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AMPHIOXUS AND THE ANCES PRY
OF THE VERTEBRATES
Columbia Gnibersity Biological Series.
a
EDITED BY
HENRY FAIRFIELD OSBORN.
1. FROM THE GREEKS TO DARWIN.
By Henry Fairfield Osborn, Sc.D. Princeton.
2. AMPHIOXUS AND THE ANCESTRY OF THE VERTEBRATES.
By Arthur Willey, B.Sc. Lond. Univ.
3. FISHES, LIVING AND FOSSIL. An Introductory Study.
By Bashford Dean, Ph.D. Columbia.
4. THE CELL IN DEVELOPMENT AND INHERITANCE.
By Edmund B. Wilson, Ph.D. J.H.U.
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222191] UOLT ‘(VNISSHJ) ONVY LY ONVINVG FHL
I SOXOTHINY
COLUMBIA UNIVERSITY BIOLOGICAL SERIES. J.
AMPHIOXUS AND THE ANCESTRY
OF THE VERTEBRATES
BY
ARTHUR, WILLEY, BSc
Tutor In BioLtocy, CotumpiA CoLLEGE; BALFouR STUDENT OF THE
UNIVERSITY OF CAMBRIDGE
WITH A PREFACE
BY
HENRY FAIRFIELD OSBORN
New Work
MACMILLAN AND GO.
AND LONDON
1894
All rights reserved
CopyrIGHT, 1894,
By MACMILLAN AND Co,
16%
Norioood Jress.
J. S. Cushing & Co.— Berwick & Smith.
Boston, Mass., U.S.A.
Dedicated
IN GRATITUDE AND ESTEEM
TO
PROPESSOR, ES RAY -LANKESTER, EER. s-
BY
HIS FORMER PUPIL
THE AUTHOR
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PRP eae B:
Tuis volume originated in a course of University lec-
tures prepared at my suggestion by the author. It seemed
important that he should bring within the reach of
students and of specialists among other groups, his own
extensive observations upon Amphioxus and other remote
ancestors of the Vertebrates, as well as the general litera-
ture upon this group. While our detailed knowledge of
the structure and habits of these animals has been rapidly
increasing in recent years, it is still in the main very
widely scattered in monographs and special papers.
Probably no single group illustrates more beautifully
the principles of transformism ; for the Protochordates in
their embryonic development exhibit remarkable reminis-
cences of past adaptations, and, in their adult develop-
ment, the most varied present adaptations to pelagic,
deep-sea, littoral, free-swimming, and sessile life. As
Lankester has shown, the Ascidians alone give us a whole
chapter in Darwinism. But degeneration and change of
function constitute only one side of their history. In
vii
Vill PREFACE.
progressive development some of these types have come
to so closely resemble, superficially, certain of the larger
groups of Invertebrates, such as the Molluscs and Worms,
that it is only at a comparatively recent date they have
found their way out of these groups into the Protochor-
data. Many of these misleading resemblances are now
interpreted as parallels of structure springing from parallels
in life habit, seen not only in the general body form, but
in special organs, such as the breathing apparatus of the
Ascidians and Molluscs.
By the side of parallelisms are real invertebrate and
vertebrate affinities; so that the problem of resolving
these various cases of original and acquired likeness in
their bearing upon descent has become one of the most
fascinating which modern Zodlogy affords. For example,
among the real invertebrate ties of the Protochordates are
the ciliated embryos of Balanoglossus and Amphioxus,
the Tornaria larva and ciliated ectoderm of Balanoglossus.
The nervous system of Balanoglossus presents both ver-
tebrate and invertebrate characters; the respiratory sys-
tem is identical with that of Amphioxus, while in the
embryonic development there are many resemblances zz¢er
se. In short, in Balanoglossus and the Ascidians the
invertebrate type of structure, whether original or ac-
quired, predominates. But in Amphioxus the balance is
far on the other or vertebrate side of the scale, and this,
with its resemblances to lower forms, gives us the con-
PREFACE. ix
necting link between Protochordate and Chordate organ-
isation. Before entering into any of these discussions,
the author has given a thorough systematic and structural
treatment, especially of Amphioxus.
This exquisite form, Amphioxus, is of almost world-wide
distribution and has enjoyed the attention of every great
zoologist for over half a century, yet the most recent
studies upon it have been among the most productive of
discovery. Its interest and value as an object of biologi-
cal education has steadily increased with the knowledge
that in contrast with all the related forms, it stands as
a persistent specialised but not degenerate type, perhaps
not far from the true ancestral line of the Vertebrates.
Hoi ©:
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CON TENTS: :
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AttrialCavity: ape <n eet oi ace sis ris aom sy aoe tila ee emo
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SUM Ge nag 5 no 6 5 5 6 ao 0 4 De oY
volutronvorathesbhymus) Glands ieee) 8 eee nO
nd ostylementiws+ (0 mys) “as tll ec. toy ya ms ey co AOE
Branchial Bars . 32
Musculature . 34
NODES meso mr-aMvabsey Bod for tk Ge. Seca Sen te. age eat Ce cS
AINA ONG ORZANIREMORUIS ) 5.2028 a0) ob ust Gees wma! fon 46
INTERNAL ANATOMY (continued). . ... . Bee tiie: VERA
NasculamSystemartre: o9cs os 4) oo ee Rhee acm Nc tems 240
Une DEO SNC Gea hoe oso 6 8 oo o op
Deyelopment.of theAtrial Cavity 2 1. 3) ees a 75
Comparison between the Excretory System of Amphioxus and
thatonethewAmmelidser) x4 <2) 5, kom ee) oe nn 07S
INerVOUS: SYStCKDIBM NR cr nc. 2p scp rea Pe asa ee 2
INGIRESHRe cnc. curs ; 2} e peteUR ese oh orb ane Nee SOS
xl
CONTENTS.
_ DEVELOPMENT OF AMPHIOXUS ....-+-« -
EMBRYONIC DEVELOPMENT
Fertilisation and Segmentation of the Ovum.
Gastrulation .
Growth of Free-swimming Embryo .
Development of Central Nervous System .
Origin of Mesoderm and Ccelom
Origin of the Notochord
The Preoral “ Head-cavities ” of Amphioxus
Endostyle and Pigment Granules . . - - + e + +
IDARAONE, IDIDBOCORVINAD 5 56 ob a a geo bs
Formation of Primary Gill-slits, etc.
Formation of Secondary Gill-slits
Club-shaped Gland and Endostyle
Continued Migration of Primary Gill-slits .
Peripharyngeal Bands
Atrophy of First Primary Gill-slit and Club- ncen Gland, etc.
The Adjustment of the Mouth, etc. .
Equalisation of the Gill-slits .
Further Growth of Endostyle, etc.
Development of Reproductive Organs .
GENERAL CONSIDERATIONS .
Larval Asymmetry Sar F achat
Explanation of Asymmetry of Mouth and Gill-slits
Larval Asymmetry not Adaptive and not Advantageous .
AMPHIOXUS AND AMMOCCETES .
Nervus Branchialis Vagi
Stomodceum, Hypophysis, and Gill-slits
Endostyle or Hypobranchial Groove
Peripharyngeal Ciliated Bands of Ammoceetes .
Thyroid Gland . An
Morphology of Club- unre Gland of tee,
Preeoral “ Nephridium” of Hatschek
Ancestral Number of Gill-slits
NOTES
CONTENTS.
THE ASCIDIANS
STRUCTURE OF A SIMPLE ASCIDIAN .
Test, Mantle, Atrium, Branchial Sac.
Dorsal Lamina, Endostyle, and ere: Band.
Visceral Anatomy . cane
Nervous System and Hypophysis
Givcwlenarsy SWAN 5 Lo GG 86 sm oa Ooo A
Renal Organs
Comparison between an Ascidian and Amphioxus .
DEVELOPMENT OF ASCIDIANS
Segmentation and Gastrulation ,
Formation of Medullary Tube and Notochord .
Origin of Mesoderm .
Outgrowth of Tail rhs
Formation of the Adhesive Papillz .
Cerebral Vesicle and its Sense-organs . ore
Comparison of Tunicate Eye with the Pineal Eye .
Stomodceal and Atrial Involutions
Formation of Alimentary Canal and Hatching of Larva.
Clavelina and Ciona .
METAMORPHOSIS OF CIONA INTESTINALIS . ... »
Vacuolization of the Notochord. . .... .
Mesenchyme and Body-cavity
Przeoral Body-cavity and Preeoral Lobe
Body-cavity of an Ascidian and Ccelom of Amphioxus
Fixation of the Ascidian Larva
Reopening of Neuropore; Degeneration of Cerebral Vesicle;
Formation of Definitive Ganglion ‘
Primary Topographical Relations and Change of Axis
Formation of Additional Branchial Stigmata
First Appearance of Musculature
Alimentary Canal and Pyloric Gland
Appendicularia A 0
Abbreviated ane O Okan. 56 5 5 6 6 6
NoTEs
X1V CONTENTS.
V. THE PROTOCHORDATA IN THEIR RELATION TO THE
PROBLEM OF VERTEBRATE DESCENT
BALANOGLOSSUS .
External Features.
Nervous System and Gonads
Metamerism
Body-cavities; Proboscis-pore; Collar-pores
Alimentary Canal .
Development; the Tornaria Larva .
The Larva of Asterias Vulgaris; Water-pores and Przoral
Lobe
Apical Plate of Vornaria
Metamorphosis of Tornaria
The Nemertines
CEPHALODISCUS AND RHABDOPLEURA
THE PRAORAL LOBE OF ECHINODERM LARVE .
THE PR4ORAL LOBE OF THE PROTOCHORDATES
Anterior and Posterior Neurenteric Canals, and the Position of
the Mouth in the Protochordates .
THE PR#ORAL LOBE IN THE CRANIATE VERTEBRATES
THE MOUTH OF THE CRANIATE VERTEBRATES
SIGNIFICANCE OF THE HypopHysIS CEREBRI .
The Ascidian Hypophysis .
CONCLUSION
NOTES
INEPERENGES: s@fio! a) goteeul sy gears biti ee aca oe oe
INDEX
PAGE
INTRODUCTION:
Tue first zodlogist to put forward, in a definite manner,
the view of the existence of a direct relationship between
Vertebrates and Invertebrates was the celebrated ETIENNE
GEOFFROY SAINT-HILAIRE.
It would appear that without any previous zoological
training, having been brought up as a botanist and
mineralogist, he was appointed Professor of Vertebrate
Zodlogy at the Museum of the Jardin des Plantes in the
year 1793, being then twenty-one years old. His col-
league as Professor of Invertebrate Zoology was the no
less distinguished Lamarck.
Saint-Hilaire’s study of the comparative anatomy and
osteology of the different groups of Vertebrates — Fishes,
Amphibians, Reptiles, Birds, and Mammals — impressed
him strongly with the conviction that, in spite of the
many obvious contrasts existing between these animals,
they are nevertheless essentially constructed upon the
same plan, the same parts recurring in all the groups
under a more or less altered form. Moreover, such
observations as, for example, that the bones of a fish’s
skull can be more readily compared with the bones of an
embryonic mammalian skull than with those of the adult,
and that the bones of a bird’s skull are separated in the
young by sutures just as they are in the skull of a
mammal, led him to frame his three great principles in
20
2 INTRODUCTION.
terms of which the phenomena of animal organisation
were to be, to a certain extent, explained.
The three principles of Saint-Hilaire, each of which
contains a large element of truth, were the following : —
1. The Theory of Analogues, according to which the
same parts occur, in various grades of form and develop-
ment, in all animals.
2. The Principle of Connexions (Le principe des con-
nexions), according to which the same parts always tend
to occur in similar topographical relations.
3. The Principle of the Correlation of Organs (Le
principe du balancement des organes), according to which,
ceteris paribus, the bulk of the animal body remains in
a measure the same, and any given organ can only become
enlarged or reduced according as another organ becomes
reduced or enlarged.
Having established these principles in his own mind
from the exclusive study of the Vertebrates, the thought
next occurred to him that probably they were capable of
equal application to the rest of the animal kingdom, and
he therefore undertook the task of identifying in the
Insects the typical structural peculiarities of the Verte-
brates.
According to his theory he would expect to find in the
Insects, in some form or other, the same organs that
occur in the Vertebrates. At the outset he was, as his
successors have since been, confronted by the palpable
fact that, while the longitudinal nerve-cord of the Insects
lies next to the ventral surface of the body, the spinal
cord of the Vertebrates lies below the dorsal surface.
Accordingly he came to the conclusion which has since
been strongly advocated by the upholders of the so-called
« Annelid-theory,” that the “back” and “belly” of an
INTRODUCTION. 3
animal were gross conceptions of the ignorant and had
no morphological meaning. These expressions merely indi-
cated the position which an animal assumed in locomotion
relative to the earth, and were in this sense convertible
terms, since many invertebrate animals prefer to swim on
their “backs,” while some fishes also do the same, others
again (flat-fishes, Pleuronectidz) swimming on their sides.
The surfaces of the body in the respective groups having
been thus reconciled, Saint-Hilaire proceeded to a detailed
comparison between an insect anda vertebrate. The chiti-
nous rings of an insect represent the vertebrz of the higher
animals. The viscera of an insect are thus enclosed within
its vertebral column, and this condition is compared with
what is found in turtles and tortoises where the carapace is
fused with the vertebral column. It was necessary to con-
clude, and Saint-Hilaire did not hesitate to do so, that the
legs of insects were equivalent to the ribs of Vertebrates.
It was not the intention of Saint-Hilaire to speculate
concerning the ancestry of the Vertebrates, for this would
have been impossible at the period in which he did his
work, but he merely wished to demonstrate the truth of
his principle of the unity of the plan of composition of the
animal body. He had therefore no reason to be satisfied
with having shown, as he believed, how the Insects could
‘be regarded as possessing a structure essentially similar to
that of the Vertebrates, but he had next to show how his
principle could be applied to other groups, above all to the
group of the Cephalopod Molluscs (squids, cuttle-fish, etc.).
This happened in the year 1830, and it precipitated the
celebrated and somewhat bitter dispute between the great
Cuvier and Saint-Hilaire with regard to the question of
“types.” While Saint-Hilaire only recognised one uni-
versal type, Cuvier arranged the different groups of animals
4 INTRODUCTION.
under four entirely distinct types; namely, Vertebrata,
Mollusca, Articulata, and Radiata. Cuvier’s system of
classification remained in use for many years; in fact, until
the progress of knowledge necessitated the adoption of a
better one.
For the first time, in 1864, the attempt was made by
Lrypic to grapple with the problem of the origin of the
Vertebrates in the light of Darwin’s Theory of Evolution
(1858). Singular to say, although Leydig approached the
subject from an entirely different point of view from that
of Saint-Hilaire, yet he also attempted to find points of
affinity between the highest Insects and the Vertebrates,
and to identify the various subdivisions of the Vertebrate
brain in the brain of the bee.
Leydig and all those later authors who would derive the
Vertebrates from an articulate ancestor, have started out
with the a priori conviction that the segmentation of the
body (metamerism) which is such a prominent feature (at
least with regard to the musculature and skeleton) in
fishes, and can be traced throughout the vertebrate series,
especially in the embryonic stages, is morphologically
identical with the familiar annulation or segmentation of
the Articulates (Annelids, Arthropods).
This is obviously a very natural assumption to make, but
there is a large mass of facts which run counter to it, some
of which will be referred to in the following pages.
An unexpected light was thrown upon the problem of
Vertebrate descent in 1866, when the Russian naturalist
KowaLevsky published an account of his researches on
the embryology of Amphioxus and the Ascidians.
The Ascidians or Tunicates form a curious and in some
respects well-defined group of animals, which used to be
generally regarded as a subdivision of the Mollusca and as
INTRODUCTION. 5
being closely related to the section of the bivalves or
Lamellibranchiata. Kowalevsky, however, discovered that
their embryonic development takes place on a plan so
similar to that of Amphioxus as almost to amount to an
identity. The development of the nervous and respiratory
systems, and of the axial skeleton or notochord in the
Ascidian embryo, as determined by Kowalevsky, showed
in the clearest manner that the relationship of the Ascidians
to Amphioxus, and through the latter to the Vertebrates,
was an extraordinarily close one.
Kowalevsky’s discovery of the chordate or sub-vertebrate
character of the Ascidian larva, was considered by HAECKEL
as affording a direct solution of the problem of the con-
necting link between Vertebrates and Invertebrates. This
was a somewhat extreme view to take of the matter, since
Kowalevsky showed that the Ascidians could no longer be
regarded as true Invertebrates.
In 1875 the foundation of the Annelid theory of
Vertebrate descent was laid independently by SEMPER and
Dourn; and Kowalevsky’s observations were explained
away in favour of the new line of speculation. It was the
discovery of the segmental origin of the excretory tubules
of the Selachian (shark) kidney, made independently and
simultaneously by SEMPER and BaLrour, which may be
said to have led to the definite framing of the Annelid
theory.
Dohrn approached the subject from a different point of
view. According to him, not only were the Vertebrates
not descended from forms allied to the Ascidians and
Amphioxus, but the latter were, by a process of almost
infinite degeneration, derived or degenerated from the
former.
That the Ascidians are degenerate animals, to the
6 INTRODUCTION.
extent that they have become adapted to a fixed habit of
life, is of course obvious; but that they have phyloge-
netically undergone the immeasurable degeneration which
was postulated by Dohrn, is a view which is entirely
unjustified by facts. We shall now proceed to a presen-
tation of some of these facts, devoting the first two
chapters to the anatomy of Amphioxus, the third to the
development of Amphioxus, the fourth to a brief sketch of
the structure and development of the typical Ascidians, and
the fifth to a consideration of the more abstruse relation-
ships of the lower Vertebrates or Protochordates.
The following classification of the forms more particu-
larly dealt with may be of service : —
Group. — PROTOCHORDATA.
Division 1. HemicHorpa (Balanoglossus, Cephalodiscus,
and Rhabdopleura. See Chap. V.).
Division 2. Urocuorpa (Ascidians).
Division 3. CEPHALOCHORDA (Amphioxus).
ANATOMY “OF AMPHIOXUS.
HISTORICAL.
THE historical progress of our knowledge of Amphioxus
has often been told, but for the sake of completeness it
may be well to sketch its main outlines once more.
It is interesting as being one of the few animals that
were not known to Aristotle, having been described and
figured for the first time in 1778 by the German zodlogist
PETER Srmon Patras. Pallas based his description on
a specimen preserved in spirit, which had been sent to
him from the coast of Cornwall; and as he confined him-
self to the examination of the external form, he made
what may appear to us the somewhat gross error of re-
garding it as a Mollusc, a species of slug, and he accord-
ingly named it Lzmax lanceolatus. He gives a perfectly
recognisable figure of it, but was led astray by its flattened
and pleated ventral surface, which might be construed
into bearing a faint resemblance to a Molluscan “ foot.”
This not very extensive knowledge of Amphioxus served
the zodlogical world for nearly sixty years, until, in 1834,
it was discovered for the second time in the Mediterra-
nean, by the Italian naturalist, GABRIEL Costa. Costa
found it on the shores of Posilippo, in the Gulf of Naples,
and was the first to make observations on the living ani-
mal and to recognise its true nature. He thought at first
¥/
8 ANATOMY OF AMPHIOXUS.
that he had absolutely discovered it, but subsequently came
across Pallas’s description. He showed that it was a fish
allied to the Cyclostomata, a group which includes the
lampreys and hag-fishes.
In his account of its habits he pointed out how sensitive
it was to light, and although without apparent eyes, yet the
light stimulated it to such an extent that it could by no
means tolerate it. Costa mistook the curious tentacle-like
processes or cirri, which form a circlet round the mouth
(see Fig. 1, p. 12), for respiratory filaments or branchiz,
which suggested to him the name of Branchiostoma for the
genus, the specific name given by him being J/udbricum,
referring to the way in which it slips through the fingers
with the rapidity of an electric spark when touched.
WILLIAM YARRELL, in his History of British Fishes
(1836), was the next to describe the remarkable creature
and to give it the name Amphioxus, by which it has become
so well known and which refers to the fact that it is pointed
at both ends. Yarrell was also the first to describe the
notochord or chorda dorsalis of Amphioxus as a cartilagi-
nous vertebral column.
Subsequently other observers had taken specimens of
Amphioxus from various points, notably from the coast of
Sweden, so that the attention of morphologists was at
last definitely directed to the interesting form, and in
1841 there were produced three independent memoirs on
the anatomy of Amphioxus, which laid the foundation
of our present knowledge. The authors of these memoirs
were JOHN Goopsir of Edinburgh, HEInrIcH RATHKE of
Konigsberg, and JOHANNES MULLER of Berlin. The work
of the last-named author is a masterpiece. With regard
to the systematic position of Amphioxus, the outcome of
all these researches was, that it was allied to the Cyclo-
HABITS AND DISTRIBUTION. 9
stomata, but,as Johannes Miiller put it, differed from them
to a greater extent than a fish differs from an Amphibian.
HABITS AND DISTRIBUTION.
In consequence of the extension of the firm, and at the
same time elastic, notochord to the tip of the snout,
Amphioxus possesses an extraordinary capacity for bur-
rowing in the sand of the sea-shore or sea-bottom. If an
individual be dropped from the hand on to a mound of
wet sand which has just been dredged out of the water,
it will burrow its way to the lowest depths of the sand-
hillock in the twinkling of an eye.
The frontispiece is designed to illustrate the chief
positions in which Amphioxus may be observed. It is
represented swimming, lying on the sand, and buried in
the sand.
Its usual modus vivendi is to bury the whole of its
body in the sand, leaving only the mouth with the ex-
panded buccal cirri protruding. When obtained in this
position in a glass jar a constant inflowing current of
water in which food-particles are involved can be ob-
served in the neighbourhood of the upstanding mouths.
The food consists almost entirely of microscopic plants
(Diatoms, Desmids, etc.) and vegetable débrzs.
While passing through the pharynx the food becomes
involved in the slimy secretion of a gland at the base of
the pharynx known as the endostyle or hypobranchial
groove (cf. Figs. 2 and 3), and is thus held in the pharynx
while the water with which it entered flows out through
the gill-slits into the atrial chamber. The food is then
carried through the intestine enveloped in a continuous
cord of slime or mucus, which is kept in perpetual motion
IO ANATOMY OF AMPHIOXUS.
and rotation by the action of. the cilia with which the
epithelium of the alimentary canal is richly provided.
After the digestible elements in the food have been dis-
solved in the secretions of the intestinal wall the cord of
slime with the attached fzeces is duly ejected.? *
The extreme shyness to a bright or sudden light which,
as Costa observed, is manifested by Amphioxus, is prob-
ably correlated with the presence of black pigment spots
in the nerve-cord. If a lighted candle is carried into a
dark room in which Amphioxus are being kept in glass
jars, the excitement produced among the small fish is
indescribable.
Occasionally it emerges from its favourite position in
the sand, and after swimming about for some time it will
sink to the bottom, and there recline for a longer or
shorter period upon its side on the surface of the sand.
When resting on the sand, it is unable to maintain its
equilibrium in the same position as an ordinary fish would
do, but invariably topples over on its side, indifferently on
the right or left side.2 In the higher fishes, including the
_lampreys, there is a special apparatus for controlling the
equilibrium ; namely, the semicircular canals of the ear.
There is nothing of the kind in Amphioxus, but in the
Ascidian larva and in the Appendiculariz there is, as
we shall see, a structure situated in the floor of the brain
known as the ofo/zth, which possibly exercises an equilib-
rating influence.
From what has been said above it follows that Amphi-
oxus is an entirely passive feeder; it does nothing in the
way of biting, or even sucking, and has not to search far
for its food, but merely takes what is brought in with the
* This number and others which are scattered through the text refer to the
Notes at the ends of the chapters.
HABITS AND DISTRIBUTION. II
water which is drawn into the mouth by the powerful
ciliary action of the cells lining the roof of the mouth and
the wall of the pharynx.
Speaking generally, Amphioxus is an inhabitant of
shallow water; it is essentially a littoral form, and is apt
to occur in the neighbourhood of any sandy shore. Its
occurrence, however, is often curiously local, as shown by
its behaviour at Messina. In the vicinity of Messina
there are a couple of rather extensive salt-water pools, at
some points of considerable depth, which, in the course of
ages, have apparently been shut off from the adjacent sea
by the formation of sandbanks. In the more northerly of
these small lakes, lying almost at the extreme north-
eastern point of Sicily, Amphioxus occurs in astonishing
abundance; while in the more southerly lake, which is
connected with the former by a narrow artificial canal, it
is entirely absent. Both of these lakes communicate
by narrow outlets with the Straits of Messina, where,
however, Amphioxus is somewhat rarely met with. In
the Gulf of Naples it is extremely abundant; while in
Plymouth Sound, in the English Channel, it is compara-
tively rare. On the coast of France it is said to grow to
an unusually large size. It has been taken in greater or
less numbers from many other localities in Europe, on
the Atlantic and Pacific shores of North and South
America, and from the shores of Australia, Japan, and
Ceylon. Its geographical distribution may therefore be
said to be pre-eminently world-wide, and, in fact, it is
liable to turn up on any shore in the temperate and
tropical regions. And yet with all this world-wide distri-
bution there is only a single genus, with some eight
species, the different species being remarkably alike,
differing slightly in the height of the dorsal fin and in
[2 ANATOMY OF AMPHIOXUS.
the number of muscle-segments, the latter forming one
of the chief diagnostic characters for a given species.
The extensive geographical distribution of Amphioxus,
combined with the fact that it is a shore-dweller and not
a roving pelagic animal, and also with its remarkably
constant features and, as a rule, trifling specific differ-
ences, shows that we have to do with an extremely
archaic form.
EXTERNAL FORM.
A good idea of the external appearance an _ propor-
tions of Amphiorus lanceolatus can be obtained from the
accompanying figure (Fig. 1). Its actual length varies
Fig. 1.— Amphioxus Lanceolatus from the left side, about twice natural size.
(After LANKESTER.) _ The gonadic pouches are seen by transparency through the
body-wall; the atrium is expanded so that its floor projects below the metapleural
fold; the fin-chambers of the ventral fin are indicated between atriopore and anus.
The dark spot at the base of the fifty-second myotome represents the anus.
from about four to as much as eight centimetres. In
the fresh condition it is semi-transparent, so that some
of the internal organs can be seen through the skin, which
is often iridescent.
The figure shows the pointed extremities of the body
and the circlet of tentacles or duccal cirrt round the mar-
gin of the mouth, or more accurately, the oval hood,
because the mouth proper is covered over by a hood-like
fold of the integument, from the margin of which these
processes grow out. Extending from near the anterior
extremity of the body to the posterior end are seen some
sixty-two oblique parallel lines, each bent upon itself in
EXTERNAL FORM. 13
such a way as to form two sides of a triangle, the apex
of which is directed forwards. These are the partitions
or septa which divide the longitudinal muscles of the
body into a series of separate muscle-chambers or *zyo-
tomes. In virtue of the longitudinal muscles being broken
up, so to speak, into a great number of segments, the
animal is enabled to swim rapidly with a_ serpentine
motion. In the remarkable pelagic animal, Sagztfa, where
the muscles are not segmented, this motion is impossible,
and instead, it darts forward by sudden and spasmodic
jerkings of its tail.
In Amphioxus, the tail or post-anal region of the body
is very much reduced, and the muscle-segments of the
trunk therefore constitute its only means of locomotion,
there being no muscular fins. Beyond the muscle-plates,
both in front and behind, the zo¢ochord, which forms the
_axtal skeleton of the body, is seen to extend to the anterior
and posterior extremities. The extension of the notochord
beyond the anterior limit of the dorsal nerve-tube is a very
exceptional condition, and has led to the creation of a
special order for the reception of Amphioxus; namely, the
Cephalochorda.
The oval structures seen lying below the muscle-plates
in Fig. 1 are the reproductive organs, male or female as
the case may be. Instead of being represented by a single
genital gland on each side of the body as they are in the
higher fishes and Vertebrates generally, they consist here
of some twenty-six pairs of perfectly distinct chambers,
occurring in correspondence with the muscle-segments or
myotomes of the region to which they belong, and extend-
ing from the tenth to the thirty-fifth myotome inclusive.
These chambers are known as the gouadic pouches. (See
Fae. 2.)
14 ANATOMY OF AMPHIOXUS.
About two-thirds of the way from the front end of the
body there is a comparatively large aperture in the mid-
ventral line. It is the excurrent orifice of a spacious
cavity which surrounds to a large extent the internal
organs, including above all the pharynx, and is known as
the atrial chamber, or simply atrium, while its opening to
the exterior is the atriopore.
The anus or outlet of the digestive tract occurs near the
posterior end of the body; it does not he in the mid-
ventral line, but high up on the left side. At its first
appearance in the young embryo, the anus does lie ap-
proximately in the mid-ventral line (cf. Fig. 64, p. 117),
but as soon as the caudal fin begins to develop, it is pushed
on to one side, always the left, and so attains its final
position. A similar displacement of the cloacal aperture
occurs in the Dipnoan fish Protopterus, where, however,
the direction of displacement is not constant, the aperture
lying now to the right, now to the left, of the middle line.
Again, in the tadpoles of certain Batrachians the cloacal
aperture is displaced to the right of the middle line.* (Cf.
Fig. 8.) The fact of the displacement of openings by the
* The asymmetrical position of the cloacal aperture of certain Batrachian
tadpoles has been systematically worked out by BOULENGER. In tadpoles
of the genera Rana and /Hy/a, the cloacal aperture is dextral, while in the
Toads and Pelobatoids it is median. (See G. A. BOULENGER, A Synopsis
of the Tadpoles of the European Batrachians. Proc. Zool. Soc. London,
1891. pp. 593-627. Plates 45-47.)
In Rana the cloacal aperture may occasionally occur in a median position
as a variation. (WILLEY, (Vole on the position of the cloacal aperture in
certain Batrachian tadpoles. Transactions New York Acad. of Sciences, Vol.
XII. 1893. pp. 242-245.) My attention to the previous literature on this
subject was kindly drawn by Mr. G. A. Boulenger.
Since writing the above my attention has been called to the following
paper by Professor Burr G. WILDER, Lateral Position of the Vent in Am-
phioxus [Branchiostoma] and in the Larve of Rana Pipiens [Catesbiana].
Proc. Amer. Assoc. Adv. Sc. XXII. 1873. pp. 275-300.
EXTERNAL FORM.
differential growth of neighbouring structures is a very -
ous one, and should be borne in mind. It will havea specia
significance when we come to consider the development.
There are no paired muscular fins in Amphioxus, but
running along the whole length of the back is a median
ridge which is called the dorsal fin. It extends round the
front end of the body, where it becomes continuous with
the right half of the oral hood. (Cf. Fig. 9.) Posteriorly
it becomes enlarged to form the tail expansion or caudal
jiu, and is continued round the hinder extremity of the
body past the anus as far as the atriopore. Along the
back, this continuous fin is supported by a series of gelat-
inous fiz-rays, each of which lies in a chamber of its own.
The fin-rays, whose number may exceed 250, do not extend
to the extreme anterior and posterior ends of the body.
The ventral portion of the fin in the region between atrio-
pore and anus is supported by a similar series of fin-rays,
but there are two of them placed side by side in each com-
partment. In other words, the fin-rays of the ventral fin
are paired.
Amphioxus, like most fishes, is laterally compressed so
that a transverse section through the body in front of
the atriopore is found to have the form of an equal-sided
spherical triangle, the base of which consists of the floor
of the atrial chamber. At each of the basal angles of
the triangle there is a fold of the integument containing
a cavity (Fig. 2). This is the metapleural fold) which
stretches on each side of the body from the region of
the mouth to slightly beyond the atriopore. (Cf. Fig. 1.)
The cavity in the folds is the metapleural lymph-space.
The apex of the triangular cross-section is formed by
one of the dorsal fin-chambers enclosing a lymph-space
into which a fin-ray is projecting.
ANATOMY OF AMPHIOXUS.
Fig. 2. — Diagrammatic transverse section through pharyngeal region of female
Amphioxus. (After LANKESTER and BOVERI, from R. Hertwig’s Lehrbuch d.
Zoologie.)
at. Atrial cavity. c. Dorsal coelom, separated from atrial cavity by the double-
layered membrane known as the ligamentum denticulatum. c#. Notochord.
dn. Dorsal spinal nerve. e. Endostyle, below which is the endostylar coelom con-
taining the branchial artery. / Fin-ray of dorsal fin. . Gonadic pouch contain-
ing ova. 4.v. Hepatic vein lying in the narrow coelomic space which surrounds
Z, the liver or hepatic coecum. Za. Left aorta separated from the right aorta by the
hyperpharyngeal (epibranchial) groove. /y. Lymph-space. mj. Metapleur.
my. Longitudinal muscles of myotomes; over against the dorsal ccoelom these
muscles are arranged vertically, and form the rectus abdominis of Schneider.
z.t. Spinal cord. 7. Pharynx. ». Excretory tubule. ¢. Transverse or subatrial
muscles. w.7. Ventral (motor) spinal nerve, the fibres of which have the appear-
ance of passing directly into the muscle-fibres.
N.B. The connective tissue (cutis, notochordal sheath, coelomic epithelium,
etc.) is indicated by the black lines
EXTERNAL FORM. 17/,
In young transparent individuals, such as that of which
the anterior portion is represented in Fig. 3, the pharynx,
or first division of the digestive tract, into which the
mouth leads directly, can be seen through the body-wall,
and it is found to be perforated on each side by a great
number of elongated vertical slits, whose number varies
with the age of the individual, but may eventually attain
the astonishing figure of 180 pairs. They are the g2//-
clefts opening from the pharynx into the atrial chamber.
In the hving Amphioxus an almost continuous stream of
water is being drawn through the mouth into the pharynx
for purposes of respiration and nourishment, then pass-
ing out of the pharynx, by way of the gill-clefts, into
the atrial chamber and thence to the exterior through the
atriopore.
Cranium and Sense-organs.
Besides lacking differentiated lateral fins, Amphioxus
differs fundamentally from the higher Vertebrates in the
absence of a cranium, of paired eyes, and paired or un-
paired auditory organs.
On account of the absence of a cartilaginous cranium
it has been placed by itself in a separate division, the
Acranta, in contrast to all the other Vertebrates proper,
from the Cyclostomata upwards, which all possess a
cranium of one sort or another and are hence known as
the craniate Vertebrates or Craniota. In Amphioxus the
only cartilage in the head-region consists of a ring lying
round the margin of the oral hood at the base of the
buccal cirri. It is formed of separate pieces correspond*
ing to the number of the cirri, and each piece sends up a
process into its adjacent cirrus, so that the latter is pro-
vided with a stiff skeletal axis (Figs. 3 and 4). These are
18 ANATOMY OF AMPHIOXUS.
the buccal cartilages. As pointed out by Johannes Miller,
they are not to be compared with the jaw-apparatus, nor
Fig. 3. — Anterior portion of body of young
transparent individual. (After J. MULLER,
slightly altered.)
ch, Notochord. cz. Buccal cirri. e. Eye-
spot. evd. Endostyle. 7. Fin-rays lying in
the fin-chambers. gs. Gill-slits; the skeletal
rods of the gill-bars are indicated by black lines.
nt. Spinal cord, with pigment granules near its
base. 7.a. Downgrowth from right aorta lying
to the right of ved. the velum; with velar ten-
tacles projecting back into pharynx. w.o. Rad-
erorgan; ciliated epithelial tracts on inner
surface of oral hood.
to the hyoid or tongue-
bone of the jaw-bearing
Vertebrates, but they
belong to the same cate-
gory as the mouth-carti-
lages of the Cyclostome
fishes (which possess a
hyoid cartilage in addi-
tion) and the /adzal car-
tilages of Selachians
(sharks).
The absence of paired
eyes and of any kind of
auditory organ has been
mentioned above. There
is, however, a median
eye, which consists of a
comparatively large un-
paired pigment spot lying at the anterior extremity of the
dorsal nerve-tube.* A row of
similar, but much smaller,
masses of pigment lie along
the floor of the spinal canal,
commencing some _ distance
behind the eye (Pig: 3):
Immediately above and be-
hind the eye-spot is a small
Fig. 4. — Buccal cartilages of Am-
phioxus. (After J. MULLER.) The
basal pieces lie end to end in the mar-
pit in the body-wall reaching gin of oral hood, and each basal piece
sends up an axial process into the
from the outer surface of the corresponding buccal cirrus.
* The eye-spot has been observed to be sometimes broken up into two
pigment masses. (See AYERS, No. 105 bibliog.)
EXTERNAL FORM.
body to the anterior wall of
the brain. This is known
as Kolliker’s olfactory pit,
The
its walls
after its discoverer.
cells which line
carry long vibratile cilia, and
it possibly subserves in some
degree an olfactory func-
tion. In the larva the cavity
of the brain opens into the
base of the olfactory pit by
a pore known as the xeuro-
pore, which we shall consider
In the adult this
pore becomes closed, but
later.
the base of the olfactory pit
appears to remain connected
with the roof of the brain
by a solid stalk. The olfac-
tory pit, like the anal open-
ing, lies asymmetrically on
the left side of the body
(Fig. 5). It is forced to one
side in the course of the
development consequent on
the formation of the fin-like
expansion of the integument
in this region, which, as we
have seen, is nothing more
than the cephalic continua-
tion of the dorsal fin.
The mouth of Amphioxus
to be well
would seem
19
Fig. 5.— Transverse section through
region of olfactory pit. (After LAN-
KESTER.)
The olfactory pit is seen as an ecto-
dermic involution on the left side in con-
tact with the wall of 4, the cerebral vesicle.
ch. Notochord. /, Lymph-space of ce-
phalic portion of dorsal fin. 7.2. and 24
Right and left portions of oral hood.
my. Muscles of first myotome; outside of
the muscles is the myoccelic lymph-space
of first myotome; inside of the muscles
is the apex of the myoccelic lymph-space
of the second myotome. 2. Cranial
nerve (second pair).
N.B.— The dotted shading represents
the thickened gelatinous connective tissue
of the head-region in which irregular
lymph-spaces occur.
20 ANATOMY OF AMPHIOXUS.
guarded against the intrusion of noxious substances.
Everything entering the mouth has to pass through a
vestibule richly provided with sensitive epithelial cells.
This vestibule consists of the oral hood with its marginal
cirri, at the back of which lies the definite oral opening or
velum, as it was called by Hux tery on account of its
resemblance to a similar structure in the young lamprey
(Ammoceetes). (Cf. Fig. 3.) In the adult the velum
carries twelve tentacles of its own, the velar tentacles,
which are not to be confused with the duccal cirri of the
oral hood. The velar tentacles project in a backward
direction freely into the pharynx.
4
A HUULUTEA TOU NITE
Ss
by
Fig. 6.— A. Portion of a buccal cirrus to show groups of sense-cells.
&. Isolated cells of the skin; two columnar sense-cells carrying a sensory hair,
and one cylindrical epidermic cell with striated cuticular border. (After LAN-
GERHANS.)
Groups of sense-cells occur on the side of the buccal
cirri at intervals (Fig. 6). Some of these cells bear a
vibratile cilium at their free ends, and others bear stiff
hairs. Both kinds of cells are mingled in the same group.
wh
EXTERNAL FORM. 21
Similar groups of sensory cells occur on the margin of the
velum and its tentacles (Fig. 7). It may be noted, in
anticipation, that the velum is derived directly from the
mouth of the larva, which
becomes secondarily hid-
den from superficial view
by the overgrowth of the
oral hood.
According to LANGER-
HANS, similar cells to
those mentioned above,
carrying stiff sensory
hairs, are scattered dif-
fusely all over the exter- Fig. '7.— Velum of Amphioxus seen from
nal surface of the body. aaa of the pharynx. (After LANKES-
(Ef Fig. 6 D5) But a v.sp. Sphincter muscle of velum. v.¢, Velar
: tentacles lying across the oral opening.
concentration of sense-
organs comparable to the /ateral line of the higher fishes .
is apparently absent.’
A remarkable structure which seems to combine the
properties of gland and sense-organ occurs on the under
surface of the oral hood. It consists of a patch of
modified epithelium drawn out into finger-shaped epi-
thelial tracts, the cells of which carry long cilia. (See
Fig. 3.) It was discovered and accurately described by
Johannes Miiller, who called it the ‘ Raderorgan”’ on ac-
count of the resemblance of its ciliary movements to those
of the wheel-apparatus of a Rotifer. The result of the
combined action of the cilia is to cause a flow of water
into the pharynx. In connection with the Raderorgan
must be mentioned a special depression forming a peculiar
sense-organ (Geschmacksorgan) lying against the right
side of the notochord, known as the groove of Hatschek.
22 ANATOMY OF AMPHIOXUS.
INTERNAL ANATOMY.
Atrial Cavity.
In making a-dissection of a frog or a fish, as soon as the
body-wall is cut through, we find ourselves groping about
in a large cavity in which the viscera lie. This is the
body-cavity or peritoneal cavity, or, again, the cwlom.
If we slit open the ventral body-wall of Amphioxus, we
discover what appears to be an exactly similar cavity. It
is, however, not the coelomic cavity, but the perzbranchial
or atrial cavity, into which the pharyngeal gill-slits open.
The older anatomists, including Johannes Miller, regarded
it as the true body-cavity, and the latter author was forced
to the conclusion that Amphioxus differed fundamentally
from all the other Vertebrates in that the gill-slits opened
into the peritoneal cavity. Although that condition of
things was hard to imagine, yet it seemed to be obviously
the case, since the reproductive organs appeared to lie in
the same cavity, and it went without saying that a cavity
containing the gonads could only be the peritoneal cavity.
In reality, the gonads do not he in this cavity; they only
project into it and lie in a space of their own which is
separated from the atrial cavity by a double-layered mem-
branes) (Ci Pigs 2;)
Hux ey threw some light on the matter in 1874, when
he compared the atrial or peripharyngeal cavity of Amphi-
oxus to the ofercular cavity which surrounds the gills of
the tadpoles of the frog and tailless Amphibia generally.
In the case of the tadpole, as is well known, there are some
four pairs of gill-slits which open at first directly to the
exterior. Subsequently an opercular fold grows backwards
over them as in fishes, but with this difference, that in the
INTERNAL ANATOMY. 23
frog-tadpole the fold of one side becomes continuous ven-
trally with that of the other, so that in effect we have one
large semicircular fold covering over the gill-slits. Event-
ually the hinder free margin of the fold undergoes con-
crescence with the body-wall, so that a single peribranchial
cavity is formed about the gills. This cavity is closed all
round except at one point, usually on the left side, but
sometimes in the mid-ventral line, where it remains open
as the porus branchialts, or so-called spzraculum.
This comparison of Hux-
ley’s was extremely well
taken, and although the two
cavities, namely, the peri-
branchial cavity of the frog-
larva and the atrial chamber
of Amphioxus, are probably
by no means homologous, or
genetically related to each
other, still the close analogy
that exists between them is
most instructive, and yet,
singular to say, it did not
lead Huxley to a correct Fig. 8.— Tadpole of Frog (Rana cla-
interpretation of the atria] 242) from ventral side. (Original.)
cl. Dextrally placed cloacal aperture.
chamber.® m, Mouth. sf. spiraculum; the dotted
line indicates the extent of the opercular
its tme nature was at) uomber., £ Pa
length established by RoLpx
in 1876. By comparing his own observations on the adult
with those of Kowalevsky on the larva, Rolph came to the
conclusion that the atrial cavity of Amphioxus originated
by the growth of two folds of the body-wall over the gill-
slits on each side, and by their subsequent fusion in the
mid-ventral line except at one point, which remained open
24 ANATOMY OF AMPHIOXUS.
as the atriopore. Although the details in the formation of
the atrium are not exactly such as they were supposed to
be by Rolph (see below), yet the end-result is virtually the
same, and his work marks a distinct advance in our knowl-
edge of the structure of Amphioxus, by showing that the
epithelium lining the walls of the atrial chamber is not
peritoneal, but is derived by a process of in-folding, from
the ectodermic covering of the surface of the body. In
other words, the atrial cavity, like the opercular cavity of
the Amphibian tadpole, is lined by ectoderm.
Viscera.
A bird’s-eye view of the internal organs, as exposed by
cutting the animal open ventrally by incisions extending
forwards and backwards from the atriopore, is shown in
Fig. 9. First and foremost, our attention is arrested by
the relatively enormous pharynx occupying more than half
the length of the body, with its right and left perforated
walls and parallel gill-bars abutting at the mid-ventral line
on the exdostyle.
The alimentary canal is seen in the dissection to have a
perfectly straight course between mouth and anus, with
no windings whatever. Growing out ventrally from what
may be termed the pyloric region of the intestine, a short
distance behind the pharynx and in front of the atriopore,
there is a large diverticulum ending blindly in front, which
in the adult lies for the greater part of its extent applied
against the right wall of the pharynx (Fig. 9). This is
the so-called hepatic cecum, corresponding to the liver of
higher forms. The permanent condition of the liver in
Amphioxus is comparable to its embryonic condition in the
Vertebrates, where it attains a much more complicated
structure in the older stages by subsequent branching and
INTERNAL ANATOMY. 25
anastomosing of the branch-
es, etc. It is essentially a
median ventral outgrowth
from the intestine, and its
lying on one side of the
pharynx in Amphioxus is
only a secondary topographi-
cal necessity.*
Attached to the
muscular body-wall on each
lateral
side are the gonadic pouches,
which project into the cavity
(Cis Eis! 23)
Their number, which is usu-
of the atrium.
ally twenty-six pairs, varies
slightly, and sometimes there
are more on one side than
on the other, as in Fig. 9.
The atrial cavity does not
end at the atriopore, but is
continued beyond it as a
blind sac lying to the right
of the intestine, and reach-
ing back nearly as far as the
~ anus. In Fig. 9 the position
of this post-atrioporal exten-
ston of the atrium is indi-
cated by means of a dotted
line.
Finally, in Fig. 9, the anus
is seen lying to the left of
eves
SSSA
eieseaaee
Fig. 9.—Amphioxus dissected from
the ventral side. (After RATHKE, slightly
altered.)
m. Entrance to mouth with the buccal
cirri lying over it. #. Pharynx. e. Endo-
style. 2 Hepatic coecum. yg. Gonadic
pouches. af. Position of atriopore; the
post-atrioporal extension of the atrium is
indicated by the dotted line passing over
to the right side of z, the intestine. az.
Anus.
N.B.— Note absence of differentiated
stomach.
* The ccecum is held in position by cord-like attachments to the ligamen-
tum denticulatum.
26 ANATOMY OF AMPHIOXUS.
the caudal fin, and the right margin of the oral hood is
shown to be continued round the front end of the body
into the cephalic expansion of the dorsal fin.
Calom.
The question now arises: if the atrial cavity is not
the true body-cavity, what has become of the latter? In
order to determine this point, it is necessary to have
recourse to transverse sections through the body, such as
the one represented in Fig. 2, which is taken through the
middle of the pharyngeal region. In a section like this,
the work of tracing the limits of the atrial cavity is often
greatly facilitated by the presence of a rich brown pigment
in the epithelium lining its walls. We find, accordingly,
that the atrial cavity has extended itself at the expense of
the ccelom, and has reduced the latter, in the main, toa
small space on either side of the dorsal aorta, the aorta
being double in this region (Fig. 2). This portion of
the ccelom is sometimes spoken of as the supra-pharyngeal
celom, and sometimes as the sabchordal celom, since it lies
dorsal to the pharynx on the one hand, and below the noto-
chord on the other. Other fragments, so to speak, of the
ccelom are found accompanying some of the branchial bars,
namely, every alternate one; and another portion occurs
below the endostyle. (See Fig. 13.) The hepatic coecum
is also surrounded by a division of the ccelom, but its
cavity is reduced to a minimum, and the same applies to
the ccelom surrounding the intestine immediately behind
the pharynx. Behind the atriopore, as we have seen, the
atrial cavity is confined to the right side, so that on the
left side of the intestine in this region the ccelom presents
its original proportions.
INTERNAL ANATOMY. 27
Structure of Pharynx.
We have already had occasion to mention the fact that
the wall of the pharynx on each side is perforated by a
great number of vertically elongated slit-like apertures - -
the gill-clefts. In the middle region of the pharynx the
gill-slits stretch almost from the roof to the base of tic
pharynx, but in front and behind they gradually become
much lower in vertical height (Fig. 10). In the fully
7h
mney) in
/
uitin i Uf
hides
“TTR
LL
iz
LL TE perinds
/\ AAA MALT ARRAL
Fig. 10.— Anterior portion of right wall of pharynx, to show arrangement of
skeletal rods. (After J. MULLER.)
e. Endostyle. e.c. Endostylar ccelom. #.6. Skeletal rod of primary gill-bar.
7.6. Skeletal rod of tongue-bar. sy. Cross-bars or synapticula.
N.B.—A simple gill-slit undivided by a tongue-bar should have been inserted
in the figure in front of the first double slit. J. Miiller failed to observe this.
expanded condition the gill-slits are nearly vertical, as in
Fig. 10, but by the contraction of the transverse muscles,
which lie in the floor of the atrium, they are often found
to be directed very obliquely backwards, and this is the
condition in which they almost invariably occur in pre-
served specimens. That is the reason why so many of
the bars are involved in a single transverse section. (Cf.
Fig. 2.) On account of the prodigious extent to which
28 ANATOMY OF AMPHIOXUS.
the pharynx is perforated by the gill-clefts, it is necessary
for it to have some sort of skeletal support to prevent it
from collapsing. This is effected by a series of stiff gelat-
inous rods which lie in the walls bounding the gill-clefts.
These rods have the consistency of chitin, —the material
that forms the exoskeleton of insects,—and are insoluble
in caustic potash. The portion of the pharyngeal wall
which lies between any two gill-slits is called a g7//-bar.
It will be seen at once in Fig. 10 that there are two
kinds of skeletal rods differing in the behaviour of their
lower extremities. Dorsally the rods arch over into one
another, but ventrally they are independent, and every
alternate rod is bifurcated, while the somewhat shorter
intermediate rods end plainly. The forked rods form the
skeletal support of the premary gill-bars, while the inter-
mediate simple rods support the secondary gill-bars, or
tongue-bars, as they are usually called. The primary bars
constitute the walls of the primary gill-clefts. The latter,
at their first origin, appear as simple oval openings in
the wall of the pharynx. Later on the simple opening
becomes divided into two by the gradual dipping down-
wards of its dorsal margin until it meets and fuses with
the ventral margin. In this way is the tongue-bar formed
and the gill-slit doubled. (Cf. Fig. 11.) The statement
which was made above, therefore, that there could be as
many as 180 openings on each side of the pharynx, signified
that there might be some ninety pairs of primary gill-clefts.
Eventually the gill-slits become still further subdivided,
though not so obviously, by the formation of small cvoss-
bars which pass over from one primary bar to another,
skipping over the tongue-bar, although eventually fusing
with the skeletal axis of the latter on their inner faces
(Fig. 10).
INTERNAL ANATOMY. 29
Evolution of the Thymus Gland.
Tongue-bars, like those occurring in the gill-slits of
Ampbhioxus, are only known otherwise to occur in the
remarkable worm-like creature, La/anoglossus. In the
higher Vertebrates they appear to be entirely absent, but
in the course of the development of the higher forms
there is a structure which arises from the dorsal wall
of the gill-slits which may very well be the homologue
of the tongue-bars of Amphioxus. This structure is the
Tee vel phb nee cae nt
aut
vs
“|
Ue Ta irr
=
ci end tb met at hep
Fig. rz. — Anterior region of young Amphioxus from left side. (After WILLEY;
the renal tubules inserted after BOVERI.)
at. Atrium, cz. Buccal cirri. ch. Notochord. d@.f Dorsal fin-chambers, e. Eye-
spot. ewvd. Endostyle. ef. Outgrowing coecum; the index line passes through
one of J. Miiller’s renal papillae. set. Metapleural fold. 2. Nephridia or renal
tubules. z¢. Spinal cord. o/f Olfactory pit. %.4. Peripharyngeal ciliated band.
Zé. Tongue-bars. ve/. Velum.
thymus gland. The thymus is one of those enigmatical
ductless glands which are so eminently characteristic of
the Vertebrate organisation, and are of the utmost phys-
iological and pathological importance to the individual.
In their structure and development they give clear indi-
cations of having undergone an extensive change of
function in the course of their evolution.
The thymus, therefore, is presumably the derivative of
an ancestral organ, which formerly possessed an active
function as opposed to the apparently passive function
which this gland, and others like it, exercise in the exist-
30 ANATOMY OF AMPHIOXUS.
ing Craniota. Amphioxus has hitherto been regarded
as forming a marked exception among thr Vertebrates
in having no thymus, whereas one might reasonably have
expected to find here the representative of the thymus
in full activity. Although contrary to the prevailing
impression, I would suggest that the thymus is repre-
sented in Amphioxus by the very actively functional
tongue-bars.
Do..2N has shown that in the Selachian (shark)
embryo the thymus arises by a series of distinct cell-
proliferations from the epithelium of the dorsal wall of
the successive gill-slits with
the exception ‘of ‘the: first,
which is the spiracle (Fig.
12). Sometimes these pro-
liferations cause a small pro-
jection downwards into the
gill-slit, comparable to an
incipient tongue-bar. Event-
ually these separate thymus
rudiments pass inwards and
come together so as to form
the definite thymus gland.
Dohrn concluded from its
Fig. 12.— Horizontal section through mode of origin that the
the branchial region of an embryo of | ited i
Scyllium canicula to show the rudiments t nymus resu te rom the
of the thymus. (After DOHRN.) metamorphosis and _intro-
sp. Spiracle. cav. Cavity (coelom) of . ;
branchial bar. I, II, III. First, second, version of gill-filaments; and
and third gill-pouches. jwg.v. Jugular
vein. ¢fy. Thymus rudiments. in point of fact, this view of
its morphological nature is
probably correct. But the tongue-bars of Amphioxus,
which correspond closely in position to the thymus rudi-
ments in the Selachian embryo, and are, like the latter,
INTERNAL ANATOMY. 31
essentially epithelial structures, are nothing else than gill-
filaments or gill-lamellz. It appears, therefore, that we
are justified in supposing that the tongue-bars of Amphi-
oxus are the functionally active organs, of which the thymus
of the higher forms is a metamorphosed derivative.
Endostyle.
Returning, then, to the consideration of the more inti-
mate structure of the pharynx, —the endostyle hag been
already mentioned as a ven-
tral groove of the pharynx
accompanying the latter
throughout its whole length.
A transverse section of it
alone is shown in Fig. 13.
It is composed of very high
columnar cells arranged
throughout in one layer, al-
though the tenuity of the
cells, whose nuclei are often
placed at different levels,
gives rise to the impression, Fi, 33.7 Transverse section through
of cells occurring in several] KESTER, slightly altered.) —
e.a. Branchial artery with blood-clot.
layers. The four groups of ec. Endostylar ccelom. s&. Skeletal plate.
gland-cells, placed symmet-
rically two on either side of the median line, are the
distinguishing feature of the endostyle. The cells are
all ciliated, but those in the middle line bear a bunch of
specially long cilia, which are of great importance in
putting in motion the cord of mucus secreted by the
glandular cells of the endostyle. Below the endostyle, there
is a well-defined portion of the true body-cavity in which
the branchial artery lies. This is the exdostylar celom.
32 ANATOMY OF AMPHIOXUS.
Besides the rods in the gill-bars, there is a series of
paired skeletal plates lying immediately below the endo-
stylar epithelium (Fig. 13). These plates correspond in
number to the primary gill-slits. Their shape and arrange-
ment are shown in Fig. 14. They slightly overlap each
other, and _ alternate
with one another just
as the primary gill-slits
alternate. This alter-
nation of paired struc-
tures is of very general
occurrence in Amphi-
oxus, andaffects almost
every system of organs,
—such as muscular,
Fig. 14. — Lower portions of skeletal rods of neryous reproductive
pharynx with three pairs of endostylar plates, : ;
seen from above. (After SPENGEL.) and branchial systems.
The substance of the skeletal rods passes into I b fared
that of the endostylar plates (e.g), thus producing t May be stated as a
an arcade like the cover of a shoe (Spengel). general rule, to which
sy. Cross-bars (synapticula).
there are some excep-
tions, that with regard to the paired organs of Amphioxus,
the organs of one side (e.g. myotomes, primary gill-slits,
gonads, spinal nerves) do not lie opposite to their aztzmeres
on the other side, but alternate with them.
Branchial Bars.
The structure of the branchial bars is shown in section
in Fig. 15. Both kinds of bars, primary and secondary,
have the same general appearance, being compressed and
band-like, but the secondary bar is the smaller of the two.
The chief point of difference between them is, that in
the primary bar a portion of the coelom is involved, which
is absent in the secondary bar. In the case of the primary
INTERNAL ANATOMY. 33
bar (Fig. 15 B), commencing from the outside, that is to
say, from the edge turned towards the atrial cavity, we
have first a patch of columnar atrial] epithelium, at the cor-
ners of which some of the cells contain a quantity of the
rich brown pigment which has been referred to above as
being characteristic of the atrial epithelium generally.
NY
Fig. 15, 4 and 2.— Transverse sections through primary (2) and secondary
(A) gill-bars. (After BENHAM, slightly altered.)
a.e. Atrial epithelium. 6.e, Branchial epithelium. c. Ccelomic space of primary
bar. s%. Skeletal rods. wv. Ccelomic vessel of primary bar. vw’’, External vessel
of both bars. v’’’. Internal vessel of both bars.
N.B.— Benham holds the space at the inner edge of the skeletal rod of
tongue-bar for a blood-vessel.
C. Isolated ciliated cells of the branchial epithelium. (After LANGERHANS.)
Next comes a cavity which is a portion of the ccelom, and
is lined by the flat ccelomic epithelium. In fact, the dor-
sal, or subchordal coelom on each side (cf. Fig. 2) is put
in connection with the endostylar ccelom by a canalicular
detachment of the ccelom which accompanies each primary
34 ANATOMY OF AMPHIOXUS.
bar of the pharynx. Wedged in between the coelomic and
atrial epithelia of the primary bar is a small blood-vessel,
v. Internal to the ccelomic space lies the skeletal rod,
which in section has the shape of a triangle, at whose apex
there is another blood-vessel, wv".
The sides and inner
edge of the bar are composed of the ciliated pharyngeal
epithelium. The cells of the latter are always arranged in
a single layer, but at the sides of the gill-bars they are
very long and thin, and the nuclei are crowded together at
different layers so as to give the idea of a many-layered
epithelium: (Fig. 15°C): Dhe cells: of one side of the bar
are in juxtaposition with those of the opposite side, except
at a point near the internal edge of the bar, where a space
occurs. In this space there is a third blood-vessel, v!’’.®
In the secondary bar, there is no vessel corresponding
to the one marked v in the primary bar, and the vessel
that corresponds with v!’
is entirely enclosed within the
skeletal rod.
The dorsal wall of the pharynx is closely appressed
against the sheath of the notochord, and separates the two
dorsal aortz from one another. It has here the form of a
eroove running parallel with and opposite to the endostyle.
It is known as the hyperbranchial groove. (Cf. Fig. 2.)
Two special tracts of ciliated epithelium form the sides of
it, and pass downwards in front to join the anterior extrem-
ity of the endostyle on each side. In front, where these
tracts bend downwards with a crescentic curve, they are
known as the pertpharyngeal bands. (See Fig. 11, p/.0.)
Musculature.
The musculature of Amphioxus is composed almost
entirely of striated muscle-fibres. Involuntary or smooth
muscle-fibres are remarkable for their extreme tenuity, and
INTERNAL ANATOMY. 35
in correlation with this condition is to be noted the absence
of a distinct sympathetic nervous system.
The striated muscles can be arranged in two groups:
(i.) the parzefal muscles constituting the myotomes or
muscular segments of the body, and (ii.) the wesceral
muscles which arise independently of the myotomes and
are not segmentally arranged. The smooth muscle-fibres,
which occur on the walls of the alimentary canal and
blood-vessels, may be grouped together as the splanchnic
muscles.
The parietal muscles are the great longitudinal muscles
which make up the thick lateral walls of the body. In
Amphioxus they form collectively the essential organ of
locomotion. The portion of them lying next to the atrium
on each side, and stretching from the notochord to the
base of the myotome, is placed at an angle to the rest, and
has) deimore, vertical direction: (Ci Fic 2))) “libisehas
been described by SCHNEIDER as the rectus abdominis. It
probably co-operates with the muscles of the floor of the
atrium to cause the contraction of the latter cavity for the
purpose either of expelling water or reproductive elements
through the atriopore.
The visceral muscles consist of (a) the transverse muscles
stretching across the floor of the atrium (cf. Fig. 2), (8)
muscles of the oral hood and cirri, (y) sphincter muscle of
the velum (cf. Fig. 7), (6) anal sphincter.
All the striated muscles of Amphioxus are composed
of highly characteristic flat lamelliform pilates, which can
often be resolved into a great number of finer fibrils. In
the longitudinal muscles of the adult, nuclei are very
rarely met with, but in other places they are to be found ;
as, for instance, in the fibres composing the velar sphincter
(Fig. 16).
36 ANATOMY OF AMPHIOXUS.
This peculiar plate-like muscular tissue is found in
connection with the lateral muscles only of the Cyclostome
fishes. The muscle-fibres of the mouth
and velum, as LANGERHANS pointed out,
closely resemble those found in the walls
of the heart of the higher Vertebrates.
In transverse section the cut edges of
the longitudinal muscle-plates are to be
seen stretching across the myotome.
(Gio Figs.2;°26;)
The transverse or szb-atrzal muscles are
divided by a median longitudinal septum
of connected tissue into right and left
halves. They are further subdivided into
a series of compartments by thin trans-
verse septa. These compartments, how-
ever, are not arranged segmentally, since
Fig. 16.— Isolated
muscle-fibre of the they are more numerous than the myo-
velar sphincter. (After
Peet NS) tomes. The muscle-plates of these mus-
cles are placed edge on, so that they do
not lie one over the other as the plates of the myotomes
do, but one behind the other. They are attached to the
septum at the base of the myotomes on the one hand, and
to the median septum or vap/e on the other, and also they
are attached at numerous points to the connective-tissue
sheath or fascea which covers them above and below.
When they contract, therefore, the floor of the atrium is
thrown into a number of characteristic pleats. (Cf.
Fig. 2.) The individual muscle-plates of Amphioxus ap-
pear universally to be devoid of a protecting sheath or
sarcolemma. The sub-atrial muscles end at the atriopore,
round which they form a sphincter muscle.
The muscles of the oral hood, which serve for the erec-
INTERNAL
ANATOMY. 37
tion and supination of the buccal cirri, consist of two por-
tions, an zzner and an outer
(Bigs ai7)i * Whe outer.-one;
by whose contraction the cirri are retracted in such a way
that they come to le across the entrance to the mouth,
those of one side interlacing
with those of the other so
as to form a perfect barrier
to the mouth, is a powerful
muscle lying outside the
The
inner muscle, which appar-
bases of the cirri.
ently serves’ to “erect the
cirrl, consists of distinct
muscular tracts lying be-
=
Fig. 1'7.— Muscles of the oral hood.
(After LANGERHANS.)
m.e. Outer muscle
(m. externus)
whose fibres interlace with those of the
tween every two consecutive velar sphincter (v.sp). .. Inner muscle
cirri.
(m. internus).
The sphincter muscle of the velum has been already
referred to.
Fig. 18.— Diagram illustrating the
different layers of the integument. (After
HATSCHEK.)
z. Epidermis. 2. Outer layer of cutis
(basement membrane of Hatschek and
Spengel). 3. Middle layer of cutis with
radial fibres. 4. Inner layer of cutis.
5. Epithelial layer of cutis (limiting mem-
brane).
(Cf. Fig. 7.) A sphincter muscle of a simi-
lar character also surrounds
the anus.
The septa which separate
the myotomes from one
another are composed of
fibrous connective tissue.
The fibres are imbedded in
The
salient feature in connexion
a gelatinous matrix.
with the entire connective
tissue-system of Amphioxus
is the great preponderance
of the gelatinous element.
It forms the bulk of the dorsal and ventral fin-rays, and
of the cephalic and caudal integumentary expansions.
38 ANATOMY OF AMPHIOXUS.
The middle layer of the cutis below the epidermis (cf.
Fig. 18) is composed mainly of this tissue with radial
fibres superadded. In the metapleural folds it attains a
greater development than in the rest of the integument.
(Cf. Fig. 2.) It also constitutes the middle layer of the
sheath of the notochord, but the fibres in this case run
concentrically, and not radially.* The outermost layer
of the cutis (Fig. 18) and the innermost layer of the
sheath of the notochord are composed of a peculiar and
very highly refringent and homogeneous tissue of the
same order as that which forms the skeletal rods of the
pharynx. The layer of connective tissue which separates
the myotomes from the body-cavity, and which springs
out from the base of the notochordal sheath (Fig. 2), occu-
pies the same position as the ribs of the higher Vertebrates.
NOTES.
1. (p.15.) Metapleural Folds. —In the development of the
paired fins of Selachians it was discovered, in 1876, by BaLrour,
that at a certain stage there appears along each side of the body
“a thickened line of epiblast (7.e. ectoderm), which from the first
exhibits two special developments.” ‘These two special thick-
enings are the rudiments of the paired fins, which thus arise as
special developments of a continuous ridge on each side, precisely
like the ridges of epiblast which form the rudiments of the
unpaired fins.” After giving more details, Balfour says, ‘The
facts can only bear one interpretation, viz. that the limbs are the
remnants of continuous lateral fins.”
Shortly afterwards (1877), but quite independently, James Kk.
THACHER was led by a comparative study of the adult skeleton of
* In that portion of the sheath of the notochord which lies above the dor-
sal groove of the pharynx there is a special tract of connective-tissue fibres
which run longitudinally. A similar tract can sometimes be observed in the
dorsal portion of the sheath below the nerve-cord. (Schneider, Lankester,
Spengel. )
NOTES. 30
Selachians and other fishes, to a belief in the homodynamy of
median and paired fins, and he therefore concluded that the
latter arose as differentiations from primitively continuous lateral
fins just as the median fins are obviously differentiated from a
continuous dorsal and ventral fin-fold. Thacher further suggested
that the original continuous lateral fins were represented in Am-
phioxus by the metapleural folds. He said, “ As the dorsal and
anal fins were specialisations of the median folds of Amphioxus,
so the paired fins were specialisations of the two lateral folds
(metapleural folds), which are supplementary to the median in
completing the circuit of the body.”
It has recently been observed by Professor E. A. ANDREws, that
in a new species of Amphioxus from the Bahamas, the right meta-
pleural fold is continued behind into the median ventral fin.
Subsequently I found the same condition to obtain in a species
of Amphioxus from the Torres Straits.
From these observations, and from the fact that the right half
of the oral hood (which apparently arises in continuity with the
right metapleur—zzde infra) is continued in front into the
cephalic expansion of the dorsal fin, it would appear that there
is a great measure of truth in Thacher’s suggestion, notwithstanding
the fact that in the condition in which we find them in the exist-
ing Amphioxus, the metapleural folds do not function as fins.
Thacher’s hypothesis has
also been supported by
Van WIJHE.
2. (p. 10.) The accom- Fig. 19. — Diagram illustrating (by a dotted
panying diagram (Fig. 19) line) the course of the food as it passes through
. : the pharynx and intestine of Amphioxus. (After
will serve to illustrate the Dats)
actual course of the food The small diverticulum on the dorsal side of
through the pharynx of the oral hood represents the groove of Hatschek
2 somewhat exaggerated. The arrows behind the
Amphioxus, as recently ccecum indicate the rotation to which the food is
determined by ANpDREws, here subjected by the action of the cilia of the
: ’ intestinal epithelium.
from observations on
transparent specimens from the Bahamas. The food, enveloped
in the mucous secretion of the endostyle, passes along the dor-
sal groove of the pharynx (hyperpharyngeal groove) into the
intestine.
40 ANATOMY OF AMPHIOXUS.
3. (p. 10.) On those occasions on which Amphioxus is not
buried in the sand, but lies on the surface of the sand, occasions
which frequently occur when it is kept in captivity, and especially
after having been confined for a considerable length of time, it
lies on one side, as mentioned in the text. The percentage of
instances in which it les on the right or left side has not been
taken, and consequently it is not possible to say that it prefers lying
on one side rather than on the other. Since the olfactory pit and
the anus occur on the left side, it is conceivable that it prefers
to lie on the right side. If this had been a definite habit, it
would probably not have escaped the observation of Johannes
Miiller. It is a fact which is too frequently overlooked, that the
lying on one side is entirely incidental, and is emphatically not
the result of adaptation to a peculiar mode of life, as it is in the
case of the Pleuronectide.
4. (p. 11.) Species and Distribution of Amphioxus. — A useful
synopsis of the genus Branchiostoma has recently been prepared by
ANDREWS, as an appendix to his paper on the remarkable species
which occurs at the Bahamas. In this species there is a long
caudal process into which the notochord extends. It is an active
swimmer. Gonadic pouches are only present on the right side,
those on the left being suppressed. ‘The latter is also true of
Branchiostoma cultellum. The peculiarities of the species from
the Bahamas were such that Andrews deemed it necessary to form
anew genus, Asymmetron.
In the table of species on page 41 it will be noticed that the
lengths of the different species are not in any proportion to the
number of myotomes.
Insufficiently described species occur off the coasts of Fapan,
Ceylon, and fiz Lslands. It is interesting to note that while in
Europe, Amphioxus occurs as far north as Scandinavia, on the
Atlantic coast of North America, Chesapeake Bay appears to be
its northern limit, and it is therefore wholly unknown at the
Marine Biological Station at Woods Holl. Attention may further
be called to the simultaneous occurrence of two distinct species,
B. cultellum and B. belcheri,in the Torres Straits. 2B. cultelum
is easily recognisable on account of the unusual height of its dorsal
fin.
NOTES. — 41
NuMBER LENGTH
NAME OF SPECIES. | OF IN MILLI- GEOGRAPHICAL DISTRIBUTION.
MYorToMEs. | METRES.
I. B.lanceolatum. . 59-61 35-80 Scandinavia, Heligoland, Eng-
land, France, Mediterranean,
and Chesapeake Bay.
a, ls Cehaloesyeiny Gc 58 43 Brazil, Mouth of La Plata,
Jamaica, Tampa Bay, Gulf of
Mexico, Beaufort, N.C.
Se bacultellumi ans 5. 52-55 25-35 | Thursday Island (Torres
Straits), Moreton pe (E.
Australia).
4. B.bassanum . . 75 — Bass Straits, Australia.
Bp 1s letelsat Go. 65 65 Borneo and ‘Torres Straits
(Prince of Wales Island).
6. B.elongatum . . 79 60 Peru.
7. B. californiense . 69 70 San Diego, California.
8. B.lucayanum-. . 66 13-16 | Bimini and Nassau Harbour
= Asymmetron lu- (Bahamas).
cayanum, Andrews
5. (p. 22.) Huxvey had recognised in 1874, in the light of
Kowalevsky’s work, that the atrial cavity of Amphioxus was lined
by an epithelial layer derived from the ectoderm, but came to the
conclusion that it was, by the very fact of its inversion within the
body, converted into peritoneal epithelium. He applied the same
interpretation to the opercular chamber of the Amphibian tadpole,
and gave to a body-cavity of this character the general name of
epicele. ROLPH’s merit consisted in distinguishing clearly between
atrial epithelium and peritoneal epithelium, and hence between
atrial cavity and true body-cavity.
6. (p. 38.) There isa great deal of difference of opinion as to
the exact nature of that dense refringent tissue which forms the
outer layer of the cutis and the skeletal rods of the gill-bars.
LANKESTER regarded them both as the products of connective
tissue-cells, hence belonging to the mesoderm, while HatrscHEK
and SpENGEL looked upon the outer layer of the cutis as the
product of the ectoderm, of the nature of a dasement membrane.
SPENGEL again has advocated the view that the skeletal rods of the
42 ANATOMY OF AMPHIOXUS.
pharynx are special developments of the basement membrane,
which separates the two opposed epithelial layers of each gill-bar
from one another. (Cf. Fig. 15.) More recently, BENHAM has
described nuclei in the latter membrane, thus showing it to be a
sheet of connective tissue. In this case the substance of the
skeletal rods should be regarded as a variety of connective tissue.
A further difference of opinion prevails as to the nature of the
space which traverses the skeletal rod of the tongue-bar. Lan-
KESTER supposed it to be a diverticulum of the coelom. SPENGEL
and Boveri interpreted it as a blood-vessel ; and, finally, BENHAM
thinks that it is both, inasmuch as he conceives there to be a blood-
vessel contained in a coelomic space. It should be added that
these finer details are extremely difficult to determine.
7. (p. 21.) Lateral Line. — Since the lateral line constitutes
one of the most characteristic and constant features in the organi-
sation of fishes, its absence in Amphioxus has always been one of
the most serious difficulties in the way of a conception of this
animal as, in any sense, an ancestral form. It need hardly be
pointed out that from whatever point of view we regard Amphi-
oxus, it must necessarily have become specialised and modified
along its own particular line of evolution, and cannot, as it stands,
be taken as a direct ancestral form, but rather as a more or less
close relative of, or an exceedingly ancient offshoot from, the
actual ancestor of the Vertebrates. The modifications which it
has undergone will, as in every other case, have resulted in more
or less extensive changes both in the function and structure of dif-
ferent parts. Thus, while the metapleural folds are very probably
the homologues of the primitive continuous lateral fin-folds, yet
in their actual form and function they may or may not represent
the primordial condition of these folds. Certain peculiar features
in connexion with the origin and innervation of the metapleural
folds of Amphioxus have led me to form a conception as to the
origin of the lateral line sense-organs which may perhaps have
some value as a working hypothesis.
In those primitive fishes which possessed the continuous lateral
fin-folds, it is very clear that the latter could not have performed
a locomotor function, but they must have served primarily as
balancers. Without going into the difficult question as to how
NOTES. 43
such structures could have arisen de xovo, we may at least attempt
to appreciate the necessity for their existence.
There is one difference between the general form of the body
in Invertebrates and Vertebrates respectively which seems to be
of fundamental importance, but which has not been sufficiently
emphasised. As a general rule, in the Invertebrates, the body
is not bilaterally compressed, but, on the contrary, is either cylin-
drical, sub-cylindrical, or flattened dorso-ventrally. Obvious ex-
ceptions to this rule are presented by the Lamellibranchiate
Molluscs and by many Arthropods; but these exceptions are
readily intelligible as secondary modifications.
On the other hand, in the more primitive Vertebrates (ze.
fishes), the bilateral compression of the body is one of the car-
dinal features of the external form. To this fundamental rule
there are of course exceptions afforded, for example, by the
skates ; but it is a self-evident fact that these again have arisen
by secondary modification from originally bilaterally compressed
forms. With the evolution of the pentadactyle appendages and
the assumption of a terrestrial existence, the shape of the body
in the higher Vertebrates has undergone such changes that the
primitive bilateral compression of the body is, as a rule, only
present at some period of the embryonic development.
Amphioxus exhibits the characteristic vertebrate bilateral com-
pression of the body in a very typical manner; while Balano-
glossus shows invertebrate affinities in regard to the shape of the
body, which is sub-cylindrical.
The bilateral compression of the primitive vertebrate body did
not arise in itself as a special adaptation to a particular mode of
life ; but rather in correlation with other characters of the organi-
sation. The development of the dorsal medullary tube and the
notochord above the digestive tube and the concentration of the
myotomes would necessarily lead to a bilaterally compressed form
of body. We see this not only in fishes, but in the course of the
development of all Vertebrates.
It is obvious that such a shape of the body is highly unfavourable
for the maintenance of the equilibrium except with the assistance
of some special mechanical and sensory apparatus.
Now in Amphioxus, the metapleural folds, whatever their exact
44 ANATOMY OF AMPHIOXUS.
function may be, do not serve in any way as balancers; and, as
mentioned in the text, Amphioxus has no means of maintaining
its equilibrium when not actually swimming.
We will therefore keep in mind more especially those Palzo-
zoic fishes which presumably possessed continuous lateral fin-folds
serving as balancers. ‘The nearest known fossil relatives of these
fishes appear to be the Cladoselachide (see BASHFORD DEAN.
Contributions to the Morphology of Cladoselache (Cladodus).
Jour. Morph. IX. 1894. pp. 87-112. Also A. SmirH Woopwarb.
The Evolution of Fins. Natural Science, I. 1892. pp. 28-35).
The lateral fin-folds may be spoken of as mechanical balancers,
and to render them efficient organs, there must be a sevsovy appa-
ratus in connexion with them. ‘The suggestion lies near that she
ectoderm which took part in the formation of the lateral fin-folds
also produced the sense-organs of the lateral line.
The lateral line, through its capacity for receiving impressions
of wave-movements, etc., would thus serve as the agent in the
co-ordination of such muscular activities as are necessary to the
maintenance of the equilibrium.
Having been once established, no special difficulty is presented
by the fact that the lateral line has spread over the head-region.
Moreover, it may be taken as a well-established morphological
fact that the auditory organ (internal ear) became evolved as a
specialisation of part of the lateral line in the cephalic region, and
that it therefore belongs to the same category as the less elaborate
sense-organs of the remainder of the lateral line.
As is well known, the internal ear has two functions, avdition
and equilibration. It must be supposed that, at its first origin,
the whole lateral line served in a general way the function of
equilibration, and that this function eventually became chiefly
localised in the semicircular canals of the ear, the remainder of
the lateral line perhaps undergoing a slight change or limitation
of function.
It seems certain that at first the sense-organs of the lateral line
must have been innervated by spinal nerves. This follows both
from @ priori considerations and also from the condition in Amphi-
oxus, where the ectoderm of the metapleural folds is innervated
by the Rami cutanet ventrales of the dorsal spinal nerves. Under
NOTES. 45
these circumstances it is necessary to suppose with Ersic that the
lateral line nerve (Ramus lateralis vagt) arose as a collector.
The removal of the lateral line from the immediate neighbour-
hood of the paired fins in existing fishes is easily intelligible on
the ground that the fins have become discontinuous and elaborated
into effective locomotor organs.
It is not impossible that the lateral line nerve (2. dateralis vag?)
is homodynamous with the remarkable Ramus cutaneus guinti
(R. recurrens trigemini et facials or Nervus lateralis trigemint,
Srannius) of Teleosteans, which runs to the base of all the fins,
paired as well as unpaired ; just as the paired fins themselves are
known to be homodynamous with the median fins. In this case
the 2. cutaneus guinti would be of primitive significance, notwith-
standing the fact that it is absent in Selachians ; and it would be
another of those features of organisation in the possession of which
Teleosteans exhibit more primitive relations than do the existing
Selachians. (Compare the functional pronephros of Teleosteans
and the entirely rudimentary pronephros of Selachians. )
The above suggestion that the lateral line arose in the first
instance as a sensory equilibrating apparatus in conjunction with
the mechanical equilibrating apparatus effected by the continuous
lateral fin-folds, will of course meet with numberless difficulties
when it is attempted to carry it out in detail. As in some other
respects, so here, a great difficulty is presented by the Cyclo-
stomes. It may, however, be pointed out that if the various con-
clusions which have been drawn with regard to the morphology of
Amphioxus are correct, it must be assumed that the Cyclostomes
have entirely lost the lateral fin-folds and that the sense-organs
of the lateral line have secondarily become diffused in their dis-
tribution over the body. The latter conclusion is also indicated,
firstly, by the fact that there is a fairly well developed internal
ear in the Cyclostomes which, as noted above, must have been
differentiated from a primitive lateral line ; and secondly, by the
fact that although the sense-organs are scattered, there is never-
theless (at least in Petromyzon) a definite lateral line nerve.
ee
ANATOMY OF AMPHIOXUS.
INTERNAL ANATOMY (continued ).
In the preceding chapter we have seen how Amphioxus,
while possessing the general facies of a fish, and the
primary essential attributes of a Vertebrate, is nevertheless
destitute of many of the most obvious structural features
which we usually associate with our conception of a fish.
Thus it has no skull, or, in other words, it 1s Acranzate
(Haeckel). It has no jaws, and is therefore a Cyclostome,
as opposed to a Guathostome. Finally, it has no paired
sense-organs and no paired muscular fins. Its eye-spot
is median, like that of a Cyclopean monster. There is no
trace of an auditory organ of any kind, while the single
so-called olfactory pit, abutting on the anterior end of the
nerve-tube, has been regarded as an indication of a mono-
rhinic condition preceding the amphirhinic, z.¢. with paired
nostrils.
Vascular Systeme.
Now, in turning our attention to the vascular system, we
shall find that Amphioxus has no heart. In any ani-
mal with a comparatively well-developed vascular system,
the presence of a heart might be regarded as a seme qua
non. This, however, is by no means always the case; and
although, among the Invertebrates, the extensive groups
46
INTERNAL ANATOMY. 47
of the Arthropoda (Insects and Crustacea) and the
Mollusca are characterised by the possession of a definite
muscular heart, yet in the various groups of worms there
are many which possess a very elaborate vascular system,
while not one of them possesses a heart. In fact, in the
last-mentioned forms, the place of a heart is taken, func-
tionally, by contractile blood-vessels. And this is the case
with Amphioxus. Among the Vertebrates, including
the Ascidians, it forms the unique instance in which such
an acardiac condition of the vascular system is met with.
Lying below the pharynx in the endostylar coelom, there
is a blood-vessel known as the branchial artery, which con-
tracts more or less rhythmically, and corresponds in its
position and relations to the heart and truncus arteriosus
of the higher forms.
Fig. 20.— Diagram illustrating the chief parts of the vascular system of
Amphioxus. (Constructed after J. MULLER and SCHNEIDER.)
The arrows indicate the direction of flow of the blood. ch. Notochord. hep.
Hepatic coecum. af Afferent branchial vessels (vascular bulbils of J. Miiller)
entering the primary bars from ér.a, the branchial artery; the efferent branchial
vessels are seen emerging from the tops of both primary and secondary bars and
running into d.a, the dorsal aorta. From the dorsal aorta, the blood enters the
capillaries over the wall of the intestine (indicated by the dark reticular shading),
and finally reaches s.7.v, the sub-intestinal vein. The latter carries the blood to the
base of the hepatic coecum, over which it passes into another system of capillaries
(not indicated), and is then collected into 4.v, the hepatic vein, which passes back-
wards and curves round into the branchial artery.
From this branchial artery, lateral branches running up
into the primary bars of the pharynx are given off on both
sides alternately. (Cf. Fig. 20.) There appears to be no
48 ANATOMY OF AMPHIOXUS.
direct communication between the vessels of the tongue-
bars and the branchial artery.
At the base of the primary bars the lateral offshoots of
the branchial artery are found to be enlarged to form
vascular bulbils, which are also contractile. Furthermore,
at this point they divide into three branches of smaller
calibre, which constitute the vessels of the primary bar.
Fig. 21.— Diagram of a section through the pharynx involving a primary bar
(to the left), and a tongue-bar (to the right), to illustrate the circulation in the
branchial bars. (After SPENGEL.)
ér.a. Branchial artery. c. Ccelom; outside of which is the atrial epithelium.
c.v. Ccelomic vessel of primary bar. e. Endostyle. e.c. Endostylar ccelom. e.v.
External vessel. z.v. Internal vessel. Z.a. Left aorta. 7a. Right aorta. 7. Cavity
of pharynx. 7.4. Tongue-bar.
(Cf. Fig. 15.) One of these branches, as we haverseen,
runs up between the coelomic and atrial epithelium, and
may be called after Boveri the c@/omic vessel, of the primary
bar (Figs. 15 and 21). Another lies at the immer edee or
the skeletal rod, and is the so-called external vessel, while
a third lies immediately below the inner pharyngeal epi-
thelium of the bar, and forms the zzternal vessel.
INTERNAL ANATOMY. 49
The two last-named vessels only are represented in the
tongue-bars, and differ in their arrangement in the latter
in so far as the external vessel is enclosed within the
skeletal rod.
The blood which circulates in the tongue-bars flows into
them, not from the branchial artery, but from the primary
bars through the cross-bars of the pharynx. The vessels
of each gill-bar unite above into a single efferent vessel,
which conducts the blood into the dorsal aorta of either
side. So that while efferent vessels issue alike from both
primary and tongue-bars, the afferent vessels, which lead
the blood directly from the branchial artery into the gill-
bars, are confined) to. ‘the prmaryebars, (Pis;: 20). The
blood, having been oxygenated during its passage through
the gill-bars, past which a constantly renewed stream of
water is kept flowing, enters the dorsal aorta, and is then
carried backwards to the region of the intestine. The
two halves of the dorsal aorta, which we have already
noted on either side of the hyperpharyngeal groove, be-
come united into a common trunk behind the pharynx, so
that in the region of the intestine there is a single dorsal
aorta (cf. Fig. 28), from which lateral branches are given
off to the wall of the intestine. These then break up into
capillaries, which anastomose freely together, and so form
a perfect vascular network round the intestine. Finally,
the blood emerges from this capillary system into a large
vein lying below the digestive canal, the s7d-¢ntestinal vein.
Here it flows in a forward direction until it reaches the
base of the hepatic ccecum. At this point the vein appears
to stop short, but in reality breaks up into another system
of capillaries surrounding the liver.! From these again
the blood is collected into the large multiple hepatic vein
lying above the ccecum. Here it flows backwards as far as
50
ANATOMY OF AMPHIOXUS.
the angle formed by the coecum with the alimentary canal,
where the vein bends sharply round into the branchial
artery, and so the cycle is completed (Fig. 20).
According
to JOHANNES MULLER, the time required for one complete
circulation of the blood in Amphioxus is one minute, and
in this time any given droplet of blood will have traversed
Fig. 22.—Transverse section through re-
gion of velum to show difference in behaviour
of right and left aortaze. (Altered from LAN-
GERHANS.)
ch. Notochord. Za. Left aorta. #2. Meta-
pleur. 2. Spinal cord. 7a. Right aorta. 7.7.
Transverse muscles ; the septum (raphe) which
divides these muscles into two halves is no
longer median, but shifted towards the right
side in consequence of the fact, discovered by
VAN WIJHE, that the right transverse muscles
dwindle out and end in this region, while the
left transverse muscles are continued into the
outer muscle of the oral hood. v. Velum.
the whole body. Con-
trary to what takes place
the shigher Verte:
brates, a single contrac-
in
fone stheshearte (Ze:
branchial artery) in
Amphioxus suffices for
a complete circulatory
cycle?
Rhesmeht ands ett
dorsal aorte differ from
one another in respect
to the behaviour of their
anterior cephalic termi-
At the front
end of the pharynx, the
nations.
right aorta opens out
into a wide vascular ex-
pansion which flanks the
velum on the right side
(Figs. 3 and
Johannes Miiller, who
2y2)
“<-)
#4;
first figured this struc-
ture, took it for the an-
teriormost aortic arch connecting the branchial artery
directly with the dorsal aorta.
However, according to the recent researches of Professor
INTERNAL ANATOMY. SI
J. W. vAN WyHE, it would appear that this so-called aortic
arch does not communicate with the branchial artery, but
ends blindly below in the neighbourhood of the right meta-
pleur. Dorsally, the aorta from which this lateral arch-like
outgrowth occurs, is continued forwards (not as a simple
vessel, but as a complex of vessels) as far as a peculiar
sense-organ known as the groove of Hatschek, after its
discoverer. This groove lies in the roof of the oral hood
to the right of the notochord, and is derived from the
preoral pit of the larva (see below). (Cf. Fig. 76.)
In front of the sense-organ this dilated continuation of
the right aorta communicates beneath the notochord by
means of a transverse vascular commissure with the left
aorta, which retains its small calibre and simple character
throughout. From the vascular complex of the right
aorta arise the vessels which supply the buccal cirri.
Hitherto we have only spoken of those blood-vessels
which are related to some part or other of the alimentary
canal. In point of fact the parietal or somatic vessels of
Amphioxus, if present at all, must have a very subordi-
nate physiological significance. Their place is taken by
lymph-spaces, of which there are a great number in various
parts of the body. Such are the dorsal and ventral fin-
chambers, the spaces in the metapleural folds, spaces at
the apices of the myotomes and in connexion with the
dorsalnerve-roots, ete. (Cf. Fig. 2.)*
The vascular system of Amphioxus presents several
features of great interest from a phylogenetic or evolu-
tionary point of view.
We have seen that the heart is in no way differentiated
from the branchial artery and is therefore a simple tubular
vessel. This is the primary condition of the heart in the
embryos of all the craniate Vertebrates. In the latter, as
§2 ANATOMY OF AMPHIOXUS.
the embryonic development proceeds, this simple tubular
heart widens out, acquires a series of constrictions, and
undergoes a remarkable flexure known as the szgmozd
fiexure. Two stages in the formation of the sigmoid
flexure of the heart of the chick-embryo are shown in
Figs. 23 and 24. At a somewhat earlier stage than
Figs. 23 and 24.— Anterior portions of chick-embryos of the 38th and 48th
hour of incubation, seen from below, to illustrate formation of heart. (After
DUVAL.)
ao. Right and left aortae. az. Auditory involution. cy . Ventricular portion of
heart. cg. Auricular portion of heart. e. Eye. 4%. Heart. of. Primary optic
vesicle. £.f4. Primary fore-brain. .m.6. Primary mid-brain. 7.4.4. Primary
hind-brain. 4a. Truncus arteriosus. v.a. Vitelline arteries. v.v. Vitelline veins. ~
1, 2,3, Transitory gill-slits.
that represented in Fig. 23 the heart was perfectly
straight. In this figure it is still a simple dilated tube,
but no longer straight. It has become bent outwards
into a U-shape. At the stage of Fig. 24 well-marked
constrictions (the indications of the later division into
auricle and ventricle, etc.) have appeared in the heart, and
the simple U-shaped flexure of the latter has become
INTERNAL ANATOMY. 53
complicated by the occurrence of a further flexure in a
different direction, in consequence of which the hinder
limb of the U has been raised, so to speak, to nearly the
same plane as the anterior limb. The shape of the heart
at this stage bears a characteristic resemblance to the
Greek letter sigma. The permanent condition of the
heart in Amphioxus therefore corresponds to an early
stage of its development in the higher Vertebrates.
Again, in the craniate embryo the dorsal aorta arises as
a pair of vessels on either side of the notochord, which
later fuse together into one median dorsal vessel. (Cf.
Fig. 24.) In Amphioxus, throughout a great portion of
its extent, — namely, in the region of the pharynx, —the two
halves of the dorsal aorta remain permanently separated
from one another by the dorsal groove of the pharynx.
(Cf. Figs. 2 and 28.)
One of the most striking peculiarities of the vascular
system of Amphioxus is the presence of the szb-cztestinal
vein, in its capacity as the main venous trunk of the body.
It collects the blood from the capillaries of the intestinal
wall, and conducts it to the base of the liver, where it again
breaks up into capillaries.* It acts, therefore, physiologi-
cally, as a portal vein, while morphologically it is the
sub-intestinal vein. Curiously enough, it is much larger in
its posterior than in its anterior moiety, and in transverse
sections through the hinder region of the intestine there
appear to be several separate vessels lying side by side,
sometimes as many as six. These, however, if traced
backwards or forwards, are found to anastomose with one
*In the larva of Amphioxus the sub-intestinal vein and branchial artery
form one continuous blood-vessel. Later, when the hepatic ccecum (liver)
grows out from the ventral wall of the alimentary canal, an interruption occurs
in the continuity of the vessel, through the insertion of a capillary portal system
in its course.
54 ANATOMY OF AMPHIOXUS.
Fig. 25.— View of portion
of sub-intestinal vein of Amphi-
oxus, to show its fenestrated
character in the posterior re-
gion. (After SCHNEIDER.)
a. Anterior. #. Posterior.
another, as shown in Fig. 25, and
so there is produced a fenestrated
structure in the vein. The hepatic
vein has a similar fenestrated char-
acter, and this was what was meant
by speaking of it above as being
“multiple.”
The sub-intestinal vein reappears
in the embryos of all the higher
fishes and Amphibia, where it breaks
up into capillaries in the liver. In
these forms, however, it does not
persist long as the main venous
trunk, but becomes replaced almost
entirely by the development of two
large veins, which arise on either
side of the dorsal aorta. These are
the so-called cardinal veins. The
sub-intestinal vein mostly disappears
after the formation of the cardinal
veins, but persists as a second-class
vessel in the lampreys and in some
sharks, lying, in the latter, in the
spiral valve of the intestine.* More-
over, its posterior portion, which
lies in the tail, persists as the caudal
vein.
* The sub-intestinal vein is also persistent in
the following Urodele Amphibia — Sa/aman-
dra, Triton, and Pleurodeles. (See F. Hocn-
STEITER. Lettrage sur vergleichenden Anatomie
und Entwicklungsgeschichte des Venensystems
der Amphibten und Fische. Morph. Jahrb.
XIII. 1888. pp. 119-172.)
INTERNAL ANATOMY. 55
The same vessel, therefore, which constitutes the main
venous trunk of the adw/t Amphioxus performs the same
function in the embryos of the higher fishes. We can thus
deduce a good deal of evidence from a consideration of the
vascular system alone, pointing to the primitive and ances-
tral character of Amphioxus.
If we compare broadly the vascular system of Amphioxus
with that of a segmented worm like the common earth-
worm, we are at once confronted with certain obvious
superficial resemblances. Here, as in Amphioxus, the
vascular system comprises two main longitudinal trunks,
one lying above the intestine and the other below it, and
furthermore, they are connected together at intervals by
circular vessels which form complete rings round the
alimentary canal in the same way as do the vessels which
pass through the pharyngeal bars of Amphioxus.
It is only when we come to enquire into the direction
of flow of the blood in the two cases that we meet with a
striking contrast between them. Whereas in Amphioxus
the blood flows in the dorsal aorta from before backwards
(see Fig. 20), and in the sub-intestinal vein together with
the branchial artery, from behind forwards, in the worm, on
the contrary, these directions are reversed, and the blood
flows from behind forwards in the dorsal vessel, and from
before backwards in the ventral vessel.
The Excretory System.
The excretory function is so intimately bound up with
the circulation that a description of the organs which
serve this function follows naturally after the consideration
of the vascular system. The apparent absence of definite
excretory organs in Amphioxus was for a long time one of
the greatest difficulties in the way of a correct appreciation
56
of the peculiarities of its organisation.
ANATOMY OF AMPHIOXUS.
Thanks, however,
to recent researches, it is now known to possess such
organs in luxuriant abundance.
From first to last several entirely different structures
have been credited with a renal function.
SY,
7
a
Ze
Ic
aioe
W,
ae
Ry
Wey
<a
mae
POPP pe
PYsIsR
JOICAES)
Er
ELS
Le
races
ZZ
i
l/
Se
aye
A feb D \
REL
i SB Wy
Fig. 26.— Transverse section through
post-pharyngeal region of young individual,
to show groups of renal cells in floor of
atrium. (After LANKESTER and WILLEY.)
ao. Aorta. at. Atrium. 4é.c. Body-cavity
(ccelom). ¢.c. Central canal of nerve-cord
(1.c). d.fic. Fin-cavity. zm. Interccelic
membrane. f/m. and rm. Left and right
metapleural folds. »7.f. One of J. Miiller’s
renal papillae. s.z.v. Sub-intestinal vein.
JOHANNES
MULLER first discovered
certain glandular epithe-
lial tracts in the floor of
the atrial chamber in its
These
cellular thickenings are
distinguished by their
high cylindrical cells from
the flattened atrial epi-
hinder portion.
thelium which surrounds
them. (Cf. Pigs. 11;and
26.) Johannes Miller sug-
gested that these groups
of cells might be renal
His observation,
however, failed to find
generalacceptanceamong
organs.
morphologists for about
thirty-five years, when,
in 1876, W. RoveH.and
PauL LANGERHANS, work-
ing independently, fully
confirmed his account
and accepted his _inter-
pretation of the bodies as
renal organs, at the same
time adding a careful histological description of them
(Fig. 27).
INTERNAL ANATOMY. 57
The individual groups of cells have an elongated and
more or less ovoid shape with the long axis parallel to the
long axis of the body. According to Langerhans their
surface is ciliated. Two kinds of cells enter into their
composition ; namely, large clear dilated cells, which are
separated from one another by fine fibre-like cells of
extreme tenuity (Fig. 27). In the latter the nucleus of
each cell is placed near the free end of the cell, while in
the former it lies nearer the
base of the cell. Langerhans
found highly refringent con-
cretions in the dilated cells
which he took for excretory
products. Phat. these cells
have a capacity for excreting
waste matters has more re-
cently been shown experiment- |:
ally by F.E. Wetss. Theatrial “
epithelium on the pharyngeal Se gE oe iter Bebra:
bars has a similar character cretions indicated by the black bodies.
(After LANGERHANS.)
to that forming these curious
renal papillae on the floor of the atrium. The distribution
of these papille in the vicinity of the atriopore is very
irregular and variable and without any regard to a sym-
metrical disposition. Although they are undoubtedly to
be regarded as a species of renal organ, yet they could
not be compared to any portion of the excretory system
of the higher Vertebrates.
Another structure, or pair of structures, which has been
considered to belong to the category of renal organs must
next be referred to.
This consists of two funnel-shaped diverticula of the
atrial cavity lying in the dorsal (subchordal) ccelom in the
58 ANATOMY OF AMPHIOXUS.
region of the twenty-seventh myotome, where the pharynx
ends and the intestine begins. They were discovered in
1875 by LANKESTER, who called them the azrio-celomic or
brown funnels, on account of the rich accumulation of
brown pigment in their walls. We have already referred
to this brown pigment as occurring very generally in the
atrial epithelium. The brown funnels have the shape of an
Fig. 28.— Plastic diagram illustrating the positions and relations of the atrio-
coelomic funnels.- A rod is passed through the peri-enteric ccelom into the sub-
chordal (suprapharyngeal) ccelom. (After LANKESTER.)
ao. Dorsal aorta. at, Atrial cavity. 4. Atrio-ccelomic funnels. go. Gonads.
Zd. Ligamentum denticulatum (pharyngo-pleural folds, Lankester). ¢.m. and
7m. Left and right metapleural folds. my. Muscles. 4. Roof of pharynx.
uz. Point of union of the right and left aortze into the median aorta.
elongated cone, the apex of which is directed forwards.
At the wide end each funnel opens into the atrial cavity,
while at the narrow end it is possible, but not certain, that
an opening exists into the dorsal ccelom (Fig. 28). The
funnels are adherent throughout their entire length to the
roof of the dorsal ccelom.*
INTERNAL ANATOMY. 59
In 1889 WE!ss undertook the task of determining ex-
perimentally whether Johannes Miiller’s renal papille and
Lankester’s dvown funnels really served an excretory
function. The method of research consisted in feeding
full-grown individuals with various colouring matters held
in solution or in suspension in sea-water. For instance,
carmine suspended in sea-water would be carried into the
digestive canal and then absorbed through the intestinal
epithelium into the capillaries surrounding the intestine.
It would thus get into the vascular system, and also by
some means into some of the lymph spaces, and finally
would be excreted by the cells of the renal papilla or by
whatever other structure, or set of structures, might
possess the renal function. In fact, Weiss found that the
so-called renal papilla did actually excrete a quantity of
the carmine with which the animals had been fed, and,
further, that a similar excretion of carmine occurred at
other points of the atrial epithelium. The atrial epi-
thelium, as a whole, probably has more or less the power
of excreting waste products which have found their way
into the vascular and lymphatic systems.
But above all, Weiss discovered a very active excretion
of carmine in certain small ¢udz/es which he found lying
in the dorsal ccelom applied against the most dorsal por-
tion of the double-layered membrane (ligamentum denti-
culatum) which separates the ccelom from the atrial cavity
(Fig. 29). There is one of these tubules to each primary
gill-cleft of the pharynx. At the top of each tongue-bar
Weiss made out an opening of the tubule into the atrial
cavity, but he did not succeed in finding any openings into
the dorsal coelom. After the operation of feeding with
carmine was completed, at the close of a week or fortnight,
and time had been allowed for its absorption and subse-
60 ANATOMY OF AMPHIOXUS.
quent excretion, the epithelium lining the walls of these
tubules was found to be full of carmine granules.
At about the same time at which Weiss was pursuing
his studies on Amphioxus THEODOR BoveERI, having been
led by independent a przorz considerations, largely induced
by the work of RuckERT on the development of the ex-
cretory system of Selachians, to suspect the occurrence
Fig. 29.— Portion of transverse section through the pharynx of Amphioxus,
to show position of excretory tubule. (After WEISS.)
ao. Left aorta. at. Atrial cavity. ate. Atrial epithelium. c.Ccelom. ch. Noto-
chord. 2z.m. Intertcelic membrane. /Zd. Ligamentum denticulatum. ff. Excre-
torv tubule. £.4. Primary bar. #.e. Epithelium of hyperpharyngeal groove.
ph. f. Pharyngo-pleural fold. s.cz. Sheath of notochord. 724. Tongue-bar.
of excretory tubules in Amphioxus comparable to those
found in the embryos of the higher Vertebrates, instituted
a search for them and discovered them independently in
the most brilliant manner.
Boveri carried his investigation to a high pitch of per-
fection, and has published an account of these tubules,
which in point of clearness and completeness leaves nothing
INTERNAL ANATOMY. 61
to be desired. The accompanying figures, taken from
Boveri's finely illustrated memoir, show the appearance
and topographical relations of the excretory tubules.
A tubule as seen in the living condition is shown in
Fig. 30. It is a curved tube consisting mainly of two
Fig. 30.—An excretory tubule of the left side, with the neighbouring portion
of the pharyngeal wall, as seen in the living condition. The round bodies in the
wail of the tubule represent carmine granules. Highly magnified. (After BOVERI.)
limbs, bent approximately at right angles to one another,
and lying over against the dorso-lateral wall of the phar-
ynx. (Cf. Fig. 29.) The anterior limb is directed verti-
cally, and the posterior longitudinally. The former opens
by a relatively wide and forwardly directed opening into
62 ANATOMY OF AMPHIOXUS.
the dorsal ccelom. The posterior end of the tube also
opens into the ccelom, and between these two terminal
openings there is a variable number of other c@lomic
openings, or funnels, as they are called, situated on the
dorsal side of the tubule, and opposite to that side which
carries the opening into the atrial chamber. The ccelomic
funnels are placed at the ends of short upstanding projec-
tions from the main body of the tubule. On the ventral
side of the tubule, opposite in each case to a tongue-bar of
the pharynx, occurs the single opening into the atrial cav-
ity. The epithelium lining the tubule consists of cubical
ciliated cells. There is a thick bunch of cilia in connec-
tion with the atrial opening of the tubule. The curious
thread-like structures, carrying a round knob at their dis-
tal extremities, which radiate out from the ccelomic open-
ings, are specially modified cells belonging to the caelomic
epithelium, which are probably concerned in promoting
the excretory activity of the tubule, and are called by
Boveri, thread-cells (Fadenzellen).
The vascular supply and exact location of the nephridial
tubules (each tubule representing a xephridium, according
to Lankester’s nomenclature) are shown in Fig. 31. The
figure represents a piece of the upper wall of the pharynx,
cut out in such a way as to expose the inner wall of the
dorsal coelom. The cross is placed at the cut edge of the
double-layered membrane which separates the dorsal ccelom
from the atrial cavity. This cut edge can be traced from
side to side of the figure. The membrane is seen to be
continued down each primary gill-bar, in company with the
extension of the ccelom, which runs down the primary bars
into the endostylar coelom as described above. On the
other hand, the membrane skips over the tongue-bars, so
that the atrial cavity is prolonged dorsalwards into a deep
INTERNAL ANATOMY. 6 3
bay, corresponding to each tongue-bar. (Cf. Fig. 29.)
This is what produces the sinuous, or notched, appearance
to the membrane in question, and led Johannes Miller to
speak of it as the /zgamentum denticulatum. (Cf. Fig. 28.)
The external or atrial opening of the tubule lies against
the tongue-bar at the head of this bay-like extension of the
atrial cavity (Fig. 31 on the right).
The vascular supply of the tubules is effected in each
case by the co-operation of two blood-vessels ; namely, the
Fig. 31.— Plastic figure illustrating the blood-supply (glomeruli) of the excre-
tory tubules. On the right, the drawing is taken at a deeper level, to show the
atrial opening of the tubule over against a tongue-bar. (After BOVERI.)
5. Cut edge of ligamentum denticulatum. c.v. Coelomic vessel of primary bar.
¢.u. External vessel. z.v. Internal vessel. d.a. Left dorsal aorta.
calomic vessel of the primary bar (cf. Figs. 15 and 21) and
the external vessel of the secondary, or tongue-bar. As
soon as the ccelomic vessel of a primary bar arrives at the
level of a tubule, it gives off a number of branches, which
not only anastomose among themselves, but become united
with a similar series of anastomosing vessels which origi-
nate from the external vessel of the next-following tongue-
64 ANATOMY OF AMPHIOXUS.
bar. In this way, a complicated plexus of blood-vessels is
formed around and about the tubule. This vascular plexus
is known as a glomerulus.
The blood charged with whatever waste matters it may
have gathered up in its course through the body arrives
eventually at the glomeruli, where it is considerably
delayed on account of the vascular plexus through which
it has to pass before reaching the dorsal aorta. During
this delay, it is exposed to the glandular excretory action
of the tubules, by which the waste products are extracted
from the blood by osmotic action. From the glomerulus
the blood is conducted by two efferent vessels, corre-
sponding respectively to the primary and_ tongue-bars,
into the dorsal aorta. The communication between two
neighbouring glomeruli, as shown in Fig. 31, is, according
to Boveri, the exception and not the rule.
The distribution of these remarkable excretory tubules
or nephridia is coextensive with that of the pharyngeal
gill-clefts. They extend from the anterior to the posterior
extremity of the pharynx, but not beyond this. They
never have more than one opening into the atrial cavity,
but those occurring in the mid-region of the pharynx have
several, sometimes as many as nine, openings into the dor-
sal coelom. The number of ccelomic openings decreases
anteriorly and posteriorly, until, at the two extremities
of the pharynx, there is only a single ccelomic opening
to the tubules.
In a full-grown individual, Boveri has counted ninety-
one tubules on one side of the pharynx, the total number
therefore being double this.
The serial distribution of the excretory tubules, one
after the other, is known broadly as a metameric arrange-
ment. But since they correspond in number and situa-
INTERNAL ANATOMY. 6 5
tion to the primary gill-clefts, which are much more
numerous than the myotomes in the region of the body
in which they occur, their arrangement is more strictly
defined as dranchiomeric. In the larva, however, the pri-
mary gill-slits correspond numerically with the myotomes
or muscle-segments of the pharyngeal region, only sec-
ondarily becoming more numerous. The branchiomeric
arrangement of the excretory tubules of Amphioxus need
not, therefore, prejudice their claim to be regarded as
segmental structures.
If, now, we attempt to compare the meee al system
of Amphioxus with the kidney of the higher types, we
shall find that here also, as in so many other instances,
the permanent state of things in the former becomes a
characteristic feature of the embryo in the latter.
As is well known, the kidney of the higher Vertebrates
comprises a mass of convoluted tubules, the wsznzferous
tubules, imbedded in a matrix of fibrous connective tissue,
and enclosed within a common sheath, and so producing
collectively a compact organ which we call the kidney.
If, neglecting the highly elaborate structure presented
by the kidney of Birds and Mammals, we take, as a typi-
cal example of a primitive Vertebrate renal organ, that of
a tailed Amphibian, we find after a superficial examina-
tion the following characteristic features. In the newt,
for instance, the surface of the elongated kidney is studded
with numerous small apertures. These are surrounded by
vibratile cilia, and lead directly from the body-cavity into
the convoluted renal tubules. They are, therefore, the
ccelomic openings or funnels of the latter, and are known
as nephrostomes. Close to the nephrostome a short diver-
ticulum of the tubule leads to a capsule which encloses a
glomerulus. After a winding course in the substance of
66 ANATOMY OF AMPHIOXUS.
the kidney, the tubules emerge from the latter as a series
of efferent ducts placed one behind the other, and these
again open into a common longitudinal duct on each side
of the body, known as the wrezer, which leads the products
of excretion backwards to the cloaca.
The permanently functional kidney of Fishes and Am-
phibia is known as the mesonephros. In Reptiles, Birds,
and Mammals, this is only functional during the embryonic
period, and later is replaced in a way not yet fully eluci-
dated by the permanent kidney of these forms which is
known as the mmetanephros.
The ureter, or duct, of the mesonephros, is spoken of as
the mesonephric duct, while the renal tubules constitute,
collectively, the glandular portion of the kidney.
The permanent kidney of the craniate Vertebrates is ab-
solutely unique among all the other glands of the body, in
the fact that the glandular portion of the organ arises
independently of the duct, and only communicates secon-
darily with it. Moreover, the duct develops in point of
time before the gland. This is a very extraordinary fact,
and taken alone would be quite inexplicable. It has been
found, however, that the mesonephric duct has primary
relations with a totally distinct set of excretory tubules,
which differ from those mentioned above, both in their
position in the body and in their mode of development.
These primitive tubules, which mark the first appearance
of a renal organ in the Vertebrate embryo, constitute the
pronephros.
The degree of development attained by the pronephros,
or primitive kidney, in the life-history of the various types
of Vertebrates, is very different in the different classes.
Frequently, as with the Selachians (sharks), Birds, most
Reptiles, and with the Mammals, the pronephros is an
INTERNAL ANATOMY. 67
entirely rudimentary structure, which puts in a fleeting
appearance during the embryonic development, but never
functions as a kidney.
In other cases, as with the Teleostomes, or bony fishes,
Amphibians, Crocodiles, and Turtles, the pronephric sys-
tem attains a higher grade of development, and actually
functions for a time as the sole kidney of the animal. In
some of the bony fishes (e.g. Zoarces and Merlucius), it
functions as the kidney for an extraordinarily long time,
apparently throughout the period of adolescence. In one
curious instance of a fish, /zervasfer, which has acquired a
semi-parasitic habit, it appears that the development has
been arrested to such an extent that the pronephros
functions as the principal organ of excretion throughout
life, the mesonephros remaining rudimentary (EMERY).
The most extensive pronephric system which has as yet
been described for any craniate Vertebrate, is that repre-
sented diagrammatically in Fig. 32. This is the /arval
excretory system of a remarkable worm-like legless Am-
phibian, /ekthyophis glutinosus, belonging to a very primi-
tive subdivision of the Amphibia known as the Cecz/ianz,
which occur in the hot regions of South America, Africa,
Seychelles, East Indies, and Ceylon.
We owe our knowledge of this elaborate pronephric
system to RICHARD SEMON of Jena.
It consists of some twelve pairs of irregularly contorted
tubules placed dorsal to the general body-cavity in a posi-
tion which is described as retro-peritoneal, and arranged seg-
mentally, one behind the other, on either side of the dorsal
aorta. Broadly speaking, the canais run outwards in a
transverse direction. Near their inner extremities they
usually divide into two short branches, which terminate
each in a funnel-shaped opening into the body-cavity.
68 ANATOMY OF AMPHIOXUS.
geo were - - - — oe
Fig. 32.— Pronephric system of embryo of Ichthyophis, reconstructed from sec-
tions, and represented as having been spread out in one plane. (After SEMON.)
a. Dorsal aorta. c. Portions of the coelom into which the nephrostomes of the
pronephric tubules open. The inner portion of ccelom (next to aorta) is shut off
from the rest of the ccelom, and becomes associated with the vascular outgrowths
from the dorsal aorta (which produce the glomeruli) to form the Malpighian cap-
sules of the pronephros. The Malpighian tractus is continued backwards as
a metamorphosed and rudimentary cord of cells, nearly to the cloaca, and con-
stitutes the so-called Nebenniere or Interrenal body. This backward extension
of the Malpighian body of the pronephros probably indicates the former existence
of a much more extensive pronephric system. #. Convoluted pronephric tubules
lying above the peritoneum (shaded light), each provided with two nephrostomes,
inner and outer, and opening peripherally into d, the longitudinal pronephric duct
(Wolffian duct), which becomes the mesonephric duct after the degeneration of
the pronephric tubules and the formation of the mesonephric tubules have taken
place. mm. Rudiments of the mesonephric tubules.
N.B.—The pronephric tubules are here characterised by the possession of
coecal outgrowths.
INTERNAL
ANATOMY. 69
These are the ccelomic openings, or nephrostomes, of the
tubules.
At their outer ends most of them open directly
into a longitudinal duct, the pronephric duct, which extends
backwards to the cloaca.
The most anterior tubules,
however, tend to fuse to-
gether at their outer ex-
tremities, before reaching
the common duct. Corre-
sponding to each tubule
there dsera
growing out from the dor-
short artery
sal aorta, and abutting with
its blind end against the
portion of the body-cavity
into which the innermost
nephrostomes open.
Later on these ccecal
outgrowths from the dorsal
aorta develop a vascular
network at their free ends,
and so produce a series of
glomerult.
If, now, we inquire into
the mode of development
of such a pronephric sys-
tem as the one above de-
scribed, we find that its
component tubules arise as
a series of knob-like seg-
mental outgrowths from
the outer or somatic layer
Fig. 33. — Schematic transverse section
through a Selachian embryo in the region
of the pronephros. (After VAN WIJHE.)
The dotted line drawn across the section
indicates the plane of division between the
upper segmented and the lower unseg-
mented portions of the primitive body-cavity
(proccelom). my. Myotome or myomere.
ms. Mesomere or nephrotome. /. Prone-
phric outgrowth. sf. Unsegmented body-
cavity or splanchnoceel. sc. Sclerotome.
n. Nerve-tube. ch. Notochord. ao. Dor-
sal aorta. a/. Digestive tube.
of the peritoneum at the base
of the segmented portion of the primitive body-cavity.
7O ANATOMY OF AMPHIOXUS.
These outgrowths are at first solid cell-proliferations of
the peritoneal epithelium, in the midst of which a lumen
is subsequently formed between the cells. As soon as
this occurs, the peritoneal thickenings represent hollow
diverticula of the ccelom, each communicating with the
latter by a single nephrostome (Fig. 33).
The incipient tubules then grow outwards until they
reach the ectoderm with which, in the Selachians, they
become fused. This has been taken by Riickert to indi-
cate that the tubules originally discharged the products
of excretion directly to the exterior by a series of indepen-
dent apertures at the points of fusion. (Cf. Fig. 34 A.)®
The pronephric tubules next commence gradually to relin-
quish their coalescence with the ectoderm from before
backwards, retaining, however, for the present the connec-
tion behind (Fig. 34 B).
Meanwhile the distal ends of the successive tubules
undergo confluence (Fig. 34 B), and in this way the begin-
ning of a longitudinal duct is produced. This duct now
gradually splits itself off from the ectoderm, so that the
posterior connection with the latter is carried farther and
farther back until it reaches the region of the cloaca, when
it leaves the ectoderm and acquires an opening into the
cloaca (Fig. 34 C). Meanwhile, however, in the Sela-
chians, the pronephric tubules begin to undergo a retro-
gressive development and atrophy, as a consequence of
which the pronephros as a gland becomes aborted.
In the same way, but at a much later stage, the remark-
able pronephric system of Ichthyophis becomes entirely
aborted. But the duct remains, and a new set of tubules
appear at the bases of the somites, which secondarily open
Into 16 (ie. 34°C):
These new tubules are the mesonephric tubules, and,
INTERNAL ANATOMY. 71
although they occur mostly behind the region of the pro-
nephros, yet rudiments of them appear in the same seg-
ments occupied by the latter. Unlike the pronephric
tubules, they arise, not as evaginations from the base of
the somites, but in such a way that an adjacent portion
of the somite, lying dorsal to the pronephric tract, loses
A
1
é
in
'
os
'
«
p
'
se
‘
t
‘
‘
7
Ll
Ul
Fig. 34.— Three diagrams illustrating the hypothetical phylogenetic develop-
ment of the excretory organs in Selachians. (After RUCKERT.)
s. Somites. fx. Pronephric tubules fused with ec, the ectoderm in 4; collected
into a common duct w.d, the Wolffian or pronephric duct in 8; and finally
aborted in C, with the exception of one, which persists as the ostium abdominale.
mn. Mesonephric tubules. w.d. Pronephric duct in B; mesonephric duct in C.
cl, Cloaca. . Posterior region.
its primary connection with the rest of the somite, which
consists of the myotome proper, and becomes bodily con-
verted into a mesonephric tubule whose blind end curves
round the pronephric duct and eventually opens into it;
while its point of communication with the unsegmented
72 ANATOMY OF AMPHIOXUS.
body-cavity persists as the nephrostome. (Cf. Figs. 33
and 35 &.)
The pronephric duct, therefore, becomes secondarily
employed in the surface of the mesonephros. So that,
while the mesonephros and its future duct form two dis-
tinct morphological structures, the pronephros and the
same duct form one inseparable whole.
From the above considerations we may conciude that
the pronephros represents the primitive and ancestral
excretory organ of the craniate Vertebrates. Just as the
notochord has been largely replaced first by cartilage and
then by bone, so the pronephros has been replaced first
by the mesonephros and then by the metanephros.
Returning now to Amphioxus, we have to note in the
first place the absence of a common matrix surrounding
the excretory tubules, and, secondly, the absence of a com-
mon duct. Since in the higher Vertebrates the interstitial
growth of connective tissue among the tubules, binding
them together into a compact organ, is a secondary phe-
nomenon, the absence of such a matrix in Amphioxus
need not detain us.
Judging from the analogy of the other systems of or-
gans in Amphioxus, it will be at once concluded that the
excretory tubules of the latter represent the pronephric
system of the embryos of the craniate Vertebrates. And
this, in fact, is Boveri’s contention.
As we have seen, the excretory tubules of Amphioxus
open separately into the atrial cavity. While they do not,
therefore, open directly to the exterior at the ectodermic
surface of the body, they do actually open at an ecto-
dermic surface, since the atrial cavity is a space enclosed
from the outside, and so is lined by ectoderm. The pri-
mary fusion of the pronephric tubules with the ectoderm,
INTERNAL ANATOMY. 73
which has been observed in some craniate Vertebrates as
described above, is therefore probably of the same nature
as the ectodermic openings of the tubules in Amphioxus.
QW
Fig. 35.— 4. Schematic transverse section through pharyngeal region of Am-
phioxus. On the left is a branchial bar, cut lengthwise, and on the right a gill-slit.
4. Schematic transverse section through Selachian embryo. (After BOVERI.)
atc. Atrial chamber. 7.7.d. Pronephric duct. c.o. Nephrostome of pronephric
tubule. 4.4. Cross-section of excretory tubule in Amphioxus. a.f Opening of
excretory tubule into atrium in Amphioxus. g.c. Gonadic cavity (perigonadial
coelom) in 4; compared by Boveri with the mesonephric tubule, mest. in B.
g?. Glomerulus. ce, Ceelom. e.c. Endostylar ccelom. s.z.v. Branchial artery in
A; sub-intestinal vein in 2.
Other letters as in previous figures.
N.B.—In & the future opening of the mesonephric tubule into the pronephric
duct is indicated by dotted lines on the right. The vessel connecting the sub-
intestinal vein with the aorta is placed on the left of the alimentary canal for com-
parison with Fig. 4. It is really only present on the right side, although a rudiment
occurs on the left. (See Note 6.)
The glomeruli of the tubules in Amphioxus are supplied
by blood-vessels which connect the dorsal aorta with the
branchial artery. It should be remembered that the bran-
chial artery represents the anterior portion of the sub-
74 ANATOMY OF AMPHIOXUS.
intestinal vein, and in the young larva the two vessels are
continuous. The direct continuity is subsequently inter-
rupted by the development of the hepatic coecum, and the
consequent insertion of a capillary portal system into the
circulation. In the Selachian embryo, a series of similar
vessels, six in number, connecting the dorsal aorta with
the sub-intestinal vein, have been shown to be in close cor-
respondence with the pronephric tubules, and to form at
the level of the tubules a series of rudimentary glomer-
uli (Figs. 35 A and B).®
Such resemblances as the above are demonstrative, and
are sufficient to prove that the excretory tubules of Am-
phioxus belong to the pronephric system, and that in this
respect, also, the adult Amphioxus presents features which
are characteristic of the embryos, or larve, of the higher
forms.
Although convinced as to the essential identity of the
excretory tubules of Amphioxus with the pronephros of
the craniate Vertebrates, it must be remembered that
there is one apparently great difference between them.
Whereas in Amphioxus the pronephros (applying this
term to the tubules considered collectively) occurs in the
region of the perforated pharynx, in all the higher Verte-
brates it occurs behind the pharynx, and is quite absent
from the region of the gill-slits. This difference, however,
which might at first sight appear serious, is, in reality,
most instructive. As Boveri points out, it shows almost
conclusively that the pharynx of Amphioxus does not
correspond to the pharynx alone of the higher forms, but
to the pharynx together with the anterior portion of the
alimentary canal.
In the Craniota the gill-clefts, which are present in a
limited number, have beaayirvorves in the complicated
rig
INTERNAL ANATOMY. 75
process of cephalisation, by which the Vertebrate head has
been evolved. They are innervated exclusively by the
cranial nerves, and in fact are considered as forming part
of the head. In Amphioxus there is, broadly speaking, no
head, and the region of the gill-slits forms part of the trunk.
In the evolution of the Craniota, therefore, what has hap-
pened is that the gill-clefts have been relegated to the
head, while the excretory tubules have become confined to
the trunk, and have ceased to occur in the neighbourhood
of the gill-clefts. Only the anterior region of the pharynx
of Amphioxus is represented by the pharynx of the higher
forms. The greater part of it corresponds to the unper-
forated portion of the alimentary canal, which follows
immediately behind the pharynx in these forms, extending
to the liver.
We have referred above to the absence of a pronephric
duct in Amphioxus. Although this is true in the strict
sense of the term, yet Boveri gives reasons for supposing
that the right and left pronephric ducts are in a measure
represented by the right and left halves of the atrial
chamber. (Cf. Fig. 35, 4 and &). We will first glance
briefly at the mode of
Development of the Atrial Cavity.
For the sake of avoiding complications, it will be well to
confine the description at present to the mode of origin of
the atrial cavity in its posterior region. It arises of course
on the same principle throughout its whole extent (except
the post-atrioporal continuation, which grows back later),
but anteriorly it is involved in the asymmetry which is such
a marked feature of the larva, and will be considered in the
chapter on the general development.
The first indication of thesfature atrial cavity appears in
76 ANATOMY OF AMPHIOXUS.
a young larva with some six or seven gill-slits in the form
of two longitudinal thickenings of the integument on the
ventral surface of the body. These are at first solid, but
eventually become hollowed out so as to enclose a longitu-
dinal canal on each side. This is the so-called metapleural
canal or lymph-space. The thickenings enlarge to the
extent of forming two well-marked folds of the body-wall ;
namely, the metapleural folds.
The next stage is marked by the formation of two small
solid longitudinal ridges on the inner opposed faces of the
metapleural folds (Fig. 36). It is by the subsequent
> Wes
“tye WM Mf
jj a ‘ f & V
i; ip V %
Gail) x
Figs. 36 and 37. — Schematic transverse sections through post-pharyngeal
region, illustrating mode of origin of atrial chamber. (After LANKESTER and
WILLEY.)
ao. Aorta. 6.c.Ccelom. +m and lm. Right and left metapleural folds. s.a.7. Sub-
atrial ridges, which fuse together to form the floor of a/, the atrium. if. Aliment-
ary canal. s.z.v. Sub-intestinal vein.
SS
meeting and coalescence of these sudatrial ridges that the
atrial cavity becomes enclosed as a small median tube lined
by ectoderm.
As soon as it has become closed off from the exterior,
the atrial tube commences to grow in size, and it gradually
INTERNAL ANATOMY.
ha
expands laterally and also in an upward direction, propor-
tionately reducing the extent of the ccelom as it does so
(Fig. 37; cf. also Figs 26):
At its posterior extremity the
atrial tube does not become closed in, but remains perma-
nently open as the atriopore.
It is a curious fact that the
fusion of the subatrial ridges
to enclose the atrial tube takes
place gradually from behind
forwards, so that for a long
time the latter has the form
of a canal open to the exterior
at both ends. The chief feat-
ures in the formation of the
atrium are shown diagrammat-
ically in Fig. 38, A, B, and C.
In Fig. 38 A the atrial tube
has not begun to be closed in,
but the two metapleural folds
are seen running side by side
for some distance. Anteriorly
the development of the right
metapleur is in advance of that
of the left, and it is seen to
bend round to the right side
of the body in correspondence
with the asymmetry of the gill-
slits (vide infra). Having ar-
rived at the front end of the
pharynx, the right metapleur
bends sharply inwards to the
gradually dies out in front.
Fig. 38.— Three plastic diagrams
of larvze of Amphioxus from the ven-
tral aspect, illustrating the mode of
enclosure of the atrial tube from be-
hind forwards. The atrium is still
entirely unclosed in 4; partially
closed in &; and almost completely
closed in C. (After LANKESTER and
WILLEY.)
p.s. Primary gill-slits. 7. Right
metapleur. 7.2. Przeoral pit. 0. Mouth.
at.p. Atriopore.
mid-ventral line and then
In Fig. 38 B the subatrial
ridges have met and fused for a short distance behind the
78 ANATOMY OF AMPHIOXUS.
pharynx, so as to enclose a tube which corresponds to that
portion of the future atrial cavity which lies between the
atriopore and the hinder end of the pharynx. Finally,
in Fig. 38 C, the closure of the atrial tube has advanced
forwards over the gill-slits almost to the anterior extremity
of the pharynx, still leaving, however, one or two gill-slits
open directly to the exterior in front. Meanwhile, the
floor of the atrium has increased in width, and the meta-
pleural folds are separated by a wider interval than before
(Fig. 38 C). Eventually the atrium closes up completely
in front, so that the gill-slits no longer open directly to
ENG vexXt Emon,
Remembering that the atrium of Amphioxus arises as an
unpaired median tube (see below, IV.), while the pro-
nephric duct is always paired, the following are some of
the reasons for supposing a partial homology between the
two structures :—
(a) They are both derived, either wholly (atrium), or in
a large measure (pronephric duct), from the ectoderm.®
(8) They both receive and carry away the excretory prod-
ucts from the pronephric tubules; and (y), they are
both, to a greater or less extent, lined by an epithelium,
which is itself glandular and excretory.’
Comparison between the Excretory System of Amphioxus
and that of the Annelids.
Having considered the relation existing between the
pronephric system of Amphioxus and the corresponding
system in the embryonic and larval stages of the higher
Vertebrates, we will now pass on to a brief comparison
with the excretory system of the Invertebrates.
The excretory system of a typical Annelid presents
INTERNAL ANATOMY. 79
certain resemblances to that of Amphioxus, in that it
occurs in the form of distinct segmental tubules, or
nephridia, each possessing a funnel-shaped opening into
the body-cavity, and an opening to the exterior at the sur-
face of the body.
It was, in fact, the recognition, some twenty years ago,
by SEMPER and BALFour, of the resemblance between the
arrangement of the nephri-
dia of the Annelids and
the primary segmental ori-
gin of the kidney of the
Craniota that was chiefly
instrumental in placing the
Annelid-theory of Verte-
brate descent on a tempo-
rarily firm basis.
A dissection of the an-
terior portion of the body
of an earthworm, exposing
Fig. 39.—Anterior portion of earth-
the nephridial tubules, is
shown in Fig. 39. A pair
of such convoluted tubules
occurs in each segment, or
worm dissected open from above to show
the nephridia and nervous system. (From
W. T. SEDGWICK and E. B. WILSON’s
General Biology.)
pr. Prostomium (preoral lobe). c.g.
Cerebral ganglion, which has receded from
the prostomium from the ectoderm of
which it arose. com. Circumcoesophageal
commissure surrounding the buccal tube
(latter not represented). v.x.c. Ventral
nerve-cord. 2. Segmental nerves. zh.
Nephridia. sf. Dissepiments.
ring, of the body, com-
mencing from the third.
Physiologically, of course,
they are directly com-
parable to the renal tubules of the Chordata, and in their
general features, allowing for the absence of a common
duct, the similarity in the two cases is striking enough.
But when this undoubted similarity is used as an argument
for deriving the Vertebrate excretory system directly from
that of the Annelids, we tread on very uncertain ground.
SO ANATOMY OF AMPHIOXUS.
If we were to consider the excretory system apart from
the rest of the organisation, this would be the only course
to follow. But when the whole organisation is taken into
account, the only justifiable conclusion seems to be, not
that the Vertebrate renal system is to be derived from that
of the Annelids, but that, as Riickert suggests, both may
possibly have been evolved from a common starting-point.
It is eminently probable that, in respect to this and the
other systems of organs, as well as the segmentation of
the body, the Annelids and Vertebrates present an in-
stance of parallel evolution. This will become more evi-
dent as we proceed. Those who uphold the so-called
Annelid-theory have no cause to complain of the absence
of a common duct to the nephridia, since this has been
found in some cases to occur.
In 1884 EpuARD MEYER discovered that in certain
marine Annelids (Lanzce conchilega and Loimta medusa)
belonging to the family of the Terebellida, the nephridia
of each side were joined together by longitudinal ducts,
which he compared, though with great reserve, to the
mesonephric ducts of the Vertebrata.* In these worms the
nephridia do not occur in all the segments of the body, but
are confined to the anterior so-called thoracic region, their
number being very limited. In the thorax, the dissepi-
ments which typically divide the segments from one
another are absent, so that the body-cavity would here
form a continuous uninterrupted space, were it not that it
is divided into two chambers, an anterior and a posterior,
of which the latter is the larger, by a muscular diaphragm.
In the anterior thoracic chamber (Fig. 40) there are three
pairs of nephridia which are united together on each side
by a short duct opening to the exterior by a single aperture.
* This discovery was also made later but independently by J. T. CuNNING-
HAM for Lance conchilega.
INTERNAL ANATOMY.
SI
In the posterior chamber there are four pairs of much
larger nephridia, which are similarly joined together by a
prominent longitudinal duct from which short processes
corresponding in number
The
duct itself ends blindly at
external apertures.
both ends, but is prolonged
posteriorly far beyond the
region of the nephridia
(Fig. 40).
(thes spresence ors sthis
longitudinal duct in these
worms is a very remark-
able circumstance, but it is
undoubtedly an expression
of the same phenomenon as
the anastomoses between
successive nephridia which
have been described by
Ersic for the Capitellidz,
as well as the complicated
series of anastomoses which
convert the entire nephri-
dial system into a marvel-
lous network of tubules dis-
covered by A. G. BouRNE
in the marine leech, Povz-
tobdella, and by BEDDARD
in the curious earthworm,
Pericheta.
to the nephridia lead to the
Fig. 40. — Schematic lateral view of
anterior end of Lanice conchilega to show
the nephridia. (After EDUARD MEYFR
from Hatschek’s Lehrbuch's der Zoologie.\
The ventral side of the body is to the
left of the figure. d. Longitudinal ducts of
the nephridia. ¢.0. Position of external
openings. /£ Nephridial funnel (=ccelomic
opening of nephridium). a. Position of
mouth; bounded by two prominent lateral
lobes, and fringed by a great number of
“feelers,” which are cut short in the figure.
?. Branchial tentacles (three on each side
of the body).
The present state of our knowledge does not admit of
an attempt to specify the particular type of nephridial
system from which that of the Annelids, on the one hand,
§2 ANATOMY OF AMPHIOXUS.
and that of the Vertebrates, on the other, took their
origin.
In view of the apparent absence of nephridial tubules
in Balanoglossus and the fact that in the Ascidians the
renal organs are special structures peculiar to this group,
it is extremely difficult to associate the Vertebrate type
of excretory system with that of any Invertebrate.
Since the Annelid-theory precludes the possibility of
Amphioxus being regarded as an ancestral form, and yet
if, nevertheless, it is, as we believe, primitive and not
essentially degenerate, the discovery of the excretory
tubules in Amphioxus happily releases us not only from
necessity, but also from the possibility of referring the
Vertebrate excretory system back to that of the Annelids.
°
Nervous System.
The central nervous system of Amphioxus consists of a
closed thick-walled tube lying along the dorsal side of the
body above the notochord.
Viewed externally, it is a perfectly plain, more or less
cylinder-shaped structure, without any constrictions or
enlargements whatever. Its largest diameter in the adult
occurs about the middle of its course, and not at its
anterior end.
Posteriorly it is nearly coextensive with the notochord,
and, like it, tapers down almost to a point.* Anteriorly it
terminates abruptly some distance behind the front end
of the notochord. (Cf. Figs. 3 and 11.)
If the dorsal nerve-cord be removed from the body and
* The extreme posterior end of the nerve-cord is usually swollen out into
a small ampulla-like dilatation. (PouCcHET, ROHON, RETzIUs.) RETzIUS
has observed that occasionally the nerve-cord is prolonged beyond the dilata-
tion and actually bends round the posterior end of the notochord.
INTERNAL
ANATOMY.
83
examined from above, its general appearance will be as
shown in Fig. 41.
In front there is a pair of nerves
which proceed symmetrically from the sides of the nerve-
tubes. “Harther back there: is
another pair of nerves which
arise more dorsally than the
anterior pair, but are likewise
placed symmetrically one oppo-
Behind this
second pair of nerves the spinal
site the other.
nerve-roots are no longer dis-
posed symmetrically, but alter-
nate with one another, in cor-
similar
respondence with a
alternation of the myotomes,
the alternation becoming more
and more pronounced as we
proceed backwards. Again, be-
hind the second pair of nerves
there are two kinds of spinal
nerve-roots, dorsal and ventral.
The former leave the nerve-cord
from its dorsal surface, and the
latter from the margins of its
ventral side. In the dorsal roots
the nerve-fibrils are collected
together to form a single com-
pact nerve round which the
sheath of the nerve-cord is con-
tinued, while in the ventral roots
4
i
Fig. 41.— Anterior portion of
spinal cord of Amphioxus; seen
from above. (After SCHNEIDER.)
Between the first pair of cranial
nerves is seen the eye-spot; one of
the branches of the second pair of
cranial nerves sometimes arises
directly from the spinal cord as
shown on the right; farther back
are seen the pigment spots of the
nerve-cord.
4
VIO
Taeeie Fr e> oO e
<v%e
the nerve-fibres emerge separately in loose bundles unsur-
rounded by a sheath, from the spinal cord.
A pair of
dorsal roots and a pair of ventral root-bundles go to each
$4 ANATOMY OF AMPHIOXUS.
segment of the body. Dorsal and ventral roots are entirely
independent of one another, and at no point do they coa-
lesce as they do in the Craniota. In further contrast to
Fig. 42 4. — Innervation of the region of the oral hood and snout. (After
HATSCHEK, slightly altered according to the statements of VAN WIJHE.)
ch. Anterior end of notochord. cz. Buccal cirri. cv, cw2. First and second
cranial nerves with their peripheral ganglia. cw. Rami cutanei dorsales. 7.4. Left
half of oral hood. 74. Right half of oral hood. 0. Olfactory pit. Spl, sp2. First
and second dorsal spinal nerves. so. Sense-organ of oral hood (groove of Hat-
schek) indicated as if seen through body-well by transparency. v. Velum.
v.n.t. Nerve to left side of velum. v2.7. Nerve to right side of velum.
N.B.— The septa between the myotomes are indicated by dotted lines. The
superficial nerves of oral hood are rendered in black; the deeper nerves, which
anastomose to form the plexus of Fusari, are left white.
the condition met with in the latter there is no ganglionic
enlargement on the dorsal root.
INTERNAL ANATOMY. 85
The first two pairs of nerves differ in many points from
those which succeed them, and are known as the cranial
nerves. Thus they have no corresponding ventral roots ;
they appear to be exclusively sensory, and do not inner-
vate any muscles; their distribution is confined to the
snout, and they are above all characterised by the pres-
ence of peripheral ganglionic enlargements which occur
chiefly on the finer branches of
the nerves near their distal ex-
tremities. Furthermore they lie
in front of the first myotome.
The first pair of dorsal sfenal
nerves (2.e. the third pair alto-
gether) belonging to the first
myotome passes from the nerve-
tube to the skin through the
dissepiment which separates the
Fig. 42 &. — Diagram illustrat-
first myotome from the second. ing the branching of a dorsal spinal
: -___ nerve of Amphioxus. (After HAT-
And so with all the succeeding .oiex)
dorsal roots, they lie at the back dy. Dorsal root. 7d. Ramus
dorsalis. yu. Ramus ventralis.
of the myotome to which they y.vi. Ramus visceralis. 7~.c. Ramus
cutaneus ventralis innervating ecto-
derm of metapleur. v7. Ventral
following segment. (Ck Figs. or motor root, indicated as if in the
= same plane as the dorsal root.
2 and 42 A.)
Shortly after leaving the central nervous system, the
belong, between it and the next
dorsal roots divide into two branches, a ramus dorsalis
and a ramus ventralis (Fig. 42). These two branches run
upwards and downwards respectively, in the gelatinous
layer of the sub-epidermic cutis; that is to say, erternal
to the muscles.
In the Craniota the corresponding branches of the
spinal nerves lie for the first part of their course zxzternal
to the muscles, between the latter and the notochord. The
86 ANATOMY OF AMPHIOXUS.
cranial nerves of the Craniota so far resemble the dorsal
spinal nerves of Amphioxus that they run external to or
ectad of the somites of the head.
The ramus dorsalis of a spinal nerve breaks up into a
number of finer nerves, which supply the skin of the back.
The ramus ventralis similarly gives rise to a number of
cutaneous nerves, but in addition it gives off a branch
which passes inwards below the longitudinal muscles of
the body-wall, between them and the transverse muscles
which lie in the floor of the atrium. This is the vzsceral
branch of the spinal nerve. The visceral nerves innervate
the transverse muscles and form an elaborate plexus on
the surface of them.*
Thus the dorsal spinal nerves of Amphioxus are of a
mixed nature, sezsory and motor, but chiefly sensory.
The ventral roots are entirely motor. On their emer-
gence from the spinal cord they spread out like a fan
and terminate upon the muscle-fibres of the myotomes
(Fig. 43).°
The muscles which are not innervated by the ventral
spinal nerves are the ¢ransverse or subatrial muscles, the
muscles of the south (velum), and oral hood, and probably
the anal sphincter. These are supplied by the so-called
visceral branches of the dorsal nerves. The nerve-supply
of the oral hood is illustrated in Fig. 42. It arises from
branches of the third to the seventh dorsal nerves. These
branches are distributed in two different ways: one set
* The visceral nerves also send up branches, which pass up through the
ligamentum denticulatum to the wall of the pharynx. (Fusari; see below,
p- -) Here they form the branchial plexus described by ROoHON, who
thought these nerves contained elements of the Vagus of the Craniota.
The portions of the visceral nerves innervating the transverse muscles (these
branches being discovered by ROLPH) were held by ROHON to contain
elements of the Syszpathetic system of Craniota.
INTERNAL ANATOMY. 87
of them runs beneath the outer surface of the oral hood
and, by the occurrence of frequent anastomoses, forms a
coarse network known as the ower plexus, while the other
set lies beneath the inner surface of the oral hood and
gives rise to the zznuer plerus. The latter was discovered
by Fusari in 1889. The two plexuses are distinct from
Fig. 43.— Transverse section through the spinal cord in the middle region of
the body. (After ROHDE.)
a. Giant fibre proceeding from the giant ganglion-cell 4 (see below). ¢.c. Cen-
tral canal. ..f1. Giant nerve-fibres, which traverse the spinal cord from before
backwards. .».f2. Giant fibres, which traverse the spinal cord from behind for-
wards. .~. Muscle-plates. 2.7. Motor nerve-fibres. 2. Longitudinal nerve-
fibres cut across. s.f Supporting fibres. s. Sheath of nerve-cord (= dura mater ;
FUSARI).
one another, except in so far as their component nerves
have a common origin from the dorsal roots (Fig. 42).
The outer plexus is continued up into the individual cirri,
while the inner plexus appears to stop short at the base
of the cirri. It has recently been discovered by VAN
88 ANATOMY OF AMPHIOXUS.
WuHE that the inner plexus on both right and left halves
of the oral hood is exclusively formed by nerves which
arise from the /ef¢ side of the central nervous system ;
and, further, that the nerve-supply of the velum is fur-
nished by branches from the fourth, fifth, and sixth dorsal
nerves of the left side only. This asymmetrical innerva-
tion of the velum and inner (glandular) surface of the
oral hood will be referred to
again after the consideration
of the larval development.
The peripheral ganglionic
enlargements which are so
characteristic of the two pairs
of cranial nerves must be cor-
related with the sensibility of
the snout. As the nerve-fibres
are continued beyond them,
they are not to be regarded as
end-organs, but simply as peri-
Fig. 44. — Peripheral ganglion- pheral ganglia. Their structure
cells of the cranial nerves of Amphi- jg shown in Fig. 44. They
oxus. (After FUSARI.) f
were discovered by the great
French naturalist QUATREFAGES in 1845. Each of them
is composed of from one to four nerve-cells, with granular
protoplasm and a large nucleus. Each group is enclosed
in a sheath which is a continuation of the sheath of the
nerve itself. The sheath is lined internally by an endo-
thelium. According to Fusari the nerve-fibres enter into
direct connexion with the cells, though some would appear
to pass round them.
The peripheral nervous system of Amphioxus can only
be compared definitely, at present, in its broadest features
with that of the higher Vertebrates. The determination
INTERNAL ANATOMY. 89
of the particular homologies in the two cases forms one of
the most difficult problems of comparative morphology. In
correlation with the low grade of cephalisation to which
Amphioxus has attained, there are only two pairs of
cranial nerves, the succeeding nerves retaining their
primitive spinal character. The dorsal spinal nerves,
furthermore, possess features which are specially charac-
teristic of the cranial nerves of the Craniota. Such are
their mixed sensory and motor functions, and the position
of their dorsal and ventral branches ectad of the muscula-
ture. As already indicated above, the walls of the gill-slits
of the craniate Vertebrates are innervated by cranial
nerves, while in Amphioxus this is done by spinal nerves.
(Cf. Fig. 92; see also below, p. 163.)
In transverse section the spinal cord of Amphioxus is
seen to have somewhat of a triangular shape. The central
canal has the form of a vertically elongated split, commenc-
ing from the vertex of the triangle, and extending two-
thirds of the way downwards into the cord. For the
greater part of its extent, however, the two sides of the
canal are closely approximated together so as to obliterate
the lumen, which widens out again below, and presents the
appearance of a circular or oval tube. The sides of the
canal are lined by an epithelium the cells of which, starting
from an indifferent condition in the embryo, have become
modified in several different directions. Some are ganglion-
cells, and others send out long radial processes which trav-
erse the substance of the nerve-cord, and serve to hold it
together. These are the supporting fibres (Fig. 43). The
cells in the nerve-cord form a much smaller proportion of
the bulk of it than the nerve-fibres do. The latter run
mostly in a longitudinal direction, and produce a punctate
appearance in cross-section.
gO ANATOMY OF AMPHIOXUS.
Anteriorly in the region of the cranial nerves the lumen
of the central canal widens out into a relatively spacious
vesicle, known as the cerebral vesicle (Fig. 45). In young
individuals this cavity opens by an aperture called the
neuropore into the base of an epidermal pit, which we
have already described under the name of the olfactory
git. Later on the neuropore closes up, but its former
A
Fig. 45.— 4. Brain and cranial nerves of a young Amphioxus of 3 mm. length.
B, C, YD. Sections through different portions of brain: B, through neuropore and
cerebral vesicle; C, through the intermediate portion, and VD, through the dorsal
dilatation of central canal. (After HATSCHEK.)
ch. Notochord, c.v. Cerebral vesicle. déZ, Dorsal dilatation (Hatschek’s Fossa
rhomboidalis), e, Eye-spot. xf. Neuropore. o/f Olfactory pit.
/, 71, First and second cranial nerves.
cy eee)
presence is indicated by a shallow groove at the base of
the otherwise solid stalk connecting the olfactory pit with
the roof of the brain.
Behind the cerebral vesicle the lumen of the central
canal widens out in its dorsal portion independently of
INTERNAL ANATOMY. QI
the ventral tube, so as to form a vesicular dilatation cov-
ered over by a thin membrane. The region of the nerve-
tube, over which this dorsal dilatation extends, has been
compared by HatscuHEk, who discovered it, to the medulla
oblongata of the craniate Vertebrates, which is similarly
roofed in only by membrane. In the fully grown condi-
tion, however, it seems to be largely obliterated by the
Fig. 46. — Transverse section through the spinal cord between the second and
third sensory roots. (After ROHDE.)
gc. Dorsal aggregation of ganglion-cells (extending between the second and
fifth pairs of sensory nerves; a somewhat similar group of ganglion-cells occurs on
ventral side of nerve-cord below the central canal between the fourth and sixth
sensory nerves.)
dr. Dorsal root. s.f Supporting fibres. c.c. central canal; in this case equally
wide throughout its entire height, and so all along the spinal cord. sf, Sheath of
nerve-cord.
development of a mass of large ganglion-cells which ex.
tend backwards as far as the fifth pair of sensory nerves
(Fig. 46).
All there is of a brain in Amphioxus is shown in Fig.
45. The cerebral vesicle is a plain cavity without any
true subdivision into ventricles.2 In the development of
92 ANATOMY OF AMPHIOXUS.
the central nervous system of the higher Vertebrates, a
stage is passed through which may be compared broadly
with the permanent condition of things in Amphioxus.
But in the former the anterior portion of the medullary
tube quickiy becomes greatly enlarged in contrast to the
spinal cord proper, and becomes divided by constrictions
into fore-, mid-, and hind-brain, which constitute the three
primary divisions of the Vertebrate brain. Then the
brain undergoes a flexure round the anterior end of the
notochord. This curvature of the primitively horizontal
brain-region in the craniate Vertebrates is known as the
cranial flexure. (Cf. Figs. 23 and 24.)
Among the numerous longitudinal nerve-fibres which
compose the bulk of the spinal cord of Amphioxus, there
are some which stand out in
marked contrast to the great
majority on account of their
large size. These are the <so-
called evant-fibres, and they form
one of the greatest peculiarities
in the spinal cord of Amphioxus.
According to RoubE there are
no fewer than twenty-six of these
_ giant-fibres present, and each of
Fig. 47.— Transverse section ;
through spinal cord in region them arises from a correspond-
of giant ganglion-cell G. (After
ROHDE.)
a, Process of giant-cell 4. gf so-called giant-cells have many
Giant-fibres.
ing gtant ganglion-cell. These
processes, z.e. they are mz/¢2-
polar, but they each send out one main stem, which is a
giant-fibre. The giant-cells lie across the middle of the
central canal, and the giant-fibres pass outwards alter-
nately to the right or left of the central canal, and then
bend downwards and pass below the central canal and up
INTERNAL ANATOMY.
to the opposite side of the canal, where
they continue their course in the longitu-
dinal direction (Fig. 47). The giant-fibre
belonging to the most anterior giant-cell
differs in several respects from the other
giant-fibres. It is much larger than the
others, and, whereas the latter lie on either
side of the nerve-cord, the fibre in question
lies in the middle line immediately below
the central canal (Figs. 43 and 47).
These giant-fibres traverse the spinal
cord almost throughout its entire length,
stopping short at some distance from its
anterior and posterior ends. The giant-
cells are arranged one after the other in
two groups, one group lying in the anterior
third of the spinal cord, the fibres from
which run backwards, and the other group
occupying the posterior third of the cord,
the fibres from which run forwards (Fig.
48).
The giant-fibres are in no direct con-
nexion with the outgoing nerves, but the
giant-cells usually occur opposite a sensory
(z.e. dorsal) root (Fig. 49).
In the spinal cord of Petromyzon giant-
fibres are present in considerable numbers,
Fig. 48.—Scheme illustrating the course of the giant-
fibres and their origin from the giant-cells 4—Z in the spinal
cord of Amphioxus. (After ROHDE.)
98
Fig. 48.
A-L. Giant ganglion-cells whose giant processes traverse the spinal cord from
before backwards. A is about at the level of the sixth sensory root, counting from
the first cranial nerve. A/—Z. Giant ganglion-cells whose giant processes traverse
the spinal cord from behind forwards. 4¢ is about at the level of the fortieth sen-
sory root.
94 ANATOMY OF AMPHIOXUS.
while in the higher Fishes and tailed Amphibia, as well
as in the tadpoles of the anourous Amphibia, the giant-
fibres are represented by the so-called fibres of Mauthner.*
They are not found in the spinal cord of adult tailless
Amphibia, Birds, and Mammals.”
Their occurrence in such large numbers in Amphioxus
is therefore the symbol of an archaic organisation.
Giant-fibres form a very striking feature in the ventral
nerve-cord of many Invertebrates. Here, however, they
Fig. 49.— Part of spinal cord seen from above; from a preparation stained
with methylene-blue. (After RETZIUS.)
g.c. Giant ganglion-cell lying across central canal. mo. Motor root. s. Sensory
root.
appear often to lose their nervous function, and serve
rather as elastic supporting rods for the nerve-cord. They
are enclosed in thick sheaths of connective tissue, and
have been found to originate in giant ganglion-cells.
When the enclosed nerve degenerates, they become hol-
low tubes containing a coagulable fluid. (ErsiG.)
With regard to the internal origin of the nerves which
pass out from the spinal cord, our knowledge only extends
to the dorsal roots. At the base of the ventral roots the
* Also known as Miillerian fibres.
INTERNAL ANATOMY. 95
fibres appear to stop, and in their place a peculiar granular
structure of unknown significance is found (Fig. 49).
The fibres which constitute a dorsal root are derived
from two sources. Part of them are continuations or
branches of the longitudinal fibres on the same side of the
nerve-cord, on which a given dorsal root may be, while the
other moiety appears to arise largely from groups of small
bipolar ganglion-cells in the neighbourhood of the central
Fig. 50.— Diagram illustrating the internal origin of the nerve-fibres of a sen-
sory root. (Combination of two figures of RETZIUS.)
The cells giving rise to the processes lying on the same side as a sensory root
S, which divide into a T at the base of the root, are naturally in contiguity with
the central canal, but are displaced for the purpose of the diagram. m./. Middle
line.
canal, which send one process each in the direction of the
dorsal root, and another process from the opposite pole of
the cell to join in with the longitudinal fibres of the other
side of the spinal cord (Fig. 50)."
We will now compare, or rather contrast, the central
nervous system of Amphioxus with that of an Annelid
such as the common earthworm. The type of nervous
system presented by the latter is common to a vast propor-
tion of the Invertebrates. It consists essentially of three
96 ANATOMY OF AMPHIOXUS.
very sharply defined parts (Fig. 39); namely, (i.) the cerebral
or supraesophageal ganglion, which is situated dorsally
over the buccal cavity; (1i.) a longitudinal solid nerve-cord
composed of two more or less distinct halves, running
along the whole length of the ventral side of the body
below the alimentary canal; (iiil.) the czrvcumesophageal
nerve-ring OY commissure Which encircles the buccal tube
and connects the cerebral ganglion with the swbesophageal
ganglion at the anterior extremity of the ventral nerve-
cord.
Viewed from above (as in Fig. 39), the ventral nerve-
cord presents a series of constrictions which are in some
forms very pronounced. The wider portions occur in the
middle of the body-segments, and constitute the ventral
ganglia, which are strung together by the intervening
nerves (connectives) in the form of a ganglionic chain.
From the ganglia, paired nerves pass out to the organs of
the body.
One of the greatest peculiarities in the type of nervous
system above described lies in the fact that the alimentary
canal passes through and is surrounded by a portion of
the central nervous system ; namely, the circumcesophageal
commissure. This fact has been one of the most serious
difficulties which the upholders of the Annelid-theory have
had to contend with.
In the Chordata the alimentary canal does not pierce
the central nervous system in any sense whatever.* Never-
theless, there have been many conjectures as to a possible
equivalent of the circumoesophageal nerve-collar in the
Vertebrates, although it is safe to say that nothing of the
kind really exists.
* Balanoglossus might be said to offer an exception to this rule (see
Chap. V.).
INTERNAL ANATOMY. 97
The ventral nerve-cord of the Annelids is no doubt in
part physiologically equivalent to the spinal cord of the
Vertebrates ; but since the two structures lie on opposed
sides of the body, it is difficult to regard them as morpho-
logically equivalent. Those who defend the Annelid-theory
have postulated the occurrence of a half-revolution of the
body in the supposed Annelid-like ancestors of the Verte-
brates, as a result of which they acquired the habit of per-
forming their locomotion, perhaps swimming, on their backs
so that the ventral surface was turned uppermost. In this
way, we are to suppose the original dorsal and ventral
surfaces became reversed. This phylogenetic acrobatic
feat with all its consequences is hard to imagine, and
there are other alternatives which make it an unnecessary
assumption. (See below, V.)
The chief fundamental differences between the dorsal
spinal cord of Amphioxus and of Vertebrates generally,
and the ventral ganglionic chain of the Annelids, may be
summed up as follows :—
Amphioxus. Annelids.
1. Nerve-cord is hollow. Nerve-cord is solid.
Be ss ‘* dorsal. ee ‘* ventral.
ee ee ‘* unconstricted. ae ‘* constricted.
4. “s ‘* single. me ‘* double.
5. Ganglion-cells lie inside the Ganglion-cells lie outside the
fibrous layer. fibrous layer.
As for the resemblances, in both cases nerves are given
off segmentally, and also giant-fibres are present, whose
function, however, is apparently very different in the two
Gasesy
98 ANATOMY OF AMPHIOXUS.
NOTES.
I. (p. 49.) LANKESTER has made the suggestion that there
are not distinct capillaries and ccelomic space around the hepatic
ccecum, but that the space itself is capillariform. This view is in
accordance with what one observes in transverse sections.
2. (p. 50.) The fullest account of the contractile blood-
vessels of Amphioxus, as observed in the living animal, is that
given by JOHANNES MULLER. He observed the peristaltic con-
tractions of the branchial artery (which is filled with a perfectly
colourless blood), beginning from its hinder end, where it is joined
by the hepatic vein (which also undergoes peristaltic contraction
from before backwards along dorsal side of coecum) and extend-
ing to the front end of the pharynx. ‘The intervals between the
successive contractions last about a minute. Immediately suc-
ceeding upon the contraction of the branchial artery, the bulbils,
which occur at the base of the primary or“forked gill-bars, contract
too. He says that the heart-like “aortic arch” which occurs to
the right of the velum (he thought there was one on the left side
as well) contracts from below upwards, and that its contraction
enabled him to discover it. As mentioned in the text, van Wijhe
states that it has no communication with the branchial artery.
Johannes Miiller also observed the peristaltic contraction of the
sub-intestinal (portal vein), and states that it extends to the
anterior end of the ccecum. It should be remembered that his
observations were made on young transparent individuals, and the
statement as to the extent of the contraction of the sub-intestinal
vein is open to doubt.
3. (p. 51.) <A genital artery running longitudinally above the
gonadic pouches has been figured by Langerhans, Rolph, Schneider,
Lankester, and Boveri, but its relations to the rest of the vascular
system have not been made out. It is doubtful whether its
presence is constant.
4. (p. 58.) The “brown funnels” were discovered by Lan-
KESTER in 1875, and were subsequently compared by Bateson with
the collar-pores of Balanoglossus. (See Chap. V.) This com-
parison was made on the supposition that the posterior free oper-
INKDIIES. 99
cular fold of the so-called collar in Balanoglossus is of the same
nature as the atrium of Amphioxus ; but this is somewhat doubtful.
5. (p- 70.) For an admirable critical and historical account
of our knowledge of the development of the excretory system in
the different groups of Vertebrates, the reader may be referred to
the report on the “ Hntwickelung der Excretionsorgane,” by Pro-
fessor RUCKERT, in Merkel and Bonnet, Argebnisse der Anatomie
und Entwickelungsgeschichte, Band I., 1891. It will be sufficient
to note here that the ectodermic origin of the pronephric duct,
as briefly described in the text, only holds for the Selachians and
Mammals. It was first discovered in the latter by Grar SPEE in
1884, and confirmed later by FLemminc. In the former it was
discovered independently by van WijHE and RUCKERT (1886-8).
On the contrary, in Petromyzon, Amphibia, Reptiles, and Birds, the
duct does not arise from the ectoderm.
Van Wijhe denied the segmenfa/ fusions with the ectoderm of
the pronephric tubules in Selachians as described by Riickert.
The account given by the latter author has, however, been
indirectly confirmed by the observations of FELIx on the chick,
where the pronephric outgrowths were found in some cases to
undergo a transitory fusion with the ectoderm.
Bovert has attempted to show how the origin of the pronephric
duct can be imagined to have been gradually transferred from the
ectoderm to the mesoderm. Finally, it may be noted that,
whereas RUCKERT compared the pronephric tubules with the
Annelid nephridia, SEMPER and others employed the mesonephric
tubules for the comparison. The fallacy of the latter comparison
was first pointed out by FURBRINGER.
6. (p. 74.) In 1887 Paut Maver discovered that the sub-
intestinal vein in the Selachian (Pristiurus) embryo communicated
with the dorsal aorta, by a series of six segmental vessels which
passed up around the intestine on the right side only. Correspond-
ing to them on the left side he found short, blind outgrowths from
the dorsal aorta similar to those figured in the text in connexion
with the pronephros of Ichthyophis. Paul Mayer’s connecting
vessels soon become aborted with the exception of one which
enlarges and forms the proximal portion of the umbilical artery.
In the following year it was shown in a brilliant manner by
100 ANATOMY OF AMPHIOXUS.
RuckeErtT that these vessels occur in the same segments as the
rudimentary pronephric tubules, and give rise to rudimentary
glomeruli at the level of the tubules. (Cf. Fig. 35 B.) There
can be no doubt that these vessels are homologous with the
vessels which run through the primary branchial bars of Amphi-
oxus, and, as shown by Bovenrl, assist in forming glomeruli at the
level of the excretory tubules.
The morphological importance of these facts is very great and
has been strongly emphasised by Boveri. Whether Paul Mayer’s
connecting vessels indicate the former existence of gill-slits in that
region is not so certain, since it is difficult to decide whether
the indefinite number of gill-slits in the adult Amphioxus is a
palingenetic (ancestral) feature or not. It should also be remem-
bered that Paul Mayer found numbers of connecting vessels,
between sub-intestinal vein and dorsal aorta, in the ¢az/.
7. (p. 78.) Boveri found that the epithelium of the pronephric
duct of Myxine was of a glandular nature, comparable in this
respect to the atrial epithelium of Amphioxus.
8. (p. 86.) As shown in Fig. 43, ROHDE was inclined to
follow SCHNEIDER in the belief that the fibres of the ventral spinal
nerves were directly continuous with the muscle-plates and, more-
over, exhibited the same striation as the latter. It has recently
been shown by Gustav Rerzius that this appearance of continuity
is an illusion, as in so many other cases where nerves have been
wrongly supposed to enter into direct continuity with peripheral
end-organs. By employing Ehrlich’s method of staining nervous
tissue, zv¢ra vifam, with methylene blue, Retzius has proved that
the motor fibres of Amphioxus pass with a somewhat winding course
between the muscle-plates, and simply end on the surface of the
plates. Rarely they branch dichotomously, but there is no special
end-apparatus as in the higher forms. ‘Their connexion with the
muscle-plates is, therefore, one of intimate contiguity, but not of
continuity.
9g. (p. 91.) The cerebral vesicle of Amphioxus was discovered
in 1858 by Leuckarr and PAGENSTECHER. OWSJANNIKOW (1868)
thought it represented the fourth ventricle of the vertebrate brain.
STIEDA (1873) was the first to homologise the cerebral vesicle of
Amphioxus with the entire brain of the higher forms, and to regard
NOTES. IOI
it as representing the latter in its simplest form without any trace
of subdivision. This view has very generally been adopted. Stieda
also recognised the dorsal and ventral groups of ganglion-cells (of
which the former is shown in section in Fig. 46) as belonging to
the hinder portion of the brain. Rohde’s conception of the brain
of Amphioxus agreed very closely with that of Stieda, but he made
a more detailed study of its histological character, and defined its
limits more precisely. He concludes that the beginning of the
spinal cord proper, in the absence of any outward mark of dis-
Y-
ZN
Fig. 51.— Sagittal section through the cerebral vesicle of Amphioxus. (After
KUPFFER.)
¢.v. Cavity of cerebral vesicle. e¢. Eye-spot. .c. Dorsal group of ganglion-
cells (cf. Fig. 46). 7%f Infundibular depression. /.0. Lobus olfactorius impar..
tp. Tuberculum posterius.
tinction from the brain-region, would lie at the point marked by
the appearance of the first of the giant ganglion-cells, which he
denotes by the letter A. (Cf. Fig. 48.)
Quite recently the attempt has been made by Professor von
KUPFFER to determine in detail the delimitation of the cerebral
vesicle of Amphioxus (Fig. 51). The slight outpushing of the
wall of the vesicle towards the base of the olfactory pit has been
mentioned in the text. It was discovered by LANGERHANS in
102 ANATOMY OF AMPHIOXUS.
1876, who called it the /odus olfactorius. Kupffer has succeeded
in finding a similar structure in the embryos of other Vertebrates,
notably in Acipenser sturio (the sturgeon). He calls it the dus
olfactorius impar, and shows that it indicates the point where the
medullary tube remained for the longest and last time in direct
connexion with the external ectoderm, precisely as is the case in
Amphioxus. ‘There is thus at least one fixed point common to
the cerebral vesicle of Amphioxus and the brain of the craniate
Vertebrates. But Kupffer has found another. While it is obvious
that the anterior wall of the vesicle containing the pigment which
constitutes the eye-spot is homologous with the primary optic tract
(vecessus opticus) of the higher Vertebrates, in which pigment is,
in many cases, deposited in the embryo, Kupffer states that he
is able to detect an infundibular depression in the floor of the
cerebral vesicle of Amphioxus. Immediately behind this depres-
sion there is a prominence in the wall of the vesicle, which Kupffer
calls the ¢saberculum posterius. This point is also to be identified
in the brains of the higher Vertebrates.
The dorsal dilatation of the central canal, which Hatschek dis-
covered and compared with the fourth ventricle of the vertebrate
brain, whose roof is similarly membranous and not nervous (Fig.
45), is certainly a very curious, and apparently constant, feature
in young individuals, as I can affirm in confirmation of Hatschek.
The conclusion come to by Hatschek, however, that the lobus
olfactorius of Langerhans is the homologue of the infundibulum of
the higher forms, would appear to be untenable in the light of
Kupffer’s researches.
It is beyond the scope of this book to discuss the difficult
problem of the origin of the paired eyes of the Vertebrates, but it
may be pointed out that there is no difficulty in identifying a
stage in the embryonic development of the optic tract in the
Craniota corresponding to the permanent condition of things
in Amphioxus. This fact was first demonstrated by WILHELM
MULLER in 1874. On account of its position in front of and
below the cerebral vesicle, it is doubtful whether the eye-spot of
Amphioxus is homologous with the eye of the Ascidian tadpole.
(See below.)
10. (p.94.) Itisa significant fact that giant nerve-fibres appear
NOTES. 103
to be present in the spinal cord of all those Vertebrates whose tail
serves as an important organ of locomotion. ‘Thus, they occur in
fishes, tailed Amphibia, in the tadpoles of tailless Amphibia, and,
finally, they have been recently discovered by Max KoppeN in the
caudal region of the spinal cord of the lizard. In the frog and higher
forms they do not occur. From these considerations Koppen
thinks that there is a causal relationship between the occurrence
of giant-fibres in the spinal cord and the presence of a locomotor
tail. The caudal locomotion, characterised by the rapid swaying
motion of the tail, is not confined to the post-anal region in
Amphioxus, but involves the whole body.
Contrary to the observations of E1sic, both NANsEN and ROHDE
are of opinion that the giant-fibres of Annelids (Polychzta) have
the same physiological significance for the central nervous system
as those of Amphioxus.
Some of the older authors mistook the giant nerve-fibres for
capillary blood-vessels. As a matter of fact no blood-vessels
traverse the central nervous system of Amphioxus. It may be
added, also, that there are no medudlated nerve-fibres.
II. (p. 95.) Several suggestions have been made as to pos-
sible representatives of the spinal ganglia of the dorsal roots of
the Craniota in Amphioxus.
Omitting earlier, and obviously erroneous, suggestions, ROHDE
(1888) regarded the nuclei, which he found imbedded in the
dorsal roots, as a collection of “nervous nuclei,” comparable to
the spinal ganglia of the higher Vertebrates (Fig. 46). According
to Rerzius (1890) these nuclei are not of a nervous nature (prob-
ably belong to supporting-cells), and he ‘tentatively suggests that
the spinal ganglia are represented by groups of bipolar ganglion-
cells which occur inside the spinal cord at fairly regular intervals
in two longitudinal rows, one on each side of middle line. The
main process (axis-cylinder) of these cells divides in T-form, and
one of the branches of the T passes into the dorsal root. (Cf.
Fig. 50.)
Finally, Hatschek (1892) finds the homologues of the spinal
ganglia at the points where the dorsal nerves divide into xamus
dorsalis and ramus ventralis.
ne
DEVELOPMENT OF AMPHIOXUS.
As an introduction to the study of embryology, and as
an indispensable aid to a reasonable appreciation of the
value of embryological facts, the life-history of Amphioxus
provides an object which, for its capability of application
to almost every branch of zodlogical discussion, is perhaps
unrivalled. It is alike useful in a text-book of human em-
bryology, and in one of invertebrate zodlogy.
The reason for this obviously lies in the fact that in
Amphioxus everything has its own definite line of de-
marcation, all the fundamental structures of the body are
laid down with schematic clearness, there are no massive
agglomerations of cells forming complicated tissues, but all
the organs are of simple epithelial origin and constitution.
Whereas in many of the higher and lower animals the
greatest difficulty is often experienced in deciding to which
of the primary layers of the body this or that structure
owes its origin, in Amphioxus there is no such difficulty.
With these advantages it is, therefore, no wonder that
Amphioxus should serve as a refuge to the perplexed
embryologist.
It is not an exaggeration to say that the researches both
of KowaLevsky and of HatscuHeEk, on the development of
Amphioxus, will always rank among the classics of embry-
ological literature; while it is a familiar fact that Kowa-
levsky’s earlier work (1867) on the development of the
104
EMBRYONIC DEVELOPMENT. 105
Ascidians and of Amphioxus marks a distinct epoch in
the progress of the science of embryology.
EMBRYONIC DEVELOPMENT.
Fertilisation and Segmentation of the Ovum.
The breeding-season of Amphioxus extends, in the Med-
iterranean, from spring to autumn.
The gonadic pouches become very much distended by
the ripening of the ova and spermatozoa in the respective
sexes, and finally burst, discharging their contents into the
atrial cavity, whence they
reach the exterior through
the atriopore.! At the time
of complete sexual matu-
rity the gonads become so
large that the atrium is
used up to its utmost
capacity, and its walls be-
come stretched to such an
extent that the meta-
pleural folds are flattened
up against the sides of the
body.
The ovum is_ semi-
opaque, contains granules
Fig. 52.— Unfertilised ovum of Amphi-
oxus. Magnified about 750 diameters.
(After LANGERHANS.)
d. Yolk granules. f. Follicle. 2. Nu-
cleus (germinal vesicle), with nucleolus.
p. Protoplasmic area, free from yolk gran-
ules, surrounding the nucleus.
of yolk equally distributed throughout its substance, and
is surrounded by a cellular membrane known as the fol/icle
of the egg, and sometimes less accurately spoken of as
the wetelline membrane (Fig. 52).
Spawning, when it occurs, invariably takes place at sun-
down, —z.e. between five and seven o’clock in the evening,
—and never, so far as is known, at any other time.
106 DEVELOPMENT OF AMPHIOXUS.
Ova and spermatozoa are discharged simultaneously by
male and female individuals into the water, and fertilisa-
tion is effected in the latter medium.
The final stages in the maturation of the ovum of Am-
phioxus are very imperfectly known, and the extrusion of
the so-called polar bodies, preparatory to the process of fer-
tilisation, has not been properly studied, only one such
Fig. 53. — Fertilised ovum of Amphioxus. Highly magnified. (From a
drawing kindly lent by Professor E. B. WILSON.)
d.c. Directive corpuscle or polar body. o. Ovum. /£f Follicle.
body having been observed, whereas from the analogy of
all other sexually reproducing animals we should expect
two polar bodies (directive corpuscles) to be given off be-
fore the egg was fully mature. As soon as an ovum has
been fecundated by the entrance of a spermatozoon, the
vitelline membrane springs away from the body of the egg-
cell, leaving a wide space between the latter and the
former (Fig. 53). This expansion of the vitelline mem-
EMBRYONIC DEVELOPMENT. 107
brane is the first outward and visible sign of the accom-
plishment of the process of fertilisation.
About an hour later, —that is to say, at about 8 p.m., —
the egg becomes flattened at its two poles, and a depression
Fig. 54.— Division of ovum into the first two blastomeres. The polar body
marks the animal pole. (After HATSCHEK.)
appears at the animal pole, the latter being indicated by
the polar body. The depression deepens and extends as a
meridional furrow round the egg. Finally, the division of
the egg into two halves or d/astomeres, which remain at-
tached to one another, is completed, and the first stage in
the segmentation of the egg is accomplished (Fig. 54).
As it is beyond the scope of
this book to discuss the mechan-
ics of cell-division, the descrip-
tion of the segmentation stages
will be very brief.
The first meridional cleavage
which divides the egg into two
blastomeres is followed by an-
: : Fig. 55.— Eight-cell stage seen
other one at right angles to it, from the upper (animal) pole. Four
dividing each of the two blasto- small blastomeres (micromeres) lie
> upon four larger blastomeres (ma-
meres again into two. In this cromeres). Radial type of cleavage.
way the stage with four equal (A** ® B. Wirson.)
blastomeres in one plane is produced. Next follows an
equatorial cleavage, by which eight blastomeres are pro-
duced, the four upper cells at the animal pole being some-
108 DEVELOPMENT OF AMPHIOXUS.
what smaller than the four lower cells at the vegetative
pole, since the latter contain a greater quantity of the
yolk-spherules (Fig. 55).
The next cleavage giving rise to an embryo of sixteen
cells is meridional. Then the eight upper and the eight
lower cells become respectively
divided by equatorial cleavages,
and so the thirty-two cell stage
is reached (Fig. 56).
The embryo is now known
as a dblastula, and consists of a
mulberry-like mass of cells sur-
rounding a central cavity called
Fig. 56.— Thirty-two cell stage, : :
consisting of four rows of eight cells, the segmentation-cavity OY blas-
each ranged around a central seg-
mentation cavity (blastoccel). The
polar body is still visible at the ani- From this point of the de-
mal pole. (After HATSCHEK.)
tocal.
velopment the blastomeres go
on dividing with more or less regularity, until the wall of
the blastula consists of a great number of cells arranged
in a single layer about the central cavity.
The segmentation of the egg of Amphioxus, however,
by no means follows the uniform and stereotyped plan
that has been hitherto supposed. It has recently been
discovered by Professor E. B. Witson that Amphioxus
presents an example of a polymorphic cleavage. Instead
of following one type, it follows three types of cleavage ;
namely, a vadial type (Figs. 55 and 56), a dzlateral type
(Fig. 57), and a spiral type (Fig. 58). These three types
of cleavage are reducible to a common basis, and are con-
nected together by all possible intermediate gradations.
Wilson points out that in the bilateral type of cleavage
Amphioxus shows a close correspondence with the Ascid-
ian embryo.
EMBRYONIC DEVELOPMENT. 109
The segmentation or cleavage of the ovum results in
the formation of a spherical blastula, closed at all points,
Fig. 5'7.-— Three stages in the segmentation of the ovum, according to the
bilateral type. From the lower pole. (After E. B. WILSON.)
A. Eight-cell stage. A, B, CD. The four macromeres, above which are seen
portions of the four micromeres.
/-/. Plane of first cleavage, with respect to which the cells divide in such a way
as to become arranged in a bilaterally symmetrical manner.
//-II, Plane of second cleavage.
2B. Transition to the sixteen-cell stage.
C. Sixteen-cell stage. The line in each cell indicates the direction in which the
next division of the cell would take place.
and consisting of some 256 cells surrounding a spacious
cavity, the blastoccel.
The stages of development lead-
ing up to the blastula are known
as the segmentation stages. At
their completion, although, of
course, cell-division continues to
take place actively, yet other pro-
cesses supervene which render the _ Fig. 58.— Eight-cell stage
pgs Sears from the upper pole, illlustrat-
mere division of the individual cells jing the spiral type of cleavage.
of minor morphological importance. (fer E- B- W11s0N.)
Gastrulation.
The next phase of the development is known as the
gastrulation of the embryo. The cells forming the lower
or vegetative side of the blastula remain, throughout the
segmentation stages, somewhat larger than the rest of the
IIO DEVELOPMENT OF AMPHIOXUS.
blastula-wall. This side now becomes flattened, as shown
in Fig. 59 A. Next, the flattened side of the blastula
becomes gradually tucked up or invaginated into the
blastoceel (Fig. 59 4) until,
finally, the segmentation
cavity is completely obliter-
ated, and the invaginated
(After HATSCHEK.)
layer of cells becomes tightly
fitted up against the outer
layer (Fig. 50°C).
The embryo, now known
as the gastrula, is a double-
layered sac, the cavity of
optical transverse section.
C, The invagination is completed and the blastocoel is obliterated; optical longitudinal section.
which was produced by in-
ZN
vagination, and is known as
the premetive gastral cavity,
a
KD
.
a
Ss
Ma
Rd
:
fa
or archenteron. This cavity
is widely open to the ex-
A
Fig. 59. — Three stages in the gastrulation of Amphioxus, seen in optical section.
A. Blastula with flattened vegetative surface; optical transverse section.
et
s
od)
OY
a.
Os
terior by the orifice of invagi-
nation, or d/astopore, which
in German is designated by
the expressive term Uvmund.
The two layers of cells which
constitute the wall of the
gastrula are the pvr7zmztive
germ-layers ; the outer layer
is the primitive ectoderm,
B. Lower pole becomes invaginated into the blastoccel ;
and the inner layer, sur-
rounding the gastral cavity,
is the primitive endoderm ; the two layers are continuous
with one another round the margin of the blastopore.
The blastopore is at first a very wide oval opening,
but it soon becomes narrowed down to a small aperture
EMBRYONIC DEVELOPMENT. Li
by the continued deepening of the archenteric cavity
(Hig: (60):
It is now a well-established fact that all multicellular
animals (Metazoa) pass through a gastrula-stage in the
course of their development, although the form of the
gastrula is often extremely modified and difficult to recog-
nise. The significance of this
fact, as was long since pointed
Cor
out by Huxley, Haeckel, Lan-
kester, and others, is very
great when it is remembered
oon
that the embryonic character-
853
istics of the gastrula are
essentially identical with the
permanent features of the
: ° Fig. 60.— Optical longitudinal sec-
organisation of the Ccelen- tion of later gastrula. Cilia (flagella)
terata (Hydra, etc. ). have been protuded from the ectoderm
f cells, and the embryo at this stage
Returning to the gastrula begins to rotate within the follicle.
5 ¢ (After HATSCHEK.)
of Amphioxus, in the course
of the further differentiation which goes hand in hand
with the progressive growth and development, we shall
find that the primitive ectoderm gives rise to (1) the
central nervous system and (2) the definitive ectoderm ,; the
primitive endoderm gives rise to (1) the mesoderm, which
is usually regarded as a third or intermediate germ-layer ;
(2) the xotochord; and (3) the definitive endoderm, which
forms the lining mucous epithelium of the alimentary
canal; finally, the primitive gastral cavity or archenteron
will become subdivided into (1) the dody-cavity or calom,
and (2) the definitive gut or alimentary canal.
The embryo shown in optical section in Fig. 60 repre-
sents the stage reached at midnight of the first night of
development. It will be noticed that one side is convex,
177 DEVELOPMENT OF AMPHIOXUS.
while the opposite side is flattened; this is an indication
that dorso-ventral differentiation has taken place, since
the flattened side marks the dorsum or back of the embryo,
while the convex side is ventral. It may be seen further
that the blastopore is inclined towards the dorsal side of
the embryo. The dorsal inclination of the blastopore is
eminently characteristic of the vertebrate gastrula from
the Ascidians up to the highest
craniate forms. In the Inverte-
brates (Annelids, Molluscs, etc.) GED
the blastopore acquires a ventral petals
inclination.* Be a
At the stage represented in Fig. Sean
60 the embryo commences to ro- Boise He
tate within the vitelline membrane, oe Sari ed a)
each ectodermic cell being now ES
provided with a vibratile cilium. Fig. 61. — Elongated gas-
6 trula. Optical longitudinal sec-
The embryo next begins to elon- tion. The cilia are omitted
gate, and the blastopore becomes) 20m ho) ecod- antes
: ; HATSCHEK.)
still narrower (Fig. 61).
A comparison of the accompanying figures will show
that the narrowing of the blastopore is effected by the
downward and backward growth of its dorsal border,
while the ventral lip remains stationary. The dorsal ecto-
derm, which is converted into the medullary plate, now
shows indications of a shallow longitudinal groove. This
is the beginning of the medullary groove which leads on
to the formation of the central nervous system.
* For a discussion of the phylogenetic relation of the blastopore or proto-
stoma (Hatschek) to the mouth and anus, the following works should be
consulted: ADAM SBDGWICK, Ox the Origin of Metameric Segmentation, etc.,
Quarterly Jour. Micro. Sc., XXIV., 1884, and by the same author, (Votes on
Llasmobranch Development, 1b. Vol. XXXIII., 1891-92.
Finally, BERTHOLD HATSCHEK, Lehrbuch der Zoologie, Jena, 1888-91.
EMBRYONIC DEVELOPMENT. 113
Growth of Free-swimming Embryo.
Between 4 and 5 A.M. in the first morning of develop-
ment, z.e. at about the eighth hour, the embryo has reached
the stage represented in Fig. 62, and it now bursts through
the vitelline membrane and becomes free, swimming by
means of its cilia at the surface of the sea, or aquarium.
The fact that Amphioxus has a free-swimming, ciliated
embryo is important as providing a general connecting
link between the Vertebrates and the Invertebrates, since
eS
BES
foto
Saris!
oa
Qrle--s=35 Ine
i |
to
re
tS]
au
aut
Fig. 62.— Embryo of Amphioxus at the stage at which it ruptures the follicle
and becomes free-swimming.
A. Seen from above as a semi-opaque object. (After KOWALEVSKY.)
B&B. Seen in sagittal (optical) section. (After HATSCHEK.)
arc. Archenteron. m.~. Medullary plate. wy.c. Myoccelomic pouches of
archenteron. 7.7.c. Posterior neurenteric canal.
the possession of a ciliated ectoderm is very common
among Invertebrate embryos, but entirely unknown among
the craniate Vertebrates.
The medullary plate is now being closed off from the
outer surface. This is effected by the co-operation of two
factors. The ectoderm which bounds the medullary plate
laterally, grows over it, and simultaneously the ectoderm of
the posterior or ventral lip of the blastopore grows for-
ward over the medullary plate so as to shut in the blasto-
pore from the exterior (Fig. 62 A and 4). The archenteric
I14 DEVELOPMENT OF AMPHIOXUS.
cavity therefore no longer opens by the blastopore to the
exterior, but it communicates with the medullary tube.
The blastopore has, in fact, become converted into the
neurenteric canal, joining the canal of the central nervous
system with the cavity of the alimentary system. This
remarkable condition of things was first discovered by
KOowWALEVSKY, who also found it in the Ascidians and in
a number of the higher Vertebrates. It has since been
found to occur in all classes of Vertebrates, including
man.
Hitherto the body-wall of the embryo has consisted of
only two primary germ-layers, ectoderm and endoderm.
At the stage now under consideration, a third interme-
diate layer, the mesoderm, has begun to put in its appear-
ance. The mesoderm arises in the first instance as a
series of paired lateral pouches of the archenteron. In
Fig. 62 the first two or three archenteric pouches are
distinctly visible. Before proceeding, however, to a more
detailed account of the origin of the nervous system and
of the mesoderm, we will trace briefly the changes in
external appearance which the embryos undergo up to the
time of the formation of the mouth.
As the embryos are very transparent, the external
appearance necessarily involves a good deal of the inter-
nal structure.
The period of embryonic development may be defined as
commencing with the first cleavage of the ovum, and end-
ing with the perforation of the mouth, thus comprising
approximately the first thirty-six hours. During this
period the embryo does not take up independent nourish-
ment, but lives on the original food-yolk which was con-
tained in the egg.
During the first few hours of its pelagic or free-swim-
EMBRYONIC DEVELOPMENT. I1l5
ming existence, the embryo keeps rigidly to the surface
of the water.
After its escape from the vitelline membrane, it grows
rapidly in length. Fresh archenteric pouches are added
to those already formed, one after the other, in metameric
order. The medullary plate (z.e. the fore-cast of the nerve-
tube) becomes completely closed in beneath the superficial
ectoderm except at its anterior extremity, where it remains
open to the exterior in the mid-dorsal line by an aperture
known as the zxeuropore (Fig. 63 A, B, C). Finally, the
notochord becomes differentiated from the primitive endo-
derm.
According to Hatschek the number of mesodermic
somites which arise as diverticula from the archenteron
is fourteen pairs. Those which are subsequently added
to these arise at the hinder end of the body by prolifera-
tion from the cells which lie behind, and at the sides of
the neurenteric canal, or in that region, so that they never
appear as actual outgrowths from the archenteron.”
In Fig. 63 C the embryo has undergone some radical
changes in form. Its body, previously cylindrical, has
become laterally compressed, the ectoderm cells of the
hinder end of the body have begun to elongate so as to
form the rudiment of a provisional caudal fin, and the
front end of the body has grown out into the shape of
a snout. In connexion with the latter there are two
remarkable structures which arise as a pair of outgrowths
from the anterior region of the archenteron, and were first
described by Hatschek as a pair of anterior intestinal
diverticula. These we shall return to later.
Near the front end of the alimentary canal a curious
sac-like structure has appeared (Fig. 63 C). It arose as
a transverse groove in the floor of the gut in the region
116
DEVELOPMENT OF AMPHIOXUS.
of the first myotome, extending from the right side under-
neath to the left side of the body.
(Cf. Figs. 63 A and 71.)
The groove deepened, and its margins coalesced, and so it
rea
mute,
my / Fe
Nae]
of
x v7 Tres
ee at a
SIE elpla o orator ole or arate
ee
seas =
Le bat acs =,
; PS LI mn os S
WY] Beso
; eles
8
a
&
Aer Be we a a wer me oS ees Ses ate
SIC Se eS Se aa ee rem ae war niet ae eae ae es ae ky
ors
~——- tnt
Fig. 63.— Growth of the ciliated embryo of
Amphioxus.
ghtly altered.)
K, sli
(After HATSCHE
with nine pairs of myoccelomic pouches ;
from left side.
&. Same stage from dorsal side.
A. Stage,
with fifteen pairs of myotomes; from
Cc. Stage
the right side.
notochord.
Vacuoles have appeared in cells of
LS.
c.s.g. Club-shaped gland.
Notochord.
Rudiment of first gill-slit.
ch.
S066
Za.d. Left
head-cavity (left anterior intestinal diverticulum).
int, Intestine.
my.c. Myoccelomic (archenteric) pouches.
np. Neu-
gment granules
Pi
p.m.c. Posterior neuren-
PS:
n.t. Medullary tube.
in floor of medullary tube.
ropore.
teric canal.
r.a.d. Right head-cavity (right anterior
intestinal diverticulum).
became constricted from the gut, and now forms a hollow
sac closed at present at both ends.
shaped gland.
It is known as the clué-
Immediately behind it, in Fig. 63 C, is seen
EMBRYONIC DEVELOPMENT. 17
a shallow depression in the floor of the
gut. This is the indication of the first
gill-slit which becomes perforated at
this point later.
From this stage it is an easy tran-
sition to the stage which marks the
close of the embryonic and the com-
mencement of the J/arval period of
development.
In the embryo shown in Fig. 64, the
mouth appears as an oval aperture placed
asymmetrically on the left side. At its
first origin it is relatively much smaller
than shown in the figure. A disc-shaped
thickening of the ectoderm appears on
the left side, in the region of the first
myotome. The subjacent endoderm
fuses with the thickening, and then the
centre of the disc becomes perforated,
and so the mouth is formed.
The club-shaped gland has acquired
an opening to the exterior immediately
below the mouth, on the left side;
while the body of the gland lies on the
right side.
Behind the club-shaped gland on the
Fig. 64.—Stage in which the external apertures of
the body, przeoral pit, mouth, first gill-slit, and anus
have become perforated. Age about 36 hours, From
the left side. (After HATSCHEK.)
ai, Alimentary canal. az. Anus. 4.c. Body-cavity.
ch. Notochord. ed. Endostyle. ./. Club-shaped gland,
which has acquired an opening to the exterior on
the left side below the mouth. g.s’. First primary gill-slit.
Fig. 64.
m. Mouth. #.c. Nerve-
tube; the neurenteric canal has closed up, but the nerve-tube still curves round
the hinder end of the notochord. mp. Neuropore. 7.0.c. Przeoral coelom (right
head-cavity). #.%. Przeoral pit (left head-cavity). 7 Provisional caudal fin.
118 DEVELOPMENT OF AMPHIOXUS.
right side is the first gill-slit, opening directly to the
exterior. At the time of its actual perforation it lies
near the mid-ventral line of the body, but as it increases
in size it becomes shifted up to the right side.
The neurenteric canal is closed up, and the nerve-tube
ends blindly behind, being curved round the hinder end of
the notochord. Immediately in front of and below the
point where the neurenteric canal formerly existed, the
anus has now made its appearance, approximately, if not
exactly, in the mid-ventral line * (Fig. 64).
We will now return to consider more closely the exact
development of the mesodermic somites, the notochord,
and the nerve-cord.
Development of Central Nervous System.
As in the craniate Vertebrates, so in Amphioxus the
medullary plate arises as a median unpaired longitudinal
specialised portion of the dorsal ectoderm. The way in
which it becomes separated from the superficial ectoderm
has already been indicated above, but it can best be
studied in transverse sections.
In the sections shown in Figs. 65 and 66, the separation
of the medullary plate from the ectoderm, and its subse-
quent conversion into a closed tube, is so clearly illus-
trated, that further description is unnecessary. A unique
feature in connexion with the formation of the central
nervous system of Amphioxus is, that the medullary plate
sinks below and becomes covered over by the superficial
ectoderm before it takes on the form of a closed tube, so
that for some time it exists as a half-canal open dorsally
* According to Hatschek, the anus breaks through slightly to the left of
the middle line.
119
EMBRYONIC DEVELOPMENT.
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aie ‘pauayey Ajawiayxa awosaq sey YoryM “wNIEyIC
‘aqny puv ajeid Areynpay, “2%
qys-is Areurid ysany "se ‘purls podeys-qni9 7.0"
ay} nq ‘(1Xe} Jy} UL O} Pedajet sy} oie fay) H 0} wo
(“MAHOSLVH J0yV)
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melee
NAAN
Wy
4
x
a <
‘ysnoua oo1vos ale Tajonu eT, *
a o1mrojaoo oy} JO Tajonu ay} sainsy OM} ysv[ 94} Ul—"A'N
*(sayTWos OTWIaposaut) sayonod orwo
*payiuo AjjeyUaploow a1OM S19}9]
ay A[BAYNIISUOD patajj}s] UPEq
‘O19 ‘SaPWIOS SIULIapOsatu ‘p1loyoo}ou ‘gqn} Alv|[npaur ay} Jo
Snoiyy suoyoas asisasuvsy,— “SO “BIA
120 DEVELOPMENT OF AMPHIOXUS.
against the ectoderm. Later the dorsal margins of this
half-canal meet and fuse in the middle line, and so
produce the medullary tube * (Fig. 66).
Origin of Mesoderm and Celom.
In consequence of the flattening and incurving of the
medullary plate, pressure is brought to bear on the
dorsal wall of the archenteron, and the dorso-lateral bor-
ders of the latter acquire the form of two longitudinal
grooves (Figs. 65 A and 4). It is from these grooves that
the archenteric pouches are split off. The grooves deepen,
and in doing so become divided up into a series of
pouches. Eventually the pouches become shut off from
the archenteron gradually from before backwards, and
then appear as closed cavities on either side of the
notochord, which has, in the meantime, been developing
(Fig. 65 /).
In the higher Vertebrates the mesoderm arises as two
solid, lateral, longitudinal bands, which are split off from
the primitive endoderm. These mesodermic bands are at
first unsegmented, and might be taken to correspond with
the longitudinal grooves of the archenteron of Amphioxus,
as described above. Later, only the dorsal portion of the
mesodermic bands undergoes segmentation, while the
ventral portion, which becomes hollowed out to form
the general body-cavity, is never segmented in the crani-
ate Vertebrates. (Cf. Fig. 33.) In Amphioxus the whole
of the mesoderm is contained in the archenteric pouches,
and is, therefore, at first entirely segmented.
As soon as the pouches have lost their primitive con-
* In the Ascidian embryo the formation of the medullary tube takes place
after the manner typical of craniate Vertebrates (see below, IV.).
EMBRYONIC DEVELOPMENT. I2I
nexion with the archenteron, they commence to extend
dorsally and ventrally between the ectoderm and the in-
ternal organs (Fig. 66).
inner or visceral wall of the pouch adjacent to the noto-
Meanwhile the cells forming the
chord elongate transversely and longitudinally, and begin
to form the plate-like muscle-fibres of the myotome. The
cells producing these fibres
are arranged in such a way
that each of them gives rise
to a muscle-fibre extending
from the anterior to the pos-
terior limit of a myotome.*
The muscles are at first
closely approximated to the
notochord and project freely
into the cavity of the pouch.
The latter gradually grows
downwards, until it meets
its fellow of the other side;
the two fuse together, and
so the cavity 1s made con-
tinuous from side to side,
Fig. 66.— Transverse section through
the middle of the body of an embryo,
with ten pairs of somites, to show the
closure of medullary tube and the dorsal
and ventral extension of the mesodermic
somites. (After HATSCHEK.)
al, Alimentary canal. ch. Notochord,
in the cells of which vacuoles have com-
menced to form. d.#. Commencing for-
mation of longitudinal muscle-plates from
the cells forming the inner wall of the
somite. my.c. Myoccelomic cavity,
below the intestine.
When this occurs, the primarily single cavity of each
archenteric pouch becomes divided into two portions ;
namely, a dorsal portion, the somfe proper or myocel,
and a ventral portion, the cw/om, by a transverse partition,
which arises through a fusion between the parietal and
* Already in the embryo shown in Fig. 63 C, and even at a somewhat ear-
lier stage, the muscles are so far developed that the body can be bent and
jerked. By the time the mouth has broken through, muscular locomotion
effectually replaces the primitive cz/ary locomotion, although the cilia persist
to a late stage.
U2Z DEVELOPMENT OF AMPHIOXUS.
visceral walls of the cavity, at about the level of the base
of the notochord (Fig. 67).
The dissepiments between the myotomes are formed
from the contiguous walls of the successive pouches, but
ventrally, in the region of the ccelom, they break down,
so that the latter then becédmes a continuous unseg-
mented cavity. On account
of the fact that the archen-
teric pouches give rise both
to the cavity of the somites
(myocel) and to the general
body-cavity (ccelom proper
or splanchnoce!), they are
often spoken of as the myo-
celomic pouches. The cav-
ity of the original archen-
Fig. 67. Scheme of a transverse
section through the body of a larva
with five gill-slits, to show the division
between myoccel and_ splanchnoccel.
(After HATSCHEK.)
z.c. Spinal cord (medullary tube).
ch. Notochord. dm. Muscles. my. Myo-
cel. sc. Rudiment of sclerotome.
al, Alimentary canal. s.z.v. Sub-intestinal
teric pouches is known as
the primitive the
epithelial walls of which
caelom,
constitute the szesoderm.
As differentiation and or-
ganogeny proceed, the meso-
vein. sp. Splanchnoccel. . :
derm gives rise to (1) the
musculature, (2) the connective tissue, (3) the blood-vessels,
(4) the reproductive organs, (5) the calomic epithelium or
lining of body-cavity, also called the perztoneum, and
(6) the excretory tubules. The development of the last-
named structures has, however, not yet been worked out
in Amphioxus.
The parietal layer of the mesoderm applies itself closely
against the ectoderm, and gives rise to the cutis of the
body-wall.
The connective tissue-sheath of the notochord and
EMBRYONIC DEVELOPMENT. 123
nerve-cord, together with the internal sheath or fascia
of the muscles of the myotome, arises from the walls of
a pouch-like diverticulum of myoccel which grows up be-
tween the muscles and the notochord and nerve-cord. (Cf.
Figs. 67 and 68.) The myoccel also grows downwards
between the somatic layer of the peritoneum and the ecto-
derm (Fig. 68). According
to Hatschek the dorsal and
ventral fin-spaces are also
derived from the myoccel.?
The diverticulum of the
myoccel which has just been
described is known as the
sclerotome, since it gives rise
to the fibrous sheath of the
notochord and_ nerve-cord,
which (z.e. the sheath) in
most of the higher forms
becomes replaced by carti-
lage, and finally by bone.
In the craniate Vertebrates nha) GbesGdhene @? | Gate
the sclerotome arises as a Section through region between atriopore
: : ; and anus, of a young Amphioxus shortly
solid proliferation of cells after the metamorphosis. (After HatT-
; ; ; SCHEK.)
from the visceral wall at the d.f.c. Dorsal fin-space. my. Myoccel.
base of the somite. This 5¢.Sclerotome. ao. Aorta. ad, Intestine.
i , : s z.m. Intercoelic membrane. 5.2.v. Sub-in-
solid proliferation is un- testinal vein. sf. Splanchnoccel. v. fc.
; : Ventral fin- b
douptedly-a medication of “°C re
a hollow diverticulum, involving, as it does, only the
visceral wall of the somite, precisely as we find it in
Amphioxus.* (Cf. Fig. 33.)
On their outer surface the muscles of the myotomes are
not provided with a sheath of connective tissue (fascia),
standing, in this respect, in contrast to the condition
which obtains in the Craniota.
124 DEVELOPMENT OF AMPHIOXUS.
Origin of the Notochora.
The notochord is formed from the endodermic cells
which lie between the mesodermic pouches and constitute
the dorsal wall of the archenteron. The dorsal wall of
the archenteron at an early stage becomes converted into
a shallow longitudinal groove whose concavity is turned
towards the archenteric cavity (Fig. 65 D). This groove
gradually deepens (Fig. 65 £), and eventually its walls
become closely appressed to one another so as to obliter-
ate the lumen (Fig. 65 /). Finally the adjoining cells of
the archenteric wall grow across the gap occasioned by
the formation of the notochord, and joining together, shut
off the latter from any participation in the enteric wall
(Fig. 66). In this way is the notochord separated from
the endoderm gradually from before backwards. Poste-
riorly it remains for a considerable time fused with the
endoderm at the point where the anterior wall of the neu-
renteric canal becomes continuous with the dorsal wall
of the archenteron.
We have indicated above that the differentiation of the
notochord takes place from before backwards. At its
anterior extremity a very noteworthy exception to this
rule is presented. In the region of the first myotome
the notochord retains an open communication with the
archenteron after its lumen has already been obliterated
behind this point. Moreover, in the embryo, with eight
pairs of myoccelomic pouches (Fig. 68 dzs), the front end
of the notochord lies some distance behind the front end
of the body, while the anterior portion of the archenteron
extends beyond the notochord. Eventually the notochord
is continued to the front end of the body by becoming
constricted off from the dorsal wall of the anterior sec-
EMBRYONIC DEVELOPMENT. I25
tion of the archenteron in the usual way. This retarded
growth of the notochord anteriorly indicates that its exten-
sion to the tip of the snout is a secondary phenomenon.
Ancestrally we are bound to assume it did not extend so
far forwards. The forward
. oO ‘e]
extension of the notochord SEE J
is, as noted above, obviously HY a> ho
. : pense aay A 772
useful to Amphioxus in ren- ASSN
dering its pointed snout Cassese mee _-Ch
sufficiently resistant to en- Eat ee | A
able it to burrow in the ee 45
7 Oisesese, Seno eo ‘a
sand. When it wants to ace ees yay
5 5 . Spray Bere reas (a os LL f
bury itself in the sand, it Poets an
; ; Pees Kooea
tort eee) == 45
has not to take pains to dig Pes sta e8
a Be, Psy en ee YO |
a hole, but darts in in the po geeagore8
. 49
fraction of a second. gy
The histological differen- =
ihe Cro,
tiation of the notochord Caan
commences soon after the
sides of the chordal groove Fig. 68 47s.— Embryo of Amphioxus,
‘= with eight pairs of somites to show the
have come together so as to primary relations of the anterior end of
F the notochord. From above. After
obliterate the lumen. The yarscuex.) (
cells composing the noto- p.c. Preechordal portion of archen-
5 teron, which becomes converted into the
chord are, at the first ap- head-cavities. .f. Neuropore. ch, Noto-
chord; over which lies the neural tube.
my. Myoccelomic pouches. ze. Neuren-
themeroove; placcas ena to) mc. canal.
2 ae : : N.B.—In this and other figures of
end, but soon begin to inter- Amphioxus embryos here reproduced
1 ‘th th after Hatschek, the so-called mesoder-
ace with one another across nic pole cells have been omitted in
the middle line (Fig 65 F) accordance with the observations of
= WILSON and LwoFF.
and finally each cell comes
to occupy the whole width of the notochord (Fig. 66).
Meanwhile vacuoles begin to appear in the cells (Fig. 66).
The vacuolisation of its component cells is an extremely
proximation of the walls of
126 DEVELOPMENT OF AMPHIOXUS.
characteristic feature of the notochordal tissue throughout
the group of the Vertebrates. It is carried on to such an
extent in Amphioxus as to
obscure the original cellular
We: WK
i it
i N
MY
structure of the notochord.
5
The cells anastomose with
one another in the longitu-
dinal direction, and so pro-
duce a reticulum the meshes
Fig. 5 sagittal section of of which represent the vacu-
notochord of a young Amphioxus of oles whose first origin is
8 mm., to show the vacuolar character :
of the notochordal tissue and the dis- shown in Fig. 66. Most of
placement of the nuclei to the dorsal and -
ventral borders. (After LWOFF.) the nuclei become eventually
displaced from the centre of
the notochord, and are, in the adult, almost exclusively
confined to its dorsal and ventral aspects (Fig. 69).
The Preoral “ Head-cavities” of Amphioxus.
Before leaving the embryonic period of the development
it is necessary to consider the origin and fate of what may
be called the “ead-cavities of Amphioxus as made known
to us by the work of Hatschek.
They arise symmetrically as a pair of diverticula from
the anterior portion of the archenteron, which lies at first
partly in front of the notochord (Fig. 68 47s) and completely
in front of the myoccelomic pouches (Fig. 70).
They begin to appear at the stage in which some eight
pairs of pouches are already present. Their origin there-
fore, in point of time and the subsequent modifications
which they undergo, show that they do not belong to the
metameric series of the mesodermic pouches, but are
structures saz generis.
EMBRYONIC DEVELOPMENT. 127.
The archenteron extends at first to the front end of the
body. Its anterior portion, after the formation of several
mesoblastic somites, becomes marked off from the hinder
region by a slight constriction, which gradually becomes
deeper and deeper (Fig. 70), until finally the whole of this
portion of the archenteron is divided into two separate
sacs, which eventually lose
all connexion with the ar-
chenteron (Fig. 71). The ali-
mentary canal now no longer
ERTOToIo >
> Se
ai
reaches to the anterior ex-
ny
tremity of the body. Very
SEAT
Loans
Sista SAS irae
st alcloial sola ios
soon after their separation
from the archenteron these
5
wea
EOE.
a \ on
ae
sacs enter upon a series of
changes by which their origi-
nally symmetrical disposi-
tion is entirely destroyed.
Already in Fig. 71 it can
be noticed that the right
sac is becoming larger than Fig. 70.— Embryo, with nine pairs of
the left, and the epithelium
primitive somites, seen in optical section
Ave fi , i ; from the ventral surface, to show the
lining its walls is losing its origin of the head-cavites. (After Har-
ioinval bical iy SCHEK.)
origimal cubical C aracter, y.a.d. Right head-cavity. /a.d. Left
the inner ends of the cells head-cavity. zy.c. Myoccelomic pouches
: . (primtive somites). arc. Archenteron.
are rounding off, and in fact
it is being converted from a cubical toa flattened pavement
epithelium (Figs. 63 C and 64). The left sac, on the con-
trary, retains its original form and dimensions for a long
time. During the asymmetrical changes affecting the two
sacs, which take place coincidently with the formation of
the snout, the left one comes to lie transversely below the
notochord, while the right sac becomes greatly enlarged
128 DEVELOPMENT OF AMPHIOXUS.
and constitutes the cavity of the snout lying below the
notochord (Fig. 63 C).
Shortly after the breaking through of the mouth the
left sac acquires an opening to the exterior on the left side
of the body (Fig. 64). The right sac becomes the preoral
body-cavity or coelom of the “head,” while the left sac is
known as the preoral pit. It is necessary to emphasise
the fact that these two structures which are so different
in their fully formed con-
dition are at first perfectly
4
eA Lad i ;
similar and symmetrical and
form a pair of “head-cavi-
Ultimately, as we
have seen, only one of them
ERCEOGEEG.
BEEQOECED
ties.”
as
statoto
aa
a
Fig. 71. — Anterior portion of em-
bryo, with thirteen primitive somites,
actually persists as a head-
cavity; namely, the right one.
The entire conversion of
from the ventral side in optical section.
(After HATSCHEK.)
r.a.d. and /.a.d. Right and left head-
cavities. c.s.g¢. Rudiment of club-shaped
gland.
the left sac into the przoral
pit is probably to be regarded
as a secondary or cenoge-
netic phenomenon, but the acquirement of an opening to.
the exterior is probably not secondary, since a similar
opening (the proboscis-pore) occurs in Balanoglossus.
In addition to the above-described peculiarities which
sufficiently distinguish the head-cavities from the myocce-
lomic pouches, must be mentioned the fact that at no point
of their epithelial walls are muscles developed.
It is probable that the praeoral head-cavities of Amphi-
oxus are homologous with the premandibular cavities of
the higher Vertebrates, from the walls of which the greater
number of the eye-muscles are developed.* This view is
* This is also the opinion of Kupffer. Singularly enough van Wijhe has
advanced the view that only the right head-cavity of Amphioxus is to be
EMBRYONIC DEVELOPMENT. 129
strongly confirmed by the mode of development of the
premandibular cavities in the Cyclostomes.
In these fishes, VON Kupr-
FER has shown that they
actually appear in the form
of a pair of diverticula from
the anterior extremity of
the archenteron (Fig. 72).
If a comparison be made
between Figs. 70 and 72, it
will be at once manifest how
close the correspondence is } us
Fig. 72. — Horizontal projection of
between the mode of de- pharynx and przoral endodermic exten-
- sion of a young Ammocetes planeri of
velopment of the head-cavi- 3% mm., reconstructed from a series of
ties in Amphioxus and in transverse sections. (After KUPFFER.)
p.e. Przeoral endodermic extension
Ammoceetes. In the Se- (preorale Endodermtasche). gm. and m.
leva st th iailacit -_ Praemandibular and mandibular portions
achnlans € similarity 1S of head-cavities. ph. Cavity of pharynx.
hardly less strikine.® 7, 2, 3. First three pairs of gill-pouches.
2 N.B.— Kupffer considers it probable
that the mandibular as well as the pre-
. mandibular cavities arise from the single
Endostyle and Pigment pair of endodermic diverticula. In the
Granules. course of the following pages I have
referred chiefly to the praemandibular
In Fig. 64 there is to be cavities alone so as to avoid complica-
tions.
noticed a vertically placed
structure lying in front of and contiguous with the club-
shaped gland. It is a tract of very high cylindrical cells
forming part of the right wall of the alimentary canal in
homologised with the preemandibular cavity (see below, V.). Kupffer regards
the premandibular and mandibular head-cavities as rudimentary or meta-
morphosed gill-pouches. This deduction is entirely foreign to the standpoint
which I have adopted. The conclusion may seem plausible from the con-
ditions observed in Acipenser alone; but when these are regarded from a
comparative point of view, the deduction is, to my mind, unjustified. It should
be added that Kupffer has shown that the head-cavities (premandibular and
mandibular) of Acipenser also arise as endodermic pouches.
130 DEVELOPMENT OF AMPHIOXUS.
this region. (Cf. Figs. 65 Gand 75.) I have shown that
this epithelial tract is the rudiment of the exdostyle (vide
anpra).
It is a curious fact that the first trace of pigment to
appear in the nerve-tube is not the eye-spot, but that at a
constant point in the region of the fifth somite a black
pigment-spot is deposited in a cell in the ventral wall of
the medullary tube. This is followed by another smaller
pigment granule slightly posterior to the first (Fig. 63 Cy
The eye-spot appears at the end of the embryonic period.
LARVAL DEVELOPMENT.
Formation of Primary Gill-slits, etc.
With the establishment of the definite relations oi the
head-cavities, the mouth, club-shaped gland, first gill-slit,
and anus, the embryo enters upon the larval phase of the
development.
It is no longer, or only very rarely, to be taken from
the surface of the sea, but descends to a depth of several
fathoms. When kept in aquaria, the larve can often be
observed to be suspended vertically, and apparently quite
motionless in the water. This suspension is, no doubt,
effected by the movement of the long cilia, or flagella,
with which the ectoderm is provided, each cell possessing
one flagellum.®
The principal changes which take place during the early
stages of this phase of the development are the addition of
new myotomes, the formation of new gill-slits, in meta-
meric order, in an unpaired series on the right side of the
larva, to the number of from twelve to fifteen, or even
sixteen (the more usual number being fourteen), and the
origin of the atrial cavity.
LARVAL DEVELOPMENT. 131
Each gill-slit breaks through in, or slightly to the right
of, the mid-ventral line, and then grows well up on the
right side of the body. A larva with three gill-slits and
the indication of a fourth is represented in Fig. 73. The
originally circular mouth has grown to a much larger size,
and extends on the left side anterior to the endostylar
Fig. 73. — Larva of Amphioxus, with three gill-slits and the rudiment of a
fourth; from the left side. (After LANKESTER and WILLEY.)
p.p. Preeoral pit. ed. Endostyle lying on right side, seen through the wide
lateral mouth. g/. Position of external aperture of club-shaped gland. 4.s’. First
primary gill-slit. az. Anus.
N.B.— Actual length of larva, nearly 1% mm.
tract (which is on the right wall of the pharynx) and
posterior to the first gill-slit. The oral opening later
attains to relatively gigantic dimensions, and forms one
of the most striking features of the larva.
The anus is now displaced from its original ventral
position to the left side in consequence of the increased
development of the provisional caudal fin. The latter
consists of elongated ectodermal cells, in which a certain
amount of brown pigment is deposited. Later, when
the dermal expansion, which has been described above as
the definitive caudal fin, begins to grow out, it pushes the
cells composing the provisional fin before it, so that they
form a fringe round its border. Eventually the provisional
fin disappears entirely.
The gill-slits now go on adding to their number, one
after the other, until the larva reaches the stage shown in
Fig. 74. In this larva there are fourteen primary unpaired
gill-slits, lying, for the most part, on the right side of the
132 DEVELOPMENT OF AMPHIOXUS.
pharynx, although the more posterior slits bend under the
pharynx, while the most posterior have a median ventral
position.
In front the gill-slits still open directly to the exterior,
but the right metapleural fold is seen to be hanging over
the tops of them; while the hinder slits now open into
the partially formed atrium, which has already closed in
. psi pss
Se
Fig. '74.— Anterior portion of larva, with fourteen primary gill-slits and rudi-
ments of the secondary gill-slits; viewed as a transparent object from the right
side. (After WILLEY.)
5.0. Sense-organ of przoral pit (groove of Hatschek). e. Endostyle. 7. In-
ternal opening of club-shaped gland. s,s. Rudiments of secondary gill-slits. 7.518,
p.si4, Thirteenth and fourteenth primary gill-slits. The lower margin of the
mouth is seen through the anterior gill-slits.
Total length of larva, nearly 342 mm.
posteriorly, as described above. The larva is remarkably
transparent, so that its internal organisation can be seen
as clearly as possible through the outer body-wall.
The long axis of the primary gill-slits is approximately
at right angles to the long axis of the body. They are
not more numerous than the myotomes in the correspond-
ing region of the body, so that the drvanchiomery at this
stage coincides with the muscular metamery. In Fig. 73
the first gill-slit was somewhat larger than the second and
third. At about that stage, however, its further growth
became arrested, and now it is seen to be considerably
smaller than those which immediately follow it.
In addition to its external opening on the left side, be-
LARVAL DEVELOPMENT. 133
lat
<3,
SSS
Sy
a>
maa OE)
poe
i
L]
Li
Go
w
o
rem
\y
Fig. 75. — Transverse sections through the region of the mouth of larve of
Amphioxus, to show the endostyle and the external and internal openings of club-
shaped gland. (After LANKESTER and WILLEY.)
A. Section passing through the anterior corner of the mouth of a larva, with
eleven gill-slits.
&B. Section passing through the middle of the mouth of a larva, with twelve
gill-slits.
al, Pharyngeal cavity. 4.c. Coelom (splanchnoccel). 67.e. Branchial epithelium.
e.a. Branchial artery. ezd. Endostyle. ex.o. External opening of club-shaped
gland. fc. Dorsal fin-space. .g/. Lower portion of club-shaped gland. g.s’. First
gill-slit. zz. Interccelic membrane. 7.0, Internal opening of club-shaped gland.
Za. Left aorta; there is no corresponding right aorta in the larva. ». Mouth.
7m. Rudiment of right metapleur; a mere ectodermic thickening in 4; a solid
thickening of the cutis in 2, in which two of the original enlarged ectoderm cells
have become imbedded. These curious cells occur over a long stretch of the
metapleural folds during this phase of the development, disappearing eventually.
In B, the left metapleur is indicated by an ectodermic thickening immediately
below the gill-slit. 2. So-called nephridium of Hatschek.
134 DEVELOPMENT OF AMPHIOXUS.
low the mouth (see Fig. 64), the club-shaped gland has
now acquired an opening at its upper extremity, on the
right side, into the pharynx.’ The gland lies, as usual,
behind, and closely approximated to, the endostylar tract,
which is bent forwards on itself at its upper end (Figs. 75
A and B&).
Pigment-spots are present in great numbers at the base
of the neural canal. The pigment is deposited in special
vn Pro
er TI
A i
HT
NMA
»
> hs
U
ATr7Tz A.r77z
Fig. '76.— Transverse sections through the region of the przeoral pit. (After
LANKESTER and WILLEY.)
A, Through a larva, with twelve gill-slits and no atrium.
4. Through a larva, in which the atrium was closed in over all the gill-slits
except the first two. (Cf. Fig. 38 C.)
arm. Anterior median portion of right metapleur. .0.c. Praeoral body-cavity
(right head-cavity) ; this cavity becomes much reduced after the metamorphosis,
and is largely filled up by gelatinous tissue. #.%. Praeoral pit. s.0. Sense-organ
of preeoral pit (groove of Hatschek). 20.4. Rudiment of left half of oral hood.
my'. Sclerotome (diverticulum of myoccel my). Other letters as above.
Section 4 is taken through a plane slightly posterior to section A.
LARVAL DEVELOPMENT. 135
cells, the pzgment-cells, which arise as modified epithelial
cells of the central canal. These cells send out several
branching processes, which lose themselves in the fibrous
tract of the spinal cord.
Already in the youngest larva — namely, that shown in
Fig. 64 — the preoral pit had become subdivided into two
portions, which, however, retained a free communication
with one another.
In the course of the changes which the left head-cavity
had to undergo in its conversion into the przoral pit it
had come to lie transversely below the notochord. Sub-
sequently it extended itself, in the form of an offshoot,
dorsally to the right of the base of the notochord.
This offshoot from the przeoral pit appears to serve as a
special sense-organ lying ultimately, as mentioned above,
in the roof of the oral hood, whose function is possibly to
test the water as it enters the mouth (Figs. 76 A and 3B,
amde big 745 (ete. ).
Formation of Secondary Gull-slits.
Above the primary gill-slits in Fig. 74, and like them, on
the right side of the body, is to be observed a longitudinal
ridge provided with a series of nodal enlargements which
alternate with the primary gill-openings, the first of them
lying above and between the third and fourth primary slits.
Each of these enlargements represents a thickening in the
wall of the pharynx, which has undergone fusion with the
bedy-wall beneath the right metapleural fold, in the angle
formed by the latter with the body-wall.
These metameric fusions of the pharyngeal wall with the
body-wall are the forecast of a second row of gill-slits, whose
relation to the primary row will become clear as we pro-
136 DEVELOPMENT OF AMPHIOXUS.
ceed. With their appearance, the larva enters upon that
phase of its development which has been called the later
larval period. It is the period of the metamorphosis of
the larva, during which the pronounced asymmetrical
arrangement of the parts is exchanged for the partial, but
not absolute, symmetry which we have noted in the adult.
The metamorphosis, therefore, consists largely in the sym-
metrisation of the larva.
The simultaneous appearance of the six nodal thicken-
ings in the exact position, shown in Fig. 74, is very
constant. Shortly afterwards a minute perforation appears
in the centre of each thickening almost simultaneously,
except in the case of the first, which usually becomes
perforated rather later than the others. The originally
small circular openings of the secondary gill-clefts gradually
increase in size and become oval in shape, their long axes
being parallel to the long axis of the body, instead of at
right angles to it as in the case of the primary slits.
Next, the upper borders of the secondary slits begin to
flatten, and later to show signs of curving downwards.
The changes in shape, which affect the secondary slits at
the stages now under consideration, may be expressed by
saying that they are at first shaped like a biconvex lens,
then like a plano-convex lens with the flat surface directed
upwards and the convex surface downwards, and finally
like a concavo-convex lens with the concavity directed
upwards (Fig. 77).
During these changes, which do not take place in all the
secondary slits at the same time, the last one especially
retaining for a long time its primitive shape, the walls of
the successive slits become sharply rounded off and distinct
from one another, and anew perforation makes its appear-
ance in front, above, and between the second and third
LARVAL DEVELOPMENT. 137
primary slits. This new slit constitutes the definitive first
slit of the secondary series (Fig. 77).
The larva shown in Fig. 77 presents a very different
aspect from that shown in Fig. 74; the transition from one
stage to the other is, of course, gradual, and all intermediate
steps can be observed. In the stage which we are now
considering (Fig. 77), the atrial cavity has become com-
pletely closed up in front, so that now none of the gill-slits
open directly to the exterior.
None of the primary slits now he entirely on the right
side, but they have become bent under the pharynx, and
EPH
ee - ee _ e Ss . : - YAS SS > / <0
psr SST 0G eae Vv
| : gl 4 psi .©
Fig. 77.— Anterior portion of larva, in which the secondary slits have become
perforated, and the primary slits are passing round to the left side. From the right
side. (After WILLEY.)
5.0. Sense-organ of przoral pit. v. Right half of velum. e. Endostyle, grow-
ing beyond the club-shaped gland g/. g.s5’. First primary slit, much reduced in
size. 5.5’. First secondary slit. 7.512, Twelfth primary slit, behind which is to be
seen a vestige of the thirteenth slit.
t
i a
thus extend round to the left side. This bodily migration
of the primary slits from one side to the other occurs in
correlation with the increase in size of the secondary slits,
which, as they continue to grow, push, as it were, the
primary slits before them, and so cause the latter to bend
under the pharynx in the way described. The peculiar
growth by which the primary gill-slits are gradually carried
from the right to the left side, may be described as a trans-
verse or rotatory growth affecting the pharynx 7 ¢ofo in
138 DEVELOPMENT OF AMPHIOXUS.
the region of the secondary slits. Such of the primary
slits as occur behind this region are not affected by the
rotatory method of growth, and retain their original position
in the mid-ventral line of the pharynx.
It is to be noted also that there are only twelve primary
gill-slits at this stage. Assuming that in the particular
larva here figured there were originally fourteen primary
slits, the fourteenth has closed up and vanished without
leaving a trace, while a vestige of the thirteenth can still
be recognised. The actual process involved in the closure
and disappearance of a certain number of the primary slits
can, as we shall see, be readily observed in the living larva.
Club-shaped Gland and Endostyle.
The internal aperture of the club-shaped gland into the
pharynx is exceptionally plain at this stage, and its refring-
ent walls and relatively large size give it a curiously slit-
like appearance. We shall find that the gland subsequently
atrophies, but the most persistent part of it — that is to say,
the last part of it to disappear —is precisely the internal
opening with its refringent border.
The endostyle, whose primary position, as we have seen,
was immediately in front of the club-shaped gland, now
presents a remarkable condition. It has begun to grow
backwards and downwards, being probably pulled down,
so to speak, by the general rotatory growth of which we
have spoken above; and so the club-shaped gland no
longer lies behind it, but upon it. The gland itself being
disconnected with the wall of the pharynx, except at its
upper end where it opens into the latter, is not affected
by the complicated changes to which the pharyngeal wall,
including gill-slits, mouth, and endostyle, is subjected, so
LARVAL DEVELOPMENT. 139
that it forms a convenient punctum fixum with relation to
which the growth of neighbouring structures, particularly
that of the endostyle, can be determined.
The upper and lower limbs of the endostyle are inclined
to one another at an acute angle, and may be said to form
two unequal sides of a triangle, the apex of which is
directed backwards between the rows of secondary and
the primary gill-clefts (Fig. 77).
Between the two rows of slits on the right side of the
body there is a blood-vessel, representing the anterior
continuation of the sub-intestimal vessel, which ends blindly
in front above the first primary slit. This is the future
ventral branchial artery, with which we are already ac-
quainted. When its final situation in the mid-ventral line
below the endostyle is remembered, its position in the
larva high up on the right side, as in Fig. 74, will appear
very striking.
Continued Migration of Primary Gill-slits.
The secondary slits now go on growing in size, and the
primary slits gradually tend to disappear entirely from the
right side until, as in Fig. 78, only the original upper por-
e tn 705°
Fig. 78. — Anterior portion of larva from right side, to show the backward
growth of the endostyle between the primary and secondary gill-slits. (After
WILLEY.)
s.o. Sense-organ of preoral pit. #.s'. First primary slit. 7. Internal opening
of club-shaped gland. e. Endostyle. 7.4, Peripharyngeal ciliated band.
140 DEVELOPMENT OF AMPHIOXUS.
tions of them are visible from this side. In some of the
secondary slits the dorsal margin, which had previously
begun to curve downwards, has now reached the ventral
margin and fused with it (Fig. 78, third secondary slit).
In this way is the tongue-bar formed, and the primitively
simple gill-opening is divided into two distinct halves.
The formation of the tongue-bars occurs in the secondary
slits considerably in advance of the primary, both actually
and relatively, since the latter have existed all through the
earlier period of the larval development without a trace of
tongue-bars.
Peripharyngeal Bands.
The endostyle has now grown a long distance behind
the club-shaped gland, and extends backwards between
the two rows of slits as far as the middle of the second
secondary slit. From the anterior part of the upper half
of the endostyle, which is now nearly equal in length to
the lower half, arises an epithelial tract in the wall of the
pharynx, which appears in the form of a band of ciliated
cells, and proceeds backwards below the notochord to the
end of the pharynx. A corresponding ciliated band occurs
in the left wall of the pharynx, proceeding from a similar
point in the lower limb of the endostyle. In their course
below the notochord the two bands take part in forming
the hyperpharyngeal (dorsal) groove of the pharynx.
Atrophy of First Primary Gill-sit and Club-shaped
Gland, etc.
We have already seen indications of a reduction in the
size of the first primary slit. This reduction has advanced
considerably in the stage we are now describing (Fig. 78),
where the slit in question is only recognisable in side
view as a small groove,
LARVAL DEVELOPMENT. I4I
The next stage to be considered is characterised above
all by the simultaneous atrophy, closure, and disappearance
of the club-shapea gland, and the first primary gill-slit
(Fig. 70). At this stage the mmerease in size of the
secondary slits has progressed to such an extent that the
primary slits have been displaced entirely from their
original position, and are no longer to be seen from the
Fig. 79.— Anterior portion of larva from right side after the disappearance of
the club-shaped gland. (After WILLEY.)
s.o. Sense-organ. e. Endostyle. 7.6. Peripharyngeal band. s,s’, First secondary
slit.
right side, except in the case of the hindermost slits of
the series, which remain, as mentioned above, in a median
ventral position until their disappearance.
A larva seen from below, so as to show the relative
positions of the gill-slits and endostyle, etc., at this stage,
is represented in Fig. 80.
It is obvious, from what has been said above, that in the
passage of the primary slits from their original position on
the right side of the body to their final position on the left
side, their dorsal and ventral margins are reversed. What
was at first the dorsal edge of a primary slit becomes its
ventral edge, and vice versa. In other words, what is
actually the dorsal border of the primary slits in Fig. 74
is morphologically the ventral border ; and conversely, what
is actually the latter is morphologically the former ; and it is
142 DEVELOPMENT OF AMPHIOXUS.
from the latter, towards the completion of the rotatory
growth, which carries the slits from one side to the other,
that the tongue-bars arise (Fig. 80).
The vertical and longitudinal axes of most of the slits,
both primary and secondary, are now almost equal, but
the original difference in this respect, which we noted
above, is still to be observed in the case of the foremost
and hindmost slits of the two series. (Cf. Fig. 80, s.st
and g.s*, and s.s§ and fs.) The first primary slit has
5 7 2 : : i ois
pis p.s® Saree La es eee ad
Revs: z eis : BBL eens 2h SE SSS as
Fig. 80.— Anterior portion of larva of same age as in Fig. 79, seen from the
ventral surface. The pharynx is flattened out. (After WILLEY.)
ch. Notochord. mm, Entrance to mouth. v. Velum. 7.51. Vestige of first
primary slit. 4.52. Secondary primary slit. .s!9, Tenth primary slit. 7.512. Ves-
tige of twelfth primary slit. s.sl. First secondary slit. e. Endostyle. s.s. Eighth
secondary slit. a. Atrium, pressed aside.
now completely closed up, and its former existence is
barely indicated by a loose granular appearance at the
place it formerly occupied.
The alternation of the gill-slits of the two series comes
out very clearly in Fig. 80. In most of the secondary
slits the formation of the tongue-bars is completed; but
not so in any of the primary slits, where it is only be-
ginning.
There are now eight secondary slits, an additional one
having been added behind, alternating with the ninth and
tenth primary slits. Usually the formation of secondary
slits stops at this point, no more being formed until the
LARVAL DEVELOPMENT. 143
number of primary slits is reduced to the same number ;
namely, eight.
Since it is usual for the primary slits to break through
in the first instance to the number of fourteen, no less
than six of them must close up and disappear before the
stage with only eight gill-slits on each side of the body is
arrived at. The six slits which are to close include the
first and the five posterior primary slits. In the larva
shown in Fig. 80, the tenth and eleventh primary slits
would have to close at a later stage ; the twelfth is on the
point of closure, and its walls present the characteristic
coarsely granular appearance spoken of above, while the
thirteenth and fourteenth slits have entirely vanished.
In addition to the fact of the closure of these primary
slits, it is important also to emphasise the fact that they
disappear without leaving a trace behind. In the higher
Vertebrates there are a number of structures not only di-
rectly connected at some stage of development with the
pharyngeal wall, but also at some distance removed from
it, which various morphologists have interpreted as the
remnants of ancestral gill-clefts, without sufficiently con-
sidering the question whether gill-clefts were in the habit
of leaving their mark behind them. In Amphioxus, at
all events, they do not.
The Adjustment of the Mouth, etc.
While the gill-slits have been adjusting themselves to
their definitive positions, the mouth has also been sub-
jected to a peculiar kind of growth, which results in its
bending round the front end of the pharyngeal wall, and
ultimately assuming an anterior and median position, as
we find it in the adult.
144 DEVELOPMENT OF AMPHIOXUS.
In Fig. 81, a larva corresponding in age approximately
to that of Fig. 74 is represented as seen from the left side.
As noted above, the posterior primary slits bend nor-
mally under the pharynx at this stage, and some of them
extend as much on one side of the body as on the other,
being continued across the ventral side of the pharynx.
The great feature of this larva is the relatively prodigious
mouth, through which the upper portions of the first four
primary slits can be seen.
From this side we look into the depths of the przoral
pit, having only seen it by transparency in the preceding
olf i wt he
{
ul
? t
7b rhe
Fig. 81.— Anterior portion of larva, with thirteen gill-slits, from the left side.
(After WILLEY.)
olf. Olfactory pit, communicating with neuropore. +x. ‘“‘ Nephridium” of Hat-
schek. 2.¢. Spinal cord. ch. Notochord. 7.f. Przeoral pit. ex. External open-
ing of club-shaped gland. cz. Rudiment of buccal cirri. 7.6. Peripharyngeal band.
m. Mouth. 7.518. Thirteenth primary slit.
i
je
CL
figures. It is continued backwards into a ciliated groove,
which abuts on the dorsal margin of the mouth. Prob-
ably most of the food which enters the mouth passes
along this groove.
Below the pointed anterior extremity of the mouth is to
be seen the external aperture of the club-shaped gland,
and a short distance behind this is a round, refringent
body, which has become differentiated from the gelatinous
LARVAL DEVELOPMENT. 145
connective tissue lying below the epidermis, and repre-
sents the rudiment of the first element of the cartilagi-
nous skeleton of the buccal cirri.
Running parallel with the lower margin of the mouth,
and curving gently upwards to the dorsal wall of the
pharynx, is a ciliated band proceeding from the lower limb
of the endostyle, and corresponding to the one on the other
side, which we found in connexion with the upper portion
of the endostyle. Its course on the left side is somewhat
different anteriorly from that of the right side, owing to
the position and size of the mouth. (Cf. Figs. 78 and 81.)
The so-called olfactory pit, which arose at a much earlier
stage as an ectodermic depression above and in connexion
with the neuropore, no longer lies in the mid-dorsal line as
in Fig. 64, but it has been displaced to the left side by the
upgrowth of the dorsal fin (Fig. 81). Here, as in the case
of the anus, the development of a median fin has no other
effect on the aperture in question than to cause it to
forsake its primitively median and symmetrical position
and to assume an asymmetrical position on the left side of
the body. This is important to bear in mind, as the asym-
metrical position of the mouth will be explained below on
an analogous basis.
For the present it is sufficient to call attention to the
fact that, with the exception of the gill-slits, whose primary
unpaired character is due to the retarded or /atent develop-
ment of their antimeres, the unpaired openings in the
body-wall—namely, neuropore, preoral pit, external aper-
ture of club-shaped gland, mouth, and anus —all lie on the
left side of the body.
At a slightly later stage than the preceding, the front
end of the mouth is found to be no longer pointed, but to
have become rounded off, and, moreover, to lie at a deeper
146 DEVELOPMENT OF AMPHIOXUS.
level than previously (Fig. 82). The posterior groove of
the przeoral pit which we described in the last stage, seems
to be preparing the way for the mouth to dip inwards
towards the right wall of the pharynx, which, in fact, it has
actually begun to do.
At a still later stage, corresponding to that shown in
Fig. 77, the shape of the mouth has become entirely altered
(Fig. 83).
It has now the form of a triangle with the apex directed
backwards and the base standing vertically in front. But
the apex and the base are not in the same tangential plane,
Ki . x ‘ »
£ , { M 5 s ‘
Fig Cx CA%cz in fre
Fig. 82.— Anterior portion of larva somewhat older than preceding, to show
commencing adjustment of the mouth. (After WILLEY.)
e. Endostyle seen through the mouth. Other letters as above.
the former being on the left side of the body, and the latter
much deeper inwards; in fact, just below the skin on the
right side of the body. (Cf. Fig. 77.)
We see, therefore, that the longitudinal diameter of the
larval mouth is gradually shortening. It is eventually
reduced to zero when the right and left sides of the mouth
or velum come to lie opposite to one another, the velum
ultimately attaining a circular form and a median sub-
vertical position underneath the oral hood. When the
larva has reached the age to which Fig. 11 refers, the right
LARVAL DEVELOPMENT. 147
half of the velum is nearly but not even yet quite opposite
to the left half (Fig. 93).
In the preceding stage (Fig. 82) there were several
additional buccal cartilages added to the first one which
we described. In the present stage these have begun to
grow outwards so as to produce small notches in the
integument, which is now commencing at this point to
form the right half of the oral hood. The left half of the
latter arises as a downgrowth of the integument from the
upper margin of the przeoral pit and its posterior continua-
tion, the above-mentioned ciliated groove. (Cf. Figs. 81,
82, and 83.) The hinder portion of this fold is at first on
Fig. 83. — Anterior portion of still older larva, from the left side, to show
change in shape and position of the mouth. (After WILLEY.)
Letters as above. The left half of the oral hood is now growing down over the
mouth and preeoral pit.
a level with the dorsal margin of the mouth, and in fact
merges into the latter, but subsequently grows over it,
extending to its posterior extremity, where it meets the
right half of the oral hood.
It is obvious from the above description and figures that
a large part of the right wall of the oral hood is derived
from the original wall of the snout below the preoral pit,
and so an explanation is afforded of the fact noted in the
first chapter that the right half of the oral hood is continu-
ous round the anterior extremity of the notochord with
the cephalic expansion of the dorsal fin.9
148 DEVELOPMENT OF AMPHIOXUS.
The przoral pit itself is absorbed, as it were, into the
oral hood, so that it eventually loses its independent exist-
ence as a pit, although the sense-organ of the przoral pit
persists in the adult as a deep groove in the dorsal wall
of the oral hood to the right of the base of the notochord.
The remaining ciliated epithelium of the original przoral
pit increases in extent, and grows out into the finger-
shaped tracts which we have already described as being
characteristic of the inner surface of the oral hood, consti-
tuting the so-called “ Raderogan.” (Cf. Fig. 3.)
Equalisation of the Gill-stits.
In the stage next succeeding that of which a ventral
view is given in Fig. 80, the first eight primary slits—that
is to say, from the original second to the ninth inclusive —
Fig. 84.— Larva toward the close of the metamorphosis, from the left side.
(After WILLEY.)
o. Olfactory pit. v.Velum. 7.4. Peripharyngeal band. e. Endostyle. 9.52. Second
primary slit, the first having closed up. m. Left metapleur. s.a. Floor of atrium.
p.s!2, 7.518, Vestiges of the twelfth and thirteenth primary slits.
have become definitely established on the /ef¢ side, their
longitudinal and vertical axes are equalised, and in most
of them the tongue-bars are completely formed (Fig. 84).
No tongue-bar is formed in the first slit on either side, and
this slit apparently remains as a rule simple throughout
life.
LARVAL DEVELOPMENT. 149
In Fig. 84 the last indications of the twelfth and thir-
teenth primary slits are to be observed as slight depres-
sions in the floor of the pharynx in the mid-ventral line.
The tenth and eleventh slits would close up later.
It should be pointed out that the closure of the poste-
rior primary slits does not proceed in perfect correspond-
ence with the age of the larva, but takes place sometimes
at an earlier and sometimes at a later stage than here
depicted.
The gill-slits of both sides now begin to elongate in
the vertical direction (Fig. 93), and eventually a very well-
marked stage is reached, which is characterised by the
presence of eight pairs of gill-clefts. This latter stage
would appear to have a considerable duration, and, as it
stands on the borderland between the larva and the adult,
and forms the commencement of what may be called the
adolescent period of the development, it may well be
regarded as a critical stage. By this time the young
Amphioxus has given up its free pelagic life in the open
sea, and has commenced to burrow in the sand, which it
continues to do for the rest of its life.*
Further Growth of Endostyle, etc.
At the point at which we left the endostyle, its two
halves were in the relation to one another of upper and
lower. During the steps in the metamorphosis which we
have recorded above, the upper half of the endostyle is
brought down to the same level as the lower half on the
right side of it, and so the definite form of the endostyle
is established by the conjunction of its right and left
halves. It then proceeds to grow backwards along the
* The duration of the larval development of Amphioxus may be estimated
at about three months.
150 DEVELOPMENT OF AMPHIOXUS.
base of the pharynx between the two rows of gilt-slits,
but does not reach the posterior end of the pharynx until
a much later period.” :
The features in the development of the endostyle which
ought to be especially emphasised are, firstly, its direc-
tion of growth from before backwards, and secondly, its
primary anterior position in the wall of the pharynx in
front of all the gill-slits.
In connexion with the modification in the shape and
position of the mouth, as described above, it is important
to insist on the fact that the mouth of the larva is directly
converted into the velum of the adult, while the oral hood
which grows over the mouth is a new formation.
During the period of the metamorphosis the larva does
not increase in length. It is rather a readjustment of
parts which is then taking place than an increase in bulk
which is the symbol of active growth. From the time of
the first indication of the secondary slits (Fig. 74) till
after the completion of the passage of the primary slits
from the right to the left side of the body, the average
length of the larva may be taken as approximately
3.5 mm.
The adolescent period is essentially the period of active
growth in bulk and maturity. The increase in length
during this period does not, however, depend on the
addition of new myotomes to those already formed, but
merely on the progressive growth in size of the latter.
The full complement of myotomes was developed during
the early larval period, and is present in the larva repre-
sented in Pig. 74:
LARVAL DEVELOPMENT. I5I
Development of Reproductive Organs.
One of the most interesting events which we have now
to chronicle is the development of the reproductive organs.
This commences when the young Amphioxus has reached
the length of about 5 mm.
Our knowledge of the details of the processes involved
in the formation of the genital organs is again due to the
work of BovERI, who has made the discovery that the
Fig. 85. — Transverse section through the pharyngeal region of a young
individual of 5 mm., to show place of origin of sexual elements. (After BOVERI.)
f Fascia. e.c. Portion of ccelom, which will form the endostylar ccelom,
ug. Primitive sexual cells in the lower angle of the myoccel. Other letters as above.
primitive sexual cells arise in the cavity of the myotome
by differentiation of certain of the epithelial cells lining
the myoccel.
It had previously been assumed that they were derivatives
152 DEVELOPMENT OF AMPHIOXUS.
of the peritoneal epithelium lining the general body-cavity.
The fact that they arise in the way shown by Boveri is one
of great morphological importance.
In a transverse section of a young individual 5 mm.
in length, the primitive sexual cells are to be recognised
as a closely packed group of cells, with large nuclei in the
lower angle of the myotome ; that is, in the angle formed
by the membrane which divides the myoccel from the
splanchnoceel, which we may call the zxztercelic membrane,
with the cutis (Fig. 85). Since the myotomes of one side
alternate with those of the other, so do the centres of
Fig. 86.— Longitudinal views of the developing gonads, obtained by dissecting
out the ventral borders of the myotomes. (After BOVERI.)
u.g. Primitive sexual cells arising from the myoccelic epithelium; the nuclei
scattered about the surface of the preparations also belong to the myoccelic
epithelium.
formation of the primitive sexual cells, and in a given
section, as in Fig. 85, only one such centre is to be observed
on the right or left side of the section, as the case may be.
Its actual position in the longitudinal aspect of the myo-
tome is shown in Fig. 86 A, B, and C. The formative
centres of the primitive sexual cells lie at first in the angle
mentioned above, but applied to the posterior faces of the
dissepiments between the myotomes (Fig. 86 A).
At a somewhat later stage, having slightly increased in
bulk, they begin to push the dissepiments before them
LARVAL DEVELOPMENT. 153
so as to make a projection into the myoceel in front (Fig.
86 42, C). This projection of the primitive gonad into the
myoccel next in front of that to which it originally belonged,
is gradually carried to such an
extent that the gonad becomes
entirely shut off from its original
myoccel and hangs freely into the
next one, being connected by a
short stalk with the azterior face — Fig. 87.— Similar prepara-
f : tion as the preceding, showing
of the dissepiment and surrounded 4 jater stage in the development
of the primitive gonad. (After
by a membrane which is obviously Bove
derived from, and for some time
continuous with, the original dissepiment (Fig. 87). In
correlation with the increase in size of the primitive gonad,
an evagination of the basal wall of the myoccel in which it
now lies, takes place, and by the time the young Amphi-
Fig. 88. — Preparation showing the rhomboidal pouches of the myoccel
which project into the atrial cavity. (After BOVERI.)
This condition is found in individuals of 13-14 mm.
oxus has attained a length of 13 or 14 mm. there is, in
connexion with each primitive gonad, a wide rhomboidal
expansion of the lower portion of each corresponding
myoccel projecting into the atrial cavity (Fig. 88).
The cavity of these sacs, to the wall of which the gonads
are at this stage still united by a stalk, constitutes the so-
called perigonadial celom,4 or cavity of the gonadic
pouches, which, at the time of sexual maturity, is entirely
filled up by the sexual elements.
154 DEVELOPMENT OF AMPHIOXUS.
The gonadic pouches next become gradually constricted
off from the myoccelic spaces, and eventually lose all com-
munication with them. In the midst of the at first solid
mass of primitive sexual
cells a cavity subsequently
appears, and the gonad be-
comes a hollow sac (Fig. 89).
In the course of its fur-
ther growth the gonadic sac
(not to be confused with the
gonadic pouch in which it
lies) grows out into a num-
Fig. 89.— Portion of transverse sec-
tion through an individual of 13 mm., ber of lappets, and so_be-
to explain the conditions observed in comes a racemose reproduc-
preceding preparation. (After BOVERI.)
é.v. Blood-vessel. go. Gonadic sac. tive eland (Langerhans).
pouch). tm Tramvene muscles, ‘The He primitive sexual cells
index line to which there is no letter remain for a considerable
indicates the fold by which the gonadic
pouch becomes constricted off from the length of time in an abso-
ee lutely indifferent condition,
and it is impossible to distinguish the male from the
female.
According to LANGERHANS, sexual differentiation does
not begin to take place until the individuals have reached
a length of 17 mm., and sometimes it does not occur until
a much later period. It is inaugurated by the commence-
ment of the processes of spermatogenesis and ovogenesis.
There are no accessory sexual characters in Amphioxus,
and the sex can only be determined by an examination of
the reproductive glands.
The segmental arrangement of the formative centres
of the reproductive organs at the base of the myotomes
is again met with in the embryonic development of the
Selachians, as shown by RuckeErt (Fig. 90). Here, also,
LARVAL DEVELOPMENT. 155
the primitive sexual cells
make their first appearance
in the segmented area of
the trunk at the base of
the somites. Later on, by
differential growth, they
come to lie on the dorsal
wall of the unsegmented
peritoneal cavity, and their
primitive segmental origin
is entirely obscured ; while
in Amphioxus the primitive
segmentation of the gonads
is maintained throughout
lite. Fig. 90. — Horizontal section through
This forms another most the ventral portion of six consecutive
h , mesodermic somites of an embryo of
interesting example of the pristiurus, to show the segmental origin
the adult of the sexual elements. (After RUCKERT).
) c. Cavities of somites. g.c. Sexual
Amphioxus, in the details cells.
: : : This observation of Riickert’s has
of its organisation, €SSe€Nn- recently been doubted, with how much
: a ] th _ justice it is difficult to say, by MINOT
tially resembles mite (Gegen das Gonotom. Anat. Anz. IX. ©
bryos of the higher types. 1894. pp. 210-213).
way in which
GENERAL CONSIDERATIONS.
We will now pass on to give a general interpretation of
some of the principal phenomena which are presented to
us in the development of Amphioxus.
Larval Asymmetry.
By far the most prominent feature of the fully formed
larva is its astounding asymmetry, and it is extremely
important, from a morphological point of view, to form a
just conception of it.
I 56 DEVELOPMENT OF AMPHIOXUS.
The phenomenon of asymmetry manifests itself in the
larva of Amphioxus under several very different aspects,
and is occasioned by various causes. For convenience we
may classify the forms of asymmetry which we have to
consider under three main divisions, according to the type
of organs involved.
1. Median Asymmetry. — This relates to such structures
as lie normally in the middle line, whether dorsal or ven-
tral, but which have been mechanically or correlatively dis-
placed from their primitive position by the differential
growth of neighbouring parts. Such are the olfactory pit
and neuropore, the anus, the mouth, and the endostyle. All
these are essentially and primordially median and unpaired
structures. We have already dealt with the neuropore
and anus, while the mouth and endostyle will be con-
sidered below.
2. Bilateral Asymmetry. — This refers to the alternation
of paired structures, such as myotomes, spinal nerves, gill-
slits, and gonads, which we have already noted in the adult
organisation. Primarily the organ of one side lies opposite
to its antimere of the other side. By a secondary displace-
ment it comes to alternate with it.*
3. Unilateral Asymmetry. — Next to the asymmetrical
mouth, this is perhaps the most striking form of asym-
metry which the larva of Amphioxus exhibits. It relates
to those structures which belong to the category of paired
organs, but which, in the course of the larval development,
appear unpaired on one side of the body. Such are the
* When the myoccelomic pouches first appear in the embryo they are
placed symmetrically. At an early stage, however (see Fig. 63 B), the alter-
nation sets in. This involves such later-appearing structures as the spinal
nerves and gonads, so that they alternate from the time of their first origin.
The alternation of the gill-slits would seem to be independent of that of the
myotomes.
LARVAL DEVELOPMENT. 157
gill-slits and the praeoral pit. As described in the fore-
going pages the asymmetry of the przoral pit is a second-
ary occurrence, since it arises at first as one of a pair of
symmetrically disposed head-cavities, or anterior intestinal
diverticula, while the unilateral asymmetry of the gill-slits
is ontogenetically primary. The unilateral gonads of the
species of Amphioxus from the Bahamas and Torres
Straits also belong to this category.
Although, on account of their essentially azygous nature,
the mouth and endostyle have been separated from the
gill-slits in the above classification, it is obvious that their
asymmetrical position in the larva must be ascribed to one
and the same cause. In the succeeding pages we shall
endeavour to demonstrate what this cause was.
Explanation of Asymmetry of Mouth and Gill-shits.
It is quite evident that the primary gill-slits which
appear on the right side of the larva belong primitively,
or ancestrally, to the left side, to which, in fact, they are
eventually transferred. Meanwhile, the left side of the
larval pharyngeal region is largely occupied by the huge
oral aperture.
We may figure to ourselves the primitively left-side gill-
slits being carried over to the right side by a semi-rotation
from left to right of the pharyngeal wall. The primitive
right side of the pharynx would thus be crowded out, so to
speak, and the right-side gill-slits would be temporarily
obliterated owing to lack of room, while the original mid-
ventral line would be carried high up on the right side,
where, in point of fact, it is plainly indicated by the bran-
chial artery, which lies actually above the primary gill-slits
in the larva (Fig. 74, etc.).
I 58 DEVELOPMENT OF AMPHIOXUS.
Thus the actual topographical conditions in the larva do
not by any means coincide with the morphological rela-
tions of parts, since the morphological mid-ventral line of
the pharynx lies high up on the right side of the body. It
should be carefully noted that the form of asymmetry
which we are now considering only affects the anterior
portion of the larval body.
The same semi-rotation of the pharyngeal region which
converted the primitive left side of the larva into the
actual right side caused the primitively median mouth to
take up its position on the actual left side. But since, as
we have noted, the rotation occurred from left to right,
the mouth must have been originally situated in the
median dorsal line.
In postulating a virtual semi-rotation of the ancestral
pharynx, we do not, of course, mean to suggest the prob-
ability of an actual movement in bulk about the longi-
tudinal axis, but merely that the formative centres of the
various structures belonging to this region of the body
(gill-slits, mouth, endostyle, etc.) have, by the correlated
interaction of their component cell-groups, been diverted
from their ancestral relations through the intercalation, in
the course of the progressive evolution of the organism, of
a new and disturbing element.
We are now in a position to say what this disturbing
element is. It is the secondary forward extension of the
notochord beyond the limits of the dorsal nerve-tube to
the tip of the snout. As already stated, there is direct
evidence to show that this is a secondary and not an an-
cestral feature, inasmuch as in the young embryo (Fig.
68 dzs) the notochord is removed from the anterior extrem-
ity of the body by a very appreciable interval, which is oc-
cupied by that portion of the archenteron which gives rise
LARVAL DEVELOPMENT. 159
to the head-cavities. Moreover, as was pointed out above,
the dorsal groove of the archenteron, which gives rise to
the notochord, remains open into the archenteric cavity
in the region of the first myotome, and even somewhat
behind the level of the neuropore, for some time after
its walls have approximated to form the solid notochord
behind this region.
The forward extension of the notochord in Amphioxus
is, therefore, de facto, to a large extent an ontogenetic
phenomenon, although, from the very beginning, it shows
what may be described as a precocious tendency to extend
beyond the nerve-tube. We shall also find that there is
every reason to suppose that it is a cenogenetic, and not a
palingenetic, feature.
Since we know for an actual fact that the primary gill-
slits of the larva belong ancestrally to the left side, it fol-
lows as an absolute topographical necessity that the mouth
has been brought to one side from an originally median
dorsal position, by the same semi-rotation of the pharynx
(in the sense explained above) which has demonstrably
carried the primitive left-side gill-slits under the pharynx
up to the right side of the larva. But this is not the only
criterion by which we can judge of the ancestral position
of the mouth.
In the larvz of the Ascidians, the nearest existing rel-
atives of Amphioxus, there is a praoral lobe and a neuro-
pore, which opens at first to the exterior in the mid-dorsal
line, just as in Amphioxus. But in contrast to the latter
form the notochord does not extend forwards into the re-
gion of the przoral lobe, but it stops short behind the
cerebral vesicle.
Immediately in front of the neuropore, in the Ascidian
larva, the wall of the pharynx comes into contact with the
160 DEVELOPMENT OF AMPHIOXUS.
ectoderm and fuses with it, and then at the point of fusion
a perforation takes place, and the mouth is established in
the mid-dorsal line. During the formation of the mouth
the neuropore temporarily closes up, but subsequently it
reopens — zzZo the mouth.
In Amphioxus we can only assume that in correlation
with the forward extension of the notochord, the mouth
was compelled to forsake its primitive relations to the
neuropore and to move to one side so as to make way for
the notochord. The growth of the latter to the front end
of the body obviously prevents the wall of the pharynx
from coming into contact with the ectoderm in the mid-
dorsal line, while it leaves the neuropore unaffected, since
the nerve-tube is essentially dorsal to the notochord, and
the pharynx, on the other hand, essentially ventral to it.
This explains the fact that the hypophysis (olfactory pit)
of Amphioxus opens dorsally directly to the exterior instead
of into the mouth as it does in the Ascidian.
The secondary gill-slits — that is, those belonging to the
primitive right side of the body — present an interesting
instance of retarded or latent development. This is due
to the fact that their own side of the body is at first
usurped by their primitive antimeres, the so-called primary
slits, as a result of which they have themselves been
temporarily crowded out as mentioned above. In con-
sequence of their retardation, when they do appear to
inaugurate the process of symmetrisation, they do not
conform to the method in which metameric structures are
normally produced, but most of them —namely, from the
second to the seventh inclusive—arise simultaneously
while the first and the eighth arise somewhat later.
LARVAL DEVELOPMENT. I6I
Larval Asymmetry not Adaptive and not Advantageous ;
Forward Extension of Notochord Adaptive and Advan-
lageous.
The conclusion to be drawn from the above considera-
tions is that the remarkable asymmetry of the larva of
Amphioxus, in respect of the pharynx and the parts con-
nected with it, is of no specific advantage whatever to the
larva, but is merely a stage, which has been preserved in
the ontogeny, of a topographical readjustment of parts
necessitated by the removal of the mouth from its primi-
tive mid-dorsal position in consequence of the secondary
forward extension of the notochord, which has thus caused
a virtual semi-rotation of the pharyngeal region of the
body. On the other hand, the forward extension of the
notochord is a distinct advantage in later life, since, by
giving resistancy to the snout, it enables the animal to
burrow its way into the sand with such astonishing facility,
while the fact that it grows to the front end of the body at
a very early stage in the embryonic development, long
before it comes to be put to this definite use, must be
regarded as an instance of precoczous development of which
there are numerous and otherwise inexplicable examples
in the field of comparative embryology.
The larval asymmetry of Amphioxus is therefore a purely
secondary or cenogenetic feature, and has no directly ances-
tral or palingenetic significance, although, as we have shown
above, it serves indirectly as a clue to what the ancestral
condition was. At the same time it is a primary feature
in the actual ontogeny; that is to say, the asymmetrical
structures (mouth and gill-slits) arise zz sztw, and are not
removed in the individual development from a primary
162 DEVELOPMENT OF AMPHIOXUS.
symmetrical to a secondary asymmetrical position, as is the
case, for instance, with the neuropore.
It may appear paradoxical, but is nevertheless correct, to
say that in the ontogeny the mouth and gill-slits appear
primarily in a secondary position.
It is quite evident that the asymmetry of the larva of
Amphioxus is of a totally different character to the well-
known asymmetry of the flat-fishes or Pleuronectide
(turbot, sole, plaice, halibut, flounder, etc.). The latter
are hatched as perfectly symmetrical larve with eyes quite
opposite to one another. Then, in adaptation toa life at
the bottom of the sea, after a short pelagic existence they
turn over on one side, in some species the right side, and
in others the left, and the eye of that side moves over the
snout, sometimes even through the snout, to the other
side, and so the eyes come to lie on the same side. In this
case, therefore, the asymmetry, which is secondary in every
sense of the word, is the result of a special adaptation to a
particular habit of life, and is accordingly of the greatest
advantage to the fishes which possess it.
On the other hand, its extraordinary asymmetry is of
no conceivable advantage to the larva of Amphioxus, and
does not represent an adaptation to any peculiar mode of
existence whatever.
It is rather the mechanical, incidental, accessory, and
subsidiary accompaniment of another organic change which
is both advantageous and adaptive, namely, the forward
extension of the notochord; and while the excessive asym-
metry is indifferent to the pelagic larva, it would be posi-
tively detrimental to the adult.
Thus in all respects the larval asymmetry of Amphioxus
is the precise converse of the adult asymmetry of the
Pleuronectidee.®
AMPHIOXUS AND AMMOCGTES. I 63
AMPHIOXUS AND AMMOCCETES.
We will now pass on to consider what new light the
larval development of Amphioxus throws on its relation-
ship to the craniate Vertebrates.
As a type of the latter with which to make the com-
parison, we will select Aszmocetes, the larva of the lamprey,
Petromyzon, which is the nearest relative of Amphioxus
among the Craniota.
Nervus Branchialis Vagt.
Although Ammoccetes possesses an organisation which,
especially in virtue of its nervous system and _ sense-
organs, entitles it to an undoubted place among the
craniate Vertebrates, yet, on the whole, its structural ele-
ments remain in such a relatively simple condition of
elaboration that it readily adapts itself to a comparison
with Amphioxus.
At the same time the system of ganglia and peripheral
cranial nerves indicated in Fig. 91 will show what a great
gap there is between the two forms. Nevertheless, a
nerve corresponding to that which lies over the gill-slits
in Fig. g1, the nxervus branchialts vagi, has recently been
discovered in Amphioxus by van WHE, so that there
need be no difficulty in comparing the pharyngeal tract
of Ammoccetes with that of Amphioxus.
It may be added here that the nerve-supply of the
pharynx of Amphioxus was described as a branchial plexus
by Rouon and Fusari, but the origin of the nerves which
gave rise to the plexus was not satisfactorily determined,
beyond the fact that they arose from the rami viscerales
of the dorsal spinal nerves. Van WIjJHE also was not
164 DEVELOPMENT OF AMPHIOXUS.
able to determine the precise origin of the longitudinal
nerve discovered by him. This nerve, which lies on either
side at the place where the ligamentum denticulatum
passes into the gelatinous lamella derived from the inter-
coelic membrane, gives off the branches which form the
“branchial plexus.” Van Wijhe states that the origin of
the “ramus branchialis vagi” of Amphioxus is to be
sought in the eighth to the tenth dorsal spinal nerves.
Fig. 91.— Anterior portion of young Ammoccetes of 4 mm., to show extension
of brain, origin of endostyle (thyroid), relations of branchial nerves, etc. (After
KUPFFER.)
I, ll, Ill, 1V. The so-called ‘‘Hauptganglia.” / and //. Trigeminus.
III, Acustico-facialis. /V. Glossopharyngeus. V. Vagus.
au. Auditory capsule. ch. Notochord. ¢. Endostyle (hypobranchial groove,
thyroid). Ay. Hypophysis, in front of which is the nasal groove. ./. Nervus
lateralis. 2.67. Nervus branchialis. 0.f. Eye. . Pineal body (epiphysis).
~.m. Przeoral endodermic pouch (median portion of przemandibular cavity.
st. Stomodceum. /, V///, First and eighth gill-pouches; the small circles behind
the gill-pouches indicate the positions of the external openings of the gill-pouches,
which will become perforated later. The small black spots in front of the (later
appearing) external openings represent the so-called ganglia pretrematica.
He found that the nerve curved ventralwards in front and
passed downwards:through the interccelic membrane until
it reached the level of the ventral transverse muscles in
front of the visceral branch of the eleventh spinal nerve.
He was unable to follow it further in the complex nerve-
plexus which lies on the surface of the muscles. It is
probable, however, that the branchial nerve arises from
AMPHIOXUS AND AMMOCGTES. 165
the visceral branch of the eighth, ninth, or tenth spinal
nerve.*
Stomodeum, Hypophysis, and Gill-slits.
It is a common fact that the time and order of forma-
tion of corresponding parts differ greatly in the develop-
ment of different species. Thus in Ammoceetes, at the
stage shown in Fig. g1, the definitive mouth, correspond-
ing to the velum in Amphioxus, has not yet formed, but
the equivalent of the oral hood is already present in the
form of a deep in-pushing of the ectoderm which, at its
blind end, is closely applied to the anterior endodermic
wall. The mouth will break through later in the middle
of the area of contact between ectoderm and endoderm.
This ectodermic invagination, whose cavity is probably
the homologue of the vestibule formed by the oral hood
which leads into the mouth in Amphioxus, is known as
the stomodeum. Immediately in front of the stomodceum
is another ectodermic involution which is in contact with
the front of the brain, and is known as the hypfophysis or
pituitary body."
It will appear later that this is the probable equivalent
of the so-called olfactory pit of Amphioxus.
In the wall of the pharynx of Ammoccetes there are, at
this stage, the indications of eight pairs of gill-slits. They
have not yet, however, broken through to the exterior, but
consist of a succession of hollow outgrowths of the phar-
ynx stretching towards the ectoderm with which they will
eventually fuse (Fig. 92 A, B, C).
In the case, however, of the first pair of gill-pouches,
* It is not impossible that many of the rami viscerales may send up branches
to the branchial plexus, as was indeed described by Rohon. In this case,
Van Wijhe’s nerve would be of the nature of a codlector.
166 DEVELOPMENT OF AMPHIOXUS.
it does not come to a fusion with the ectoderm; but in-
stead they begin to undergo a retrogressive development
and eventually flatten completely out (Fig. 92 £). They
are thus shown to be rudimentary structures, morphologi-
cally representing the first pair of gill-clefts, but never
achieving their full development.
Fig. 92. — Horizontal sections through the pharyngeal region of Ammoccetes,
to show the relation of the first pair of gill-pouches to the peripharyngeal grooves.
(After DOHRN.)
A, Two days after hatching; first pair of gili-pouches well developed.
&B. Six days after hatching; first pair of gill-pouches flattened out.
Cc. Nine days after hatching; appearance of peripharyngeal grooves.
I-VI, Gill-pouches. 6.w. Body-wall. oes. (Esophagus. gf. Pharynx.
ph.g. Peripharyngeal groove. sf, Stomodceum. ve/. Velum.
As to their position, they occupy the extreme anterior
angles of the pharynx formed by its lateral walls with the
anterior transverse wall against which the stomodceum is
applied. Whatever may be the reason for it, the atrophy
of the first pair of gill-pouches in Ammoceetes is of pre-
cisely the same nature as the atrophy of the first gill-slit
in Amphioxus, with the distinction that the latter actually
opens to the exterior for a time.
AMPHIOXUS AND AMMOCGTES. 167
Endostyle or Hypobranchial Groove.
At a stage in the development of Ammoccetes which
precedes the flattening out of the anterior gill-pouches,
a median depression occurs in the extreme anterior
region of the ventral wall of the pharynx between the
first pair of gillpouches. In its production the wall of
the pharynx at this region projects itself ventrally and
slightly forward. This groove, which is known as the
hypobranchial groove, develops in the direction from before
backwards, and eventually extends backwards as a longi-
tudinal groove as far as the fifth pair of gill-pouches
(Fig. 91).
WILHELM MULLER showed that it was the homologue
of the exdostyle of Ascidians and Amphioxus, and he has
been amply confirmed by Dourn. It agrees with the lat-
ter structure in its origin at the anterior extremity of the
pharynx and subsequent growth backwards and in its
histological structure, the most marked feature of the lat-
ter being the four longitudinal rows of gland-cells which
were noted above in the endostyle of Amphioxus. (Cf. Fig.
13.) Like the latter, also, it is a slime-secreting gland.
In Ammoccetes the hypobranchial groove becomes
largely shut off from the cavity of the pharynx by the
gradual ingrowth of a diaphragm-like lamella which pro-
ceeds from the angle made by the groove in front with the
anterior wall of the pharynx (Fig. 91). Subsequently a
similar diaphragm grows in from the posterior margin of
the groove, and finally the latter only communicates with
the pharynx by a small aperture in the mid-ventral line
between the fourth pair of gill-pouches.
168 DEVELOPMENT OF AMPHIOXUS.
Peripharyngeal Cilitated Bands of Ammocetes.
Corresponding with the right and left peripharyngeal
ciliated bands which we described as proceeding from the
anterior borders of the endostyle in Amphioxus there is
a pair of ciliated grooves in the pharyngeal wall of Ammo-
coetes which proceed from the anterior lip of the hypo-
branchial groove after the latter has become to a large
extent shut off from the pharynx by the above-mentioned
diaphragm. These grooves curve forwards and upwards
SS
Che
Fig. 93. — Young Amphioxus, after the metamorphosis, having eight gill-slits
on each side. From the right side. (After WILLEY.)
?.6. Peripharyngeal band. v. Velum; shown separately below the main figure,
with rudiments of four velar tentacles. e¢. Endostyle, extending backwards to the
level of the fourth gill-slit. 7.7. Right metapleur.
in front of the gill-clefts (after the obliteration of the first
pair of gill-pouches), and then proceed backwards on either
side of the dorsal middle line of the pharynx as far as the
commencement of the cesophagus. Here they appear to
curve downwards again, and uniting together, extend for-
wards as a median ventral groove to the posterior lip of
the hypobranchial aperture.
AMPHIOXUS AND AMMOCGTES. 169
The last-mentioned median ciliated groove would appear
to be unrepresented in Amphioxus, but the downward
curvature of the ciliated bands of the latter behind the gill-
slits can be observed (Fig. 93).
In Ammoceetes the ciliated peripharyngeal grooves,
where they curve upwards in front along the anterior wall
of the pharynx, apparently occupy the same position which
was previously occupied by the first pair of gill-pouches.
Since the latter have already entirely disappeared, there is
nothing in the way of their occupying this position (Fig.
g2 C). In Amphioxus, where the corresponding gill-slit
remains open for a long time, the peripharyngeal band exists
without connexion of any sort with the portion of the wall
occupied by the slit, and when the latter closes up, it leaves
no trace behind.
Thyroid Gland.
When the metamorphosis of Ammoccetes into Petromy-
zon takes place (which happens after a larval existence of
some two years’ duration), the hypobranchial groove loses
all connexion with the pharynx and becomes broken up
by the ingrowth of connective tissue into a number of
separate capsules which collectively constitute the thyroid
gland of Petromyzon.
The thyroid gland is one of those enigmatical ductless
glands which form such a curious and constant feature of
the Vertebrate organisation.
There is considerable doubt as to the specific physio-
logical function which it has to perform, but at the same
time it is a necessary factor in the Vertebrate economy,
and is of great importance from a pathological point of view.
In the higher forms it is attached to the lower side of
the larynx, and appears to have received its name on
170 DEVELOPMENT OF AMPHIOXUS.
account of its close proximity to the thyroid cartilage of
the latter, the older anatomists assuming a functional
relation between the two structures.
We know perhaps more about the morphological than
about the physiological significance of the thyroid gland,
since it is the vestige of the very actively functional endo-
style or hypobranchial groove of the Ascidians, Amphioxus,
and Ammoceetes.
Morphology of Club-shaped Gland of Amphioxus.
In describing above the formation of the second row of
gill-slits in Amphioxus, we found that the first secondary
slit paired with the second primary slit. It now remains
to consider what has become of the antimere of the first
primary slit.
The probability is that, unlike the antimeres of the suc-
ceeding primary slits, that of the first has not suffered a
retardation of development, but is present from the very
beginning of the larval development, although in a some-
what modified form. I refer to the club-shaped gland.
The club-shaped gland fulfils the requirements of a gill-
slit in so far as it opens at one end into the pharynx, and
at the other to the exterior. Since, as we have shown, the
morphological mid-ventral line lies high up on the right
side, immediately above the primary gill-slits, it is evident
that its anterior continuation would pass through the en-
dostyle precisely at the point where the latter is redoubled
upon itself. But the internal opening of the club-shaped
gland lies above the upper limb of the endostyle, and
therefore it is placed not only on the actual right side of
the larva, but in opposition to the first primary slit, on the
morphological right side as well.
AMPHIOXUS AND AMMOCGTES. Ld
It must be supposed that the original gill-slit, from
which the club-shaped gland is derived, acquired, for some
reason or other, a tubular form.
A familiar precedent for gill-slits being drawn out into
elongated tubes, the effect of which is to separate the in-
ternal from the external opening by a long interval, is
presented by the hag-fish, JZyazze. Myxine also shows us
that, in correlation with the canalisation of the gill-slits,
their external apertures may enter into new relations dif-
fering considerably from the primitive condition. As is
well known, the elongated tubular gill-clefts of Myxine do
not open separately to the exterior, but fuse together at
their distal extremities, so as to give rise to a longitudinal
duct on each side, which opens to the exterior some dis-
tance behind the gill-region.
It is only on some such supposition as this—namely, that
the external aperture of the gill-slit represented by the
club-shaped gland of Amphioxus has assumed new topo-
graphical relations in correlation with the canalisation of
the original slit — that its position on the opposite (left) side
of the body to the internal opening of the gland is ren-
dered intelligible. The position of the internal opening
furnishes the criterion by which to judge of the primitive
relations of the original gill-slit.
With the above point of view, therefore, we may signal-
ise the following facts to prove that the club-shaped gland
is the antimere of the first primary gill-slit.
1. They arise simultaneously in the embryo as grooves
in the ventral wall of the pharynx.
2. They come to lie on opposite sides of the morphological
median line —the first gill-slit entirely so, and the
club-shaped gland in respect of its internal opening
into the pharynx.
172 DEVELOPMENT OF AMPHIOXUS.
3. They atrophy and disappear simultaneously during the
metamorphosis of the larva.
4. No secondary gill-slit ever arises to pair with the first
primary slit.
As the stage represented in Fig. 64 marks such a vital
turning-point in the development of the individual, being
the stage at which the embryo becomes a larva and the
struggle for existence in obtaining independent nourish-
ment genuinely sets in, it is important to be able to define
it accurately. In view of the above considerations, we
arrive at the conclusion that the larva is at this stage
possessed morphologically of a pair of gill-slits.
It should be pointed out that this opening stage of the
larval development appears to be of the nature of a vest-
ang phase, during which the larva accumulates energy for
future growth.
Preoral “ Nephridium”’ of Hatschek.
In the larvee of Amphioxus there is a structure lying at
the base of the notochord on the left side, immediately
above the preoral pit, which we have not yet consid-
ered. (Cf. Figs. 81 and 82, x.) According to Hatschek, who
first described it, it arises in the larva as a mesodermal,
ciliated funnel and canal in front of the mouth, in the
region of the first metamere. It lies in a narrow division or
prolongation of the body-cavity, beneath the left aorta. (CE
Fig. 768.) At its hinder end it opens into the pharynx.
Hatschek interprets this structure as a nephridium. Its
true physiological, and especially its morphological, sig-
nificance is, however, very perplexing and requires further
study.
AMPHIOXUS AND AMMOCCTES. 173
Ancestral Number of Gill-slits.
The unlimited number of gill-slits in the adult Amphi-
oxus has led to a good deal of controversy as to the ap-
proximate number present in the ancestral Vertebrate,
some authorities being of the opinion that Amphioxus
presents the primitive condition in this respect, and
others that the multiplication of gill-slits in this form
was a secondary phenomenon.
Sometimes as many as fourteen pairs of gill-clefts are
found in a remarkable cyclostome fish from the Pacific,
allied to Myxine, and called Sdellostoma.* With this ex-
ception, no true fishes, recent or fossil, are known which
possess more gill-slits than the existing sharks belonging
to the family of the JVotzdanide. Of these the genus
Heptanchus possesses eight gill-clefts (ze. seven plus the
spiracle) on each side, and Heranchus seven. In Ammo-
coetes, as we have seen, there are at one time indications
of eight pairs of gill-slits. The first pair of these, how-
ever, never breaks through to the exterior, and eventually
disappears, but Dohrn has shown that the primary rela-
tion in which the seventh pair of cranial nerves stands to
it, indicates that it is the homologue of the spzvacle of the
higher forms.
Moreover, in the larval development of Amphioxus
several facts combine to produce the impression that the
indefinite number of gill-slits in the adult is a secondary
acquirement. First of all, there is the series of primary
gill-slits which, while varying within narrow limits, usually
numbers fourteen. Their unpaired unilateral character is
merely incidental, as explained above, and it may be stated
* For a recent account of Bdellostoma, consult HowARD AYERS, No. 69,
bibliography.
174 DEVELOPMENT OF AMPHIOXUS.
that they are potentially paired, the first of them in all
probability being actually paired (with the club-shaped
gland).
In the second place, after the closure of a number of
the primary slits, the so-called crztzcal stage occurs with
eight pairs of gill-slits. This is another resting phase in
the development, and marks the turning-point from the
Jarval to the adolescent period. Subsequently the addi-
tion of new gill-slits behind those already present com-
mences and goes on indefinitely throughout life.
Counting in the first pair of slits (z.e. first primary slit
plus club-shaped gland) which is destined to atrophy, we
must regard it as probable that the proximate common
ancestor of Amphioxus and the higher Vertebrates was
characterised by the presence of from xzne to fourteen
pairs of gill-clefts, although it is also probable that there
was a variable tendency to add to this number by fresh
perforations.
NOTES.
I. (p. 105.) It is unaccountable how there can have been
conflicting statements as to the ejection of the genital products
(male and female) through the atriopore. It was first observed by
DE QUATREFAGES in 1845, and his observations have since been
fully confirmed by PauL Bert, A. WILLEY, and E. B. WiLson. On
the other hand, both Kowatevsky and Hartscuexk affirm that they
are discharged through the mouth. It is to be regretted that two
such eminent observers should have committed this error, since it
is difficult to eradicate it from the text-books.
2. (p. 115.) The primitive endoderm cells in the neighbour-
hood of the neurenteric canal apparently retain an undifferentiated
character, until the completion of the myotome-formation. In the
young embryo they are to be observed in transverse section in pro-
cess of division, numbers of karyokinetic figures being present.
But the cells divide without regard to the median plane of sym-
NOTES. 175,
metry, and the recent researches of E. B. Witson and Lworr lead
to the conclusion that the so-called mesoblastic pole-cells, which
were described by HarTscHEk, have no real independent existence.
3. (p. 123.) Whether the dorsal and ventral fin-spaces are
actually derived from the original myoccel, as described by Hat-
schek, or do not rather arise by a splitting of an originally solid
thickening of the gelatinous connective tissue which surrounds
them, must remain doubtful. The cavity of the metapleural folds
certainly arises as a schizocel, t.e. by a hollowing out of a solid
thickening. Even in case the fin-spaces also arise as schizoccels,
Hatschek’s interpretation of their morphological significance might
still hold good.
4. (p. 123.) A transitory pouch-like diverticulum of the myo-
coel has been observed in connexion with the formation of the
sclerotome in the Selachian embryo by Rast and H. E. ZIecver.
5. (p. 129.) Since the work of BaLrour on the development
of Elasmobranch fishes (Selachians), it has been known that the
paired praemandibular head-cavities communicate with one another
across the median line in the embryo. ‘The important results
obtained by the researches of KupFFER (Petromyzon, Acipenser),
KAsTSCHENKO (Selachian), and Juia Piatr (Selachian), not only
established the fact that the praeemandibular cavities arose essen-
tially as anterior archenteric pouches (cf. Fig. 72), but also that
the median cavity which effected their communication across the
middle line, from side to side, arose by constriction from the front
end of the archenteron (using the latter term with some latitude),
and that, therefore, the wnzon of the right and left premandibular
cavities in the embryo of the craniate Vertebrates is primary, and
not secondary, as was previously supposed.
For an excellent historical and critical summary of our knowl-
edge of the origin of the head-cavities in the craniate Vertebrates,
the reader may consult Froriep. (See bibliography.)
6. (p. 130.) The ciliation of the ectoderm in the larva of
Amphioxus continuing, as it does, long after the muscles have been
fully differentiated, and when the cilia are therefore no longer
required for purposes of locomotion, should be especially noted as
evidence of a very archaic organisation.
We shall find in the last chapter that the possession of a ciliated
176 DEVELOPMENT OF AMPHIOXUS.
ectoderm is a prime characteristic of Bal/anoglossus and many of
the lower worms (e.g. /Vemertines). In none of the craniate
Vertebrates is the ectoderm at any time ciliated.
7. (p. 134.) The exact stage at which the club-shaped gland
reopens into the pharynx must remain an open question. It is,
very probably, subject to a good deal of variation in this respect,
occurring now earlier, now later. Experiments to determine the
physiological role of this gland are much needed.
8. (p. 143.) In accordance with Dohrn’s conception of the
principle of the change of function (Das Princip des Functions-
qwechsels), the number and nature of the organs of the Vertebrate
body, which have been interpreted as modified gill-clefts, are truly
astonishing. First and foremost, Dohrn supposed that the Verte-
brate mouth arose by the fusion of two gill-slits across the middle
line, the old Annelid-mouth, which perforated the central nervous
system, having been lost. A great many forcible arguments have
been brought forward in support of this hypothesis. Dohrn him-
self would probably admit that it is only tenable on his further
hypothesis that Amphioxus is a form which has undergone a retro-
gressive evolution from the craniate Vertebrates. This was a
better hypothesis than that of Semper, who, perceiving that
Amphioxus would not fall in with the Annelid-theory, declared,
“er sel kein Wirbelthier ; also, auch kein Fisch.”
Besides the mouth, many other structures have similarly been
referred back to modified gill-slits, among which may be mentioned
the nose, hypophysis, thyroid gland, lens of the eye, and the anus.
None of these comparisons is supported by the facts of develop-
ment and anatomy of either Amphioxus or the Tunicates, while
most of them would appear to be definitely disproved by these
facts.
9. (p. 147.) Since the right metapleural fold bends round to
the median ventral line of the snout, as shown in Fig. 38, and
since, further, at a later period, the right half of the oral hood is
similarly continued round the front end of the body into the
dorsal fin, it is clear that the right half of the oral hood must
arise essentially in continuity with the right metapleur. On the
contrary, the left half of the oral hood arises entirely independently
of the left metapleur. It is possible that this discontinuity of
NOTES. 177
development of the left half of the oral hood and the left meta-
pleur has been secondarily brought about.
10. (p. 150.) The study of transverse sections has led me to
the conclusion that the backward extension of the endostyle is
effected by interstitial growth, and not by the conversion of the
cells which form the primary floor of the pharynx into endostylar
elements. These cells are probably disintegrated and absorbed
by the endostyle as it grows backward.
It. (p. 153.) For a comparison between the perigonadial
cavities of Amphioxus and the mesonephric tubules of the
craniates the reader should consult Boveri’s original memoirs.
(See bibliography.)
12. (p.159.) The following definition of the so-called bio-
genetic law of recapitulation (Haeckel’s biogentisches Grund-
gesetz) will explain the meaning of Haeckel’s terms “ cenogenesis ”
and “ palingenesis.” According to this law: The development of
the individual (onfogeny) is a compressed summary of the gradual
modifications which have resulted in the evolution of the species,
or type (phylogeny = Stammesgeschichte) ; this recapitulation
(summary, or Auszug) of the phylogenetic stages in the ontogeny
is the more perfect according as the ancestral development
(Palingenesis, Auszugsentwicklung) has been the less disturbed
or falsified through secondary or “recent” adaptation (ceno-
genesis, Stdrungsentwickelung) of the embryo or larva to a new
environment.
13. (p. 162.) The explanation of the asymmetry of the larva
of Amphioxus given in the text was first suggested by me in 1891.
It may be well to state that it has not as yet received very general
recognition in the more recent literature on the subject. It was,
however, fortunate enough to receive the endorsement of the late
Professor MitNes MarsHALt in his text-book of Vertebrate Em-
bryology. When the pelagic larvae of Amphioxus are confined in
glass jars, after a certain lapse of time they sink to the bottom,
like all other pelagic organisms. When they arrive at the bottom,
they fall over on to one side, owing to a physical impossibility to
rest in any other position, just as was described above for the
adult. It ought not to require to be emphasised that their inci-
dentally lying on one side is not due to a pressing desire or
I 78 DEVELOPMENT OF AMPHIOXUS.
instinct to assume that position, but rather because they cannot
help it. It is apparently in consequence of a misunderstanding
of this observation that KorscHetr and Hetper ascribe the larval
asymmetry of Amphioxus to the same causes which brought about
the asymmetry of the Pleuronectidz. Another, and, as it appears,
a still more impossible view, has recently been expressed by vAN
WijHE. According to van Wijhe, the left-sided mouth occupies its
normal and primitive position in the larva of Amphioxus, and in
that position it represents a gill-slit, whose antimere is the club-
shaped gland. Van Wijhe arrived at this view as a result of his
very important discoveries as to the musculature and innervation
of the adult mouth. These discoveries may be summarised as
follows : —
1. The outer muscle of the oral hood represents the anterior
continuation of the /e/t half only of the transverse and subatrial
muscles.
2. The inner nerve-plexus of the oral hood is formed on both
sides, exclusively from nerves which arise from the left side of the
central nervous system.
3. The velum is innervated entirely from nerves of the left side.
From these observations van Wijhe concludes that the mouth of
Amphioxus, even in the adult, is essentially an organ of the left
side, and is neither homologous with the Ascidian nor with the
craniate mouth.
It would seem, however, that the more obvious and justifiable
interpretation of these facts is that the asymmetrical musculature
and innervation described by van Wijhe are merely the partial
persistence in the adult of the more complete asymmetry of the
larva.
Van Wijhe’s observations, therefore, do not affect the question
of the cause of the asymmetry in any degree.
14. (p. 165.) As first shown by Dohrn, the hypophysis of
Ammoceetes first arises from the roof of the stomodceum, from
which it is subsequently removed to the dorsal surface of the head
by the enormous development of the upper lip.
15. (p. 169.) The ciliated tracts in the pharynx of Ammo-
coetes were first described and figured by ANTON SCHNEIDER in
NOTES. 179
1879. In 1886 DouRN thought he had proved that the anterior
portion of them, which bends upwards on either side of the
pharynx and forms the sevipharyngeal grooves, represented the
last traces of the aborted first pair of gill-clefts. Although they
appear at the place which was formerly occupied by these rudi-
mentary gill-pouches, yet, according to Dohrn’s own account, they
do not appear until after the gill-pouches have completely flattened
out. Under these circumstances, but above all, in view of the
relations of the homologous peripharyngeal bands in Amphioxus
which exist both before and after the disappearance of the first
pair of gill-clefts (¢.e. first primary gill-cleft and club-shaped
gland), it must be assumed that Dohrn’s interpretation, though
most natural, was nevertheless somewhat at fault.
LV.
THE ASCIDIANS:
Tue Ascidians, Tunicates, or sea-squirts, as they are
indifferently called, constitute one of the most clearly
defined and yet most heterogeneous groups of animals
which it is possible to imagine. There is a great variety
of families, genera, and species occurring all the world
over, and in all depths of the ocean from the tide-marks
to the profoundest depths.
Most of them are sedentary animals, remaining fixed
all their lifetime on one spot, whether attached to rocks,
stones, shells, or sea-weeds, from which they are incapable
of moving. There are, however, several very extraordi-
nary genera of Ascidians which swim or float about per-
petually in the open ocean, and have become adapted in
the extremest manner to a purely pelagic environment.
These pelagic Ascidians have become so modified in adap-
tation to their oceanic existence, and their development
diverges, as a rule, so much from the normal, that they
will hardly enter at all into the present discussion, with
the exception of one family, the Appendiculariea.
Just as there are two kinds of sessile Ascidians, szwple
and compound or colonial, so there are two analogous kinds
of pelagic Ascidians. In some of the latter, however,
where there is an alternation of generations, one genera-
tion, namely, the asexual generation, is a solitary form,
while the sexual generation is a colonial form, as, for
example, the solztary Salpa and the chain-Salpa.
180
ANATOMY AND DEVELOPMENT. I8I
For convenience, the Ascidians, as a whole, may be
arranged as follows :—
SESSILE ASCIDIANS.
SIMPLE. COLONIAL.
e.g. Ascidia. e.g. Clavelina.
Phallusia. LBotryllus.
Ciona. Aniaroucium.
Molgula. Distaplia.
Cynthia. Didemnum.
PELAGIC ASCIDIANS.
SIMPLE. COLONIAL
e.g. Appendicularia. (or capable of producing a colony
by budding).
e.g. Pyrosonma.
Salpa.
Dotiolum.
The compound sessile Ascidians consist of colonies of
individuals or asczdiozooids produced by budding from a
parent individual. Such colonies are often brilliantly
coloured and of massive proportions, as Amaroucium and
Fragarium. Others form thin encrusting expansions on the
surfaces of marine plants and shells, as Botryllus and L epto-
clinum. In others, again, the individuals are entirely
separate, except at the base, where they are connected
together by a common creeping stolon from which new
buds are periodically produced, as Clavelina and Perophora.
STRUCTURE OF A SIMPLE ASCIDIAN.
Test, Mantle, Atrium, Branchial Sac.
The simple or solitary Ascidians which do not produce
buds, present hardly less striking differences among the
different families than do the compound, but their general
shape is much more uniform.
182 THE ASCIDIANS.
An average simple Ascidian, as Phallusta or Cynthia,
has been aptly compared to a leather bottle provided with
two spouts. The spouts occur in the form of two funnel-
like prominences projecting from the surface of the body
and bearing at their free extremities the zzcurrent or buc-
cal and excurrent or cloacal apertures respectively, the
latter usually occurring at a lower level than the former.
The most prominent and, apart from the two apertures,
the only external feature of a simple Ascidian, is the char-
acteristic ¢azc or zest which surrounds the whole body. As
a rule, all Ascidians of whatever kind possess this external
tunic, and it is one of their chief diagnostic characters.
According to the species this test may be of a cartilagi-
nous, coriaceous, fibrous, or membranous consistency,
usually opaque, but sometimes hyaline and transparent, as
in Corella, Salpa, etc. Its outer surface may be smooth,
wrinkled, or rough, capillated, papillated, or mammillated.
In 1845 Kart ScHMIDT made the discovery that the test
of the Ascidians was largely composed of the substance
which forms the cell-walls in plant tissues ; namely, ce//u-
Jose. When treated with the proper chemical reagents, it
gives the cellulose-reaction. This is interesting as show-
ing the fundamental identity of protoplasm whether it
occurs in animal- or in plant-cells, since in both cases it -
is capable of depositing cellulose.
Judging by external appearances an ordinary Ascidian
resembles nothing so little as Amphioxus, and yet it is
probably more closely related to the latter than is the
lamprey larva, Ammoccetes, whose external resemblance
to Amphioxus is incomparably greater.
It is only in its internal organisation that we meet with
structures which remind us strongly of corresponding
parts in Amphioxus.
ANATOMY AND DEVELOPMENT. 183
A schematic representation of a dissection of a typical
Ascidian after Professor W. A. HERDMAN, whose reports on
the Ascidians collected during the voyage of H. M. S.
Challenger have done so much to advance our knowledge
of the group, is given in Fig. 94. The greater part of the
thick cartilaginoid test (also called tunic, outer mantle, or
cellulose mantle), 4 is supposed to be removed from the
right side, and its cut edge can be traced all the way round.
Below the test comes the inner or muscular mantle, 72,
which is the true body-wall, to which the external tunic is
secondarily superadded.t The muscular mantle is limited
externally (below the test) by the epidermis, and beneath
the latter are the interlacing muscle-fibres which compose
the bulk of the mantle.
Beneath the mantle is an extensive cavity surrounding to
a large extent the viscera. This is the perzbranchial or
atrial cavity which communicates with the exterior by the
atrial or cloacal aperture, az.s.
The mouth, os, leads into the pharynx or branchial sac,
ph, which is of surprising dimensions, and stretches nearly
to the posterior end of the body. The walls of the bran-
chial sac are perforated by innumerable gill-openings, the
so-called stzgmata, arranged in successive transverse rows,
through which the water which enters at the mouth passes
out of the sac into the atrial cavity.
Dorsal Lamina, Endostyle, and Peripharyngeal Band.
On cutting through its right wall we open into the
cavity of the branchial sac along the dorsal side of which
a fold is seen projecting freely into the cavity, the so-called
dorsal lamina corresponding to the dorsal groove in the
pharynx of Amphioxus, while along its ventral side is a
184 THE ASCIDIANS.
\\
unl nas uN ai ;
mee F
\ gaqnsnnel
Too
coo sr
Fig. 94. — Diagram of a dissection of Asczdia, from the right side. (After
HERDMAN.)
The peribranchial cavity is indicated by the black shading.
an. Anus. at.s. Atrial siphon. c.g. Cerebral ganglion, beneath which is the
subneural gland and its duct. a@./. Dorsal lamina. ewzd. Endostyle. 2. Gonad.
g.d. Genital duct. zz¢. Intestine. 2. Muscular mantle. oes. Aperture, leading
from branchial sac into cesophagus. o7.s. Buccal siphon. ff. Branchial sac.
st. Stomach. ¢# Test or cellulose mantle. ‘7. Buccal or coronary tentacles.
ty. Typhlosole; internal fold of intestinal wall, to increase the digestive surface.
ANATOMY AND DEVELOPMENT. 185
well-defined groove with white glistening walls, which is
the exdostyle. The groove of the endostyle is deeper here
than in Amphioxus, but its epithelial walls have the same
histological differentiation, with the two rows of gland-
cells on each side of the middle line, the latter being
occupied by a median group of cells carrying very long
cilia. The food which enters the mouth together with the
water does not pass out of the pharynx into the atrial
chamber, but is caught up by the slime secreted by the
endostyle and is then carried forwards along the endostyle,
and, having arrived at the anterior extremity of the latter
at the base of the buccal tube, is carried round along a
circular ciliated groove which surrounds the base of the
mouth at the entrance to the branchial sac, until it reaches
the dorsal side of the animal, when it is led backwards by
the ciliary action of the cells of the dorsal lamina in the
form of a cord of slime in which the food-particles (micro-
scopic organisms, vegetable débris) are imbedded.
The ciliated groove round the base of the buccal tube
connecting the anterior extremity of the endostyle with the
dorsal lamina is known as the peripharyngeal band or
pericoronal groove. Ne have already made the acquaint-
ance of the homologue of this structure both in Amphi-
oxus and in Ammoccetes. It forms a complete circle
round the base of the buccal tube and is indicated in
Fig. 94 by the black line which limits the pharyngeal
wall anteriorly. It is still better shown in Fig. 96, which
represents a young individual of Clavelina.
The cord of slime containing the food passes backwards
along the dorsal lamina to the opening of the cesophagus,
which lies near the posterior end of the branchial sac, in
the dorsal middle line, through which it passes into the
stomach. The dorsal lamina is continued to one side of
186
THE ASCIDIANS.
the oesophageal aperture, as a low ridge, which joins the
posterior extremity of the endostyle.*
Visceral Anatomy.
Except in its most anterior region, the dorsal border of
the pharynx lies freely in the atrial chamber.
On the
contrary, along its ventral border, throughout the whole
section
(After
HERDMAN.) ‘The muscular mantle is indicated
by the black shading.
a, Peribranchial cavity traversed by numerous
vascular trabeculze, through which the blood flows
into the branchial bars. 47.5. Branchial sac.
é.v. “ Blood-vessels.” d./. Dorsallamina. e. Endo-
style. ec. Ectoderm. gy. Gonad. gd. Double
genital duct. 7. Intestine, with tvphlosole. 7. Rec-
tum, 7.0. Renal vesicles. 7# Test.
Fig. 95. — Diagrammatic transverse
through the middle of the body of Asczdza.
length of the endo-
style, it is attached to
the muscular mantle.
In other words, the
right and left halves
of the atrial cavity are
continuous round the
dorsal side of the
pharynx, but)! Gare
separated from one
another ventrally by
the concrescence of
the endostyle with
the mantle. (Cf. Fig.
95.) In Amphioxus,
as we have seen, the
opposite condition ob-
tains. There, the dor-
sal wall of the pharynx °
is closely applied to
the notochord, while
the endostylar tract
* Compare the above with
the description of the course
of the ciliated tracts in the
pharynx of Ammoccetes,
given on p. 168.
ANATOMY AND DEVELOPMENT. 187
is free, so that the right and left halves of the atrial
cavity are continuous ventrally, instead of dorsally.
In order to see the stomach and intestine, it is necessary
to cut through the left wall of the pharynx, since the vis-
cera lie, at least in the genus Ascidia (or Phallusia), on
the left side of the pharynx. It should be pointed out
that the topographical arrangements vary considerably
among the different genera of Tunicates. In Clavelina,
for example, the viscera lie behind the pharynx, as shown
in Fig. 96.
On the left side of the pharynx (Fig. 94) the short
cesophagus leads into the dilated stomach, which again
narrows down to the looped intestine, and finally the lat-
ter bends sharply forwards into the rectum, which opens
by the anus into the atrial cavity, the excrement being
carried to the exterior by the constant stream of water
which flows out through the atrial or cloacal aperture.
Instead of being straight, as in Amphioxus, the aliment-
ary canal is here doubled round upon itself. This U-shaped
character of the alimentary canal of Ascidians is shown
with great clearness in the case of Clavelina (Fig. 96),
where there are no secondary convolutions in the course
of the intestine.
The Ascidians are one and all hermaphrodite, and the
reproductive glands frequently lie between the loops of
the intestine, while two ducts, ovzduct and vas deferens,
which often present the appearance of a single duct with
a double lumen, proceed forwards by the side of the rec-
tum, to open into the cloacal region of the atrial cavity
near the anus (Fig. 94, ¢ and gd).
The ovary and testis, though quite separate in the adult,
originate, according to the account given by the Belgian
zoologists, EDOUARD VAN BENEDEN and CHARLES JULIN,
188 THE ASCIDIANS.
from a common centre of formation, which subsequently
undergoes a division into two portions, one of which be-
comes the ovary, and the other the testis. Similarly the
oviduct and vas deferens are derived by division of a
primarily single structure, which arises in continuity
with, and in fact as an outgrowth from, the primitive
sexual gland.
In spite of their hermaphroditism, it would appear that
not all the Ascidians are self-fertilising, although many, if
not most of them, are. In some cases it is supposed that
in different individuals the male and female organs attain
maturity at different times, so that in a given individual,
when the ovary is ripe the testis is unripe, so that it must
be fertilised from another individual, in which the testis is -
ripe, but the ovary unripe, and so on.
Nervous System and Hypoplysts.
(Neurohypophysial Systent.)
The central nervous system of an Ascidian usually bears
a ridiculously small proportion to the bulk of the organ-
ism. Its main constituent is a ganglion which lies im-
bedded in the thickness of the mantle, between the oral
and the atrial siphons, the two latter structures being
innervated by nerves proceeding from the ganglion. As
belonging to the central nervous system must also be
mentioned a solid nerve-cord which runs along the dorsal
border of the branchial sac from the cerebral ganglion
to the visceral region (Fig. 96). This was discovered by
van Beneden and Julin, and is derived from a persistent
portion of the central nervous system of the larva.
Beneath the cerebral ganglion is a lobulated glandular
organ known as the sabneural gland. It is provided with
ANATOMY AND DEVELOPMENT.
189
a duct which runs forward and opens at the end of a
ciliated funnel-shaped dilatation into the branchial sac at
the base of the buccal tube
(Figs. 94, 96, and g7) in
front of the peripharyngeal
band.
The branchial opening of
the duct of the subneural
gland appears primarily as
a simple circular orifice, but
it does not usually retain
this character in the adult.
Generally it assumes a
crescentic form by the in-
curving of its anterior or
posterior lip, and then in
many cases the horns of the
crescent so formed become
coiled over and over con-
centrically, and usually in
the
plane, so that the lips of
approximately same
the aperture assume a very
complicated appearance and
constitute the so-called dor-
sal tubercle (Fig. 97).
It has taken a long time
and the work of a great
many zoologists to achieve
our
(which
present knowledge
is by no means
Fig. 96. — Young Clavelina, shortly
after the metamorphosis, from the right
side. (After VAN BENEDEN and JULIN.)
at. Atrial opening. afc. Atrial cav-
ity. 3.5. Blood-sinus. ed. Endostyle.
ep. Epicardium; outgrowth from bran-
chial sac behind endostyle, which grows
down into the creeping stolon, forming
a septum in the latter, and being the
chief element in the production of buds.
f Lobes of the fixing organ, which give
rise to the creeping stolon. .. Ganglion.
gs. Stigmata. 4. Heart. Ay. Hypophysis
(dorsal tubercle). 7zz/. Intestine. 7.
Mouth. oes. Esophagus. 4.0. Periphar-
yngeal band. fc. Pericardium. 7 Re-
mains of tail, withdrawn into the body.
v.m, Visceral nerve.
complete) of the subneural gland of Ascidians and its
duct.
Fig. 97. — Hypophysis of Phad/usia
mentula, prepared out and seen from the
inside. (After JULIN.)
g- Subneural gland, above which may
be seen the outline of the ganglion and its
nerves. ad. Duct of the subneural gland.
z. Dorsal tubercle, the opening of the
hypophysis into the branchial sac. The
actual opening is indicated in black.
pc. Peripharyngeal groove. ep. Epi-
branchial groove. d./. Dorsal lamina,
slightly displaced, to show the duct of the
subneural gland above it.
N.B.—In this species, the atrial and
buccal siphons are widely separated, and
the duct of the subneural gland is very long.
THE ASCIDIANS.
The dorsal tubercle was
discovered by the celebrated
SAVIGNY in 1816, and was
for a long time supposed to
be an independent sense-
organ of an olfactory nature.
The subneural gland was
detected not as a gland, but
aS an enigmatical structure
lying below the brain by
the English naturalist Han-
COCK in 1868.
character was demonstrated
by NassonorF and Ussow
in 1874-75, the last-named
author showing its connex-
ion by means of the duct
with the dorsal tubercle. In
1881 JULIN produced an
admirable memoir on the
Its glandular
subneural gland and its duct,
and strongly urged its ho-
mology with the pituitary
body or hypophysis cerebri
of the higher Vertebrates.
The same suggestion was
made in a more tentative
form in the same year by
BaLrour. We shall have
to consider this question
Suffice it to say at
present that Julin’s sugges-
later.
tion has been accepted to
ANATOMY AND DEVELOPMENT. IOI
the extent that the subneural organ of the Ascidians is
frequently spoken of as the Aypophyszs.
Circulatory System.
With regard to the circulatory system the Ascidians
differ markedly from Amphioxus in the possession of a
well-defined eart which lies in a distinct pericardium.
The heart lies ventrally and usually in the neighbourhood
of the stomach. (Cf. Fig. 96.) Its wall is muscular, but
consists only of a single layer of cells whose deeper portions
(2.c. towards the cavity of the heart) are drawn out into
striated muscular fibres, while the outer portions of the
cells containing the nuclei project into the cavity of the
pericardium.
There is therefore no true endothelial lining to the heart,
and the cells which build up its wall offer a most interest-
ing example of epithelio-muscular tissue, as was first pointed
out by Edouard van Beneden. This type of muscular tis-
sue, in which the muscle-fibres occur as basal prolonga-
tions of cells which still retain their epithelial character, is
found, as is well known, in the case of the body-muscles of
the Nematode or thread-worms, and is above all character-
istic of the Coelenterata (Hydroids and Medusz).
There are no true blood-vessels in Ascidians, but the
passages along which the blood percolates are merely
lacunze in the connective tissue and musculature of the
body and between the viscera. They are not lined by an
endothelium, and are more correctly described as. b/ood-
sinuses. They are often irregular in their outline, as shown
in the transverse section represented in Fig. 95, but often
again they simulate the appearance of true blood-vessels,
as in the case of those branches which pass from the
mantle into the substance of the test, as well as the tubes
192 THE ASCIDIANS.
which traverse the wall of the branchial sac in every
direction.
In the second chapter it was pointed out that the
Vertebrate heart arose as a specialisation of a portion of
the primitive sub-intestinal blood-vessel whose calibre was
originally uniform throughout, and that in Amphioxus the
cardiac region of the vascular system retains its primitive
tubular character.
Very different is the actual origin of the Ascidian heart ;
although it is simply a dilated tubular structure, yet it
arises entirely independently of and prior to the rest of
the vascular system at a time, in fact, before the formation
of the muscular mantle and before the atrial cavity has so
far extended itself as to almost entirely replace the original
body-cavity. The blood-sinuses of the Ascidians are rem-
nants of the latter.
With the formation and growth of the atrial cavity, the
perforation of the stigmata, and the development of the
muscular mantle, the original body-cavity becomes reduced
to a system of narrow canal-like spaces which constitute
the above-mentioned blood-sinuses. The general distribu-
tion of the blood-sinuses can be made out from Fig. 95.
There are two main longitudinal sinuses, one below the
endostyle and another above the dorsal lamina, while
others are scattered irregularly in the muscular mantle ;
others again lie in amongst the viscera forming the inter-
spaces between the various parts; and finally the bran-
chial bars between the stigmata are all hollow, and their
cavities are placed in communication with the system of
sinuses at intervals as shown in Fig. 95.
The periodic contraction of the heart of Ascidians takes
place on a highly characteristic and unique plan. Each
systole occurs as a peristaltic wave of contraction passing
ANATOMY AND DEVELOPMENT. 193
from one end of the heart to the other; but the chief
peculiarity in connexion with it is, that after a certain
number of contractions in one direction the heart makes a
brief pause and then commences to contract again in the
opposite direction, and so it goes on contracting now in one
direction and now in the other. This phenomenon of
the periodic reversal of the direction of contraction of the
Tunicate heart is known as the vecurrent action of the
heart, and was discovered in 1824 by vAN HASSELT.
The discovery was first made in the case of Salpa, but it
has since been found to hold good for all Tunicates.
When the heart contracts from its posterior to its an-
terior extremity, that is to say, in the postero-anterior
direction, —the blood is thereby propelled forwards into the
blood-sinus which lies below the endostyle, and from this it
passes into sinuses which run transversely into the bran-
chial bars. In the basket-work formed by the intercross-
ing of the branchial bars, the blood has a complicated
and irregular course, and is finally collected into the dorsal
sinus which lies above the dorsal lamina. Here it flows
backwards, and after passing in amongst the viscera arrives
back to the heart. (Other branches of the sinuses pass
into the test, where they end in curious knob-like dilata-
tions.)
On the contrary, when the heart contracts in the reversed
or antero-posterior direction, the blood which has already
been oxygenated in its passage through the branchial bars
is sent to the viscera direct, and from there it collects
into the dorsal sinus, from which it is distributed over the
branchial sac, and so into the sub-endostylar or ventral
sinus, in which, it flows backwards to the heart.
On account of the above peculiarities relating to its
independent origin, the histological structure of its wall,
194. THE ASCIDIANS.
and its recurrent action, the Tunicate heart would appear
to be a unique organ peculiar to the group of the Ascid-
ians and analogous but not homologous, or only incom-
pletely so, with the heart of the Vertebrates.
Again, the vascular system of an Ascidian is only func-
tionally comparable to that of Amphioxus, since true vessels
provided with an endothelial lining are entirely absent,
their place being taken by sinuses which arose by reduction
from the original body-cavity.
Renal Organs.
The renal organs of the Ascidians have no apparent
morphological relation to those of Amphioxus, and therefore
need not detain us. They consist of a group of bladder-like
vesicles with cellular walls lying around the intestine. The
products of excretion (uric acid, etc.) are deposited inside
the vesicles in the form of solid concretions. There is no
excretory duct. In Molgula, there is a single large cylin-
drical renal sac closed at both ends and lying on the right
side of the body, behind the heart, known as the organ of
Bojanus.
Comparison between an Ascidian and Amphioxus.
Having sketched in rough outline the organisation of an
adult Ascidian, we are now in a position to consider in
what respects it resembles and in what it differs from that
of Amphioxus. We shall see that some of the most funda-
mental differences will be made good by the structure of
the larva,— such as the absence of a dorsal nerve-tube and
of a notochord.
Let us first consider the resemblances between an adult
Ascidian and Amphioxus.
ANATOMY AND DEVELOPMENT. 195
In both cases the pharynx is perforated by a great num-
ber of g2/l-apertures (gill-slits, stigmata), converting it into
a branchial sac and opening into an atrial or peribranchial
cavity instead of directly to the exterior. At the base of
the pharynx there is a longitudinal gland consisting of a
groove open throughout its whole length towards the cavity
of the pharynx, and known as the exdostyle, whose histo-
logical character is closely similar in the two cases. From
the anterior extremity of the endostyle a ciliated band of
columnar cells passes round the wall of the pharynx on
each side, in front of the gill-openings, and abuts on the dor-
sal border of the pharynx, along which it is continued back-
wards in connexion with the dorsal lamina in the one case
and the kyperpharyngeal groove in the other. This band
forms a circlet round the pharynx behind the velum, and is
the peripharyngeal band.* We shall find also that the
Ascidian hypophysis is essentially homologous with the
olfactory pit of Amphioxus.
In the Ascidians there are sphincter muscles round the
buccal and atrial siphons, and inside the former, in front of
the peripharyngeal band (pericoronal groove), there is a
circlet of tentacles corresponding perhaps to the velar
tentacles of Amphioxus. (Cf. Fig. 94, ¢z.)
The differences between the structure of an adult Ascid-
ian and of Amphioxus may appear to outweigh the resem-
blances, but it must be remembered that they are all
correlated with and accessory to the one great difference
in the mode of existence of the respective types.
An Ascidian is sessile ; Amphioxus is free. The former,
as it were, builds its house upon a rock and is immovable ;
the latter lives in the shifting sands, and is capable of
extremely active locomotion.
* As mentioned above, this band is usually grooved in the Ascidians.
196 THE ASCIDIANS.
In correlation with this sessile habit of existence we find
that the Ascidians, in contrast to Amphioxus, are hermaph-
rodite, —an almost universal condition among sessile organ-
isms of every description. They are unsegmented, the
muscles not being divided up into myotomes ; and none of
their organs (gonads, renal organs, etc.) are metamerically
repeated, unless we regard the successive transverse rows
of stigmata in the wall of the branchial sac as evidence of
metamerism. It is, however, of a totally different nature
from the metamerism of the gill-slits of Amphioxus, and
we shall see that only in the earlier stages of their devel-
opment can the stigmata of the Ascidians be compared
with the former.
Another of the most characteristic accompaniments of
a sessile mode of life is the U-shaped alimentary canal.
Instead of being a straight tube with a posteriorly directed
anus as in Amphioxus, the alimentary canal of the Ascid-
ians is doubled up upon itself, the rectum is directed for-
wards, and the anus opens into the atrial cavity. The
absence of a dorsal nerve-tube and notochord in the adult
Ascidian has been indicated above. t
In spite of these great differences, the presence of the
endostyle and the perforated wall of the pharynx in the
adult, and above all the features in the embryonic and
larval development, entitle the Ascidians to be defined as
more or less Amphioxus-like creatures which have become
adapted to a sessile habit of existence.
DEVELOPMENT OF ASCIDIANS.
The first accurate and detailed account of the embryonic
development of Ascidians was the classical memoir pub-
lished in 1867 by Kowa.evsxky in the Mémoires de
l Académie impériale des Sciences de St. Pétersbourg.
ANATOMY AND DEVELOPMENT. 197
The Ascidian larva was known long before this time,
and the external features of its metamorphosis were de-
scribed in 1828 jointly by AupouIN and MILNE-Epwarps,
to whom the discovery of the free-swimming larva is due.
Furthermore, the internal structure of the tailed larva,
and even the histological structure of the axial rod of the
tail, was described with some accuracy by KRouN in 1852,
but in ignorance of the details of the embryonic devel-
opment, he was unable to give the right morphological
interpretation to the various parts, and did not identify
the axial rod with the notochord of the higher forms.
Segmentation and Gastrulation.
The segmentation of the egg, the formation of a hollow
one-cell-layered blastula, and the flattening and_ subse-
quent invagination of one side of the blastula to form
the two-cell-layered gastrula, take place on a plan so
essentially similar to what has been described above for
Amphioxus that it is not necessary to dwell at length
upon them here. Suffice it to point out that the segmen-
tation of the Ascidian egg takes place typically, according
to VAN BENEDEN and JULIN, on a strictly bilateral plan.
That is to say, when the ovum has divided into two
blastomeres, right and left, each blastomere represents
and will give rise to the corresponding half of the larval
body, and the descendants of the first two blastomeres
can be distinguished for a remarkably long time on each
side of the middle line of the embryo, —a fact which is
highly characteristic of Ascidian development.
After the gastrula has begun to elongate, and the blas-
topore has been narrowed down by the approximation of
its lips to a small aperture situated at the posterior dorsal
extremity of the embryo, the formation of the medullary
plate occurs.
198 THE .ASCIDIANS,
Formation of Medullary Tube and Notochord.
Here, as in Amphioxus, the dorsal wall of the embryo
flattens, while the ventral remains convex, and the ecto-
dermic cells on the dorsal side become marked off from
the rest by their larger size and columnar shape. The
medullary plate extends nearly to the front end of the
embryo, while posteriorly its cells form a ring round
the blastopore.
In the formation of the medullary tube, however, there
is an important difference, and the Ascidian embryo con-
forms in this point more to the mode of development
Fig. 98.— Transverse sections through embryo of Clavelina Rissoana, to show
mode of formation of medullary tube and mesoderm. (After DAVIDOFF.)
A. Through anterior region of embryo, with medullary groove still open.
8. Through posterior region, with closed medullary tube.
ch. Rudiment of notochord. ec. Ectoderm. ez, Endoderm, mes. Mesoderm.
m.g. Medullary groove. m.¢, Medullary tube.
which is typical of the higher Vertebrates than does
Amphioxus. In the latter the medullary plate sinks
bodily below the level of the surrounding ectoderm, which
then grows over it. Subsequently while underneath the
ectoderm the medullary plate assumes the form of a
half-canal open towards the ectoderm, and eventually its
margins come together and so form a complete tube.
In the Ascidian embryo the overgrowth of the surround-
ing ectoderm and the folding up of the margins of the
ANATOMY AND DEVELOPMENT. 199
medullary plate occur simultaneously, so that when the
latter has the form of a half-canal it is not closed over
by a layer of ectoderm, but is open to the exterior
(Fig. 98).
At a somewhat later stage the two medullary folds meet
together and fuse in the middle line (Fig. 98 4), and this,
combined with a slight forward growth of the posterior
lip of the blastopore, leads to the inclusion of the latter
in the medullary tube,
so that we arrive at the
condition already de-
scribed for Amphioxus,
in which the nerve-tube
opens in front to the
exterior by the zewropore
and behind into the ar-
nteron t -
chentero by he blasto Fig. 99. — A. Embryo of Phallusia mam-
pore, which has now miata seen in optical section from above, to
: show notochord.
become converted into B, Section through: tail of older embryo
the xeurenteric canal. of Phallusia mammillata. (After KOWALEV-
: SKY.)
Meanwhile the cells ch. Notochord. ec. Ectoderm. ez, Endo-
derm. mes. Mesoderm. z¢. Medullary tube.
forming the dorsal wall
of the archenteron in its posterior two-thirds begin to
gather themselves together to form the notochord (Figs.
98 and gg). The cells forming the notochord are at first
arranged end to end (Fig. 99), and subsequently interlace
in the manner described above for Amphioxus.
Origin of Mesoderm.
At about the same time in which the formation of the
medullary tube and notochord is going on, the mesoderm
begins to put in its appearance, and this is the first event
in the development in which there is an important dif-
200 THE ASCIDIANS.
ference between the Ascidian and Amphioxus. The
mesoderm in the Ascidian embryo does not arise as a
series of archenteric pouches, but is produced on each side
by a solid proliferation of cells from the primitive endoderm
which lines the archenteric cavity. This solid proliferation
begins in the middle region
of the embryo near the an-
terior limit of the notochord,
and extends backwards (Figs.
98 and 100). It takes place
from the dorso-lateral cells
of the endoderm, in a posi-
tion corresponding to that
at which the mesoblastic
pouches of Amphioxus grow
out from the archenteron.
The mesoderm of the As-
cidian embryo therefore
Fig. 100.— Embryo of Clavelina Ris- agrees with that of the em-
soana seen from above, to show the re- : ¥
lation of parts. (Simplified after van bryo of Amphioxus in being
Se ane EN) derived from the primitive
np. Neuropore. ez, Endoderm. ent.c.
Enteric cavity. .f. Medullary tube. endoderm, but differs in be-
mes. Mesodermic band. ch. Notochord. . :
ec. Ectoderm. ing solid and unsegmented.*
* For a recent and elaborate discussion of the origin of the mesoderm in
the Ascidians see VON DAVIDOFF’s Untersuchungen zur Entwicklungsgeschichte
der Distaplia magnilarva, etc., I. Allgemeine Entw. der Keimblitter. Mitth.
Zool. Stat. Neapel, IX. 1891. pp. 533-651.
As shown by van Beneden and Julin in Clavelina, the primary mesoderm
of the Ascidian embryo can be detected at a much earlier stage of development
than in Amphioxus.
I have studied the origin of the mesoderm in Cynthia papillosa and found
that the primary mesoderm cells are to be distinguished, by their poverty in
food-yolk, from the remaining endoderm, at the commencement of gastrula-
tion (at the so-called p/akula-stage). They occur in the form of a crescent
round the posterior margin of the blastopore, and are carried in by the invagi-
nation, and then increase in number by mitotic division. In Cynthia, these
ANATOMY AND DEVELOPMENT. 201
We thus have two solid longitudinal mesodermic bands
inserted between the ectoderm and endoderm. Anteriorly
the mesodermic bands consist of several layers of cells super-
imposed one above the other (Fig. 98), but farther back
they consist of only one layer of cells. Both portions of
the mesoderm—namely, the anterior two- or three-layered
and the posterior one-layered portions —arise in continuity
with one another, but they have different fates, the former
eventually breaking up into loose cells which float about
in the body-cavity and constitute the so-called mesenchyme,
the latter, on the other hand, becoming converted into the
musculature of the tail; whence the former is spoken of
as the gastra/ and the latter as the caudal mesoderm.
Outgrowth of Tart.
In Amphioxus, at the stage corresponding to that of
which we have been speaking — namely, when the embryo
has an oval or sub-elliptical shape—it bursts through the
vitelline membrane inside which it has already been rotat-
ing for some time by means of the cilia of the ectoderm,
and escapes into the open sea. This is not the case,
however, with the Ascidian embryo. The latter is never
ciliated externally, and it remains enclosed within the fol-
licular membrane throughout the whole of the emédryonic
period of development.
After the stage in question, the growth in the length of
the embryo is accompanied by a ventral curvature, owing
to the confined space in which it is contained. Moreover,
the increase in length is not due to a simple elongation of
the entire body of the embryo, as is the case with Amphi-
primary mesoderm cells appear to give rise almost exclusively to the caudal
mesoderm, while the gastral mesoderm appears to be added in front by prolifera-
tion from the primitive endoderm as described above.
202 THE ASCIDIANS.
oxus, but it is merely due to the outgrowth of the tail from
the body of the embryo (Fig. 101).
The structures involved in the outgrowing tail are the
dorsal nerve-tube, the notochord, the caudal mesoderm,
which lies on each side of the notochord, and will give rise
to the muscles of the tail, and finally a solid cord of endo-
derm consisting of two rows of cells placed side by side
below the notochord (Fig.
99 £). As soon as the tail
begins to grow out, the neu-
53 ‘ss Sree cos SOW ea
g SOR x a
FS Sek
@ renteric canal becomes ob-
ld ee :
oe literated, and shortly after-
wards the anterior neuropore
Fig. 101. — aes of Phallusia closes up temporarily. Ata
mammillata in side view, to show com- ] 5
mencing outgrowth of tail. (After ater period, as we shall see,
KOWALEVSKY.) S :
reo
ch. Notochord. ec. Ectoderm. ev. En- at ie Pe no NORTE to
doderm. mes. Mesoderm; the cells in- the exterior, but into the
dicated by dark outlines, beneath which 5 1
may be seen the notochord and caudal uccal tube.
endoderm. 2.9. Neuropore. 2.¢. Medul- As the tail grows in
lary tube.
length, it becomes coiled
round about the body of the embryo, attaining two or
three times the length of the latter.
The cord of endoderm cells in the tail of the Ascidian
larva has been supposed to represent a rudimentary intes-
tine homologous with the straight intestine of Amphioxus,
the larval tail being on this view equivalent to the
post-branchial portion of the trunk in Amphioxus. This
view, however, is probably not correct, although there is
something to be said in favour of it. The probability is
that the tail of the Ascidian larva or tadpole, as it is often
called, is an organ which has been specially elaborated in
the course of its evolution for the particular benefit of the
Ascidians, since (exclusive of the pelagic forms) it is their
ANATOMY AND DEVELOPMENT. 203
sole organ of locomotion, and hence of transportation from
place to place; this only being possible during the larval
period.
As arule, the larval phase of an Ascidian’s existence is
a remarkably brief one, and there is on this account all the
more need for an effective propelling organ, which will
enable the larva to arrive at a suitable resting-place.
In Amphioxus, as described above, locomotion is ef-
fected by serpentine movements of the whole trunk in
virtue of its muscle-segments, and there is therefore no
need for a tail in addition; but there is, nevertheless, a
short post-anal extension of the body, which alone can be
regarded as the homologue of the tail of the Ascidian larva.
In the latter (¢.g. Ciona, Phallusia, etc.) the muscles are
entirely confined to the tail, none being formed in the body
proper, until after the resorption of its caudal appendage.
On the view which I am endeavouring to make clear,
it follows that the tail of the Tunicate tadpole is of the
same nature as that of the Amphibian tadpole, and, in fact,
of the craniate Vertebrates generally, and, as has just been
said, is only represented by the short post-anal section of
the trunk in Amphioxus.
The solid cord of endoderm in the tail is not, therefore,
a rudiment of a primitive intestine, but it is analogous to,
even if not, as first suggested by BaLrour, homologous
with, the so-called post-anal gut which occurs in the em-
bryos of the higher Vertebrates, and bears a similar rela-
tion to the formation of the tail that the endoderm-cord in
the Ascidian embryo does.
Thus in the typical Ascidian embryo the elongation of
the trunk (body proper) does not take place to any consid-
erable extent during the embryonic or even larval period,
but only after the metamorphosis.
204. THE ASCIDIANS.
With the formation of the tail the enteric cavity be-
comes confined as a closed sac to the anterior portion of
the embryo. It is bounded dorsally by the nerve-tube,
which is somewhat dilated in this region, and in front, at
the sides and below, it is in close contiguity with the
ectoderm.
Formation of the Adhesive Papille.
At a much later stage than that represented in Fig. Ior,
the ectoderm bounding the convex anterior extremity of
the body becomes raised up into three prominences, whose
relations to one another are those of the corners of a tri-
angle. They are due to the ectodermic cells at the respec-
tive points assuming a high columnar shape. They become
eventually raised very much above the adjoining surface of
the ectoderm, and become the adhesive papille or fixing
glands of the larva. The cells composing them acquire the
power of secreting a viscid substance, by which the larva
can fix itself to any favourable surface (Fig. 102).
Cerebral Vesicle and its Sense-organs.
We have spoken above of the dilated anterior portion of
the nerve-tube. This is the part of the central nervous
system which undergoes the most striking subsequent
changes. By a gradual widening of its cavity, accom-
panied by a local thinning out of its wall, this portion
of the neural tube lying in front of the notochord becomes
transformed into a spacious sub-spherical vesicle, known
as the cerebral vesicle (Fig. 102).
While the anterior portion of the neural tube is enlarg-
ing to form the cerebral vesicle, granules of black pigment
are deposited by certain cells in the dorsal wall of the
vesicle. The granules are at first scattered about in the
ANATOMY AND DEVELOPMENT.
interior of the cells.
205
The most anterior of the cells con-
taining the pigment is at first distinguished from the
others solely on account
of the fact that the pig-
ment-granules which it
contains are somewhat
larger than those in the
succeeding cells, (Cf.
Fig. 103.)
Later on, however,
the first pigmented cell
is seen to separate itself
eret.c
Fig. 102. — Embryo of Ascidia mentula
shortly before hatching; from the right side.
(After WILLEY.)
ch. Notochord, undergoing vacuolisation.
e. Eye. ent.c. Enteric cavity. Adhesive
papilla. #7. Anterior portion of nerve-tube
(spinal cord). 0. Otocyst, lying on the floor
of the cerebral vesicle and projecting up
freely into its cavity. 7.a. Right atrial involu-
tion. s#, Stomodcoeum,
from the others, and it
becomes gradually trans-
ferred by a differential
growth of the wall of
the vesicle down the right wall to its final position in the
ventral wall of the vesicle (Figs. 102, 103). This cell is
the ofocyst, and the pigment-granules become consolidated
together to form the ofo/ith. The latter is apparently
Fig. 103.— Optical sections through cerebral vesicle of embryos of Ascidia
mentula, to show mode of origin of eye and otocyst. (After WILLEY.)
e. Eye. o. Otocyst.
extruded from the cell (otocyst) in which it was originally
formed, and the latter assumes a cup-shape, in the hollow
of which the otolith lies. The two structures together
form the so-called auditory organ, whose function may be
not so much of an auditory nature as that of an equilibrat-
ing apparatus.
206 THE ASCIDIANS.
The other pigment-cells of the dorsal wall of the cerebral
vesicle collect themselves together and form a slight pro-
tuberance in the right dorso-lateral corner of the vesicle,
while the pigment-granules, which were at first scattered
about in the interior of the cells, become concentrated at
their converging extremities towards the cavity of the
vesicle. And in this way is formed the single eye of the
Ascidian tadpole; the original pigment-producing cells
constitute the vetzza, which retains its primitive position
as part of the epithelial wall of the brain.*
Subsequently two or three cells from the adjoining wall
of the vesicle take up a position, one above the other, in
front of the mass of pigment and, having previously, by
an alteration in the character of their protoplasmic con-
tents, acquired a high refractive index, constitute the J/ens
of the eye, which projects obliquely downwards into the
cavity of the vesicles (Gh) Big, 105-45)
The cerebral vesicle of the Ascidian tadpole is the un-
doubted homologue of the corresponding, but less pro-
nounced, structure in Amphioxus. It differs from the
latter in lying wholly in front of the anterior extremity of
the notochord, in possessing a more highly organised eye,
provided with a cellular lens, and in the presence of an
otocyst, which, as we have seen, is evolved from the same
group of cells which gave rise to the eye.
The eye of the Tunicate tadpole agrees fundamentally
with the type of eye peculiar to the Vertebrates, in that
the retina is derived from the wall of the brain. On this
* The fact that the lens of the Tunicate eye as well as the retina and
the otocyst arise by differentiation of one and the same epithelial layer of
the primitive cerebral vesicle, has recently been described by SALENSKy for
the larva of Distaplia, magnilarva. (W.SALENSKY. JMorphologische Studien
an Tunicaten: TI. Ueber das Nervensystem der Larven u. Embryonen vor
Distaplia magnilarva. Morph. Jahrb. XX. 1893. pp. 48-74.)
ANATOMY AND DEVELOPMENT. 207
account it is called a myelonic eye. In the typical Inverte-
brate eye, on the contrary, the retinal cells are differen-
tiated from the external ectoderm.
Comparison of Tuntcate Eye with the Pineal Eye.
The Tunicate eye, however, differs essentially from the
paired eyes of the craniate Vertebrates in that the lens, as
well as the retina, is derived from the wall of the brain.
The lens of the lateral eye of the Vertebrates is derived
by an invagination of the external ectoderm, which meets
and fits in with the retinal cup at the end of the optic
vesicle.
It is, therefore, an extremely interesting fact which was
pointed out by BALDWIN SPENCER, that the Tunicate eye
agrees, in respect of the origin of its lens, with the parietal
or pineal eye of the Lacertilia, in which the lens is likewise
derived from cells which form part of the wall of the:
cerebral outgrowth which gives rise to the pineal body.
The pineal body is another of those remarkable rudi-
mentary structures whose constant presence in all groups
of Vertebrates forms such an eminently characteristic
feature of their organisation. It develops as a_ hollow
median outgrowth from the dorsal wall of the brain
(thalamencephalon), the distal extremity of which dilates
into a vesicle and becomes separated from the proximal
portion.*
For a long time the pineal body was a persistent enigma
* According to the most recent work on the subject the distal vesicle be-
comes entirely constricted off from the primary epiphysial (pineal) outgrowth
of the brain, and the parietal nerve does not represent the primitive connex-
ion of the pineal eye with the roof of the brain, but it arises quite inde-
pendently of the proximal portion of the epiphysis.
See A. KLINCKOwsTROM, Bettrage zur Kenntniss des Parietulauges.
Zoologische Jahrbiicher (Anat. Abth.), VII. 1893. pp. 249-280.
208 THE ASCIDIANS.
and the subject of much speculation, one of the most cele-
brated hypotheses with regard to its significance being
that of DrscarTEs, who regarded it as the seat of the
soul.
More recently it has been shown to represent a rudi-
mentary, unpaired eye. Although in most cases, curiously
enough, it exhibits in existing forms no trace of an eye-
structure, it has been shown by DE GRAAF and SPENCER
that, as a matter of fact, in many lizards the distal vesicle
does actually become converted into an eye which, though
of a rudimentary character, is possessed of a retina, pig-
ment, and lens. In these forms the pineal body pierces
the roof of the cranium, occasioning the parietal foramen,
which is so characteristic of the Lacertilian skull, and the
pineal eye lies outside the cranium immediately below the
skin, through which it can be distinguished in external
view by the presence of a modified scale placed above it.
In the animals below the lizards in the scale of organi-
sation (Amphibians and Fishes), as well as in those above
them, the distal vesicle of the pineal body apparently does
not become so far differentiated as to be recognised as
an actual eye, except in the case of the Cyclostome fishes,
where, as shown by BEarpD, it presents the three essential
elements of an eye; namely, retina, pigment, and lens,
lying, however, inside the cartilaginous cranium.
The facts in our possession would seem to indicate
that the remote ancestors of the Vertebrates possessed
a median, unpaired, myelonic eye, which was subsequently
replaced in function by the evolution of the paired eyes.
It would, however, be premature either to assert this or to
express it as a definite opinion, especially since, in refer-
ring to the evolution of the paired eyes of Vertebrates,
we are bordering on ground upon which I have no imme-
ANATOMY AND DEVELOPMENT. 209
diate intention of treading. The pineal eye may not have
been primitively so much an organ of vision as a light-
perceiving organ, as is no doubt the case with the eye of
the Tunicate tadpole.
We may at least conclude that there can be no doubt
that the Tunicate eye is the functional homologue of the
pineal eye of the higher Vertebrates, as Spencer sug-
gested.
Stomodeal and Atrial [Involutions.
By the time that the cerebral vesicle of the Ascidian
embryo with its contained sense-organs (eye and otocyst)
is approaching the completion of its full development, no
less than three ectodermic invaginations occur in the body
of the embryo. One of these is situated immediately in
front of and in contact with the anterior wall of the cere-
bral vesicle, the blind end of the involution pressing
against the subjacent endoderm. This is the stomodeum.,
and its formation is preliminary to the perforation of the
mouth which takes place later, and places the stomodceum
in open communication with the portion of the enteric
cavity which will become the branchial sac (Fig. 102). It
should be emphatically noted that the stomodceal invagi-
nation occurs in the dorsal middle line immediately adja-
cent to the anterior extremity of the central nervous
system.
The other two ectodermic invaginations occur symmetri-
cally, one to the right and the other to the left of the
dorsal middle line, behind the region of the cerebral vesicle,
and constitute the pair of atrial involutions, which, by their
subsequent growth and modification, give rise to the atrial
or peribranchial cavity. We see, therefore, that the epi-
thelium which forms the lining membrane of this cavity
is, as in Amphioxus, derived from the external ectoderm.
210 THE ASCIDIANS.
For some considerable time after the metamorphosis the
young Ascidian possesses two separate atrial cavities, right
and left, each opening to the exterior by its own atrial
aperture. Eventually the two cavities extend round the
branchial sac dorsally, so that their walls come into contact
in the dorsal middle line, and finally the dividing line
breaks down, and they become continuous one with another
dorsally, remaining separated ventrally, as described above.
At the same time that the two atrial cavities grow
towards one another, their external apertures become in-
volved in the same process of growth, and, moving together,
finally fuse in the dorsal middle line, and so form the single
atrial or cloacal aperture of the adult.*
Beyond agreeing in its ectodermal origin, there might
appear to be not much in common between the mode of
development of the atrial cavity in the Ascidians and in
Amphioxus.
No morphologist would recognise a fundamental differ-
ence in the fact that the right and left halves of the atrial
cavity in Amphioxus arise by a single median involution of
the ectoderm, instead of from a pair of involutions, and that
they are from the first continuous with one another instead
of becoming so secondarily (Fig. 104).
In like manner, the fact that the two halves of the atrial
cavity are continuous with one another ventrally in Amphi-
oxus and dorsally in the Ascidians, is easily brought into
correlation with the other differences in the organisation
of the two types, which have been described above, and is
no bar to our regarding the atrial cavity of the one as being
homologous with that of the other.
* The time at which the atrial cavities fuse together varies very much in
different genera. In Molgula manhattensis, for instance, whose stigmata
develop on a similar plan to those of Ciona (see below), there is a single
atrial aperture at the moment of the metamorphosis.
ANATOMY AND DEVELOPMENT. 201
One feature in connexion with the formation of the
atrial cavity, in which the Ascidians stand in marked
contrast to Amphioxus, does, however, require a special
explanation.
Whereas in Amphioxus the atrial involution has the form
of a longitudinal groove, in the Ascidians it occurs on each
side, as a local inpushing of the ectoderm with a minute
circular orifice of invagination.”
The fact has already been stated above that the elonga-
tion of the body proper of an Ascidian embryo or larva does
not, in the main, take place until after the metamorphosis.
Fig. 104. — Diagrammatic transverse sections, to illustrate the mode of forma-
tion of the atrium in (A) an Ascidian and (2) Amphioxus. (After WILLEY.)
The atrial involutions occur at a time when the tail is
rapidly increasing its length; the body proper, on the con-
trary, remaining stationary so far as increase in size is
concerned, and retaining at this stage approximately the
dimensions which it possessed when the tail first began to
grow out. Moreover, they occur defore the appearance of
any gill-clefts in the wall of the branchial sac, so that in the
Ascidians the gill-slits never open directly to the exterior.
In Amphioxus, on the other hand, there is no such delay
in the elongation of the body of the embryo, but it goes on
continuously till the full complement of myotomes has been
212 THE ASCIDIANS.
formed. The post-anal portion of the body, which we sup-
pose to be the homologue of the tail of the Ascidian tad-
pole, does not appear until a somewhat late period in the
development. There is very little of it present in the larva
with three gill-slits (Fig. 73).
The reason of this, as explained above, is that the post-
anal section of the trunk is of only minor functional sig-
nificance in Amphioxus, but is all-important to the
Ascidian larva, and consequently, as is the case with
many other structures of great functional importance in
the various groups of the animal kingdom, it exhibits a
precocious development.
Not only, therefore, has the elongation of the body of
Amphioxus already taken place before the occurrence of
the atrial involution, but the primary gill-slits have also
broken through the wall of the pharynx, and open freely to
the exterior before the atrium begins to be closed in.
In Amphioxus, then, the atrial involution has been drawn
out into the form of a longitudinal groove because it
occurs subsequently to the elongation of the body and
the perforation of the gill-slits.
In the Ascidian embryo the (paired) atrial involution
has the form of a simple pit with a circular margin, be-
cause it arises before the elongation of the body proper
of the embryo and before the perforation of the gill-clefts,
so that no influence has been at work to draw it out into
the form of a groove.
We see, therefore, that a great many of the differences
between the Ascidian tadpole and the larva of Amphi-
oxus can be explained sufficiently to allow of their being
brought into genetic relation with one another, by consid-
ering the relative time at which corresponding develop-
mental processes take place in the two cases.
ANATOMY AND DEVELOPMENT. 213
The following table will help to make this matter
clearer.
ORDER
OF ASCIDIAN. AMPHIOXUS.
OccuURRENCE.
It Gastrulation. Gastrulation.
2s Oval embryo with medullary | Oval embryo with medullary
tube, neurenteric canal, tube, neurenteric canal,
notochord, and mesoblast. | notochord, and mesoblast.
(Last two commencing. ) (Last two commencing.)
Be Outgrowth of tail. Commencing elongation of
body of embryo, and escape
from vitelline membrane.
4. Continued growth of tail. Continued elongation of em-
bryo.
ie Formation of stomodceum and | Formation of mouth, and com-
atrial involutions. mencing perforation of gill-
clefts.
6. Escape from vitelline mem- | Continued formation of gill-
brane. clefts and outgrowth of tail
(z.e. post-anal section of
trunk).
le Commencing perforation of | Formation of longitudinal atrial
gill-clefts. involution.
8. Metamorphosis and commenc- | Metamorphosis.
ing elongation of body
proper.
Of course the above table has no concern with the
actual time (hours and days) from the commencement
of the development at which such and such an event
occurs.
The type of Ascidian referred to in the above
description is a simple Ascidian like Czova or Phallusia.
The above table also shows how the development of
the Ascidian and of Amphioxus moves along parallel
lines up to a certain point, and then at the time of the
outgrowth of the tail in the embryo of the former and the
hatching of the embryo of the latter, divergences set in.
214 THE ASCIDIANS.
It has long been recognised that the development of an
Ascidian is much abbreviated in comparison with that of
Amphioxus, since in the former it neither comes to the
formation of a ciliated embryo nor to the production of
archenteric pouches for the mesoderm. One of the chief
evidences, however, of abbreviation in the Ascidian devel-
opment is the precocious formation of the larval tail.
Formation of Alimentary Canal and Hatching of Larva.
When the enteric cavity of the Ascidian embryo begins
to grow in length so as to give rise to the stomach and
intestine, which it does shortly after the appearance of
the atrial involutions, there is only one resource open to
it on account of the limited space in which it lies, and that
is to double round upon itself. This it accordingly does.
As the growth progresses, the posterior dorsal angle of
the enteric cavity bends sharply downwards on the right
side, and then upwards and slightly forwards on the left
side, ending at first blindly in the vicinity of the left atrial
sac. In this way the four divisions of the alimentary
canal become established ; namely, pharynx or branchial
sac, cesophagus, stomach, and intestine. (Cf. Fig. 105.)
By the time these changes have taken place, the embry-
onic development is at an end, and the larva is ready to
hatch. By spasmodic jerkings of its tail, the larva finally
succeeds in bursting the egg-follicle or vitelline membrane
in which it has been hitherto enclosed, and so escapes
into the open sea.
Clavelina and Ciona.
While the development of most forms of Tunicata is re-
ducible to a common type, yet the details vary within very
wide limits in different genera. The tendency here, as
ANATOMY AND DEVELOPMENT. 215
elsewhere, is to abbreviate the development by omitting
certain ontogenetic processes, and so arriving at the de-
sired end, as it were, by a short cut.
One of the most impressive instances of such an abbre-
viated development, and one which can be demonstrated
with the utmost certainty, is afforded by the genus Clave-
fina, in contrasting it with the closely allied genus Czona.
Clavelina (see Fig. 96) is an Ascidian, provided at its
base with creeping processes or stolons containing a lumen
continuous with the body-cavity, by which it adheres to
rocks and weeds. Buds are formed from the stolon, which
grow up into new individuals precisely like the parent form
which developed from the egg, and soa colony is produced.
Ciona also has similar basal processes of the test, con-
taining prolongations of the original body-cavity, but no
buds are produced.
In Clavelina, the embryonic development, up to the time
of the hatching of the larva, takes place inside the peri-
branchial chamber of the parent, which becomes converted
into a kind of brood-pouch.
In Ciona, the eggs are extruded into the water, where
they are fertilised by the simultaneous extrusion of sper-
matozoa from the same individual. Finally, in Clavelina
the egg is much larger and contains more food-yolk than
that of Ciona.
We see, therefore, that in these two genera the egg is at
the outset subjected to different sets of conditions, both
internally and externally.
METAMORPHOSIS OF CIONA INTESTINALIS.
Three stages in the metamorphosis of the larva of Czona
entestinalis are shown in Fig. 105. First, there is the free-
swimming larva, which, after a pelagic existence of one or
216 THE ASCIDIANS.
perhaps two days’ duration, is on the point of fixing itself
to a foreign object by means of the sticky secretion of its
three adhering papille.
This larva possesses features which we have not yet
considered. Let us give our attention in the first place
to the tail.
Vacuoltsation of the Notochord.
The vacuolisation of the notochordal tissue, which was
described above for Amphioxus, has already proceeded to
such an extent that there is no longer any trace of cellu-
lar structure in the centre of the notochord. It is entirely
filled with a perfectly colourless substance, probably of
gelatinous consistency, while the nuclei have been dis-
placed entirely from the centre and can be seen to lie
closely pressed against the dorsal and ventral sides of the
sheathing membrane of the notochord (Fig. 105 A).
There is one respect in which the above vacuolisation
of the cells of the notochord differs considerably from
the corresponding process in Amphioxus and the higher
Vertebrates.
Whereas in the latter forms the vacuoles appear inside
the individual cells, —in other words, are zztrace//ular, — in
the Ascidian tadpole they occur between the cells, and are
therefore zztercellular. This was first made out by
Kowalevsky, and can readily be observed. (Cf. Fig. 102.)
The intercellular spaces separate the cells which were
previously fitted accurately together, end to end, and,
gradually increasing in size, they eventually flow together
and so constitute a continuous space, while the cells with
their nuclei become thrust aside.
Assuming that the vacuoles contain a more or less fluid
substance secreted by the protoplasm of the cells, the
ANATOMY AND DEVELOPMENT. 217
above difference in the vacuolisation of the notochordal
tissue in Amphioxus and the Ascidian larva would resolve
itself into saying that the secretion was retained inside
the cells in the one case, and deposited outside them in
the other.
Mesenchyme and Body-cavity.
The endoderm cells of the tail, which formed at first a
solid cord below the notochord, have now become con-
verted into loose corpuscles, which have mostly floated
out of the tail into the hinder portion of the body-cavity,
and have become indistinguishable from the mesoderm-
cells. The latter are beginning to lose their compact dis-
position in the form of the two mesodermic bands, espe-
cially in the hinder region, and to be scattered about in the
body-cavity.
The body-cavity of the young Ascidian is not unre-
servedly homologous with that of Amphioxus, on account
of this remarkable behaviour of the mesoderm. The
cavity does not arise in the midst of the mesoderm by a
splitting apart of its component cells, but it is simply
produced by a separation of the endoderm from the ecto-
derm, the two layers being at first in contact at the sides
and below; in fact, everywhere, except where the dorsal
nerve-tube intervenes.
In the cavity thus produced between ectoderm and
endoderm the mesodermic bands at first lie freely, and
then their component cells break away from their compact
association and float about the cavity in the form of
scattered corpuscles, known collectively as mesenchyme.
This mesenchyme later gives origin to the muscula-
ture of the body proper of the Ascidian, and also to
the definitive blood-corpuscles, genital organs, and renal
218 THE ASC/DIANS.
vesicles.* All these structures are differentiated from the
loose mesenchyme cells, all of which at first course round
about the body of the young Ascidian like blood, being
kept in motion by the beating of the heart.
In the stage shown in Fig. 105 A the mesodermic bands
are still fairly compact in front, having extended them-
selves anteriorly at the sides of the enteron by interstitial
growth.
Preoral Body-cavity and Preoral Lobe.
When the larva first hatches, the endoderm and ecto-
derm are in contact with one another at the anterior
extremity of the body, just as they are in the earlier
stages. (Cf. Fig. 102.) Soon, however, the ectoderm,
with the adhering papille, springs away from the endo-
derm at this point, leaving a space into which the two
lateral mesodermic bands force their way.
In this way a special anterior portion of the body-cavity,
preoral and preenteric, is produced, and is at first com-
pletely filled by a compact mass of rounded cells derived
from the mesodermic bands. —
The end of the body of the larva at which the adhering
papilla are placed of course corresponds to the tip of the
snout in Amphioxus.
Just as Amphioxus burrows into the sand with its snout,
so the Ascidian larva fixes itself to the surface of a rock
or weed by its snout. The anterior or przoral portion of
the body-cavity, of which we have just traced the origin,
is, and subsequently becomes in a still more pronounced
way, the cavity of the snout, or preoral lobe.
* The pericardium arises ventrally from the endodermic wall of the bran-
chial sac, and the heart is formed by an infolding of the dorsal wall of the
pericardium.
ANATOMY AND DEVELOPMENT. 219
50 99° 0
7 > 10% % 32%
' - ———
ot. : ‘a She EN
% 1
}
ay
ed
Fig. 105.— Metamorphosis of Czona intestinalis; above is represented the
anterior portion of the free-swimming larva from the left side; on the left, the
larva, shortly after fixation, from the right side; and on the right, the stage at
which the change of axis commences, from the left side. (After WILLEY.)
a. Atrial aperture. 4. Branchial sac. ch. Notochord. e. Endostyle. # Organ
of fixation. g. Ganglion. %. Neuropore (having reopened into branchial sac).
z, Intestine. 72 Pyloric gland. mm. Mouth. 2. Nerve-tube. oe, (Esophagus.
ob. Eye. of. Otocyst. g. Pericardium. s.Stomach, s¢. Stigmata. 4 Tail.
220 LHE ASCIDIANS.
Body-cavity of an Ascidian and Celom of Amphioxus.
We must now endeavour to show how the body-cavity
of the Ascidian can be brought into genetic relationship
with the cclom of Amphioxus. The question of the
absence of metamerism in connexion with the origin of
mesoblast in the Ascidians need not detain us, since it is
so obviously correlated with their mode of life. It may
safely be asserted that the Ascidian mesoderm, as a whole,
is homologous with that of Amphioxus as a whole, but in
the details of its origin and fate it is widely different.
If we figure to ourselves the coelomic epithelium of
Amphioxus losing its character as a membrane and break-
ing up into its constituent cells, which would then lie loosely
in the body-cavity, we should have essentially the same
condition of things as in the Ascidians. There are numer-
ous precedents in the animal kingdom for such a disinte-
gration of an epithelial membrane.
A most perfect instance of it has been described by Dr.
R. von ERLANGER* in connexion with the origin of the
mesoderm in the fresh-water snail, Paludina vivipara. Here
the mesoderm appears at first in the form of a median
bilobed archenteric pouch of relatively large dimensions.
Soon, however, the cells forming the wall of the pouch begin
to assume irregular shapes, and so disturb the contour of
the epithelium, and eventually they break apart entirely
and fill every nook and corner of the available space with
a loose mesenchyme. Similar out-wanderings of cells from
an epithelial wall, though not often of such a complete
character as the instance above cited, are by no means
infrequent.
* Zur Entwicklung der Paludina vivipara, Parts I. and II. Morpholo-
gisches Jahrbuch, XVII. 1891.
ANATOMY AND DEVELOPMENT. Zo
A striking example is afforded by the body-cavity
of the worm-like Balanoglossus, of which we shall speak
later.
Here, according to Bateson, the cells lining the cavity
are continually budding off daughter-cells, which fall into
the cavity, and eventually almost entirely fill it up with
mesenchymatous tissue. In this case, therefore, mesen-
chyme and an epithelial wall coexist.
Similarly, the epzthelial sclerotome of Amphioxus is rep-
resented by a mesenchymatous sclerotome in the higher
Vertebrates. It is not necessary to multiply instances,
but many others could be adduced.
If, now, this disintegration of partetal and visceral layers
of the mesoderm, which we have imagined above to take
place in the ontogeny of an animal like Amphioxus, be
supposed to be thrown back in the development, or, in
other words, abbreviated to such an extent that the pre-
liminary formation of a continuous ccelomic epithelium no
longer takes place, we should have precisely those condi-
tions which we actually find in existing Ascidians.
As in the cases above quoted for purposes of illustra-
tion, so in the Ascidians the mesenchymatous condition
undoubtedly originated ancestrally from what we may call
an epithelial condition.
In the Ascidians we may conclude, therefore, that while
ontogenetically the mesenchymatous condition is to all
intents and purposes primary, from a phylogenetic point
of view it is pre-eminently secondary or cenogenetic.
Having made the reservations implied in the above
statements, we may confidently assert that as a whole
the body-cavity of the Ascidians is homologous with the
coelom of Amphioxus, and we may define the former as
a ccelom in which the cells, instead of associating together
222 THE ASCIDIANS.
to form a lining membrane round the cavity, remain
independent of one another and scattered about inside the
cavity.
Fixation of the Ascidian Larva.
When the larva first fixes itself to some available surface,
the tail remains for a time stretched straight out and
almost motionless, giving perhaps an occasional twitch.
Soon the tail is observed to become shorter and to finally
disappear, having been drawn within the body proper of
the young Ascidian. The entire tail, with the whole of
the notochord, musculature, and caudal portion of nerve-
tube, becomes thus retracted and invaginated into the
posterior region of the body-cavity, wnere it forms a coiled
amorphous mass, which goes through a gradual series of
histolytic changes, and is finally absorbed by being dissolved
in the fluid of the body-cavity (Fig. 105 2).
By the time the tail has been completely drawn up into
the body, the organ of fixation or snout, as we have called
it above, becomes drawn out into a long probosciform
structure in a line with the long axis of the body. Its
cavity is no longer completely filled with mesoderm-cells
as it was at first (Fig. 105 A), but it has become so volu-
minous that its contained cells are loosely scattered about
(Fig. 105 B). In the concluding chapter we shall endeav-
our to show, what has been already implied, namely,
that the organ of fixation is seen to the best possible
advantage from a morphological point of view in the
species now under consideration, viz. Czona intestinalis,
and that it is homologous with the przoral lobe (snout) of
Amphioxus, including under that term both the przoral
body-cavity and the preoral pit, and further that it is
homologous with the proboscis of Balanoglossus.
ANATOMY AND DEVELOPMENT. 223
At the stage shown in Fig. 105 A, the lumen of the
alimentary canal is extremely reduced, and in many places,
as in the region of the endostyle, ¢, its opposite walls are
in actual apposition, so that the lumen at these points is
almost obliterated.
This temporary reduction of the lumen of the alimentary
canal is due to the narrow space into which it has to be
compressed, combined above all with the relatively enor-
mous size of the cerebral vesicle, which exercises a great
pressure on the subjacent dorsal wall of the branchial sac.
It may be added that the larva of Ciona does not take in
food independently until after fixation.
Reopening of Neuropore; Degeneration of Cerebral Vesicle ;
Formation of Definitive Ganglion.
One of the most obvious features of the metamorphosis
is the rapid expansion undergone by the enteric and body
cavities and the no less rapid degeneration of the cerebral
vesicle. This expansion, by relieving the crowded char-
acter of the various parts, facilitates greatly the study of
the changes which take place in the internal organisation.
The neuropore, which we have described above as having
closed up at an early period, now reopens again and places
the neural tube —that is to say, as much of it as remains
after the atrophy of the tail—in open communication
with the base of the buccal tube (Fig. 105 4, 7).
The spacious cavity of the cerebral vesicle has vanished,
and its walls have undergone disintegration, and, except
for a portion of the dorsal wall which becomes converted
into another channel, are now represented by a mass of
histolytic residua filling the original cavity of the vesicle
and lying below the anterior portion of the nerve-tube.
pogpHyal THE ASCIDIANS.
This remnant of the cerebral vesicle of the larva with its
sense-organs becomes eventually absorbed, and the eye and
otolith may often be found floating about the body-cavity
with the ordinary mesenchyme-cells, and occasionally they
can be seen actually passing through the heart.
The anterior portion of the nerve-tube itself, which now
opens into the base of the buccal tube or stomodceum,* is
derived from a portion of the dorsal wall of the original
cerebral vesicle which was constricted off from the latter in
the form of a narrow tube slightly to the left of the mid-
dorsal line (Fig. 105 B, 7).
Subsequently the cells forming the dorsal wall of this
portion of the nerve-tube proliferate and form a solid
thickening which becomes the definitive ganglion of the
adult (Figs. 105 C, 106, and 107, g).
The lumen of the nerve-tube behind the region of
the definitive ganglion finally becomes obliterated by the
mutual approximation of its constituent cells, and that
portion of the primitive nerve-tube which in the larva lay
between the cerebral vesicle and the root of the tail is thus
represented in the adult by a solid “cordon ganglionnatre
viscéral”’ (van Beneden and Julin) which starts from the
posterior end of the adult cerebral ganglion, and, proceed-
ing along the dorsal side of the pharynx above the dorsal
lamina, becomes lost among the viscera. (Cf. Figs. 96,
105, and 107.)
Below and in front of the definitive ganglion, which
finally becomes quite separate from the dorsal wall of the
neural tube, the lumen of the latter persists and becomes
* According to renewed observations on Ciona, I find that the neuropore
reopens into the buccal tube precisely in the line of junction of the stomo-
dceum with the wall of the branchial sac, so that its upper margin is continu-
ous with the (ectodermic) stomodceal epithelium, and its lower margin with
the (endodermic) branchial epithelium. (See below, V.)
ANATOMY AND DEVELOPMENT. 225
by subsequent extension the lumen of the subneural gland
and its duct.
Thus the anterior portion of the primitive neural tube,
having become constricted off from the cerebral vesicle
of the larva, and having given rise by proliferation from
its dorsal wall to the definitive ganglion, becomes bodily
converted into that structure which we shall call, in agree-
ment with JuLin, the “ypophysts.
The opening of the latter into the base of the buccal
tube becomes the dorsal tubercle of the adult. Finally, at
a much later stage, the glandular portion of the hypophy-
sis arises by proliferation of
spongy tissue from the ven-
tral wall of that portion of
the xeuro-hypophysial tube
which lies immediately be-
low the ganglion.
A section through the
cerebral vesicle of a larva
of Distaplia, a colony-build-
ing Ascidian, showing the
hypophysis in process of
being constricted off from
the vesicle, is given in Fig.
100.
dition of things generally is
In this genus the con-
very different from what
obtains in Ciona, but it is
introduced to show the
Fig. 106. — Frontal section through
cerebral vesicle of a larva of Distaplia
magnilarva, to show the origin of the
ganglion and hypophysis. (After HJORT;
combination of two figures.)
In the larva of Distaplia, the hypophy-
sis opens into the branchial sac _ be-
hind the stomodoeum.
c.v. Cerebral vesicle. ec. Ectoderm.
en. Endoderm. gg. Ganglion. Ay. Hy-
pophysis (neuro-hypophysial tube).
essential similarity in the mode of origin of the hypophy-
sis in this form, as observed by Dr. JoHAN Hyjorv.
In Distaplia, as is also the case to a less extent in
Clavelina, the ganglion begins to develop from the wall
226 THE ASCIDIANS.
of the neuro-hypophysial tube while the latter is still in
connexion with, and therefore before the atrophy of, the
cerebral vesicle, thus indicating a hastening in the devel-
opment as compared with Czona.
The convexity caused in the dorsal wall of the branchial
sac by the pressure of the cerebral vesicle persists as the
anterior portion of the dorsal lamina, and in many or most
simple Ascidians becomes grooved, forming the efzbran-
chial groove of JULIN (Fig. 97). At present it is merely a
ridge, the epzbranchial ridge.
In Fig. 105 C the proximal (oral) end of the endostyle,
eé, is seen to be connected with the epibranchial ridge by
the peripharyngeal band, which we have already described
in the adult. It apparently arises 27 sztw by simple spe-
cialisation of the cells forming the epithelial wall of the
pharynx at this point.
Primary Topographical Relations and Change of Axis.
It must be especially noted that the long axis of the
young Ciona for some time after fixation is identical with
that of the tailed larva, and therefore the primary topo-
graphical relations of the various parts are maintained at
the stage shown in Fig. 105 4, and we can accordingly make
use of this stage in which different structures are much
clearer than in the free-swimming larva for the purpose of
describing the primary topography, which is of the utmost
importance when it is desired to institute a comparison
with Amphioxus.
Since, as we have seen, the details of the embryogenetic
processes differ in many respects widely from what occurs
in Amphioxus, we are inevitably compelled to rely to a
very large extent on topographical relations in order to
estimate the homology of this or that structure in the
ANATOMY AND DEVELOPMENT. 227
Ascidians and in Amphioxus. Fortunately there is one
structure as to whose complete homology, in the Urochorda
(Tunicata), on the one hand, and the Cephalochorda, on the
other, no one entertains a doubt, and that is the exdostyle.
We thus have in the endostyle a firm basis upon which to
ground our deductions.
In the larva and in the young Ascidian before the
primary long axis has been disturbed in the way which we
shall shortly describe, the endostyle is the most anterior
endodermic structure in the body, and lies dorso-ventrally
at right angles to the long axis of the body (Fig. 105 A
and B, e).
As described above in the larvz of Amphioxus, particu-
larly in the younger larvae (see Figs. 64 and 73), the endo-
style, though lying asymmetrically on the right side, being
involved in the general asymmetry of the larva, is quite
anterior in position, in front of all the gill-slits and partly
in front of, though also partly opposite, the mouth (on
account of its asymmetry), and almost at right angles (see
especially Fig. 64) to the long axis of the body. As there
is only a short stretch of simple endoderm in front of the
endostyle in the larva of Amphioxus, we may describe it
as the most anterior differentiated endodermic structure
in the larva, thus corresponding with remarkable precision
to the condition described above in the larval and newly
fixed Ascidian.
In the middle of the wall of the branchial sac in Fig.
105 4 are seen, somewhat in front of and below the atrial
aperture, a, of this side, two lens-shaped structures whose
slightly concave sides face each other. These are the
borders of the two first-formed primary branchial stigmata
or gill-clefts. Their actual openings into the atrial chamber
are at present so small that they can hardly be seen in
228
THE ASCIDIANS.
surface-view, but they are situated at the inner or con-
cave sides of the two thickenings.
Fig. 107. — Young Ciona intestinalis after
the completion of the change of axis; from the
left side. (After WILLEY.)
7, 7V. Primary stigmata. a. Anus, situated
immediately below the left atrial aperture. end.
Endostyle. ££ Organ of fixation. .. Ganglion.
hy. Hypophysis. 7zw¢. Intestine. Zaz, Left atrial
aperture. /.. Longitudinal muscle. 2. Mouth.
oes. CXsophagus. 7.6. Peripharyngeal band.
py. Pyloric gland. st. Stomach. ¢ Coronary
tentacles. v.7. Visceral nerve (cordon ganglion-
naire viscéral).
On either side of the
latter can be seen the
ordinary cavity of the
pharynx proceeding to-
wards the cesophagus.
At a later stage the
openings of the two
first-formed stigmata
become distinctly visi-
ble(Fig. 105 C). Mean-
while a change of axis
is taking place in the
body of the
Ascidian.
During the extraor-
young
dinary change of axis
which we are about
to describe the probos-
lobe
(snout, organ of fixa-
ciform przoral
tion) remains station-
ary, and the rest of the
body actually rotates
through an angle of 90
degrees, using the or-
gan of fixation as a
pivot about which it
turns. Invbigs Tos G
the which
takes place very gradu-
rotation
ally is only half performed; while in Fig. 107 it is complete.
The method of growth by which this rotation takes place
ANATOMY AND DEVELOPMENT. 229
is of a very singular character, and it is difficult to define
it in precise terms.
In this way then the endostyle (and branchial sac
generally) comes to be placed at right angles to its primary
position.
Since in Amphioxus the endostyle altered its primary
axis by a process of independent growth while the long
axis of the pharynx was constant throughout the develop-
ment, we find that here again, as in so many previous
instances, the details by which similar end-results are
arrived at are widely dissimilar.
This complete change of axis by which the przoral lobe
(organ of fixation) becomes placed at the posterior extrem-
ity of the body can only be regarded as a cenogenetic
feature.*
It is therefore chiefly to the primary relations which the
various structures bear to one another, before the change
of axis, that we must turn for purposes of comparison. If
we do this, we find that the following sequence of organs
obtains as well in the larva of Amphioxus as in the newly
fixed larva of Ciona; namely: 1, praeoral lobe; 2, endo-
style ; 3, mouth; 4, gill-clefts.
Formation of Additional Branchial Stigmata.
After the change of axis of the body, the long axes of
the stigmata lie transversely. In their further growth
they go on elongating in the same (transverse) direction,
and after they have attained a certain size their ventral
ends — that is to say, the ends nearest the endostyle— bend
round towards each other, and from each of the two first-
* Tt goes without saying that the primary long axis of the Ascidian larva is
homologous with the long axis of Amphioxus.
230 THE ASCIDIANS.
formed stigmata a minute portion becomes gradually con-
stricted or nipped off. Thus between and cut off from the
two original stigmata, there come to lie two intermediate
stigmata of much smaller size. (Cf. Fig. 107.)
In this way, then, in Ciona, we arrive at the stage with
four branchial stigmata on each side of the pharynx. For
convenience we shall refer to these by the Roman nu-
merals, I., 11, Til“andihV. Wts a remarkable fact that
II. and III. do not arise by new perforations, but are cut
off from I. and IV. respectively.
On account of the close relations which the two first-
formed stigmata, I. and IV., bear to one another during
the production of the intermediate stigmata, their ventral
extremities coming into contact and apparently some-
times fusing together so that II. and III. might almost
be described as a joint production of I. and IV. rather than
as entirely independent offshoots, one is forced to the
conclusion that the two first-formed stigmata themselves,
though they actually appear simultaneously as separate
perforations, in reality represent the two halves of a
single primitive gill-slit divided into two by a tongue-
bar. If, moreover, we examine the exact origin of these
two stigmata (I. and IV.) by means of transverse and
horizontal sections, we may become convinced that such
is indeed the case; namely, that they represent the two
halves of a primitive gill-slit which, on account of the
precocious formation of the tongue-bar between them,
become perforated separately.
For the formation of any two or more consecutive gill-
slits, we usually expect to find separate endodermic pockets
or pouches of greater or less depth growing out towards
the ectoderm. (Cf. Figs. 72 and 92.)
We ought to find something analogous to this in Ciona
ANATOMY AND DEVELOPMENT. 231
if the two first-formed stigmata had the value of indepen-
dent gill-slits.
Instead, however, of anything approaching to two endo-
dermic outgrowths, we find at the base of the atrial invo-
lution a single endodermic ingrowth making its appearance
(Fig. 108).
The angles made by this ingrowth with the neighbour-
ing wall of the branchial sac remain in contact with the
floor of the atrium, then fuse with it, and finally become
a A os at
MALLILILSELLIELULLIMLILIUIEUA Ey | pp
t
Uy
19)
UN LLL LL
YW
WLLL
2b
at
Sa C D
i, LLL LLL ILL. PE
TILL ped STE
Ys
75
Fig. 108. — Diagrams illustrating the mode of origin of the two first-formed
branchial stigmata in Ciona. (After WILLEY.)
at, Atrial involution. ec. Ectoderm. em. Endoderm. g.s. Stigmata. 726.
‘Tongue-bar.
perforated (Fig. 108). This is the way in which the stig-
mata, I. and IV., arise, and it is difficult, if not impossible,
to interpret the above-mentioned endodermic ingrowth
otherwise than as a precocious tongue-bar.
Even in Amphioxus it was seen how the tongue-bars
of the secondary slits arose relatively much earlier than
those of the primary slits. If they arose still a trifle
earlier, we should have the two halves of each slit becom-
ing separately perforated, just as it happens in Ciona.
In a species of Balanoglossus an analogous precocious
232 THE ASCIDIANS.
formation of tongue-bars, before the perforation of the
slits, has been described by Professor T. H. Morean.
From what has been said above, we conclude that the
first four pairs of primary branchial stigmata of Ciona
(and this probably applies equally to many species of
Phallusia) represent and are derivatives of one pair of
primitive, ancestral gill-slits.
After a comparatively long interval, during which the
intermediate stigmata, II. and III., increase in length
transversely, two more stigmata, V. and VL., arise at inter-
vals, one after the other, by sepa-
rate perforations behind those
already formed (Fig. 109).
On account of the independent
origin of V. and VI., it might be
supposed that they would have
the morphological value of dis-
tinct gill-slits, and that we had
before us three pairs of ancestral
Fig. 109.— Primary branchial gill-slits represented by six pairs
sigmata sof the might isidevet a) of: | primany, joranchialstiematas
young Ciona. (After WILLEY.)
For this interpretation to hold
good, we should expect to find that in other forms in which
six primary branchial stigmata were produced, their origin
was either the same or reducible to the same type as that
of the branchial stigmata of Ciona.
This, however, is not the case, since I have found
that in Molgula manhattensis,* a simple Ascidian which
occurs in great numbers at New Bedford, Mass., the six
primary stigmata, corresponding precisely to those in
* My observations on the development of Molgula manhattensis were
made at the Marine Biological Laboratory, at Woods Holl, Mass., in the
summer of 1893.
ANATOMY AND DEVELOPMENT. 233
Ciona, have a somewhat different mode of origin. The
two first-formed stigmata (=I. and IV. in Ciona) appear
simultaneously as in Ciona. Then after growing to a cer-
tain size, they curve round at their ventral ends, not in
opposite directions so as to meet each other as they do in
Ciona, but in the same direction (Fig. 110). The recurved
ends then become constricted off from the parent stig-
mata. Later on, a fifth gill-opening arises behind the
first four stigmata by independent perforation, and after
Fig. 110. — Diagram illustrating the mode of origin of the six primary bran-
chial stigmata of Molgula manhattensis. The numbers are placed at the ventral
ends of the slits. The figure is a combination of several hitherto unpublished
drawings of different stages in the development. /, ///, and V arose by separate
perforation.
attaining a certain size, it, in its turn, curves round at its
ventral end, and eventually the sixth stigmatic opening is
constricted off from the fifth.
Since the first six primary stigmata have such different
origins in two different species, it is obvious that in
attempting to make a comparison with Amphioxus we can
only use the two first-formed stigmata, because they agree
in the above-mentioned species, and in many others in
234 THE ASCIDIANS.
arising simultaneously, and in representing, in all proba-
bility, the two halves of a primitive gill-slit, cut in two by
a tongue-bar.
The stigmata which are added to these must, therefore,
be regarded as secondary modifications, hardly comparable
to the successive formation of new gill-slits in Amphioxus.
In the Ascidians, therefore, we can only detect the
representatives of one pair of primitive gill-slits, and there
is every reason for supposing them to be homologous with
the first pair of gill-slits in Amphioxus as defined above.
The six primary stigmata of each side give rise, by re-
peated subdivision, to the innumerable stigmata of the
adult, both in Ciona and Molgula. The following de-
scription, however, applies more particularly to Ciona.
In the first place, the primary stigmata grow to a sur-
prising transverse length, and then commence to divide
into two equal portions by small tongue-like projections,
which grow across the aperture indifferently from the
anterior or posterior walls of the respective stigmata, and,
fusing with the opposite wall, divide the transversely
elongated slit into two completely separated halves. Then
each of the latter divides again in the same manner, and
so the process of subdivision of existing stigmata goes on.
In this way six transverse rows of stigmata arise. These
may be distinguished as secondary stigmata, since they
arise by division from the primary.
Gradually, by a peculiar process of growth, the long
axes of the secondary stigmata change their direction, and
instead of lying transversely they become directed antero-
posteriorly. This is their definitive position, and the
stigmata now go on rapidly dividing again, and the num-
ber of transverse rows of stigmata is in this way doubled,
trebled, quadrupled, etc., and we thus arrive at the adult
ANATOMY AND DEVELOPMENT. 235
condition. Out of the multitude of stigmata which are
present in the adult Ciona only four arise by independent
perforation; namely, the primary stigmata I. and IV.
(which we regard as the two halves of a primitively single
slit) and V. and VI.
First Appearance of Musculature.
By the time the change of axis of the entire body of
the young Ciona has been effected the musculature
characteristic of the adult begins to put in an appear-
ance. In Fig. 107 circular sphincter muscles are present
round the buccal and atrial apertures. The latter are still
paired, but are carried by differential growth dorsalwards
at a later stage, and finally coalesce together in the dorsal
middle line to produce the single atrial aperture of the
adult.
One strand of the longitudinal muscles of the later
muscular mantle is likewise to be seen in Fig. 107. It
tends to branch dichotomously. Posteriorly it is inserted
on the inner surface of the organ of fixation near the point
where it joins on to the body. Later new muscle-bands
arise similar to the first, and become distributed over the
body-wall in a spreading fan-like fashion, but posteriorly
they are all inserted in the same region of the organ of
fixation.
Alimentary Canal and Pyloric Gland.
The course of the alimentary canal can be gathered so
plainly from the accompanying figures (Figs. 105 and 107)
that it hardly needs a verbal description. From the
posterior dorsal corner of the branchial sac the cesophagus
leads into the wide stomach, and from the latter, again,
the intestine, which often possesses a strangulated appear-
236 THE ASCIDIANS.
ance, doubles up obliquely forwards to the left atrial
chamber, into which it opens by the anus (Fig. 107).
In the angle made by the outgoing intestine with the
stomach, a blind diverticulum arises. It is at first a sim-
ple coecum, but soon begins to branch (Fig. 105 C), and
finally forms an arborescent growth embracing the in-
testine (Fig. 107). This is the so-called pyloric gland,
and it is probably homologous with the hepatic caecum of
Amphioxus.
Appendicularia.
It is generally agreed among those who have a voice in
the matter, that most of the pelagic Ascidians (Salpa,
Doliolum, Pyrosoma) are
highly modified forms, spe-
cially adapted to a pelagic
life, one of the results of
which is that their repro-
duction is marked by a
complicated alternation of
generations.
It would, therefore, not
assist us in Our comparison
with Amphioxus to describe
these types.
There is, however, one
family of pelagic Ascidians,
the Appendicularie, with re-
spect to which there are two
widely different opinions.
Fig. 111.— Appendicularia (Fritil- The Appendicularize are
Zaria) furcata, from the ventral surface. 5 F : A
(After LANKESTER.) pelagic, free-swimming As-
a. Anus. g?/. Unicellular glands. gs. jj; whose adult condi-
Gill-slits. %. Dorsal hood-like fold of cidians, See
integument. 2. Mouth. 4. Tail. tion is so far similar to the
ANATOMY AND DEVELOPMENT. 237
larval condition of the fixed Ascidians, that they retain the
tail as their organ of locomotion throughout life (Fig. 111).
The tail is inserted in the middle of the ventral surface
of the body proper, and is obviously a mere appendage of
the latter.
The mouth is terminal or sub-terminal. There is a sin-
gle pair of branchial stigmata, which open into a pair of
tubular atrial cavities, whose separate external apertures
are seen in front, on the ventral surface behind the mouth.
The alimentary canal is U-shaped, and the anus opens
on the ventral surface to the right of the middle line, some-
times behind and some-
times (according to the
species) in front of the
stigmata (Figs. III,
Piz); ~dWhevendostyle
is always quite anterior
in position, and some-
times, as in Fig. 112,
removed by a consider-
able interval from the
Fig. 112. — Diagram of the organisation of
stigmata. a species of Appendicularia, from the right side.
I 7 _ (After HERDMAN.)
n the posterior cx a. Anus; the index line was accidentally
tremity of the body drawn about % of an inch in front of the anus.
1 é.s. Branchial sac. ch. Notochord. e. Endostyle.
are p aced the gonads, g. Ganglion, from which the nerve-cord proceeds
male and female. in backwards to the tail, passing to the right of the
? alimentary canal. g.s. Gill-slit. 4. Heart. zmz.
close proximity to one Intestine. 7. Mouth. 2c. Nerve-cord, with
h i‘ .. ganglionic enlargements in the tail. of. Otocyst;
another, the testis 1M feneath which the hypophysis opens into the
front and the ovary branchial sac. ov. Ovary. 7.6. Peripharyngeal
band. s¢.Stomach. Ze. Testis.
behind. The heart, as
described by LANKESTER, is a unique example of a func-
tional organ reduced to the lowest possible level of histo-
logical structure. It consists simply of two cells placed
238 THE ASCIDIANS.
opposite one another and connected together by contractile
protoplasmic threads, which keep up a pulsating motion.
The tail is, as might be expected, more elaborately or-
ganised than that of the Ascidian larva. The dorsal nerve-
cord is solid, and proceeds backwards from the ganglion,
passing to the 7zgfz¢ of the alimentary canal until it reaches
the tail, along which it is continued, lying to the /eft of
the notochord; it possesses ganglionic enlargements at
intervals in the tail, from which nerves pass out.
The caudal musculature also shows somewhat doubtful
traces of being segmented in correspondence with the
ganglionic swellings of the nerve-cord.
In connexion with the cerebral ganglion there is a
sense-organ in the form of an otocyst, with an enclosed
otolith, and below this a ciliated pit opens into the ante-
rior region of the branchial sac, corresponding to the
hypophysis, or sub-neural organ, of the fixed Ascidians.
According to one view, Appendicularia is the living rep-
resentative of the free-swimming ancestor of the Ascidians.
According to the other view, it is less primitive than the
fixed Ascidians, and was derived from the latter by the
gradual increase, from generation to generation, of the du-
ration of the pelagic existence of the larva, until they
ceased to metamorphose, and so retained the larval struct-
ure throughout life, becoming at the same time sexually
mature.®
These two views are, of course, antagonistic, and the
former of them is held by a number of well-known author-
ities. As we are ignorant of the development of Appen-
dicularia, it is impossible to decide definitely between them.
With the facts which are at our disposal, however, the
second view — namely, that the Appendiculariz represent
Ascidian larvze which have become secondarily adapted to
ANATOMY AND DEVELOPMENT. 239
a pelagic life, and have acquired the faculty of attaining
sexual maturity — would be more in harmony with what
we know of the relation of Amphioxus to the Ascidians.
And it would seem that this affinity can be better demon-
strated through the comparison of Amphioxus, both adult
and larva, with a fixed Ascidian like Ciona than with
Appendicularia.®
On the latter view, therefore, the so-called metamerism
of the tail of Appendicularia, on which so much stress has
been laid, would be simply a secondary elaboration of the
tail for the purpose of serving as a permanent locomotor
organ.
The dorsal nerve-cord of Appendicularia was regarded
by Fo. as a simple peripheral nerve. We have described
above how a portion of the primitive nerve-tube in Ciona
and other Ascidians becomes reduced to a solid nerve.
It would be of the greatest interest to discover the mode
of origin of this nerve-cord in Appendicularia.
Abbreviated Ontogeny of Clavelina.
In order to demonstrate clearly the relatively primitive
character of the development of Ciona it is sufficient to
enumerate a few facts drawn from the development of
Clavelina as described by Dr. OswaLp SEELIGER. As
mentioned above, Clavelina is a near relative of Ciona, and
in the adult condition resembles it very closely in many
respects.
The development of Clavelina was formerly regarded as
being of a primitive character, but is in reality, more
especially in the later stages, abbreviated and hastened to
a remarkable extent.
Like Ciona it possesses in the adult numerous trans-
verse rows of stigmata. Each opening, however, arises by
240 THE ASCIDIANS.
an independent perforation, so that all those preliminary
ontogenetic processes which precede the establishment of
the transverse rows of stigmata in Ciona are dropped out
of the development of Clavelina.*
In Clavelina, again, the change of axis of the body
proper occurs in the unhatched larva; so does the fusion
of the two atrial apertures to form the dorsal cloacal
siphon. The longitudinal muscles of the body proper
commence to appear in the free-swimming larva, while the
caudal muscles are enjoying their highest functional
activity. The vacuolisation of the notochord does not
proceed so far as in Ciona, since the cells are never actu-
ally removed from the centre of the notochord, but remain
as thin discs stretching across the latter, so that the
vacuolar spaces do not become continuous.
The behaviour of the organ of fixation in the larva of
Clavelina is such that it could hardly be recognised as a
przoral lobe except in the light of Ciona.
NOTES.
1. (p. 183.) The test or cellulose mantle of the Ascidians con-
tains great numbers of cells of various kinds. These were formerly
supposed to be derived from the subjacent ectoderm of the body-
wall. Kowa.evsky has recently shown, however, that the cells of
the outer (cellulose) mantle of the Ascidians are derived from
wandering mesenchyme-cells which wander from the body-cavity
through the ectoderm (either de/ween the ectodermic cells or
actually passing ¢hvough the individual cells) into the mantle.
* A mode of formation of the branchial stigmata, intermediate between
that of Clavelina and Ciona or Molgula, has been described by GARSTANG
for Botryllus. In this genus, the primary branchial stigmata all arise by in-
dependent perforations, and then later become divided up into the transverse
rows of stigmata. (W. GARSTANG. Ox the development of the stigmata
in Ascidians. Proc. Roy. Soc., Vol. LI. 1892.)
NOTES. 241
2. (p. 211.) In Clavefina the atrial involutions do not merely
arise as minute circular invaginations of the ectoderm, but at first
they appear as short, though quite distinct, longitudinal grooves.
Compare also the remarkable longitudinal atrial tubes of Pyvosoma.
3. (p. 238.) There is another possible way of interpreting the
structure and systematic position of Appendicularia which may
perhaps be nearer the truth than either of the views mentioned in
the text. It is not absolutely necessary to suppose that the
ancestors of Appendicularia were fixed Ascidians; but both
Appendicularia and the fixed Ascidians may have descended from
a common free-swimming stock, and have undergone certain
modifications in common, such as loss of true vascular system and
celom. Then, while the Ascidians proper became adapted toa
sessile existence, Appendicularia may be supposed to have gone
to the opposite extreme, and have become adapted to an absolutely
pelagic existence. In becoming adapted to such a purely pelagic
or oceanic environment as that of Appendicularia, it is eminently
conceivable that an animal would have to undergo as radical a
modification of structure as it would in becoming adapted to a
sessile existence. (Compare Sa/a, Doliolum, etc.)
V.
fAE PROTOCHORDATAIIN THEIR RELADION
TO THE -PROBLEM OF VERTEBRATE, DES
SCE Nae
“ Den Schlissel richtigen Verstandnisses gibt nicht das Hineinpressen
neuer Thatsachen in eine alte Schablone, sondern das Aufsuchen des
genetischen Zusammenhangs der Erscheitnungen.” — WEISMANN.
BALANOGLOSSUS.
External Features.
Or the free-living protochordates, the lowest type of
organisation is undoubtedly presented by the Exteropneusta
(Hemichorda), the group to which Balanoglossus belongs.
Balanoglossus is a remarkable worm-like creature which
lives buried in the sand or mud of the sea-shore. By
means of numerous unicellular integumentary glands which
are distributed over the surface of the body, it secretes a
mucous substance to which particles of sand adhere, and
so makes for itself tubes of sand in which it lives at about
the level of the low tide-mark. It possesses such a
characteristic external form and odour (like iodoform) as to
render it peculiarly easy of recognition.
In front there is a long and extremely sensitive proboscis
which is capable of great contraction and extension, and is,
in the living animal, of a brilliant yellow or orange colour.
Behind the proboscis follows a well-marked col/lar-region,
242
BALANOGLOSSUS. 243
consisting externally of a collar-like expansion of the
integument, with free anterior and posterior margins over-
lapping the base of the proboscis in front and the anterior
portion of the gz//-slzts behind.
In the ventral middle line, at the base of the proboscis
and concealed by the collar, is situated the mouth (Fig.
113). Following behind the collar is the region of the
trunk or body proper, which, in the adult of some species,
reaches a relatively enormous length, even extending to
Fig. 113. — Larva of Balanoglossus Kowalevskii, with five pairs of gill-slits ;
from the right side. (After BATESON.)
a. Anus. a.~. Temporary pedicle of attachment. c¢. Collar. cz. Notochord.
g.s. Gill-slits. mm. Mouth. gr. Proboscis.
two or three feet. The ectodermal covering of the body
consists in general of ciliated cells, among which are scat-
tered unicellular mucous glands ; the cilia, however, appear
to be more prominent on the proboscis than elsewhere.
In the region of the trunk, which immediately follows
upon the collar region, there are a great number of paired
244 THE PROTOCHORDATA.
openings on the dorsal side of the body, placing the anterior
portion of the digestive tract in communication with the
outer world. Theseare the gz//-s/zts, and they are arranged
strictly in consecutive or metameric pairs to the number of
upwards of fifty in the adult. In their structure, and more
especially in the possession of tongue-bars, they bear a
remarkable resemblance to the gill-slits of Amphioxus.
This is particularly striking in young individuals. As the
adult form is approached in the development, the bulk of
the gill-slits sinks below the surface, only opening at the
latter by small slit-like pores, and thus their true character
is obscured in a superficial view.
Projecting into the interior of the proboscis is a rod-like
structure which arises as an outgrowth from the alimentary
canal dorsal to the mouth. The lumen of this endodermic
diverticulum becomes narrowed down and, in fact, partially
obliterated, while the cells constituting its walls give rise
to a spongy vacuolar tissue which strongly resembles the
notochordal tissue of Amphioxus and the higher Verte-
brates. On account of its dorsal position above the mouth,
its endodermic origin, and the vacuolisation of its cells, this
structure was identified by BaTEson in 1885 as the zofo-
chord.
Nervous System and Gonads.
The nervous system of Balanoglossus presents many
features of the utmost interest and suggestiveness. It
consists essentially of an ectodermal network of nerve-fibres
forming the inner layer of the skin (ectoderm) all over the
body. In this primitive nervous sheath, which envelops
the whole body, there are certain definite local thickenings.
Two of these thickenings occur respectively along the
whole length of the dorsal and ventral middle lines in the
trunk-region, thus producing the dorsal and ventral median
BALANOGLOSSUS. 245
longitudinal nerve-cords. In the region of the collar the
dorsal nerve-cord becomes entirely separated from the
ectoderm, and this portion of it contains, at least in young
individuals, a central canal which, from its origin and
relations, was shown by BATEsoN, and more recently by
MorGan, to be homologous with the central canal of the
vertebrate spinal cord. Anteriorly the dorsal nerve-cord
becomes continuous with a specially dense tract of the
general nerve-plexus at the inner posterior surface of the
ov bc* Com
Fig. 114.— Diagram of the organisation of Balanoglossus, from the left side.
(From a drawing kindly lent by Professor T. H. MORGAN.)
al. Alimentary canal. 6cl1. Coelom of proboscis (anterior or preeoral body-
cavity). 6c?. Coelom of collar. 4c3. Coelom of trunk. 4.v. Blood-vessel, proceed-
ing from the so-called heart (which lies at base of proboscis above the noto-
chord) to the ventral blood-vessel. ch.,Notochord. com. Commissure, between
dorsal and ventral nerve-cords. dz. Dorsal nerve-cord, separated from the integu-
ment in the collar-region. d.d.v. Dorsal blood-vessel. g/. Proboscis-gland ;
modified ccelomic epithelium surrounding heart and front end of notochord.
m. Mouth. #.v. Pulsating vesicle, lying inside the “heart.” v.4.v, Ventral blood-
vessel. v.2. Ventral nerve-cord.
proboscis (Fig. 114). This proboscidian plexus thins out
somewhat towards the anterior extremity, but nevertheless
forms a complete nerve-sheath for the proboscis and indi-
cates the sensitive character of the latter (Fig. 115).
The ventral nerve-cord does not extend into the region
of the collar, but from the point where the collar joins on
to the trunk the ventral cord is connected with the dorsal
nerve-cord by a commissure-like thickening of the integu-
mentary plexus, which passes in the skin on each side
round the hinder end of the collar-region (Fig. 114).
2406
Fig. 115.— Diagrammatic transverse sec-
tion through hinder region of proboscis of
Balanoglossus. (From a drawing kindly
lent by Professor T. H. MORGAN.)
D. Dorsal. V. Ventral. cl, Proboscis-
cavity, almost filled up by mesenchymatous
and muscular tissue,* proliferated from the
THE PROTOCHORDATA.
The
testes or ovaries, accord-
genital organs,
ing to the sex of the
individual, occur as a
paired metameric series
of pouch-like bodies or
gonadic sacs which ex-
tend backwards far be-
yond the region of the
gill-slits.
sacs are suspended in the
The gonadic
body-cavity by solid cords
attached to the dorsal
which _ be-
come perforated in the
integument,
spawning season to ad-
original coelomic epithelial layer (indicated
by the black line below the ectoderm).
p.v. Pulsating vesicle. #4. Heart. ch. Noto-
chord. .s. Integumentary nerve-plexus.
mit of the expulsion of the
reproductive elements.
Metamerism.
Although there is no muscular metamerism in Balano-
glossus, yet we have seen that other organs (gill-slits and
gonads) are arranged metamerically. And in point of
fact, among those Invertebrates which are not included
under the phylum of the Articulata, if there is one pecu-
liarity of organisation more sporadic in its occurrence than
another, it is metamerism. It may affect the most differ-
ent organs of the body either collectively or individually,
and nothing is more patent than the fact that the meta-
meric repetition of parts has arisen independently over
and over again in different groups of animals.1
* This tissue is not represented in Figs. 114 and 116, although it is present
throughout the body-cavity.
BALANOGLOSSUS. 247
Far from assuming as a self-evident fact that the
extreme metamerism of the Annelids and Arthropods is
genetically identical with that of the Vertebrates, we have
every reason to suppose that it has been elaborated entirely
independently in the two cases, and that the apparent simi-
larity is due, as already intimated, to a parallel evolution.
Body-cavities ; Proboscts-pore ; Collar-pores.
Corresponding to the
three regions into which
the body of Balanoglossus is
divided, — namely, probos-
cis, collar, and trunk, —the
body-cavity is divided up into
three systems of cavities.
These are (a) the anterior
body-cavity or cavity of the
iam
ae) I
<
proboscis, (8) a pair of collar-
“t
1
1
cavities, and (y) a pair of
body-cavities which form the
unsegmented ccelom of the
trunk (Figs. 114, 115).
These cavities arise essen-
WNW
comm | ANdHANEAANADLDADINAT THI
mM ||
tially as pouches from the
@Ooe® @® Le RAaannn
archenteron (Fig. 117), al-
though their actual develop-
, : : Fig. 116. — Diagram of the organisa-
ment differs considerably IN tion of Balanoglossus, from the dorsal
different species (MorGAN). side. (From a drawing kindly lent by
: ° ’ Professor T. H. MORGAN.)
lie proboscis-cavity 1S c.p. Collar-pores. go. Gonads. g.s.
. : : Gill-slits; the dark lines converging be-
placed in communication hind indicate the superficial portions of
with the exterior by an open- the gill-slits; below the surface are seen
. : the free ends of the tongue-bars. ff.
ing th rough the posterior Pproboscis-pore. Other letters as above.
248 THE PROTOCHORDATA.
wall of the proboscis known as the proboscis-pore. In
B. Kowalevskii this pore lies asymmetrically to the left of
the dorsal middle line (Fig. 115), while in B. Kupfferi a
corresponding opening occurs
Fig. 117. — Diagrammatic horizontal
section through an embryo of Balanoglos-
sus (type of the direct development), to
show the origin of the body-cavities as
archenteric pouches. (After BATESON.)
ap. Tuft of cilia at the apical pole
(indication of an apical plate). écl. Probos-
cis-cavity. dc. Collar-cavities. cé3, Trunk-
cavities. cd. Circular band of cilia.
to the right of the middle
line, so that in this species
there are two proboscis-
pores constituting a sym-
metrical pair.
The left proboscis-pore
of Balanoglossus is obvi-
ously to be compared with
the przoral pit of Amphi-
OXUS.
The collar-cavities also
open to the exterior by
pores, one on each side
underneath the dorsal pos-
terior. “free, fold yor the
collar, and on a level with
the opening of the first
gill-slit. These are the
funnel-shaped col/ar-pores.
SPENGEL states that water
is taken in through the
collar-pores into the cavity
of the collar in order to swell the latter up, so that it
may serve as an accessory organ of locomotion in so far
as an alternate inflation and collapse of the collar would
assist the animal in its slow burrowings in the sand.
BALANOGLOSSUS. 249
Alimentary Canal.
The mouth cannot be closed, as there is no sphincter
muscle, and accordingly, as the animal progresses through
the sand, it swallows a large quantity of the latter in
which food-particles (unicellular organisms, etc.) may also
be involved. As the sand passes through the intestine,
it becomes enveloped in the mucous secretion of the intes-
tinal epithelium, and is ejected through the anus in a cord
of slime.
The alimentary canal is a straight tube between mouth
and anus. In its hinder portion it is usually sacculated,
z.e. provided with paired
lateral saccular dilatations
comparable to the so-called
intestinal ceca of the Ne-
mertine worms. (See below.)
In the region of the pharynx
the lumen of the alimentary
canal is incompletely divided
by lateral constrictions into
y Fig. 118. — Transverse section through
two portions, an upper Or the gill-region of Balanoglossus. (After
he peal fi : SPENGEL.)
vanchiat portion Carrying al, Digestive portion of gut. 47.
the gill-slits, and a lower or Branchial portion of gut. bc8, Third
. ; ; e body-cavity (trunk ccelom) ; this is also
digestive portion (Fig. I 18). nearly obliterated in the adult by the pro-
liferation of mesenchyme or “paren-
The latter was compared by chyme” from its walls. d@.c. Dorsal
GEGENBAUR* to the endo- nerve-cord. d.d.v. Dorsal blood-vessel.
ahs go. Gonad. g.s. Gill-slit. £4. Tongue-
style of the Ascidians, but bar. v.4.v. Ventral blood-vessel. v.1.c.
ae | nerve-cord.
it is probable that this com- Vem"! nervecord
parison, although a very natural and useful one at the time
at which it was made, will not hold good, since there is
* CARL GEGENBAUR, Elements of Comparative Anatomy. Translated by
F. Jeffrey Bell. London, 1878.
250 THE PROTOCHORDATA.
nothing in the structure or development of this part of the
alimentary tract in Balanoglossus which will bear compari-
son with the endostyle.* As indicated in the larvae of
Amphioxus and the Ascidians, it would seem that the
endostyle first became evolved or differentiated at the
anterior end of the pharynx, zz front of the gill-slits, in
correlation with the dorsal position of the mouth.
Development; the Tornaria Larva.
The development of Lalanoglossus Kowalevskit as made
known to us by the admirable work of BATESON is what
is knownas a strictly direct development; that is to say, the
embryonic, larval, and adult stages follow one another by
gradual transitions concomitantly with the simple progres-
sive growth of the individual and without any striking
metamorphosis. In other species of Balanoglossus the
larval form is remarkably different from the adult, and
becomes transformed into the latter by a very distinct
metamorphosis. The extraordinary larval form here re-
ferred to was discovered in 1848 by JOHANNES MULLER,
who named it 7ornzaria, and regarded it, as did his succes-
sors KrouHn, ALEXANDER AGAssiZz, and Fritz MULLER, as
the larva of an Echinoderm (Starfish).
It was not until 1869 that its true character as the larva
* A ciliated tract in the floor of the cesophagus of a Tornaria from the
Pacific has recently been compared to the endostyle by W. E. Ritrer. (Ox
a New Balanoglossus Larva from the Coast of California and its Possession
of an Endostyle. Zool. Anz. XVII. 1894. pp. 24-30.)
The comparison is at present somewhat doubtful. More recently GARSTANG
has suggested that the endostyle is derived from the adoral ciliated band of the
Echinoderm larva. (See Fig. 119.) The suggestion is an interesting one, but
Garstang’s idea of the relations of the preeoral lobe is very different to the one
here set forth. (WALTER GARSTANG, Preliminary Note on a New Theory of
the Phylogeny of the Chordata. Zool. Anz. XVII. pp. 122-125.)
BALANOGLOSSUS. 251
of a species of Balanoglossus was demonstrated by Extras
METSCHNIKOFF. Shortly afterwards, Metschnikoff’s dis-
covery was confirmed and amplified by ALEXANDER
AGASSIZ.
The superficial likeness between Tornaria and such Echi-
noderm larve as Bipinnaria or Auricularia is astonishing,
and a renewed study of the detailed organisation of
Tornaria, recently made by MorGan, appears to have
established the fact, originally insisted upon by Metschni-
koff, that this resemblance can only be accounted for on
the ground of genetic affinity.
In Figs. 119 and 120 two types of larve, Tornaria
and Auricularia, are shown side by side; and although
unfortunately they are not figured from exactly the same
aspect, yet it is obvious at a glance that, in spite of certain
differences which will be enumerated below, they both
belong to the same category of larval forms.
A highly characteristic feature of these larve is the
remarkable ectodermal ciliated band which constitutes a
perfectly symmetrical but somewhat complicated undulat-
ing seam round the body. The larve are strictly pelagic,
and swim about in the open sea by means of their cilia ;
but the latter, instead of being distributed evenly over the
whole surface of the body, are concentrated in the region
of the ciliated bands which are composed of thickened
ectoderm.
In Tornaria there are two ciliated bands, viz.: 1) the
above-mentioned undulating seam which is usually known
as the cercumoral or longitudinal ciliated band, and 2)a
postoral circular ciliated band. Only the former is present
in Auricularia, and the absence of the circular band in this
form constitutes one of the chief differences between the
two larvae.
252 THE PROTOCHORDATA.
From a morphological point of view a more striking
resemblance between the two larve than that furnished
by the longitudinal ciliated bands exists in connexion with
the anterior body-cavity or exteroce/l. In the Echinoderm
eeircibietlctne eI frene mee . ‘
Figs. 119 and 120.— Auricularia, larva of Synapta (after SEMON); and
Tornaria, larva of Balanoglossus. (After MORGAN.)
a. Anus. aj. Apical plate. cl, Anterior body-cavity, communicating with
exterior by the water-pore. 4c?, 6c8, Second and third body-cavities of Tornaria.
¢.6, Circular ciliated band of Tornaria. c.c. Contractile cord between apical plate
and anterior body-cavity of Tornaria. gf. Gill-pouches. 4.c. Hydroccel of
Auricularia (anterior body-cavity). /.c.6. Longitudinal (circumoral) ciliated band.
Ze. Left enteroccel (body-cavity). . Mouth. z. Lateral (paired) nerve-band
of Auricularia. 7e. Right enteroccel. sf. Calcareous spicules. s¢, Stomach.
wp. Water-pore.
N.B.—In Auricularia, the margin of the mouth is surrounded by a ciliated
band discovered by SEMON, and known as the adoral ciliated band. The poste-
rior, V-shaped portion of this band lies inside on the ventral floor of the larval
cesophagus.
larva this cavity arises as a median pouch of the archen-
teron, and there is every reason to suppose that it has a
similar origin in Tornaria, although this point has not yet
BALANOGLOSSUS. 253
been determined. The primary anterior enteroccel in the
Echinoderm larva is not quite the same as the correspond-
ing cavity in Tornaria, since it contains also the elements
of the general body-cavity. Apart from slight differences,
the collar-cavities and general body-cavities arise essen-
tially in the same way in Tornaria as they do in the case
of the direct developing larva of Balanoglossus (see above).*
In the Echinoderm larva, however, the paired body-
cavities do not arise as independent archenteric pouches,
but they become constricted off from the anterior entero-
ceel. Making allowance for these deviations in the origin
of the body-cavities, — deviations which are by no means
fundamental, since in both cases the body-cavities are
ultimately reducible to archenteric pouches, —it is an
extremely striking fact that both in Tornaria and Auricu-
laria the anterior enteroccel acquires an opening to the
exterior on the dorsal surface to the left of the middle line.
This opening is called the waterpore, since it forms the
outlet (possibly both outlet and inlet) of the water-vascular
system of the Echinoderm. In Tornaria it persists after
the metamorphosis as the proboscis-pore, which has been
described above.
The Larva of Asterias vulgaris; Water-pores and
Preoral Lobe.
In view of what was said above as to the occurrence of
paired proboscis-pores in B. Kupfferi, it is interesting to
note that sometimes there are two water-pores, a right and
a left, in Echinoderm larvae. This has been observed by
* As to the origin of the body-cavities in different species of Balanoglos-
sus, MORGAN summarises his observations as follows: “They may arise as
enteric diverticula, as endodermal proliferations, or even arise from mesenchy-
matous beginnings.” (See Morcan. No. 125 bibliog.)
254 THE PROTOCHORDATA.
Brooks and G. W. FIELp in the larvz of a common star-
fish, Asterzas vulgaris. In this case the primary enteroccel
becomes constricted off from the archenteron in the form
of two equal pouches. The right and left enteroccelic sacs
then take up a symmetrical position on each side of the
larval cesophagus, and each sac next opens to the exterior
by a water-pore. The pore in connexion with the right
sac (Fig. 121) is, however, of a transitory, rudimentary
character, and soon closes
up, while the left pore per-
sists as the definitive water-
pore. As in Tornaria, so
here, the cavity of the larval
body generally, and of the
preeoral region (pre@oral lobe)
in particular, is the primary
body-cavity or blastoccel,
and contains scattered mes-
enchyme-cells. At a later
Fig. 121. — Young larva of Asterias stage In the larva of As-
vulgaris, from the dorsal side. (After terjag the right and left
G. W. FIELD.) : ; ;
pl. Preoral lobe. 4.c.5. Circumoral enteroccelic sacs, having in-
(longitudinal) ciliated band. oes, G¢soph- :
agus. ve. and Ze. Right and left en- creased greatly mM length,
teroccelic sacs, each opening bya“water- meet one another in the
pore” to the exterior. sf. Stomach. zz.
Aperture, leading from stomach into in- region of the preeoral lobe
en and fuse together, thus put-
ting their two cavities into communication across the
median line. The median portion of the enteroccel thus
produced extends up into the przoral lobe, and so the
primary blastoccelic cavity of the latter is replaced by a
secondary ingrowth of the enteroccel (Fig. 122).
Similarly with the metamorphosis of Tornaria, the
anterior enteroccel, which is at first of very inconsid-
BALANOGLOSSUS. 255
erable extent (Fig. 120), increases greatly in size, and
assumes its definite position and proportions as the cavity
of the preeoral lobe (z.e. proboscis), thus replacing the
original blastoccelic space,
while the water-pore remains
as the proboscis-pore.
As described in the previ-
ous chapter, the cavity of
the preoral lobe (fixing
stolon) of the Ascidian tad-
pole is of the nature of a
blastocoel or primary body-
cavity, containing loose mes-
enchyme-cells, and it is
2 Fig. 122.— Older larva (Bipinnaria)
therefore of great IMPOT- of Asterias vulgaris, from the ventral
tance to note that whether side. (After G. W. FIELD.)
a By a fusion of the two przeoral loops
the cavity of the preoral of the ciliated band across the apex of the
o 5 przeoral lobe, followed by a separation in
lobe is a 6lastocwl or an the transverse direction, the originally
enterocel, the morphological single circumoral band (cf. Figs. 119 and
5 121) has become divided into two bands,
value of the structure itself a preoral ciliated band #.c.6. and a post-
remains the same oral longitudinal ciliated band /.c.6. The
; posterior transverse portion of the pra-
oral ciliated band has undergone a fusion
Apical Plate of Tornaria. With the front end of the originally dis-
tinct adoral band (cf. Fig. 119). 7.2. Prae-
At the anterior end of oral lobe, into which the enterocoel has
extended. mm. Mouth. me. and Ze. Right
the body, or, in other words, and left enteroccelic cavities. s¢, Stomach,
at the apex of the praoral “ ees
lobe, in Tornaria, there is an ectodermic thickening in
which nerve-cells and nerve-fibres and a pair of simple
eyes have become differentiated. This is the so-called
apical plate, and it constitutes the central nervous system
of the larva. It can be recognised for some time after the
metamorphosis at the tip of the proboscis, but eventually
disappears completely. A similar apical plate occurs in
256 THE PROTOCHORDATA.
a great number of Invertebrate larvae, and is especially
characteristic of the free-swimming larve (Trochophores,
or Trochospheres) of Annelids and Molluscs. We shall
return to this later.
In Tornaria a single contractile cord passes from the
apical plate to the anterior enteroccel.
There is no apical plate in Auricularia, nor in most of
the other Echinoderm larve ; but there is reason to sup-
pose that it has been secondarily lost, since a transitory
ectodermal thickening at the apical pole can frequently
be observed in the course of their development ; and,
moreover, in what is probably the most primitive Echino-
derm larva known (viz. the larva of the Crinoid, Axzedon),
there is a well-developed apical plate.
Metamorphosis of Tornaria.
The metamorphosis of Tornaria, as originally described
by Alexander Agassiz, takes place with relative sudden-
ness. According to the more recent account of the meta-
morphosis given by MorGan, a marked diminution in size
occurs; the internal organs are drawn together in such a
way that the larval cesophagus, with the gill-pouches (see
Fig. 120), is drawn backwards into the body, and the
anterior enteroccel, as already described, is carried for-
wards into the przeoral lobe. The longitudinal (circum-
oral) ciliated band, which was the first to develop, is also
the first to disappear, while the posterior circular band
persists to a somewhat later stage.
The Nemertines.
It is thus evident that Balanoglossus, especially through
its Tornaria larva, shows undoubted marks of affinity to
NEMERTINES. 257
the Echinoderms. It will next be shown that there are
certain features in the adult anatomy which apparently
indicate a distinct genetic relationship to another group of
the Invertebrates ; namely, the Vemertine worms.
The Nemertines are elongated, flattened, or cylindrical
worms, with a smooth cz/zated skin and no external seg-
mentation, occurring, as a rule, in a closely similar habitat
to that of Balanoglossus, buried in the sand or mud of the
sea-shore.
Like Balanoglossus, they also possess unicellular integu-
mentary glands, by means of which they secrete a mucous
substance, to which frequently sand-grains adhere, thus
producing a tube of sand round the body. Some of them
reach an enormous length, and one at least must be
measured in yards (Lzneus longissimus exceeding three
yards in length).
The chief anatomical features which offer material for
direct comparison between the Nemertines and Balano-
glossus relate to the ectoderm, proboscis, nervous system,
mesenchymatous tissue, the reproductive organs, and the
alimentary canal.
As for the ectoderm, considered apart from the nervous
system, it need only be repeated that in both cases it is
composed of ciliated cells and scattered mucous glands.
The proboscis of the Nemertines is one of the most
characteristic organs of this group of animals. It is not
permanently protruded, and does not serve as an organ of
locomotion, as in Balanoglossus, but is usually carried
about entirely withdrawn within the body of the animal,
from which it can be shot out with great force and rapidity
when the occasion demands it. During the process of
extrusion it is turned completely inside out, and conversely,
during the process of zxtroverszon, the retraction takes
258 THE PROTOCHORDATA.
place from the tip backwards by the in-rolling of its walls.
According to the graphic description of HuBRECHT, it is
retracted ‘fin the same way as the tip of a glove finger
would be if it were pulled backwards by a thread situated
in the axis and attached to the tip.”
When at rest within the body the proboscis lies freely
within a hollow cylinder, the wall of which is thick and
muscular, and constitutes the prodoscis-sheath (Fig. 123).
Fig. 123. — Diagrammatic transverse section through the middle of the body
of a Nemertine. (After LANG, Text-b00k of Comp. Anat.)
én, Basement-membrane. c.m. Circular muscles. d.z. Dorsal or “ medullary”
nerve. d.v. Dorsal blood-vessel. g. Gonads. wz. Intestine. /.m. Longitudinal
muscles. 7. Lateral nerves. ¢.v. Lateral blood-vessel. ~. Proboscis. #.s. Pro-
boscis-sheath.
Sometimes beneath the ectodermal epithelium of the
Nemertine proboscis there is a continuous sheath of nerve-
fibres, comparable to the nervous plexus in the proboscis
of Balanoglossus.
Partly, therefore, on account of its structure, and partly
on account of its topographical relations when extruded,
we are led to suppose that a certain homology exists
NEMERTINES. 259
between the retractile proboscis of the Nemertines and
the non-retractile proboscis of Balanoglossus (BATESON).
In the most primitive Nemertines the nervous system
consists essentially of a somewhat complicated pair of
cerebral ganglia and a diffuse nerve-plexus, with nerve-
cords lying at the base of the ectoderm.* As the cerebral
ganglia probably belong to the same category as the cere-
bral ganglia of all other typical Invertebrates, and are not
represented in Balanoglossus, we can afford to neglect
them at present. Confining our attention to the ecto-
dermal nerve-plexus, we find occurring in it, along definite
lines, local thickenings, after the same principle, but not
all on the same lines, as was described above for Balano-
glossus. Directly comparable with the dorsal longitudinal
nerve-cord of Balanoglossus, there is a similar thickening
or concentration of the integumentary nerve-plexus in
some of the Nemertines, in the dorsal middle line (Car-
inina, Cephalothrix). Hubrecht, who discovered this, calls
it the medullary nerve. There is, however, no correspond-
ing ventral nerve-cord in the Nemertines, but, instead of
this, there is a pair of lateral thickenings, constituting the
well-known /ateral nerves of the Nemertines (Fig. 124).
It is usually supposed that the lateral nerves of the
Nemertines are homologous with the two halves of the ven-
tral nerve-cord in the Annelids. In the Annelids the
primitive lateral nerves (which are so typical of the Platy-
helminths, or flat-worms) have approached one another in
the mid-ventral line, and have often undergone intimate
fusion together. In some cases, however, they are separated
from one another by a wide interval (Sabellaria, etc.).
* HUBRECHT compared the lobes of the cerebral ganglia of a Nemertine to
the cranial ganglia of the Vertebrates, the lateral nerves to the Rami laterales
vagi, and the proboscis-sheath to the notochord.
260 THE PROTOCHORDATA.
In the Annelids, in contrast to the Nemertines, the gan-
glion-cells are not distributed uniformly along the whole
length of the nerve-cord, but are collected together to
form definite ganglionic swellings.
It is, therefore, very significant that in the Nemertines
we have a median dorsal ‘medullary”’ nerve, in addition
to the elements which constitute the ventral nerve-cord of
the Annelids.
In many Nemertines the dorsal and lateral nerve-cords
do not continue to lie in the ectoderm throughout life, but
Fig. 124.— Diagrammatic view of anterior portion of a Nemertine, from the
left side. (After HUBRECHT, from LANG.)
a./. Anterior lobe of brain. £./. Posterior lobe of brain. . Opening of pro-
boscis. . Mouth. d.#. Dorsal nerve. /. Lateral nerve. 7.7. Ring-nerves.
sink deeper into the body, and so come to be separated
from the ectoderm, first by the basement membrane, and
then by one or more muscular layers of the body-wall. In
the Hoplonemertea (those in which the proboscis is armed
with stylets) the medullary nerve is absent. In all cases,
however, the longitudinal nerve-cords remain connected
with one another by a more or less plexiform arrangement
of nerve-fibres ; although sometimes a more definite con-
nexion, by means of metameric ring-nerves, has been
observed by Huprecut (Fig. 124).
NEMERTINES. 261
There is no true ccelom in the Nemertines, and the
space between the alimentary canal and body-wall is oc-
cupied by a gelatinous mesenchyme, containing muscular
and connective tissue elements. In Balanoglossus the cav-
ity of the coelom becomes largely obliterated in the adult,
by the proliferation of cells from the epithelium of its
walls, thus filling up the cavities with a more or less solid
parenchymatous tissue.
Like Balanoglossus, the Nemertines have a straight all-
mentary canal, provided with paired lateral outgrowths or
tntestinal ceca, and a terminal anus.
The gonadic sacs of the Nemertines offer a striking re-
semblance to those of Balanoglossus. They occur as a
metameric series of paired sacs, which alternate with the
above-mentioned intestinal cceca, and communicate with
the exterior by short tubes, which are at first solid, as in
Balanoglossus, subsequently becoming hollowed out and
opening above the lateral cords (Fig. 124).
Finally it should be pointed out that, while excretory
organs, in the form of a well-developed single pair of
elongated nephridia, provided with numerous internal
‘“end-sacs,” are present in the Nemertines, nothing of the
kind has yet been detected in Balanoglossus.
CEPHALODISCUS AND RHABDOPLEURA.
It is interesting to note that there are some remarkable
animals which stand in a similar relation to Balanoglossus
that the Ascidians do to Amphioxus. While Balano-
glossus is free-living, does not produce buds, and has a
straight alimentary canal, these creatures, of which only
two genera are at present known, Cephalodiscus and Rhab-
dopleura, \ead a sessile existence, produce buds, and have
262 THE PROTOCHORDATA.
a U-shaped alimentary canal. Both are deep-sea forms,
Cephalodiscus having been dredged during the Challenger
Expedition, from the Straits of Magellan, at a depth of 245
fathoms ; while Rhabdopleura was first dredged indepen-
dently, off the Shetland Islands, at go fathoms, by the Rev.
Wins
EN ‘i ih
\ —\ ‘
Fig. 125. — Cephalodiscus dodecalophus, from the ventral side. (After
M’'INTOSH.)
Actual length of polypide from extremity of branchial plumes to the tip of the
pedicle is about 2 mm.
4.s. Buccal shield; the shading on its surface indicates pigment-markings.
At the tip of the pedicle, buds are produced.
Canon NormMav, and off the Lofoten Islands, at 200 fath-
oms, by Professor G. O. Sars (1866-68). Rhabdopleura is
the name given by ALLMAN (1869), who published a short
account of it; and it has since been described by Sars,
LANKESTER, and G. H. FOWLER.
CEPHALODISCUS. 263
The account which we possess of Cephalodiscus forms
one of the Challenger Reports, and was written by Pro-
fessor W. C. M’Inrosa, who made out the main features
of its anatomy. It was further treated, from a morpholog-
ical standpoint, by SipNey F. HARMER, who pointed out
its remarkably close affinity to Balanoglossus.
The most important morphological features in the anat-
omy of Cephalodiscus are shown in Figs. 125-127. The
individuals live in colonies, in a “house” or ce@n@ecium,
which consists of a ramifying and anastomosing system of
tubes, the walls of which are composed of a semi-trans-
parent, gelatinous material, whose outer surface is covered
with spinous projections. The walls of the coencecium
are furthermore perforated by numerous apertures, which
allow of the ingress and egress of water.
The adult members of a colony have no organic con-
nexion between themselves, but each one is independent
and free to wander about the tunnels of the coencecium.
Although Cephalodiscus has not been studied in the living
condition, there is every reason to suppose that it moves
about in its tube by means of the large duccal shield (Fig.
125) overhanging the mouth, by which it can attach itself
to the inner surface of the tube, and then help itself
along by the curious pedicle which occurs ventrally near
the hinder end. It thus seems probable that this pedicle
can be used as a sucker, but its chief function lies in the
production of buds which grow out from it, and eventually
become detached. Bateson has described a somewhat
similar sucker at the hinder end of the body in young
individuals of Balanoglossus (Fig. 113).
Behind and above the buccal shield there is a row of
twelve tentacles or branchial plumes, each possessing a
central stem or shaft which carries numerous lateral
2064 THE PROTOCHORDATA.
pinne. An important function of these plumes is to
produce currents of water by the action of their cilia,
which vibrate in such a direction that the water with
food-particles is led into the mouth. The superfluous
water is led out from the proximal portion of the aliment-
ary canal by a single pair of gz//-sits which are not visible
in surface view, since they
are overhung by a fold of
the integument known as
the post-oral lamella or
operculum, corresponding to
the posterior free fold of
the collar in Balanoglossus
(Pigs126):
In its internal organisa-
tion, 1f due allowance be
made for its U-shaped ali-
mentary canal, Cephalodis-
cus greatly resembles Bala-
noglossus (Figs. 126, 127).
The buccal shield of the
Fig. 126. — Longitudinal frontal (right former is obviously the
and left) section through an adult Cephalo- equivalent of the probos-
discus. (After HARMER.)
bc2, Second portion of body-cavity cis of the latter, and the
(collar-coelom). 4c8. Third portion of : igh S ai
body-cavity (trunk ccelom). 67. Pharynx. cavity whic it contains
cp. Collar-pores. .g.s. Gill-slits. z¢, In- corresponds to the probos-
testine. 7.5. Nervous system. of. Oper- :
culum, oes. (Esophagus. sf. Stomach. C1S-Cavity. Moreover, the
zt. Base of tentacle.
proboscis-cavity in Cephalo-
discus (z.e. the cavity of the buccal shield) communicates
with the exterior by ¢wo proboscis-pores placed right and
left of the dorsal middle line.
Following behind the buccal shield is the collar-region,
from which the branchial plumes arise dorsally, while
CEPHALODISCUS. 265
laterally and ventrally it is produced into a free fold to
form the above-mentioned operculum. The collar-region
contains a section of the coelom which is precisely homolo-
AB
Fig. 127. — Longitudinal sagittal section through an adult Cephalodiscus.
(After HARMER.)
The section is supposed to be taken sufficiently to one side of the middle line to
allow of the representation of one of the ovaries and one of the proboscis-pores.
a. Anus. 6.c. Trunk-ccelom. c¢.c. Collar-ccelom. chk. Notochord. zm#f¢, Intes-
tine. mm. Mouth. .s. Nervous system. of. Postoral lamella (operculum).
ov. Ovary; the oviduct is deeply pigmented. f.c. Preeoral ccelom (cavity of
buccal shield). £#%. Pharynx. 7.f. Proboscis-pore. fed. Base of pedicle.
st, Stomach.
gous with the collar-cavities of Balanoglossus. As in the
latter form, it communicates with the exterior by a pair
of collar-pores which open at the level of the gill-slits.
266 THE PROTOCHORDATA.
The collar-ccelom is continued posteriorly into the opercu-
lum, and anteriorly into the twelve tentacular appendages.
Finally, behind the collar comes the region of the body
containing the viscera, which are surrounded by the third
section of the ccelom.
Only the female reproductive organs have been observed
up to the present time in Cephalodiscus. They occur as
a pair of gonadic sacs, opening to the exterior on each
side of the dorsal middle line between the anus and the
central nervous system. The latter is very simple, being
represented merely by a dorsal thickening of the ectoderm,
with nerve-fibres in the region of the collar and posterior
portion of proboscis.
Finally, a short notochordal diverticulum projects into
the base of the buccal shield as in Balanoglossus.
Rhabdopleura differs considerably from Cephalodiscus
in many respects, but, nevertheless, has some fundamen-
tal characteristics in common with it. In Rhabdopleura
the individuals of a colony are not independent, but are
connected with each other by a common cord or cawlus,
which represents the remains of the contractile stalks of
the polyps. As the growth of the colony proceeds, the
distal portions of the stalks (z.e. the portions farthest away
from the animals) become shrunken and hard. The buds
arise from the soft portions of the caulus, and never be-
come detached as they do in the case of Cephalodiscus.
There is only a single pair of tentacular plumes in Rhab-
dopleura.
Fow Ler has recently shown that in Rhabdopleura the
cceelom, whose existence was first established by Lan-
KESTER, exhibits the same subdivisions as have been
mentioned above for Cephalodiscus; namely, (1) the cavity
of the large buccal shield, (2) the collar-cavity opening
PRAZORAL LOBE. 267
to the exterior by a pair of dorsally placed collar-pores,
and (3) the body-cavity proper surrounding the alimentary
canal. According to Fowler, who has recently described
them in Rhabdopleura, the nervous system and notochord
have essentially similar relations to those which obtain in
Cephalodiscus, but there are no proboscis-pores and no
gill-slits.
THE PRAORAL LOBE OF ECHINODERM LARV#.
In the previous pages a good deal of stress has been
laid on the existence of a przoral lobe in the various types
considered. We have recognised it in the snout of Am-
phioxus (przeoral coelom + przeoral pit), in the proboscis
of Balanoglossus, the fixing organ of the Ascidian tadpole,
and in the buccal shield of Cephalodiscus and Rhabdo-
pleura.
From a morphological standpoint the przoral lobe is
probably one of the most important, as it is certainly one
of the oldest, structures of the body of bilateral animals,
and it becomes, therefore, a matter of the first moment to
be able to trace the modifications which it has undergone
along the different lines of evolution which have culmi-
nated in the existing types of animal life. The subject is
a very large one, and can only be treated here in its
broadest outlines.
It is now very generally admitted by zodlogists that the
Echinoderms (star-fishes, sea-urchins, etc.) owe the vadzal
symmetry, which is one of the most obvious characteristics
of their organisation, to their having been derived from
bilaterally symmetrical ancestors, which became adapted
to a fixed or sessile existence. If this view is correct,
and there is good reason for supposing that it is, it follows
that the majority of living Echingderms have secondarily
268 THE PROTOCHORDATA.
lost their sessile mode of existence, and have again become
free-living, retaining, however, their radial symmetry. At
the present time the fixed habit of life is only retained
by the members of one of the subdivisions of the Echino-
derm class ; namely, the Crznozdea.
Most genera of Crinoids (Akzzocrinus, Pentacrinus, etc.)
remain fixed by a long, jointed stalk throughout life; but
the well-known “feather-star,” <Antedon rosacea, is only
fixed during a certain period of its larval development. At
the close of the period of fixation the body of the animal,
or, as it is called, the calyx, breaks away from the stalk by
which it was attached to the rocks, and so begins to lead a
free existence, being capable of swimming vigorously by
the flapping of its arms.
Although the existing Crinoids have become extensively
modified along their particular line of evolution, yet there
is reason to believe that they represent the more im-
mediate descendants of the primzval form which ex-
changed its primitively free life and bilateral symmetry for
a sessile existence and radial symmetry. This view is
strengthened by the character of the free-swimming larva
of Antedon. This larva does not possess, in any extrava-
gant degree, those fantastic structures which are so
characteristic of other Echinoderm larvz, such as the
provisional ciliated processes or arms of the “ Pluteus”’
(larva of sea-urchins), or the undulating ciliated bands of
Auricularia.
On the contrary, the larva of Antedon is a simple
barrel-shaped organism, with regular ciliated bands pass-
ing around it (Fig. 128).
Perhaps the structure which, above all, stamps the free-
swimming larva of Antedon as having, from a phylogenetic
point of view, a more primitive type of organisation than
PRAORAL LOBE. 269
that of other Echinoderm larvz, is the well-developed
apical plate at its anterior extremity. We may express
this in other words by saying that the larva of Antedon
possesses a central nervous system at the apex of its
preoral lobe. That the pre-
oral lobe in this larva is not
sharply marked off from the
rest of the body is a detail
of no morphological signifi-
cance.
The apical nervous sys-
tem of the Antedon larva
was discovered in 1888 by
H. Bury, and has_ been Fig. 128.—Free-swimming larva of
Antedon rosacea, from the ventral side.
more clearly brought out (after servicer.)
and emphasised in a recent ap. Apical pole. cb. Ciliated bands.
/. Fixing disc. v. Vestibulum (so-called
work by Dr. OSWALD SEELI- larval mouth, although at this stage
GER At thepoint whichis ~™PY sniccodenmic groove).
marked externally by the anterior tuft of long cilia in
Fig. 129 there is a slight groove in the ectoderm below
which nerve-fibres and ganglion-cells can be identified.
Seeliger further describes a pair of longitudinal nerves
running from the nervous area of the apex along the
ventro-lateral margins of the body.
As already indicated, the apical plate is, as a general
rule, conspicuous by its absence in the typical Echinoderm
larva. In the free-swimming larva of Antedon, however,
it is emphatically present, although destined to become
entirely aborted after the fixation of the larva.
In most Invertebrate larve in which an apical plate is
present (e.g. the Trochophore-larva of Annelids and Mol-
luscs) it becomes, during the metamorphosis, involved in
other ectodermic thickenings of the przoral lobe, which
270 THE PROTOCHORDATA.
collectively give rise to the cerebral or supracesophageal
ganglion. The apical plate may thus be defined as a
primitive central nervous system at the apex of the
przoral lobe, being the forerunner and formative centre
of the cerebral ganglion of the Invertebrates.
Although, with the exception of the Crinoids, there is
no apical plate in the typical Echinoderm larva, yet, as
noted above, in many cases a curious transitory lengthen-
ing of the ectodermic cells at the apical pole has been,
and can be without great
difficulty, observed in larvze
of star-fishes and sea-urchins.
This alone would seem to
indicate the former exist-
ence of a central nervous
system at the apex of the
przeoral lobe in the bilateral
ancestor of the Echinoderms.
The way in which the
_ Fig. 129. —Larva of Asterina gibbosa, primary blastocaelic cavity
viewed as a transparent object from the
left side. (After LUDWIG.) of the przoral lobe can be
acta, Emeric evi. 1s, Lat eter- replaced by a dilatation of
coel through #./, the preeoral lobe. st. the enteroccel has been de-
ae ti scribed above, both for Tor-
naria and for the larva of Asterias vulgaris (Figs. 121-122),
In some cases, as in Asterina gibbosa, the przoral lobe is
occupied by the enteroccel from the very beginning. In the
“Pluteus” larva of the Echinids (sea-urchins) the praeoral
lobe is much reduced; but in other Echinoderms, as in
the singular larva of Asterina gibbosa, and in the so-called
Brachiolaria-larva of the Asterids (star-fishes) in general, it
is very prominent, and serves as an effective locomoton
(creeping) organ.
PRAZORAL LOBE. 271
The very interesting observation has recently been
made by MacBripg, that the larva of Asterina gibbosa
actually undergoes temporary fixation at the beginning of
the metamorphosis, the fixation being effected by the
preoral lobe in a manner strikingly similar to that of the
larvee of Antedon and of Czona.
In the larva of Antedon the adhering disc, by which the
larva eventually fixes itself to some foreign surface, is
placed near the front end of
the praeoral lobe immediately
below the apical plate.
The central nervous sys-
~ tem of the adult Echinoderm
arises in entire indepen-
dence of the actual or sup-
Suess gel ad area as Fig. 130. — Larva of Asterina gibbosa,
tem of the larva, and not at viewed as an opaque object from the left
all from the ectoderm of the coos pen ede
preoral lobe.
We have thus seen how within the limits of a single
group (viz. the Echinoderms) the przoral lobe can become
completely emancipated from the central nervous system ;
and we have further recognised the fact that whether the
cavity of the przeoral lobe is a derivative of the primary or
secondary body-cavity, whether it contains loose mesen-
chyme or is lined by an endothelium, the morphological
value of the przeoral lobe itself remains the same.
THE PRAORAL LOBE OF THE PROTOCHORDATES.
It is probable that the misunderstandings and disagree-
ments which are of such frequent occurrence among mor-
phologists with regard to the comparison of the types of
central nervous system presented respectively by the
272 THE PROTOCHORDATA.
Vertebrates and the Invertebrates, are largely due to the
failure to detect some general principle of evolution to
which that archaic structure, the przoral lobe, has been
subjected.
Nevertheless, there are many indications which point
irresistibly to the conclusion, which I have recently
brought forward, that the prime factor which must be
recognised in the evolution of the przoral lobe, from the
relations which it presents in the Invertebrates to those
which it holds in the Protochordates and Vertebrates, is
its emancipation from the central nervous system.
In the great groups of the Annelids, Molluscs, and
Arthropods, the praoral lobe (prostomium, procephalic
lobe) is essentially the seat of the brain or cerebral gan-
glion. The latter, through its representative, the apzcal
plate, is the main and often the sole element of the central
nervous system in the Trochophore-larva of Annelids and
Mollusces.*
* In speaking of the apical plate as the forerunner or formative centre of
the cerebral ganglion, it must not be assumed that these are not distinct
structures. The apical plate is essentially median and unpaired, while the
cerebral ganglion is paired. They can both, however, be included under the
general term, afical nervous system, since they arise from the ectoderm of
the preoral lobe. On the other hand, the cerebral ganglion may arise inde-
pendently of an apical plate; as, for instance, in Zzbricus, where there is
no apical plate, or in the /Vemertines, where the apical plate is discarded
together with other larval structures (Pilidium). Again, as in Lumbricus and
many other cases, the cerebral ganglion, after having separated from the
ectoderm of the przeoral lobe, may recede backwards for a considerable dis-
tance, so as not to lie in the preeoral lobe in the adult. It is possible that the
position of the cerebral ganglia of Nemertines may be accounted for by some
such phylogenetic recession from the przeoral lobe.
If necessary, it might be said that the preeoral lobe can acquire emancipa-
tion from the central nervous system by a simple recession of the cerebral
ganglion. In the case of the Protochordates, however, on the view here advo-
cated, the preeoral lobe has acquired emancipation from the central nervous
system, not by the mere recession, but by the complete disappearance of the
Invertebrate cerebral ganglion.
PREORAL LOBE. 273
At a later stage of development the longitudinal nerve-
cord (confining the description to the Annelids for the
sake of simplicity) arises zudependently of the cerebral
ganglion, from a pair of longitudinal thickenings of the
ectoderm near the mid-ventral line, becoming secondarily
connected with the cerebral ganglion by the circumcesoph-
ageal nerve-collar or commissure.
As already indicated, it seems probable, as was sug-
gested by BaLtrour and GEGENBAUR, that the ventral
nerve-cord of the Annelids is to be regarded as having
arisen phylogenetically by the mutual approximation of
two such lateral cords as occur in the Nemertines, and
like the latter may be supposed to have originated by a
concentration on the ventral side of the body of that
ptimitively continuous sub-epidermic nerve-plexus which
is such a characteristic feature of the Nemertines. From
a consideration of the adult nervous system in the
Echinoderms, Nemertines, Enteropneusta (Balanoglossus),
Annelids, and Molluscs, it is evident that such a con-
centration of nervous tissue has from first to last occurred
along very different lines.
Speaking in broad terms, it may be said that the only
portion of the Invertebrate nervous system which, in its
prime essence, is invariable and universal (due allowance
being made for exceptional cases) is the cerebral ganglion
or its forerunner, the apical plate, the seat of which lies in
the przoral lobe.?
Under these circumstances it will suffice to confine our
attention to the przoral lobe, in the belief that if an
understanding can be arrived at with regard to that impor-
tant structure, one of the chief difficulties in the way of a
just conception of the relations existing between Verte-
brates and Invertebrates will have been overcome.
274. THE PROTOCHORDATA.
Returning now to Balanoglossus, we have to remark
that in the Tornaria larva the central nervous system is
represented entirely by the apical plate of the przoral
lobe, the situation of the apical plate corresponding to the
anterior tip of the proboscis of the adult. Unlike the
Annelids, however, the apical plate of Tornaria does not
become replaced after the manner of the Invertebrates by
the development of a cerebral ganglion arising like it from
the ectoderm of the przoral lobe and with it as a formative
centre. On the contrary, it completely disappears after
the metamorphosis, having become replaced physiologically
by the development of the medullary tube in true Verte-
brate fashion from the dorsal ectoderm of the collar-region
behind the przeoral lobe.*
In the Ascidian larva, however, and in Amphioxus, the
characteristic Invertebrate apical nervous system no longer
appears in any stage of development, its physiological func-
tion having been once for all assumed by the medullary
tube (cerebral vesicle + spinal cord) which lies par excel-
lence behind the preoral lobe (Fig. 131).
Anterior and Posterior Neurenteric Canals, and the
Position of the Mouth in the Protochordates.
After the postoral medullary tube had led indirectly to
the complete obliteration of the praoral apical nervous
system, and had attained to such a degree of development
as we find, for instance, in the Ascidian tadpole, the central
canal of the cerebro-spinal nervous system appears to
have acquired remarkable relations with the alimentary
canal. At both ends of the body connecting ducts be-
* For a detailed account of the formation of the medullary tube in the col-
lar-region of Balanoglossus see MORGAN (Bibliography, Nos. 124 and 125).
PRAORAL LOBE. 275
came established between the nervous and digestive
systems, known respectively as the azterior and posterior
neurenteric canals.
The posterior neurenteric canal is only of transitory
occurrence in all existing Vertebrates, and leads from the
rel a m we ne ue
=
ina
Th A ih wt
an fi
hy vil
I
mt
LAU Ti
1
Viiitiaen
Site ue au! war
ia
a CULAR tint!
Fig. 131.— Diagrammatic representations of the anterior region of the body
in (A) an Ascidian larva, (8) larva of Amphioxus, and (C) Balanoglossus.
(After WILLEY.)
The figure of Balanoglossus was compiled from Bateson’s figures; the pro-
boscis-pore is indicated rather too far forwards.
p.2. Preoral lobe (fixing organ, snout, proboscis). ed. Endostyle. #.f. Praoral
pit or proboscis-pore. #. Mouth. 2p. Neuropore. zc. Medullary tube. ch. Noto-
chord. e. Eye. of. Otocyst. g/, and #. Proboscis-gland and proboscis-heart of
Balanoglossus
270
Fig. 132. — Sagitta hexaptera from the
ventral surface ; nearly three times natural
size. (After O. HERTWIG.)
a. Anus. Jécl. Head-cavities. c?.
Trunk-ceelom. 4c3, Caudal ccelom. c./.
Caudal septum. com. Commissure, from
the cerebral ganglion to the single ventral
ganglion, 7/1, /2, f8. Fins. m. Mouth.
o.a. Oviduct. ov. Ovary. spf. Prehen-
sile bristles. s.v. Seminal vesicle. #, Tes-
tis. v.g. Ventral ganglion.
THE PROTOCHORDATA.
neural tube into the extreme
posterior end of the aliment-
ary canal; in fact, into that
portion of it which, in the
embryos of the higher forms,
is known as the post-anal
gut. The anterior neuren-
teric canal, in its most primi-
tive condition, opens into the
base of the buccal tube
(Eugene 1)
On this account we find
in the Ascidian tadpole that
the mouth is no longer ven-
tral, as it isin Balanoglossus,
but is placed dorsally, im-
mediately in front of the
anterior extremity of the
This in-
timate relation between the
medullary tube.
mouth and the central ner-
vous system gives a reason
for the contrast between the
dorsal position of the mouth
in the Ascidian tadpole and
its ventral position in Bala-
noglossus.
In Amphioxus we have
seen that the mouth has been
forced aside from its more
primitive dorsal position by
the forward extension of the
notochord to the tip of the
PREORAL LOBE. 277
preeoral lobe. The origin of the main cavity of the pre-
oral lobe in Amphioxus from the right of a symmetrical
pair of head-cavities (anterior intestinal diverticula of
Hatschek) has been described in a previous chapter. In
Balanoglossus there is no such complete division of the
preeoral body-cavity, but it is throughout a single space,
its right and left halves being confluent. If we now com-
pare the condition of things in the embryo of Amphioxus,
where we have a symmetrical pair of head-cavities, with
that of some other form which, in the adult condition,
possesses a distinct pair of such cavities, it may assist us
in imagining how the mouth could have assumed such
opposite relations as have been mentioned above.
But first it may be pointed out that in Appendicularia,
where, as it would appear, in correlation with the second-
ary acquirement of a purely pelagic habit of life (although
this point of view is not shared by such authorities as
Herdman, Seeliger, and Brooks), the praoral lobe has
been reduced to a minimum, or to zero, the mouth has
thereby come to lie in a terminal, or sub-terminal, position,
with a slight tendency towards the dorsal side.*
In the curious pelagic worm, Sag7tta, we meet with
another instance of an animal in which the przoral lobe,
in the ordinary sense of the term, is reduced to a mini-
mum, and the mouth has therefore a sub-terminal position,
with a ventral inclination (Fig. 132). But although there
is no distinct przoral lobe in Sagitta, there is, neverthe-
less, a patr of head-cavities, which are directly comparable,
if not perfectly homologous, with the above-mentioned
* Whatever the truth may be as to the precise systematic position and
phylogenetic value of Appendicularia, one thing, to my mind, remains abso-
lutely certain, namely, that it has descended from a form which possessed a
preoral lobe, and that it has secondarily lost that structure.
278 THE PROTOCHORDATA.
head-cavities of Amphioxus, although they have a some-
what different origin.
It should not be forgotten that Sagitta occupies a very
isolated position in the zodlogical system, being placed in
a group by itself, the Chetognatha, and that therefore the
peculiarities of its organisation cannot be taken as repre-
senting any definite intermediate stage in the phylogeny
of other forms, yet, from a general standpoint, the con-
ditions which it presents in its life-history are highly
instructive.
The head-cavities of Sagitta arise by constriction from
the anterior extremities of the single pair of archenteric
pouches which give rise to the ccelom of the adult. They
remain distinct and separate on either side of the head
throughout life. If, now, we imagine them to grow for-
ward and fuse together in front of the mouth, in a simi-
lar manner to that described above for the enteroccelic
pouches of Asterias, we should have a przoral body-cavity
of a similar character to that of Balanoglossus.
Now, the ultimate position of the mouth under these
new conditions would depend upon circumstances affect-
ing the whole organisation of the animal.
In an animal whose grade of organisation was on an
approximate level with that of Sagitta the mouth would
undoubtedly remain on the ventral side of the body. But
in an animal whose organisation had reached the stage
of evolution represented by that unknown ancestor of
Amphioxus (most nearly represented at the present time
by the Ascidian tadpole), whose notochord did not extend
beyond the anterior limit of the neural tube, the mouth
would pass to the dorsal side of the body to come into
connexion with the neural canal.
PRA(ORAL LOBE. 279
THE PRAORAL LOBE IN THE CRANIATE VERTEBRATES.
After what has been said above, in this and the preced-
ing chapters, the question as to how the przoral lobe is
represented in the craniate Vertebrates need not detain us
long.
Since, as shown above, the nervous element of the prez-
oral lobe (apical plate and cerebral ganglion) is entirely
lacking in the Vertebrates, we can only expect to find the
mesodermal element represented in the head-cavities of
the higher forms.
In consequence of the great development of the brain,
even in the lowest craniate Vertebrates, as compared with
Amphioxus, and in consequence too of the cranial flexure,
the head-cavities have been made to assume a more sub-
ordinate position, and no longer take part in the formation
of a prominent lobe in front of the body. This is a perfect
illustration of “le principe du balancement des organes”’
of Geoffroy Saint-Hilaire, the przeoral lobe decreasing as
the brain increases. A comparison between Figs. 70,
72, 117, and 135 will show at once that the przoral head-
cavities of Amphioxus and Balanoglossus are the homo-
logues of the premandibular head-cavities of the craniate
Vertebrates.
These cavities lie at first below the mid-brain, and later
their walls give rise to most of the eye-muscles. In Figs.
gt and 135 the median portion of the pramandibular
cavities can be seen still in the form of an anterior pocket
of the endoderm, and it may be noticed how far it is
removed from the anterior extremity of the body to which
it extends in Amphioxus, etc. In the craniate Verte-
brates the brain extends forwards, and the head-cavities
ic}
280 THE PROTOCHORDATA.
remain behind. This is, as we should expect, the exact
reverse to what obtains in Amphioxus.
In connexion with the evolution of the przoral lobe,
we thus have an excellent example of repeated change of
function.
We may conclude, therefore, that the przoral lobe,
which, in the /zvertebrates, is above all the bearer of the
cerebral ganglion, and in the Protochordates is released
from this function and becomes in part a locomotor
(Balanoglossus, Cephalodiscus) fixing (Ascidian) and bur-
rowing (Amphioxus) organ, is represented in the craniate
Vertebrates by the premandibular head-cavities, whose
walls give rise to most of the eye-muscles,
THE MOUTH OF THE CRANIATE VERTEBRATES.
In consequence of the increase in the size of the brain,
its forward extension and its cranial flexure, together with
the relative reduction of the head-cavities, it is obvious
that the mouth has been carried round from its primitively
dorsal position to its final position on the ventral side of
the head in the craniate Vertebrates. (Cf. Fig. 91.) This
would have been all that need be said about the mouth
were it not for the fact that the view, originally started by
Donrn, that the Vertebrate mouth was a new formation
resulting from the fusion of two gill-slits, has received such
wide support and still in a measure holds its own.
Since the Annelid mouth perforates the central nervous
system in passing through the circumcesophageal nerve-
collar, it was necessary to frame a theory which would
get over the difficulty that nothing of the kind occurs in
the Vertebrates. Accordingly Dohrn supposed that the
old Annelid mouth had become aborted, and was replaced
MOUTH. 281
by a new mouth derived from a fusion across the mid-
ventral line of a pair of gill-clefts. DoHRN was a trifle
uncertain as to the rudiment of the old mouth, but BEARD
was more certain on this point, and thought he had estab-
lished the fact that the hy-
pophysis cerebri represented
the remains of the old An-
nelid mouth.
Dohrn certainly succeeded
in bringing forward some
apparently good evidence in
support of his theory of the
gill-slit origin of the mouth.
This evidence was derived
from the study of the de-
velopment of the mouth in
Teleostean or bony fishes.
In many Teleosteans the
mouth has at first an appar-
ently double origin, in that
two separate ectodermal in-
growths occur which fuse
with the endoderm, instead
of the median stomodceal
involution which is so char-
acteristic of other Verte-
brates. This double origin
Fig. 133. — Two frontal views of an
embryo of Batrachus tau, to show the
double nature of the stomodceum. (From
hitherto unpublished drawings kindly lent
by Miss C. M. CLAPP.)
The embryo is lying upon the yolk,
and the septum which divides the stomo-
dceum passes from the upper lip to the
surface of the blastoderm which covers
the yolk. The lower figure is a drawing
of the same embryo as the upper, a few
hours later. Above the stomodceum are
seen the small nasal pits (rudiments of
the external nares), and at the sides of
the head are the rudiments of the eyes.
of the mouth is particularly
well shown in the embryos of the remarkable toad-fish,
Batrachus tau, as observed by Miss CorNELIA CLAPP at
the Marine Biological Laboratory of Woods Holl, Mass.,
in 1889 (Fig. 133). In this case the mouth-cavity is seen
to be divided into two halves by a median septum.
Subsequently the septum becomes absorbed, and the
282 THE PROTOCHORDATA.
two halves of the mouth coalesce. In view of the pre-
vious existence of the gill-slit theory of the mouth, some
such theory being a necessary accessory to the Annelid-
theory, it is not surprising that this undoubted double
origin of the mouth in Teleosteans should be regarded as
a striking confirmation of Dohrn’s hypothesis. And yet,
occurring as it does only in the Teleosteans, whose devel-
opment is admittedly in many respects highly modified,
the interpretation which Dohrn and his followers have
placed upon this observation must always have been open
to doubt. The simplest explanation of the double origin
of the Teleostean mouth is that, owing to certain condi-
tions (possibly mechanical) of development, the two angles
of the mouth develop before the median portion. This is
the conclusion which H. B. PoLuarp has also reached in
his recent studies on the development of the head in the
Teleostean fish, Godzus capito.
According to the standpoint I have adopted in the fore-
going pages, there is no a friorz reason for doubting that
the Vertebrate mouth is completely homologous with the
Protochordate mouth; and that the latter in its turn is
the direct descendant of the typical Invertebrate mouth.
Again, the anatomy and development of the Protochor-
dates and of the Cyclostomi (Ammoccetes) show no indica-
tion whatever of a discontinuity in the evolution of the
most highly elaborated mouth of the gnathostomous or
jawed Vertebrates.
We conclude, therefore, that the ventral mouth of the
craniate Vertebrates is the homologue of the primordial
dorsal mouth as we find it in the Protochordates, and that
its direction of evolution has been, as was so ably main-
tained by BaLFour, from the cyclostomous to the gnatho-
stomous condition.
HYPOPHYSIS. 283
SIGNIFICANCE OF THE HYPOPHYSIS CEREBRI.
The pituitary body, or hypophysis, belongs to the series
of ductless “glands” (pineal body, thyroid gland, thy-
mus, etc.) which are such a characteristic feature of the
vertebrate organisation. It arises as an ectodermal invo-
lution from the roof of the stomodceum, directed towards
the base of the primary fore-brain, from which the infun-
dibulum grows out.
The pituitary involution becomes in most forms nipped
off from the stomodceum, and then les as a closed sac
in contiguity with the infundibulum. Later on it produces
a system of branches, the lumina of which tend to dis-
appear; and in some forms (e.g. Mammalia) it undergoes
actual fusion with the infundibulum.
The very constant relation of the hypophysis to the
infundibulum in the craniate Vertebrates (see Fig. 134)
naturally led to the supposition that there must originally
have been a functional connexion between the two struct-
ures of a similar nature to that which exists between the
olfactory pit and neuropore in Amphioxus. Recent re-
searches, however, have rendered it probable that such a
supposition is erroneous. VON KupFFER has discovered
the homologue of the lobus olfactorius of Amphioxus in
the craniate Vertebrates, and has shown that it occurs at
a point far removed from the infundibular region.
Until recently it was also very generally thought that
the infundibulum represented the anteridr end of the
brain, which had become bent downwards and backwards
by the cranial flexure. Kupffer, however, has brought for-
ward weighty reasons for doubting this view. According
to him, the infundibulum is essentially a downgrowth or
284 THE PROTOCHORDATA.
evagination from the floor of the brain, occurring behind
the anterior terminal extremity of the brain.
It follows that the morphological anterior extremity of
the craniate brain coincides with the median Jobus olfac-
torius tmpar, which also represents the point of last con-
nexion of the medullary tube with the superjacent ecto-
derm. The lobus olfactorius impar lies in the anterior
vertical wall, which forms the boundary of the primary
fore-brain in front, known as the /amzna terminalis. RABL-
RUCKHARD has also observed the median olfactory lobe in
Fig. 134. — Sagittal section through the head of an embryo of Acanthias..
(After RABL-RUCKHARD.)
a.c. Position of anterior commissure. a/. Alimentary canal. cer. Cerebellum.
ch, Notochord; the black shading below the notochord indicates the aorta.
fo. Fore-brain. 4.6. Hind-brain. Ay. Hypophysis, already shut off from the
stomodceum and lying as a closed sac at the base of zzf the infundibulum.
Zo. Lobus olfactorius. . Mouth. m.é. Mid-brain. o.c. Optic chiasma. £.d.
Pineal body (epiphysis).
the Selachian embryo (Fig. 134), and it has since been
found by BurRCKHARDT in other forms.
It can thus hardly be doubted that the median rudi-
mentary olfactory lobe of the embryos of the higher
Vertebrates is homologous with the lobus olfactorius of
Amphioxus (Fig. 51), and, like the latter, represents the
remains of the neuropore. In Amphioxus, however, the
HMPOPHYVSIS, 285
olfactory lobe abuts against the olfactory pit, and, in fact,
in young individuals opens into it by the neuropore
(Fig. 45).
On the view which I have urged above, that the
olfactory pit of Amphioxus is homologous with the
hypophysis cerebri of the craniate Vertebrates, it must
be assumed that in the latter forms, the neuropore hav-
ing ceased to be in any way a functional organ, the hy-
pophysis, which has likewise become (morphologically) a
vestigial structure, has been mechanically separated from
the neuropore, with which it was primitively in functional
connexion. It must be supposed that this separation of
the hypophysis from the neuropore has been effected by
the more rapid downward growth of the ectoderm (from
which the hypophysis arises) than of the wall of the brain,
so that the hypophysis has been carried farther round to
the lower side of the head than the neuropore (Fig. 135).
The reason for this unequal growth of the external body-
wall and of the cerebral wall may, perhaps, be sought for
in the great and independent increase in the cubical con-
tents of the brain.®
We thus arrive at the conclusion that the present
relation of the hypophysis to the infundibulum in the
craniates, however intimate it may be in some cases, is,
nevertheless, incidental and secondary.
That this conclusion is not so strained as might appear
at first sight is clearly shown by the fact that the in-
fundibulum is not the only structure with which the
hypophysis enters into close relations.
In the exceptional cases of Myxine and Bdellostoma,
for instance, the distal end of the hypophysis has nothing
to do with the infundibulum, but actually opens into the
pharynx. In these hag-fishes, as also in the lamprey
286 THE PROTOCHORDATA.
(where there is no internal opening of the hypophysis
into the pharynx), the external opening of the hypophysis
does not close up, as in the higher forms, but persists
throughout life, becoming carried round to the top of
the head during the embryonic development by differ-
ential growth of neighbouring parts, as has been actually
observed in Petromyzon.
ee ae
Ear mBNNcECCOOIOGO aca LET DRG Re
QE ON 逢
Sil SNON
Y
Tere ceOceJOCOOOOOGOG gaa MM e SONON ii
OFA \e\\e)
ci IN KA i) Ue, ay
InN SN 5
Ys 3
a S Ze e
oe peat OMS,
ahepretoeae foe <
Gs ees
Fig. 135.— Median sagittal section through the head of young Ammoceetes.
(After KUPFFER.)
The arrow indicates the extent to which the hypophysis has been (hypothetically)
removed from the neighbourhood of the neuropore (lobus olfactorius impar).
ch. Notochord. ec. Ectoderm. ez. Endoderm. ef. Epiphysis. Ay. Hypo-
physial involution. 7.0. Lobus olfactorius impar. 7. Nasal involution. pm. Me-
dian portion of praemandibular cavity. st Stomodceum. /.4/.H. Primary fore-
mid-, and hind-brain.
In other cases, as, for example, in the embryo of the
rabbit, it has been observed that the hypophysis actually
undergoes a temporary fusion with the front end of the
notochord; and in all cases the distal end of the hypophysis
grows inwards as much towards the notochord as towards
the infundibulum, so that for the embryonic stages of the
craniate Vertebrates it might be said that the relations of
HYVPOPHYSITS. 287
the hypophysis to the front end of the notochord are as con-
stant as its relations to the infundibulum. So close is the
apparent relation of the hypophysis to the notochord that
at least one zoologist, HUBRECHT, has suggested that there
was originally a functional connexion between the two
structures.
Again, in the embryo of Aczpenser, the sturgeon, as
shown by KuprFrer, the distal end of the hypophysis
undergoes temporary fusion with the subjacent wall of
the alimentary cavity. In spite of the extremely modified
character of the embryo of Acipenser (the embryo being
flattened out like a disc over the yolk), Kupffer regards
this fusion of the hypophysis with the endoderm as being
of great morphological significance.
On the contrary, for the reasons mentioned above, I
would regard all these fusions of the hypophysis in the
craniate Vertebrates, whether with the infundibulum,
notochord, or endoderm, as being of an entirely incidental
character, often due, perhaps, to a tendency of such con-
tiguous embryonic tissues to fuse together.
I therefore suggest that: Zhe hypophysis arose in con-
nexton with a functional neuropore ; when the neuropore
ceased to be functional, there was no longer any bond of
union between its tuner portion, which opened into the
cerebral cavity, and its outer portion, which opened into the
buccal cavity; and these two portions became separated by
differential growth of the cerebral and body-walls (cf. Fig.
135).
The Ascidian Hypophysts.
The development of the hypophysis in a typical As-
cidian, its constriction from the wall of the cerebral
vesicle in the form of a tube, and its opening into the
288 THE PROTOCHORDATA.
buccal cavity, or branchial sac, have been described above.
The most serious objection which has been raised against
the comparison of the hypophysis of the Ascidians with
that of the craniate Vertebrates is, that in the former
the hypophysis opens, not at an ectodermal surface into
the stomodceum, but at an endodermal surface (behind the
stomodceum) into the branchial sac. This is undoubtedly
the case in some Ascidians, e.g. Distaplia, and probably
also in Clavelina, etc. In Czona, however, as I can state
after renewed study of the question, it apparently opens at
first into the buccal cavity precisely in the line of junction
between the stomodoeum and the branchial sac, so that its
upper margin is continuous with the stomodceal epithelium,
while its lower margin is continuous with the epithelium
of the branchial sac.
It is probable that too much stress has been laid on the
question whether the hypophysis of the Ascidians opens
at an endodermic or at an ectodermic surface, and that
thus the attention has been diverted from the essential
fact that the hypophysis opens into the buccal tube at the
entrance to the branchial sac. In the case of the Ascid-
ians, therefore, I should also regard the fusion of the
hypophysis, whether with the ectoderm of the stomodceum
or with the endoderm of the branchial sac, as being in
itself non-essential, while the actual opening of the hy-
pophysis (itself derived by constriction from the nerve-
tube) into the buccal cavity, apart from the question of an
ectodermal or endodermal surface, is the essential point.
CONCLUSION. 289
CONCLUSION.
From the facts that have been recorded and the consid-
erations that have been urged in these pages, it would
follow that one of the chief factors in the evolution of the
Vertebrates has been the concentration of the central
nervous system along the dorsal side of the body (in
contrast to the position of the longitudinal nerve-cord of
Annelids, etc., along the ventral or /ocomotor surface), and
its conversion into a hollow tube. If it be admitted that
the hypophysis became evolved in connexion with a func-
tional neuropore, it 1s obviously a structure which has
arisen within the limits of the Vertebrate phylum, and can,
therefore, have no representative in the typical Invertebrate
organisation. It has been suggested by ADAM SEDGWICK
and vAN WiHE that the original function of the central
canal of the spinal cord was to promote the respira-
tion (oxygenation) of the tissue of the central nervous
system, water entering by the neuropore, and passing out
through the posterior neurenteric canal. |
It is not so easy to form a conception as to the prime
origin of the other two cardinal characteristics of a
Vertebrate (Chordate); namely, gill-slits and notochord.
As to the origin of gill-slits, it has been suggested inde-
pendently by HarMeErR and Brooks, that they arose at first
not so much to perform the direct function of respiration,
as to carry away the bulk of the water which constantly
entered the mouth with the food, so as to avoid the neces-
sity and discomfort of the never-ceasing flow of water
through the entire length of the alimentary canal. In
Cephalodiscus, for example, the luxuriant branchial plumes
must be sufficient for the respiration of the minute animal,
290 THE PROTOCHORDATA.
while the usefulness of the pair of gill-slits, in allowing the
surplus water to pass out of the pharynx, is evident.
The notochord is more difficult to explain, and the fact
of its occurrence in the proboscis of Balanoglossus and
in the tail of the Ascidian tadpole is very puzzling. The
mode of its occurrence in Balanoglossus is undoubtedly
divergent, and not in the direct line of Vertebrate. descent.
It is possible that the notochord has not arisen through a
process of elaborate change of function from a pre-existing
structure, but simply as a solidification of the endoderm
which was continued into the caudal or post-anal extension
of the body to form the axial support for a locomotor tail ;
while the subsequent extension of the notochord into the
pree-anal region of the body is not difficult to understand.
The general capacity of the endoderm for producing
skeletal tissue is already present in some of the Medusze
and Hydroid polyps whose tentacles are stiffened by a
solid endodermal axis.
From a purely morphological point of view it now
seems as though the przoral lobe and in a lesser degree,
perhaps, the hypophysis, would materially assist in furnish-
ing the key to a correct appreciation of the relationship
between the craniate Vertebrates, the Protochordates,
and the Invertebrates.
As we have indicated above, in the formulation of the
Annelid-theory* no allowance has been made for the prin-
ciple of parallelism in evolution; but it is impossible to
doubt that this is a very potent factor which should always
be borne in mind in estimating the genetic affinity between
widely different groups of animals. The closer the super-
ficial resemblance between an Annelid and a Vertebrate
(in the possession of somites, segmental organs, etc.) is
shown to be, the more perfect appears the parallelism
CONCLUSION. 291
in their evolution and the more remote their genetic
affinity.
For the present we may conclude that the proximate
ancestor of the Vertebrates was a free-swimming animal
intermediate in organisation between an Ascidian tadpole
and Amphioxus, possessing the dorsal mouth, hypophysis,
and restricted notochord of the former; and the myo-
tomes, coelomic epithelium, and straight alimentary canal
of the latter. The ultimate or primordial ancestor of the
Vertebrates would, on the contrary, be a worm-like animal
whose organisation was approximately on a level with
that of the bilateral ancestors of the Echinoderms.
NOTES.
I. (p. 246.) For the discussion of the phenomena of meta-
merism and the enumeration of examples of independent metameric
repetition of parts, consult the following: Lanc, ARNoLp. Der
Bau von Gunda Segmentata und die Verwandtschaft der Plathel-
minthen mit Calenteraten und Hirudineen. Mitth. Zool. Stat.
Neapel, Bd. III. 1882. p.187 e¢ seg. SEDGWICK, ADAM. On
the Origin of Metameric Segmentation, and Some Other Mor-
phological Questions. Quarterly Jour. Micro. Sc. XXIV. 1884.
pp- 43-82. Bareson, WituiaM. Zhe Ancestry of the Chordata.
Quarterly Jour. Micro. Sc. XXVI. 1886. pp. 535-571. CaLD-
WELL, H. Slastopore, Mesoderm, and Metameric Segmentation.
Quarterly Jour. Micro.Sc. XXV. 1885. pp. 15-28. HuUBRECHT,
A. A.W. Report on the Nemertea collected by H. M.S. Challenger,
1873-76. Chall. Rept. Zool. XIX. 1886. (Also, HuBrecurt.
The Relation of the Nemertea to the Vertebrata. (Quarterly Jour.
Micro. Sc. XXVII. 1887. pp. 605-644.) VAN BENEDEN,
Epouarp. Recherches sur le Développement des Arachnactis.
Contribution a la Morphologie des Cérianthides. Archives de
Biologie, XI. 1891. pp. 115-146. Also consult the recent
great work of Bateson, Materials for the Study of Variation.
London, 1894.
292 THE PROTOCHORDATA.
2. (p. 273.) On the subject of the preoral lobe and the api-
cal nervous system of Invertebrates, see the following: BaLrour,
F. M. Comparative Embryology. 1881. Vol. II. Chap. 12.
Observations on the Ancestral Form of the Chordata. Brarv,
J. Zhe Old Mouth and the New, A Study in Vertebrate Mor-
phology. Anat. Anz. III. 1888. pp. 15-24. Witson, E. B.
The Embryology of the Earthworm. Jour. Morph. III. 1889.
pp. 337-462. HarscHeKk, B. Lehrbuch der Zoologie. 3d Liefer-
ung. Jena,1891. Wiutiey, A. Ox the Evolution of the Preoral
Lobe. Anat. Anz. IX.* 1894. pp. 329-332.
3. (p. 285.) From what has been said in the text, it is obvious
that the hypophysis of the craniate Vertebrates, in becoming
separated from the neuropore, has retained (at least in the embryo)
its primitive relations with the buccal cavity, and, like the latter,
has been made to assume its present position in consequence of
the forward growth of the brain and the ensuing cranial flexure.
In Amphioxus, the hypophysis (7.e. olfactory pit) arises as an
ectodermic involution immediately over the neuropore, but still
independent of the latter. In other words, the neuropore exists
in Amphioxus for a considerable length of time before the hypoph-
ysis forms ; and this is in accordance with what we should expect
from the analogy of the craniate Vertebrates. In the Ascidians,
however, the conditions are somewhat different, and there is at first
no such obvious differentiation between neuropore and hypoph-
ysis. For the simple Ascidians (e.g. Ciona) it must at present
remain doubtful whether the increase in size of the hypophysis
takes place entirely by interstitial growth, or whether there is any
ingrowth from the wall of the buccal tube at the lips of the aper-
ture (dorsal tubercle) of the hypophysis. In any case there are
not wanting indications in the Ascidians of a distinction, and even
separation, between the distal portion of the hypophysis, which
at first opens into the cerebral vesicle, and the proximal portion,
which opens into the buccal cavity. In the adult, the proximal
portion of the hypophysis has the form of a simple duct, opening
by the so-called dorsal tubercle into the buccal cavity, while the
subneural gland arises as a proliferation from the ventral wall of
the distal portion. In Phallusia mammillata, as was discovered ~
by Juuin (Archives de Biologie, WI. 1881. pp. 211-232), num-
NOTES. 293
bers of secondary tubules grow out from the principal duct of the
hypophysis, and acquire ciliated funnel-like openings into the
peribranchial chamber ; subsequently HErpMaNn (Proc. Roy. Soc.
Edinburgh, XII. 1882-84. p. 145) found that in this form the
dorsal tubercle, or opening of the hypophysis into the buccal cavity,
is sometimes absent. In Crona intestinalis | have found in young
individuals an obliteration of the lumen of the hypophysis between
the proximal and the distal portions. In other cases, as in Afppen-
dicularia, the glandular portion of the hypophysis may be reduced
or absent.
On the subject of the Ascidian hypophysis, the following papers
should also be consulted : SHELDON, LiniAn. Vote on the Ciliated
Pit of Ascidians and its Relation to the Nerve-ganghon and So-
called Hypophysial Gland. Quarterly Jour. Micro. Sc. XXVIII.
1888. pp.131-148. Hyort, JoHan. Ueber den Entwicklungs-
cyclus der Zusammengesetsten Ascidien. Mitth. Zool. Stat. Neapel,
X. 1893. pp. 584-617. Mercatr, Maynarp M. Zhe Eyes and
Subneural Gland of Salpa. Baltimore, 1893. (Published as
Part IV. of Professor Brooks’s Monograph of the Genus Salpa.)
4. (p. 290.) The most complete presentation of the Annelids-
theory is contained in the classical Monographie der Cafpitel-
liden des Golfes von Neapel, by Dr. Huco Ersic. It is needless
to add that this monograph will command the gratitude and
admiration of zodlogists to the end of time.
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REFERENCES:
INTRODUCTION.
Carus, J. Victor. Geschichte der Zoologie. Miinchen, 1872.
DoOHRN, ANTON. Der Ursprung der Wirbelthiere und das Prin-
cip des Functionswechsels. Leipzig, 1875.
HAECKEL, ERNST. Anxnthropogenie oder Entwickelungsgeschichte
des Menschen. Leipzig, 1874; 4th Edit., 1891.
LANKESTER, E. Ray. Article “Vertebrata.” Encycl. Brit.,
gth Edit. Republished in “ Zoodlogical Articles,” London, 1891.
PERRIER, EDMOND. La Philosophie Zoologigue avant Darwin,
2d Edit. Paris, 1886.
SEMPER, CARL. De Verwandtschafisbeziehungen der gegheder-
ten There. Parts I. toIII. Wiirzburg, 1875-76.
I. AND II.
ANATOMY OF AMPHIOXUS.*
ANDREWS, E. A. The Bahama Amphioxus (preliminary ac-
count). Johns Hopkins University Circulars, Vol. XII. p. 104.
June, 1893.
ANDREWS, E. A. An Undescribed Acraniate: Asymmetron
lucayanum. Studies from the Biol. Lab. Johns Hopkins Uni-
versity, Vol. V. No. 4. 1893. pp. 213-247. Plates XIII.-
XIV.
Contains bibliography of systematic and faunistic works on
Amphioxus.
ANTIPA, GR. Ueber die Beziehungen der Thymus zu den soge-
nannten Kiemenspaltenorganen bet Selachiern. Anat. Anz.
VII. 1892. pp. 690-692. One figure in text.
* This bibliography does not by any means include all that has been written
on the anatomy of Amphioxus. Some of the older and shorter works, as well
as some of those relating to special points of histological detail, have been omitted,
as they are fully dealt with in many of the memoirs here cited.
295
296
| fe)
1
12
8.
14
15
16
17
18
19
20
REFERENCES.
BALFourR, F. M. A Preliminary Account of the Development of
the Elasmobranch Fishes. Quarterly Jour. Micro. Sc. XIV. N.S.
1874. pp. 323-364. Plates 13-15.
Paper in which Balfour first published his discovery of the seg-
mental origin of excretory tubules. This was made out also in the
same year by Semper and. Schultz. (Vide infra, Schultz.)
BALFour, F. M. On the Origin and History of the Urino-
genital Organs of Vertebrates. Jour. of Anat. and Physiol. X.
1875. pp. 17-48. Eight figures in text. Amplification of his pre-
vious work, with bibliography up to date.
BALFour, F. M. The Development of Elasmobranch Fishes.
Development of the Trunk. Jour. of Anat. and Physiol. XI.
1876. pp. 128-172. Plates 5 and 6. First account of origin of
paired limbs from continuous epiblastic thickenings.
BALFour, F. M. A Monograph on the Development of Elasmo-
branch Fishes. London, 1878.
BEDDARD, FRANK EvERS. Ox the Occurrence of Numerous
Nephridia in the Same Segment in Certain Earthworms, and on
the Relationship between the Excretory System in the Annelida and
in the Platyhelminths. Quarterly Jour. Micro. Sc. XXVIII. N.S.
1888. pp. 397-411. Plates 30-31. Contains discovery of neph-
ridial network in Pericheta.
BENHAM, W. BLAXLAND. The Structure of the Pharyngeal
Bars of Amphioxus. Quarterly Jour. Micro. Sc. XXXV.N.S.
1893. pp. 97-118. Plates 6-7.
BOURNE, ALFRED GIBBS. Contributions to the Anatomy of
the Hirudinea. Quarterly Jour. Micro. Sc. XXIV. N.S. 1884.
pp- 419-506. Plates 24-34.
Contains discovery of nephridial network in Pontobdella.
BOvERI, THEODOR. Ueber die Niere des Amphioxus. Miin-
chener Medicin. Wochenschrift. No. 26. 1890. Sep. Abd.
pp. I-13. Two figures in text. (Preliminary note.)
BOVERI, THEODOR. Die Mierencandalchen des Amphioxus. Ein
Beitrag zur Phylogenie des Urogenitalsystems der Wirbelthiere.
Zoolog. Jahrbiicher. Abth. fiir Morphol. V. 1892. pp. 429-510.
Taf. 31-34 and five figures in text.
Costa, O. GABRIELE. Cenni zoologict ossia descrizione som-
maria delle specie nuove adi aninrali discoperti in diverse contrade
del regno nell’ anno 1834. Napoli, 1834. See also Fauna del
regno di Napoli. 1839-50.
CuENoT, L. Etudes sur le sang et les glandes lymphatiques
dans la série animale. Archives de zool. expérimentale, XIX.
1891. Amphioxus. pp. 55-56.
iS)
ta
23
24
25
26
27
28
‘29
REFERENCES. 297
Notes absence of blood-corpuscles in Amphioxus. Those
described by previous authors must therefore require another ex-
planation.
DOHRN, ANTON. Studien zur Urgeschichte des Worbelthier-
korpers. IV. Section 5. Entstehung und Bedeutung der Thymus
der Selachier. Mitth. Zool. Stat. Neapel. V. 1884. pp. 141-151.
Taf. 8. Figs. 1 and 2.
E1sic, HuGco. Die Segmentalorgane der Capitelliden. Mitth.
Zool. Stat. Neapel. I. 1879. pp. 93-118. Taf. IV.
Discovery of numerous nephridia in single segments and an-
astomoses between successive nephridia.
EMERY, CARLO. Le specie del genere Fierasfer nel Golfo di
Napoli. 2d Monograph in the “ Fauna und Flora des Golfes von
Neapel.” Leipzig, 1880.
EMERY, CARLO. Zur Morphologie der Kopfniere der Teleostier.
Biologisches Centralblatt, I. 1881. pp. 527-529. See also
Zoologischer Anzeiger, VIII. 1885. pp. 742-744.
FuSARI, ROMEO. Settrag zum Studium des peripherischen
Nervensystems von Amphioxus lanceolatus. Internationale Mo-
natsschrift fiir Anatomie und Physiologie, VI. 1889. pp. 120-140.
Taf. VII.-VIII.
GoopsIR, JOHN. Ox the Anatomy of Amphioxus lanceolatus.
Transactions of the Royal Society of Edinburgh, Vol. XV. Part I.
1841. pp. 241-263.
GRENACHER, H. Settradge zur nahern Kenntniss der Muscu-
latur der Cyclostomen und Leptocardier. (Leptocardia proposed
by Haeckel as a classificatory name on account of the simple
tubular “heart” of Amphioxus.) Zeitschr. fiir Wiss. Zoologie,
XVII. 1867. pp. 577-597. Taf. XXXVI. First isolation of
muscle-plates of Amphioxus.
GUNTHER, ALBERT. Synopsis of Genus Branchiostoma. In
Report on Zool. Collections of H. M.S. Alert. 1881-82. pp. 31-
33. London, 1884. ;
HATSCHEK, BERTHOLD. Die Metamerie des Amphioxus und
des Ammocetes. Verh. Anat. Gesellschaft, 6th Versammlung.
Wien, 1892. pp. 137-161. Eleven figures in text.
29 61s. HATSCHEK, BERTHOLD. Zur Metamerie der Wirbelthiere.
- 30
Anat. Anz. VII. Dec. 1892. pp. 89-91.
Hux ey, T. H. Preliminary Note upon the Brain and Skull
of Amphioxus lanceolatus. Proceedings of the Royal Society,
XXIII. 1874. pp. 127-132.
Points out that in Myxine and Ammoceetes a velum is present
separating the buccal (stomodceal) from the branchial cavity.
298
31
32
33
34
35
36
37
38
REFERENCES.
The resemblance of the buccal cavity and tentacles (cirri) of
Ammoceetes to the corresponding parts in Amphioxus is so close
that there can hardly be any doubt the two are homologous. The
anterior end of the nerve-tube of Amphioxus corresponds to the
lamina terminalis of the craniate Vertebrates.
Huxtey, T. H. Ox the Classification of the Animal Kingdom.
Journal of the Linnzan Society (London), XII. 1876. pp. 199-
226. (Read 3d Dec., 1874.)
Section on “efical,” p. 216 et seg. Atrial cavity of Amphi-
oxus and Ascidians is an epiccel like the opercular cavity of the
Amphibian tadpole.
KOLLIKER, ALBERT. Ueber das Geruchsorgan von Amphioxus.
Miiller’s Archiv fiir Anat. Physiol., etc. 1843. pp. 32-35. Taf.
Ey igs
Discovery of olfactory pit and first description of the spermatozoa
of Amphioxus.
KOPPEN, Max. Settrage zur vergleichenden Anatomie des
Centralnervensystems der Worbelthiere. Zur Anatomie des
Lidechsengehirns. Morphologische Arbeiten (Schwalbe), I. 1892.
pp- 496-515. Taf. 22-24.
Contains discovery of giant-fibres in caudal portion of spinal
cord of Lacerta viridis.
KouHL, K. Lenzge Bemerkungen iiber Sinnesorgane des Amphi-
oxus lanceolatus. Zool. Anz. 1890. pp. 182-185.
States that sometimes there is a shallow olfactory groove on the
right side as well as that in the left. Such grooves are often due
to artificial crumpling, and the observation requires confirmation.
KRUKENBERG, C. FR. W. Zur Kenntnts des chemischen Baues
von Amphioxus lanceolatus und der Cephalopoden. Zool. Anz.
1881. pp. 64-66. See also HOPPE-SEYLER’S reply. pp. 185-187.
Compare also CUENOT (supra).
KUPFFER, CARL VON. Studien zur vergleichende Entwick-
lunesgeschichte des Kopfes der Kranioten,l. Die Entwicklung des
Kopfes von Acipenser sturio an Medianschnitten untersucht. 95
pp. 8°. g Tafeln. Miinchen und Leipzig, 1893.
Contains also a chapter on brain of Amphioxus, with figures.
LANGERHANS, PAUL. Zur Anatomie des Amphioxus lanceolatus.
Archiv fiir mikroskopische Anatomie, XII. 1876. pp. 290-348.
Taf. XII.-XV.
Standard work on the histology of Amphioxus.
LANKESTER, E. Ray. On Some New Points in the Structure of
Amphioxus and their Bearing on the Morphology of Vertebrata.
Quarterly Jour. Micro. Sc. XV. N.S. 1875. pp. 257-267.
39
40
4I
REFERENCES. 299
LANKESTER, E. Ray. Contributions to the Knowledge of Amphi-
oxus lanceolatus, Yarrell. \b., Vol. XXIX. 1889. pp. 365-408.
Five plates.
Lworr, Basitius. Uber den Zusammenhang von Markrohr
una Chorda beim Amphioxus und dahnliche Verhdaltnisse bet
Anneliden. Zeitschrift fur wiss. Zoologie. Bd. 65. 1893. pp.
299-308. Taf. XVII.
Describes those supporting fibres of the spinal cord of Amphi-
oxus which descend in successive paired groups to the notochordal
sheath and penetrate the latter in order to insert themselves on
the inner surface of the sheath. The openings in the notochordal
sheath of Amphioxus, through which the ventral supporting fibres
pass, were first observed by WILHELM MULLER in 1871. (W.
MULLER, Ueber den Bau der Chorda dorsalis. Jenaische Zeit-
schrift, VI. 1871. pp. 327-354.) See also PLATT (infra) and
LworF (88). Latter contains complete bibliography of literature
relating to structure of notochord.
Mayer, Paut. Uber die Entwicklung des Herzens und der
grossen Gefassstamme bet den Selachiern. Mitth. Zool. Stat.
Neapel. VII. 1887. pp. 338-370. Taf. 11-12.
MEYER, EDUARD. Studien iiber den Korperbau der Anneliden.
Mitth. Zool. Stat. Neapel. VII. 1887. pp. 592-741. Taf. 22-27.
42 bts. MOREAU, CAMILLE. echerches sur la Structure de la Corde
43
pods
46
dorsale de VAmphioxus. Bull. Acad. Belg. Tome 39. No. 3.
1875. 22pp. One plate.
MULLER, WILHELM. Ueber die Stammesentwicklung des
Sehorgans der Wirbelthiere. 76 pp. Five plates. 4°. Leipzig,
1874.
MULLER, WILHELM. Ueber das Urogenitalsystem des Amphi-
oxus und der Cyclostomen. Jenaische Zeitschr. fiir Naturwissen-
schaft, Bd. II. (neve Folge). 1875. Sep. Abdruck. pp. 1-38.
Two plates.
This is the important work in which the pronephros and
mesonephros were for the first time clearly distinguished from one
another. The author was, however, in error regarding Johannes
Miiller’s renal papillae of Amphioxus.
MULier, JOHANNES. Uber den Bau und die Lebenserscheinun-
gen des Branchiostoma lubricum Costa, Amphioxus lanceolatus,
Yarrell. Berlin, 1844. 4°. 40 pp. Five plates.
Read at the konigl. Akademie, 1841.
NANSEN, FriptTjJoF. The Structure and Combination of the His-
tological Elements of the Central Nervous System. Bergens
Museums Aarsberetning for 1886. Bergen, 1887.
48
49
REFERENCES.
OWSJANNIKOW, PHILIP. Ueber das Centralnervensystem des
Amphioxus lanceolatus. Bulletin de Acad. imp. des Sciences de
St. Pétersbourg, Tome XII. 1868. pp. 287-302, with one plate.
Also in Mélanges Biologiques, T. VI. pp. 427-450.
Introduced a method of maceration by which he was able to
shake out the central nervous system and thus isolate it from the
body. In this way he was able to correct the erroneous descrip-
tions of de Quatrefages and others (who stated that there were
ganglionic enlargements in the spinal cord), and to discover the
alternate arrangement of the spinal nerves.
PLATT, JULIA B. /72bres connecting the Central Nervous System
and Chorda in Amphioxus. Anat. Anz. VII. 1892. pp. 282-
284. Three figures in text.
PoLuarRD, E. C. A Mew Sforozoin in Amphioxus. Quarterly
Jour. Micro. Sc... XXXIV. N.S. 1893. pp. 311-316. Plate
XXIX.
Unicellular parasites in intestinal epithelium.
49 bts. POUCHET, GEORGES. On the Laminar Tissue of Amphioxus.
5oO
Le!
52
Quarterly Jour. Micro. Sc. XX. N.S. pp. 421-430. Plate XXIX.
DE QUATREFAGES, ARMAND. J/émotre sur le systéme nerveux
et sur Vhistologie du Branchiostome ou Amphioxus. Annales des ~
sciences nat. Zoologie. 3d series. IV. 1845. pp. 197-248.
Plates 10-13.
First observation of passage of ova through atriopore; and
discovery of the peripheral ganglion-cells in connexion with the
cranial nerves.
RATHKE, HEINRICH. Semerkungen iiber den Bau des Ampht-
oxus lanceolatus, eines Fisches aus der Ordnung der Cyclostomen.
Konigsberg, 1841. 4°. pp. 1-38. One plate.
REtzius, GusTAvV. Zur Kenntniss des centralen Nervensystems
von Amphioxus lanceolatus. Biologische Untersuchungen. Neue
Folge II. pp. 29-46. Taf. XI.-XIV. Stockholm, 1890.
52 d2s. RetTzius, Gustav. Das hintere Ende des Ruckenmarks und
53
54
sein Verhalten zur Chorda dorsalis bet Amphioxus lanceolatus.
Verh. Biol. Vereins. (Biologiska Foreningens Forhandlingar.)
Stockholm. Bd. IV. pp. 10-15. 9g figs. 1891.
RouvDE, EMIL. Héstologische Untersuchungen tiber das Nerven-
system von Amphioxus lanceolatus. In Anton Schneider’s Zoo-
logische Beitrage. Bd.II., Heft 2. Breslau, 1888. pp. 169-211.
Plates XV.—XVI.
Standard work on the central nervous system of Amphioxus.
Rowon, JOSEF Victor. Untersuchungen iiber Amphioxus
lanceolatus. Ein Beitrag zur vergleichenden Anatomie der Wur-
55
56
57
58
59
- 60
61
REFERENCES. 301
belthiere. In Denkschriften der Math.-Naturwiss. Classe der kais.
Akad. der Wissenschaften. Bd. XLV. Wien, 1882. 64 pp. 4°.
Six plates.
Relates chiefly to nervous system. Describes also the smooth
muscle-fibres in wall of pharynx, etc. Finds that the majority of
sensory nerve-fibres to the skin end freely between the cells of the
ectoderm in bush-like ramifications. For the rest, see NANSEN
ROHDE, RETzIUS, and FUSARI.
RotpH, W. Untersuchungen iiber den Bau des Amphioxus
lanceolatus. Morphologisches Jahrbuch, II. 1876. pp. 87-164.
Taf. V.-VII.; also figures in text.
RUCKERT, JOHANNES. L£xtwickelung der Excretionsorgane.
Ergebnisse der Anatomie und Entwicklungsgeschichte (Merkel
und Bonnet), I. 1891. pp. 606-695. Includes an extensive bibli-
ography.
SCHNEIDER, ANTON. Settrage zur vergleichenden Anatomie
und Entwicklungsgeschichte der Wéorbelthiere. L. Amphioxus
lanceolatus. pp. 3-31. Taf. XIV.-XVI. 4°. Berlin, 1879.
SCHULTZ, ALEXANDER. Zur Entwickelungsgeschichte des Sela-
chieretes. Archiv. fiir Mikr. Anat. XI. 1875. pp. 569-580.
Mat. 34.
Preliminary notes of both Sewer and Schultz, regarding the
segmental origin of the excretory tubules, were published in the
Centralblatt fiir Medicinische Wissenschaft, 1874.
SEMON, RICHARD. Studien tiber den Bauplan des Urogenital-
systems der Wirbelthiere; dargelegt an der Entwickelung dieses
Organsystems bet Ichthyophis glutinosus. Jenaische Zeitschrift,
XXVI. 1891. pp. 89-203. Taf. I.-XIV.
SPENGEL, J.W. Beitrag zur Kenntniss der Kiemen des Amphi-
oxus. Zool. Jahrbiicher. Abth. fiir Morphol. IV. 1890. pp. 257-
296. Taf. 17-18.
SPENGEL, J. W. Benham’s Kritik meiner Angaben iiber die
temen des Amphioxus. Anat. Anz. VIII. 1893. pp. 762-765.
STIEDA, LupwiG. Studien iiber den Amphioxus lanceolatus.
Mém. de l’Acad. Impériale des Sciences de St. Pétersbourg, 7th
series, Vol. XIX. No.7. 7opp. Four plates. 1873.
Contains some good observations on the central nervous system.
First to show that the split-like structure above central canal did
not correspond to the posterior fissure of the vertebrate spinal cord,
but was a portion of the original central canal itself, the lumen of
which had been partially obliterated by approximation of its walls.
First identification of ventral (motor) roots of spinal nerves in
Amphioxus.
302
63
64
65
66
67
68
69
REFERENCES.
THACHER, JAMES K. Median and Paired Fins ; a Contribution
to the History of Vertebrate Limbs. Transactions Connecticut
Academy, III. No. 7. 1877. pp. 281-310. Plates 49-60.
WEIsS, F. Ernest. L2xcretory Tubules in Amphioxus lanceolatus.
Quarterly Jour. of Micro. Sc. XXXI. N.S. 1890. pp. 489-497.
Plates 34-35.
VAN WIJHE, J].W. Ueber Amphioxus. Anat. Anz. VIII. 1893.
pp. 152-172.
VAN WIJHE, J. W. Die Kopfregion der Crantoten beim Amphi-
oxus, nebst Bemerkungen iiber die Wirbeltheorie des Schadels.
Anat. Anz. IV. 1889. pp. 558-566.
VAN WIJHE, J. W. Ueber die Mesodermsegmente des Rumpfes
und die Entwicklung des Excretionssystems bet Selachiern. Archiv.
f. Mikr. Anat. XXXIII. 1889. pp. 461-516. Taf. 30-32.
WILLEY, ARTHUR. Report on a Collection of Amphioxus, made
by Professor A. C. Haddon, in Torres Straits, 1888-89. Quarterly
Jour. Micro. Sc. XXXV.N.S. January, 1894. pp. 361-371. One
figure in text.
Branchiostoma cultellum. Peters.
TT:
DEVELOPMENT OF AMPHIOXUS.
AYERS, HowarpD. Sdellostoma Dombeyt, Lac. A Study from
the Hopkins Marine Laboratory. Biological Lectures, Marine
Biological Laboratory, Woods Holl. 1893. No. VII. Boston,
1894.
69 dts. BERT, PAUL. Ox the Anatomy and Physiology of Amphioxus.
Annals and Mag. of Nat. Hist., 3d Series. Vol. XX. 1867.
pp- 302-304. (Translated from Comptes Rendus. Aug. 26th,
1867. pp. 364-367.)
Breeding season of Amphioxus at Arcachon is from March to
May. Was the first to observe the ejection of the sperm through
the atriopore. Calls attention to remarkable lack of regenerative
power in Amphioxus. Individuals cut in two will live for several
days, but will not regenerate. “If the extremity of the body of
an Amphioxus be cut off, the wound does not cicatrize; on the
contrary, the tissues become gradually disintegrated. I have
seen animals, with only the tail mutilated, become gradually
eaten away up to the middle of the branchial region, and live
thus without any intestines, without abdominal walls, and without
branchiz for several days.” These observations of Paul Bert are
7O
71
72
73
74
75
76
77
78
79
REFERENCES. 303
capable of easy confirmation, and should be borne in mind in
view of the extraordinary regenerative power which Wilson dis-
covered in the segmentation stages of the embryo.
Boveri, THEODOR. Uder die Bildungsstitte der Geschlechts-
driisen und die Entstehung der Genitalkammern beim Amphi-
oxus. Anat. Anz. VII. 1892. pp. 170-81. Twelve figures.
DoHRN, ANTON. Studien zur Urgeschichte des Wirbelthier-
korpers. Ill. Die Entstehung und Bedeutung der Hypophysis
bei Petromyzon Planert. Mitth. Zool. Stat. Neapel. IV. 1882.
Dourn, ANTON. Studien, VIII. De Thyreoidea bei Petromy-
zon, Amphioxus und Tunicaten. Ib. VI. 1885.
Dohrn lays unnecessary stress upon the fact that often in
transverse section, especially in the anterior region of the
pharynx, the endostyle of Amphioxus projects up into the cavity
of the pharynx in the form of a convex lens-shaped ridge. This
is merely due to the muscular contraction of the pharynx, which
almost invariably takes place when Amphioxus is placed in a
killing reagent. It is, therefore, not an anatomical feature of
any significance.
DouRN, ANTON. Studien, XII. Zhyreotdea und Hypobran-
chialrinne, Spritzlochsack und Pseudobranchialrinne bet Fischen,
Ammocetes und Tuntkaten. \b. VII. 1887.
Dourn, ANTON. Studien, XIII. Uber Nerven und Gefiisse
bet Ammocetes und Petromyzon Planerz. \b. VIII. 1888.
FRORIEP, AuGUST. ELxtwickelungsgeschichte des Kopfes.
Ergebnisse der Anat. und Entwickelungsgesch (Merkel und
Bonnet), I. 1891. pp. 561-605. Eleven figures.
Includes an extensive bibliography.
HATSCHEK, BERTHOLD. Studien iiber Entwicklung des Amphi-
oxus. Arbeiten a. d. Zool. Institute. Wein, 1881. 88 pp.
Nine plates.
HATSCHEK, BERTHOLD. J/@tttheilungen iiber Amphioxus.
Zoologischer Anzeiger, VII. 1884. pp. 517-520.
Olfactory pit, sense-organ of preoral pit, anterior preoral
“ nephridium.”
HATSCHEK, BERTHOLD. Uber den Schichtenbau von Amphi-
oxus. Anat. Anz. III. 1888. pp. 662-667. Five figures.
Origin of sclerotome, etc.
KASTSCHENKO, N. Zur Entwicklungsgeschichte des Selachier-
embryos. Anat. Anz. III. 1888. pp. 445-467.
One of the first to bring forward definite embryological facts to
prove that the anterior (pra-auditory) head-cavities of VAN WIJHE
(Ueber die Mesodermsegmente, etc., des Selachierkopfes. Amster-
304
80
81
83
84
85
86
REFERENCES.
dam, 1882) are not homodynamous with the true somites. He
was followed in this respect by RABL (Theorie des Mesoderms.
Morphologisches Jahrbuch, XV. 1889).
KORSCHELT, E., und HEIDER, K. Lehrbuch der vergleichen-
den Entwicklungsgeschichte der wirbellosen Thiere. 3a Heft.
Jena, 1893.
KOWALEVSKY, ALEXANDER. Lutwicklungsgeschichte des Am-
phioxus lanceolatus. Mém. de l’Acad. Imp. des Sciences de St.
Pétersbourg..’ VIT?* Series) F2> XI> No: 4. 16672)7 dehree
plates.
IKOWALEVSKY, ALEXANDER. lWWeztere Studien iiber die Ent-
wicklungsgeschichte des Amphioxus lanceolatus, nebst einem
Beitrage zur Homologie des Nervensystems der Wiirmer und
Wirbelthiere. Arch. f. Mikr. Anat. XIII. 1877. pp. 181-204.
Two plates.
Among the definite discoveries communicated by Kowalevsky
in these two memoirs may be mentioned the following: General
features of segmentation and gastrulation, origin of mesoderm
from archenteric pouches, unique method of formation of
nerve-tube (see text), origin of notochord, neurenteric canal,
asymmetrical origin of gill-slits and mouth, and zz fart the
metamorphosis.
KUPFFER, CARL VON. Die Entwicklung von Petromyzon
Planerz. Arch. f. Mikr. Anat. XXXV. 1890. pp. 469-558.
Six plates.
Origin of head-cavities, hypophysis, etc.
KUPFFER, CARL VON. Die Entwicklung der Kopfnerven der
Vertebraten. Verhandl. Anat. Gesellschaft in Miinchen. 1891.
pp. 22-55. Eleven figures. (Erganzungsheft zum Anat. Anz.
VIEW SIcor.)
Ammoceetes (see Fig. 92 in text).
KUPFFER, CARL VON. Studien zur vergleichende Entwick-
lungsgeschichte des Kopfes der Kranioten I. Die Entwicklung
des Kopfes von Acipenser sturio an Medianschnitten untersucht.
pp. 95. Nine plates. Seven figures in text. Miinchen and
Leipzig, 1893.
Important contribution to the delimitation of the wall of the
brain. On page 84 is a reconstruction of head-cavities of Am-
moccetes (see Fig. 72). Figs. 21 and 22 in the plates repre-
sent cerebral vesicle of Amphioxus. (Cf. Fig. 51.)
LANKESTER, E. Ray, and WILLEY, A. The Development of
the Atrial Chamber of Amphioxus. Quarterly Jour. Micro. Sc.
XXXI. 1890. pp. 445-466. Four plates.
87
88
89
go
/ 9I
g2
93
REFERENCES. 305
LEUCKART, RUDOLPH, und PAGENSTECHER, ALEX. Untfer-
suchungen tiber niedere Seethiere. Amphioxus Jlanceolatus.
Miiller’s Archiv f. Anat. u. Physiol. 1858. pp. 558-569. Taf.
XVIII.
Description of larve of Amphioxus taken off Heligoland.
Drew attention to larval asymmetry, and to the existence of the
brain-ventricle (cerebral vesicle). In absence of knowledge of
early development their interpretation of many of the structures
(especially preoral pit, mouth, and _ gill-slits) was incorrect.
Latter applies also to Schultze’s observations.
Lworr, Basitius. Uber Bau und Entwicklung der Chorda
von Amphioxus. Mittheilungen a. d. Zool. Station. Neapel.
IX. 1891. pp. 483-502. One plate.
Consult this memoir for previous literature on histology of
notochord.
Lworr, BasILius. Ueber einige wichtige Punkte in der Ent-
wicklung des Amphioxus. Biologisches Centralblatt, XII. 1892.
pp- 729-744. Eight figures.
Notes absence of mesodermal “ pole-cells.” From frequency
of mitoses in dorsal ectoderm of gastrula, concludes that the
material destined to form dorsal wall of archenteron, from which
notochord and myoccelomic pouches arise, grows in from the
ectoderm round dorsal lip of blastopore. Hence notochord and
mesoderm are essentially derived from ectoderm!
MARSHALL, A. MILNES. Vertebrate Embryology. London,
1893.
MULLER, JOHANNES. Uber die Fugendzustande einiger See-
thiere. _Monatsbericht der konigl. preuss. Akad. der Wissen-
schaften zu Berlin. 1851. pp. 468-474.
First accurate description of larva of Amphioxus, p. 474. In
1847 Johannes Miiller obtained a young Amphioxus of 2} mm. at
Helsingfors. He says that the appearance of the gill-slits was
peculiar, in that there were two rows of slits in the pharyngeal
wall, placed one above the other. In the upper row were five
round slits, while the lower slits were vertically elongated and
were fourteen in number. Headds that it was doubtful whether
it represented the young “ Branchiostoma lubricum ” or belonged
to a new species.
MULLER, WILHELM. Ueber die Hypobranchialrinne der Tunt-
katen und deren Vorhandensein bet Amphioxus und den Cyklo-
stomen. Jenaische Zeitschrift f. Naturwiss. VII. 1873. pp. 327-332.
PLATT, JuLIA B. Further Contribution to the Morphology of
the Vertebrate Head. Anat. Anz. VI. 1891. pp. 251-265.
96
97
98
99
I0o
Io!
103
REFERENCES.
RaB1, CarL. Uber die Differenzierung des Mesoderms. Anat.
Anz. III. 1888. pp. 667-673. Eight figures.
Discovery of the sclerotome-diverticulum in embryo of Pristiurus.
RIcE, HENRY J. Observations upon the Habits, Structure, and
Development of Amphioxus lanceolatus. American Nat. XIV.
1880. pp. 171-210. Plates 14 and 15.
Author was the first to find Amphioxus in Chesapeake Bay.
With regard to development, he gives some fairly good figures of
larvee, and observed some of the more obvious features of the
metamorphosis, as already described by Kowalevsky.
RUCKERT, JOHANNES. Ueber der Entstehung der Excretions-
organe bet Selachiern. Arch. fiir Anat. u. Physiol. (Anatomische
Abtheilung). 1888. pp. 205-278. Three plates.
Contains also the discovery of segmental origin of gonads.
SCHNEIDER, ANTON. JSezttrage zur vergleichenden Anatomie
und Entwicklungsgeschichte der Wirbelthiere, IT. Anatomie und
Entwickl. von Petromyzon und Ammocetes. 4°. Ten plates.
Berlin, 1879.
Figure of the ciliated grooves in pharynx of Ammoccetes, at
page 84.
SCHULTZE, MAx. Seobachtung junger Exemplare von Amphi-
oxus. Zeit. f. Wiss. Zool. III]. 1851-2. pp. 416-419.
Two larve from Heligoland. Good description of structure of
notochord.
VAN WIJHE, J. W. Ueber Amphioxus. Anat. Anz. VIII.
1893. pp- 152-172.
WILLEY, A. Ox the Developmeut of the Atrial Chamber of
Amphioxus. (Preliminary communication.) Proceedings of the
Royal Society, XLVIII. 1890. pp. 80-89.
Wittey, A. Zhe Later Larval Development of Amphioxus.
Quarterly Jour. Micro. Sc. XXXII. 1891. pp. 183-234. Three
plates.
WILSON, EDMUND B. On Multiple and Partial Devolopment
in Amphioxus. Anat. Anz. VII. 1892. pp. 732-740. Eleven
figures.
In this and the following more detailed paper, the author
describes and interprets a remarkable series of experiments on
the artificial production of twins and dwarfs. Besides this. there
are many important observations on the normal cleavage of the
egg.
WILson, EDMUND B. Amphioxus and the Mosaic Theory of
Development. Journal of Morphology, VIII. 1893. pp. 579-
638. Ten plates.
104
REFERENCES. 307
ZIEGLER, H. Ernst. Der Ursprung der mesenchymatischen
Gewebe bei den Selachiern. Archiv f. Mikr. Anat. XXXII. 1888.
pp. 378-400. One plate.
Independent discovery of sclerotome-diverticulum. (See Rabl.)
IV.
ASCIDIANS.
For bibliography relating to the Ascidians, see Professor W. A. HERD-
105
~ 106
107
108
109
IIo
MAN’S Reports on the Tunicata collected during the ‘‘ Challenger”
expedition — Parts I.-III. 1882-88; and also KORSCHELT und
HEIDER, “ Lerhbuch der vergleichenden Entwicklungsgeschichte
der wirbellosen Thiere.” Heft III. Jena, 1893.
Vi
PROTOGHORDATES, -ETC.
AYERS, HOWARD. Concerning Vertebrate Cephalogenesis.
Jour. Morph. IV. 1890-91. pp. 221-245.
BATESON, WILLIAM. JJemoirs on the Development of Balano-
glossus. Quarterly Jour. Micro. Sc. Vols. XXIV.-XXVI.
1884-86.
Brooks, W. K. The Systematic Affinity of Salpa in its
Relation to the Conditions of Primitive Pelagic Life ; the Phylogeny
of the Tunicata ; and the Ancestry of the Chordata. Part II. of
Monograph of the Genus Salpa. Johns Hopkins University.
Baltimore, 1893.
BURCKHARDT, RUDOLF. De Homologieen des Zwischenhirn-
daches und thre Bedeutung fiir die Morphologie des Hirns bet
niederen Vertebraten. Anat. Anz. IX. 1894. pp. 152-155 and
320-324.
Relates to neuropore of craniate Vertebrates. Author calls the
lobus olfactorius impar of Kupffer, the recessus neuroporicus.
CLAPP, CORNELIA M. Some Points in the Development of the
Toad-fish (Batrachus Tau). Jour. Morph. V. 1891. pp. 494-
gol.
Observations on the double origin of mouth, made in 1889, not
published in this paper.
DaviporF, M. von. Ueber den “Canalis neurentericus
anterior bet den Ascidien.” Anat. Anz. VIII. 1893. pp. 301-303.
308 REFERENCES.
1s DOHRN, ANTON. Studien zur Urgeschichte des Worbelthier-
korpers, I. Der Mund der Knochenfische. Mitth. Zool. Stat.
Neapel. III. 1881-2. pp. 253-263. ‘
112 FIELD, GEORGE W. The Larva of Asterias vulgaris.
Quarterly Jour. Micro. Sc. XXXIV. 1892. pp. 105-128.
113 FowLerR, G. HERBERT. The Morphology of Rhabdopleura
Normant Allman. Festschrift fiir Rudolf Leuckart. pp. 293-297.
Leipzig, 1892.
II4 HARMER, S. F. See M’INTOSH.
O05 HERDMAN, W. A. Article ‘‘ Tunicata.” Ency. Brit. gth ed.,
republished in “ Zoological Articles” by Lankester, etc.
116 HUuBRECHT, A. A. W. Article “ Nemertines.” Ency. Brit.
oth ed., republished in “ Zodlogical Articles” by Lankester, etc.
116 67s. HUBRECHT, A. A. W. On the Ancestral Form of the
Chordata. Quarterly Jour. Micro. Sc. XXIII. 1883. pp. 349-368.
For later works on this subject see Notes to Chap. V.
117 KUPFFER, C. VON. Lntwickelungsgeschichte des Kopfes. In
Merkeland Bonnet’s Ergebnisse der Anatomie und Entwickelungs-
geschichte, II. 1893. pp. 501-564.
118 LANG, ARNOLD. Zum Verstandnis der Organisation von
Cephalodiscus dodecalophus M°’Znt. Jenaische Zeitschrift f.
Naturwiss. XXV._ 1891.
119 LANG, ARNOLD. Ueber den Einfluss der festsitzenden Lebens-
weise auf die Thiere. Jena, 1888.
120 LANKESTER, E. Ray. Degeneration: a Chapter in Darwinism.
Nature Series. London, 1880. Republished in “ The Advance-
ment of Science; Occasional Essays and Addresses.” London,
1890.
I2I LANKESTER, E. Ray. <A Contribution to the Knowledge of
Rhabdopleura. Quarterly Jour. Micro. Sc. XXIV. 1884. pp.
622-647.
122 MacBripE, E. W. The Organogeny of Asterina Gibbosa.
Proceedings Royal Society. Vol. 54. 1893. pp. 431-436.
123 M’INTosH, WILLIAM C. Report on Cephalodiscus dodecalo-
phus, M’Intosh. ‘‘ Challenger” Reports. Zodlogy,XX. 1887.
With Appendix by S. F. HARMER.
124 MorGan, T.H. Zhe Growth and Metamorphosis of Tornaria.
Jour. Morph. V. 1891. pp. 407-458.
125 MorGan, T. H. Zhe Development of pete Jour.
Morph. IX. 1894. pp. 1-86.
126 =Pxarr, JuLIA B. Further Contribution to the Morphology of
the Vertebrate Head. Anat. Anz. VI. 1891. pp. 251-265.
Describes the double origin of mouth in Batrachus.
REFERENCES. 309
127 POLLARD, H.B. Observations on the Development of the Head
in Gobius capito. Quarterly Jour. Micro. Sc. XXXV._ 1894.
PP 335505"
127 ds. POLLARD, H. B. The “ Cirrhostomial” Origin of the Head
in Vertebrates. Anat. Anz. 1X. 1894. pp. 349-359.
128 RABL-RUCKHARD, H. Der Lobus Olfactorius Impar der
Selachier. Anat. Anz. VIII. 1893. pp. 728-731.
129 SEDGWICK, ADAM. The Original Function of the Canal of the
Central Nervous System of Vertebrata. Studies from Morph.
Lab. Cambridge, II. 1884. pp. 160-164.
130 SEDGWICK, ADAM. Wotes on Elasmobranch Development.
Quarterly Jour. Micro. Sc. XXXIII. 1891-92. pp. 559-586.
Contains important observations on the first appearance of the
mouth, and its relation to the pituitary body.
131 SEELIGER, OSWALD. Studien zur Entwicklungsgeschichte der
Crinotden. (Antedon rosacea.) Zoologische Jahrbiicher. Abth.
f. Anat. VI. 1892. pp. 161-444.
132 VAN WIJHE, J. W. Ueber den vorderen Neuroporus und die
phylogenetische Function des Canalis Neurentericus der Wirbel-
thiere. Zool. Anz. VII. 1884. pp. 683-687.
133 WILLEY, A. Studies on the Protochordata, 1.-I/T. Quarterly
Jour. Micro. Sc. XXXIV.-XXXV._1893.
Contain further bibliographical references.
INDEX.
Acipenser sturio, 102, 129, 287.
Acrania, 17, 46.
AGASSIZ, A., 250, 251, 256.
ALLMAN, 262.
Ammocetes, 163-170, 173, 178, 182, 186,
282.
ANDREWS, 39, 41.
Annelid theory, 5, 79, 82, 97, 176, 282,
290, 293.
Annelids, excretory system of, 78-82, 99.
giant fibres of, 97, 103.
nervous system of, 95-97.
segmentation of, 4.
vascular system of, 55.
Antedon rosacea, 256, 268-269, 271.
Anus, 14, 25, 118, 131, 187.
Aorta, dorsal, 49, 50, 53-
Aperture, buccal, 182.
cloacal, 182, 183, 2I0.
Appendicularia, 180, 236-239, 241, 277.
Archenteron, IIo.
Artery, branchial, 47, 50, 98, 139.
genital, 98.
Ascidians, pelagic, 181, 236.
sessile, 181.
Asterias vulgaris, 254, 270.
Asterina gibbosa, 270, 271.
Asymmetron lucayanum, 40, 41.
Asymmetry, 155-162, 177.
Atriopore, 14, 77, 105.
Atrium (see also Cavity, peribranchial),
14, 22, 186, 195.
development of, 75-78, 210-212.
post-atrioporal extension of, 25.
Audition, 44.
AUDOUIN, 197.
Auricularia, 251-253, 256, 268.
Axis (see Relations, axial),
AYERS, 18, 173.
Balancers, 42.
Balanoglossus, 29, 43, 98, 128, 221, 222,
231, 242-253, 259, 261, 264, 265,
274, 276.
Balanoglossus, nervous system of, 244-
246.
Kowalevskii, 248, 250.
Kupffert, 248, 253.
BALFOUR, 5, 38, 79, 175, 190, 203, 273,
283, 292.
Band, adoral ciliated, 250.
circumoral ciliated, 251, 256.
longitudinal ciliated, 251.
post-oral (circular) ciliated, 251, 256.
Bands, mesodermic, 120, 217, 218.
peripharyngeal, 34, 140, 145, 168-169,
179, 185, 195, 226.
Bars, branchial (see Gill-bars).
BATESON, 98, 221, 244, 245, 250, 259,
263, 291.
Batrachus tau, 281.
Bdellostoma, 173, 285.
BEARD, 208, 281, 292.
BEDDARD, 81.
VAN BENEDEN, 187, I9I, 197, 200, 224,
2gl.
BENHAM, 33, 42.
BERT, 174.
Bipinnaria, 251.
Blastoceel, 108, 254, 255.
Blastomeres, 107.
Blastopore, IIo, I12, 197.
Blastula, 108, 197.
Blood-sinuses, I9I, 192.
Blood-vessels, contractile, 47, 98.
origin of, 122.
Bodies, polar, 106.
Body, pineal, 207.
pitituary (see Hypophysis).
Body-cavity (see also Ccelom), 217, 220-
222, 247.
preoral, 128, 218.
Bojanus, organ of, 194.
Botryllus, 181, 240.
BOULENGER, 14.
BOURNE, A. G., 81.
BOVERI, 42, 48, 60, 98, 99, 100, I51, 177.
Brachiolaria, 270.
311
312
Brain, 92, Io.
Branchiomery, 65, 132.
Branchiostoma cultellum, 40.
lubricum, 8.
Breeding-season, 105.
Brood-pouch, 215.
BROOKS, 254, 277, 289.
Bulbils, vascular, 48.
BURCKHARDT, 284.
Bury, H., 269.
CALDWELL, 291.
Canal, alimentary, 24, III, 187, 196, 214,
235, 249, 264.
neurenteric, 114, 118, 199, 202, 275.
Capillaries, 49, 98.
Capitellide, 81.
Cartilages, buccal, 18, 147.
labial, 18.
Caulus, 266.
Cavity, opercular, 22.
peribranchial (see also Atrium), 22,
183, 186, 195, 209.
peritoneal, 22.
Cells, epithelio-muscular, Ig1.
Cellulose, 182.
Cenogenesis, 177.
Cephalisation, 75, 89.
Cephalochorda, 13.
Cephalodiscus, 261-267, 280, 289.
Chetognatha, 278.
Ciona intestinalis, 203, 210, 215, 222, 224,
226, 229, 230-235, 240, 271, 288,
292, 293.
Cirri, buccal, 12, 20, 145.
Cladoselachid@, 44.
CLAPP, CORNELIA, 281.
Clavelina, 181, 185, 187, 200, 215, 225,
241, 288.
Cleavage, 107, 197.
polymorphic, 108.
Cceca, intestinal, 249, 261.
Ceciliant, 67.
Coecum, hepatic, 24, 236.
Ceelom, 22, 26, 31, 33, III, I2I, 122, 220-
222, 247-248, 265, 266.
perigonadial, 153, 177.
Coencecium, 263.
Collar-pores, 98, 248, 265.
Collar-region, 242, 264.
Collector, 45, 165.
Commissure, circumoesophageal, 96, 273,
280.
Compression, bilateral, 15, 43, 115.
INDEX.
Contraction, peristaltic, 98, 192.
Cordon ganglionnaire viscéral, 224.
COSTA, 7, 10.
Craniota, 17.
Crinoidea, 268.
Cross-bars, 28.
CUNNINGHAM, J. T., 80.
Cutis, 38, 41, 122.
CUVIER, 3.
Cyclostomata, 8, 10, 45, 208.
Cyclostome, 46.
Cynthia papillosa, 200.
DAVIDOFF, 200.
DEAN, B., 44.
Degeneration, 5.
Development, abbreviated, 214, 215, 239.
adolescent period of, 149, 150.
direct, 250.
duration of larval, 149, 169, 203, 215.
embryonic, 114, 201.
larval, 117, 130.
latent, 145, 160.
precocious, 161, 212.
Differentiation, sexual, 154.
Dissepiments (see Septa).
Distaplia magnilarva, 206, 225, 288.
Distribution, 11, 40-41.
Diverticula, anterior intestinal (see also
Head-cavities), 115.
DOHRN, 5, 30, 167, 173, 176, 178, 179, 280,
281, 282.
Duct, mesonephric, 66.
pronephric, 69, 78, 99.
Dura mater, 87.
Echinoderms, 250-256, 267-271, 291.
Ectoderm, 24, 78.
ciliated, 112, 113, 130, 175, 243, 257-
definitive, 111.
primitive, IIo.
EISIG, 45, 81, 94, 103, 293.
Embryo, ciliated, 113, 214.
ventral curvature of Ascidian, 201.
EMERY, 67. '
Endoderm, definitive, 111.
primitive, IIo.
Endostyle, 9, 24, 31, 39, 130, 138, 149, 150,
167, 177, 185, 195, 227, 229, 250.
Enteroccel, 252, 254, 255.
Enteropneusta, 242.
Epiccele, 41.
Epithelium, atrial, 33, 59, 100, 209.
coelomic, 33, 122, 220-222.
INDEX. ete)
Equilibration, 44, 205.
Equilibrium, Io, 43.
ERLANGER, 220.
Evolution, parallel, 80, 247, 290.
Eye of Ascidian tadpole, 102, 206,
Eye, median, 18, 102, 130.
myelonic, 207.
pineal, 207-209.
Eyes, paired, Io2.
Fascia, 36, 123.
FELIX, 99.
Fertilisation, 106, 188.
Fibres, giant, 92-94, 103.
Miillerian, 94.
of Mauthner, 94.
supporting, 89.
FIELD, G. W., 254.
Fierasfer, 67.
Fin, definitive caudal, 131.
provisional caudal, 115.
Fin-rays, I5.
Fins, 15, 44.
lateral, 38, 42.
Fixation, organ of, 222, 229, 271, 280.
FLEMMING, g9.
Flexure, cranial, 92, 279.
FOL, 239.
Folds, medullary, 199.
metapleural, 15, 38, 42, 43, 76, 132, 176.
Follicle, tos.
Food, 9, 39, 185, 249.
FOWLER, G. H., 262, 266, 267.
FRORIEP, 175.
Function, change of, 176, 280.
Funnels, atrio-ccelomic, 58, 98.
brown (same as preceding).
coelomic (see also Nephrostomes),
62.
FUSARI, 87, 163.
Fusari, plexus of, 87, 178.
FURBRINGER, 99.
Ganglia, peripheral, 85, 88.
spinal, 84, 103.
Ganglion, Ascidian, 188, 224, 225.
cerebral, 96, 270, 272-274.
Ganglion-cells, 89, 91.
bipolar, 95.
giant, 92.
multipolar, 92.
GARSTANG, 240, 250.
Gastrula, IIo, 197.
significance of, III.
Gastrulation, Iog.
GEGENBAUR, 249, 273.
Germ-layers, primitive, Ifo, 114.
Gill-bars, 28, 32-34.
blood-vessels of, 48-49.
Gill-pouches, 165, 166.
Gill-slit, first, 117, 118, 132, 141, 166, 170-
172.
Gill-slits (see also Stigmata), 17, 27, 100,
130-132, 135-138, 139, 148-149, 160,
173-174, 195, 229, 234, 243, 244, 264,
289.
asymmetry of, 157-158.
atrophy of, 140, 143, 149.
Gland, club-shaped, 116, 117, 134, 138,
141, 170-172, 176.
pyloric, 236.
subneural, 188-191, 225.
thyroid, 169-170.
thymus, 29, 30.
Glands, fixing, 204.
Glomerulus, 64, 65, 69, I00,
Gnathostome, 46.
Gobius capito, 282.
GOopDsIR, 8.
DE GRAAF, 208.
Groove of Hatschek, 21, 51, 135.
Groove, epibranchial, 226.
hyperbranchial, 34, 39, 195.
hyperpharyngeal (same as preceding).
hypobranchial (see also Endostyle),
9, 167.
medullary, 112, 198.
pericoronal (see Bands, peripharyn-
geal).
peripharyngeal (see Bands, peripha-
ryngeal).
Gut, post-anal, 203,
HAECKEL, 5, 46, III, 177.
HANCOCK, Igo.
HARMER, 263, 289.
VAN HASSELT, 193.
HATSCHEK, 41, 91, 102, 103, 104, 112, II5,
118,174, 175, 292.
Hatschek’s nephridium, 172.
Head-cavities of Ammoceetes, 129.
of Amphioxus, 126-128.
praemandibular, 128, 175, 279-280.
of Sagitta, 277.
Heart, 46, 51-53, I91, 192.
recurrent action of, 193.
HEIDER (see KORSCHELT and HEIDER).
fleplanchus, 173.
314
HERDMAN, 183, 277, 293.
Hermaphrodite, 187, 196.
Hexanchus, 173.
HJORT, 225, 293.
HOCHSTETTER, 54.
Hood, nerve-plexus of oral, 84, 178.
oral, 12, 147, 150, 178.
HUBRECHT, 258, 259, 260, 287, 291.
HUXLEY, 20, 22, 41, IIT.
Hypophysis, 160, 165, 178, 190, 191, 195,
225, 283-288, 290, 292.
Ichthyophis slutinosus, 67.
Infundibulum, ro02, 283, 285.
Insects, compared with Vertebrates, 2-4.
Involutions, atrial, 209, 241.
JULIN, 187, 190, 197, 200, 224, 225, 226,
292.
KASTSCHENKO, 175.
Kidney, 65.
KLINCKOWSTROM, 207.
Kolliker’s olfactory pit, 19.
KOPPEN, 103.
KORSCHELYT and HEIDER, 178.
KOWALEVSKY, 4, 104, I14, 174, 196, 216,
240.
KROHN, 197, 250.
KUPFFER, IOI, 102, 128, 129, 175, 283, 287.
Lamella, post-oral, 264.
Lamina, dorsal, 183, 185, 195, 226.
terminalis, 284.
Lamprey (see Petromyzon).
LANG, 291.
LANGERHANS, 21, 56, 98, TOI, 154.
Lanice conchilega, 80.
LANKESTER, 38, 41, 58, 62, 98, III, 237,
262, 266.
LEUCKART, Ioo.
LEYDIG, 4.
Ligamentum denticulatum, 25, 63, 164.
Limax lanceolatus, 7.
Line, lateral, 21, 42-45.
Liver, 24.
Lobe, przeoral, 218, 222, 228, 229, 254,
267-280, 290, 292.
procephalic, 272.
Lobus olfactorius impar, 102, 283, 284.
Locomotion, caudal, 103, 203.
ciliary, 121.
muscular, I2I.
Loimia medusa, 80.
INDEX.
Lumbricus, 79, 272.
LWOFF, 175.
Lymph-spaces, 15, 51.
MACBRIDE, 271.
Mantle, cellulose, 183.
muscular, 183.
MARSHALL, MILNES, 177.
Maturation, 106.
Mauthner, fibres of, 94.
MAYER, PAUL, gg, Ioo.
Medulla oblongata, 91.
Membrane, interccelic, 152.
vitelline, 105.
Merlucius, 67.
Mesenchyme, 201, 217, 220-222, 261.
Mesoderm, III, 114, 120, 122, I99-201,
221.
Mesonephros, 66.
Metamerism, 64, 132, 196, 246-247, 291.
Metamorphosis, 136, 150, 215, 223, 250, 256.
Metanephros, 66.
METCALF, 293.
METSCHNIKOFF, 25I.
MEYER, EDUARD, 80.
MILNE-EDWARDS, 197.
MINOT, I55.
M'INTOSH, 263.
Molgula, 194.
Molgula manhattensis, 210, 232, 240.
MorGA\N, T. H., 232, 245, 247, 253, 256,
274.
Mouth, 19, 117, 131, 143-144, 146, 150,
176, 178, 229, 276, 280-282.
asymmetry of, 157-160.
MULLER, FRITZ, 250.
MULLER, J., 8, 18, 50, 56, 59, 250.
MULLER, W., I02, 167.
Muscles, 34-37, 86, 122, 195, 203, 222,
235.
Muscle-fibres, origin of, r2t.
Musculature (see Muscles).
Myoceel, 121.
Myotomes, 13, 150.
Myxine, gill-slits of, 171.
hypophysis of, 285.
pronephric duct of, roo.
NANSEN, 103.
NASSONOFF, Igo.
Nemertines, 249, 256-261, 272, 273.
lateral nerves of, 259.
medullary nerve of, 259, 260.
Nephridium, 62, 79, 99, 261.
INDEX.
Nephrostomes, 65, 69, 72.
Nerve-cord, ventral, 96, 259, 273, 289.
Nerves, cranial, 85.
motor, 86, Ioo.
R. branchialis vagi, 163, 164.
Rr. cutanei ventrales, 44.
. recurrens trigemini et facialis, 45.
. cutaneus quinti (same as preced-
ing).
. lateralis trigemini (same as pre- |
ceding).
. dorsalis, 85, 103.
. lateralis vagi, 45, 259.
. ventralis, 85, 103.
. visceralis, 86.
sensory, 86.
spinal, 83.
Nerve-tube (see Tube, medullary).
Nervous system, origin of central, 111,
11g, 198.
Neuropore, 19, 90, II5, I60, I99, 202,
223, 225, 283, 285, 287, 292.
NORMAN, CANON, 262.
Notidanide, 173.
Notochord, 8, 13, III, 115, 124-126, 158,
I6I-162, 199, 216, 222, 244, 266,
286, 287, 290.
AAAF FF BAA
Ontogeny, 177.
Operculum, 264.
Organs, renal, 55, 194.
reproductive (see also Pouches,
gonadic), 122, I51-155, 187-188,
246, 266.
Otocyst, 205.
Otolith, Io, 205, 224.
Oviduct, 187.
Ovum, 105.
OWSJANNIKOW, Ioo.
PAGENSTECHER, Ioo.
Palingenesis, 177.
PALLAS, 7.
Paludina vivipara, 220.
Papillze, adhesive, 204.
renal, 56-57, 59.
Pericardium, IgI, 218.
Perich@ta, 81.
Petromiyzon, 93, 163, 169, 286.
Phallusia, 203, 232, 292.
Pharynx, 27, 183.
Phylogeny, 177.
Pigment, 18, 26, 33, 102, 130, 131, 134,
204.
315
Pigment-cells, 135.
Pilidium, 272.
Pit, olfactory, 19, 90, 145, 160, 165, 195,
283, 285, 292.
preoral, 51, 128, 135, 144, 148, 267.
Plate, apical, 255-256, 269, 270, 272-274,
292.
medullary, 113, 115, 118, 198.
Plates, skeletal (endostylar), 32.
PLATT, JULIA, 175.
| Pleuronectid@, 3, 40, 162, 178.
Plexus, branchial, 163, 164, 165.
Pluteus, 268, 270.
Pole-cells, mesoblastic, 175.
POLLARD, H. B., 282.
| Pontobdella, 81.
Porus branchialis, 23.
Pouches, archenteric, 114, II5, 120, 247,
248.
gonadic, 13, 25, 40, 153-154.
myoccelomic, 122.
POUCHET, 82.
Pristiurus, 99.
Proboscis, 221, 242, 247, 257, 264.
Proboscis-cavity, 247.
Proboscis-pore, 128, 248, 253, 264.
Proboscis-sheath, 258.
Products, genital, 174.
Pronephros, 66-75, 78.
blood-vessels of, 63, 69, 74, 100.
development of, 69, 78.
Prostomium, 272.
Protopterus, 14.
Pyrosoma, 181, 236, 241.
QUATREFAGES, 88, 174.
RABL, 175.
RABL-RUCKHARD, 284.
Raderorgan, 21, 148.
RATHKE, 8.
Recessus opticus, 102.
tectus abdominis;35-
, axial, 226-229.
RETZIUS, 82, 100, 103.
Rhabdopleura, 261, 262, 266, 267.
Ridge, epibranchial, 226.
Ridges, subatrial, 76.
RITTER, 250.
Rods, skeletal, 28.
ROHDE, 100, 101, 103.
ROHON, 82, 86, 163, 165.
ROLPH, 23, 41, 56, 86, 98.
RUCKERT, 60, 99, 100, 154.
316
Sac, branchial (see also Pharynx), 183,
195, 227.
Sagitta, 13, 277-278.
SAINT-HILAIRE, I, 279.
principles of, 2, 279.
SALENSKY, 206.
Salpa, 180, 182, 193, 236, 241.
Sarcolemma, 36.
SARS, G. O., 262.
SAVIGNY, Igo.
Schizoccel, 175.
SCHMIDT, KARL, 182.
SCHNEIDER, ANTON, 35, 38, 98, 100, 178.
Sclerotome, 123, 175, 221.
SEDGWICK, ADAM, I12, 289, 291.
SEELIGER, 239-240, 269, 277.
Segmentation (see Cleavage).
Segmentation-cavity, 108.
SEMON, 67.
SEMPER, 5, 79, 99, 176.
Sense-cells, 20, 21.
Sense-organ of przoral pit (see Groove
of Hatschek).
Septa, 13, 37, 122.
Sheath, notochordal, 38, 123.
SHELDON, LILIAN, 293.
Shield, buccal, 263.
Skeleton, axial, 13.
Snout, 115, 218.
Somites, mesodermic, II5, 121.
Spawning, Ios.
Species of Amphioxus, 41.
SPEE, GRAF, 99.
SPENCER, BALDWIN, 207, 208, 209.
SPENGEL, 38, 41, 248.
Spermatozoa, Ios.
Spinal cord, 83, 222.
central canal of, 89, 289.
Spiracle, 173.
Spiraculum, 23.
Splanchnoccel, 122.
Stage, critical, 149, 174.
STANNIUS, 45.
STIEDA, Ioo.
Stigmata, 183, 195, 196, 227.
formation of, 229-235.
Stomodceum, 165, 209.
Sympathetic system, 35, 86.
Synapticula (see Cross-bars).
Table, showing order of development of
Ascidian and Amphioxus, 213.
INDEX.
Tadpole, Batrachian, 14.
Tail of Ascidian tadpole, 201-204, 212,
222.
Teleosteans, 45, 281.
Tentacles, velar, 20, 195.
Test, 182, 240.
THACHER, 38.
Thymus, 29.
Tissue, connective, 37, 41, 122.
mesenchymatous, 221.
Tongue-bars, 28, 140, 142, 148, 231.
Tornaria, 250-253, 255-256, 270, 274.
Trochophore, 256, 272.
Tube, medullary, 114, 120, 198, 274.
neuro-hypophysial, 225.
Tubercle, dorsal, 189, 225.
Tuberculum posterius, 102.
Tubules, excretory, 59-65, 72, 100, 122,
mesonephric, 70, 177.
pronephric, 67, 70, 78, 100.
uriniferous, 65.
Tunic (see Test).
Ureter, 66.
Urmund, IIo.
Ussow, Igo.
Vacuolisation of notochord, 125, 216,
240, 244.
Vas deferens, 187.
Vein, cardinal, 54.
caudal, 54.
hepatic, 49, 98.
portal, 53, 98.
sub-intestinal, 49, 53-55.
Velum, 20, 50, 150, 178.
Vesicle, cerebral, 90, 100, 204, 223, 224,
226.
Water-pore, 253, 254.
WEISS, F. E., 57, 59.
VAN WIJHE, 39, 50, 51, 88,99, 128, 163,
164, 165, 178, 289.
WILDER, BURT G.,, 14.
WILSON, E. B., 108, 174, 175, 292.
WOODWARD, A.S., 44.
YARRELL, 8.
ZIEGLER, H. E,, 175.
Zoarces, 67.
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