vesicle. Fresh preparation (copied from Fol).

Fol finds immediately after the stage just described that a star is visible between the remains of the
germinal vesicle and the surface of the egg, which is connected with an imperfectly-formed nuclear
spindle extending towards the germinal vesicle[28]. At the end of the nuclear spindle may be seen the
broken up fragments of the germinal spot.
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. 24), one ovoid and nearer the surface, and the second more
irregular in form and situated rather deeper in the vitellus. In the upper space parallel striæ may be
observed. By treatment with reagents the first clear space is found to be formed of a horizontally-
placed spindle with two terminal stars, near which irregular remains of the germinal spot may be
seen. Slightly later (fig. 25) there may be seen on the lower side of the spindle a somewhat irregular
body, which may possibly be part of the remains of the germinal spot, though Fol holds that it is
probably part of the membrane of the germinal vesicle. The lower clear space visible in the fresh
ovum now contains a round body, fig. 25. Fol concludes that the spindle is formed out of part of the
germinal vesicle and not from 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.

Fig. 25. Ovum of Asterias glacialis, at the same stage as fig. 24, treated with picric acid
(copied from Fol).

The following is Hertwig’s (No. 92) account of the changes in the germinal vesicle in Asteracanthion.
Shortly after the egg is laid the protoplasm on the side of the germinal vesicle towards the surface of
the egg develops a prominence which presses inwards the wall of the vesicle. At the same time the
germinal spot develops a large vacuole, in the interior of which is a body consisting of nuclear
substance, and formed of a firmer and more refractive material than the remainder of the germinal
spot. In the prominence first mentioned as projecting inwards towards the germinal vesicle first one
star, formed by radial striæ of protoplasm, and then a second make their appearance; while 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 its vacuole

forms a rod-like body, the free end of which is situated between the two stars which occupy the
prominence indenting the germinal vesicle. At a later period granules may be seen at the end of the
rod and finally the rod itself vanishes. After these changes by the aid of reagents there may be
demonstrated a spindle between the two stars, which Hertwig believes to grow in size as the last
remnants of the germinal spot gradually vanish, and he maintains that the spindle is formed at the
expense of the germinal spot. The stage with this spindle corresponds with fig. 25.
Several of Hertwig’s figures closely correspond with those of Fol, and considering how conflicting is
the evidence before us, it seems necessary to leave open for Asterias the question as to what parts of
the germinal vesicle are concerned in forming the first spindle.

A clearer view of the phenomena which take place at this stage has been
obtained by Fol in the case of Heteropods (Pterotrachæa). In the ovum a
few minutes after it has been laid the germinal vesicle becomes very pale,
and two stars make their appearance round a clear substance near its poles.
The nucleus itself is somewhat elongated, and commences to exhibit at its
poles longitudinal striæ, which gradually extend towards the centre at the
expense of the nuclear reticulum, from a metamorphosis of which they are
directly derived. When the striæ of the two sides have nearly met,
thickenings may be observed in the recticulum between them, which give
rise, where the striæ of the two sides unite, to the central thickenings of the
fibres (nuclear plate). In this way a complete nuclear spindle is
established[29].
The important result of Fol’s observations on Heteropods, which tallies also
with what is found in Asterias, is that a spindle with two stars at its poles is
formed from the metamorphosis of the germinal vesicle and surrounding
protoplasm (fig. 25).

Fig. 26. 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).

Polar cells. The spindle has up to this time been situated with its axis
parallel to the surface of the egg, but in somewhat older specimens a
vertical spindle is found, with one end projecting into a protoplasmic
prominence which makes its appearance on the surface of the egg (fig. 26).
Hertwig believes that the spindle simply travels towards the surface, and
while doing so changes the direction of its axis. Fol asserts, however, that
this is not the case, but that between the two phases 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 body with a dentated outline. He has not
been able to arrive at a conclusion as to what meaning is to be attached to
this occurrence, which does not appear to take place in Heteropods.

Fig. 27. Portion of the ovum of Asterias glacialis, with the first polar cell as it
appears when living (copied from Fol).

In any case the spindle which projects into the prominence on the surface of
the egg divides into two parts, one in the prominence and one in the egg
(fig. 26). The prominence itself with the enclosed portion of the spindle
becomes constricted off from the egg to form a body, well known to
embryologists as the polar body or cell (fig. 27). Since more than one polar
cell is formed, that which is the earliest to appear may be called the first
polar cell.

Fig. 28. Portion of the ovum of Asterias glacialis immediately after the formation of
the second polar cell. Picric acid preparation (copied from Fol).

The part of the spindle which remains in the egg becomes directly
converted into a second spindle by the elongation of its fibres, without
passing through a typical nuclear condition. A second polar cell next
becomes formed in the same manner as the first (fig. 28), and the portion of
the spindle remaining in the egg becomes converted into two or three clear
vesicles (fig. 29), which soon unite to form a single nucleus (fig. 30). The
new nucleus which is clearly derived from part of the original germinal
vesicle is called the female pronucleus, for reasons which will appear in the
sequel.

Fig. 29. 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).

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 process of cell division and have the value of cells.
A peculiar phenomenon makes its appearance in the eggs of Clepsine shortly after the formation of
the polar cells, which has been spoken of by Whitman (No. 100) as the formation of the polar rings.
The following is his description of the occurrence.
“Fifteen minutes after the elimination of the polar globules (i.e. cells) a ring-like depression or
constriction appears in the yolk around the oral pole, and in this depression a transparent liquid
substance (nuclear?) is collected forming the first polar ring.... The same phenomena repeat
themselves later at the aboral pole.... The rings concentrate to form two discs.... Before the first
cleavage both discs plunge deep into the egg.”
The nature of these rings is at present quite obscure.

Fig. 30. Ovum of Asterias glacialis with the two polar cells and the female pronucleus
surrounded by radial striæ, as seen in the living egg (copied from Fol).

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.
There is however 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 an 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, the
disappearance of the reticulum, and the breaking up and disappearance of
the germinal spot. The exact fate of the single germinal spot, or the
numerous spots where they are present, is still obscure.
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 of the ovum 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
Cœlenterata, the Echinodermata, and the Mollusca, some of the Vermes
[Turbellarians (Leptoplana), Nematodes, Hirudinea, Alciope, Sagitta],
Ascidians, etc. It is very possible, not to say probable, that such changes are
universal in the animal kingdom, but the present state of our knowledge
does not justify us in saying so.
In the Craniata especially our knowledge of the formation of the polar bodies is very unsatisfactory.
In Petromyzon Kupffer and Benecke have brought forward evidence to shew that one polar body is
formed prior to the impregnation, and a second in connection with a peculiar prominence of
protoplasm after impregnation. Part of the germinal vesicle remains in the egg as the female
pronucleus. In the Sturgeon the germinal vesicle atrophies and breaks up before impregnation, and
afterwards part is found as a granular mass on the surface of the egg, while part forms a female
pronucleus.
In Amphibia the observations of Hertwig (90) and Bambeke (77) tend to shew that after the germinal
vesicle has assumed a superficial situation at the pigmented pole of the ovum its contents become
intermingled with the yolk, and are in part extruded from the ovum as a granular mass after
impregnation. Part of them remains in the ovum and forms a female pronucleus. Whether there is a
proper division of the germinal vesicle as in typical cases is not known.
Oellacher (95) by a series of careful observations upon the egg of the trout, and subsequently of the
bird, demonstrated that in the ovum while still in the ovary, the germinal vesicle underwent a kind of
degeneration and eventually became ejected, in part at any rate. My own observations on
Elasmobranchs, which require enlargement and confirmation, tend to shew that this part may be the
membrane. Ed. van Beneden (78) has contributed some important observations on the rabbit. His
account is as follows. As the ovum approaches maturity the germinal vesicle assumes an eccentric
position, and fuses with the peripheral layer of the egg to constitute the cicatricular lens. The
germinal spot next travels to the surface of the cicatricular lens and forms the nuclear disc: at the
same time the membrane of the germinal vesicle vanishes, though it probably unites with the nuclear

disc. The plasma of the nucleus then collects into a definite mass and forms the nucleoplasmic body.
Finally the nuclear disc assumes an ellipsoidal form and becomes the nuclear body. Nothing is now
left of the original germinal vesicle but the nuclear body and the nucleoplasmic body, both still
situated within the ovum. In the next stage no trace of the germinal vesicle can be detected in the
ovum, but outside it, close to the point where the modified remnants of the vesicle were previously
situated, there is present a polar body which is composed of two parts, one of which stains deeply and
resembles the nuclear body, and the other does not stain but is similar to the nucleoplasmic body. Van
Beneden concludes that the parts of the polar body are the two ejected products of the germinal
vesicle. We may be perhaps permitted to hold that further observations on this difficult object will
demonstrate that part of the germinal vesicle remains in the ovum to form the female pronucleus.
With reference to invertebrate forms attention may be called to the observations of Bütschli (80).
Although in Cucullanus a normal formation of the polar bodies takes place, yet in the Nematodes
generally, Bütschli has been unable to find the spindle modification of the germinal vesicle, but states
that the germinal vesicle undergoes degeneration, its outline becoming indistinct and the germinal
spot vanishing. The position of the germinal vesicle continues to be marked by a clear space, which
gradually approaches the surface of the egg. When it is in contact with the surface a small spherical
body, the remnant of the germinal vesicle, comes into view, and eventually becomes ejected. The
clear space subsequently disappears.

In addition to the types just quoted, which may very probably turn out to be
normal in the mode of formation of the polar bodies, there is a large number
of types, including the whole of the Rotifera and Arthropoda with a few
doubtful exceptions[30], in which the polar cells cannot as yet be said to have
been satisfactorily observed.
The more important of the doubtful cases amongst the Rotifera and Arthropoda are the following.
Flemming (83) 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.

Hoek[31] believes that he has found a polar body in the ovum of Balanus balanoides, but his
observations are not perfectly satisfactory.
Bütschli, who has expressly searched for the polar bodies in the ova of Rotifera, was unable to find
any trace of them, though he found that as the egg became ripe the germinal vesicle became half its
original size. In the parthenogenetic eggs of Aphis he also failed to find a trace of polar bodies,
though the germinal vesicle, after the germinal spot had broken up into fragments, approached the
surface and disappeared.

Whatever may be the eventual result of more extended investigation, it is
clear that the formation of polar cells according to the type described above
is a very constant occurrence. Its importance is increased by the discovery
by Strasburger of the existence of an analogous process amongst plants.
Two questions about it obviously present themselves for solution: (1) What

are the conditions of its occurrence with reference to impregnation? (2)
What meaning has it in the development of the ovum or the embryo?
The answer to the first of these questions is not difficult to find. The
formation of the polar bodies is independent of impregnation, and is the
final act of the normal growth of the ovum. In a few types the polar cells are
formed while the ovum is still in the ovary, as, for instance, in some species
of Echini, Hydra, etc., but, according to our present knowledge, far more
usually after the ovum has been laid. In some instances the budding-off of
the polar cells precedes, and in other instances follows impregnation; but
there is no evidence to shew that in the latter cases the process is influenced
by the contact with the male element. In Asterias, as has been shewn by O.
Hertwig and Fol, the formation of the polar cells may indifferently either
precede or follow impregnation—a fact which affords a clear demonstration
of the independence of the two occurrences.
To the second of the two questions it does not unfortunately seem possible
at present to give an answer which can be regarded as satisfactory.
The retrogressive changes in the membrane of the germinal vesicle which
usher in the formation of the polar bodies may very probably be viewed as a
prelude to a renewed activity of the contents of the vesicle; and are perhaps
rendered the more necessary from the thickness of the membrane which
results from a protracted period of passive growth. This suggestion does
not, however, help us to explain the formation of polar bodies by a process
identical with cell division. The ejection of part of the germinal vesicle in
the formation of the polar cells may probably be paralleled by the ejection
of part or the whole of the original nucleus which, if we may trust the
beautiful researches of Bütschli, takes place during conjugation in Infusoria
as a preliminary to the formation of a fresh nucleus. This comparison is due
to Bütschli, and according to it the formation of the polar bodies would
have to be regarded as assisting, in some as yet unknown way, the process
of regeneration of the germinal vesicle. Views analogous to this are held by
Strasburger and Hertwig, who regard the formation of the polar bodies in
the light of a process of excretion or removal of useless material. Such
hypotheses do not, unfortunately, carry us very far.

I would suggest that in the formation of the polar cells part of the
constituents of the germinal vesicle, which are requisite for its functions as
a complete and independent nucleus, is removed, to make room for the
supply of the necessary parts to it again by the spermatic nucleus.
My view amounts to the following, viz. that after the formation of the polar
cells the remainder of the germinal vesicle within the ovum (the female
pronucleus) is incapable of further development without the addition of the
nuclear part of the male element (spermatozoon), and that if polar cells
were not formed parthenogenesis might normally occur. A strong support
for this hypothesis would be afforded were it to be definitely established
that a polar body is not formed in the Arthropoda and Rotifera; since the
normal occurrence of parthenogenesis is confined to these two groups. It is
certainly a remarkable coincidence that they are the only two groups in
which polar bodies have not so far been satisfactorily observed.
It is perhaps possible that the part removed in the formation of the polar cells is not absolutely
essential; and this seems at first sight to follow from the fact of parthenogenesis being possible in
instances where impregnation is the normal occurrence. The genuineness of the observations on this
head is too long a subject to enter into here[32], but after admitting, as we probably must, that there
are genuine cases of such 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 impossible.
Selenka found in the case of Purpura lapillus that no polar body was formed in the eggs which did
not develop, but in the case of Neritina, Bütschli has found that this does not hold good.
The remarkable observations of Greeff (No. 88) on the parthenogenetic development of the eggs of
Asterias rubens tell, however, very strongly against the above hypothesis. Greeff has found that
under normal circumstances the eggs of this species of starfish will develop without impregnation in
simple sea-water. The development is quite regular and normal, though much slower than in the case
of impregnated eggs. It is not definitely stated that polar cells are formed, but there can be no doubt
that this is implied. Greeff’s account is so precise and circumstantial that it is not easy to believe that
any error can have crept in; but neither Hertwig nor Fol have been able to repeat his experiments, and
we may be permitted to wait for further confirmation before absolutely accepting them.
To the suggestion already made with reference to the function of the polar cells, I will venture to add
the further one, that the function of forming polar cells has been acquired by the ovum for the express
purpose of preventing parthenogenesis.
The explanation given by Mr Darwin of the evil effects of self-fertilization, viz. the want of sufficient
differentiation in the sexual elements[33], would apply with far greater force to cases of
parthenogenesis.
In the production of fresh individuals, two circumstances are obviously favourable to the species. (1)
That the maximum number possible of fresh individuals should be produced, (2) That the individuals

should be as vigorous as possible. Sexual differentiation (even in hermaphrodites) is clearly very
inimical to the production of the maximum number of individuals. There can be little doubt that the
ovum is potentially capable of developing by itself into a fresh individual, and therefore, unless the
absence of sexual differentiation was very injurious to the vigour of the progeny, parthenogenesis
would most certainly be a very constant occurrence; and, on the analogy of the arrangements in
plants to prevent self-fertilization, we might expect to find some contrivance both in animals and in
plants to prevent the ovum developing by itself without fertilization. If my view about the polar cells
is correct, the formation of these bodies functions as such a contrivance.
Reproduction by budding or fission has probably arisen as a means of increasing the number of
individuals produced, so that the coexistence of asexual with sexual reproduction is to be looked on
as a kind of compromise for the loss of the power of rapid reproduction due to the absence of
parthenogenesis. In the Arthropoda and Rotifera the place of budding has been taken by
parthenogenesis, which may be a frequent, though not always a necessary occurrence, as in various
Branchiopoda (Apus, Limnadia, etc.) and Lepidoptera (Psyche helix, etc.); or a regular occurrence for
the production of one sex, as in Bees, Wasps, Nematus, etc.; or an occurrence confined to a certain
stage in the cycle of development in which all the individuals reproduce their kind
parthenogenetically, as in Aphis, Cecidomyia, Gall Insects (Neuroterus, etc.), Daphnia[34].
On my hypothesis the possibility of parthenogenesis, or at any rate its frequency, in Arthropoda and
Rotifera is possibly due to the absence of polar cells. In the case of all animals, so far as is known to
me, fertilization of the ovum occasionally occurs[35], but there are instances in the vegetable kingdom
where so-called parthenogenesis appears to be capable of recurring for an indefinite period. One of
the best instances appears to be that of Cœlebogyne, an introduced exotic Euphorbiaceous plant
which regularly produces fertile seeds although a male flower never appears. The recent researches of
Strasburger have however shewn that in Cœlebogyne and other parthenogenetic flowering plants,
embryos are formed by the budding and subsequent development of cells belonging to the ovule.
This being the case, it is impossible to assert of these plants that they are really parthenogenetic, for
the embryos contained in the seed of a flower which has certainly not been fertilized, may have been
formed, not by the development of the ovum, but by budding from the surrounding tissue of the ovule.
The above view with reference to the nature of the polar bodies is not to be regarded as forming more
than an hypothesis.

Impregnation of the Ovum.
A far greater amount of certainty has 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.

Fig. 31. Small portions of the ovum of Asterias glacialis. The Spermatozoa are shewn
enveloped in the mucilaginous coat. In A. a prominence is rising from the surface of the
egg towards the nearest spermatozoon; and in B. the spermatozoon and prominence have
met. (Copied from Fol.)

Fig. 32. Portion of the ovum of Asterias glacialis after the entrance of a spermatozoon
into the ovum. It shews the prominence of the ovum through which the spermatozoon has
entered. A vitelline membrane with a crater-like opening has become distinctly formed.
(Copied from Fol.)

It will be convenient again to take Asterias glacialis as the type. 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.
29), which aggregate themselves into a single clear nucleus, which
gradually travels toward the centre of the egg and around which, as a centre,

the protoplasm becomes radiately striated (fig. 30). This nucleus is known
as the female pronucleus. By the action of reagents a nucleolus may be
shewn in it. In Asterias glacialis the most favourable period for fecundation
is about an hour after the formation of the female pronucleus. If at this time
the spermatozoa are allowed to come in contact with the egg, their heads
soon become enveloped in the investing mucilaginous coat. A prominence,
pointing towards the nearest spermatozoon, now arises from the superficial
layer of protoplasm of the egg, and grows till it comes in contact with the
spermatozoon (fig. 31, A and B). Under normal circumstances the
spermatozoon which meets the prominence is the only one concerned in the
fertilization, and it makes its way into the egg by passing through the
prominence. The tail of the spermatozoon, 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. 32). It eventually becomes absorbed
into the body of the ovum.
At the moment of contact between the spermatozoon and the egg the
outermost layer of the protoplasm of the latter raises itself as a distinct
membrane, which separates from the egg and prevents the entrance of other
spermatozoa. At the point where the spermatozoon entered a crater-like
opening is left in the membrane, through which the metamorphosed tail of
the spermatozoon may at first be seen projecting (fig. 32).

Fig. 33. Ovum of Asterias glacialis, with male and female pronucleus and a radial
striation of the protoplasm around the former. (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,
probably by assimilating material from the ovum, and around it is formed a
clear space free from yolk-spherules. Shortly after its formation the
protoplasm in its neighbourhood assumes a radiate arrangement (fig. 33). At
whatever point of the egg the spermatozoon may have entered, it gradually
travels towards the female pronucleus. The latter, around which the
protoplasm no longer has a radiate arrangement, remains motionless till the
rays of the male pronucleus come in contact with it, after which its
condition of repose is exchanged for one of activity, and it rapidly
approaches the male pronucleus, apparently by means of its inherent
amœboid contractions, and eventually fuses with it (figs. 34‑36).
As the male pronucleus approaches the female the latter, according to
Selenka, sends out protoplasmic processes which embrace the former. The
actual fusion does not take place till after the pronuclei have been in contact
for some time. While the two pronuclei are approaching one another the
protoplasm of the egg exhibits amœboid movements.

Figs. 34, 35, and 36. Three successive stages in the coalescence of the male and female
pronuclei in Asterias glacialis. From the living ovum. (Copied from Fol.)

The product of the fusion of the two pronuclei forms the first segmentation
nucleus (fig. 37), which soon, however, divides into the two nuclei of the
two first segmentation spheres.

Fig. 37. Ovum of Asterias glacialis, after the coalescence of the male and female
pronuclei. (Copied from Fol.)

The phenomenon which has just been described consists essentially in the
fusion of the male cell and the female cell. In this act the protoplasm of the
two cells as well as their nuclei coalesce, since the whole spermatozoon
which has been absorbed into the ovum is a cell of which the head is the
nucleus.
It is clear that the ovum after fertilization is an entirely different body to the
ovum prior to that act, and unless the use of the same term for the two
conditions of the ovum had become very familiar, a special term, such as
oosperm, for the ovum after its fusion with the spermatozoon, would be
very convenient.
Of the earlier observations on this subject there need perhaps only be cited one of E. van Beneden, on
the rabbit’s ovum, shewing the presence of two nuclei before the commencement of segmentation.
Bütschli was the earliest to state from observations on Rhabditis dolichura that the first segmentation
nucleus arose from the fusion of two nuclei, and this was subsequently shewn with greater detail for
Ascaris nigrovenosa, by Auerbach (76). Neither of these authors gave at the first the correct
interpretation of their results. At a later period Bütschli (80) arrived at the conclusion that in a large
number of instances (Lymnæus, Nephelis, Cucullanus, &c.), the nucleus in question was formed by
the fusion of two or more nuclei, and Strasburger at first made a similar statement for Phallusia,
though he has since withdrawn it. Though Bütschli’s statements depend, as it seems, upon a false
interpretation of appearances, he nevertheless arrived at a correct view with reference to what occurs
in impregnation. Van Beneden (78) described in the rabbit the formation of the original segmentation
nucleus from two nuclei, one peripheral and the other central, and deduced from his observations that
the peripheral nucleus was derived from the spermatic element. It was reserved for Oscar Hertwig

(89) to describe in Echinus lividus the entrance of a spermatozoon into the egg and the formation
from it of the male pronucleus.

The general fact that impregnation consists in the fusion of the
spermatozoon and ovum has now been established for some forms in the
majority of invertebrate groups (Arthropoda and Rotifera excepted).
Amongst Vertebrata also it has been shewn by E. van Beneden that the first
segmentation nucleus is formed by the coalescence of the male and female
pronucleus. Calberla, and Kupffer and Benecke have demonstrated that a
single spermatozoon enters at first the ovum of Petromyzon.
The contact of the spermatozoon with the egg membrane causes in Petromyzon active movements of
the protoplasm of the ovum, and a retreat of the protoplasm from the membrane.

In Amphibia the appearance of a peculiar pigmented streak extending
inwards from the surface of the pigmented pole of the ovum, and containing
in a clear space at its inner extremity a nucleus, has been demonstrated as
the result of impregnation by Bambeke (77) and Hertwig (90). There can be
little doubt that this nucleus is the male pronucleus, and that the pigmented
streak indicates its path inwards. Close to it Hertwig has shewn that another
nucleus is to be found, the female pronucleus, and that eventually the two
join together. In Amphibia the phenomena accompanying impregnation are
clearly of the same nature as in the Invertebrata. A precisely similar series
of phenomena to those in Amphibia has been shewn by Salensky to take
place in the Sturgeon.
Although there is a general agreement between the most recent observers, Hertwig, Fol, Selenka,
Strasburger, &c., as to the main facts connected with the entrance of one spermatozoon into the egg,
the formation of the male pronucleus, and its fusion with the female pronucleus, there still exist
differences of detail in the different descriptions, which partly, no doubt, depend upon the difficulties
of observation, but partly also upon the observations not having all been made upon the same species.
Hertwig does not enter into details with reference to the actual entrance of the spermatozoon into the
egg, but in his latest paper points out that considerable differences may be observed in the
occurrences which succeed impregnation, according to the relative period at which this takes place.
When, in Asterias, the impregnation is effected about an hour after the egg is laid, and previously to
the formation of the polar cells, the male pronucleus appears at first to exert but little influence on the
protoplasm, but after the formation of the second polar cell, the radial striæ around it become very
marked, and the pronucleus rapidly grows in size. When it finally unites with the female pronucleus
it is equal in size to the latter. In the case when the impregnation is deferred for four hours the male
pronucleus never becomes so large as the female pronucleus. With reference to the effect of the time
at which impregnation takes place, Asterias would seem to serve as a type. Thus in Hirudinea,
Mollusca, and Nematoidea impregnation normally takes place before the formation of the polar
bodies is completed, and the male pronucleus is accordingly as large as the female. In Echinus, on the
other hand, where the polar bodies are formed in the ovary, the male pronucleus is always small.

Selenka, who has investigated the formation of the male pronucleus in Toxopneustes variegatus,
differs in certain points from Fol. He finds that usually, though not always, a single spermatozoon
enters the egg, and that though the entrance may be effected at any part of the surface it generally
occurs at the point marked by a small prominence where the polar cells are 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.

One important point has been so far only indirectly alluded to, viz. the
number of spermatozoa required to effect impregnation.
The concurrent testimony of almost all observers tends to shew that one
only is required for this purpose. But the number of cases tested is too small
to admit of satisfactory generalization.
Both Hertwig and Fol have made observations on the result of the entrance
into the egg of several spermatozoa. Fol finds that when the impregnation
has been too long delayed the vitelline membrane is formed with
comparative slowness, and several spermatozoa are thus enabled to
penetrate. Each spermatozoon forms a separate pronucleus with a
surrounding star; and several male pronuclei usually fuse with the female
pronucleus. Each male pronucleus appears to exercise a repulsive influence
on other male pronuclei, but to be attracted by the female pronucleus. When
there are several male pronuclei the segmentation is irregular and the
resulting larva a monstrosity. These statements of Fol and Hertwig are up to
a certain point in contradiction with the more recent results of Selenka. In
Toxopneustes variegatus Selenka finds that though impregnation is usually
effected by a single spermatozoon yet several may be concerned in the act.
The development continues, however, to be normal up to the gastrula stage,
at any rate, if three or even four spermatozoa enter the egg almost
simultaneously. Under such circumstances each spermatozoon forms a
separate pronucleus and star. Selenka is of opinion (apparently rather on a
priori grounds than as a result of direct observation) that normal
development cannot occur when more than one male pronucleus fuses with
the female pronucleus; and holds that, where he has observed such normal
development after the entrance of more than one spermatozoon, the
majority of male pronuclei become absorbed.
It may be noticed that, while the observations of Fol and Hertwig were
admittedly made upon eggs in which the impregnation was delayed till they
no longer displayed their pristine activity, Selenka’s were made upon quite

fresh eggs; and it seems not impossible that the pathological symptoms in
the embryos reared by the two former authors may have been due to the
imperfection of the egg, and not to the entrance of more than one
spermatozoon. This, of course, is merely a suggestion which requires to be
tested by fresh observations.
Kupffer and Benecke have further shewn that although only one
spermatozoon enters the ovum directly in Petromyzon yet other
spermatozoa pass through the vitelline membrane, and are taken into a
peculiar protoplasmic protuberance of the ovum which appears after
impregnation.
The act of impregnation may be described as the fusion of the ovum and
spermatozoon, and the most important feature in this act appears to be 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, as stated above, contains part of the nucleus of the
primitive spermatic cell. The spermatic cells originate from cells
indistinguishable from the primitive ova, so that the fusion which takes
place is the fusion of morphologically similar parts in the two sexes.
These conclusions tally very satisfactorily with the view adopted in the
Introduction, that impregnation amongst the Metazoa was derived from the
process of conjugation amongst the Protozoa.

Summary.
In what may probably be regarded as a normal case the following series of
events accompanies the maturation and impregnation of an ovum:—
(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 and nuclear reticulum.
(3) Assumption of a spindle character by the remains of the germinal
vesicle, these remains being probably in part 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 becoming at the same time nearly
constricted off from the egg as a polar cell.
(6) Formation of a second polar cell in the same manner as the first, part of
the spindle still remaining in the egg.
(7) Conversion of the part of the spindle remaining in the egg into a nucleus
—the female pronucleus.
(8) Transportation of the female pronucleus towards the centre of the egg.
(9) Entrance of one spermatozoon into the egg.
(10) Conversion of the head of the spermatozoon into a nucleus—the male
pronucleus.
(11) Appearance of radial striæ round the male pronucleus, which gradually
travels towards the female pronucleus.
(12) Fusion of male and female pronuclei to form the first segmentation
nucleus.

(76) Auerbach. Organologische Studien, Heft 2. Breslau, 1874.
(77) Bambeke. “Recherches s. Embryologie des Batraciens.” Bull. de l’Acad. royale de Belgique,
2me Sér., T. LXI., 1876.
(78) E. van Beneden. “La Maturation de l’Œuf des Mammifères.” Bull. de l’Acad. royale de
Belgique, 2me Sér., T. XL. No. 12, 1875.
(79) Idem. “Contributions à l’Histoire de la Vésicule Germinative, &c. ” Bull. de l’Acad. royale de
Belgique, 2me Sér., T. XLI. No. 1, 1876.
(80) O. Bütschli. Eizelle, Zelltheilung, und Conjugation der Infusorien. Frankfurt, 1876.
(81) F. M. Balfour. “On the Phenomena accompanying the Maturation and Impregnation of the
Ovum.” Quart. J. of Micros. Science, Vol. XVIII., 1878.
(82) Calberla. “Befruchtungsvorgang beim Ei von Petromyzon Planeri.” Zeit. f. wiss. Zool., Vol.
XXX.
(83) W. Flemming. “Studien in d. Entwickelungsgeschichte der Najaden.” Sitz. d. k. Akad. Wien, B.
LXXI., 1875.
(84) H. Fol. “Die erste Entwickelung des Geryonideneies.” Jenaische Zeitschrift, Vol. VII., 1873.
(85) Idem. “Sur le Développement des Ptéropodes.” Archives de Zoologie Expérimentale et

Générale, Vol. IV. and V. 1875‑6.
(86) Idem. “Sur le Commencement de l’Hénogénie.” Archives des Sciences Physiques et Naturelles.
Genève, 1877.
(87) Idem. Recherches s. l. Fécondation et l. commen. d. l’Hénogénie. Genève, 1879.
(88) R. Greeff. “Ueb. d. Bau u. d. Entwickelung d. Echinodermen.” Sitzun. der Gesellschaft z.
Beförderung d. gesammten Naturwiss. z. Marburg, No. 5, 1876.
(89) Oscar Hertwig. “Beit. z. Kenntniss d. Bildung, &c., d. thier. Eies.” Morphologisches Jahrbuch,
Vol. I., 1876.
(90) Idem.Ibid. Morphologisches Jahrbuch, Vol. III. Heft 1, 1877.
(91) Idem. “Weitere Beiträge, &c.” Morphologisches Jahrbuch, Vol. III., 1877, Heft 3.
(92) Idem. “Beit. z. Kenntniss, &c. ” Morphologisches Jahrbuch, Vol. IV. Heft 1 and 2, 1878.
(93) N. Kleinenberg. Hydra. Leipzig, 1872.
(94) C. Kupffer u. B. Benecke. Der Vorgang d. Befruchtung am Eie d. Neunaugen. Königsberg,
1878.
(95) J. Oellacher. “Beiträge zur Geschichte des Keimbläschens im Wirbelthiere.” Archiv f. mikr.
Anat., Bd. VIII., 1872.
(96) W. Salensky. “Befruchtung u. Furchung d. Sterlets-Eies.” Zoologischer Anzeiger, No. 11, 1878.
(97) E. Selenka. Befruchtung des Eies von Toxopneustes variegatus. Leipzig, 1878.
(98) Strasburger. Ueber Zellbildung u. Zelltheilung. Jena, 1876.
(99) Idem. Ueber Befruchtung u. Zelltheilung. Jena, 1878.
(100) C. O. Whitman. “The Embryology of Clepsine.” Quart. J. of Micr. Science, Vol. XVIII., 1878.

[28] By the term ‘nuclear spindle’ I refer to the peculiar form of a double striated
cone assumed by the nucleus just before division, which is no doubt familiar to all
my readers. I use the term star for the peculiar stellate figure usually visible at the
poles of the nuclear spindle. For a further description of these parts the reader is
referred to Chapter IV.
[29] For the further details on the nuclear spindle vide the next Chapter.

[30] The best instance of what appears like a polar cell in Arthropoda is a body
recently found by Grobben (“Entwicklungsgeschichte d. Moina rectirostris.” Claus’
Arbeiten, Vol. II., Wien, 1879) near the surface of the protoplasm at the animal pole
of the summer and parthenogenetic eggs of Moina rectirostris, one of the
Cladocera. The body stains deeply with carmine, but differs from normal polar cells
in not being separated from the ovum; and its identification as a polar cell must
remain doubtful till it has been shewn to originate from the germinal vesicle.
[31] “Zur Entwicklung d. Entomostraken.” Niederlandischer Archiv. f. Zoologie, Vol.
III. p. 62.

[32] The instances quoted by Siebold, Parthenogenesis d. Arthropoden, are not quite
satisfactory. In Hensen’s case, p. 234, impregnation would have been possible if we
can suppose the spermatozoa to be capable of passing into the body cavity through
the open end of the uninjured oviduct; and though Oellacher’s instances are more
valuable, yet sufficient care seems hardly to have been taken, especially when it is
not certain for what length of time spermatozoa may be able to live in the oviduct.
For Oellacher’s precautions, vide Zeit. für Wiss. Zool., Bd. xxii., p. 202. A better
instance is that of a sow given by Bischoff, Ann. Sci. Nat., series 3, Vol. II., 1844.

The unimpregnated eggs were found divided into segments, but the segments did
not contain the usual nucleus, and were perhaps nothing else than the parts of an
ovum in a state of disruption.
[33] Darwin, Cross- and Self-Fertilization of Plants, p. 443.

[34] Mr J. A. Osborne has recently shewn (Nature, Sept. 4, 1879), that the eggs of a
Beetle (Gastrophysa raphani) may occasionally develop, up to a certain point at any
rate, without the male influence.
[35] Dicyema, which is an apparent exception, has not yet been certainly shewn to
develop true ova. If its germs are true ova it forms an exception to the above rule.

CHAPTER III.

THE SEGMENTATION OF THE OVUM.

The immediate result of the fusion of the male and female pronucleus is the
segmentation or division of the ovum usually into two, four, eight, etc.
successive parts. The segmentation may be dealt with from two points of
view, viz. (1) the nature of the vital phenomena which take place in the
ovum during its occurrence, which may be described as the internal
phenomena of segmentation. (2) The external characters of the
segmentation.

Internal Phenomena of Segmentation.
Numerous descriptions have been given during the last few years of the
internal phenomena of segmentation. The most recent contribution on this
head is that of Fol (No. 87). He appears to have been more successful than
other observers in obtaining a complete history of the changes which take
place, and it will therefore be convenient to take as type the ovum of
Toxopneustes (Echinus) lividus, on which he made his most complete series
of observations. The changes which take place may be divided into a series
of stages. The ovum immediately after the fusion of the male and female
pronucleus contains a central segmentation nucleus.
In the first stage a clear protoplasmic layer derived from the plasma of the
cell is formed round the nucleus, from which there start outwards a number
of radial striæ, which are rendered conspicuous by the radial arrangement of
the yolk granules between them. The nucleus during this process remains
perfectly passive.
In the second stage the nucleus becomes less distinct and somewhat
elongated, and around it the protoplasmic layer of the earlier stage is
arranged in the form of a disc-shaped ring, compared by Fol to Saturn’s
ring. The protoplasmic rays still take their origin from the perinuclear
protoplasm. This stage has a considerable duration (20 minutes).

In the third stage the protoplasm around the nucleus becomes transported to
the two nuclear poles, at each of which it forms a clear mass surrounded by
a star-shaped figure formed by radial striæ. The nucleus is hardly visible in
the fresh condition, but when brought into view by reagents is found to
contain many highly refractive particles, and to be still enveloped in a
membrane.
In the fourth stage the nucleus when treated by reagents has assumed the
well-known spindle form. The striæ of which it is composed are continuous
from one end of the spindle to the other and are thickened at the centre. The
central thickenings constitute the so-called nuclear plate. The clear
protoplasmic masses and stars are present as before at the apices of the
nucleus, and the rays of the latter converge as if they would meet at the
centre of the clear masses, but stop short at their periphery. There is no trace
of a membrane round either the nuclear spindle or the clear masses; and in
the centre of the latter is a collection of granules. The striæ of the polar stars
are very fine but distinct.
Between the stage with a completely formed spindle and the previous one
the intermediate steps have not been made out for Toxopneustes; but for
Heteropods Fol has been able to demonstrate that the striæ of the spindle
and their central thickenings are formed, as in the case of the spindle
derived from the germinal vesicle, from the metamorphosis of the nuclear
reticulum. They commence to be formed at the two poles, and are then (in
Heteropods) in immediate contiguity with the striæ of the stars. The striæ
gradually grow towards the centre of the nucleus and there meet.
In the fifth stage the central thickenings of the spindle separate into two
sets, which travel symmetrically outwards towards the clear masses,
growing in size during the process. They remain however united for a short
time by delicate filaments—named by Fol connective filaments—which
very soon disappear. The clear masses also increase in size. During this
stage the protoplasm of the ovum exhibits active amœboid movements
preparatory to division.
In the sixth stage, which commences when the central thickenings of the
spindle have reached the clear polar masses, the division of the ovum into
two parts is effected by an equatorial constriction at right angles to the long

axis of the nucleus. The inner vitelline membrane follows the furrow for a
certain distance, but does not divide with the ovum. All connection between
the two parts of the spindle becomes lost during this stage, and the
thickenings of the fibres of the spindle give rise to a number of spherical
vesicular bodies, which pass into the clear masses and become intermingled
with the granules which are placed there. The radii of the stars now extend
round the whole circumference of each of the clear masses.
In the seventh stage the two clear masses become elongated and travel
towards the outer sides of their segments; while the radii connected with
them become somewhat bent, as if a certain amount of traction had been
exercised on them in the movement of the clear masses. Shortly afterwards
the spherical vesicles, each of which appears like a small nucleus and
contains a central nucleolus, begin to unite amongst themselves, and to
coalesce with the neighbouring granules. Those in each segment finally
unite to form a nucleus which absorbs the substance of the clear mass. The
new nucleus is therefore partly derived from the division of the old one and
partly from the plasma of the cell. The two segments formed by division are
at first spherical, but soon become flattened against each other. In each
subsequent division of these cells the whole of the above changes are
repeated.
The phenomena which have just been described would appear to occur in
the segmentation of ova with remarkable constancy and without any very
considerable variations.
The division of the ovum constitutes a special case of cell division, and it is important to determine to
what extent the phenomena of ordinary cell division are related to those which take place in the
division of the ovum. Without attempting a full discussion of the subject I will confine myself to a
few remarks suggested by the observations of Flemming, Peremeschko and Klein. The observations
of these authors shew that in the course of the division of nuclei in the salamander, newt, etc. the
nuclear reticulum undergoes a series of peculiar changes of form, and after the membrane of the
nucleus has vanished divides into two masses. The masses form the basis for the new nuclei, and
become reconverted into an ordinary nuclear reticulum after repeating, in the reverse order, the
changes of form undergone by the reticulum previous to its division.
It is clear without further explanation that the conversion of the nuclear reticulum of the
segmentation nucleus into the striæ of the spindle is a special case of the same phenomenon as that
first described by Flemming in the salamander. There are however some considerable differences. In
the first place the fibres in the salamander do not, according to Flemming, unite in the middle line,
though they appear to do so in the newt. This clearly cannot be regarded as a fact of great
importance; nor can the existence of the central thickenings of the striæ (nuclear plate), constant as it
is for the division of the nucleus of the ovum, be considered as constituting a fundamental difference

between the two cases. More important is the fact that the striæ in the case of the ovum do not
appear, at any rate have not been shewn, to form themselves again into a nuclear network.
With reference to the last point it is however to be borne in mind (1) that the gradual travelling
outwards of the two halves of the nuclear plate is up to a certain point a repetition, in the reverse
order, of the mode of formation of the striæ of the spindle, since the striæ first appeared at the poles
and gradually grew towards the middle of the spindle; (2) that there is still considerable doubt as to
how the vesicular bodies formed out of the nuclear plate reconstitute themselves into a nucleus.
The layer of clear protoplasm around the nucleus during its division has its homologue in the case of
the division of the nuclei of the salamander, and the rays starting from this are also found. Klein has
suggested that the extra-nuclear rays of the stars around the poles of the nucleus are derived from a
metamorphosis of the extra-nuclear reticulum, which he believes to be continuous with the intra-
nuclear reticulum.
The delicate connective filaments usually visible between the two halves of the nuclear plate would
seem from Strasburger’s latest observations (No. 104) to be derived from the nuclear substance
between the striæ of the spindle, and to become eventually reabsorbed into the newly-formed nuclei.

We are it appears to me still in complete ignorance as to the physical causes
of segmentation. The view that the nucleus is a single centre of attraction,
and that by its division the centre of attraction becomes double and thereby
causes division, appears to be quite untenable. The description already
given of the phenomena of segmentation is in itself sufficient to refute this
view. Nor is it in the least proved by the fact (shewn by Hallez) that the
plane of division of the cell always bears a definite relation to the direction
of the axis of the nucleus.
The arguments by which Kleinenberg (93) attempted to demonstrate that
cell division was a phenomenon caused by alterations in the molecular
cohesion of the protoplasm of the ovum still in my opinion hold good, but
recent discoveries as to the changes which take place in the nucleus during
division probably indicate that the molecular changes which take place in
the cohesion of the protoplasm are closely related to, and possibly caused
by, those in the nucleus. These alterations of cohesion are produced by a
series of molecular changes, the external indications of which are to be
found in the visible alterations in the constitution of the body of the cell and
of the nucleus prior to division.

Bibliography.
In addition to the papers cited in the last Chapter, vide

(101) W. Flemming. “Beiträge z. Kenntniss d. Zelle u. ihrer Lebenserscheinungen.” Archiv f. mikr.
Anat., Vol. XVI., 1878.
(102) E. Klein. “Observations on the glandular epithelium and division of nuclei in the skin of the
Newt.” Quart. J. of Micr. Science, Vol. XIX., 1879.
(103) Peremeschko. “Ueber d. Theilung d. thierischen Zellen.” Archiv f. mikr. Anat., Vol. XVI., 1878.
(104) E. Strasburger. “Ueber ein z. Demonstration geeignetes Zelltheilungs-Object.” Sitz. d.
Jenaischen Gesell. f. Med. u. Naturwiss., July 18, 1879.

External Features of Segmentation.

Fig. 38. Various stages in process of segmentation.
(After Gegenbaur.)

In the simplest known type of segmentation the ovum first of all divides
into two, then four, eight, sixteen, thirty-two, sixty-four, etc. cells (fig. 38).
These cells so long as they are fairly large are usually known as segments or
spheres. At the close of such a simple segmentation the ovum becomes
converted into a sphere composed of segments of a uniform size. These
segments usually form a wall (fig. 39, E), one row of cells thick, round a
central cavity, which is known as the segmentation cavity or cavity of Von
Baer. Such a sphere is known as a blastosphere. The central cavity usually
appears very early in the segmentation, in many cases when only four
segments are present (fig. 39, B).

Fig. 39. The Segmentation of Amphioxux.
(Copied from Kowalevsky.)
sg. segmentation cavity. A. Stage with two equal segments. B. Stage with four equal
segments. C. Stage after the four segments have become divided by an equatorial furrow into
eight equal segments. D. Stage in which a single layer of cells encloses a central segmentation
cavity. E. Somewhat older stage in optical section.

In other instances, which however are rarer than those in which a
segmentation cavity is present, there is no trace of a central cavity, and the
sphere at the close of segmentation is quite solid. In such instances the solid
sphere is known as a morula. It is found in some Sponges, many
Cœlenterata, some Nemertines, etc., and in Mammals; in which group the
segmentation is not however quite regular. All intermediate conditions
between a large segmentation cavity, and a very minute central cavity which
may be surrounded by more than a single row of cells have been described.
The segmentation cavity has occasionally, as in Sycandra, the Ctenophora and Amphioxus, the form
of an axial perforation of the ovum open at both extremities.

When the process of regular segmentation is examined somewhat more in
detail it is found to follow as a rule a rather definite rhythm. The ovum is
first divided in a plane which may be called vertical, into two equal parts
(fig. 39, A). This division is followed by a second, also in a vertical plane,
but at right angles to the first plane, and by it each of the previous segments
is halved (fig. 39, B.) In the third segmentation the plane of division is
horizontal or equatorial and divides each of the four segments into two
halves, making eight segments in all (fig. 39, C). In the fourth period the
segmentation takes place in two vertical planes each at an angle of 45° with
one of the previous vertical planes. All the segments are thus again divided
into two equal parts. In the fifth period there are two equatorial planes one
on each side of the original equatorial plane, and thirty-two spheres are
present at the close of this period. Sixty-four segments are formed at the
sixth period, but beyond the fourth and fifth periods the original regularity
is not usually preserved.
In many instances the type of segmentation just described cannot be distinctly recognized. All that
can be noticed is that at each fresh segmentation every segment becomes divided into two equal
parts. It is not absolutely certain that there is not always some slight inequality in the segments
formed, by which, what are known as the animal and vegetative poles of the ovum, can very early be
distinguished. A regular segmentation is found in species in most groups of the animal kingdom. It is

very common in Sponges and Cœlenterates. Though less common so far as is known amongst the
Vermes, it is yet found in many of the lower types, viz. Nematoidea, Gordiacea, Trematoda,
Nemertea (apparently as a rule), Sagitta, Chætonotus, some Gephyrea (Phoronis); though not usual it
occurs amongst Chætopoda, e.g. Serpula. It is the usual type of segmentation amongst the
Echinodermata. Amongst the Crustacea it appears (for the earlier phases of segmentation at any rate)
not infrequently amongst the lower forms, and even occurs amongst the Amphipoda (Phronima). It is
however very rare amongst the Tracheata, Podura affording the one example of it known to me. It is
almost as rare amongst Mollusca as amongst the Tracheata, but occurs in Chiton and is nearly
approached in some Nudibranchiata. In Vertebrata it is most nearly approached in Amphioxus[36].

Most of the eggs which have a perfectly regular segmentation are of a very
insignificant size and rarely contain much food-yolk: in the vast majority of
eggs there is present however a considerable bulk of food material usually
in the form of highly refracting yolk-spherules. These yolk-spherules lie
embedded in the protoplasm of the ovum, but are in most instances not
distributed uniformly, being less closely packed and smaller at one pole of
the ovum than elsewhere. Where the yolk-spherules are fewest the active
protoplasm is necessarily most concentrated, and we can lay down as a
general law[37] that the velocity of segmentation in any part of the ovum is
roughly speaking proportional to the concentration of the protoplasm there;
and that the size of the segments is inversely proportional to the
concentration of the protoplasm. Thus the segments produced from that part
of an egg where the yolk-spherules are most bulky, and where therefore the
protoplasm is least concentrated, are larger than the remaining segments,
and their formation proceeds more slowly.
Though where much food-yolk is present it is generally distributed
unequally, yet there are many cases in which it is not possible to notice this
very distinctly. In most of these cases the segmentation is all the same
unequal, and it is probable that they form apparent rather than real
exceptions to the law laid down above. Although before segmentation the
protoplasm may be uniformly distributed, yet in many instances, e.g.
Mollusca, Vermes, etc., during or at the commencement of segmentation the
protoplasm becomes aggregated at one pole, and one of the segments
formed consists of clear protoplasm, all the food-yolk being contained in
the other and larger segment.
Unequal Segmentation. The type of segmentation I now proceed to
describe has been called by Haeckel (No. 105) ‘unequal segmentation’, a

term which may conveniently be adopted. I commence by describing it as it
occurs in the well-known and typical instance of the Frog[38].
The ripe ovum of the common Frog and of most other tailless Amphibians
presents the following structure. One half appears black and the other white.
The former I shall call the upper pole, the latter the lower. The ovum is
composed of protoplasm containing in suspension numerous yolk-
spherules. The largest of these are situated at the lower pole, the smaller
ones at the upper pole, and the smallest of all in the peripheral layer of the
upper pole, in which also pigment is scattered and causes the black colour
visible from the surface.

Fig. 40. Segmentation of Common Frog. Rana Temporaria. (Copied from Ecker.)
The numbers above the figures refer to the number of segments at the stage figured.

The first formed furrow is a vertical furrow. It commences in the upper half
of the ovum, through which it extends rapidly, and then more slowly
through the lower. As soon as the first furrow has extended through the egg,
and the two halves have become separated from each other, a second
vertical furrow appears at right angles to the first and behaves in the same
way (fig. 40, 4).

Fig. 41. Section through Frog’s ovum at the close of segmentation.
sg. segmentation cavity. ll. large yolk-containing cells. ep. small cells at formative pole
(epiblast).

The next furrow is equatorial or horizontal (fig. 40, 8). It does not arise at
the true equator of the egg, but much nearer to its upper pole. It extends
rapidly round the egg and divides each of the four previous segments into
two parts, one larger and one smaller. Thus at the end of this stage there are
present four small and four large segments. At the meeting point of these a
small cavity appears, which is the segmentation cavity, already described
for uniformly segmenting eggs. It increases in size in subsequent stages, its
roof being formed of the smaller cells and its floor of the larger. The
appearance of the equatorial furrow is followed by a period of repose, after
which two rapidly succeeding vertical furrows are formed in the upper pole,
dividing each of the four segments of which this is composed into two.
After a short period these furrows extend to the lower pole, and when
completed 16 segments are present—eight larger and eight smaller (fig. 40,
16). A pause now ensues, after which the eight upper segments become
divided by an equatorial furrow, and somewhat later a similar furrow
divides the eight lower segments. At the end of this stage there are therefore
present 16 smaller and 16 larger segments (fig. 40, 32). After 64 segments
have been formed by vertical furrows which arise symmetrically in the two
poles (fig. 40, 64), two equatorial furrows appear in the upper pole before a
fresh furrow arises in the lower; so that there are 128 segments in the upper
half, and only 32 in the lower. The regularity is quite lost in subsequent

stages, but the upper pole continues to undergo a more rapid segmentation
than the lower. While the segments have been increasing in number the
segmentation cavity has been rapidly growing in size; and at the close of
segmentation the egg forms a sphere, containing an excentric cavity, and
composed of two unequal parts (fig. 41). The upper part, which forms the
roof of the segmentation cavity, is formed of smaller cells: the lower of
larger yolk-containing cells.
The mode of segmentation of the Frog’s ovum is typical for unequally
segmenting ova, and it deserves to be noticed that as regards the first three
or more furrows the segmentation occurs with the same rhythm in the
unequally segmenting ova as in those which have an uniform segmentation.
There appear two vertical furrows followed by an equatorial furrow. The
general laws which were stated with reference to the velocity of
segmentation and the size of the resulting segments are well exemplified in
the case of the Frog’s ovum.
The majority of the smaller segments in the segmented Frog’s ovum are
destined to form into the epiblast, and the larger segments become
hypoblast and mesoblast.
With a few exceptions (the Rabbit, Lymnæus, etc.) the majority of the smaller segments always
become epiblast and of the larger segments hypoblast.

The Frog’s ovum serves as a good medium type for unequally segmenting
ova. There are many cases however in which a regular segmentation is far
more closely approached, and others in which it is less so.
One familiar instance in which a regular segmentation is nearly approached
is afforded by the Rabbit’s ovum, which has indeed usually been regarded
as offering an example of a regular segmentation.
The ovum of the Rabbit[39] becomes first divided into two sub-equal
spheres. The larger and more transparent of the two may, from its eventual
fate, be called the epiblastic sphere, and the other the hypoblastic. The two
spheres are divided into four, and then by an equatorial furrow into eight—
four epiblastic and four hypoblastic. One of the latter assumes a central
position. The four epiblastic spheres now divide before the four hypoblastic.
There is thus introduced a stage with twelve spheres. It is followed by one
with sixteen, and that by one with twenty-four. During the stages with

sixteen spheres and onwards the epiblastic spheres gradually envelop the
hypoblastic, which remain exposed on the surface at one point only. There
is no segmentation cavity.
In Pedicellina, one of the entoproctous Polyzoa, there is a sub-regular
segmentation, where however the two primary spheres can be distinguished
much in the same way as in the case of the Rabbit.
A very characteristic type of unequal segmentation is that presented by the
majority of Gasteropods and Pteropods and probably also of some
Lamellibranchiata. It is also found in some Turbellarians, in Bonellia, some
Annelids, etc. In many instances it offers a good example of the type where
in the course of segmentation the protoplasm becomes aggregated at one
pole of the ovum, or of its segments, to become separated off as a clear
sphere.
The first four segments formed by two vertical furrows at right angles are
equal, but from these there are budded off four smaller segments, which in
subsequent stages divide rapidly, receiving however, a continual accession
of segments budded off from the larger spheres. The four larger spheres
remain conspicuous till near the close of the segmentation. The process of
budding, by which the smaller spheres become separated from the larger,
consists in a larger sphere throwing out a prominence, which then becomes
constricted off from it.
In the extreme forms of this unequal segmentation we find at the end of the
second cleavage two larger spheres filled with yolk material and two
smaller clear spheres; and in the later stages, though the large spheres
continue to bud off small spheres, only the two smaller ones undergo a
regular segmentation, and eventually completely envelop the former. Such a
case as this has been described in Aplysia by Lankester[40].
The types I have described serve to exemplify unequal segmentation. The
Rabbit’s ovum stands at one end of the series, that of Aplysia at the other;
and the Frog’s ovum between the two.
Great variations are presented by the ova with unequal segmentation as to
the presence of a segmentation cavity. In some instances, e.g. the Frog, such

a cavity is well developed. In other cases it is small, e.g. most Mollusca,
while not unfrequently it is altogether absent.
Before leaving this important type of segmentation, it will be well to enter with slightly greater detail
into some of the more typical as well as some of the special forms which it presents.
As an example of the typical Molluscan type the normal Heteropod segmentation, accurately
described by Fol[41], may be selected.
The ovum divides into two and then four equal segments in the usual vertical planes. Each segment
has a protoplasmic and a vitelline pole. The protoplasmic pole is turned towards the polar bodies. In
the third segmentation, which takes place along an equatorial plane, four small protoplasmic cells or
segments are segmented or rather budded off from the four large segments, so that there are four
small segments in one plane and four large below these. In the fourth segmentation the four large
segments alone are active and give rise to four small and four large cells; so that there are formed in
all eight small and four large cells. The four small cells of the third generation next divide, forming in
all twelve small cells and four large. The small cells of the fourth generation then divide, and
subsequently the four large cells give rise to four new small ones, so that there are twenty small cells
and four large. The small cells form a cap embracing the upper pole of the large segments. It may be
noted that from the third stage onwards the cells increase in arithmetical progression—a
characteristic feature of the typical gasteropod segmentation.
In the later stages of segmentation the large cells cease to give rise to smaller ones in the same
manner as before. One of them divides first into two unequal parts, of which the smaller becomes
pushed in towards the centre of the egg. The larger cell then divides again into two, and the three
cells so formed occupy the centre of a shallow depression. The remaining larger cells divide in the
same way, and give rise to smaller cells which line a pit which becomes formed on one side of the
ovum. The original smaller cells continue in the meantime to divide and so form a layer enclosing the
larger, leaving exposed however the opening of the pit lined by the latest products of the larger cells.
The eggs of Anodon and Unio serve as excellent examples of the type in which the ovum has a
uniform structure before the commencement of segmentation, but in which a separation into a
protoplasmic and a nutritive portion becomes obvious during segmentation.

In Anodon[42] the egg is at first uniformly granular, but after impregnation it throws out on one side a
protuberance nearly free from granules (fig. 42, 1)

Fig. 42. Segmentation of Anodon piscinalis. (Copied from Flemming.) r. polar cells. v.
vitelline sphere. 1. Commencing division into two segments; one mainly formed of protoplasm,

the other of yolk. 2. Stage with four segments. 3. Formation of blastosphere, and segmentation
cavity. 4. Definite segmentation of the yolk sphere.

In the case of this clear protuberance and of the similar protuberances which follow it, the protoplasm
is not at first quite free from food-yolk, but only becomes so on being separated from the yolk-
containing part of the ovum. We must therefore suppose that the production of the clear segments is
in part at least due to the yolk-spherules becoming used up to form protoplasm. Such a formation of
protoplasm from yolk-spherules has been clearly shewn to occur in other types by Bobretzky and Fol.
The protuberance soon becomes separated off from the larger part of the egg as a small segment
composed of clear protoplasm. From the larger segment filled with food-yolk, a second small clear
segment is next budded off, and simultaneously (fig. 42, 2) the original small segment divides into
two. Thus there are formed four segments, one large and three small; the large segment as before
being filled with food-yolk. The continuation of a similar process of budding off and segmentation
eventually results in the formation of a considerable number of small and of one large segment (fig.
42, 3). Between this large and the small segments is a segmentation cavity.
Eventually the large yolk segment, which has hitherto merely budded off a series of small segments
free from yolk, itself divides into two similar parts. This process is then repeated (fig. 42, 4) and there
is at last formed a number of yolk segments filled with yolk spheres, which occupy the place of the
original large yolk segment. Between these yolk segments and the small segments is placed the
segmentation cavity.

The segmentation of the ovum of Euaxes[43] resembles that of Unio in the budding off of clear
segments from those filled with yolk, but presents many interesting individualities.
A very peculiar modification of the ordinary Gasteropod segmentation is that described by Bobretzky
for Nassa mutabilis[44].
The ovum contains a large amount of food-yolk, and the protoplasm is aggregated at the formative
pole, adjoining which are placed the polar bodies. An equatorial and a vertical furrow (fig. 43 A), the
former near the upper pole, appear simultaneously, and divide the ovum into three segments, two
small, each with a protoplasmic pole, and one large entirely formed of yolk material. One of the two
small segments next completely fuses with the large segment (fig. 43 B), and after the fusion is
complete, a triple segmentation of the large segment takes place as at the first division, and at the
same time the single small segment divides into two. In this way four partially protoplasmic
segments and one yolk segment are formed (fig. 43 C). One of the small segments again fuses with
the large segment, so that the number of segments becomes again reduced to four, three small and
one large. The protoplasmic ends of these segments are turned towards each other, and where they
meet four very small cells become budded off, one from each segment (fig. 43 D). Four small cells
are again budded off twice in succession, while the original small cells remain passive, so that there
come to be twelve small and four large cells. In later stages the four first-formed small cells give rise
to still smaller cells and then the next-formed do the same. The large cells continue also to give rise
to small ones, and finally, by a continuous process of division, and fresh budding of small cells from
large cells, a cap of small cells becomes formed covering the four large cells which have in the
meantime pressed themselves together (fig. 43 E). A segmentation cavity of not inconsiderable
dimensions becomes established between this cap of small cells and the large cells.

Fig. 43. Segmentation of Nassa mutabilis (from Bobretzky). A. Upper half divided into two
segments. B. One of these has fused with the large lower segment. C. Four small and one large
segment, one of the former fusing with the large segment. D. Each of the four segments has
given rise to a small segment. E. Small segments have increased to thirty-six.

Many eggs, such as those of the Myriapods[45], present an irregular segmentation; but the
segmentation is hardly unequal in the sense in which I have been using the term. Such cases should
perhaps be placed in the first rather than in the present category.
The type of unequal segmentation is on the whole the most widely distributed in the animal kingdom.
There is hardly a group without examples of it.
It occurs in Porifera, Hydrozoa, Actinozoa and Ctenophora. Amongst the Ctenophora this
segmentation is of the most typical kind. Four equal segments are first formed in the two first
periods. In the third period a circumferential furrow separates four smaller from four larger segments.
This type is also widely distributed amongst the unsegmented (Gephyrea, Turbellaria), as well as the
segmented Vermes, and is typical for the Rotifera. It appears to be very rare in Echinoderms
(Echinaster Sarsii). It is not uncommon in early stages of the segmentation of the lower Crustacea.
For Mollusca (except Cephalopoda) it is typical. Amongst the Ascidia it occurs in several forms
(Salpa, Molgula) and amongst the Craniata it is typical in the Cyclostomata, Amphibia, and some
Ganoids, e.g. Accipenser.

Partial segmentation. The next type of segmentation we have to deal with
has long been recognized as partial segmentation. It is a type in which only

part of the ovum, called the germinal disc, undergoes segmentation, the
remainder usually forming an appendage of the embryo known as the yolk-
sack. Ova belonging to the two groups already dealt with are frequently
classed together as holoblastic ova, in opposition to ova of the present
group in which the segmentation is only partial, and which are therefore
called meroblastic. For embryological purposes this is in many ways a very
convenient classification, but ova belonging to the present group are in
reality separated by no sharp line from those belonging to the group just
described.

Fig. 44. Surface views of the early stages of the segmentation in a fowl’s egg.
(After Coste.)
a. edge of germinal disc. b. vertical furrow. c. small central segment. d. larger peripheral
segment.

The origin and nature of meroblastic ova will best be understood by taking
an ovum with an unequal segmentation, such as that of the frog, and
considering what would take place in accordance with the laws already laid
down, supposing the amount of food-yolk at the vitelline pole to be
enormously increased. What would happen may be conveniently illustrated
by fig. 44, representing the segmentation of a fowl’s egg. There would first
obviously appear a vertical furrow at the formative or protoplasmic pole.
(Fig. 44 A, b.) This would gradually advance round the ovum and
commence to divide it into two halves. Before the furrow had however
proceeded very far it would come to the vitelline part of the ovum; here,
according to the law previously enunciated, it would travel very slowly, and
if the amount of the food-yolk was practically infinite as compared with the

protoplasm, it would absolutely cease to advance. A second vertical furrow
would soon be formed, crossing the first at right angles, and like it not
advancing beyond the edge of the germinal disc. (Fig. 44 B.)
The next furrow should be an equatorial one (as a matter of fact in the
fowl’s ovum an equatorial furrow is not formed till after two more vertical
furrows have appeared). The equatorial furrow would however, in
accordance with the analogy of the frog, not be formed at the equator, but
very close to the formative pole. It would therefore separate off as a distinct
segment (fig. 44 C, c), a small central, i.e. polar, portion of each of the
imperfect segments formed by the previous vertical furrows. By a
continuation of the process of segmentation, with the same alternation of
vertical and equatorial furrows as in the frog, a cap or disc of small
segments would obviously be formed at the protoplasmic pole of the ovum,
outside which would be a number of deep radiating grooves (fig. 45),
formed by the vertical furrows, the advance of which round the ovum has
come to an end owing to the too great proportion of yolk spheres at the
vitelline pole.

Fig. 45. Surface view of the germinal disc of fowl’s egg during a late stage of the
segmentation.

c. small central segmentation spheres; b. larger segments outside these; a. large, imperfectly
circumscribed, marginal segments; e. margin of germinal disc.

It is clear from the above that an immense accumulation of food-yolk at the
vitelline pole necessarily causes a partial segmentation. It is equally clear

that the part of meroblastic ova which does not undergo segmentation is not
a new addition absent in other cases. It is on the contrary to be regarded
merely as a part of the ovum in which the yolk-spherules have attained to a
very great bulk as compared with the protoplasm; sometimes even to the
complete exclusion of the protoplasm.
An ordinary meroblastic ovum consists then of a small disc at the formative
pole, known as the germinal disc, composed mainly of protoplasm in which
comparatively little food-yolk is present. This graduates into the remainder
of the ovum, being separated from it by a more or less sharp line. This
remainder of the ovum, which almost always forms the major part, usually
consists of numerous yolk-spherules, embedded in a very scanty
protoplasmic matrix.
In some cases, e.g. the eggs of Elasmobranchii[46], the protoplasm is present in the form of a delicate
network; in other and perhaps the majority of cases, too little protoplasm is present to be detected, or
the protoplasm may even be completely absent. In some Osseous Fishes, e.g. Lota, the yolk forms a
homogeneous transparent albuminoid substance containing a large globule at the pole furthest
removed from the germinal disc. In this case the germinal disc is sharply separated from the yolk. In
other Osseous Fishes the separation between the two parts is not so sharp[47]. In these cases we find
adjoining the germinal disc a finely granular material containing a large proportion of protoplasm;
this graduates into a material with very little protoplasm and numerous yolk-spherules, which is in its
turn continuous with an homogeneous albuminoid yolk substance. In Elasmobranchii we find that
immediately beneath the germinal disc there is present a finely granular matter, rich in protoplasm,
which is continuous with the normal yolk.
The Elasmobranch ovum may conveniently serve as type for the Vertebrata. The ovum is formed of a
spherical vitellus without any investing membrane. The germinal disc is recognizable on this as a
small yellow spot about 1½ millimetres in diameter. In the germinal disc a furrow appears bisecting
the disc, followed by a second furrow at right angles to the first. Thus after the formation of the
second furrow the disc is divided into four equal areas. Fresh furrows continue to rise, and eventually
a circular furrow, equivalent to the equatorial furrow of the frog’s ovum, makes its appearance, and
separates off a number of smaller central segments from peripheral larger segments. In the later
stages the smaller segments at first divide more rapidly than the larger, but eventually the latter also
divide rapidly, and the germinal disc becomes finally formed of a series of segments of a fairly
uniform size. So much may be observed in surface views of the segmenting ovum, and it may be
noted that there is not much difference to be observed between the segmentation of the germinal disc
of the Fowl’s ovum and that of the Elasmobranchii. Indeed the figure of the former (fig. 44) would
serve fairly well for the latter. When however we examine the segmenting germinal discs by means
of sections, there are some differences between the two types, and several interesting features which
deserve to be noticed in the segmentation of the Elasmobranchii. In the first stages the furrows
visible on the surface are merely furrows, which do not meet so as to isolate distinct segments; they
merely, in fact, form a surface pattern. It is not till after the appearance of the equatorial furrow that
the segments begin to be distinctly isolated. In the subsequent stages not only do the segments
already existing in the germinal disc increase by division, but fresh segments are continually being
formed from the adjacent yolk, and added to those already present in the germinal disc. (Fig. 46.)

This fact is one out of many which prove that the germinal disc is merely part of the ovum
characterized by the presence of more protoplasm than the remainder which forms the so-called food-
yolk. During the latest stages of segmentation there appear in the yolk around the blastoderm a
number of nuclei. (Fig. 46, nx´.) These are connected with a special protoplasmic network (already
described) which penetrates through the yolk. Towards the end of segmentation, and during the early
periods of development which succeed the segmentation, these nuclei become very numerous. (Fig.
47 A, n´.) Around many of them a protoplasmic investment is established, and cells are thus formed
which eventually enter the blastoderm.

Fig. 46. Section through germinal disc of a Pristiurus embryo during the segmentation.
n. nucleus; nx. nucleus modified prior to division; nx´. modified nucleus of the yolk; f. furrow
appearing in the yolk adjacent to the germinal disc.

The result of segmentation is the formation of a lens-shaped mass of cells lying in a depression on the
yolk. In this a cavity appears, the homologue of the segmentation cavity already spoken of. It lies at
first in the midst of the cells of the blastoderm, but very soon its floor of cells vanishes, and it lies
between the yolk and the blastoderm. (Fig. 47 A.) Its subsequent history is given in a future Chapter.
Segmentation proceeds in Osseous Fishes in nearly the same manner as in Elasmobranchii. In some
cases the germinal disc is small as compared with the yolk, in other cases it is almost as large as the
yolk. The only points which deserve special notice are the following: (1) Nuclei, precisely similar to
those in the Elasmobranch yolk, appear in the protoplasmic matter around the germinal disc; (2) After
the deposition of the ova there is present in some forms a network of protoplasm extending from the
germinal disc through the yolk[48]. At impregnation this withdraws itself from the yolk. It is to be
compared to the protoplasmic network of the Elasmobranch ovum.

Fig. 47. Two longitudinal sections of the blastoderm of a Pristiurus embryo at stages
prior to the formation of the medullary groove.

ep. epiblast; ll. lower layer cells; m. mesoblast; hy. hypoblast; sc. segmentation cavity; es.
embryo swelling; n´. nuclei of yolk; er. embryonic rim.

There are two types of meroblastic ova. In one of these (Aves,
Elasmobranchii) the germinal disc is formed in the ovarian ovum. In the
second type the germinal disc is formed after impregnation by a
concentration of the protoplasm at one pole. This concentration is
analogous to what has already been described for Anodon and other
Molluscan ova (p. 100).
The ova of some Teleostei are intermediate between the two types.
The ovum of the wood-louse, Oniscus murarius[49], may be taken as an example of the second type
of meroblastic ovum. In this egg development commences by the appearance of a small clear mass
with numerous transparent vesicles. This mass is the protoplasm which has become separated from
the yolk. It undergoes segmentation in a perfectly normal fashion. Examples of other cases of this
kind have been described by Van Beneden and Bessels[50] in Anchorella, and in Hessia by Van
Beneden[51]. It appears from their researches that the protoplasm collects itself together, first of all in
the interior of the egg, and then travels to the surface. It arrives at the surface after having already
divided into two or more segments, which then rapidly divide in the usual manner to form the
blastoderm.
There are some grounds for thinking that the cases of partial segmentation in the Arthropoda are not
really quite comparable with those in other groups, but more probably fall under the next type of
segmentation to be described. The grounds for this view are mentioned in connection with the next
type.

In most if not all meroblastic ova there appear during and after
segmentation a number of nuclei in the yolk adjoining the blastoderm,

around which cells become differentiated. (Figs. 46 and 47.) These cells
join the part of the blastoderm formed by the normal segmentation of the
germinal disc. Such nuclei are formed in all craniate meroblastic ova[52]. In
Cephalopods they have been found by Lankester, and in Oniscus by
Bobretzky. They have been by some authors supposed to originate from the
nuclei of the blastoderm, and by others spontaneously in the yolk.
Some of the earliest observations on these nuclei were made by Lankester[53] in the Cephalopods. He
found that they appeared first in a ring-like series round the edge of the blastoderm, and subsequently
all over the yolk in a layer a little below the surface. He observed their development in the living
ovum and found that they “commenced as minute points, gradually increasing in size like other free-
formed nuclei.” A cell area subsequently forms around them.

By E. van Beneden[54] they were observed in a Teleostean ovum to appear nearly simultaneously in
considerable numbers in the granular matter beneath the blastoderm. Van Beneden concludes from
the simultaneous appearance of these bodies that they develop autogenously. Kupffer at an earlier
period arrived at a similar conclusion. My own observations on these nuclei in Elasmobranchii on the
whole support the conclusions to be derived from Lankester’s, Kupffer’s and Van Beneden’s
observations. As mentioned above, the nuclei in Elasmobranchii do not appear simultaneously, but
increase in number as development proceeds; and it is possible that Van Beneden may be mistaken on
this point. No evidence came before me of derivation from pre-existing nuclei in the blastoderm. My
observations prove however that the nuclei increase by division. This is shewn by the fact that I have
found them with the spindle modification (fig. 46, nx´), and that in most cases they usually exhibit
the form of a number of aggregated vesicles[55], which is a character of nuclei which have just
undergone division. It should be mentioned however that I failed to find a spindle modification of the
nuclei in the later stages. Against these observations must be set those of Bobretzky, according to
which the nuclei in Oniscus are really the nuclei of cells which have migrated from the blastoderm.
Bobretzky’s observations do not however appear to be very conclusive.

It must be admitted that the general evidence at our command appears to
indicate that the nuclei of the yolk in meroblastic ova originate
spontaneously. There is however a difficulty in accepting this conclusion in
the fact that all the other nuclei of the embryo are descendants of the first
segmentation nucleus; and for this reason it still appears to me possible that
the nuclei of the yolk will be found to originate from the continued division
of one primitive nucleus, itself derived from the segmentation nucleus.
The existence of these nuclei in the yolk and the formation of a distinct cell
body around them is a strong piece of evidence in favour of the view above
maintained, (which is not universally accepted,) that the part of the ovum of
meroblastic ova which does not segment is of the same nature as that which
does segment, and differs only in being relatively deficient in active
protoplasm.

The following forms have meroblastic ova of the first type: the Cephalopoda, Pyrosoma,
Elasmobranchii, Teleostei, Reptilia, Aves, Ornithodelphia (?). The second type of meroblastic
segmentation occurs in many Crustacea, (parasitic Copepoda, Isopoda Mysis, etc.). It is also stated to
be found in Scorpio.

The ova of the majority of groups in the animal kingdom segment
according to one of the types which have just been described. These types
are not sharply separated, but form an unbroken series, commencing with
the ovum which segments uniformly, and ending with the meroblastic
ovum.
It is convenient to distinguish the ova which segment uniformly by some
term; and I should propose for this the term alecithal[56], as implying that
they are without food-yolk, or that what little food-yolk there is, is
distributed uniformly.
The ova in which the yolk is especially concentrated at one pole I should
propose to call t e l o l e c i t h a l . They constitute together a group with an
unequal or partial segmentation.
The telolecithal ova may be defined in the following way: ova in which the
food-yolk is not distributed uniformly, but is concentrated at one pole of the
ovum. When only a moderate quantity of food-yolk is present the pole at
which it is concentrated merely segments more slowly than the opposite
pole; but when food-yolk is present in very large quantity the part of the
ovum in which it is located is incapable of segmentation, and forms a
special appendage known as the yolk-sack.
There is a third group of ova including a series of types of segmentation
nearly parallel to the telolecithal group. This group takes its start from the
alecithal ovum as do the telolecithal ova, and equally with these includes a
series of varieties of segmentation running parallel to the regular and
unequal types of segmentation which directly result from the presence of a
greater or smaller quantity of food-yolk. The food-yolk is however placed,
not at one pole, but at the centre of the ovum. This group of ova I propose to
name centrolecithal. It is especially characteristic of the Arthropoda, if not
entirely confined to that group.
Centrolecithal ova. As might be anticipated on the analogy of the types of
segmentation already described, the concentration of the food-yolk at the

centre of the ovum does not always take place before segmentation, but is
sometimes deferred till even the later stages of this process.
Examples of a regular segmentation in centrolecithal ova are afforded by
Palæmon (Bobretzky) and Penæus (Hæckel). A type of unequal
segmentation like that of the Frog occurs in Gammarus locusta (Beneden
and Bessels), where however the formation of a central yolk mass does not
appear to take place till rather late in the segmentation. More irregular
examples of unequal segmentation are also afforded by other Crustaceans,
e.g. various members of the genus Chondracanthus (Beneden and Bessels)
and by Myriapods. In all these cases segmentation ends in the formation of
a layer of cells enclosing a central mass of food-yolk.

Fig. 48. Segmentation of a Crustacean ovum (Penæus).
(After Hæckel.)
The sections illustrate the type of segmentation in which the yolk is aggregated at the centre
of the ovum.
yk. central yolk mass.
1 and 2. Surface view and section of the stage with four segments. In 2 it is seen that the
furrows visible on the surface do not penetrate to the centre of the ovum.
3 and 4. Surface view and section of ovum near the end of segmentation. The central yolk mass
is very clearly seen in 4.

The peculiarity of the centrolecithal ova with regular or unequal
segmentation is that (owing to the presence of the yolk in the interior) the
furrows which appear on the surface are not continued to the centre of the
egg. The spheres which are thus distinct on the surface are really united
internally. Fig. 48, copied from Hæckel, shews this in a diagrammatic way.
Many ova, which in the later stages of segmentation exhibit the
characteristics of true centrolecithal ova, in the early stages actually pass
through nearly the same phases as holoblastic ova. Thus in Eupagurus
prideauxii[57] (fig. 49), and probably in the majority of Decapods, the egg is
divided successively into two, four and eight distinct segments, and it is not
till after the fourth phase of the segmentation that the spheres fuse in the
centre of the egg. Such ova belong to a type which is really intermediate
between the ordinary type of segmentation and that with a central yolk
mass. Eupagurus presents one striking peculiarity, viz. that the nucleus
divides into two, four and eight nuclei, each surrounded by a delicate layer
of protoplasm prolonged into a reticulum, before the ovum itself
commences to become segmented. The ovum before segmentation is
therefore in the condition of a syncytium.

Fig. 49. Transverse section through four stages in the segmentation of Eupagurus
Prideauxii. (After P. Mayer.)

The segmentation of Asellus aquaticus[58] is very similar to that of Eupagurus, etc. but the ovum at
the very first divides into as many segments (viz. eight) as there are nuclei.
In Gammarus locusta the resemblance to ordinary unequal segmentation is very striking, and it is not
till a considerable number of segments have been formed that a central yolk mass appears.

In all the above types, as segmentation proceeds, the protoplasm becomes
more and more concentrated at the surface, and finally a superficial layer of
flat blastoderm cells is completely segmented off from the yolk below (fig.
49 D).
In cases like those of Penæus, Eupagurus, etc., the yolk in the interior is at
first nearly homogeneous, but at a later period it generally becomes divided
up partially or completely into a number of distinct spheres, which may
have nuclei and therefore have the value of cells. In many cases nuclei have
however not been demonstrated in these yolk spheres, though probably
present; yet, till they have been demonstrated, some doubt must remain on
the nature of these yolk spheres. It is probable that not all the nuclei which
result from the division of the first segmentation nucleus become concerned
in the formation of the superficial blastoderm, but that some remain in the
interior of the ovum to become the nuclei of the yolk spheres.

Fig. 50. Segmentation and formation of the blastoderm in Chelifer.
(After Metschnikoff.)

In A the ovum is divided into a number of separate segments. In B a number of small cells
have appeared (bl) which form a blastoderm enveloping the large yolk spheres. In C the
blastoderm has become divided into two layers.

In Myriapods (Chilognatha) a peculiar form of segmentation has been observed by Metschnikoff[59].
The ovum commences by undergoing a perfectly normal, though rather irregular total segmentation.
But after the process of division has reached a certain point, scattered masses of very small cells
make their appearance on the surface of the large spheres. These small cells have probably arisen in a
manner analogous to that which characterizes the formation of the superficial cells of the blastoderm
in the types of centrolecithal ova already described. They rapidly increase in number and eventually
form a continuous blastoderm; while the original large segments remain in the centre as the yolk
mass. In the interesting Arachnid Chelifer segmentation takes place in nearly the same manner as in
Myriapods (fig. 50).

Fig. 51. Four successive stages in the segmentation of the egg of Tetranychus Telarius.
(After Claparède.)

It is clear that it is not possible in centrolecithal ova to have any type of
segmentation exactly comparable with that of meroblastic ova. There are
however some types which fill the place of the meroblastic ova in the
present group, in as much as they are characterised by the presence of a
large bulk of food-yolk which either does not segment, or does not do so till
a very late stage in the development. The essential character of this type of
segmentation consists in the division of the germinal vesicle in the interior,
or at the surface of the ovum into two, four, etc. nuclei (fig. 51). These

nuclei are each of them surrounded by a specially concentrated layer of
protoplasm (fig. 51) which is continuous with a general protoplasmic
reticulum passing through the ovum [not shewn in fig. 51]. The yolk is
contained in the meshes of this reticulum in the manner already described
for other ova.
The ovum, like that of Eupagurus before segmentation, is now a syncytium.
Eventually the nuclei, having increased by division and become very
numerous, travel, unless previously situated there, to the surface of the
ovum. They then either simultaneously or in succession become, together
with protoplasm around them, segmented off from the yolk, and give rise to
a peripheral blastoderm enclosing a central yolk mass. In the latter however
many of the nuclei usually remain, and it also very often undergoes a
secondary segmentation into a number of yolk spheres.
The eggs of Insects afford numerous examples of this mode of
segmentation, of which the egg of Porthesia[60] may be taken as type. After
impregnation it consists of a central mass of yolk which passes without a
sharp line of demarcation into a peripheral layer of more transparent
(protoplasmic) material. In the earliest stage observed by Bobretzky there
were two bodies in the interior of the egg, each consisting of a nucleus
enclosed in a thin protoplasmic layer with stellate prolongations. This stage
corresponds with the division into two, but though the nucleus divides, the
preponderating amount of yolk prevents the egg from segmenting at the
same time. By a continuous division of the nuclei there becomes scattered
through the interior of the ovum a series of bodies, each formed of nucleus
and a thin layer of protoplasm with reticulate processes. After a certain
stage some of these bodies pass to the surface, simultaneously (in Porthesia)
or in some cases successively. At the surface the protoplasm round each
nucleus contracts itself into a rounded cell body, distinctly cut off from the
adjacent yolk.
The cells so formed give rise to a superficial blastoderm of a single layer of
cells. Many of the nucleated bodies remain in the yolk, and after a certain
time, which varies in different forms, the yolk becomes segmented up into a
number of rounded or polygonal bodies, in the interior of each of which one
of the above nuclei with its protoplasm is present. This process, known as

the secondary segmentation of the yolk, is really part of the true
segmentation, and the bodies to which it gives rise are true cells.
Other examples of this type may be cited. In Aphis[61] Metschnikoff shewed that the first
segmentation nucleus divides into two, each of which takes up a position in the clearer peripheral
protoplasmic layer of the egg (fig. 52, 1 and 2). Following upon further division the nuclei enveloped
in a continuous layer of protoplasm arrange themselves in a regular manner, and form a syncytium,
which becomes segmented into definite cells (fig. 52, 3 and 4). The existence of a special clear
superficial layer of protoplasm has been questioned by Brandt.

Fig. 52. Segmentation of Aphis Rosae. (Copied from Metschnikoff.)
In all the stages there is seen to be a central yolk mass surrounded by a layer of protoplasm.
In this protoplasm two nuclei have appeared in 1, four nuclei in 2. In 3 the nuclei have arranged
themselves regularly, and in 4 the protoplasm has become divided into a number of columnar
cells corresponding to the nuclei.
w. pole of the blastoderm which has no share in forming the embryo.

In Tetranychus telarius, one of the mites, Claparède found on the surface of the ovum a nucleus
surrounded by granular protoplasm (fig. 51); which is no doubt the first segmentation nucleus. By a
series of divisions, all on the surface, a layer of cells becomes formed round a central yolk mass. The
result here is the same as in Insects, but the nucleus with its granular protoplasm is from the first
superficial. In other cases, such as that of the common fly[62], a layer of protoplasm is stated to
appear investing the yolk; and in this there arise simultaneously (?) a number of nuclei at regular
intervals, around each of which the protoplasm separates itself to form a distinct cell. Closely allied is
the type observed by Kowalevsky in Apis. Development here commences by the appearance of a
number of protoplasmic prominences, each forming a cell provided with a nucleus, the nuclei having
no doubt been formed by previous division in the interior of the ovum. They appear at the edge of the
yolk, and are separated from one another by short intervals. Shortly after their appearance a second
batch of similar bodies appears, filling up the interspaces between the first-formed prominences. In
the fresh-water Gammarus fluviatilis the protoplasm is stated first of all to collect at the centre of the
ovum, where no doubt the segmentation nucleus divides. Subsequently cells appear at numerous
points on the surface, and by repeated division constitute an uniform blastoderm investing the central

yolk mass. This mode of formation of the blastoderm is closely allied to that observed by
Kowalevsky in Apis.

Between ova with a segmentation like that of Insects, and those with a
segmentation like that of Penæus, there is more than one intermediate form.
The Eupagurus type, with the division of the first nucleus into eight nuclei
before the division of the ovum, must be regarded in this light; but the most
instructive example of such a transitional type of segmentation is that
afforded by Spiders[63].

Fig. 53. Three stages in the segmentation of Philodromus Limbatus.
(After Hub. Ludwig.)

The first phenomenon which can be observed after impregnation is the
conglomeration of the yolk spheres into cylindrical columns, which finally
assume a radiating form diverging from the centre of the egg. In the centre
of the radiate figure is a protoplasmic mass, probably containing a nucleus,
which sends out protoplasmic filaments through the columns (fig. 53 A).
After a certain period of repose the figure becomes divided into two rosette-
like masses, which remain united for some time by a protoplasmic thread:
this thread is finally ruptured (fig. 53 B). The whole egg does not in this
process divide into two segments, but merely the radiate figure, which is

enclosed in a finely granular material. The two rosettes next become
simultaneously divided, giving rise to four rosettes (fig. 53 C): and the
whole process is repeated with the same rhythm as in a regular
segmentation till there are formed thirty-two rosettes in all (fig. 54 A). The
rosettes by this time have become simple columns, which by mutual
pressure arrange themselves radiately around the centre of the egg, which
however they do not quite reach.

Fig. 54. Surface view and optical section of a late stage in the segmentation of
Philodromus Limbatus (Koch). (After Hub. Ludwig.)
bl. blastoderm; yk. yolk spheres.

When only two rosettes are present the protoplasm with its nucleus
occupies a central position in each rosette, but gradually, in the course of
the subsequent subdivisions, it travels towards the periphery, and finally
occupies, when the stage with thirty-two rosettes is reached, a peripheral
position. The peripheral protoplasm next becomes separated off as a
nucleated layer (fig. 54 B). It forms the proper blastoderm, and in it the
nuclei rapidly multiply and finally around each an hexagonal or polygonal
area of protoplasm is marked off; and a blastoderm, formed of a single layer
of flattened cells, is thus constituted. The columns within the blastoderm
now form (fig. 54 B) more or less distinct masses, which are stated by
Ludwig to be without protoplasm.
From observations of my own I am inclined to differ from Ludwig as to the nature of the parts within
the blastoderm. My observations have been made on Agelena labyrinthica and commence at the
close of the segmentation. At this time I find a superficial layer of flattened cells, and within these a
number of large polyhedral yolk cells. In many, and I believe all, of the yolk cells there is a nucleus
surrounded by protoplasm. It is generally placed at one side and not in the centre of a yolk cell, and
the nuclei are so often double that I have no doubt they are rapidly undergoing division. It appears to

me probable that, at the time when the superficial layer of protoplasm is segmented off from the yolk
below, the nuclei undergo division, and that a nucleus with surrounding protoplasm is left with each
yolk column. For further details vide Chapter on Arachnida.

Although by the close of the segmentation the protoplasm has travelled to a
superficial position, it may be noted that at first it forms a small mass in the
centre of the egg, and only eventually assumes its peripheral situation. It is
moreover clear that in the Spider’s ovum there is, so to speak, an attempt at
a complete segmentation, which however only results in an arrangement of
the constituents of the ovum in masses round each nucleus, and not in a true
division of the ovum into distinct segments.
It seems very probable that Ludwig’s observations on the segmentation of Spiders only hold good for
species with comparatively small ova.
In connection with the segmentation of the Insects’ ovum and allied types it should be mentioned that
Bobretzky, to whose observations we are largely indebted for our knowledge of this subject, holds
somewhat different views from those adopted in the text. He regards the nuclei surrounded by
protoplasm, which are produced by the division of the primitive segmentation nucleus, as so many
distinct cells. These cells are supposed to move about freely in the yolk, which acts as a kind of
intercellular medium. This view does not commend itself to me. It is opposed to my own
observations on similar nuclei in the Spiders. It does not fit in with our knowledge of the nature of
the ovum, and it cannot be reconciled with the segmentation of such types as Spiders or even
Eupagurus, with which the segmentation in Insects is undoubtedly closely related.
The majority if not all the cases in which a central yolk mass is formed occur in the Arthropoda, in
which group centrolecithal ova are undoubtedly in a majority. In Alcyonium palmatum the
segmentation appears however to resemble that of many insects.
One or two peculiar varieties in the segmentation of ova of this type may be spoken of here. The first
one I shall mention is detailed in the important paper of E. Van Beneden and Bessels which I have
already so often had occasion to quote: it is characteristic of the eggs of most of the species of
Chondracanthus, a genus of parasitic Crustaceans. The ovum divides in the usual way but somewhat
irregularly into 2, 4, 8 segments which meet in a central yolk mass; but after the third division instead
of each segment dividing into two equal parts it divides at once into four, and the division into four
having started, reappears at every successive division. Thus the number of the segments at successive
periods is 2, 4, 8, 32, 128, etc. In another peculiar case, an instance of which[64] is afforded by
Asellus aquaticus, after each of the earlier segmentations all the segments fuse and become
indistinguishable, but at the succeeding segmentation double the number of segments appears.
Although, as has been already stated, it does not seem possible to have a true meroblastic
segmentation in centrolecithal ova, it does nevertheless appear probable that the apparent cases of a
meroblastic segmentation in the Arthropoda are derivatives of this type of segmentation. The manner
in which the one type might pass into the other may perhaps be explained by the segmentation in
Asellus aquaticus[65]. In this ovum large segments are at first formed around a central yolk mass, in
the peculiar manner mentioned in the previous paragraph, but at the close of the first period of
segmentation minute cells, which eventually form a superficial blastoderm, are produced from the
yolk cells. They do not however appear at once round the whole periphery of the egg, but at first only
on the ventral surface and later on the dorsal surface. If the amount of food-yolk in the egg were to

increase so as to render the formation of the yolk cells impossible, and at the same time the formation
of the blastodermic cells were to take place at the commencement, instead of towards the close of the
segmentation, a mass of protoplasm with a nucleus might first appear at the surface on the future
ventral side of the egg, then divide in the usual way for meroblastic ova, and give rise to a layer of
cells gradually extending round to the dorsal surface. A meroblastic segmentation might perhaps be
even more easily derived from the type found in Insects. It is probable that the cases of Scorpio,
Mysis, Oniscus, the parasitic Isopoda, and some parasitic Copepoda belong to this category; and it
may be noticed that in these cases the blastopore would be situated on the dorsal and not on the
ventral side of the ovum. The morphological importance of this latter fact will appear in the sequel.

The results arrived at in the present section may be shortly restated in the
following way.
(1) A comparatively small number of ova contain very little or no food-yolk
embedded in their protoplasm; and have what food-yolk may be present
distributed uniformly. In such ova the segmentation is regular. They may be
described as alecithal ova.
(2) The distribution of food-yolk in the protoplasm of the ovum exercises an
important influence on the segmentation.
The rapidity with which any part of an ovum segments varies ceteris
paribus with the relative amount of protoplasm it contains; and the size of
the segments formed varies inversely to the relative amount of protoplasm.
When the proportion of protoplasm in any part of an ovum becomes
extremely small, segmentation does not occur in that part.
Ova with food-yolk may be divided into two great groups according to the
eventual arrangement of the food-yolk in the protoplasm. In one of these,
the food-yolk when present is concentrated at the vegetative pole of the
ovum. In the other group it is concentrated at the centre of the ovum. Ova
belonging to the former group are known as telolecithal ova, those to the
latter as centrolecithal.
In each group more than one type may be distinguished. In the first group
these types are (1) unequal segmentation, (2) partial segmentation. The
features of these three types have been already so fully explained that I need
not repeat them here.
In the second group there are three distinct types, (1) equal segmentation,
(2) unequal segmentation. These two being externally similar to the
similarly named types in the first group. (3) Superficial segmentation. This

is unlike anything which is present in the first group, and is characterized
by the appearance of a superficial layer of cells round a central yolk mass.
These cells may either appear simultaneously or successively, and their
nuclei are derived from the segmentation within the ovum of the first
segmentation nucleus.
The types of ova in relation to the characters of the segmentation may be
tabulated in the following way:
Segmentation.
(1) alecithal ova
regular
(2) telolecithal ova
(a) unequal
(b) partial
(3) centrolecithal ova
(a) regular (with segments united in central yolk mass)
(b) unequal (with segments united in central yolk mass)
(c) superficial.
Although the various types of segmentation which have been described
present very different aspects, they must nevertheless be looked on as
manifestations of the same inherited tendency to division, which differ only
according to the conditions under which the tendency displays itself.
This tendency is probably to be regarded as the embryological repetition of
that phase in the evolution of the Metazoa, which constituted the transition
from the protozoon to the metazoon condition.
From the facts narrated in this chapter the reader will have gathered that
similarity or dissimilarity of segmentation is no safe guide to affinities. In
many cases, it is true, a special type of segmentation may characterize a
whole group; but in other cases very closely allied animals present the
greatest differences with respect to their segmentation; as for instance the
different species of the genus Gammarus. The character of the segmentation
has great influence on the early phenomena of development, though
naturally none on the adult form.

External Features of Segmentation.
(105) E. Haeckel. “Die Gastrula u. Eifurchung.” Jenaische Zeitschrift, Vol. IX. 1877.
(106) Fr. Leydig. “Die Dotterfurchung nach ihrem Vorkommen in d. Thierwelt u. n. ihrer
Bedeutung.” Oken Isis. 1848.

[36] In the Rabbit and probably other Monodelphous Mammalia the segmentation is
nearly though not quite regular.
[37]Vide F. M. Balfour, “Comparison of the early stages of development in
Vertebrates.” Quart. Jour. of Micr. Science, July, 1875.
[38] Vide Remak, Entwicklung d. Wirbelthiere; and Götte, Entwicklung d. Unke.

[39]Van Beneden, “Développement embryonnaire des Mammifères.” Bull. de
l’Acad. Belgique, 1874.
[40] Phil. Trans. 1875.

[41] Fol, Archives de Zoologie Expérimentale, Vol. IV. 1875.

[42] Flemming, “Entwick. der Najaden,” Sitz. d. Akad. Wiss. Wien, Bd. 4, 1875.

[43] Kowalevsky, Mem. Akad. Petersburg, Series VII, 1871.

[44] Archiv. f. mikr. Anat. Vol. XIII. 1877.

[45] Metschnikoff, Zeitschrift f. wiss. Zoologie, 1874.

[46] Vide Schultze, Archiv. f. mikr. Anat. Vol. XI.; and F. M. Balfour, Monograph on
the Development of Elasmobranch Fishes.
[47] Vide Klein, Quart. Journal of Micr. Science, April, 1876. Bambeke, Mem. Cour.
Acad. Belgique, 1875. His, Zeit. für Anat. u. Entwicklung. Vol. I.
[48] Vide Bambeke, loc. cit.

[49] Vide Bobretzky, Zeitschrift für wiss. Zoologie, Vol. XXIV., 1874.

[50] Loc. cit.

[51] Bulletins de l’Acad. Belgique, Tom. XXIX., 1870.

[52] Though less obvious in the ovum of the fowl than in that of some other types,
they may nevertheless be demonstrated there without very much difficulty.
[53] Quart. Journ. of Micr. Science, Vol. XV. pp. 39, 40.

[54] Quart. Journ. of Micr. Science, Vol. XVIII. p. 41.

[55] At the time when my observations on Elasmobranchii were carried out, this
peculiar condition of the nucleus had not been elucidated.

[56] For this term as well as for the terms telolecithal and centrolecithal I am
indebted to Mr Lankester.
[57] Mayer, Jenaische Zeitschrift, Vol. XI.

[58] Ed. van Beneden, Bull. d. l’Acad. roy. Belgique, 2
me série, Tom. XXVIII. No. 7,
1869, p. 54.
[59] Zeitschrift für wiss. Zool., Vol. XXIV. 1874.

[60] Bobretzky, Zeit. f. wiss. Zool., Bd. XXXI. 1878.

[61] Metschnikoff, “Embry. Stud. Insecten,” Zeit. für wiss. Zool., Bd. XVI. 1866. My
own observations on this form accord in the main with those of Metschnikoff.
[62]Vide Weismann, Entwicklung d. Dipteren; and Auerbach, Organologische
Studien.
[63] Vide Ludwig, Zeit. f. wiss. Zool., 1876.

[64] and [65] Ed. van Beneden, Bull. Acad. Belgique, Vol. XXVIII. 1869.

PART I.

SYSTEMATIC EMBRYOLOGY.

PART I.

SYSTEMATIC EMBRYOLOGY.

Introduction.
In all the Metazoa the segmentation is followed by a series of changes
which result in the grouping of the embryonic cells into definite layers, or
membranes, known as the germinal layers. There are always two of these

layers, known as the epiblast and hypoblast; and in the majority of instances
a third layer, known as the mesoblast, becomes interposed between them. It
is by the further differentiation of the germinal layers that the organs of the
adult become built up. Owing to this it is usual, in the language of
Embryology, to speak of the organs as derived from such or such a germinal
layer.
At the close of the section of this work devoted to systematic embryology,
there is a discussion of the difficult questions which arise as to the complete
or partial homology of these layers throughout the Metazoa, and as to the
meaning to be attached to the various processes by which they take their
origin; but a few words as to the general fate of the layers, and the general
nature of the processes by which they are formed, will not be out of place
here.
Of the three layers the epiblast and hypoblast are to be regarded as the
primary. The epiblast is essentially the primitive integument, and constitutes
the protective and sensory layer. It gives rise to the skin, cuticle, nervous
system, and organs of special sense. The hypoblast is essentially the
digestive and secretory layer, and gives rise to the epithelium lining the
alimentary tract and the glands connected with it.
The mesoblast is only found in a fully developed condition in the forms
more highly organized than the Cœlenterata. It gives origin to the general
connective tissue, internal skeleton, the muscular system, the lining of the
body cavity, the vascular, and excretory systems. It probably in the first
instance originated from differentiations of the two primary layers, and in
all groups with a well-developed body cavity it is divided into two strata.
One of them forms part of the body wall and is known as the somatic
mesoblast, the other forms part of the wall of the viscera and is known as
the splanchnic mesoblast.

Fig. 55. Diagram of a Gastrula. (From Gegenbaur.)
a. blastopore; b. archenteron; c. hypoblast; d. epiblast.

A very large number not to say the majority of organs are derived from
parts of two of the germinal layers. Many glands for instance have a lining
of hypoblast which is coated by a mesoblastic layer.
The processes by which the germinal layers take their origin are largely
influenced by the character of the segmentation, which, as was shewn in the
last chapter, is mainly dependent on the distribution of the food-yolk. When
the segmentation is regular, and results in the formation of a blastosphere,
the epiblast and hypoblast are usually differentiated from the uniform cells
forming the wall of the blastosphere in one of the two following ways.
(1) One-half of the blastosphere may be pushed in towards the other half. A
two-layered hemisphere is thus established which soon elongates, while its
opening narrows to a small pore (fig. 55). The embryonic form produced by
this process is known as a gastrula. The process by which it originates is
known as embolic invagination, or shortly invagination. Of the two layers
of which it is formed the inner one (c) is known as the hypoblast and the
outer (d) as the epiblast, while the pore leading into its cavity lined by the
hypoblast is the blastopore (a). The cavity itself is the archenteron (b).

(2) The cells of the blastosphere may divide themselves by a process of
concentric splitting into two layers (fig. 56, 3). The two layers are as before
the epiblast and hypoblast, and the process by which they originate is
known as delamination. The central cavity or archenteron (F) is in the case
of delamination the original segmentation cavity; and not an entirely new
cavity as in the case of invagination. By the perforation of the closed two-
walled vesicle resulting from delamination an embryonic form is produced
which cannot be distinguished in structure from the gastrula produced by
invagination (fig. 56, 4). The opening (M) in this case is not however
known as the blastopore but as the mouth.

Fig. 56. Diagram shewing the formation of a Gastrula by delamination.
(From Lankester.)
Fig. 1. Ovum.
Fig. 2. Stage in segmentation.
Fig. 3. Commencement of delamination after the appearance of a central cavity.
Fig. 4. Delamination completed, mouth forming at M.
In fig. 1, 2 and 3 Ec. is ectoplasm, and En. is entoplasm.
In fig. 4 Ec. is epiblast and En. hypoblast.

Fig. 57. Transverse section through the ovum of Euaxes during an early stage of
development. (After Kowalevsky.)

ep. epiblast; ms. mesoblastic band; hy. hypoblast.

When segmentation does not take place on the regular type the processes
above described are as a rule somewhat modified. The yolk is usually
concentrated in the cells which would, in the case of a simple gastrula, be
invaginated. As a consequence of this, these cells become (1) distinctly
marked off from the epiblast cells during the segmentation; and (2) very
much more bulky than the epiblast cells. The bulkiness of the hypoblast
cells necessitates a modification of the normal process of embolic
invagination, and causes another process to be substituted for it, viz. the
growth of the epiblast cells as a thin layer over the hypoblast. This process
(fig. 57) is known as epibolic invagination. The point where the complete
enclosure of the hypoblast cells is effected is known as the blastopore. All
intermediate conditions between epibolic and embolic invagination have
been found.

Fig. 58. Two stages in the development of Stephanomia pictum.
(After Metschnikoff.)
A. Stage after the delamination. ep. epiblastic invagination to form pneumatocyst.
B. Later stage after the formation of the gastric cavity in the solid hypoblast. po. polypite; t.
tentacle; pp. pneumatophore; ep. epiblastic invagination to form pneumatocyst; hy. hypoblast
surrounding pneumatocyst.

In delamination, when the segmentation is not uniform, or when a solid
morula is formed, the differentiation of the epiblast and hypoblast is
effected by the separation of the central solid mass of cells from the
peripheral cells (fig. 58 A).
In the case of epibolic invagination as well as in that of the type of
delamination just spoken of, the archenteric cavity is in most cases
secondarily formed in the solid mass of hypoblast (fig. 58 B).
In ova with a partial segmentation there is usually some modification of the
epibolic gastrula.
Many varieties are found in the animal kingdom of the types of
invagination and delamination just characterized, and in not a few forms the
layers originate in a manner which cannot be brought into connection with
either of these processes.

Fig. 59. Epibolic Gastrula of Bonellia. (After Spengel.)
A. Stage when the four hypoblast cells are nearly enclosed.
B. Stage after the formation of the mesoblast has commenced by an infolding of the lips of
the blastopore.
ep. epiblast; me. mesoblast; bl. blastopore.

The mesoblast usually originates subsequently to the two primary layers. It
then springs from one or both of the other layers, but its modes of origin are
so various that it would be useless to attempt to classify them here. In cases
of invagination it often arises at the lips of the blastopore (fig. 57 and 59),
and in other cases part of it springs as paired hollow outgrowths of the walls
of the archenteron. Such outgrowths are shewn in fig. 60, B and C at pv.
The cavity of the outgrowths forms the body cavity, and the walls of the
outgrowths the somatic and splanchnic layers of mesoblast (fig. C. sp. and
so.). The archenteron is in part always converted into a section of the
permanent alimentary tract and the section of the alimentary tract so derived
is known as the mesenteron. There are however usually two additional parts
of the alimentary tract, known as the s t o m o d a e u m and
p r o c t o d a e u m , derived from epiblastic invaginations. They give rise
respectively to the oral and anal extremities of the alimentary tract.

Fig. 60. Three stages in the development of Sagitta. (A and C after Bütschli and B after
Kowalevsky.) The three embryos are represented in the same positions.
A. Represents the gastrula stage.
B. Represents a succeeding stage in which the primitive archenteron is commencing to be
divided into three parts, the two lateral of which are destined to form the mesoblast.
C. Represents a later stage in which the mouth involution (m) has become continuous with
alimentary tract, and the blastopore has become closed.
m. mouth; al. alimentary canal; ae. archenteron; bl. p. blastopore; pv. perivisceral cavity; sp.
splanchnic mesoblast; so. somatic mesoblast; ge. generative organs.

Bibliography.
(107) K. E. von Baer. “Ueb. Entwicklungsgeschichte d. Thiere.” Königsberg, 1828‑1837.
(108) C. Claus. Grundzüge d. Zoologie. Marburg und Leipzig, 1879.
(109) C. Gegenbaur. Grundriss d. vergleichenden Anatomie. Leipzig, 1878. Vide also Translation.
Elements of Comparative Anatomy. Macmillan and Co., 1878.
(110) E. Haeckel. Studien z. Gastræa-Theorie. Jena, 1877, and also Jenaische Zeitschrift, Vols. VIII.
and IX.
(111) E. Haeckel. Schöpfungsgeschichte. Leipzig. Vide also Translation. The History of Creation.
King and Co., London, 1876.
(112) E. Haeckel. Anthropogenie. Leipzig. Vide also Translation. Anthropogeny (Translation). Kegan
Paul and Co., London, 1878.
(113) Th. H. Huxley. The Anatomy of Invertebrated Animals. Churchill, 1877.
(114) E. R. Lankester. “Notes on Embryology and Classification.” Quart. J. of. Micr. Science, Vol.
XVII. 1877.
(115) A. S. P. Packard. Life Histories of Animals, including Man, or Outlines of Comparative
Embryology. Holt and Co., New York, 1876.
(116) H. Rathke. Abhandlungen z. Bildung und Entwicklungsgesch. d. Menschen u. d. Thiere.
Leipzig, 1833.

CHAPTER IV.

DICYEMIDÆ AND ORTHONECTIDÆ.

Dicyemidæ.
The structure and development of these remarkable parasites in the renal
organs of the Cephalopoda have recently been greatly elucidated by the
researches of E. van Beneden; and although a male element has not been
discovered, yet the embryos originate from bodies which have a close
similarity to ordinary ova.
Van Beneden has shewn that Dicyema consists in the adult state of (1) a
single layer of ciliated epiblast cells, somewhat modified anteriorly to form
a cephalic enlargement; and of (2) one large nucleated hypoblast cell
enclosed within the epiblast. There are two kinds of embryo, both
developed from germs which originate in the hypoblast cell. The two kinds
of embryo arise in individuals of somewhat different forms. The one kind,
called by Van Beneden the vermiform embryo, arises in the more elongated
and thinner examples of Dicyema which have been named Nematogens.
These embryos pass directly into the parent form without metamorphosis.
The second kind of embryo, called infusoriform, is very different from the
parent, and has a free existence. Its eventual history is not known. It
originates in the shorter and thicker individuals of Dicyema; which have
been called Rhombogens.
The Vermiform Embryos. The germs or cells which give rise to the
vermiform embryos originate endogenously in the protoplasmic reticulum
of the axial hypoblast cell. They appear as small but well-defined spheres,
with a minute body in the centre. In these spheres a cortical layer becomes
differentiated, which gradually increases in thickness and gives rise to the
body of a cell, the nucleus and nucleolus of which are respectively formed
from the inner part of the original sphere and the minute central body. These
germs can originate in all parts of the hypoblast cell and are frequently very
numerous.

Fig. 61. A. Gastrula stage of Dicyema typus. B. Veriform embryo of Dicyema typus.
(From Gegenbaur, after E. van Beneden.)

The germ when completely formed undergoes a segmentation very similar
to that of an ordinary ovum. It divides first into two and then into four
approximately equal segments. Of the four segments one, however, remains
passive for the remainder of the development. The other three divide and
arrange themselves so as partially to enclose in a cup-like fashion the
passive cell (fig. 61 A). The six cells resulting from their division again
divide, giving rise to twelve cells, which nearly enclose the passive cell,
leaving only a small aperture at one point. The whole process by which the
central cell becomes enclosed is, as E. van Beneden points out, identical
with a gastrula formation by epibole, and the space where the central cell is
left uncovered is the blastopore. The central cell itself gives origin to the
hypoblast cell of the adult, and the peripheral cells to the epiblast.
By this time the embryo has assumed an oval form, and the blastopore is
situated at the pole of the long axis of the oval where the cephalic
enlargement is eventually formed.
The subsequent development consists mainly in the closure of the
blastopore, and an increase in the number of the epiblast cells. Before the
development is completed, and while the embryo is still in the body of the
parent, two germs, destined themselves to give rise to fresh embryos,
appear in the hypoblast cell, one on each side of the nucleus (fig. 61 B). The
embryo continues to elongate, while the anterior cells become converted
into the polar cells. Cilia appear simultaneously over the general surface,

and the embryo makes its way out of the body of the parent, usually at the
cephalic pole, and becomes itself parasitic in the renal organ of the host in
which it finds itself. At the time of birth the embryo may contain a number
of germs and sometimes even developing embryos.
Infusoriform Embryos. The infusoriform embryos are capable of living in
sea-water and almost certainly lead a free existence. In their most fully
developed condition so far known they have the following rather
complicated structure (fig. 62 D, E, F, G).
The body is somewhat pyriform, with a blunt extremity which is directed
forwards in swimming, and a more pointed extremity directed backwards.
The former may be spoken of as the anterior, and the latter as the posterior
extremity or tail. At the anterior extremity are situated a pair of refractive
bodies (r) which lie above an unpaired organ which may be called the urn.
The structure of the urn, the refractive bodies, and the tail may be dealt with
in succession.
The urn consists of three parts: (1) a wall (u), (2) a lid (l), and (3) contents
(gr). The wall of the urn is hemispherical in form, and composed of two
halves in apposition (fig. F). Its concavity is directed forwards, and in its
edge are imbedded a number of rod-like corpuscles which appear as a ring
near the surface in a full-face view (fig. D). The lid has the form of a low
pyramid with its apex directed outwards. It is made up of four segments
(fig. D). The contents of the urn, which completely fill up its cavity, are four
polynuclear cells arranged in the form of a cross which appear with low
powers as granular bodies (fig. F). They are frequently ejected, apparently
at the will of the embryo.
The refractive bodies (r), two in number, one on each side of the middle
line, are composed of a material which is not of a fatty nature, and which is
passive to the majority of reagents. Each is enveloped in a special capsule,
and at times more than one refractive body is present in each capsule. The
tail is a conical structure formed of ciliated granular cells.
No plausible guess has been made as to the function either of the urn or of
the refractive bodies.

The infusoriform embryos originate from germs, which have however a
different origin to the germs of the vermiform embryos. One to five cells
appear in the axial hypoblast cell, in a way not clearly made out, and each
of them gives rise by an endogenous process to several generations of cells,
all of which develop into infusoriform embryos.

Fig. 62. Infusoriform embryo of Dicyema.
A. B. C. Three of the later stages in the development.
D. E. F. Three different views of the full-grown larva. D. from the front, E. from the side, and
F. from above.
G. side view of urn.
u. wall of urn; l. lid of urn; r. refractive bodies; gr. granular bodies filling the interior of the
urn.

The primitive cell is called by Van Beneden a Germogen. In its protoplasm
a number of germs first appear endogenously, but the nucleus of the
germogen does not assist in their formation. They eventually become
detached from the parent cell, around which they are concentrically
arranged. A second and then a third generation of germs are formed in the
same way, till the whole of the protoplasm of the primitive cell is absorbed
in the formation of these germs, and nothing of it remains but the nucleus.
The germs so formed are arranged in about three concentric layers, of
which the innermost is the youngest. One to five masses of germs may be
present in a single Rhombogen. The germs undergo a division, in the course
of which their nuclei exhibit very beautifully a spindle modification. In the
course of the segmentation the embryo gradually assumes its permanent
form, and four of the cells composing it can be distinguished from the

remainder by their greater size (fig. 62 A, u). The two largest of these give
rise to the wall of the urn, and also give origin to four smaller cells (fig. 62
B, gr) which eventually become polynuclear and constitute the four
granular cells in the urn. The two other cells become the lid of the urn. The
parts of the urn lie at first side by side, but in the course of development the
cells which form the wall of the urn travel inwards, and the four granular
cells are carried into their concavity. At the same time the cells which form
the lid of the urn alter their position so as to overlie the wall of the urn. The
two cells immediately above the urn give rise to the refractive bodies (fig.
62 A, B, C, r) and the remainder of the cells of the embryo become the tail
(fig. 62 C). The embryo becomes ciliated, and attains its nearly full
development before leaving the parental tissues. It usually passes out at the
cephalic extremity.
As has already been stated, it is probable that the infusoriform embryos
leave the renal organs of their host and lead a free existence. What becomes
of them afterwards is not however known, though there can be little doubt
that they serve to carry the species to new hosts.
Till the further development of the infusoriform embryo is known it is not
possible to arrive at a definite conclusion as to the affinities of this strange
parasite. Van Beneden is anxious to form it, on account of its simple
organization, into a group between the Protozoa and the Metazoa. It appears
however very possible that the simplicity of its organization is the result of
a parasitic existence; a view which receives confirmation from the common
occurrence of the process of endogenous cell formation in the axial
hypoblast cell. It has been clearly shewn by Strasburger that endogenous
cell formation is secondarily derived from cell division; so that the
occurrence of this process in Dicyema probably indicates that the hypoblast
was primitively multicellular. It is not improbable that the enigmatical
infusoriform embryo may develop into a sexual form, the progeny of which
are destined to complete the cycle of development by becoming again
parasitic in the renal organ of a Cephalopod.

Bibliography.
(117) E. van Beneden. “Recherches sur les Dicyemides.” Bull. d. l’Académie roy. de Belgique, 2e
sér. T. XLI. No. 6 and T. XLII. No. 7, 1876. Vide this paper for a full account of the literature.

(118) A. Kölliker. Ueber Dicyema paradoxum den Schmarotzer der Venenanhänge der
Cephalopoden.
(119) Aug. Krohn. “Ueb. d. Vorkommen von Entozoen, etc.” Froriep Notizen, VII. 1839.

Orthonectidæ.
A number of minute parasites infesting various Nemertines, Turbellarians, and Ophiuroids have
recently been studied by Giard and Metschnikoff, the former of whom has placed them in a special
group which he calls the Orthonectidæ. They were first discovered by W. C. McIntosh.

In the adult state they are[66] (Metschnikoff) somewhat pear-shaped bodies formed of a kind of
plasmodium of cells with irregular lobate processes. In the interior of this body are eggs in all stages
of development. In the type observed by Metschnikoff (Intoshia gigas) the ova undergo a regular
segmentation, resulting in the formation of a blastosphere in which an inner layer is subsequently
formed by delamination. A smaller and a larger kind of embryo are formed; but all the embryos in
each female belong to one type. The larger become females and the smaller males.
The female embryos are ovoid. The outer layer of cells or epiblast becomes ciliated, and divided into
nine segments, of which the second is marked off from the remainder by the absence of cilia, and by
being provided with refractive corpuscles. The inner layer which surrounds a central cavity, and
might be supposed to be the hypoblast, becomes according to Metschnikoff converted into ova.
The male embryos are more elongated than the female, from which they further differ in only having
six segments. The cells of the inner layer eventually divide up into spermatozoa.
The larvæ probably become free, and while in the free state impregnation would appear to be
effected. When the female larvæ become parasitic they undergo a metamorphosis, the stages of which
have not been observed; but in the course of which the epiblast cells probably unite into a
plasmodium.
The observations of Giard are in several points irreconcilable with those of Metschnikoff, but from
the statements of the latter it appears possible that Giard has made two genera from the males and
females of one species; and that Giard’s account of an unequal segmentation followed by an epibolic
gastrula, in one of his species, has arisen from two segmenting ova temporarily fusing together. Giard
has given a description of internal gemmiparous reproduction, upon the accuracy of which doubts
have been thrown by Metschnikoff. The affinities of the Orthonectidæ are as obscure as those of the
Dicyemidæ; though there can be but little doubt that their organization has been much simplified in
correlation with their parasitic habits. The origin of the genital products in the axial tissue is a feature
they have in common with the Dicyemidæ.

Bibliography.
(120) Alf. Giard. “Les Orthonectida classe nouv. d. Phylum des Vers.” Journal de l’Anat. et de la
Physiol., Vol. XV. 1879.
(121) El. Metschnikoff. “Zur Naturgeschichte d. Orthonectidæ.” Zoologischer Anzeiger, No. 40‑43,
1879.
[Ch. Julin. “Rech. sur l’organization et le devel. d’Orthonectides.” Arch. Biol. Vol. III. 1882.
E. Metschnikoff. “Untersuchungen üb. Orthonectidæ.” Zeit. f. Wiss. Zoologie, Vol. XXXV. 1881.
For general account of Orthonectidæ, vide Spengel. Biolog. Centralblatt, No. 6.]

[66] This at any rate holds true for the type investigated by Metschnikoff. The full
history of other forms is not yet known.

CHAPTER V.

PORIFERA.

Although within the last few years greater advances have probably been
made in our knowledge of the development of the Porifera than of any other
group, yet there is much that is still very obscure, and it is not possible to
make general statements applying to the whole group.
Calcispongiæ. The form which has so far been most completely worked out
is Sycandra raphanus, one of the Calcispongiæ (Metschnikoff, Nos. 132
and 134, F. E. Schulze, Nos. 139 and 142), and I shall commence my
account with the life history of this species.
The ovum in Sycandra as in other Spongida has the form of a naked
amœboid nucleated mass of protoplasm. From the analogy of the other
members of the group, there is no doubt that it is fertilized by a male
spermatic element, though this has not as yet been shewn to be the case—
and the changes which accompany fertilization are quite unknown.

Fig. 63. Successive stages in the segmentation of Sycandra raphanus.
(Copied from F. E. Schulze.)
A. stage with eight segments still arranged in pairs, from above.
B. side view of stage with eight segments.
C. side view of stage with sixteen segments.
D. side view of stage with forty-eight segments.
E. view from above of stage with forty-eight segments.
F. side view of embryo in the blastosphere stage, eight of the granular cells which give rise to
the epiblast of the adult are present at the lower pole.
cs. segmentation cavity; ec. granular cells which form the epiblast; en. clear cells which form
the hypoblast.

The segmentation and early stages of development take place in the tissues
of the parent. The segmentation is somewhat peculiar, though a
modification of a regular segmentation. The ovum divides along a vertical
plane, first into two, and then into four equal segments. But even when two
segments are formed, each of them has one end pointed and the other
broader. The pointed ends give rise to the ciliated cells of the future larva,
and the broad ends to the granular cells. Instead of the next division taking
place, as is usually the case, in a horizontal (equatorial) plane, it is actually
effected along two vertical planes intermediate in position between the two
first planes of segmentation. Eight equal segments are thus formed, each of
which has the form of a pyramid. All the segments are situated in a single
tier, and are so arranged as to give to the whole ovum the form of a flat
cone, the apex of which is formed by the pointed extremities of the
constituent segments (fig. 63 B). The apices of the segments do not
however quite meet, but they leave a central space, which is an actual
perforation (fig. 63 A) through the axis of the ovum, open at both ends. The
first indications of this perforation appear when only four segments are
present, and it is to be regarded as the homologue of the segmentation
cavity of other ova. The next plane of division is horizontal (equatorial),
and the apices of the eight cells are segmented off as a tier of small cells. At
the completion of this division (fig. 63 C), the ovum is formed of sixteen
cells arranged in two superimposed tiers. The ovum now assumes
somewhat the form of a biconvex lens, in the axis of which the central
perforation is still present. At the close of the next stage, forty-eight cells
are present arranged in four tiers (fig. 63 D and E), the two outer tiers
containing eight cells each, and the two inner sixteen. The two inner tiers

probably arise by the simultaneous appearance of two equatorial furrows
dividing the original tiers into two, and by the subsequent simple division of
the cells of the two inner of the tiers so formed. At the close of the stage the
eight basal cells become granular (fig. 63 F). At the same time the central
part of the segmentation cavity becomes enlarged, while its terminal
apertures become narrowed and finally, shortly after the end of this stage,
closed. The axial perforation thus acquires the character of a closed
segmentation cavity. While the ovum itself becomes at the same time a
blastosphere.

Fig. 64. Larva of Sycandra raphanus at pseudogastrula stage, in situ in the maternal
tissues. (Copied from F. E. Schulze.)

me. mesoblast of adult; hy. collared cells forming hypoblast of the adult; en. clear cells of
larva which eventually become involuted to form the hypoblast; ec. granular cells of larva
which give rise to the epiblast, which at this stage are partially involuted.

This stage nearly completes the segmentation: in the next one, the cells of
the poles of the blastosphere increase in number, and the cells of the greater
part of the blastosphere become columnar and ciliated, (fig. 64 en.) while

the granular cells (ec.) increase to about thirty-two in number and appear to
be (partially at least) involuted into the segmentation cavity, reducing this
latter to a mere slit. This stage forms the last passed by the embryo in the
tissues of the parent. The general position of the embryo while still in this
situation may be gathered from fig. 64, representing the embryo in situ. The
embryo is always placed close to one of the radial canals. From this
situation it makes its way through the lining cells into a canal and is thence
transported to the surrounding water. By the time the larva has become free,
the semi-invaginated granular cells have increased in bulk and become
everted so as to project very much more prominently than in the encapsuled
state. To the gastrula stage, if it deserves the name, passed through by the
embryo in the tissues of the parent, no importance can be attached.

Fig. 65. 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 epiblast; en. ciliated cells
which become invaginated to form the hypoblast.

The larva, after it has left the parental tissues, has an oval form and is
transversely divided into two areas (fig. 65 A). One of these areas is formed
of the elongated, clear, ciliated cells, with a small amount of pigment near
their 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 (c.s.) 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 a m p h i b l a s t u l a stage. During the
later periods of the amphiblastula stage a cavity appears in the granular
cells dividing them into two layers. After the larva has for some time
enjoyed a free existence, a remarkable series of changes take place, which
result in the invagination of the half of it formed of the clear cells, and form
a prelude to the permanent attachment of the larva. The entire process of
invagination is completed in about half an hour. The whole embryo first
becomes flattened, but especially the ciliated half, which gradually becomes
less prominent (fig. 65 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 epiblast and hypoblast. 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 epiblast cells, which, together with the other
epiblast cells, now become amœboid. They become at the same time clearer
and permit a view of the interior of the gastrula. Between the epiblast cells
and the hypoblast cells which line the gastrula cavity there arises a hyaline
structureless layer, which is more closely attached to the epiblast than to the
hypoblast, and is probably derived from the former. A view of the gastrula
stage after the larva has become fixed is given in fig. 66.

Fig. 66. Fixed Gastrula stage of Sycandra raphanus. (Copied from Schulze.)
The figure shews the amœboid epiblast cells (ec.) derived from the granular cells of the
earlier stage, and the columnar hypoblast cells, lining the gastrula cavity, derived from the
ciliated cells of the earlier stage. The larva is fixed by the amœboid cells on the side on which
the blastopore is situated.

There would seem according to Metschnikoff’s observations (No. 134) to
be a number of mesoblast cells interposed between the two primary layers,
which he derives from the inner part of the mass of granular cells.
After invagination the cilia of the hypoblast cells can no longer be seen, and
are probably absorbed; and their disappearance is nearly coincident with the
complete obliteration of the blastopore, an event which takes place shortly
after the attachment of the larva.
Not long after the closure of the blastopore, calcareous spicules make their
appearance in the larva as delicate unbranched rods pointed at both
extremities. They appear to be formed on the mesoblast cells situated
between the epiblast and hypoblast[67]. The larva when once fixed rapidly
grows in length and assumes a cylindrical form (fig. 67 A). The sides of the
cylinder are beset with calcareous spicules which project beyond the
surface, and, in addition to the unbranched forms, spicules are developed
with three and four rays as well as some with a blunt extremity and serrated
edge. The extremity of the cylinder opposite the attached surface is
flattened, and, though surrounded by a ring of four-rayed spicules, is itself
free from them. At this extremity a small perforation is formed leading into
the gastric cavity, which rapidly increases in size and forms an exhalent

osculum (os.). A series of inhalent apertures is also formed at the sides of
the cylinder. The relative times of appearance of the single osculum and the
smaller apertures are not constant for the different larvæ. On the central
gastrula cavity of the sponge becoming placed in communication with the
external water, the hypoblast cells lining it become ciliated afresh (fig. 67
B, en.) and develop the peculiar collar characteristic of the hypoblast cells
of the Spongida (vide fig. 64, hy.). When this stage of development is
reached we have a fully formed sponge of the type made known by Haeckel
as Olynthus.

Fig. 67. The young of Sycandra raphanus shortly after the development of the Spicula.
(Copied from Schulze.)
A. View from the side.
B. View from the free extremity.
os. osculum; ec. epiblast; en. hypoblast composed of ciliated cells. The terminal osculum and
lateral pores are represented as oval white spaces.

When young examples of Sycandra come in contact shortly after their
attachment they appear to fuse together temporarily or else permanently. In
the latter case colonies are produced by their fusion.
Amongst other calcareous sponges the larva of Ascandra contorta (Haeckel No. 126, Barrois No.
122) presents the typical amphiblastula stage, and so probably does that of Ascandra Lieberkühnii
(Keller No. 128). In Leucandra aspera (Keller No. 128, Metschnikoff No. 134) the larva passes
through an amphiblastula stage, but the characters of the cells of the two halves of the larva do not
differ to nearly the same extent as in Sycandra.
Although the majority of calcareous sponges appear to agree in their mode of development with
Sycandra, nevertheless the concordant researches of O. Schmidt (No. 138) and Metschnikoff (No.
134) have shewn that this is not true for the genus Ascetta (As. primordialis, clathrus and blanca).
The larvæ of these forms are very differently constituted to those of Sycandra. They have an oval
form and are composed of a single row of ciliated columnar cells: their two extremities only differ in
the cells at one extremity being longer than those at the other. Especially at the pole where the shorter
cells are situated (Schmidt) a metamorphosis of the cells takes place. One after the other they lose
their cilia, become granular, and pass into the interior of the vesicle. Here they become differentiated
into two classes (Metschnikoff); one of larger and more granular cells, and the other of smaller cells
with clearer protoplasm. Cells of the former class are mainly found at one of the poles. When the
larva becomes free the cells in the interior of the vesicle increase in number and nearly fill up its
central cavity. After a short free existence the larva becomes fixed, and the epiblast cells lose their
cilia and become flattened. At a later period the large granular cells assume a radiate arrangement
round a central cavity and become clearly marked out as the hypoblast cells. The smaller cells
become placed between the epiblast and hypoblast and constitute the mesoblast.

Myxospongiæ. In this group Halisarca has been investigated by Carter (No.
123), Barrois (No. 122), Schulze (No. 141) and Metschnikoff (No. 134).
The ova develop in the mesoblast, and when ripe occupy special chambers
lined by a layer of epithelial cells. Schulze has found the spermatozoa of
this genus of sponge and has been able to shew that the sexes may be
distinct, though many species of Halisarca are hermaphrodite.
The segmentation is, roughly speaking, regular, and a segmentation cavity
is early formed, which is never, as in Calcispongiæ, open at the poles. When
the larva leaves the parent it is an oval vesicle formed of a single layer of
columnar ciliated cells. Slight differences may be observed between the two
extremities of the larvæ of most species. One of these—the hinder
extremity—is directed backwards in swimming.
The further history of the larva has been investigated by Metschnikoff. He
has found that the interior of the vesicle becomes gradually filled with
mesoblast cells of a peculiar type, called by him rosette-cells, which are
probably derived from the walls of the vesicle.

When the metamorphosis commences, the larva assumes a flattened form,
and cells of a new type, viz. normal amœboid cells, grow in amongst the
rosette cells. The new cells are also derived from the epiblast. The larvæ
appear to fix themselves by the hinder extremity. The cilia gradually
disappear, and the epiblast cells flatten out and form a kind of cuticle. For
some time the larva remains in the two-layered condition, but gradually
canals (? ciliated chambers) lined by hypoblast cells become formed. They
appear as closed spaces with walls of ciliated cells derived from the
amœboid cells, and the different parts of the system of chambers are
established independently. In H. pontica the ciliated chambers are formed
before the attachment of the larva. The development was not followed up to
the formation of the pores placing the canal system in communication with
the exterior.
The young sponges at a somewhat later stage have been studied by Schulze
and Barrois. They are formed of an external layer of flattened cells, not
clearly ciliated as in the adult, within which are a normal mesoblastic tissue,
and several spherical chambers lined by ciliated cells exactly like the
ciliated chambers of the full-grown sponge. Irregular invaginations of the
epiblast give to the young sponge a honeycombed structure. The ciliated
chambers in the youngest condition of the sponge are closed; but in slightly
older examples they come into communication with the passages lined by
hypoblast, and so indirectly with the external medium.
Ceratospongiæ. Amongst the true Ceratospongiæ the embryos of two of the Aplysinidæ, and of
Spongelia and Euspongia have been to some extent worked out by Barrois and Schulze. The form
worked out by Barrois is called by him Verongia rosea. The segmentation is nearly regular, but from
the first the segments may be divided according to their constitution into two categories. At the close
of segmentation the embryo is oval and covered by a single layer of columnar ciliated cells; these
cells may however be divided into two categories, corresponding with those observable during the
segmentation. A certain number are coloured red and form a definite circular mass at one pole, while
the remainder, which constitute the major part of the embryo, have a pale yellowish colour. Those at
the red pole lose their cilia in the free larva, but around the area formed by them is a special ring of
long cilia. The chief peculiarity of the embryo (made known by Schulze) consists in the fact that the
layer of cells which covers the embryo does not, as in other sponge embryos, simply enclose a space,
but the interior of the embryo is formed of a mass of stellate cells like the normal mesoblast of full-
grown sponges.
This feature is also characteristic of the embryos of Spongelia and Euspongia.
The embryo of the Gummineæ (Gummina mimosa) has been investigated by Barrois (No. 122), and
has been shewn closely to resemble the typical larvæ of calcareous sponges; one-half being formed
of elongated ciliated cells and the other of rounded granular ones.

Silicispongiæ. The development of marine silicious sponges is but very imperfectly understood. The
larvæ of various forms—Reniera (Isodyctia), Esperia (Desmacidon), Raspailia, Halichondria, Tethya
—have been described. Barrois has shewn that the egg segments regularly and that in the earlier
stages a segmentation cavity is present. In the later stages the embryo appears to become solid.
Externally there is a layer of ciliated cells, and within a mass of granular matter in which the separate
cells cannot be made out. The granular matter projects at one pole, and forms a prominence possibly
equivalent to the granular cells of Sycandra. In some forms, e.g. Reniera, the edge of the unciliated
granular prominence may be surrounded by a row of long cilia. In later stages the granular material
may project at both poles or even at other points. One remarkable feature in the development of the
Silicispongiæ is the appearance of spicula between the ciliated cells and the central mass, while the
larva is still free.
Professor Schulze has informed me that these spicula are developed in mesoblast cells; while the
horny fibres of the sponge are developed as cuticular products of special mesoblast cells
(spongioblasts).
The attachment and accompanying metamorphosis are so diversely described that no satisfactory
account can be given of them. The general statements are in favour of the attachment taking place by
the posterior extremity where the granular matter projects.
Carter especially gives a very precise account, with figures, of the attachment of the larva in this way.
He also figures the appearance of an osculum at the opposite pole[68].
A very elaborate account of the development of Spongilla has been published in Russian by Ganin, of
which a German abstract has also appeared (No. 124).
The ovum undergoes a regular segmentation and becomes a solid ova morula. An epiblast of smaller
cells is early differentiated, and in the interior of the inner cells an archenteron becomes subsequently
formed. The inner cells next become divided into an hypoblastic layer lining the archenteron, and a
mesoblastic layer between this and the now ciliated epiblast. At the narrow hinder end of the embryo
the mesoblast becomes thickened, and largely obliterates the archenteron. In this part of the
mesoblast silicious spicula are formed. The larva becomes attached by its hinder extremity, and in the
course of this process flattens itself out to a disc-like form. From the nearly obliterated archenteric
cavity outgrowths take place which give rise to the ciliated chambers. These are not placed directly in
communication with the exterior, but open, if I understand Ganin rightly, into a space in the
mesoblast, which subsequently acquires an exterior communication—the primitive osculum. The
subsequent pores and oscula are also formed as openings leading into the mesoblastic cavity, which
communicates in its turn with the ciliated chambers.

It appears that in the present unsatisfactory state of our knowledge the larvæ
of the Porifera may be divided into two groups: viz. (1) those which have
the form of a blastosphere or else of a solid morula; (2) those which have
the amphiblastula form.
In the former type the mesoblast and hypoblast are formed either from cells
budded off from the outer cells of the blastosphere or from the solid inner
mass of cells; while the outer ciliated cells become the epiblast. This type of
larva, which is found in the majority of sponges, is very similar in its
general characters and development to many Cœlenterate planulæ.

The second type of larva is very peculiar, and though in its fully developed
form it is confined to the Calcispongiæ, where it is the usual form, a larval
type with the same characters is perhaps to be found in other sponges, e.g.
amongst the Gumminæ, and amongst the Silicispongiæ where one-half of
the embryo is without cilia, though in the case of the Silicispongiæ the cells
of the ciliated part of the embryo correspond to the granular cells of the
larva of Sycandra.
The later stages in the development of the larvæ of the Porifera are not
similar to anything we know of in other groups.
It might perhaps be possible to regard sponges as degraded descendants of some Actinozoon type
such as Alcyonium, with branched prolongations of the gastric cavity, but there does not appear to me
to be sufficient evidence for doing so at present. I should rather prefer to regard them as an
independent stock of the Metazoa.
In this connection the amphiblastula larva presents some points of interest. 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; but, assuming that this is
not the case, it appears to me that the characters of the larva may be plausibly explained by regarding
it as a transitional form between the Protozoa and Metazoa. According to this view the larva is to be
considered as a colony of Protozoa, one-half of the individuals of which have become differentiated
into nutritive forms, and the other half into locomotor and respiratory forms. The granular amœboid
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.
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 Spongida.
It is as follows:—When the free-swimming ancestor of the Spongida became fixed, the ciliated cells
by which its movements used to be effected must have to a great extent become functionless. At the
same time the amœboid 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 amœboid cells over them. Though respiration was, no doubt,
mainly effected by the ciliated cells, it is improbable that it was completely localized in them, but
they were enabled to continue performing this function through the formation of an osculum and
pores. The 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
epiblastic cells, which in most cases line the inhalent passages through its substance[69], ought to be
employed to absorb nutriment. The recent researches of Metschnikoff (No. 134) on this head shew

that the nutriment is largely carried into the mesoblast cells, which in Sycandra appear to be derived
from the granular cells, and also that it is taken up by the cells which line the passages, though not by
the superficial epiblast cells. Whether the collared cells generally absorb nutriment is not clear from
his statements: but he finds that they do not do so in Silicispongiæ.
Professor Schulze has informed me by letter that he finds the collared cells to be respiratory in
function, while the cells derived from the granular cells in Sycandra are nutritive. Carter[70], on the
contrary, from his observations on Spongilla, has fully satisfied himself that the food is absorbed by
the cells lining the ciliated chambers.
If it is eventually proved by further experiments on the nutrition of sponges, that digestion is mainly
carried on by the general cells lining the passages and the mesoblast cells, and not for the most part
by the ciliated cells, it is clear that the epiblast, mesoblast and hypoblast of sponges will not
correspond with the similarly named layers in the Cœlenterata and other Metazoa. The invaginated
hypoblast will be the respiratory layer and the epiblast and mesoblast the digestive and sensory
layers; the sensory function being probably mainly localized in the epithelium on the surface, and the
digestive one in the epithelium lining the passages and in the mesoblast. Such a fundamental
difference in the primary function of 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.

Bibliography.
(122) C. Barrois. “Embryologie de quelques éponges de la Manche.” Annales des Sc. Nat. Zool., VI.
ser., Vol. III. 1876.
(123) Carter. “Development of the Marine Sponges.” Annals and Mag. of Nat. Hist., 4th series, Vol.
XIV. 1874.
(124) Ganin[71]. “Zur Entwicklung d. Spongilla fluviatilis.” Zoologischer Anzeiger. Vol. I. No. 9,
1878.
(125) Robert Grant. “Observations and Experiments on the Structure and Functions of the Sponge.”
Edinburgh Phil. J., Vol. XIII. and XIV., 1825, 1826.
(126) E. Haeckel. Die Kalkschwämme, 1872.
(127) E. Haeckel. Studien zur Gastræa-Theorie. Jena, 1877.
(128) C. Keller. Untersuchungen über Anatomie und Entwicklungsgeschichte einiger Spongien.
Basel, 1876.
(129) C. Keller. “Studien üb. Organisation u. Entwick. d. Chalineen.” Zeit. f. wiss. Zool., Bd. XXVIII.
1879.
(130) Lieberkühn. “Beitr. z. Entwick. d. Spongillen.” Müller’s Archiv, 1856.
(131) Lieberkühn. “Neue Beiträge zur Anatomie der Spongien.” Müller’s Archiv, 1859.
(132) El. Metschnikoff. “Zur Entwicklungsgeschichte der Kalkschwämme.” Zeit. f. wiss. Zool., Bd.
XXIV. 1874.
(133) El. Metschnikoff. “Beiträge zur Morphologie der Spongien.” Zeit. f. wiss. Zool., Bd. XXVII.
1876.
(134) El. Metschnikoff. “Spongeologische Studien.” Zeit. f. wiss. Zool., Bd. XXXII. 1879.
(135) Miklucho-Maklay. “Beiträge zur Kenntniss der Spongien.” Jenaische Zeitschrift, Bd. IV. 1868.
(136) O. Schmidt. “Zur Orientirung über die Entwicklung der Schwämme.” Zeit. f. wiss. Zool., Bd.
XXV. 1875.
(137) O. Schmidt. “Nochmals die Gastrula der Kalkschwämme.” Archiv für mikrosk. Anat., Bd. XII.
1876.

(138) O. Schmidt. “Das Larvenstadium von Ascetta primordialis und Asc. clathrus.” Archiv für
mikrosk. Anatomie, Bd. XIV. 1877.
(139) F. E. Schulze. “Ueber den Bau und die Entwicklung von Sycandra raphanus.” Zeit. f. wiss.
Zool., Bd. XXV. 1875.
(140) F. E. Schulze. “Zur Entwicklungsgeschichte von Sycandra.” Zeit. f. wiss. Zool., Bd. XXVII.
1876.
(141) F. E. Schulze. “Untersuchung üb. d. Bau, etc. Die Gattung Halisarca.” Zeit. f. wiss. Zool., Bd.
XXVIII. 1877.
(142) F. E. Schulze. “Untersuchungen üb. d. Bau, etc. Die Metamorphose von Sycandra raphanus.”
Zeit. f. wiss. Zool., Bd. XXXI. 1878.
(143) F. E. Schulze. “Untersuchungen ü. d. Bau, etc. Die Familie Aplysinidæ.” Zeit. f. wiss. Zool.,
Bd. XXX. 1878.
(144) F. E. Schulze. “Untersuchungen ü. d. Bau, etc. Die Gattung Spongelia.” Zeit. f. wiss. Zool., Bd.
XXXII. 1878.

[67] Metschnikoff was the first to give this account of the development of the
spicules in Sycandra, but Prof. Schulze has informed me by letter that he has
arrived at the same result.
[68] Keller (No. 129) has recently given an account of the development of
Halichondria (Chalinula) fertilis. He finds that there is an irregular segmentation,
followed by a partial epibolic invagination, the inner mass of cells remaining
exposed at one pole and forming there a prominence, equivalent to the granular
prominence in the larvæ of other Silicispongiæ. The free-swimming larva resembles
the larva of other Silicispongiæ in the possession of spicula, etc., and after
becoming laterally compressed attaches itself by one of the flattened sides. A central
cavity is formed in the interior with ciliated chambers opening into it, and is
subsequently placed in communication with the exterior by the formation of an
aperture which constitutes the osculum.
[69] That the greater part of the flat cells which line the passages of most Sponges
are really derived from epiblastic invaginations appears to me to be proved by
Schulze’s and Barrois’ observations on the young fixed stages of Halisarca.
Schulze’s (No. 140) observations have however proved that the flat cells lining the
axial gastric chamber of Sycandra are hypoblastic in origin, and the observations of
Keller (No. 129) and Ganin (No. 124) have led to the same result for the flat
epithelium lining part of the passages of the Silicispongiæ.
[70] “On the Nutritive and Reproductive Processes of Sponges.” Ann. and Mag. of
Nat. Hist., Vol. IV. Ser. V. 1879.
[71] There is a Russian paper by the same author, containing a full account, with
clear illustrations, of his observations.

CHAPTER VI.

CŒLENTERATA[72].

Hydroidea. The most typical mode of development of the Hydroidea is that
in which the segmentation leads directly to the formation of a free ciliated
two-layered larva, known since Dalyell’s observations as a planula. The
planula is characteristic of almost all the Hydromedusæ with fixed
hydrosomes including the Hydrocoralla (Stylasteridæ and Millepora), the
most important exceptions being the genus Tubularia and one or two other
genera, and the fresh-water Hydra.
In a typical Sertularian the segmentation is approximately regular[73] and
ends according to the usual accounts in the formation of a solid spherical
mass of cells. A process of delamination now takes place, which leads to the
formation of a superficial layer of cubical or pyramidal cells, enclosing a
central solid mass of more or less irregularly arranged cells.
The embryo, in the cases in which it is still contained within the sporosack,
now begins to exhibit slight changes of form, and one extremity of it begins
to elongate. It soon becomes free, and rapidly assumes an elongated
cylindrical form, while a coating of cilia, by means of which it moves
sluggishly about, appears on its outer surface. A central cavity appears in
the interior, and the inner cells form themselves into a definite hypoblast.
The larva has now become a planula, and consists of a closed sack with
double walls. It continues for some few days to move about, but eventually
drops its cilia, and becomes dilated at one extremity, by which it then
becomes attached. The base of attachment becomes gradually enlarged so as
to form a disc, which spreads out and is frequently divided by fissures into
radiating lobes. The free extremity becomes enlarged to form the eventual
calyx.
Over the whole exterior a delicate pellicle—the future perisarc—now
becomes secreted. Round the edge of the anterior enlargement a row of
tentacles makes its appearance. These, in the embryos of the Tubularian
genera, lie some little way behind the apex of the body. After a certain time

the perisarc, which has hitherto been continuous, becomes ruptured in the
region of the calyx, and the tentacles become quite free. At about the same
period a mouth is formed at the oral apex.

Fig. 68. Three larva stages of Eucope polystyla.
(After Kowalevsky.)
A. Blastosphere stage with hypoblast spheres becoming budded off into the central cavity.
B. Planula stage with solid hypoblast.
C. Planula stage with a gastric cavity.
ep. epiblast; hy. hypoblast; al. gastric cavity.

The development of Eucope polystyla (fig. 68), one of the Campanularidæ,
deviates according to Kowalevsky (No. 147) in somewhat important points
from the usual type. The whole development takes place after the deposition
of the ovum. The segmentation results in the formation of a single-walled
blastosphere with a large central cavity (fig. 68 A). This cavity, somewhat
as in Ascetta, becomes filled up with a not clearly (?) cellular material
derived from the walls of the blastosphere, which must be regarded as the
hypoblast (fig. 68 B). The larva elongates and becomes ciliated, and the
epiblast at its two extremities becomes thickened, and is stated by
Kowalevsky also to become divided into two layers. The alimentary cavity
appears as a slit in the middle of the hypoblast (fig. 68 C). The cilia after a

time disappear, and the larva then becomes fixed by one extremity. It
flattens itself out into a disc-like form, becomes divided into four lobes, and
covered by a cuticle (perisarc). From the disc the stalk grows out which
dilates at its free extremity into the calyx.

Fig. 69. Longitudinal section through a larva of Tubularia mesembryanthemum while
still in the gonophore. The lower end is the oral one.

ep. epiblast; hy. hypoblast of tentacle; en. enteric cavity.

In both the groups (Tubularia and Hydra) which are exceptional in not having a ciliated planula stage,
its absence may be put down to an abbreviation of the development, and in fact a two-layered
quiescent stage, through which the embryo passes, may be regarded as representing the planula stage.
The development of Tubularia, which has been described in detail by Ciamician, takes place in the
gonophore[74]. The segmentation is irregular and leads to the formation of an epibolic gastrula, four
large central cells constituting the hypoblast[75]. The larva now elongates, and grows out laterally into
two processes which constitute the first pair of tentacles. At this stage it closely resembles the larvæ
of some Medusæ. Additional tentacles are soon formed; and a central cavity appears in the hypoblast,
the cells of which have in the meantime become more numerous (fig. 69). The tentacles are directed
towards the aboral side, which is considerably more prominent than the oral one. They contain a
hypoblastic axis. The aboral end continues to grow and the tentacles gradually assume a horizontal
position. A constriction now appears, dividing the larva into an aboral portion which will eventually
form the stalk, and an oral portion. At the apex of the latter a row of short tentacles—the future oral
tentacles—now appears. The larva has at this stage the form known as Actinula. In this condition it
becomes hatched, and shortly afterwards it becomes fixed by the aboral end and grows into a colony.
The development of Myriothela (Allman, No. 150) takes place on the Tubularian type. The ovum
invested by a delicate capsule becomes freed by the rupture of the gonophore, and is then taken up by
the remarkable claspers characteristic of the genus. In the claspers it becomes fecundated and
undergoes its further development. After segmentation a gastric cavity is formed, and provisional
tentacles arise as a series of conical involutions which subsequently become evoluted. Permanent

tentacles are formed as conical papillæ on a truncated oral process. After hatching it has a few days’
free existence, and then becomes attached, and loses its provisional tentacles.
Although Hydra itself constitutes the simplest type of Hydrozoon, its development, which has been
fully investigated by Kleinenberg (No. 161), is in some respects a little exceptional. The
segmentation is regular, but a segmentation cavity is not formed. The peripheral layer of cells
gradually becomes converted into a chitinous membrane, which is perhaps homologous with the
perisarc of marine forms. Between the membrane and the germ a second pellicle makes its
appearance. The above changes require about four days for their completion, but there next sets in a
period of relative quiescence which lasts for some 6‑8 weeks. During this period the remaining
development is completed. The cells of the germ first fuse together. In the interior of the protoplasm
a clear excentric space arises, which gradually extends itself and forms the rudiment of the gastric
cavity. The outer shell in the meantime becomes less firm, and is finally burst and thrown off, owing
to the expansion of the embryo within.
The outermost layer of the protoplasm becomes, relatively to the inner layer, clear and transparent,
and there thus arises an indication of a division of the walls of the archenteric cavity into two zones,
or layers. These layers, which form the epiblast and hypoblast, are definitely established on the
appearance of cells with contractile tails[76] in the clear outer zone, between which the interstitial
epiblast cells subsequently arise.
The embryo, still forming a closed double-walled sack, elongates itself, and at one pole its wall
becomes very thin. And at this point a rupture takes place which gives rise to the mouth.
Simultaneously with the mouth the tentacles become formed as hollow processes, according to
Mereschkowsky two being formed first and subsequently the others in pairs. Very shortly afterwards
the hitherto uniform hypoblast becomes divided up into distinct cells. The thin inner pellicle which
persists after the rupture of the outer membrane becomes in the meantime absorbed. With these
changes the embryo practically acquires the characters of the adult.

Trachymedusæ. Amongst the Trachymedusæ, which as has now been
satisfactorily established develop directly without alternations of
generations, the embryology of species both of the Geryonidæ and the
Æginidæ has been studied.
In all the types so far investigated the hypoblast is formed by delamination,
and there is a more or less well-marked planula stage.

Fig. 70. Diagrammatic figure shewing the delamination of the ovum of Geryonia.
(Copied from Fol.)
cs. segmentation cavity; a. endoplasm; b. ectoplasm. The dotted lines shew the course of the
next planes of division.

The development of Geryonia (Carmarina) hastata has been studied by Fol
(No. 155) and Metschnikoff (No. 163)[77]. The ovum, when laid, is invested
by a delicate vitelline membrane and mucous covering. Its protoplasm is
formed of an outer granular and dense layer, and a central mass of a more
spongy character. The segmentation is complete and regular, and up to the
time when thirty-two segments have appeared each segment is composed of
both constituents of the protoplasm of the ovum. A segmentation cavity
appears when sixteen segments are formed, and becomes somewhat larger
at the stage with thirty-two. At this stage the process of delamination
commences. Each of the thirty-two segments, as shewn in the
accompanying diagram (fig. 70), becomes divided into two unequal parts.
The smaller of these is formed almost entirely of granular material; the
larger contains portions of both kinds of protoplasm. In the next
segmentation the thirty-two large cells only are concerned, and in each of
these the line of division passes between the granular and the transparent
protoplasm. The sixty-four lenticular masses of granular protoplasm thus
formed constitute an outer closed epiblastic vesicle, within which the thirty-
two masses of transparent protoplasm form an hypoblastic vesicle. The
embryo at this stage is shewn in optical section in fig. 71.

Fig. 71. Embryo of Geryonia after delamination. (After Fol.)
ep. epiblast; hy. hypoblast.

The epiblastic vesicle now grows rapidly, while the hypoblastic vesicle
remains nearly passive and becomes somewhat lens-shaped. At one point its
wall comes in close contact with the epiblast. Elsewhere a wide cavity is
developed between the two vesicles which becomes filled with gelatinous
tissue. At this period cilia appear on the surface, and the larva becomes a
planula.
The succeeding changes lead rapidly to the formation of a typical Medusa.
Where the epiblast and hypoblast are in contact the former layer becomes
thickened and forms a disc-shaped structure. The centre of this becomes
somewhat protuberant, fuses with the hypoblast and then becomes
perforated to form the mouth (fig. 72 o). The edge of the disc forms a
thickened ridge, the rudiment of the velum (v), which is entirely formed of
epiblast. At its edge six tentacles (t) arise, into which are continued solid
prolongations of the wall of the now somewhat hexagonal gastric chamber.
The hypoblastic axes of the tentacles soon lose their connection with the
gastric wall.

Fig. 72. Optical section through the oral pole of Geryonia after the appearance of the
gelatinous tissue of the disc. (After Fol.)

o. mouth; v. velum; t. tentacle.
The shaded part represents the gelatinous tissue.

Up to this time the larva has retained a more or less spherical form, and the
cavity on the under side of the umbrella has not yet become developed. The
latter now becomes established by the whole disc assuming a vaulted form
with the concavity directed downwards. The lining of the cavity so formed
is derived from the epiblast of the disc already spoken of.
The exact mode of formation of the gastrovascular canals has not been worked out. It has however
been established by the researches of the Hertwigs (No. 146) and Claus (No. 153) that the radial and
circular vessels of this system are connected together in adult Medusæ by an hypoblastic lamella; so
that these canals would seem to be the remnants of an once-continuous gastric cavity. This mode of
formation is established in the case of the medusiform buds; and it would therefore seem, as pointed
out by the Hertwigs, a fair deduction that it occurs in the larva—a conclusion which is confirmed by
the primitive extension of the gastric cavity to the edge of the disc at the time when its walls give rise
to the solid axes of the tentacles. In the course of the subsequent retirement of the gastric cavity from
the edge of the disc the gastrovascular canals probably take their origin, though Fol was unable to
follow the changes which result in their formation.

On the completion of the above changes the larva has become a fully
formed Medusa, but it undergoes a not inconsiderable metamorphosis
before the attainment of the adult state.

Fig. 73. A three-days’ larva of Æginopsis with two tentacles.
(After Metschnikoff.)
m. mouth; t. tentacle.

Two species of Æginidæ have been studied by Metschnikoff (163), viz.
Polyxenia leucostyla (Ægineta flavescens), and Æginopsis mediterranea. In
both of these forms the segmentation results in the formation of an
elongated two-layered ciliated planula, without a central cavity. The two
ends of this grow out into two long processes—the rudiments of a pair of at
first aborally directed arms—which contain a solid hypoblastic axis (fig.
73). At this stage the larva closely resembles the larva of Tubularia. An
alimentary cavity is hollowed out in the centre of the hypoblast which soon
opens by a wide oral aperture (m). A second pair of arms becomes formed,
which are at first much shorter than the original pair; with their formation a
radial symmetry is acquired. Sense organs become at the same time
developed, and the whole embryo assumes a medusiform character. Fresh
tentacles arise, the velum and cavity of the umbrella become established,
but these changes do not involve any points of very special interest.
Siphonophora. The development of the Siphonophora has been the subject
of careful investigation by Haeckel (158) and Metschnikoff (163). The ova
are large and usually (except Hippopodius) without a membrane.
They are formed of a peripheral denser layer of protoplasm and a central
spongy mass. They usually undergo their entire development in the water.
In some instances they have been successfully reared by artificial
impregnation.
As an example of the Calycophoridæ I shall take Epibulia aurantiaca, a
form allied to Diphyes, the development of which has been studied by
Metschnikoff[78].

Fig. 74. Three larval stages of Epibulia aurantiaca.
(After Metschnikoff.)
A. Planula stage.
B. Six-days’ larva with nectocalyx (nc) and tentacle (t).
C. Somewhat older larva with gastric cavity.
ep. epiblast; hy. hypoblast; so. somatocyst; nc. nectocalyx; t. tentacle; c. large yolk cells; po.
polypite.

There is a regular segmentation, unaccompanied by the formation of a
segmentation cavity. At its close the ovum becomes a spherical ciliated
embryo. This embryo soon becomes elongated, and its cells differentiate
themselves into a central and a peripheral layer—the epiblast and the
hypoblast (fig. 74 A). At this stage the larva has the typical planula form.
The epiblast is especially thickened at a pole, which may be called the oral
pole, and towards the side of this, which will be spoken of as the ventral
side. Adjoining this thickened layer of epiblast a special thin layer of
hypoblast becomes differentiated, which in opposition to the main mass of
large nutritive cells forms the true hypoblastic epithelium (fig. 74 B, hy).
On this thickening two prominences make their appearance (fig. 74 B). The

oral of these is the rudiment of a tentacle (t), and the aboral of a nectocalyx
(nc).

Fig. 75. An advanced larva of Epibulia aurantiaca with one large nectocalyx. (After
Metschnikoff.)
so. somatocyst; nc. second imperfectly developed nectocalyx; hph. hydrophyllium; po.
polypite; t. tentacle.

The former of these elongates itself in succeeding stages into a process of
both epiblast and hypoblast. The central part of the nectocalyx on the other
hand appears to originate from a thickening of the epiblast in which the
cavity of the bell becomes subsequently hollowed out. Between this part
and the external epiblast which gives origin to the outermost layer of the
nectocalyx a layer of hypoblast is interposed. When the nectocalyx has
become to a certain extent established a cavity—the commencement of the
primitive gastrovascular cavity of the adult—appears in the general

hypoblast between the epithelial and nutritive layers in the immediate
neighbourhood of its attachment. This cavity becomes prolonged into the
nectocalyx to form the four gastrovascular canals; while the hypoblast at the
upper end of the nectocalyx forms the somatocyst (fig. 74 C, so). The
primitive enteric cavity once formed rapidly extends, especially in an oral
direction (fig. 74 C), and forms a widish cavity in the oral part of the
embryo. At the pole of this part (fig. 74, po) is eventually formed the
opening of the mouth, and the contained cavity becomes in a special sense
the gastric cavity. This region of the embryo may be spoken of as the
polypite. The nectocalyx grows with great rapidity and soon forms by far
the most prominent part of the larva (fig. 75). The true gastric region or
polypite (fig. 75, po) continues also to grow, and a mouth becomes formed
at its extremity. The aboral end of the original body of the embryo gradually
atrophies.

Fig. 76. Two stages in the development of Stephanomia pictum.
(After Metschnikoff.)
A. Stage after the delamination. ep. epiblastic invagination to form pneumatocyst.
B. Later stage after the formation of the gastric cavity in the solid hypoblast, po. polypite; t.
tentacle; pp. pneumatophore; ep. epiblastic invagination to form pneumatocyst; hy. hypoblast
surrounding pneumatocyst.

At the junction of the nectocalyx and polypite the cœnosarc becomes
formed, and rudiments of a second nectocalyx (nc) and second polypite
early become visible; while a hydrophyllium is formed as a bud which
covers over the first polypite and tentacle (hph). With the development of
the hydrophyllium the first segment, if the term may so be used, is
complete. The second segment of which a rudiment is already present as a
second polypite is intercalated between the first segment and the
nectocalyces.
Amongst the Physophoridæ there is a considerable range of variation in
development; though the variations concern for the most part not very
important points. The simplest type hitherto observed is that of
Stephanomia (Halistemma) pictum. The segmentation and formation of a
two-layered planula (fig. 76) take place in the usual way. Between the solid
central mass of nutritive hypoblast cells and the epiblast an epithelial
hypoblastic layer becomes interposed which undergoes a special thickening
at the aboral pole. At this pole a solid involution of epiblast next becomes
formed, to which a layer of hypoblast becomes applied. The structure so
formed is the rudiment of the pneumatocyst (ep). In the next stage the air-
cavity of the pneumatocyst becomes established within the epiblast.
The gastrovascular cavity is formed in the midst of the nutritive hypoblast
cells, which then become rapidly absorbed leaving the gastrovascular cavity
entirely enclosed by the epithelial layer of hypoblast (fig. 76 B).
By the above changes the more important organs of the larva have become
established. The one end forms the pneumatophore, and the other, the oral
part, the polypite. Between the two there is already present the rudiment of
a tentacle, and a second tentacle soon becomes formed. The mouth arises as
a perforation at the oral end of the larva.
The pneumatophore contains a prolongation of the gastrovascular cavity,
the fluid in which bathes the outer hypoblastic wall of the pneumatocyst. It
has however no communication with the enclosed cavity of the
pneumatocyst. In the later developmental stages the size of the
pneumatophore becomes immensely reduced in comparison with the
remainder of the larva.

The development of Physophora agrees closely with that of Stephanomia except in one somewhat
important point, viz. in the development of a provisional hydrophyllium. This arises as a prominence
at the aboral pole, containing a prolongation of the gastrovascular cavity. Between the epiblast and
hypoblast of the prominence gelatinous tissue becomes deposited, and the hydrophyllium is thus
converted into a large umbrella-like organ enclosing the polypite. The two together have a close
resemblance to an ordinary Medusa, the polypite forming the manubrium, and the hydrophyllium the
umbrella. The hydrophyllium is eventually thrown off.
An important type of Physophorid development is exemplified in Crystalloides, a genus closely
allied to Agalma. In this type the greater part of the original ovum, instead of directly giving rise to
the polypite, becomes a kind of yolk-sack, from which the polypite is secondarily budded (fig. 77,
yk). Agalma sarsii is in this respect intermediate between Crystalloides and Physophora. Both these
types are remarkable for developing a series of provisional hydrophyllia (fig. 77, h.ph.). In both
genera the first of these develops as in Physophora, and for a long time is the only one functional.

The conclusions to be drawn from the above description may be summed
up as follows. In all the Siphonophora, so far observed, the starting point
for further development is a typical ciliated two-layered planula. The inner
layer or hypoblast is mainly formed of large nutritive cells. From these cells
an epithelial hypoblastic layer becomes secondarily differentiated, the exact
relations of which differ somewhat in the various types. The nutritive cells
themselves do not appear to become directly converted into the permanent
hypoblastic tissues. The development of the adult from the planula
commences by the thickening of the epiblastic layer, usually at one pole
(the future proximal or aboral pole), and the formation at this pole of a
series of bud-like structures (in the growth of which both embryonic layers
have a share), which become converted into the hydrophyllia, nectocalyces
etc. The main oral part of the planula becomes generally converted into the
polypite, though in some instances (Crystalloides) it remains as a yolk-sack,
and only secondarily gives rise to a polypite.
Two very different views have been taken as to the nature of the various
component parts of the Siphonophora, and the embryological evidence has
been appealed to by both sides in confirmation of their views. By Huxley
and Metschnikoff the various parts—nectocalyces, hydrophyllia,
hydrocysts, polypites, generative gonophores etc. are regarded as simple
organs, while by Leuckart, Haeckel, Claus etc. they are regarded as so many
different individuals forming a compound stock. The difference between
these two views is not merely as to the definition of an individual[79]. The
question really is, are these parts originally derived by the modification of
complete zooids like the gonophores and trophosomes of the fixed

Hydrozoa stocks, or are they structures derived from the modification of the
tentacles or some other parts of a single zooid?

Fig. 77. Larva of Crystalloides, (After Haeckel.)
h.ph. hydrophyllium; h. hydrocyst; t. tentacle; pp. pneumatophore; po. polypite; yk. yolk-
sack.

The difficulty of deciding this point on embryological evidence depends on
the fact that ontologically a tentacle and a true bud arise in the same way,
viz. as papilliform outgrowths containing prolongations of both the
primitive germinal layers. The balance of evidence is nevertheless in my
opinion in favour of regarding the Siphonophora as compound stocks, and
the views of Claus on this subject (Zoologie, p. 271) appear to me the most
satisfactory.
The most primitive condition is probably that like Physophora in an early stage with an
hydrophyllium enclosing a polypite (cf. Haeckel and Metschnikoff). In this condition the whole larva
may be compared to a single Medusa in which the primitive hydrophyllium represents the umbrella
of the Medusa, and the polypite the manubrium. The tentacle which appears so early is probably not
to be regarded as a modified zooid, but as a true tentacle. The absence of a ring of tentacles is
correlated with the bilateral symmetry of the Siphonophora.
The primitive zooid of a Siphonophora stock is thus a Medusa. Like Sarsia and Wilsia this Medusa
must be supposed to have been capable of budding. The ordinary nectocalyces by their resemblance
to the umbrellas of typical Medusæ are clearly such buds of the medusiform type. The same may be
said of the pneumatophore, which, as pointed out by Metschnikoff, is identical in its development

with a nectocalyx. Both are formed by a solid process of epiblast in which a cavity—the cavity of the
nectocalyx or pneumatocyst—is eventually hollowed out. Around this there appears a double layer of
hypoblast containing a prolongation of the gastrovascular cavity; and this is in its turn enclosed by a
layer of epiblast which forms the covering of the convex surface of the nectocalyx and the external
epiblast of the pneumatophore.
The generative gonophores are clearly also zooids, and the hydrophyllia are probably a rudimentary
form of umbrella. In many cases (Epibulia, Stephanomia, Halistemma etc.) the hydrophyllium of the
primitive polypite (manubrium) is absent. In such instances it is necessary to suppose that the
umbrella of the primitive zooid of the whole colony has become aborted. Leuckart originally took a
somewhat different view from the above in that he regarded the starting point of the Siphonophora to
be a compound fixed Hydrozoon stock, which became detached and free-swimming.

Acraspeda[80]. The embryonic development of several of the forms of the
Acraspeda has been investigated by Kowalevsky (No. 147) and Claus (No.
153). Their observations seem to point to an invaginate gastrula being
characteristic of this group.
Amongst the forms with alternations of generations and a fixed larval form
Chrysaora and Cassiopea have been most fully investigated. The ovum of
the former undergoes the first embryonic phases while still in the ovary. In
the latter it is enclosed amongst the oral processes. A complete and more or
less regular segmentation leads to the formation of a single-walled
blastosphere with a small segmentation cavity. The wall of the blastosphere
next becomes invaginated, giving rise to an archenteron (fig. 78 A). The
blastopore soon closes up, and the archenteron is converted into a closed
sack completely isolated from the epiblast (fig. 78 B). The surface of the
larva becomes in the meantime covered with cilia. The free larval stage thus
reached is similar to the ordinary Hydrozoon planula. After the closure of
the blastopore the larva becomes elongated, and one end becomes
narrowed. By this narrowed extremity the larva soon attaches itself, and at
the opposite and broader end a fresh involution of the epiblast appears (fig.
78 C); this gives rise to the stomodæum, which is placed in communication
with the archenteron on the absorption of the septum dividing them. The
relation of the stomodæum to the original blastopore has not been
determined.
At the point of attachment there is developed a peculiar pedal disc, and
around the mouth there appears a fold of epiblast which gives rise to an oral
disc (fig. 78 D). Two tentacles first make their appearance, but one of these
is primarily much the largest, though eventually the second overtakes it in

its growth. A second pair of tentacles next becomes formed, giving to the
larva a 4-radial symmetry. Between these four new tentacles subsequently
sprout out, and in the intermediate planes four ridge-like thickenings of the
hypoblast, projecting into the cavity of the stomach, make their appearance.
They imperfectly divide the stomach into four chambers, to each of which
one of the primary tentacles corresponds; they may be regarded as
homologous with the mesenteries of the Actinozoa. The number of tentacles
goes on increasing somewhat irregularly up to sixteen. All the tentacles
contain a solid hypoblastic axis. Muscular elements are developed from the
epiblast.

Fig. 78. Four stages in the development of Chrysaora.
(After Claus.)
A. Gastrula stage.
B. Stage after closure of blastopore.
C. Fixed larva with commencing stomodæum.
D. Fixed larva with mouth, short tentacles, etc.
ep. epiblast; hy. hypoblast; st. stomodæum; m. mouth; bl. blastopore.

With the above changes the so-called Hydra tuba or Scyphistoma form is
reached (vide fig. 85). The peculiar strobilization of this form is dealt with
in the section devoted to the metamorphosis.
Aurelia is stated by Kowalevsky to develop in the same way as Cassiopea; and the one stage of
Rhizostoma observed is that in which it has a (probably invaginate) gastrula form.

In Pelagia the ovum directly gives rise to a form like the parent. The segmentation and the
invagination take place nearly as in Cassiopea, but the archenteric cavity is relatively much smaller,
and the large space between it and the epiblast becomes filled with the gelatinous tissue which forms
the umbrella. The blastopore does not appear to close but to become directly converted into the
mouth. As in Cassiopea the larva takes a somewhat four-sided pyramidal form. The mouth is placed
at the base. The pyramid becomes subsequently flatter, and at the four corners four tentacles grow out
which increase to eight by division. The flattening continues till the larva reaches a form hardly to be
distinguished from the Ephyra resulting from the strobilization of the fixed Scyphistoma form of
other Acraspeda.

Alcyonidæ. In the Alcyonidæ the segmentation appears always to lead to
the formation of a solid morula, which becomes a planula by delamination.
The true enteric cavity is formed by an absorption of the central cells, but
the axial portion of the gastric cavity and mouth are formed by an epiblastic
invagination.
The development of these types has been mainly studied by Kowalevsky (147), and my knowledge of
his results is derived from German abstracts of the original Russian memoirs.
In Alcyonium palmatum the impregnation is external. The segmentation is very exceptional in
character. It commences with the formation of a series of irregular prominences on the surface of the
ovum, which become segmented off to form a superficial layer of epiblast cells. The inner mass of
protoplasm then divides up into polygonal cells to form the hypoblast, which would thus seem to be
formed by a kind of delamination. In Clavularia crassa (No. 168) there is a complete segmentation
followed by a delamination. The larva of Al. palmatum elongates and becomes ciliated, and so
assumes the characters of a typical planula. The central hypoblast is formed of an outer granular
stratum with imperfectly differentiated cells—the true hypoblast—and an inner homogeneous mass
with vacuoles.
Some of the larvæ become fixed, while others coalesce together and form a large mass, the fate of
which has not been further studied. An invagination of epiblast takes place at the free end of the fixed
larva, which gives rise to the so-called gastric cavity, i.e. the axial portion of the general enteric
cavity, which would appear to be in reality a kind of stomodæum. Around the gastric cavity the
hypoblast forms eight mesenteries, the chambers between which are filled with the homogeneous
material which occupied the centre of the ovum in the previous stage. It is to be presumed, though
not stated, that by an absorption of the blind end of the stomodæal invagination the gastric chamber is
placed in free communication with the spaces between the mesenteries[81]. During the next stage the
young Alcyonium also acquires eight tentacles, which arise as hollow papillæ opening into the eight
mesenteric chambers. By this stage also the matter filling up the mesenteric chambers is nearly
absorbed.
Between the epiblast and hypoblast there is formed an homogeneous membrane, which penetrates in
between the two layers of hypoblast which form the mesenteries. On the outer side of this membrane,
and therefore presumably derived from the epiblast, is a layer of connective-tissue cells, which
eventually gives rise to the abundant gelatinous tissue (cœnenchyma) in which the skeletal elements
are deposited. In Sympodium coralloides Kowalevsky (No. 168) has shewn still more completely the
derivation of the stellate mesoblast cells from the epiblast. He finds that the calcareous spicula
develop in these cells as in the mesoblast cells of sponges. The branched gastrovascular canals in this
tissue are outgrowths of the primitive enteric cavity. A layer of circular muscles is formed at a late

period from the epiblast, but the longitudinal muscles of the mesenteries on the inner side of the
homogeneous membrane are regarded by Kowalevsky as hypoblastic.
A ciliated planula with delaminated hypoblast is also found in Gorgonia and Corallium rubrum. In
the former genus at the time when the larva becomes fixed, the hypoblast is formed of two strata, an
outer one of columnar cells, and an inner one of round ciliated cells lining a central enteric cavity.
The inner layer is believed by Kowalevsky to become eventually absorbed and to be homologous
with the inner granular mass of Alcyonium.

Zoantharia. Amongst the Zoantharia several forms have been investigated
by Kowalevsky (147) and Lacaze Duthiers (170), of which some are stated
by the former author to pass through an invaginate gastrula stage, while in
other instances the hypoblast is probably formed by delamination.
To the first group belongs an edible form of Sea Anemone found near
Messina, Cerianthus, and perhaps also Caryophyllium. In the first of these
segmentation results in the formation of a blastosphere. A normal
invagination obliterating the segmentation cavity then ensues, and the
blastopore narrows to form the mouth. The borders of the mouth bend
inwards and so give rise to the gastric cavity (stomodæum) which as in the
Alcyonidæ is lined by epiblast. Simultaneously with the formation of the
mouth there appear the two first mesenteries.
In Cerianthus the segmentation is unequal, the early stages are the same as in the Actinia just
described, but the hypoblast cells give rise to a mass of fatty material filling up the enteric cavity,
which becomes eventually absorbed.

In the majority of the Zoantharia so far investigated, including species of
Actinia, Sagartia, Bunodes, Astroides, Astræa, the segmentation, which is
often unequal[82] and not accompanied by the formation of a segmentation
cavity, results in a solid two-layered ciliated planula. In these forms the
impregnation takes place in the ovary, and the early stages of development
are passed through in the maternal tissues.
One end of the planula becomes somewhat oval and develops a special
bunch of cilia. At the other end a shallow depression appears, which
becomes deeper and forms an involution lined by epiblast. This involution
is the stomodæum, and becomes the so-called gastric cavity. The true
enteric cavity lined by hypoblast is for some time filled with yolk material.
The larva always swims with the aboral end directed forwards.

Between the two embryonic layers a homogeneous membrane is formed,
similar to that already described in the Alcyonidæ.
The further development of the larvæ especially concerns the formation of mesenteries, tentacles and
calcareous skeleton. With reference to this subject the observations of Lacaze Duthiers are especially
valuable and striking.
In the adult it is usually possible to recognise in the tentacles a symmetry of six. There are six
primary tentacles, six secondary, twelve tertiary, twenty-four quaternary, etc. In the hard septa of the
skeleton the same law is followed up to the third cycle, but beyond that, in the cases where the point
can be verified, there appear to be only twelve septa in each additional cycle. The observations of
Lacaze Duthiers have shewn that this symmetry is only secondarily acquired and does not in the least
correspond with the succession of the parts in development.
His observations were conducted on three species of Zoantharia without a skeleton, viz. Actinia
mesembryanthemum, Sagartia, and Bunodes gemmacea; while Astroides calycularis served as the
type for his investigations on the corallum. It will be convenient to commence with his results on
Actinia mesembryanthemum which served as his type.
The free cylindrical embryo, with the aboral end directed forwards in swimming, first becomes
somewhat flattened and the mouth elongated. A bilateral symmetry is thus brought about. Two
mesenteries now make their appearance transversely to the long axis of the mouth, which divide the
enteric cavity into two unequal chambers. The mesenteries consist of a fold of hypoblast with a
prolongation of the epiblast between the two limbs of the fold. The larger chamber next becomes
divided by two fresh mesenteries into three, and a similar division then takes place in the smaller
chamber. The stage with six chambers is almost immediately succeeded by one with eight, owing to
the appearance of two fresh mesenteries in the second-formed set of chambers. At the stage with
eight chambers there is a marked period of repose. The number of chambers is increased to ten by the
division of the third-formed set of chambers, and to twelve by the division of the fourth-formed set. It
will be observed that the number of the chambers increases in arithmetical progression by the
continual addition of two, alternately cut off from the primitive large and small chambers. The
freshly formed chambers are always formed immediately on one side of the primitive mesenteries.
The stages with six and ten are of very short duration. The two primitive chambers are necessarily at
the ends of the long axis of the mouth. After the division of the enteric cavity into twelve chambers,
these chambers become about equal in size, and the formation of the tentacles commences. The law
regulating the appearance of the tentacles is nearly the same as that for the mesenteries, but is not
quite so precise. One tentacle makes its appearance for each chamber. The most remarkable feature in
the appearance of the tentacles is due to the fact that the tentacle surmounting the primitive largest
chamber arises before any of the others, and long retains its supremacy (fig. 80 A). This fact, coupled
with the inequality of the two primitive chambers, supplies some grounds for speculating on a
possible descent of the Cœlenterata from bilaterally symmetrical forms with distinctly differentiated
dorsal and ventral surfaces. The supremacy of the first-formed tentacle is not confined to the
Actinozoa, but as has already been indicated, is also found in the Scyphistoma (p. 166) of the
Acraspeda.

Fig. 80. Two stages in the development Of Actinia mesembryanthemum. (After Lacaze
Duthiers.)
In the younger ciliated embryo A, viewed from the side, only one tentacle is developed. m.
mouth.
The older larva B is viewed from the face when 24 tentacles have just become established.
The letters shew the true order of succession of the tentacles; but e and f are transposed.

After the twelve tentacles have become established they become secondarily divided into two cycles
of six respectively larger and smaller tentacles, which alternate with each other. The two tentacles
pertaining to the two original chambers belong to the cycle of larger tentacles. The mesenteric
filaments appear first of all on the primary pair of septa. The increase in the number of tentacles and
chambers from 12 to 24 has been found to take place in a very remarkable and unexpected way. The
law is expressed by Lacaze Duthiers as follows. “The appearance of the new chambers is not, as has
been believed, a consequence of the production of a single chamber between each of the twelve
already existing chambers, but of the birth of two new chambers in each of the six elements
(chambers) of the smaller cycle.” The result of this law is that a pair of tentacles of the third cycle is
placed in every alternate space, between a large and a small tentacle, of the two already existing
cycles, which may conveniently be called the first and second cycles (fig. 80 B).
The twenty-four tentacles formed in the above manner are obviously at first very irregularly arranged
(fig. 80 B), but they soon acquire a regular arrangement in three graduated cycles of 6, 6 and 12. The
first cycle of the six largest tentacles is the large cycle of the previous stage, but the two other cycles
are heterogeneous in their origin, each of them being composed partly of the twelve tentacles last
formed, and partly of the six tentacles of the second cycle of the previous stage.
The further law of multiplication has been thus expressed by Lacaze Duthiers: “The number of
chambers and still later that of the corresponding tentacles is carried from 24‑48 and from 48‑96 by
the birth of a pair of elements in each of the 12 or 24 chambers, above which are placed the smallest
tentacles which together constitute the fourth or fifth cycle. Since, after the formation of each fresh
cycle, the arrangement of the tentacles again becomes symmetrical, it is obvious that all the equal
sized cycles except the first are formed of tentacles entirely heterogeneous as to age.”
The fixation of the free-swimming larva takes place during the period when the tentacles are
increasing from 12 to 24.
The general formation of the chambers in Bunodes and Sagartia is nearly the same as in Actinia.

In the two types of Actinozoa with an embolic gastrula stage the laws as to the formation of the
tentacles do not appear to be the same as those regulating the forms observed by Lacaze Duthiers.
In Cerianthus four tentacles are formed simultaneously at the period when only four chambers are
present. In Arachnitis (Edwarsia) the succession of the tentacles is stated (A. Agassiz, 166) to
resemble that in Cerianthus. There are originally four tentacles, and at one extremity of the long axis
of the mouth are the oldest tentacles, while at the other tentacles are constantly added in pairs. An
odd tentacle is always found at the extremity of the mouth opposite the oldest tentacles.
In the other species with an embolic gastrula eight tentacles would seem to appear simultaneously at
the period when eight chambers are present; though on this point Kowalevsky’s description is not
very clear. The presence of such a stage would seem to indicate a close affinity to the Alcyonidæ.
Amongst the sclerodermatous Actinozoa, except Caryophyllium, the embryo closely resembles that
of the delaminate Malacodermata. The first stages occur in the ovary, and the larva is dehisced into
the body cavity as a two-layered ciliated planula.
The laws affecting the formation of the first twelve tentacles and septa appear to be nearly the same
as for the Malacodermata. The hard parts begin as a rule to be formed when twelve tentacles have
appeared, at which period also the fixation of the larva takes place. On fixation the larva becomes
very much flattened.
The first parts of the corallum to appear are twelve of the septa, which arise simultaneously in folds
of the enteric wall in the chambers between the mesenteries, and correspond therefore with the
tentacles and not, as might be supposed, with the mesenteries. Each septum is formed by the
coalescence of three calcareous plates which originate in separate centres of calcification. The
concrescence of the three produces a Y-shaped plate with the single limb directed inwards and the
two limbs outwards (fig. 81). The theca does not arise till after the septa have become formed, and is
at first a somewhat membranous cup quite distinct from the septa. The columella is formed still later
by the coalescence of a series of nodules which are formed in a central axis enclosed by the inner
ends of the septa.

Fig. 81. Larva of Astroides calycularis shortly after it has become attached. (After
Lacaze Duthiers.)

The figure shews the development of the Y-shaped septa in the intervals between the
mesenteries. The position of the latter is indicated by the faint shading. The theca has become
developed externally.

After the formation of the theca the septa become divided into two cycles by the predominant growth
of six of them. On the coalescence of the septa with the theca the space between the two limbs of the
Y becomes filled up with calcareous tissue. The law of the formation of the third cycle of septa
(12‑24) has not been worked out, so that it is not possible to state whether it follows the peculiar
principles regulating the growth of the tentacles.
The whole of the skeletal parts occupy a position between the epiblast and hypoblast, and are exactly
homologous in this respect with the skeleton of the Alcyonidæ. By Lacaze Duthiers they are however
believed to originate in the hypoblast, but from the observations of Kowalevsky there be little doubt
that they arise in the connective tissue between the two embryonic layers which is probably epiblastic
in origin.

A peculiar larva, probably belonging to the Actinozoa, has been described by Semper[83]. It has an
elongated form and is provided with a longitudinal ridge of cilia. There is a mouth at one end of the
body and an anus at the opposite extremity. The mouth leads into an œsophagus, which opens freely
into a stomach with six mesenteries. In the skin are numerous thread-cells. A mesotrochal worm-like
larva, also provided with thread-cells, and found at the same time, was conjectured by Semper to be a
younger form of this larva.

Ctenophora. The ovum of the Ctenophora is formed of an outer granular
protoplasmic layer and an inner spongy mass with fatty spherules. It is
enveloped in a delicate vesicle, the diameter of which is very much greater
than that of the contained ovum. This vesicle appears to be filled with sea-
water, in which the ovum floats.
Fertilized ova may usually be easily obtained by keeping the captured
adults in water from 12‑24 hours. The two main authorities on the
development of these forms (Kowalevsky, No. 147 and 178 and Agassiz,
No. 172) are unfortunately at variance on one or two of the most
fundamental points. It seems however that the embryonic layers are formed
by a kind of epibolic gastrula; while the true gastric cavity, as distinct from
the gastrovascular, is formed by an invagination, and deserves therefore to
be regarded as a form of stomodæum.

Fig. 82. Five stages in the development of Idyia roseola.
(After Agassiz.)
The protoplasmic layer of the ovum is represented in black.

The early stages are very closely similar in all the types so far observed.
Segmentation commences by the outer layer of the ovum, which throughout
behaves as the active layer, forming a protuberance at one pole, which may
be called the formative pole. Close below this protuberance is placed the
nucleus. In the median line of the protuberance a furrow appears (fig. 82 A),
which gradually deepens till it divides the ovum into two. The granular
layer follows the furrow so that each of the fresh segments, like the original
ovum is completely invested by a layer of granular protoplasm. Each
segment contains a nucleus. A second similar division at right angles to the
first gives rise to four segments (fig. 82 B), and the segments so formed
become again divided into eight (fig. 82 C). In the division into eight,
which takes place in a vertical plane, the segments formed are of unequal
size, four of them being much smaller than the others. The eight segments
are arranged in the form of a slightly curved disc round a vertical axis—the
future long axis of the body;—and there is a cavity in this axis which, like
the segmentation cavity of Sycandra raphanus, is open at both extremities.
The disc with its concavity on the side of the formative pole has the shape
sometimes of an ellipse (fig. 82 C) and sometimes of a rectangle, in which
the four small spheres occupy the poles of the longer axis. A bilateral
symmetry is thus even at this stage clearly indicated.
In the next phase of segmentation the granular layer surrounding each
segment again forms a protuberance at the formative pole, but, instead of

each segment becoming divided into two equal parts, the protoplasmic
protuberance alone is divided off from the main segment. In this way
sixteen spheres become formed, of which eight are large and are formed
mainly of the yolk material of the inner part of the ovum, and eight are
small and entirely composed of the granular protoplasm. The eight small
spheres form a ring on the formative surface of the large spheres (fig. 82 D).
The small spheres now increase very rapidly (fig. 82 E), partly by division
and partly by the formation of fresh cells from the large spheres; and spread
over the large spheres, forming in this way an epibolic gastrula. They
constitute a layer of epiblast. (fig. 83 A.) The large cells in the meantime
remain relatively passive, though during the process they divide, in some
cases more or less irregularly, while in Eucharis they divide into sixteen.
The axial segmentation cavity would seem during the process to become
obliterated.
There is an important discrepancy between the statements of Kowalevsky and Agassiz as to the
course of the growth of the small cells. According to Agassiz the small cells grow most rapidly at the
formative pole and cover this before they meet at the opposite pole. The reverse statement is made by
Kowalevsky. It would seem that the above discrepancy is due to an interchange on the part of the one
or the other of these authors of the two poles of the embryo, in that according to Agassiz the
formation of the mouth takes place at the formative pole, and according to Kowalevsky at the pole
opposite to this.
Without attempting to decide between the above views, we shall speak of the pole at which the
mouth is formed as the oral pole.

Fig. 83. Four stages in the development of Idyia roseola. (After Agassiz.)

s.c. sense capsule; st. stomodæum.

The formation of the alimentary cavity commences shortly after the
complete investiture of the embryo by the epiblast cells. At the oral pole an
invagination of epiblast cells takes place (fig. 83 B), which makes its way
towards the opposite pole. More especially from the figures given by
Agassiz, and from the explanation of his plates, it would seem that a large
chamber is formed in the hypoblast at the end of the invaginated tube, into
which this tube soon opens (fig. 83 C). The invaginated tube would seem to
give rise to the so-called stomach, while the chamber at its aboral extremity
is no doubt the infundibulum, which as may be gathered from
Kowalevsky’s statements, is lined by a flattened epithelium. At a later
period the gastrovascular canals grow out from the infundibulum as four
pouches, which are surrounded by, and grow at the expense of, the large
central cells, which have in the meantime arranged themselves in four
masses, and appear to serve as a kind of yolk. The nuclei of these large cells
according to Kowalevsky disappear, and the cells themselves break up into
continually smaller masses.
The main difficulty in the above description of Agassiz is the origin of the infundibulum. In the
absence of definite statements on this head it seems reasonable to conclude that it arises as a space
hollowed out in the central cells, and that its walls are formed of elements derived from the yolk
cells[84]. On this interpretation the alimentary canal of the Ctenophora would consist, as in the
Acraspedote Medusæ and Actinozoa, of two sections: (1) A true hypoblastic section consisting of the
infundibulum and the gastrovascular canals derived from it; and (2) an epiblastic section—the
stomodæum—forming the stomach.
The observations of Kowalevsky on the alimentary system do not wholly tally with those of Agassiz.
He finds that the oral side of the embryo becomes hollowed out, and that the hollow, lined by
flattened cells, becomes constricted off as the infundibulum, from which the radial canals
subsequently grow out. To the infundibulum there leads a narrow canal lined by a columnar
epithelium which becomes the gastric cavity.

While the alimentary canal is becoming formed a series of important
changes takes place in other parts of the embryo. The rows of locomotive
paddles first appear as four longitudinal equidistant linear thickenings of the
epiblast near the aboral pole (fig. 83 D). On the projecting surface of these
ridges stiff cilia appear which coalesce together to form the paddles. While
the embryo is still within the egg the rows of paddles are quite short and
also double. There are in Pleurobrachia about eight or nine pairs of paddles
in each row. Each double row eventually separates into two.

In all the forms except the Eurostomata (Beroe) two tentacles grow out as
thickenings of the epiblast (fig. 84 B, t.). They are placed at the opposite
poles of the long transverse axis of the embryo.
A process of the contractile gelatinous tissue of the body, the origin of
which is described below, makes its way, according to Kowalevsky, into the
tentacles.
The central apparatus of the nervous system and the otoliths are formed at
the aboral pole from a thickening of the epiblast, but the full details of their
formation have not been elucidated. It may be well to preface my account
of their development with a short statement of their adult structure.
They consist in the adult of a vesicle with a ciliated lining situated at the bifurcation of the two anal
tubes, and of certain structures connected with this vesicle. From the floor of the vesicle is suspended
a mass of otoliths by four leaf-like bodies known as suspenders. The roof is very delicate and has the
form of a four-sided pyramid. Six openings lead into the vesicle. Through four of these, placed at the
four corners, there pass out four ciliated grooves continuous with the suspenders. These grooves,
after leaving the otolithic vesicle, bifurcate and pass to the eight rows of paddles. At the two sides the
walls of the vesicle are continuous with two thickened ciliated plates with swollen edges, opposite
the centres of which are two lateral openings into the vesicle, completing the six openings. Through
the lateral openings the sea-water is driven by the action of the cilia of the plates.

The development of these parts is as follows—In the aboral thickening of
epiblast a cavity makes its appearance, the walls of which constitute the
rudiment of the otolithic vesicle (fig. 83 B and C, s.c.). The roof of the
cavity is extremely delicate. On each side of it a thickening of cells
becomes established, regarded by Kowalevsky as the rudiment of the
nervous ganglia. These thickenings appear to give origin to the lateral
ciliated plates. The otoliths arise from cells at four separate points at the
corners of the ciliated plates opposite the rows of paddles (fig. 84 A, ot.).

Fig. 84. Two stages in the development of Pleurobrachia rhododactyla. (After Agassiz.)
ot. otolith; t. tentacle.

In Pleurobrachia there is at first only one otolith at each corner. The otoliths
are gradually transported towards the centre of the vesicle (fig. 84 B, ot.)
and are there attached, though the four leaf-like suspenders do not arise till
very late. The otoliths go on increasing in number throughout life.
The gelatinous tissue of the Ctenophora appears as a homogeneous layer
between the epiblast and the yolk cells, and is probably homologous with
the layer formed in the same situation in all other cœlenterate forms. Into
the layer a number of anastomosing cells, mainly derived from the epiblast,
though according to Chun (No. 174) also in part from the hypoblast, make
their way. These cells would appear to be mainly, if not entirely (Chun), of
a contractile nature. It is probable that the great mass of the gelatinous
tissue of the adult is an intercellular substance derived from these cells.
The whole of the above changes are completed while the embryo is still
enclosed in the egg-capsule. During their accomplishment the oro-anal axis,
which was originally very short, increases greatly in length (fig. 83), so that
the embryo acquires an oval form similar to that of the adult.
The exact period of leaving the egg does not appear to be very constant but the hatching never takes
place till the embryo has practically acquired all the organs of the adult.
In the majority of types the differences between the just hatched larva and the adult are
inconsiderable, and in all cases the larva has a somewhat oval form. In the case of the Tæniatæ
(Cestum, etc.), the larva has the characteristic oval form, and the subsequent changes amount almost
to a metamorphosis.
The larva of the Lobatæ, such as Eucharis, Bolina, etc., can hardly be distinguished from
Pleurobrachia, and undergoes therefore considerable changes after hatching.
Eucharis multicornis while still in the larval condition is stated by Chun to become sexually mature.

The new genus Ctenaria recently described by Haeckel, which is
intermediate between the Ctenophora and the Medusæ clearly proves that
the Ctenophora are more closely related to the Medusæ than to the
Actinozoa but their development, especially the presence of a stomodæum,
shews that they have affinities (in spite of the rudimentary velum of
Ctenaria) with the Acraspedote as well as with the Craspedote Medusæ; and

it may be noted that the Acraspeda have undoubted affinities with the
Actinozoa.

Summary and general considerations.
Even in the adult condition the lower forms of Cœlenterata do not rise in
complexity much beyond a typical gastrula. Ontogeny nevertheless brings
clearly to light the existence of a larval form—the planula—which recurs
with fair constancy amongst all the groups except the Ctenophora.
We are probably justified in assuming that the planula is a repetition of a
free ancestral form of the Cœlenterata. The planula, as it most frequently
occurs, is a two-layered ciliated nearly cylindrical organism, with at most a
rudimentary digestive cavity hollowed out in the inner layer, and as a rule
no mouth. In the outer layer are numerous thread-cells.
How many of these characters did the ancestral planula possess? I think it is not unreasonable to
assume that the only two characters about which there can be much doubt are the rudimentary
condition of the digestive cavity and the absence of a mouth. Paradoxical as it may seem, it appears
to me not impossible that the Cœlenterata may have had an ancestor in which a digestive tract was
physiologically replaced by a solid mass of amœboid cells. This ancestor was perhaps common to the
Turbellarians also. The constant presence of thread-cells in the inner layer of their epiblast fits in with
their derivation from a form similar to the planula. While the solid parenchymatous digestive canal of
Convoluta and Schizoprora and other forms amongst the Turbellarians, though very probably
secondary, may perhaps be explained by such a view of their origin.
The planula in its primitive condition is not bilaterally symmetrical, but frequently, as amongst the
Actinozoa, it becomes flattened on two sides before undergoing its conversion into the adult form.
Perhaps the bilateral form of planula is the starting point both for the Cœlenterata and the Turbellaria.
In this connection the peculiar unilateral development of a tentacle in Scyphistoma and Actinia
should be noted.

The planula occurs in the majority of sessile forms of Hydrozoa except the
Tubularidæ and Hydra. It is also characteristic of the Trachymedusæ and
Siphonophora. Amongst the Acraspeda it is also present, but has an
exceptional mode of ontogeny which is discussed in connection with the
germinal layers.
It is characteristic both of the Octocoralla and Hexacoralla, but is not found
in the Ctenophora.
In the Tubularidæ and in Hydra an abbreviated development leads no doubt
to the absence of a free planula stage, and the absence of a larval form

amongst the Ctenophora may, as has already been stated, be probably
explained in the same way.
The Cœlenterata of all the Metazoa are characterized by the greatest
simplicity in the arrangement of their germinal layers; and for this reason
very considerable interest attaches to the mode of formation of the layers
amongst them. Two germinal layers are constantly found, which correspond
in a general way to the epiblast and hypoblast. It might have been
anticipated that a certain amount of uniformity would have existed in the
mode of formation of the layers. This however is not the case. In perhaps
the majority of forms they become differentiated by a process of
delamination, but in a not inconsiderable minority the two layers owe their
origin to an invagination.
Delamination is constant (with the doubtful exception of some Tubularidæ)
amongst the Hydromedusæ and Siphonophora. It is perhaps in the main
characteristic of the Actinozoa.
Invagination by embole takes place, so far as is known, constantly amongst
the Acraspeda and frequently amongst the Actinozoa; and an epibolic
invagination is characteristic of the Ctenophora.
If confidence is to be placed in the recorded observations on which this
summary is founded, and there is no reason why in a general way it should
not be so placed, the conclusion is inevitable that of the above modes of
development the one must be primitive and the other a derivative from it,
for, if this conclusion be not accepted, the absolutely inadmissible
hypothesis of a double origin for the Cœlenterata would have to be adopted.
Two questions arise from these considerations:—
(1) Which is the primitive, delamination or invagination?
(2) How is the one of these to be derived from the other?
There is a great deal to be said in favour of both delamination and
invagination; but it will be convenient to defer all discussion of the question
to the general chapter on the formation of the layers throughout the animal
kingdom.
The hypoblast cells are often filled with yolk material, and secondary
modifications are thus produced in the development. The most important

examples of such modifications are found in the Siphonophora and
Ctenophora.
In the simplest forms amongst the Hydrozoa there is no trace of a third
layer or mesoblast. The epiblast is typically formed, as was first shewn by
Kleinenberg, of an epithelial layer and a subepithelial interstitial layer of
cells. The cells of the former are frequently produced into muscular or
nervous tails, and those of the latter give rise to the thread-cells and
generative organs and in some cases to muscles[85]. In many cases, amongst
all the Cœlenterate groups, and constantly amongst the Ctenophora the
epiblast is simplified and reduced to a single layer. The hypoblast undergoes
in most cases no such differentiation but simply forms a glandular layer
lining the gastric chamber and its prolongations into the tentacles; but in the
Actinozoa it appears to give rise to muscles, and strong evidence has been
brought forward to shew that in some groups it gives rise to the generative
organs.
Between the epiblast and hypoblast a structureless lamella appears always
to be interposed.
In many Cœlenterata further differentiations of the epiblast are present. In
many forms the layer gives rise to a hard external skeleton. This is most
widely spread amongst the Hydrozoa, where in the majority of cases it takes
the form of the horny perisarc, and in the Hydrocoralla (Millepora and
Stylasteridæ) of a hard calcareous skeleton. The skeleton in these forms,
though closely resembling the mesoblastic skeleton of the Actinozoa, has
been shewn by Moseley (164) to be epiblastic.
In the Actinozoa an epiblastic skeleton is exceptional, and according to
most authorities absent. Quite recently however Koch (167) has found that
the axial branched skeleton of most of the Gorgonidæ, viz. the Gorgoninæ
and Isidinæ, is separated from the cœnosarc by an epithelium, which he
believes to be epiblastic, and to which no doubt the axial skeleton owes its
origin. A similar epithelium surrounds the axis of the Pennatulidæ.
In the Medusæ the epiblast also gives rise to a central nervous system,
which however continues to form a constituent part of the layer, and to the
organs of special sense[86].

A special differentiation of the hypoblast is found in the solid axis of the
tentacles. This axis replaces the gastric prolongation found in many forms,
and the cells composing it differentiate themselves into a chorda-like tissue,
which has a skeletal function, and is no longer connected with nutrition.
This axis is placed by many morphologists amongst the mesoblastic
structures.
In all the higher Cœlenterata certain tissues become interposed between the
epiblast and hypoblast, which may be classified together as the mesoblast.
The most important of these are:
(1) The various distinct muscular layers.
(2) The gelatinous tissue of the Medusæ and Ctenophora.
(3) The skeletogenous tissue of the Actinozoa.
In most cases the muscular fibres are connected with epithelial cells, but in
certain forms amongst the Medusæ and in the majority if not all the
Actinozoa they constitute a distinct layer, sometimes separated from the
epiblast by a structureless membrane, Æquorea Mitrocoma. Such layers
when on the outer side of the membrane separating epiblast and hypoblast
are undoubtedly epiblastic in origin, but in some cases amongst the
Actinozoa they adjoin the hypoblast, and are very probably derived from
this layer.
The origin of the gelatinous tissue is still involved in much obscurity.
It originates as a homogeneous layer between epiblast and hypoblast, which
in the Hydromedusæ never becomes cellular though traversed by elastic
fibres.
In the Acraspeda it contains anastomosing cells in the main apparently
(Claus) derived from the hypoblast, and in the Ctenophora it is richly
supplied with muscular stellate cells for the most part of epiblastic origin,
though some are stated by Chun to come from the hypoblast. On the whole
it seems probable, that the gelatinous tissue may be regarded as a product of
both layers; and there are some grounds for thinking that it is an immense
development of the membrane always interposed between the two primary
layers. It must however be borne in mind that a membrane, regarded by the
Hertwigs as the equivalent of the ordinary membrane between the epiblast

and hypoblast, can be usually demonstrated on both surfaces of the
gelatinous tissues in Medusæ. The skeletogenous layer of the Actinozoa is
probably the morphological homologue of the gelatinous tissue; but the
evidence we have is on the whole in favour of the connective-tissue cells it
contains being epiblastic in origin. It gives rise to the skeleton of the
Hexacoralla, to the spicular skeleton of Alcyonium, the axial skeleton of
Corallium, and the skeleton of the Helioporidæ and Tubiporidæ.

Alternations of generations.
Alternation of generations is of common occurrence amongst the Hydrozoa,
and something analogous to it has been found to take place in Fungia
amongst the Actinozoa. It is not known to occur in the Ctenophora.
The chief interest of its occurrence amongst the Hydromedusæ and
Siphonophora is the fact that its origin can be traced to a division of labour
in the colonial systems of zooids so characteristic of these types.
In the Hydromedusæ an interesting series of relations between alternation
of generations and the division of the zooids into gonophores and
trophosomes can be made out. In Hydra the generative and nutritive
functions are united in the same individual. The generative swellings in
these forms cannot, as has been ably argued by Kleinenberg, be regarded as
rudimentary gonophores, but are to be compared to the generative bands
developed in the Medusæ around parts of the gastro-vascular system. A
condition like that of Hydra, in which the ovum directly gives rise to a form
like its parent, is no doubt the primitive one, though it is not so certain that
Hydra itself is a primitive form. The relation of Hydra to the Tubularidæ
and Campanularidæ may best be conceived by supposing that in Hydra
most ordinary buds did not become detached, so that a compound Hydra
became formed; but that at certain periods particular buds retained their
primitive capacity of becoming detached and subsequently developed
generative organs, while the ordinary buds lost their generative function.
It would obviously be advantageous for the species that the detached buds
with generative organs should be locomotive, so as to distribute the species
as widely as possible, and such buds in connection with their free existence
would naturally acquire a higher organization than the attached

trophosomes. It is easy to see how, by a series of steps such as I have
sketched out, a division of labour might take place, and it is obvious that the
embryos produced by the highly organized gonophores would give rise to a
fixed form from which the fixed colony would be budded. Thus an
alternation of generations would be established as a necessary sequel to
such a division of labour. To test the above explanation it is necessary to
review the main facts with reference to alternations of generations amongst
the Hydromedusæ.
Hydromedusæ[87]. In many instances amongst the Tubularidæ, Sertularidæ
and Campanularidæ medusiform buds are produced which become
detached and develop sexual organs.
Such Medusæ are divided into two great groups, the Ocellata and Vesiculata, according to the
characters of the marginal sense organs. In the Ocellata the sense organs have the form of eyes, and
in the Vesiculata of auditory vesicles. The latter seem to be usually budded off from the
Campanularia stocks, and the generative organs extend in folded bands over the radial canals. These
bands have been regarded by Allman as composed of rudimentary gonophores, and he called the
Medusæ which give rise to them blastochemes. He regards them as representing a more complicated
type of alternation of generations with three instead of two generations in the series. The Hertwigs
have brought what appear to me conclusive grounds for rejecting this view, and have demonstrated
that the generative organs of these types resemble those of ordinary Medusæ.
In many forms the medusiform buds though fully developed do not become detached; whether
detached or not they are known as phanerocodonic gonophores. In other forms again buds which
begin as if they were going to form Medusæ never reach that condition but remain permanently in an
undeveloped state. They have been called by Allman adelocodonic gonophores.

In all the above cases two generations at the least interpose between the
successive sexual periods, viz.:—
(1) A trophosome produced directly from the ovum.
(2) A gonophore budded from this.
In a very large number of types the gonophores do not develop directly on
the hydroid stem, but arise on specially modified zooids resembling
rudimentary trophosomes which have been named blastostyles by Allman.
On the sides of each blastostyle a series of gonophores usually becomes
developed. The blastostyles either remain exposed as in all the
Gymnoblastic or Tubularian Hydroids, or as in all the Calyptoblastic
Hydroids (Sertularidæ and Campanularidæ) they become invested by a
special case—known as the gonangium—which is formed of perisarc lined
by epiblast. In the forms with blastostyles three generations interpose

between the successive stages of sexual reproduction, (1) the trophosome
developed directly from the ovum, (2) the blastostyle budded from this, (3)
the gonophore budded from the blastostyle.
Such being the main facts, in order to prove that the existing condition of polymorphism amongst the
Hydromedusæ is to be explained as hypothetically suggested above, it is still necessary to shew that
(1) the free medusiform gonophores are really only modified trophosomes, or rather that the
trophosomes and gonophores are both modifications of some common type, and (2) that the fixed so-
called adelocodonic gonophores are retrograde derivatives of the free medusiform gonophores.
Unless these points can be established it might be maintained that the Medusæ were special zooids,
developed de novo and not by a modification of trophosome zooids. To demonstrate these
propositions at length would carry me too far into the region of simple Comparative Anatomy, and I
content myself with referring the reader to a discussion of the Hertwigs (No. 146, p. 62) where the
first point appears to me fully established. With reference to the second point I will only say that the
structure and development of the adelocodonic gonophores can only be explained on the assumption
that they are retrograde forms of the phanerocodonic gonophores, and that the opposite view, that the
phanerocodonic gonophores are derived from the adelocodonic, leads to a series of untenable
positions.
The Trachymedusæ, as has been shewn above, develop directly. They are probably derived from
gonophores in which the trophosome has disappeared from the developmental cycle.

To sum up, three types of development are found amongst the
Hydromedusæ.
(1) No alternations of generations. Permanent form, a sexual trophosome.
Ex. Hydra.
(2) Alternations of generations. Trophosome fixed, gonophore free or
attached. Ex. Gymnoblastic and Calyptoblastic Hydroids, and Hydrocoralla.
(3) No alternations of generations. Permanent form, a sexual Medusa. Ex.
Trachymedusæ.
Siphonophora. In the Siphonophora alternations of generations take place
in the same way as in the Hydromedusæ, but the starting point appears to be
a Medusa. The gonophores may remain fixed or become detached.
Acraspeda. With the exception of Pelagia and Lucernaria, in which the
development involves a simple metamorphosis, all the Acraspeda undergo a
form of alternations of generations. The ovum, as already described,
develops into a fixed form—the Scyphistoma—which increases asexually
by normal budding, and can even form a permanent colony.

Fig. 85. Three stages in the alternations of generations of Aurelia aurita. (From
Gegenbaur.)
A. Polype stage.
B. Commencing strobilization.
C. Completed strobilization.

The formation of the sexual Medusa form takes place by a kind of
strobilization of the body of the fixed Scyphistoma. A series of transverse
constrictions becomes formed round the body below the mouth, dividing it
up into corresponding rings, each of which eventually gives rise to a
Medusa known as an Ephyra (fig. 85). In each of these rings is a dilation of
the stomach, and a section of each of the four rudimentary mesenteries
described in connection with the development of the Scyphistoma. As the
constrictions become deeper the segments of the body between them
become disc-like, and their edges are produced into eight lobes containing
prolongations of the gastric cavity (fig. 85 C). The lower surface of each
disc, which forms the future aboral surface of the Medusa, becomes convex,
in part owing to the development of gelatinous tissue. On the opposite
surface a muscular layer becomes developed. During the above process the
body of the Scyphistoma gradually grows in length and continues to be
segmented, so that a series of Ephyræ are uninterruptedly formed, of which
those near the base are the youngest. The original terminal ring of tentacles
of the Scyphistoma gradually atrophies.

In the further development of the Ephyræ each of their eight lobes becomes
bifid at its extremity.
As the Ephyræ successively reach this condition they become detached, and
by a series of remarkable changes, amounting almost to a metamorphosis,
and accompanied by an enormous growth in size, reach the adult condition.
The alternation of generations in the Acraspeda cannot be quite so simply
explained as in the Hydromedusæ, though the principle is probably the
same in the two cases.
Actinozoa. Amongst the Actinozoa there occurs in Fungia a peculiar
process which is, as shewn by Semper (171), in many ways analogous to
alternations of generations[88]. From the larva a nurse-stock is developed, at
the end of which a cup-like coral resembling the adult is formed as a bud.
The bud becomes detached and then gives rise to a permanent sexual
Fungia. From the nurse-stock there is formed however a fresh bud at the
centre of the scar left on the detachment of the old one. The fresh bud
eventually becomes separated from the nurse-stock leaving a small portion
of its stem behind; each succeeding bud similarly leaves a small portion of
its stem, so that the nurse-stock eventually acquires a jointed appearance. In
the above process we clearly have, as in the Hydromedusæ, a non-sexual
form—the nurse-stock—produced directly from the larva, giving rise by
budding to a sexual form; all the conditions of an alternation of generations
are therefore fulfilled. It seems however possible that the nurse-stock itself
may eventually become sexual.

Bibliography.
Cœlenterata. General.
(145) Alex. Agassiz. Illustrated Catalogue of the Museum of Comparative Anatomy at Harvard
College, No. II. American Acalephæ. Cambridge, U. S., 1865.
(146) O. and R. Hertwig. Der Organismus d. Medusæ u. seine Stellung z. Keimblättertheorie. Jena,
1878.
(147) A. Kowalevsky. “Untersuchungen üb. d. Entwicklung d. Cœlenteraten.” Nachrichten d. kaiser.
Gesell. d. Freunde d. Naturer kenntniss d. Anthropologie u. Ethnographie. Moskau, 1873. (Russian.)
For abstract vide Jahresberichte d. Anat. u. Phys. (Hoffman u. Schwalbe), 1873.

Hydrozoa.

(148) L. Agassiz. Contributions to the Natural History of the United States of America. Boston,
1862. Vol. IV.
(149) G. J. Allman. A Monograph of the Gymnoblastic or Tubularian Hydroids. Ray Society,
1871‑2.
(150) G. J. Allman. “On the structure and development of Myriothela.” Phil. Trans., Vol. CLXV. p. 2.
(151) P. J. van Beneden. “Mém. sur les Campanulaires de la Côte d’Ostende considérés sous le
rapport physiologique, embryogénique, et zoologique.” Nouv. Mém. de l’Acad. de Brux., Tom. XVII.
1844.
(152) P. J. van Beneden. “Recherches sur l’Embryogénie des Tubulaires et l’histoire naturelle des
différents genres de cette famille qui habitent la Côte d’Ostende.” Nouv. Mém. de l’Acad. de Brux.,
Tom. XVII. 1844.
(153) C. Claus. “Polypen u. Quallen d. Adria.” Denk. d. math.-naturwiss. Classe d. k. k. Akad. d.
Wiss. Wien, Vol. XXXVIII. 1877.
(154) J. G. Dalyell. Rare and Remarkable Animals of Scotland. London, 1847.
(155) H. Fol. “Die erste Entwicklung d. Geryonideneies.” Jenaische Zeitschrift, Vol. VII. 1873.
(156) Carl Gegenbaur. Zur Lehre vom Generationswechsel und der Fortpflanzung bei Medusen und
Polypen. Würzburg, 1854.
(157) Thomas Hincks. “On the development of the Hydroid Polypes, Clavatella and Stauridia; with
remarks on the relation between the Polype and the Medusoid, and between the Polype and the
Medusa.” Brit. Assoc. Rep., 1861.
(158) E. Haeckel. Zur Entwicklungsgeschichte d. Siphonophoren. Utrecht, 1869.
(159) Th. H. Huxley. Oceanic Hydrozoa. Ray Society, 1858.
(160) Geo. Johnston. A History of British Zoophytes. Edin. 1838. 2nd Edition, 1847.
(161) N. Kleinenberg. Hydra, eine anatomisch-entwicklungsgeschichtliche Untersuchung. Leipzig,
1872.
(162) El. Metschnikoff. “Ueber die Entwicklung einiger Cœlenteraten.” Bull. de l’Acad. de St
Pétersbourg, XV. 1870.
(163) El. Metschnikoff. “Studien über Entwicklungsgeschichte d. Medusen u. Siphonophoren.” Zeit.
f. wiss. Zool., Bd. XXIV. 1874.
(164) H. N. Moseley. “On the structure of the Stylasteridæ.” Phil. Trans. 1878.
(165) F. E. Schulze. Ueber den Bau und die Entwicklung von Cordylophora lacustris. Leipzig, 1871.

Actinozoa.
(166) Al. Agassiz. “Arachnitis (Edwarsia) brachiolata.” Proc. Boston Nat. Hist. Society, 1860.
(167) Koch. “Das Skelet d. Alcyonarien.” Morpholog. Jahrbuch, Bd. IV. 1878.
(168) A. Kowalevsky. “Z. Entwicklung d. Alcyoniden, Sympodium coralloides und Clavularia
crassa.” Zoologischer Anzeiger, No. 38, 1879.
(169) H. Lacaze Duthiers. Histoire nat. du Corail. Paris, 1864.
(170) H. Lacaze Duthiers. “Développement des Coralliaires.” Archives de Zoologie expérimentale
et générale, Vol. I. 1872 and Vol. II. 1873.
(171) C. Semper. “Ueber Generationswechsel bei Steinkorallen etc.” Zeit. f. wiss. Zool., Bd. XXII.
1872.

Ctenophora.
(172) Alex. Agassiz. “Embryology of the Ctenophoræ.” Mem. of the Amer. Acad. of Arts and
Sciences, Vol. X. No. III. 1874.
(173) G. J. Allman. “Contributions to our knowledge of the structure and development of the
Beroidæ.” Proc. Roy. Soc. Edinburgh, Vol. IV. 1862.

(174) C. Chun. “Das Nervensystem u. die Musculatur d. Rippenquallen.” Abhand. d. Senkenberg.
Gesellsch., B. XI. 1879.
(175) C. Claus. “Bemerkungen u. Ctenophoren u. Medusen.” Zeit. f. wiss. Zool., XIV. 1864.
(176) H. Fol. Ein Beitrag z. Anat. u. Entwickl. einiger Rippenquallen. 1869.
(177) C. Gegenbaur. “Studien ü. Organis. u. System d. Ctenophoren.” Archiv. f. Naturgesch., XXII.
1856.
(178) A. Kowalevsky. “Entwicklungsgeschichte d. Rippenquallen.” Mém. Acad. St Pétersbourg, VII.
série, Tom. X. No. 4. 1866.
(179) J. Price. “Embryology of Ciliogrades.” Proceed. of British Assoc., 1846.
(180) C. Semper. “Entwicklung d. Eucharis multicornis.” Zeit. f. wiss. Zool., Vol. IX. 1858.

[72]
I. HYDROZOA.
1. Hydromedusæ.
Hydroidea.
Trachymedusæ.
2. Siphonophora.
Calycophoridæ.
Physophoridæ.
3. Acraspeda.
II. ACTINOZOA.
1. Alcyonaria.
(Octocoralla.)
2. Zoantharia.
(Hexacoralla.)
III. CTENOPHORA.
[73] For a detailed description of the development of a single species the reader
referred to Allman’s description of Laomedia flexuosa, No. 149, p. 85 et seq.
[74] Vide Ciamician, Zeit. f. wiss. Zool., Bd. XXXII. 1879.

[75] In examining the segmentation by means of sections I have failed to detect an
epibolic gastrula or such irregularity as is described by Ciamician. Prof.
Kleinenberg informs me that he has been equally unsuccessful.
[76] These cells are the so-called nerve-muscle cells. Their nature is discussed in the
second part of this work.
[77] In the succeeding account I have followed Fol, who differs in some minor
points from Metschnikoff.
[78] In my description of the development of the Siphonophora I employ Huxley’s
terminology.
[79] From the expressions used by Huxley, Anatomy of Invertebrated Animals, p.
149, it appears to me possible that his opposition to Leuckart’s view is mainly as to
the nature of the individual.

[80] I use this term for the group, often known as the Discophora, which includes the
Pelagidæ, Rhizostomidæ, and Lucernaridæ.
[81] The German abstract is very obscure as to the formation of the mouth.

[82] I have this on the authority of Kleinenberg. The existence of an unequal
segmentation probably indicates an epibolic gastrula.
[83] “Ueb. einige tropische Larven-formen.” Zeit. f. wiss. Zool., vol. XVII. 1867.

[84] Chun (No. 174) gives a short statement of his observations, which accords with
the interpretation in the text.
[85] The questions relating to the generative organs of the Cœlenterata are dealt with
in the second part of this work.
[86] The differentiation of the nervous and muscular systems in the Hydrozoa is
treated of in the second part of this work.
[87] For a full account of this subject the reader is referred to the beautiful memoir
of Allman (No. 149).
[88] Vide also Moseley. Notes by a Naturalist of the Challenger, pp. 524 and 525.

CHAPTER VII.

PLATYELMINTHES[89].

Turbellaria.
Although there is perhaps no group in the animal kingdom the ontogeny of
which would better repay a thorough investigation than the Turbellarians,
yet the difficulties to be overcome have hitherto proved too great.
The fresh-water Rhabdocœla and Dendrocœla do not undergo any
metamorphosis, and leave the ovum in a condition in which they cannot
easily be distinguished in their general appearance from Infusoria. Many
marine Dendrocœla also develop directly, while, as was first shewn by Joh.
Müller, other marine Dendrocœla undergo a more or less complicated
metamorphosis.
Marine Dendrocœla. Of the marine Dendrocœla which do not undergo a
metamorphosis the form most fully worked out is Leptoplana tremellaris—
(vide Keferstein, No. 187, and Hallez, No. 185).
The ova are surrounded by large albuminous capsules secreted by a special
gland. They are laid a great number at a time, and adhere together so as to
form masses not unlike the spawn of nudibranchiate Molluscs.
Within the egg-capsule the ovum floats freely and undergoes a
segmentation similar in many respects to the characteristic molluscan type.
The ovum divides into two, and then into four parts, from each of which a
small segment is then separated off. The four small segments, which appear
to give rise to the epiblast, increase in number by division and gradually
envelop the large segments[90]; so that an epibolic invagination clearly takes
place. Between the small and the large cells is a small segmentation cavity,
fig. 86 A and B. At the time when twelve epiblast cells are present, each of
the four large cells divides into two unequal parts (Hallez), fig. 86 A. In this
way four large (hy) and four small cells (m) are formed. The latter are
placed at the opposite pole of the ovum to the epiblast cells, and give rise to
the mesoblast, while the four large cells remain as the hypoblast.

Fig. 86. Sections through the ovum of Leptoplana tremellaris in three stages of
development.
(After Hallez.)
ep. epiblast; m. mesoblast; hy. yolk cells (hypoblast); bl. blastopore.

In the course of the enclosure of the hypoblast cells by the epiblast, the
mesoblast cells gradually travel towards the formative pole (fig. 86 B). In
the process they become first of all divided so as to form four linear streaks,
and finally unite into a continuous layer between the epiblast and hypoblast,
which obliterates the segmentation cavity (fig. 86 C, m).
Before the completion of the epibole a closely packed layer of fine cilia
appears, which causes a rotation of the embryo within the egg-capsule.
During the above changes a fifth hypoblast cell is formed by the division of
one of those already present; and at a later period four of the hypoblast cells
give rise within the nearly closed blastoporic area to four small cells. In
connection with these cells a complete hyploblastic wall becomes
subsequently established, which encloses the original large hypoblast cells.
The latter then become resolved into a vitelline mass.
From a comparison with other types it may be regarded as probable that the
enteric wall originates by a process of continuous budding off of small cells
from the large cells, which commences with the formation of the four cells
above mentioned.
The blastopore becomes nearly obliterated, but whether it gives rise to the
mouth, which is formed in the same place, has not been determined. In front
of the mouth a small and very transitory rudiment of an upper lip makes its
appearance. The protrusible pharynx is stated by Hallez to arise as an

hypoblastic bud, while its sheath has an epiblastic origin. Two pairs of eyes
and the supra-œsophageal ganglia also become early developed.
The peripheral ciliated layer of small cells becomes divided into two strata,
of which the outer remains ciliated and forms the true epiblast: the inner
probably forms the cutis. In it are developed rod-like bodies, which seem to
be homologous with the thread-cells of the Cœlenterata, so that if the views
put forward in the previous chapter as to the similarity of the turbellarian
and cœlenterate larvæ are correct, the cutis corresponds with the deeper
layer of the cœlenterate epiblast. The mesoblast, like the epiblast, becomes
divided into two strata. The outer one is stated to form the circular and
longitudinal muscles; the inner one to give rise to a muscular reticulum, the
spaces within which constitute the parenchymatous body cavity.
The later changes are not of great importance. At a period slightly after the formation of the mouth
and ganglia two pairs of stiff hairs become formed at the sides of the body. The embryo has by this
time grown so as to fill up its capsule, in which however it continues rapidly to rotate, and also
commences to exhibit active contractions. It next becomes hatched, and passes from a spherical to a
flattened elongated form. The ventral oral opening is at first central, but soon, by a process of
unequal growth, becomes carried towards the posterior end of the body. The pairs of stiff hairs in the
meantime considerably increase in number. The remains of the yolk cells now disappear, and the
enteric walls become more distinct. The alimentary canal, which is at first simple in outline like that
of a rhabdocœlous Turbellarian, soon assumes a dendritic form. The young animal after these
changes resembles its parent, except in the possession of only two pairs of eyes and in the absence of
generative organs.

Of the types with a complete metamorphosis the free larvæ of various
species of Thysanozoon have been observed by Joh. Müller (190) and
Moseley (189), and the complete development of Eurylepta auriculata has
been studied by Hallez.

Fig. 87. Larva of Eurylepta auriculata immediately after hatching. Viewed from the
side. (After Hallez.)

m. mouth.

The stages within the egg of this latter type agree precisely with those
already described in Leptoplana. After the formation of the mouth the body
elongates, remaining however cylindrical. A fold forms on the anterior side
of the mouth, giving rise to a large upper lip. Two posterior processes are
next formed, and other processes soon arise, constituting the whole of those
found in the free larva. The embryo next shakes off its egg membranes by a
series of vigorous contractions. When free it has the form represented in the
annexed figure (fig. 87).
It is so similar to Müller’s (fig. 88) and Moseley’s larvæ that all three may
be dealt with together.
The body is somewhat oval, and slightly pointed behind. At the anterior end
are placed the eyes, two in the youngest larva of Müller, and twelve in the
older larva (fig. 88), and in the middle of the ventral surface is the mouth. It
is surrounded by a strong fold, and leads into an alimentary canal, which is
at first simple, but in the older larvæ is much branched. A bilobed ganglion

connected with two nerve cords is placed anteriorly. The superficial
epithelium is ciliated, and below it is a layer of cells (cutis) derived from
the primitive epiblast, in which are formed the usual rods (Hallez). The
chief peculiarity of the larva consists in the presence of elongated processes
covered with long cilia, and so connected together by a ciliated band that
the whole together forms, in Müller’s larva at any rate, a lobed præoral
ciliated band (fig. 88). This band is not quite so clear in Hallez’ figures.
Müller’s youngest larva was provided with eight very long lobes; three
were dorsal, viz. a median anterior, and two lateral placed far back; three
ventral, viz. a median in the front of the mouth forming a large upper lip,
and two processes at the sides of the mouth. The number was completed by
two lateral processes of the body. All the processes except the dorsal
median one are shewn in fig. 88. In Hallez’ larva, fig. 87, the six posterior
processes form a rather definite ring, while one flagellum projects from the
front end of the body immediately below the eyes, and a second flagellum
behind. In Moseley’s youngest larva six processes only were present,
though subsequently eight became formed as in Müller’s larvæ.

Fig. 88. Müller’s Turbellarian larva (probably thysanozoon). Viewed from the
ventral surface. (After Müller.)

The ciliated band is represented by the black line.

m. mouth; u.l. upper lip.

The metamorphosis consists in the whole animal growing longer and flatter,
and in the arms becoming gradually shorter and shorter till they finally
disappear altogether, and the larva acquires the ordinary adult form.
The lobed larval form of the Turbellaria has some points of resemblance to
the Pilidium form of nemertine larva described below, yet its resemblance
to this interesting larva is less close than would appear to be the case with
certain turbellarian larval forms recently described by Götte and
Metschnikoff, which are in some respects intermediate in character between
the larva of Leptoplana and those just described.
The observations of Götte (No. 184) were made on Planaria Neapolitana and Thysanozoon Diesingi,
and those of Metschnikoff (No. 188) on Stylochopsis ponticus. The larvæ of all these forms undergo
more or less of a metamorphosis, but the accounts of their development are not easily reconciled.[91]
The early stages of Planaria are like those of Leptoplana, as described by Keferstein. Four large
hypoblast cells become surrounded by small epiblast cells, which commence to be formed on the
dorsal side. The hypoblast cells divide and arrange themselves in two bilaterally symmetrical rows. A
small blastopore is left by the small cells on the ventral surface, which communicates with an
otherwise closed and ciliated cavity which is formed between the two rows of hypoblast cells. The
blastopore would seem to remain permanently open, and to be placed at the base of a deep pit, lined
by epiblast cells, which constitutes the stomodæum.

Fig. 89. Planarian larva (probably Planaria angulata). (From Agassiz.)

Fig. 90. Planarian larva (probably Plamaria angulata). (From Agassiz.)

The embryo now becomes dorsally convex, while the ventral surface becomes marked with a median
furrow and grows out laterally into two lobes, and anteriorly into a ventrally-directed upper lip. The
whole surface becomes ciliated, and the cilia are especially prominent on the ventral processes and
the summit of the dorsal dome. A bunch of strong cilia becomes formed in front of the dome, and a
less marked bunch behind. The larva is now stated by Götte closely to resemble a Pilidium. It soon,
however, extends itself, and the two bunches of cilia become situated at the anterior and posterior
extremities of the body. The ventral processes become inconspicuous prominences of the side of the
body. Götte believes that the larva undergoes no further metamorphosis.
A type of Planarian larva (figs. 89 and 90)—possibly Plan. angulata, observed by Alex. Agassiz (No.
181),—is very different from any other so far described, and is remarkable for being divided into a
series of segments corresponding in number with the diverticula of the digestive cavity. In the
youngest specimen (fig. 89) the body was nearly cylindrical, and divided into eleven rings,
corresponding with as many digestive diverticula. Two eye-spots were present. In a later stage (fig.
90) the body was considerably flattened and had approached more to the planarian form.
If Agassiz’ interesting observations can be trusted we have in this larva indications of a distinct
segmentation, which are of some morphological importance, especially when taken in connection
with the traces of segmentation found amongst the Nemertines.
A further type, with an incomplete metamorphosis, has been observed by Girard (183). It is
remarkable for having an uniform segmentation, and for presenting a quiescent stage after passing
through a free larval condition with a large upper lip.

Fresh-water Dendrocœla. The development of the fresh-water Dendrocœla
has been especially investigated by Knappert (No. 186) and Metschnikoff
(No. 188).
The ova are very delicate minute naked cells, which to the number of 4‑6 or
more become enveloped in a capsule or cocoon together with a large mass
of yolk cells derived from the vitellarium. The yolk cells exhibit peristaltic
movements and send out amœboid processes. Each ovum when laid
becomes surrounded by an extremely delicate membrane, which disappears
during the course of development. The capsules consist of a spherical case
and a stalk. The latter is first emitted from the female opening as a thread-
like body. Its free end becomes attached, and then the remainder of the
capsule is ejected.
Impregnation takes place before the formation of the capsule. The segmentation is complete. The
ovum first divides into two segments. One of these next divides, forming three segments. There are
subsequently stages with four, eight, sixteen, and thirty-two segments.
Metschnikoff’s results on the stages subsequent to the segmentation are not in complete harmony
with those of Knappert; but no doubt represent an advance in our knowledge, and I shall follow them

here. His observations were made on Planaria polychroa.
In the earliest stage observed by him the segmentation was already far advanced, but no membrane
was present round the ovum. At a later stage the ovum becomes more or less bell-shaped or
hemispherical, and encloses within its concavity a mass of yolk elements. It is now formed of three
concentric layers. An outer layer of flattened cells—the epiblast, a middle layer of fused cells—the
mesoblast, and an inner solid mass of yolk cells—the hypoblast.
At the upper pole is formed the protrusible pharynx (cf. Knappert), which is provided with a
provisional musculature and a lumen. By its contractions it takes up the yolk elements which
surround the embryo, and the rapid growth of the embryo no doubt takes place at their expense. The
embryo gradually loses its hemispherical form, and assumes an elongated and flattened shape. It
acquires a coating of cilia by means of which it rotates. On the fifth day it is hatched.
The alimentary tract long remains solid, even after it has acquired its branched form. The pharynx
becomes withdrawn as soon as the larva is hatched. It loses its provisional muscles, and subsequently
acquires a permanent musculature. The young after hatching attach themselves to the body of their
parent, on which they feed (?).

Rhabdocœla. The development of some of the Rhabdocœla has recently
been studied by Hallez. The ova are mostly laid in capsules, one in each
capsule. Sometimes the development commences before the capsules are
laid, at other times not till afterwards. In certain forms (Mesostomum) there
are summer eggs with thin capsules which develop within the parent, while
hard capsules, forming what are known as winter eggs, are laid in the
autumn, and the embryo hatched in the spring.
The ova of the Rhabdocœla like those of the fresh-water Dendrocœla are enveloped in yolk elements
derived from the vitellarium.
The segmentation probably takes place in the same way as in Leptoplana. A stage with four equal
cells has been observed by Hallez, and there is subsequently an epibolic gastrula. The embryo
becomes ciliated while still within the capsule and, according to Hallez, the pharynx arises as a bud
of the hypoblast. The proboscis in Prostomum originates as an epiblastic invagination.

Nemertea.
Some Nemertea develop without and some with a metamorphosis.
The most remarkable type of Nemertine development with a metamorphosis
is that in which the ovum develops into a peculiar larval form known as
Pilidium, within which the perfect worm is subsequently evolved. Closely
allied to this type is one in which the sexual worm is developed within a
larval form as in Pilidium, but in which the larva has no free-swimming
stage, and is therefore without the characteristic appendages of the

Pilidium. This is known as the type of Desor and is confined (?) to the
genus Lineus. The Pilidium and the Desor type may be first considered
(vide Barrois, No. 192).
The type of Desor. The segmentation is regular and leads to the formation
of a blastosphere with a large segmentation cavity. The blastosphere is
converted by invagination into a gastrula (fig. 91 A). The blastopore is soon
carried relatively forwards by the elongation backwards of the archenteron,
and, according to Barrois, actually forms the mouth. Owing to the
elongation of the archenteric cavity the embryo assumes a bilateral form
(fig. 92 A) in which the dorsal and ventral surfaces can be distinguished, the
mouth (m.) being situated on the ventral surface.

Fig. 91. Three stages in the development of Lineus.
(After Barrois.)
A is a side view in optical section.
B and C are two later stages from the ventral (oral) surface.
ae. archenteron; sc. segmentation cavity; hy. hypoblast; me. mesoblast; ep. epiblast; m.
mouth; st. stomach; pr.d. prostomial disc; po.d. metastomial disc; pr. proboscis.

Fig. 92. Three Stages in the development of Lineus.
(After Barrois.)
A. Side view of an embryo at a very early stage as an opaque object.
B and C. Two late stages, seen as transparent objects from the ventral surface.
ae. archenteron; m. mouth; pr.d. prostomial disc; po.d. metastomial disc; cs. lateral pit
developing in B as a diverticulum from the œsophagus; pr. proboscis; ms. muscular layer (?); ls.
larval skin about to be thrown off; me. mesoblast; st. stomach.

Immediately after the completion of the gastrula a remarkable series of
phenomena takes place. The embryo when viewed from the ventral surface
assumes a pentagonal form (fig. 91 B), and four invaginations of the
epiblast make their appearance on the ventral surface (fig. 92 A), two in
front of (pr.d.) and two behind (po.d.) the mouth; they result in the
formation of four thickened discs. These discs soon become separated from
the external skin, which closes in forming an unbroken layer over them (fig.
91 C). The discs grow rapidly, and first the prostomial pair and
subsequently the metastomial fuse together, and finally the whole four unite
into a continuous ventral plate; analogous it would seem to the ventral plate
of chætopodan and arthropodan embryos. The plate so formed gradually

extends itself so as to close over the dorsal surface, and to form a complete
skin within the primitive larval skin, which at this period is richly ciliated,
though the embryo is not yet hatched (fig. 91 C). While these changes are
taking place, there are budded off from the invaginated discs a number of
fatty cells, which fill up the space between the discs and the archenteron,
and eventually form the mesoblastic reticulum. During this stage the
rudiment of the proboscis also makes its appearance as a solid process of
epiblast, which grows backwards from the point of fusion of the two
prostomial discs at the front end of the embryo (fig. 91 C, pr.). A lumen is
excavated in it at a later period. The lateral organs or cephalic pits arise in a
somewhat unexpected fashion as a pair of diverticula from the œsophagus
(fig. 92 B, cs.)[92], which soon fuse with the walls of the body at the junction
of the prostomial and metastomial plates (fig. 92 C, cs.), although they
remain for some time attached to the œsophagus by a solid cord.
During these changes the original larval skin separates itself from the
subjacent layer formed by the discs (fig. 92, B and C), and is soon thrown
off completely, leaving the already ciliated (fig. 92 C) external layer of the
invaginated discs as the external skin of the young Nemertine. During, and
subsequently to, the casting off of the embryonic skin, important changes
take place in the constitution of the various layers of the body, resulting in
the formation of the vascular system and other mesoblastic organs, the
nervous system, and the permanent alimentary tract. These changes appear
to me to stand in need of further elucidation; and the account below must be
received with a certain amount of caution.
It has been already stated that the two discs give rise to fatty cells, which occupy the space between
the walls of the body and the archenteron. At the period of the casting off of the embryonic skin fresh
changes take place. The discs become very much thickened, and then divide into two layers, which
become the epidermis and subjacent muscular layers. The muscular layers arise in two masses,
separated by the two cephalic sacks. The anterior mass is formed as an unpaired anterior thickening,
followed by two lateral thickenings. The posterior mass is much thinner, in correspondence with the
rapid elongation of the metastomial portion of the embryo.
The cells originally split off from the discs undergo considerable changes, some of them arrange
themselves around the proboscis as a definite membrane, which becomes the proboscidean sheath,
some also form a true splanchnic layer of mesoblast, and the remainder, which are especially
concentrated during early embryonic life in the anterior parts of the body, form the general interstitial
connective tissue. The cephalic ganglia are stated to become gradually differentiated in the
prostomial mesoblast, and the two cords connected with them in the metastomial mesoblast.
At the time when the larval skin is cast off the original mouth becomes closed, and it is not till some
time afterwards that a permanent mouth is formed in the same situation. During the early part of

embryonic life the intestine is lined with columnar cells, but, before the loss of the larval skin, the
walls of the intestine undergo a peculiar metamorphosis. Their cells either fuse or become
indistinguishable, and their protoplasm appears to become converted into yolk-spherules, which fill
up the whole space within the walls of the body, and are only prevented from extending forwards by
a membrane of connective tissue. This mass gradually forms itself into a distinct canal, lined by
columnar cells.

Pilidium. In the case of the true Pilidium type, the larva is hatched very
early and leads the usual existence of surface larvæ. A regular segmentation
is followed by an invagination which does not however cause the complete
obliteration of the segmentation cavity (fig. 93 A, a.e.).

Fig. 93. Two stages in the development of Pilidium.
(After Metschnikoff.)
ae. archenteron; œ. œsophagus; st. stomach; am. amnion; pr.d. prostomial disc; po.d.
metastomial disc; c.s. cephalic sack.

The primitive alimentary tract so formed becomes divided into œsophageal
and gastric regions (fig. 93 B, œ. and st.). Even while the invagination of
the archenteron is proceeding, the larva becomes ciliated throughout, and
assumes a somewhat conical form, the apex of the cone being opposite the
flat ventral surface on which the mouth is situated (fig. 93, A and B). From
the apex a flagellum projects in many forms, giving the larva a helmet-like

appearance. In other forms a bunch of long cilia takes the place of the
flagellum (fig. 94), and in others again the flagellum is not represented.
After the completion of the invagination a lobe grows out on each side of
the mouth, and less well-developed lobes may appear anteriorly and
posteriorly. Round the edge of the ventral surface a ciliated band makes its
appearance.
Two pairs of invaginations of the skin, just as in the type of Desor, now
make their appearance, one pair in front of and the other behind the mouth
(fig. 93 B, pr.d. and po.d.), and each of them by the closure of the opening
of invagination forms a sack, the outer wall of which becomes very thin and
the inner wall (corresponding with the whole invagination of the type of
Desor) very thick. The inner walls of the four thickenings, which I may
speak of as discs, now fuse together, each disc first uniting with its fellow,
and finally the two pairs uniting.

Fig. 94.
A. Pilidium with an advanced nemertine worm.
B. Ripe embryo of the Nemertea in the position it occupies in Pilidium. (Both after
Bütschli.)
œ. œsophagus; st. stomach; i. intestine; pr. proboscis; lp. lateral pit; an. amnion; n. nervous
system.

A ventral germinal plate is thus established, which gradually grows round
the intestine of the Pilidium to form the skin of the future Nemertine. The
outer thin layer of each of the discs grows pari passu with the inner layer,
and furnishes an amnion-like covering for the embryo which is forming
within the Pilidium (fig. 94, an).
In connection with the young vermiform Nemertine there is formed on each
side an outgrowth from the œsophagus (fig. 94) which is eventually placed
in communication with the exterior by a ciliated canal[93]. The proboscis
arises as an hollow invagination at the point where the two anterior discs
fuse in front.
When the young Nemertine has become pretty well formed within the
Pilidium it becomes ciliated, begins to move, and eventually frees itself and
leads an independent existence, leaving its amnion in the Pilidium which
continues to live for some time.
The central nervous system (fig. 94) is developed either before or after the
detachment of the young Nemertine, according to Metschnikoff as a
thickening of the epiblast. The young Nemertine is at first without an anus.
The development of the Nemertine within the Pilidium is clearly identical
with that of the Lineus embryo within the larval skin; the formation of an
amnion in the Pilidium constituting the only important difference which can
be pointed out between the modes of origin of the young Nemertine in the
two types.
So far as is known the forms which develop in a Pilidium, or according to
the type of Desor, all belong to the division of the Nemertines without
stylets in the proboscis, known as the Anopla.

Development without Metamorphosis. The majority of the Nemertea,
including the whole (?) of the Enopla, develop without a metamorphosis.
The observations which have been made on this type are not very
satisfactory, but appear to indicate that the formation of the hypoblast may
take place either by invagination or by delamination.
Invaginate types have been observed by Barrois (No. 192), Dieck (No. 196) and Hubrecht.
Barrois’ fullest observations were made on Amphiporus lactifloreus (one of the Enopla), and those of
Dieck on Cephalothrix galatheæ (one of the Anopla).
A regular segmentation is followed by a blastosphere stage with a small segmentation cavity. In
Barrois’ type the inner ends of the cells of the blastosphere are stated to fuse into a kind of
syncytium. A small invagination takes place, and the cells which take part in it separate from the
epiblast, and then fuse with the syncytium within the blastosphere. Dieck finds that in Cephalothrix
the invaginated mass simply vanishes.
Barrois’ statements about the fusion of the syncytium derived from the epiblast cells with the
invaginated cells must be regarded as very doubtful. The formation of the germinal layers takes
place, according to Barrois, by the separation of the internal mass of cells into mesoblast and
hypoblast. The proboscis is formed, according to this author, from the mesoblastic tissues. Dieck, on
the other hand, with greater probability, states that the proboscis is formed by an invagination. In
Cephalothrix a further point deserves notice, in that the whole of the primitive epiblast becomes shed.
In this fact there may perhaps be recognised the last trace of a metamorphosis like that in the type of
Desor.
Delaminate types have been studied by Barrois (No. 192) and Hoffman (No. 198), both of whom
give circumstantial accounts of their development.
Hoffman’s account is especially deserving of attention, since his observations were, to a great extent,
made by means of artificial sections. The following account is taken from him. His observations were
made on Tetrastemma varicolor, and Tetrastemma appears to be the genus in which this type of
development has been most completely made out. After a regular segmentation the embryo forms a
solid mass of cells, the outermost of which soon become distinguished as a separate epiblastic layer.
At the same time the larva leaves the egg, and the epiblast cells become coated by an uniform
covering of cilia. At the anterior extremity of the body is a bunch of long cilia; and at the hinder end
two stiff bristles are formed, but soon disappear.
The internal mass of cells is still quite uniform, but as the larva grows in length the outermost of
them arrange themselves as a columnar layer, constituting the mesoblast. Of the cells internal to the
mesoblast the outer become columnar, and are converted into the walls of the alimentary tract, while
the inner ones undergo fatty degeneration, and form a kind of food-yolk. In the later development the
characters of the adult are gradually acquired without metamorphosis, and the larval skin passes
directly into that of the adult. Both mouth and anus are formed nearly simultaneously by a rupture of
the enteric wall from within. The nervous system arises as a thickening of the epiblast, which
Hoffman states he has been able to see in sections. Hoffman also states that the epithelium of the
proboscis is formed as a diverticulum of the alimentary tract, and that its sheath is formed by a
special mesoblastic growth.
Barrois is less precise than Hoffman, from whom he differs in certain particulars. Hoffman’s
statements about the proboscis are important if accurate, but require further confirmation.

Malacobdella. The early stages in development of the peculiar ectoparasitic Nemertine
Malacobdella have been worked by Hoffman (No. 199) by means of sections, and there appears to be
a close agreement between the development of Malacobdella and that of Tetrastemma.
The segmentation is uniform, and there is no trace of a segmentation cavity. On the third day after
impregnation the outermost cells of the embryo become flattened and ciliated, and distinguished from
the remaining spherical cells of the embryo as the epiblast. With the appearance of cilia a rotation of
the embryo commences. On the fourth day the embryo becomes oval, and at one of the poles—the
future anal pole—a separation takes place between the epiblast and the inner cells, giving rise to the
body cavity. In it are a number of loose oval cells, which soon become stellate, and form a
mesoblastic reticulum connecting the body wall and central cells of the embryo, which may now be
spoken of as hypoblast. The body cavity increases in size, leaving at last the hypoblast and epiblast
united only at one point—the oral pole—at which, on the fifth day, a crown of long cilia appears. The
solid mass of hypoblast in the interior becomes differentiated into an outer layer of cells—the true
glandular epithelium of the alimentary tract—and an inner core, the cells of which soon undergo fatty
degeneration, and serve as food-yolk.
The later stages of development, and the formation of the proboscis, etc., have not been worked out.

General considerations. Of the types of larvæ hitherto found amongst the
Nemertea, those with a metamorphosis, viz. the Pilidium type and that of
Desor, are to be regarded as the primitive. But even in Pilidium there are
evidences of a great abbreviation in development. Pilidium itself is
probably a more or less modified ancestral form, while the peculiar
development of the Nemertine within it is to be explained as a very much
shortened record of a long series of changes by which the Pilidium became
gradually converted into a Nemertine. The formation of the body wall of the
Nemertine by four epiblastic invaginations is a remarkable embryological
phenomenon, for which it is not easy to assign a satisfactory meaning; and
it is probable that it is merely a secondary process of growth similar to the
formation of imaginal discs in the larvæ of Diptera (vide Chapter on
Tracheata), which has had its origin in the abbreviation of the development
just alluded to. The development of the type of Desor is clearly a
simplification of the Pilidium type, and its peculiarities are to be explained
by the fact that the first larval form has no free existence. The types without
metamorphosis have no doubt a development of a still more simplified
character; they are remarkable however in presenting us, if the existing
descriptions are to be trusted, with examples of delamination and
invagination coexisting in closely allied forms.

Trematoda.

The eggs of the Trematoda consist of a germ or true ovum enclosed in a
mass of yolk cells, which undergo disintegration and subsequent absorption
at varying periods of the development. From the observations of E. van
Beneden (No. 218), Zeller (No. 217), etc. it is known that the segmentation
is usually complete, but generally somewhat irregular.
Unfortunately we are still completely in the dark as to the mode of
formation of the germinal layers. The embryos of the entoparasitic forms or
Distomeæ become free in a very imperfect condition, and the ova are small
while in the Polystomeæ the development is as a rule nearly completed
before hatching, and the ova are large. It will be convenient to treat
separately the development of the two groups.
Distomeæ. The embryos of the Distomeæ are hatched either in some moist
place or more usually in water. In the majority of genera the larvæ pass
through a complicated metamorphosis, accompanied by alternations of
generations. But for some genera, e.g. Holostomum, etc., the life history has
not yet been made out. The whole life history of comparatively few forms
has been followed, but sufficient fragments are known to justify us in
making certain general statements, which no doubt hold true for a large
proportion of the Distomeæ.
The larvæ are usually ciliated (fig. 95 A), but sometimes naked.
The ciliated forms are generally completely covered with cilia, but in Distomum lanceolatum the cilia
are confined to an area at the front end of the body, in the centre of which a median spine is placed.
An x shaped pigment spot, sometimes provided with a rudimentary lens (Monostomum mutabile), is
also generally situated on the dorsal surface.
In some instances a more or less completely developed alimentary tract is present (Monostomum
capitellum, Amphistomum subclavatum), but usually there can only be distinguished in the interior of
the larva a transparent mass of cells bounded by a more or less distinctly marked body wall with
ciliated excretory channels.
Ed. van Beneden has shewn that the ciliated covering is developed while the embryo is still in the
egg, and long before the yolk cells are completely absorbed. It would seem that even before hatching
this ciliated covering is to a great extent independent of the mass within. In the larva of Monostomum
mutabile (fig. 95 A), which offers an example of an extreme case of the kind, there is present within
the ciliated epidermis a fully developed independent worm.
The non-ciliated larvæ are less highly organized than the ciliated forms, and are covered by a cuticle:
their anterior extremity is sometimes provided with a circular plate armed with radiate ridges and
spines.

The free-swimming or creeping embryos make their way into or on to the
body of some invertebrate (occasionally vertebrate) form, usually a
Mollusc, to undergo the first stage in their metamorphosis. They may either
do this on the gills of their host, or very frequently they bore their way into
the interior of the body. Soon after the larvæ have reached a satisfactory
position the epidermis becomes stripped off, and there emerges a second
larval form developed in the interior of the first larva, much as a Nemertine
is developed within the larva of Desor. In the case of Monostomum
mutabile the new worm is, as stated above, fully formed within the ciliated
larva at the time of hatching.
The worm which proceeds from the above metamorphosis has different
characters corresponding with those of the larva from which it proceeded. If
the original larva had an alimentary canal it has one also, and then grows
into the form known as a Redia (Fig. 95, B and C).
The Redia has anteriorly a mouth leading into a muscular pharynx and
thence into a cæcal stomach. Posteriorly the body is prolonged into a kind
of blunt caudal process, at the commencement of which are a pair of lateral
papillæ. There is a perivisceral cavity, and the body walls are traversed by
excretory tubes.
If the original larva is without an alimentary tract, the second form becomes
what is known as a Sporocyst. The Sporocyst is a simple elongated sack
with a central body cavity; when derived from the metamorphosis of a
ciliated embryo its walls are provided with excretory tubes, but such tubes
are absent in Sporocysts developed from non-ciliated larvæ. Some
Sporocysts send out numerous branches amongst the viscera of their hosts.

Fig. 95. Various stages in the Metamorphosis of the Distomeæ (from Huxley.)
A. Ciliated larva of Monostomum mutabile. a. larval skin. b. Redia developed within it. B.
Redia of Monostomum mutabile. C. Redia of Distomum pacificum, with germs of a second
brood of Rediæ. D. Redia containing Cercariæ. E. Cercaria. F. Full-grown Distomum.

The Rediæ and Sporocysts rapidly grow in size and sometimes increase by
transverse division. In the course of their further development one of two
things may happen. They may either (1) develop fresh Rediæ or Sporocysts
by a process of internal budding (fig. 95 C); or else (2) there may be formed
in them, by an analogous process, larvæ with long tails known as Cercariæ
(fig. 95 D.) The direct development of Cercariæ is the usual course, though
in Distomum globiparum the reverse is true; but where this does not take
place the Rediæ or Sporocysts of the second generation give rise to
Cercariæ.
The Cercariæ are developed from spherical masses of cells found in the
body cavity of the Sporocyst or Redia. The exact origin of these masses is
still somewhat obscure, but they are stated by Wagener (No. 212) to be
derived from the body wall. They are probably to be regarded as internal
buds.
The spherical bodies grow rapidly in size, their posterior extremity is
prolonged into a process which forms the tail, while the anterior part forms
the trunk. When fully formed (fig. 95 E), the trunk has very much the
organization of an adult Distomum. There is an anterior and a ventral

sucker, the former of which contains the opening of the mouth, and is often
provided with a special chitinous armature. The mouth leads into a
muscular pharynx, and this into a bilobed cæcal alimentary tract. An
excretory system of the ordinary type is present, consisting of longitudinal
contractile trunks continuous anteriorly with branched ciliated canals,
which, as has recently been shewn by Bütschli, may be provided with
funnel-shaped ciliated internal openings[94]. The contractile trunks unite
posteriorly, but instead of opening directly to the exterior are prolonged into
a vessel which traverses the substance of the tail, and after a longer or
shorter course bifurcates into two branches which open laterally.
The tail is provided with an axial rod of hyaline connective tissue, like the
notochord of the tail of a larval Ascidian, and is frequently provided with
membranous expansions. It is used as a swimming organ. Beneath the
epidermis are layers of circular and longitudinal muscular fibres, the latter
arranged in the tail as two bands.
The Cercariæ when fully developed leave the Sporocyst or Redia, and then
their host, and become free. In most Rediæ there is a special opening, not
far from the mouth, by which they pass out. There is no such opening in
Sporocysts, but the Cercariæ bore their way through the walls.
After leaving their parent the Cercariæ pass into the external medium, and
for a short period have a free existence. They soon however enter a new
host, making their way into its body by a process of boring, which is
effected by the head (especially when armed with chitinous processes)
assisted by movements of the tail.
The second host is usually some Invertebrate (Mollusc, Worm, Crustacean,
Insect larva, &c.), but occasionally a Fish or Amphibian or even a
vegetable. The tail is very often lost as the Cercaria bores its way into its
host, but whether it is so or not, the Cercaria, after it has once reached a
suitable post in its new host, assumes a quiescent condition, and surrounds
itself with a many-layered capsule. The cephalic armature and tail (if still
present) are then exuviated, and the generative organs gradually become
apparent though very small. In other respects the organization is not much
altered.

Though an encysted Cercaria may remain some months without further
change, it eventually dies unless it be introduced into its permanent
vertebrate host, an act which is usually effected by the host in which it is
encysted being devoured. It then becomes freed from its capsule as a fully
formed Trematode, in which the generative organs rapidly complete their
development.
In some cases the Rediæ or Sporocysts do not give rise to tailed Cercariæ,
but to tailless forms. In such cases, as a rule, the encystment takes place in
the host of the Redia or Sporocyst, but the tailless larvæ sometimes pass
through a free stage like the Cercariæ. In the case of Distomum cygnoides,
parasitic in the bladder of the Frog, the Cercaria passes directly into the
adult host without the intervention of an intermediate host.
The life history of a typical entoparasitic Trematode is shortly as follows:
(1) It leaves the egg as a ciliated or non-ciliated free larva.
(2) This larva makes its way on to the gills or into the body of some
Mollusc or other host, throws off its epidermis and becomes a Redia or
Sporocyst.
(3) In the body cavity of the Redia or Sporocyst numerous tailed larvæ,
known as Cercariæ, are developed by a process of internal gemmation.
(4) The Cercariæ pass out of the body of their parent, and out of their
host, and become for a short time free. They then pass into a second,
usually invertebrate host, and encyst.
(5) If their second host is swallowed by the vertebrate host of the adult of
the species, the encysted forms become free, and attain to sexual
maturity.
The majority of these stages are simply parts of a complicated
metamorphosis, but in the coexistence of larval budding (giving rise to
Cercariæ or fresh Rediæ) with true sexual reproduction there is in addition a
true alternation of generations.
Polystomeæ. The ova of the Polystomeæ are usually large and not very
numerous, and they are in most cases provided with some process for

attachment. Some species of Polystomeæ, e.g. Gyrodactylus, are however
viviparous. The young leave the egg in a nearly perfect state, and at the
utmost undergo a slight metamorphosis and no alternations of generations.
Some however (Polystomum, Diplozoon) are provided with temporary
cilia, but the number investigated is too small to determine whether ciliation
is the rule or the exception. The ciliated larvæ have a short free existence.
The cilia are developed on special cells which may be arranged in
transverse bands in the same way as in the larvæ of many Chætopods, but
are not, in the larvæ at present known, distributed uniformly. When the free
larvæ become parasitic the cells with cilia shrink up.
In Polystomum integerrimum, which lives in the urinary bladder of Rana temporaria, the eggs when
laid in the spring pass out into the water. The segmentation is complete, and the embryo when
hatched is provided with most of the adult organs, but presents certain striking larval characters. It
has five rings of ciliated cells. Three of these are placed anteriorly, and are especially developed on
the ventral surface, the posterior one being incomplete dorsally; two are placed posteriorly, and are
especially developed on the dorsal surface. Anteriorly there is a tuft of cilia.
The larva itself resembles somewhat an adult Gyrodactylus, and is provided (1) with a large posterior
disc armed with hooks, and (2) with two pairs of eyes which persist in the adult state. After a certain
period of free existence the larva attaches itself to the gills of a tadpole. The rings of ciliated cells
shrink up, and some of the six pairs of suckers found in the adult commence to be formed on the
posterior disc. When the bladder of the tadpole is developed, the young Polystomum passes down the
alimentary tract to the cloaca, and thence to the urinary bladder, where it slowly attains to sexual
maturity. When the larva becomes attached to the gills of a very young tadpole, its development is
somewhat more rapid in consequence of better nutrition from the more delicate gills. It then reaches
its full development in the gill cavity, and, though smaller and provided with differently organised
generative organs to the normal form, produces generative products and dies without being
transported to the bladder (vide Zeller, Nos. 216 and 217).
The ova of Diplozoon, a form parasitic on the gills of freshwater fish (Phoxinus, etc.), are provided
with a long spiral filament (Zeller, No. 215). The embryo has five ciliated areas, four lateral and one
posterior. The young form is known as Diporpa. Sexual maturity is not attained till two individuals
unite permanently together. They unite by the ventral sucker of each of them becoming attached to
the dorsal papilla of the other. Subsequently these parts coalesce, and the ventral suckers disappear in
the process. Gyrodactylus, parasitic, like Diplozoon, on the gills of freshwater fishes (Gasterosteus,
etc.), is remarkable for its mode of reproduction. It is viviparous, producing a single young one at a
time, and, what is still more remarkable, the young while still within its parent produces a young one,
and this again a young one, so that three generations may be present within the parent. It seems
probable that the second and third generations are produced asexually, the generative organs not
being developed; while the young Gyrodactylus of the first generation springs from a fertilized ovum
(Wagener, No. 214).

Cestoda.

On anatomical grounds the affinity of the Cestoda to the Trematoda has
been insisted on by the majority of anatomists. The existence of such
intermediate forms as Amphilina tends to strengthen this view; and the
striking resemblances between the two groups in the structure of the egg
and characters of the metamorphosis appear to me to remove all doubt
about the matter.
The ripe egg is formed of a minute germ enveloped in yolk cells, the whole
being surrounded by a membrane, which is very delicate in most forms, but
in certain types has a firmer consistency, and is provided with an aperture,
covered by an operculum, by which the larva escapes.
The early development, up to the formation of a six-hooked larva, generally
takes place in the uterus, but in the types with a firmer egg-shell it takes
place after the egg has been deposited in water.
The segmentation (E. van Beneden, No. 218, Metschnikoff, No. 228) is
complete, and during its occurrence the yolk cells surrounding the germ are
gradually absorbed, so that the mass of segmentation spheres grows in size,
till at the close of segmentation it fills up nearly the whole egg-shell.
As was first shewn by Kölliker for Bothriocephalus salmonis, the
embryonic cells separate themselves at the close of segmentation into a
superficial layer and a central mass.
The further development takes place on two types. In the cases where the
egg-shell is strong, and the egg is laid prior to the formation of the embryo,
a ciliated larva is developed (Bothriocephalus latus, ditremus,
Schistocephalus dimorphus, Ligula simplicissima, etc.[95]).
Of these forms Bothriocephalus latus may be taken as type.
The development of the embryo requires many months for its completion.
The outer layer becomes ciliated while the central mass has already become
developed into a six-hooked embryo. The embryo leaves its shell by the
opercular aperture, and for some time swims rapidly about by means of its
long cilia. The ciliated coating is eventually stripped off, and the six-hooked
larva emerges.

In the second type of embryo the external cellular layer does not become
ciliated. This is the most usual arrangement, and is even found in many
species of Bothriocephalus.
The central mass of cells becomes developed, as in the other type, into a
six-hooked (rarely four-hooked) embryo (fig. 96 G), but the superficial
layer separates from the central, and either disappears or becomes
(Bothriocephalus proboscideus) a cuticular layer. Between the six-hooked
embryo and the outer layer of cells one or more thick membranes become
deposited (E. van Beneden). The eggs are carried out of the alimentary
canal in the proglottis and transported to various situations on land or in
water. They usually remain within the proglottis, invested by their thick
shell, till taken up into the alimentary canal of a suitable host, or they may
be swallowed after the death and decay of the proglottis. They are
subsequently hatched after their shell has become softened by the action of
the digestive fluids.

Fig. 96. Diagrams of various stages in the development of the Cestoda.
(From Huxley.)
A. Cysticercus. B. and C. Cysticerci in the everted (B) and inverted (C) condition. D.
Cœnurus. E. and F. Diagrams of Echinococcus. It is most probable that Tænia heads are not
developed directly from the wall of the cyst as represented in the diagram. G. Six-hooked
embryo.

Before proceeding to describe their further history, the close resemblance
between the first developmental stages of Cestoda, especially in the case of
the ciliated larvæ, and those of Trematoda, may be pointed out.

In both there is a ciliated larva, and in both there is developed within the
ciliated skin a second larva, which becomes freed by the stripping off of the
ciliated skin.
The type of development has moreover many analogies with that of the
Nemertine larva of Desor, p. 163 (cf. Metschnikoff), and is probably like
that an abbreviated record of a long history.
The suitable host for the six-hooked embryo to enter is rarely the same as
the host for the sexual form. The embryos having become transported into
the alimentary canal of such a host, and become free, if previously invested
by the egg-shell, soon make their way, apparently by the help of their
hooks, through the wall of the alimentary tract, and are transported in the
blood or otherwise into some suitable place for them to undergo their next
transformation. This place may be the liver, lungs, muscles, connective
tissue, or even the brain (e.g. Cœnurus cerebralis in the brain of sheep).
Here they become enclosed in a granular deposit from the surrounding
tissues, which becomes in its turn enclosed in a connective-tissue coat.
Within lies the solid embryo, the hooks of which in many cases disappear or
become impossible to make out. In other forms, e.g. Cysticercus limacis,
they remain visible, and then mark the anterior pole of the worm (fig. 98,
c.). The central part of the body next becomes transformed into a material
composed of clear non-nucleated vesicles. Accompanying these changes the
embryo grows rapidly in size; a cuticle is deposited by its outer layer, in
which also an external layer of circular muscular fibres and an internal layer
of longitudinal fibres become differentiated, and internal to both there is
formed a layer of granular cells.
With the rapid growth of the body a central cavity is formed, which
becomes filled with fluid, and the embryo assumes the form of a vesicle. At
the same time a system of excretory vessels, sometimes opening by a
posterior pore, becomes visible in the wall of the vesicle.
The embryo has now reached a condition in which it is known as a cystic-
or bladder-worm, and may be compared in almost every respect with the
sporocyst of a Trematode (Huxley).

Fig. 97. Cysticercus cellulosæ. (From Gegenbaur, after von Siebold.)
a. Caudal vesicle. c. Anterior part of body. d. head.

Fig. 98. Cysticercus with small caudal vesicle.
A. Head involuted. B. Head everted.
a. Scolex. b. caudal vesicle. c. (in A) six embryonic hooks.

The next important change consists in the development of a head, which
becomes the head of the adult Tænia. This is formed in an involution of the
outer wall of the anterior extremity of the cystic worm. This involution
forms a papilliform projection on the inner surface of the wall of the cystic

worm, with an axial cavity opening by a pore on the outer surface. The
layer of cells forming the papilla soon becomes divided into two laminæ, of
which the outer forms a kind of investing membrane for the papilla. The
papilla itself now becomes moulded into a Cestode head, which however is
developed in an inverted position. The suckers and hooks (when present) of
the head are developed on a surface bounding the axial lumen of the papilla,
which is the true morphological outer surface, while the apparent outer
surface of the papilla is that which eventually forms the interior of the (at
first) hollow head. Before the external armature of the head has become
established, four longitudinal excretory vessels, continuous with those in
the body of the cystic worm, make their appearance. They are united by a
circular vessel at the apex of the head. The development is by no means
completed with the simple growth of the head, but the whole inverted
papilla continues to grow in length, and gives rise to what afterwards
becomes part of the trunk. The whole papilla eventually becomes everted,
and then the cystic worm takes the form (fig. 97) of a head and
unsegmented trunk with a vesicle—the body of the cystic worm—attached
behind. The whole larva is known as a C y s t i c e r c u s . The term
s c o l e x , which is also sometimes employed, may be conveniently
retained for the head and trunk only. The head differs mainly from that of
the adult in being hollow.
There are great variations in the relative size of the head and the vesicle of Cysticerci. In some forms
the vesicle is very small (fig. 98), e.g. Cysticercus limacis; it is medium-sized in Cysticercus
cellulosæ (fig. 97), and in some forms is much larger. The embryonic hooks, when they persist, are
found at the junction of the trunk and the vesicle (fig. 98 A, c). Though the majority of cystic worms
only develop one head, this is not invariably the case. There is a cystic worm found in the brain of the
sheep known as Cœnurus cerebralis—the larva of Tænia cœnurus, parasitic in the intestine of the
dog—which forms an exception to this rule. There appears, to start with, a tuft of three or four heads,
and finally many hundred heads are developed (fig. 96 D). They are arranged in groups at one (the
anterior?) pole of the cystic worm.
A still more complicated form of cystic worm is that known as Echinococcus, parasitic in the liver,
lungs, etc. of man and various domestic Ungulata. In the adult state it is known as Tænia
echinococcus and infests the intestine of the dog. The cystic worm developed from the six-hooked
embryo has usually a spherical form, and is invested in a very thick cuticle (fig. 96 E and F, and fig.
99). It does not itself directly give rise to Tænia heads, but after it reaches a certain size there are
formed on the inner side of its walls small protuberances, which soon grow out into vesicles
connected with the walls of the cyst by narrow stalks (figs. 96 F and 99 C). In the interior of these
vesicles a cuticle is developed. It is in these secondary vesicles that the heads originate. According to
Leuckart, they either arise as outgrowths of the wall of the vesicle on the inner face of which the
armature is developed, which subsequently become involuted and remain attached to the wall of the
vesicle by a narrow stalk, or they arise from the first as papilliform projections into the lumen of the

vesicle, on the outer side of which the armature is formed. Recent observers only admit the second of
these modes of development. The Echinococcus larva, in addition to giving rise to the above head-
producing vesicles, also gives rise by budding to fresh cysts, which resemble in all respects the parent
cyst. These cysts may either be detached in the interior (fig. 96 F) of the parent or externally. They
appear to spring in most cases from the walls of the parent cyst, but there are some discrepancies
between the various accounts of the process. In the cysts of the second generation vesicles are
produced in which new heads are formed. As the primitive cyst grows, it naturally becomes more and
more complicated, and the number of heads to which one larva may give rise becomes in this way
almost unlimited.

Cysticerci may remain a long time without further development, and human
beings have been known to be infested with an Echinococcus cyst for over
thirty years. When however the Cysticercus with its head is fully developed,
it is in a condition to be carried into its final host. This takes place by the
part of one animal infested with cysticerci becoming eaten by the host in
question. In the alimentary canal of the final host the connective-tissue
capsule is digested, and then the vesicular caudal appendage undergoes the
same fate, while the head, with its suckers and hooks, attaches itself to the
walls of the intestine. The head and rudimentary trunk, which have been up
to this time hollow, now become solid by the deposition of an axial tissue;
and the trunk very soon becomes divided into segments, known as
proglottides (fig. 99 A). These segments are not formed in the same
succession as those of Chætopods; the youngest of them is that nearest to
the head, and the oldest that furthest removed from it. Each segment
appears in fact to be a sexual individual, and is capable of becoming
detached and leading for some time an independent existence. In some
cases, e.g. Cysticercus fasciolaris, the segmentation of the trunk may take
place while the larva is still in its intermediate host.

Fig. 99. Echinococcus veterinorum. (From Huxley.)
A. Tænia head or scolex. a. hooks. b. suckers. c. cilia in water vessel. d. refracting particles in
body wall.
B. single hooks.
C. portion of cyst. a. cuticle. b. membranous wall of primary cyst. c. and e. scolex heads. d.
secondary cyst.

The stages in the evolution of the Cestoda are shortly as follows:
1. Stage with embryonic epidermis either ciliated (Bothriocephalus, etc.) or
still enclosed in the egg-shell. This stage corresponds to the ciliated larval
stage of the Trematoda.
2. Six-hooked embryonic stage after the embryonic epidermis has been
thrown off. During this stage the embryo is transported into the alimentary
tract of its intermediate host, and boring its way into the tissues, becomes
encapsuled.

3. It develops during the encapsuled state into a cystic worm, equivalent to
the sporocyst of Trematoda.
4. The cystic worm while still encapsuled develops a head with suckers and
hooks, becoming a Cysticercus. In some forms (Cœnurus, Echinococcus)
reproduction by budding takes place at this stage. The head and trunk are
known as the scolex.
5. The Cysticercus is transported into the second and permanent host by the
infested tissue being eaten. The bladder-like remains of the cystic worm are
then digested, and by a process of successive budding a chain of sexual
proglottides are formed from the head, which remains asexual.

Fig. 99 a. Tetrarhyncus. (From Gegenbaur; after Van Beneden.)
A. Asexual state.
B. Sexual stage with ripe proglottides.

The above development is to be regarded as a case of complicated
metamorphosis secondarily produced by the necessities of a parasitic
condition, to which an alternation of sexual and gemmiparous generations
has been added. The alternation of generations only occurs at the last stage
of the development, when the so-called head, without generative organs,
produces by budding a chain of sexual forms, the embryos of which, after
passing through a complicated metamorphosis, again become Cestode
heads.
In the case of Cœnurus and Echinococcus two or more asexual generations
are interpolated between the sexual ones. It is not quite clear whether the
production of the Tænia head from the cystic worm may not be regarded as

a case of budding. There are some grounds for comparing the scolex to the
Cercaria of Trematodes, cf. Archigetes.
As might be anticipated from the character of the Cestode metamorphosis, the two hosts required for
the development are usually forms so related that the final host feeds upon the intermediate host. As
familiar examples of this may be cited the pig, the muscles of which may be infested by Cysticercus
cellulosæ, which becomes the Tænia solium of man. Similarly a Cysticercus infesting the muscles of
the ox becomes the Tænia mediocanellata of man. The Cysticercus pisciformis of the rabbit becomes
the Tænia serrata of the dog. The Cœnurus cerebralis of the sheep’s brain becomes the Tænia
cœnurus of the dog. The Echinococcus of man and the domestic herbivores becomes the Tænia
echinococcus of the dog.
Cystic worms infest not only Mammalian forms, but lower Vertebrates, various fishes which form the
food of other fishes, and Invertebrates liable to be preyed on by vertebrate hosts. So far the Cestodes
(except Archigetes) are only known to attain sexual maturity in the alimentary tracts of Vertebrata.
The rule that the intermediate host is not the same as the final host does not appear to be without
exception. Redon[96] has shewn by experiments on himself that a Cysticercus (cellulosæ) taken from
a human subject develops into Tænia solium in the intestines of a man. Redon took four cysts of a
Cysticercus from a human subject, and after three months passed some proglottides, and
subsequently the head of Tænia solium.
Some important variations of the typical development are known.
The so-called head or scolex may be formed without the intervention of a cystic stage. In Archigetes
(Leuckart, No. 227), which infests, in the Cysticercus condition, the body cavity of various
invertebrate forms (Tubifex, etc.), the six-hooked embryo becomes elongated and divided into two
sections, one forming the head, while the other, with the six embryonic hooks, forms an appendage,
homologous with the caudal vesicle of other Cysticerci.
The embryo of Tænia elliptica similarly gives rise to a Cysticercus infesting the dog-louse
(Trichodectes canis), without passing through a vesicular condition; but the caudal vesicle
disappears, so that it forms simply a scolex. These cases may, it appears to me, be probably regarded
as more primitive than the ordinary ones, where the cystic condition has become exaggerated as an
effect of a parasitic life.
In some cases the larva of a Tænia has a free existence in the scolex condition. Such a form, the larva
of Phyllobothrium, has been observed by Claparède[97]. It was not ciliated, and was without a caudal
vesicle; and was no doubt actively migrating from an intermediate host to its permanent host.
Scolex forms, without a caudal vesicle, are found in the mantle cavity of Cephalopoda, and appear to
be occupying an intermediate host in their passage from the host of the cystic worm to that of the
sexual form.
Archigetes, already mentioned, has been shewn by Leuckart (No. 227) to become sexually mature in
the Cysticercus state, and thus affords an interesting example of pædogenesis. It is not known for
certain whether under normal circumstances it reaches the mature state in another host.
A m p h i l i n a . The early stages of this interesting form have been investigated by Salensky (No.
229), and exhibit clear affinities to those of the true Cestoda. An embryonic provisional skin is
formed as in Cestodes; and pole cells also appear. Within the provisional skin is formed an embryo

with ten hooks. After hatching the provisional skin is at once thrown off, and the larva, which is then
covered by a layer of very fine cilia, becomes free. The further metamorphosis is not known.

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(198) C. K. Hoffmann. “Entwicklungsgeschichte von Tetrastemma tricolor.” Niederländisches
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(202) E. Metschnikoff. “Studien üb. die Entwicklung d. Echinodermen u. Nemertinen.” Mém. Acad.
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embryogénique, etc.” Bul. Acad. Scien. Bruxelles. Vol. XVII. 1850.
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(222) Th. H. Huxley. “On the Anatomy and Development of Echinococcus veterinorum.” Proc.
Zool. Soc. Vol. XX. 1852.
(223) J. Knoch. “Die Naturgesch. d. breiten Bandwürmer.” Mém. Acad. Imp. Pétersbourg, Vol. V.
Ser. 7, 1863.
(224) F. Küchenmeister. “Ueber d. Umwandlung d. Finnen Cysticerci in Bandwürmer (Tænien).”
Prag Vierteljahrsschr. 1852.
(225) —— “Experimente üb. d. Entstehung d. Cestoden. 2o Stufe zunächst d. Cœnurus cerebralis.”
Günsburg, Zeitsch. klin. Med. IV. 1853.
(226) R. Leuckart. Die Menschlichen Parasiten, Vol. I. Leipzig, 1863. Vide also additions at the end
of the 1st and 2nd volume.
(227) R. Leuckart. “Archigetes Sieboldii, eine geschlechtsreife Cestodenamme.” Zeit. f. wiss. Zool.,
Vol. XXX. Supplement, 1878.
(228) El. Metschnikoff. “Observations sur le développement de quelques animaux (Bothriocephalus
proboscideus).” Bull. Acad. Imp. St Pétersbourg, Vol. XIII. 1869.
(229) W. Salensky. “Ueb. d. Bau u. d. Entwicklungsgeschichte d. Amphilina.” Zeit. f. wiss. Zool.,
Vol. XXIV. 1874.

(230) Von Siebold.Burdach’s Physiologie.
(231) R. von Willemoes-Suhm. “Helminthologische Notizen.” Zeit. f. wiss. Zool., Vol. XIX. XX. XXII.
1869, 70 and 73.

[89]
I. Turbellaria.
1. Dendrocœla.
2. Rhabdocœla.
II. Nemertea.
1. Anopla.
2. Enopla.
III. Trematoda.
1. Distomeæ.
2. Polystomeæ.
IV. Cestoda.
[90] It is probable, though it has not been observed, that the growth of the layer of
small cells is assisted by the formation of fresh cells from the hypoblast spheres.
[91] The account of Metschnikoff’s observations on Stylochopsis ponticus given in
the German abstract is too obscure to be placed in the text, but the following are the
more important points which can be gleaned from it.
The ovum becomes first divided into eight segments. By further division along the
equatorial zone, a ring of small cells is formed which becomes the epiblast. The two
poles are at this time formed of large cells. At one pole four small cells appear,
which are compared by Metschnikoff to the pole cells of the Diptera (vide Chapter
on the development of the Insecta). At the opposite pole a blastopore is formed
leading into a small segmentation cavity. The epiblast also now gradually grows
over the large cells. At the blastopore pole the large cells give rise to the hypoblast
and the small cells at the opposite pole assist in forming the epiblast. The blastopore
disappears, and with it the segmentation cavity, while the hypoblast, forming a solid
mass, becomes divided into two halves (Cf. Planaria Neapolitana). The embryo
becomes ciliated and begins to rotate; and the eyes, and somewhat later (?) the
nervous ganglion make their appearance.
In the interior a wide cavity develops between the hypoblast cells, which becomes
ciliated and is placed in communication with the exterior by an invaginated
stomadæum which forms the pharynx.
The larva now, as in Planaria Neapolitana, takes on a Pilidium-like form. Lateral
lobes and an anterior lip grow out from the under surface, and become covered with
long cilia, while at the upper pole a long flagellum makes its appearance.
[92] Bütschli for Pilidium regards these pits as formed by invaginations of the
epiblast, but Metschnikoff’s statements are in accordance with those in the text.
[93] This is the view of both Metschnikoff (No. 202) and Leuckart and Pagenstecher
(No. 201), and is further confirmed by Barrois, but Bütschli (No. 193), though he

has not observed the earliest stages of their outgrowth, believes them to be
invaginations of the Nemertine skin.
[94]O. Bütschli, “Bemerkungen üb. d. excretorischen Gefässapparat d.
Trematoden.” Zoologischer Anzeiger, 1879, No. 42.
[95] Vide for list of such forms at present known Willemoes Suhm, No. 231.

[96] Annal. d. Scien. Nat., 6th Series, Vol. VI. 1877.

[97] Beobachtungen üb. Anat. u. Entwick. Wirbell. Thiere. Leipzig, 1863.

CHAPTER VIII.

ROTIFERA.

For many reasons a complete knowledge of the ontogeny of the Rotifera is
desirable. They constitute a group which retain in the trochal disc an organ
common to the embryos of many other groups, but which in most other
instances is lost in the adult state. In the character of the excretory organs
they exhibit affinities with the Platyelminthes, while in other respects they
possibly approach the Arthropoda (e.g. Pedalion ?). The interesting
Trochosphæra æquatorialis of Semper closely resembles a monotrochal
polychætous larva.
Up to the present time our embryological knowledge is mainly confined to
a series of observations by Salensky on Brachionus urceolaris, and to
scattered statements on other larval forms by Huxley, etc.
In many cases Rotifers lay summer and winter eggs of a different character.
The former are always provided with a thin membrane, and frequently
undergo development within the oviduct. They are hatched in the autumn.
The winter eggs are always provided with a thick shell.
The summer eggs are of two kinds, viz. smaller eggs which become males,
and larger, females. On the authority of Cohn (No. 232) they are believed to
develop parthenogenetically. Males are not found in summer, and only seem
to be produced from the summer eggs. Cohn’s observations, especially on
Conochilus volvox, are however not quite satisfactory. Huxley (No. 234)
came to the conclusion that the winter eggs of Lacinularia developed
without previous fertilization.
The following are the more important results of Salensky’s observations
(No. 236) on Brachionus urceolaris.
The ovum is attached by a short stalk to the hind end of the body of the
female, in which position it undergoes its development. It will be
convenient to treat separately the development of the female and male, and
to commence with the former. The female ovum divides into two unequal

spheres, of which the smaller in the subsequent stages segments more
rapidly than the larger. The segmentation ends with the formation of an
epibolic gastrula. The solid inner mass of cells derived from the larger
sphere constitutes the hypoblast, and is more granular than the epiblast. The
evolution of the embryo commences with the formation of a depression on
the ventral surface, at the bottom of which the stomodæum is formed by an
invagination. At the hinder part of the depression there rises up a rounded
protuberance which eventually becomes the caudal appendage or foot.
Immediately behind the mouth is formed an underlip.
On the sides of the ventral depression are two ridges which form the lateral
boundaries of the trochal disc. They appear to unite with the under lip.
In a later stage the anterior part of the body becomes marked off from the
posterior as a præoral lobe, and the hypoblast is at the same time confined
to the posterior part. The supra-œsophageal ganglion is early formed as an
epiblastic thickening on the dorsal side of the præoral lobe.
The first cilia to appear arise at the apex of the præoral lobe. At a later
period the lateral ridges of the trochal disc meet dorsally and so enclose the
præoral lobe. They then become coated by a ring of cilia, to which a second
ring, completing the double ring of the adult, is added later.

Fig. 100. Embryo of Brachionus urceolaris shortly before it is hatched. (After
Salensky.)

m. mouth; ms. masticatory apparatus; me. mesenteron; an. anus; ld. lateral gland; ov. ovary; t.
tail, i.e. foot; tr. trochal disc; sg. supra-œsophageal ganglion.

In the trunk an indication of a division into two segments makes its
appearance shortly after the development of the præoral lobe. Before this
period the proctodæum is established as a shallow pit immediately behind
the insertion of the foot. The latter structure soon becomes pointed and
forked (fig. 100, t).
The complete establishment of the alimentary canal occurs late. The
stomodæum (fig. 100) gives rise to the mouth (m), œsophagus and
masticatory apparatus (ms). The mesenteron is formed from the median part
of the hypoblast; the lateral parts of which appear to give rise to the great
lateral glandular structures (ld) which open into the stomach, and to the
ovaries (?) (ov) etc. The proctodæum becomes the cloaca and anus (an).
The origin of the mesoblast is not certainly known. The shell is formed
before the larva is hatched—an occurrence which does not take place till
the larva closely resembles the adult.
The early developmental stages of the male are closely similar to those of
the female; and the chief difference between the two appears to consist in
the development of the male being arrested at a certain point.
The larvæ of Lacinularia (Huxley, No. 234) are provided with a præoral
circlet of cilia containing two eye-spots[98], and a peri-anal patch of cilia.
They closely resemble some telotrochal polychætous larvæ.
Salensky has compared the larva of Brachionus to that of a cephalophorous
Mollusc, more especially to the larva of Calyptræa on which he has made
important observations. The præoral lobe, with the ciliated band, no doubt
admits of a comparison with the velum of the larva of Molluscs; but it does
so equally, as was first pointed out by Huxley, with the ciliated præoral lobe
of the larvæ of many Vermes. It further deserves to be noted that the trochal
disc of a Rotifer differs from the velum of a Mollusc in that the eyes and
ganglia are placed dorsally to it, and not, as in the velum of a Mollusc,
within it. The larva of Lacinularia appears to be an exception to this, since
two eye-spots are stated to lie within the circlet of cilia. More important in
the comparison is the so-called foot (tail), which arises in the embryo as a

prominence between the mouth and anus, and in this respect exactly
corresponds with the Molluscan foot.
If Salensky’s comparison is correct, and there is something to be said for it,
the foot or tail of Rotifers is not a post-anal portion of the trunk, but a
ventral appendage, and the segmentation which it frequently exhibits is not
to be compared with a true segmentation of the trunk. If the Rotifers, as
seems not impossible, exhibit crustacean affinities, the ‘foot’ may perhaps
be best compared with the peculiar ventral spine of the Nauplius larva of
Lepas fascicularis (vide Chapter on Crustacea) which in the arrangement of
its spines and other points also exhibits a kind of segmentation.

Bibliography.
(232) F. Cohn. “Ueb. d. Fortpflanzung von Räderthiere.” Zeit. f. wiss. Zool. Vol. VII. 1856.
(233) F. Cohn. “Bemerkungen ü. Räderthiere.” Zeit. f. wiss. Zool. Vol. IX. 1858, and Vol. XII. 1862.
(234) T. H. Huxley. “Lacinularia socialis.” Trans. of the Microscopical Society, 1853.
(235) Fr. Leydig. “Ueb. d. Bau u. d. systematische Stellung d. Räderthiere.” Zeit. f. wiss. Zool. Vol.
VI. 1854.
(236) W. Salensky. “Beit. z. Entwick. von Brachionus urceolaris.” Zeit. f. wiss. Zool. Vol. XXII. 1872.
(237) C. Semper. “Zoologische Aphorismen. Trochosphæra æquatorialis.” Zeit. f. wiss. Zool. Vol.
XXII. 1872.

[98] In Leydig’s figure of the larva, Zeit. f. wiss. Zool. Vol. III. 1851, the eye-spots lie
just outside the ciliated ring.

CHAPTER IX.

MOLLUSCA[99].

Although the majority of important developmental features are common to
the whole of the Mollusca, yet at the same time many of the subdivisions
have well-marked larval types of their own. It will for this reason be
convenient in considering the larval characters to deal successively with the
different subdivisions, but to take the whole group at once in considering
the development of the organs.

Formation of the layers and larval characters.
Odontophora.
Gasteropoda and Pteropoda. There is a very close agreement amongst the
Gasteropoda and Pteropoda in the general characters of the larva; but owing
to the fact that the eggs of the various species differ immensely as to the
amount of food-yolk, considerable differences obtain in the mode of
formation of the layers and of the alimentary tract.
The spheres at a very early stage of segmentation[100] become divided into
two categories, one of them destined to give rise mainly to the hypoblast,
the other mainly to the epiblast. According as there is much or little food-
yolk the hypoblast spheres are either very bulky or the reverse. In all cases
the epiblast cells lie at one pole, which may be called t h e f o r m a t i v e
p o l e , and the hypoblast cells at the opposite pole. When the bulk of the
food-yolk is very great, the number of hypoblast spheres is small. Thus in
Aplysia there are only two such spheres. In other cases, where there is but
little food-yolk, they may be nearly as numerous as the epiblast cells. In all
these cases, however, as was first shewn by Lankester and Selenka, a
gastrula becomes formed either by normal invagination as in the case of
Paludina (fig. 107), or by epibole as in Nassa mutabilis (fig. 105). In both
cases the hypoblast becomes completely enclosed by the epiblast. The
blastopore is always situated opposite the original formative pole. In the

large majority of cases (i.e. Marine Gasteropoda, Heteropoda, and
Pteropoda) the blastopore becomes gradually narrowed to a circular
opening which eventually occupies the position of the mouth. It either
closes or remains permanently open at this point. In some cases the
blastopore remains permanently open and becomes the anus. The best
authenticated instance of this is Paludina vivipara, as was first shewn by
Lankester (No. 263).
In some instances the blastopore assumes before closing a very narrow slit-
like form, and would seem to extend along the future ventral region of the
body from the mouth to the anus. This appears, according to Lankester (No.
262), to be the condition in Lymnæus, but while Lankester believes that the
closure proceeds from the oral towards the anal extremity, other
investigators hold that it does so in the reverse direction. Fol (No. 249) has
also described a similar type of blastopore. In an undetermined marine
Gasteropod, with an embolic gastrula, observed by myself at Valparaiso, the
blastopore had the same elongated form as in Lymnæus, but the whole of it
soon became closed except the oral extremity; but whether this finally
closed could not be determined. It is probable that the typical form of the
blastopore is the elongated form observed by Lankester and myself, in
which an unclosed portion can indifferently remain at either extremity; and
that from this primitive condition the various modifications above described
have been derived[101].
Before the blastopore closes or becomes converted into the oral or anal
aperture, a number of very important embryonic organs make their
appearance; but before describing these it will be convenient to state what is
known with reference to the third embryonic layer or mesoblast.
This layer generally originates in a number of cells at the lips of the
blastopore, which then gradually make their way dorsalwards and forwards,
and form a complete layer between the epiblast and hypoblast. The above
general mode of formation of the mesoblast may be seen in fig. 107,
representing three stages in the development of Paludina.
In some cases the mesoblast arises from certain of the segmentation spheres
intermediate in size between the epiblast and hypoblast spheres. This is the
case in Nassa mutabilis, where the mesoblast appears when the epiblast

only forms a very small cap at the formative pole of the ovum; and in this
case the mesoblast cells accompany the epiblast cells in their growth over
the hypoblast (fig. 105).
In other cases the exact derivation of the mesoblast cells is quite uncertain.
The evidence is perhaps in favour of their originating from the hypoblast. It
is also uncertain whether the mesoblast is bilaterally symmetrical at the
time of its origin. It is stated by Rabl to be so in Lymnæus[102].
In the case of Paludina the mesoblast becomes two layers thick, and then
splits into a splanchnic and somatic layer, of which the former attaches
itself to the hypoblast, and gives rise to the muscular and connective-tissue
wall of the alimentary tract, and the latter attaches itself to the epiblast, and
forms the muscular and connective-tissue wall of the body and other
structures. The two layers remain connected by protoplasmic strands, and
the space between them forms the body cavity (fig. 107). In most instances
there would appear to be at first no such definite splitting of the mesoblast,
but the layer has the form of a scattered network of cells between the
epiblast and the hypoblast. Finally certain of the cells form a definite layer
over the walls of the alimentary canal, and constitute the splanchnic
mesoblast, and the remaining cells constitute the somatic mesoblast.

Fig. 101. Diagram of an embryo of Pleurobranchidium. (From Lankester.)
f. foot; ot. otocyst; m. mouth; v. velum; ng. nerve ganglion; ry. residual yolk spheres; shs.
shell-gland; i. intestine.

We must now return to the embryo at the time when the blastopore is
becoming narrowed. First of all it will be necessary to define the terms to be
applied to the various regions of the body—and these will best be
understood by taking a fully formed larva such as that represented in fig.
101. The ventral surface I consider to be that comprised between the mouth
(m) and the anus, which is very nearly in the position (i) in the figure. As a
great protuberance on the ventral surface is placed the foot f. The long axis
of the body, at this period though not necessarily in the adult, is that passing
through the mouth and the shell-gland (shs.): while the dorsal surface is that
opposite the ventral as already defined.
Before the blastopore has attained its final condition three organs make
their appearance, which are eminently characteristic of the typical
molluscan larva. These organs are (1) the velum, (2) the shell-gland, (3) the
foot.
The velum is a provisional larval organ, which has the form of a præoral
ring of cilia, supported by a ridge of cells, often in the form of a double row,
the ventral end of which lies immediately dorsal to the mouth. Its typical
position is shewn in fig. 101, v. There are considerable variations in its
mode and extent of development etc., but there is no reason to think that it
is entirely absent in any group of Gasteropoda or Pteropoda. In a few
individual instances, especially amongst viviparous forms and land
Pulmonata, it has been stated to be absent. Semper (No. 274) failed to find
it in Vitrina, Bulimus citrinus, Vaginulus luzonicus, and Paludina costata. It
is very probably absent in Helix, etc.
In some cases, e.g. Limax (Gegenbaur), Neritina (Claparède), Pterotrachæa
(Gegenbaur), the larva is stated to be coated by an uniform covering of cilia
before the formation of the velum, but the researches of Fol have thrown
very considerable doubt on these statements. In some cases amongst the
Nudibranchiata (Haddon) and Pteropoda there are one or two long cilia in
the middle of the velar area. In many Nudibranchiata (Haddon) there is
present a more or less complete post-oral ring of small cilia, which belongs
to the velum.
The cilia on the velum cause a rotation of the larva within the egg-capsule.
Cilia are in most cases (Paludina, etc.) developed on the foot and on a small

anal area.
The shell-gland arises as an epiblastic thickening on the posterior and dorsal
side. In this thickening a deep invagination (fig. 101, shs.) is soon formed,
in which a chitinous plug may become developed (Paludina, Cymbulia?
etc.), and in abnormal larvæ such a chitinous plug is generally formed.
The foot is a simple prominence of epiblast on the ventral surface, in the
cavity of which there are usually a number of mesoblast cells (fig. 101, f).
The larval form just described has been named by Lankester the
trochosphere larva.
Before considering the further external changes which the larva undergoes,
it will be well to complete the history of the invaginated hypoblast.

Fig. 102. Embryo of A Heteropod. (From Gegenbaur; after Fol.)
o. mouth; v. velum; g. archenteron; p. foot; c. body cavity; s. shell-gland.

The hypoblast has after its invagination either the form of a sack (fig. 102)
or of a solid mass (fig. 101). Whether the mouth be the blastopore or no, the
permanent œsophagus is formed of epiblast cells, so that the œsophagus and
buccal cavity are always lined by epiblast. When the blastopore remains
permanently open the outer part of the œsophagus grows as a prominent
ridge round the opening.
The mesenteric sack itself becomes differentiated into a stomach adjoining
the œsophagus, a liver opening immediately behind this, and an intestine.

The cells forming the hepatic diverticula and sometimes also those of the
stomach may during larval life secrete in their interior peculiar albuminous
products, similar to ordinary food-yolk.
The proctodæum, except when it is the blastopore, arises later than the
mouth. It is frequently developed from a pair of projecting epiblast cells
symmetrically placed in the median ventral line behind the foot. It
eventually forms a very shallow invagination meeting the intestine. Its
opening is the anus. The anus, though at first always symmetrical and
ventral, subsequently, on the formation of the pallial cavity, opens into this
usually on the right and dorsal side.
In the cases where the hypoblast is not invaginated in the form of a sack the
formation of the mesenteron is somewhat complicated, and is described in
the sequel.
From the trochosphere stage the larva passes into what has been called by
Lankester the veliger stage (fig. 103), which is especially characteristic of
Gasteropod and Pteropod Mollusca.
The shell-gland (with a few exceptions to be spoken of subsequently) of the
previous stage flattens out, forming a disc-like area, on the surface of which
a delicate shell becomes developed, while the epiblast of the edges of the
disc becomes thickened. The disc-like area is the mantle. The edge of the
area and with it the shell now rapidly extend, especially in a dorsal
direction. Up to this time the embryo has been symmetrical, but in most
Gasteropods the shell and mantle extend very much more towards the left
than towards the right side, and a commencement of the permanent spiral
shell is thus produced.

Fig. 103. Larvæ of Cephalophorous Mollusca in the veliger stage.
(From Gegenbaur.)
A. and B. Earlier and later stage of Gasteropod. C. Pteropod (Cymbulia).
v. velum; c. shell; p. foot; op. operculum; t. tentacle.

The edge of the mantle forms a projecting lip separating the dorsal visceral
sack from the head and foot. An invagination appears, usually on the right
in Gasteropods, and eventually extends to the dorsal side (fig. 103 B). It
gives rise to the pallial or branchial cavity, and receives also the openings of
the digestive, generative and urinary organs. In most Pteropods it is also
formed to the right, and usually eventually extends afterwards towards the
ventral surface (fig. 103 C). In the pallial cavity the gills are formed, in
those groups in which they are present, as solid processes frequently
ciliated. They are coated by epiblast and contain a core of mesoblast. They
soon become hollow and contractile.
The velum in the more typical forms loses its simple circular form, and
becomes a projecting bilobed organ, which serves the larva after it is
hatched as the organ of locomotion (fig. 103 B and C). The extent of the
development of the velum varies greatly. In the Heteropods especially it
becomes very large, and in Atlanta it becomes six-lobed, each lateral half
presenting three subdivisions. It is usually armed on its projecting edge with
several rows of long cilia, and below this with short cilia which bring food
to the mouth. It persists in many forms for a very long period. Within the
area of the velum there appear the tentacles and eyes (fig. 103 B). The latter
are usually formed at the base of the tentacles.

The foot grows in most forms to a very considerable size. On its hinder and
dorsal surface is formed the operculum as a chitinos plate which originates
in a depression lined by thickened epiblast, much in the same way as the
shell (fig. 103 B and C, op). In the typical larval forms it is only possible to
distinguish the anterior flattened surface of the foot for locomotion and the
posterior opercular region, but special modifications of the foot are found in
the Pteropods and Heteropods, which are described with those groups. The
foot very often becomes richly ciliated, and otic vesicles are early
developed in it (fig. 101, ot).
All the Gasteropods and Pteropods have a shell-bearing larval form like that
first described, with the exception of a few forms, such as Limax and
perhaps some other Pulmonata, in which the shell-gland closes up and gives
rise to an internal shell.
The subsequent metamorphosis in the different groups is very various, but
in all cases it is accompanied by the disappearance of the velum, though in
some cases remnants of the velum may persist as the subtentacular lobes
(Lymnæus, Lankester) or the lip tentacles (Tergipes, Nordmann). In
prosobranchiate Gasteropods the larval shell is gradually added to, and
frequently replaced by, a permanent shell, though the free-swimming
veligerous larva may have a long existence. In many of the
Opisthobranchiata the larval shell is lost in the adult and in others reduced.
Lankester, who has especially worked at the early stages of this group, has
shewn that the larvæ are in almost every respect identical with those of
prosobranchiate Gasteropods. They are all provided with a subnautiloid
shell, an operculated foot, etc. The metamorphosis has unfortunately been
satisfactorily observed in but few instances. In Heteropods and Pteropods
the embryonic shell is in many cases lost in the adult.
The following sections contain a special account of the development in the
various groups of Gasteropoda and Pteropoda which will complete the
necessarily sketchy account of the preceding pages.
Gasteropoda. To illustrate the development of the Gasteropoda I have given a detailed description of
two types, viz. Nassa mutabilis and Paludina vivipara.