TEX T-B OOK
OP THE
EMBRYOLOGY OF INVERTEBRATES
By Props. KOESCHELT and HEIDEE.
TEXT-BOOK OF THE
EMBRYOLOGY OF INVERTEBRATES.
Vol. I. — Porifera, Cnidaria, Ctenophora, Vermes, Enteropneusta,
Echinodermata. 15s.
Vol. II. — Phoronidea, Bryozoa, Ectoprocta, Brachiopoda,
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Onychophora, Myriopoda, Insecta. 14s.
Vol. IV. 18s.
TEXTBOOK
OF THE
EMBRYOLOGY OF INVERTEBRATES
BY
Dr. E. KORSCHELT, Dr. K. HEIDER,
PROFESSOR OF ZOOLOGY AND COMPARATIVE PROFESSOR OF ZOOLOGY IN THE UNIVERSITY
ANATOMY IN THE UNIVERSITY OF BERLIN.
OF MARBURG.
TRANSLATED FROM THE GERMAN
BY
MATILDA BERNARD.
REVISED AND EDITED WITH ADDITIONAL NOTES
BY
MARTIN F. WOODWARD,
DEMONSTRATOR OF ZOOLOGY, ROYAL COLLEGE OF SCIENCE, LONDON.
Vol IV.
AMPHINEURA, LAMELLIBRANCHIA, SOLENOCONCHA,
GASTROPODA, CEPHALOPODA, TUNICATA, CEPHALOCHORDA.
LONDON: '
SWAN SONNENSCHEIN AND CO., Ltd.
NEW YORK: THE MACMILLAN CO.
1900.
a
^i. **.+ <*(i. I, however, did not feel that it lay within my province
to rewrite this section, so I have contented myself with ap-
pending numerous footnotes pointing out wherein the recent
investigators differ in their observations and conclusions from
those cited in these pages. It is, however, impossible to do full
justice to this subject by means of footnotes, and the student
who desires to study the subject thoroughly is referred to the
original monographs.
VI PBEFACE.
The Tunicates, more than any other group, seem of recent
years to have occupied the attention of embryologists, and the
large amount of work which has been done on this group,
especially in France, with regard to both the sexual and the
asexual methods of reproduction, will be gathered from the
additional literature appended to Chapter xxxv., only a small
proportion of which could be referred to in the footnotes.
In the Mollusca also a great deal of work has been done,,
especially in connection with cell-lineage, and the formation of
the mesoderm and of the larval kidney, in spite of which the
last two points still remain obscure. Since I am more familiar
with the Mollusca than with any other group of Invertebrata,
I have revised the chapters dealing with this phylum some-
what more thoroughly than the rest of the volume ; I have
appended numerous notes, inserted some fresh paragraphs, and
made certain alterations in the text which appeared justified
by recent investigations.
I must again express regret that so long a time has inter-
vened between the publication of the German edition of this
work and the appearance of the last volume of the English
translation. Volumes ii., iii. and iv. came into the hands of
the translator only in 1897, and the task of bringing them out
being necessarily somewhat lengthy, it has been impossible
sooner to offer the completed work to the English-speaking-
student, to whom it should be of
Fig. 1. — A-D, sections through embryos of Chiton Polii at the blastula and gastrula
stages (after Kowalevsky). bl, blastopore ; »i, rudiment of the mesoderm ; w, rudi-
ment of the ciliated ring [velum].
continue to divide, an invagination of the vegetative half (B) takes
place. In this way the cleavage-cavity, which wras never large, is
further compressed.* The invagination-gastrula (B) which at first is
somewhat depressed, now elongates in the direction of the invagina-
tion (C). The archenteron also grows larger. In its wall, near the
blastopore, there appear two cells which, as compared with the rest,
* [Metcalf (No. I.) finds a large blastocoele which is not wholly obliterated
during the later development. — Ed.]
4 AMPHINEUEA.
are specially large (C, m). These cells which, as well as others
situated near them, at first lie in continuity with the entoderm,
represent the rudiment of the mesoderm. They soon shift out of the
series of entoderm-cells into the cleavage-cavity (D, m). The meso-
derm-rudiment which thus arises seems at first to have a regular
bilateral arrangement in keeping with its origin, i.e., two groups of
large cells lying near the blastopore can be seen, but this regularity
is soon lost, the cells, which subdivide further, becoming scattered.
In this respect, and perhaps also in the manner of its origin, the
mesoderm of Chiton may be compared with that of other Molluscs
(Lamellirranchia, p. 29, Gastropoda, p. 117).
2. The Development of the Larval Form.
Even before the development of the germ-layers has progressed
thus far, alterations take place in the external shape of the embryo.
Two adjacent rows of cells in the ectoderm of the gastrula become
distinguished from the rest as bearing cilia (Fig. 1 C, w), and these
divide the larva into an anterior and a posterior section. Similarly,
a group of cells lying at the pole furthest away from the blastopore
becomes covered with cilia. These two groups of ciliated cells are
the rudiments respectively of the ciliated ring [velum] and of the
frontal or apical ciliated tuft (Figs 2 and 3, w and tvs). Very similar
embryonic stages are met with in the ontogeny of other Mollusca, e.g.,
Patella (Fig. 50, p. 124). The pre-oral ciliated ring in the Lamelli-
branch larvae is also formed of two rows of cells. Indeed, the
ciliated ring seems usually to be biserial ; though, in Patella, there
are three rows of cells (Figs. 52 and 53, pp. 126, 127).
As the body extends in the direction of its principal axis, the blas-
topore, which has hitherto lain at the posterior pole, assumes another
position and form. It shifts to that side of the larva which later
becomes the ventral surface, and, owing to the growth of the dorsal
surface, gradually approaches the ciliated ring (Fig. 1 B-D). The
blastopore, as it shifts its position, loses its circular form, and, as far
as we can make out from the figures, assumes the form of a trans-
verse slit (Fig. 3 B). Meantime, the continuous growth of the dorsal
surface causes the aperture to shift more and more towards the
ciliated ring, and it is finally found immediately behind it (Fig. 2 A).
This slit-like aperture, however, no longer corresponds fully to the
blastopore, since the ectoderm surrounding the latter has sunk below
the surface, and the actual primitive mouth thus comes to lie at the
inner end of a laterally compressed ectodermal tube which for some
THE DEVELOPMENT OF THE LARVAL FOHM. ■)
time longer continues to deepen (Fig. 2 A, oe). This ectodermal
invagination, the stomodaeum, represents the rudiment of the fore-gut
(buccal mass and oesophagus). In connection with it there appears
later, as a ventral outgrowth, the radular sac (Fig. 2 I>, r).
The "shifting "of the blastopore just described agrees closely with the
processes to be met with in the Gastropoda (p. 141), and we are inclined in both
cases to assume that we are really dealing with the closing from behind forward
of an originally slit-like blastopore.
a.
JS.
Fig. 2. — .1 and B, median longitudinal sections through embryos of Chiton Polii at
different ages (after Kowalevsky). fd, pedal gland ; m, mouth ; md, enteron ; mes,
mesoderm ; oe, stomodaeum ; r, radular sac ; w, ciliated ring (velum).
The more active growth of the part lying behind the ciliated ring-
is accompanied by reduction of the anterior section which formerly
preponderated (Figs. 1 and 2). The embryo, which is now almost
pear-shaped, may become free at this stage {e.g., Chiton marginatus,
Loven). The larvae of this latter form carry a large ciliated tuft at
the frontal pole (Fig. 3 .4). The embryos of other Chitones remain
longer in the egg, and before attaining free life approach more nearly
the form of the adult (Fig. 3 C).
The larvae of the Chitones resemble those of the Annelida, and since a
Trochophore exceedingly like that of the Annelida is found in other Molluscs
(Figs. 18, 51, 53), we are justified in instituting such a comparison here also,
even although the resemblance is not so close. We have here a pre-oral
ciliated ring, and the origin and position of the different sections of the
intestinal canal is the same as in the Trochophore. The larva, at first, has no
anus, as the terminal segment of the alimentary canal only appears later at
the posterior end of the body in the form of an ectodermal invagination, the
b AMPHINEURA.
proctodaeum (Fig. 9). An organ which is of great importance in interpreting
the larva, the apical plate, is not present in the early stages of Chiton, but
the cerebral ganglia arise later in the position which this organ occupies in
the Annelida ; in the free-swimming larva of Chiton Polii these ganglia are
found beneath the ciliated tuft on the frontal pole (Fig. 5.), and may therefore
be regarded as representing the apical plate. Thus, to make the comparison
complete, only the primitive kidneys are wanting. So far these have not
been found, although they occur in other Molluscs (pp. 39 and 136).
a.
rtt>u, Fullarton, No. 14). This form of oviposition is
common among marine forms, but among fresh-water and a few
marine forms the female takes considerable care of the brood. In
these latter cases, fertilisation occurs either in efferent genital ducts
or in the branchial cavity, into which the spermatozoa have passed
from outside. In U/u'n and Anodonta, for instance, the eggs which
are discharged into the inner division of the supra-branchial cavity
are driven by the stream of respiratory water filled with sperm into
the cloaca, and thence into the external division of the supra- branchial
cavity, and so into the interlobar cavity of the outer gill-lamella whei'e
they pass through their embryonic development. In Pisidium, the
eggs lie in special brood-pouches at the base of the gills, and, in
C)/rf>is also, brood -capsules are formed in the gills by growths of the
epithelium between the septa, and in each of these an egg or embryo
lies. Embryos have even been observed in such pouches nourishing
themselves by swallowing the branchial epithelial cells (Stepanoff,
No. 54, Ziegler, No. 60). Dreisseyisia is peculiar among fresh-
water Lamellibranchs in this respect, and it discharges its eggs direct
into the water like the marine forms mentioned above (Korschelt,
No. 27). On the other hand, in some marine Lamellibranchs, care is
taken of the brood. The eggs of Teredo, for example, are retained
in the branchial chamber (Hatschek), and in Odrea edulis they are
found, up to the time when the free-swimming larva develops,
within the mantle-cavity (Mobius No. 37, Horst, No. 19). Ento-
valva mirabilis forms a bell -shaped brood-cavity at the posterior end
of the body through the fusion of the two halves of the mantle, in
which the ernbryos remain till the Trochophore stage is reached
(Voeltzkow, No. 57).
The spherical eggs are loosely surrounded by a thin, structureless
membrane (vitelline membrane), which may be lost even during
embryonic life (e.g., in Teredo). Sometimes the egg-integument is
exceedingly delicate, and disappears even during the earliest stages
of development, and then the eggs pass out direct into the water
(Dreissensia, Mytilus, Ostrea). On the other hand, the envelope may
be thicker and multilaminar as in Cardinal exiguum, the eggs of which
with their vitelline membranes have a lenticular form and are
attached to firm objects by the mother (Loven, No. 33). In some
genera (Anodonta, U/rio, Ci/cIuh), a chimney-like appendage, the
micropyle, is found on the egg-integument (Fig. 22, m^jjuJK)).
24
LAMELLIBRANCHIA.
2. Cleavage and Formation of the Germ-layers.
In those forms in which the cleavage of the egg has been carefully
investigated {Unio, Anodonta, Gardium, Gydas, Teredo), its course
is so uniform that we may conclude that it is the same in those eggs
of which only a few but similar stages have been observed (Odrea
edulix, Pectm, Mytitus edulis, Mobius, Horst, Fullarton, Barrois
and Wilson). Cleavage is always unequal ; the first cleavage- plane
divides the egg
into two cells, a
very large macro-
mere and a much
smaller micromere
(Fig. 11 A). In
Teredo, a corres-
ponding differen-
tiation is indicated
even before cleav-
age by the different
constitution of the
protoplasm at the
vegetative and at
the animal poles
of the egg. The
plane dividing the
two blastomeres passes through the point where the polar bodies
lie. The micromere next divides into two (Fig. 11 B), and almost
at the same time, or else a little later, the macromere gives origin
to a new micromere (G). The new cell then divides, and the process
of the abstriction of a micromere from the large cleavage-sphere is
repeated (D) again and again, the large cell yielding micromeres
which then divide (E). Finally, the micromeres, seen from the
surface, resemble a cap placed upon the remains of the macromere,
which at last also divides into two similar cells (macromeres)
(Fig. 11 F)*
Fig. 11. — A-F, diagrams illustrating the cleavage of the
egg in the Lamellibranchia. The lines connecting the
nuclei of two cells indicate that the pair has arisen from
the division of one cell.
* [It is commonly held that the entoderm arises solely from the macromeres
after the latter have ceased giving origin to micromeres, and that, at the four-
celled stage (Fig. 11 C), the rudiment of the entoderm lies entirely within the
single macromere. This appears to be the case in Cyclas according to
Stauffacher (No. VI.), but in Unio, on the contrary, Lillie (No. III.)
asserts that, at this stage, eacli blastomere contains the rudiments of both
ectoderm and entoderm. The cleavage in Unio appears, on superficial
CLEAVAGE AND FORMATION OF THE GERM-LAYERS. 25
The cells do not necessarily always divide in exactly the way described.
For example, a new micromere may be constricted off before tbe one lasi
formed has divided; but this does not indicate auy essential deviation from
the course above described. This is also the case in the apparently divergent
method of cleavage seen in Modiolaria and Ostrea virginiana, as was recognised
long ago by Loven, and was again pointed out by Ziegler. In the two
Lamellibranchs just named, during the first stages of cleavage, a very
remarkable process takes place, a part of the large sphere rising up from it
like a distinct blastomere, but not, like the true blastomeres, entirely separating
from it ; at a later stage, this protuberance is withdrawn into the macromere.
On account of this process, which is probably determined by the relative
distribution of the protoplasm and the yolk in the egg, the first stages of
Mucin, I, in, i and Ostrea virginiana differ in appearance from the diagrams given
above ; they may, however, be referred to these, as is evident after the de-
generation of the false blastomere.
Ray Lankester long ago described the cleavage of the egg in Pisidium
pusillum, a form nearly related to Cyclas, into four spheres of equal size, from
each of which a smaller cell became constricted (No. 29). If this is really the
case, this method of cleavage would not correspond to that known to occur in
other Lamellibranchs, but would rather closely resemble the cleavage of the
Gastropod egg (p. 108). This condition of the egg of Pisidium is however so
peculiar when compared with that of other Lamellibranch eggs that it requires
to be further investigated.
In describing the stages of cleavage, we have so far dealt only with
their outward form. Although the manner in which this arises in
the various eggs is very similar, nevertheless certain differences of
internal constitution are very soon evident. In one case, a cavity,
the cleavage-cavity, soon appears between the micromeres and the
macromeres. [In Cyclas, at the 13-celled stage, Stauffacher.]
This increases considerably in size, as the division of the cells
continues, and leads to the formation of a blastula, such as is found
in Cyclas, Pisidiv/m and the Unionidae, the wall of which is not
uniform in thickness. In other cases, the cleavage-cavity is not so
large, especially at first (Mytilus),* while in Teredo, as well as in
examination, to be precisely similar to that described above, but neither
the first nor the second cleavage separates the animal from the vegetative
cells, as Rabl asserted, this separation, according to Lillie, only occurring
at a later period, and thus the entoderm arises both from the micromeres and
the macromeres. Lillie suggests that the unequal cleavage in Unio is due
to the fact that the rudiment of the immense shell-gland is to be found in
the large cell, and he further accounts for the minute size of the entomeres
on the ground that the intestine remains undeveloped until a late stage. — Ed.]
*The observations of Barrois, made on Mytilw (No. 1) are only known to
us from the abstract in the Jahrsberichte, but, taken together with the
statements of Wilson (No. 59) are probably to be understood in the way
indicated above.
26
LAMELLIBRANCHIA.
Fig. 12. — A-C, embryos of Teredo during the for-
mation of the germ-layers (after Hatschek). The
entoderm-cellsare lightly dotted, while the mesoderm -
cells are more darkly marked ; the unshaded part is
ectoderm.
Ostrea virginiana, it is altogether wanting (Figs. 12 and 14 A). The
micromeres then lie immediately upon the macromeres, the con-
sequence being that, as they multiply, they surround the latter.
An epibolic gastrula is
C. t s~~ >—^ thus pi'oduced (Figs.
12 and 14 .4), such as,
according to Loven,
is found in Modiolaria
and Cardium. In the
last stages of cleav-
age, the two primary
germ- layers are
already differentiated,
the micromeres corre-
sponding to the ectoderm and the macromeres to the entoderm.
This also applies to those cases in which a cleavage-cavity forms and
the gastrula arises through invagination (fresh- water Lamellibranchs,
Ray Lankester, Ziegler, Lillie). In Cydas, for instance,
a shallow depres-
sion forms in the
blastula (Fig. 13
^4), the vegeta-
tive pole of which
is no longer to be
distinguished by
the larger size of
its cells, and, by a
further invagina-
tion of the cells at
this point, a small
archenteron is
formed (Fig. 13
B). This is also
the case in Pisi-
dium. The blas-
topore takes the
form of a slit lying
in the median line,
and in this way the embryo early assumes a bilateral symmetry.
The blastopore soon closes, so that the archenteron loses its
connection with the exterior and lies as a closed sac in contact
Itt.
Fig. 13. — A-V, sections through embryos of Cyclas cornea, .1 ,
blastula-stage, B, gastrula-stage, C, stage succeeding the
closure of the blastopore (after Ziegler). hi, blastopore ;
'■nt, entoderm ; m, mesoderm ; oes, rudiment of the stomo-
daeum.
CLEAVAGE AND FORMATION OF THE GERM-LAYERS. 27
with the ectoderm (Fig. 13 C). It is not known whether the
blastopore closes from behind forward, so that its relations to
the month and anus are still uncertain. [In Unio (Lillie) the
blastopore is said to close by the forward growth of its posterior
lip, the ventral plate.]
In the Unionidae also there is an invagination-gastrula, but the
archenteron is here still smaller than in Cycla* (Goette, Fig. 23
A-C. '. p. -"'1).
The presence of an invagination-gastrula in the Unionidae was first ob-
served by Rabl in 1876 (No. 43), and Schierholz in 1878 (Nos. 47-49), and
the gastrula was said to have a specially large archenteron (Fig. 22, p. 50), but it
is impossible to reconcile either the position or the large size of this arch-
enteric invagination with the later development of the embryo, especially as
the alimentary canal is at first very inconspicuous. According to Goette's
recent description (No. 15), this deep depression represents the shell-gland
which is here specially strongly developed, the archenteron, on the contrary,
being reduced (Fig. 23 A-C, sd and e). The subject will be discussed more
in detail in connection with the further development of the Unionidae (p. 49).
[Lillie (No. III.) has shown definitely that the large invagination observed
by Rabl and Schierholz was the temporarily inturned shell-gland, the true
archenteron being very small.]
Between the extreme cases of epibolic and embolic gastrnlation,
such as are offered by Cyclas on the one hand and Teredo on the
other, Ostrea forms to a certain extent a transition. In the Euro-
pean as well as in the American Oyster, the micromeres have been
observed to grow round the macromeres, of which there are only one
or two present at this stage (Fig. 14 A). Horst and Brooks agree
in denying the presence up to this stage of a cleavage-cavity, but
such a cavity arises as soon as the macromeres increase in number.
As the micromeres even during epibole projected slightly beyond
the macromeres at the vegetative pole, a depression arises in this
i-egion. When the macromeres now divide, a stage arises, with an
almost triangular blastopore, which cannot be distinguished from an
invagination-gastrula (Fig. 14 B). During these processes, important
alterations have taken place in the form of the embryo ; an invagina-
tion closely resembling the archenteron in form, the so-called shell-
gland, has appeared (Fig. 14 B and C, sd). To this and the further
transformation of the embryo (C'-E) we shall return later.
Conditions similar to those in the Oyster are found also in the Lamelli-
branchs examined by Lovkn (Modwlaria and Cardium), in which the abund-
ance of yolk determines the early circiuucrescence of the entoderm-elements,
28
LAMELLIBKANCHIA.
which latter only then commence to divide. A cavity then appears to arise
between the ectoderm and the entoderm, and stages occur exactly resembling
Fig. 14 B. In Teredo, the separation of the two primary germ-layers and the
increase of the entoderm-cells takes place at later stages (Figs. 12 and 15,
pp. 26 and 31).
During the act of gastrulation (Teredo, Unionidae) or even before
it commences (Cyclas), the rudiment of the mesoderm appears in the
embryo. In the epibolic gastrula of Teredo, there are two large cells
which, according to Hatschek, are to be traced back to the macro-
R
B
mes
R
E.
m-
meSr
Sr-
7)V
IMS-
Fig. 14. — A-E, various stages of development of the Oyster (A of Ostrea virginiaua
after Brooks, B-E, of Ostrea edulis after Horst). a, anus; hi, blastopore; m,
mouth ; ma, stomach ; mes, mesoderm-eells ; rk, polar bodies ; s, shell (in D, un-
paired embryonic shell-rudiment) ; sd, shell-gland ; sm, the anterior adductor muscle ;
w, pre-oral ciliated ring.
meres, lying symmetrically to the median plane at the posterior
edge of the blastopore (Fig. 12 A and B). They are soon grown
round by ectoderm and are thus drawn into the interior of the
embryo (Fig. 12 C). In Ostrea edvlis, corresponding cells are
found in a similar position (Fig 14 C), and conditions similar on the
whole are also found in Gyclas.* These two cells have been assumed
to be lyrimitive mesoderm-eelU [mesodermal teloblasts] homologous to
* [In Cyclas, after the macromere has given origin to the last micromere
(about the 30-celled stage), it divides into two cells of equal size, from each of
which a large cell segments off into the cleavage-cavity. These are the two
primary mesoderm-cells. The two small remnants of the macromeres form
the entoderm (Stauffacher, No. VI). — Ed.]
CLEAVAGE AND FORMATION OF THE GERM-LAYERS. 29
those in the Annelida, from which by repeated division the mesoderm-
banda are formed. In this way, the bilateral symmetry of the body
would find an early expression in the rudiment of the mesoderm.
Two mesoderm-bands, which, however, are not nearly so regular in their
arrangement as in the Annelida, have also been discovered by Rabl and
Hatschek. Horst has described similar conditions in Ostrea, and Ziegler's
account of Cj/clas also, on the whole, agrees with the above. The latter
author, however, does not exclude the idea of a further participation of the
ectoderm in yielding the mesoderm-elements, and Ray Lankester also was
formerly in favour of the partial derivation of the mesoderm from the ecto-
derm (Pisidivm). There was therefore a general inclination not to derive the
whole of the mesoderm in the Lamellibranchia from the primitive mesoderm-
cells.
I'nio, a form in which the mesoderm and the germ-layers in general were
first demonstrated by Rabl, although indeed not very accurately (c/. pp.
27 and 50), shows most markedly the method of formation of the primitive
mesoderm-cells [mesodermal teloblasts] and the mesoderm-bands. But since
the entodermal nature of the large invagination in the Unionidac must be
considered as refuted, these conditions also cannot be regarded as sufficiently
established. Rabl found, in Unio, two cells which even in the blastula-stage
are distinguished by their size from the rest. At the commencement of
gastrulation, these pass into the cleavage-cavity, and then lie symmetrically
to the median line. The active multiplication of these two cells is said to
give origin to the mesoderm-bands.
It must here be mentioned that the presence of the large cells that were
found by Rabl within the young embryo is confirmed by the later descriptions
of Schierholz (No. 49) and Goette (No. 15) (Fig. 23 -4, p. 51). According
to Goette's figures, these might also lie near the blastopore, since the latter
is apparently not far removed from the shell-invagination which Rabl mis-
took for the archenteron (Fig. 23 .4). The mesoderm-bands in the Lamelli-
branchia cannot, as a rule, be said to be very distinct.
[The primitive mesoderm-cells in Unio lie in the cleavage-cavity imme-
diately posterior to the blastopore, and give rise to two mesoderm-bands by
teloblastic growth. There are in addition certain mesoblastic cells (the larval
mesoblast of Lillie) situated anteriorly to the archenteron, which have the
character of a mesenchyme, and possibly form the larval adductor muscle and
the myocytes.]
Summary. The differentiation of the germ-layers in the Lamelli-
branchia takes place very early. Even during cleavage the two
primary layers can be clearly distinguished, and the rudiment of
the middle germ-layer can also be recognised very early (Figs.
12-14). After the gastrula-stage is reached, the mesoderm is found
in the form of more or less massive accumulations of cells (mesoderm-
bands), apparently proceeding from the posterior pole, between the
ectoderm and the entoderm. The bilateral symmetry of the germ
30 LAMELLIBRANCHIA.
early finds expression in the rudiment of the mesoderm and in the
position of the blastopore.
3. Development and Structure of the Trochophore Larva.
There is, in the development of the Lamellibranchia, a stage
which more or less closely resembles the Trochophore larva of the
Annelida, and which has therefore received the same name (Ray
Lankester, Hatschek). This stage is most marked, as we should
naturally expect, when it is represented by a free-swimming larva,
such as is found among the marine Lamellibranchs [Teredo, Car-
dium, Mijtilux, Ostrea, etc.), but can be clearly recognised also in
other forms (Cyclas, Pisidinm). In the Unionnlap, the Trocliophore
stage has undergone much greater modification. Thus among the
marine Lamellibranchs we find, as a rule, that the primitive larval
form has been retained in a less specialised condition than among the
fresh-water forms, and this affords a further confirmation of a pheno-
menon which is very wide-spread in the animal kingdom. One fresh-
water Lamellibranch, however, Dreissemia polymorpha (evidently in
consequence of its late transference to fresh water) exhibits a larva
agreeing exactly with those of the marine Lamellibranchia (Kor-
schelt, No. 27, .Blochmann, No. 3, Weltner, No. 58).
The structure and development of the Trochophore larva have been
best investigated by Hatschek in Teredo ; in addition, Brooks and
Horst have published observations upon the larva of the Oyster,
and Loven upon those of various other Lamellibranchs (Modiolaria,
Cardium, Montacuta). The Trochophore stage of the fresh-water
Lamellibranchs has been carefully investigated in Ct/clas by Ziegler.
We shall here for the most part follow Hatschek' s account of the
larva of Teredo, since this form, of all those as yet known, most
clearly exhibits the Trochophoran condition. The larva of Ostrea
edulis which, with regard to the formation of the alimentary canal,
shows (according to Horst) a still simpler condition, agrees very
closely with Teredo.
A. The Trochophore stage as a free-swimming larva.
We have already (p. 25) described a few stages in the development
of Teredo, in which an epibolic gastrula is formed (Fig. 12 A-O).
Further changes begin by the overgrowth of the mesoderm-cells lying
at the edge of the blastopore by the ectoderm ; the former thus
become enclosed within the embryo, the blastopore closing in con-
THE TROCHOPHORE STAGE AS A FREE-SWIMMINQ LARVA.
31
Y.m.
sequence of the further growth of the ectoderm (Fig. 12 C). The
relation of the blastopore to the mouth which now forms could not
be established in Teredo, but the closure of the blastopore on the
ventral sick' seems to take place in the neighbourhood of the future
mouth. This latter arises at a somewhat later stage in the form of
an ectodermal invagination (Fig. 15 A). A comparison of this stage
with those that lead to the Trochophore shows us that the longitu-
dinal axis of the latter
is not identical with
that of the gastrula,
but apparently cuts
it at almost a right
angle. A similar con-
dition is found in
Ostrea (Fig. 14 A-E).
In the Oyster, the
blastopore does not
close, but becomes
carried into the in-
terior of the embryo
by an invagination of
the ectoderm, the
stomodaeum. The
blastopore thus per-
sists as the opening
between the stomodaeum and the enteron. The transformation
of the archenteron into the enteron of the larva can take place
more simply in Ostrea., inasmuch as the embryonic entoderm here
consists, even at an early stage, of a large number of cells (Fig.
14 A-D). In Teredo, on the contrary, the two large entoderm-cells
are retained for a very long time, only a few smaller entoderm-cells
becoming abstracted from them (Fig. 15 B). The development
of the enteric cavity and its close connection with the stomodaeal
invagination thus occur later (Fig. 15 U).* Consequently, the in-
testine of Teredo can only become capable of functioning at a much
Fig. 15. — A-C, embryos and larva of Teredo (after
Hatschek). The entoderm-cells are lightly and the
mesoderm-cells more darkly dotted ; a, anus ; d,
rudiment of the enteron ; dm, dorsal, vm, ventral
retractor muscles ; m, mouth ; s, shell-gland ; ah,
shell.
* The statement of Brooks that, in the American Oyster, the blastopore
closes and the mouth and anus appear as new structures in no way connected
with it, cannot be reconciled with the account given by Horst. We should
then have a condition such as is found in the fresh-water Lamellibranchia
{p. 40). Such a condition would have to be regarded as a specialised one, and
we should therefore the less expect to find it in the free-swimming larvae of
the marine Lamellibranchia.
32 LAMELLIBRANCHIA.
later stage than that of Osirea. The proctodaeum also seems to
develop earlier in the latter. In Teredo, according to Hatschek,
the terminal portion of the intestine arises as an ectodermal invagina-
tion at the -posterior end of the body (proctodaeum), which afterwards
becomes connected with the enteron (Fig. 15 C, a).
Even before the processes just described are completed, other im-
portant changes, especially affecting the external shape of the embryo,
have taken place. At the time of the formation of the stomodaeum,
the ectoderm began to separate from the entoderm, thus giving rise
to the primary body-cavity and at the same time causing a striking
alteration- in the shape of the embryo (Figs. 14 and 15). The latter,
which hitherto was almost egg-shaped, now broadens anteriorly, the
pre-oral part assuming the shape of a somewhat flattened cupola,
while post-orally the body tapers slightly ; in fact, the larva assumes
the shape with which we became familiar in the Annelidan Trochophore
(Vol. i., p. 265, etc.).
During this alteration in the shape of the embryo, the ciliation
characteristic of the Trochophore also appears, two rows of cells lying-
in front of the mouth and encircling the cephalic area becoming
covered with cilia (Fig. 15 ^4). The pre-oral ciliated ring consisting
of a double row of cells thus arises, but, in the following ontogenetic
stages of Teredo, this is the less distinct, as the whole body becomes
covered with cilia, most of which are lost again later. Then, only
the biserial pre-oral ciliated ring persists, while behind the mouth
are seen the first indications of a post-oral ciliated ring. These are
gradually continued towards the dorsal side until the closed post-oral
uniserial ciliated ring is produced (Fig. 18 w„). Between the two
rings, a zone of more delicate cilia is retained ; this is called by
Hatschek the ad-oral ciliated zone. Behind the anus, also, a small
ciliated area is found. A tuft of strong cilia or a single thick cilium,
found in many Lamellibranch larvae in the centre of the cephalic area,
makes the likeness to the Annelidan Trochophore, already produced
by the form of body and distribution of the cilia, still more striking-
(Fig. 18).
While the post-oral ciliated ring and the ad-oral zone no doubt
assist in the capture of food, the pre-oral ring is specially adapted for
locomotion. In accordance with this function it is always found
specially well developed in the free-swimming larvae, in which the
post-oral ring and the other ciliation may degenerate. This important
locomotory organ attains in many larvae so great a development that
the anterior part of the body carrying it projects beyond the rest of
THE TROCHOPHORE STAGE AS A FREE-SWIMMING LARVA. 33
the body. This becomes very pronounced at a stage when a slight
constriction of the body behind the pre-oral ring is found, as in the
Oyster depicted in Fig. 16.
Ir is this specially noticeable
part of the larval body thai
lias been called the velum.
it can, in later stages, be
retracted within the shell
by special muscles (ventral
and dorsal retractor muscles,
Fig. 16, vm and dm, and
Fig. 18), so that the larva
appears highly contractile.
In the anterior (pre-oral)
part, i.e., in the region of
the velum, the larva is
often more or less strongly
pigmented ( Dreissensia) ,
and has thus a peculiar and
striking appearance (Fig.
17 A).
ma .--
Fig. 16.— Larva of Ostrea edulis (from Ryder,
No. 46, after Huxley) ; a, anus; dm, dorsal
retractor muscle ; I, liver ; m, mouth ; ma,
stomaeli ; s, shell; sm, anterior adductor
muscle; ss, shell-hinge; Vet, velum; vrn,
ventral retractor muscle.
The velum is such a powerful locomotors organ that the larva is able to
swim with great rapidity in definite directions, and thus does not merely float
about in the water like many ciliated larvae. Such a swimming larva, in the
position in which it is usually seen at the surface of the water, i.e., with the
velum directed upward, presents a very characteristic appearance (Fig. 17 A).
The strong covering of cilia carries on an almost continual rowing°motion
When the larva is in this position, the whole of the upper part of the body is
covered by the velum. The large size of this organ in comparison with the
rest of the body can be distinctly seen in older stages of, for example the
Dreissensia larva (Fig. 17 C) in which the massive velum is extended far be-
yond the valves of the shell. In this form, the retraction of the velum is
assisted by the development of a median groove which divides the velum
into two and enables these two cushion-like halves to be folded together
The velum in this way has a peculiar double appearance which is most
marked when it is being extended, but is also evident even when it is fully
expanded (Fig. 17 B, and Fig. 20). The double velum of the Gastropoda is
thus recalled, and the resemblance is much more striking here than in the
reduced velum of Cyclas, in which Ziegler pointed it out (p. 45).
Most Lamelli branch larvae seem to leave the egg-envelope at a very early
stage, and either remain sheltered within the body of the mother for a Ion"
period, like Teredo and the European Oyster, or else at once enter on free
hfe. Tins latter is the case with the American Oyster and Modiolaria as well
as with Mytilm and Dreissensia. The minute and somewhat pear-shaped
D
34 LAMELLIBRANCHIA.
larvae of the last-named form are met with swimming freely on the surface of
the water before attaining the TrochopJwre stage as well as at that stage.
Before indicating further points of resemblance between the
Lamellibranch larvae and the Anne-lidan Trodiophore connected speci-
ally with the internal organisation, we must first draw attention to
a character, not hitherto considered, which distinguishes these larvae
at once from all other (non-Molluscan) larvae. This is the so-called
shell-gland. At a somewhat early period in O-strea, as early as the
^■astrula-stage (Fig. 14 B), in Teredo rather later, a part of the
ectoderm, which is somewhat thickened by the lengthening of its
cells, forms a trough-like depression on the dorsal surface near the
posterior pole (Fig. 15 B). This depression, which represents the
rudiment of the shell-gland, soon deepens considerably, so that it
appears like a blind tube (Figs. 14 G, and 22, p. 50), It has a
glandular character, inasmuch as its cells show the longitudinal
striation characteristic of many glandular cells : it soon also begins
to secrete a substance which can be seen as a thin integument over
the external aperture and the margin of the shell-gland (Figs. 14 C,
and 15 B). This is the first indication of the shell, and it is thus
seen that the latter in its earliest rudiment is unpaired.
In the further course of development the invagination of the
shell-gland flattens out again, first becoming induced to a shallow
depression covered by the rudiment of the shell (Figs. 14 D, and 23),
and later disappearing altogether. The shell at the same time in-
creases in size, and now, like a saddle, covers a part of the dorsal
and lateral surfaces (Figs. 15 C, 14 E, and 23 C). By the extension
of the shell over the sides of the larvae, the way is prepared for the
duplication of the former, and very soon a median dorsal dividing line
can be seen separating the shell into two laterally situated valves.
This line corresponds to the hinge-margin of the adult shell ; it is indi-
cated in Figs. 15 C and 14 A' by the straight line on the back of the
larva (';/'. also the method of formation of the definitive shell in
( 'ycla*, p. 43). The large size subsequently attained by the shell in
the free-swimming larva is to be seen in Figs. 1 (1 and 17 Z? and C.
Tlir shell is seen to project beyond the body, a condition only ren-
dered possible by the formation of the right and left mantle-folds
which has already taken place. These folds are formed as lateral out-
growths of the ectoderm, the outer layer of ectodermal cells being in
close contact with the shell, while the inner surface of the outgrowth
is separated from the keel-shaped ventral region of the larva by a
deep fissure — the mantle-cavity (Hatschek). The reader should
THE TROCHOPHOKE STAGE AS A FREE-SWIMMING LARVA. 36
A
B.
compare this with the formation of the mantle in Oyclas at a later
stage (p. 43).
The shell, in the condition just described, is already a real pro-
tection to the larva, for, .»n account of the contractility of the velum,
the whole body can he withdrawn between the two valves. The
shell increases in size as the larva -rows ; in Dreissensia concentric
bands of growth can soon be recognised, their number increasing
more and more with age. The growth of the larva of Dreissensia,
and also that of the larvae
of marine Lamellibranchs
before metamorphosis, is
very considerable.
It need hardly be speci-
ally pointed out that the
Trochophoreof theLamel-
libranchia and of the
Mollusca in general is, by
the possession of a shell,
distinguished in a very
noteworthy manner from
the Trochophore larva of
other groups. Thus we
see that, in spite of all
the important points of
agreement, differentiation
in a special, and, for the
Mollusca, characteristic
direction, takes place at
this early stage. Other
Molluscan characters
affecting the body of the
Trochophore externally,
are the foot which arises
as an outgrowth of the
body-wall between the mouth and the anus, and the gill-rudi-
ments, which are first indicated by papilla- or ridge-like outgrowths
of the ectoderm: but these changes will be dealt with later when
considering the transformation of the larva into the adult, Before
entering upon this subject, we have to describe an important char-
acter of the Trochophore larva itself, which marks still more strongly
its resemblance to the Annelidan Trochophore.
'u;- 17- — A-G, larvae of Dreissensia polymorphs, in
various positions: .1, surface view of the velum -
P>, antero-ventral aspect ; 0 (older larva), seen'
from the side (original) ; ,„, oral region ; s, shell.
The velum, especially in .1 , appears strongly pig-
mented. In/', retractors are faintly seen running
back from the velum.
36
LAMELLIBEANCHIA.
Restricting ourselves for the present to the ectodermal structures,
we find, in the centre of the cephalic area, beneath the strong flagella,
where such are present, an ectodermal thickening which, in form and
position, corresponds essentially to the neural plate of the Annelid
larvae (Fig. 18, sp ; ef. also Vol. i., Fig. 118, p. 265, and Fig. 120,
/ ^
feC
HV
*P§fflii
-k I
iM&'i
i I 7/7
\
\
1\
JTL.
•>vm.
Fig. 18. — Larva of Teredo (after Hatschbk). a, anus ; dm, dorsal retractor muscle ;
g, ventral (pedal) ganglion ; I, liver ; m, mouth ; me, stomach ; mes, mesoderm ; mu,
retractor muscles; n, head-kidney; ot, otocysts ; s, shell ; sp, neural plate ; vm, ven-
tral retractor muscle ; w, post-anal ciliated tuft ; wJt pre-oral, wIJt post-oral ciliated
ring.
p. 269, &c). From this thickening, which must be regarded as the
neural or apical plate, and which later yields the cerebral ganglia,
a system of peripheral nerves is said to extend. [In Ostrea there is
a distinct hut shallow depression formed in this thickened area during
the development of the cerebral ganglia.]
THE TROCHOPHORE STAGE AS A FREE-SWIMMING LARVA. 37
In the Annelidas Trochophore, a nerve-ring is found beneath the pre-oral
ciliated ring (Vol. I., p. 266). Such a nerve-ring is, as far as we know, not yet
demonstrated in the Laniellibranch larva, but, considering the great agree-
ment in other respects between the two larval forms, it is very probable that
it is present.
Besides the neural plate, there is, according to Hatschek, in the
larva of Teredo, another constituent part of the nervous system, viz.,
the rudiment of the ventral, sub-oesophageal ganglion, lying as a
large ectodermal thickening between the mouth and the anus (Fig.
18, g) ; this becomes the pedal ganglion of the Mollusca. Com-
missures between the two central organs of the nervous system which
would make the comparison with the supra-oesophageal ganglion and
the chain of ventral ganglia of the Annelida still more striking, have
not been found at this stage (Hatschek).
On either side of the ventral ganglionic mass, the otocysts arise
as small ectodermal invaginations in the same position as in the
Annelidan Trochophore (Fig. IIS B, p. 265). Fine hairs are attached
to their walls, and in the centre of each is a strongly refractive round
otolith (Fig. 18, ot)*
The eye-spots with lenses embedded in them, which Loven observed in a
few pelagic Laniellibranch larvae (e.g., Mytilus), apparently arise at a later
stage of development, i.e., after the larva has passed out of the actual Trocfaj-
phore stage. They then lie near the oesophagus, and thus behind the pre-
oral ciliated ring, and cannot therefore be compared with the eyes of the
Annelidan larva which lie on the cephalic area, i.e., in front of the pre-oral
ciliated ring.
[Pelseneer (No. IV.) has recently discovered that these eyes are retained
in the adult Mytilidae and in Arvicula, where they are situated at the base
and under cover of the anterior filament of the internal branchial lamella ;
they are innervated from the brain. They are not homologous with the larval
eyes of the Gastropoda, which occur on the velum, and are therefore true
cephalic eyes, but are possibly homologous with the larval eyes of Chiton
IP- 14)-]
The oesophagus and the base of the intestine of Teredo arose, as
has already been mentioned, as ectodermal invaginations (Fig. 15
A and C). Before they both become finally connected with the
enteron, the latter assumes a sac-like shape, through the active
* [Although arising near the pedal ganglia, the otocysts are innervated from
the cerebral ganglia, as in the Gastropoda. This primitive condition is still
to be seen in Xiicula and its allies, where also the otocysts retain, even in the
adult, their connection with the exterior by a long canal opening on the surface
of the foot. In other forms the nerve of the otocyst is bound up with the
cerebro-pedal commissure so as to be indistinguishable in the adult. — Ed.]
38 LAMELLIBRANCHIA.
growth ;md division of the large entoderm cells, which until now
have remained only slightly differentiated. These cells are, in Teredo,
retained in this primitive condition for a very long time (Fig. 15 B) :
it is evident that they contain, stored up in them, a rich supply of
nutritive material, which is gradually used up in the formation of the
larval body ; the presence of this food renders an early development
of the intestine, such as takes place in Oxfrea, unnecessary (Fig.
14). At first the intestine makes but a simple bend, and seems to
resemble in shape that of the Annelidan Troclwphore, but soon, as a
consequence of its elongation, it forms several coils (Fig. 18).
We have, so far, left out of consideration the primitive inesoderm-
rudiment and its derivatives, which are, nevertheless, of great import-
ance. According to Rabl and Hatschek, the symmetrically arranged
mesoderm-bands run forward from the two primitive mesoderm-cells
[mesodermal teloblasts] which at first lie near the blastopore and
afterwards (vent rally) at the sides of the anus. The constituents of
these mesoderm-bands are, as in the Annelida, yielded by the division
of the primitive mesoderm-cells, which long retain unchanged the
character of the blastomeres (Fig. 15). The mesoderm-bands of the
Lamellibranchia do not appear so distinct or so highly developed as
those of the Annelida, since, from an early period, cells bud off
from the main mass of the mesoderm which become distributed in the
primary body-cavity.* These give rise to the muscles of the larva;
the originally round cells lengthen, send out processes, and, finally,
by assuming a fibrous structure, produce the fibres of the retractor
muscles (Figs. 15 C, and 18). The retractors of the velum which
run from the posterior part of the shell to the cephalic area form first.
Then several shorter muscles are added, also running from the inner
surface of the shell in the region of the hinge, and finding points of
insertion in the post-oral region of the body (Fig. 18). These muscles
seem to serve chiefly for closing the shell (Hatschek), but this func-
tion is carried out principally by the muscles which, soon forming
from long mesoderm-cells, traverse the body -cavity dorsally to the
intestine, running from one shell-valve to the other. This shell-
adductor appears very early in the larvae of many Lamellibranchs
(Fig. 16, sm).
* [According to Lillie (No. III.), this larval mesoderm has in Unio an
origin quite distinct from the mesodermal teloblasts which form the mesoderm-
bands. The larval mesoderm has more the character of a mesenchyme, and
is situated in front of the blastopore, whereas the mesodermal teloblasts are
situated behind the blastopore ; the former gives origin to the larval muscles.
The position of the larval aud adult mesoderm is well seen in Figs. 22 and
2H .1.— Ed.]
THE TBOCHOPHOEB STAGE OF FRESH-WATEB LAMELLIBBANCHIA. 39
Quite near the mesoderm-bands, at their anterior end, an organ
is developed which makes the comparison of the Laruellibranch
Trochophore with the Annelidan larva almost complete, viz., the larval
or liead-kidney. According to the observations of Hatschek, who
tirst discovered this organ, it is a long tubular structure with a
narrow cavity (Fig. 18 n). In later stages it lengthens further; its
external end becomes applied to the ectoderm and opens on to the
exterior through a hue aperture. Its cavity is lined with fine cilia
directed outwards, and its inner end seems to widen out like a funnel
towards the body-cavity. This organ, which was also observed by
Zieglek in Cyclas, thus possesses all the peculiar characteristics of
the head-kidney found in the Annelidan larva. The same primitive
excretory organ is also found in the Trochophore of the Gastropoda
(p. 136).
Hatschek thinks it probable that, in Teredo, the canal of the larval kidney
(■"liimunicates with the hody-cavity, but Zieglbr was not able to convince
himself that this is the case in Cyclas. In the latter, the inner end of the
canal is lost in a mass of mesoderm-cells. Ziegler assumes that the canal
i> formed of large perforated cells such as occur in this organ in the Gastro-
poda.*
B. The Trochophore stage of Fresh-water Lamellibranchia.
Among the fresh -water Lamellibranchs, as has already been
pointed out (p. .'50), only Dreissensia has a free-swimming larva,
which, indeed, exhibits exactly the same characteristics as are found
in the Trochophore ami later stages of the marine Lamellibranchia.
For this reason, the larva of Dreissensia has already been considered
in the previous section (Fig. 17, p. .'55). A special resemblance
exists between the larvae of Dreissensia and those of Mytilus as
described by Wilson (No. oil).
The conditions found in Dreissensia form an interesting contrast to those
met with in other fresh-water Molluscs and to those of fresh-water Annelida,
Turbellaria and Hydrozoa, since all these forms have lost the free-swimming
larva. This is explained on the belief that Dreissensia, which is a near rela-
tion of Mytilus, has migrated from the sea into fresh-water only at a recent
date, and has consequently retained the free-swimming larva together with
other characteristics of a marine form, v. Martens (No. 34).
[The recent observations of Meissenheimer (App. Lit. Gastropoda, No.
XVIII.) on the head-kidney of Limax tend to show that there is no com-
munication between the lumen of this organ and the body-cavity. On the
other hand, Stauffacher (No. VII.) maintains that, in Cyclas, this organ
does communicate with the primary schizocoele. — Ed.]
40
LAMELLIBRANCHIA.
nes.''
nxr.y'
"0
- m
The other fresh-water Lamellibranchs show the Trochophore form merely
as one of the stages of their embryonic development, and in them, as
compared with the marine Lamellibranchia, it has greatly degenerated.
The fact that this degeneration has taken place is made clear by the compli-
cated form of the alimentary canal. In Cyclas and Pisidium, as well as in
the Unionidae, the blastopore closes ; the ectoderm then becomes separated
from the archenteron, so that there is now an entirely closed entoderm-
sac. This latter only becomes connected again with the ectoderm at a later
stage. This takes place
__ hrst through the stomo-
daeal invagination, whose
relation to the blastopore,
in consequence of the entire
obliteration of the latter,
has not been ascertained,
and then through the forma-
tion of the proctodaeunr'"
When the entoderm-sac
thus becomes connected
with the ectoderm at two
points, the rudiment of the
alimentary canal is formed.
This latter is probably
composed of the same con-
stituent parts as that of
the Trochophore, although
its formation has been less
direct.
The velum, that specially
important organ of the
Lamellibranch larva, is
very much reduced in those forms which do not swim about freely at the
Trochophore stage. In Cyclas, all that remains of the ciliated apparatus of
the Trochophore is a small ciliated area extending above and below the mouth
and at its sides. Ziegler has homologised this ciliated area with the ad-
oral ciliated zone of the Trochophore, and believes that the part of the velum
connected with feeding is partly retained while the part chiefly connected with
locomotion and which was no longer used has completely disappeared. The re-
duction of the velum has led to a corresponding reduction of the larval muscles.
It has already been mentioned that the larval kidney is found in
( 'yclas. Of the other Trochophoral organs, Ziegler was only able
stf
PS
\
~-f
Fig. 19.— Embryo of Cyclas cornea at the Trocho-
phore stage (com! lined from E. Ziegler's figures) ;
by, byssus ; eg, cerebral ganglion ; d, enteron ;
./', foot; in, mouth ; vies, mesoderm ; mr, rudiment
of the mantle ; pg, pedal ganglion ; sd, shell-gland ;
vd, stoinodaeum ; re/, velar area.
* The statements that the blastopore becomes directly transformed into the
anus (as in Pisidium, Ray Lankester) require confirmation, since the more
primitive Lamellibranchia show an entirely different relationship (p. 31).
Ziegler's account of the processes in Cyclas, indeed, seems to show that the
anus arises at the posterior end of the slit-like blastopore which has already
closed. A proctodaeal invagination seems in any case to be absent in this
form.
THE TRANSFORMATION INTO THE ADULT. 41
to demonstrate the presence of the mesoderm-bands, the shell-gland
and the neural plate.
The organisation of the embryos of fresh-water Lamellibranchs
just described renders it indisputable that they represent the Trorlm-
tfkore stage. As in Gyclas, so in Pisidmm this point can be proved ;
in the Unionidce, indeed, the modification has been greater, and it is
therefore very difficult to recognise in them the organisation of the
Trochophore. Even here, however, there is a remains of the ciliated
apparatus (Figs. 22-24, p. 53) which causes the well-known rotation
• >f the embryo within the egg-integument, but this ciliated area,
according to the definite accounts of Schierholz, Schmidt and
Goette, does not lie anteriorly, but in the posterior part of the
body, so that it cannot here be considered as a vestige of the velum,
as some have attempted to maintain, but rather as corresponding to
the ciliated anal tuft.
4. The Transformation into the Adult.
It will be seen from the foregoing account that the presence of a
free-swimming larva is to be regarded as an indication of a primitive
condition in the Lamellibranchia. We should consequently expect
to find in those forms that possess this ontogenetic stage that the
changes which bring about the transformation of this free larva into
the adult would also be of a primitive character. But, unfortunately,
the whole of the further development is not known in the case of any
marine Lamellibranch, so that we are obliged to confine ourselves-
chiefly to the fresh-water Lamellibranchia in discussing this subject,
although, as we have seen, we must, for the most part, regard
them as modified forms. In Cycfas, however, among the latter, the
Trochophore stage is distinctly developed, and we are therefore per-
haps justified in assuming that the process of metamorphosis has,
in this case, not undergone any very great modification. For
purposes of comparison, we shall avail ourselves of the few data which
have been obtained relating to the development of the marine
Lamellibranchs.
The mantle develops as early as the Trochophore stage in the
marine Lamellibranchia, and, with the shell, surrounds a large part
of the body. On each side, the mantle-folds are separated by a narrow
but deep fissure-like cavity from the keel-shaped body ( Teredo). The
foot is not to be seen at this stage (Fig. 18) ; it arises at a later stage
42
LAMELLIBKANCHIA.
.as a hollow outgrowth of the ectoderm into which a great mass of
mesoderm -cells find their why. The gills arise in its neighbourhood
•either as two ectodermal ridges one on either side of the body at the
point where the inner lamella of the mantle-fold is continuous with
the body-epithelium {Teredo and Gyclas), or else at the same spot as
a single row7 of papillae {Mytilus, Dreisse.nsia
and the Unionidae, and, according to Jackson,
in Ostreri).
In those stages of Gyclas and Pisidium
which must be regarded as the equivalents
nt' the Trochoj/horv, the foot has already
attained a considerable size. It occupies
the whole of the ventral surface between
the mouth and anus in the form of a massive
projection of the ectoderm (Fig. 19/). At
a later stage it extends in length and, in form
and position, shows the same relation to the
rest of the body as it does in the adult
(Fig. 21).
In the free-swimming larva, the foot is
already of considerable size. Although at
first merely a truncated structure projecting
only slightly below the shell, it soon grows in length, and can be
protruded far beyond the shell when it appeal's to make vermiform
movements and to function as a tactile organ (Fig. 20).
Fig. 20. — Older larva of
/hrissnisii'i jiiih/iiinr/ihii
(original). /, foot; m,
mouth ; s, shell ; v,
velum.
At this stage, therefore, the larva, besides its provisional locomotor}- organ,
the velum, also possesses the locomotor}' organ of the adult Lamellibranch.
Further, the foot usually, as far as we can judge from Dreissensia, is retracted
while the larva (which is still very active) swims about ; in this respect Fig.
20, which depicts the foot as extended in a larva with an expanded velum,
is not quite true to nature. Such a condition does, however, occasionally
occur when a larva has just extended the velum and is beginning to retract
the foot which was protruded beyond the shell as a sensory organ.
The surface of the foot, at the Trochophore stage as well as later,
is covered with fine cilia. At the posterior upper boundary of this
ciliated area, in Gyclas, a pit-like depression of the ectoderm is found
on each side of the middle line, lying exactly above the mass of cells
from which the pedal ganglion develops (Figs. 19 and 21). This is
the paired rudiment of the byssal gland.
THE TRANSFORMATION INTO THE ADULT. 43
These two depressions together with the whole of the ectoderm lying be-
tween them soon sink in deeper, having then only one common aperture;
their epithelium becomes modified into glandular cells which secrete the well-
known byssal threads that serve for the attachment of the embryo or yffung
Lamellibtanch (Fig. 21, by). As the body grows further, the paired rudiment
of the byssal gland is drawn further and further inward, and finally opens out
through a long duct with a narrow aperture. This gland degenerates later
(in Cyclas), and in the adult is a mere sac-like vestige. In other Lamelli-
branchs, on the contrary, as is well known, it functions throughout life and
is very highly developed (cf. p. 59).
In Entovalva, discovered by Voeltzkow (No. 57) living in the intestinal
canal of Synapta, at the posterior margin of the keel-shaped foot, a similar
structure was found, which is brought into use as the Lamellibranch moves
forward and attaches itself. From its position, it might well correspond to the
modified byssal gland but this requires further investigation. In Gastrochaena,
a Lamellibranch that inhabits a calcareous tube, there \s an attaching
apparatus in the foot consisting of ectodermal depressions surrounded by
glandular cells ; the secretion of the latter serves for attaching the broad sole
of the foot to the inner surface of the tube, but is said not to correspond to
the byssus which, according to Sluiter (No. 53), completely degenerates in
this animal. In Entovalva, the foot attains a very high degree of develop-
ment and the mantle grows over the shell (as also in Gastrochaena, cf. p. 62) :
in other ways the development of this parasitic Lamellibranch is not peculiar.
It shows typical Trochophore larvae, which develop in a brood-cavity formed
by the mantle ; they pass thence into the intestine of the Holothurian host,
reach the exterior with its excrement, and there develop further (no doubt
in the usual way): Not until fairly well developed do these young Lamelli-
branchs enter the mouth of a Holothurian and pass into the oesophagus.
At the time when the external form of the foot is already well
n the outer surface of the gill-plate, and ;t
corresponding series also appears on the inner side of the fold.
These grooves deepen until individual members of the outer series
meet and Fuse with the corresponding grooves of the inner series.
Perforation takes place along this line <>f fusion, and in this way
gill-slits arise which lie vertically to the longitudinal axis of the
branchial lamella. As the grooves start from the extreme venti'al
edge, the slit is open below, and the branchial plate becomes broken
up into filaments (Fig. 21 B).
We have here described the way in which the gills arise in the
two Lamellibranchs whose ontogeny happens to be best understood,
but this description does not apply to all Lamellibranchs ; indeed, it
is even probable that the condition described above is a specialised
one. Thus, in various Lamellibranchs which possess a typical Trocho-
phore larva, e.g., Mytilus, Dreissensia and Ostrea', the gills arise as
a row of papillae consecutively arranged, which become subsequently
connected together to form the gill-lamellae. The formative pro-
cesses which take place in these cases will be detailed below (p. 68).
[A third method which occurs in Scioberetia (Bernard, No. I.)
and Pholas (Singerfoos, No. V.) somewhat resembles that seen in
Oydas and Teredo. As in the latter, a gill-plate first appears, but
the gill-slits do not at first extend to the ventral edge of the fold,
consequently, perfectly distinct gill filaments are not formed, but
only gill-bars alternating with slits, the gill-plate retaining its
original continuity below the slits.]
In connection with the external form of the Lamellibranchia we
have still to mention the labial palps {oral lobes). These, in the
adult, are divided into an upper (anterior) and a knver (posterior)
pair. In Gyclas, according to Ziegler, they arise in the following
manner. The ciliated area surrounding the mouth becomes divided
into an upper and a lower portion by a gi'oove which runs out on either
.side from the angle of the mouth. The first of these must be reck-
oned as the upper and the second as the lower lip. These two areas
by further growth give rise to the labial palps. At the time when
the mantle grows down over the upper lip, a median depression ap-
pears in the latter, and a similar depression is to be found in the
lower lip, each of the lips being thus divided into two lateral portions.
These now begin to grow out as folds, and develop into the labial
palps.
[In most Lamellibranchs the two halves of the upper and lower
lips are connected by bridges above and below the mouth, the divi-
46 LAMELLIBRANCHIA.
sion into right and left palps being more apparent than real. This
condition appears to be brought about by the stronger growth of the
lateral parts of these structures.]
This origin of the labial palps partly confirms the assumption made by
Loven that the velum of the larva may pass over directly into the adult
palps. In the double nature of this organ Lovkn finds agreement with the
double velum of the Gastropoda, a resemblance which is strengthened by
Ziegler's observation of the median division of the ciliated area of Cyclas.
The small section of the ciliated area lying above the mouth might then
be regarded as the last vestige of the former ciliated ring of the Twcho-
phore. The ciliated area of Cyclas, however, as we have just shown, seems
rather to correspond to the ad-oral ciliation of the larva (p. 40). And since
this serves for feeding more than for locomotion we see that a part of the larval
body passes over into a similarly functioning organ of the adult animal.
The significance of the labial palps lies principally in their relation to the
capture of food, in which they assist through their position and their ciliation
(Thiele, No. 55). An exact knowledge of the fate of the entire velum, i.e.,
of the pre-oral ciliated portion of the body in a marine Lamellibranch, would
be of great value.
The metamorphosis of the Lamellibranch larva into the adult is
characterised chiefly by the complete degeneration of the pre-oral
part of the body which was so large in the former. In the larva, the
highly developed velum spreads out between the mouth and the
shell (Figs. 15-18, pp. 31-36 and Fig. 19, p. 40), but, as develop-
ment proceeds, this area becomes contracted (Fig. 21 A), and finally
almost entirely disappears, in keeping with the condition of the
adult, in which the cephalic region is almost completely lost.
While the external changes of form just described have been taking-
place in the embryo, a marked advance has also taken place in the
inner organisation, but this will be entered into later on. The young
of Cyclas and Pisidiwm leave the mother only when they possess, on
the whole, the same organisation as the adult.
Divergencies in the Metamorphosis accompanying the Monomyarian
Condition.
Among those forms classed by the older malacologists as the
Monomyaria, the transition from the larva to the adult has only been
well investigated in Ostrea, and their development, judging from
this form, seems up to a certain point to agree closely with that of
other marine Lamellibranchia. We have already seen how close the
agreement is in the early stages of development (p. 28 Fig. 14
and Fig. 16. p. 33). The Trochophare larva already possesses an
DIVERGENCIES IN THE METAMORPHOSIS, ETC. 47
adductor muscle (Fig. 16, stri), formed from elongate mesoderm-cells
which become arranged side by side and attached to the two valves
of the shell. This adductor in Ostrea lies dorsally to the alimentary
canal, and thus corresponds in position to the anterior adductor of
the Dimyarian forms, which also lies dorsally to the oesophagus (Fig.
31, vsm, p. 7-r>). The adductor in the adult Monomyarian, how-
ever, lies ventrallv to the intestine (Fig. 31, hsm) ; it thus occupies
the same position as the posterior muscle in the Dimyaria, and is
undoubtedly to be homologised with this latter. The adductor of
the larval oyster therefore cannot he the same as that of the adult.
This difference, which has been emphasised by several investigators
(Huxley, Hokst, etc.), is explained by the study of the later
development (Jackson, Nos. 22 and 23.)
A larval stage in which only one adductor muscle (the anterior) is-
present, or in which the anterior adductor is better developed than the
posterior adductor, which is only in the act of appearing, is met with in a
large number of Lamellibranchs, e.g., < 'ardium, Montacuta, Mortlolaria,
Mytilus, Dreissensia, Pisidium. In the Unionidae also the anterior
adductor seems to appear first, as, indeed, is the case in nearly all
the Lamellibranchs as yet investigated in this respect.
In Cyclas, on the contrary, according to Ziegler, the posterior adductor
develops before the anterior, but it has already been pointed out that in the
related form, Pisidium, the anterior appears first. Lacaze-Duthiers (No. 28)
maintained that the posterior adductor develops first in Mytilus, but this
is due to the fact that the larval stages examined by this author as well as by
Loven (No. 33) were too old. According to Wilson (No. 59), in the young
Mytilus larva the anterior adductor develops earlier than the posterior, and
this is also the case in the nearly related form Dreissensia (Korschklt,
No. 11).
After the anterior adductor has appeared in Ostrea, a posterior
adductor lying ventrally to the intestine arises in the same manner
as in the Lamellibranchs mentioned above (Jackson). Ostrea, and
no doubt the other Monomyaria as well, possess for a time two
adductors (an anterior and a posterior) of almost equal strength, and
thus resemble the Dimyaria. Only as the anterior of these two
muscles degenerates does Ostrea assume a Monomyarian condition.
Even if the Lamellibranch larvae do for a time possess only one ad-
ductor, we have no right to speak, as has often been done, of a Monomyarian
stage, and to consider the permanent condition of the Monomyaria as having
arisen through an arrest of development in this direction, i.e., through the
defective development of a second muscle. The Dimyaria hence do not pass
through a Monomyarian stage in the proper sense of the term, but the
48 LAMELLIBRANCHIA.
Monomyaria probably invariably possess in youtb the two typical adductors
of the Dimyarian.
[The fact that the anterior adductor almost invariably appears
before the posterior, not only in the Dimyaria, but also in the
Monomyaria, in which latter group it is only a larval structure,
might seem to suggest that this muscle was a phylogenetically older
structure than the posterior adductor, and that the Lamellibranchia
•were originally Monomyarians, not, like the existing Monomyaria,
with a single muscle represented by the posterior adductor, but with
the anterior adductor alone developed (Jackson). Palaeontology
does not, however, bear out this view ; the oldest known Lamelli-
branchs found in the Cambrian belong to the Nuculidae and Arcidae,
which are typically Dimyarian.]
The young of Ostrea agrees, not only in the possession of two ad-
ductors, but also in other points of its organisation, with the larvae
of other Lamellibranchs, but at a later stage it changes from a free
to an attached manner of life.
The larva, which has hitherto swum about freely, possessing two
quite symmetrical shell-valves and two adductor muscles, attaches
itself by means of a secretion produced by the left lobe of its mantle ;
the latter stretches beyond its valve, and, applying itself to the stone
or shell to which the valve is to adhere, secretes shelly matter which
serves to cement the valve to its support (Huxley, Ryder). In the
further development, we now from this time find an inclination to
that radial symmetry which can be recognised in the adult Oyster,
and which is often found in animals that assume an attached manner
of life. The anterior adductor now degenerates and the only remain-
ing adductor muscle (the posterior adductor) enlarges and shifts
ulmost to the centre of the animal. The anterior part of the body
gradually rotates (round its vertical axis) * through an angle of
about 90°, so that the mouth, which at first lay very near the free
edge of the shell, comes to lie near the umbo. This rotation also
explains the great and almost circular extension of the gills and the
mantle found in the adult. The condition of the foot in the Lamelli-
branchia depends largely upon its use or disuse. In Ostrea, the shell
becomes permanently attached at the close of the free-swimming
Trochophore stage ; the foot is therefore unnecessary before fixation
* [Vertical in relation to the substratum, the true transverse axis of the
animal. This rotation is possibly due in large measure to tbe degeneration
of the anterior adductor muscle and of the velum. — Ed.]
THE DEVELOPMENT OF THE UNIONIDAE. id
and useless afterwards, and has almost entirely disappeared from
even the embryonic stages of growth (Jackson). In Pecten* another
Myomyarian, <>n the contrary, the foot is very well developed in the
nepionic period, and serves as a locomotor^ organ ; during metamor-
phosis it becomes considerably reduced though, with its byssal gland, it
is still present in the adult, but no longer serves as a locomotory organ,
since the animal now swims by clapping its shell-valves together.
In other Lamellibranchs also, viz., those forms which spend the
greater part of their life attached to some foreign body, e.g., Dreis-
sensia polymorpha, the foot which, at first, is very large (Fig. 20,
p. 42), becomes very much reduced in size as the animal develops.
After the velum has degenerated and before attachment, Dreissensia
passes through a stage in which it creeps about very actively with
the help of its foot (No. 27). This form at a later stage also occa-
sionally moves about, Vint, in consequence of the great redaction
of the foot, its movements are very slow (No. 58).
[In those Lamellibranchs which, in the adult stage, lead a fixed
life, attached by means of a byssus to the substratum, the portion of
the foot carrying the byssal gland is retained, although the loco-
motory function of the foot may be completely lost, e.g., Anomia.
In Ostrea, where the attachment is brought about by a secretion of
the left mantle-lobe, all trace of the foot is lost in the adult.]
5. The Development of the Unionidae.
The development of the Unionidae differs so essentially from that
of the other Lamellibranchia that, except with regard to the cleavage
of the egg, it must be treated separately. It has evidently under-
gone radical modification through change of the external conditions
of life, and the whole of its later development is no doubt influ-
enced by the assumption of a temporary parasitism by the young
or larvae, which become attached to the gills or to the integument
of fishes. We thus find, in the Unionidae, superadded to the normal
course of development, as observed in the marine Lamellibranchs, an
additional and unique larval form which cannot be compared with
the larva of the latter, and which possesses characters not present
in the adult.
* The development of Pecten has been investigated by Fullarton, from
whose treatise, which is illustrated by four plates (No. 14), we gather that
this form develops exactly like other marine Lamellibranchs up to the later
larval stages. The transformation of the larva into the adult was not observed.
E
50
LAMELLIBKANCHIA — UNIONIDAE.
The ontogeny of the Uniunidae has been studied by a number of
zoologists. Flemming, Eabl, Goette and Schierholz have in-
vestigated their embryonic development, while the later stages of
their development, which were examined by Forel (No. 13), Lbydig
(No. 32), Braun (Nos. 4 and 5), Balfour, F. Schmidt (No. 50)
and others, have recently been reinvestigated by Schierholz and
Goette.
[Still more recently, Lillie (No. III.) has reinvestigated the entire
course of development in Unto complanata, paying special attention,
however, to the cell-lineage.]
the cleavage-cavity
JB-
mes
A. Development of the Early Stage.
It has already been mentioned that the Unionidae show an in-
vagination-gastrula (p. 27, etc.) and that, before the latter develops,
large mesoderm-eells bud oft' from the wall of the blastula and enter
Before the formation of the very insignifi-
cant archenteron
which, like that of
other Lamellibranchs,
is derived from the
macromeres resulting
from the unequal
cleavage, a depression
appears on the blastula
and deepens more and
more (Fig. 22, sd).
This depression is
formed by large cells
which are granular
and therefore appear
dark, and its whole
form is such that we
can easily understand
why it was long mis-
taken for the archen-
teron (p. 27). This depression, however, does not occur on the ventral
side of the embryo, but upon its dorsal surface ; it gradually flattens
out again and above it the shell-integument appears (Figs. 23 A-C, 24
A). This structure is therefore, as Goette proved, the shell-gland.*
* [According to Lillie (No. III.) the entomeres which eventually become
invaginated fco form the archenteron are derived from all the four cleavage-
*d?~-'
mes
Fig. 22. — Embryo of Anodonta in the vitelline mem-
brane (after Schierholz) ; ent, entoderm-rudiment
(archenteron) ; eh, vitelline membrane ; m, micropyle;
mes, mesoderm-cells. some of which have turned into
muscle-cells ; rk, polar bodies ; sd, shell-gland ; sz,
lateral cells ; w, posterior ciliated area [ventral plate].
DEVELOPMENT OF THE EARLY STAGE.
51
The shell forms in exactly the same way as in the marine Lamellibranchs
(Figs. 14, p. 28, and 15, p. 31) and in Cyclas (Fig. 19, p. 40), except that
the shell-gland is specially large and appears very early. This early develop-
ment of the shell, as suggested bj GtOETTE, is probably due to the great im-
portance of the shell to the larva in its free life which we shall discuss later,
and, in the same way, we may explain the degeneration of the intestine by
the parasitic life of the larva, in consequence of which the intestine is not
required to fulfil its ordinary functions until a late stage.
In spite of the highly modified character of the larvae of the
Unionidae, we are able to make a comparison between their organs
and those of the typical Trochophore larva. Apart from the ento-
dermal and mesodermal parts which have already been mentioned
a.
cB.
c.
sdr'
~r%.
FlG. 23. — .1-' ', embryos of .1 nodonta piscinalis, median optical section (after Goette) ;
e, entoderm-rudiment (arehenteron); m, mesoderm ; rk, polar bodies ; s, shell; sd,
shell-gland ; sm, adductor muscle ; w, posterior ciliated area [ventral plate].
(pp. 27 and 28), the most striking feature is the ciliated area (Figs.
22-24, w), which is evidently the last vestige of the ciliation of the
free-swimming larva. This ciliated area, termed the ventral plate,
does not, as was at first supposed, correspond to a remains of the
velum, but represents the whole ventral surface plus the posterior
end of the body, and is therefore rather to be compared with the
ventral ciliation or with the anal ciliated area of the Trochophore
spheres resulting from the first two divisions, that is to say, neither the first
nor the second cleavage-plane divides the egg into an animal cell and a vege-
tative cell as stated by Rabl. Lillie further finds that the small arehenteron
is formed before the invagination of the shell-gland, which latter, however,
soon eclipses the former. Of the two groups of mesoderm-cells represented
in Figs. 22 and 23 A, those above the shell-gland would correspond with
Lillie's larval mesenchyme, while those below this structure and behind the
blastopore, e.g., the large cell in Fig. 23 A, represent the adult mesoderm
which forms teloblastically from the pair of mesoderm-cells. For more
detailed figures see Lillie's paper. — En.]
52 LAMELLIBRANCHIA — UNIONIDAE.
larva (Figs. 15 and 18). The broad part of the body in the embryo
of Anodonta which lies in front of the shell and of the entodermal
vesicle would correspond to the velum, i.e., to the pre-oral part of
the Trochuphore. In the younger embryo depicted in Fig. 22, this
part appears to be formed solely by a somewhat thin layer of cells,
while, in the embryo represented in Fig. 24 A, it has a thick wall,
consisting of cells containing vacuoles such as Ziegler has described
in the reduced velum of Cyclas, The shape of this part of -the
embryo recalls the swollen pre-oral portion or cephalic vesicle of the
Gastropodan embryos, a condition still more marked in them than in
Cyclas, as Ziegler pointed out. [Lillie also regards this area as
the head-vesicle].
In this region of the embryo, the polar bodies are occasionally met
with (Figs. 22 and 23 C) and these afford an indication for the
correct orientation of the embryo which is not otherwise very easy to
determine, and which was usually misinterpreted by the earlier
investigators.
B. The Development of the Embryo into the Parasitic Larva.
It is evident from the above that the peculiarities in the develop-
ment of the Unionidae appear very early and affect both the inner
and the outer organisation of the embryo. In the stage up to which
we have followed its development, it resembles a rounded vesicle of
somewhat irregular form consisting of a single layer of ectoderm on
the inner side of which there appear here and there single muscle-like
cells ; these belong to the mesoderm, the cells of which have increased
in number, some becoming lengthened (Figs. 23 and 24). In this
young embryo, the shell at first lies like a saddle upon the dorsal
side (Fig. 23 C, and 24, s).
The rudiments of the shell-valves appear later beneath the
unpaired cuticular shell. The shell probably arises here in the same
way as in Cyclas ; each shell-valve in the Unionidae appears to be
three-sided and has its ventral point bent like a hook, a modification
connected with the manner of life of these forms. The shell carries
on its outer surface a number of small hooklets which, together with
the two terminal hooks just mentioned, serve for attaching the
Lamellibranch to the body of its host during its parasitic life (Figs.
2o and 2(i, sh). Before the shell has developed thus far, a radical
transformation of the whole body takes place. The ventral part
of the body, which was not previously covered by the shell but
THE DEVELOPMENT OF THE EMBRYO INTO THE PARASITIC LARVA. 53
projected beyond it (Fig. 24 />'), now becomes withdrawn or rather
invaginated towards the hinge of the shell, i.e., towards the dorsal
side (Fig. 25 A), and the whole body is thus divided into two halves,
each belonging to one of the valves of the shell (Fig. 25 A and B).
The mantle arises in this way and at this stage is remarkably large,
greatlj preponderating over the rest of the body, which only later
redevelops bv the outgrowth of the central portion of the body (Fig.
25).
Before the withdrawal of the central portion of the body, four groups
of bristles were developed from the ectoderm on either side of the
embyro (Fig. 24 B, -so) ; during the invagination-processes just described
these organs lengthen and, in consequence of these changes, are then
R
B.
mes
->TO.
Fig. 24. — Embryos of Atwdonta. (.1 founded on a figure by Flemming, somewhat
diagrammatic, /I alter Schikrhulz). .1, optic section with the outline of the shell
superimposed ; B, superficial view; eat, entoderm (archenteric rudiment); mes,
mesoderm ; s, unpaired shell ; sd, shell-gland ; so, sensory bristles ; w, ciliated area
[ventral plate].
found on the inner surface of the mantle. Each of these organs
consists of a long columnar cell which gives origin to a number of
long and fine sensory bristles (at first four to ten in number, later as
many as thirty) that perforate the thin ectodermal cuticle (Flemming).
These sensory organs are apparently of importance to the larva in the
process of attaching itself to the fish-host and are acquired at a late
embryonic stage.
We may accordingly regard these sensory organs as differentiationE
of the mantle, and can hardly consider them to be related to the
velum, as Schierholz was led to believe on account of the position
of one of them. This particular organ occupies an isolated position
and has shifted in front of the oral aperture (Fig. 26 A).
54
LAMELLIBRANCHIA— UNIONIDAE.
These peculiar organs are believed to communicate to the larva the stimu-
lus produced by coming into contact with a fish, and thus to give rise to the
muscular movements which cause the shell-valves to close and the larva to
become hooked on to the host.
There are a few more important organs to be mentioned in
connection with the further development of the larva of the
Unionidae, the first of these being the powerful adductor muscle
of the shell. This arises very early through the increase in number
of the mesoderm-cells, which are still only slightly differentiated
[larval mesenchyme, Lillie] (Fig. 23 0, sm), these cells lengthening
and becoming attached to the shell-valves. The short but broad
muscle thus passes through the body-cavity from one valve to the other
(Fig. 25 B, sm). Besides this large muscle, there are a number of
B.
J
lx-sh.
¥^IXU
Fig. 25. — Older embryo (within the egg-envelope) and free larva (Glochidium) of Ano-
donta (after Schierholz and Forel). /, larval filaments; g, lateral pits.; s, shell;
sh, shell-hooks; sm, adductor muscle; so, tufts of setae representing the sensory
organs ; w, ciliated area.
other weaker muscles in the form of long mesoderm-cells attached in
various directions to the ectoderm, like the muscles which, in the
Trockophore, bring about the contractions of the larval body.
Schierholz [and Lillie] ascribe to the continuous contraction of
these muscles the withdrawal of the central part of the embryo above
mentioned. There are also, according to Schmidt, special muscles
in the form of modified mantle-cells connected with the shell-hooks.
A peculiar and characteristic larval organ arises in the median line
between the two halves of the mantle as an invagination of the
ectoderm (Babl). It grows inwardly as a long glandular tube which
coils several times round the adductor of the shell and secretes a
filament of tough substance which projects from the aperture of the
gland (Figs. 25 B and 26 A,f). This organ has been regarded as
THE DEVELOPMENT OF THE EMBRYO [NTO THE PARASITIC l.\U\ \. 55
a byssal gland corresponding to the homonymous organ of other
Lamellibranchs, but this view, in spite of the similar function of the
two organs, is not justified, since the two organs do not agree in
position, and since two ectodermal invaginations appear later on
the foot of the larva which must be considered as the homologues
of the byssal -land (Carrier^, F. Schmidt, Schierholz). The
glutinous filament must therefore be regarded as a distinct larval
organ.
The position of this filament is very remarkable in so far as it is
said to be pre-oral (Fig. 26 A). The mouth has been pressed un-
usuallv far hack and. like the intestinal canal (//), now belongs to the
small posterior part of the larva. This displacement has been traced
to the o-reat development of the adductor muscle (sm), hut the
morphological conditions of this larval stage as compared with
the former 7T/W,^//o/c-like stage seem to us to require further
elucidation.
[Lillie (No. III.) describes the thread-gland as arising from one of
the cells of the head-vesicle ; this cell elongates and grows backward
beneath the hinge-line until it reaches the posterior end of the body.
The cell now becomes tubular, the thread occupying the lumen of the
gland. Lillie believes that the thread is formed as an actual meta-
morphosis of the substance of the cell ; he regards this gland as
primarily excretory, and thinks that the utilisation of its secretion
as an attaching filament was secondarily acquired. During the
transformation of the larva into the Glochidium, the aperture of the
thread-gland undergoes a remarkable change in position, shifting
from its former antero-dorsal situation to the middle of the ventral
surface.]
Between the brush-like sensory organs and the ciliated area and near the
posterior angle of the valves, two ectodermal depressions are to be seen on
the embryo; these are the so-called lateral pits, as to the significance of
which authors are not very clear. If we rightly understand the somewhat
obscure description given by Schierholz, he implies that large cells at the
base of these pits (no doubt corresponding to the lateral cells of the young
embryos) give rise to the pedal ganglia. But since the pedal ganglia, as in
las, lie° below the depressions which yield the byssal gland, these early-
t. Mined pits may be related to the latter (?). In Cyclas also the paired rudi-
ment of the byssal gland appears very early (Figs. 19 and 21). Taking these
facts into consideration, together with the position of the pits with relation
to the foot, it is possible that this interpretation of the lateral pits as the first
rudiments of the byssal glands is correct. The formation of the actual b\ ssal
gland in Anodonta, however, seems to take place at a later stage.
56 LAMELLIBRANCHIA — UNIONIDAE.
When the embryo has attained the stage of organisation just
described, it is ready for ejection from the mother ; on coming into
free contact with the water, the egg-envelope bursts and the embryo
emerges from it. The larva thus set free is known as the Gloehidium.
The embryos found by the older investigators (Rathke, Jacobson)
in the gills of Lamellibranchs and considered to be parasites were
called Glochidiv/m pavasiticum.
The remarkable fact that the Glochidia remain for a time parasitic
on fishes was discovered by Leydig (No. 32) and then further in-
vestigated by Bkaun. F. Schmidt and Schierholz have recently
given a detailed description of what takes place, and we shall here
follow chiefly their account. The larvae, when freed from the mother,
become connected together in large masses by means of their glutinous
filaments, and in this form rest at the bottom of the water, occa-
sionally rotating upwards.* Chance brings them no doubt into
contact with fish, and a few of them succeed in attaching themselves
to these by the help of their shell-hooks. Unio only attaches itself
to the gills of fish, but the Glochidia of Anodonta, which are more
richly provided with hooks, may also become attached to the fins and
the skin.
The hook-apparatus, according to Schierholz, is less developed in Unio,
and it is an interesting fact that it may be altogether wanting in certain
North American Unionidae (Lea). The same is the case, according to v.
Jhering's recent observations (No. 25), in the larvae of Soutli American
Unionidae, which are devoid of the tufts of setae, and perhaps also of the
larval filament. In these American Unionidae, therefore, the biological con-
ditions seem to differ somewhat from those of the European forms, and it
would be interesting to ascertain the conditions of parasitism in the larvae of
these Lamellibranchs. t The larval filament and the shell-hooks are wanting
in the Gloehidium of Anodonta complanata, although in other respects the
organisation of these larvae is the same as that of other Glochidia, and they
lead a parasitic life (Schierholz).
■ [It is often stated that the Glochidia arc only discharged when fish are in
the neighbourhood, but Latter (Proc. Zool. Soc, 1891) found that he could
produce a discharge of Glochidia by gently stirring the water in which the
Anodons were lying. He also observed cord-like ejection of Glochidia from an
undisturbed Anodon in its native water. The Glochidia cannot swim, but
when discharged sink to the bottom, where they lie on their dorsal surfaces,
the thread streaming up into the water. In this position the Gloehidium lies
powerless to move in any direction, and here, too, it dies unless a suitable
" host " is brought into contact with its thread. — Ed.]
t We do not know of any other statements upon this subject, although it is
not impossible that such may exist among the mass of malacological literature
which is difficult to review ; v. Jhkring mentions that he found Unionid
larvae on fish in Soutli America.
THE TRANSITION TO THE WHI/r. 57
A cyst Boon forms From the tissues of the fish and encloses the
parasitic Glochidium. A peculiar mushroom-like growth formed by
large cylindrical rolls of the embryonic mantle serves for absorbing
the tissues (if the host, and especially the tin-rays in which the shell-
hooks are embedded. The larva is no doubt nourished in this way
until its intestinal canal becomes functional.
'The time during which the Glochidium remains parasitic on the
fish appears to be determined by the favourable or unfavourable
conditions of temperature, and varies from a few weeks to several
months. Schierholz and Beaun found that the larvae remained
seventy-two to seventy-three days on the fish, during which time
they develop the definitive form.
The South American relations of our Anodonta have larvae differing greatly
in shape, so that v. Jhering, who found these larvae within the mantle-cavity
of the parent, would have taken them for parasites had not all doubt as to
their being Lamellibranchs been removed by the agreement of the egg-
envelope and its micropyle with the envelope of the ovarian eggs (No. 25). In
these forms the embryos are found in the inner gills, not, as in our native
Uwionidae, in the outer gills. The body in the South American forms is com-
posed of three sections : (1) a conical anterior portion covered with cilia ;
(2) a large middle portion containing internally the entoderm-elements and
two kidney-like structures (byssal glands ?) ; the dorsal side of this region is
only partly covered by a delicate shell-integument; (3) the short caudal end.
which forks, and consequently terminates in two rounded prominences, beset
with bent hook-like setae.
A very peculiar organ possessed by these larvae is a very thin but broad and
rlat band considered by v. Jhering to be the byssus. This band is almost at
the middle of the body and is attached to the ventral surface, from which it
runs forward. It is somewhat broader than the body, and six to ten times as
long. It is said also to be connected with the anterior part of the body.
According to the somewhat vague account given by v. Jhering of the larva
named by him "Lasidium," and in the absence of any statements as to the
development of this larval form, it is at present impossible to compare it with
the entirely different Unionid larvae (Glochidia) or with the larvae of other
Lamellibranchs.
C. The Transition to the Adult.
Very soon after attachment, as early as the second day. the larval
organs which enabled the Glochidium to establish itself on its host, viz.,
the glutinous filament and the brush-like sensory organs, degenerate.
A wide pit like depression of the ventral surface arises behind these
organs as they degenerate ; this depression involves the two lateral
pits already present in the embryo (Fig 2<> A and B} g). At this
58
LAMKLLIHKAXCHIA — UNIONIDAE.
Sc.
place, the foot now appears as a blunt cone and soon grows rapidly.
The wall-like outer margins of the two lateral pits also increase in
height. These prominences become the rudiments of the gills which
first appear in the form of two knobbed papillae (F. Schimdt).
Fig. 26 C shows the rudiments of the gills at a somewhat later
stage. The foot is here
found well developed,
and both it and the
gills are ciliated. The
posterior ciliated area
of the embryo (ic),
which was still visible
when the foot had
attained a considerable
size, now disappears.
Of the larval organs,
the shell-hooks and the
large adductor muscle
are still to be seen.
The first are for the
present retained, the
shell in other respects
also retaining its em-
bryonic form until the
young Lamellibranoh
leaves the fish ; indeed
( be embryonic shell can
still be made out in tbe
shell of the adult. The
longer of the two free
sides of the three-sided
embryonic shell must
be considered to corre-
spond to the anterior
end of the animal, and
in this position it can
actually be found as a small prominence on the umbo of the adult
shell (Braun).
The powerful adductor muscle of the larva agrees in position with
the anterior adductor of the marine Trochophore larva. It is, accord-
in- to Braun and F. Schimdt, merely a larval organ, and degene-
Fig. '35. — A~0, larvae of Anodonta (after Schierholz).
d, rudiment of the intestine ; /, larval filament ;
fu, foot ; ,'/. lateral pits; /. , gills; m, mouth; sh,
shell-hooks ; sm, adductor muscle ; so, sensory
organs ; w, ventral plate (ciliated are.:!.
THE TRANSITION TO THE ADULT. 59
rates completely later, so thai the two adductors of the adult must
be regarded as new formations. In opposition to this view we have
the statement of Schierholz that the larval muscle only partly
degenerates, some of it passing over into the anterior adductor of
t lie adult. This latter condition would agree with the fact that the
anterior adductor appears first in most Lamellibranchs, and for a long-
time is the only adductor present (p. 48) ; Braun, however, has
maintained his original view against that of Schierholz.
The formation of the intestine is also apparently greatly influenced
by the specialised conditions of the larva. The archenteron had
already lost its connection with the ectoderm before the commence-
ment of parisitism, and lay in contact with the ectoderm as an
entodermal vesicle closed on all sides. In this condition it remains
for a very long time ; the larva either does not require nourishment
or obtains it as described above through the mushroom-shaped growth
of the mantle. The small entoderm-vesicle is now found in the pos-
terior part of the larva lying rather closely applied to the ectoderm.
The swelling carrying an invagination known by authors as the oral
shield (Fig. 26 A, m) has also shifted posteriorly. The sac of the
oral or middle shield of authors is the rudiment of the stomodaeum,
and appears as a transverse slit (Fig. 26, m). By the development
of the foot this organ is pressed forward. The entoderm-vesicle also
lengthens from behind forward and fuses with the ectodermal rudi-
ment of the stomodaeum. At the posterior end where the entoderm
vesicle is in contact with the ectoderm, the anus now breaks through,
without the formation of an ectodermal invagination (F. Schmidt,
Schierholz). The formation of the other organs, in so far as they
present peculiar features, will be described later.
When the young Lamellibranch leaves the fish, it moves about
with great activity by means of its foot, which has in the meantime
become perfected, having lengthened very much and become geni-
culate. On its lower surface it carries a groove which represents tin1
rudiment of the byssal gland. The latter arises, as in Cyclats, in the
form of two pits situated posteriorly on the pedal swelling. In conse-
quence of an invagination which forms later, these pits come to lie at
the base of a funnel-shaped pit which is afterwards continued into
the longitudinal groove just mentioned. The persistent byssal gland
of other Lamellibranchs exhibits similar morphological conditions
to those already described in connection with the (Jnionidae and
i 'yclas.
t>o
LAMELLIBRANCHIA.
6. The Formation of the Organs.
A. The Shell.
The shell, as in the Gastropoda, is unpaired in its origin, and is
formed by a secretion of the epithelium of the shell-gland (Figs. 14,
]). 2rhi>jihor. 40), at tlie point where it is
to form, a number of cells become detached from the ectoderm.
These at first lie beneath the floor of the invagination, but then
separate from the latter and shift further forward, at the same time
coming closer together, forming the rudiments of the pedal ganglia
(Fig. 21 B, p. 44, and Fig. 31, p. 75).
In Teredo, the pedal ganglion, according to Hatschkk, arises as an
ectodermal thickening even before the foot begins to form (Fig. 18,
g, ]). 36). It oecupies at first a large part of the ventral surface.
but appears to decrease in size after its detachment from the ecto-
derm. During its severance, the mesoderm grows round it. The
division into two parts is not SO distinct here, but is indicated by a
median line. The two halves of the ganglion are thus in this case
connected from the first. When the foot rises up and grows out on
the ventral side of the larva, the ganglion remains lying at its base.
In their manner of formation the rixri-rtil ganglia agree closely with
the cerebral and the pedal ganglia. They arise in the groove
between the gills and the body, almost at the posterior end of
the foot.
The cerebro-visceral pleuro-iyisceral\ commissure has its origin,
according to Zieglek, in a cell-strand which becomes detached from
the ectoderm in the groove between the gill and the body, and runs
forward from the visceral ganglion, and later becomes a commissure.
[In Nucula and the Protobranchia generally, distinct pleural
ganglia are present. These are situated immediately behind the
cerebral ganglia at the commencement of the visceral commissures ;
here, also, the pleuro-pedal commissures are for some distance in-
dependent of the cerebro-pedals. In other Lamellibranchs, the
pleural ganglia are fused with the cerebral. Drew was, however,
unable to trace a distinct origin for the pleural ganglia in Yoldia."]
C. The Sensory Organs.
The Eyes. It may be stated with some certainty that the
simply constituted eyes of the border of the mantle, i.e., the so-called
invaginations, or optic pits, and the compound eyes arise through a
comparatively slight differentiation of the mantle-epithelium.
64 LAMELLIBRANCHIA.
The invaginations, the optic nature of which is, indeed, doubtful, are pit-
like depressions of the epithelium, in the cells of which pigment is deposited,
while the pit itself becomes filled with a mass of what appears like a secretion
(conjectured to be a lens).
The compound eyes arise as convex thickenings of the mantle-epithelium
at certain points. In these, conical sensory cells are distinguished from the
pigment-bearing and supporting cells lying between them by the development
of crystal cones and a cornea. The visual cells are connected with the fibres
of a nerve which is a branch of the mantle-nerve (Carriere, Patten, Rawitz).
The eye which thus arises shows some similarity to the compound eye of
the Annelida as recently described by Andrews.* These eyes of the Lamelli-
branchia cannot well be compared with the compound eyes of the Arthropoda,
since the latter are far more complicated in structure. It is evident that
in neither case can there be any real homology.
The Eyes of Pecten. The mantle-eyes of Pecten, the morphology
and physiology of which are still somewhat obscure, were investigated
from the ontogenetic point of view by Patten (No. 39), but his study
of them was not altogether satisfactory, so that we must content
ourselves with a short reference to them.
The eyes of Pecten, unlike the two modifications of the edge of the mantle
just described in other Lamellibranchs, are highly developed organs (Fig.
28). The principal constituents of the eye of Pecten are as follows : there is a
cornea behind which lies a large lens ; behind the lens comes a retina com-
posed of a ganglionic layer, followed by a layer of rod-bearing cells, the most
remarkable feature of the retina being that the rods are directed away from
the light and towards the posterior wall of the eye. This latter is covered
behind by an integument of pigment-cells, in front of which lies the tapetum,
which has a metallic lustre. The innervation of the eye is double, and takes
place by means of a nerve (Fig. 28, 7), which sends out one branch to the
base of the eye, and thence direct to the optic cells, while the second branch
enters the eye laterally, becoming connected first with the ganglionic layer,
and through it coming into contact with the optic cells. For the further com-
plications found in this eye we must refer our readers to the special works of
Carriere, Butschli, Patten and Rawitz.
Patten was able to establish ontogenetically that the eyes at the
edge of the mantle in Pecten arise as knob-like thickenings of the
ectoderm. As these thickenings rise up and become more and more
distinct from the surrounding ectoderm, an ectodermal cone grows
down from the surface towards the interior. While active increase
in number of the cells brings about the growth of the whole struc-
ture, the ectodermal mass directed inwards becomes marked off from
the outer epithelium, a process which is assisted by the growth of
* Compound eyes of Annelids, Journal of Morphology, Vol. v., 1891.
THE SENSORY ORGANS.
65
connective tissue-cells between the inner ectoderm-mass, this tissue
forming a continuous layer between the two. From this, i.e., from
mesodermal elements, the lens, according to Patten, is formed, while
the inner ectodermal mass yields the principal constituent of the eye.
Mo. 28.— A section through an eye of Pecten (after Patten ironi Hatschek s Text-
book oj Zoology). 1, cornea; 2, lens; 3, pigmented ectoderm; L blood-
si mis round the lens; 5, retina, with superficial ganglionic layer and backwardlv
directed rods; 6', pigmentdayer, with the tapetum lying in front of it; 7, opti'e
nerve. * r
The way in which the various layers, the ganglionic cell-layer, the
retina, the argentea, and the tapetum, etc., arise out of this mass
is described, but these difficult points are not made sufficiently
clear.
Further details concerning the ontogeny of these very peculiar eyes and
especially as to the origin of the rods are much to be desired. The solution
P
gg LAMELLIBRANCHIA.
of these problems seems all the more desirable as the eye of Pecten* in its
structure stauds almost alone among Molluscan eyes. With regard to their
morphological interpretation, we are inclined to agree with Butschm (No.
7) who showed how the pigment cell-layer of the posterior wall of the eye
passes over into the retina, a closed vesicle being thus formed in the eye its
anterior wall consisting of the retina and its posterior wall of the pigmented
integument. This vesicle must be supposed to have arisen by invagination
and abstraction from the ectoderm, a view with which Patten's observation
of a solid ingrowth can be reconciled. The description given by Patten also
of the rise of the lens outside of the optic vesicle supports such a condition it we
do not assume a mesodermal origin for the lens but rather imagine a second
process of invagination such as occurs in the Cephalopodan eye. The
the lens outside of the optic vesicle makes it possible for the more superficial
wall of the latter to be changed into the retina, a change which is impossible
where the lens has itself arisen from this outer wall, as is the case m the
Gastropoda and in some of the Cephalopoda also. The position of the rods
is hereby explained (Butschli). Since these always arise at the free ends
of the cells, they are directed forward when the deeper wall of the optic-
vesicle is transformed into the retina (Gastropoda, Cephalopoda) ; but are,
on the contrary, directed backward when the retina is derived from the outer
or superficial wall of the vesicle. The latter must originally have been the
case in Pecten.
The otocysts arise, in Teredo and Anodonta, near the pedal gang-
lion as invaginations of the ectoderm which then become abstracted
from the latter and provided with otoliths and sensory hairs (Fig. 18,
U p 36) In Cyclas, the otocysts lie at the two sides of the embryo,
behind the lateral end of the ciliated area. [In the Protobranchia the
Oocysts retain their connection with the exterior throughout life.]
Spengel's olfactory organs and the abdominal sensory organs
(Thiele) show, by their structure, that they are mere modifications
of the body-epithelium.
D. The Alimentary Canal.
The structure of the alimentary canal, being greatly influenced by
adaptation to different conditions of life, varies in certain points in
the different forms. In Odrea, for example, the archenteron is said
to pass over direct into the definitive intestine the blastopore remain-
iJ open, while in Teredo, as well as in Cyclas and the Unwnulae, the
blastopore closes and a true stomodaeum forms. This condition, and
:^^^S^=i = =^ altogeker
different ways.
n
o
THE ALIMENTARY CANAL. 67
Its relation to the other ontogenetic processes, have already been
described in a former section (p. 30). The ectodermal invagination
yields the oesophagus; the stomach, liver and intestine are ento-
dermal. The anus, in the majority of cases observed, seems to have
been formed by direct fusion of the entoderm with the ectoderm, so
that the posterior part of the intestine would be entodermal ;' in
Teredo, however, there is, according to Hatschek, a proctodaeal' in-
vagination, and a similar invagination is described bv Voeltzkow
as occurring in Entovalva (No. 57).
The further development of the intestine consists in its increase
in length, as a result of which it becomes coiled. A circular con-
striction marks off the stomach from the intestine. As early as the
Trochophore stage, a pair of sac-like outgrowths appear in connection
with the stomach; this is the rudiment of the liver (Fig. ]6, p. 33,
with which the yolk-laden remains of the macromeres become incor-
porated (Fig. 18, p. 36). A peculiar phenomenon in connection with
these two liver-sacs, which at first are spherical, is the occurrence of
rhythmical movements ; these are no doubt to be traced back to the
action of mesoderm-cells which have become apposed to the entoderm
wall (Love'n, Ziegler). The passages from the liver into the
stomach which at first are wide, become narrow later and form the
efferent ducts; the bulgings found on the liver-sacs mark its separate
lobes and lobules (Fig. 31, /, p. 75).
In the stoniodaeum of Cardium, Lovkx observed a small bulging of the
ventral wall which involuntarily recalls the radula-sac of other Molluscs an
organ which is known to be wanting in the Lamellibranchia. It cannot be
connected with the crystalline style-sac, as this is invariably an entodermal
derivative The sac which contains the crystalline style is formed as an out-
growth of the wall of the stomach. This structure which, as has Ion* been
known, occurs also in the Gastropoda, appears, according to the most recent
view, to yield a secretion (the crystalline style) which serves for enveloping
solid particles of food, and thus protects the wall of the intestine (Barrois)
No statements as to the ontogenetic formation of the crystalline style-sac
are known to us.
The layer of muscle and connective tissue which forms the outer
wall of the intestine is yielded by the mesoderm-cells distributed in
the primary body-cavity, which become applied either to the ento-
derm or to the ectoderm.
68
LAMELLIBRANCHIA.
E. The Gills.
In those Lamellibranchs in which the formation of the gills has
heen studied, they are found to arise in one of two [three, of. p. 45 j
different ways which are somewhat difficult to harmonise in then-
early stages. According to one method, which has already been
described for Gyclas and Teredo (pp. 42 and 44), a fold resembling the
mantle-fold rises between the latter and the foot, and develops from
behind forward. The outer and inner surfaces of these folds show
oroove-like depressions lying at right angles to the longitudinal axis
of the folds ; these grooves deepen and, meeting those of the opposite
surface fuse together. As the gill-fold becomes perforated along
these lines, fissures result which extend in from the free margin
of the folds towards their bases (Fig. 31, p. 75). The gill now con-
sists of a series of consecutive lobes which decrease in size from
ltefore backward. .
According to the other method of gill-formation, which has been
observed in Myttius, Dreissensia, Ostrea (a somewhat similar method
being found also in the Uvionidae),* a papilla arises on each side of
the body between the mantle and the median visceral mass, and
behind these new papillae arise (Fig. 26 C). A longitudinally
placed row of papillae thus arises by the continued development of
fresh papillae behind those already formed. These, by the develop-
ment of interfilamentar junctions, form the inner branchial leaf
while the outer leaf is produced by a similar row of papillae which
arise somewhat later.
The further development of the papillae was studied by L-acaze-
Duthiers in a form belonging to the last category, viz., m Mytilus
edulis (No 28). Jackson also has recently investigated the forma-
tion of the gills in Ostrea, and has arrived on the whole at the same
results as Lacaze-Duthiers (No. 22).
During the development of the inner branchial leaf, the papillae
increase in number, new ones continually budding out posteriorly.
* This seems also to be indicated by the observations made by Loven on
mmmmmm
the primitive condition.
THE GILLS.
69
The papillae are thickened al their free ends (Fig. 29 A). The
continued extension, anteriorly and posteriorly, of these free ends
leads to fusion of the papillae, so that the series may now be regarded
us a membrane perforated by parallel vertical slits, this membrane
representing the rudiment of the inner branchial leaf. In most
Lamellibranchs, however, each leaf consists of two lamellae. The
second or ascending lamella of the inner leaf arises by the bending
inward of the free edge of the primary fold formed by the fusion of
the papillae (Fig. 29 B) ; this new lamella then grows upward parallel
to the (now outer or descending) lamella towards the base of the
latter. The inner lamella thus formed is at first an unbroken mem-
brane, the slits only appearing in it when it has increased in size.
Fig. 29.— Diagram of the development of the gills in a Lamellibranch possessing two
branchial leaves on each side, i, inner. >: outer branchial leaf;/, foot; m, mantle.
The outer branchial leaf now appears and becomes applied to the
posterior half of the base of the inner leaf when the latter consists
of about twenty papilla* and when its inner or ascending lamella is
partly formed (Fig. 29 0). The outer leaf forms on the whole in
the same way as the inner, but, in it, papillae are said to form
anteriorly as well as posteriorly, and the leaf, in order to yield a
second lamella, bends outwards and not inwards (Fig. 29 D). The
fusions of the free edge of the inner lamella of the inner leaf and the
outer lamella of the outer leaf with the integument of the body take
place later, and vary in extent greatly in different Lamellibranchs.
being altogether wanting in some.
70 LAMELLIBRANCHIA.
In Mytilus, as in some other Larnellibranchs (e.g., Pecten, Area) the gills,
even in the adult, consist of individual filaments which, however, are arranged
in just the same way as the branchial leaves of other forms. The inner row
becomes bent inward to form the ascending lamella of the inner leaf, while,
in the case of the outer leaf, the filaments are bent outward (Fig. 29 E). A
section of these gills has the form of a W, and thus resembles a section of the
gill-leaves in the Eulamellibranchs (Fig. 80 E). The free ends of the fila-
ments seem to be connected by a continuous strand of tissue running parallel
to the length of the gill-leaf. This latter must be regarded as the modified
representative of that transverse connection found uniting the free ventral
ends of the papillae when the gill first arose, shifted dorsally. The papillae
themselves correspond to the filaments of the adult gill. Since, in Mytilus
also, the reflected or ascending portion of the gill is at first represented by a
solid plate (see the above description of the development of the gill) in which
the slits arise secondarily, the Mytilus gill, in its later stages, passes through a
condition resembling that seen in the earliest gill-rudiment in such Larnelli-
branchs as Cyclas and Teredo [or better still, in Pholas, Singerfoos], the
gills of which originate as leaves. There is therefore some difficulty in
regarding, with many authors, the later filiform condition of the gill as an
original condition. This difficulty is increased by the fact that the gills of
Mytilus, Pecten, etc., which consist of single filaments, have, when regarded
as a whole, the general characters of a branchial leaf with descending and
reflected or ascending lamellae, the descending and ascending limbs of the
same filament being united together by fusions of tissue at certain points, the
so-called interlamellar junctions ; further, the adjacent filaments of the same
row, both in the ascending and descending limbs, are held together by the
interlocking of some specially long cilia. Wherever, therefore, we have gills
consisting of independent but reflected filaments, the assumption that these
filaments might have arisen by a secondary separation of the gill-bars in a
primary branchial plate is suggested (p. 1'2).
It appears that the papillae correspond to the gill-bars or, as they
are generally termed, filaments of the adult and the slits to the
interstices between these bars. The differentiation of the bars would
then have to take place from the posterior end of the gills. The gill
of the adult Lamellibranch is usually a much more complicated struc-
ture than the larval gill up to the stage we have described. Between
the filaments of each lamella, as well as between the ascending and
descending lamellae of each leaf, there are connections which may
consist of solid cell-strands, of hollow vascular junctions, or simply
of interlocking cilia, so that the leaves are connected by longitudinal
interfilamentar and by transverse lamellar junctions. The mesoderm
of the papillae yield the connective tissue, the blood-vessels and the
skeletal rods which support the gill-bars, and from thence extend
in certain forms into the complicated junctions found in most
Larnellibranchs (Eulamellibranchs and Pseudolamellibranchs).
THE GILLS. 71
In cases in which, as in Cyclas, the rudiment of the gill is leaf-like
and only breaks up later into consecutive lobes through the slits
which arise in it, we may assume that these lobes unite later, like
the papillae, to form the branchial leaf.
If we compare the origin of the gills in Teredo and Cyclas on the one hand
and Mytilus, etc., on the other, we might at first feel inclined to regard the
method seen in the foi-mer as the more primitive, since the formation of the
leaf precedes that of the papillae. The gill originates as a leaf, and is only
later broken up by incisions into separate lobes which are arranged in the
same way as the papillae in other cases. This view, which is founded on the
ontogeny of a few forms such as Teredo and Cyclas, which in other respects
are undoubtedly specialised, cannot, however, in any way be reconciled with
the morphological conditions of the definitive gill in the different Lamelli-
branchs. A comparative study of these latter suggests rather that the origin
of the gills in the form of papillae; as in Mytilus, was the primitive condition.
Unfortunately very little is as yet known as to the mode of formation of the
gills, but if we examine the apparently carefully investigated development of
these organs in Mytilus and Ostrea, we find that certain ontogenetic stages can
be most exactly matched in the shape of the gills of certain adult Lamelli-
branchs. Thus, in Dimya, according to Dall, the gill on each side consistsof one
row of branchial filaments (Fig. 30 B) and in Amusium Dalli (and as it appears
also in Area ectocomata) there are two such rows on each side (Fig. 30 C).*
The brauchial filaments are not connected, and thus represent the ontogenetic
stage at which there are one or two rows of papillae. The further develop-
ment of the gills may be imagined to have taken place by the free ends of the
branchial filaments becoming connected, in the manner illustrated in the
ontogeny of Mytilus (p. 68). In this way the row of branchial filaments gave
rise to the branchial leaf. This leaf doubled back on itself, when an increase
of surface was needed and growth in a straight direction was not possible on
account of the want of room in the shell (Fig. 29 B-E). The ascending (re-
flected) lamella of the branchial leaf thus arose ; the free edge of which may
finally fuse with the mantle, as is the case, for example, with the ascending
lamella of the outer branchial leaf in the I nionidae (Fig. 30 E).
That form of gill which consists of single filaments, bent back upon them-
selves, thus indicating the two lamellae of the later branchial leaf (Fig. 30 />)
has repeatedly been held to be very primitive and has been thought to repre-
sent the stage succeeding that in which the gills consisted of two straight rows
of filaments (Fig. 30 C). Such gills are found in Trigonia (Pelseneer) and
Area noae which may be considered as very old forms. The gill-leaf consisting
of two lamellae was thought to have arisen from the union of these reflected
filaments. To us, the reflection of the single filaments and their regular.
almosl leaf-like arrangement, such as is seen in the gills of Pecten and Mytilus
' We follow here the accounts given by Pelseneer, Dall and Mitsuklhi
of the morphological conditions of the Lamellibranch gills. It is impos-
sible to decide how far these may represent primitive conditions or may to
some degree be degeneration-phenomena, for it is evident that these latter d<>
occur and cause a reduction of the gill-leaves.
72
LAMELLIBRANGHIA.
and even in Area, is very difficult to explain. When isolated filaments for the
sake of increase of surface grow in length, they are not likely to retain such
a regular arrangement, even if we bear in mind their position in one row,
the limited space within the Lamellibranch shell, and the circulation of the
water between them. We therefore think ourselves justified in assuming, in
the case of those Lamellibranch gills which, while filiform in structure, show
such a regular leaf-like shape, a secondary breaking up of a gill which
originally consisted of two plates to which allusion has already been made
(p. 70). A satisfactory explanation of these obscure points can, however,
only be obtained by comprehensive investigation not only of the gills them-
selves but also of the whole structure of those Lamellibranchs which may be
regarded as transitionary forms.
Fig 30 -Diagrams illustrating the position of the gills in the Lamellibranchia A
ToMia, BTDimya; 0, Amusium Dalli; />, Area noae; K, Aiwdonta;^ toot;
in, mantle;' i, inner, e, outer branchial leaf.
We may regard as the most primitive form of the Lamellibranch gill a
ridge [the' ctenidial axis] with two rows of branchial filaments. In place of
the filaments, triangular leaflets must originally have been present, with
vertically expanded surfaces, placed transversely to the long axis of the ridge,
a condition permanently retained in the gills of Nv^ula and Yoldia (Fig. 30
A, Mitsukuri). Taking into account the similar form of the gills in the
Aspidobranchiate Gastropoda, this latter condition might be regarded as the
original condition. It is, indeed, not essentially different from that with the
double row of papillae, since the leaflets correspond in every respect to the
still unreflected papillae.
THE BODY-CAVITY, ETC. 7^
The leaflets by lengthening and narrowing gave rise to the filaments. The
gill of Nucula is further primitive in its free pointed posterior termination, and
may without further question be directly honiologised with the bipeetinate
gill of the lowest Gastropods. This hist view of the Lamellihranch gill, which
was advanced years ago by Lkickh art (No. 30), has recently, owing to the
researches of Pelseneeb iN'os. 40 and 41), Menegadx (No. 35), and others.
received great support and has become almost universally adopted. The
ontogenetical fact that one of the rows (the inner row) appears first and the
other (outer) row only much later does not, indeed, appear to be in harmony
with it. In tracing the gill back to that primitive form, we should expect
that the two rows of papillae would arise almost simultaneously.
The rise of the gills in the form of leaves, as in Teredo and Uyclas, ma\ .
according to the present state of our knowledge, best be compared to the pro-
duction of the branchial filaments or £>apillae from the ridge. We should,
indeed, require to understand more exactly the way in which the second
branchial leaf found in these animals arises. We must be careful not to
ascribe too great significance to the method of formation of the gills in Teredo
and Cyclas, because these are, as has already been shown, highly specialised
Lamellibranchs, and because, in the nearly related Pisidium, the leaf-like
rudiment of the gills is far less distinct (according, at least, to Ray Lan-
kester). These varied conditions are somewhat difficult to reconcile, and
their explanation is very desirable. So far, there are many indications that,
in the development of the Lamellihranch gills, great modifications have been
introduced which render it very difficult to form conclusions as to their
original constitution.
F The Body-cavity, the Blood-vascular System and the Kidney.
The development of the closely related structures, the body-cavity.
the blood-vascular system and the kidney, have been investigated in
the UniunidaH and in Cyclas, but are best known in the latter. Our
information on these points is due to the investigations of Leydig.
Stepanoff, Ganin and v. Jhering, which have recently been ex-
tended and supplemented by Ziegler. The history of the meso-
dermal structures, in Cyclas and the remaining Lamellibranchs has,
indeed, not yet been exhausted, as will be evident from the following
account.
The first rudiment of these mesodermal structures appears at a
time when the embryo, through the development of the foot and the
formation of the mantle-folds passes out of the Trocfwphvre stage, i.e.,
at a stage occurring between the two depicted in Figs. 19, p. 40, and
21 A, p. 41.
In the Trochophure there is on each side of the intestine a compact
mass of mesoderm-cells (Fig. 19, ines) which Zieglek claims as the
lnesoderin-liands. In the anterior end of each of these masses, a
■74 LAMELLIBRANCHIA.
cavity arises which soon, by the regular arrangements of its cells into
an epithelium, assumes the form of a vesicle. This is the paired
rudiment of the pericardium.
The rise of the paired pericardial vesicles out of the bilateral
mesoderm-rudiment so nearly resembles the formation of the primitive
segments in the Annelida and the Arthropoda that we must regard
the pericardial vesicles as coelomic sacs and their cavities as the
secondary body-cavity. The coelom in the Lamellibranchs, however,
only attains a very small size, and the definitive body-cavity which
contains the organs arises independently of the former as a pseudocode.
The view that the pericardial sacs must be regarded as the coelom
rests chiefly on the fact that the kidney shows the same relation
to this cavity (Fig. 3.2) as do the nephridia in the Annelida to the
cavities of the primitive segments (secondary body-cavity). This
relationship is very early developed in the embryo of Cyclas.
The kidney (organ of Bojanus). Behind the pericardial vesicle,
the mesoderm-cells soon become grouped in the form of a tube, the
lumen of which communicates with the cavity of this vesicle. This
tube, which at first runs upwards, and then again bends downwards,
is the rudiment of the organ of Bojanus (Fig. 21 A, n, p. 44). ^ Its
upper end, which opens into the pericardial vesicle (Figs. 21, 32) is
lined with cilia. The resemblance thus brought about between the
organ of Bojanus and a nephridium is heightened later when the
lower end of the canal fuses with the ectoderm and communication
with the exterior is thus established (Fig. 31, n„).
From Ziegeer's description, it is not clear whether the formation of the
efferent duct takes place through the direct fusion of the lower end of the rudi-
ment of the kidney with the ectoderm, or whether an invagination of the ecto-
derm takes part in it. Ziegler's statements on the whole support the first
hypothesis, which also agrees with the manner of formation of the nephridia
in the Annelida as described by Bergh.* But since, as we shall see, in the
( Gastropoda and also in the Annelida (Vol. i., p. 297), an ectodermal invagination
takes part in the formation of the nephridia, this question cannot here he
decided.
The statements which have been made as to the rise of the kidneys as mere
depressions of the ectoderm (Ray Lankester, Ganin) must be considered as-
refuted, especially as the morphological agreement of the organs with the
nephridia of the Annelida points to a similar method of formation. We are
indeed led to look for a still closer relation of the nephridia, when forming,
with the coelomic sacs, and such a relation will be found in the Gastropoda.
* R. S. Bergh. Neue Beitrage zur Embryologie der Anneliden. I. Zur
Kntwicklung und Differenzirung des Keimstreifens von Lumbncus. Zatscn.
r. wiss. Zool. Bd. 1. 1890.
THE KIDNEY.
75
As the kidney develops further, its tube becomes coiled (Figs. 21
A p. 44, and 31). Three sections can then be made out in it : a short
ciliated section, a long glandular section and an efferent section.
The latter, which is not ciliated in the embryo, shows ciliation at a
later stage when the efferent duct of the genital organs opens into
it near its end, and it thus serves to transmit the genital cells.
The three sections of the embryonic kidney are the same as those
that can be distinguished in the adult organ, but the latter is further
modified in so far as the middle section is more coiled. This gives
rise to the renal sac and to the more complicated portion, the renal
i. v. p. ai.
ma.
"..
. \
_-._\ vnt.
hsm. /--
s
m.T.
W.
x
-— -^. of
£.
P9-
Fig. 31.— Embryo of Cydas cornea (combined from figures by E. Ziegler). a, anus ;
at, auricle; by, byssal thread and gland; eg, eereln-al ganglion; •, but
the area of the secretory epithelium is increased by the formation
of internal folds. In the primitive forms (Nttcula, Solenomya), the
kidney retains the form of a slightly coiled tube, the inner wall
of which shows no great increase of surface.
When the body grows longer, as in the Unionidae, the gills also lengthen
and the organ of Bojanus takes up a somewhat different position. Its original
position between the pericardium and the posterior adductor which is illus-
LAMELLIBKANCHIA.
76
i nf nwlailVia 3D and is retained in the adult in the
the anterior end, the two efferent ien«u u anterior end of
the fact that it also an.es in th .torn _<* t) These tubes, as in
connection with the aduU, ^f^J^SLaiom «"»" "8 a °™tj
the kidney. , « . ■,
The Formation of the Heart. In following the development of the
„,,,„ of Bojanns, we left the periearaia, «*. =b «* *
though they also
underwent essen-
tial modifications
of form. After
the vesicles have
slightly lengthened,
they become partly
constricted, the
outer wall becoming
invaginated (Fig.
32 A, p). In this
way, each vesicle
appears to be
divided into two,
but the division is
not complete and
the two halves of
the vesicle still
■al wall of the lower
be recognised (Fig.
?■
ft.
B
u\
Fig 32. -Diagram of the formation of the heart in Cyclas
^constructedlfrom Ziegler's descriptions) a auricle ■■{£
B the pericardial invagination which leads to its forma
tion) ; I intestine; g, vessels opening into the auricles .
„. renal funnel; p, pericardium ; v, ventrice.
communicate with one another. In the venti
section, the internal opening of the kidney can
THE PERICARDIUM AND HEART. 77
32 A, n). The right and left pericardial vesicles now grow towards
each other and unite above the intestine at the two sides of which
they formerly lay : in exactly the same way they unite below the
intestine, i.e., ventrally to it (Fig. 32 AD), the intestine having been
previously invested by certain of the niesoderm-cells which were
distributed in the primary body-cavity.
The circumcrescence of the intestine by the pericardial vesicles
and the fusion of these latter, as described by Ziegler, strikingly
recalls the fusion of two primitive segments in the Annelida to form
a segmental cavity (Vol. i., p. 290). We have already drawn atten-
tion to the relation of the kidneys (nephridia) to the pericardial
cavity. The walls of the pericardial vesicles which come into contact
and which, in following the comparison, would be the equivalent of
the intestinal mesenteries, seem completely to degenerate, so that the
cavities of the two pericardial vesicles unite together to form a
common cavity. The formation of the heart, which will be described
immediately, takes place outside of this space, i.e., outside of the
secondary body-cavity and within the primary body-cavity. This
also would agree with the condition in the Annelida, where the dorsal
vessel arises between the splanchnic layer of the mesoderm and the
entoderm, and therefore in the primary body-cavity (Vol. i., p. 291).
The formation of the heart is introduced by the circumcrescence of
the intestine by the pericardial vesicles. The wall of the vesicles
which is turned to the intestine yields the wall of the ventricle.
This statement made by Ziegler must be taken to mean that,
from that wall of the vesicle, elements are produced by delamination
which yield the heart, while the wall of the pericardial vesicle itself
represents the investing peritoneal epithelium (Fig. 32 B and G).
The same process would be repeated in the formation of the auricles.
These latter had already arisen as the invaginations of the pericardial
vesicles described above (Fig. 32 .A). These invaginations unite
with the opposite wall of the pericardial vesicle and the auricles,
which form by the widening of the originally narrow invaginations,
fuse with the rudiment of the ventricle (Fig. 32 B-D). At the
points of junction, the apertures and valves between the ventricles
and the auricles arise.
The efferent and afferent vessels of the heart (aortae and branchial
veins) arise separately from the rudiment of the heart and are no
doubt formed by the grouping together of those mesoderm-cells
which are derived from the wall of the pericardium, or were already
present in the body-cavity, i.e., they originate as cavities between
rjQ LAMELLIBRANCHIA.
the mesodermal tissues of the latter. The passage of these out of
the pericardium that surrounds them is, owing to the nature of their
origin, easily understood (Fig. 32 C and D).
This method of formation of the heart from the mesial walls of the pericardial
vesicles explains how, in the adult, the intestine traverses the heart. Phylo-
genetically, this condition is supposed to have arisen through a blood-sinus
surrounding the intestine developing thicker walls and thus becoming the
heart (Gbobben). Since the vessels arise distinct from the heart, such an
origin of the latter is not in any way improbable. On the other hand the
fact that in the Lamellibranchia, a paired heart lying dorsally to the
intestine and with each half enclosed in a separate pericardium may occur
, irca) has led to the conclusion that the unpaired heart which, m the higher
forms surrounds the intestine, might have arisen by the fusion of these two
hearts (Thiele, Chap. xxx.). This view seemed to be supported by the fact
that the double heart is found in just those forms that are very primitive, and,
further that a double heart is also present in various Annelids.
The paired origin of the heart (Figs. 32 and 33 C), might perhaps be regarded
as a primitive feature and as indicating that the heart was originally a paired
vessel but this view is not justified, since it is supported merely by the paired
development of the coelom and the part taken by the latter in the formation
of the heart A comparison with the manner in which the heart arises in the
Annelida and its formation in the Lamellibranchia should help to elucidate
these points (cf. Vol. i., p. 291).
In the Annelida, the paired origin of the heart is still more
marked than in the Lamellibranchia. Even during the growth of the
primitive segments towards the dorsal middle line the rudiment of
the dorsal vessel appears on that side of the splanchnic layer which
is turned towards the entoderm (Fig. 33 A, I. and II.). The dorsal
vessel is therefore paired and, as the primitive segments grow further,
shifts towards the dorsal line (.4 II. and III.) On this line, the two
rudiments of the heart finally meet (A IV.) and fuse to form the
unpaired dorsal vessel, except in those forms in which they remain
distinct in the adult. With this latter condition in which the dorsal
vessels remain distinct, the heart of Am, shows the greatest agree-
ment We must suppose that, in Area, each of the two pericardial
sacs by the invagination of its inner wall, developed a ventricle (Fig.
33 B I -IV h). The fusion of the pericardial sacs above and below
the intestine did not take place, and in this way the union of the
two rudiments of the heart was prevented. In most Lamelhbranchs,
on the contrary, the circumcrescence of the intestine takes place:
the whole median wall of the pericardial vesicles takes part in the
formation of the ventricle, and the latter thus surrounds the intestine.
(Fig 33 G, I. -IV.). The rise of this single ventricle from distinct
THE BODY-CAVITY, ETC.
79
rudiments is suggested here also, and the double character is still
more recognisable in the rise of the auricles, which originate as
invaginations of the outer walls of the pericardial vesicles (Fig. 32).
But this double character may, as already mentioned, be derived
from the connection of the formation of the heart with the paired
eoelomic sacs. Further, the paired character of the heart, as repre
sented in the adult condition, seems to us easily explained by these
ontogenetic processes.* The fact that, in the paired heart of Area,
Fig. 33. — A-ll, diagrams illustrating the formation of the heart. A, in the Annelida,
B, in Area, C, in other Lamellibranchs. (The auricles are omitted for the sake ot
clearness), d, intestine ; //. paired rudiment of the heart (united, in .1 IV. and C
IN", to form an unpaired heart) ; //. the two pericardial vesicles (united in C IV. to
form the pericardium) ; so, somatic, sp. splanchnic layer of the eoelomic sac (primi-
tive segments).
•there is a common anterior and posterior aorta, seems to point rather
to the breaking up of an originally single heart than to the union of
two distinct hearts. The paired dorsal vessel of the Annelida often
-shows connection between the two parts, j- and this also might be a
* Grobben, who advocates such a view of the Lamellibranch heart, speaks
of the " retention of au ontogenetic stage through an arrest of develop-
ment." It appears to us also that the method of formation described would
facilitate the development of a double heart in cases in which such a heart
would be of advantage to the animal.
t Megascolex, Microchaeta and Acanthodrilus show the recurrence of connec-
tions between the two hearts. In another Acanthodrilus almost the whole
•of the dorsal vessel is paired and is without transverse connections, but in its
anterior part there is still a connection. Beddard, Note on the Paired Dorsal
Vessel of Certain Earthworms. Proc. Roy. PJu/s. Soc. Edinburgh. Vol. viii.,
1885.
QQ LAMELLIBRANCHIA.
consequence of its having developed from an originally single
rudiment.
An attempt has been made to explain the rise of a paired heart (as.
the original condition) through the relation of the two parts to the
-ills lying at the two sides of the body (Thiele, Chap. xxx.). If
the paired heart really represents the primitive condition, this ex-
planation would be very plausible, but the Annelida, Arthropoda
and Amphineura all agree in showing us the heart as an unpaired
organ lying dorsally to the intestine.
We have still to mention that the heart in a few more modified
forms {Teredo, Ostrea, Mulleria) lies ventrally to the intestine. In
these cases, the union of the pericardial vesicles to form the unpaired
heart has no doubt taken place beneath the intestine. [In Nucula,
Area and Anomla, the heart is dorsal to the intestine.]
The condition of the secondary body-cavity and the kidneys in the
Lamellibranchia recalls very strikingly those found in the Crustacea
and Peripatus (cf. Vol. ii., p. 180, and Vol. hi., p. 204). In these
latter, a part of the coelom is directly incorporated in the kidney, with
which it is also functionally united. We are perhaps justified in
regarding the pericardium of the Lamellibranchia, into which the
renal funnel opens as it does in the Arthropoda into the cavities of
the primitive segments (or coelom), as the homologate of the end-sae
of the excretory organs in these forms. The fact that the coelom-
sacs of the two sides are here united, can make no difference, for this
does not cause the heart to lie, as may at first appear, in the secondary
body-cavity, but it is still found outside that cavity, as it is also in
the forms mentioned above.
If the pericardium possesses the morphological significance ascribed
to it. we might perhaps expect that its physiological function should
be modified in the same way as in those forms in which the secondary
body-cavity has entered into such close relation to the kidney. Tin*
assumption seems actually to be confirmed, when we consider the
so-called pericardial gland. This gland, the so-called red-brown
organ or Keber's organ, arises as outgrowths of the epithelium of the
pericardial wall and lies either on the auricles or on the anterior part
of the pericardium (Grobben). This organ is most probably ex-
cretory and, since it owes its origin to the pericardial epithelium, it
seems not unsuitable to ascribe to the latter a similar significance.
The close relation in point of position existing between both the
pericardium and the pericardial gland and the blood- vascular system.,
makes such a view appear possible.
MUSCULATURE AND CONNECTIVE TISSUES. 81
According to our present anatomical and ontogenetical knowledge,
the communication between the pericardia] cavity and the blood-
vascular system which was formerly assumed, does not exist. The
idea of an admixture of water with the blood which was also held
must be regarded as exploded, quite apart from the fact that the
transmission of water from outside through the organ of Bojanus
into the pericardium seems from recent researches to be highly im-
probable (Rankin). The structure of the organ itself as well as the
direction of the cilia within it are unfavourable to such a process.
Indeed the whole idea of the reception of water into the body of the
Lamellibranch from without, which has often been adopted as an
explanation of the swelling of the foot, must be regarded as refuted.
The pores which were supposed to conduct water from without into
the foot could not be demonstrated ontogenetically (Ziegler). The
swelling of the foot, as is evident from the statements of a number of
authors (Carriere, Fleischmann, Schiemenz, Rankin, etc.), is
rather due to the fact that the greater part of the blood is driven
into this organ. This is brought about through the blood being-
retained in the foot, the valve at the entrance to the sinus venosus
being closed and the blood which was emerging from the foot being
thus retained within it. Besides this, the quantity of blood already in
the foot is increased through the flow of fresh blood from the anterior
aorta. When the foot is extended, the sphincter at the point where
the posterior aorta emerges from the heart contracts, so that the
greater part of the blood is obliged to flow through the anterior aorta
into the foot. During this process, a certain amount of blood still
circulates in the heart, so as to prevent an arrest of the whole circula-
tion. When the valve in the sinus venosus opens, the blood flows
out of the foot, and as the latter ceases to extend, the sphincter of
the posterior aorta opens again, until, when the animal moves on
again the same process is repeated.
G. Musculature and Connective Tissue.
The only organs as yet referred to as differentiations of the mesoderm
have been the coelom, the kidney and the blood-vascular system, but
there are other structures mesodermal in origin, which, indeed, up to
the present have received little attention from zoologists; these are the
musculature and the connective tissue, and, further, the genital organs.
which will be dealt with immediately. The muscle-cells are formed
by the detachment of single cells from the mesoderm-mass, the distri-
G
82 LAMELLIBRANCHIA.
bution of these in the pseudocode, and the further growth of the
isolated cells into contractile fibres. When considering the larval
forms, we pointed out that these fibres become applied to one another
to form larger complexes which are the muscles of the larva and the
adult (Fig. 15, p. 31 ; Fig. 18, p. 36). The musculature of the foot
arises from the great increase in number of the cells detached from
the mesodermal mass, and the massive connective tissue both of the
foot and of the rest of the bodv has the same origin.
H. The Genital Organs.
The ontogeny of the genital organs has not as yet been sufficiently
studied. In Cyda*, the genital glands originate from the two meso-
derm-bands and lie, as a rather large mass of cells, beneath the peri-
cardial vesicle and close under its wall (Ziegler). A somewhat later
stage in the development of these glands is depicted in Fig. 21 A, 0 Horst R. Embryogenie de l'hultre (Ostrea edulis). Tijdschrift
der Nederlandsche Dierkundige Vereenigung. Supplement Deel
I. 1883-84. .
21. Huxley, T. H. Oysters and the Oyster Question. English
Illustr. Mag. 1883.
22 Jackson, R. T. The Development of the Oyster, with Remarks
on Allied Genera. Pro. Boston Soc. Nat. Hist. Vol. xxiii.
1888. 4 ...
23. Jackson, R. T. Phylogeny of the Pelecypoda. The Avuhdae
and their Allies. Mem. Boston Soc. Nat. Hist. Vol. iv. No.
viii 1S90 See also "Studies of Pelecypoda' and the
« Mechanical Origin of Structure in Pelecypods ". Arm rican
Naturalist. Vol. xxv. (p. 1,132), and xxv. (p. 11). 1890-
1891- ,, „ ,
24. Jhering, H. v. Zur Morphologie der Niere der sog. Mollusken.
Zeitschr. f. wiss. Zool. Bd. xxix 1887.
25. Jhering, H. v. Anodonta und Glabaris. Zool. Anz. Jahrg.
xiv. 1891.
26. Jhering, H. v. Ueber die Ontogenie von ( lyclas und die Homo-
LITERATURE. 85
logie der Keimblatter bei den Mollusken. Zeitschr. f. wiss.
Zi.nl. Bd. xxvi. 1876.
27. Korschelt, E. Ueber die Entwicklung von Dreissena poly-
morpha Pallas. Sitzungaber. Gesellsch. Naturforsch. Freunde.
Berlin, July, 1891.
28. Lacaze-Duthiers, H. Memoire sur le developpement des
branchies des Mollusques ac^phales lamellibranches. Ann.
Sci. Nat Zool. (iv.) Tom. v. 1856.
29. Lankester, E. Eay. Contributions to the Developmental History
of the Mollusca. Phil. Trans. Roy. Soc. London. Vol. clxv.
Part i. 1ST-").
30. Leuckart, K. Ueber die Morphologie unci Verwandtschaftsver-
haltnisse der wirbellosen Thiere. Brunswick, 1848.
31. Leydig, F. Ueber Cyclas cornea Lam. Archiv. Anat. mid
Phys. 1855.
32. Leydig, F. Mittheiluhg fiber den Parasitismus junger Unioni-
den an Fischen in Noll : Tubing. Inaug. -Dissert. Frank-
fort a. M. 1866.
33. Lovex, S. Bidraytil kanned oin. Utreckl. af. Moll. Acephala
Lamellibr. Vetensk. akad. Hand/. 1848, and Archiv. f. Naturg.,
1849.
34. Martens, E. von. Eine eingewanclerte Muschel. Der Zoolo-
gische Garten. Jahrg. vi. 1865.
35. Menegaux, M. (1) Sur le coeur et la branchie de la Nucula
nucleus. (2) Sur la branchie chez les Lamellibranches et sur
la comparaison avec celle des Scutibranches. Ball. Soc.
Philom. Paris, (viii.) Tom. i. 1888-89.
36. Mitsukuri, K. On the Structure and Significance of some
Aberrant Forms of Lamellibranchiate Gills. Quart. Journ.
Micro. Sci. Vol. xxi. 1881.
'M. Mobius, K. Die Auster und die Austerwirthschaft. Berlin,
1877.
3t>. Muller, F. Leber die Schalenbildung bei Lamellibranchiaten.
Schneiders Znnl. Beitrdge. Md. i. Breslau, 1885,
39, Patten, W. Eyes of Molluscs and Arthropods. Mitt/nil.
Zool. Stat. Neapel. Bd. vi. 1886.
-10. Pelseneer, P. Sur la classification phylogenetique des Pelecy-
podes. Bull. sci. France et Belgique (.1. Giard). Tom. xx.
1889.
11. Pelseneer, 1'. Contributions a I'etude des Lamellibranches.
Archiv. Bid/. Tom. xi. 1891.
ua LAMELLIBRANCHIA.
42. Quatrefages, M. A. de. Memoire sur l'embryogenie des
' Tarete (Teredo). Ann. Sci. Nat. Zool. (Hi.) Tom. xi. 1849
43. Rabl, C. Ueber die Entwicklungsgeschichte der Malermuschel.
Jen. Zeitschr. f. Naturw. Bd. x. 1876.
44 Rankin, W. M. Uebev das Bojanus'sche Organ der leich-
muschel etc. Jen. Zeitschr. f. Naturw. Bd. xxiv. 1890.
45. Rawitz, B. Der Mantelrand der Acephalen. Jen. Zeitschr. j.
Naturw. Bd. xxii. and xxiv. 1888 and 1890.
46 Ryder J A. The Metamorphosis and Post-larval Stages of
' Development of the Oyster. Annual Report of the Commis-
sioners of Fish and Fisheries for 1882. Washington, 1884.
47 Schierholz, C. Zur Entwicklungsgeschichte der Teich- und
Flussmuschel. Zeitschr. f. wiss. Zool. Bd. xxxi. 1878.
48. Schierholz, C. Zur Entwicklungsgeschichte der Teich- und
Flussmuschel. Berlin, 1878.
49. Schierholz, C. Ueber die Entwicklung der Umomdea.
Denkschr. k. Akad. icdss. Wien. Math. Vat. CI. Bd. xlv. 1889.
50 Schmidt F. Beitrag zur Kenntniss der postembryonalen
Entwicklung der Najaden. Archiv. f. Noturg. Jahrg. h.
1885.
51. Schmidt, Osc. Ueber die Entwicklung von Cyclas cahculata.
Archiv. f. Anat. n. Win*. 1854.
52. Sharp, B.' Remarks on the phylogeny of Lamellibranclnata.
Ann. Mag. Nat. Hid. (vi.) Vol. ii. 1*uiik\ indeed, of Kowaleysky's figures the bilateral symmetry is distinct, but
in others it appears to be less regular. This also applies to the mesoderm in
its later development. A cavity does, indeed, appear in the mesoderm which
Kowalevsky is inclined to regard as the coelom, but the stage in which it
appears is a comparatively late stage, the body being already somewhat de-
veloped. These points are, in fact, not sufficiently well understood to justify
us in drawing any definite conclusions.
In connection with the formation of the mesoderm, it should be mentioned
further that, at the blastulastage, i.e., when invagination is commencing,
isolated cells of various sizes are to be met with in the cleavage-cavity : these
maj possibly be mesoderm-cells, although Kowalevsky himself seems to be
inclined t>> think that the mesoderm arose in the way above described, and to
consider the occurrence of the^c cells in the cleavage-cavity as abnormal.
90
SOLENOCONCHA.
2. The Development of the Form of the Larva.
As early as the gastrula-stage, the embryo becomes free and is
capable of active locomotion, some of the ectoderm-cells being already
covered with cilia (Fig. 34 C). -Besides those ciliated cells which lie
at the cephalic pole and later form the ciliated tuft, the young larva
has three rows of such cells lying one behind the other at the middle
of the body of which they form a large part (Figs. 34 C and 35 .4).
Since these ciliated cells represent the pre-oral ciliated ring, the post-
oral part of the larva is very little developed. At this early stage,
the larva consists of comparatively few cells, which are still very large,
as is evident from a glance at Fig. 35 .4. In later stages, as the larva
grows in size and as its cells increase in number, the rows of ciliated
mot.
Ki,; 35 _ i-C three larvae of Dentaliuvi aged respectively 12, 24 and 37 hours (after
Kow'vlevsk'y) U, blastopore ; m, mantle-fold ; moe, permanent posterior aperture
of the mantle; //. posterior part of the body; w, ciliated ring; ws, apical ciliated
tuft,
cells are less conspicuous as compared with the rest of the body (Fig.
36 .4), and finally appear as a single though somewhat broad ciliated
ring (Fig. 35 .4-0). Meantime, the ciliated tuft at the cephalic pole
has become more conspicuous, and a large part of the anterior section
of the body has also become covered with delicate cilia (Fig. 35 B).
in the youngest larvae, #•/;:., at the gastrula-stage, the blastopore
was terminal, i.e., opposite to the cephalic pole (Fig. 34 C), but it
soon changes its position, shifting forward towards the ciliated ring-
along the future ventral surface (Fig. 35 .4). The larva thus
assumes a somewhat irregular shape, the flattened ventral surface
being somewhat backwardly inclined. At the same time, the pre-
oral part of the larva, that lying in front of the ciliated ring, has
THK DEVKI-Ol'JIKN'T OK THE FORM OK THE LARVA.
ill
become more conical, and the posterior (post -oral) part somewhal
lengthened (Fig. 36 A). Tin1 blastopore, which lias now become
narrow and slit-like, is displaced inwards by the development of an
ectodermal depression, the stomodaeum, which gives rise to the
buccal mass and the external aperture of which persists as the adult
month (Fig. 36 .4). The early larval stages of Dentalium closely
resemble those of Patella., as may be seen by comparing Figs. 35 and
36 with Fig. 50, p. 124.
If we were justified in comparing the larvae of the Amphinenra
and of the Lamellibranchia with the Annelidan Trochophore (pp.
5, 32 and 128), we may also attempt a similar comparison for the
fl.
d5.
Fig. :iti. .1 and />', median longitudinal sections through larvae of Dentalium aged
respectively about 14 and 34 hours (after Kowalevsky). ///, month : md, enteron ;
mes, mesoderm; oes, stomodaeum; sd, shell-gland; w, ciliated ring; ws, ciliated
tuft at the cephalic pole.
larva of Deiitnlium. In spite of the fact that the neural plate and
the kidney, two important organs of the Tmchojjhwe, have not as
yet been demonstrated in the larva of Dentalium, we can still see a
very striking resemblance to the Trochophore. Thus, in the conical
pre-oral region with its apical tuft of cilia, in the pre-oral ciliated
ring, in the relation of the blastopore to the future month, and in
the development of the body by an elongation of the post-oral region,
we see distinct Trochophoran characters. The aims only appears at
a later stage together with the paired rudiment of the cerebral
ganglion (which is perhaps connected with the cephalic plate). The
larva of Deninlium, however, may be distinguished by the presence
92 SOLENOCONCHA.
of a certain character typical of the Molluscan larva. Thus, a dorsal
invagination of the ectoderm (Fig. 36, *<7) becomes differentiated at a
very early stage (^4), then deepens and flattens out again later ; this
organ, from its development and subsequent modification, as well as
in its position, is seen to be the shell-gland, a structure peculiar to
the Mollusca. A comparison of the figures of the Dentalium larva
with those of the Lamellibranch and Gastropodan larvae (Figs. 14,
p. 28, 15, p. 31, and Fig. 50, p. 124) will enable the reader without
further assistance to recognise the great resemblance in the position
of the organs in these different larval forms. As the shell of
Dentalium is secreted on the dorsal surface of the posterior section of
the body, just where the shell-gland appears, it shows the same
manner of origin and shape as the young shells of other Molluscs.
It shows special resemblance with that of the Lamellibranchs, since
it extends like a saddle from the back on to the two sides of the body,
but, whereas the young Lamellibranch shell soon becomes bivalve,
the shell of Dentalium remains single, i.e., it remains to a certain
extent at ;t stage which, in the Lamellibranchs, was found to precede
the bivalve shell (p. 60).
Before the shell develops, further important changes take place in
the free-swimming larva of Dentalium, the post-oral region being the
first affected by them. During the early stages, this section is very
inconspicuous (Fig. 34 C), but it soon increases in size. This region
by its growth gives rise to the greater part of the adult body, the pre-
oral section degenerating almost completely. We find in this respect
a similarity between Dentalium and the Amphineura (pp. 5 and 6),
and when treating of these processes in the latter, they were compared
with the corresponding processes of metamorphosis in the Annelida.
At an early stage, the pre-oral portion of the body becomes
somewhat swollen and distinctly marked off' from the post-oral part
(Figs. 35 and 36 B). The definitive mouth is derived frqm an
invagination lying immediately behind the ciliated ring (Fig. 36, //>).
The depression on the dorsal side which is to be regarded as the shell-
gland (srl) has already been mentioned. When the post-oral section
has increased still further in size, two folds laterally placed arise on
it ; these grow out towards the ventral middle line and at a some-
what later stage meet, at first near the posterior end (Fig. 35 C, >//).
These folds, the free edges of which fuse later, represent the rudi-
ment of the mantle which thus rises here very much in the same way
as in the Lamellibranchia. The folds enclose a ventral swelling,
the foot (Fig. 38 B,f), at the base of which the otocysts are to be
THE DEVELOPMENT OP' THE FORM OF THE LARVA. 93
recognised early. These lie rather near the ciliated ring and arise as
depressions of the ectoderm which become detached from the latter
as closed vesicles. The pedal ganglia also develop as paired thicken-
ings of the ectoderm near the otocysts ; at a later stage, they also
become detached through delamination. In the middle line of the
foot, there seems to be an invagination which perhaps corresponds to
the pedal gland described fin- Chiton.
While these changes are taking place in the post-oral part of the
larva, the pre-oral section which, in consequence of the preponderance
of the former region, appears comparatively reduced, also under-
goes modification. Tims, two ectodermal depressions appear close to
the ciliated tuft ; these at first are shallow, but deepen more and
more (Fig. 37 .4 and B, eg) and eventually give rise to two closed
vesicles which are the paired rudiment of the cerebral ganglion.
The cells lining these depressions are, at first, directly continuous
with the ectoderm of the cephalic pole, the two depressions being
connected together by the cells surrounding the apical ciliated tuft,
and thus they represent a common brain-rudiment. The invagina-
tions, which have become tubular, grow in further and further until
they reach the walls of the stomodaeum (Fig. 37 B). At the same
time, by the active proliferation of their cells, they become con-
siderably thickened. They also finally become detached from the
ectoderm (C) and undergo differentiation into fibrous masses and
ganglionic cells, so that there is no room for doubt as to their
ganglionic character. Only at a later stage does a commissure form
between the two halves of the ganglion which now lose their vesicular
character.
The pedal ganglia, as above shown, arise- by delamination from the ectoderm,
while the cerebral ganglia originate as invaginations. This is somewhat re-
markable, since the cerebral ganglia arise, as a rule, through delamination,
in other Mollusca. Considering the greater contractility of the larva, the
presence of such invaginations suggests a more or less temporary infolding oi
the surface. Kowalevsky assumes that these ganglia first arose as a surface
thickening, and explains the invagination of the ganglionic rudiment as due
to the absence of room for surface-expansion owing to the limitation of the
pre-oral area by the forward con -'-titration of the ciliated ring. The develop-
ment of the cerebral ganglion in Dentalium recalls the condition which we
shall find in various Gastropods, where it undoubtedly arises by invagination
(p. 191). Since, in these latter cases, we have to do with more specialised
forms, it would be desirable, in instituting a comparison with Dentalium, to
ascertain in what way the cerebral ganglion arises in the more primitive
Gastropoda, especially in the Diotocardia.
94
SOLENOCONCHA.
While the nervous system is forming through the processes just
described, both the ciliated tuft and the ciliated ring undergo reduc-
tion (Fig. 37). This is especially
the case with the latter which, in
accordance with the nomencla-
ture used for other Molluscs,*
is here also called the velum.
The velum is the chief swim-
ming organ and, when it degene-
rates, the larva has to adopt
another method of locomotion.
At the stage depicted in Fig.
38, the velum appears still
greatly developed, but, as the
conical apical pole has degene-
rated, the anterior section of
the larva now) seems flattened
and plate-like. When the
velum is more reduced and
the other parts of the body
(the shell, the foot, etc.) better
developed, the larva sinks to
the bottom, where it still swims
to some extent by means of the
velum, but also creeps with
the assistance of its foot, just
as do other Molluscan larvae
when passing over to the adult
form (<■/. p. 42 and Figs. 53,
54, 67, etc.). The free-swim-
ming life of the larva lasts
quite four days, during which
time it does not, like the
larvae of the Lamellibranchia
and the Gastropoda, move at
the surface of the water, but appears to maintain itself at various
depths (Lacaze-Duthiers).
Otf.
s.
.
Fig. 37. — A-C, frontal sections through
older larval stages of Dentalium, showing
the formation of the brain (after Kowa-
LEVSKT). eg, rudiment of the cerebral
ganglion ; ///. mantle ; oes, stomodaeum :
s, cephalic pole; w, pre-oral ciliated ring.
Cf. on this point pp. 33 and 125.
THE TRANSFORMATION OF THE LARVA INTO THE ADULT. 95
3. The Transformation of the Larva into the Adult.
Even at the time wrhen the larva sinks to the ground, though still
at first moving with the help of the velum, the principal organs of
the adult are already present as rudiments. This last period of its
development is therefore marked by the growth and the further
development of rudiments already present in it.
tf we examine the larva externally (Fig. 38 B), we find that the
shell has grown much larger. At first it was a disc-like structure
lying on the hack, but then it became saddle-shaped, growing down the
sides of the larva till its free edges united in the ventral middle line
(Fig. 38 A). In the
ventral parts of the
shell, a parallel
striation can be recoer-
nised (Fig. 38 />'),
representing lines of
growth, so that the
growth takes place
here in the same Way
as in the shells of the
Lamellibranchia (Fig.
27, p. 60). As the
shell increases in size,
the fusion of the
ventral margins be-
comes closer. At first
the anterior aperture of the shell is still considerably wider than the
posterior, a condition connected with the shape of the larva (Fig.
38 B), but when the velum degenerates and the shell lengthens, the
anterior aperture becomes relatively smaller. The shell now appears
almost cylindrical, its anterior aperture being somewhat wider than
its posterior aperture. Its increase in size is caused by the secretion
of new shell-material from the anterior tubular margin of the fused
mantle-folds, the newly formed parts being marked off from the older
parts by circular boundary lines ; these latter give the shell the
appearance, especially in older animals, of being segmented (Fig. 39).
At a later stage the shell assumes a dorsal curvature and gradually
acquires the tubular. conical shape found in the adult. The anterior
and posterior apertures, which originated through the lateral growth
Fig. 38.— Larvae of Uentalium, .1 at the end of the
3econd day ami /,' (in the third or fourth day. J,
seen from the ventral .side, B, seen somewhat obliquely
from the same side (after Lacaze-Duthiers). /', foot ;
nine, posterior aperture of the mantle; s, shell; w,
ciliated ring (v, velum) ; ws, ciliated tuft.
96
SOLENOCONCHA.
and ventral fusion of the shell-plate (Fig. 39 A and />), are retained
throughout life.
The shape of the shell, which is at first cylindrical and then tusk-
like, is due to the mantle first assuming this form. The latter has
already been mentioned as growing out, like the shell, from the back
in the form of two folds, which fuse ventrally. Like the shell also
it remains open anteriorly and posteriorly. Anteriorly it grows to-
gether with the shell in the form of a tube for some distance over
the body which lies entirely hidden within it. The foot which, as
B.
I s.
%
--r"' /
— - d.
Fig. 39. — A, a larva of Dentalium undergoing metamorphosis ; I',, anterior portion of
a young Dentalium (after Lacaze-Duthiers). d, intestinal canal;/, foot; moe,
posterior aperture of the mantle ; •-;, shell ; /, tentacle-rudiment ; v, velum.
we saw, originated as a large ventral swelling behind the oral aper-
ture, can be extended for some distance beyond the anterior aperture
of the mantle. It soon assumes the triangular form characteristic of
Dentalium (Fig. 39 .4 and B, /). In spite of the early development
of this exceedingly characteristic shape, it is not to be considered
a primitive featui'e, but must be regarded rather as a later acquisi-
tion, as it is wanting in a few genera Plate (No. 3). In Siphono-
dentalium and Gadulus the two lateral lobes are wanting, these genera
apparently exhibiting a more primitive form of foot.
THK TRANSFORMATION OK THE LARVA INTO THE ADULT. 97
At a somewhat later stage, al which the velum is still retained, the
fool is found protruded from the shell (Fig. 39 A). This sta^e as
well as the younger one depicted in Fig. 38 B, recalls that stage
in the Lamellibranch larva in which the larval and the adult organs
of locomotion are present and functional at the same time (Fig. 20,
p. 42). At the posterior end of the larva, an early specialisation
of the mantle-folds produced a well-marked channel, lined with
powerfully ciliated cells (Fig. 38 and 39, m»e). This ciliation is
connected with the circulation of the water, which is further pro-
moted by the ciliation of the mantle-cavity.
The foot, as already mentioned, lies in front of the oral aperture.
It is here that the prominences arise which give origin to the
tentacles (Fig. 39 />', /). According to Lacaze-Duthiers, there are
at first three of these, two lateral and one smaller median prominence
(Fig. 39 B). These structures, by lengthening, give rise to the
tentacular filaments which are so numerous in the adult. The
description given does not explain the relation of the filaments to the
prominences and to the oral aperture, but the condition of the
tentacles in the adult enables us to form some conclusions on this
subject. In the adult, the mouth lies surrounded by leaf-like labial
appendages at the apex of an egg-shaped projection which, together
with the tentacular filaments that are innervated from the cerebral
ganglion, must be regarded as the cephalic region. The tentacular
filaments arise from two lobes lying at the base of the cephalic
projection, so that here also, there are three prominences which
might be traced back to those found in the larva. We should then,
as m the (histropoda, consider the middle prominence as the rudiment
of the oral cone, and the lateral prominences as the two original
tentacles, from which later the tentacular filaments arise.
\ similar view of the tentacle-filaments of the adult is taken by Thiele
(Literature to Chapter xxxiii.). who compares the two lobes or tentacular
shields with the large tactile lobes of Haliotis which are beset with tufts.
These latter, if lengthened, would result in structures resembling the ten-
tacular filaments. Quite recently Plate (No. 3) also has accepted this view,
ascribing to the three prominences on the head of the young animal the'
above significance.
The radular sac arises during the later stages of larval life as an
outgrowth of the stomodaeuin. The anus also appears in the larva
as a slight depression of the ectoderm behind the base of the foot.
The enteron, according to Kowalevsky, becomes connected with it
direct, without the formation of an ectodermal rectum.
H
98 SOLENOCONCHA.
Further ontogenetic processes especially connected with the development of
the inner organs, are described by Lacaze-Duthiers, but these processes, which
are evidently very difficult to make out, could, at the time when he wrote,
only be studied in the complete animal, and could not thus be clearly under-
stood. The above account, in which the most essential ontogenetic phenomena
are described, must here suffice, and for further information we must refer the
reader to the original treatise on the subject (No. 2).
LITERATURE.
1. Kowalevsky, A. Etude sur l'embryogenie du Dentale. Ann.
Musee Hist. Nat. Marseille Zool. Tom. i. 1883.
2. Lacaze-Duthiers, H. de. Histoire de l'organisation et du
developpement du Dentale. Ann. Sri. Xat. (4.) Tom. vi.
and vii. 1856 and 1857.
3. Plate, L. Ueber den Ban und die Verwandtschaftsbeziehungen
der Solenoconchen. ZooJ. Jahrb. Al.tli. f. Anat. Bd. v.
1892.
APPENDIX TO LITERATURE ON SOLENOCONCHA
{SCAl'HOPODA).
I. Simroth, H. In Bronn's Klass. u. Ord. d. Thierreichs. 1894-95.
Anatomy, Ontogeny, Phylogeny and Literature.
CHAPTER XXXII.
GASTROPODA.
Systematic Order : —
1. Prosobranchia (Streptoneura).
The gill or gills lie in front of the heart. The pleurovisceral
connectives are crossed. The sexes are distinct (save in
Valvata, Marsenina and a few parasitic forms).
Sub-order 1.- — Diotocardia. The heart has usually two
auricles. The ctenidia are bipectinate and free distally.
The pedal centres form long ganglionic cords connected
by transverse commissures and closely associated with
the pleural centres. Gonad opens into right nephridium
(save in Neritidae). The nephridium is generally paired.
(") Zygobranchia. Ctenidium paired, ventricle tra-
versed by rectum, two nephridia ; shell with apical or
marginal slit or row of perforations.
Haliotis, FusmreUa, Pleurotomaria.
(/') A zygobranchia. One ctenidium (left of Zygo-
branchs) ; two auricles (right ending blindly) ; heart
traversed by rectum (except in Helicinidae) ; nephridium
generally paired, operculate.
Turbo, Trnchus, Neritina (one kidney, distinct genital
aperture). Helicina (pulmonate, no ctenidium, one
auricle).
(c) Docoglossa. Gill single or absent ; heart with
single auricle, ventricle not traversed by rectum ; two
osphradia : two kidneys.
Patella (ctenidia absent), Acmaea.
Sub-order 2. — Monotocardia. Heart with one auricle ;
kidney and gill unpaired, the latter monopectinate and
100 GASTROPODA.
attached for its whole length (save in Valvafa). The
nerve-ganglia distinct and concentrated round oesophagus ;
pedal commissures rare. Genital aperture distinct,
dioecious with rare exceptions.
To this order belong by far the greater number of
Prosobranchia, all, indeed, of those the development of
which is dealt with here except the forms named above.
Janthina, Murex, Baccinnm, Purpura, Nassa, Fulgur,
Fusux, Fasciolaria, Strombus, Rostellaria, Crepidula,
Calyptraea, Vrrmetus, Bythinia, Paludinq, Thyca, Stili-
fer, Entoconcha, etc.
Sub-order 3. — Heteropoda (Nucleobranchia). The char-
acter of the nervous system, the position of the gill,
ventricle and auricle the same as in the Monotocardia.
Foot developed into a fin.
Oxygyrus, Af/m/ta, Pfemtrachea, Carinaria, Firoloida.
II. Opisthobranchia.
The gill and auricle generally behind the ventricle (except in
Actaeon). Pleurovisceral commissures rarely crossed
{Actaeonvlae). Hermaphrodite, marine.
Sub-order 1. — Tectibranchia. Shell generally present, often
much reduced and interna], wanting in Rancina and
Pleurobranchea ; with mantle-cavity containing a cteni-
dium.
Actaeon, Bulla, Acera, Gasteropteron, Philine, Apli/sia,
Pleurobranchun, Pleurobranchea, Umbrella.
Sub-order 2. — Nudibranchia. Without shell in adult stage ;
mantle, ctenidium and osphradium wanting.
Tritonia, Do?'is, Chromodon's, Polycera, Tergipes, Elysia,
Aeolin, Doto, Fiona.
III. Pteropoda.
Pelagic Gastropods in which the head is much reduced, and
the foot is developed like a fin ; now generally classed
with the Opisthobranchia.
Sub-order 1. — Thecosomata. With calcareous or carti-
laginous shell, with mantle and mantle-cavity.
Spirialis, Liwacina, Tiedentannia, Cymbub'a, Cavolinia,
Hyalocylix, Styliola, Cleodora, Creseis.
OVIPOSITION AND CHARACTEP. OF THK EGG-CAPSULES AND EGG. 101
Sub-order 2. Gytunosomata. Without shell and mantle.
Olione., Pneumodermon.
IV. PULMONATA.
Principally fresh-water or terrestrial. Ctenidium wanting ;
mantle-cavity modified as a lung. The pleurovisceral
commissures are not crossed. Hermaphrodite.
Sub-order 1. — Onchidiacea. Marine or littoral, without
shell ; anal and pulmonary orifice posterior.
Onchidium, Vaginulus.
Sub-order 2. — Basommatophora. Fresh-water and terres-
trial (usually maritime) Pulmonates. Eyes at the bases
of the tentacles.
Limnaea, Planorbis, Ancylus, Aurictda.
Sub-order 3. — Stylommatophora. Terrestrial Pulmonates.
Eyes at the tips of the tentacles.
Succinea, Vitrina, Claimlia, Bulimus, Helix, Test art'/ hi,
Daudebardm, Limaz, Arhn.
1. Oviposition and Character of the Egg-capsules and Egg.
The Gastropoda * are mostly oviparous, but oviposition takes place
in such a variety of ways that we can only give a few examples.
An exceedingly simple method of oviposition is found in Patella,
the eggs of which are laid singly and are apparently fertilised in the
water, as copulatory organs are wanting in this genus. It was there-
fore possible to fertilise these eggs artificially (Patten, No. 82).
Each egg is surrounded by a somewhat thick radially striated en-
velope which has a funnel-like projection with a wide aperture (the
micropyle).
In most Gastropoda, however, fertilisation takes place within the
body of the mother, and the eggs are not laid singly but unite to
form larger or smaller masses of spawn. The spawn may have the
form of disc-shaped or long hyaline gelatinous masses (fresh- water
Pulmonates). Each egg within the gelatinous mass is further
* A more detailed description of the spawn of land and fresh-water Gastro-
pods is given by Pfkiffkh (No. 88). A detailed account of oviposition in
Gastropods and notices of the literature on the subject are given by KEFEB-
. i No. 52) and can also be obtained from the treatises referred to in the
Literature. [A good general account of the egg-capsules will be found in
Fischer's Manuel ch C"/u7/////<>/<>, 1S87. — Ed.]
102 (.ASTROPODA.
surrounded by a transparent membrane. In certain marine Gastro-
poda, e.g., in various Opisthobranchia, tbis gelatinous spawn attains
a great size, forming long, ribbon-like coils (Aeolis) or round cords
repeatedly bent back on themselves (Aplysia). In these cords, the
eggs either lie irregularly or else are arranged in one or more rows.
The mass of spawn often takes the form of a ribbon which is spirally
coiled (Doris, Doto, Pleurobranchus, etc.). These gelatinous masses
frequently contain a very large number of eggs, the spawn of a single
Doris having been estimated to contain 600,000 eggs. The spawn
sometimes has the form of a gelatinous sac attached to the substratum
by a stalk and containing thirty to forty eggs (Ten/ijjp*, according to
Salenka, No. 114).
The eggs of the Heteropoda are also laid in gelatinous masses
which take the form of long ropes (Carinaria, Pterotrachea, Firo-
loida) according to Fol (No. 31); only the Atlantidae {Atlanta,
Oxygyrus) seem to lay their eggs singly, each surrounded by a
gelatinous envelope. The eggs of the Pteropoda also are found in
gelatinous masses which are usually tubular in sbape. These tubes
contain a great number of eggs placed either one behind the other
or else close together. The spawn less frequently appears in the
form of a thin membranous plate (Ore-ins aciculata), or as round
balls containing a large number of eggs (Olione).*
In Fissurelln also the spawn forms a gelatinous mass containing a
large number of eggs and deposited on stones. The Prosobranchia for
the most part differ greatly from the above in their method of
oviposition. A variable number of eggs are usually enclosed in an
egg-capsule, the shape of which varies in different forms. Besides
the eggs, this capsule contains a fluid or viscid substance which
serves as nourishment to the embryo. We are hereby reminded of
the Oligochaeta and Hirudinea (Guat/iobdellidae) in the cocoons of
which several embryos are found floating in a nutritive fluid (Vol. i.,
pp. 281 and -'591). The comparison becomes all the more striking
when we find that in a few Prosobranchs, as in the Oligochaeta (p.
281), not all the eggs in a capsule develop, but a few, or it may be
a large number disintegrate, and serve as food for those that survive.
In many Prosobranchia, however, all the eggs in a capsule develop,
in Fulgur, from 12 to 14, in Nassa, from 5 to 15, etc. In Purpura
floridana, the capsules contain many eggs, all of which undergo
* Detailed statements as to the oviposition in the Pteropoda and also in the
Heteropoda are found in the works of Fol (Nos. 31 and 32).
OVIPOSITION \N1> CHABACTEE OF THE EGG-CAPSU LES AND EGG. lO-'J
cleavage, some of the embryos, however, develop no further, but
perish, their remains being devoured by the other embryos. This
is also the ease, according to McMubbich, in a few species of
Crepi'liila, and in Uracil '/>//ix (Brooks). Fa-sciolaria lavs about 200
eggs in each capsule, but only I to 6 of these develop, and this is also
the ease with Buccinam widntum. Each capsule of Pur/jura lapiHus
contains 400 to 600 eggs, only 10 to Hi of which develop into mature
embryos (Selenka). The egg-capsule of Neritina fluviati/is also
shelters a large number of eggs i according to Blochmann 70 to 90)
although <>nlv a single embryo in it attains complete development
(Clapakede). In this case, the unfertilised eggs divide soon after
the polar bodies have formed, and break np into irregular heaps of
protoplasmic spheres, being in this way distinguished from the eggs
undergoing cleavage.
In shape and structure, these egg-capsules vary greatly. As a
ride they are formed of tough leathery or parchment-like integument
and are in some cases approximately spherical, but appear flattened
on the side by which they are attached to foreign objects. This is
the case in Nerltin-i. the older cocoons of which easily divide into
two hemispherical halves. To allow the brood to escape, the capsule
occasionally has an aperture closed by a delicate membrane, situated
opposite to the point of attachment. Several capsules are usually
found together, as in r>n>-<-iinni< widatum, Fusus antiqnus and others,
the capsules of which are piled one upon another, thus forming an
enormous mass of spawn. They occasionally appear laterally com-
pressed and, in one species of F/isus observed by Bobretzky, are
round plano-convex discs, attached by the flattened side. The
capsules of Bitsycon (Ftdgur) also are leaf-like or rather disc-shaped;
these are arranged in a row like a roll of coins, and are attached to a
common filament. These capsules have an aperture opposite to the
points of attachment for the escape of the brood.
hi Na,isa mutabilis, the capsules are cup-shaped and attached by
the obliquely truncated end, the opposite pointed end carrying an
aperture at first closed by a membrane. The surface of these capsules
shows polygonal markings which form rib like or membranous ridges.
They are found united into large clumps on sea-weeds and worm-tubes.
The •cup-like capsules of many Prosobranchia are arranged in
groups attached by their narrow ends drawn out into stalks {Murex).
Here also, the aperture of the cup is closed by a membranous cover,
which opens when the brood is ready to hatch. In Purpura lapillus
10 to 1 •"> such capsules, which, however, are more Mask-shaped and of
104 GASTROPODA.
leathery consistency, are fastened to a similarly constituted, structure-
less membrane which, in its turn, is attached to a stone. The same
is the case with the capsules of Fasciolaria tulipa, in which the edges
of the cup are continued into a wavy membrane. The form of this
latter capsule seems to come nearest that of the well-known Janthina,
the cup-like capsules of which are attached to a kind of raft by
means of which the animal floats in the sea. This float is a large
spindle-shaped body formed of the same substance as the capsules
and containing air-spaces. It is connected by its pointed end with
the foot of the animal and from its lower side the capsules hang.
The float is also found in the male, and without its aid the animal
cannot move about freely in the water, so that it must not be
regarded merely as an organ connected with oviposition, although it
may perhaps be considered to have been primarily developed for this
purpose.
The conditions of oviposition in the terrestrial Gastropoda differ
somewhat from those of the aquatic forms. The eggs of the for-
mer may also be surrounded bv a gelatinous albuminous substance
and may be connected together into spawn-masses which resemble
rows of beads (Lima.'1) or else may be massed in larger numbers to
form gelatinous balls {Onchidium). In the latter case, the structure
of the spawn is rather more complicated, each egg being surrounded
by a mass of albumen which is enclosed in a transparent but resist-
ant envelope. The latter lengthens in a line with the two opposite
poles of the oval albuminous mass, forming at each end a thread
winch is continued into the envelope of another egg, so that the
eggs constituting the spawn are connected into wreath like chains
which are again surrounded by the common gelatinous mass. The
albuminous mass surrounding the egg usually, in the terrestrial
Gastropoda, becomes still further protected by a firm membrane
impregnated by lime-salts. A more or less thick calcareous shell
is thus formed around the egg : this, even in Helix [xmiatia, is of
somewhat firm consistency. The eggs are usually deposited in great
numbers (60 to 80 in Helix pomatia) in small holes in the ground pre-
pared by the parent animal and are then covered over with earth.
Species of BuUmus which live on trees roll up leaves into the form
of cornucopia' and lay in these their soft-shelled eggs.
The eggs of the terrestrial Pulmouata attain a considerable size.
Even the eggs of Helix pmivitia measure 6 mm. in diameter. Those of
the Ceylon form, Helix (Aoivtttt) Waltoid are as large as a sparrow's
egg (P. and F. Sakasix. No. 102), and those of an American species
OVIPOSITION AND CHARACTEB OF THE EGG-CAPSULES AND EGG. 105
of liul 'Hi //.-• which are oval, measui'e 5 cm. in length and are there-
fore larger than the eggs of pigeons. These eggs, in consequence of
their firm, smooth shell, closely resemble the eggs of birds, but are
distinguished from the latter by the fact that the actual egg (the
yolk) is always very small and floats in a great mass of viscid trans-
parent matter enclosed within the egg-shell. But although the yolk
or the egg-cell, as compared with the size of the egg is almost nil,
the mature embryo almost completely tills the shell, having increased
in size to this extent at the expense of the surrounding mass of
nutrient material.
Some Gastropods take care of their eggs. Those species of Crepi-
dida which are immovably tixed to one spot (C. fornicata, plana,
and convexa, McMubbich, No. 70, Coxklix, Xo. IV) retain the egg-
capsules, which are attached to the substratum, under cover of
the shell. The wall of the capsules thus protected are naturally of
delicate nature. Verinetus attaches a few capsules to the inner sur-
face of its shell, near the aperture of the latter (Lacaze-Duthiers).
In comparatively few Gastropods, the whole development is passed
through within the body of the mother. These forms are therefore
viviparous. The best known example is Pain/Una ( Vivipants) oivi-
para, the eggs of which develop in the oviduct, which functions
as a uterus, until the form of the adult is reached. Its course :>f
development, however, exactly resembles that of other Prosobranchia.
The egg is surrounded by a conspicuous layer of albumen, which
again is enclosed in a membrane that runs out into a twisted stalk,
so that a kind of cocoon is formed. As a rule, only one egg lies
within this envelope, but two are sometimes found in it (Leydig,
No. 68), the resemblance to the egg capsules of other Prosobranchia
being thus heightened. Similarly, in a few species of Melaitia [in
Typhobia and Nass and E, has been termed the spiral
cleavage. Thus, as early as the third cleavage, i.e., the formation of the first
quartette of micromeres, a curious obliquity becomes evident. This obliquity
is visible in the nuclear spindle even before the completion of the division,
but becomes more apparent at its close, when the cells of the upper quartette
(micromeres) lie in the furrows between the cells of the lower quartette
(macromeres). This "spiral" character is generally more apparent than is
represented in Fig. 40 C, but is well shown in D in the case of the second
quartette of micromeres. Spiral cleavage is of particular interest in view of
the fact that, in sinistral Gastropoda, the obliquity takes the reverse inclination
to that which is found in dextral forms (Crampton, No. V and Holmes, No.
XII I a i. For a general discussion of the significances of the forms of cleavage
in the Gastropodan egg see Conklin (No IV, pp. 185-192).— Ed.]
CLEAVAGE \M> FORMATION OP Till-: c; K KM -LAYERS.
109
bo the Turbellaria, but tin- mode of formation of the mesoderm described by
this author so little agrees with what is found in other Gastropods, that it
must be regarded as quite improbable, especially when we remember that
I'.i.oc mm \\\. who investigated the untogenv of A/ili/sia at the same time as
M \NKKi:i)i. saw nothing of this process, and M v/.y. mu.li.i who, quite recently,
lias made similar investigations, describes the formation of the mesoderm in
an eut irelj different way.
a.
J3.
Fig. 40.- -I-//, diagrams in illustration of the cleavage and formation of the germ-
layers in the Gastropoda ^principally after Rabl and Blochmamn). A and /.', seen
from the side; ('-/■'. seen from the animal, and // from the vegetative pole ; G
represents an optical section. I- IV denote the large cleavage-spheres, from which
the micromeres (I'-IV, I' -IV" are abstricted by successive divisions, 1-4, micro-
meres, arising from /'-/I", eet, ectoderm; ent, entoderm; mes, mesoderm; >/.-.
polar bodies.
The rudiments of the germ-layers develop, as in the Amphineura
and Lamellibranchia, very early. In Planorhis, according to Eabl,
110 GASTKOPODA.
the posterior of those two macromeres which are in contact with one
another mesially, divides into two cells, the smaller of which shifts
towards the centre of the egg. The other three macromeres also give
oft' such a small cell towards the centre, so that there are now four
small entoderm - cells (Fig. 40 H). The posterior macromere then
divides into two large cells of about equal size (//, mes) and the other
macromeres also divide (H, rut). In Neritina, a similar process takes
place, hut the size and position of the cells is somewhat different (Fig.
40 G, me-i and ent). In Crepidala and Umbrella also (Fig. 48 B, p.
120), one of the posterior macromeres gives rise to an entomere and
to a cell which divides into a right and a left half. These two last
cells are the primitive mesomeres and, according to their origin,
either already lie in the primary body-cavity (G) or else are pressed
into that cavity later. This latter is the case when, as in Planurbis
(Fig. 40 H), these cells (mes) at first form a continuous circle with
the large cells (ent). A cleavage-cavity is sometimes first developed
at this stage, by the partial separation of the layer of micromeres
from the macromeres, or else it forms still earlier, so that even before
the stage represented in Fig. 40 H, the embryo may exhibit the
form of a blastula with a wall much thickened at the vegetative pole,
in which case an invagination-gastrula restilts (Planorbis).* In the
first case, however, in spite of the fact that the formation of an
epibolic gastrula has already commenced (G) or has been actually
attained through the failure of the micromeres to rise up from the
macromeres, an invagination may also take place later owing to the
appearance of a rather large cleavage-cavity. In this latter case,
however, the germ-layers may also already have appeared as rudi-
ments. The macromeres next give off at the vegetative pole a few
small cells (G and H, mt) which, together with the former, repre-
sent the rudiment of the entoderm. The rudiments of the tlrree
germ-layers are now visible ; the ectoderm has arisen from the micro-
meres, the entodern. is represented by the macromeres and their last
derivatives, and, finally, the mesoderm is found in the form of two
cells (derived from one of the [posterior] macromeres). \
* [The cleavage-cavity seems to be very variable in the Gastropoda, and even
in those forms in which it is most conspicuous, it is found to vary at different
stages of cleavage. This variation is most noticeable in Limax, and Kofoid
(No. XIV) thinks that this cavity is connected with the excretory processes of
the lilastomeres. The cavity is most developed in those Gastropods in which
the gastrula is embolic and, during invagination, it becomes temporarily
obliterated, but re-appears later (Planorbis, Uabl, No. 90). — Ed.]
+ [It will be seen that if the interpretations given on p. 107 of the relation
between the first and second cleavage-plaurs and the axis of the adult body
CLEAVAGE AND FORMATION OF THF GEKM- LAYERS.
HI
The formation of the germ-layers does not take place in all Gastro-
pods in the manner just described, indeed, the layers form in very
different ways in diverse Gastropods, as might be expected from the
variations found in the manner of cleavage- It has already been
mentioned that such variations occur in spite of strong general
resemblance. The method of cleavage described above applies, with
slight modifications, to many Gastropods. We append a list of a few
genera chosen as representatives from the different divisions in which
this is the case: among the I'rosobranchia, Fissurella (No. 12),
Neritina (No. 7), Crepidula (Nos. '-'4 and 25), Bytkinia (No*. 91/
101 and 28), Vi rmetus ( No. 99), Ftisus (No. 11), Entoconcha (No. 76) ;
anions the Heteropoda, Firoloida and Pterotrachea (No. 31) ; among
the Pulmonata, Planorbis (No. 91), Limnaea (Nos. 130 and 131),
Fig. 11. stages in the cleavage ol Cavolinia tridentata (.1) and Aplysia limacina \J'>)
(after F"i. ami Blochmann). I. -IV., tin- four macromeres, above them lie the
micromeres ami the polar bodies irk).
Limax (Nos. 130 and 73), Onchidium (No. 51); among the Opistho-
branchia, Doto, (No. 91), Ercolania (No. 124), Tethys (No. XXVI),
Umbrella (No. XII); among the Pteropoda, Cavolinia, Cymbulia
(No. 32), Clime (No. .".5).
Certain modifications in the cleavage are no -doubt principally
determined by the amount of yolk in the egg. These are connected
specially with the size of the macromeres. In Cavolinia and ( 'ymbulia,
are correct, then there must be two anterior and two posterior macromeres,
and it is from one of the latter that the primitive mesomere is now said to
arise. It seems further probable that the first mesomere arises from the left
posterior macromere in dextral and from the right iu sinistral Gastropoda. In
spite, however, of the large amount of evidence which is accumulating in favour
of this view we must, when we consider the great difficulty in tracing the rela-
tions of the early cleavage-planes, wait for further observations, especially on
Prosobranchs. before we finally conclude that this origin of the mesoderm is
typical of all Gastropoda. See footnote, p. 119. — Ed.]
112
GASTROPODA.
for instance, one of the four macromeres is markedly smaller than the
others, although the cleavage, in other respects, follows the usual
course (Fig. 41 A). At the four-celled stage in A'plysia, two blasto-
meres are distinguished by their smaller size, a difference which can
be recognised in the later stages also (Fig. 41 B). Although the two
smaller macromeres are still visible at this stage (B, III. and IV.), yet
in later ontogenetic stages, only the two larger ones are still distinct,
and these are apparent until grown over by the micromeres (epibolic
gastrulation, Kay Lankester, Chap, xxvi., Lit. Xo. 29 ; Manfredi,
No. 72, Blochmann, No. 8). Another Opisthobranch, Acera, re-
sembles Aplvsia in this respect (Rabl, No. 91 ).
Fig. A2.—A-E stages of cleavage in Nassa mutabilis (after Bobretzky from Balfour's
Text-book). A-C, formation of the macromeres, on which, in I), four, and in E a
large number of micromeres lie.
The first stages of cleavage, in Nasso, mutabilis, are very striking
and peculiar (Bobretzky, No. 11). The egg contains a large
amount of food-yolk, and the formative protoplasm is aggregated at
the animal pole, over which the polar bodies are situated. An
equatorial and a vertical furrow, the former near the animal pole,
appear simultaneously, and divide the ovum into three segments,
two smaller blastomeres which are produced by the vertical furrow
and one large brown sphere, minus a nucleus and consisting entirely
of yolk-material (Fig. 42 A). The two blastomeres thus rest upon
this sphere somewhat like a germ-disc, except that the yolk has in
tli is case not attained to any great size. This condition soon dis-
THE FORMATION OF THE ( i ERM-LA VKKS.
113
appears, the yolk-sphere fusing- with one of the blastomeres (Fig. 12
/>') ; at the four-celled stage, produced by a triple segmentation of the
large sphere and division into two of the small blastomeres, it re-
appears (C). The yolk-sphere, which at this stage is distinct from
the blastomeres, again fuses with one of the cleavage-spheres, and it
thus happens that the eight-celled stage (D) does not essentially
differ from the usual condition (Fig. 40 G) except for the fact that
one of the macromeres is specially large, the greatest mass of the
yolk having accumulated in it. The further cleavage seems to take
place in a regular manner and in a way similar to that above
described. Finally, here also, a large number of very small micro-
meres lie like a disc or cap upon the four macromeres (Fig. 42 E).
At a later stage, in Nassa, there is one large cell which is specially
distinguished from the rest. While the other cells divide further
it remains, on account of its large amount of yolk, almost unchanged.
It represents a kind of food-yolk which, in a much more specialised
form, will be found again in the Cephalopoda.
The preponderance of one macromere over the three others is found
to a striking degree in Purpura (Selenka, No. 115) and in Uro-
salp in.r (Brooks, No. 17; Conkdin, No. 24), forms which in their
ontogeny seem to resemble Nassa.
3. The Formation of the Germ-layers.
The first appearance of the germ-layers in a few forms has already
been alluded to in connection
with the phenomena of cleav-
age, but in other forms these
layers arise in a somewhat
different way, their origin in
some cases being so differently
described by authors that this
point calls for special atten-
tion.
Gastrulation is attained in
different ways in accordance
with the variations in cleav-
age. In the simplest cases,
e.g., Planorfiu and Patella,
a blastula with a compara-
tively large cleavage-cavity
arises (Fig. 43). The vegetative pole of the blastula is formed by the
I
Fig. 43.— Blastula-stage of Patella (after
Patten). The ciliated tuft (at the cephalic
pole) and the ciliated ring are already
indicated.
114
GASTROPODA.
macromeres and consequently appears much thickened. After the
mesoderm has become differentiated, the entomeres begin to increase
in number (Fig. 40 H, ent), and the whole entoderm becomes in-
vaginated into the cleavage-cavity, and thus a typical invagination-
gastrula forms (Planorbis, Eabl). In Patella, on the contrary, an
extremely large solid ingrowth of macromeres takes place from the
vegetative pole of the blastula (Figs. 49 and 50, p. 124). From this
ingrowth, the mesoderm and entoderm become differentiated and,
at a later period, an archenteric cavity forms within the till now solid
entoderm (Patten, Xo. 83).
In a few Gastropods, such as Bythinia and Limnaea, a cleavage-
cavity is present at an eaily stage, but this soon disappears ; the
Hi -<£>
Fig. 44 — A-C, embryos of Firoloida Desmaresti in the stage of gastrula-formation
(after FoLb hi. blastopore ; ect, ectoderm ; rk, polai* bodies.
blastula now becomes flattened, the macromeres prepare to invaginate,
and the micromeres, advancing towards the vegetative pole, grow over
the mesoderm which, has already formed, and a part of the entoderm
(Bay Lankester, Xo. 63; Wolfson, Xo. 131; Erlanger, Xo.
28). Gastrulation follows the same coui'se in Palwlina, with the
distinction that, in this form, the cleavage-cavity is from the first
very small, and the mesoderm only later becomes recognisable
(<■/. p. 134, Butschli, Xo. 18). In the Heteropoda also {Firoloida
and Carinaria) a more or less flattened blastula with a slit-like
blastocoele, the animal end of which is composed of small and the
vegetative of large cells (Fig. 44 ^4), gives rise by a similar process
TIIK FORMATION OF THE GERM-LAYERS.
115
to the gastrula (Fig. 44 B). When gastrulation commences, and
during- its course, the cleavage-cavity is but slightly developed, or
even entirely degenerates, but enlarges considerably at a later
period through the greater development of the ectoderm. The
archenteric cavity also is large (Fig. 44 0), and the archenteron thus
represents a wide sac (Fol, No. 31). These stages resemble those of
Paludina.
The partial circumcrescence of the macromeres by the ectoderm,
as it occurs in the last-named form, is a first indication of the
transition to the epibolic gastrula which is formed at an early stage
in the Pteropoda (Cymbulia, Clione). The cleavage-cavity here is
either entirely reduced or but slightly indicated. The thin layer of
ectoderm-cells then lies in close contiguity to the entoderm (Fig. 45
^4). But even here an invagination takes place. The middle ento-
a.
J3.
ect.
Fig. 45. — .4 and B, embryos of Clione limaeina showing the formation of the germ-layers
(after Knipowitsch). hi, blastopore ; ect, ectoderm ; eat, entoderm ; mes, meso-
derm.
derm-cells shift upwards, the ectoderm at the same time growing out
still further towards the vegetative pole and thus narrowing the
blastopore, and the epibolic gastrula thus has the appearance of an
invagination-gastrula (Fig. 45 B). A similar process was described
in connection with the Lamellibranchia {Ostrea, p. 27).
The gastrula arises by epibole in Fmus (Bobretzky, No. 11),
Aplysia (Blochmann, No. 8), Grepidula (Conklin, No. 24) and
Verinetu* (Salensky, No. 99). In these forms, the ectoderm, as a
thin layer, surrounds the four yolk-laden macromeres, from which,
at a later stage, small cells become detached, chiefly at the vegetative
pole, that is, in the neighbourhood of the blastopore ; by the develop-
ment of these small cells an archenteron is formed, bounded dorsally
by the four macromeres and ventrally by these small cells. In Neri-
Una, these cells form early, before the circumcrescence of the macro-
116
GASTROPODA.
meres has proceeded so far (Fig. 40 G, ent). According to Blochmann
(No. 7), the smaller entoderm-cells shift beneath the layer of ectoderm
towards the animal pole and here form, above the macromeres, a kind
of cap (Fig. 46). In this way an archenteron arises, which is bounded
partly by smaller
(All...
t.
Tim.
Fig. 46. — Embryo of Neritina flvmatilis in optical
section (after Blochmann). bl, blastopore ; erf, ecto-
derm ; ent, entoderm ; mes, mesoderm.
entoderm-cells and
partly by the mac-
romeres. Neritina
in this point more
nearly resembles the
forms considered
above, in which there
was a transition from
an epibolic to an in-
vagination - gastrula.
A cap of micromeres at
first lies on the large
macromeres, somewhat as in Fig. 40 F and G, but a cleavage-cavity
soon appears between the micromeres and the macromeres. As the
circumcrescence of the macromeres advances, the archenteron de-
velops, although in a way which deviates from that commonly met
with.
In Urosalpinz, Fulgur, Purpura and Nassa also, gastrulation takes
place through epibole (Brooks, No. 17; McMurrich, No. 70;
Bobretzky, No. 11), and in these forms, on account of the great
abundance of yolk, other variations in the formation of the germ-
layers are caused. It has already been shown that in Nassa mutdbilu
the one of these forms which has received most attention, as well as
in Urosalpinx and Purpura, one of the macromeres which is specially
rich in yolk is far larger than the others (Fig. 42 D). The micro-
mere-layer lies on the macromeres in the form of a disc or cap (Fig.
42 E). When the micromeres grow out towards the vegetative pole,
the three smaller maci'omeres also take part in the process of shifting
and in so doing increase in number (Fig. 47 B, hi/). Finally, these
cell-complexes, which represent the rudiment of the entoderm, become
more and more shifted towards the vegetative pole (Fig. 47 C and
D). They line a cavity which corresponds to the future lumen of
the enteron. It is the protoplasmic parts of the macromeres that
are at first used for the formation of the epithelium of the enteron ;
the rest forms a kind of food -yolk upon which the cells of the germ-
layers lie like a germ-disc (Fig. 47 B). As far as can be seen from
THE FORMATION OP' THE MESODERM.
117
Brooks' description, the entoderm forms in an exactly similar way
in Urosalpinx. A mass of food-yolk is also formed in Fusus, Ver-
metus, Aplysia, etc., by those macromeres which attain to so con-
siderable a size.
The Mesoderm. In connection with the account given of the
processes of cleavage, it was stated that the middle germ-layer arises
very early. In Planorbis, one of the posterior of the four macro-
7?i e
ju
PIG. 47.— A-D, longitudinal sections through embryos of different ages of Nassa muta-
1'ihs (after Bobretzky, from Balfour's Text-hook), bl, blastopore ; ep, ectoderm ,
r. rudiment of the foot ; hy, entoderm ; in, intestine ; m, mouth ; me, mesoderm ;
sf/, shell-gland ; st, enteron.
meres * divides, giving rise to an entomere and to the primitive meso-
mere, which latter eventually yields the two primitive mesoderm-
cells, as already shown (p. 110). These are soon pressed into the
cleavage-cavity, and, by their increase in number, give rise to the
two mesoderm-bands. This seems also to be the case in the Ptero-
* [This cell is believed to be homologous in all Gastropods and is now desig-
nated D by students of cell-lineage. — Ed.]
118 GASTROPODA.
poda (Clione, Knipowitsch, No. 55). In this case also, the division
of one of the four macromeres is said to give rise to two cells which
are soon driven inwards, these two symmetrically placed cells denot-
ing the posterior end. Knipowitsch conjectures that in those
Pteropoda in which, according to Fol, one of the macromeres is
distinctly smaller than the others, this smaller macromere yields the
primitive mesoderm-cells (Fig. 41 A, III). In Clione, each of the
two cells which arise by the division of the macromere again divides
into two large cells (mesoblasts, Fig. 45 B, mes), which now take up
a symmetrical and bilateral position at the posterior end and, by
continuous multiplication, give rise to smaller cells.
The radial character of the cleavage, which is so marked during the
early stages (Fig. 40 C-E), is much modified by the differentiation
of the mesoderm, and, when the two mesoderm-cells appear, the germ
attains a true bilateral symmetry (Fig. 40 H). This is the case
in Planorbis and a similar condition is shown in Bythinia also. As
in Planorbis, the primitive mesoderm-cells in Bythinia arise from one
of the posterior blastomeres, which is to be regarded as a mesentomere,
i.e., it divides into two cells, one of which remains as an entomere
in the position occupied by the posterior macromere, while the other
shifts slightly forward. This latter cell divides into two cells in
such a way that the two lie side by side ; these are the mesodermal
teloblasts which give rise to the mesoderm-bands (v. Erlanger, No.
28). The mesoderm rises in a similar manner in Grepidula (Conklin,
No. 24) * and Neritina (Blochmann, No. 7), although a few slight
modifications are here brought about by gastrulation taking place
through epibole in consequence of the large size of the macromeres,
or by a near approach to this form of gastrulation. In Neritina,
a cell becomes detached from one of the posterior macromeres which,
by division, gives rise to the two mesoderm-cells (Fig. 40 G). This
process can be made out very distinctly in the eggs of an Opistho-
branch {Umbrella) examined by Heymons (Fig. 48). Here also a
smaller entoderm-cell and a larger mesoderm-cell (B, ent and n>)
arise through the division of one of the postei'ior macromeres (^4 and
11). This primitive mesomere divides into two laterally placed meso-
derm-cells (C, urn) which soon give rise to the two mesoderm-bands,
formed of a few large cells containing yolk and other smaller cells
(I) and K). The rise of the mesoderm from one of the posterior
* [Conklin (No. IV.) now finds that, in Crepidula, the mesoderm does not
arise until after two further divisions, hut regards this as an exceptional con-
dition.— Ed.]
THE FORMATION OK THE MESODERM.
119
macromeres described in the last-named form seems to represent the
method of formation of the mesoderm most commonly found in the
Gastropoda.*
Far greater modification seems to prevail in the formation of the
mesoderm in those forms which, like Nassa, are exceedingly rich in
yolk, and yet it appears to its that it would be possible to trace back
* [The early developmental history of the mesoderm has now been investi-
gated in so many different Gastropods, all of which show such close agree-
ment on this point, that we must carefully bear in mind the possibility of this
method of mesodenn-formation being typical of the entire group. The -meso-
derm almost invariably first appears as a single cell which is constricted
from one of the posterior macromeres ; this unpaired mesomere then
divides into two cells, bilaterally arranged, which, as mesodermal teloblasts,
give origin to the paired mesoderm-bands. The macromere from which
the first mesomere originates is possibly the left posterior in all dextral
(ni-~tropods, and the right posterior in sinistral forms (Crampton). In the
great majority of the Gastropoda, soon after the last quartette of micromeres
has arisen, this macromere divides, thus giving origin to two cells, one of
which is an entomere, while the other is usually the primary mesomere, more
rarelv, Patella Patten), and Crepidula (Conklin now withdraws the account
given above), the two cells represent an entomere and a mesentomere, the
complete separation of the mesoderm from the entoderm only taking place
after further divisions. The origin of the inesoderm in Crepidula is expressed
by Coxklim as follows : —
'm1 small mesomere.
fME
D
(left posterior
macromere).
ME1 (right)-;
Me1
I , p [ fM1 mesodermal teloblast.
1 e {e1 secondary entomere.
E1 primary entomere.
E- primary entomere.
V- '- ' e" secondary entomere.
. ., j e \ M2 mesodermal teloblast.
L ME2 (left) l'
I m- small mesomere.
D ento-
mere.
In the majority of Gastropoda in which this point has been investigated,
as, for instance, Planorbis, Limax, Physa, Siphonaria, Tethys, Umbrella, etc.,
the condition is, as stated above, much simpler and may be expressed thus : —
MM
1>-
( M1 right mesodermal teloblast.
( M2 left mesodermal teloblast.
D entomere.
While the greater part of the mesoderm arises from the paired mesoderm-
bands, a smaller and more scattered portion appears to arise on either side of
the body from the ectoderm. This was suggested by Heymons in Umbrella
(No. XII.) and has since been confirmed by Conklin for Crepidula (No. IV.)
and Wierzejski for Physa (No. XXVII.) ; the scattered mesoderm has been
compared with the larval mesoderm of Unio (Lilue). — Ed.]
120
GASTROPODA.
the mode of formation of this layer in Nassa as given by Bobretzkv
(No. 11) to the method described above. In sections made through
such a stage in the egg of Nassa (Fig. 42 E), under a cover of
smaller cells, a few larger cells can be seen projecting into the
cleavage-cavity. The projecting cells detach themselves and yield
a few somewhat large cells which from this time lie in the cleavage-
cavity. These are the first mesoderm-cells and, since the cells
from which they were abstricted evidently correspond to one of
the smaller macromeres (Fig. 12 E), the mesoderm has an origin
similar to that in the cases previously considered. The smaller
tint,
Fig. 48.— A-E, a few stages of the cleavage and formation of the germ-layers of
Umbrella (after Heymons). A shows the four macromeres ; B, the division of the
mesentomere ; C, the formation of the primitive mesoderm-cells ; I) and E, the
formation of the mesoderm-bands. I-IV, the four macromeres, or their derivatives.
ect, ectoderm ; ent, entoderm ; m, the primitive mesomere ; mes, mesoderm ; urn, the
paired mesoderm-cells (mesodermal teloblasts) resulting from the division of m.
mesoderm-cells at first present soon again divide (Fig. 47 ^4), and
here also seem to yield structures akin to mesoderm-bands (Fig.
47 B).
The mesoderm is also found to arise from the macromeres in various other
forms, e.g., in Limnaea (Wolfson, No. 131) and Fulgur (McMurrich, No.
70), and Janthina, in which form, according to Haddon (No. 40) it becomes
separated from the macromeres at the top of the blastopore. At a stage in
which the ectoderm-cap has not completely grown round the macromeres, the
peripheral macromeres yield the mesoderm-cells. Haddon's account is too
slight and his figures too vague to allow any conclusions to be arrived at
THE FORMATION OF THE MESODERM. 121
regarding the origin of the mesoderm in Janthina. There are also various
other descriptions of the origin of the mesoderm in the Gastropoda which, an
they are still less well founded, cannot here be considered.
The mesoderm arises in Patella, as above, in connection with the
entoderm, but at a stage when further differentiation has taken place
in the embryo (Patten, No. 83). In Patella, there is a blastula,
from which the entoderm arises/as already shown, by the ingrowth
of large cells at the vegetative pole (Figs. 49 and 50). There are at
first four large cells, occupying the same relative positions as do the
four macromeres in other forms. Nowr, however, according to
Patten, a cell arises on each side of these four blastomeres which,
by division, gives oft* into the cleavage -cavity another rather large
cell. These two cells are regarded by Patten as mesentoderm-cells
(Fig. 50 A, em), and from them the two primitive mesoderm-cells
(mesodermal teloblasts) are derived. These lie near the blastopore,
at the posterior end of the larva and increase in number later from
behind forward (teloblastically). In this way the mesoderm-bands
arise, these being, according to Patten, developed with special
regularity in Patdla (Figs. 51 and 52, p. 126).
The mesoderm, in the Gastropods, has generally been considered to arise in
connection with the primitive entomeres before the formation of the arch-
enteron, but it has recently been asserted that it arises in the form of coelomic
sacs, an assertion which was specially startling because it was supposed that
the Molluscs showed no sign of the formation of enterocoeles, such condi-
tions having so far never been observed. In the differentiation of the meso-
derm, especially in the development of the pericardium, the Mollusca, it is
true, shew great agreement with certain " Enterocoelia," and there is no doubt
that, like these, they possess a secondary body -cavity, but, in this respect, they
approximate most nearly towards the Annelida, the formation of the meso-
derm from mesodermal teloblasts being like that in the latter group. Con-
sidering all that is as yet known of the formation of the mesoderm, we cannot
agree with the results obtained by Erlanger for Paludina, and must continue
to be sceptical about them until they are better supported or are actually
confirmed by new investigations (if possible made on other forms as well).
v. Erlanger's account is as follows : From the rather wide archenteron of
Paludina a bilobed outgrowth appears which gives the impression of a double
coelomic sac such as occurs for instance in various Echinoderms (Vol. i., pp.
407-409). This sac, which rises from the archenteron near the blastopore,
becomes detached later from the entoderm and now represents a vesicle
closed on all sides and symmetrical in form. The outer and inner walls
approach the ectoderm and the entoderm respectively so that at this stage
we might speak of a somatic and a splanchnic layer. It is evident that, up
to this point, the condition of the mesoderm closely resembles that of the
coelomic sacs in other animals. This, however, soon changes, for the coelo-
mic sacs, by giving off single cells, break up altogether, leaving only two
122
GASTROPODA.
insignificant vesicular vestiges surrounded by irregularly distributed meso-
derm-cells on the ventral side of the archenteron. These will be referred to
again later.*
Other descriptions in which the middle germ-layer is derived direct from
the ectoderm are difficult to reconcile with the accounts we have given of the
formation of the mesoderm. Such an ectodermal origin is attributed to the
mesoderm in Fusus (Bobretzky, No. 11) in Vermetus (Salensky, No. 99) and
in various other Gastropods (Fol). The eggs of Vermetus are very rich in yolk..
The ectoderm lies as a thin layer upon the macromeres, almost entirely en-
closing them. Near the blastopore, the increase in number of the cells of the
ectoderm is said to give rise to a thickening which is the rudiment of the
mesoderm. In Fusus, Bobretzky regards the latter as arising by a prolifera-
tion of cells from the lips of the blastopore. According to Salensky, this
mesoderm-rudiment is bilaterally symmetrical like the mesoderm-bands, but
another independent formation of mesoderm is said to take place in the
neighbourhood of the shell-gland. Salensky is inclined to regard this part
of the mesoderm as having arisen through delamination from the ectoderm
near which it lies, i.e., from the dorsal part of the body. There is some
similarity between this last view and the account given previously by P.
Sarasin (No. 101) of the origin of the mesoderm. According to Sarasin,
growths of the ectoderm occur at certain points of the body from which
mesodermal elements become detached. This takes place partly at an early
stage of embryonic development and partly later. Since this material becomes
abstricted at various times and at different parts for the formation of those
organs which are usually regarded as mesodermal, Sarasin is unable to assume
the existence of one uniform mesoderm-layer and therefore takes somewhat
the same stand-point as that adopted later by Kleinenberg in so decided a
manner for the Annelida (Vol. i., pp. 292 and 293). Primitive mesoderm-
cells and mesoderm-bands in Bythinia have been more recently described by
Erlanger (No. 28) and, according to the very definite account of Sarasin, we
should have to show whether, besides this distinct mesoderm-rudiment, a
further formation of mesodermal elements takes place from the ectoderm, as
* [In spite of the more recent investigations on this point, the true origin of
the mesoderm in Pabulum must still be regarded as undecided. In his
most recent publication, Erlanger (No. N.) gives figures which are difficult to
interpret in any other way than he has done. Consequently, he still regards
Paludina as enterocoelic, but he finds, besides the coelomic sac, paired
primitive mesoderm-cells near the blastopore which may be the forerunners
of the cells which form the enterocoeles. He suggests that the sparsity of
yolk has made Paludina more primitive in this respect than other Gastropoda.
Tonniges (No. XXV.). who has specially investigated this point in Paludina,
concludes, but without reference to Erlanger's latest work, that the meso-
derm arises shortly after the formation of the gastrula by a wandering in of
ectoderm-cells from that portion of the ventral surface which is formed by the
closing of the blastopore ; the mesoderm then spreads out to form a ventral
sheet which extends by growth on either side of the archenteron. Soon, how-
ever, its cells become scattered in the cleavage-cavity without forming a second-
ary coelom. Schmidt (Nos. XX. and XXL), who has confined his attention to
Pulmonates, finds no support for Erlanger's views in the origin of the meso-
derm of these forms. An investigation on this point in some of the primitive
Prosobranchia is very desirable. — Ed.]
THE K1SE OF THE LABVA, ETC. 123
has been assumed or conjectured in connection with other forms (Annelida,
Echinodermata) and specially for the Mollusca (cf. Gyclas, p. 29). It must be
regarded as a striking fact that even those zoologists who, like Erlanger,
are very decided as to the derivation of the whole mesoderm from the meso-
derm-bands, allow that some of the elements of the connective tissue arise
from the ectoderm. For example, the so-called "nuchal" cells on the pos-
terior edge of the velum on the " neck," i.e., an accumulation of specially
large ectodermal cells, pass inward so as to become distributed in the con-
nective tissue. Although of different appearance from the other elements of
the connective tissue, they appear to belong to the latter.*
4. The Rise of the Larva and its Relation to the Adult Form.
The variations which we have found in the development of the
germ-layers among the Gastropoda naturally lead us to expect varia-
tions in the external form of the embryo. In the development of the
latter, an important part is played by the smaller or larger amount
of yolk contained in the egg. Besides this, however, adaptation to
the manner of life of the various forms has to be considered, for the
greater number of Gastropod larvae swim about freely for a long-
time before assuming the adult form. Now although the larvae, in
essential points, can be traced back to a fundamental form, the
differentiations found in the vai-ious divisions are somewhat far-
reaching, so that we are obliged to consider the different larval forms
apart. We shall first, however, describe the development of a few
specially characteristic forms so as to give the reader a general
idea of the subject and to make possible a comparison with other
divisions of the Mollusca.
The development of the larval form of Patella has been described
in detail by Patten (No. 83), and since this Prosobranch, which
belongs to one of the most lowly groups, apparently most nearly
attains the typical larval form, its ontogeny will occupy us first.
Unfortunately the development of this form has only been followed
by Patten up to a stage at which the larva is still far removed from
the shape of the adult.
The ontogeny of Patella shows primitive conditions in so far as
the egg-envelope is thrown off very early, even while cleavage is still
* [The above somewhat conflicting accounts of the rise of the mesoderm,
taken in connection with the more recent observations of Conklin (No. IV.),
Heymons (No. XII.), and Wierzejski (No. XXVII.), seem to render it highly
probable that the middle germ-layer has, in all Gastropoda, as has been
suggested for the Lamellibranchia, a double origin : (1) from primitive
mesoderm-cells giving origin to the lateral mesoderm-bands ; and (2) from
the ectoderm at a later stage as paired differentiations nearer the anterior
end of the body. — En.]
124
GASTBOPODA.
going on
Since cilia appear as early as the blastula-stage (Fig. 49),
the embryo is very soon able to move about freely and thus becomes
a larva. In this way, Patella resembles a Lamellibranch, but such
early locomotion is not common among the Gastropods, most of the
stage.
larvae hatching at a much latei
The ingrowth of entoderm
Figs. 49 and 50. — Embryos of Patella at the blastula-stage and at the commencement
and completion of gastrulation (after Patten), bl, blastopore ; em, mesentomere ;
ent, entoderm; mes, mesoderm; sd, sbell-gland; w, ciliated ring.
and the differentiation of the mesoderm take place, as already de-
scribed (pp. 114 and 121), from the thickened vegetative pole of the
blastula (Figs. 49 and 50). The blastopore lies at the vegetative
pole which at the same time corresponds to the posterior end of the
larva. The principal axis of the larva, at this stage, passes through
THE RISE OP THE LARVA, ETC.
125
the middle of the blastopore and the opposite pole at which later the
apical plate develops. Through the appearance of the mesoderm,
the larva becomes bilaterally symmetrical. The blastopore soon
changes its position, shifting forward on the ventral surface, as a
consequence of the active growth of the dorsal surface. The rudi-
ment of the velum which was indicated at the blastula-stage has now
become more distinct (Figs. 49 and oO). In later stages, the dis-
placement of the blastopore becomes much more striking, and recalls
the condition already described in connection wTith Dentalium (Figs.
34 and 36, p. 91). The blastopore, during this process, changes
from its round form and becomes slit-like (Fig. 51 B). At its
Fig. 51. — Trochophore larvae of Patella at two different stages (after Patten). Iu .1,
the two lateral pedal swellings can be seen near the circular blastopore. In B, the
blastopore appears lengthened. Near it can be recognised the rudiments of the two
mesoderm-bands, and behind it the anal ciliated tuft.
posterior end, two cells are distinguished by their special size. They
soon become covered with cilia (Figs. 51 and 52), and may well be
compared to the anal cells of other Gastropods which will be described
later (p. 142). The slit narrows and closes in from behind forward.
The anterior part of the blastopore remains in the form of a round
pit in the position of the future mouth ; later, the blastopore is
carried inwards by a depression of the ectoderm, the stomodaeum,
which occurs at this point. This depression represents the rudiment
of the oesophagus (Fig. 50 B), the blastopore persisting as the opening
betwreen the stomach and oesophagus. Out of this solid mass of
cells, which still represents the entoderm, the enteron forms later
126
GASTKOPODA.
~ nua.
through a rearrangement of the cells which also increase greatly in
number (Fig. 52). From the posterior end, where the mesoderm-
cells lie, two very regular mesoderm-bands grow out (Fig. 52). The
shell-gland appears dorsally before this stage as a depression formed
of columnar ectoderm-cells ; over this gland, the shell-integument is
secreted later.
Patten asserts that the foot arises at a very early stage in a
remarkable manner. It is said to be produced from two prominences
which lie ventrally at the posterior end of the body (Fig. 51 A). These
flank the blastopore on
either side at a time when
the latter still is a round
aperture. As soon as it is
displaced anteriorly, they
shift together and unite to
form the foot, the double
origin of which can be
recognised even in later
stages through the presence
of a median groove.
Up to this stage, the
pre-oral region was speci-
ally large and bell-shaped
(Fig. 51). It is Separated
from the posterior section
by the pre-oral ciliated
ring, which is composed
of three rows of cells, the
middle row being provided with the strongest cilia (Fig. 52). A tuft
of long cilia appears on the apical plate, and near it lie two promi-
nences bearing stiff cilia (Fig. 51 B). These would recall the cephalic
tentacles of the Annelida did not each of them consist of a single cell.
As development advances, the pre-oral part flattens out considerably,
and the apical plate, which has already appeared as a median
thickening (Fig. 52, s), now takes up a considerable part of the pre-
oral section (Fig. 53, sp). At the posterior end of the larva also, a
tuft of long cilia can be seen ; these belong to the anal cells above-
mentioned. The shell-gland which was previously invaginated has
now flattened out, and the dorsal surface even appears convex. The
epithelium, which was formerly very thick in this region, now consists
merely of flattened cells (Fig. 53). The shell itself has become cup-
Fig. 52. — Horizontal section of an older larva
of Patella (after Patten). a, ciliated anal
cells ; md, enteron ; mes, mesoderm ; s, apical
plate ; w, ciliated ring.
THE KISE OF THE LARVA, ETC.
127
-i-
shaped. The somewhat swollen edge which is seen bordering the shell
represents the margin of the mantle, the mantle itself being covered
by the thin horny shell. The enteron has considerably widened and
is now sac-like and, connected with it posteriorly, a pointed appendage
can be seen ; this unites later with the ectoderm to form the aims.
In the stomodaeum, which has now enlarged, an outgrowth (/•) is
visible ; this is the rudiment of the radular sac which was found to
appear in an exactly
similar way in the
Amphineura and the
Scaphopoda.
On each side of the
mouth, right and left,
a depression appears
even at an earlier
stage ; this deepens to
form a vesicle, which
finally becomes sepa-
rated from the ecto-
derm. The two vesicles
thus formed are the
otocysts. They lie at
the base of the foot,
which is commencing
to develop into a large
prominence and in
which there is a rich
accumulation of meso-
derm-cells. The meso-
derm has lost its regular arrangement, single cells becoming detached
from the mesoderm-bands, and being distributed in the primary
body-cavity ; these no doubt represent the rudiment of the covering
of the ectodermal and entodermal organs already formed. Certain
of these cells elongate and give rise to muscle-fibres, a number of
which become attached to a point on the dorsal surface, where they
finally become firmly connected with the shell, and yield the retractor
muscle by means of which the larval body can be withdrawn into
the shell, as soon as the latter has attained the pi'oper size.
In the stages depicted in Figs. 51 and 52, and even in the later
condition, a median section of which is given in Fig. 53, the Patella
larva closely resembles the Trochophore stage met with in the
Fig. 53.— Median longitudinal section through the
larva of Patella in the later Trochophore stage (after
Patten), a, the ciliated (anal) cells at the posterior
end ; ./', foot ; m, mouth ; md, enteron ; mes, meso-
derm ; /•. radular sac ; s, shell ; sp, apical plate.
128 GASTROPODA.
Lamellibranchs (cf. Figs. 15 and 18, pp. 31 and 36). This re-
semblance is not only an external one, but extends to the inner
structure also. There is thus a Trochophore stage in the Gastropods
also (Kay Lankester, No. 63) ; it is not, indeed, usually developed
in so typical a way as in Patella, but shows certain modifications.
These modifications are either definite characteristics of the Gastropod
larva or are transformations undergone by the primitive larval form
as a consequence of altered conditions of life, especially by the
presence of a greater abundance of yolk causing an abbreviation or
the suppression of the larval stage and many modifications of the
processes of development.
Besides the outward resemblance to other Molluscan larvae
(Lamellibranchia, Scaphopoda, Amphineura) which is at once evident,
we have the inner oi"ganisation correspondingly developed. We have
already mentioned the apical plate and the pre-oral ciliated ring (Figs.
52 and 53), but we have to add to these the post-oral ciliated ring
which has been demonstrated in the Gastropod larvae, e.g., in Crepidiila,
Fulgur, Fasciolaria and other Prosobranchia, as well as in Heteropoda,
Opisthobranchia and Pteropoda (Gegenbaur, Krohn, Fol, Brooks,
McMurrich, etc.). It consists of a row of cilia which lie immedi-
ately behind the mouth and run parallel with the pre-oral ciliated
ring (Fig. 54, pu, p. 130). Between this and the pre-oral ring there
are also delicate cilia which correspond to the so-called ad-oral ciliated
zone of the Lamellibranch larva. The whole apparatus, in any case,
serves, as in the Lamellibranchs, for forwarding particles of food to
the mouth, while the pre-oral ring, as the velum proper, is chiefly
of locomotory significance. The ciliated tuft at the cephalic pole
completes the resemblance to the Trochophore of other Molluscs (Fig.
3, p. 6, and Fig. 36, p. 91) and the Annelida (Vol. i., Fig. 118, p.
265). In the pre-oral section, in the region of the apical plate, eye-
spots may occur. The post-oral otocysts lying at the sides of the
mouth have already been mentioned.
The alimentary canal, like the other organs, shows the same
structure as in other Trochophore larvae. It is composed of the
entodermal mid-gut, the enteron, and of an ectodermal fore-gut, the
stomodaeum, and perhaps also of an ectodermal hind-gut, the procto-
daeum (?) ; at a later stage, the radular sac, that special character of
the Gastropods which distinguishes them from the Lamellibranchs,
appears in the stomodaeum (Fig. 53, r).
Among the organs found in the Gastropod larva, one is of special
significance when comparison is made with the Annelidan Trocho-
THE RISE OF THE LARVA, ETC. 129
phore, viz., the paired primitive (larval or head-) kidney. This organ,
as already noted, is conspicuous in the larval Lamellibranchs and in
the Annelida (c/. p. 39 and Vol. i., p. 267). It has not, indeed, been
discovered in Patella, but we may reasonably expect that it will be
found in this form which in most other points is so primitive,
especially as it is found in other Gastropods of a less simple type of
development, such as the fresh-water Prosobranchia (Bythinia, Pahi-
diita, p. 136) and the Pulmonata (p. 178). A tubular primitive
kidney has recently been described as occurring in the larva of an
unidentified marine Gastropod (v. Erlanger, No. 28). The
primitive kidneys in their original form appear as tubular structures,
the relation of which to the primary body-cavity is probably the
same as in the Lamellibranchs, and these organs open outwards on
the ventral side of the body behind the velum. These primitive
excretory tubes are either quite short (Paludina, Fig. 59 B, un, p. 139)
or else longer, as in Planorbis, in which case each kidney consists
of a Y-shaped tube (Fig. 78, un, p. 177).
Besides the primitive tubular kidney, various groups of ectoderm-cells have
been claimed as primitive excretory oi-gans. Bobretzky thus interpreted two
rounded cell-growths which appear near the rudiment of the foot. Similar
organs have been found by McMurrich in Fulgur (No. 70). Sarasin de-
scribes, in Bythinia, ectoderm-cells of excretory nature which are connected
with the velum. [In Crepidula, Conklin (No. IV.) finds paired groups of ecto-
dermal cells, situated just behind the velum, which are eventually cast off ; he
regards them as excretory.] These ectodermal cells frequently contain concre-
tions which are said to be extruded, a fact which has led authors to attribute
an excretory function to them. They are very soon to be recognised owing to
their granular contents ; in Neritina, such granular cells, which later give rise
to velar cells, may be clearly distinguished even during cleavage among the mic-
romeres (Blochmann, No. 7). Two rows of granular cells which lie along the edge
of the velum have been described in Onchidium by Joyeux-Laffuie (No. 51).*
*[Heymons describes, in Umbrella, the presence of paired groups of ecto-
dermal excretory cells, situated near the anus ; of these, the right group alone
attains functional development and sinks under the surface of the ectoderm.
He regards these as homologous with the similar cells situated near the velum
in the Prosobranchia. Conklin (No. IV.), however, thinks that they are
only analogous, since they arise from totally distinct blastomeres ; the anterior
ectodermal excretory cells are found in three of the great Gastropodan orders.
Mazzarelli (No. XV.), who has studied the ectodermal or anal kidney of
Aplysia, considers that it is not to be regarded as a larval organ; he main-
tains that it does not disappear, but represents the rudiment of the definitive
kidney. The true internal primitive kidney is so far known to occur only in
the Pulmonata and in two fresh-water Prosobranchia and possibly in one
marine Gastropod, concerning which Erlanger is unable to inform us whether
it was an Opisthobranch or a Prosobranch. Thus it will be seen that this
supposed primitive organ is found to be most highly developed in those most
specialised forms, the Pulmonata, and that it is only elsewhere known to
occur in two Prosobranchs. A further search for this organ in some of the
more primitive marine Prosobranchia is much needed. — Ed.]
K
130
GASTROPODA.
vr...
It is only in comparatively few Gastropods that the Trochophore is
developed in such a pronounced manner as in Patella, this being no
doubt due to the fact that, in most Gastropods, a great part of the
development of the embryo takes place under the protection of the
eo-cshell or in the egg-capsule. The Trochophore stage is neverthe-
less to be found in all Gastropods, although it is more distinct in some
than in others. In these latter, as a rule, the larva attains free life
at a stage in which its shape has already undergone several modifica-
tions The later ontogenetic stages of Patella are not known, but
the larva, at the stage in which it is provided with a foot and a fairly
developed shell, still resembles the Trochophore, so that we may
assume that it does not undergo any further changes except those
which are determined
by its transformation
into the adult. This
also seems to be the
case in Fissurella as
far as its develop-
ment is known
(Boutan, No. 12).
In this Gastropod,
the velum broadens
somewhat and as-
sumes a bilateral
form. This was also
already described in
the Lamellibranch
larva, and Fissurella
does actually show a
certain resemblance to the later stages of these forms (Fig. 17, p. 36),
if we leave out of consideration the shell which in the one case is
single and in the other bivalve.
In the two last-named primitive Gastropods, the velum does not
differ essentially from the Lamellibranch velum, but in most other
forms its shape becomes modified in a manner specially characteristic
of the Gastropoda. The bilateral development of the velum which
is already indicated in Fissurella is, in those Prosobranchs the eggs
of which are rich in yolk (Neritina, Vermetvs, Fulgar), evident when
the velum first appears as a rudiment, This organ appears in the
embryo at first in the form of two specially marked rows of cells
(Neritrruc) or two curved ridges which unite only later to form the
v.
Fig 5i-Velige?- larva with four-lobed velum (after
McMukrich). f foot ; m, oral aperture ; f-PjJ^gj
p , post-oral ciliated ring ; s, shell ; t, tentacle wren
eye at its base ; v, velum.
THE VELIGER LARVA.
131
velum, the dorsal union of the two ridges often taking place very
late. In its later development, in the Prosobranchia and especially in
the Opisthobranchia, Heteropoda, and Pteropoda, the velum by its
great lateral growth, assumes a bilobed form (Fig. 55 A-C). It
becomes at the same time very large and is a most efficient locomotory
organ. It is beset with large, strong cilia, which may be replaced by
much smaller cilia at the junction of the two wing-like lobes, the bila-
7 \W' \ \ r-'-"- ^■■■'■■■r\
PlG. 55. — A, embryo, B and C, Veliger larvae of Vermetus at different stages (after
La.caze-Duthikrs). A, dorsal aspect; B, ventral aspect; C, lateral aspect, a,
eyes ; c, rudiments of the cerebral ganglia ; /, foot ; m, mouth ; ot, otocyst ; ,
operculum ; s, shell, t, tentacle ; v, velum.
teral character thus becoming still more apparent (Fig. 72, p. 162). The
larval stage which is provided with this very characteristic locomotory
apparatus has been called the Veliger stage (Kay Lankester). The
great size which may be attained by the velum can be seen from
Fig. 54, which represents the Veliger larva of a Prosobranch (species
1 32 GASTROPODA.
unknown). Each of the velar lobes is drawn out longitudinally so
that the whole velum appears to consist of four lobes. In Atlanta,
the velum is very large and here each of the lateral parts splits up
into three, the velum thus consisting of six lobes (Fig. 67, p. 155).
In other respects the development of the body has advanced consider-
ably at the Veliger stage. The shell, which at first is cup- or cap-shaped,
increases in size through the addition of new layers, this fact being
indicated, as in Dentalium and the Lamellibranchs, by the appearance
of lines of growth. But as the addition of new material takes place
in an irregular manner, i.e., as the new layers of shell are not all of
equal width and, further, follow the curvature of the visceral sac, the
shell soon loses its symmetrical shape and begins to coil (Fig. 55).
The visceral sac is separated by the projecting lip-like edge of the
mantle from the rest of the body, especially from the head and trunk.
A slit-like depression usually appears on the right side in front of the
edge of the mantle ; this depression extends posteriorly so that the
mantle now covers a cavity, the mantle- (or pallial) cavity, in which
the gills arise later as outgrowths of the body-wall. The intestine
opens into this cavity, the anus having arisen as an ectodermal
depression primarily situated somewhat ventrally at the posterior end
of the body. At first this lies in the median plane, but is usually
displaced to the right side later, shifting at the same time forward,
and somewhat dorsally. This displacement is a result of the fixed
and rigid nature of the shell covering a large part of the body (cf.
p. US).
The rudiment of the foot appears early and may attain large pro-
portions in the Veliger larva. In Vermetus, it is paired at least
anteriorly (Fig. 55 B and C). In this larva the foot, however, is
more complicated than Fig. 55 would lead us to believe. The double
character of its rudiment is noteworthy as a peculiarity which recurs
in other Gastropods (Patella, Fig. 51 A ; Limnaea, Bay Lankester,
No 63 ; Sucdnea, F. Schmidt, No. 109) in very early stages. In
Succinea, the foot arises in the form of two distinct prominences
separated by a broad furrow ; these outgrowths afterwards approach
each other and fuse to form the median foot, a process similar to that
described for Patella (p. 126).
On the postero-dorsal surface of the foot, a plate composed of the
same substance as the shell is secreted (Fig. 55 0, op). This is the
operculum. The otocysts lie in close contact with the foot (B, at).
In the young stages of the Veliger larva two prominences appear
on the velar area ; these soon extend and lengthen and can be recognised
THE VELIGER LARVA. 133
us the tentacles (Fig. 55, /). At their bases, the eyes (a) arise.
Both the tentacles and the eyes are, by their origin, indisputably
proved to belong t<> the primary cephalic section, and it is of special
interest that the tentacles occupy the same position as the cephalic
tentacles of the Annelida and the Annelidan larvae (Vol. i., Figs. 120
B, p. 269, and 121, p. 270).
The velum may still persist after the foot has attained a consider-
able size and when the development of the other organs also is far
advanced, but it gradually diminishes in size and finally degenerates,
the larva thereby passing over to the adult condition which, indeed,
had already been nearly approached. Two small rounded ciliated lobes
may pei'sist near the mouth as the remains of the velum, as was
observed by Kay Lankester in Limnaea (No. 63), and Joyeux-
Laffuie in Onchidium (No. 51). These are said to give rise to the
sub-tentacular lobes or lip-tentacles ; these two structures would thus
have an origin similar to that which we felt inclined to assume for
the oral lobes of the Lamellibranchs (p. 45).
The perfectly developed Veliger larva is found almost exclusively
among the marine Gastropoda, the young of which swim about freely
for a long time. Among fresh-water Gastropods, Neritina passes
through a stage with a well-developed bilobed velum resembling that
depicted in Fig. 55 ( Vermetus), but the Veliger larva does not lead a
free life, but passes through this stage within the egg-capsule. When
the embryo leaves the capsule it shows the adult form (Claparede,
No. 23). Neritina is one of those fresh-water forms which can also
live in salt water. This fact, and the presence of the well-developed
I religer stage, suggest that it has only recently adopted a fresh-water
existence. In other fresh- water Prosobranchs, as well as in aquatic
and terrestrial Puhnonates, the Veliger stage is much reduced.
Onchidium, however, among the Pulmonates, in this respect resembles
Neritina.
Onchidium, a Pulmonate living between tide-marks, not only passes
through a TrocJiophore stage but, while still within the egg-shell,
becomes a Veliger larva with coiled shell and a large bilobed velum.
In the course of further development, the velum degenerates, only
two rounded lobes which lie laterally to and somewhat in front of the
mouth being retained as the lip-tentacles. The embryo, on leaving
the eug-shell has, on the whole, the same shape as the parent
(Joyeux-Laffuie, No. 15). The condition we have just described
would be very remarkable in a Pulmonate, did not the organisation and
the manner of life of this form give some cause for the assumption
^34 GASTROPODA.
that it may have been derived from a marine ancestor (possibly an
Opisthobranch). Onch Mum lives in the littoral zone, within the reach
of the tides, hidden in rocky fissures, where it lays its gelatinous
e-a-masses. These are washed by the sea water, and Joyeux-
lTffuie was able to develop them by keeping them damp and
immersing them from time to time in sea water. The eggs therefore
develop under conditions not very different from those of marine
Gastropods.
Although, as a rule, the Veliyer stage is much reduced in fresh-
water and terrestrial Gastropods, the Trochophore form is still more
or less distinctly developed in them. In the Pulmonates, the
Trochophore stage is present but is not very conspicuous (p. 177);
in Paludina, however, it is unmistakable, although this Gastropod
is viviparous (Fig. 56). Paludina, in many other respects besides
the retention of the Trochophore stage, is an archaic form and, as its
ontogeny has been so carefully studied, we shall give a special
account of its development. The principal sources of our knowledge
concerning the ontogeny of Paludina are the works of Leydig (No.
68), Ray Lankester (No. 64), Butschli (No. 18) and v. Erlanger
(No. 27), and we have also observations made by Rabl (No. 92) and
Blochm'ann (No. 8). Erlanger's account is the most recent and
the most complete in every respect.
The Development of Paludina. The fertilised egg of Paluduia
vivipara develops into an almost spherical blastula which becomes
somewhat flattened later and contains a distinct cleavage-cavity.
The flattening takes place in connection with gastrulation, the
cleavage-cavity during this latter process being almost completely
obliterated by the development of the archenterou, so that a stage
is here brought about similar to that which occurs in other Gastro-
pods, especially in Firoloida (Fig. 44 B, p. 114). The gastrula,
which at first is almost kidney-shaped, with a wide blastopore,
expands by growth and becomes bell-shaped in Firoloida (Fig. 44 C).
The blastopore narrows to a slit.
The formation of the mesoderm has already been described. On
this point, we follow the older statements of Butschli, according to
which the mesoderm is present in the form of two mesoderm-bands
which, during the gastrula-stage, consist of few cells but increase
later (Fig. 56 A), i.e., show the same condition as in other Gastropods
(cf. p. 121). The greater part of these bands soon undergoes dis-
integration, breaking up into separate cells which become irregularly
distributed in the cleavage-cavity.
THE DKVKLOl'MKNT OF PALUDINA.
135
Meanwhile, by the development of two rows of large ciliated
ectoderm-cells, placed transversely to the gastrula-axis, the Trocho-
phore stage is reached. The pre-oral ciliated ring thus borders
the cephalic area, which has become larger by the increase in
number of the cells (Fig. 56 A). The blastopore marks the posterior
end of the embryo, but in consequence of somewhat stronger growth
and the consequent bulging of the ventral surface it is shifted slightly
dorsally. The blastopore is said to be retained in Paludina and to
pass over into the anus (Butschli, v. Eklanger). It has, however,
been asserted that the blastopore closes (Rabl) and that the mouth
and the anus are only indirectly related to the primitive mouth, as
we shall describe later (c/. p. 141).* A large, somewhat sunken
a
V.
•nw*.-
v.
- - ma> .
■A.--
--T1U&.
FlG. 56. — .1 frontal and 1> sagittal section of two embryos of Paludina of different
ages (after Tonniges). m, region where the mouth develops at a later stage ; mes,
mesoderm -bands (in A) and scattered mesoderm-cells (in B) ; sd, shell-gland; nd,
archenteron ; r, velum.
area, which lies dorsally in front of the blastopore and consists of
columnar ectoderm-cells (Fig. 56 B, cd), represents the shell-gland,
above which the chitinous shell soon appears. An ectodermal de-
pression (in) which appears on the ventral side behind the ciliated
ring, ami which becomes connected later with the archenteron, yields
the stomodaeum. At this stage, the anterior part of the embryo has
lost its former bell-shape and has become more flattened (Fig. 56 B).
The mesoderm has lost its regular arrangement and has become for
* [Tonniges (No. XXV.), the most recent investigator of the development of
i'uludina, finds that the oval blastopore closes from before backward, and
that it does not give rise to the anus, which, as a secondary formation, appears
at the point where the blastopore closes. — Ed.]
136 GASTROPODA.
the greater part distributed in the form of isolated spindle-shaped
cells in the primary body-cavity. Its further development will be
described later, but we must here refer to one of the organs formed
from the mesoderm, the primitive kidney, since this is essentially a
larval organ.
Each of the primitive kidneys arises from a compact mass of
mesoderm-cells, two such masses lying at the sides of the embryo
behind the velum. A lumen now appears in the mass, which, by
lengthening somewhat, becomes a short tube and, coming into con-
tact with the ectoderm, fuses with the latter and thus opens externally
not far behind the velum. The ectoderm sinks in somewhat at this
point later ; in Bytliinia, this ectodermal invagination is even very
deep and forms the longer, distal part of the primitive kidney (v.
Erlanger). The inner surface of the tube becomes covered with
cilia especially at the blind end. The primitive kidney remains short
in Paludina, but, in the Pulmonata, appears as a long bent tube.
This is said to possess an internal aperture, that is to say, it com-
municates with the (primary) body-cavity (p. 179). v. Erlanger
wras unable to convince himself of the presence of such an aperture in
Paludina and Bythinia * and, taking into consideration the condition
of the primitive kidneys in the Annelida, we may conclude that it is
wanting in these forms and that the two renal tubes end blindly.
This is certainly the case in the earlier stages. At the inner end of
each kidney, there is a bundle of spindle cells which in all cases
extend to the ectoderm, and serve for suspending the renal tube.
This latter attains its highest degree of development at the somewhat
advanced stage shown in Fig. 99, and degenerates later (Butschli,
v. Erlanger).
The Trochophore form of the embryo is now speciall}r modified by
the development of the foot on the ventral surface as a massive pro-
minence (Figs. 56 B and 57,,/'). The appearance and rapid increase
in size of this organ leads to a considerable displacement of the other
parts of the body (Figs. 56 B and 58). The pre-oral part of the body
becomes still more flattened out. The mouth shifts to the anterior
end and the velum finally appears displaced to a dorsal position (Fig.
58). The oral aperture and the anus lie at the two opposite ends of
* [v. Erlanger (No. 71), however, describes an internal aperture in
Pulmonates. Meissenheimer (Nos. XVII. and XVIII.) has made a most
careful investigation of this point in Limax and is firm in his belief that
there is no internal opening in that Pulmonate. He derives the entire
organ from the ectoderm. — Ed.]
THE DEVELOPMENT OF PALUDINA.
137
the body. The shell-gland now becomes modified by the invagination
of its greatly thickened epithelium and by the appearance within the
invagination of the brown "chiton-plug" described by Butschli
(Fig. 57). During the further growth of the embryo, the gland
becomes flattened out and its cells lose their long columnar character
row.
Pigs. 57 and 58. —Sagittal section of two embryos of Palvdina oivipara (after T6n-
NIOES). ", anus; ent, entoderm; f, rudiment of foot; I, rudiment of liver; m,
mouth ; md, enteron ; mes, mesoderm-cells ; mf, lirst indications of the mantle-fold ;
s, shell-gland ; sf, shell-groove ; r, velum.
and the epithelium finally becomes very thin (Fig. 58). At this
stage, lying above the shell-gland which is now slightly depressed,
there can be seen not only the remains of the chitinous plug but the
shell-integument itself (■<). The shell now extends rapidly over the
138 GASTROPODA.
dorsal surface by the growth of its free edge which is still in close
contact with a thickened layer of ectoderm, the cells of this
thickening being concerned in the secretion of the shell. Beyond
this thickening, the mantle-fold (Fig. 58, nif), as a slight upgrowth
of the ectoderm, is situated dorsally to the anus. When the latter is
displaced forward by the more rapid growth of the posterior dorsal
part of the body (Fig. 59 .4), the mantle either grows out further or
else the surface of the body behind the mantle and in front of the
anus sinks in somewhat ; the depression which is thus formed is the
rudiment of the mantle-(pallial) or branchial cavity (Fig. 59 A, nth).
The anal aperture now comes to lie in this depression.
Turning to the internal organs, we find that the fusion of the
stomodaeum with the enteron has now taken place (Fig. 58). The
rudiment of the liver appears ventrally as a sac-like outgrowth
of the enteron, and the radular sac arises from the stomodaeum.
As the mesodermal structures (the pericardium, the heart and the
kidneys, Fig. 59) become differentiated, those on the right side
attain a greater size than those on the left, so that a marked asym-
metry is already evident in these internal organs. The rectum, which
formerly ran directly backward, now comes to lie at right angles to
the longitudinal axis in consequence of the displacement of the anus
described above and, later, runs obliquely to the right side.
The inner asymmetry precedes the outer, and has therefore been
used as an explanation of the asymmetrical structure of the body
(Bytliinia, P. Sarasin, No. 101). When we spoke above of a dis-
placement of the anus the expression used was not strictly accurate,
since the distance between the mouth and the anus remains almost
the same. Marked growth, on the contrary, takes place first in the
dorsal surface and later especially in the left posterior part of the body.
Although the area lying between the mouth and the anus does not
grow appreciably, considerable increase in size occurs in the posterior
region (Fig. 59 A-C), and it results that the parts that have not grown
now seem to belong more to the anterior portion of the body which
as a whole is now much larger. Butschli has paid special attention
to these processes in Paludina (No. 19). The left posterior part of
the body, in consequence of the processes of growth just described, is
much swollen and this leads to the formation of the visceral sac
directed backward to the left and to the (apparent) shifting forward
to the right of the anus and the parts surrounding it. The swelling
of the posterior dorsal parts of the body to form the visceral sac is
determined by the advancing growth of the inner organs. The
THK DKVELOPMKNT OF PALUDINA.
139
subject of the asymmetrical shape of the body will be alluded to
further on (p. 143).
S s ™h
ma jnr
Fig. 59. — A-C, embryos of Paludina oivipara of different ages (after v. Erlanger).
<*, anus ; an, eye \f, foot ; h, heart ; /, liver ; lp, left pericardial sac ; m, mouth : ma,
enteron ; mj\ mantle-fold ; nth, mantle-cavity ; mr, edge of the mantle ; na, efferent
renal duct ; ot, otocyst ; p, pericardium ; s, shell ; .<•■/', shell-groove ; sy, edge of shell ;
I, tentacle ; wn, primitive kidney ; c, velum,
It has already been mentioned that the anal aperture lies in the
mantle-cavity. This latter has deepened during the processes just
140 GASTROPODA.
described through the rising up and growth of the margin of the
mantle, but it also becomes affected by the asymmetrical develop-
ment of the embryo. It is soon evident that the part of the cavity
lying on the right side is much deeper than that lying on the
left, and the cavity shortly becomes confined almost entirely to the
right side in consequence of the twisting of the embryo. On
this side there opens into it not only the rectum, but the efferent
ducts of the now developed definitive kidney and of the genital
organs. At a later stage, the mantle-cavity extends dorsally and
thence over to the left side. Above the mantle lies the shell which
passes from its earlier flat shape to a more arched form, till it becomes
a somewhat deep cup (Fig. 59 A and B), and, finally, in consequence
of its one-sided growth, becomes coiled (ef. p. 147).
While the above processes have been going on, the anterior part of
the body also has undergone essential alteration. The velum has
degenerated more and more, while the foot has greatly increased in
size (Fig. 59 A-C). At its base, the otocysts (of) have appeared as
ectodermal depressions which soon became cut off as closed vesicles.
In the posterior dorsal part of the foot, the operculum is secreted in
a manner similar to the secretion of the shell (Fig. 99, o/>, and Fig.
92, op).
The tentacles arise on the velar area as two very large swellings
which soon increase in height and thus become conical (Fig. 59 A-C,
t). At their bases the eyes appear. At the stage depicted in Fig.
59, both these organs can be recognised as belonging to the
velar area, since the ciliated ring is still present as a narrow band.
In these later stages, when, in keeping with the shape of the body,
the velum has become almost bilobed, it may be compared with the
sail of the Veliger larva of the marine Gastropods which, however, is
much more distinctly bilobed.
The further development of the embryo is chiefly determined by
the continued growth of the visceral sac as a result of the perfecting
of the inner organs, and by the increase in size of the foot and of the
tentacles. This may best be seen by comparing Fig 59 with Figs. 99
and 100.
Before closing this section we must deal with one or two other
morphological points which could not earlier receive the consideration
they deserve. The first of these concerns the shape and transforma-
tion of the blastopore. In its simplest form, the blastopore has been
described as a rounded aperture appearing at the vegetative pole ;
this aperture, without undergoing essential c'hange of form, may pass,
TRANSFORMATION OF THE BLASTOPORE. 141
by gradually narrowing, into the mouth. An ectodermal depression
does, indeed, regularly accompany this process, pushing the actual
blastopore some distance inward. Such a direct passage of the
blastopore into the mouth has been claimed by Bobretzky for Fusus
and by Fol for the Pteropoda and Heteropoda. The narrowing of
the blastopore may, further, lead to its direct closure, but even in
such cases, the stomodaeum forms at the same spot, as, for instance,
in Nassa and Neritina (Bobretzky and Blochmann). The point
at which the blastopore closes and where the adult mouth eventually
forms, no longer corresponds to the vegetative pole, i.e., to the end
of the embryo which is turned away from the animal pole, but, in
consequence of the growth of the postero-dorsal region, has shifted
somewhat towards the animal pole and is found behind the velum.
This last condition of the blastopore is that which is by far the most
frequent among the Gastropoda. Here also the blastopore is at first
round and may have a considerable diameter, but it soon becomes
narrow and slit-like (Planorbis, Patella, Palwlina and many other
< Jastropods). The slit-like blastopore closes from behind forward,
and its anterior end either passes direct into the mouth, as in Plan-
orbis, Linninea, and Patella (according to Eabl, Eay Lankester,
Wolfson, Patten) or closes completely, in which case, at the last
point to close, an ectodermal depression forms which yields the
stomodaeum. This latter is the case in Aplysia, Bythinia, and
Grepidula (Blochmann, Sarasin, v. Erlanger, Conklin). The
formation of the definitive mouth is always connected with an
invagination of the ectoderm.
The slit-like blastopore, if regarded as open from its posterior to
its anterior end, seems to occupy the whole length of the later ventral
surface. Its posterior end no doubt still corresponds approximately
to the former vegetative pole, its anterior end lying immediately be-
hind the velum. Now while, in the majority of cases as yet known,
the blastopore closes from behind forward, in Paludina, as already
described, the posterior part of it is said to persist and to yield the
anus in the same way as the anterior part in the above cited cases
yielded the mouth. If this is actually the case, it can only be
explained by means of the view adopted by Butschli, according
to which both the mouth and anus arise by the differentiation of the
blastopore. Bctschli found an indication of this in Ray Lan-
kester's observations on Limnaea, in which form, the slit-like
blastopore, the anterior end of which becomes the mouth, extends as
far as to the anal region. Since that observation was made, other
142 GASTROPODA.
cases have become known of certain relations existing between the
amis and the blastopore, v. Erlanger, for instance, described the
blastopore of Bytkinia as a slit, the posterior end of which lies at the
spot where the anus forms later (Fig. 96 B, p. 210), and even in
Pahuliva itself it appears indisputable that the slit-like blastopore
extends almost to the velum, i.e., to the spot which corresponds to
the mouth that forms at a later stage. Further support for this view
is found in the condition of some Opisthobranchs (Don*, Aplysia,
according to Langerhans and Blochmann), in which the anal cells
are found exactly at the posterior end of the blastopore which here
also is slit-like. It should be mentioned further of those two anal
cells that, in various Gastropods, they mark at an early stage and in
a striking manner the position of the anus (pp. 154 and 160). They
coincide in position with the two cells which, in Patella, appear be-
hind the blastopore (p. 125). The anterior end of the blastopore in
the forms just named, also, becomes the mouth, so that the relations
of the blastopore to the mouth and to the anus in these forms are
specially distinct and the apparently divergent condition of Paludina
is thus explained.
Greater attention has been paid to the form and the transformations of the
blastopore in the Gastropoda than in other animals, and the subject there-
fore has received special consideration from us. It was not our intention to
give an exhaustive account of the observations made in connection with it
chiefly because these are to some extent unreliable. We have therefore
selected only such statements as seem to some degree well-founded, though
even these need more careful examination. It seems, however, to be proved
by these observations that, in the Gastropoda, there are relations between the
blastopore on the one hand and the mouth and anus on the other. We conse-
quently find, in the Mollusca, conditions similar to those previously met with
by us in the Arthropoda, in which class also, the mouth and anus are either
directly or indirectly related to the blastopore (cf. Vol. iii., p. 412). The condi-
tion of Paludina may recall the Echinoderms, in which the blastopore passes
direct into the anus (Vol. i., p. 359). The condition of the Gastropods is, how-
ever, in any case, to be| traced back to corresponding processes met with in
the formation of the Annelidan Trochophore (Vol. i., p. 265). In the latter, the
blastopore at first lies at the vegetative pole of the embryo. It then extends
and occupies the whole length of the ventral surface which, however, is not
very great. When it closes from behind forward, its anterior end passes over
into the mouth, this latter lying behind the pre-oral ciliated ring, as in the
Gastropoda. The anus, however, arises at the posterior end of the larva which
previously corresponded to the vegetative pole and thus to the position of
the blastopore. The conditions here are thus evidently very like those in the
Molluscs.
RELATING TO THE ASYMMETRY OF THE GASTROPODA. 143
These Last considerations lead us to the changes of shape undergone
by the embryos in early stages. Even before the Gastropod egg is
affected by cleavage, and while it is undergoing this process, the animal
and vegetative poles may be distinguished. The blastopore at first
corresponds to the vegetative pole, but, as it lengthens, it encroaches
upon the future ventral surface, while the animal pole appears to lie
on the dorsal surface. The part of the ectoderm that forms at the
animal pole seems to shift later to the anterior end of the embryo
around which the velum is developed. The axis which passes through
the animal and vegetative poles of the early stages does not, there-
fore, in the Gastropoda, correspond, as might be supposed, to that
passing through the apical plate and the anus of the larva, but lies
more or less at an angle to the latter. It has already been shown
that the definitive axes are laid down at an early stage in the embryo
(p. 107). The identification of these axes is by no means easy, especi-
ally as the shape of the larva undergoes a certain amount of modifi-
cation according to the quantity of yolk deposited in the egg. On
this account, Fol's statement that the shell-gland appears at the
animal pole requires further investigation. It is a striking fact,
however, that in the Cephalopoda it actually has such a position,
a fact which will be discussed later.* The shell-gland, as is well
known, lies dorsally on the embryo, whereas the pedal prominence
arises on the ventral side between the mouth and the anus. In their
most primitive condition the embryos, or larvae of the Gastropoda,
are quite symmetrical ; only later does the body become asymmetrical
through displacement of the internal and external organs.
Considerations relating to the asymmetry of the Gastropoda.
The development of the body during its ontogeny follows the
course which we are inclined to believe was taken by the Gastropoda
phylogenetically in attaining their present asymmetrical condition.
There can be no doubt that the Gastropoda are derived from symmetrical
forms, for we find the other members of the Molluscan phylum, which
had the same ancestors as the Gastropoda, symmetrically developed.
This is confirmed by ontogeny, for the symmetrical form is long retained
in the embryo although it is eventually lost in consequence of the
unequal growth of the various regions of the bod}'. It is especially
* [For a review of the facts relating to the shifting of the larval axes see
Conklin (No. IV.) and Lillie (App. to Literature on Lamellibranchia,
No. III).— Ed.]
144
GASTKOPODA.
the left side that grows more actively, and this is the reason why the
posterior parts (especially the anus and the organs surrounding it)
a.
95 .
C.
•3-
r...
-vc.
,,vc.
■a*.
--vc.
Fig. 60. — A-E, Diagrams illustrating the displacement of the pallial complex and the
manner in which the asymmetry of the Gastropod body was developed (constructed
after BUtschli and Lang). The pallial complex shifts first to the right and then for-
ward. In E, it has passed the median line, and here the mantle-cavity has sunk in
more deeply. The gills grow back and thus sink deeper into the cavity. The heart,
auricles and anterior aorta are outlined in red, the intestinal canal in blue, the nerve-
ganglia and visceral loop in black. «, anus ; ao, anterior aorta ; eg, cerebral
ganglion ; /, foot ; k, gills ; m, mouth ; n, renal aperture ; peg, pedal ganglion ; pig,
pleural ganglion; r, edge of the mantle and shell ; vc, visceral commissure.
RELATING TO THE ASYMMETRY OF THE GASTROPODA. 145
are displaced anteriorly to the right, but at the same time they
retain their original position with relation to the anterior end, because
the region lying between them and the anterior end on the right side
• lues not grow. These phenomena have been described by various
zoologists who have treated of the ontogeny of the Gastropoda (P.
Sarasin, Fol, Bobretzky, etc.).* Spengel (No. 122), also, has
made them the subject of detailed consideration in adult animals,
and more recently Butschli especially has given a careful descrip-
tion of them (No. 19). Lang has recently made a further attempt to
explain them from a phylogenetic point of view (No. 61).
Ontogenetically as well as phylogenetically, the asymmetry rests
in any case upon the greater growth of one side, usually the left,
and the consequent shifting of the left posterior part of the body
to the right and of the whole posterior region anteriorly. In this
process we start with a very simple, Chiton-like Mollusc, whose dorsal
surface with its investing shell is only slightly arched. The foot
projects only a little way beyond the visceral sac. The anus lies at
the posterior end, the paired apertures of the nephridia and the gills
lying near and symmetrically to it (Fig. 60 ^4). The mantle-cavity
also, to which these organs belong, is found at the posterior end.
The way in which the shifting forward to the right of this posterior
complex of organs (pallial complex) may be imagined to have taken
place may best be seen from the diagrams given in Fig. 60 (Butschli
and Lang). The asymmetry which is brought about by the shifting
of the pallial complex to a position near the anterior end of the body
(D) is found in the Opisthobranchia and Pulmonata ; when the
pallial complex, in shifting forward, crosses the median line (E), as in
the Prosobranchia (including the Heteropoda), the pleuro-visceral
commissures become crossed (chiastoneury, streptoneury, Fig. 60 E),
a condition not found in the two divisions mentioned above, and
indicating a specially high degree of asymmetry. f
*[It is manifestly impossible in a work of this nature to review all the
numerous theories relating to the asymmetry of the Gastropoda. The views
adopted by our authors are those of Butschli and Lang, but the reader should
consult Simroth's account of the Mollusca in Bronn's Klass. u. Ordnung. d.
Thierreichs, Bd. iii. Lief. 22 u. 23, 1896, where an excellent summary of
both the earlier and the more recent views, including those of Pelseneer and
Plate, will be found. — Ed.]
t [In Actaeon, a form which, in spite of its peculiarities, must be regarded
as most nearly allied to the Opisthobranchs, we find that pleuro-visceral
connectives exhibit a streptoneurous condition, and in certain other forms
also (I'Jiiliiic, Aplysia, etc., a streptoneurous condition is also found in the
Pulmonate genus, Chilina) an indication of this condition is to be seen. The
condition met with in these forms is thought to be a highly specialised one,
L
146 GASTROPODA.
The cause of thi* asymmetry is to be sought in the manner of life of
the Gastropoda, i.e., in the development of the foot as a massive creeping
organ and in the simultaneous development of the shelly covering of the
body. At first the visceral mass was fairly equally distributed over
the body, which was covered only by a flattish shell. These original
forms no doubt most nearly resembled the Chitones, apart from the
segmentation of the shell found in the latter. So as to give greater
freedom to the head which carried the sensory organs and the mouth,
to allow the foot to grow larger and also to make it independent of
the rest of the body, this organ became restricted to a smaller part
of the body. This led to the formation of the high visceral sac, to
which, as the part specially needing protection, the shell also became
restricted, although the head and foot might still be drawn in under
the latter, which consequently had to be of larger size than would be
necessary in a merely protective covering. The animal was thus
obliged to carry not only the high visceral dome, but a calcareous
.shell capable of accommodating the whole body. If this heavy
mass became too high, it would be in a state of unstable equilibrium
and would naturally become inclined, the best inclination being-
backward, as hindering the animal least in creeping. But since the
mantle-cavity with its important organs (the gills, the apertures of
the intestinal canal, the kidneys and the genital organs) lay at the
posterior end of the body, such a backward inclination of the visceral
mass would be so unfavourable as to be at first impossible and the
only inclination which seems possible would be to the side. This
lateral projection of the sac, however, too greatly impeded locomotion,
and in spite of the disadvantages mentioned above, the visceral dome
tended to incline backward. If we assume that the visceral dome
inclined to the left side, the great pressure from the left would tend
to squeeze the pallial complex towards the right. Herein, therefore,
lay the cause of that displacement to the right and then forward
which has been described above (Fig. 60). Ontogenetically, this pro-
cess takes the form of more active growth of the posterior part of the
body on the left side, which leads to the bulging of the visceral sac,
and the forward displacement of the anus then follows (cf. p. 138).
It would not be surprising if the pressure of the inclined visceral
for, from the study of other points in their anatomy it has long been concluded
that the Opisthobranchs and Pulmonates (i.e., the Euthyneura) are to be
derived from the Prosobranchia after the latter attained the streptoneurous
condition. If this is the case, we must regard the condition met with in the
Euthyneura as a retrogressive one and not as an arrested stage in the rotation
of the pallial complex. — Ed.]
RELATING TO THE ASYMMETRY OF THE GASTROPODA. 147
mass led, not only to the shiftings we have mentioned, but also to
the degeneration of single organs. Lang, in this way, traces back
the absence of the organs originally forming the left part of the
pallia! complex (the left gill and the left renal aperture, etc.) which
is to be noticed in various ( Gastropods («..'/., the Monotocardia among
the Prosobranchia and the Opisthobranchia) to the fact that the left
side was exposed to specially strong pressure, through which these
organs were prevented from functioning and degenerated. In other
cases (Haliotis) the right (originally the left) gill is said to be smaller
than the left (originally the right), and there is also an inequality in
the kidneys of those Gastropods (Haliotis, Patella) in which the
excretory organ is paired.*
The inclination of the visceral sac naturally led to its becoming
coiled. Lang rightly traces this to the fact that, in order to avoid
distortion, the upper side has to grow more than the lower. This
unequal growth gives rise finally to the spiral coiling of the sac, which
is followed in its shape by the shell. In those shells that are inclined
to the left, further room for extension is given on this side, especially
when the shell and visceral sac are directed backward. This unequal
growth determines the formation of the so-called dextrally twisted
shell. An original inclination to the right must be assumed for the
shell that shows the sinistral twist. In other respects the process is
the same in the two cases. The causes that lead to the inclination
to one side or the other ai*e difficult to determine, indeed, at the
present time, they are hardly known. -j-
Sonie of the sinistrally twisted Gastropods have their inner organs
arranged in the same way as the ordinary dextrally twisted forms.
In such cases we have a false coiling which, it has been assumed,
arose through the flattening of a dextrally twisted shell to such an
extent that it became coiled in one plane. In this case the spiral
might again assert itself on the side opposite to that on which the
umbilicus originally lay, and in this way a false spiral might form
on the umbilical side and a false umbilicus on the spiral side (Sim-
ROTH, v. Jhering, Lang, No. 61). An indication of such a process
*[This unequal development of the gills is very marked in Pleurotomaria,
the right (originally left) gill being much the shorter of the two ; this is the
gill which is suppressed in the Monotocardia. Curiously enough the kidneys
in some Diotocardia {e.g., Haliotis, Patella) show exactly the reverse condition
to that seen in the gills, i.e., the right (primary left) kidney is much larger
than the left (primary right) ; nevertheless, it is apparently the latter
nephridium which persists in the Monotocardia.— Ed.]
t [See footnote, p. 108, on the cleavage of the egg of sinistral Gastropods. —
Ed.]
148 GASTROPODA.
is found in the Pteropoda that have a sinistrally twisted shell, but
in other respects show the structure of dextrally twisted forms ;
these have the operculum also sinistrally twisted, whereas spiral
opercula elsewhere always have a twist opposite to that of the shell
(Pelseneer, No. 86).
[Forms with a dextral organisation in a sinistral shell, and which
are supposed to have arisen as above, have been termed ultra-dextral.
The commencement of an ultra-sinistral coiling is seen in Planorbis
context, which possesses a true sinistral organisation with a shell
which otherwise would be regarded as a flattened dextral coil. The
embryo of this Gastropod, however, possesses a well-marked sinistral
shell.]
The asymmetry characteristic of the Gastropoda may, however, be-
come more or less marked by the acquisition of a secondary bilateral
symmetry. This is the case in forms which, like the Pteropoda, have
become adapted to a free-swimming manner of life. In such cases
the principal cause of the asymmetry, which we found to be the
creeping manner of life in connection with the development of a
high visceral mass, falls into the background. The fact, however,
that there are Gastropods which again become almost symmetrical
while still leading a creeping life, but in which the shell has al-
together or partly degenerated, as is the case in Onrhidium and the
Limaeidae, shows what an important part is played in these processes
by the covering of the body.
5. The Development of the External Form of the Body in
the Different Divisions of the Gastropoda.
A. Prosobranchia.
We have already repeatedly alluded to the development of the
larval form of the Prosobranchia and to its transformation into the
adult,* the principal features in these processes, the development of
the Troclwphore and Veliger larvae and their transformation into the
adult are thus known to the reader. Certain divergences, however,
occur among the Prosobranchia, especially in the earlier ontogenetic
stages, causing a modification of the external form of the body, and
thus requiring special consideration.
It has already been stated (pp. 112, 116) that the eggs of many
Gastropods are very rich in yolk, and this influences not only the
* @f- PP- 123, 131 and 134 on the development of Patella, Vermel us and
I'aliulina, also Figs. 49-59.
DEVELOPMENT OF THE EXTERNAL FORM — PROSOBRANCHIA. 149
formation of the germ-layers but also the development of the external
shape of the body. This is the ease, for instance, in Nassa, Fusus,
Fulgur, Natim and others. Even in Veiinetus, the Veliger stage of
which we became acquainted with (Fig. ")">), the Trochophore form is
no longer distinctly developed. The velum appears at first in the form
of two wavy cell-bands at the anterior end of the ventral surface and
near it appear the rudiments of the tentacles ; immediately behind
them are the mouth and the pedal swelling. The latter appears as
a rudiment when the velum is only slightly developed and is far
from complete dorsally. The rudiments of the organs, with the
exception of the dorsally placed shell-gland, are thus here crowded
together into a very limited area of the very large embryo. This is
the case to a far greater extent when the egg is still richer in yolk,
as, for instance, in Fulgur (McMurrich, No. 70). The first rudi-
ments of the organs are here so crowded together that we might
almost speak of a germ-disc in contrast to the large yolk-mass of
the egg. We should then see the commencement of processes which,
in a far higher degree, will be met with in the Cephalopoda. Thus
in eggs very rich in yolk we may speak of a " blastoderm " which
grows round the yolk, i.e., the macromeres, and, indeed, the layer of
micromeres is here greatly reduced as compared with the yolk-mass
of the macromeres, as may be seen by a glance at Fig. 42 D and E,
p. 112, and Fig. 47 A and B, p. 117. If we compare these figures with
those of the blastula and invagination-gastrula of Patella (Figs. 49
and 50), Planorbis or PalwUna, it is evident that these altered condi-
tions must bring with them modifications in the external shape of
the body.
In Nassa mutabili*, which we select for description as the best
investigated if not the most extreme form in this respect, there is
a point at the vegetative pole which remains for some time uncovered
l>\ cells (Figs. 61 ^4, hi, and 47 C, bp). This is the blastopore which
closes later, the stomodaeum arising in this region (Fig. 47 D, »>).
In Fusus, the eggs of which exhibit a similar condition, the blastopore
is said to persist and to pass over into the mouth (Bobretzky).
The toot appears very early as a broad swelling behind the blastopore,
even before the rudiment of the velum has arisen (Fig. 61 A, f).
Near it lie the groups of ectoderm-cells {ex) which have been claimed
as an excretory apparatus (external kidney). The velum (r) appears
in front of the blastopore, advancing from the ventral to the dorsal
Bide. Dorsally, the shell-gland appears, and over it the shell-integu-
ment. At a later stage, the anterior part together with the foot
150
GASTROPODA.
becomes marked off from the principal part of the embryo which
contains the yolk (Fig. 61 D), the anterior part becoming swollen up
like a vesicle (Fig. 63, ce, v). This phenomenon can be observed, still
better than in Nassa, in a species of Fusus examined by Bobretzky.
In this form, the foot and especially the anterior part of the body
appear to be swollen into a large vesicle (Fig. 62 A and B, kb), and
this part is therefore here also sharply marked off from the posterior
A.
B.
Fig. 61. — A -K, embryos of Nassa mutaMlis of different ages (after Bobretzky). bl,
blastopore ; d, posterior tubular portion of the enteron ; dr, yolk : ex, group of
ectodermal excretory cells ; /', foot ; fd, pedal gland ; h , rudiment of the heart ; hi,
posterior hepatic lobe, near which can be seen, to the left, the anterior hepatic lobe,
and above the latter the intestine (d) and the anus ; l\ rudiment of gill ; kh, pallial
cavity ; Ih, larval heart ; op, operculum ; /■, margin of the shell (s) ; v, velum.
part of the embryo. This swollen part, which corresponds to the
pre-oral section of the Trochaphore larva, and which is found in other
Prosobranchs, as well as in various other Gastropods (Pulmonates),
has been called the cephalic vesicle. The embryo in consequence
presents a very characteristic appearance (Figs. 62, kl, and 81, kbl).
The condition of the entoderm or yolk is of special significance for
the embryos now under consideration. The sac-like rudiment of the
DEVELOPMENT OF THE EXTERNAL FORM — PROSOBRANcrflA. 151
HU.
•a..
enteron is seen to be open towards the yolk (Figs. 47 C and I), 62 B,
and 63), which occupies the posterior and dorsal portion of the em-
bryo. The enteron consists of an anterior wider section and a posterior
tubular section (Figs. 47 I), and 62, mil). The latter is at first
parallel to the longitudinal axis, but soon lies obliquely to it, becomes
connected with the ectoderm, and opens out through the anus which
still lies in the ventral middle line (Fig. 61 C). At a later stage,
the posterior part of the
intestine assumes a still ££,
more oblique position
and the anus comes to
lie on the right side
(Fig. 61 I) and E).
Here also the pallial
cavity arises as a sickle-
shaped depression of the
ectoderm, this cavity in
Nassa being altogether
restricted to the right
side of the embryo. The
asymmetry seems still
more marked here than
in Palndina (p. 138).
The shell also shares
in this asymmetry ; by
its rapid growth it has
become cup-shaped and
covers the greater part
of the visceral dome
(Fig. 61 D). The
operculum appears as a
delicate plate in the
posterior dorsal part of
the foot (C and D, op).
In the foot can be seen a ventral tubular ectodermal depression,
which is no doubt the rudiment of the pedal gland (Figs. 61 E
and I), and 63). The velum, which is not yet closed dorsally,
has lost its former almost circular shape through the shifting
forward of the mouth and the appearance at this point of a notch
(Fig. 61 C). It at the same time increases in size and thus assumes
the bilobed form which we have already described in connection with
vtL—
Fr;. 62. — .1. surface view, ami B, median longitudinal
section through an embryo of Fus-us (after Bo-
hketzky). d, yolk ; /, foot : M), cephalic vesicle;
Oliver; m, mouth; md, enteron; mg, stomach;
<>t, otoeyst ; s, shell; ', tentacle: v, velum : vd,
stomodaeum ; :., sub-velar cells.
152
GASTROPODA.
other Gastropod larvae. Nassa now shows a strong general resem-
blance to such larvae, as is evident from Fig. 61 E. This is also the
case with Fums, the embryos of which also at first deviate in
several points from the usual shape and resemble those of Nassa.]
Bobretzky has described in connection with Nassa and Fusus an organ of
which no account has as yet been given ; this is the so-called " larval heart,'7
which has also been found in other Gastropoda {e.g., by Salensky in
Calyptraea, No. 98). This larval heart (Fig. 61 E, Ih) is said to be a part of
the ectoderm lying dorsally behind the velum, which is connected with
mesodermal elements and carries on contractile movements. Other parts of
the embryo, such as parts of the cephalic vesicle and the foot, are said to be
capable, like this region, of contractile movements.
Cr.v
Fig. 63. — Longitudinal section through an
embryo of Nassa m utabilis at a slightly
older stage than in Fig. 61 D (after Bo-
bretzky from Balfour's Text-book).
The cephalic section and the foot of the
embryo have separated to a great extent
from the yolk which forms the posterior
part of the embryo, ce.v, cephalic vesicle ;
/, foot ; hi, mouth ; st, stomach.
Remarkable transformations
in the shape of the body take
place in some Prosobranchs
which become adapted to a
parasitic life on or in various
Echinoderms (Asteroids, Echi-
noids and Holothuroids). An
excellent example of this is
afforded by Entoconcha miralrilid
described by Joh. Mltll.ee
(No. 76,) as occurring in the
body-cavity of Synapta digitata
attached to the wall of the
intestine. The body of this
animal has the form of a long
vermiform coiled tube which
in no way recalls that of a
Gastropod, but its brood-cavit}T contains embryos very like those
of other Prosobranchs. These have a velum (not, it is true, very
highly developed), a spirally coiled shell, a foot with an operculum,
otocysts, etc. Their further development is not known, but it is
probable that they live freely for a time, like the young Entovalva
(p. 13), and only later wander into a Holothurian.
In explaining the remarkable transformation undergone by Ento-
concha in consequence of its parasitic life, two Prosobranchs described
by P. and F. Sakasin {Thyca tntoconcha and Stilifer Linckiae) are of
great value (No. 103). These forms live parasitically on Asteroids,
either piercing the integument by means of a proboscis-like structure
{Thyca) or else sinking bodily into it {Stilifer). Even these ecto-
DEVELOPMENT OF THE EXTERNAL FORM — HETEROPODA. 153
parasitic Gastropods show decided changes in their structure, and
this would be still more the ease if they were to penetrate through
the integument of the host and reach the body-cavity. The possibility
of such a breaking in of the parasite from without is shown by the
StiliftH', which has already buried itself deep in the skin. The
cMerual shape as well as the inner organisation finally undergo, as
in many other parasites, such a far-reaching alteration, that there is
hardly any resemblance left to the former Gastropod, the parasite
having degenerated into a mere tube, like Entocolax or Entoconcha, on
which are devolved the functions of feeding and reproduction alone
{W. Voigt, Xo. 129; Braun, No. 15; Schiemenz, No. 108).
B. Heteropoda/
The ontogeny of the Heteropoda closely resembles that of the
Prosobranchia to which in other respects also they are nearly related,
but the special form of the adult Heteropod determines certain
variations especially affecting the later stages of development. The
ontogeny of the Heteropoda has been made the subject of special
study by Leuckart (No. 67), Gegenbaur (No. 37), Krohn (No.
58a) and Fol (No. 31).
We have already become acquainted with a few of the younger
stages of the embryo of Firoloida (Fig. 44
A-O, \>. 1 14). The oldest of these stages
was an invagination-gastrula. The inner
end of the archenteron soon assumes a
remarkable bilobed form, which recalls the
enterocoelic formation of the mesoderm as
described by Erlanger in connection with
Palvdina (p. 121), but which is no doubt
explained by the fact that the shell-gland
. . a Fig. 64.— Embryo of Fvroloida
which arises dorsally grows as a conical Desmaresti (after Fol). c,
• j . , i the primary body-cavity ; q,
invagination towards the archenteron, archenteric cavity ; o, mouth ;
causing a depression in the latter. When £• f°°*; s> shell-gland ; s\
1 shell-plug ; v, velum.
the shell-gland begins to flatten out again
(Fig. 64), the archenteron also assumes a more regular form, becoming
wider and sac-like. The blastopore passes over into the permanent
mouth (Fig. 64, >>). The shell-gland at first appears tilled by a plug
of brownish substance (s') ; in Palvdina, where a similar feature was
* [The Heteropoda, or Nucleobranchia, are very generally regarded as a
minor branch of the Prosobranchia, being classed under the Monotocardia as
a subdivision of the Taenioglossa.— Ed.]
154
GASTROPODA.
observed by Butschli, the plug was said to be expelled before the
actual shell formed, whereas Fol believes here that this mass which
fills the shell-gland passes directly into the shell when that depression
flattens out again.
In the stage depicted in Fig. 64, the pre-oral ciliated ring has
made its appearance and in this way the velar area (vv) becomes
bounded. Behind the mouth, the rudiment of the foot (p) appears
as a prominence which widens and thus assumes the form of a plate
(Fig. 65 B). On either side at its base, the otocysts (ot) appear,
while, anteriorly, the bilobed pedal gland forms as an ectodermal
invagination. The posterior part of the foot at this early stage
secretes a thin plate (op) which, in position and function, coi-responds
a.
eJ3.
Fig. 65. — Embryos of Firoloida Desmaresti. A, seen from the right side, B, from
the ventral side (alter Fol). ac, anal cells ; d, posterior part of the enteron ; /, foot \.
fd, pedal gland ; m, mouth ; md, enteron ; op, operculum ; ot, otocyst ; .?, shell ;
sp, apical plate ; w, ciliated ring.
to the operculum of the Prosobranchia. Fine calcareous concretions
become deposited beneath the shell-integument, and lead to the
development of the calcareous shell. Unequal growth here also
causes the shell soon to assume a coiled form, at least in the later
stages. In Firoloida and Pterotracliea, the shell has only two
whorls ; in Garinaria and Atlanta it coils several times.
Up to this [joint, the alimentary canal is without an anus.
According to Fol, two large cells which appear behind the foot
indicate, even in the stage depicted in Fig. 64, the position of this
organ, and at this point the enteron, which is bent anteriorly, be-
comes connected with the somewhat depressed ectoderm (Fig. 65, ac).
DEVELOPMENT OK THE EXTERNAL FORM HETEROPODA.
155
FlG. 66. — Larva of Firoloida with velum ex-
tended (after KROHN). ,/', foot; fl, rudi-
ment of fin ; .s\ shell ; /, right tentacle, at
the base of which the right eye is visible ;
the left tentacle is still wanting, but the eye
is present ; r, velum.
These specially marked cells lay originally in the ventral middle line;
they however shift towards the right side in consequence of the un-
equal growth which takes place also among the Heteropoda, and the
anus is thus found on the right
side, as we have already seen
to be the case in various other
Gastropods (p. 142). At this
stage, the embryo is almost in
the condition of the Trocho-
phore. it then soon passes
over to the Veliger stage, the
velum being bilobed (Fig. 66).
This bilobed character is at first
made evident by the mouth
shifting into a notch of the
pre-oral ciliated ring.
So far, the course of de-
velopment in the various
Heteropoda seems to be very similar (Fol). The round embryo,
which is now provided with a bilobed velum, a foot and a cup-shaped
shell, moves about by means
of its cilia within the gela-
tinous egg-rope, which has
become hollow ; it, however,
soon leaves this to swim about
as a free larva (Fig. 66),
circling slowly in the water
(Gegenbaur). The move-
ments become more rapid and
the larva more active when
the lobes of the velum increase
in size and are able to act
independently of one another.
According to Krohn, in
Firoloida and PterotracTiea,
the velum becomes drawn out
on each side into two l">ng
and very narrow streamers,
the larva then presenting an
appearance similar to that of the Veliger larva depicted in Fig. 54,
p. 130. In Atlanta, the velum is drawn out into three streamers
Fig. 67. — Larva of Atlanta with extended
velum (after Gegenbaur). ./', foot; H,
rudiment of the fin ; op, operculum ; ot,
otocyst ; s, shell ; v, velum.
156
GASTROPODA.
(Fig. 67), which, however, are considerably shorter than those just
mentioned. In Carina r/'a, again, the streamers are longer, and the
lobes, cut up into three parts, cause this larva greatly to resemble
that of Firoloida (Gegenbauk and Krohn).
The great development of the locomotory organs in the Heteropoda
causes their metamorphosis to be very marked. At its commence-
ment, a cylindrical process with a rounded free end appears on the
anterior side of the foot immediately in front of its base (Figs. 66 and
67, fl) ', this soon lengthens and carries on continuous swinging
movements. This is the rudiment of the fin which, in its origin, must
be regarded as belonging to the foot. In the course of metamor-
phosis, the cylindrical process becomes flattened laterally, and thus
77Z-.
Fig. 68.- Lateral aspect of a Oarinaria (after Souleyet and Gegenbaur). a, anus ;
abfj, abdominal ganglion: at, auricle; "", eye; bg, buccal ganglion; bm, buccal
mass ; eg, cerebral ganglion ; d, intestine ; /, tentacles ; ,//, fin ; k, gill ; /, liver ; m ,
mouth; ///", stomach; n, kidney;^, pedal ganglion; s, sucker; sc, shell; sj>,
salivary gland ; sw, tail ; vd, oesophagus : re, ventricle.
approaches the form of the keel-like fin of the adult (Fig. 68, fi).
This flattening extends from behind forward ; for a time, in the already
keel-shaped fin, a portion of the former cylindrical process is found ;
this, in Firoloida, is attached somewhat nearer the anterior margin,
but in Pterolrw.kea somewhat further back. By degrees this also is
drawn into the flattened fin (Krohn). In some species of Atlanta,
the fin appears from the first as a laterally flattened projection on the
anterior side of the foot and thus here more nearly resembles its
definitive shape. In this form, also, the sucker can already be seen,
lying close to the posterior margin of the keel-like foot, this position
DEVELOPMENT OP THE EXTERNAL FORM — HETEROPODA.
157
St.—
-- S.
J5
showing it to be the principal part of the Gastropod foot. This is
evident from the fact that the fin originates at the anterior end of
the foot, the posterior side of the latter being covered by the
operculum (Figs. 66, 67) ; the intermediate part, i.e., the actual
rudiment of the foot, must therefore in any case be concerned in the
Formation of the sucker (Fig. 69 A), unless we are to regard the
latter as a secondary formation. The sucker usually appears much
later ; in Firoloida, it is only found in the male, and has therefore
here become merely a
sexual character. Here
and in Carinaria (Fig.
68), the sucker lies some-
what far down at the
margin of the fin, and
thus becomes absorbed
in the latter, its pedal
character being in this
way still more marked.
That the sucker is not
merely a supplementary
differentiation of the fin
is proved by forms such
as Oxyijyrus in which it
is independent of the fin
and lies behind the
latter (Fig. 69/1). We
have here great agree-
ment with the condition
of some Prosobranchs
(Rostellaria, Strombus,
Fig. 69 B), in which the
posterior part of the
foot, as the carrier of the
operculum, is sharply marked off from the anterior part. This view
corresponds on the whole with that adopted by Gegenbaur and
recently especially by Grobben (No. 38), as to the significance of
the foot in the Heteropoda.
The tail found in the Heteropoda (Fig. 68, sw), also arises from the
foot, in Atlanta as a projection lying close behind the sucker (Krohn).
As it increases in size, this process, which also is cylindrical, presses
that part of the foot which bears the operculum more to the dorsal
sc
"Sg£y
Fig. 69. — A, Oxyyyrus, B, Strombus, each viewed
from the side (after Sodleykt and Kiener). a,
eyes ; /, tentacle ; h, posterior part of the foot ;
op, operculum ; r, proboscis ; s, sucker ; sc, shell ;
sw, tail (most posterior section of the foot) ; v,
anterior part of the foot.
158 GASTROPODA.
side, a position which is constant in forms like Atlanta, in which the
operculum is retained throughout life. The operculum, however, as
well as the shell, is frequently thrown off during the metamorphosis
(Firoloida, Pterotrachea).
While these changes have been taking place in the foot, the velum
has gradually attained its highest development and then commences
to degenerate. The rudiments of the tentacles have already appeared
on the velar area ; these arise, curiously enough, quite asym-
metrically. One tentacle only is present at first (Fig. 66, t). At
the bases of the tentacles, the eyes appear. In some forms, the
tentacles may be reduced again {Pterotrachea). Before the shell is
thrown off, the velum has for the most part degenerated, only a few
traces of it being still found near the eyes.
The body increases greatly in length, not only on account of the
development of the caudal section just described, but also through
the extension of the anterior part (the development of the so-called
proboscis, Fig. 68). In consequence of the great lengthening of the
foot and the anterior part of the body, the visceral sac lies, as in
other Gastropods, on the upper side of the body (Fig. QS). At the
junction of the visceral sac and the dorsal wall of the anterior part
of the body, the mantle-cavity has arisen and the gill has formed.
Where the shell is retained, it covers the visceral sac (Carinaria,
Fig. 68), and in Atlanta, which also as an adult possesses a shell, the
whole animal can still be withdrawn into it.
C. Opisthobranchia.
The ontogeny of various forms of the Opisthobranchia has been
studied by many zoologists. The embryonic development and the
younger stages of the free-swimming larvae were those usually in-
vestigated, the animals being difficult or even impossible to keep in
confinement during the later stages. Saks (Nos. 104 and 105) and
Loven (No. 69) established the chief features of their ontogeny,
while at a later period Adler and Hancock (No. 1), Nordmann
(No. 80), Vogt (No. 127), Schultze (No. 113), and Keferstein
(Nos. 52 and 53), occupied themselves principally with the develop-
ment of the larval forms and of the shape of the body. Bay Lan-
kester (Lamell. Lit., No. 29), Trinchese (No. 125), Blochmann
(No. 8), Bho (No. 93), turned their attention also to the internal
processes, especially to the earliest ontogenetic stages. References
DEVELOPMENT OP THE EXTERNAL FORM OPISTHOBRANCHIA. 159
to the other authorities on this subject will be found in the literature
a[>] tended to this section and in the course of our account.*
In consequence of the rich supply of yolk in the egg, gastrulation
seems usually to take place by epibole.-f- The blastopore, at one
period, is a slit of variable length (e.g., in Fiona and Elysia, Haddon,
No. 40; JErcolania, Trinchese ; Aplysia, Blochmann). This slit
-closes from behind forward and, in some cases, altogether disappears,
the mouth then arising as an ectodermal invagination at the point at
which it closes. This is the case, according to Blochmann, in
Aplysia and a similar condition may, according to Vogt's account,
be found in Elysia. In Fiona, according to Haddon, the slit-like
blastopore closes from behind forward and either passes directly into
the mouth or the latter is invaginated at the spot where the former
filially closes. Such a condition can be gathered from the descriptions
given by Trinchese (No. 125) and Langerhans (No. 62) of the
Aeolidae and Doris, but these accounts are not very clear. From
all these statements, however, it appears tolerably certain that the
mouth corresponds in position to the anterior end of the slit-like
blastopore.
The changes that take place in the large entoderm-cells are
significant in connection with the further shaping of the embryo.
These have been specially observed in Aplysia by Blochmann.
Cleavage is unequal from the first and, at the four-celled stage, two
of the cells are very much larger than the remaining two, and this is
still apparent after the abstriction of the micromeres, when we find
two very large and two smaller macromeres (Fig. 41 B). In conse-
quence of the smaller amount of the yolk contained in the latter,
they soon divide and give rise to a mass of small entoderm-cells,
while the two large macromeres (Fig. 41 / and //) are retained in
their full size. The ectoderm-cells grow over the entomeres and the
smaller entoderm-cells separate from the two large macromeres which
* [Recent workers on this group have devoted themselves mainly to the
question of cell-lineage, see Heymons (No. XII.) and Viguier (No. XXVI.).
Mazzarelli (No. XVI.) has, however, rnade soine additional observations on
the larval Aplysia. — Ed.]
f [Heymons (No. XII.), who has investigated the early stage in the
ontogeny of Umbrella, finds that the gastrula is here intermediate between
the epibolic and the embolic type, as is the case in so many other Gastropods.
His work, which is an important one, deals largely with the cell-lineage and
the early ontogenetic stages. Umbrella, in its cleavage, appears to conform to
the normal Gastropod type, the process of entoderm-formation is quite
unlike that described by Blochmann in Aplysia, the yolk being equally
distributed between the four macromeres and the entodermic epithelium
■arising in a more normal manner.— Ed.]
160
GASTROPODA.
are still undivided. An archenteron forms between them, lined partly
by the small entomeres and partly by the two persistent macromeres
(Fig. 70). Here also there
ed.
ent.
ent.
Fig. 70. — Embryo of Aplysia limacina in optical
section (after Blochmann). bl, blastopore ; ect,
ectoderm ; ent, entoderm.
is a suggestion of a condition
intermediate between an
epibolic and an invagination -
gastrula, as is said to be the
case in other Gastropods
(<■/. p. 115). The closure
of the blastopore and the
sinking in of the stomo-
daeum already described
(Fig. 71, in), take place
immediately after this stage.
Where the macromeres are not in direct contact with the ectoderm,
the smaller entoderm-cells spread out (Fig. 71). The gut, still partly
bordered by the macromeres which have shifted apart, now resembles a
closed sac* Up to this point there has been no sign of the mesoderm-
rudiment which, according to Blochmann, appears late in the form of
two small masses of cells lying to the right and left of the stomodaeum,
the origin of which could not be established. Trinchese, on the other
hand, described, in the Aeolidae, two large and distinct primitive
mesoderm-cells which may be traced back, like those of the mesoderm-
rudiment found by Eho in Chromodoris, to the macromeres. [See
the more exact work of Heymons (No. XII.) on Umbrella in this
connection, and footnote, p. 119].
At the side of the embryo opposite to the mouth, the shell-gland
arises as a depression which at first is shallow, but deepens later
(Fig. 71 A, sd) ; above this, the shell-integument is soon secreted.
Two cells (az), which lie on the ventral side in front of the shell-
gland and which, in consequence of their large size, rise above the
surface (Fig. 71), mark the position of the anus, which appears late.
These anal cells could be seen in Aplysia in earlier stages, lying at
the posterior edge of the blastopore. They had been already described
by Langerhans in several Opisthobranchs (Aeera, Aeolix, Doris)
and had been connected with the formation of the anus ; the same
* [Mazzarelli (No. XVI.) does not appear to have traced the ultimate fate
of the two smaller macromeres, but one would imagine, from his description,
that they form part of the ectoderm. He regards the small entomeres seen in
Fig. 71 as derivatives of the two large macromeres and, judging from his Fig.
12, PI. x., small cells are constricted off from the macromeres. His observa-
tions are not clear, hut they seem to differ from those of Blochmann. — Ed.]
DEVELOPMENT OF THE EXTEBNAL FOBM — OPISTHOBBANCHIA. 161
significance is ascribed to' them by Tbinchese in the Aeolidcu and
by For, in the Heteropoda and Pteropoda.
The ciliated cells of the pre-oral ring have already become differ-
entiated, the velar area being thus marked off (Fig. 71, v). Ventrally
behind the mouth, the font appears as a swelling (/) ; behind it ran
be recognised the anal cells ((c). The shell-integument has already
developed further. The Trochophort stage is here less marked than
in many other Gastropods, as the embryo undergoes certain modifica-
tions in consequence of the richer supply of yolk. Such a stage,
however, has been distinctly recognised by Ray. Ijankester and
Tbinchese and other observers in Opisthobranchs which have been
tt.
J5
jn«>.
Fig. 71.— Two stages in tin- development of Aplysia limacina (after Blochmann), «'.,
anal cells ; ect, ectoderm ; ent, entoderm ; /. foot : »<. mouth : mes, mesoderm ; mr,
margin of the mantle ; ••■'. shell; sd, shell-gland; sh, shell-integument; <•. velum.
investigated by them. An embryo of Aplysia figured by Bay Lan-
kesteb* shows the greatest resemblance to the embryos of Firo-
/<■;,/,! depicted in Fig. ii") .1.
The Trochnphore stage, by the transverse extension of the velum,
pa>srs into the Veliger stage, in which, owing to processes of growth
similar to those already described, the symmetrical shape undergoes
certain modifications. In most respects, indeed, the ontogenetic
processes which now follow closely resemble those described for the
Prosobranchia, so that we need here only touch upon the principal
features.
• (See Lit. to Lamellibramhia. No. 29, PI. 8, Pig. 17. |
M
162
GASTROPODA.
The two lottos of the velum are very large and give the larva a
characteristic appearance (Fig. 72, v). They remain undivided, are
very broad and are beset with long thick cilia ; the fissure between
them, however, usually carries short and delicate cilia, the bilobed
character of the velum being in this way emphasised. The shell has
lost its flat and (later) cup-like shape and, in the free-swimming larva,
has already become coiled. The foot (/) develops an operculum on
its dorsal surface. We thus find, in the Opisthobranchia, the same
general condition already met with in the Prosobranchia and the
Heteropoda. Although most Opisthobranchs, as adults, are entirely
Fig. 72. — Veliger larva oi an Opisthobranch. a, anus ; ad, anal gland (? probably an
excretory organ, like n) ; d, alimentary canal; di, diverticulum of the stomach ; /,
toot ; in, mouth ; mil, muscle (retractor of the velum) : op, operculum : ot, otocyst :
S, slu-11 ; V, velum.
devoid of a shell, or else, as in the majority of the shell-bearing forms,
have a highly specialised, often greatly reduced, or even internal
shell, the larva possesses a coiled, often nautiloid shell into which
the body can be withdrawn and which can be closed by an operculum
(M. Sars). The shell is usually thrown off and the operculum al-
most invariably has the same fate. When, however, the adult
possesses a shell, we may fairly safely assume that this has been
derived from the larval shell. In only a few Opisthobranchs is the
shell of the adult so large that the whole body of the animal can be
DEVELOPMENT OF THE EXTERNAL BODY— OPISTHOBBANCHIA. L63
withdrawn into it; the retention of the operculum as in Acta
{Tornatella) is quite exceptional. According to Tkinchese, the
larval shell in some forms (Saccoixlossa) shows a delicate reticulate
Structure on its surface ; in most other larvae it is smooth.
Passing now to the internal organisation of the Veliger larva, we
notice first that, from the oral aperture which lies at the ventral
incision of the velum, the stomodaeum (which only at a later stage
is provided with a radula) runs backward and becomes connected
with the large enteron. From this latter, there are two lateral
outgrowths which differ in size (Fig. 72, di) ; these are formed of
specially yolk-laden cells and thus no doubt owe their origin to
the macromeres. The intestine also arises as a diverticulum of the
entoderm-sac ; it then lengthens considerably, bends forward and,
after uniting with the ectoderm at the right side of the body, opens
outward rather far forward, near the edge of the shell (Fig. 72).
Little is as yet known as to the differentiation of the mesoderm in
the Opisthobranchia. A strong muscle, sometimes composed of two
branches, runs back from the velum, becoming attached to the shell
posteriorly (Fig. 72, mu). Another shorter retractor of the velum
extends between the base of this organ and that of the foot. This
arose from single spindle- or star-shaped mesoderm-cells which came
to lie on the right side of the larva in this region.
This latter muscle carries on regular rhythmical movements and, on this
account, has, according to Trinchese, falsely been regarded by several
observers as a heart. The so-called larval heart which has been described
in connection with the Prosobranchia (Nassa, Fig. 61 E, Ih, p. 150) differs
somewhat in position from this retractor, but is, like it, composed of long
mesoderm-cells.
According to the accounts of the Opisthobranchs now under con-
sideration, no primitive kidneys resembling in shape those occurring
in the Prosobranchia (Paludina) and Pulmonata (p. 136) have been
found in them, but vesicular structures which lie in the dorsal
region behind the velum to the right and left of the oesophagus
have been described as primitive kidneys. These have been regarded
- excretory oi-gans chiefly because they are filled with strongly
refractive concretions. They seem never to possess efferent ducts.7"
The views taken of the excretory organs of the Opisthobranchia seem
to us to be somewhat confused. Tkinchese, for instance, has described a
paired or unpaired sac-like gland with a longer or shorter efferent duct which
* [These appear to be ectodermal in origin (Heymons) and analogous to the
ectodermal anal kidney of the Prosobranchia (p. 129 and No. XV.;. — Ed.]
164 GASTROPODA.
opens out near the anus as an anal gland. In Ercolania, this gland is un-
paired and strongly pigmented. A glandular structure described by Rho in
vmodoris is said also to open near the anus. This involuntarily recalls the
rudiment of the kidney of the adult, a view which has recently been adopted
by Mazzarelli (No. 74 and No. XV.). This author derived similar structures
from the mesoderm. One organ especially which, curiously enough, was
assumed to be an " anal eye," excited attention. This lies in various Opistho-
branch larvae (in Aplysia, Philine, Pleurobranchus, Doris, Aeolis, Lacaze-
Duthiers and Pruvot, No. 60) on the ventral side, near the anus ; it is
strongly pigmented and is no doubt identical with the glandular structures
above mentioned. According to Mazzarelli, as already mentioned, it is
derived from the mesoderm, but Lacaze-Duthiers and Pruvot, who in-
vestigated the origin of this hypothetical larval eye more closely, traced it
back to the ectoderm. This was also the result of the ontogenetic researches
of Heymons as to the origin of this structure, and it cannot therefore be
regarded as a nephridium, but must rather be compared with those excretory
organs which, like the sub-velar cells described in the Prosobraachia, are
yielded by the ectoderm (p. 129). The excretory character of the organ seems
indisputable, but no decision as to its homology can be arrived at until its
development and future fate in the different forms of Opisthohranchs are
better known.
Among the sensory organs of the larva, the large otoevsts at the
base of the foot deserve special mention. As in other pelagic larvae,
strong cilia appear at the centre of the velar area in various forms
[Fiona, Pa/yeem, Elyda, Philine, Haddon, No. 40). In the Aeolidae,
the end of the foot carries a few long stiff cilia. Eyes are found on the
velar area in those cases at any rate in which tentacles also appear
there as rudiments, but are altogether wanting in many larval forms.
The greatly modified forms found among the Opisthobranchia,
such as the genera Di.mapontia and Phyllirhoe, like the more primitive
forms, have larvae with bilobed velum and shell provided with an
operculum (Adler and Hancock, No. 2; Schneider, No. 111').
Our knowledge of the transformation of the larva into the adult
rests principally upon the statements of Max Schultze and Nord-
mann made with regard to Tergipes Edwardsii and T. lacimdatus
(Nos. 80 and 113).
The larva of Tergipes Edicanhii, when still provided with a shell,
already seems to have lengthened somewhat. The two velar lobes
are unusually large and oval. On the velar area are situated a pair
of tentacles and, at the base of these, the eyes. The larvae probably
swim about for some time at this stage. The mantle then with-
draws from the shell and comes into closer contact with the body.
The way is thus prepared for the casting of the shell which takes
place while the velum is still fully developed. We thus have a
DEVELOPMENT OF THE EXTERNAL FORM — OPISTHOBRANCHIA. L65
Veliger larva without shell or operculum, which presents a very
peculiar appearance (Fig. 73 A). This larva, in the length of its
body already shows a distinct approach towards the adult condition.
In the Tergipes oI.sci-v.mI by M. Schultze, the passage from the larva
to the adult is somewhat different, the velum degenerating in this
form before the shell is thrown off. lu this last case, the larva must
have adopted earlier the creeping manner of life. The shelldess larvae
of Tergipes Edwarddi, with their large vela at first swim about with
even greater rapidity than the shelled forms, but then gradually
begin to creep, as the body increases in size (Fig. 73 B). The lobes
of the velum commence to degenerate until they are reduced to a
pair of rounded processes lying in front of the mouth (Fig. 73 C),
which, it has been assumed, change into the labial palps.
(L
, Veliger larvae ami young of the Tergipes Edwardsii (after NORDMANN).
d, alimentary canal ; //. dorsal papillae.
This view of the transformation of the remains of the velum into the sensory
organs near the mouth, has been adopted especially by Loven, who already
held a similar view as to the origin of the oral lobes in the Lamellibranchs
(p. 46). Ray Lankester holds that, in Limnaea, the remains of the velum
pass over into these subtentacular lobes ; but this point has been disputed
in connection with this form. It has already been stated (p. 133) that the
observations made by Ray Lankester for Onchidium were confirmed by
Joyeux-Laffuie.
While the larva is still provided with the large velar lobes, one pair
of the dorsal appendages (cerata) arise which are so characteristic of
the Nudibranchs and into which the diverticula of the enteron soon
extend (Fig. 71 0). Another pair of these intestinal diverticula has
already formed and these belong to the next pair of cerata. As other
processes develop^ the young animal approaches more and more
166 GASTROPODA.
nearly to the adult form, but has first to pass through a moult
(Nordmann), during which it remains entirely quiescent, surrounded
by the cast skin as by a transparent sheath. This membrane is no
doubt to be regarded as the cast off cuticle.
D- Pteropoda.
The early development of the Pteropoda closely resembles that of
other Gastropods. We have already seen that the embryo at first
has the form of an epibolic gastrula and passes from this to an
invagination -gastrula (Fig. 45 A and B, p. 115). The entoderm, at a
later stage, by the great increase in number of its cells, is transformed
direct into the epithelium of the archenteron ; but, in some forms,
the macromeres seem to be retained for a long time, the transition to
the definitive entoderm being then less simple. The blastopore is
slit-like and situated at the vegetative pole. After its closure, the
mouth arises at the same spot through an ectodermal depression.
From the published accounts, we may assume that the mouth then
shifts its position or, in consequence of the further growth of the
embryo, changes its shape. At one end of the embryo a circle of
strongly ciliated cells marks oft' the velar area, immediately behind
which the mouth now lies. At a point almost opposite the cephalic
area, on the dorsal surface of the embryo, an ectodermal depression
appears which varies in size in the different genera ; this is the
shell-gland. The whole of the interior of the embryo is filled with
yolk-laden macromeres. The velum heroines more distinct, and,
behind the mouth, the foot appears as a large outgrowth. When
the otocysts arise near the foot and the two anal cells (which also
occur in the Pteropoda) behind it, the embryo passes into the
Trochophora stage which greatly resembles that met with in the
Opisthobranchs, or the corresponding stage in Firoloida (Fig. 65).
At the stage just described, or even earlier, the embryo may
become free and may swim about actively, since it is already provided
with a velum. Up to this point the different Pteropods develop in
much the same way, but differentiations soon appear in the develop-
ment of the larval form, especially with regard to the shape of the
velum and the shell. The Gymnosoniata also diverge from the other
forms in so far as the Veliger stage gives rise to a peculiar larval
form encircled with several ciliated riny;s.
■&*■
A certain differentiation in the development of the early larval stages is
also caused by the fact (stated by Fol) that the order in which the organs
DEVELOPMENT OF THE EXTERNAL FOUM--PTKHOPODA.
L67
(velum, mouth, shell-gland, foot, etc.) appear, varies greatly in different forms.
The comparison of corresponding stages is in this way rendered somewhat
more difficult, but the final result is. a-> already stated, very similar.
The embryonic development of a large number of Pteropoda (Cavolinia
(Hyalea), Hyalocylix, Creseis, Styliola, Cleodora, Cymbulia, Clione) has been
closely studied by Foi„ who has also described the further development and
the metamorphosis of these animals (No. 82). The phenomena connected
with metamorphosis had previously been investigated especially by Joh.
Mdller, Gegenbaor, and Krohn in the above genera as well as in Tii'ilemanma
and Pneumodermon (Nos. 77-79, 37 and 58a).
Thecosomata. The Trochophore stage soon passes into the Veliger
stage, a dorsal and a ventral incision appearing in the velum, which
thus becomes bilobed. This organ is bordered anteriorly by a circle
of strong cilia serving for locomotion, and posteriorly by weaker cilia
which conduct food to the mouth
(Gegenbaur, Fol). In Cleodora
a band of cilia appears on the velar
area at a time when the larva is
still at the Trochophorn stage.
Other Pteropods, e.g., Cavolinia,
carry on the velar area a central
ciliated tuft, such as has been met
witli in other Molluscan larvae.
The size of the velum varies
greatly. In Cavolinia, where it
is retained for only a short time,
it is less extensive. In Fig. 71,
we see the velum in a slightly
older larva of such a form. In
Cleodora, Cymbulia, Tiedemanuia
(Fig. 75 .4 and B) the velum is
much larger, and each of the two
lobes is again subdivided, so that
the whole appears to consist of
four lobes. This condition is
specially distinct in a larva be-
longing to the genus Creseis and
described by Gegenbaub (Fig.
75 C), in which the velum is still
of considerable size when the shell has grown to a great length. A
strong retractor starts from the anterior part of the body and is
inserted at the posterior end of the shell (Fig. 7(5 A,)').
m<
Fig. 74.- Larva of Cavolinia tridentata,
seen from the right and ventral side
(alter l-"oi., from Bai. four's Text-
book). ". anal region, with the two
anal eells ; /, mesopodium ; A, heart;
/. intestine : kn, contractile dorsal
sinus : m. oral region : mb, mantle ;
mc, mantle-cavity; ot, otocyst; ////.
rudiment of tin ; q, shell ; /'. renal sac :
s, stomach ; a. food-yolk.
168
GASTKOPODA.
The shell originates from the shell-gland which has shifted towards
the end of the body. According to Fol, a ping of strongly refractive
substance is very often to be found in the shell-gland ; in some cases,
this plug is perhaps formed abnormally, but in Cymbulia it no doubt
represents the normal condition. The substance is then said to
spread out under the shell which is secreted as a cuticular integu-
ment, after the shell-gland has gradually flattened out. It is at first
shaped like a watch-glass, then deepens and becomes cup-shaped
(Carol in in, Oleodora, etc.), or else it becomes rounded and almost
oviform like the embryonic chamber of the Cephalopoda. This is
V.r
Fig. 7:"'. — Larvae of Tiedemanniu (.1). Cymbulia Peronii(B) ; and Oreseis acicula (C)
(after Kkohn and (tEGEnbaur). d, operculum ; ,/'. foot : .//. fins : s, shell ; v, velum.
the case in Creseia, Cymbulia, and the Gymnosomata. The shell,
which now becomes calcified, grows by the addition of new layers to
the margin of the embryonic shell, their boundaries being recognisable
as /ones of growth. In this way, the large larval shell which, in the
Cavollniidae and Gymnosomata is long and in the Cymbuliidan coiled
is formed (Figs. 74, 7, 75 A-C, 76 A, «).
In the Cacoliniidae, the shell of the adult forms very simply from
the larval shell, by the addition of further layers to its anterior
DEVELOPMENT OF THE EXTERNAL FORM — PTEKOPODA. L69
margin, but the latter is marked offby a constriction from the part
which represents the adult shell : here also, in Caoolinia, a transverse
wall is secreted, after the body of the animal has withdrawn from
the posterior pari of the shell. This larval shell is afterwards lost.
In other Cavuliniidae, the larval shell is retained even in the adult
(Styliola), the posterior part of the body not being withdrawn from
it (Creseis). The coiled larval shell of the Limacinidae passes directly
over into the adult shell, new coils merely being added to those
already present (Limacina, Spinalis), in the Gymbvliidae, the
larval shell can hardly hi' distinguished from that of the young
animal undergoing metamorphosis. This calcareous shell is thrown
off, the cartilaginous shell of the adult surrounded by the mantle
then appearing ; this shell arises by the thickening of the connective
tissue and can therefore not he in any way compared to a true
Molluscan shell (Pelseneer).
The transformation of the shell just described is one of the most
conspicuous features among the external alterations undergone by
the larva. In the Cavoliniidae, the shell lengthens, and, in the Gym-
buliidae and Limacinidae, becomes rolled up (Fig. 75 A and B).
Even in the straight shells of the Gacoliaiidae we find a slight flexure
of the posterior end which gives the shell the shape of a hunting
horn. It is a curious fact that the concavity of this slightly bent shell
dors not correspond to the ventral side, but lies dorsally. This must
lie connected with a twisting undergone by the posterior part of the
body in these forms (Boas, Nos. 9 and 10). The coiled shell in any
case represents the more primitive condition and persists throughout
life in the Limacinidae, which are also provided with an operculum.
The development of the foot exercises a great influence on the
changes that take place in the external form of the body. The foot
originally was a large projection lying behind the mouth. While
tin- middle parr of the foot does not increase greatly in size, and at
first is conical or linguiform, two projections arise at its sides and
grow out rapidly (Fig. 71, ////, and 75 A, fi) in the form of two large
lobes, the so-called bus (Fig. "■"> IKJI). The great size which may
lie attained by the tins in the further course of metamorphosis is
already sufficiently known. The median lobe of the foot also in-
creases in size. In the Cymbitliidar, a filiform appendage develops
on it posteriorly. Ontogeny proves indisptitably that the fins owe
their origin to the foot, as was observed long ago by JOH. MuLLEK
and Kkohx.
The Veliijer larva of the Pteropoda shows great agreement with
170 GASTROPODA.
that of the Opisthobranchia, a fact which is specially evident in
the forms that have a coiled shell (Figs 75 A, and 72, p. 162). The
posterior part of the foot here also usually carries an operculum
which, in the Lima tin I doe, is retained throughout life, and in the
Cymbuliidae, is thrown oft' after the shell has been lost ; but in those
Pteropods that have straight shells an operculum is not found. A
well-developed primitive kidney is not known to occur in the Ptero-
poda ; they may, in this respect, resemble the Opisthobranchia, a
comparison which would be supported by their internal organisation.
We have here, for instance, as in the Opisthobranchs, the two sacs
rilled with food-yolk as appendages of the enteron. In the formation
of the alimentary canal, the entoderm becomes differentiated in such
a way that the median (ventral and dorsal) parts become the epi-
thelium of the archenteron, while the lateral parts which appear
composed of large cells rich in yolk, by growing out into caeca, be-
come the nutritive diverticula. These caeca have been supposed to
yield the liver, but this organ, according to Fol's statements, forms
independently of them as an outgrowth of the archenteron. A pos-
terior tubular diverticulum of the archenteron runs out towards the
ventral surface and fuses with the ectoderm at the spot where the
anal cells lie to form the anus. This lies either in the middle line
behind the foot, shifting secondarily to the left side (Gavoliniidae) or
else it lies from the first on the right side of the body {Cymbuliidae,
Gymnosomata). There are also other indications of asymmetry, such,
for instance, as the lateral position of the mantle-cavity. This indi-
cates that the Pteropoda which, as adults, are somewhat symmetrical
in structure, are derived from asymmetrical forms.
As the fins increase in size, the velum gradually degenerates. The
mouth takes up its final position between the fins. The disappear-
ance of the velar area leads to the great redaction of the large section
of the larcal body which lies in front <>f the foot. At a later stage,
the two tentacles bud out in this region, carrying the eyes. This
reduction of the anterior part of the body as compared with the
massive foot, which has shifted far forward, is specially characteristic
of the Thecosomata. In Tiedemnnnia, however, the oral region be-
comes raised up to form the proboscis which bends backward. After
the growing shell has reached the base of the foot, a slit-like invagina-
tion appears in the Caoolini.idae (according to Fol) on the right side
between the base of the foot and that of the velum, extending then
dorsally and ventrally. The mantle-cavity thus formed finally
encircles the body (visceral dome) on three sides, so that the latter
DKYKl.Ol'MKNT OF THE PATERNAL FORM l'TKKOPOD.V.
171
is connected with the mantle or shell (in the Caooliniidae) only on
the left dorsal side.
The ventral position of the mantle-cavity in the Cavoliniidae is very striking,
as i his cavity, in other Gastropods, is dorsal in position. According to Boas,
the visceral dome and the shell connected with it have undergone torsion.
This view is supported by the fact that, in younger larvae, the bent apex of
the shell is directed not, as in the adult, dorsally, but to tVie left. It is at
once evident that this process may be classed with those already described in
connection with the acquisition of asymmetry by the Gastropoda (p. 143), but
in this case other changes have been added iu adaptation to a different manner
of life.
We shall not here give any special account of those ontogenetic
processes such as the formation of the otocysts, the radular sac, etc.,
which take place in the same way as in other Gastropods.
Gymnosomata. The Trochophore is followed by a larva provided
with a large bilobed velum
and a pointed foot (Fig.
76 A,/). The shell, which
at first is cup-shaped but
later oviform, as it grows in
length, becomes a tube
widening out anteriorly
(Fig. 76 A), on which, as a
rule, the zones of growth
are recognisable as intervals
varying in width. The
larva does not long remain
at this stage, in which it
closely resembles the
straight-shelled Thecoso-
niata. The shell is thrown
off' and the velum degene-
rates. When it disappears,
or even sooner, three ciliated
rings appear on the body
(Figs. 76 Band 77 A). In
those larvae that develop
ciliated rings even before
the disappearance of the
velum and the casting of
the shell, these are distri-
buted in such a way that the most anterior ring lies between the
Fit;. 76. Larvae of Clione at two different stages
of development latter KROHNandGEGENBAUR).
./', toot ; /, live]-; »<. stomach ; "<-. oesophagus;
,. retractor muscle; s, shell; v, velum; w,
ciliated rings.
172
GASTROPODA.
velum and the foot, and the posterior ring immediately in front of the
aperture of the shell. In this case, the posterior part of the body is
still of some length ; in other larvae, the posterior ciliated ring is
found almost at the end of the body (Fig. 76 B). The velum seems to
bear no relation to the ciliated rings. After it degenerates, the larva
presents an appearance which, for a Mollusc, is very peculiar, recalling
rather the Annelid larvae which are encircled with several ciliated
rings. These also are at a stage following the Trochuphore larva,
as already mentioned (Vol. i., p. 277), and as we were able to see
in various polytrochan larvae. Tins comparison to an Annelid
larva has already been instituted by Gegenbaur, and the fact has
been emphasised that the resemblance is accidental and of no great
significance.
Our knowledge of the ontogeny of the Gymnosomata relates entirely to Clione
and Pneumodermon, two forms which seem to agree pretty closely in the
general features of their development, as shown hy Joh. Muller, Gegenbaur,
Krohn and Fol. As most of these larval Gymnosomata have not been traced to
the adult stage, it is by no means certain that the larvae examined belonged
to these genera.
The mouth lies on the anterior, proboscis-like projection, and the
anus, which is displaced to the right, ventrally between the first and
second ciliated rings. Two pointed outgrowths lying near the mouth
represent the rudiment of the so-called cephalic cone (Fig. 77 />').
Somewhat further back, but
in any case in front of the
anterior ciliated ring, the rudi-
ments of the acetabuliferous
appendages appear (Joh.
Muller). [These, according
to Pelseneer, are derivatives
of the proboscis.] When the
proboscis is evaginated at a
later stage, these seem shifted
further back, being now situ-
ated on its posterior part
(Fig. 77 B). The foot was
previously referred to as a pointed ventral appendage, lying behind
the first ciliated ring. Before this stage, an anterior, horseshoe-
shaped lobe forms in the posterior concavity of the pointed part
of the foot. Immediately behind the anterior lobe of the foot, on
either side of the posterior lobe, the first rudiment of the fins can
Fig. 77. Two larvae ot Pneumodermun at
different ages (after Gegenbaur, from
Balfour's Text-book), mi, amis.
DEVELOPMENT OF THK i:\ I I'.KNAL FORM— PTEROPODA. 173
be seen as very small, rounded lobes projecting- from depressions in
the body ( Krohn).
The further metamorphosis consists in the growth of these parts
and the degeneration of the ciliated rings. The most anterior of
these is the first to disappear and then the middle ring ; the posterior
ring is still to he found when the young animal attains its full size,
hut no doubt degenerates later.
We must here add a few words of explanation as to the position assigned by
u- fco the Pteropoda. Until recent times, the Pfceropoda were often regarded
as a special class equivalent to the Gastropoda, Cephalopoda, etc., although
some zoologists objected to such a classification. For anatomical and outo-
genetic reasons the Pteropoda are now classed with the Gastropoda,* being
placed specially near the Opisthobranchia, as is indicated by the form of
the central nervous system and their circulatory apparatus, as well as by the
structure of their genital ducts and by their hermaphroditism. Another im-
portant factor in classing the Pteropoda is found in the organ which gives the
body its characteristic shape, viz., the swimming apparatus. The manner in
which the tins arise proves that they are derived from the transformed lateral
parts of the foot. It is an interesting fact that in some Pteropoda (the
Gymnosomata) the propodium has still retained its function as a creeping
sole, serving, like the sucker of the Heteropoda, for attachment (Souleyet,
No. 121 ; Grobben, No. 3(J). The fins have been regarded by some as epipodia,
but Pelseneer, on the contrary, considers them to he widenings of the whole
margin of the foot. Such fin-like widenings (swimming lobes) are found in
certain Opisthobranchs, and the derivation of the Pteropoda from such forms
seems to be suggested. Grobben. as well as Boas and Pelseneer (No. 8 1 .
the two more recent investigators of this subject, have recently given active
adherence to this view. Lateral widenings of the sole of the foot are found in
Acera, Gasteropteron. These Opisthobranchs which, like the Pteropoda, can
swim freely by flapping these fin-like foot-lobes have therefore been regarded
as the starting-point for the latter group. From such Opisthrobranchs the
Thecosomata would first have to be derived, as has been done by Pelseneer,
who traced back the Thecosomata to forms like Acera among the Bulloidea,
\ bereas he derives the Gymnosomata from forms like Aplysia, in which latter
the swimming lobes are, as in the (ivmuosomata, somewhat more dorsal in
position. Pelseneer, in his classification of the Opisthobranchia, places the
Thecosomata directly after the Bulloidea. and the Gymnosomata near the
Aplysoidea. Boas also regards the Pteropoda as very nearly related to the
\niong the maintainers of this view we may mention Fol, Spengel,
ibben, Boas, and Pelseneer. In It. Hertwig's text-book, the Pteropoda
are classed as a subdivision of the Gastropoda, and Glaus also recently gives
them a similar position, placing them after the Opisthobranchia. [Practi-
cally all zoologists now class the Pteropoda with the Gastropoda and most
accept Pelseneer's views according to which they find their nearest allies
in the Tectibranchiate Opisthobranchs. Pelseneer fimher separates the
Gymnosomata from the Thecosomata. placing the latter with the Bulloidea
and the former with the Aplysoidea (see Challenger Reports, Vol. xxiii.) —
Ed.]
174 GASTROPODA.
Opisthobranchia and points out the great similarity existing between the in-
ternal organisation of the Bulloidea and that of the Thecosomata. Between
the Gymnosomata and the Thecosomata he finds a great distinction, since he
cannot regard the fins in the two divisions as homologous. Since, however,
according to him, the Gymnosomata, like the Thecosomata, are to be traced
back to Tectibranchia, they have in any case a common root. It appears to
us that their development is in favour of a connection between them. Their
larval forms agree closely, the resemblance between the long, straight shell of
the Gymnosomatous larva and that of the Thecosomata being specially strik-
ing. This is a feature which points to a long period of pelagic life of the
adult, for the larvae of the Opisthobranchs also live in the sea. We might
therefore assume that the Gymnosomata are to be traced back to forms
resembling the ancestors of the Thecosomata, which only later underwent
the changes now found in their structure and development. We can hardly
regard as of much importance the apparent retention of a primitive feature
in presence of a small creeping foot in the Gymnosomata, since single
primitive characters may be retained in forms which in other respects are
highly specialised. It is also by no means certain that this character has
not been secondarily acquired.
We have felt justified in treating the Pteropoda separately from the
Opisthobranchia on account of the great deviations found in the structure of
the body. In so doing, we do not wish in any way to deny their relation to
forms like the Bulloidea and especially Gasteropteron. It is possible that
there may be even closer ontogenetic relationship to these forms than is at
present known. This would be the case if the ontogeny of a Cephalophoran
described by C. Vogt were really found to refer to Gasteropteron, as was con-
jectured by Gegenbaur (No. 128). This Veliger larva develops two fin-like
structures, and yet, in consequence of various other characteristics, is not
comparable to a Pteropod-larva. The conical shell with its transverse lines
of growth, further, resembles the shell of the Gymnosomata and would be
little suitable to an Opisthobranch. It is thrown off even within the egg-
shell. The view that the larva now under consideration belongs to Gasterop-
teron has been directly denied by Krohn (No. 58b) who regards another larva
as being that of Gasteropteron. We are not acquainted with any more recent
accounts of this very interesting larva which may be of great importance in
determining the view which should be taken of the Pteropoda.
E. Pulmonata.
The transition from the ontogeny of the Opisthobranchia to that
of the Pulmonata is afforded by Onchidium, a form which has already
been alluded to p. 133. This amphibious form, which lives on the
sea-shore, develops embryos with a large bilobed velum. The two
lobes are beset with long cilia, while small and delicate cilia are found at
the incisions between the lobes. This embryo thus greatly resembles
the Veliyer larva of the Opisthobranchia. Although the adult is shell-
less, the embryo has a coiled shell like that of a marine Gastropod.
DEVELOPMENT OF THE EXTERNAL POEM — PULMONATA. 1 75
The operculum, on the contrary, is wanting according to Joyeux-
Laffuie (No. 51) and the foot which, even in the Veliger stage, is
very large is also covered at its anterior and dorsal side with delicate
cilia. The shell is thrown off during embryonic life, and the velum
also degenerates within the egg-shell.
With regard to the absence of the operculum which, according to
Joveux-Laffuie can hardly be doubted, it should he pointed out
that this organ is as a rule not found in the I'ulmonates.
The marine Arnphibola, however, lias an operculum showing the usual
structure and position (i.e., lying posteriorly on the back of the foot, No. 66).
Unfortunately, this Australian form is little known ; a more accurate know-
ledge of its anatomy and ontogeny is very desirable. According to Semper
(No. lis, ii.. p. 100), the embryos of Auricula and Scarabus have opercula.
In Onchidium, after the shell has been thrown off, the mantle,
with the reduced pulmonary cavity, shifts dorsally and, with the
kidney, opens by a median aperture at the posterior end of the body.
The hitherto asymmetrical aims (lying on the right side) also assumes
a median position at the posterior end of the body. In some species,
the pulmonary, renal and anal orifices open through a common
aperture on to the surface of the body. The loss of the shell thus
leads to the acquisition of a secondary symmetrical position of the
organs, a phenomenon that may also occur in other slug-like forms
(as also in various < >pisthobranchs).
With regard to the further development of Onchidium, it need here
only be noted that the form of the adult is attained within the egg.
The Vaginulidae, forms usually placed near to Onchidium, no
longer possess, according to Semper and v. Jhering, either the fully
developed bilobed velum or the larval shell (Xo. 116), although the
spawn appears to have the same constitution as that characteristic of
Onchidium (p. 104). These forms would therefore appear more
adapted to a terrestrial existence, if the short statements as to their
development should be corroborated.
Onchidium and Vaijinulm are both opisthopneumonic, and this
fact, taken together with the other features of their organisation as
well as their ontogeny, suggests that they represent forms which,
from a condition like that of the marine Opisthobranchs, have become
adapted to a terrestrial existence. The classification of Onchidium
and Vayinidus among the Pulmonata which might, on account
of the peculiarities above mentioned, appear doubtful (Joyeux-
Laffuie), has been strengthened by the more recent observations on
176 GASTROPODA.
this subject (v. Jhering, No. 46 ; Simroth, No. 120).* Since the
I Teliger stage may still be found even among the undoubted Pulmon-
ates, although usually in a somewhat reduced condition, no object ion
can be made to this classification from the ontogenetic stand-point.
Their development, however, shows in an unmistakable manner that
we have to do with transitionary forms, a fact which is further con-
firmed by their manner of life, especially by that of Ondiidium
(p. 133).
The velum, it should be mentioned, is, according to Semper, well
developed in some tropical forms (Auricula, Scarabu*; No. 118), in
the same way as in Onchidiam (R. Bergh, No. 5, p. 175). Semper
assumes that the larvae of these forms swim about freely in the
sea. Since they, as already stated, also possess an operculum, they
bear a great resemblance to the Opisthobranch larvae. As a rule, the
velum is much reduced in the Pulmonates. These pass through the
invagination-gastrula stage, the manner in which this gastrula arises
being modified in many ways according to the varying amount of the
yolk. Thus the archenteron, in consequence of being composed of
the large, yolkdaden cells, appears at first as a massive structure
with a narrow lumen, but at a later stage widens out and becomes
a spacious sac. The originally narrow cleavage-cavity also gradually
widens out. The embryo is now spherical. Its animal pole is often
marked by the presence of the polar bodies ; at the opposite vegetative
pole is found the blastopore, which at first is wide, but narrows later
and usually becomes slit-like. It closes from behind forward, but,
apparently, a small anterior aperture may remain. At this point,
in the midst of an ectodermal depression, the mouth forms, and,
when the blastopore is retained, it becomes displaced somewhat far
inward by the stomodaeum to the point at which the stomach com-
mences (Fol, No. 33 ; Rabl, No. 91 ; Wolfson, No. 131).
The spherical or often somewhat ventrally flattened form of the
embryo undergoes some alteration in consequence of the appearance
of the shell-gland, the foot and the velum. The shell-gland arises
as an ectodermal invagination on the dorsal surface opposite the
mouth (Fig. 78). It may sink in so deep that it has repeatedly been
mistaken for the rudiment of the proctodaeum. It flattens out again
* [Plate (Z<><>1. Jahrb. Anat., Bd. vii., 1891) who has recently made a thorough
study of the anatomy of Onchidium, concludes that while these forms are
ti.if Pulmonates, they nevertheless show affinities with the Tectibranchiate
Opisthobranchs. He places the Onchidiidae and Vaginulidae as direct
derivatives of the primitive pulmonate on a branch quite independent of the
Stvlommatophora or Basommatophora. — Ed.]
DEVELOPMENT OF THE EXTERNAL FORM — PULMONATA.
177
later, secreting the shell in the usual way ; in Li max, however, the
shell of which is at first internal, the shell-gland is pouch-like and
becomes abstrieted from the ectoderm (Fol). A swelling of the body
behind the month indicates the position of the foot (Fig. 78). The
velum appears in the form of two transverse swellings (formed of
large, richly vacuolated cells) in front of the mouth, which run as
bands round a large part of the anterior body, but for a time do
not meet, or else, as in Planorbis, in consequence of the very much
reduced condition of the velum, never completely unite (Fig. 78, v).
At this stage, we may, with Ray Lankester, consider the embryo
as equivalent to the Trochophore ; occasionally, as in Llmnaea, even
Fig. 78. — Planorbis embryo, seen from the side (after Rabl). air, eye; m, mouth;
md, enteron and digestive gland (large cells); mes, mesoderm; ot, otocyst; r,
radular sac: s, shell: sd, shell-gland; sp, apical plate: wti, primitive kidney; v.
velum.
the external form of the Trochophore is preserved, a large prc-oral
portion of the body being marked off from the posterior portion b}-
the velum (Bay. Lankester, Fol). A thickening at the pre-oral
pole denotes the apical plate. That the bilobed character of the
velum so characteristic of the 1 religer larva is found here also is due
to its mode of origin. As a rule, not only the Veliger stage but the
Trochophore stage as well is much reduced, the principal features of
the latter, however, are still to be found.
At the stage which more or less corresponds to the Trochophore,
the alimentary canal consists of a stomodaeum from which a radular
sac soon grows out ventrally (Fig 78, r) and the still undivided and
N
178 GASTROPODA.
exceedingly large archenteron (mil). Some of the cells of the latter, in
consequence of the albuminous matter which has been brought from
without through the mouth into the lumen of the intestine, have a
swollen- appearance (Figs. 70-80) ; others, however, which lie pos-
teriorly and ventrally are smaller, indeed, through more active
division, they may even be specially small. They form a diverti-
culum of the entoderm which is directed backward (Fig. 78) and
represent the rudiment of by far the greater part of the enteron.
The cells containing albumen, which continue to increase in size, pass
over into the formation of the liver later. At first the intestinal
cavity appears bounded partly by a large-celled and partly by a
small-celled epithelium. The posterior diverticulum of the enteron
comes into contact with the ectoderm in the ventral middle line,
behind the foot. This part at first bulges somewhat outward, form-
ing the anal prominence. Later on, the entoderm-diverticulum here
fuses with the ectoderm to form the anus.
The resemblance of the stage just described to the Trochophore
stage is heightened by the presence of a paired primitive kidney,
which, in the fresh-water Pulmonates, has a very characteristic
origin and shape (Figs. 78-80, uri). Even at an early stage, a
remarkably large cell can be seen on each side below the dorsal part
of the velum ; these two cells yield the pi'incipal constituents of the
primitive kidney, and have been claimed as velar cells which have
entered the body-cavity (Wolfson), this view being no doubt sug-
gested by the vacuolated character of the velar cells as well as by
the condition of those Prosobranchs in which complexes of ecto-
dermal cells which are certainly excretory are apparently closely
related to the velum. This view can, however, hardly be correct,
and, taking into consideration the usual method of formation of the
primitive kidneys, we prefer the view of Babl that these large cells
are to be derived from the mesoderm.* They lie at the posterior
part of the mesoderm-bands which are already disintegrating. In
each of these cells, a cavity which at first resembles a vacuole ap-
pears, lengthening as soon as the cell itself lengthens. The cell then
becomes bent and forms the principal part of the primitive kidney,
the canal of which is thus intra- cellular in its origin (Ganin, No. 35 ;
Eabl, No. 91 ; Wolfson, No. 131). The large cell yielding the
primitive kidney is joined by a few of the adjacent mesoderm-cells
and the canal, by becoming connected with the ectoderm, opens
* [See footnote, p. 179.— Ed.]
DEVELOPMENT OF Till. EXTERNAL FORM — PUL.MONATA. 179
externally. The apertures of the two kidneys lie at the two sides of
and behind the velum. The inner end of the primitive kidney is
usually regarded by authors as communicating with the primary
body-cavity by a ciliated aperture.* In the terrestrial Pulmonates
this has been maintained with certainty for Helix (Acavus) by
P. and F. Sarasin (No. 10l>) and Jourdain, as well as Meuron
(Nos. 50 and 75), arrived at the same result.
The primitive kidneys of the terrestrial Pulmonates, which were
early recognised by O. Schmidt and Gegenbaur, are somewhat
differently constituted from those of the aquatic forms. They also
ha\c the form of bent tubes opening externally through wide aper-
tures in front of the border of the mantle, but they are composed
of a large number of cells arranged like an epithelium, none of which
are distinguished by their special size (Jourdain, Meuron, Sarasin).
De Meuron considers that, in Helix, the primitive kidney arises chiefly
from the ectoderm, but holds also that the innermost part may be derived
lrom the large mesoderm-cells. But since these latter, in the aquatic Pul-
monates, yield the principal part of the primitive kidneys, the derivation of
these organs from the mesoderm appears more probable. We need not,
however, exclude the supposition that, as in the primitive kidneys of the
Prosobranchs, an ectodermal invagination takes part in the formation of
the peripheral part and that this latter, in terrestrial Pulmonates, is specially
extensive.
At the time when the primitive kidneys attain their full develop-
ment, the external form of the embryo also undergoes further altera-
tion. The shell-gland begins to lose its pouch-like form and gradually
flattens out. The ectodermal epithelium belonging to the shell-area
still appears formed of columnar cells. Over this area lies the shell
* [v. Erlanger (No. VII.) has since described the detailed structure of the
larval kidney in Planorbis and Limnaea ; he finds a specialised ciliated cell
(the funnel-cell) which puts the tube into communication with the body-cavity,
and then a long tubular segment containing a flagellum and a terminal por-
tion which opens on to the exterior, this latter portion Erlanger thinks may
be ectodermal in the Euthyneura, while the remainder is mesodermal. In
the Pulmonata he finds a swollen ampulla at the junction of the two seg-
ments. The development of this organ has been more recently investigated
by Meissenheimer (No. XVII.), and this observer maintains that, in Limax,
the primitive kidney is wholly ectodermal, aud here he is at variance with most
other observers. As he also maintains that the heart and definitive kidney
similarly arise from a common ectodermal rudiment, we think that his views
require further confirmation before we can accept them. Meissenheimer (No.
XVIII.) has also given a most elaborate account of the structure of this organ
in which he differs from Pan. anger in one important respect, viz., he is un-
able to find any opening into the body-cavity and thinks that Erlanger
mistook a large vacuole which is invariably present in the end-cell for an
opening. — Ed.]
180 GASTROPODA.
which has now become cap-like. The margin of the shell seems
buried in a groove, a swelling of the ectoderm, the margin of the
mantle, having formed here. The whole embryo has somewhat
lengthened, and the foot stands out more distinctly (Fig. 79).
The foot in Limnaea, which at first appears as an unpaired swelling, is
said to assume a bilobed form (Ray-Lankester). Such a bilobed foot seems
often to occur among the Gastropoda. We have already met with it in
Succinea, Patella and Vermetus (p. 132). Fol also observed this later develop-
ment of the bilobed form in the foot of Limnaea, as well as in Planorbis and
ma.
ere,
i
a* / .
au.
/
y-J'
ot>
';•
/
Pig. 79. — Older embryo of Planorbis, seen from the side (after Rabl). au, eye;/,
foot ; ma, margin of the mantle ; md, enteron and digestive gland (large cells) ;
at, otocyst ; pg, pedal ganglion ; r, radular sac ; s, shell ; t, tentacle ; un, primitive
Ancylus, though in these last two animals it was less striking. Ray Lan-
kester compares this to the transformation of the foot into the paired fin in
the Pteropoda.
The outgrowth of the body-epithelium to form the foot causes a
considerable enlargement of the ventral portion of the inner cavity
of the larva, and a similar cavity is produced pre-orally by the dilata-
tion of the part which is encircled by the velum. A similar process
has already been met with in the Prosobranchia (p. 150). The anterior
swollen part of the embryo is known as the cephalic vesicle and the
DEVELOPMENT OK THE EXTERNAL FORM — I'ULMONATA. 181
wide space as the cephalic cavity. Special attention has been directed
to this part in consequence chiefly of the pulsating movements which
may occur here, a peculiarity also found in the nuchal and the pedal
regions of the embryo.
It has repeatedly been stated that certain regions of the body-covering,
those to which a large number of niesoderm-cells became attached, carry on
contractions which sometimes follow one another with considerable regularity,
this last fact having led to their being called " larval hearts." The circulation
of the body-fluid is, in any case, promoted by these contractions, but it seems
doubtful whether they should be described as actual pulsations. Sometimes
the movements that thus occur are somewhat irregular, and Rabl found that,
occasionally, contraction of one part of the body is followed by extension of
another part, but we cannot consider this to be regular rhythmical move-
ment. The embryo moves in consequence of these contractions. It is well
known, however, that Gastropod embryos are able in addition, in consequence
of their rich ciliation, to rotate within the egg-envelope.
Since the embryo, by taking in the albuminous fluid contained within the
egg-shell, feeds independently and also has a circulation of its own and special
excretory organs, the velum may serve as a respiratory apparatus, this func-
tion being also exercised by it ifi addition to its locomotory function in the
free-swimming larvae. In the embryos of terrestrial Pulmonates, a special
respiratory organ develops, the caudal vesicle (podocyst), which will be further
described below.
The very large apical plate of the embryo has considerably thickened
and has become bilobed. According to Rabl, the cerebral ganglion
is derived from it, though in other Pulmonates the formation of this
ganglion has been thought to arise differently (p. 191). At the
posterior end of the "apical plate " the eyes arise as ectodermal pits.
Two large superficial prominences, which soon become conical, arise
laterally to the optic vesicles and represent the rudiments of the
tentacles. Both eyes and tentacles belong to the pre-oral section,
whereas the otocysts arise behind the velum (Figs. 79, (SO au, f, ot).
Up to this point, the embryo is fairly symmetrical in shape, but
this symmetry is disturbed chiefly by the further development of
the shell which grows towards the right more strongly than towards
the left (Fig. 80). The edge of the mantle, which now bulges out
more than before, is of course also affected by this unequal growth.
The anus is pressed out of its median position to the right. It is
evident from this that processes occur in the later development of the
Pulmonates similar to those already met with in the metamorphosis
of other Gastropods.
As the mantle extends further, its growth takes place more rapidly
on the right than on the left side. In front of the anus an indenta-
182
GASTROPODA.
tion forms which at first is shallow but soon becomes deeper ; this
is the rudiment of the respiratory cavity which continues to widen
and thus comes to include
md. v.
ma^
aw.
Fig. 80. — Older Planorbis embryo, seen from the
back (after Rabl). au, eye ; eg, cerebral ganglion ;
/, foot ; ma, edge of the mantle ; mrf, enteron
and digestive gland ; [>g, pedal ganglion ; s, shell ;
t, tentacle ; un, primitive kidney ; v, velum ;
vd, stomodaeum.
the anus and the aper-
tures of the adult kidney.
This cavity itself opens
externally only through
a narrow aperture, the
respiratory aperture,
which lies rather far-
forward on the right
side of the body.
The formation of the res-
piratory cavity has also been
viewed in another way ; viz.,
as a fusion taking place
between the margin of the
mantle and the body, only
a small aperture being left,
wbich, as respiratory aperture, leads into the greatly deepening cavity. In
this way, the respiratory cavity is shown to be the transformed pallial or
branchial cavity. In the Basommatophora this is indisputable, as a gill
is in some forms found in the cavity (Amphibola). The respiratory cavity
in the Stylommatophora has, on the contrary, been regarded as not homo-
logous with the branchial cavity, but rather as the ureter transformed
into a respiratory organ. On this account v. Jhering termed the terrestrial
Pulmonates the Nephropneusta, thus distinguishing them from the aquatic
Pulmonates, which he named the Branchiopneusta (Nos. 45 and 46.) We
ourselves do not find anything in the manner of formation of the respira-
tory cavity in land Pulmonates to justify so different an interpretation of it.
The mantle-cavity in the Prosobranchia may also at first, as here, arise appar-
ently in the form of an ectodermal depression. The homology between the
respiratory cavity of the land Pulmonates and that of the water Pulmonates,
which in itself is so probable, is further supported by the fact that in some of
the former (Testacellidae, Plate, No. 89) a sensory organ is present in it which
corresponds to Spengel's olfactory organ found lying near the gills in the
mantle-cavity of other Gastropods.
Towards the end of that period of embryonic life during which the
embryo may be compared with the larva of other Gastropods, the
sinuses in the head and the foot which gave rise to the embryonic
circulation above described undergo gradual degeneration. In the
same way the primitive kidney disappears and the permanent kidney
functions in its stead.
The final form of the animal is reached by the growth of the parts
DEVELOPMENT OF THE EXTERNAL FORM PULMONATA.
183
now present. The respiratory cavity and the edge of the mantle
extend more to the left, the shell taking the same course. The head
becomes more distinct, rising up from the foot, which, in its turn has
increased considerably in size and has approached nearer its definitive
form. The velum has disappeared, a portion of it, according to
Ray Lankester, giving origin to the labial palps (p. 133). This
latter view seems quite in keeping with the position of the velum,
but is set aside as improbable by Fol and is directly refuted by
WOLFSON.
tiu
y\m.
Fig. 81. — Embryo of Helixpomatia seven days old. seen from the side (after Fol). ".
anus;/, toot: Kbl, cephalic vesicle; m, mouth; mil, enteron and digestive gland;
r, radular sac ; sd, shell-gland ; mi. primitive kidney.
The shell is still cup-shaped, but is already asymmetrical. Further
unequal growth on one side leads to coiling both of the shell and the
visceral dome.
<)ur account has, so far, referred chiefly to the development of the
freshwater Pulmonates, especially to that of a few forms which have
been particularly carefully investigated, such as IAmnaea and Plan-
vrUs. These latter have been described in detail by Ray Lankester
(No. 63), Rabl (No. 91), Fol (No. 33), and Wolfson (No. 131) to
whose descriptions we must refer the reader for further details. Fol
184
GASTROPODA.
has also included various other fresh-water Pulmonates as well as
terrestrial Pulmonates in his comprehensive researches. These latter
forms, which had already been studied by Gegenbauk, differ from
the aquatic Pulmonates in some points of their development and
therefore require separate treatment.*
The ontogeny of the stylomatophorous terrestrial Pulmonates
is characterised by the development of exceedingly large provisional
organs, viz., the cephalic and pedal vesicles. These larval organs
appear early. At a stage which corresponds somewhat to the
Fig. 82. — Embryo of Helix pnmatia, ten days old, seen from the side (after Pol), a,
anus; ,/', foot; Kbl, cephalic vesicle ; ///, larval heart ; m, month ; md, enteron and
digestive gland ; r, radular sac ; sd, shell-gland : un, primitive kidney.
Trochophore stage, the embryos (<>!' Limax, Avion, Helix, Glausilia)
are distinguished by the great swelling of the pre-oral section of the
body. At the stage of which we speak, this cephalic vesicle is so
large as almost to eclipse the rest of the embryo. At a rather later
stage also (Fig. 81), the cephalic vesicle (kbl) is still very large, but
*[See also the more recent works of Holmes (No. XIII.), Kofoid (No. XIV.),
Meissenheimer (No. XVII.), Schmidt (No. XX.) and Wierzk.tski (No. XXVII.),
These deal for the most part with the cleavage and cell-lineage. Meissen-
heimer's researches on Ziimax, however, are carried further and should be
consulted in connection with the development of the Stvlommatophora. —
Ed.]
THE ONTOGENY OF THE STYLOMMATOPHOKA.
I Ho
the foot now bulges out and also commences to swell up into a vesicle
Little now remains of the Trochophore shape. At a stage somewhat
younger than that depicted in Fig. 81, a slight vestige of the velum
is still to be found in two transverse ciliated ridges which lie on
either side of the mouth and run towards the shell-gland. These,
however, do not extend up to the mouth, and soon disappear. In
Arion and Li, mix, no traces of the velum are to be found (Fol).
These embryos, like those of the aquatic Pulmonates, are able to
rotate within the egg, being covered with cilia.
'
-
d.
1LTI
•fid-'
Fig. 83. — Older embryo of Limax WMxiiniis, seen from the side (.after Fol). ">>, eye;
eg, cerebral ganglion; d, yolk-material ;/, foot ; It, labial palp ; ma, mantle-fold;
md, enterou and digestive gland ; ol, upper lip ; pd, podocyst ; pg, pedal ganglion ;
rs, radular sac ; s, shell ; t, tentacle ; un, primitive kidney.
The position of the different organs of the embryo can be under-
stood most easily by reference to Fig. 81. The oesophagus is followed
by the enteron from which the digestive gland composed of large
albumeniferous cells is already becoming differentiated, posteriorly
the enteron is lined by smaller entoderm-cells. The anus lies behind
the pedal swelling, and behind it again, marking the dorsal side, is
found the shell-aland. A pit lying near the mouth represents the
rudiment of the radular sac which, according to Fol, arises in the
stomodaeum, which lias not yet fully sunk in, and is thus near the
oral aperture, but is soon drawn into the buccal cavity. Near the
186
GASTROPODA.
enteron can be seen the tube of the primitive kidney which is as yet
unbent and which, according to Fol, opens outward at the posterior
base of the foot. Almost in this region, but somewhat behind the
foot, lies an organ described by Fol as the larval heart.
The so-called larval heart (Fig. 82, Ih) consists of a bulging of the ectoderm
with which numerous mesoderm-cells become connected. This specially
differentiated part of the covering of the body which, when the mantle-
cavity forms later, is drawn into it and thus comes to lie more to the right,
carries on regular pulsations and is regarded by Fol as an organ for promoting
the embryonic circulation. It thus belongs to the category of larval hearts
which have already been alluded to (p. 152).
While the cephalic vesicle in the later stages decreases in size, the
foot lengthens considerably. At first it is cylindrical, but it soon
spreads out more and more and now becomes a massive club-shaped
organ (Fig. 83), which is known as the caudal vesicle, and more
recently has been named the podocyst (Jourdain, Sarasin). As it is
richly supplied with mesoderm-cells which become applied to its wall,
it is capable of contraction and carries on rhythmical movements which
alternate with those of the cephalic vesicle. It is evident that this
large vesicular swelling is a circulatory or respiratory apparatus and
it may be that it also serves for nutrition, since diosmotic processes
take place in it.
The podocyst is specially large in the embryos of various species of
Helix (Gegenbaur, v. Jhering, Fol, Sarasin). It here spreads
out laterally, and thus assumes the form of a broad plate which,
towards the end of the " larval period," lines the whole of the inner
cavity of the egg-shell. P.
and F. Sarasin, in describing
a Helix {Acavus Waltoni, Fig.
Si) found in Ceylon, show that
the podocyst covers like a cap
nutr.
the shell of the very large
embryo in which several coils
have already developed. In this
form also, in which the pedal
vesicle is specially highly de-
veloped, pulsating movements
were perceived in that organ.
When it has reached its highest
development, two wide canals within the foot start from the vesicle,
one passing to the brain along the ventral side and the other running
Fig. 84. — Embryo of Helix (Acavus)
Waltoni, seen from the side (after I'. and
F. Sarasin). Icb, cephalic vesicle; ml,
oral Lobes; «"'•, mantle-swelling (collar) ;
//
"---'' •• <\ .«,».V»v
"'*' ---I i ' ■ *""
21
Fk;, 90.— Eyes. — A, Patella rota; />'. Trochus magus; <', Turin, creniferus ; 1>.
Murex brandaris (after Hilger). bg, connective tissue; ep, ectoderm; gl, vitreous
body ; I, lens ; ,i , optic nerve ; /<, pigmenl ; r, retina ; st, rods.
The ontogeny of the Gastropod eye is of great interest in so far as
it may, at some of its stages, be compared with the adult condition
of the eye in various forms. Patella, for instance, has eyes which are
placed in the usual position, but which arc mere pit-like depressions
of the surface (Fig. 90 A). In llalioti.% Trochus, etc., the pit is deeper
THE FORMATION OF THE OKGANS — THE SENSORY ORGANS. l!)i)
and becomes a vesicle which, however, remains open (Fig. 90 B). Its
lumen is filled with a strongly refractive gelatinous mass (. 85). [In most Diotocardia the
optic vesicle is open, but in the specialised Helicinidae and
Neritldae (the Gymnopoda of Fischer) and in the Turbinidae it is
closed as in all the Monotocardia.]
The first-named Prosobranchs are held on other grounds to be
primitive forms, and the simple structure of the eye seems therefore
probably a primitive condition, if this supposition is correct, we
should here see with special clearness the gradual development of
the optic organ up to its present level.
According to Carrikre (No. 22), in eases where the eyes are regenerated,
their formation takes place in the same way as when they arise ontogene-
bically. The ectodermal epithelium is thus at a later time also capable of
giving rise to the sensory organs.
The otocysts, which are specially distinct in the larva, and the
origin of which has already been alluded to several times (Figs. 55,
59, 65, 72, T^t), appear as depressions of the ectoderm on either side
of the pedal rudiment, near the pedal ganglion, with which, however,
they do not come into any closer relation as they are innervated from
the brain (Lacaze-Duthiers). When cut oft' from the ectoderm,
these walls are still formed of long cylindrical cells which flatten
later; hut, for a time, the anterior and ventral part of the vesicles
still remain thick. From this part of the wall, the otolith or otoliths
(otoconia) are secreted : these structures become detached from the
wall and rest upon the sensory hairs which have arisen on the
cells.
Spengel's (olfactory) organ (osphradium) only develops at a later
stage (l'uhhlimt). It arises as an ectodermal thickening composed
of several layers of cells. Where, as in Paludina, pits are found in
tin organ, these are caused by depressions in the thickened ectoderm
(v. Erlanger).
The pectinate condition of this organ, which is found in many Gastropods,
arises in a similar way. The organ was originally paired and lay neai
the gill, as may still be the case in Zygobranchiate Diotocardia. Where
it is single, as in the Monotocardia and the Kuthyneura, this is in all cast s
connected with the asymmetry caused by the torsion of the visceral mass.
200
GASTROPODA.
D. The Pedal Glands.
In the larvae of various Gastropods, e.g., Nassa (Figs. Gl D and E, 63),
Vermetus, Murex, Firoloida (Fig. 65), etc., a deep tubular or sac-like ectodermal
depression has been described in the foot; this shows great agreement in
position with the pedal gland found by Kowalevsky in the embryos of Chiton.
Such a rudiment is perhaps also present in DentaHuin. In Nassa, this gland
forms a rather long tube, and in Murex it has a similar form (Bobretzky,
No. 11) ; in Firoloida, it is said to be much shorter and bilobed (Fol, No. 31,
Fig. 65, fd.). Salensky describes, in Vermetus, the formation of two ectodermal
invaginations in the foot, the one lying at the anterior and the other at the
posterior end. The canals lengthen inwards and fork, so as to yield the
glandular portion. Various glands are knowji in adult Gastropods also lying
one behind the other in the sole of the foot (Carriere, No. 21). The connec-
tion of the rudiments we have just described with these glands does not as
yet appear to be clearly demonstrated. It is well known that various
glands also occur at the anterior end and in the sole of the foot in Lamelli-
branchs which have'been homologised with the anterior and posterior pedal
glands of the Prosobranchia (Barrois, No. 3), but whether such a homology is
correct still seems doubtful.*
E. The Alimentary Canal.
The Stomodaeum first appears as an ectodermal depression in
which can soon be recognised a ventral outgrowth, the radular sac
(Figs. 53, p. 127, 78, p. 177 and other figures). This sac sometimes
appears even before the stomodaeum is completely invaginated and
consequently lies near the aperture of invagination, as in Helix
(Figs. SI and 82, p. 184). When the radular sac lengthens, it
undergoes dorso-ventral flattening. Its lateral margins then bend
upward so that it assumes the form of a channel, the dorsallv directed
cavity of which is filled with a mass of connective tissue. The wall
of the channel is formed of the upper and the lower epithelium, the
latter taking the principal part in the formation of the radula.
The first indication of this organ is found early in the form of a thin
cuticle in the radular sac. The formation of the radula, an organ
which has been studied in the adult by Rossler (No. 95), and Ruckeb
(No. 96), and others, takes place in the following way: The teeth
themselves are secreted by the cells which lie ventrally at the blind
end, while the basal membrane upon which the teeth are borne is
*[The pedal glands may attain enormous development in the Pulmonata;
this is especially noticeable in Natalina, where the gland takes the form of a
very large tube bent on itself and extending along the greater part of the foot.
The gland either opens between the head and foot, as in Heli.r, or on the
postero-dorsal surface of the latter, as in Helicarion. — Ed.]
THK FORMATION OF THE ORGANS — THE ALIMENTARY CANAL. 201
yielded by the lower epithelium (Fig. 91 ..1). The large groups of
tooth-forming colls (odontoblasts) form a kind of cushion or bed upon
which the teeth are modelled (Fig. 91 A and A'). In the shape of
this cushion, the future form of the tooth is already shown. In the
Opisthobranchia and the Pulmonata, a special differentiation occurs,
only a few (four to five as seen in longitudinal section) * very large cells
undertaking the formation of one tooth (Fig. 91 11, ocf) ; the most
anterior of these large cells is said to yield the part of the basal
membrane that underlies the tooth now in course of formation.
Pig. 91. .1 and B, Longitudinal sections through the radular sac of Octopus
vulgaris (A) and Helix memoralis (JS) (after Ro'ssler). Imi, basal membrane; <>d,
odontoblasts ; o, ',j, upper epithelium ; srm, sub-radular membrane ; », ep lower
epithelium : ".. teeth.
The tooth thus produced fuses with the basal membrane and with
the prolongation of the basal part of the last tooth (Fig. 91 B).
When a tooth is thus completed, this cell-group undertakes the
* [There are in reality eight to ten of these large cells concerned in the secre-
tion of each tooth, the cells being arranged in two parallel series, so that, in a
longitudinal section, like that shown in Fig. 91, only one row is seen at a time.
It is probable that the three most posterior pairs of these odontoblasts secrete
the main body and hook of the tooth, the next transverse pair secreting the
base, while the most anterior pair secretes the sub-radular membrane. — Ed.]
202 GASTROPODA.
formation of the next tooth of the same longitudinal row. The
number of teeth in a transverse row corresponds to the number of
groups of odontoblasts. The formation of the radula is, however,
not altogether completed by the processes just described, for the
upper epithelium yields a viscid fluid secretion which forms an
enamel-covering to the teeth. The gradual shifting forward of the
newly-formed teeth to replace those which are continually being
worn away in front, is brought about to a great extent by the
growth of the surrounding tissues, and is no doubt also caused by
the action of the muscles at the anterior part of the odontophore
(Rossler).
The radula appears to form in other Molluscs that are provided
with it (Cephalopoda, Fig. 91 A, and Amphineura) in just the
same way as in Gastropods : it will not, therefore, be necessary to
describe it in detail again.
The salivary glands arise somewhat late as diverticula of that
part of the stomodaeum which lies in front of the radular sac.
The enteron, in various Gastropods, arises to a certain extent in
a different way, as the accumulation of yolk or of a secondary
nutritive mass at various points of the gut frequently retards its
development and may even, where the mass is very voluminous,
strongly influence the manner of formation of the intestinal canal.
In many cases, however, the formation of the enteron takes a very
simple course, the invaginated entoderm-vesicle increasing in size by
the continuous division of its cells, fusing anteriorly with the stomo-
daeum and growing out posteriori}' into a conical terminal section
which becomes connected with the ectoderm to form the anus. It
has already been explained that the posterior section of the enteron
may at first run straight back, but may later bend forward to the
right, and that this is connected with the acquisition of asymmetry.
The coils made by this section of the gut as it lengthens are not of
essential importance and need not therefore be specially described.
There are, however, other important alterations brought about by the
deposition of nutritive masses in the enteron. This process of deposi-
tion takes place in a very simple manner in Paludina (Butschli).
The ventral part of the entoderm here becomes even at early stages
especially large through the increase in size of the cells and the
deposit in them of drops of secondary yolk (Figs. 57, 58 and 59, p.
137, etc.). This thickening of the wall of the enteron is evidently
due to the absorption of the surrounding albumen ; this albumen being
received especially into the ventral entoderm and deposited there. At
THE FORMATION OF THE ORGANS — THE ALIMENTARY CANAL. 203
;i later stage, the whole of the sac like anterior part of the enteron is
affected by these deposits, which, however, arc always greatest on
the ventral side. The dorsal and anterior part, with which the
oesophagus becomes connected, is marked off into a sac-like stomach,
while the part that lies vcntrallv and more posteriorly, and which
contains by far the largest amount of deutolecithal constituents,
yields the liver. 'The latter, originally spherical, soon becomes lobate.
LiEYDIG describes the gradual development which commences with a
few large lobes; then, by subdivision of these, an increasing number
of small ones arise, until, when the embryo is ready for birth,
continued division has led to the formation of numerous long
follicles.
It has been observed in most cases that those parts of the entoderm
that are laden with nutritive substance pass over into the liver or
else are connected with its formation ; it appears doubtful to us
whether this is invariably the rule, since these parts vary greatly in
the position they occupy in the enteron, as will be shown later.
The accumulation of nutritive material in the ventral entoderm is
still more striking in the Heteropoda than it is in Paludina. Fol,
in connection with the Heteropoda, speaks of a ventral nutritive sac
formed of immense, greatly swollen cells which is abstricted from the
stomach so as to become the rudiment of the live)', its glandular
character being soon proved by the development of several lobes. A
ventral nutritive sac is also found in the later stages of Limnaea :
hut it is expressly stated that this does not take part in the forma-
tion arts give rise to the
posterior portion of the
intestine winch takes the course already described. The small-
celled portion of the entoderm spreads out further at a later
I'n.. 92.— .4 and B, embryos of BytMnia tentaculata
at different stages (after v. Erlanger). a, anus ;
eg, cerebral ganglion ; /, foot ; 1*1. posterior lobe of
the liver ; m . mouth ; mes, mesoderm ; nig, stomach ;
//. rudiment of the kidney; op, operculum; p, peri-
cardial sac; /«>, pericardium; r, radular sac; s,
shell; t, tentacle ; v, velum; /•/. anterior hepatic
sac.
THE FOKMATION OF THE ORGANS THE ALIMENTARY CANAL. 205
stage, and the albuminiferous cells seem to be pressed more to
the left (Fig. 78).
The complexes of nutritive cells arc said to be dorsal in position in
the land Pulmonates also, and the direct rise of the liver from them
has been described (JouKDAiN, No. 49). It appears, however, from
the figures of Pulmonates, especially of the land-form before ns, that
the large-celled mass extends well to the ventral side of the stomach.
so that there is here perhaps after all a near approach to the con-
Fr<.. (.t:;. .1-'', sagittal sections of tin- embryos of Fusus at various stages (after
Bobretzky). d, yolk; /, toot; kb, cephalic vesicle; /, liver; m, mouth: mil,
entemu ; mg, stomach ; s, shell ; sd, shell-gland ; vd, stomodaeum.
ditions described above. The fact that the intestine, the stomach
and the liver are not clearly marked, makes it difficult to ascertain
the exact relation of these parts which is further complicated by
a frequent displacement of these organs. In Bythinia, the intestine
arises from the posterior part of the conical enteron, while the larger
part gives rise to the liver and stomach (P. Sarasin, v. Erlanger).
The liver appears in the form of a very wide anterior and a smaller
206
GASTROPODA.
posterior outgrowth (Fig. 92, vl, hi), while the stomach {mg) arises
from a small dorsal part of the enteron lying between these two.
Into the stomach open the oesophagus, the intestine and the two
hepatic sacs.
In the cases so far considered, the enteron has at first a sac-like
form : this, however, soon becomes differentiated by the concentration
of the nutritive yolk or by the absorption of albumen by the cells in
one part of the enteron. In other cases, however, the accumulation
of food-yolk in the entoderm is so great that the sac-like rudiment of
the enteron is not able to develop at once. In Fusus, for instance,
according to Bobretzky, at a time when the oesophagus, the shell-
gland and the mesoderm are already well developed, the entoderm
consists of only a few large cells which are to a great extent filled
a.
3$.
fiG- 94. — Two transverse sections of an embryo of Fusus, A, through the foot; />, a
more posterior section (after Bobretzky). d, yolk ; ect, ectoderm ; /, foot ; I, liver ;
mil, entoderm lining the stomach ; mes, mesoderm ; <>t, otocyst ; pg, pedal ganglion ;
■.. sub-velar cells.
with yolk, having a small protoplasmic portion directed towards the
mouth (Fig. 93 A). At this point, the division of the macromeres
gives rise to new entoderm-cells which are much smaller and soon
rise up from the macromeres, tints forming the rudiment of the
midgut, especially that of the stomach, which then, through the
formation of a posterior conical process, gives rise to the intestine
(Fig. 93 A and B, md). The increase in number of the entoderm-
cells is continued at the expense of the food-yolk, which is now
pressed further back. While, ventrally, the stomach becomes more
distinctly marked oft' (Fig. 62, p. 151 and 93, mg), the recently
developed dorsal parts of the entoderm become filled with deuto-
lecithal spherules and thus have a glassy appearance like the
THE FORMATION OF THE ORGANS — THE ALIMENTARY (ANAL. 207
albuminous cells of other Gastropods described above. The yolk-
mass, which is still very large, limits directly the lumen of the
entoderm-vesicle (Figs. 92 and 93). This latter is already found to
be partly rilled with disintegrated yolk-substance (Fig. 62 B), this
being taken up by the large entoderm-cells, which, according to
Bobrktzkv, represent the rudiment of the liver (Figs. (52, 93 and
'.'!./). The large-celled "hepatic vesicle" may be said to form the
Fig. 95.— A-D, longitudinal sections through embryos of JVassa mutabilis at different
ages (after Bobketzkv, from Balfour's Text-book). /-//, blastopore ; ep, ectoderm :
/. rudiment of foot; hy, entoderm; in, epithelium of the enterou ; m, mesoderm;
sg, shell-gland ; st, lumen of the enterou.
dorsal and posterior part of the entoderm-sac, if the rudiment of the
intestine is left out of consideration (Figs. 93 and 94, md). It
occupies the left side of the body while the food-yolk is pressed more
to the right. From the sections given in Figs. 93 and 94 a good
idea of the relative positions of these parts and of the stomach may
be gained. The food-yolk still directly limits the lumen of the
intestine, but is gradually absorbed as development advances.
208 GASTROPODA.
A still further specialisation of the enteron along the lines seen in
Fusus is found in the egg of Na**a which is still more richly supplied
with yolk. The formation of the germ-layers in this egg has already
heen described (p. 116). The entoderm is found here as a slightly
developed single layer of cells on the ventral side of the embryo.
The stomach and rudiment of the intestine appear when the massive
food-yolk which, at first, presses closely upon the entoderm, separates
from it (Fig. 95 C and D). Owing to this origin of the enteron, its
lumen is here also directly bounded on one side by the yolk, which,
even at a later time, is very extensive (Fig. 61 D and E, p. 150),
and fills the whole of the posterior part of the body. The intestine
still appears open towards the yolk-mass (Fig. 63, p. 152) and, in its
farther development, no doubt follows the same course as that of
Fusus.
The nutritive substance is, as we have seen, stored up in various
parts of the entoderm, and seems frequently to influence the develop-
ment of the liver. It is inherently probable that the liver originates
from definite parts of the entoderm, always appearing in the same
region of the enteron, but this process may be modified through the
various ways in which the nutritive mass is deposited. From the
different conditions found, we seem to be able to conclude with some
certainty that the whole of the anterior part of the enteron was
originally specially utilised for the storing of the nutritive material.
The anus forms in most cases through the direct fusion of the
entodermal intestine with the surface of the body, though some
authors (Wolfson, No. 131 ; P. Sarasin, No. 101 ; Jourdain, No.
49, etc.) speak of the development of a proctodaeum. As the latter
is said to occur in other Molluscs, e.g., Chiton, Teredo, Eniovalva, and
as it is found in the Annelid larvae, the structure of which is
remarkably similar to that of the forms we are now considering, its
presence cannot be regarded as a priori improbable. In by far the
greater number of Molluscan embryos, however, a proctodaeum is not
developed.
F. The Gills.
The gills have been found to develop in some Prosobranchia as
consecutive prominences on the ectoderm. These prominences corre-
spond to single branchial leaflets. Mesoderm-cells enter into them
and form a septum in each leaflet. The gill commonly seems to
appear only after the mantle-cavity has formed, arising within the
latter (Figs. 61, k, p. 150, and 99 and 100, p. 214), but occasionally it
THE DIFFEBENTIATION OF THE MESODEBM-BUDIMENT, ETC. 209
may be Found at an earlier period on the surface of the body, as in
Fasciolaria (Osbobn, No. 81).
Bipectinate plumose gills, a pair of which is found in Fissurella and Haliotis,
are considered as the mosl primitive, and we may assume that the single
monopectinate gill of the Monotocardia is to he derived from these, one of
the gills (originally the left) disappearing through the shifting of the pallial
complex while the other (originally the right), by fusion with the inner wall
of the mantle-cavity, loses one of the rows of its leaflets.* So little attention
has as yet been bestowed on I be development of the gills in the Gastropoda
that it is impossible to confirm by their ontogeny this view which in any
case is very probable. The derivation of the single gill from the double gill is
also plausible because the former is found not only in the most primitive
Gastropods, but also in the Amphineura, the lowest Lamellibranchs and the
Cephalopoda, i.e. in all the principal divisions of the Mollusca.
G. The Differentiation of the Mesoderm-rudiment, the
Development of the Body-cavity, the Nephridial
and Circulatory Systems.
Apart from the primitive kidneys (pp. 136, 178) little has yet
been recorded of the formation of the mesodermal organs. We have
already shown that the mesoderm appears as a bilateral rudiment
which is soon found in the form of two cell-masses, comparable to
the mesoderm-bands of the Annelida, at the posterior end of the
body near the blastopore (Figs. '.Mi, 48, 51, 52, 56). The distinctness
of these two cell-masses varies in the different forms; they may also
he considerably reduced in size at an early stage, single cells being
detached from them and becoming distributed in the primary body-
cavity. By the development of a cavity in each of these cell-masses,
right and left coelomic sacs are formed (Fig. 56 A and C), in which
a somatic and a splanchnic layer can be distinguished. As a rule,
however, this process is not so simple as that described for Bffthinia
by v. Erlangee. The detachment of the cells from the two masses
usually occurs very quickly, the two coelomic sacs being then much
more difficult to recognise. They represent, in the main, the rudi-
*[ln Trochus, the septum, which separates the two sets of leaves of the
single gill, is attached (except al the free end) to the mantle-wall along ; bol h
its margins; in this way one set of gill-leaves becomes enclosed in a small
cavity which only communicates with the general pallial cavity in front.
These gill-leaves arc much reduced in size as compared with the set which
project into the main mantle-cavity, and it is easy to see that a further stage
in this process might resull in a complete fusion of the septum with the
mantle-wall and thus cause a suppression of the one set of gill-leaves. There
is every reason to believe thai the monopectinate -ill arose in this way. — Ed.
I'
210
GASTROPODA.
merit of the pericardium ; the process is therefore very similar to
that described (p. 74) in connection with the Lamellibranchs. The
lumen of the sacs is to be regarded, here also, as further development
shows, as the secondary body-cavity, while the definitive body-cavity
proceeds from the cleavage-cavity which contains numerous scattered
mesoderm-cells.
The whole mesoderm-rudimeut is not, as already mentioned, used
up in the formation of the coelomic sacs ; occasionally even com-
pact masses of mesoderm remain which have been distinguished as
a.
mu>.
Pig. 96. Diagrammatic representations of young embryos of Bythinia tentaculata ;
.1, frontal section; />' and C, from the right side (after v. Erlanger). a, anal
region; hi. Iilastopore ; c, coelom ; e?it, entoderm; m, mouth; mrs, mesoderiu-
radiment ; x (after v. Erlanger). /, liver ; Ih,
body-cavity; m, stomach; ines, mesodermal tissue; mf, mantle-fold; mli, mantle-
cavity; ", rudiment of definitive, n', of abortive kidney; /»', //"'. rudiments of
efferent ducts of the same ; />. pericardium : s, shell.
where they fuse. Occasionally, in later stages, a septum is retained
as an indication of the former partition-wall (Fig. 98 J, sp). In the
further course of development, the right half of the sac grows much
more vigorously than the left, and the whole sac extends dorsally to
thr right side (Figs. 59 A, and 97). Differentiation now sets in, the
walls of the two later ventral angles of the sac becoming thickened
and subsequently forming distinct outgrowths (Fig. 97, // and //').
These outgrowths, according to Erlangek, are the rudiments of the
definitive kidneys which are consequently, like the pericardial sacs.
paired on their first appearance. The left rudiment soon disappears,
212
GASTROPODA.
while the right forms a sac (Fig. 101, re) and unites with the ecto-
derm to form the efferent duct. In Bythinia, the kidney can at this
stage be recognised as a derivative of the posterior part of the peri-
cardial sac (Fig. 92 B, re). At a later stage, a process grows out
from its postero-ventral part and becomes connected with the ecto-
derm of the mantle-cavity, so that the lumen of the kidney now
communicates with the latter. In Paludina, the formation of the
efferent renal duct (ureter) takes place from the mantle-cavity, which
at an earlier stage sank in on the right ventral side. The pallial
7WL'
Fig. 98.— J, transverse section through the pericardial region of au embryo of
Paludina vivipara at the .stage depicted in Fig. 59 C. B, the kidney of an almost
mature Paludina embryo (after v. Bblanger). i'. intestine ; h, rudiment of heart ;
/ liver; Ih, body-cavitv ; m, stomach; mes, mesodermal tissue; u, definitive, n ,
abortive kidney'; »", efferent duct of the former; oe, aperture of the kidney into
the pericardium ; /-, pericardium ; -y>, pericardial septum (remnant of partitim,-
wall).
depression is prolonged in the direction of each of the kidney-rudi-
ments (Fig. 97, na and na'). The branch running towards the right
kidney is specially distinct, being longer than that running towards the
left rudiment ; the latter, indeed, has no permanent significance on
account of the degeneration of this left rudiment. The right branch
of the mantle-cavity, however, then fuses with the right kidney, and
thus becomes its ureter (Figs. 59 /:. and 98, na).
THE DIFFERENTIATION OK THE MESODERM-RUDIMENT, ETC. 213
The ectodermal origin of the ureter ran be recognised even at a later stage
in its histological structure. The duel tunned as above lias been distinguished,
as primal \ ureter, from the secondary ureter met with in the terrestrial
Pulmonates. In some of these latter, the primary ureter opens into the
pulmonary cavity in the way above described. In others, it is continued as
a channel in the wall of this cavity, and in others, again, this channel partly
or altogether closes and, becoming finally altogether detached from the wall
of the respiratory cavity, yields the secondary ureter which, in the most
extreme cases, such as Helix />niintti'*surrlla, Tiwhw*) have a second kidney. It
is an interesting fad that this original paired character still finds
expression in the development of the kidney in P'ttudirut. In the
adidt. this kidney lies, as in most Gastropods, to the left of the
rectum and must therefore, as was shown above, have been the right
kidney before the twisting of the posterior part of the body took
place (Fig. luo A-E, p. 214). This view is admirably supported by
v. Erlanger's researches, since, according to his account, it is
the rudiment of the right kidney which develops further, while the
left degenerates. P. Sarasin's researches also show that, in
Bythinia, the rudiment of the kidney lies on the right side and is
displaced to the left later.
The one kidney which persists in most Prosobranchs (Monotpcardia) thus
corresponds to the (definitive) left kidney which, before the twisting took
place, was the right kidney of those forms which still possess two renal organs.
In these latter, however {Hnliotis, Wissurella, Turbo, Trochus) the right kidney
is usually well developed, the left, on the contrary, being reduced. It thus
appeared possible that the permanent kidney of the Monotocardia might
correspond to the right kidney of the Diotocardia, a" view which has been
put forward several times (Perrier, No. 87). Ontogeny, however, as well
as the fact that, in the Diotocardia, the right uephridium serves for con-
ducting to the exterior the genital products (see below, p. 2iiO) indicate that
it is the left (which before torsion is the right) kidney that persists and is
alone retained in the Monotocardia (Hay Lankester, Nq. 65; v. Erlanger,
No. 29).
The pericardial sac has several times been mentioned. The term
pericardial is here hardly correct, since the kidney also originates
from tins sac. to which, further, the heart owes its origin. This
organ has now become very large and has thin walls (Fig. 9.9).
Dorsally, and to the left of the renal outgrowth <>f the pericardium,
a channel-like invagination representing the rudiment of the heart
(Fig. US, h) appears and occupies the whole length of the sac. The
channel becomes more and more marked off from the pericardium i.e.,
it becomes a tube winch at first still remains open toward the primary
body-cavity. This tube, by finally closing ami remaining connected
with the wall of the pericardium only at its two ends. Liive^ rise to
the heart which now, as a tithe, lies within the pericardium, its two
ends opening into the primary body-cavity. At a somewhat earlier
stage, a constriction appears near the middle of this tube, by means
of which the auricle and ventricle are divided from one another
(Figs. 99 and 100).
The vessels arise as inter-cellular spaces in the mesodermal tissue of
216 GASTROPODA.
the primary body-cavity, and are thus at first quite independent of
the heart. We have already repeatedly spoken of embryonic or
larval blood-sinuses, some of which, being capable of carrying on
rhythmical movement, have been assumed to be larval hearts. The
rudiments of the vessels first appear as such blood-sinuses of different
sizes : in Paludina, for instance, a large sinus is found beneath the
intestine (Fig. 88 B, m, p. 1 i>4). The gradual narrowing of these
spaces, which are surrounded by a layer of flat cells, and their con-
nection with the open ends of the heart gives rise at the end of the
ventricle to the aorta and at that of the auricle to the efferent
branchial vein. The other vessels arise in a corresponding manner.
The heart, in the Gastropoda, forms in a less primitive way than in the
Lamellibranchia (p. 76). This is not surprising, since the circulatory and
respiratory organs of the Gastropoda have undergone far-reaching alterations
in consequence of the asymmetrical shape of the body. The presence of two
auricles, however, and the perforation of the heart by the alimentary canal
in a few Prosobranchs (Diotocardia) point to conditions resembling those
found in the Lamellibranchs. We might even believe that the heart in both
divisions arose ontogenetically in a similar way, and might then consider the
region at which the heart formed in the pericardium as the boundary between
the two coelomic sacs.
It is an interesting fact that we have, persisting throughout life, in
Dentalium, a condition similar to that seen in the developing heart in the
Gastropoda, which, as we have seeu, arises as an infolding of the pericardium.
According to Plate (Solenoconch. Lit., No. 3), the heart of Dentalium
represents a sac-like invagination of the pericardium, and the blood-vessels
also are found in a condition similar to that in Gastropod embryos, being
mere spaces in the mesoderm between the other organs. The structures re-
garded by Plate as pericardium and heart, however, are but slightly developed,
and the nephridia are not connected with the pericardium. It is well known
that Dentalium is a form already highly differentiated, but it may be possible
that in this respect a primitive character is retained. It appears also that,
among the Amphineura, the Solenogastres show a similar primitive condition,
while, in the Chitonidae, the circulatory system is much more highly organised,
the heart being entirely surrounded by the pericardium and provided with
efferent and afferent vessels.
The different positions assumed by the heart in the various
divisions of the Gastropoda, which are considered of great systematic
significance, are connected with the shifting of the different regions
of the body to which allusion has already repeatedly been made
(p. 144). (hie of the auricles, as was seen, is almost always lost in
the process. If the pallial complex is only displaced to the side, the
-ill lies behind the heart, the auricle behind the ventricle (this is
notably the ease in the Opisthobraiiehia) : but, if the pallial com-
THE FORMATION OF THE ORGANS THE GENITAL ORGANS. 217
shifts quite to the front, the gill will be found in from of the
heart and the auricle in front of the ventricle (Prosobranchia).
Other descriptions of the rise of the pericardium, the kidney and the
heart." In the formation of the pericardium as described above, this organ
wa- treated as if it corresponded to the whole of thecoelom, but v. Erlanger's
rvations on Paludina and Bythinia may also be interpreted as showing
only a pan of the original coelom persists as the pericardium while the
rest disintegrates, as we saw to be the east- in the formation of the definitive
body-cavity in the Arthropoda. Salenskv also, at a somewhat later stage of
the embryos of Vermetus, speaks of a somatic and a splanchnic layer which
are apposed to the ectoderm and the entoderm respectively and which enclose
a large space as a (temporary) secondary body-cavity. The two layers of tin
mesoderm are, however, so indistinct in the Mollusca that we are unable to
-peak of them with any certainty and, until more detailed statements are
made, must regard them as only definitely differentiated in the pericardium.
Sajjsssky, who regarded this large space as the coelom, considers that the
heart arose from it in a way similar to that above described. With this may
he reconciled the earlier accounts of Ganin {No. 35), Butschli (No. 18) and
especially of P. Sarasin (No. 101) and Schalfeew (No. 106) which refer
partly to the Prosobranchia and partly to the Pulmonata.
It is easier to reconcile the older and more recent researches with regard
to the rise of the heart than with respect to the origin of the kidney. This
organ was indeed early derived from the mesoderm by constriction from the
:ardium (Schalfeew) or at least in the neighbourhood of the latter
(Salbnsky), the efferent ducts being derived from an (ectodermal) invagina-
tion of the mantle-cavity, but the majority of authors trace back the whole
kidney to an ectodermal invagination. After what has been said above
(p. 74) as to the formation of the nephridia in the Lamellibranchia and the
Auuelida, it cannot he doubted that the first method is the more probable. t
H. The Genital Organs.
The development of the genital organs has been best observed in
Palvdina, a form belonging to the Prosobranchia in which the sexes
are distinct (v. Erlangek). In these animals, the condition of the
*The literature connected with the formation of the mesodermal organs is,
like that connected with the ontogeny of the Gastropoda in general, rich in
contradictory statements. Where recent researches may be considered to
have disproved older statements, we have ignored the latter. Lack of space
Da- prevented us from taking into consideration all the published data of a
confirmatory nature. A summary of these is to be found in v. Erlanger's
works (Nos. ->1 and 28).
+ [The recent investigations made by Meissenheimeb (No. XVII.) on the
development of these organs in Limax do not at present help to clear up the
confusion relating to their origin, as they are too startling to be accepted
unsupported. Meissenheimer maintains that the heart and kidney arise from
a common ectodermal rudiment, a condition which, so far a- we are aware.
appears to lie quite unique. — Ed.]
218
UASTKOPODA.
genital organs is far simpler than in the hermaphrodite Pulmonates-
which have repeatedly been studied but are far from being fully
understood, and we shall therefore consider Paludina first. The
first rudiment of the genital organs here appears at a time when the
velum is still present, and the primitive kidney at its highest de-
velopment, i.ff.j somewhat at the stage of Fig. '.Ml. The male and
female genital rudiments are similar.
The germ-gland arises as a rounded outgrowth of the pericardia]
sac near the rudiment of the (original) left kidney (Fig. 101, /, vd).
The hermaphrodite gland arises
independently of this strand from
the mesoderm .'primitive blastomeres . A short process of the
mesodermal rudiment yields the proximal portion of the efferent
duct, while the distal part arises from the cellular strand mentioned
above (Fig. 103,-zg, Brock, Klotz). The spermetheca becomes
*) are self-evident.
i III. FORMATION OF THE ORGANS — THK GENITAL ORGANS. 228
fn cases in which, finally, the penis becomes shifted towards the
female genital aperture, and the two join to form a common atrium, as
in the Stylommatophora (Fig. [04 A'), the rudiment of the ectodermal
parts form from a common rudiment. In these cases, we have only
t" distinguish between the mesodermal rudiment of the hermaphro-
dite gland (or the hermaphrodite organ) and the ectodermal rudiment
of the primary and secondary ducts and copulatory apparatus.
The significance of these processes is still little understood, and it is doubt-
ful if ontogeny will throw much light upon the subject. ' Summaries and
critical descriptions of these ontogenetic processes are given by Rouzaud,
Brock, Sempeb (No. 1171, Schiemenz (No. 107), and Klotz (No. 54).
a.
.
Fig. I'M. .I-/-;, diagrams illustrating the manner in which the genital apparatus opens
out at different ontogenetic stages. .1. in a dioecious Gastropod ; B-M, in herma-
phrodite Gastropods, os, ovoseminal duct ; //. penis; vd, vas deferens; 5 and J
genital apertures or the terminal portions of the corresponding efferent ducts.
[The interpretation of the complicated conditions met with in the herma-
phrodite genitalia of the Opisthohranchia and Pulmonata is one of those
difficult problems upon which ontogeny throws little light. We think there
can be little doubt, that it will be found more profitable to leave the onto-
genetic side alone and accept the obvious and comparatively simple interpre-
tation offered by the study of tbe comparative anatomy of these organs.
In existing Gastropoda, we seem to have every stage in the development of
the secondary genital ducts preserved to us, so that, starting from the simple
condition of the Diotocardia, where the gonads discharge by the still functional
right kidney, we pass to the Monotocardia. where the right kidney has lost
its excretory function and serves solely to transmit the genital products, and
where also we find a secondary duct appearing in the male in the form of a
groove leading forward to a non-introvertible penis. A condition similar to
this is found in many of the hermaphroditic Tectibranchia, which, how-
ever, generally show an albumen-gland and a sperinetheca, while the open
224 GASTROPODA.
groove-like vas deferens leads down to an introvertible cephalic penis. The
next change which occurs is the closure of the groove-like vas deferens and its
separation from the ectoderm as a tube. This brings us to the condition, seen
in Actaeon and then to the Basommatophorous Pulmonata, where the male
aperture is distinct from the female. The only break in the series is that
between the Basommatophorous and Stylommatophorous Pulmonata, due to
the development in the latter of a secondary oviduct which extends from the
primitive genital aperture (now closed) down to the cephalic penis, and opens
with that structure through an atrium. With regard' to the origin of this
secondary oviduct, two possible interpretations present themselves, one being
that the secondary oviduct has arisen as a groove, like the vas deferens, and,
like that structure, has secondarily closed together with the primary genital
aperture, so that .both products are discharged by a single anterior aperture,
or it may be that the primitive genital orifice has shifted by growth down the
side of the body towards the penis and, finally, an atrial involution has caught
up both these apertures, so that they now communicate with the exterior by
a common aperture. The fact that these stages are not recapitulated in the
ontogeny is not, we think, of much importance, for we know that ontogeny
by no means always recapitulates phylogeny, and that this is especially the
case in forms which, like these Mollusca, have a considerable amount of yolk.
Ed.]
LITERATURE.
1. Alder, J., and Hancock, A. Observations on the structure
and development of Nudibranchiate Mollusca. Ami. Mag.
Nat. Hut. Vol. xii. 1843.
2. Alder, J., and Hancock, A. On a proposed new order of
Gastropodous Mollusca. Aim. Mag. Nat. Hi. Barrois, Th. Les glandes du pied et les pores a.quiferes chez
les Lamellibranches. Lille, 1885. (Cowpt. Rend. Acad. Sci.
Pari*. Torn, c.)
1. Behme, Th. Beitrage zur Anatomic und Entwicklungsgesch-
ichte des Harnapparates der Lungenschnecken. Arc.hiv. f.
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LITERATURE. 233
VIII. Erlanger R. von. Mittheilungen iiber Bau und Entwick-
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X. Erlanger, R. von. Zur Bildung des Mesoderms bei des
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XVII. Meissenheimer, J. Entwicklungsgeschichte von Limax
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XVIII. Meissenheimer, J. Zur Morphologie der Urnieren der
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XX. Schmidt, F. Beitrk'ge der Entwicklungsgeschichte der
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234 GASTROPODA.
XXIV. Thiele, J. Zur Phylogenie der Gastropoden. Biol..
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XXV. Tonniges, C. Die Bildung des mesoderms bei Paludina
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XXVII. Wierzejski, A. Ueber die Entwicklung des Mesoderm bei
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CHAPTER XXXIII.
CEPHALOPODA.
Systematic : —
I. Tetrabranchia, with two pairs of gills, two pairs of auricles,
two pairs of kidneys, external chambered shell and a large number
of tentacles round the mouth. Funnel consisting of two lobes ; with-
out ink-sac.
1. Nautiloidea.
2. Ammonoidea.
II. Dibranchia, with one pair of gills, one pair of auricles, one
pair of nephridia, with internal shell, the chambers of which are
seldom distinct (Spirilla, Belemnites) often reduced or absent. Round
the mouth eight to ten arms. The two halves of the siphon united
to form a tube ; an ink-sac generally present.
1. Decapoda, with ten arms.
(a) Phragmophora.
Spirulidae.
Belemnitidae.
Belemnoteuthidae.
Acanthoteuthidae.
(b) Oigopsida.
Ommastrephidae.
Oni/choteuthidae.
Cranchiidae.
Ghiroteu th it lae.
(c) Myopsida.
Loliginidne.
Sepiolidae.
Sepiidae.
'2. Octopoda, with eight arms.
Civrhoteuthidae, with fins.
Fhilonexidae, Tremoctopus, PhUonejcis.
Argonaut idae.
Octopoflidae, Octopus, Eledone.
236 CEPHALOPODA.
1. Oviposition and the Constitution of the Egg.
The egg of a Cephalopod, before it is mature and at the time of
oviposition, is surrounded by a protective envelope which, in the
different forms, may assume very various shapes. A large number
of eggs are usually laid at one spot, forming a large mass of spawn.
In Sepia, the eggs constituting the mass are distinct from one
another. Each of them is surrounded by a compact, spindle-shaped,
black capsule of leathery consistency which, at one end, runs out
into a process, by means of which the eggs are attached close to one
another to some firm object. The egg-capsules attain about the
size of a hazel nut. In Rossia and Sepiola * also, the eggs are laid
separately and are attached to some object or else to each other,
but the envelope is less thick and is even transparent (Sepiola).
The eggs of Loligo, on the contrary, are laid in gelatinous tubes,
each tube containing a large number (in Loligo vulgaris, as many
as eighty or more). The tubes are attached by one end to some firm
substratum. As they stand out from their point of attachment
radially, they form a kind of tassel. Such large tassels are found
attached to plants, pieces of wood, stones, etc.
The eggs composing a mass of spawn, resembling Cephalopodan
sjjawn — dredged by Gkenacher off the Cape de Verde Islands and
attributed by Steenstkup to one of the Teuthidae (i.e., to a form
something like Ommastrephes, No. 14), are also surrounded by a
gelatinous mass, but are not contained in distinct tubes. This spawn
forms a gelatinous mass 75 cm. long and 15 cm. thick which
resembles a sausage. Within the gelatinous cover, the violet-coloured
spherical eggs are arranged in fairly regular spiral coils, their number
amounting to thousands. Each egg, as in Loligo, is surrounded by
a firm envelope. A similar envelope which must be regarded as the
chorion (p. 246) also surrounds the eggs of the Octopoda.
In Octopus and Argonauta, the chorion of the oval egg is drawn
out into a stalk. The stalks of a number of eggs become connected
* According to Steenstrup (No. 42), the ontogeny of Sepiola as given by
various authors (P. van Beneden, Metschnikofp, Ussow) refers rather to a
species of Loligo : further obscurity being due to the fact that the masses of
spawn found and investigated have been attributed to Cephalopods to which
they did not belong. Egg-masses produced by Loligo vulgaris, a Myopsid, are
said to have been ascribed to Ommastrephes sagittatus, a form belonging to
the group of the Oigopsida. This led to the inaccurate conclusion that forms
remote from one another in systematic position showed great similarity in
their development. According to Steenstrup, this resemblance in develop-
ment is due rather to the fact that they all belong to the genus Loligo, and
theoretical conclusions founded on this similarity would thus be of no value.
OVIVOSITION AND THE CONSTITUTION OF THE EGG. 237
together, large egg-bundles being thus produced, the bundles again
uniting to form aciniform masses {Argonauta). In Eledone also, the
threads from the chorion of the long eggs unite to form a stronger
strand, which then becomes attached to the substratum (Joubin, No.
21). We have ourselves found that the eggs of Eledone (apparently
E. moschata) are attached by their stalks to the substratum in pairs
or in groups of two or four. A number of such groups are found in
close juxtaposition, giving rise to a spawn-mass consisting of sixty
to seventy eggs. The long ovate eggs of this Eledone are very large,
measuring (including the envelope) 15 mm. in length, while those
described by Joubin are only about half this length.
In Sepia, the stalks of the individual eggs become twisted together,
the result being a rather lai'ge strand of eggs closely arranged round
a central axis. These strands are attached to rocks, the female
covering them with her body and, by the promotion of a continuous
How of water, assisting in their development (Schmidtlein).* The
eggs of Argonauta are still further protected by the mother, as the
spawn is attached to the inner side of her shell and carried about by
her. [Nautilus (Willey, No. IV.) lays solitary eggs of great size,
each egg-capsule measuring 45 mm. by 16 mm. and containing one
egg 17 mm. long and very rich in yolk. — Er>.]
The capsules or the gelatinous masses which surround the eggs and the
cementing substance by means of which they are attached are secreted by
special glandular portions of the oviducal wall and by the nidimental glands.
Where there is no such special development of glands in the genital apparatus,
as in the Octopoda, the eggs are surrounded by the chorion alone. This latter,
however, is also found round eggs surrounded by firm capsules or gelatinous
masses. At the animal pole of the egg, the chorion is perforated by the
micropyle (Fig. 105, m).
The conditions under which copulation and the fertilisation of the egg take
place in the Cephalopoda are so peculiar that we must devote some attention
to them. In the Octopoda, fertilisation probably takes place in the oviduct.
The spermatophores are introduced by the help of the hectocotylised arm into
the mantle-cavity or the oviduct. In Argonauta, Trcm-octopus and Philonexis,
it is well-known that the detached hectocotylised arm of the male is found in
the mantle-cavity of the female. The female in the two last-mentioned forms
possesses a receptaculum seminis in the form of an outgrowth of the oviduct
which serves for the reception of the sperm (Beock).
In the Oigopsida, as in the Octopoda, fertilisation takes place within the
mantle-cavity, the spermatophores being introduced into that cavity and
attached to various parts of its inner wall. Among the Myopsida, in the
* Beobachtung iiber die Trachtigkeit.und Eiablage verschiedener Seethiere.
Mittheil. Zool. Stat. Neapel. Bd. i. 1879.
238
CEPHALOPODA.
female of Rossia (according to the verbal statements of F. C. v. Maerenthal)
there is a well-marked area near the mouth of the oviduct within which the
spermatophores are attached. In the nearly related Sepiola (also according
to researches by v. Maerenthal not yet published), there is a pouch-like
depression of the integument lying laterally to the mouth of the oviduct
for the reception of the spermatophores ; this has been hitherto erroneously
regarded as a terminal portion of the oviduct itself.
In the other Decapoda, copulation takes place in an exceedingly peculiar
way, the spermatophores not being brought into the mantle-cavity, but
attached near the mouth ou the outer integument of the lip (buccal membrane)
■of the female. Glandular invaginations of the integument, in which the
spermatozoa that escape from the spermatophores are stored, are found in
this position iu Sepia and Loligo (Vialleton), in Sepioteiithis and no doubt
also in the other genera (v. Maerenthal).
In this last case, it is evident that fertilisation takes place only when the eggs
:are expelled through the funnel and are retained for a time near the mouth by
the arms. The future leathery egg-capsule (of Sepia) is either still soft at
this time and penetrable by the spermatozoa (?) or only forms after these
have penetrated the egg (through the micropyle of the chorion), the still fluid
glandular secretion being subsequently poured over the eggs by the funnel.
This would then also no doubt apply to the gelatinous mass (in Loligo). It
is an interesting fact that artificial fertilisation of mature eggs taken from
.a female Loligo Pealii was brought about by means of seminal fluid found in
the spermatophores of the buccal
membrane (Watase, No. 50). The
-*1 same conditions are found in Rossia.
m
eft
*k
B
Fig. 105. — The upper pole of the egg of
*"? Arf/onauta argo in optical section.
."'.1, before fertilisation; B, shortly
after fertilisation (after Ussow). ch,
£[ chorion; d, yolk; ks, germ-disc; m,
micropyle ; pi, peripheral protoplasm ;
r&,Spolar bodies.
longitudinal diameter. The food
The eggs of the Cephalopoda
are unusually rich in yolk, and
consequently attain a considerable
size, a point in which they are
essentially distinguished from
those of other Molluscs. The
eggs of Sepia, for instance, are
fully as large as a pea (Sepia
officinalis). The eggs of Eledone
may be still larger and are ex-
ceedingly rich in yolk (p. 237).
The eggs of other Cephalopods,
such as Loligo and Octopus, are
less rich in yolk and therefore
distinctly smaller ; those of Argo-
nauta are even rather small,
measuring, however, 1*3 mm. in
■yolk, which consists of rather fine
OVirOSITION AND THE CONSTITUTION OF THE EGG.
239
granules, always constitutes by far the greatest mass of the egg. The
egg, in shape, is usually oval (Loligo, Eledone, Octopus, Argonauta)
or spherical, as in Sepia and the Cephalopoda investigated by
Grenacher (p. 267). The massive food-yolk is completely invested
by a comparatively thin layer of the formative protoplasm, which
thickens to form a disc-shaped accumulation at the upper or future
animal pole of the egg beneath the micropyle. This is the future
germ-disc (Fig. 105, /rx) and is sharply marked off from the food-yolk.
In consequence of this peculiarity, and others to be described later,
the eggs of the Cephalopoda att'ord the most perfect examples of
meroblastic clt a vage.
a.
Fig. 106. — Diagrammatic longitudinal sections through the egg of Loligo Pealii (after
WaTase). B is a median sagittal section ; A, a transverse vertical section at right
angles to B. The black line on the periphery of the egg represents the formative
protoplasm, while the food-yolk is shaded, d, dorsal side ; v, ventral side ; h,
posterior ; vo, anterior ; I, left ; /•, right.
A bilateral symmetry can be recognised not only in the early stages
of cleavage but even before cleavage sets in ; this symmetry bears a
definite relation to the later development of the embryo. In the oval
eggs of Loligo Pealii, it is expressed not only in the form of the egg,
but also in the way in which the germ-disc spreads over it (Watase,
No. 50). The eggs of this Cephalopod appear somewhat flattened on
one side while, on the opposite side, they are arched (Fig. 106 B).
The positions of the anus and the mouth in the embryo correspond
to these two sides. At the part which becomes the anterior end (vo),
the protoplasm of the germ-disc extends further down towards the
equator than on the opposite side (h). The germ-disc, however,
240 CEPHALOPODA.
spreads to right and left for an equal distance (Fig. 106 A, r and /).
A comparison of Fig. 106 B with the median sagittal sections of
later embryonic stages (Figs. 132, 133, p. 282) shows that the
animal pole of the egg (d) corresponds to the area of the dorsal
surface, the vegetative pole (v), on the conti'ary, to the ventral
surface.
In the germ-disc we find the egg-nucleus and later the first cleav-
age-nucleus. Neither of these, however, quite coincides with the
animal pole of the germ-disc (Fig. 105 A) but occupies a somewhat
excentric position, i.e., it is slightly nearer the posterior edge of the
disc. The nucleus appears to be surrounded by a more hyaline zone
of protoplasm which passes externally into a more granular proto-
plasm. The protoplasm of the germ-disc is in any case distinguished
by its granular character from the thin protoplasmic layer that
surrounds the whole egg. The thickness of the disc appears to vary
in different cases, so far as can be gathered from the statements of
authors. This is perhaps to be accounted for by the various stages
of development at which the disc is represented.
A vitelline membrane is apparently never developed in the eggs of'
the Cephalopoda. The membrane, which is perforated by the micropyle
and is often very tough, is secreted by the follicular epithelium (Ussow,
Vialleton) and may therefore be termed the chorion. Between this
egg-shell and the surface of the egg there is a somewhat wide space
filled with clear albuminous fluid. This enables the embryo to extend
considerably within the chorion, which is itself said to be extensible,
and thus to admit of further growth on the part of the embryo.
At the animal pole, in the mature egg, there are two polar bodies,
one of which has been observed to divide (Loligo and Argonemtd) and
give rise to a third body (Fig. 105, rk). Such division is said by
Vialleton not to occur in Sepia, but the fact that one of the two
polar bodies possesses two nuclei shows that these bodies, even in
Sepia, are quite normal. Vialleton denies that there is any con-
stant relation between the polar bodies and the first cleavage-plane,
but the deviations from such a relation are very rare, and from his
own figures and those of other authors this line of cleavage is seen to
occur in the closest proximity to the polar bodies.
2. Cleavage and Formation of the Germ-layers.
The cleavage of the egg is incomplete, a fact connected with the
great abundance of the food-yolk in it and the distribution of this
CLEAVAGE AND FORMATION OF THE GERM-LAYERS.
241
and of the formative yolk ; cleavage is at first limited to the germ-
disc. The conditions of this process therefore differ essentially from
those in the other Mollusca. The principal features of these pro-
cesses have been known for many years, being described in Kolli-
ker's famous work on the development of the Cephalopoda (No. 24).
These investigations which, from the nature of the case are far from
being exhaustive, appeared in 1S4.">, and were followed by observa-
tions made by Bobretzky (No. 4), Ussow (Nos. 44-46), Vialleton
(No. 48) and more recently by Watase (No. 50). We shall here
follow the last-named author, dwelling especially on the detailed
descriptions of the processes of cleavage in Lolicjo Pealii as given by
him and of Sepia officinalis as described by Vialleton. So far as
r/t.^.
B
v
K.
V
/.
Fig. 107. — Two germ-discs ol Sepia officinalis showing the first (J) and second (//)
cleavage-planes and the polar bodies (rk) (after Vialleton).
is at present known, cleavage seems to take place in the different
Cephalopods in very much the same way.
The spindle of the first cleavage-nucleus which is preparing for
division lies with its longitudinal axis running from right to left
(Watase), and therefore in the plane depicted in Fig. 106 A*
It therefore, curiously enough, does not appear to lie, according to
the usually accepted rule, in the direction of the widest extension of
the formative protoplasm.
The first line of cleavage runs, in correspondence with the position
of the spindle, from before backward, cutting the axis of the spindle
at right angles. The first furrow thus lies in the median sagittal
* Cf. p. 239 on the bilateral symmetry of the egg before cleavage.
R
242
CEPHALOPODA.
plane of the egg or later embryo, i.e., in the plane given in Fig. 106
B. This first furrow (/) above which the polar bodies are, as a rule,
found (Figs. 107 and 105 B, rk), starts from the middle part of the
germ-disc where the cleavage-nucleus lies and is continued to the
periphery of the disc. It cuts deepest in the centre of the disc,
dividing the whole of the protoplasm at this point into two segments
(Fig. 106 B), while, further back and especially beyond the actual
\
ft
vo.
vo
B
•<.[
• ft
7
Fig. 108. — Eggs of Loligo Pealii representing various stages of the cleavage of the
germ-disc, the bilateral symmetry of which can be recognised (after WATASE).
2ZT .■
I.
^•- W*
ML'
r%_
v\F
/'
f$
to '
\ -T
I
I
r.i
' 9 if
v-, -.^ k.
• j i a.
M&^i83SlBB
HI' C
i
c. *■
ml i" e: .~ .
r: .
7. Z,nriM'
■
l.I.'
w.
I.
^.
S.
/
Jf.
r.
Fig. 109. — Germ-disc of Sepia officinalis at the eight-celled stage i.l) ami at two later
stages (/,' and '') (alter Viai.LETon). The germ-discs are placed in such a way that
the anterior side is directed upwards, ami the posterior side downwards. I, left side
r, right side ; l-V, directions of the first live meridional planes of cleavage.
109 A and 108 B). Of these new furrows (///' and III") only the
anterior ones (III) make an angle of 45° with the median plane and
therefore cut the two anterior segments into almost equal halves.
The two posterior furrows (III") run somewhat parallel to the median
plane (Figs. 108 B and 109 A), and it thus happens that here, at the
posterior part of the germ-disc, two narrow segments bounded by
parallel sides are cut oft'. Through this course of cleavage, concerning
244 CEPHALOPODA.
which observers are agreed, the germ-disc becomes markedly bilateral,
a character which is retained in the later stages also (Figs. 108 and
109 B and C, 110), the two segments mentioned above and the
blastomeres that proceed from them retaining their characteristic
shape, i.e., retaining their regular position with regard to the median
plane, the other cleavage-cells also continuing to be symmetrically
arranged with regard to that plane.
The broad segments of the eight-celled stage (Figs. 109 ^4 and
108 B) are directed forward, the narrow segments, on the contrary,
backward (Watase, Ussow). In this way the bilateral symmetry
of the germ-disc after cleavage and the relation to the form of the
adult animal are shown still more distinctly than in the egg before
cleavage (rf. p. 239 and Fig. 106 A and B).
It should be added that Vialleton also describes the striking bilateral
symmetry of the germ-disc after cleavage which is evident from Fig. 109, but
does not assume so definite a symmetry in the shape of the egg before cleavage.
It may be more difficult to establish these points with certainty in the spheri-
cal egg of Sepia. The identity of the median sagittal line of the blastoderm
with that of the embryo which is emphasised by Ussow is also apparently
assumed by Vialleton as probable, so that, according to him also, the
bilateral symmetry of the germ-disc after cleavage corresponds to that of
the embryo.
Siuce, in consequence of the continuous division of the cells, the shape of
the germ-disc is less regular in the later stages (Fig. Ill), it is very difficult
to prove that the bilateral symmetry of the germ disc passes directly over
into that of the embryo ; this has, indeed, not yet been exactly proved, so
far as we can see. But the bilateral character of the germ-disc found in
Cephalopods otherwise very different from one another [Loligo, Sepia, Argon-
auta *) makes its relation to the form of the embryo appear more than
probable, and we must therefore for the present hold to the view of Watase,
although, indeed, this seems to be somewhat conjectural.
As cleavage advances further, an equatorial furrow cuts off from the
two narrow posterior segments, towards the middle of the germ-disc,
two small blastomeres (Fig. 109 B) ; a continuation of this equatorial
furrow cuts off, in Loligo, similar blastomeres from the large segments
in front (Fig. 109 G). In Sepia, however, additional meridional
furrows appear first and divide these segments into narrower sections
(Fig. 109 B,.IV and V), after which they become divided by an
* With regard to Argonauta, we have to rely on the statement repeatedly
made by Ussow that he saw cleavage taking place, in the forms observed by
him, in a similar manner to the above. A confirmation of these statements
with respect to the Octopoda is, indeed, very desirable. With reference to the
conjectural Sepiola, also investigated by Ussow, see the remarks made p. 236.
CLEAVAGE AND FORMATION OF THE GERM-LAYERS.
245
equatorial furrow. The two narrow posterior segments, so character-
istic in shape and position, still remain unaltered even after this
division, but two further blastomeres gradually become detached
from them by equatorial division and pressed towards the centre
(Fig. 109 C).
The number of segments increases more and more through the
appearance of other furrows, some meridional and others equatorial
(Figs. 10^ (', 110). From the accounts of Kolliker and Vialle-
ton, it appears that the segments at the middle of the germ-disc are
not at first in close contact with each other (Figs. 107 and 109). A.S
cleavage advances, this space in the centre disappears.
Kir,. HO. — Germ-disc of Loligo Pealii at a later stage of cleavage, the bilateral sym-
metry still being evident. The blastomeres and blastocones lie symmetrically to the
middle line /-/ (after Watase). w, anterior; h, posterior; /. 'left : r, right, /-!',
direction of tin- first five furrows.
The bilateral symmetry evident up to this time and still visible in some-
what later stages is still further heightened by the division of the cells taking-
place at somewhat different times, a fact which finds expression in the
different conditions of their nuclei. Such a case is represented, for instance,
in Fig. 110, in which the posterior cells lying near the middle line contain
resting nuclei while the nuclei of all the other cells are found to be dividing.
This phenomenon is also frequent in the larger cell-complexes. The almost
diagrammatic aspect thus produced corresponds, as Watase expressly states,
246
CEPHALOPODA.
to the actual condition of the disc. This is also confirmed by Vialleton's
earlier description [e.g., Figs. 25 and 26, No. 48), in which the various condi-
tions of the nuclei in symmetrical division are given. Further, whole
complexes of cells such as the posterior cells or those of a lateral part may
advance more rapidly in their division, whilst the division of others may he
retarded, this being again visible in the state of their nuclei.
In the germ-disc depicted in Fig. 110 two complexes of segments lying
symmetrically and marked off by the planes II and III', are distinguished by
the fact that the furrows lying between them are less distinct than those in
other parts of the germ-disc These segments are thus shown to be connected
together, and have most probably proceeded from the segments bounded by
the furrows II and III' of the stage represented in Fig. 109 A, which is passed
through in Loligo and in Sepia in the same way (Watase). Such a condition
also renders the bilateral symmetry specially clear.
/
"' - 5 *-•*■* li
■ . •• **•'•
f-r y
-:
■
i ■ . • ■ •■ ;t *-" -'-* -.-■,-
- >* > • fc i>-« =< . ' ■ - - ~\
-< -*■ ■••.-' f- • e» 'i* ---?■* ^
-->^V '• " ■-/ - V
his / ■ . - • \.Y
^f,L
\L.
Fig. 111. Germ-disc of Sepia officinalis at a late stage of cleavage (after Yialleton).
W, blastomeres ; Wc, blastocoues; d, yolk.
Up to this point, the origin of the cells is clearly recognisable in
their arrangement ; their position with regard to the middle line also
is very regular. As cleavage proceeds further, and the blastomeres
continually decrease in size, this regularity of form is no longer
perceptible in the germ-disc. A certain regularity of position may at
first be retained in the peripheral cells, especially in the blastocones,
but even this is finally lost as the cells continue to increase in
number. The animal pole of the egg now appears covered by a
CLEAVAGE AND FORMATION OF THE GERM-LAYERS. 247
onilaminar "disc"* of polygonal plate-like cells (Fig. 111). The
cells at the edge of the disc (blastocones), however, are not polygonal,
having no outer edge (Fig. Ill, blc), bul passing ever into the
remaining mass of formative yolk. In Fig. 1 11, a certain difference
of size can be perceived in the blastomeres, but this apparently
cannot yet be related with certainty to the later form of the embryo.
The germ-disc spreads out and increases in size as is evident in
Figs. 107-1 1 1 , at first no doubt chiefly at the expense of the formative
yolk in contact with it : only later is the abundant food-yolk utilised
as nourishment for the growing embryo.
3Iy-f£>-
■\
ft.—"
vi.—~-
2*.
m
>-■<£
Z.
I IG L12. Germ-disc of Sepia officinalis at the commencement of the formation of the
germ-layers (after Viallbton). d, yolk; ,. onilaminar portion of the germ-disc;
vd, thickened (multilaminar) portion of the germ-disc (area opaca); Z. cells in the
act of separating from the germ-disc.
After the cleavage-cells have considerably increased in number, the
peripheral cells somewhat change in shape : their tree ends narrow
and they show a tendency towards becoming detached from the
germ-disc (Fig. 11 2 Z). They finally become rounded off and move
away from the disc. They are then found scattered round the latter
at the surface of the food-volk. It should here be mentioned that
* This so-called disc is actually a more or less arched cap.
248 CEPHALOPODA.
these cells, according to Vialleton, wander beneath the cell-material
of the germ-disc, there becoming arranged into a connected cell-layer
which is said gradually to spread over the whole of the food-yolk.
But this brings us to the formation of the germ-layers, and in order
to comprehend this, we must first refer to another process and also
mention the views which have hitherto prevailed on the subject.
The problem of the formation of the germ layers in the Cephalopoda
must be regarded as exceedingly complicated. The fact that the
significance of the different cell-layers forming in the germ has not
been recognised and that it has not yet been possible satisfactorily to
trace back the method of their formation to corresponding processes
in the other Molluscs or in the members of other animal groups, is
evidently due to the highly modified conditions under which the
Cephalopodan egg develops on account of the large amount of food-
yolk deposited in it and the marked distinction between the food-
yolk and the formative yolk.
Fig. 113.— Longitudinal section through an egg of Loligo at the stage in which the
edge of the germ-disc becomes thickened (alter Bobijetzky from Balfour's Text-
book), c, peripheral cells ; d and ms, the thickenings of the edge.
The following is a brief statement of the view hitherto held as to the formation
of the germ-layers. The germ-disc consisting of a single layer of cells which
at first covered only a small part of the animal pole of the egg, at a certain
time, undergoes at the periphery a thickening of the cell-layer (Fig. 113).
The layer which thus arises and which soon gains considerably in size by the
active increase in number of its cells, and spreads out beneath the whole of
the upper layer of the disc, has been derived either through delamination
from the cell-layer already present (Metschnikoff, Ussow) or else through
the bending in of this layer (Bobretzky).
In contrast to the upper (ectodermal) cell-layer, the massive cell-accumula-
tion has been claimed as chiefly mesodermal although the mid-gut epithelium,
which elsewhere is always entodermal in origin, is said to be derived from this
accumulation. Beneath the latter which, for the present, we must regard as
mesoderm, a new layer is now found which, in its origin and relation to the
other layers is of special interest. This is the " vitelline membrane " of authors
which, starting from the periphery of the germ-disc, no doubt spreads below
the disc (and the " mesoderm ") as well as over the whole food-yolk, surround-
ing it as a uuilaminar cell-integument.
CLEAVAGE AND FORMATION OF THE GERM-LAYERS. 249
Ray Lankestkr assumes, with considerable inherent probability, that the
•vitelline membrane owes its origin to cells (or nuclei) freely distributed in the
yolk, these being at once comparable to the yolk-cells and merocytes in the
eggs of the Arthropoda and Vertebrata which are also very rich in yolk.
These nuclei arc said to shift to the surface, to become surrounded with
protoplasm and to unite to form the vitelline membrane.
Other investigators {e.g., Qssow) have been inclined to derive the cells of
the vitelline membrane rather from the deeper layers of the germ-disc, and
thus from the "mesoderm." In any case, this enveloping membrane of the
yolk lias the same significance as the vitellophags in the Arthropoda and the
Vertebrata. As the terms vitelline membrane and yolk-integument are not
specially happy, being commonly used in another sense, we shall give this
cellular integument another name (also applied to it by Rav Lankester),
calling it the yolk-epithelium.
During the formation of the yolk-epithelium, the superficial cell-layer, the
eetoderm, has spread over the whole of the food-yolk, which thus, beyond the
germ-disc, is covered by two cell-layers. Besides this, there is, as far as the
germ-disc extends, the "mesodermal" cell-mass lying between the ectoderm
and the yolk-epithelium. The three germ-layers are thus apparently repre-
sented, if we may for the time assume the yolk-epithelium to be the entoderm.
The difficulty arises, however, that the yolk-epithelium is not found to be
connected With the formation of the enteron, which owes its origin rather to
the breaking up of the middle layer.
Having now arrived at some comprehension of the germ-layers
from which the Cephalopodan body is built up, we must trace the
way in which the latter originates, as described in the most recent
accounts.
We traced the origin of the germ up to the point at which the
animal pole of the egg is covered by a unilaminar plate of polygonal
cells, and at which the irregular peripheral cells of this plate begin
to detach themselves from it (Fig 112). Almost simultaneously with
this process, the thickening of the edge of the plate already mentioned
occurs, i.e., the plate here becomes multilaminar through more active
increase in number of its cells (Figs. 1 L2, <"/, and 113). This is the
process which was described by earlier authors as the formation
(delamination) of the mesoderm.
Before the layer which lias formed in this way loses its close connection
with the superhcial layer of the germ-disc, the cells previously detached from
that disc undergo, according to Vialleton, an essential alteration. Their
cellular character disappears, they are no longer distinctly although irregularly
bounded, but now appear as a syncytium, i.e., as nuclei lying in the thin
layer of protoplasm that surrounds the food-yolk. There can be no doubt
that we have before us, in them, the same nuclei which, according to
Lankester, give rise to the yolk-epithelium. This last significance actually
belongs to these cellular structures which, according to Vialleton, arise
250
CEPHALOPODA.
from the germ-disc ; they increase greatly in number and at first unite to
form a cell-layer which not only penetrates beneath the disc (Fig. 114 A-Cr
de), but also extends beneath the ectoderm over the whole of the yolk. The
formation of this yolk-epithelium and the thickening of the edge of the
disc which affects the whole of its periphery are clearly illustrated in Pig.
114 A-C. These figures show, at the same time, how the yolk-epithelium
presses in towards the middle of the disc, as assumed by both Vialleton and
Watase.
31^v®\5?
*~ a. ^
V
1 mt\®T:~-Jis.
! — d.
; : "'.- — d.
■
Fig. 114. — Sections through a marginal portion of the germ-disc (ks) of Sepia officinalis
(after Vialleton). d, yolk ; de, yolk-epithelium ; /•, the thickened edge of the
germ-disc.
The separation from the superficial or ectodermal layer of the cell-
mass, formed by the thickening of the margin of the disc, gives rise
to the layer claimed by earlier authors as the mesoderm. So as to
understand the real significance of this layer, we must follow its
further fate. Since, to do so, we should have to pass on to some-
what later stages, it will be advisable first to turn our attention to
the external changes taking place in the germ-disc or in the whole
blastoderm.
3. The Development of the External Form of the Embryo.
While the formation of the yolk-epithelium and the simultaneous
thickening of the edge of the germ-disc are taking place, another rapid
increase in number of cells occurs in the superficial layer of the disc,
and results in the gradual extension of this upper cell-layer over the
whole egg. This layer is known as the blastoderm, although this
term is not cpiite correct for, apart from the fact that a differentia-
tion of this layer has already taken place round the animal pole, it
DEVELOPMENT OF THE EXTERNAL FORM OF THE EMBRYO. 251
is soon followed in its circumcrescence of the egg by a second layer, the
yolk-epithelium. Two areas can now be distinguished in the egg.
The germ-disc, which tonus the embryonic rudiment and which now
increases by the thickening of its margins (Figs. 112 and 113) only
later extends over the yolk, and a second, the yolk-sac, which at
first is bounded by the two cell-layers, the ectoderm and the yolk-
epithelium. A middle layer is added to the two cellular integuments
which at first cover the yolk-sac, this third layer appearing either
simultaneously with them or very soon after them (p. 277).
The extension of the part known as the germ-disc over the yolk
varies greatly in different Cephalopods. In the egg of Sepia, which
is unusually rich in yolk, the embryonic rudiment is represented only
by a small cup-shaped region of the spherical egg. Here, therefore,
we can best speak of a germ-disc, and the yolk-sac is from the first
very large. In other Cephalopods, indeed, so far as is yet known, in
the majority, the embryonic rudiment and thus also the so-called
germ-disc spread over a much larger portion of the egg (Fig. 115),
but as, at a later stage, the embryonic rudiment again draws back
more towardsHhe animal pole, a yolk-sac is formed in these cases also
(Figs. 116- US). In the Cephalopod investigated by Grenacher,
there is hardly any development of an external yolk-sac (Fig. 126,
]). 270) and the yolk-mass which is comparatively small is here found
enclosed by the embryonic rudiment at a very early stage. This
form would thus have to stand at the end of a series, the starting
point of which would be formed by Sepia with its unusually large
development of yolk. Transitionary forms between Sepia and the
Cephalopod described but not identified by Grenacher would be
found in such forms as Loligo, Octopus, Argonaida, in which the yolk-
sac is more and more reduced and the embryonic rudiment at the
first contains the larger part of the yolk.
If we may judge from the large amount of yolk in the egg (p. 237) and the
large size of the yolk-sac in older embryos (No. 26) the condition of Eledone
in this respect ma}- resemble that of Sepia.
It should here be mentioned that the cleavage and the formation of the
germ-layers in forms which differ somewhat in their later development is, so
far as is known, very much alike, and takes place in the way described above.
In forms in which the rudiment of the embryo can early be dis-
tinguished from the large yolk-sac, the ectoderm, in the region of
the germ-disc consists of cubical cells while in the yolk-region it is
formed of flat cells. During its gradual extension over the yolk,
the blastoderm becomes ciliated. The filiation may extend over the
252 CEPHALOPODA.
whole of the blastoderm or may at first be found only at definite
parts, appearing, for instance, especially at the growing edge of
the blastoderm (Figs. 115 and 116, p. 255). If this ciliation develops
strongly and spreads over the whole of the blastoderm which covers
the greater part of the yolk, as is the case in Loligo, the embryo
rotates within the egg-integument, a phenomenon which recalls the
free-swimming larvae in other divisions of the Molhisca. In Argo-
nauta and Octopus, the only movement that takes place in the embryo
is the shifting of the pole at which cleavage began away from the
micropyle-region to that of the egg-stalk (Ray Laxkester). Some
of the embryos of Octopus are, in fact, found lying at the micropyle
end of the egg and others at the opposite pole : in the older embryos
examined by us the last position was the more frequent.
The ciliation of the embryo either soon disappears, or else is
retained for a long time, as, for instance, in Sepia, where it is found
both in the embryonic region, which is already far developed, and on
the yolk-sac. The embryos of Sepia, however, notwithstanding this
ciliation, do not rotate like those of Loligo, a fact evidently due to
the large amount of the yolk (Kolliker).
Even before the circumcrescence of the yolk by the blastoderm is
completed, indications of the future shape of the Squid appear in the
blastoderm or germ-disc (Figs. 115 and 116 A). We shall describe
the rudiment and further development of the body-form at first in
one of those species in which the blastoderm grows round the yolk
very early and the embryonic rudiment at first encloses the greater
part of the yolk. The ontogeiry of such a form, Loligo Pealii, was
studied in a very thorough manner by Brooks (No. 7). Ray Lan-
kester has also published investigations as to the ontogeny of
Loligo (No. 30) and representatives of this genus, as has already been
mentioned, were studied by earlier zoologists (P. van Beneden, No.
3 ; Metschnikoff, No. 32). Our own investigations, made with
very rich material of Loligo vulgaris, as well as Octopus vulgaris and
Argonauta have enabled us to supplement the discoveries of earlier
observers.
A. Development of the Embryonic Rudiment through its
extension over the greater part of the egg with
subsequent development of a Yolk-sac.
(a) Loligo.
In the region in which cleavage began, i.e., at the animal pole of
the egg, a swelling forms in consequence of the thickening of the
DEVELOPMENT OF THE EMBRYONIC RUDIMENT LOLIGO.
253
cell-layers ; this corresponds to the highest point of the dorsal side,
as may be seen by a comparison with the later embryonic stages.
This swelling, which is the rudiment of the mantle, soon becomes
large, and, in the Loligo examined by Brooks, rests like a cap upon
the embryo (Fig. 115 A), but, in Loligo vulgaris, is less distinctly
marked at this stage. At the stage depicted in Fig. 115 A, the
greater part of the circular margin of this cap-like swelling has risen
up in the form of a fold from the embryonic body (Figs. 116 and 117,
ma), the mantle thus forming in the same way as in the other
Mollusca. As already mentioned, the swelling lies on the dorsal side
and a structure appears here which is comparable with the shell-gland
of other Molluscs. This is an ectodermal depression (Fig. 115 B,
and 116 A, sv/) which at first is shallow but deepens later, and does
R
B
sd
an
s ea-
rn
Sv
\
■ i
I
d r
Fig. 115. — Two early stages in the development of Loligo PecUii (after Brooks), ar,
rudiment of arm ; au, rudiment of eye ; tl, yolk ; m, rudiment of mantle; r, the
ciliated margin of the blastoderm ; sd, shell-gland.
not flatten out again as in other Molluscs (pp. 34, 92, 126), but
becomes a large pouch (Fig. 132, sd, p. 282). This peculiarity is
connected with the fact that Loligo possesses an internal shell.* In
those land-Pulmonates that are provided with an internal shell, we
also found (p. 187) that such a shell-pouch formed from the shell-gland.
There is a certain similarity between the swelling which becomes
differentiated into the rudiment of the mantle and the shell-gland
and the first indications of the eyes which also arise in the form of
swellings each carrying a pit-like depression (Fig. 115 B). They lie
at the two sides of the body below the mantle (Fig. 116 B, au).
* ('/. p. 287, on the significance of the internal shell of the Cephalopoda.
254 CEPHALOPODA.
Other much larger paired prominences are found lower down at the
sides of the body in Loligo Pealii as the first indications of the arms
(Fig. 115 A, ar, Brooks). It seems to be specially characteristic of
this form that the rudiment of the embryo spreads over a very con-
siderable portion of the egg ; in other forms this is not the case, as
may be seen by comparing Figs. 115 A and 116 B.
Orientation of the Cephalopod body. A few words must be said as to the
position in which we have represented the embryo, since it is not that formerly
ascribed to Cephalopodan embryos, which are generally placed with the head
and arms pointing upward. Our orientation of the embryo is in conformity
with the now universally accepted view as to morphology of the Cephalopodan
body, the ventral side being directed downward as is usual in other animal
forms. If we regard the part of the body which lies between the mouth and
the anus as the ventral surface, we have to consider by far the greater part of
the body as the dorsal surface. That end of the body which, as opposed to
the head appears as the posterior end must, according to this view, which was
first adopted by Leuckhart (No. 31), be regarded as the apex of the dorsal
surface. In such an assumption, according to which the ventral surface lies
in the horizontal line, the embryo ought really to be placed obliquely, but
this position was departed from for practical reasons and the head with the
arms was simply directed downward. The (ascending) part of the dorsal
surface which is directed forward will be called the antero-dorsal, and the
(descending) part which is directed backward the postero-dorsal surface.
These points are best illustrated by the median sagittal section of an older
embryo (Fig. 133, p. 283) which cuts through the mouth and the anus.
In the two ontogenetic stages of Loligo (Fig. 115 A and B) as yet
considered, the circumcrescence of the yolk by the blastoderm is not
yet completed, although the rudiments of the mantle (»?), the eyes
(au) and indications of the arms (ar) are pi'esent. At a somewhat
later stage, the yolk appears completely enclosed hy the blastoderm
and a number of new structures appear, especially on the ventral
surface. Among these, the oral aperture deserves special mention ;
this appears as a transverse oval pit somewhat in front of or between
the optic rudiments, this pit arising like those rudiments very early.
In Fig. 116 B the mouth is seen at a somewhat later stage.
In front of the oral aperture a swelling appears (Fig. 116 5, ar),
which runs right round the embryo, being divided into separate pro-
minences. These latter are the rudiments of the arms which thus
appear in Loligo vulgaris in a manner somewhat different from that
described by Brooks in the case of Loligo Pealii. In the latter, the
arms first appear in a very early stage as a pair of prominences, one
on each side of the body (Fig. 165 A, ar),. the individual arms
appearing later by the breaking up of these. There is no mention of
DEVELOPMENT OF THE EMBRYONIC RUDIMENT LOLIGO.
255 l
a circular swelling such as foreshadows the development of the arms
in L. vulgaris (Fig. llii B, dr). Further, in L. vulgaris, the indi-
vidual arms develop more distinctly in consecutive order, the first,
which appear as button like prominences, being those which lie next to
R
r.-Sd
Fig. 116. — Various stages in the development of Loligo vulgaris (original). A, early
stage at which the eyes ami the shell-gland appear ; B, seen from the oral side ; G
and D, from the anal side. 1> is seen obliquely from above, and for the sake of
clearness, rather more of the yolk-sac is shown in this figure than is actually visible.
ar, rudiments of the arms ; ",-"-• lirst three pairs of arms ; au, rudiments of eyes, or
the swellings that carry the optic pits ; d, yolk; ds, yolk-sac; htf, posterior funnel-
folds ; k, gills ; between the two branchial prominences lies the rudiment of the anus ;
m, oral aperture; ma, mantle : ot, otocysts ; r, edge of the blastoderm ; sd, shell-
gland ; vtj\ anterior tunnel-fold.
the funnel. At this period, the rudiments of various other organs are
already visible, the most striking of these being the paired branchial
fold (Fig. 116 C, /.) which lies immediately in front of the mantle
256 CEPHALOPODA.
(ra). In front of and somewhat laterally to these folds, a rather long
paired ridge appears (O, htf) running at first almost parallel with the
branchial folds; it then passes back round the "mantle" at the
margin of which it can be seen even on the opposite side of the embryo
(i.e., when the embryo is viewed from the oral side, B, htf). This
paired ridge, which appears very early, assists in the formation
of the funnel, the chief part of which, however, is derived from a pair
of folds which arises somewhat later more anteriorly (0, vtf). These
two pairs of ridges will be distinguished as the posterior (htf) and
anterior (vtf) funnel-folds. At first they are not prominent, and this
is still the case with the anterior pair at the stage depicted in Fig.
116 C, but they rise up more and more and then become very con-
spicuous (Fig. 141, //•, p. 297). Between the anterior ends of the two
posterior folds a slight curved prominence appears, apparently uniting
the folds of the two sides (D). A very narrow superficial prominence
now also connects the anterior folds ; this latter fold is the first
indication of the complete connection of the two anterior folds which
takes place in later stages (Figs. 117 and 118).
When the anterior funnel-folds appear, two vesicular depressions
of the surface are seen behind them (Fig. 116 C, ot ; Fig. 141 A,
]). 297) ; these are the otacysts which, when the posterior funnel-folds
shift forward, are found lying near them (Figs. 116 Z> and 117 A and
B). They lie also in the closest proximity to the large swellings
which carry the optic pits. These swellings, which are very large
even in an early embryonic period (Figs. 116 A and 115 B, au),
continue to increase in size, and give the Cephalopodan embryo a
highly characteristic appearance at the stage just described and
especially in the following stage (Figs. 117 and 118). Only a part
of these large projections is yielded by the eyes themselves which
first appear on them in the form of depressions (Fig. 116 B). These
depressions close later, a second depression then forming above the
first (primary) optic vesicle, and the lens being secreted inwards at
this point (<■/. Figs. 142 and 143, pp. 298 and 299).
The formative processes hitherto described affect merely a limited
part of the egg, for the embryonic rudiment which extended earlier
over the larger part of the egg (Fig. 11")) has drawn back more
towards the animal pole. There is therefore a part entirely free from
the rudiments of organs, formed only of the yolk-mass and enclosed
by several cellular integuments (Fig. 133, p. 283). This is the
yolk-sac, which in later stages is much more distinct, the embryo
becoming marked oft' from it by a constriction (Figs. 117-119). The
DEVELOPMENT OF THE EMBRYONIC RUDIMENT — LOLIGO. 257
yolk-sac may contract (Kolliker, Metschnikoff) and, according
to Ray Lankestek, carries out rhythmical movements which are
made possible by the fact that its envelopes do not consist, us is
generally supposed, merely of a layer of ectodermal cells and another
of entodermal cells, but also of a mesodermal layer intercalated
between these (Fig. 133) which evidently contains contractile elements.
This mesodermal layer, the presence of which in a number of other
Cephalopods {Sepia, Sepiola, Octopus, A rgonauta) has been established
through the examination of sections, seems only slightly developed
in the forms which have smaller yolk-sacs, but in those with large
yolk-sacs as, for instance, Si-j>i'i, this layer is highly developed, long
straight, Hhredike cells here lying one above the other.
It appears that, by the contraction of the yolk-sac, its contents
are pressed into the interior of the embryo, extending far into the
embryonic rudiment (Figs. 132 and 133, p. 282). A distinction is
therefore made between the outer and the inner yolk-sac, the latter
extending as far as to the mantle and into the optic swellings. Here
also it is enclosed in the "yolk-epithelium"' and does not, as lias
been assumed, stand in direct communication with the intestinal
canal of the embryo, so that the yolk-suhstance can he utilised by
the embryo only with the help of the yolk-epithelium. As the yolk-
sac extends so far into the embryo, the surfaces are in contact over
a very large area, a fact which explains the absorption of the yolk
without direct communication existing with the intestine and with-
out the intervention of special vessels. The whole embryo (including
the yolk-sac) increases .in size during development, the later stages
1 icing much larger than the earlier.
Although the great development of the external yolk-sac at first
recalls the conditions which prevail in the Vertebrates, some difference
is brought about in the Cephalopoda by the fact that the yolk-sac
is here devoid of any direct communication with the intestine.
Special vessels also seem to he wanting in the yolk-sac, as already
mentioned, and it therefore enters far into the embryonic body.
Further, the yolk-sac in the Cephalopoda is ventral, its position at
the anterior end of the body surrounded by the arms being merely
apparent. In reality, it lies ventrally (between the mouth and the
anus) and a comparison of Pigs. ll(i II and D, and 113, p. 248,
shows that the mouth lies at one side of the yolk-sac (the anterior
side) and the anus at the other (posterior) side.
It has already been mentioned (p. 254) that the mouth appears as
a rudiment at an early embryonic period (Fig. 116 />')■ The anus
s
258 CEPHALOPODA.
docs not appear until later, sinking in at the middle of a slight
prominence, the anal papilla (Fig. 116 D) ; the posterior part of the
intestinal canal, starting from this point, runs towards the mantle,
its course being externall}- marked by a slight rising on the surface
(Figs. 117 and 118).
In the embryo of Loligo Pealii, at a stage intermediate between
those depicted in Figs. 116 B and C we find, in the oral region,
starting from the two angles of the mouth and running first to the
optic pits and then passing anteriorly, two rows of cilia; these have
been compared by Bkooks with the velum, i.e., with the pre-oral
ciliated ring of other Molluscan larvae. We should, in tins case,
have to regard the part including the eyes and the very limited
region between them as the pre-oral part of the body.
Among the changes which take place on the dorsal side of the
embryo, those that occur in the mantle exercise a special influence
on the external form of the animal. The pit representing the shell-
gland which, at first, is very wide (Fig. 116, sd) narrows with time,
and in later stages is only a small aperture (Fig. 117 B) and finally
closes entirely. The external aperture of the continually deepening
| lit becomes surrounded by a kind of circumvallation, the surface
again sinking in, though not to any great extent (Fig. 116 D). The
almost rhomboidal swelling [m) which surrounds this shallow de-
pression represents the marginal part of the mantle which now
begins to rise above the rest of the bod}'. At a slightly later stage
(Fig. 117 A), we find the mantle becoming marked off by the
swelling of its margin. The large depression round the circular wall
of the shell-gland flattens out again and becomes rounded off like the
edge of the mantle itself (Fig. 117 I>). Two pointed prominences,
the rudiments of the fins, are visible upon it (Fig. 117 A and />').
Another change has taken place in the mantle-region on the
dorsal side, the posterior funnel-folds having shifted more towards
the middle line, there ending in a kind of plate which is the rudiment
of the nuchal cartilage (Fig. 117 IS). The posterior funnel-folds are
thus recognisable as the broad muscle-bands (the so-called nuchal
muscles) which even in the adult appear as lateral continuations of
the funnel. They run to the nuchal cartilage and become attached
to it.
In tracing the further development of the funnel, we find that the
anterior folds form the essential factor in determining the alterations
that take place in its principal parts. These anterior folds, which
soon rise much higher than the posterior folds, become united in the
DEVELOPMENT OF THE EMBRYONIC KUDIMKNT I.OMGO.
■J.V.I
ventral middle line (Figs. 116-117). At first they form together
merely a slightly undulating line (Fig. 117 A), but their lateral ends
soon bend back further (Fig. 117 A') and as the folds at the same
time swell up more, the later form of the funnel becomes indicated
(Fig. 118 A and /!). At the same time, the posterior funnel-folds
become modified in shape, now appearing forked at the point where
they come into contact with the anterior folds (Fig. 118 A). This
is caused by the rise of a new fold at this point, which runs towards
the mantle. This is, like the other folds, an expression of the
greater growth of the mesodermal tissue and represents a part of the
retractors of the funnel (muse, depressores infundibuli).
A
B
mi
ds
Fig. 117. Two stages in the development of Loligo vulgaris (original). .1. seen fr
the anal or funnel-side ; /<'. obliquely from above. (The remarks made on Fig. 116
/' apply to B). "j "-;. first three pairs of anus; au, optic swelling; ds, yolk-sac;
hif. posterior funnel-fold ; /.-, branchial folds or gills ; ma, mantle ; nk, nuchal carti-
lage ; ot, otocysts ; vtf, anterior funnel-fold. The circular fold out of which the
arm-rudiments arise can still be recognised, especially in .1. In B, the long promi-
nences indicating a pair of arms (lying behind "-) still form part of it. The funnel-
folds [vtf and hii) meet in the middle line. Between the two gills (k) lies the
impaired anal papilla; on the mantle, are the two prominences representing the
rudiments of the tins [cf Fig. 118,/).
In the adult, these muscles are attached to the funnel laterally, some of
t hem running further forward to end within the funnel and in its dorsal parts.
This is perhaps indicated even in the embryo iFigs. 117 and 118) by the
course of the anterior folds, but we have hitherto been unable to make any
careful examination of the fate of these raised parts which anteriorly become
connected with the posterior funnel-folds, and must therefore refrain from
conjectures as to their significance.
260
CEPHALOPODA.
It is evident from the above that not only do the anterior funnel-
folds from the two sides unite to form a common fold but that the
posterior folds also fuse with the anterior. At the point of junction
of these two sets of ridges, the posterior folds appear as a mere pro-
longation backward of the anterior (Figs. 118 and 119). By this
process and by the simultaneous extension of the anterior folds, the
funnel has already approximated closely to its final shape (Fig. \\9).
The free edges of the two anterior folds become apposed, but do not
as yet fuse (Figs. 141, tr, p. 297 and 143, /, p. 299) and the funnel
a
B
on.
Fig. 118. — Two embryos of Loligo vulgaris, seen from the posterior or funnel-side
(original). LH.(>.
261
as an unpaired fold (Brooks).
.-fl
120 .1 and />', hin). They continue to increase in breadth and
represenl the nuchal muscles (musculi collares) which, together with
the retractors (Fig. 120 .1, rt) that run backward direct to the
mantle, form a kind of lateral chambers, not communicating with
the actual funnel, i.e., with the middle funnel-cavity. The fv/txnel-
valve appears in the anterior part of the funnel, i.e., in the wall
which is in contact with the body,
While the changes just described
have taken place in the funnel,
the mantle also has undergone
repeated modifications of form. It
now rests like a cap on the end of
the body ( Fig. I is, ma) as its
edge has extended forward further
and has become raised from the
body. The further growth of this
overhanging margin leads to the
formation of the mantle-cavity,
into which the gills are drawn, these
not having essentially, changed
their shape (Fig. 118, /•). The
increase in size of the mantle is now
the chief feature of its develop-
ment (Figs. 11S-121). The tins
at its upper end also increase in
size. The optic swellings have
become very la rue. It has already
been pointed out that in this way
the embryo acquires a specially
characteristic appearance which it
retains in later stages also (Figs.
I I'll J and IS).
We have so far mentioned only tin' first stage in the rise >>' the
nrms (p. 254). From the circular fold which runs round the whole
embryo at the boundary line between the embryonic rudiment and
the yolk-sac (Fig. 1 1 (i B, ar), the separate prominences which repre-
sent the arms become differentiated, each first appearing as a long
.-welling which soon assumes a button-like form (Fig. 1 16 B-D). The
first pairs of arms to become distinct are the two that lie nearest
the funnel, the second pair of arms, however, in Lolujo attains a far
higher degree of development than the first and than the one that
Kn,. 119.— Older embryo of Loluju
mdgaris, seen from tlie posterior
or funnel-side (original). /,; tunnel.
The rest of the lettering as in Fig.
U.S. The gills lie p.utly hidden
by the overhanging margin of the
mantle; between them is the anal
papilla.
262
CEPHALOPODA.
follows it, a distinction which is retained in later stages. This pair
of arms, the prehensile arms, is soon followed by a third pair (Fig.
116 C and D). When the first three pairs have become distinctly
differentiated as button-like prominences, the other two which lie
nearest the mouth are still mere transverse swellings : the first of
— met
an
a
-■®mL
w
/
\
ds
Fig. 120. -Two older embryos of Loligo vulgaris, .1, seen from the tunnel side, B'
from the oral side (original). ",-"i- arms; aw, eyes; ds, yolk-sac ; ft, tins; km,
nuchal muscle ; ma, mantle; rt, retractor of the funnel (tr). In .1, the gills project
below the mantle : between them is the anal papilla.
these to become distinct is the fourth, then follows the fifth.* As
the embryo continues to develop, the arms grow in length, and the
sucking discs appear on them. The change of shape undergone by
* In speaking here of the first to fifth pairs of arms, they are numbered
according to the order in which they originate in the embryo, not according
to the order sometimes adopted (for which we can see no good reason) in
which, on the contrary, the pair of arms which lies furthest dorsally counts
as the first and the most ventral pair as the fourth, the prehensile arms being
reckoned separately, evidently on account of their different development,
which seemed to give them a claim to a special position.
DKVKLOl'MKXT OF THE EMBRYONIC RUDIMENT LOLIGO.
263
the embryo in rising up from the yolk produces a change in the
position of the arms which shift from the funnel-side more towards
the oral side (Fig. I 17-120).
In Loligo Pealii, the three pairs of arms depicted in Pig. L15, ar, deve
first ;m-/)). although it can also be recognised in older embryos
i Fig. 120 .1 and A). The mouth here still lies outside of the circle
of arms, but soon shifts within it (Fig. 120 B) or rather is surrounded
by the arms as they shift dorsally. This occurs simultaneously with
the degeneration of the yolk-sac that now begins. The mouth finally
ds
Fig. 121. < flder eninryo ol
Loligo vulgaris, seen from
the posterior or tunnel-side
(original), a, the arm- oi
the second pair and be-
tween them the first pair
of arms ; an, <•> es ; ds,
yolk-sac : ,/'. fins ; /.-. gills ;
between the two gills js
the anal papilla; tr, funnel.
The embryo is alreadj
covered with chromato.
phores.
264 CEPHALOPODA.
occupies the place of the yolk-sac, i.e., is surrounded by the arms, a
position which, as is well-known, is occupied by it in the adult.
When the yolk-sac begins to degenerate, i.e., in the last stages of
development, the embryo approaches ever nearer the form of the
adult (Fig. 121). The arms are still rather small, the eyes still
remind us of their former condition, but the funnel, the mantle, the
gills and the anal papilla have almost attained their final form. The
chromatophores have already formed and they also give the embryo
a characteristic appearance more like that of the adult. The
ch rowatophores appear first on the mantle on the posterior (postero-
dorsal) side and are only somewhat later found on the arms and on
the head. When the embryo leaves the egg, the external yolk-sac
has, to a great extent, disappeared.
(b) Octopus.
Although, systematically, Octopus is far removed from Loligo, the
course of development of the two forms is very similar. The em-
bryonic rudiment extends at first over a larger part of the egg and
later withdraws again more towards the animal pole, just as in Loligo.
The shell-gland appears very early, at a time when the blastoderm
has not yet grown round the yolk, as a depression at the animal pole.
This fact is of special interest, because Octopus, like most other
Octopoda {Cirrhotenrihis perhaps forming an exception?) has no
internal shell. The shell-gland in this case, therefore, has the
significance of a vestigial orpin. At somewhat later stages, when
the rudiments of the external organs appear, it can be recognised as
a distinct depression at the apex of the rudiment of the mantle, and
even later is perceptible (Fig. 122 A). According to Ray Lankester,
it disappears without having closed.
At a stage somewhat earlier than that illustrated in Fig. 122 A, a
pair of small prominences appear on the mantle, resembling, in shape
and position, the fins described in Loligo. Indeed, the aspect of the
mantle-rudiment in Octopus in the younger stages closely resembles
that of the mantle-rudiment of Loligo. The prominences are retained
for some time; they can be recognised in Fig. 122 J and B, and in
later stages arc still present, but, finally, they decrease in size and
altogether disappear. They cannot be regarded as anything else than
the vestiges of a pair of fins, and must be considered as an indication
thai tin- Octopoda originally carried fins, like the Decapoda. This
fact affords further support to the view which in itself is probable
DEVELOPMENT OF THE EMBRYONIC lU'lHMENT — OCTOPUS.
265
that the Octopoda must be regarded as derived and the Decapoda as
primitive forms. The conjecture as to the nature of these promin
ences is further rendered probable by the fact that tins occur in some
adult Octopoda (Octopus menitoanaceux, Pinnoctopus, Girrhoteutliis).
The oral aperture appeal's in Octopus at a very early stage and
SOOl) takes the shape of a semicircular groove bordering a swelling.
The appearance of the rudiments that lie on the ventral side closely
resembles that described for Loligo and will best he understood h\
a study of Fig. [22 A and B, and by comparing this figure with the
illustrations of the Loligo embryo given in Figs. 117 and lis.
It should be noted that the funnel forms, in the Octopoda, in the
same complicated way as in Loligo and the other Decapods. A paired
posterior fold appears and, in the course of development, unites with
an anterior fold which is also paired to form the funnel and its lateral
parts (Figs. 122 and 123, hff, vtf and /•/).
Fig, 122. — Two embryos of Octopus vulgaris at different ages, seen from tin- posterior
side (original). ar, arms : aw, optic swellings ; ds, yolk-sac ; htf, posterior funnel-
told ; / , ui]l> : /". mantle ; "'. otocysts ; vtf, anterior funnel-fold.
In comparing Loligo and Octopus, we are struck by the tact that, in the
latter, the separate organs appear very early, hut do not develop further with
corresponding rapidity, so that, as contrasted with organs that appear later,
their development is retarded. This peculiarity was pointed out by Brooks
(No. 7), in comparing the form examined by him (Loligo Pealii) with
Grenacher's Cephalopodan embryo. In Octopus, for instance, the rudi-
ments of the arms appear early, their number being complete even earlier
than the stage depicted in Fig. 122 .!, hut they then develop very slowly.
With regard to the order in which the arms appeal1. this seemed to us to be
the same as in Loligo, i.e. from the rudiment of the funnel towards the
mouth. Two pairs of arm- appear :i- slight swellings in front of. the optic
266
CEPHALOPODA.
prominences; a third and a fourth pair are soon added; this latter pair, i.e.,
the one near the mouth, the most dorsal of the.
arms, is always the least developed. The pairs
of arms appear very quickly one after the other,
so that the above statements are made with a
certain reserve.
In tlm development of Octopus, it is of
special interest that the yolk-sac is some-
what less developed than in Loligo, as is
evident from a comparison of Figs. 122 and
123 with Figs. US and 119, p. 261. In
earlier stages, this difference is less marked ;
later, on the contrary, it is still more notice-
able. In itself, this comparatively slight
difference in the development of Octopus
would be hardly worthy of note, but it
affords a transition to those forms in which
Octopus, seen from the
funnel - side (original). the yolk-sac develops still less (Argoitauta)
('/■.arms; mi, optic swell- ".,... , ,
• »_ ". . .... ,,..l..,..l ... ..l +- ..l*-. 4-\ *.:~ ...
Fig. 1:
do,
-Older embryo of
ings ; inn, nuchal muscle ;
rt, retractor muscle of tbe
funnel (tr).
or, indeed, is almost altogether wanting
(Grenachek's ( lephalopod).
(c) Argonauta.
Argoiututa, in its development, also closely agrees with the forms
hitherto considered. Special interest attaches here to the appearance
of the shell gland at an early embryonic stage and to its retention
for a long period, although the shell of the adult does not develop in
it, having another origin and significance, as will be shown later, p.
294). The shell-gland, as in Octopus, is said gradually to flatten out
again (Kay Lankestek, No. 29 ; Ussow, No. 44, p. 352), and the
Argonaut shell forms after embryonic life is over, as was shown by
Kolliker in opposition to former statements (Nos. 24, 1 and 9).
The embryos of Argonauta show, at various stages, in the rise of
the different organs, great similarity with the Cephalopods already
considered (c/., the late stage depicted in Fig. 124) especially with
the embryos of Octopus and Loligo of about the same age (Figs. 123
ami 119), but the small size of the yolk-sac seems to determine a
more compact form of body.
As in Loligo, the embryonic rudiment at first extends over a large
part of the egg, but becomes at a later stage more concentrated,
withdrawing more to the animal pole, and rising from the volk, thus
DEVELOPMENT WITHOUT ACTUAL XOLK-SAC.
267
giving origin to an external yolk-sac which, however, is nor nearly
m> large as in cases already mentioned
(Fig. 124). As development advances, this
yolk-sac decreases in size, and, in mature
embryos, at hatching, there is not any
i race of it.
The differences in size and shape of body
existing between the two sexes of Argonauta,
also rind their first expression during posl
embryonic life. Xo sexual dimorphism
could be observed in any of the many
embryos examined by us. This applies
also to the strikiug hectocotylised arm of
the male, which in other Cephalopods
also, becomes differentiated only us sexual
maturity is gradually attained. Mature
embryos of Octopus, Loligo and Sepia show
no siejn of this modification ; This is the less strange as the arms
are still far from being fully developed in these embryos.
Fig. 124. — Embryo of
Argonauta argo, with
funnel still incompletely
developed (original), or,
arms ; an, eyes : ds, yolk-
sac ; hm, nuchal muscle ;
m, mantle ; tr, funnel.
B- Development without actual yolk-sac.
The description of the above forms may best be followed by that
of the Cephalopod observed by Grenacher (No. 14), a form the
systematic position of which has not yet been determined. It
probably, however, belongs to the large division of the Oigopsida,
perhaps to the genus Tuuthis. Streenstrup (No. 42) believes
that it resembles Ommastrephes (see also p. 236). The eggs, unlike
those of the forms hitherto mentioned, are spherical and distinguished
by the violet colour of the yolk which elsewhere is yellow. They
are about 1 mm. in diameter, and thus much smaller than those
of Argorviuta. This is a remarkable fact since, judging from the
quantity of spawn and the number of eggs contained in it (p. 236),
this Cephalopod is most probably a large animal. The small size
of the eggs, and the small quantity of yolk contained in them afford
an indication of the manner of development of this form, which is
marked l»v an almost entire absence of the external yolk-sac.
* The number of eggs laid by the female Argonaut is very large so thai a
considerable number of embryos are to bo found in bhe egg-bunches within
the shell. The eggs to which we had access belonged to various females and
were at different stages of development, and, although no fully mature embryos
were found by us, we were justified in forming the above conclusion Erom those
in a late stage of development.
268
CEPHALOPODA.
Since, in Grenacher's Cephalopod, we apparently have a comparatively
primitive form, it has been thought that paucity of yolk might be regarded
as the primitive condition. So long as the first ontogenetic processes are not
known, no decided opinion can be given on this point, but the development
of this form in general shows such close similarity to that of other Cephalopods
that a reduction of the yolk seems more probable. We may also regard the
early appearance of the chromatophores which elsewhere appear late as
secondary (see below). Although the Oigopsida are very primitive forms among
the Cephalopods now living {Nautilus and Spirula excepted) they themselves
appear highly specialised when fossil Cephalopods are taken into account.
There is a great gap between them and the forms with chambered shell, and
yet Nautilus even has large eggs rich in yolk, as is shown by examination of.
the ovary (Owen, No. 33). [The egg-capsule measures 45 x 16 mm. and the
actual egg is 17 mm. long (Willey, No. IV.). — Ed.]
The earliest development seems to agree with that of the other
Cephalopods. A blastoderm forms which, however, in this case very
soon grows round the yolk. Even
before distinct rudiments of organs
can be seen on the blastoderm, it
has grown almost to the vegetative
pole, leaving only a small portion
of the yolk free (Fig. 125). The
growing edge of the blastoderm is
beset with cilia, but these do not
lead to any rotation of the embryo.
The first indication of organs is
the appearance at the animal pole
of star-like cells containing red
pigment, which rapidly increase
in number (Fig. 125. ch). These
are the chromatophores which thus
form, not as in other ( lephalopods,
towards the end of the embryonic-
period (Fig. 121), but, strange to
say, arise quite at the commencement of that period. They soon
spread over the upper third of the blastoderm, at the edge of which
a circular fold now forms. The upper pigmented part of the embryo
thus rises from the rest of the body as the rudiment of the mantle,
this process beginning at the postero-dorsal surface, i.e., in the
neighbourhood of the future anal pit, and proceeding towards the
antero-dorsal surface. During these differentiations, the originally
spherical embryo becomes cylindrical. In Fig. 126 A and 11 the
b'K
N&
a
125. Young embryo ot Gkena-
cher's Cephalopod at the stage In
which the blastoderm grows round
the yolk (after Grenacher). cA, chro-
matophores; d, yolk : r, margin of the
blastoderm.
DEVELOPMENT WITHOUT ACTUAL YOLK-SAC. 269
rudiment of the mantle is seen in a later Btage thickly covered with
chromatophores.
It is curious i hat ( , optic
vesicle; au, rudiment of eye; ch, chro-
matophores'. ds, yolk-sac ; '). This makes the
processes of development somewhat more difficult to understand, but
we are assisted in following them by comparison with the same
processes in eggs less rich in yolk.
The first indications of the embryo on the germ-disc take the form
of various prominences and swelling's which soon show bilateral
symmetry in their shape and arrangement. Tins symmetry most
probably corresponds to that already evident in the germ-disc during
DEVFLOl'RIENT OF SEl'IA.
273
,'-P.i
!■>
II.
cleavage (see Fig. 109, and Fig. 110, of Loligo). The swellings
of the surface which at first are very vague and indistinct, become
gradually clearer and can soon be recognised as the rudiments
of the different organs, one of the first to grow distinct being a
circular depression at the centre of the germ-disc. This becomes
surrounded with a flat wall which is more or less pentagonal with
rounded corners (Fig. 12^ A, sd, and ma). This represents the
rudiments of the shell-gland and the mantle, in the early appearance
of which Sepia resembles
the other Cephalopods J{
already described.
Two broad prominences
which, at an earlier stage,
occupy almost half of the
germ-disc, may, following
Kolliker, be described
as cephalic lobes. A large
I lit appearing on each of
them identifies them as
those highly developed
structures which, in other
( iephalopods, we regarded
as the optic swellings.
In Fig. 128 J, they are
represented at a some-
what later stage (//).
The divergent character
of the development of
Sepia is specially shown
in these structures, which
here appear on an almost
flat surface ; elsewhere
they form two large and
very prominent swellings,
one on either side of the
body.
The germ-disc, on the side opposite to the optic swellings, is
bordered by a narrow band-like prominence which at fust is almost
semicircular but soon extends round the greater part of the germ-
disc and then resembles an incompletely closed circular swelling.
This corresponds to the circular swelling which, in Loligo, runs round
Y
A KL
■ct
*?>■
<£%.
• -.i -
^vtf.
a,.
\
a..
s£.
Fig. 128. — Germ-discs with young embryonic
rudiments oi' Sepia officinalis (after Vialleton
and Kolliker). a, anus ; Oj-ag, the five pairs of
arms ; au, rudiments of eyes ; ktf, posterior funnel-
fold ; k, gills ; //, cephalic lobes : hs, germ-disc ;
in, oral aperture ; ma, mantle ; /of ^the rudiment, of the organs already present. The
covers the gills, only parts of which project from beneath it (Fig
"' ''• k)\ ' ,';'. ™diment of th* -nus (a) appears between the gills.
A depress^ which at first is crescent-shaped appears on the opposite
%«* e7fe^ulteat^ edge of the germ-disc; thisTs the
The /W>bW. also deserve mention. They have now united,
"<<1 the principal parts of the
funnel can ahvady be made
out in them, viz., the anterior
folds (vtf) which yield the chief
part of the funnel, the lateral
parts (nuchal muscle, km) which
run back to the nuchal cartilage
(nk) and, finally, the retractor-
folds (rf) which run towards the
gills. These parts are, indeed,
far less distinct than in Loligo
(Fig. 117 A and B, p. 259),
but are nevertheless homologous
with the similarly named struc-
tures found in that genus. The
origin of the funnel from two
halves is, on the other hand,
more distinct, that organ being
formed here, as in Loligo,
through the rising of the two
anterior folds which, after
obtaining in this way an increase
of surface, bend toward one
another and fuse (Fig. 129 (?)
FiG.129.-Germ-discs and embryos of Sepia
officials, lying upon the yolk-sac. I
and /,, seen from the oral side ; (J, from
the anal side (after KoluKER). „ ,.
arms; an eyes ; ds, yolk-.,,; ,/, tj'.
hm nuchal muscle ; htf, posterior funnel
tolds; k, gills; Ja, cephalic lobes; Jes
germ-disc; m, mouth; ^.mantle oi
otocyste; rt, retractor of the siphon-
vtf, anterior funnel-folds.
l.o principal part of the funnel derived from two half tubes
tln.s comes to lie in front of the mantle ; its posterior aperture is
turned toward the latter and opens into the mantle-cavity after the
mantle has grown over the funnel. The narrow anterior aperture
is turned away from the mantle.
In adult Cephalopods, the efferent aperture of the funnel is directed to
wards the mouth, for the funnel lies on the ventral surface between he anal
and oral apertures (Figs. 120 and 121, p. 262). In the early stages of ££
276
CEPHALOPODA.
embryos tins is not self-evident, as apparently different conditions are brought
about by' the intercalation of the yolk-mass and the superficial extension o
the germ The efferent aperture of the funnel does not appear to be directed
towards the mouth but rather turned away from it (Fig. 128 B). A com-
parison with the embryos of Loligo shows, however, that quite the same
conditions prevail in the two cases. If we imagine a LoUgo embryo, such as
the one seen obliquely from above in Fig. 117 B, p. 259, spread out flat, we
should find that the anterior aperture of the funnel is here also turned away
from the oral aperture which lies on the further side of the mantle and, apart
from the modifications peculiar to the LoUgo embryo, we should have a view
something like that given in Fig. 128 B.
The further development of the Sepia embryo is characterised by
the fact that its superficial extension is arrested and it rises up from
the yolk-sac, the yolk then pressing in beneath the arched embryonic
rudiment; in this way, an internal yolk-sac is formed as already
described for LoUgo. The rise
of the embryo from the yolk
is very gradual, and has a fairly
similar effect on the different
organs. Fig. 129 A-C repre-
sents a few stages in this
process. In the first two, the
embryo is seen from the oral
side. The posterior funnel -
folds (hit) at first still lie rather
far from the mantle, but the
latter, by extending laterally,
soon projects beyond them. At
the same time, the mantle
bends over and thus begins to
assume its final shape. 1 lie
embryo in its further rise from
the yolk is also followed by
the cephalic lobes and the
eyes, organs which, as in Loligo,
at this time and even later form
the largest part of the embryo
(Fig. 129 B). Fiff. 129 G,
m.a
OM
Fig 130.— Older embryos of Sepia officinalis,
seen from the oral side (after Kolliker).
The yolk-sac, near the embryo ought to
be narrower. Lettering as in Fig. 129.
representing the embryo at a somewhat later stage from the anal
side, shows its great resemblance in external shape to the
embryos of Loligo at about the stage depicted in Fig. 119, p- *>1.
The -ills are not yet completely grown over by the mantle; the
FUBTHEK DIPPEBENTIATION OK THE GERM-LAYERS, ETC. 277
junction of the two posterior funnel-folds has taken place but these
folds have not yet fused in the median line. On the mantle, the
tins are visible, these apparently forming late in Sepia. The mouth
lies at the opposite side; its position can be ascertained from
Fig. 130 of a later stage. The yolk-sac is still very large, and is
directly connected with the internal mass of yolk. As the yolk-sac
is gradually absorbed, the large cephalic section decreases in size,
approaching the final shape of the adult Sepia. By the time that
the embryo is mature and ready to hatch, the greater part of the
external yolk-sac has been absorbed. Only after its complete reduc-
tion can the arms occupy their final position round the month. At
hatching, they are still rather short, and only attain their full length
during free life. The prehensile arms which, as rudiments in Sepia
also, are not specially distinguished from the others (Figs. 128 and
129), become characterised at later stages not only by their length
(Fig. 1:50, a) but also by their bases sinking into the body. The
depression thus caused is, in older embryos, visible even externally
in the form of a horse-shoe-shaped fold lying above the first pair
of arms.
4. The further differentiation of the Germ-layers and the
formation of the Organs.
A. The separation of the Germ-layers and the formation of the
Yolk-epithelium and the Alimentary Canal.
Only after the external form of the body is known is it possible to
enter in detail into the further development of the germ-layers.
These, in the Cephalopods, develop very late, or rather, they do not
appear so distinctly here as in the other divisions of the Mollusca.
As we have already remarked, the great accumulation of yolk in the
embryo has, in this direction also, essentially modified the ontogenetic
processes.
Our description of the body-layers was interrupted at the stage at
which there had formed, at the margin of the germ-disc which covered
only a small part of the egg, a peripheral thickened ring (Fig 112,
p. 247 and 131 J) and cells became detached from the edge which,
according to the view adopted by Vialleton, wandered beneath the
superficial cell-layer (Fig. 114, p. 250) there to give rise to a con-
nected layer. This lower cell-layer then extends over the whole yolk,
and is followed by a middle layer * so that the yolk is now surrounded
* See also p. 126, etc.
27* CEPHALOPODA.
by three cell-integuments. Yolk-cells are not found in the Cephalo-
poda, and the yolk thus attains, in them, a greater independence
than in the eggs of most Arthropoda and Vertebrata, which are also
very rich in }rolk.
Very different conclusions have been arrived at as to the signifi-
cance of these cell-layers. We shall consider first the inner layer,
the so-called yolk-epithelium.
The yolk-epithelium is formed of large flattened cells which are
swollen in the region of their nuclei. The only function of this layer
is to yield an envelope for the yolk, and to bring about its utilisation
by the embryo. In later stages it is found surrounding the yolk still
in the same state as before. The yolk, especially in the typical forms
of Cephalopodan development in which it is plentiful, is accumulated
principally in the external yolk-sac. This latter is directly continuous
with the mass which lies now within the developing embryo (Fig.
132) ; at a later stage, in consequence of the processes of growth
that take place in the embryo, a constriction forms in the region of
the arms (Fig. 120, p. 262), and a rather narrow duct here arises
connecting the external with the internal yolk-sac (Fig. 133, a, ds,
and i, ds). In this latter, again, various parts may be distinguished
as lying respectively in the cephalic, the pallial, or the nuchal region.
The part lying in the head gives off two outgrowths into the optic
stalks, the nuchal portion narrows later and leads to the voluminous
pallial portion. The embryo no doubt absorbs the yolk in the follow-
ing way : the external yolk-sac passes on its contents to the internal
sac, partly in consequence of the rhythmic contractions of its wall and
partly in consequence of the processes of growth in the embryo itself,
1 1 ion the nutritive masses are conducted to the embryo from the inner
yolk-sac through the intervention of the yolk-epithelium. Since, so
far as we know, there are no vessels in the external sac, its dis-
appearance cannot be accounted for in any other way.
It has already been pointed out that the yolk-epithelium is a
closed unilaminar layer of cells extending round the whole yolk. In
consequence of its close connection with the yolk, the yolk-epithelium
must certainly be regarded as the inner layer of the Cephalopod
germ. The question now arises, What is its relation to the futun
entoderm .' This latter first becomes perceptible in the Following
way.
About the time when the first rudiments of organs appear ex-
ternally on the embryo, there is seen, on the ventral side, contiguous
to the yolk, an epithelial plate which at first consists of only a few
THE SEPABATION OF THE GERM-LAYERS, ETC. 279
cells. 'This is the first indication of the enteron, which soon increases
somewhat in size (Fig. 13] D, iml) and finally separates from the
yolk and appears sac-like (Fig. 132 A, nnl). Beneath it, the yolk-
epithelinni is now seen, which, in earlier stages, was wanting at this
Spot ( KoRSCHELT, Xo. 25).
The sac-like rudiment of the enteron was known long ago and it
was assumed, with great probability, that it might be connected
with the yolk-epithelium, and thus to a certain extent might be
regarded as an outgrowth of the latter (Kay Lankester, Vialleton,
Bruce). The two together would represent the entoderm, the
vesicle being regarded as the permanent and the yolk-epithelium as
the provisional part of the entoderm. Bobretzky, on the other
hand, considered that the vesicle arose as a mere differentiation of
the lowest cell-layer of the middle layer, i.e., of the so-called
" mesoderm." There, indeed, appear to be no yolk-epithelium at the
stage when the epithelial plate above described as the first indica-
tion of the enteron forms, either beneath that plate or in its near
neighbourhood, and this has led to the assumption that the cells of
the yolk-epithelium as well as the enteric plate arose as differentia-
tions of a cell-layer which grew from the edge of the germ-disc
towards its centre.
This last view seems not without justification because it is very
difficult to decide whether the yolk-epithelium pi'esses beneath the
germ-disc (Fig. 114, p. 250) or whether these cells are differentiated
from the whole cell-mass. The cells which are directly in contact
with the yolk actually bear a very close resemblance to those of the
middle layer.
These questions are of importance as determining the manner in
which the germ-layers form. We have to imagine that the cell-mass
pressing from the edge towards the centre of the germ-disc (Fig. 131
A and B) represents the meso-entoderm. The whole process is then
to be regarded as a much modified invagination. The edge of the
germ-disc corresponds to the blastopore which is filled by the large
yolk-plug. The yolk-mass also fills the whole of the archenteric
cavity (Fig. 131 B).
In the Molluscs considered earlier in this work, especially in the Gastro-
poda, we have already found the mouth related to the blastopore. In Gren-
achkr's Cephalopodan embryo, we saw that the oral aperture arises in the
neighbourhood of the aperture of the blastoderm which closes only at a very
late stage (p. 270). Since we regard the latter as the blastopore, relations
between it and the mouth may exist here also.
280
CKPHALOPODA.
t^t- *
l-'ii.. 131. — Diagrams illustrating tlie formation of the germ-layers. A, thickening of
the edge of the germ-disc ; B ami 0, differentiation of the yolk-epithelium. Further
extension of the germ-disc over the yolk. 1), differentiation of the rudiment of the
enteron and the mesoderm ; de, yolk-epithelium ; ect, ectoderm ; md, rudiment of
eiiteron; mes, mesoderm ; ect (in />), the rudiment of the cerebral ganglion.
THE SEPARATION OF THE GERM-LAYERS, ETC. 281
At a later stage, as already described, the lowest cell-layer, that
which is in contact with the yolk, becomes differentiated and yields
the provisional and the final entoderm (Fig. 171 G and I), de, iml).
The cell -material which remains between these two and the ectoderm
corresponds to the mesoderm, which, in its development is, like the
entoderm, greatly influenced by the excessive abundance of the yolk.
During these processes, the germ-disc has extended far over the egg
(Fig. 131 (J and D).
We need hardly point out that the formation of the germ-layers
in the Cephalopoda, as compared with that in other Molluscs is much
modified ; transitions between the two types of formation may, how-
ever, be found in the eggs of many Gastropods that are rich in yolk
(e.g., Nassa, Fig. 95, p. 207) although, in these latter cases, the
modifications undergone by the process are not nearly so great.
The entoderm, indeed, was there seen forming in a disconnected
manner and the rudiment of the enteron was open towards the yolk
(Figs. 123-135), as in the Cephalopoda, except that, in the
latter, the yolk is still covered by the thin epithelial layer.
The alimentary canal now develops, the enteron (Fig. 132 A, nul)
increasing in size and soon dividing into two parts, as is seen in Fig.
132 C which represents a later stage. The lower part, which appears
sac-like (tb), represents the rudiment of the ink-sac, and the upper-
part, which is open towards the yolk-epithelium, the actual stomach
and intestine. Where this comes into contact with the ectoderm (a),
fusion subsequently takes place and results in the anus. There is
at this point only an inconsiderable depression of the ectoderm, and
there is therefore no proctodaeum of any size, as is evident from the
fact that the ink-sac, which originates from the entoderm, opens into
the intestine in the adult quite near the anus.
The enteron grows out towards the apex of the yolk-sac, this
being still more marked in later stages. It is growing toward the
stomodaeum which is approaching it from the other side of the
yolk-sac. This latter rudiment arose as an ectodermal depression
on the opposite side of the blastoderm and farther down, i.e., more
anteriorly.
The positions of the mouth and the anus have already been men-
tioned and are made clearer by the sections now before us (Figs. 1 ■">'_'
and 133, also Figs. 116-120, pp. ii55-i)62). The oral invagination arises
below the ectodermal thickening depicted on the left in Fig. 131 A,
'',, anal
region ; ar, arm-rudiment ; c, cerebral commissure ; eg, cerebral ganglion ; G) and still
more in transverse
sections (Fig. 134 A
and B). It here
appears as a plate, a
large part of which is
in close contiguity to
the yolk. The in-
folding of the edges of
this plate (Fig. 134 B)
gives rise to the two
hepatic tubes which
open into the enteron
in the region of the
caecum.
The wide opening
<»f the enteron towards the yolk-epithelium gradually narrows,
but can still be distinctly made out even in later stages (Fig.
133). Below it, large cells of the yolk-epithelium can be seen
lying, and sending off lateral processes into the yolk (Fig. 133).
The yolk is thus completely covered by the yolk-epithelium even
beneath these gaps in the intestinal epithelium, where a con-
nection of the lumen of the intestine with the yolk-sac might be
assumed, as well as below the former wide aperture of the enteron.
There is, therefore, no direct communication between yolk-sac and enteron.
Fig. 134. — The ventral portions of two transverse sec-
tions of embryos of Loligo vulgaris at different ages
(original), a, anal region; de, yolk-epithelium;
ect, ectoderm ; /.-, branchial rudiments ; /, liver ; mil,
enteron ; mes, mesoderm ; v, vascular spaces in the
mesoderm.
i hi: separation ok the germ-layers, etc. 285
The yolk-material thus does not pass directly into the intestinal
cavity, but lias first to pass through the yolk-epithelium. The latter
consequently promotes the absorption of the yolk by the embryo, this
being its principal function. A specially active inception of nutritive
substance probably takes place at the open part of the enteron by
means of the yolk-epithelium. This view is confirmed by the rise of
the liver in this region, this organ showing in other Molluscs also
a close relation to the nutritive substance of the egg, and also by
the appearance of the large rhizopod-like cells in the yolk-epithelium
which separate the cavity of the enteron and the yolk-sac.
When the gap in the intestinal epithelium closes as development
advances, the internal yolk-sac appears to lie in the body-cavity
quite unconnected with the enteron. The external yolk-sac gradually
decreases in size as its contents are transported to the internal sac
whence they are absorbed and, when completely taken up, the internal
sac itself shares the same fate, the yolk-epithelium being the last to
disappear, its function being now fulfilled.
The function of the yolk-epithelium resembles that of the yolk-cells of the
Arthropoda and the Vertebrates, described above. This comparison has
already been made by Ray Lahkbster, Vialleton, Watase and others, and
the resemblance is heightened by the fact that the yolk-cells may also appear
as a peripheral layer, the outer merocyte-layer of the Selachians or the so-
called periblasts of the Teleosteans. Some difference between these and the
yolk-epithelium of the Cephalopoda still, however, remains, since, in the
Vertebrates, these cells are at first distributed throughout the yolk and then
collect into a continuous layer, whereas, in the Cephalopoda, the cells are
never found in the yolk, the yolk-epithelium being produced direct from the
cells of the germ-disc. The type of the meroblastic egg is thus specially
marked in the Cephalopoda.
In order to complete our description of the development of the
alimentary canal, some reference must be made to the ink-sac. We
have already seen that it arises from the rudiment of the enteron as
a vesicular structure (Fig. 132 0, md). It soon deepens, and grows
out as a tube which is surrounded by mesoderm-cells. In this tube,
two sections can soon be distinguished, the inner blind end, the walls
of which are much folded (Girod), and the superficial part which
opens externally and becomes greatly dilated, but remains lined with
a simple epithelial layer. The inner part of the ink-bag represents
the glandular secreting part, while the dilated portion which finally,
through a long efferent duct, opens into the intestine near the anus,
forms the reservoir for the secretion. As lias already been pointed
out (p. 281), the fact that this entodermal structure opens close to
286
CEPHALOPODA.
the anus proves conclusively that there is here no long proctodaeum.
Nevertheless, a very considerable part of the alimentary canal has
actually, by some authors, been attributed to a proctodaeal invagina-
tion. Although we considered this view as disproved, we mention it
here as having formerly been, supported by the majority of authors
(Metschnikoff, No. 32; Geenachee, No. 14; Ussow, No. 44;
Gieod, No. 12 ; Watase, No. 49).
According to these authors, the structure spokeu of as the enteron was
already connected with the ectoderm from its earliest development, and, as
this gives rise to the intestine, the latter must therefore have arisen in the
form of an ectodermal depression, i.e., as a proctodaeum. Ussow, as well as
Girod and Watase, who later investigated this subject very thoroughly, must
be regarded as having adopted this view, the details of which are here un-
necessary. The hypothetical proctodaeum grows up over the yolk, becoming
differentiated in the way described above for the enteron. As to the point to
which the proctodaeum extends forward (or the stomodaeum backward)
opinions are divided, but according to this view, the liver, tht; caecum and the
stomach are all derived from the ectoderm, since the whole alimentary canal
is produced by the union of the stomodaeum growing backward and the
proctodaeum advancing forward. The whole of the entoderm is represented
by the yolk-epithelium and is quite transitory (Watase). Similar statements
as to the ectodermal origin of the alimentary canal have been made in
connection with other animals (e.g., Insects, Ganin, Witlaczil, Graber,
Heymons), but are, in such cases also, altogether improbable, as is proved by
the condition of nearly related forms.
As opposed to the view to which we have just briefly referred, we have given
that maintained by RayLankester (No. 29) ; Vialleton (No. 48) ; Bobretzky,
(No. 4) and confirmed by ourselves (No. 25). in much earlier stages of de-
velopment, as, apart from its greater probability, this derivation of the
alimentary canal seems much better founded.
B. The Covering of the Body and the Shell.
The ectoderm which covers the body of the embryo seems to pass,
with only slight modifications, direct into the body-epithelium
(epidermis) of the adult. The shell appears as the secretion of a
specially modified part of the ectoderm. In studying the embryonic
formation of this organ which is of such importance for the compre-
hension of the Cephalopodan body, we are unfortunately restricted to
those forms in which it no longer attains full development. Only in
a few recent Cephalopods such as Nautilus and Spirula * is the shell
* [It is very questionable if the shell of Spirula can be regarded as perfect ;
it is almost internal and evidently much reduced. — Ed.]
interpretation of the shell in recent cephalopods. 287
found in its perfect form, and the development of these rare animals
is not known. The shell of Argonauta exemplifies other conditions
which will be discussed later (p. 294). In those recent Cephalopods
in which the development of the shell has been investigated, it lies,
enclosed in the mantle (and is thus internal) on the antero-dorsal
surface of the body, and either develops into the so-called pen, of a
horny character {OmmaUrephes, Loligo, and others) or consists of
numerous calcareous layers built upon a horny foundation {Sepia).
It forms in an invagination of the ectoderm, the shell-gland.
In a very early embryonic period, a depression appears at the
centre of the mantle-rudiment, this being the first indication of the
shell-gland (Figs. 115, 116, p. 255, Fig. 131 D, p. 280). At first, in
Loligo, this is a wide, shallow pit, but the margin of the pit soon grows
inwards and constricts its aperture, the pit finally assuming the form
of a sac connected with the exterior by a small opening. This sac is
lined with an epithelium composed of cells which, at its base,
are specially long, and is surrounded by mesodermal tissue. The
aperture of invagination completely closes at a later stage, and the
shell-gland then lies internally as a closed sac, surrounded by the
mesodermal tissue (Fig. 132 C). It extends later especially anteriorly
and then occupies a large part of the antero-dorsal side of the mantle
(Fig. 133). The secretion of the shell then takes place within it
(USSOW, BOBRETZKY).
The Interpretation of the Shell in Recent Cephalopods-
There can be no doubt that we have in this case an internal shell,
hut the question remains, \\ hat is its relation to the large external
shell met with in the (living) NautilibS, in the Ammonites and other
extinct forms 1 This is a point of importance in studying the manner
of formation of the Cephalopodan shell and its relation to that of
other Molluscs. In solving this question it is necessary to institute
comparisons with the shells of various extinct forms.
The shell of the recent THbranchia is very differently developed in the
various forms. It occasionally consists merely of a long, narrow, horny,
plate, shaped like a symmetrical bird's feather, but otherwise not specially
ditTerentiated (c.i/., in Loligo . In other cases, the plate is less simply formed,
its posterior end forming a hollow cone, the whole shell thus being slipper-
shaped (Ommastrephes, Fig. 140).
The calcareous shell of Sepia (Figs. 137, 138 .4) is much more complicated
in structure, and is composed of many calcareous layers. Its structure is still
not fully understood, but it has been compared with the more highly
288
CEPHALOPODA.
developed Cephalopodan shells. Among the living Dibranchia, the shell
which appears to approach most nearly to those of the extinct forms is that
of Spirilla ; here we find a spirally coiled and chambered shell which, how-
ever, is grown over and enclosed by the mantle. This approximates most
nearly to the shell of certain Belemnites which was also an internal shell
though, so far as its chambered portion (phragmocone) was concerned, it was
less highly developed than that of Spirula.
The shell of the Belemnite is not, like that of Nun til its or most Ammonites,
spirally coiled, but is straight like that of the Orthoceratidae (Nautiloidea).
It is characteristic of the Belemnite that in addition to the part of it, the
phragmocone, that may be regarded as corresponding to the actual cham-
bered Cephalopodan shell (that of the Ammonites
and Nautilus) there is a calcareous pointed external
investing piece, the so-called guard or rostrum. A
good example of this latter is afforded in the fossil
Spirulirostra (Fig. 135) the phragmocone of which
is curved and thus bears a certain resemblance to
that of Spirilla, but has, in addition, dorsally and
late rally, a large conical rostrum. It has also been
maintained that traces of such a rostrum are to be
found in Spirula, although these were not found by
us in an examination of a large number of shells.*
The shell of the Belemnite is, as already men-
tioned, straight. Two parts can be distinguished in
it. The chambered part {phragmocone) is provided
with a siphon and is surrounded by the actual shell-
wall (the ostracum) ; this latter becomes specially
dilated towards the head of the animal as the so-
called proostracum, and is not here followed by the
phragmocone. This first portion of the shell might
.be compared with the Ammonite or Nautilus shell,
but on the side opposite to the proostracum, sur-
rounding the posterior part of the phragmocone and
prolouged in the same direction, there is a second
part, a very large rostrum, which is usually the
only part of the whole Belemnite to be preserved
in a fossil condition. That this shell was internal,
i.e., surrounded by the mantle, seems to be highly
probable from observations made on forms resembling Belemnites but better
-r
Fig. 135. —Longitudinal
section through the
shell of a Spiruli-
rostra (restoration).
/J/, phragmocone ; r,
rostrum ; si, siphon.
* The position of Spirula as a branch of the Belemnite stock connected to
it by forms like Spirulirostra seems to us doubtful. While the position of
the siphon and the orientation of the shell with regard to the body would
seem to favour this view, the constitution of the shell, on the other hand.
with its well-retained chambers and the siphon renders it improbable that
it has undergone a process of degeneration which led to the total loss of the
rostrum. The shells of other recent Cephalopods, in which such degeneration
took place, underwent, in consequence, great change of structure. We must,
in any case, take into account the view that Spirula may have separated from
bhe Decapodan stock before acquiring a rostrum.
INTERPRETATION OK THE SHELL IX RECENT CEPHALOPODS. 289
preserved, and as is also shown by the so-called
externa] surface of bhe rostrum of many
Belemnites.*
Attempts have been made to deduce the
constituent parts of the shell oi Sepia from
bhe above parts of the Belemnite shell
(Volt/. Riefstahl, No. 39). The shell of
Sepia, or, as it isgenerallj bermed, the cuttle-
bone, is very complicated. The whole forms
an oval shield-like structure, which, Eor the
most part, is biconvex, but in the more dorsal
region it becomes concave on its posterior
or inner side, its shape is well shown in
Pigs. 137, 138 A. Its antero-dorsal surface
is covered externally by a roughly calcified
shagreen-like layer, the outer layer, under
which is a deposit of horn-like matter (con-
ehyolin), the middle layer, the latter being
freely exposed at the margin of the shell
i Fig. 137, mp). Dorsally, the shell is
produced into a small pointed structure
(Figs. 137 and 138, k. ,/> which consists
essentially of a prolongation of the outer
calcified layer but has become covered by a
secondary development of horny (oonchyolin) ;
matter which is quite distinct from the
horny middle layer. This calcareous spine
may in some species project freely on to
the exterior (S. andreanoides). On the
posterior or internal surface of the shell is
a prominent swelling produced by a great
deposit of calcareous material arranged in
thin oblique layers (Pig. 138 A, w), separated
from one another by air-spaces closed by
calcareous supporting trabeculae ; this
structure which is most developed near the
antero-ventral portion of the shell serves as
a float. Dorsally this portion of the shell
is less developed and consequently the mar-
gins of the shield are here much more pro-
nounced. Surrounding the posterior remnant
of the calcareous swelling is a modified forked
or V-shaped area (Fig. 137, g), the two ends
of which are directed forward; this ledge,
vascular impressions on t be
Pis. 136. — Median longitudinal
section through the shell of a
Belemnite, somewhat diagram-
matic, e.k, embryonic chamber;
/'/'. phragmocone ; po, proos
tracum ; /•, rostrum : s, siphon.
The dotted lines indicate the
anterior edge of bhe shell the
limits of which are at present
not accurately known.
to locomotion. P " arr0W' an adaPtatiou favourable
U
290
CEPHALOPODA.
the posterior part of which is somewhat raised and arched forward, forms
a cavity which in some cases (S. officinalis) is shallow, but in other species
(S. aculeata, Pig. 137) tolerably deep.
These parts of the Sepia shell have been homologised with those of the
Belemnite shell in the following way. The spine, together with the outer
calcareous plate, have been thought to correspond to the rostrum of the
Belemnite (cf. Figs. 136 and 137) which is continued far on to the actual
shell, almost as if the proostracum of the Belemnite were covered by an
external calcareous investment connected with the rostrum, as perhaps may
actually be the case. A similar condition is found in Spirulirostra, in which
the rostrum embraces a large part of the shell (Fig. 135, r).
The actual shell of the Belemnite, i.e., the
phragmocone and proostracum, corresponds
to the two inner layers of the shield in Sepia,
the prominence and the fork (Figs. 136-138,
w and g). While the two outer layers are to
be regarded as the wall of the shell (ostracum),
the lamellae of the prominence may perhaps
be considered as partition-walls between the
chambers. These lamellae end posteriorly
in free edges (Figs. 137 and 138) ; laterally,
however, they are continued into corres-
ponding lamellae of the forked ledge. As
this latter rises anteriorly over the posterior
end of the prominence and forms a rather
deep cavity posteriorly, a structure arises
which actually resembles the phragmocone
of the Belemnite. If the comparison is
carried further, the wide aperture of the
posteriorly directed partition-walls of the
chambers might be compared to the siphonal
spaces in the Ammonites, which, however,
have become very wide and in which a con-
siderable part of the body lies.
This view seems to be supported by bhe
condition of a fossil form (Belosepia) the shell
of which bears a general resemblance to that
of Sepia but still shows the phragmocone
fairly distinctly (Fig. 138 B and ( '■). In place of the siphon there is, in this
Eorm a wide cavity (Fig. 138 B), and this may be regarded as marking a
transition to the condition of Sepia. The rostrum in these forms resembles
that of Sepia, hut is still more strongly developed (Fig. 138 A and B).*
If the lamellae are regarded as partition-walls of the chambers, it appears
remarkable that these latter extend anteriorly, that is, that the proostracum
thus completely disappears, for the whole prominence would then correspond
to the phragmocone.
* We refrain from comparing the anterior part of the shell (of which usually
only the hind or dorsal end is retained) with the shell of Sepia, but it seems
possible that here also resemblance can be found.
Fig. 137. — Shell of Sepia aculeata,
seen from tin- ventral surface
(original). '/, spine ; g, forked
ledge ; ip, inner layer ; mp,
middle layer of the shield (s) ;
"',
prominence, showing the
In- iui-s el the lamellae
[NTBRPEBTAT10N OF THE SHELL TN RECENT CEPHALOI'ODS. 291
W.—
i— r.
The lamellae are connected by numerous delicate calcareous trabeculae, so
that the spaces between them are not empty, as one might expect if tbey
represented chambers. But this can hardly be reckoned as an argument
against the above interpretation of the Sepia shell, as such a modification of
bhe shell in adaptation bo new functions (as a lloat) is quite explicable.
The development of the different parts of the Sepia shell has been investi-
gated in detail by Appeloff, but has, so far as we know, been described only
in a short Swedish treatise (No. 2) from which it is impossible to judge
whether factors of import-
ance for the morphological
interpretation of the shell
have been discovered.
Finally, it appears ueees
sary to point out that this
whole comparison is still
far from being well founded,
although it may be con-
sidered as extremely
plausible.
Other recent Cephalo-
pods, especially those which
are universally regarded
as more primitive than
Sepia, have a shell of very
simple structure, carrying
at its end at the most a
hollow cone (Ommastrephes,
Fig. 140). If this structure
is compared with the phrag-
mocone, the rest of the
shell would have to be
regarded as the proostra-
cum, and this suggests the
idea that, in Sepia also,
the fork which bifurcates
anteriorly and the con-
tained cavity may be
regarded as such a much-
reduced phragmocone. The
whole of the part lying
anteriorly to it (the prominence) would then have to be considered as the
proostracum, which has perhaps attained such a large size in adaptation
to its present function, the diminution of the specific gravity of the body.
The lamellate structure of the prominence would then be traceable to a
secondary modification causing the secretion of the shell in layers, to form
the air-cavities of the float ; under these circumstances the higher morpholo-
gical significance could not be ascribed to it. Further light upon the subject
of the significance of the shell of Sepia and its relation to the shells of the
.-r
PlG. 138. — A, Diagrammatic longitudinal section of
the shell of Sepia; B, shell of Belosepia Blain-
villei, seen from the side; C, posterior part of the
same, seen from the ventral side (B and C after
Zittel). d, spine ; ph, phragmocone ; r, rostrum ;
s, siphon ; w, prominence.
292
CEPHALOPODA.
fossil forms may be expected from detailed palaeontological investigations and
perhaps also from more comprehensive ontogenetic researches.
\ comparison of the shell of Sepia with that of Bclcmnites, such as was
attempted above, suggests a relation between the Dibranchia in general and
the Belemnitidae. This indeed seems a bold proceeding, since nothing certain
is known of the soft parts of these Cephalopods, but forms like Belemnoteuthis,
a Cephalopod living in Triassic times with
well-preserved phragmocone and arms
carrying hooks, as well as Acanthoteuthis, a
Decapod much nearer the recent Decapods
and also armed with hooks (Jaekel, No.
17), indicate with considerable certainty
that the Dibranchia or at least the Deca-
poda are to be derived from forms resemb-
ling the Belemnitidae.
There can be no doubt that the shell of
the Belemnitidae was internal and was
almost completely enclosed in the mantle.
Of the transitionavy forms, moreover,
BelemnoteutMs shows on the phragmocone
which is still provided with chambers and
siphon a large and distinctly bounded
proostracum (Fig. 139, po) recalling, in its
shape, the Sepia shell. The rostrum, in
these forms, is either wanting or, when
present, is only a slight appendix to the
phragmocone. In this respect, these forms
would approximate to the recent forms
in which the shell has a posterior cup
(Qmmastrephes, Onychoteuthis, Taoniu.s,
Leaelna).
It is of interest that, in Ommastrephes,
regular transverse striatum is found on the
hollow cone (Fig. 140) ; this is quite distinct
from the lines of growth in other parts of
the shell and may perhaps be regarded as
the last vestige of the chambering of the
phragmocone. [< ronatus Fabricii, according
to Steenstrup, has a series of chambers
at the end of its horny pen.] Such a view
does not appear unjustifiable, as Ommas-
treplws is among the most primitive of the extant Cephalopoda. Jaekel
has already pointed out (No. 17) that Ommastrephes also, in the possession of
small hooks, shows a primitive character and recalls the hook-bearing tradi-
tionary forms mentioned above (Belemnoteuthis, Acanthoteuthis).
Pig. 139. —Shell of Belemnoteuthis
from the lower Lias, Lyme
Regis, somewhat diagrammatic
(original).* The shell is seen
from the funnel-side with the
ink-sac lying (tb) upon it. In
the phragmocone (/ the most
posterior part is wanting and is
indicated by dotted lines. The
partition-walls of the chambers
are seen on the surface owing to
the posterior portion being
broken away ; /«', proostracum.
* Fie 1*) represents a very instructive and as yet undescnbed specimen
from the collection of Dr. O. Jaekel, kindly placed at our disposal. Our
thanks are due to him also for revising the figure.
INTERPRETATION OF THE SHELL IN RECENT CEl'HALOPODS. 293
The reduction of the shell goes still farther in other recent Cephalopods ;
the terminal cone, in older specimens of Dosidicus, is found to be solid,
whereas, in the younger animals, it was hollow (Stbensteup). In some
ichiidcu the hollow cone is still present at the end of the shell, in others
it lias disappeared and, in its place, i here is mere solid swelling.
Finally, a simple horny plate develops, as in Loligo. The
hollow cone does not even appear ontogenetically, so far as we
know at present.
The above comparison seems to show with certainty that the
shell in the Cephalopoda is internal, the manner in which it
arose from an external shell being still exemplified in a living
form, Spirilla. In Nautilus, only a small part of the mantle
covers the external shell, but the process of circumcrescence
oi the shell went farther, until the shell became covered, though
incompletely, by the mantle, as in Spirula. During this process,
the size of the shell as compared with that of the animal became
reduced in most cases ; at the same time, it changed its position
and gradually degenerated, since it no longer functioned in the
same way. Externally, new calcareous layers became added
to the primitive shell, for we find that only the inner part of y,.
the shell of Belemnites or Sepia corresponds to the shell of
Nautilus, the rostrum and its continuation as a covering of the
proostracum are secondary structures, no doubt secreted by the
mantle-sac which surrounded the shell. We are here again
brought to the question of chief interest in connection with this
subject, viz., the manner of formation of the shell.
We saw above that the shell is formed in an ectodermal
depression, the shell-gland. It would be well to discover
whether this shell-gland is homologous with the organ of the
same name in the Lamellibranchia and Gastropoda or not.
This question has been raised before now by Ray Lankester
(No. 28) who maintained the negative because he believed that
the shell of Sepia corresponds to the Belemnite shell and conse-
quently must be formed in a mantle-sac and not in the primitive
shell-gland. Ray Lankester was obliged to take up this
position decisively since he considered the Sepia shell as
homologous with the external part only of the shell of
Belemnites and left the phragmocone out of account.
In deciding the question as to the significance of the shell-
gland in the Cephalopoda, we are inclined from the first to
ascribe to this organ which appears so early, in consequence
of its position and development, the same significance as is
possessed by the shell-gland in the other Mollusca, and thus %
Fig. 110. — Posterior part of tin- shell .>t Ommastrephes from the Indian Ocean, seen
from the posterior surface (original). /■, conical appendage at the dorsal end; s,
plate of the shell which narrows dorsally, again broadening oul ;i- the conical
appendage ; /. the strong hornj ledges between which tin- shell consists merely of a
thin membrane strengthened by ribs.
294 CEPHALOPODA.
to consider it as fully homologous with this latter structure. The most
natural course is to seek for a confirmation of this view in the ontogeny of
those Cephalopods which are provided with an external shell. Since the
development of the shell is unknown both in Nautilus and Spirilla, em-
bryos being unobtainable at present, we might turn to the only Cephalopod
with external shell which is more accessible, viz., Argonauta, if the conditions
in this case were not essentially modified.
It has already been shown (p. 266) that a shell-gland does indeed appear in
the embryo of Argonauta, but that it disappears later and does not give rise
to the shell of the adult. The latter is not formed within the egg-shell, as
was assumed by a few of the older authors (Poli, Delle Chiaje, No. 9) but
arises later, as was observed by Mrs. Power, Adams and Kolliker (Nos. 1
and 24). The statements made as to the origin of the shell are somewhat
peculiar and obscure. According to the almost universal view, the shell is
secreted by the expanded surfaces of the dorsal arms which cover the shell
when fully formed. This view, which at first sight is rather improbable, is
rendered still more so by the fact that the regeneration of parts of the shell
which are lost is said to take place from within. The mantle might also be
regarded as a source of the shell, but it is not closely connected with the
latter and so this view also has no support.
The disappearance of the shell-gland in the embryo of Argonauta shows
that the adult shell, in this case, is not a structure which can be homologised
with the shells of other Cephalopods. If, as is stated, the shell-gland actually
flattens out, the shell may have arisen from a part of the mantle which
originally corresponded to the shell-gland. The position of the animal with
respect to the shell is the same as in the Ammonites and Nautilus, while, in
Spirula, on the contrary, the orientation is different, the concave and not the
convex side of the shell here corresponding to the ventral side.
An attempt has recently been made to derive the Argonaut shell directly
from that of Scaphites, the external form in the two cases having a certain
similarity (Steinmann, No. 43). We are unable to accept such a view be-
cause we do not regard the Argonaut shell as directly homologous with the
Ammonite shell, apart from the fact that a long period elapsed between the
disappearance of Scaphites and the appearance of Argonauta, the latter, more-
over, belongs to the order Octopoda and is thus closely related to the other
living Dibranchia.
If the shell of Argonauta is to be derived from that of Scaphites, a com-
paratively quick disappearance of the chambering of the shell without
essential modification of the external form must be assumed. The chamber-
ing of the shell, however, and the manner in which the animal is connected
with it reappears in so marked a manner in all Cephalopoda (in which the
shell is well preserved) that we are not warranted in assuming that Argonauta
relinquished the chambering shell and received sea-water into the living
chamber, a change which would involve a complete alteration of the manner
of life of the animal.
From what is known of the modifications undergone by the Cephalopod
shell, it always appears to take place in the same way as in the forms with
internal shells. Although, in them also, the significance of the shell is
essentially modified, the chambering is retained (Belemnites) and disappears
THE SENSOR'S OBG ^NS. 295
only when the degeneration of the shell has reached it-- highest limit (horny
shell of the Dibranchia). We tnighl presuppose a similar process in the
ancestors of Argonauta, and thus claim the shell which occurs only in the
female anil is altoget her wanting in the ma le, as a new formation.*
The only Cephalopod provided with an external shell, the ontogeny of
which is at present known, is thus not adapted to assist m the solution of
the problem as to the significance of the shell-gland: we are therefore
restricted to the embryological fads concerning the forms with internal
shell.
Since the invagination known as the shell-gland secretes tin: whole shell,
and therefore also the part of it which corresponds to the rostrum of the
Belemnites, and as this is a part added to the primitive (Ammonite or
Nautilus) shell, there can be no doubt that the invagination is the equivalent
of at least that part of the mantle-sac which covers the internal shell. The
extraordinarily early appearance of the invagination indicates, however, that,
in the Cephalopoda as in other Molluscs, the original shell owes its origin to
a shell-gland. If this is the case, we might assume that in the course of
development the shell-gland became connected with this secondary mantle-
sac. The position of the primitive invagination is easily reconcilable with
this assumption. This question can be satisfactorily answered only when the
formation of the shell in recent Cephalopods with external shell such as
Spirula and above all Nautilus, is understood. Since the first of these forms
i- closely allied with the Decapoda and since, from the examination of the
ovaries in the latter (Owen, No. 33) it is known that, like other Cephalopoda,
it has large eggs rich in yolk, it is not too much to assume that similar
processes of development took place in these forms also, the conditions
of development of the shell especially being similar.
C. The Sensory Organs.
The sensory organs of the Cephalopoda (olfactory, auditory and
visual organs) show much similarity in their development, till appear-
ing first us invaginations of the ectoderm. The olfactory organs are.
throughout life, mere ectodermal invaginations, but the auditory
organs and especially the eyes become partly or altogether separated
from the ectoderm and reach a high degree of development. In
these cases also, however, traces of the connection with the ectoderm
may he retained either as vestigial or specialised structures (as in
the auditory organs) or by the retention of the original aperture of
invagination, tins latter condition being exhibited in the eye of
Nautilus.
* Cirrhoteuthis is --aid, unlike other Octopoda, to possess :i -hell, the nature
of which, however, is not well understood. If it is a true shell, it no doubt
arises from a shell-gland as in the Decapoda, and we should he justified in
assuming that forms like Octnpu* and Anjoimutu, in which a shell-gland
occurs, once possessed vestigial shells. The case inhabited by Argonauta
could then no longer be homologised with a true Cephalopodan shell.
296 CEPHALOPODA.
The Olfactory Organs.
These organs, unlike the eyes and the auditory vesicles, appear in the
embryo at a very late stage. In Sepia^ in which they were observed
by Zernoff (and previously by Kolliker) at a time when all the
arms, the funnel and the chromatophores have already formed, there
appears, behind each of the eyes, a round prominence. The edges of
this rise and curve over towards the centre and thus an invagination
of the ectoderm is brought about which at first is rather shallow and
sac-like, its floor being much thickened, while the covering consists
of thinner' cell-layers. Some of the ectodermal elements in the floor
of the olfactory sac take the form of spindle-shaped sensory cells pro-
duced into stiff' setae. This is the condition in the adult El<' .
while in Sepia and Loligo the intermediate and supporting epithelial
cells become much lengthened and invested with movable cilia. The
organ at a later stage becomes deeper and sac-like this being the
usual adult condition.
The papillae which, in Argonauta, usually take the place of the
olfactory pits, are considered by Kolliker as the equivalent of
the prominences which, in other Cephalopods, ontogenetically precede
the invagination, this author consequently regarding them as a lower
stage of development of the olfactory organ.
These organs cannot be homologised with the osphradial olfactory organs
which are so strikingly developed in the Prosobranchia, and iu a lesser degree
in many other Molluscs, since the latter are found in the mantle-cavity near
the gills, whereas the former occur on the head near the eye. In Nautilus,
true osphradia occur near the gills. [According to Willey. two pairs of
these organs are present. This author also described two pairs of olfactory
tentacles, the pre- and post-occular tentacles.]
Otocysts.
The rise of the otocysts has been observed in most of the forms
of which the ontogeny is known, and these organs have already been
depicted in many of the figures here given (Figs. 1 16-1 18, p. 260, 122,
}». 265, 126 p. 270 and 128 p. l'7M). Kolliker examined in detail
their (later) structure, and they were subsequently carefully studied
by Ran I jANKEster and Grenacher.
The position of the otocysts in the embryo may lie ascertained
from the above-mentioned figures. They form as depressions of the
ectoderm (Fig. 141 J) which gradually deepen and become vesicular
(Fig. 1-fl // and <'). The aperture of invagination does not close
THE SENSOR? ORGANS— 0T0C1
297
for sonie time, and its connection with the sac becomes elongated
and tubular (B and C). This appendage, which was described by
Kollikeb and by Grenacher, named Kolliker's duct, seems at
Hrst to communicate with
the exterior, but is said
later to become separated
from the surface and to
end blindly. Its interior
is lined with cilia directed
towards the aperture of
the otbeyst which are in
constant undulating move-
ment. Tins appendage
is also found in the adult.
Balfour compares it with
the r< '■' ssus vestibtdi of the
Vertebrates, the blind
appendage of the primitive
auditory vesicle which re-
presents its former connec-
tion with the point of
invagination.
In that part of the wall
of the auditory vesicle
which lies almost opposite
to the point at which
Kollikek's duct enters,
the epithelial cells thicken
to form the crista acustica,
and it is here that the
secretion of the otolith
fakes place (Fig. 141 D).
Tin' further development
of the otocysts is brought
about by the differentiation
of the crista acustica which
extends far over the wall
of the vesicle. The cells
of the rrixtn acustica lengthen, the inner free ends developing a
number of tine hairs. In this way arise the sensory epithelia which
compose the auditory ridges described by Kowaeevsky ami
£>
Fig. 1 11. Sections through the funnel-region oi
several advanced embryos of Loligo vulgaris
(original). A-C, transverse sections, D, sagittal
section, somewhat diagrammatic. The yolk
has been omitted. de, yolk-epithelium ; ect,
ectoderm; mes, mesoderm; tit, otocyst ; tr,
funnel-folds.
298
CEPHALOPODA.
( )\\ sjannikow (and also probably the auditory plate which only
develops later). In examining the formation of this terminal sensory
apparatus, Grenacher thought he could also recognise the nerves
which give off branches to the cells in the form of delicate fibrous
strands.
While the internal structure of the otocysts is thus developing,
the organs change their position, gradually shifting from a lateral
position to below the funnel (Fig. 141 A-C) where, as large closed
sacs, they are found in close contact with the pleuro- visceral ganglia
(Figs. 133, ot, p. 283 and 143, ac). Finally they come into close
contact with one another and flatten by mutual pressure, as was
observed in Grenacher's embryo and in Sepia. Their definitive
position being attained, the cephalic cartilage develops round them.
The Eyes.
The origin of the eyes in the Cephalopoda has been carefully
studied by Grenacher (No. 14), Ray Lankester (No. 2(.'). and
BOBRETZKY (No. 4).
Figs. 115-119, pp. 253-261 will help the reader to understand the
orientation of the eye-rudiments in the embryo. These organs
i >riginate in connection
with the large swellings
(Fig. 115, mi) as two
large, rather shallow
ectodermal depressions
(Fig. 142). The floor of
each depression soon
thickens considerably and
its margins grow up and
over it towards the centre
(Fig. 142 B). A vesicle
is thus produced with
a thin outer and thickened
inner wall and this is connected with the exterior by a small aperture.
The inner wall of this vesicle yields the retina, while the outer wall
yields a part of the lens and the ciliaiy body.
It is an interesting fact that this stage of development is retained
throughout life in the eye of one Cephalopod, Nautilus (Fig. 145).
The adult eye, in Nautilus, corresponds to the primitive optic vesicle,
the cavity of which is lined by the retina, i.e., modified ectoderm, and
-ri«l
Fig. 142. — Transversa sections through two stages
of the eye in Loligo (after Ray Lan'kksteu, from
Balfouk's Text-book). 'Pin- ectoderm is repre-
sented dark.
THE SENSORY ORGANS— THE EYES.
299
communicates with the exterior through an aperture. The sensory
epithelium is consequently directly bathed by the sea water, and its
ectodermal character thus becomes very evident. Eyes thus simply
(•(instituted have already been met with in a few primitive Gastropods
(Fig. 90, ]). 198).
In the Dibranchiate Cephalopoda, the eye reaches a higher grade
ot development. The first advance is the closing of the primitive
optic vesicle and its abstraction from the ectoderm. Mesoderm-cells
then press in between the latter and the outer wall of the vesicle, a
process the commencement of which is indicated even in Fig. 112 H.
After the abstriction of the optic vesicle, this stage may he compared
to the permanent condition of the eye in the majority of the
Gastropoda ( Fig. 1 45 />).
vd
ff.VS
Fig. 1 V-\. Transverse section through the bead of an advanced embryoof Loligo (aftei
Bobretzkt, from Balfour's Text-book), ac, otocyst ; adk, optic cartilage : ak and
//, lateral cartilage and white body : cc, iris ; //, funnel-fold : gc, cerebral ganglion ;
.'/"'. membrana limitans; gls, duct of the salivary gland : (ff.op), optic ganglion : (g.vs) .
visceral ganglion; rt, retina; vc, vena cava : vd, stomodaeum ; vk, ciliarj region
of the eye ; c, thickened ectoderm in the Boor of the tunnel.
A second circular ectodermal fold now rises above the optic vesicle.
enclosing a depression which strongly resembles the primitive optic
pit (Fig. 1 l-~> B). Almost simultaneously, the (cuticular) secretion of
a conical structure (Fig. 143) commences on the inner surface of the
external wall of the vesicle; this is the first indication of the lens.
This rudiment increases in size through the deposit of concentric
layers (Fig. 1U A).
300
CEPHALOPODA.
The lens of the Cephalopodan eye is not yielded by the outer wall
of the primitive optic vesicle alone, since the floor of the second
invagination above the vesicle also takes part in its formation (Fig.
143). From this latter is formed an anterior and smaller section of
the lens (Fig. 144 A and B). The cell-layers formerly lying above
the first-formed lens are in
this way gradually used up
(Figs. 143 and 144).
The primitive optic
vesicle and the invagination
lying above it also }deld the
ciliary body, the wall of the
former, which is directed
outward, and the floor of
the latter uniting for its
formation (Fig. 144 .4 and
B). The mesoderm present
between these two ecto-
dermal cell-layers no doubt
a;ives rise to the musculature
of the ciliary body. The
anterior or outer part of
the invagination (or rather
fold) becomes the iris (Figs.
144 and 145). Mesoderm-
elements find their way in
large numbers into this
anterior fold also.
Another circular fold now
grows over the eye at this
stage of its development
and gives rise to the cornea
(Fig. 145 C). This fold, in
many Cephalopoda {e.g.,
Oigopsida) does not close,
the cornea retaining its
aperture which is often somewhat wide and through which the
sea water can enter the external optic chamber, while in others
{e.g., the Myopsida among the Decapoda and the Octopoda), the
cornea either retains only a minute aperture or else completely closes,
thus precluding any communication between the optic chamber and
Flu. 144. -Sections through the eye of Loligo
in two stages of development (after BOBRKTZKY,
from Balfour's Text-book). <* and "', the
epithelium lining the anterior optic chamber ;
ni. and if, iris fold : aq, equatorial cartilage ;
cc, small ectoderm-cells of the ciliary body ,
', eg), appear as spindle-
shaped bodies. The ectoderm, at the formative centre of the
cerebral ganglia (above the mouth) is now again a thin layer (Fig.
14li A' and 0). In the median section (C), the cerebral commissure
(c) can here be recognised.
The paired rudiment of the cerebral ganglion was early observed
(by the above-named zoologists as well as by Geenachee). The
two ganglia greatly increase in size and finally fuse together. In
consequence of processes of growth, the relative position of the
cerebral ganglion and the mouth is modified in a striking manner
(Fig. 133, p. 283).
The optic ganglia also form as massive thickenings of the ectoderm
in the cephalic region. They are directly connected with the ecto-
dermal thickenings which become the cerebral ganglia and soon press
in below the optic vesicles, a process which evidently gave rise to the
statement that the optic ganglion arises on the posterior side of the
optic vesicle, from the mesodermal cell-elements there present. The
optic ganglion soon shows a close connection with the optic vesicle,
a connection which leads to the formation of the optic nerve.
The pedal and the pleuro-visceral ganglia, like the other ganglia,
are said to originate through differentiation of the cell-masses lying
between the ectoderm and the alimentary canal. In reality they are
due to ectodermal thickenings in the ventral part of the embryo.
The pleuro-visceral and pedal ganglia, like the cerebral ganglion, are
each composed of two parts of distinct origin. The two cell-masses
which yield the pleuro-visceral ganglion lie behind the otocyst, and
the masses that produce the pedal ganglion in front of that vesicle
(Bobretzky, Ussow, Fig. 133, p. 283).
During the course of development, the three ganglia just mentioned
gradually shift nearer one another and, as the yolk-sac disappears,
move towards the stomodaeum, where they finally fuse, the pleuro-
visceral and pedal ganglia uniting to form the sub-oesophageal mass
which is connected with the cerebral ganglion by two short com-
missures, a broad posterior and a narrow anterior commissure.
The anterior section of the sub-oesophageal mass, which is, to a
certain extent, marked off from the rest, and into which the narrow
commissure enters, is distinguished as the brachial ganglion. This
part becomes differentiated from the pedal ganglion at a time when
304 CEPHALOPODA.
the latter has not yet fused with the visceral ganglion (Pblseneek).
According to the above author, who is confirmed by Bobretzky,
the buccal ganglia originate in the same way, becoming abstricted
from the cerebral ganglia and shifting forward, but Ussow states that
they have a separate origin like the principal ganglia, and unite with
these only at a later period. A similar origin is claimed by Ussow
for the splanchnic and the stellate ganglia.
The ganglia can easily be recognised by the fact that, soon after
their appearance, a differentiation into an outer cellular layer and
a central fibrous mass takes place.
The connection of the ganglia with the sensory organs and the
peripheral parts of the body takes place only at a somewhat later
stage. Ussow assumes that the cells of the layer which produced the
y tin; blastoderm is completed and before the organs have
appeared (Fig. 125, p, 268). In the last ease, a very early differen-
tiation of these mesoderm-layers seems to have taken place.
The chromatophores are said to be derived from mesoderm-cells
which are distinguished from the surrounding cells by their large
310 CEPHALOPODA.
size and by the early deposit of pigment in their protoplasm (Gieod,
No. 1 3). At a later stage, they are covered by a thick envelope ;
the cells in the neighbourhood stretch out into spindles and become
connected with the chromatophoi^al cells. In this way arises the
well-known appearance of the (contractile) fibre-bundles connected
radially with the chromatophoral cells. The change of shape in the
pigment-cells which is accompanied by change of colour was usually
attributed to the contractility of these bundles, i.e., they have been
regarded as muscle-fibres, while some authors have ascribed a capacity
for contraction to the pigment-cells themselves, the radial fibres being-
considered as merely connective tissue which, it was assumed, held
the actual chromatophores in position (Girod).
Another account of the origin of the chromatophores has recently
been given (Joubin, No. 23). According to this view, the ectoderm-
cells, which are especially distinguished by their size, sink inwards
through a funnel-like depression. In the large cell at the base of
the depression, the protoplasm becomes differentiated and, later, pig-
ment appears. The cell then loses its connection with the ectoderm.
A number of mesoderm-cells which could be seen even earlier regularly
arranged below it, and which soon multiply still further, yield the
radial fibres. The chromatophores would thus be due to the com-
bined action of the outer and the middle germ-layers (Joubin).
LITERATURE.
1. Adams, A. Mollusea. The Zoology of the Voyage of H.M.S.
Samarang. London, 1848.
•J. Appelloff, A. Om skalets bildning hos Sepia officinalis. Ofver-
sigt kongl. Vet.-Akad. Forlandl. Stockholm. No. 7. 1887.
3. Beneden, P. J. van. Recherches sur rembryogenie des
Sepioles. Nouv. mem. Acad. roy. sci. Bruxelles. Tom. xiv.
1841.
4. Bobretzky, N. On the Development of the Cephalopoda.
(Russian.) Izvyest. imp. Obshch. lyubit. estestv. Antrop. i
Ethnog. Moscow. Tom. xxiv. 1877.
5. Brock, J. Ueber die 4. Owen, R. Spirula Peronii. The Zoology of the Voyage of
H.M.S. Samarang, edited by A. Adams. Mollusca. London,
1848.
35. Owen, R. On the External and Structural Characters of the
Male of Spirula australis. Proc. Zool. Soc. London, 1880.
36. Owsjannikow und Kowalevsky, A. Ueber das Central-
nervensystem und des Gehdrorgan der Cephalopoden. M$m.
d, rant, I de St. Petersbourg (7). Tom. xi. 1867.
LITERATURE.
313
:?7. Pelseneer, P. Sur la valour morphologique des bras et la
composition du systeme nerveux central des Cephalopodes.
Arch. d( Biologie. Tom. viii. 1888.
38. Pelseneer, P. Sur la nature pedieuse des bras des Cephalo-
podes. -l/'». Soc. Roy. Malacolog. di Belgique. Tom. xxiv.
1889.
:'.9. Riefstahl, E. Die Sepienschale und ihre Beziehungen zu den
Belemniten. Palaeontographica. Bd. xxxii. 1886.
10. Schimkbwitsch, W. Note sur le developpement des Cephalo-
podes. Zool. Anz. Bd. i.\. 1886.
41. Steenstrup, J. De Ommatostrephagtige Blaekspruthers ind-
byrdes Forhold. Om Ommatostrephernes A.eglaegning og
Udvikling. Oversigt over d. k. Danske Vidensk. Selsk.
Forhandl. 1880.
42. Steenstrup, J. Zur Orientirung liber die embryonale Ent-
wicklung verschiedener Cephalopoden-Typen. Biol. Centralbl.
Bd. ii. 1.^4-:>.
43. Steinmann, G., u. Doderlein, L. Elemente der Palaonto-
logie. Leij nig, 1890.
44. Ussow, M. Zoologisch-embryologische Untersuchungen. Die
Kopffiissler. Arch. f. Natwrg. Jahrb. xl. 1874.
15. Ussow, M. On the Development of the Cephalopoda. (Russian,
with abstract in German by Stieda.) Izvyest. imp. Obshch.
lyvhit. estestv. Antrpp. i Ethnog. Moscow. 1879.
46. Ussow. M. Untersuchungen iiber die Entwicklung der Cephalo-
poden. Arch, de Biol. Tom. ii. 1881.
47. Yialleton, L. Sur la fecondation chez les Cephalopodes.
Comptes rend. Acad. Sri. /'oris. Tom. ci. 1885.
48. Yialleton, L. Recherches sur les premieres phases du de-
veloppement de la Seiche (Sepia officinalis). Ann. sci. nat.
(7). Zo,,l. Tom. vi. 1888.
49. WATASE, S. Observations on the development of Cephalopods :
Homology of the germ-layers. Stud. Biol. Lab. Johns Hopkins
Univ. Baltimore. Vol. vi. 1888.
50. WATASE, S. Studies on Cephalopods. 1. Cleavage Of the Ovum.
Journ. Morphol. Vol. iv. 1891.
51. Zeknoff, D. Ueber das Geruchsorgan der Cephalopoden.
Bull, de la Soc. imp. d. Naturalistes de Moscou. Tom. xlii.
1869.
52. Zittel, K. Handbuch der Palaontologie. Bd, i. Cephalopoda.
Miinchen and Leipzig, 1884,
314 CEPHALOPODA.
APPENDIX TO LITERATURE ON CEPHALOPODA.
I. Faussek, V. Zur Cephalopodentwicklung. Zool. Anz. Jahrg.
xix. 1896.
II. Kerr, J. Graham, (hi some points in the Anatomy of Nautilus
pompilius. Proc. Zool. Soc. London. 1895.
III. Korschelt, E. Ueber den Laich unci die Embryonen von
Eledone. Sitmngsber. Ges. Naturf. Berlin. 1893 (1894).
IV. Willey, A. The Oviposition of Nautilus macromphalus. Proc
Rot/. Soc. London. Vol. ix. 1897.
CHAPTEE XXXIV.
General Considerations on the Mollusca-*
In attempting to combine into one general scheme the de-
velopmental phenomena described in the preceding chapters, in
connection with the different divisions of the Mollusca, we cannot, of
course, take into account all the very different ontogenetic processes,
but can only select from among them those that are of the more
general significance.
Even in the cleavage of the egg, great variety prevails. Thus we
rind, on the one hand, that the meroblastic type of cleavage attains-
its highest development among the Mollusca (Cephalopoda) but, on
the other, that total and, at first equal, but soon after unequal
cleavage is still more common in eggs of this phylum (Chiton,
Gastropoda), and so also is a type of cleavage which from the first is
unequal (Solenogastres, Lamellibranchia, Solenoconchae). The cause
of this difference is to be sought in the varying amount of yolk
contained within the eggs but, even among eggs showing total
cleavage, there are some that, through a secondary separation of the
volk-mass from the blastomeres, lead us to the meroblastic method
of cleavage (Nassa). The latter is to he explained as due to the
extraordinarily large amount of yolk in the egg, and this same
peculiaritv further determines so great a modification of the early
ontogenetic phenomena in the Cephalopoda, that this division must
be left almost entirely out of account in our comparative review.
Within each separate division of the Mollusca, the phenomena of
cleavage are very similar and very regular.
The formation of the primary germ-layers takes place through the
invagination of a blastula with a more or less wide cleavage-cavity,
or, where the latter is wanting, and the egg is richer in yolk, through
epibole. These two processes are found in nearly related forms, or
* See note, p. 1.
316 GENERAL CONSIDERATIONS ON THE MOLLUSCA.
else an invagination-gastrula appears as a stage following the epibolic
gastrula, as, for instance, in Ostrea and various Gastropods, in which
;a cleavage-cavity arises only at a later stage, and the macromeres
which are continuing to multiply press in towards it. There is also
no essential difference between these two types of formation of the
germ-layers. In the Cephalopoda also the germ-layers may be traced
back to the same processes, although these are influenced in a marked
manner by the large amount of yolk in the egg.
The middle germ-layer arises in a very similar way in all those
forms in which it has been investigated'. It originates in two
primitive mesoderm-cells derived from one of the macromeres (primary
entoderm). In the Gastropoda, in which this point has been best
•examined, the formation of the primitive mesoderm-cells from the
macromeres was found to be very regular.* The large primary cells
of the mesoderm have been discovered to exist in all the following
divisions of the Mollusca : the Amphineura, the Lamellibranchia, the
Solenoconchae and the Gastropoda. In the Cephalopoda, on the
-contrary, the development of the mesoderm lias been considerably
•modified by the conditions mentioned above.
The two mesoderm-bands arise through the multiplication of the
primitive mesoderm-cells. It has repeatedly been stated that
mesodermal tissue is not due to the multiplication of these cells, but
is yielded later partly by the ectoderm, as described for the Annelida.
The first of these views, i.e., the derivation of the mesoderm from the
primary cells is, so far, the more probable, but the other view should
not be summarily dismissed, and in any case deserves more careful
investigation. j-
It is very characteristic of the Mollusca that the mesoderm-bands
are retained for only ;t short time. They soon disintegrate, single
cells separating from them and becoming distributed in the cleavage-
cavity as the so-called mesenchyme. Before this happens, however,
or else during this process, a cavity appears in each of the mesoderm-
bands ; this is bounded by a more or less regular epithelial wall and
is thus recognisable as the coelom. This process is the same already
met with in the Annelida (Vol. i., p. 290), and Arthropoda (Vol. Hi..
p. 41:5). In these latter it leads to the formation of two mesodermal
layers, one applied to the ectoderm and the other applied to the
entoderm : these are the somatic and splanchnic layers. This seems
(See footnote, p. 119, En.| + [See p. 29, Ed.]
GENERAL CONSIDERATIONS ON" THE MOLLUSCA. 317
likewise to be the rase in the Chitons which in other respects also
appear to be very primitive animals (Fig. 4 A and B, p. 8); thev
do not, however, show any suggestion of the segmentation of the
mesoderm (formation of the primitive segments) so characteristic of
the segmented animals.
The Amphineura, even as adults, show the secondary body cavit \
well preserved. It is still very large, and contains the principal
organs, such as the alimentary canal, the liver and the heart. In the
higher Mollusca (Lamellibranchia and Gastropoda) it is much more-
reduced in comparison with the primary body-cavity and is even
quite small. The primary body-cavity with the mesenchymatous
tissue distributed in it is very large and becomes the definitive body-
cavity, just as in the Arthropoda (Vol. iii., p. -423). In spite of this,
the Molluscs have been regarded as typical Schizocoelata, i.e., as forms
devoid of a true coelom. Such a true coelom, however, is retained
1 ► v them, though only slightly developed.
While in the Arthropoda, the coelomic sacs (primitive segments)'
usually completely disintegrate or at the most persist to a small
sxtent in the genital glands {Peripatus, Myriopoda) the coelom of the
Mollusca is always retained in the form of the pericardium from which
the nephridia and the genital glands are formed (Gastropoda) in a
manner recalling the primitive conditions in the Annelida. Where
the connection between the kidneys, the genital organs and the
pericardium has not yet been made evident in the embryo in conse-
quence of insufficient investigation, or else where, in consequence of
secondary modifications in the forms examined, it can no longer be
demonstrated, the anatomical condition of the systems of oi'gans
clearly proves such a connection. In various Molluscs, the cavity of
the genital glands is directly connected with the pericardial cavity
( Amphineura, Cephalopoda), the nephridia entering the latter through
an open funnel, a condition which recalls the open connection existing
between the nephridia of the Annelida and the secondary body-
cavity (Amphineura, Lamellibranchia, Gastropoda, Cephalopoda).
There run consequently no longer be any doubt that Hi" pericardium of
the Mollusca should I" regarded as the secondary body-cavity; and,
apart from the absence of segmentation, the resemblance in this point
to the Annelida is very great.
The condition of the mesoderm and the structures belonging to
it is thus evidently of great importance in interpreting the Mollusca-
it has therefore been considered in connection with the early onto-
genetic processes. Hardly less important, however, is the larval
318 GENERAL CONSIDERATIONS ON THE MOLLUSCA.
form which also in several ways throws light upon the relationships
of the Molluscs.
Although the larvae of the different divisions, e.g., those of the
Amphineura, the Solenoconchae, the Lamellibranchia, and perhaps
also those of the Heteropoda and the Opisthobranchia appear with
very diff'ei-ent forms, all of them may without any difficulty be traced
back to the Trochophore, the typical form of which was met with
in the Annelida. In some cases, such, for instance, as the larvae of
Dondersia and Dentaliwn (Figs. 10, pp. 17 and 138, p. "291) as well as
in those of a few Gastropoda (perhaps of the Gymnosomatous Ptero-
poda, Fig. 77, p. 172) this is less evident, while in the larvae of other
Gastropods such as Patella, Paludina and most Lamellibranchia, the
resemblance is exceedingly striking (Figs. 51-53, p. 127 ; 56, p. 135 ;
14, p. 28 ; 18, p. 36). But even in larvae in which the resemblance
is not so great (Figs. 66 and 67, p. 155 ; 72, p. 162 ; 75, p. 168), com-
parison with other forms or the examination of the younger stages
enable us easily to trace back the larval form to the Trochophore
{Figs. 61 and 65, pp. 153 and 151 ; see also p. 166). In the greatly
modified ontogeii}r of the Cephalopoda, traces of the larval form have
hitherto not been established with certainty.
The development of the Molluscan Trochophore closely resembles
that of the Annelidan larva. It arises from the gastrula-stage,
several rows of cells at the anterior region becoming covered with
strong cilia and thus yielding the pre-oral ciliated rim/, the velum
of the Molluscan larva. The blastopore, which at first lies at the
posterior end, usually becomes slit-like ; it probably closes from
behind forward and generally, at its anterior end, passes into the
mouth through the formation of an ectodermal depression, the
stomodaeum. A i>i>4-i>rnl ciliated ring appearing behind the mouth
heightens the resemblance to the typical Trochophore, the external
form of the Molluscan larva now also agreeing with that of the
latter, the anterior end being much widened and the posterior
narrowed.
At the posterior end of the body, and thus at the point where the
blastopore at first lay and from which its closure commenced, the
anus now forms. It thus appears as if it also bore some relation
to the blastopore ; indeed, an attempt has been made to prove this
td be the case in some Molluscs {e.g., the Opisthobranchia), and in
another Gastropod, Paludina, the direct transformation of the blasto-
pore into the anus has been assumed. We thus find in the Mollusca
■conditions altogether similar to those met with in the Annelida and
GENERAL CONSIDERATIONS ON THE MOLLUSCA. 319
the Arthropoda, in which also relations were proved to exist between
the mouth and the aims on the one hand and the blastopore on the
other.
The intestine, which like the oesophagus, is usually formed by an
ectodermal invagination in the Invertebrata, appears to be derived
entirely from the entoderm in the Mollusca ; thus the enteron
usually fuses direct with the ectoderm, without any depression of
the latter. This has been regarded as an important peculiarity in
the organisation of the Mollusca, and much stress has been laid
upon it, but if, as has been stated, an ectodermal intestine actually
occurs in a few Molluscs {Chiton, Teredo, etc., pp. 15, 66, 208), the
usual absence of the proctodaeum cannot be considered as a dis-
tinctive feature.
At the opposite end of the larval body, i.e., at the cephalic pole,
and in the midst of the velar area, an ectodermal thickening known
as the apical, plate is found, occupying the same position as in many
other pelagic larvae. In the Annelida, the supra-oesophageal ganglion
is thought to originate from the apical plate, and in the Mollusca
also the cerebral ganglion is said to arise from it (Chiton, Lamelli-
branchia) or else to bear some relation to it {Dentalium). In the
Gastropoda, indeed, the cerebral ganglia originate as two ectodermal
thickenings of the pre-oral part of the body, but these also do not
differ much in position from the apical plate, so that even here there
may be some relation to the latter.
An organ of special importance in comparing the Molluscan Trocho-
phore with other larval forms is the prim it in' kidney. This arises
from cells derived from the mesoderm-bands,* in the same way as
in the Annelida, as a tubular paired structure. Its relations to the
primary body-cavity also seem to be the same as those met with in
the Annelida and in the c;tse of the adult excretory organ of the
Plathelminthes.
It is evident from the above that the resemblance of the Molluscan
larva with the Trochophore of other animal phyla, and especially
with that of the Annelida is exceedingly striking not only in external
form but in internal structure. Attempts have been made to account
for this resemblance by the supposition that the larvae of these
phyla gradually assumed the same organisation as a consequence
of similarity in their manner of life. We do not share this view,
and can only explain the remarkable external and internal similarity
* [See footnote, p. 179. Ed.]
320 GENERAL CONSIDERATIONS ON THE MOLLUSCA.
through actual relationship to one another of all those groups which
have the Trochophore as their larval form.
If we accept this latter view, there can be no doubt as to the
significance to be attributed to the larval form. Its reappearance in
the development of phyla so different as the Annelida, the Mollusca,
and the Molluscoida, points to a racial form having this structure.
This brings us to the difficult and much discussed question of the
origin of the Mollusca.*
Of the theories as to the origin of the Mollusca, two seem to us
to demand our special attention, these being the theory that the
Mollusca are derived from Turbellaria-like forms and that which
derives them from a Trochophore-like ancestor.
The derivation of the Mollusca from Turbellaria-like forms has much
in its favour, especially as it affords a partial explanation of the
perplexing conditions of the nervous system. The pedal strands,
according to this view, would correspond to the ventral longitudinal
nerves of the Turbellaria, while the pleuro-visceral strands correspond
to the lateral nerves. The resemblance is specially striking in the ner-
vous system of the Amphineura (forms which somewhat resemble the
Turbellaria in shape) which consists of four longitudinal strands with
connecting commissures. A similar ladder-like nervous system with
a ventral and a lateral strand on each side occurs in the Turbellaria
(Triclada and especially Gunda). The anus, which is wanting in the
Turbellaria, was acquired later, and so was the blood vascular system.
The coelom is to be explained by the dilation of the genital glands,
for the genital products originate, as was shown, from its epithelial
wall. The shell, an important component part of the Molluscan
organisation, arose for the protection of the body in the form of
a cuticular secretion of the dorsal surface in which were deposited
calcareous concretions. The foot, an equally essential part of the
organism, resulted from the transformation of the ventral surface of
the body, which was used for creeping, into a muscular sole, or else
is assumed to be a modification of the ventral sucker. t
* A great deal has been written on the relationships of the Mollusca. We
refrain from discussing the different and often opposite views which have been
propounded on this subject as they would merely add length to our account
and make it the less clear. We shall only allude in passing to the Trochophore
I lit< iry adopted by Ray Lankester and still more ardently by Hatschek, and
to Lang's theory of the derivation from Turbellaria-like forms. A list of the
most important works on the subject will be found at the end of this chapter.
Lang's view has recently been published in his Text-book of Comparatvoe
Anatomy (Engl. Trans., Vol. ii.).
t Thiele, like Lang, derives the Mollusca from Turbellaria-like forms and
regards the ventral sucker of the Polyclada as the organ from which, without
GENERAL CONSIDERATIONS ON THE MOLLUSCA. 321
The above may, on the whole, be described as possible, but this
origin has the disadvantage of starting from very highly differentiated
animals ; and, a point which appears to us as very important, affords
no clear explanation of the striking resemblance existing between the
larvae of the Mollusca and those of the Annelida. This resemblance
is made possible if we go back farther, to a form from which may be
derived both the Trochophore and the ancestors of the Turbellaria.
Since, in such speculations, it is only right to try to start from existing
forms, the common ancestral form of the Trochophore and the Tur-
bellaria has been sought among the Ctenophora, but it is impossible
to construct from them the desired ancestor without unduly forcing
the comparisons. It is true that the Ctenophora, on account of their
locomotion by means of cilia, their possession of the apical plate and
the condition of the entoderm and mesoderm may be brought into
relation with the Turbellaria and perhaps even with the Trochophore,
but it appears to us still more certain that in them we have forms
already strongly specialised in a definite direction and thus no longer
suited to serve as the ancestral forms of the Mollusca. Instead then
of attempting to derive these forms from known and specialised groups,
it seems to us simpler and at least equally justifiable to fall back
upon some form with a more primitive organisation.
In considering the ontogeny of the Annelida, we started from a
gastrula-like form, ciliated all over, which developed at the cephalic
pole a ciliated tuft, and in which also the locomotory cilia were
specially arranged in the form of a ring running round the body (the
later pre-oral ciliated ring or velum). The primitive mouth (blasto-
pore), originally lying at the posterior end of the body, becomes dis-
placed forward owing to the development of a ciliated apparatus in
this very limited region ; thus the mouth shifts towards the locomotory
apparatus which at the same time serves for conducting food to the
mouth, as is still seen to be the case with the ad-oral zone and the
post-oral ring of the Trochophore. In the primary body-cavity of this
form, mesodermal elements are already found ; among these lie the
gonads which no doubt are derived from the entoderm as well as from
the mesoderm [probably from distinct blastomeres which are neither
mesodermal nor entodermal but are the germ-teloblasts], and which
doubt, the foot arose (No. 20). The transformation of the sucker into the
foot and the relation of the latter to the rest of the body is treated in detail
by this author. It may here also be mentioned that Thiele ascribes to the
Ctenophora a very important part, not only in the phylogeny of the Mollusca
but in that of the bilateral animals generally.
Y
322 GENERAL CONSIDERATIONS ON THE MOLLUSCA.
are either still connected with the gastral cavity or already open
externally through special efferent ducts (nephridia ?). A specially
important organ of this hypothetical form which also lies in the
primary body-cavity is the excretory organ, the origin of which is
one of the most difficult points to explain. Since we see the ex-
cretory organs rising from the mesoderm, and are inclined to derive
this latter from the entoderm, we hold it as most probable that the
primitive excretory organ was a diverticulum of the entoderm which
became secondarily connected with the ectoderm. At a later stage,
it loses its connection with the entoderm and thus becomes the
structure known as the primitive kidney (protonephridium).
From a form possessing such an organisation, the Plathelmintb.es
also may be derived. Their excretory system remains on the level
of the protonephridium, merely branching and extending further
through the body. Their larval form corresponds more or less to
that described, but does not possess a primitive kidney. The Pilidium
of the Nemertini already shows a certain similarity to the Trocho-
phore, and it has been pointed out that transition forms between it
and the Muller's larva of the Turbellaria are to be found (Vol. i.,
p. 168). The Pilidium is distinguished, like the Trochophore, by the
possession of an apical plate.
Through the concentration of the ciliated apparatus and the
acquisition of an anus, the ancestral form ascended to the level of
the Trochophore, and then became the starting-point for the
Rotatoria, the Mollusca, and the Molluscoida. Its relation to the
Rotatoria and the Annelida, i.e., its ascent to the level of the latter,
has already been discussed (Vol. i., p. 342). The most important
features in this process are the appearance of segmentation and the
rise of the coelom, the hatter being perhaps explicable through the
enlargement of the gonads of the primitive form. As already
mentioned, the genital products originate from the epithelial wall
of the coelom, a fact which favours such an origin. The Mollusca
exhibit, on the whole, similar conditions, but show an important
difference in the absence of segmentation, remaining in this respect
more like the primitive form.
We therefore assume that the Molluscan larva [Trochophore) still
closely resembles the ancestral form; it already shows, however,
some new characters which clearly indicate differentiation in a certain
direction, two of these, the shell and the foot, being specially dis-
tinctive of the whole organisation of the Mollusca. The first of these,
especially, can very early be recognised through the appearance of
GENERAL CONSIDERATIONS ON THE MOLLUSCA. 323
the shell-gland on the dorsal surface of the larva, and thus gives the
larva the special character of the Mollusc without at first affecting its
general appearance (Figs. 14, 15, 18, pp. 28,31 and 36 ; Figs. 51 and
56, pp. 1 25 and 135). Somewhat later, but also at a very early stage,
the foot appears on the ventral side of the larva. The very early rise
of this organ which may in a few cases be found even before the
Trochophore form fully develops, must be regarded as a shifting back
to an early period of embryonic development of this feature which was
only a recent acquisition. It is all the more easy to admit this, as the
shell-gland is found to arise exceptionally early in those forms, the
development of which show marked specialisation, as, for instance, in
the Unionidae (Fig. 22, p. 50) and in the Cephalopoda (Figs. 116
A, p. 255 and 131 D, p. 280). The shifting back of the shell to the
earliest possible embryonic period can easily be explained by its im-
portance as a protection to the larva, a fact which may be observed
in every Lamellibranch or Gastropod larva whether young or old ;
the slightest disturbance causes the animal rapidly to retreat into its
shell and thus to sink to the bottom of the water.
The larvae of the Amphineura have no true shell-gland, a peculiarity
that would increase the resemblance between them and the Annelida
if their organisation were better understood. It must at present be
confessed that the larvae of the higher Molluscs are far more like those
of the Annelida than are the larvae of these more primitive forms, in
which we should expect a closer resemblance. The shell-plates of
Chiton, further, arise in the same region as the typical shell of the
higher forms (Fig. 5, p. 9).
The manner in which the shell appears in the embryo favours the
view that it is derived phylogenetically from a cuticular dorsal cover-
ing, within and beneath which calcareous concretions were deposited.
The shell-plates of Chiton have, indeed, with some probability, been
traced back to the transformed spines of this animal (p. 12), but on
the whole it seems more likely that the Chiton shell, which consists
of a number of plates, arose in consequence of a secondary distribution
(determined by the manner of life of the animal) of an originally
continuous dorsal carapace.* From this flattened, bowl-shaped shell
*The shell has also been regarded as a partly internal dermal skeleton in
consequence of its condition in Chiton, where it is traversed by strands of
connective tissue (Fig. 8, p. 12), and the retractors of the body inserted into
it have been thought to play an important part in its development (Thiele,
No. 20). This last factor is in any case of importance in connection with the
various modifications of the shell (where the latter is already present).
324 GENEKAL CONSIDERATIONS ON THE MOLLUSCA.
were derived later all the varied shapes of shell met with in the
different divisions of the Mollnsca.
The protective dorsal covering which became the shell was, in any
case, of great significance for the further development of the Mollusca.
Since, starting from the back, the shell had to cover a large part of
the body so as to be able to shelter it as completely as possible, the
locomotory organ could only develop on the ventral surface, the
creeping manner of life leading to the development of the foot, an
equally important organ and one highly characteristic of all the
Mollusca.
It has already been mentioned that attempts have been made to
derive the foot of the Mollusca from the ventral sucker of the
Polyclada, but it appears to us that the exclusive use of the ventral
surface as creeping sole, simultaneously with the development of the
dorsal shell which necessitated a firmer adhesion to the sub-stratum,
alone suffices to explain the greater development of the ventral part
of the body into a muscular foot. In a few Annelida and Annelidan
larvae, there is a ventral ciliated area extending between the mouth
and the anus which evidently assists the animal in creeping. Such
a differentiation may in any case be ascribed to the primitive form,
and this, together with a strengthening of the ventral musculature,
led to the formation of the foot when the primitive form became
adapted to a creeping manner of life, an adaptation which, again,
was connected with the development of a shell.
In the Solenogastres, which are elongated and evidently very
lowly Molluscs, the foot is only slightly developed and appears
as a ciliated ridge lying in the ventral longitudinal groove. This
groove, which is represented in Fig. 147 A and B, might be compared
with the ciliated area mentioned above as occurring in the Annelida,
in some forms becoming depressed in such a way as to produce a
ventral ciliated groove. In Ch■ v,
indicates the anterior end of the body. B. anterior end of the same animal seen
from the ventral side, and showing the oral aperture and, behind it, the aperture of
the pedal gland and the ventral groove (after Kowalevsky and Marion).
show no such structures. As an example of this we would recall the
Turbellarian described by v. Graff, Enantia spinifera. Here we
have true euticular spines which can only be considered as analogous
to those of other animals, but in connection with the origin of such
structures this illustration is of interest.
In comparing the spines of the Amphineura with the setae of the
Annelida it must be remembered that we can certainly not derive
the Mollusca from such highly developed forms as the Chaetopoda.
The most primitive Annelida, however (the Archi-Annelida), have no
setae, but even these are certainly too much differentiated to serve as
326 GENERAL CONSIDERATIONS ON THE MOLLUSCA.
starting points for the Mollusca in which segmentation is altogether
wanting.
The temptation is certainly very great to derive the elongate,
worm-like Solenogastres which are provided with a coelom and
nephridia (Fig. 47 .4) from the Annelida, but they also show no
segmentation. Either segmentation or the distinct remains of it
must, however, be found if they are really to be more nearly related
to the Annelida. We are thus inclined to regard the elongate form
of the Solenogastres rather as a secondary phenomenon and to con-
sider as such also the growing out of the posterior part of the larva
into the adult body which recalls similar processes in the Annelida
(Vol. i., p. 268). It is possible that the development of the Soleno-
gastres, when better known, will throw further light upon their origin.
In the young Dunderda, seven calcareous plates are said to cover the
back, as in Chiton. This stage thus resembles that of Chiton and
this perhaps supports the conjecture that we have in the Amphineura
a less primitive form than was assumed a priori. The absence of
the shell also would no longer have to be regarded as a primitive
feature, nor would the slight development or absence of the foot.
We still indeed have to take into account the important fact that
the shell is wanting in these forms. The covering of the body with
spines and the very primitive internal organisation in any case
indicate that the Solenogastres are very primitive forms. If we
actually have, in them, merely an aberrant branch of the Molluscan
stock, this branch in any case diverged very near the root.
If we are unable to find any direct relations between the Soleno-
gastres and the Annelida, such might perhaps be found between
them and other divisions of the Vermes, such as the Turbellaria or
the Xemertini. The coelom, that very important part of the internal
organisation might, as above shown, with some probability be derived
from the dilation of the gonads in these forms. The conditions of
the coelom in the Mollusca agree in such a striking manner with
those in the Annelida that it is difficult to believe that two structures
so remarkably alike arose in different ways ; in this case we should
have to derive both the Mollusca and the Annelida from Turbellaria
or some similar form. This brings us, however, back to our former
view as to the racial form of the Mollusca made in connection with
the Trochophore larva (p. 321) which, however, was not favourable to
the derivation of the latter from the Turbellaria.
Starting from a creature still more simple in organisation than the
Trochophore, we arrived at the form of the latter and traced the
GENERAL CONSIDERATIONS ON THE MOLLUSCA. 327
acquisition of those characters which determine the typical Mollusc.
We then touched chiefly upon features of the outer organisation, but
some points of internal organisation were also pointed out, such as
the supposed rise of the coeloni from the gonads of the primitive form
and the primary excretory organ, the primitive kidney. A further
important characteristic of the Mollusca is the occurrence of the
(adult) nephridia and their connection with the coelom (pericardium).
We believe the origin of the adult nephridia to be the same as
in the Annelida, Le., we derive them from the protonephridium.
Although nothing is known ontogenetically on this subject, the adult
nephridia, like the primitive kidney, are derived from the middle
germ-layer, a fact which, indeed, indicates a common origin, if only
because the mesoderm originally distributed in the body-cavity
(mesenchyme) and the coelomic mesoderm (the former gonads) had
in any case the same origin, i.e., were derived from the entoderm.
The connection now existing between the nephridia and the coelom
is secondary, for it is wanting in the primitive kidney. The nephridia
took over the transmission to the exterior of the genital products,
when special efferent ducts for them were not developed.*
The circulatory system of the Mollusca, like the coelom and the
nephridia, shows great resemblance to that of the Annelida, a fact
winch inclines us to ascribe it to the primitive form from which the
two stocks are derived. The simplest form of circulatory system was,
in any case, that of a contractile sac open at one end and lying
dorsally. The heart belonged to the primary body-cavity. Where
the coelomic sacs were specially large it was found squeezed in
between them and the intestine, dorsally to the latter. The rise of
the heart between the entoderm and the splanchnic layer of the
mesoderm, still characteristic of many forms, and which, in the
Lamellibranchia, even leads to its development round the intestine
( Figs. 31-3.3, p. 75), led some authors to trace back the heart to one
of the blood-sinuses which encircles the intestine. -f- According to
this view, the blood-sinus would have to be located dorsally to the
intestine. The blood passed into the muscular sac which represented
the primitive heart and which carried on rhythmical contractions, by
means of which the blood was again driven out. There were no
vessels, but the blood ran through spaces anil slits in the mesodermal
* [Sec footnote p. 179 and Goodrich, Quart. Jam. Micro. Set. Vol.
XXX VII.— Ed.]
t This view Which was adopted b\ Grobben lias been discussed in con-
aection with the formation of the heart in the Lamellibranchia (p. 79).
328 GENERAL CONSIDERATIONS ON THE MOLLUSCA.
tissue of the primary body-cavity, a condition which is still passed
through by the embryos of the Mollusca, in which the heart arises
independently of the vessels (pp. 77 and 216).
The blood-vessels must have first arisen when the gills developed.
These later, in any case, arose as very simple leaf like or tubular out-
growths of the body-wall, such as are found as the most primitive
gills in the Annelida, the Arthropoda and the Echinoderma. An
increase of surface soon took place and led to the bipectinate gill,
the so-called ctenidium so characteristic of the Mollusca. This gill
was paired, i.e., a ctenidium was found on either side of the body
concealed in a cavity formed by a fold of the integument. The fold
is the mantle which gx-ew out on each side from the back, and de-
veloped simultaneously with the shell and the gills. As the primitive
Mollusc we must thus imagine an animal somewhat flattened dorso-
ventrally, whose back was covered by a bowl-shaped shell while its
ventral side formed a muscular and slightly projecting creeping sole.
Beneath the lateral parts of the shell lay the mantle enclosing the
pallial cavity and within this the gills. On the pre-oral part of the
body (the head) there were perhaps also the eyes and two tentacles,
corresponding to the cephalic feelers of the Archi-Annelida. In the
oesophagus, the radular sac with the radula became differentiated as
outgrowths, these occurring even in the most primitive of known
Molluscs (Amphineura, Solenogastres). The anus lay at the posterior
end, the nephridia opening out at either side of it. These latter
opened inwardly into the coelomic sacs with which the genital glands
were connected. The two coelomic sacs, dorsally to the intestine, held
the heart between them. The primary body-cavity was traversed
by mesodermal tissue, which became differentiated into connective
tissue and muscles.
From such a simple form of Mollusc can be derived the types
represented in the different divisions known to us. Nearest to it
stand the Chitones, the characteristics of which have been drawn upon
for the above description. The somewhat aberrant conditions of the
Amphineura have already been described above (p. 326). After the
Chitones come the most primitive Gastropods (Diotocardia), the
Chitones themselves being for a long time regarded as Gastropods.
The foot of the Gastropoda, apart from exceptions to be mentioned
presently, has the primitive form of the creeping sole. The marked
development of the head which carries the tentacles and eyes is
characteristic of most Gastropoda. The shell also has attained higher
development and is a constant feature of the Gastropoda; where it
GENERAL CONSIDERATIONS ON THE MOLLUSCA. 3291
is wanting, it has evidently degenerated. To the actual shell, the
operculum lias been added. The position of this latter is like that of
the shell itself, i.e., it lies on the dorsal side of the foot at the point
where the latter passes over into the back. The shifting of the anus
makes it difficult to establish the origin of the operculum. It h;is
been suggested that it arose through abstriction from the shell, but
its independent development and position in the embryo point rather
to an independent origin.
The simple bowl-shaped shell, assumed by us for the primitive
form is no longer retained in this form in the Gastropoda, for the
shell has become twisted. This condition is connected with the
asymmetry of the body which, again, is the result of the one-sided
development of the visceral sac, a feature which is specially character-
istic of the Gastropoda. This one-sided development brings about
displacements of both external and internal organs, and leads to
processes of degeneration {e.g., in the gills, the kidneys, parts of the
circulatory and nervous systems) ; these now occur on one side of the
body only and thus still further increase its asymmetry.* In forms
which lead a pelagic life, such as the Pteropoda, or in creeping forms
that have lost the shell {Onchidivm, Opisthobranchia, Limacidae, etc.)-
there is a more or less complete return to the symmetrical shape.
In the form of the gills, the paired character of the kidneys ami
the auricles, the relations of the coelom and of the nephridia, the
Diotocardia are among the forms most nearly resembling the primitive
Mollusc, but they appear essentially differentiated from it, as the
asymmetry of the body is already found in them.
The relation of the Gastropoda to the primitive form is easier to
trace than is that of the other great branches of the Molluscan stock
(the Solenoconchae, the Lamellibranchia and the Cephalopoda).
The Solenoconchae may be derived from the primitive form by the
extension of the body in a dorsal direction ; the head is much reduced
but develops a large number of tentacular filaments. The foot
becomes the long burrowing foot, the mantle is found to be influenced
by the above-mentioned growth of the body, but on the whole
exhibits the usual features, except that it retains an aperture at its
dorsal apex. In the same way also we can explain the shape of the
shell which resembles a tube open at both ends. According to the
most recent investigations as to the structure of Dentalium it seems
most probable that this form is related to the Gastropoda, the
* Cf. on the asymmetry of the body, Chapter XXXII., p. 143.
330 GENERAL CONSIDERATIONS ON THE MOLLUSCA.
supposed relation to the Lamellibranchia and the Cephalopoda being
untenable.* The Solenoconchae are an aberrant although insignificant
branch of the Molluscan stock, certain resemblances between them
and the Lamellibranchia are to be explained by the fact that they
both branched off' from the same primitive form.
The Lamellibranchia also are much specialised, but may still,
through their lowest representatives, be related to the primitive form.
The Protobranchia, for instance, still possess a foot with a creeping
sole, as well as bipectinate gills. The foot and the gills in the
higher forms, however, though modified, may still be traced back to
the fundamental type. The creeping sole is, in any case, lost in
consequence of their burrowing habit, but, on the other hand, one of
the pedal glands which are found in the different divisions of the
Mollusca develops into the hvssal apparatus.
The reduction of the head and absence of the radula, structures
which are such constant features in nearly all other Molluscs, are
•characteristic of the Lamellibranchia. It has been said, no doubt
rightly, that the radula has been lost ; it is occasionally also wanting
in other forms whose relations possess it as, for instance, in various
Opisthobranchia (Phyllidia, Doridium, Doridopsis, Tethys, etc.).-|-
The shell of the Lamellibranchia has a specially typical develop-
ment. At first it is shaped like a shallow bowl, lying upon the back,
like the shell assumed to have been possessed by the primitive form :
later, however, it bends over on the two sides, calcifies as two pieces,
and thus assumes the typical bivalve form. The formation of the
mantle corresponds to that of the shell.
Among the internal organs, the nervous system, the circulatory
Apparatus, the pericardium (coelom) and the nephridia form in the
way usual among the Mollusca, and this probably also may be said of
these organs in the Cephalopoda.
The Cephalopoda. Of the external organs of this class, the mantle
and gills also resemble those of other Molluscs. The shell too may
he derived from a simpler form, as is evident from the rounded
-chambers found in the embryo. The highly complicated form of the
* Plate, in his recent work on the anatomy of Dentalium, gives a detailed
.account of the relationships of these forms (see Literature to Chapter
XXXI., No. 3, p. 98).
t According to Simroth (No. 17), Tethys (and the related form Melibe), fox-
instance, does not require the radula because its food is soft. A Prosobranch
also (Magilus) has no radula. It lives in a tube covered by corals and feeds
on the offal of these animals. [The Prosobranch families Pyramidellidae and
Eulimidae are also devoid of radulae. — Ed].
GENERAL CONSIDERATIONS ON THE MOLLUSC A. 331
chambered shell of NavAilun, the highest development of the Mollus
can shell, was attained later.
The head, in the Cephalopoda as in the Gastropoda, is well de-
veloped. The arms, which surround the mouth, at first sight appear
to helong to it, and yet, according to the results of more recent re-
search, another significance must be ascribed to them, i.e., they must
be regarded as parts of the foot. A fact which causes surprise and,
at first sight, is unfavourable to this view, is that some of the arms
shift to the dorsal side of the head, being here found behind the
mouth. This makes it difficult to understand how the foot could
have become transformed in this way, but when we sec how extremely
plastic it is, judging from different transformations which it has
undergone in the Lamellibranchia, the Prosobranchia, the Hetero-
poda and the Pteropoda, further modification is not so inconceivable,
especially when we find that the lateral parts of the foot in certain
Prosobranchia (Diotocardia) even develop tentacular structures.
Another part of the foot of the Cephalopoda has at any rate be-
come changed into the funnel, which at first is paired. The pedal
character of this structure has never been doubtful, its origin being
at once betrayed by its position between the mouth and the anus.
The change uudergone by the foot in yielding the funnel is also very
great. We cannot here enter into the cpaestion as to whether, as has
been assumed, we have in this case to do with epipodia. The com-
parison of the different parts of the foot known as the propodium,
mesopodiiun, metapodium, parapodium and epipodium becomes very
difficult in modified forms, the inter-relationships of which alone pre-
sent great difficulties. The conditions of transformation and adapta-
tion may, in the various forms, have developed and modified very
different parts of the foot.
In the Cephalopoda, the organisation of the Mollusca has attained
its highest development. In the structure of the adult the most far-
reaching differentiation has taken place and thus also in its ontogeny
we have the greatest complications found in the Molluscan stock, the
greatest departure being made from those features (total cleavage
of the egg, larval forms, etc.) which we have learnt to regard as
primitive in the lower as well as the higher representatives of the
Mollusca.
332 LITERATURE.
LITERATURE.
1. Brooks, W. K. The development of the digestive tract in
Molluscs. Proc. Boston Soc Nat. Hist. Vol. xx. 1880.
2. Brooks, W. K. The acquisition and loss of food-yolk id
Molluscan eggs. Stud. Biol. Lab. Johns ffopk. Univ. No. 4.
1880. (This and the preceding work were inaccessible to us.)
3. Giard, A. On the relationship of the Annelida and Mollusca.
Ann. Mag. Nat. Hist. (6). Vol. v. 1890.
4. Graff, L. von. Enantia spinifera, der Reprasentant einer
neuer. Polycladen-Familie. Mittheil. Naturw. Vereins Steier-
niark. Graz, 1889.
5. Hatschek, B. 1. Studien uber die Entwicklungsgeschichte der
Anneliden. Arb. Zool. Inst. Wien. Bd. i. and ii. 1878.
Lehrbuch der Zoologie. Jena, 1888-91.
6. Jhering, H. von. Das Nervensy stern und die Phylogenie der
Mollusken. Leipzig, 1878.
7. Jhering H. von. Sur les relations naturelles des Cochlides et
des Ichnopodes. Bull. Sci. France et Belgique (A. Giard).
Tom. xxiii. Paris, 1891.
8. Lankester, E. Ray. Contributions to the developmental
history of the Mollusca. Phil. Trans. London, 1875.
9. Lankester, E. Ray. Contributions to the developmental
history of the Mollusca. Phil. Trans. London, 1875.
10. Lankester, E. Ray. Notes on the Embryology and Classifica-
tion of the Animal Kingdom, etc. Quart. Journ. Micro. Sci.
Vol. xvii. 1877.
11. Lankester, E. Ray. Mollusca in Encyclopaedia Britannica.
Ninth Edition. Vol. xvi. 1883.
12. Lang, A. Die Polycladen des Golfes von Neapel. Leipzig,
1884,
L3. Lang, A. Untersuchungen zur vgl. Anatomie und Histologie
des Nervensystems der Plathelminthen. iv. Tricladen.
Mittheil. Zool. Stat. Neapel. Bd. iii. 1882.
14. Pelseneer, P. Sur l'epipodium des Mollusques. Bull. Sci.
France et Belg. (A. Giard). Tom. xix., xxii., xxiii. 1888-1891.
15. Pelseneer, P. La classification generate des Mollusques.
Bull. Sci. France et Belgique (A. Giard). Tom. xxiv. Paris,
1892.
LITERATURE. 333
16. Roule, L. Consideration sur lembranchement des Trochozo-
aires. Ann. Sci. jYat. (7). Zoo/. Tom. xi. 1891.
17. Simroth, H. Ueber einige Tagesfragen der Malacozoologie, etc.
Zeitschr./. Nattmo. Bd. lxii. Halle, 1889.
18. Spengel, J. W. Die < Jeruchsorgane mid das Nerveusystem
der Mollusken. Zeitschr. f. wiss. Zool. Bd. xxxv. 1881.
19. Thiele, J. Ueber Sinnesorgane der Seitenlinie und das Nerveu-
system von Mollusken. Zeitschr. f. wiss. Zool. Bd. xlix.
1890.
20. Thiele, J. Die Stammesverwandtschaft der Mollusken, etc.
Jen. Zeitschr. f. Naturw. Bd. xxv. 1891.
CHAPTER XXXV.
TUNICATA.
Systematic (after Herdman) : —
Order I. Larvacea (Appendicularia).
Order II. Ascidiaeea.
1. Ascidiae Simplices.
2. Ascidiae Compositae.
3. Ascidiae Luciae (Pyrosvma).
Order III. Thaliacea.
1. Cyclomyaria (Doliolum).
2. Hemimyaria (Salpa, Octaenemus).
I. Sexual Reproduction.
1. Larvacea {Appendicvlaria).
Very little is as yet known as to the development of Appendi-
cularia, since the small eggs which are discharged into the surround-
ing water are not easy to obtain and exceedingly difficult to examine.
Fol (No. 1) and Kowalevsky (treatise on Amphioxus) have, how-
ever, stated that the development of this form closely resembles that
of the Ascidiacea. The paired respiratory tubes of Append icularia
are formed in the same way as the first gill-slits of the Ascidian
larvae (p. 366), an ectodermal invagination appearing at each side and
a diverticulum of the pharynx growing out to meet it until the blind
ends come into contact, perforation taking place at the point of
junction.
2. Ascidiae Simplices and Compositae
A. Oviposition, Fertilisation and Egg-envelopes.
The eggs of most of the solitary Ascidians, soon after passing from
the oviduct into the atrial (peribranchial) cavity, are ejected into the
ASCIDIAE SIMl'LICES AND COMPOSITAE.
33o.
surrounding water where they pass through their embryonic develop-
ment, being supported at the surface by the large, foam-like follicle-
cells (Fig. 149, c). Fertilisation usually takes place either in the
peribronchial (atrial) cavity or after the egg is laid, but exceptions
to this rule are found in the genera Cynthia and Lithonepkrya
(Giakd), these forms passing through their embryonic development
Fig. 148. — Three stages in the development of the egg of Phaliusia tnammillata (after
Kowalevmky, adapted from Ktjpffer, Fol and others). ". basal membrane of the
follicle ; 6, superficial layer of pavement-epithelium ; r, follicle-cells ; ) recently observed in a few Poiyelividae
336 TUNICATA.
(Amarotieittm, Circinalium, Fragarium.) a fusion of the embryo with
the atrial wall of the mother. At this spot a thickening, the placenta,
is formed, derived in part from the atrial wall (placenta materna),
from the follicle-epithelium enveloping the embryo and from an
■accumulation of test-cells (kalymmocytes).
These Ascidiacea are hermaphrodite. Self -fertilisation seems, in-
deed, to be prevented, in most cases, by the maturation at different
times of the male and the female genital products, but is not im-
possible in other cases, in which both products ripen simultaneously.
[In Ciona (Castle, No. II.), although the products ripen at the same
time, self-fertilisation does not occur.]
The mature eggs are surrounded, at the commencement of em-
bryonic development, by a complicated system of envelopes, which
we are inclined to regard as derivatives of the original egg-follicle.
In this respect we agree with Kowalevsky, whose views were con-
firmed later by Van Beneden and Julin (No. 10) as well as by
Morgan (No. 46), but we must point out that the origin of these
envelopes is still an open question. This point will be further dis-
cussed in the section on the formation of the egg under the heading
of general considerations.
Very young eggs, while still in the ovary, appear to be surrounded
by a pavement-epithelium consisting of flattened cells (Fig. 148 A, c).
The elements of this primary follicular epithelium (c) are derived
from undifferentiated cells of the ovary (Van Beneden and Julin).
A structureless basal membrane (a) seems to be secreted early at the
surface of the follicular epithelium. The follicle-cells multiply by
division, and soon lose their flattened form and become cubical ; a
few of these cells ai-e displaced inwai'ds (Fig. 148 B, e) in such a
way as to become deposited on the surface of the egg into which
they may even find their way, passing into the most superficial layer
of the vitellus. These cells, which can usually be distinguished by
their yellow colour, have been called test-cells (<■) because it was
erroneously supposed that they gave rise to the cells of the cellulose
mantle (test) of the adult Ascidian, a view which was refuted by
O. Hertwig (No. 25).* These test-cells, which soon increase very
* [These are the abortive eggs (Abortiveier) of Davidopp (No. 14) and the
kalynvmocytes of more recent authors. There seems to be much uncertainty
about the fate of these cells. Salensky (No. XXIX.), from his investigations
on the compound Aseidiaus, regards them as giving rise to the test (see p.
356) whereas the similarly named cells of Sal/pa appear to be transitory
nutritive structures (Heider, No. XIII. ; Korotneff, No. XVIII. ; Metcalf,
No. XXIV. ; Pizon, No. XXVII.), the most recent investigator of the origin of
the follicle- and test-cells seems to agree with the account given above. — Ed.]
ASCIDIAE SIMPLICES AND COMPOSITAE.
337
Fig. 149. — Mature egg from the oviduct
of Asddia canina * (after Kutffer). c,
follicle-cells (foam-lite cells) ; d, chorion ;
e, test-cells ; f, egg-cell ; ./■, gelatinous
substance.
greatly in number, at first form an inner epithelial layer over the
surface of the egir known as the test-cell-layer (Fig. 148 C, e). In
later stages they undergo a process of degeneration. They then lose
the regularity of their arrange-
ment and are found embedded
separately in a gelatinous nuiss
secreted over the surface of the
egg. Their original cellular
character is then less distinct
and has been altogether denied
by some authors (Sempek, Fol).
After the development of the
test-cell-layer, a structureless
membrane (Figs. 148, 149, t' the body
becoming swollen in consequence
of the increased curvature of its
two layers (Fig. 152 B). This
arching is connected with the
gradual narrowimjof the blastopore
which takes place on the dorsal
side of the embryo in such a way
that its last vestige lies near the
posterior end of the body (Fig.
153 ('). ( friginally, the blastopore
is a wide oval aperture, but in
later stages it is pear-shaped, and
it filially becomes a small posterior
aperture (Fig. 153, b-b"). This
narrowing of the blastopore is
caused principally by the inward
growth of its anterior and lateral
margins, the posterior edge re-
maining unchanged. We have
here conditions exactly similar to
those in Amphioxus, and we may
assume a continuous closure from
before backward of the blastopore
which originally extended along
the whole length of the dorsal
surface.
During these stages even, the
embryo becomes somewhat elon-
gated in the direction of the
longitudinal axis (Fig. 152 G).
The dorsal side is recognisable by
its flatter condition, and shows, at
its posterior end, the remains of
the blastopore (j>) ; the ventral
side, on the contrary, is arched.
vax Bf.neden and Julin have
pointed out that the posterior end
of the body, at the gastrula-stage,
is always marked by the presence
of two small wedge-shaped ectoderm-cells lying ;it the edge of the
Fig. 152. Three consecutive gastrula-
stages of Phalhisia maininillata (alter
Kowai.evsky). .1. the invagination
commencing ; B, appearance of the
bilateral symmetry; C, narrowing of
the blastopore : a-b, principal axis oi
tin- gastrula-stage; c-c', later longi-
tudinal axis nt the body ; d, 'I'
side; ec, ectoderm; en, entoderm ;f,
cleavage-cavity ; /<. blastopore ; <\
ventral side.
344
TUNIC ATA.
blastopore and representing the boundary between the ectoderm and
the entoderm (Fig. 154, ./■).
In these later gastrula-stages the commencement of histological
differentiation is already evident.
This does not consist merely in
the distinction between the ecto-
dermal and the entodermal elements,
although the latter are larger, more
strongly granular and darker in
colour; but differentiations are
already to be found within these
germ-layers. The ectoderm-cells
which bound the blastopore, for
instance (Fig. 154 A, n), are dis-
tinguished by the large size of their
nuclei, their greater affinity for
carmine stain, and their cubical
shape from the other ectoderm-cells, which soon become flattened.
This ring of cells is the first rudiment of the central nervous system,
and, as the blastopore closes more and more, changes into the
Fig. 153. — Dorsal aspect of an embryo
of Clavelina (after Sebliger). b, V,
b", outlines of the blastopore at three
consecutive stages of development.
Fig. 154.— Gastrula-stage oi Clavelina Rissoaiux (after van Beneden and Junxi
.1. dorsal aspect; /,', medial: sagittal section, b, blastopore; ec, ectoderm- en
entoderm ; n, cells ot the nerve-ring; x, small, wedge-shaped cells.
\KCIM u K \ -FORMATION OK THE GERM-LAYEBS.
34a
medullary plate.* This rudiment, when it first appears, consists, at
the sides of the still open blastopore, of a single row of cells, while,
in front of the blastopore, it is composed of several rows of cells.
In later stages (Fig. 154), as the blastopore narrows, the part of
the medullary plate in front of it extends more and more, and, at the
time when the blastopore is represented by merely a small aperture
(Fig. 155), is a large and slightly depressed area. The medullary
groove thus formed, which is open anteriorly, is bounded by two
6 en'
Fn;. 155. — Later ontogenetic stage of Clavelina Rissoana with the blastopore much
narrowed, and the medullary groove appearing (after van Benedex and Julin). A,
dorsal aspect; /,', median sagittal section, h, blastopore: <•/', rudiment of tin-
chorda; ec, ectoderm; era, entoderm; m, medullary groove ; n, cells of the nerve-
ring.
lateral swellings (medullary swellings, m) which pass into one another
behind the blastopore, thus forming a semicircle.
A differentiation similar to the above is evident in the entoderm
(Fig. 158). The cells of the latter, as a rule, are large and turgid,
but in the region of the dorsal wall smaller cells appear which are
originally arranged so as to form a ring encircling the blastopore, one
* [According to Castle (No. II.), the cells lying behind the blastopore and
marked n in Figs. 154 and 155 are not part of the rudiment of the central
nervous system as stated by Jdlin and van Beneden, but are in reality
muscle-cells. The rudiment of the nervous system is situated entirely in
front of the blastopore. In Ciona the posterior margin of the blastopore does
not grow forward over the blastopore, covering in the medullary canal, as
described bv van Beneof.n and Julin in the ease of Clavelina. — Ed.]
346
TUNICATA.
side of which, however, as the blastopore narrows, soon extends to
form a cell -area in front of it. The whole of this area represents the
en
ec
Fig. 156. — -Transverse sections through two gastrula-stages of Distaplia magnilarva
(after Davidoff). A, younger stage: B, transverse section through the posterior
part of an older stage, b, blastopore ; ec, ectoderm; en, entoderm; n, nerve-ring.
common rudiment of the mesoderm and the chorda, the " chorda-
1116861101171116' ' ring. The middle cells of this area soon become more
n distinctly separated from
the rest, and represent the
plate-like rudiment of the
chorda (Fig. 158, ch), while
the cells that lie laterally
give rise to the mesoderm -
bands (ms).*
In the eggs of the composite
Ascidians, which are rich in
yolk, the formation of the
germ-layers is to a certain ex-
tent modified. The cleavage-
cavity which, in Phallusia,
is rather large, is smaller in
Clarclina, while in Distaplia
(according to Davidoff) it
can only be seen in the first
£*.
Fig. 157. — Transverse section through an embryo
of Distaplia magnilarva after the closing of the
blastopore (after Davidoff). ec, ectoderm ; en,
entoderm; ms, mesoderm ; it, neural plate.
*[In Ciona, according to Castle, the mesoderm-rudiment is made up of cells
derived from both hemispheres and all four quadrants, a condition very
different from that seen in the Mollusca, where the mesoderm typically arises
from the left posterior entodermal macromere. — Ed.]
ASCIDIACEA — FORMATION OF THK GEKM-LAYKKS.
347
stages as a narrow slit. The entoderm-cells also, in tltis latter form, do not long
retain their unilaminar arrangement, hut become distributed in a radial direc-
ILT~-
~~~ec
~ms
ec-
ertr
-71'
Fn;. 158. — Stage of Clon'li ,m Itisxnuiia showing the f'oriiiation of the neural tube
(after VAN Beneden and Julin). A, dorsal view ; the cell-boundaries drawn are
those between the cells of the dorsal entoderm-wall ; B, median sagittal section.
ch, rudiment of the chorda; ec, ectoderm; en, entoderm ; ?ns, mesoderm : n, cells of
the neural plate; n', roof of the medullary tube; nr, medullary tube; n/>, the
neuropore, still very large.
tion. the entoderm thus becoming multilaminar
in reality reached through epibole (Fig.
156). In the anterior region of the body
this overgrowth is especially marked, while in
the posterior half, a small pit-like depression
(Fig. 156 B) indicates the last remains of an
invagination-cavity. This cavity, however,
completely disappears after the blastopore has
closed. The entoderm then represents a solid
mass, the cells of which are soon found to
vary in size. The position of the blastopore
is occupied by the neural plate (»).
The gastrula-stage is here
ch
During these stages, the medullary
plate, which is already somewhat invagin-
ated, changes into a closed medullary
tube, its lateral walls, the medullary
folds, growing towards one another and
fusing (Fig. 160).
■ee
Fig. 159. — Transverse section
through an embryo of Clave-
lina (after van Beneden and
Julin* ). ch, rudiment of the
chorda : ec, ectoderm ; en, ento-
derm ; ins, mesoderm-diverti-
culum ; in"', medullary told- ;
», medullary plate.
The medullary tube develops from behind forward, a special part being
taken in the process by the fold which connects the two medullary swellings
348
TUNICATA.
posteriorly in the form of a semicircle (Figs. 155 and 158). It then appears,
especially in longitudinal sections (Fig. 158 B), as if the medullary tube was
formed solely by the posterior lip of the blastopore growing over the anterior
lip. We must, however, bear in mind that, as this posterior medullary fold
Fig. 160. — Transverse sections through an embryo of Claoclina Rissoana, at the same
stage as in Fig. 158 (adapted from van Benedex and Julix). A, through the
anterior, B, through the middle, and C, through the posterior part of the body.
rh , chorda ; d, lumen of intestine ; en, entoderm ; n, medullary plate ; nr, medullary
tube.
grows forwards, the lateral medullary swellings are drawn into it, so that the
posterior fold does not actually represent the lip of the blastopore, but a purely
ectodermal fold lying at this point ; in this way, after the medullary tube has
developed, its roof (»') which is derived from the inner layer of the folds is
also to be regarded as ectodermal. This is a point which deserves to be
emphasised in opposition to the view of Metschnikofp (No. 42). [Cf. foot-
note, p. 345.]
Fig. 161. — Transverse sections through an embryo of Clavelina Rissoana, at the same
stage as in Fig. 162 (adapted from van Benedex and Julix). A, through the
anterior, Jl, through the middle, and C, through the posterior section of the body.
eh, chorda'; en, entoderm ; rns, mesoderm ; nr, medullary tube; x, cells which com-
plete the dorsal wall of the intestinal canal.
We shall see (Chap. XXXVI.) that, in Amphioxus, the medullary tube forms
by the sinking in of the somewhat depressed medullary plate and its separa-
tion as such from the ectoderm; hence it is only covered by a single layer
of cells. Only at a later stage does the plate curl round under the ectoderm
to fi'i in a tube. This manner of formation is probably a modification of the
WIDIACEA FORMATION OF THE (iKKM- LAYERS.
349
origin from folds and is stated by Seeligeb (No. 50) as occurring in ClaveUna
also, but his observations on this subject were not confirmed by van Benedkn
and Julin (No. 10). These latter authors also do not agree in Seelig i ib -
view thai the medullary groove, at the time when it appears, lengthens
posteriorly beyond the blastopore.
At the time when the medullary tube develops, the blastopore has not com-
pletely closed. The remains of it, which originally lie in the floor of the de-
veloping medullary groove, are retained for some time longer as the neurenteric
ritual and form a communication betweeen the lumen of the intestine and the
central canal of the medullary tube (Fig. 158 B).
— Tip
■nr
ms
FlG. 162. — Stage at which, in ClaveUna Rissoana, the trunk-region begins to separate
from the caudal region (after van Beneden and Juun). .1. median sagittal section ;
/i, lateral aspect, ch, chorda; d, archenteric cavity; ec, ectoderm ; en, entoderm ;
en', sub-chordal entoderm-strand ; ms, anterior portion of the mesoderm-haii'ls
composed of small cells ; ,,/s', posterior portion of the same composed of large cells ;
rip, neuropore; ///-, medullary tube.
AlS the medullary tube develops from behind Forward, the aperture
at its anterior cud, known as the neuropore (Fig. 162, np), is retained
for a long time. The separation of the mesoderm from the chorda
dorsalis takes phice simultaneously with the development of the
medullary tube. These two rudiments arise, as may be ascertained
from the detailed accounts of van Beneden and Julin, essentially
through the same processes of development as in Amphioxus, although
the conditions are in this case not so evident, and seem specially
modified in the posterior region of the body. The embryo soon
assumes a long, pear-shaped form (Fig. 162), the posterior, narrowed
350 TUNICATA.
region corresponding to the future tail of the larva. In the anterior,
diluted region, the mesoderm arises through the development of
paired diverticula of the archenteron (Figs. 159, A, ms), the lumens
of these sacs very soon disappear and the cells of their walls,
which originally were arranged in two layers (the somatic and the
splanchnic layers), then appear irregularly distributed between the
ectoderm and the entoderm. Between the two coelomic diverticula,
the i*oof the archenteric wall is completed by entoderm-cells (Figs.
159, 160 A, 161 A, ch) which represent the rudiment of the chorda.
At a later stage, these cells become shifted into closer proximity, and
thus form a solid strand which, in cross-section, is round. The fact
that this strand is to be traced back to a median fold of the arch-
enteron is proved by transverse sections through the most anterior
part of the rudiment of the chorda (Figs. 160 A, 161 A), where the
infolding of the cell -plate which represents the rudiment of the
chorda can actually be seen (van Beneden and Julin, No. 10).
In Amphioxus, according to Hatschek, the median fold of the intestinal
wall is not completely absorbed in the formation of the chorda. Its lateral
cells, which are in contact with the coelomic diverticula, yield the cells which
complete the dorsal wall of the intestine after the chorda has separated from
the mesoderm, van Beneden and Julin conjecture that similar conditions
exist in the anterior part of the chorda-rudiment in the Ascidians (cf. Fig.
161 A, x).
A certain guarantee of the accuracy of the observations made by van
Beneden and Julin seems to be afforded by the striking resemblance to the
formation of the mesoderm in Amphioxus. Their observations, however,
have not been confirmed either by Davidopf (No. 14), who investigated the
formation of the mesoderm in CI are Una and Distaplia or by Willey (No.
54a). According to the former author, the mesoderm-cells become abstricted
from definite entoderm-cells at the margin of the blastopore (mesoderm-
gonads), and become arranged in an originally single layer below the
entoderm. This would be a kind of mesoderm-formation by delamination.
Davidoff was unable to find coelomic diverticula. The "mesoderm-gonads"
are said to remain in connection with the entoderm, and, after the mesoderm
has been produced, some of them are said to take part in the formation of the
chorda and others in that of the alimentary canal. *
In the posterior region of the body (the future caudal region), the
condition appears to be modified through the early disappearance of
the lumen of the intestine (Fig. 160 C). The strand-like chorda is
* [In Ciona, the mesoderm-cells form temporarily part of the wall of the
archenteron between the chorda and the entoderm. Eventually they become
displaced outwardly and the entoderm and chorda come into contact. Ac-
cording to Castle (No. II.) there does not appear to be any enterocoelic
formation in this genus. — Ed.]
ASCIDIACKA — FORMATION OF THE GEK.M-LAVKKS.
351
here pressed inward by the developing medullary tube, so that it
then fills the whole lumen of the intestine. The lateral cells of the
wall of the enteron, three of which are usually seen on either side
JK".
Fig. 163.— Later stage of development of Clavelina Rissoana (after vam Beneden and
Juux). A, median sagittal section; A', lateral aspect, ch, chorda ; ec, ectoderm;
en, entoderm: en', subchordal entoderm-strand in the caudal region; ms, anterior
small-celled portion of the mesoderm-bands ; ms', posterior large-celled caudal
section of the same ; np, neuropore ; nr, medullary tube.
in cross-section, pass directly into the large mesoderm-elements
which cover the chorda laterally and subsequently yield the caudal
musculature. There then still remain the entoderm-cells that lie
352
TUNICATA.
in the ventral middle line (Figs. 160 C and 161 G, en) ; these, which
are arranged in two parallel rows, retain the character of ordinary
entoderm-cells and form a permanent cell-strand connected with the
intestine, in which we recognise the vestiges of a caudal section of
the alimentary canal (Fig. 162 A, 163 A, en').
FlQ. 164. — Median sagittal sections of two stages of development of Distaplia magni-
larva (after Davidoff). c, rudiment of the caudal section of the intestine ; ch,
rudiment of the chorda; d, enteric cavity; ec, ectoderm; en, entoderm; n,
medullary plate ; up, neuropore ; nr, medullary tube.
In the caudal region, the separation of the mesoderm and the chorda takes
place in a very simple way, the archenteron merely breaking up into the two
rudiments. These structures, however, are probably to be derived in a way
similar to that described above for the anterior region of the body. We
ASCIDIACEA FORMATION OP THE GERM-LAYERS.
353
shall have here to assume (with van Beneden and Julin) in these regions,
the presence of a lumen of the archenteron compressed through the growth of
the chorda-rudiment to the shape of a crescent. The question here arises
whether the mesoderm-layer of the caudal section is to be referred to the
splanchnic or the somatic layer of the former mesoderm-rudiment. van
Beneden and .Il'lix incline bo the first assumption, and Seeliger (No.' 50)
has also pointed out the resemblance of the mesoderm-cells of the caudal
section to to the cells of the inner layer (if the mesoderm in the anterior
region of the body.
Fie. 165. — A later stage in the development of Distaplia magnilarva (after Davidoff).
c, caudal prolongation of the alimentary canal; ch, rudiment of the chorda;
d, enteric cavity; ec, ectoderm; en. entoderm; h. adhesive papillae; ms, mesen-
clivme-cells ; nr, medullary tube.
^
The mesoderm and the chorda are therefore derivatives of the
primary entoderm.* Their origin can be traced back to the form of
folding which is also found in Amphioxus. The principal distinction
between the process hei'e and in Amphioxus seems to be that, in the
mesoderm-rudiment of the Ascidians, no trace is to be found of the
segmentation which appears so early in Amphioxus. In the Ascidians
the mesoderm-bands appear composed of two different parts (Figs.
162 B, 163 B) ; an anterior part (ms), consisting of several layers of
small cells, which has arisen through folding in the anterior part of
the archenteron, and a posterior part composed of a single layer of
large cells (ms') belonging to the caudal region. The anterior part of
the mesoderm, at a later stage, forms a mesenchyme filling the
* [See footnote, p. 340.— Ed.]
AA
354 TUNICATA.
primary body-cavity (Fig. 167, ms) which yields the blood-corpuscles,
the connective tissue, the body- musculature, as well as the genital and
excretory organs, while the posterior part gives rise to the larval
caudal musculature (Fi^. 168 B, m).
In Distaplia, in which, after the closure of the blastopore, the
entoderm forms a solid cell-mass (Figs. 157, 164 A), the enteric
cavity arises only later through the shifting apart of these cells (Fig.
164 B). In this way a posterior part of the body is marked off; in
this the cells of the entoderm separate into the rudiment of the
chorda (Fig. 164, ch) and into that of the solid sub-chordal enteric-
process (c), while the large entoderm-cells in the anterior region of
the body (Fig. 165, en) mix later with the mesenchyme and probably
disintegrate. In other respects there is no essential difference be-
tween the development of Distaplia as described by Davidoff (No.
14) and that of other Ascidians. It should be pointed out that the
elements of the food-yolk here appear equally distributed in all the
tissues (the ectoderm, the mesoderm and the entoderm).
D. Development of the free-swimming larva.
External form of the body. We have already pointed out that,
at the time when the medullary tube develops, the embryo becomes
elongate and pear-shaped. In this way a broader anterior section is
marked off from a narrower posterior section (Fig. 162) which gives
rise to the tail of the larva. This latter part of the body next grows
greatly in length, less, as Seeligek points out, by the multiplication
than by the elongation of the cells composing it. At the same time,
it becomes more distinctly constricted from the anterior section and
curves round ventrally (Fig. 163). As the tail, which is now bent
downwards and forwards, increases in length, its posteiuor end not
only reaches the anterior end of the body but even grows upwards
again at the right side of the latter. In this process, the tail be-
comes twisted on its longitudinal axis, so that the nerve-tube appears
shifted to the left side of the embryo (Fig. 170, p. 368).
The anterior region of the body, which at first appears more or less
spherical, lengthens later, and in the larva is ovate (Figs. 167 and
168). Three prominences, arising as thickenings of the ectoderm,
can soon be seen at its anterior end ; these are the rudiments of the
papillae for attachment (Figs. 167, 168, 170, h), through which, by
means of a secretion yielded by the glandular epithelium, the fixation
of the larva takes place.
ASCIDIACEA — DEVELOPMENT OF THE FREE-SWIMMING LARVA. 355
Balfour lias pointed out that, since a similar attaching apparatus is found
in Amphibian larvae and (in front of the mouth) in the larvae of many
Ganoids (Acipenser, Lepidostetis) we may perhaps have here an inherited
feature common to the Chordata. It seems doubtful, however, to what ex-
tent these structures are really homologous and not merely analogous.
After the egg-envelope has burst, the larva straightens out. The
tail then forms a direct posterior continuation of the longitudinal
axis of the body (Figs. 167 and 17:'. A, p. 375).
PlG. 166. — Transverse section through an attached larva of Phallusia manimiUata
(after Eowalbvskt). ", mesenchyme-cells in the act of passing through the
ectoderm; b, mesenchyme-cells in the cellulose mantle; d, alimentary canal;
• '•. ectoderm; ms, mesenchyme-cells; ot, otolith; s, transverse section through
tin' sensorv vesicle; t, cellulose mantle.
The mantle. The ectoderm-cells, which originally were somewhat
cubical but assumed a more flattened form, at the time when the
caudal region develops, secrete, at their outer surface, a homogeneous
cuticular layer which, from its first appearance, gives a cellulose
reaction. This is the first rudiment of the Ascidian test or tunic.
In the caudal region, this layer grows out to form a median dorsal
and a ventral fin (Fig. 169, //, p. 363). While, in Doliolwm and
Appendicularia, such a simple, homogeneous cuticular layer is
retained throughout life, in the Ascidiacea and Hemimyaria it is
considerably thickened, single cells immigrating into the cellulose
356
TUNICATA.
layer. It has hitherto been believed that, as 0. Hertwig (No. 25)
maintained, the cells that wandered into the cellulose substance came
from the ectoderm, but Kowalevsky (No. 32) has recently proved*
that the mantle-cells were derived from the mesoderm, being meso-
dermal cells which traverse the ectoderm and thus migrate outwards
(Fig. 166). Subsequently, in the cellulose substance, they assume
3
-Ml.
Cfl
,M th. V
Fig. 167. — Embryos of Phallusia mammillata at a later stage (after Kowalevsky)'
.1. lateral aspect; B, dorsal aspect, au, eye; ch, chorda; cl, cloaca! vesicle; d,
rudiment of the alimentary canal ; en, entoderm-sac ; f, ciliated pit ; /;, adhesive
papillae ; ;', mouth ; ms. mesendiynie-cells ; <>t, otolith ; r, trunk-section, s, caudal
section of the medullary tube ; sb, sensory vesicle ; sc, sub-chordal entoderm-
strand ; v, vacuoles between the cells of the chorda.
the character of star-shaped connective-tissue cells. We have to
regard the mantle of the Tunicates as a cuticular gelatinous secretion
permeated by phagocytes (mesoderm-cells).t When, in the composite
Ascidians, some of the individuals disintegrate, the phagocytes of the
* Salensky's recent statements as to Pyrosoma (No. 74) fully agree with this
observation (see below, p. 401).
[+ Seeliger (No. XXXIII.) agrees with Kowalevsky that the true test-
cells are mesodermal. In Oikopleura, however, the cells of the "Haus" are
ectodermal. -Ed.]
ASCIDIACEA — DEVELOPMENT OF THE FREE-SWIMMING LARVA. 367
mantle play art important part in the process (Maurice, No. 40).
The histological character of the mantle-tissue may undergo further
modification, such as the vesicular transformation of the mantle-cells
ii. Phalltma, and the appearance of fibrillae in the ground-substance
in Cynthia.
Since the surface of the embryo is, from the earliest stage, surrounded by
a gelatinous covering, in which lie embedded the yellow test-cells, it was
formerly thought that this layer was to be regarded as the rudiment of the
future mantle (Kowalevsky, Kupffer), an error to which the test-cells owe
their name. Zoologists were inclined to consider the mantle of the Ascidians
as a persisting embryonic envelope. O. Hertwig first proved that the test-
cell-layer is lost and that the mantle arises from the ectoderm. The im-
migration of the mantle-cells was only recently observed by Kowalevsky.
Salensky, however, in a recent treatise (No. 49, also No. XXIX.) has returned
to the older view, ascribing to the test-cells (kalymmocytes) in Bistaplia the
principal part in the formation of the cellulose mantle [see footnote, p. 336.]
The nervous system. The rudiment of the central nervous system
which has hitherto been called the medullary tube, from the early
stages onward, shows a dilatation of its anterior section (Fig. 163,
>n\ p. 351). In the later stages which lead to the development of
the free-swimming larva, this dilated anterior part gives rise to a
vesicle, the so-called cerebral <>r sensory vesicle (Fig. 167, sb, vesicuh.
ante'rieure ou cere'brale of van Beneden and Julin) while the
posterior, narrowed part yields the caudal section (region caudate) of
the nerve-cord (s). These two parts appear connected by a middle
part (/■) with a narrow central canal and thickened wall which
Kowalevsky (No. 30) has called the trunk-ganglion (portion viscerale
'in myelencephale of van Beneden and Julin). The former con-
nection between the neural tube and the exterior (the neuropore)
completely closes even before the appearance of the oral aperture,
which lies near the same point.
The <■> ,■< i>rnl or sensory vesicle represents the most anterior part of
the medullary tube swollen out into a vesicle by the dilatation of its
central canal. Its walls consist for the most part of pavement-
epithelium, but the dorsal wall is thickened and divided into a right
and a left swelling by a median furrow (van Beneden and Julin,
Xo. 7). The two organs known as the eye and the otocyst {on and -'), is
a cup-like deposit of pigment at the inner ends of several radially
placed columnar cells, the cavity being occupied by a lens with a
superimposed meniscus (Fig. 168).
358
TUNICATA.
According to Seeliger, the lens and the meniscus develop within a single
cell derived from the wall of the sensory vesicle. Kowalevsky, on the
contrary, believes that they arise from three cells, and this agrees with
Leuckart's statement (No. 37) that three biconvex lenses are found within
the pigmented eye-cup.
K"-
i-
Fig. 168. — Anterior region of the body in the free-swimming larva of Phallusia
mammillata (after Kowalevsky). A, lateral aspect; B, dorsal aspect. an. eye;
b, blood-sinus between the gill-clefts . ch, chorda ; <■/, cloacal aperture ; tl, alimentary
canal; ed, intestine; es, eudostyle ; /. ciliated pit; k, adhesive papillae ; i, mouth
(branchial aperture); k', k", first and second gill-slits; //;, caudal muscles; ms,
meseuchyme-cells ; ot, otolith ; r, trunk-section of the medullary tube ; s, caudal
section of the medullary tube ; sb, sensory vesicle.
Tlie so-called auditory organ (Fig. 168, ot) consists of a pear-shaped
or conical cell (otolith-cell) projecting into the interior of the sensory
vesicle, the narrowed end of which is inserted between the cells of
ASCIDIACEA — DEVELOPMENT OF THE FREE-SWIMMING LARVA. 369
the ventral wall of the vesicle while the free euT
from the eye, i.e., as a rule, on the left side, although Lakille
(No. 37) considers that this condition varies in the different forms.
Lahille (No. 37), Sheldon (No. 52), Willey, (No. 54), and
Hjort (No. 59), on the contrary, have been led by their researches,
to confirm in almost all points the older observations of Ko\vai,k\
sky as to the rise of the ciliated pit, Le., t<> regard it, in its origin,
as much more closely connected with the central nervous system.
After the neuropore has completely closed, the most anterior section
of the cephalic vesicle lengthens and fuses with an ectodermal
depression, the stomodaeum (rudiment of the larval mouth, branchial
aperture). At this point perforation takes place (Figs. 167 A, 168
.1,/), so that now the cephalic cavity, by means of this short tube
which represents the rudiment of the ciliated pit, communicates with
the most anterior ectodermal section of the alimentary canal. Only
in later stages when, after the fixation of the larva, the larval
nervous system degenerates, is the connection between the ciliated
pit and the nervous system lost. The pit then forms a blind in-
testinal diverticulum contiguous with the definitive ganglion (Fig.
173.7/).*
According to these statements, the ciliated pit opens into the ectodermal
or stomodaeal portion of the branchial sac, and we thus have a condition
agreeing with that of the hypophysis in the Vertebrata.
The chorda. The chorda arises through the transformation of a
plate-like rudiment (Fig. 159, ch), which originally formed the roof
of the archenteron, into a cell-strand which, in cross-section, is
round (c/. Figs. 160 and 161, ch). We have seen above (p. 348)
that we must suppose this to have been brought about by the forma-
tion of a groove (as in Amphioxus). In cross-section, the chorda-strand
is originally composed of several cells. Both in lateral (Fig. 162 A)
and in dorsal aspect it appears composed of two rows of cells, the
ends of which dove-tail with one another. This dove-tailing of
the cells denotes the commencement of a change of position which in
most cases leads to the chorda-cells appearing- arranged one behind
the other in a single row like a roll of coins (Fig. 163 A). In those
* [ Willey (No. XXXVI.) has recently reinvestigated this point both in
(',10)1(1 and Clavelina. He is convinced that van Beneden and Julih were
quite mistaken in their interpretation of the origin of the hypophysial tube
in Clavelina. The whole is derived essentially from the neural tube, and
thus the lumen of the hypophysis is at Hist in direct communication with
the lumen of the central nervous system, the opening of this structure into
the pharvnx being, according to Willky. a reopening of the neuropore. —
Ed.]
362 TUNICATA.
later stages which are connected with ;i lengthening of the caudal
section, the cells of the chorda-strand also lengthen (Figs. 167 A,
170, ch). The chorda then begins to undergo a transformation which,
at its commencement, is comparable to the changes in the chorda
of Amphioxus, but, in the Ascidians, leads to peculiar modifications in
this organ. Between each two consecutive cells there appears a
vacuole filled with a gelatinous substance (Fig. 167, v; cf. also Fig.
170). These vacuoles, which, at first, lie in the axis of the chorda-
strand, as they enlarge, compress the chorda cells in such a way that
the latter soon assume the biconcave form of fish- vertebrae and, as
the gelatinous mass extends further, can be recognised merely as
thin septa between its different sections. These sections soon come
into contact and fuse, and in this way a strand of homogeneous
gelatinous substance arises which at first resembles a string of beads
but is later uniform and cylindrical (Fig. 168 A), while the chorda-
cells which are pressed out to its surface surround it as a kind of
sheath (Kowalbvsky, Kupffer, Seeliger, and others).
The transformation of the chorda is not, in all Ascidians, so complete.
According to Seeliger, in Clavelina, it does not advance beyond the stage in
which the chorda-cells assume the form of transverse septa.
Mesoderm, body-cavity, musculature. The two mesoderm-bands
accompany the chorda along its whole length and project a little
beyond it anteriorly. Two parts can be distinguished in them (Figs.
162 B, 163 B). In the posterior part (ms) where they consist of a single
layer of large cells arranged in three longitudinal rows, they yield
the musculature of the larval tail. The cells of this part lengthen
in later stages of development (Fig. 168 />', m) becoming hexagonal,
while, on their inner and outer surfaces they produce longitudinal
fibrils of contractile substance (Fig. 169, nr.) which appear to lie
somewhat obliquely to the longitudinal axis of the body in such a
way that the fibres of the inner layer cross those of the outer layer
at an acute angle (Seeliger). The caudal musculature of the larva
which arises in this way shows indistinct transverse striation.
Anteriorly, in the trunk-region, the mesoderm-bands consist of
several layers of smaller cells at first closely crowded together (Figs.
161 J, ms, 162, 1 ()."), ms). The innermost layer which lies next to
the chorda is evidently a direct prolongation of the myoblast-layer of
the caudal region. It undergoes the same transformations as the
latter and yields the anterior part of the larval musculature. The con-
nection between the other mesoderm-cells of this region soon becomes
ASCID1ACEA DEVELOPMENT OK THE FREE-SU I M MING LARVA. 363
somewhat loosened ; they assume a spherical form and constitute a
mesenchyne which tills the primary body-cavity of the trunk-section
(Fig. 168, ms).
We have seen (p. 350) that, according to van Beneden and Julin,
the mesoderm in this anterior part heroines detached from the ai-ch-
enteron in the form of paired coelomic
diverticula (Figs. L 59 and ISO A). The
true eoelom that arises in this way
belongs, however, merely to the earliest
embryonic stages, and disappears even
as early as the time when the mesoderm
completely separates from the entoderm.
The mesoderm then tills the space
between the ectoderm and the entoderm,
which, in later stages, becomes consider-
ably widened and, as it appears, filled
with a gelatinous mass ; this forms the
-round - substance of the mesenchyme
that arises through the transformation
of this anterior portion of the mesoderm.
The lacunae which arise later in this
mesenchyme must be regarded, like
the blood-vessels (which, according to
van Beneden and Julin are entirely
devoid of an endothelial wall) as the
pseudocoele.
The mesenchyme of the trunk-region,
which is derived in the above wav, yields
the mesodermal organs of the adult
AAcidian. Its histological differentiation
uives rise to the connective tissue, as
well as to the pigmented elements,
and to the body-musculature of the
adult which appears arranged in radial
and circular muscles surrounding the
inhalent and exhalent orifices as well as into longitudinal muscles
<>f the trunk, etc. Single cells of the mesenchyme, which become
tree and reach the pseudocoele, become changed into blood-
corpuscles. We shall see later (p. 380) that the genital organs
also, with their efferent ducts, and the urinary organs originate in
the mesoderm.
FlG. 169. — Transverse section
through the caudal portion oi
the free - swimming larva of
( Vavelina (after Seeliger). ch,
chorda ; ee, ectoderm : Jt,
median tin ; m, cellulose
mantle ; mf, muscle-fibrillae in
transverse section : »>".. muscle-
cells; />/•. neural tube; s, sub-
chordal entoderm - strand ; .
mantle- cells.
364 TUNICATA.
It must be mentioned that at a later stage (especially during the transforma-
tion connected with fixation) the mesenchyme becomes apparently enriched
by elements which, when the entodermal strand (Fig. 169, s) and the larval
nervous system disintegrate, become free. Kowalevsky thought that these
cells became changed into blood-corpuscles, and later, Seeliger (No. 50)
utilised this fact in constructing his theory of the budding in compound
forms. It, however, appears doubtful to us whether these elements take any
part whatever in the formation of the organs of the adult or of their buds or
whether they do not rather, after reaching the blood, undergo degeneration.
The alimentary canal. The rudiment of the alimentary canal is
derived from the archenteron by the separation of the mesoderm
bands and the chorda-strand. In early embryonic stages (Figs. 162,
163, p. 351) it consists of an anterior pre-chordal dilatation (en) and,
following this, of a narrowed part lying already below the chorda but
still belonging to the trunk-region. This narrowest part is directly
continued into the sub-chordal entoderm-strand of the caudal region
(en') which must be regarded as the intestinal rudiment of this
part of the body.
Since the mesoderm and the chorda (as seen above, p. 350) arise
by a process of folding from the dorsal wall of the archenteron, the
dorsal wall of the intestine is defective at this point ; this gap be-
comes closed in later stages by certain cells as described above
(p. 350). This defect is only found in the trunk-region in the
posterior narrowed part of the alimentary canal, as the rudiment of
the caudal region undergoes no further advance in form and, on the
other hand, the pre-chordal section of the intestine takes no part in
the foldings which give rise to the mesoderm and the chorda. This
narrowed sub-chordal trunk-portion of the intestine, after the gap
just mentioned has closed, forms a blind diverticulum projecting
backward (Fig. 167 A, d, p. 356), the end of which, according to
Kowalevsky, at those stages in which the caudal section becomes
more sharply marked off from the trunk, bends slightly towards the
dorsal side, thus severing its connection with the cellular entoderm-
band of rlie caudal region (sc). In this way is introduced the de-
generation of this last part of the intestine mentioned above, which
leads to the cells of this band becoming disconnected and assuming
a resemblance to blood-corpuscles. We then find, beneath the chorda
in the caudal region, a cavity apparently filled with blood-corpuscles
and in direct communication with the spaces of the pseudocode.
According to Kowalevsky, with whom the .majority of later
authors (Kupffer, Seeliger) agree, the branchial sac or pharynx
is derived from the pre-chordal dilatation of the intestinal rudiment,
\SCIDIACEA DEVELOPMENT OK THE FREE-SWIMMING LARVA. 365
while the sub-chorda] diverticulum, which is directed backward (d),
yields, through simple growth, the other parts of the alimentary
canal (the oesophagus, the stomach and the intestine proper). This
diverticulum, as the larva lengthens, is said to form a eoil in which
we can distinguish a right descending portion, a ventral connecting
piece, and a left ascending part which ends blindly. The right
portion is said to give rise to the oesophagus, the connecting piece
to the stomach and the left ascending portion to the intestine (c/.
Fig. 168, '/and ed with Fig. 170, oe, m, and erf). The anus only
arises later, during larval life, by the blind end of the intestine be-
coming connected with one of the two so-called cloacal vesicles (that
on the left), these latter being ectodermal invaginations which will
be described further later.
The account given by van Beneden and Julin (Xo. 10) differs
from that given above in so far as they derive only the descending
portion of the intestinal coil (consisting of the oesophagus and the
stomach) through direct growth from the posterior diverticulum
mentioned above, while they believe that the intestine proper arises
from the ventral surface of the dilated stomach as a secondary out-
growth. The point of origin of this secondary caecum, which is
directed to the left and upward, is said to lie somewhat far forward,
i.e., to be almost pre-cbordal. We shall see below (p. 521) that these
authors ascribe some significance to this observation.
The oral apertun of the larva (which gives rise to the inhalent or
branchial aperture of the adult) is formed only shortly before the
larva hatches. The anterior pointed end of the alimentary canal,
just before reaching the sensory vesicle, bends dorsally. It there
comes into contact with an invagination which has arisen from a
thickened disc of ectoderm-cells. By the apposition of these two
structures and a breaking down or separation of the cells, the oral
aperture is formed (Figs. 167 and 168, p. 358).
The emdostyle develops as a ciliated furrow in the antero-ventral
region of the branchial sac (pharynx), owing to the formation of two
lateral longitudinal swellings. We cannot here enter further into
the histological details of this structure, but must refer the reader
for these to the treatises of R. Hertwig, Fol and Seeliger (No.
50). We may, however, mention that this furrow is not purely
ventral in position, its anterior portion extending up towards the
dorsally placed oral aperture (Fig. 170, es). According to a recent
treatise by Willey (No. 54a), the rudiment, of the endostyle
originally lies in the most anterior part of the branchial sac in which
366 TUNICATA.
it has a dorso-ventral position. Only later does it shift farther back
and come to lie ventrally. This observation is of importance in
connection with the condition of this organ in Amphioxus, where
it undergoes a similar displacement.
The digestive or pyloric gland arises as a caecal outgrowth at the
boundary between the stomach and the intestine ; it, however, soon
branches repeatedly, and these ramifications extend over the surface
of the intestine where, by anastomosing, they form a network (Fig.
175 A, dr, p. 379). It has been homologised by Willey (No. 54a)
with the hepatic caecum of Amphioxus.
Peribranchial, atrial, or cloacal cavity. The first rudiments which
lead to the development of the peribranchial cavity are found, shortly
before the larva hatches, in the form of a pair of ectodermal invagina-
tions lying dorsally at the boundary between the sensoiy vesicle and
the trunk-ganglion, called by Metschnikoff, who was the first to
observe them, the cloacal vesicles (Fig. 167, cl, p. 356). Two
diverticula grow out from the pharynx towai"ds these invaginations,
one on each side, and fuse with them, thus giving rise to the first
gill-slits (Fig. 168, k, p. 358). According to Kowalevsky, a second
pair of these slits (k") soon forms in Phallusia behind the other in
the same way. If the interpretations of Kowalevsky and Seeliger
are correct, the cloacal vesicles, by enlarging, give rise to the paired
halves of the peribranchial cavity. In this case, the latter would be
lined throughout with ectoderm, and the wall of the pharynx, which
is perforated by the gill-slits, would on its inner side be covered with
entoderm and on its outer with ectodermal epithelium. We should
then perhaps be justified in homologising the peribranchial cavity of
the Ascidians with the atrium of Amphioxus; we can hardly, in any
case, doubt the homology of the gill-slits in these two groups.
Another view has, however, been adopted by van Beneden and
•Iulin (Xos. 9 and 10). According to these observei\s, the first gill-
slit arises through the fusion of a rather long entodermal diverticulum
with the cloacal vesicle of the same side which, according to these
authors, is never very large. The Ascidian larva at this stage is
exactly in the condition in which Appendicular i a remains through-
out life, the pharynx, in the latter, communicating through a
branchial passage on either side with the exterior. These passages
represent a pair of gill-slits, and this pair, in the Ascidian as in
Appendicularia, remains the only pair. \n the Ascidian, the branchial
passages are considerably enlarged secondarily, and in this way the
peribranchial or atrial cavity arises. Since these passages, according
ASCIDIACEA — DEVELOPMENT OF THE PRBE-SWIMMINQ LARVA. 367
bo van Beneden and Julin, are for the most part of entodermal
origin, a large although not sharply marked portion of the peri
branchial cavity must be lined with entoderm. These observers
therefore maintain that these spaces cannot be homologised with the
atrial cavity of Amphioxus, and the future perforations in their inner
walls can in no way be homologised with the gill-slits of Amphioxus
and the Vertebrates, and are therefore distinguished from true gill-
slits by these authors as branchial stigmata. We have some hesita
tion in accepting the view of van Beneden and Julin. The origin
of the peribranchial cavities in the Ascidians does not appeal- to us-
sufficiently understood to justify its utilisation in the formation of
such important conclusions. It should be pointed out that, in the
embryo of Pyrosoma, the purely ectodermal origin of the peribranchial
cavities can hardly be doubted (see below, p. 394), and this seems-
also to apply to Doliolwm (see the statements as to the Anchinia buds,,
p. 481). Again, we are probably not justified in concluding without
further evidence that the condition of Appendicularia is primitive.
Since an Appendicularian was found by Moss (No. 5.) possessing
many gill-clefts like those of Doliolum, we may have to regard the
apparently simple res] nratory organs of other Larvacea as degenerate.
We shall have to speak of the further transformations in the
branchial region when describing the metamorphosis of the attached
larva, although, in some cases, the multiplication of the gill-slits
commences in the free-swimming larva (Botryllus, Distaplia, Fig.
230, ]». 457).
Lahille (No. 88) and Willey (No. 54a) have both recently expressed their
belief in the purely ectodermal origin of the peri branchial sacs. According to
Lahille, they arise, in the Didemnidae, through the enlargement of the
cloacal vesicles. Their outer aperture then disappears and an unpaired
ectodermal invagination appears on the dorsal side ; this is the cloacal in-
vagination proper, which only secondarily becomes connected with the
peribranchial sacs. Willey (No. 5ia) observed, in Clavelina, as the pre-
cursor of the cloacal vesicle, a longitudinal furrow, from the posterior end of
which the cloacal vesicle develops. Willey is therefore inclined to assume
that the peribranchial cavity of the Ascidians is homologous with that of
.1 m/ili in. i ■n.s.
The outer apertures of the two peribranchial spaces (Fig. 231,
p. 160) shift continually towards each other and towards the dorsal
middle line till they meet and fuse. In this way arises the cloacal,
atrial or inhalent orifice (Fig. ^30, e). van Beneden and Julin
(Xo. 9) have pointed out that, during this fusion, the part of the
ectoderm which lies between the two apertures becomes depressed
368
TUNICATA.
and this depression gives rise to the true cloacal cavity, i.e., to the
unpaired part which connects the two peribranchial cavities and
which is thus lined with ectoderm.
The terminal portion of the intestine which had, at an earlier
stage, become connected with the left cloacal vesicle (see above,
p. 365) now opens into the common peribranchial cavity.
The heart, the pericardium and the epicardium. We owe to
Seeliger the proof that the heart and the pericardium of the
Ascidians are entodermal structures, the first rudiment of which can
be recognised in the form of an outgrowth from the pharynx arising
between the posterior end of the endostyle and the entrance to the
oesophagus. A vesicle which becomes abstricted from this caecum
ot Jif„ e f
m
/ i \ \- i ■'■.-■ < ■
es ep> p,0
FlG. 170. — Lett lateral aspect of a Clavelina embryo (after Seeliger). au, eye; ch,
-chorda ; >\ exhalent orifice ; ed, rectum ; ep, epicardial outgrowth ; es, endostyle ;
/', infolding of the body-surface in anticipation of the rotation that takes place after
fixation; /,
peribranchial sac ; /»'. pericardium ; s, larval tail ; sb, sensory vesicle.
(Fig. 170, jic) is the common rudiment of the pericardium and the
heart. The remainder of the caecum (ep) has been named by van
Beneden and Julin the epicardnvm* These authors were able
essentially to confirm the statements of Seeliger, although they
repeatedly differ from him in points of detail. They also recognised
the significance of the epicardium in connection with budding, and
the originally double rudiment of these structures.
The first rudiment of these organs was observed in the form of two
solid cell-strands which run side by side in close contiguity to the
*[Damas (No. IX.) fluids that in Ciona the epicardium has a paired origin
and opens by two distinct orifices into the pharynx. — Ed.]
ASCIDIACEA — DEVELOPMENT OF THE FREE-SWIMMING LARVA.
369
ventral wall of the alimentary canal near the point at which the
oesophagus enters the pharynx. The origin of these cell-strands
{procevrdiwn) is less clearly stated, van Beneden and Julin have
no doubt that they become detached from the entodermal intestinal
epithelium. Willey has recently (No. 54a) made the same observa-
tion, finding, however, that the procardial rudiment is impaired and
also not entirely agreeing with van Beneden and Julin with regard
to its furl her development. The left procardial strand always appears
stronger than the right. The strands soon develop lamina and thus
become tubes. In later stages, the posterior ends of these tubes fuse,
while, anteriorly, they open into the branchial sac. The whole rndi-
PlG. 171. — Three consecutive transverse sections through the trunk-region of a Clav-e
Una larva (diagrammatic, after van Benedkn and Julin). .1. shows the posterior
blind end of the branchial sac or pharynx with the apertures of the oesophagus and
the epicardial tubes [ep.o). Ji, shows the connection between tin- epicardial tubes
(.//) and the pericardial vesicles (j>c). C. shows the blind ends of the epicardial
tubes [ep) and the pericaridal vesicle severed from them (/»•)• ec, ectoderm ! >/*.
epicardial tubes; ep', blind ends of the epicardial tubes ; ep.o, the epicardial tubes
near their openings into the pharynx; h, heart; m, cellulose mantle: n, neural
tube : oe, oesophagus : /<. peribronchial sac ; pc, pericardial cavity.
iiient now consists of an unpaired posterior caecum (Fig. 171 B, ep
and //-), which forks anteriorly into two tubes that open separately
into the branchial sac (Fig. 171 A, ep.o). From the posterior
caecum, a vesicle becomes abstrictecl (Fig. 171 C, pc) and this
represents the common rudiment of the heart and the pericardium.
The lumen of this vesicle (pc) is the future pericardial cavity.
The form of the vesicle is complicated in consequence of the invagina-
tion of its dorsal wall as a furrow running along its whole length ;
this makes the vesicle cx-escent-shaped in cross-section. The lumen
of this invagination is the future cavity of the heart (h). The in-
BH
370 TUNICATA.
vaginated part of the wall of the vesicle becomes the wall of the
heart while the non-invaginated part changes into the pericardial
epithelium.
The lumen of the heart is thus, according to the above description,
a cavity which has arisen through the invagination of the outer
surface of the pericardial vesicle. This cavity communicates, by
means of the long dorsal aperture of invagination, with the lacunar
blood-spaces of the surrounding mesenchyme. This communication
is partly closed later by a lamella arising from the epicardium ; it
is, however, retained at the anterior and the posterior ends as the
anterior and posterior apertures of the cardiac tube.
That part of the procardial rudiment which remains after the
abstriction of the pericardial vesicle is from that time known as the
epicardium. It consists, as before, of a posterior unpaired diverticu-
lum (.vac bpicardique) which forks anteriorly into two paired epicardial
tubes {tubes epicardiques) ; these, in their turn, entering the pharynx
to the right and left of the median line (Fig. 171 A). The point at
which they enter lies between the posterior end of the hypobranchial
furrow and the point of entrance of the oesophagus. The posterior
caecum of the epicardium now grows out backward considerably, and
thus reaches the dorsal side of the heart-rudiment (Fig. 173 C, ep
and h, p. 375) with which it comes into such close contact that its
ventral wall is drawn in to close the dorsal aperture of the heart.
The epicardium is a structure of great significance in those forms
which reproduce asexually, being intimately connected with the pro-
duction of the buds. By extending farther and farther backward it
reaches the stolon (Fig. 173 C, st) in which it forms a transverse
partition. In this process it becomes so much compressed dorso-
ventrally that its two layers come into close contact and (in Clavelina)
fuse completely. The epicardial transverse partition separates, in the
stolon, two blood-spaces in which the blood flows in opposite direc-
tions. As this partition- wall does not reach quite to the blind end
of the stolon (Fig. 229, x, p. 45(3,) the two blood-spaces pass into
each other at this point. We shall have to return later (p. 450) to
the significance of the epicardium in connection with the development
of buds.
The wall of the heart consists of pavement-epithelium directly
connected with the pericardium, and bears to the latter the same
relation as exists between the visceral and the parietal layers of ;i
vertebrate pericardium. In later stages, the cells of the wall of
the heart secrete, on the surface turned to the lumen of the heart,
ASCIDIACEA— ORGANISATION OF THE FREE-SWIMMING LARVA. 371
muscle-fibrils in which transverse striatum can be distinctly seen.
An endocardium is wanting in the Ascidian heart, and its vessels
have no endothelial lining.
E. Review of the Organisation of the Free-swimming
Larva iFigs. 168-173 A).
It should be mentioned that there is considerable variation in the
degree of development attained by the organisation at the moment
of hatching in the different species and even in the individuals of the
same species.
The form of the larva, the development of which has just been
traced in detail, recalls somewhat that of a tadpole. Anteriorly,
there is an oral region (cephalic and trunk-region) the end of which
carries the three adhesive papillae (Fig. 173, hp) ; this region is
followed by a long, flatly compressed swimming tail. This latter,
which shows markings like those of fin-rays (Fig. 173 A) attains its
characteristic form through the great development of the mantle-
substance (Fig. 169, Jl) which further covers the whole surface of
the body, even passing over the oral and cloacal apertures.
The axis of the tail is occupied by the chorda which extends
anteriorly into the trunk-region. Above it lies the neural tube,
while a cell-strand that runs below it and soon disintegrates repre-
sents the remains of that part of the intestine which belongs to the
caudal region. Running along this part of the body and extending
along its whole length, are the massive muscle-bands.
In the anterior region, the neural tube swells out to form a sensory
vesicle (Fig. 173, sb) and a swollen trunk-section (>■) immediately
following the latter. The primitive enteron gives rise to the
pharynx or branchial sac, the oesophagus, the stomach and the
intestine. The oral aperture (or inhalent orifice, i) is established
and is distinguished by its dorsal position. Near it, the ciliated pit
(fl), which extends as far as the base of the sensory vesicle, opens
into the pharynx. The intestine opens into the atrial cavity which
has formed by the union of the two originally separate peribranchial
sacs. There is now a single atrial aperture (or exhalent orifice, e).
The number of gill-slits which have at this stage developed varies
in different species.
The heart {It), the pericardium and the epicardium (ep) have
developed. The heart already pulsates ; the endostyle (hypobranchial
groove) has developed. The mesenchyme becomes differentiated into
372 TUNICATA.
connective tissue, blood-corpuscles and the first rudiments of the
future body-musculature.
The free-swimming larva (Fig. 173, ^-i) thus already shows the
typical organisation of the adult Ascidian. The further transforma-
tions which take place after fixation are therefore slight. They
consist of the degeneration of the provisional larval organs, the
further development of the organs of the adult (especially of the
branchial sac) and the development of the reproductive structures
(stolon, genital organs).
It should be mentioned that the free-swimming larvae of the various
families of Ascidians differ in many respects. On this subject, we must refer
the reader to the descriptions and figures of Lahille (No. 38) who has also
utilised the larval forms for systematic purposes. The above account applies
mainly to the larvae of the Phallusia and Clavelina. The .larvae of the
Distomidae (Distaplia) are distinguished by their large size and by the early
development and separation from them of several small buds which again
divide (Fig. 230, p. 457), while in the larva of the Didemnidae, only one large
additional individual is at first developed, thus giving rise to the appearance
of double individuals (p. 459). The larvae of the Botryllidae are devoid of
the three adhering suckers ; these seem to be represented merely by three
conical processes. They are further distinguished by an equatorial ring of
dilated mantle-vessels surrounding the body. The Styelidae resemble them
closely, and such a ring of mantle-vessels also occurs in many Didemnid
larvae which otherwise are distinguished from the Botryllid larvae by the
development of double individuals and the presence of adhering suckers.
F. Fixation and Retrogressive Metamorphosis.
The transformations which take place after fixation may to some
extent be considered retrogressive, as the sensory organs, the nervous
system, and the locomotory organs undergo degeneration. The other
systems of organs, on the contrary, often become more perfect.
The free-swimming condition does not last for more than a few
hours. The larval tail begins to degenerate when attachment takes
place. According to Kupfper, the larva attaches itself by means of
only one of the three adhering papillae (Fig. 173 B, hp), the other
two degenerating. Even the papilla that is utilised for fixation soon
disappears, so that the young Ascidian then seems to be attached
by the surface of the cellulose mantle. In other cases {Clavelina),
stolon-like outgrowths from the lower end of the body bring about
fixation.
The defeneration of the caudal region is introduced by the detach-
ment of the soft parts of this region from the gelatinous mantle
which envelops them and their withdrawal towards the trunk-region
ASCIDIACEA — FIXATION AND METAMORPHOSIS.
373
(Fit*. 173 B), to which they are then appended as a short truncated
process. The internal organs of the caudal region are retracted more
and more into the trunk (Fig. 172). They there coil up spirally, but
the separate elements (the chorda, the muscle-bands, the neural tube)
which compose this coiled strand retain for a long time their relative
pu>
,,I(; 172 -Degeneration of the caudal region during me^?rPf°Qspi^*^r0S jj
nSe-ceUs^f the tail ; ' . aerve-cells oi bhe caudal section ; ns, neural tube.
positions (c/. Fig. 172 /;,.--, where the strand is cut through trans-
versely) The degeneration of the chorda commences, according to
KOWALEVSKY'S most recent researches (No. 32), by the disappearance
of its gelatinous substance, while its cells (Fig. 172, oh) again become
374 TUNICATA.
arranged into a simple strand. The degeneration of the chorda-cells
which are distinguished by their granular contents, is finally brought
about by phagocytosis. This is also the case with the muscle-cells.
The ectoderm- cells, as the caudal section shortens, become larger
(Fig. 172 A), and spherical, strongly refractive bodies appear in
them, so that they come to resemble the so-called granulated spheres
of the pupa of the 'Musddae (Vol. iii., p. 379). When the internal
organs of the caudal section have been completely taken up into
the body-cavity of the trunk, the ectoderm is invaginated (Fig. 172
B, ens). This invagination soon becomes completely abstricted from
the epidermis of the larva and then forms a closed vesicle lying
within the body-cavity ; -the cells of this vesicle soon lose their
cohesion, the lumen disappears, and finally nothing remains but
a mass of detached and gradually disintegrating granular cells. The
gelatinous envelope (Fig. 173 C, ss) of the caudal region is, finally,
lost either by being simply absorbed according to Kupffer's obser-
vations, or thrown off, as Seeligek and Milne-Edwards agree in
maintaining.
Since the attachment of the larva is accomplished by means of the
anterior end of the body, the oral aperture (inhalent orifice) appears
to lie near the point of attachment (Fig. 173 B). In the adult
Ascidian, on the contrary, the oral aperture lies at the end of the
principal axis of the body opposite to the point of attachment (Fig.
173 C). This shifting of the position of the oral aperture is the
result of a rotation made by the body round its transverse axis
after attachment, during which the part of the body between the
mouth and the point of attachment lengthens. This lengthening, in
Clavelina, according to Seeliger, is made possible by the develop-
ment of a deep infolding of the surface of the body (Figs. 170, 173
A and B, /) which slightly separates a pre-oral portion carrying the
adhering papillae from the rest of the body. This pre-oral region
represents the basal section of the young Clavelina from which the
branching stolon soon grows out. The folding just mentioned
renders it possible for the Clavelina, which originally was placed
with its longitudinal axis at right angles to the basal plane (surface
of attachment), first to bend sharply towards this plane and then
to lie with its longitudinal axis parallel to it, finally however, to
rise up from it in such a way that the oral aperture comes to
lie opposite to the point of attachment. During this rotation round
the transverse axis, which was pointed out first by Kupffer and
later by Seeliger, the angle passed through is one of almost 180.°
ASCIDIACEA FIXATION AND METAMORPHOSIS.
375
ft /"
Pig. 173.— Diagram illustrating the metamorphosis of the larva of Clavdina during
and after fixation (mainly after Seeliger). A, free-swimming larva ; B, larva just
attached; (', older metamorphosed stage, ch, chorda; e, atrial aperture; e')
and each becomes divided by projecting outgrowths of the trabeculae
lying between them. In this way the six primary slits give rise to
six rows of secondary slits. In later stages, new slits are said to
break through between these.
In Clavelina, according to Seeligkr, two transverse rows of gill-slits are
found even in the free-swimming larva (Fig. 173 A). A new row forms in
front of these and behind them another is added after fixation. In this case
the number of slits is increased by the appearance of new independent perfora-
tions (and thus not by the division of those already present). This is also the
case, according to Garstaxg (No. 21, papilla-like rudiment of the longitudinal ribs ;
rs, renal vesicles; t, ring of tentacles; tr, transverse ribs of the branchial network.
and posteriorly and give rise to papillae. The papillae on the con-
secutive branchial arches lie so near each other as to come into
ASCIDIACEA FIXATION AND METAMORPHOSIS.
379
contact and fuse, giving rise to the internal longitudinal bars (Ir)
of the branchial region.
At an early stage, the first rudiment of the pericoronal circle
(peripharyngeal bauds, ciliated arch, Fig. 174 A,fb), as well as that of
the coronal circle, which lies in front of it and is beset with tentacles,
can be seen. The arrangement of the tentacles when they first appear
is bilateral.
The development of the genital organs has still to be described.
In the compound Ascidians, the individual that develops from the egg
has no genital organs, but multiplies exclusively through budding.
This is also the case with the social Ascidians (Ganin). In studying
the development of the genital organs we are consequently restricted
to the simple Ascidia if we wish to study their origin in a sexually
<&
Fig. 1 75. — A, dorsal aspect of the intestinal coi] in the bud of Perophora Listeri with
the rudiment of the genital organs; B, somewhat older genital vesicle (after van
Benedex and Julis). g, genital vesicle; gs, genital strand; dr, digestive gland;
oe, oesophagus; m, stomach; i, intestine.
produced embryo, otherwise we must trace their rise in the asexually
produced buds of other Ascidians. The course of development in
these two cases is, however, so uniform that we may take as our
example the buds of Perophora which were examined with special
reference to this point by van Beneden (No. 10).
The Ascidians are hermaphrodite. The male and female genital
rudiments, however, are derived from a common rudiment which is
always unpaired and lies on the intestinal loop medianly and dorsally
(Figs. 174 B, gs', 238 E, g). This is found at the point at which the
efferent duct of the digestive gland first branches (Fig. 175 A). It
consists of an accumulation of cells indistinguishable from ordinary
380
TUNICATA.
mesenchyme-eells^ and of a uniserial cell-strand which runs forward
and reaches the atrial aperture (genital strand, Fig. 175 B, gs). In
the next stage, a cavity appears
B
in the cell-accumulation (Fig.
175 A). This vesicular rudi-
ment of the genital glands is
soon divided into two diverticula
by a transverse constriction (Fig.
1 75.#), one of these representing
the rudiment of the male gland
and the other that of the female
gland and its efferent duct. Of
these two diverticula, the inner
one, that which lies ventrally,
develops first and becomes flask-
shaped. Its dilated terminal
swelling (Fig. 176 A, h) becomes
the testis, and in this an ex-
ternal flat epithelial layer can
soon be distinguished from an
inner layer of spermatogonia.
The narrowed efferent duct (vas
deferens, vd) opens at first into
the female genital vesicle. In
this latter also considerable
elongation can be noticed (Fig.
176). While, near the blind
end, the germ-epithelium (k)
becomes differentiated, the re-
maining elongated part of the
rudiment becomes the oviduct
{<><]). At the time when this
oviduct elongates, the genital
strand ((/) which functions as
gubernaculum becomes corre-
spondingly shortened. It is
probable that the oviduct
develops to some extent at the
expense of the latter. In
this way, the end of the oviduct approaches the atrial wall more and
more till, after the complete disappearance of the genital strand, it
Fig. 176. — Later stages in the development
of' the genital organs in the bud of Pero-
phora Listeri (after van Beneden and
Julin). (j, genital strand ; //, rudiment
of the testis ; h, germ-layer of the ovary;
od, oviduct ; i, and
1f muscle-plates derived from the mesoderm-bands. At the
anterior end of the caudal region, a pari of the mass of mesoderm-
eells (Fig. L 79, ms") is not transformed into spindle-shaped muscle
fibres. Two cell-masses (//) are subsequently given off from this into
the ectodermal vesicle, where they break up and change into blood-
corpuscles.
The anterior region of the body contains the very large rudiment
of the central nervous system (Fig. 1 7'.» J, n) and the anterior
386
TUNICATA.
portion of the lateral mesoderm -bands (ms) which also give off' into
the ectodermal vesicle from their posterior ends elements that change
into blood-corpnscles. An ectodermal invagination can also be seen
forming ventrallv (/>) and from this is derived the whole intestine
of the " nurse " form. This invagination first gives rise by its dilata-
tion to the pharyngeal cavity (Fig. 179 B, j>), while the intestine
proper is derived from a solid cone of cells which develops at the
base of the invagination. This cone very soon develops a lumen at
first closed at both ends, and this becomes differentiated into the
oesophagus, the stomach and the intestine, the rudiment of the
digestive gland also becoming visible. The rudiment of the intestine
opens only later into the atrial cavity (cl). The latter develops later
than the pharyngeal cavity from an independent dorsal ectodermal
invagination (Fig. 181, cl) which, as it enlarges, comes into close
contact with the posterior wall of the pharynx. In this \va}^ the
transverse and somewhat diagonally-placed branchial lamella arises,
in which the four pairs of gill-clefts found in this generation (Fig.
245, p. 47-*>) soon appeal1 in the form of small round perforations.
According to ULJANIN, the two pairs that lie dorsal ly develop before
those that lie ventrallv.
Fig. 181.— Dorsal region of an older larva of Doliolum MiiUeri (after Uljamnj. d,
atrium ; fl, ciliated pit; m. muscle-hoops; /'. ganglion; nb, branchial nerve.
< hilv the middle part of the rudiment of the central nervous system
(Fig. 181, n) retains its original massive character, while the anterior
and posterior ends soon become narrower In the anterior narrowed
portion, an irregular cavity develops and breaks through into the
pharynx. At this point, the ciliated pit (_//) appears and a delicate
canal connects it with the sub-ganglionic body (the homologue of
the " glande hypophysaire " of the Ascidians). From the middle
swelling of the neural rudiment, the actual ganglion and the sub-
ganglionic body develop, while the posterior narrowed portion gives
rise to an unpaired nerve which runs backwards (nervus branchialis, nb,
DOLIOLL'M LARVAL DEVELOPMENT.
387
Uljanin) in which we perhaps have the homologue of the ganglionic
cell-strand discovered by van Beneden and Julin in tlie Ascidians
(p. 376). The peripheral nerves and the sensory organs develop
later, and among these the vesicular auditory organ which belongs
to the left side of the body deserves special mention (Fig. 245 A, <>t) ;
the vesicle itself arises as an ectodermal invagination into which a
cell wanders and develops into the otolith. According to Uljanin,
the auditory organ of Doliolvmn Mullen remains throughout life a
mere cup-shaped ectodermal invagination.
ms
ms'
Ki'.. 182. Transverse section through two ontogenetic stages of Doliolum (after
I i j \nixi. . I. section through anterior region of the body at a stage somewhat
holder tan that depicted in Fig. 17'-1 .1 ; 11. section through an older stage, d,
paired pharyngeal outgrowth, which takes part in the formation of the ventral
stolon; ec, ectoderm; en, entoderm; h, rudiments of the heart and pericardium;
ms, mesoderm ; ms', mesoderm of the ventral stolon : n, rudiment of the nervous
-\ stem ; p, pharynx.
The mesoderm of the anterior region of the body gives rise
principally to the muscle-hoops (Fig. 181, m), the pericardial rudi-
ment (Fig. 182 B, h) and the mesoderm-mass (ms) of the ventral
proliferating stolon of the "nurse" stage (the rosette-shaped organ
of KEFERSTEIN and Ehlers). Two cell-groups become separated
posteriorly and Neutrally from the mesoderm-layer which envelops
the pharyngeal cavity like a mantle; one of these, in close contact to
the ectoderm, becomes the mesoderm of the ventral stolon (ms'),
while the Other, near the rudiment of the alimentary canal, changes
into the pericardial vesicle (h), a cavity appearing within it round
which the cells become arranged into an epithelium. As in other
Tunicates, the heart is derived from a dorsal invagination of this
388 TUNICATA.
vesicle.* It should here be mentioned that the dorsal closure of the
cardiac tube is brought about by a histologically differentiated lamella
(the " mittelfeld" of Grobben) as to the development of which, how-
ever, we have no detailed information, but we are reminded of the
participation of the epicardial lamella in the formation of the heart
in the Ascidians (van Beneden and Julin, p. 370).
The muscle-hoops develop in the way described by Leuckart for
8al}xi democratica (see p. 431), through the fenestration of the meso-
dermal lamella, these perforations separating one muscle-hoop from
another.
In this way, the general course of the most important systems of
organs occurring in the first " nurse " generation is indicated (Figs.
180, 243, 245, p. 475). To these, two stolons connected with the
formation of buds have to be added. One of these (Figs. 180, /•, and
245 A, rs) lies behind the fifth muscle-hoop, close to the posterior
end of the pericardial vesicle ; this we shall call the ventral stolon
(the rosette-shaped organ). The second ox, dorsal stolon (Figs. 180, d,
245, ds)-\ arises from the dorsal surface in the seventh intermuscular
space and forms a geniculate process pointed posteriorly, into the
base of which an open coil of the seventh muscle-hoop extends (Fig.
243, st'). We shall have to enter into the details of the structure
and development of these stolons and of their relation to the forma-
tion of the subsequent generations later (p. 470).
After the young barrel-shaped "nurse" has developed fully, the
provisional larval organs gradually atrophy. While the internal
parts undergo fatty degeneration and the cells become mixed with
the blood, the ectodermal envelope gradually shortens so that the
ectodermal vesicle and the larval tail soon form merely a rounded
prominence on the body of the " nurse ". This outgrowth strikingly
resembles an embryonic organ consisting of reserve nutrition found
in the Thaliacea, the so-called elaeoblast, a fact which makes the
derivation of the latter from the transformed tail of the Ascidian
larva, attempted by Salensky, appear somewhat probable (see below
p. 432)
The first "nurse" generation of Doliolvm, at a later period, as
Fol first pointed out, undergoes a remarkable metamorphosis, the
* Grobben's statements as to the formation of the heart in the larval
Doliolum have beem misunderstood and misrepresented by Uljanin.
+ [Th is is better termed the dorsal outgrowth, as it does not itself give rise
to buds, but receives those structures in rudiment from the ventral stolon and
miiK gives attachment to them (pp. 472-47G). — Ed.]
PI ROSOMA —EMBRYONIC DEVELOPMENT. 389
gills, the endostyle and the whole of the alimentary canal degenerat
inu' completely, while the muscle-hoops considerably increase in size,
and the nervous system develops correspondingly. The "nurse"
then, like a swimming bell of a Siphonophoran stock, carries out the
locomotory function, while the nutritive and respiratory functions
of the whole stock are fulfilled by certain laterally- placed buds (tropho-
zooids) on the dorsal outgrowth.
4. Pyrosoma.
Ihe development of Pyrosoma from the egg resembles in many
respects that of the Thaliacea. Embryonic development takes place,
as in them, within the body of the mother and is consequently direct
or abbreviated. It even takes place, as at first in the Thaliacea.
within the egg-follicle. Pyrosoma is, however, specially distinguished :
(1) by the large amount of food-yolk in the egg, which leads to a
discoidal cleavage and the development of a germ-disc and (2) by
the early asexual multiplication of the embryo. The primary indi-
vidual which develops from the embryo and which has been called
the Cyathozooid by Huxley, at an early embryonic stage, gives rise
by a kind of transverse fission to four more individuals, the first
Ascidiozooids of the colony < Fig. 193, etc).
We owe our knowledge of the embryonic development of Pyrosoma
chiefly to Huxlky (No. 72), Kowalevsky (No. 71), and Salenskv
X. 71).
A. Cleavage and Formation of the Germ-Layers.
Only a single egg matures in the genital rudiment of the A.scidio-
zooid which has arisen through budding, as also is the case in the
Thaliacea. Part of the remaining cell-material of the so-called genital
strand becomes arranged round the egg as the follicle, while another
part is used up in forming the rudiment of the testes and of the
oviduct which appears as an outgrowth of the follicle. The egg
grows greatly by the addition of food-yolk, so that finally the forma-
tive yolk and the germ-vesicle within it form a mere prominence
upon the large yolk-sphere (Fig. is:; .|). After the oviduct has
become connected with the atrial cavity, spermatozoa pass into it
and remain in it until the egg is ready for fertilisation, while the
oviduct partly degenerates. At the same tiine.au active immigra-
tion of follicle-cells takes place into the space extending between
tie surface of the egg and the follicular epithelium (Fig. 183 .)./:).
390
TUNICATA.
These cells, which have been called by Kowalevsky inner follicular
cells and by Salensky kalymmocytes, and as to the derivation of
which from the follicle-cells there can be no doubt, are homologous
with the test-cells of the Ascidians and the inner follicle-cells of the
Thaliacea (Salensky's gonoblasts). According to Salensky. they
take a certain part in the formation of the embryo here as in the
Thaliacea. The statements on this subject, however, appear to us
somewhat inconclusive.
An epithelial lamella further becomes separated from that part
of the inner surface of the follicle which lies next the oviduct (Fig.
184, >•) ; this covers the germ-disc like a cap and represents a
secondary germ-envelope that takes no further part in the develop-
ment of the embryo. This has been called by Salensky the cover-
ing layer.
Fiu. 183. — A. lateral aspect of the egg of Pyrosoma, showing the first cleavage ; U,
the gerni-disc of /'i/msm/iii at the six-celled stage, viewed from above (after Kowa-
levsky). fz, inner follicle-cells.
The cleavage of the egg of Pyrosoma, first made known through
the investigations of Kowalevsky, is discoidal and recalls that of
the Teleostei. The first stages seem to have a fairly regular course,
the germ becoming divided into two, four and eight blastomeres by
the successive appearance of meridional furrows (Fig. 36). The stage
of three blastomeres observed by Salensky and that of six found by
Kowalevsky (Fig. 183 B) must be regarded as accidental irregu-
larities. We have no further details as to the course of cleavage,
but its result is a so-called morula-stage (Fig. 184 l>) in which the
germ-prominence is composed of blastomeres apparently irregularly
arranged and already forming several layers.
The numerous inner follicle-cells (kalymmocytes) wander by means of
amoeboid movements into the spaces between the blastomeres (Fig. 1S4 A, fz)
and arc even able to penetrate the cell-substance of the latter. This seems to
PYBOSOMA CLEAVAGE OK THE BGG.
39]
be the case, however, only in the first stages oi cleavage and bo have do further
significance, since the follicle-cells, as it appears, do not remain inside tlie
blastomeres. Many inner follicle-cells, as cleavage advances arc, however,
found scattered between the blastomeres (Fig. LSI B,fz) and, as the distinc-
ion of size between the two kinds of ceils disappears when the blastomeres
divide further, and the original histological character of the inner follicle-cells
can also no longer be recognised, It is finally impossible to distinguish thefollicler
cells from ilit- actual germ-cells or blastomeres. For this reason, and because
Pig. 184. Sections of two germ-discs of Pyrosoma (diagrammatic after Salensky).
I. eight-celled stage; II, older stage, b, blastomeres; do, food-yolk ; ds, covering
layer ; dz, yolk-cells ; i . egg-follicle ; fz, immigrated follicle-cells : ov, oviduct. ',\
Sai.knskv was unable bo find follicli
si]
c-cells sin
iwing the commencement of dis-
integration, this author concluded that the inner follic
lis i ake part in t he
formation of the embryo, a view resembling that held by him in connection
with the Thaliacca (p. 420). We consider it to be more probable that the
embryo here, as in the Thaliacea, is produced solely by the blastomeres, and
that the follicle cells which wander in between the blastomeres undergo final
disintegration. [See footuotes, pp. 420 and 421].
392
TUNIC'ATA.
Mention must now lie made of cells which, in the later stages of
cleavage, are found in large numbers in the yolk, near the point at
which the germ-disc lies on it, and which may be called yolk-cells
(Fig. 184, dz). Salensky, who traced back these cells to follicle-
cells that had immigrated into the yolk, has named them the yolk-
kalymmocytes. Since, however, as we shall see below (p. 395), these
yolk-cells take part in the formation of the intestinal wall, we are
inclined to regard them as blastomeres belonging to the entoderm-part
of the germ-mass. We here have a repetition of the conditions found
in the meroblastie egg of the Vertebrata, in which also yolk-cells (to
be considered as entoderm) are said to take a similar part in the
formation of the intestinal gland-cells.
For information as to the formation of the germ-layers in Pyrosoma
we are dependent entirely on Salensky's statements. The embryo,
after a number of eell-
divisions, lies on the yolk
as a prominence composed
of uniform polygonal cells
which are irregularly distri-
buted. This prominence
soon becomes bilaterally
symmetrical, the largest
mass of cells collecting in
the posterior half of the
germ-disc, so that the pos-
terior slope is more abrupt
than the anterior (Fig. IS.")).
According to Salensky, the
separation of the germ-layers
takes place through delamination, the most superficial cell-layer (ec)
first becoming arranged into an epithelium (ectoderm) ; the mass that
remains (the meso-entoderm) then undergoes a similar transformation,
the lowest layer, that in contact with the yolk, becoming separated
as the intestinal epithelium (entoderm). Between the ectoderm and
the entoderm the mesoderm extends, being greatly developed in the
posterior half of the germ-disc while, in the anterior half, it is want-
ing or else is represented merely by a tew cells (Fig. 186 .1 and R).
Taking into account the process of formation of the germ-layers in the
men ihlastic eggs of the Vertebrata, we may pe] haps be allowed to conjecture
that in Pyrosoma also the separation of the germ-layers is not an actual
delamination, but an invagination or infolding of the posterior edge of the
germ-disc, such :is. for instance, occurs in the Selachians.
k
Fig. 185. — Median section through a germ-disc
of Pyrosoma (after Salensky). ch, cavities
of the chorda : n
-p
\
.
y""*-- en
Fig. 189. Germ-disc of Pyrosoma with the atrial orifice developed (after KLowa-
lbvskt). cl, cloaca; en, endostyle ; n, aervous system; p, peribranchial tubes;
pc, pericardia] sac : pc', the posterior tubular eontinuatiou of the same.
the cavity, its lateral edges bending downward and growing towards
one another (Kowalevsky). According to Salensky, the yolk-cells
also take part in this ventral closure of the enteric rudiment (Fig.
188, -/:) by coming to the surface of the food-yolk and changing into
ma
Fig. 190. Transverse section through the posterior region of a germ-disc at the stage
depicted in Fig. Is'.' (after Salensky). dh, enteric cavity ; ec, ectoderm ; en, ento-
derm ; es, rudimenl of the endostyle : his, mesoderm ; ///<. peribranchial tubes; pc,
pericardial tube.
epithelial cells of the entoderm (p. 392). While the enteric rudiment
in this way becomes a tube closed on all sides (Fig. 190), a median
infolding, the rudiment of the endostylt (es) becomes visible in the
posterior half of its upper wall.
:;'.t.
TUNICATA.
The transformations undergone, in the further course of develop-
ment, by the paired coelomie sacs, the lumina of which had become
T.C.
Fig. 191. -Three germ-discs of Pyrosoma, diagrammatic (after Salensky). d, enteric'
cavity; es, endostyle ; Ic, left coelomie sac ; n, rudiment of the nervous system ;
p, peribranchial tubes; pc, pericardial sac = re, right coelomie sac.
connected posteriorly, are of importance. Only the right coelomie
sac is retained (Fig. 191, re), while the left* undergoes degeneration
(Fig. 191 A-C), its lumen becoming smaller and its cells losing their
- .es
en
'IV I^-~1.T embly°s "f Pyrosoma (after Kowalevsky). cl, atrial aperture of the
yatnozooid. en, eudostyle-folds ; n, nervous system ; o, aperture of one of the peri-
bran ehial tubes ; p, peribrauehial tube ; pe, pericardial sac : pc', posterior tubular
continuation of the pericardial sac ; ... posterior pari oi the germ-disc raised up from
the surface oi the egg (rudiment of the stolon) ; -.. .-ell-zone'.
i 'l'-™:," ngh\ and " left " refer t0 the arrangement of the organ., in
he adult < yathozooid, in whirl, the atrial aperture denotes the posterior end
oi the body. Asm our orientation of the germ-disc, the atrial aperture lies
I : ho anterior edge of the disc, the right and left organs appear to be reversed.
Our orientation of the germ-disc is. however, intentional (p. 404), having been
retained in accordance with the views of authors, since the opposite orienta-
wouhl also lead to certain difficulties in describing .he processes (especially
m connection with the development of the Ascidiozooid).
PYBOSOMA DEVELOPMENT OF THE CYATHOZOOID.
397
epithelial continuity, so thai finally, only a mass of irregularly
arranged cells remains to take part in the formation of the mesenchyme
which is developing in the primary body-cavity. A similar disin-
tegration is undergone by the median strand which was regarded as
the equivalent of the chorda, and which, after the disappearance of
its lumen, retains its independence only For a short time, and is called
by Salensky the axial mesoderm-strand. The right coelomic sac
gives rise to the pericardial rudiment (Figs. L92 C, L's<->, 190, pc),
Fig. 193. Two Cyathozooids with their first-formed buds (alter Kowalevsky, some-
what altered). A, with straight stolon; />'. with curved stolon; the Cyathozooid
is commencing t" rise from the surface of the food-yolk (d). cl, atrial aperture : d,
food-yolk; i'h. rudimenl oi the endostyle; I, body-cavity of the Cyathozooid; /'.
peribronchial tubes; /"'. pericardial sac of the I yathozooid; :. cell-zone.
which soon becomes chib-shaped, a diluted, anterior, sac-like parr
changing into the pericardial vesicle of the Cyathozooid, while the
tube that runs backward from this part does not develop further but
soon loses its lumen : the connection of its cells then becomes loosened,
h appears that these elements then mingle with the mesenchyme
and assist in the formation of the mesoderm of the Ascidiozooid. In
the pericardial sac of the Cyathozooid the surface adjacent to the
intestinal wall is seen to thicken, this part then becoming Lnvaginated
and forming the rudiment of the heart proper.
39b TUN I CAT A.
The germ-disc appears surrounded by a semicircular zone of cells
lying on the surface of the yolk (Fig. 192, z) ; Kowalevsky believes
that this zone consists of immigrated cells, the so-called inner follicle-
cells or kalymmocytes, but Salensky holds that mesodermal elements
(corresponding to the disintegrated left coelomic sac) also contribute
largely to it. When, at a later stage, the surface of the yolk is
grown over by the continually extending germ-disc, this cell-zone
also passes under the ectoderm of the disc and thus into the primary
body-cavity of the Cyathozooid (Fig. 19.'S />', .:). It then soon breaks
up into separate islands (Fig. 194, :) which are still for a long time
visible near the surface of the food-yolk. Kowalevsky thought that
the elements of this cell-zone took no further part in the formation
of the embryo, or at the most changed into blood-corpuscles, but
Salensky ascribes to them a very important part in the development
of the mesoderm of the Ascidiozooid (see below, p 410).
C. The Development of the Primary Tetrazooid Colony.
The edge of the germ-disc, by continually extending, overgrows
the yolk-sphere (Figs. 193 />', 194), which was originally covered
merely by the follicular epithelium. The food-yolk in this way
comes to lie inside the Cyathozooid, i.e., in its body-cavity. No
part is taken iu this circumcrescence, however, by the posterior region
of the elongated disc (Fig. 19l' />', x). This soon protrudes and
grows out into a long sac-like appendage (Fig. 193) which is cut up
by transverse furrows into four sections (recalling the strobilation of
the tape-worm) : these sections are the rudiments of the first four
Aseidiozooids. This chain of Ascidiozooids, which is known as the
stolon, and is evidently homologous with the ventral stolon of Doliolum
and Salpa, is originally straight, lying parallel to the principal axis
of the Cyathozooid (Fig. 193 A). Later, however, as it lengthens,
it curves and finally lies equatorially (Figs. 194, 195, 196) so that
the Ascidiozooids form a ring surrounding the gradually diminishing
Cyathozooid. The individual Ascidiozooids at the same time alter
their positions ; at first they lay with their longitudinal axes in the
same direction as that of the whole stolon (Fig. 194), but later there
is a tendency for these axes to lie parallel to the principal axis of the
Cyathozooid (Fig. 19G). The stolon then, as a whole, forms a series
of zig-zags, as the thin, drawn out trabeculae (Fig. 196, s, s) con-
necting the individual Ascidiozooids lie obliquely, ascending from the
posterior end of one zooid to the anterior end of the next.
PYROSOMA — THE PRIMARY TETRAZOOID COLONY.
399
While the four Ascidiozooids continue to increase in size and develop
the structure of the adult individual (Figs. 194-196), the Cyathozooid
which lies in the midst of them gradually atrophies (Fig. 196, c).
Only m»w (Fig. L96 B) does the colony, which is enveloped in a large,
rnou cellulose mantle, attainan independent existence. It passes
out of the parental brood-sac into the cloaca of the colony, and thence
to the exterior. The youngest free colonics of Pyrosoma are only
found at considerable depths (Chun), but older and larger stocks are
met with at the surface of the water.
I L94 Two stages in the development of the colony of Pyrosoma (after Kowa-
levsky) In .4, the yolk-mass (do) is partly surrounded by the Cyathozooid (c),
while in /;. it lies entirely within the body-cavity of the latter, c, Cyathozooid;
d atrial pore of the Cyathozooid; d, alimentary canal ol the Cyathozooid; do
volk; ec, ectoderm; el, elaeoblast; en, endostyle oi the Ascidiozooid ; fl, ciliated
pit ■ g ganglion of the Cyathozooid ; i, inhalent orifice of the Ascidiozooid ; hs, gUl-
slits :' J body-cavity of the Cyathozooid ; m, cellulose mantle; n, nervous system o
the Ascidiozooid; p, peribranchial cavitj ; sn, lateral uerve ; v, eutodermal canal
uecting the Ascidiozooids with one another ; s, remains of the cell-zone.
The organ-rudiments of the young Ascidiozooid chain are. originally,
direct continuations of the imperfectly developed organ in the Cyatho-
zooid (Figs. 192 A', L93). The ectoderm of the chain is in continuity
with that of the germ-disc. The intestine of the Cyathozooid is
continued into the enteric rudiment of the Ascidiozooid. and the
endostyle-fold also proceeds direct from the rudiment of this fold in
the germ-disc (Figs. 192, 193, en). In a similar way the peribranchial
400 TUNICATA.
tubes (/>) on either side of the intestine, and, on the right side of the
body, the pericardial tube (Fig. 192, pc), are continued direct from
the Oyathozooid into the chain of Ascidiozooids. The central nervous
system, on the contrary, arises independently in the Ascidiozooids
(Salensky). From this point the development of the Cyathozi
and that of the Ascidiozooids will be treated separately.
D. Further Development of the Oyathozooid.
The structure of the < 'yathozooid is fairly simple. One of the poles
of the body is marked by the presence of an ectodermal invagination,
the atrial invagination (Fig. 193 B, 194, cl) which occupies the most
anterior end of the germ-disc (Fig. 189, »•/), and the origin of which
has already been discussed (p. 394). This invagination originally
communicates with the peribranchial tubes (Figs. IS!), 192 B, 193
A, ]>). Very soon, however, that part of these tubes which lies in the
Oyathozooid degenerates and completely disappears (Fig. 193 B).
The atrial invagination, on the contrary, in which a narrow thick-
walled portion can be distinguished later from a thin-walled portion,
the actual cloaca, becomes connected with the alimentary canal of
the Oyathozooid, the lamellae that separate the two cavities being
perforated (Fig. 194). The alimentary canal (Fig. 194, d) of the
Oyathozooid is a simple thin-walled sac, nan-owed in the shape of
a funnel posteriorly, which adopts a somewhat curved position in
accordance with the curving of the stolon in later stages. Its
posterior, narrowed end passes over into the enteric rudiment <>i
the Ascidiozooids. There is no sign of endostyle-folds in the intestine
of the Oyathozooid, that part of the organ in which, in the germ-disc,
the rudiments of these folds appeared (Fig. 189 en) being used up
in the formation of the Ascidiozooids (Fig. 193, en).
The rudiment of the nervous system of the Oyathozooid, which is
derived from an ectodermal invagination lying close behind the atrial
rudiment near the anterior margin of the germ-disc (Fig. 189. u) is
originally a somewhat long and completely closed vesicle which, when
the alimentary canal changes its position, in consequence of the
curvature of the stolon, also shifts from its original position. The
posterior end of the neural vesicle now enters into open communica-
tion with the enteric cavity (Figs. 194 B, g, and 197). This is the
rudiment of the ciliated pit ( //). The anterior part of the vesicle
now becomes divided by a furrow from that part which is used for
the formation of the ciliated nit : it swells and changes into the rudi-
PYROSOMA — -FURTHER DEVELOPMENT OK THE CYATHOZOOID.
401
ment of the ganglion () with a diagram of a Cyathozooid
404
TUNICATA.
do -
(Fig. 199 A) shows that the inhalent aperture is wanting in the
latter. The point at
■f / ft . which we should expect
it to lie is indicated
by >. It is evident that
the whole of the area
which corresponds to
the inhalent apertui'e
and the endostyle is
much abbreviated in
the Cyathozooid. The
stolon which, in com-
parison, is very highly
developed, thus appears
to be shifted forward.
We also find that
the atrial invagination
which appeared quite
at the anterior edge
of the germ-disc, actu-
ally corresponds to the
most posterior end of
the body of the Cyatho-
zooid and consequently
the terms "anterior"
and ' ' posterior " are
applied arbitrarily to
the germ - disc and
FIG. 199.— A, Diagram of a Pyrosoma embryo in the
stage of Fig. 193 A ; B, diagrammatic median section
through a Salp (a solitary form), c, atrium; d,
alimentary canal of the Cyathozooid ; do, food-yolk ;
e, cloacal or exhalent orifice ; es, endostyle ; .//,
ciliated pit ; g, ganglion ; h, heart ; i (in />), inhalent
or branchial orifice, in A, the point at which it may
be conjectured to lie; r, edge of the germ-disc
growing over the yolk ; st, ventral stolon.
germ - disc
have nothing to do
with the orientation of
the Cyathozooid.
E. Development of the four primary Ascidiozooids.
The chain of Ascidiozooids, from the time it forms, contains
within it three longitudinal parallel tubes (Fig. 193), the middle
one representing the intestinal tube, the enteric rudiment of the
consecutive individuals, and the two lateral ones the peribronchial
tubes (p). These tubes are originally nothing more than direct
prolongations of the corresponding organs in the Cyathozooid (Fig.
192 B). When, at a later period, the individual Ascidiozooids
PYKOSOMA — THE FOUR PRIMARY ASCIDIOZOOIDS. 405
beoome more markedly constricted from one another, these rud
ments also are cut up into sections corresponding to the different
individuals. The peribronchial tubes become completely dissevered
at the boundaries of the individuals (Fig. 193 B), each Ascidiozooid
then containing a pair of lateral closed sacs, the peribronchial cavities
(/>). The remains of the peribronchial tubes in the Cyathozooid, as
already mentioned (p. 400) then atrophy. The enteric rudiment,
however, does not at first undergo such complete constriction
between the individual Ascidiozooids, but a canal is retained in the
connecting trabeculae which establishes communication between the
consecutive individuals (Fig. 194 B, v). This canal does not dis-
integrate until the Ascidiozooids separate completely on attaining
their full development. A vestige of it plays an important part in
the later development of buds, changing into the so-called endostyle-
process or entoderm-process of the stolon (Seeliger, p. 486).
The rudiment of the endostyle- furrow was recognisable in the
primary enteric rudiment of the Cyathozooid even before the chain
of Ascidiozooids began to form (Figs. 189, 190, en). That part of
the alimentary canal of the Cyathozooid which was distinguished by
the presence of the endostyJe-rudiment was the part which, by
lengthening, changed into the common enteric rudiment of the
four primary Ascidiozooids. Consequently, the endostyle-rudiment
originally runs through all the four Ascidiozooids (Fig. 193, en). At
a later stage, however, only the posterior part of it is retained in each
individual (Figs. 194, en, 200, es), becoming the definitive endostyle
of the zooid. In cross-section, the endostyle-rudiment originally has
the form of a broad fold projecting into the lumen of the intestine
(Fig. 203 A), the lateral part of which shows epithelial thickenings
which, in a surface view, appear as dark bands. The depression
between them flattens out later, but, on either side, the paired
endostyle-folds project inwards (Fig. 203 B, es). It is not yet
clearly understood in what way these lateral endostyle-folds together
with the middle part yield the endostyle of the adult.
In front of the anterior end of the endostyle-rudiment there is, in
the developing Ascidiozooid, a pit-like ectodermal depression (Figs.
194, 200, i), the rudiment of the inhalent or branchial aperture.
The space in front of this is occupied by the rudiment of the central
nervous system (Figs. 194, 200, n).
The lateral walls of the branchial sac of the Ascidiozooid are in
contact with the peribronchial tubes (Fig. 193, p). Here the gill-slit$
(/»>) break through (Fig. 200), a small entodermal outgrowth fusing
406
TUNICATA.
on either side with the wall of the peribranchial sacs, and the
perforation then taking place in the base of the outgrowth. The
entodermal lamella thus takes a more active part in the development
of the gill-slits than does the ectodermal wall of the peribranchial
sac. The vertical bars between the adjacent gill-slits which, in
cross-section, are almost quadrangular, are not merely covered on
their inner surfaces with entoderm, but their lateral surfaces also
which are turned towards the slits belong to the entoderm. Only
the covering of the external surface is derived from the ectodermal
Fig. 200. — Diagrammatic views of an Ascidiozooid at the stage depicted in Pig. 194
(following Salensky). A, viewed from above ; B, from below, cl, atrium ; d,
pharynx (branchial sac) ; ed, rectum ; el elaeoblast ; es, rudiment of endostyle ; fl,
ciliated pit ; i, inhalent or branchial aperture ; ks, gill-slits ; m, stomach ; n,
nervous system ; oe, oesophagus ; p, peribranchial sacs ; jjc, pericardial vesicle ; m.
rudiment of the lateral nerves.
wall of the peribranchial cavities. The gill-slits in Pyrosoma, accord-
ing to Salensky, appear in order from before backward, the most
anterior slit forming first. After the gill-slits have broken through,
they very soon lengthen ; those of Pyrosoma, indeed, are distinguished
for their length. The internal longitudinal bars, which cross the
slits at right angles and give rise to the characteristic lattice-like
appearance of the branchial wall, develop later as independent in-
growths from the vertical bars which become secondarily connected.
The gill-slits, as Seeliger has pointed out, seem always to lie
at right angles to the endostyle (Fig. 201, ks and es). Since the
endostyle of the Ascidiozooids originally runs horizontally, as may
be seen in the diagram Fig. 201 A, and then later adopts a vertical
position (Fig. 201 C) the gill-slits pass gradually from a vertical to
I'YKOSOMA — THE POUK l'KIM AHY ASL'IDIOZOOIDS.
407
an oblique position and finally lie horizontally. This leads us to the
general changes of form which characterise the development of the
Ascidiozooid. The longitudinal axis of the adult Ascidiozooid (Fig.
201 C) seems to be marked by the branchial and atrial apertures (/) ;
in the bud, however, these two apertures do not lie at the ends
Ki<.. 201. -Three consecutive ontogenetic stages of two Ascidiozooids. side view,
diagrammatic (following Salensky). cl, atrium; d, alimentary canal; e, atrial
aperture; es, endostyle ; i, branchial aperture ; ks, gill-clefts ; n, nervous system;
/.. peribrancnial cavity.
of the longitudinal axis (Fig. 201 A). This shows that through the
changes brought about by growth during the course of development,
the longitudinal axis of the bud is replaced by a new one running
at right angles to it. The longitudinal axis of the young Ascidio-
zooid, the two poles of which are represented by trabeculae join-
ing one Ascidiozooid to another becomes, later, the transverse axis of
408 TUNICATA.
the adult Ascidiozooid. The upper surface of the body in the Ascidio-
zooid thus contains one half of the later dorsal side and the corre-
sponding half of the later ventral side. The boundary between these
two halves is marked by the position of the branchial aperture (Fig.
201 A, >'). In comparing the adult with the young Ascidiozooid, we
must bear in mind the distinctions, which may be tabulated as
follows : —
YOUNG. ADULT.
Upper surface of the body. = Surface of the anterior half of the
body.
Lower surface of the body. = Surface of the posterior half ol the
body.
The anterior part of the embryo from = Neural surface of the body,
the branchial aperture to the corre-
sponding point of the lower side.
The posterior part of the embryo, from - Haemal surface of the body (marked
the branchial aperture to the corre- by the endostylel.
sponding point on the lower side.
The terms " right " and " left," however, are applicable to the
same sides of the body in the young and the adult.
As the gill-slits increase in number and in size, the peribranchial
sacs, the epithelium of which flattens, enlarge coiTespondingly. Each
of them gives off a diverticulum to the lower surface of the body
which, by fusing with a corresponding diverticulum from the other
side, leads to the formation of an unpaired atrial cavity (Fig. 200, cl).
The branchial aperture (Fig. 200, i) is derived from an ectodermal
invagination on the upper surface of the embryo between the nervous
system and the anterior end of the endostyle. We cannot here enter
further into the somewhat complicated processes which, according to
Salensky, lead to the development of this aperture and its valve-
like closing apparatus.
The branchial aperture appears at a rather early stage, but the
exhalent or atrial aperture only forms at a late stage after the
development of the Ascidiozooid is, in other respects, completed.
The common cloacal cavity of the colony, into which the atrial
apertures of the individuals open, was traced back by Kow alrysky
to the atrial cavity of the Cyathozooid. Salensky on the contrary,
observed that, when the Cyathozooid degenerates, its atrial aperture
closes, and consequently atrophies with the rest of the body. We
must therefore assume that the common cloacal cavity of the Pyro-
*<>n«i colony is a new structure which arises later, though its develop-
ment has not so far been described (p. 403).
The primary enteric rudiment in the Ascidiozooids gives rise first
directly only to a pharyngeal cavity which functions as a respiratory
PYROSOMA- THE FOUR PRIMARY ASIDIOZOOIDS. 409
cavity. The rudimenl of the stomach and intestine is found on the
lower surface of the entoderm-tube in the form of a blind horseshoe-
shaped diverticulum (Fig. 200 B) closely bent upon itself, the free
ends being directed anteriorly. The two limbs of the horseshoe are
seen cut through in the cross-section given in Fig. 204 (oe and ed).
One limb (ed) of this rudiment separates early from the entoderm-sac
and, as a blind diverticulum, represents the rudiment of the intestine,
while the other gives rise to the stomach and oesophagus. The com-
munication between this latter limb and the pharyngeal cavity is re-
tained as the entrance to the oesophagus (oe). Only in later stages
does the blind end of the intestine become connected with the atrial
cavity and the alimentary canal attains complete development with
the appearance of the so-called digestive gland.
ms
Fig. 202. — Transverse section through the anterior region of an Ascidiozooid' of
Pyrosoma with the rudiment of the nervous system (after Salenskt). ec, ectoderm ;
i-ii, entoderm; ms, mesoderm-cells ; n, rudiment of the nervous system ; p, peri-
branchial tube.
The central nervous system arises in the most anterior region of
the Ascidiozooid as an ectodermal invagination (Fig. 202, n) on the
upper surface of the body, which soon becomes separated from the
ectoderm as an elongate closed vesicle. This, at a later stage, becomes
triangular (Fig. 200, n). The anterior part* of this vesicle forms the
rudiment of the ganglion proper principally by a growth of its upper
wall. From this region, two lateral hollow processes arise (Fig 200.
m) which, at a later period, grow and embrace the sides of the ali-
mentary canal. These are the rudiments of the lateral nerves which
thus arise here in a way similar to that described by Seeliger for
the later buds of Pyrosoma. The narrowed portion of the neural
rudiment which is directed towards the branchial aperture becomes
connected with the ectoderm of the alimentary canal, and, by a per-
* [Anterior in relation to the long axis of the bud. poste/fo^B^ibM^scl&iltyV
|lu LIBRARY ^J
410 TUNICATA.
foration which takes place between the neural and the enteric
cavities, becomes the rudiment of the so-called ciliated pit (Fig. 200,
ff). According to Salensky, the lumen of the neural tube is obliter-
ated later, through the encroachment of the cells forming its walls,
as the ganglion develops further. The lumen of the embryonic ciliated
pit is also said to disappear ; the similarly-named organ of the adult
is thought to arise anew from the enteric wall. The blind end of the
ciliated pit changes later into a large sac lying beneath the ganglion
which probably forms the rudiment of the sub-neural gland.
Since the chain of Ascidiozooids arose as an outgrowth from the
body of the Cyathozooid, its primary body-cavity, which extends from
the enteric tube and the peribronchial cavities to the ectoderm, is in
open communication with the primary body-cavity of the Cyathozooid.
It is therefore possible for mesenchyme-elements to pass over from
the Cyathozooid into the chain of Ascidiozooids. According to
Salensky, this actually happens to a great extent, large numbers of
the elements of the cell-zone passing over into the chain. According
to this author, the cell-zone which was described above (p. 398), and
which is to some extent derived from inner follicle-cells (kalymmocytes),
but for the greater part from elements of the disintegrated left coelemic
sac, is the principal source of the whole of the mesoderm in the Asci-
diozooids. It must indeed be pointed out that the pericardial tube
which is derived from the right coelomic sac and extends posteriorly
as a prolongation of the pericardial rudiment of the Cyathozooid, after
breaking up into separate cells, may also contribute to the formation
of the mesenchyme in the Ascidiozooids, and this may also be the
case with the so-called axial mesoderm-strand which arose from the
tube interpreted as the remains of the chorda. The later fate of
these structures is difficult to make out from Salensky's account.
This author in any case seeks the origin of the mesoderm of the
Ascidiozooids in the cell-zone which, in its turn, is derived principally
from the elements of the disintegrated left coelomic sac. The immi-
gration of the mesoderm into the germ-stock (the chain of Ascidio-
zooids) takes place first in the form of an ingrowth of crowded
cell-masses. Later, when the cell-zone has broken up into separate
islands, detached cell-groups or single elements pass over into the
body-cavity of the Ascidiozooids.
The mesodermal elements become distributed in the primary body-
cavity of the Ascidiozooids. Two groups of them, however, soon take
up a definite position in the posterior region of the zooid at either
side of the body, and their elements are found to be arranged in two
PYROSOMA THE FOUR PKniAliY ASCIDIOZOOIDS.
411
layers, the external layer (Fig. 203 A, el) being the rudiment of the
elaeoblast, and the inner that of the so-called pericardial strands,
which must not be confounded with the pericardial tube mentioned
above, an organ that disappears at an early stage (Fig. 203 A, pc and
pc'). The cells of the elaeoblast-rudiment soon increase in size and
form a rather high cylindrical
epithelium. At a later stage.
they are less regular in their
arrangement, vacuoles develop
within them and they change
into large elements, resem-
bling vegetable parenchyma-
cells, and thus assume the
features characteristic of the
elaeoblast-tissue (Fig. 203 C).
The elaeoblast is here at first
paired and consists of rounded
groups of cells lying in the
posterior part of the body
which cause the surface of
the bodyr to bulge out some-
what (Figs. 194 and 200 el).
The inner layer of the
paired mesodermal rudiment
just described gives rise to
two cell-strands which develop
differently (Fig. 203, pc, pc').
The strand to the right
extends somewhat further
forward than the other, and
its anterior end becomes
transformed into a closed
vesicle, the pericardial vesicle
(Fig. 203 Sand C, pc). The
heart develops through the
thickening of that wall of the
vesicle which is in contact
with the alimentary canal and its invagination into
The heart consequently forms here in the same way as
Tunicates.
The right pericardial strand (Fig. 203, pc) is not completely used
Fig. 203. — Transverse sections through the
distal region of au Aseidiozooid of Pyrosoma
in three consecutive stages of development
(after Salensky). ec, ectoderm : el, rudi-
ment of elaeoblast ; en, entoderm; es, paired
endostyle-folds ; .). This
fold within which the blood now runs becomes completely separated
from the dorsal wall of
the intestine, and then
forms a tube running
freely through the intes-
tine from the neural
rudiment (Fig. 205, n)
to the beginning of the
endostyle - furrow (en).
This peculiar structure,
which has been called
by Salensky the 'pha-
ryngeal blood-sinus, and
by Huxley the diax>ha-
ryngeal band, may be
compared with the gill
of the Thaliacea with
which Salensky even homologises it, although topographically it is
clearly only an analogous structure. The diapharyngeal band is
merely a provisional adaptation which atrophies in the further
course of development.
Two structures, the significance of which is obscure, the elongate aud the
lenticular cell-masses (Keferstein and Ehlers) are to be traced back to the
mesoderm. The lenticular masses are paired and symmetrical accumulations
of cells lying at the entrance to the branchial sac between the wall of the
peribranchial cavities and the entoderm (Figs. 196, /, and 106, liii. p).
Salensky considers that they are to be derived from the kalymmocytes
(inner follicle-cells). They are said to be phosphorescent organs. The
elongate masses, which lie on the neural side "near the gills in the blood-
sinus," form later from an unpaired accumulation of mesoderm-cells which
originally lies below the so-called languets of the entoderm (Figs. 196, d.
106, dm).
Fis. 205. — Longitudinal section through an Ascidio-
zooid of Pyrosoma (after Salensky). db, diapha-
ryngeal band ; el, elaeoblast ; en, endostyle ; i,
branchial aperture ; m, stomach ; ms, sphincter
muscle ; >i, rudiment of the ganglion ; oe, oesoph-
agus ; v, connective strand.
414 TUNICATA.
The body - musculature, which is only slightly developed in
Pyrosoma, arises from mesenchyme-cells arranged in bands. The
fibrils of contractile substance are arranged round the periphery of
these cell-bands which, in cross-section, appear triangular and extend
in a radial manner towards the interior of the muscle-bundle.
As may be seen from Fig. 196, p. 402, the four primary Ascidio-
zooids of the young colony are placed radially to the principal axis
in such a way that their branchial apertures appear to lie equatorially
on the outer surface. The centre of the colony is at first occupied
by a Cyathozooid but later by the common cloacal cavity which opens
externally at the pole marked cl in Fig. 196. The dorsal surface of
each Ascidiozooid is turned towards the cloacal cavity ; its ventral
surface, on the contrary, seems turned towards the opposite pole.
Since it is here (at the end of the endostyle) that the first buds
become abstricted, it might be expected that the oldest Ascidiozooid
of the colony would lie nearest to the common cloacal aperture, while
the younger Ascidiozooids would occupy the posterior part of the
colony, that turned away from the cloacal aperture. According to
Seeliger, however, this is not the case ; but the young buds, after
becoming separated from the parent individual, wander to its dorsal
side so that they become intercalated between it and the common
cloacal aperture. Each Ascidiozooid gives off towards the cloacal
aperture two mantle- vessels which, in Fig. 196 B, can already be
seen as dorsal processes in the neighbourhood of cl. In large colonies,
the four primary zooids surround the posterior pole of the colony,
that turned away from the cloacal aperture and their mantle-vessels
must consequently have the longest course.
5. The Hemimyaria (Salpidae).
The embryonic development of the Sulpiride stands in somewhat
sharp contrast to that of other Tunicates. The fact that the
developing embryo fuses with the wall of the atrial cavity of the
mother and that, at the point of fusion, there develops a nutritive
organ known as a placenta derived in part from the remains of the
egg-follicle, has brought about divergent ontogenetic conditions.
The development is abbreviated, as it usually is where it takes place
within the body of the mother. Neither the larval tail nor the
chorda develops. It must be at once admitted that our knowledge
of the embryonic development of the Salpidae must not be regarded
as in any way complete. Even with regard to the most important
THE HEMIMYARIA (SALPIDAE). 415
points, such as the cleavage, the formation of the germ-layers and the
development of the placenta, the recorded investigations are incom-
plete and contradictory, and we have statements which we must
hesitate to accept because they are at variance with all that is known
of the development of other Tunicates (and of animals in general).
In our account we shall have these difficulties to contend with
and must restrict ourselves to giving a brief survey of what at the
present time seems to lie fairly well established. We cannot enter
upon the many contradictory and obscure points in connection with
this subject.
Among the Salpidae, the sexual individuals (the forms belonging
to the chain) are hermaphrodite, but the time of maturation of the
male and female products differs. The individuals of the young
chain set free from the stolon of the "nurse" generation (solitary
• /
Fig. 206. — Side-view of Salpa demooratica-mucronata (combined after Claus and
Salbnskt). '/. atrial cavity; e, atrial aperture; end, endostyle ;/, peripharyngeal
band; i, branchial aperture ; k, gill; /*, nerve-ganglion ; /"/, nucleus; od, oviducl ,
ov, ovary (consisting of a single egg-follicle) ; ph, pharyngeal cavity ; x, aperture of
the oviduct.
form) are at first female ; they are fertilised by the individuals of
another chain, and each develops one embryo. Only as this develops,
do the testes become functional.
The Sal pidae, as a rule, develop only one egg. The whole ovary
( Fig. 206, ov) consists, in such cases, of a single follicle which con-
tains the egg and is connected with the epithelium of the atrial
cavity * by a strand-like oviduct in which two portions can be dis-
* [Owing to the peculiar relations existing between the pharynx and the
atrial cavity in Salpa, it becomes extremely difficult to decide their limits ;
the term respiratory cavity (Ath.emb.dhle) is commonly loosely applied to the
greater part of this chamber. We have, however, thought it advisable to drop
this word and to use in its stead the more specific terms atrial cavity and
pharyngeal cavity in those cases in which we were able to determine the
portion of the general cavity which was being referred to. — Ed.]
416
TUNIC ATA.
tinguished (Fig. 207). One of these (st) is directly connected with
the follicle and consists of a single row of cells (the so-called stalk
Fig. 207. — Female genital apparatus, A, of Salpa pinnata (after Salbnskt); B, of
Salpa virgula (after Todaro). a, epithelium lining peribraneliial sac (atrium) of
parent animal; b, blood-sinus; e, egg-cell; em, embryonic chamber; ep, epithelial
prominence; /, follicle; m, aperture of the oviduct; od, distal dilated part of the
oviduct ; ov, ovarian chamber ; s, process of the embryonic chamber ; st, narrowed
part of the oviduct (so-called stalk of the follicle).
of the follicle) and the other is a dilated efferent portion (od), with
a distinct lumen. The egg-follicle lies at the base and to the right
rill: IIKMIMYAKIA (SALPIDAE).
417
of the nucleus near th< sophagus (Fig. 206) ami is surrounded by
ramifications of the circumvisceral network of blood-vessels. The
oviduct also appears to be accompanied until near its aperture by
a vascular network (Fig. 207 A', b). The point at which the oviduct
opens (Fig. 206, .<■) is found on the right side of the body behind the
penultimate muscle-hoop above the nucleus. Round the aperture,
the epithelium of the atrial cavity is thickened into a shield (Fig.
207 A. '/-) and projects slightly inward (Fig. 207 A, e/i). This
swelling is the rudiment of the epithelial pro?ninence of Salensky
which TODARO calls the ul, rus.
--/
-/
The question now arises whether the members of a Salpa-chain, after the
birth of the mature embryo, remain sterile or are able to produce a new ovary
which may yield a new embryo. Some of Salexsky's observations seem to
favour the latter view. The individuals composing a chain grow consider-
ably in size while the embryo is developing within them, so that the largest
individual contains the most advanced embryo. Salensky, in such a large
individual, found the remains of a placenta
which indicated the previous expulsion of «
an embryo and, side by side with this, a
mature egg or a quite young embryo.
Exceptions to the rule that each individual
of a chain produces only one embryo are
found in Salpa zonaria (Chamisso and P^scn-
richt), .S'. Thilesii (Kbohn) and S. hexagona
iTraustedt), in which several embryos
develop simultaneously, although they are
not all at the same stage of development.
In consequence of this and of the presence
of a special point of attachment for each
embryo, Lf.uckart (No. 98) concluded that
several egg-follicles with distinct ducts must
be present. These forms have recently been
united to form the genus Iasis (Lahii.i.i .
No. 38), the above feature being one of its
eric characters.
In many of the Salpidae {S. maxima, S.
pinnata, S. />/tiut'). into two chambers, one
of which (the ovarian sac, ov) contains the
egg during the stages of its maturation, while
the other (the embryonic sue, cm) receives it
during the first embryonic stages. Inmate,
forms (e.g., S. maxima) the embryonic sac is
continued into a pointed process (s) which
soon degenerates. The remains of this process, in later stages, when the
KE
f
Fig. 208. — Dorsalaspecl of Salpa
Mcaudata (original). ". point
.it which this individual is
connected with its neighbour
in tin- chain : e, atrial aperture :
end, endostyle : ./'. periphar-
yngeal band ; g, genital tube .
i, branchial aperture ; /.•, Kill ;
n . nerve-ganglion ; nu, nucleus.
418
TUNICATA.
embryonic sac, in consequence of the shortening of the oviduct, shifts towards
the epithelial prominence, serves for attaching the sac to the epithelium.
The development of the female genital apparatus of Salpa (Pegea) bicau-
data is quite exceptional. Here (Fig. 208) at about the middle of the body
of the individual of the chain, at the right side, there is an outgrowth of the
body-wall with a somewhat curved eud (genital tube, g, Salensky, No. 104).
Fig. 209. — Two stages in the development of Salpa bicaudata (after Salensky). In
.1 (a combined figure after Salensky), the embryo e still lies at the base of the
genital tube (//) within the dilated oviduct. In /.'. the embryo, at a more advanced
stage, has passed out of the tube together with the placenta. ", wall of the respira-
tory cavity; b, blood-forming bud (remains of the follicle); c, umbilical cord
(connection between the embryo and the placenta) : e, embryo in the dilated oviduct ;
el, elaeoblasl ; en, endostyle ; /, genital fold ; fl, ciliated pit ; ) we recognise the follicular epithelium. It appears
that, in this stage, the opening of the oviduct into the atrial cavity
has completely closed.
After cleavage has ended, the embryo forms a solid, rounded body
composed of numerous cells which, according to Salensky, are
mostly derived from the follicular epithelium, but, according to
Todaro, have been produced by fission from the blastomeres. We
shall for the present adopt the latter view as the more probable.*
* | Sec editorial note, p. 421 |.
SAU'Ih \i: I'OKMS WITHOUT COVERING FOLDS. L23
According to Todako, the cells derived from the follicle-epithelium
which are fated to disintegrate, can still be distinguished between
these embryonic cells. It should, indeed, be mentioned that
Salenskv was able to find within the embryo, long after cleavage
had ended, at a time when the first rudiments of organs grow dis-
tinct, a feu large blastomeres definitely arranged. The significance of
these is obscure, and we are altogether in the dark as to those stages
in the development of Salpa winch lie between cleavage and the be-
ginning of the formation of the organs, i.e., the stages in which we
should expect the germ-layers to form.* The cleavage-cavity appears
to be wanting in all Salpidae [Salensky, Heider and Korotneff] .
Brooks, however, suggests that the follicular cavity may be thus
interpreted.
Certain divergencies are found in the different species of Salpa in
the further processes of development, hut these apparently are not
due to any fundamental difference. The development of most species
being as yet only very partially known, we shall restrict ourselves to
a closer account of the two forms which have been best investigated,
viz., S. democratica-mucronata and S. pinnata. These represent two
types of development which are to he distinguished by the absence
or presence of a covering fold and by the structure of the placenta. t
A. Forms without Covering Folds.
The embryo of Salpa [Thalia) democratica-mucronata, in the stages
that mark the completion of the cleavage-processes (Fig. 211 C) pro-
jects in the form of a cone into the atrial cavity of the parent. It
lengthens later and becomes more cylindrical, its end being rounded
(Fig. 212 />')• It is still surrounded by the two walls of the brood-
[Recent investigations tend to show that germ-layers, as we understand
them in other animals, cannot be said to exist in Salpa, since the various
germ-cells, which give rise to the different organs, appear to be mixed in an
irregular way throughout the germ-mass. Gradually, however, certain of the
blastomeres take up definite positions, and, from what is known of their sub-
sequent history, can now be definitely stated to give rise to certain tissues.
The first of these rudiments to be recognised is the ectoderm ; this takes the
form of certain large blastomeres which migrate to the surface opposite the
phuenta and there give rise to the ectoderm and its derivatives. Other large
blastomeres which remain nearer the placenta have been found to give rise to
In entoderm and possibly some mesoderm ; the latter layer, however, appears
to arise largely from the smaller blastomeres which, with the kalymmocytcs.
make up the main mass of the germ. — Ed.]
t [Korotneff (No. XVIII.) expresses grave doubts as to the advisability of
i his subdivision, and there can be no doubt from recent investigations that
the developmental differences between these two divisions have been greatly
exaggerated. — Ed.]
424
TUNIC AT A.
sac (Figs, l'11 C, 212 A, a and b). The first differentiation in the
embryo consists in the appearance of a continuous superficial cell-
la yer, in which we recognise the ectoderm of the embryo (Fig. 212
A, ec).* Important changes in the brood-sac take place at the same
time, its outer lamella, which represents a layer continuous with the
epithelium of the atrial-cavity of the parent (Fig. 212, a) soon chang-
ing into an extremely thin pavement-epithelium. The inner lamella
of the brood-sac (Fig. 212, b) represents the modified epithelium of
the oviduct and the follicle. In it we can distinguish a simple cell
layer which at first completely encircles the embryo. This is the
inner lamella of the brood-sac in the strict sense of the term, and is
-ec
Fiii. 212.— Two sections through embryos oi Salpa democratica-mucronata (diagram-
matic, after Salensky). .1. younger stage; /.'. sagittal section through an older
stage, a, outer lamella of the brood-sac; h. inner lamella of the same; ec, ecto-
derm [layer ot kalymmocytes, ectoderm not yet formed, Korotneff] ; i. inner cell-
mass (entoderm, mesoderm?); /. rudiment of elaeoblast;
mesoderm ( .'
rudiment of the nerve-centre ; j*. remains ot the follicle = rudiment of the placental
tissue ; c, ectodermal thickening, from which the covering of the placenta is derived
[this is follicular, i.e., maternal in origin according to Korotneff],
no doubt derived from the modified oviduct. To the base of the sac
formed by the inner lamella is attached a cell -accumulation (p) which
probably represents the modified cell-material of the follicle ; this
forms the first rudiment of the placenta. [The placenta, including
the basal plate, according to Kokotneff (Xo. XX".) is wholly
maternal in origin.
•[According to Korotnkff (No. XVIII.) the embryo becomes covered in the
first instance by a layer of kalymmocytes; these Salensky mistook for the
ectoderm. The latter layer forms later by a rupture in trie layer of kalym-
mocytes covering the embryo and a discharge of blastomeres through the gap
into the follicular cavity, where they become arranged as a layer, the future
ectoderm between the follicle and the embryo. AIoseneh\ ine-eells are also dis-
charged into this cavity, and arrange themselves under the ectoderm. — Ed.]
SALPIDAB — POEMS WITHOUT COVERING FOLDS. t36
It appears thai the inner lamella of the brood-sac is very soon
reduced (Fig. 212 /I) and completely degenerates. This degeneration
at tirst affects a zone running obliquely round the embryo, Leaving
only a cap of the lamella covering the anterior end of the embryo and
a posterior cup-like portion connected with the rudiment of the
placenta, which completely unites with the latter at a subsequent
period : the anterior cap appears soon to disintegrate. The embryo
is then covered by only one envelope, the outer lamella of the brood -
sac (" ).
The above i> in accordance with Salbnsky's earlier description of the fate
of the inner lamella (No. 100). The more recent statements of this author
>u^gesi t hat 1 he inner lamella does net disintegrate, hut enters into close con-
nection with the embryo, finally changing into the ectoderm of the latter.
The ectoderm in S. democratica-rmicronata would then have to he traced
back to the transformed epithelium of the oviduct, a view which is a prion
improbable, and less in accordance with our own investigations than the older
statements. [The ectoderm, like the other embryonic organs, is now generally
regarded as arising from the blastomeres. See footnote, p. -124, and Korotnefk
(No. XVIII.) on S. democratica.]
In the next stage (Fig. 212 B) important differentiations are evident
in the embryo. The mesoderm {in) has appeared between the ecto-
derm and the entoderm in the form of a cell-accumulation, which
spreads out like a germ-layer to right and left over the sides of the
embryo. 'The central nervous system (>i) is also found as a cell-
growth proceeding from the ectoderm. Its position marks the plane
of symmetry and the anterior end of the body in the embryo.*
Diametrically opposite to it is another cell-accumulation (/), which
Salkxsky also traces back to the ectoderm, and which seems to be
the first rudiment of the elaeoblast. That part of the ectoderm which
is in contact with the rudiment of the placenta is already distinguished
by the large size and the height of its cells (./■). This is the rudiment
of the lamella, which takes part in the formation of the epithelium
eo\ ering the placenta.
The fundamental features of the organisation of the embryo of
Salpa, which are thus already sketched out, appeal' still more dis
tinctly in the following stage (Fig. 213), in consequence of the
development of a system of cavities. The inner cell-mass severs
* [Kobotnbpf believes that the aervous system is termed as ;i closed vesicle,
which lies at tirst quite independently in the mesoderm without any relation
i.i the ectoderm or to the pharynx. The elaeoblast also arises from the
embryonic blastomeres and aol from follicular cells, as Salensky stated. —
Ed.]
426
TUNICATA.
itself from the ectoderm, giving rise to a cleft which gradually widens
to form the rudiment of the 'primary body-cavity (I). A cavity rises
in a similar way within the entodermal cell-mass, this being the first
rudiment of the alimentary canal, especially of the branchial sac
(pharnyx, Fig. 213, d). This chamber, when it first appears, con-
sists of two lateral cavities connected across the middle line by a
narrower part (Fig. 213 B, k).* The dorsal ingrowth that partly
separates the two halves of the enteric cavity must be regarded as
the rudiment of the gill (Fig. 213 B, /•). It becomes separated from
t—
-.-J
--x
Fw. 213. -Transverse sections through two ontogenetic stages of Salpa democraticce-
mucronata (schematic, original). ", miter lamella of brood-sac ; d, rudiment of the
alimentary canal ; ec, ectoderm ; /', rudiment of the .nill ; /. primary body-cavity ;
ms, mesoderm ; /). rudiment of tin- placenta (remains of tin- follicle) ; / , the epithelial
covering (basal plate) of the placenta ; x, tissue of the placenta ; "., large marginal
■ ells .it the placental tissue.
the enteric rudiment, by the fusion of the atrial cavity, which
develops between it and the ectoderm, with the projecting lateral
diverticula of the pharyngeal cavity. The atrial cavity of Salpa is
derived by Todako (No. 113) from an ectodermal invagination. The
-ill, which is originally a solid ingrowth of cells, changes later into
* [Investigations both on this and other species show that, in every case,
the atrial cavity is the first to appear. Hkider and Korotnkff agree in
describing it as a single cavity from its earliest origin, while Brooks ascribed
a paired origin similar to that found by Salensky for the atrium and, on this
account, Brooks concludes that Salensky mistook the atrium for the pharynx.
The pharynx appears below this as cither a single or paired cleft in the
embryonic mass, and the gill arises from the horizontal septum between
these two cavities (atrium and pharynx), by the appearance in it of a pair of
laterally placed longitudinal slits. — Ed.]
SALPIDAE POEMS WITHOUT COVKKINd FOLDS. 127
,i tube, the inner cells bean;1 transformed into blood-corpuscles which
pass into the blood.
Before passing on to describe the other changes that take place in
the embryo we must dwell for a moment on the degeneration of the
brood-sac and the development of the placenta. After the inner
lamella of the brood-sac has degenerated as described above, the
lnbrvo remains surrounded solely by the very thin epithelium of the
>uter lamella (Fig. 212 B, a), which consists of a differentiated part
)f the atrial epithelium of the parent. This outer lamella is unable
to keep pace with the further increase in size of the embryo : it
becomes ruptured at the point at which the aperture of the oviduct
was originally situated and shrinks downwards over the embryo (Fig.
213). In consequence of this contraction of the outer lamella the
embryo, which originally lay in the follicle (Fig. 211 .1), and then
shifted forward into the dilated oviduct (Fig. 211 />'), protrudes
into the atrial cavity of the parent, in which from this time it lies
Freely.
We have already seen (p. 424) that a compact cell-mass is attached
to the lower surface of the embryo (Fig. 212, ji) : this, which
represents the first rudiment of the placenta, is derived from the
transformed cell-material of the egg-follicle. The outer lamella of the
brood-sac now shrinks completely back overthis cell-mass, and finally,
as a constricted funnel-like annulus, surrounds and strengthens the
connection between the rudiment of the placenta and the parent (Fig.
214, '()• The placenta-rudiment would lie exposed, after the with-
drawal of the outer lamella, were it not covered by a thin ectodermal
layer of the embryo (Fig. 214, ec), which develops as the brood-sac
is withdrawn. Through this circumcrescence of the placenta by an
ectodermal lamella, which was not observed by Salensky, but of
which we were able clearly to convince ourselves, the placenta is
incorporated in the embryo and then appears enclosed in a capsule
derived from the ectoderm of the embryo. The lateral walls of this
capsule are formed by the thin lamella just mentioned ; its upper
wall or the so-called roof (Fig. 213, f), on the contrary, is yielded by
the thick ectoderm-layer, the origin of which was traced above (p. 425).
(This is of follicular origin according to Korotnefk ( No. XXa.).] < hi
its underside the ectodermal capsule of the placenta possesses an
aperture through which the placental cavity communicates with the
blood-vascular system of the parent. The placental cavity arises in
the form of gaps or clefts in the placental tissue, which thus assumes
a loose structure. Some of the cells of this originallv compact tissue
428
TUNICATA.
now form a layer of large, swollen cells in contact with the ectodermal
capsule, while others form a granulated trabecular network traversing
the cavity of the placenta (Figs. 213 B, 214, x and z). The cavity of
the placenta, therefore, as Leuckart rightly pointed out (No. 98),
communicates with the blood-vascular-system of the parent, but never
with the body-cavity of the embryo, from which it is always divided
by the continuous ectodermal capsule of the placenta. Our own
researches have hei*e led us to differ from Salensky, according to
whom the placental cavity appears as a part of the body-cavity of the
embryo.
Fig. 214. -Longitudinal sections through two later embryonic stages of Salpa demu-
cratica-mucronata (after Salensky, somewhat altered), n, contracted outer lamella
of brood-sac ; b, blood-sinus within the"placenta ; cl, atrium or peribranchial cavity ;
'/. rudiment of the alimentary canal ; e, epithelium of the atrial cavity of the parent ;
ec, ectodermal covering of the placenta; el, elaeoblast; />. rudiment of the heart;
n, nervous system ; pc, pericardial vesicle; j>h, pharyngeal cavity; I, so-called rool
of the placenta (basal plate) ; '.tissue of the placenta; :. marginal cells of the
placental tissue.
The placenta is concerned in the nourishment of the embryo. In
later stages it attains greater independence, its connection with the
embryo becoming constricted (Fig. 216). The point at which the
placenta is inserted lies on the ventral side of the embryo, between
the two endostyle-folds. When the embryo separates from the parent,
the placenta remains hanging to it; in the free-swimming solitary
forms, a vestige of this organ is long visible as a small stalked body
enclosed in the mantle-substance (Leuckart). The wound formed
in the wall of the respiratory cavity of the parent when the embryo
detaches itself is, according to Leuckart, closed by the remains of
SALPIDAE — FORMS WITHOUT COVERING FOLDS. 129
the brood-sac which can still be recognised for some time as a kind
nf corpus luteum. The embryo, at birth, passes out through the
atrial aperture of the parent .
The development of the final shape of the body goes hand in hand
with the development of the placenta. The embryo at first formed
a cone projecting into the atrial cavity of the mother (Fig. 212), its
principal axis corresponding to the future dorso-ventral axis. It now
lengthens at right angles to this axis, i.e., in accordance with itrs
future longitudinal axis (Fig 214). It soon becomes cylindrical and,
after the cellulose mantU has developed, resembles a tetragonal prism.
The mantle-substance develops in just the same way as in the
Ascidians (p. 355). It arises on the outer surface of the ectoderm
as a secretion into which single cells soon wander. Finally, the two
conical processes characteristic of Salpa democratica (solitary form)
develop (Fig. 262, p. 495).
The nervous system has been seen to arise as a solid ingrowth of
the ectoderm.* This soon severs its connection with the latter, a
cavity develops within it, and it becomes a vesicle characterised by
its size and the thickness of its walls (Fig. 214, u). Kowalevsky
(Xo. 96) was aware of the fact that this vesicle lengthens later and
is indistinctly divided by constrictions into three consecutive parts
which show a certain resemblance to the primary cerebral vesicles
of the vertebrate embryo (Fig. 214 B, n). The anterior vesicle
1m ■(■dines closely connected anteriorly with the adjacent wall of the
pharynx, and this connection which is at first solid soon develops
a lumen which puts the neural cavity into communication with the
pharyngeal cavity. The canal thus formed is the first rudiment of
the future ciliated pit (Fig. 216, //). While this organ develops
further, the walls of the ganglionic vesicle thicken, it shortens, its
lumen disappears and the vesicular rudiment thus gradually assumes
the character of the definitive ganglion of the adult. A conical
process rising on the dorsal side of the ganglion on which three
accumulations of pigment appear represents the rudiment of the
eye.
further details as to the development of the eye have recently been pub-
lished by Metcalf (No. 99) and Butschli (No. 94). t The eyes seem to develop
differently, not only in the different species but also in the solitary and the
colonial forms of the same -pecies. According to Butschli, the simplest Eorm
[See footnote, p. 425.— En.]
t [See also Mktcai.f in Brooks' Monograph (No. I.), and Goppert
\(,. 94a).— Ed.]
130
TUNICATA.
^"7*
of eve is a mound-like swelling of the brain (Pig. 215 .4) ; at the sides of this
swelling are arranged the pigment-cells while, from the centre, closely packed
rod-bearing cells are found radiating
towards the surface, the nerve-fibres
being connected with the inner ends of
the rods. In this eye, the rods are
tberefore turned directly towards the
source of light. In other forms, the
rudiment of the eye becomes differenti-
ated into three parts which either remain
united in the shape of a horse-shoe, or
form three entirely distinct eyes, the
unpaired median eye retaining the
original simple condition (Fig. 216 />, a)
while the two lateral eyes are formed
on the plan of an inverse eye (b), i.e., the
rods are directed away from the surface
and the nerve -fibres are connected with
their outer ends. Butschli, assuming
an optic vesicle which cannot be observed,
homologised the median non-inverted
eye with the cephalic eye of the Verte-
brates, and the lateral inverted eyes with
the paired eyes of the Vertebrates, but,
independent of this theoretical vesicle,
the structure of the lateral eye of the
Ascidian larva seems directly to suggest the paired vertebrate eyes by the
fact that the rods are directed towards the cerebral cavity (see, however, the
objections raised by Metcalf, No. 9'Ja, and Goppert, No. 9±. 426). The wall of the pharyngeal
cavity is formed by a simple epithelium, the cells are either cubical
or somewhat flattened. The rudiment of the endostyle (hypobranchial
furrow) appears in the form of paired folds of this epithelium origin-
ating at some distance from each other (Fig. 216, es) ; these shift
towards one another later and then form the boundaries of a hypo-
branchial furrow which runs from the peripharyngeal bands to near
the entrance of the oesophagus. The rudiments of the peripharyngeal
hands which run towards the anterior end of the gill from the anterior
end of the endostyle, encircling the aperture of the respiratory cavity,
first appear as similar prominences. The rudiments of the branchial
and atrial apertures (Fig. 216, i and e) appear only in later stages
in the form of transverse depressions of the ectoderm which break
through into the pharynx and atrial cavities. The rudiment of the
(trial aperture originally lies almost at the centre of the dorsal side
Pig. 215.— Diagram of the eye of a
Salp (after Butschli). A, typical
single eye ; B, typical tripartite eye.
c, median part, /*, lateral part of
the tripartite eye: u. nerve-fibres;
]>, pigment-cells : /'. retina.
S.VUMDAK KOK.MS WITHOUT COVERING FOLDS.
43 I
of the bodv (Fig. 216), but later, as the partof the body known as the
nucleus decreases in size, it shifts further back.
The rudiment of the alimentary canal, in the strict sense of the
term (Fig. I'll B, d), originally forms a posteriorly directed diverti-
culum of the pharynx. This caecum becomes divided later by two
folds rising into it from below into three spaces (Fig. 216, oe, m, ed),
the anterior space being the rudiment of the oesophagus, while the
posterior space represents the intestine. The middle space is the
rudiment of the stomach-caecum. The intestine curves upward
Fig. 216.— Later embryonic stage of Salpa denweratica-mucrouata (after Salensky).
e, atrial aperture ; eb, elaeoblast ; ed, intestine ; es, endostyle ; il , ciliated pit ; i,
branchial (oral) aperture ; /•, ,uill ; m, stomach-caecum ; n, ganglion ; oe, oesophagus ;
//, pericardial sac : /). In this respect this group
would seem to differ from the Ascidiacea, in which, according to
van Beneden and Julin, such an intima is wanting (rf. pp. 363
and 371).
The elaeoblast (Fig. 216, eb), the rudiment of which has- already
been described (p. 425), attains its full development only in the later
stages of embryonic life, and, after the birth of the embryo, under-
goes gradual degeneration [by phagocytosis, according to Korotneff
(No. XIX.)]. It is a mass of large polygonal cells, which are filled
with reserve nutrition. The remarkable resemblance between the
elaeoblast and the degenerating larval tail of Doliolum (p. 388) caused
Salensky to assume that this problematical organ is the homologue
of the tail and the chorda of the Ascidian larva. But the presence
of the rudiment of the elaeoblast, as we shall see in the buds of the
Salpidae and of Pyrosoma, is not very favourable to this view.
Physiologically, the elaeoblast is probably, as Leuckart suggests,
a reservoir of food-material, which is gradually used up as the
embryo develops.
At a later stage of development the rudiment of the stolon can
be seen (Fig. 216, at). This consists first of a diverticulum of the
pharyngeal wall lying at the posterior end of the endostyle, and is
turned toward the left side of the body. The ectoderm soon bulges
over this entodermal diverticulum. The space between the two
layers is, according to Seeliger (No. 105), filled with mesenchyme-
cells, the short conical stolon thus consisting of three germ-layers
(p. 495).
* [According to Korotneff (No. XVIII.), the pericardium arises as in other
Tunicates as a diverticulum <>f bhe pharynx. — Ed.]
SAlil'IDAE — FORMS WITH COVERING FOLDS.
433
B. Forms with Covering Folds.
The development <>t" the forms belonging to this type (.>'. (Cyclo&alpa)
pinnata, S. africana-maxima, S. rundnata-t'»s/j'ornu's, S. p-nndatu)
differs in many essential points from that <>f S. democratica-niucronata.
The principal distinction consists in the presence in the former of an
external covering which after the degeneration of the primary brood-
sac (present also in S. democratica-niucronata), forms a secondary sac
investing the embryo, and in the peculiar development of the placenta.
The development of the organs also appears to follow another type.*
The forms just mentioned seem to agree fairly well in their develop-
ment, which has been studied by many zoologists, especially by
B
\
th
.->■ ■
m
u
>**;
Fig. 217.— Two ontogenetic stages of Salpa pinnata (after Salenskt) forming a
sequence to Fig. 210 B. b, blastomeres ; bk, "blood-forming bud"; hi, blood-
cavities in the placenta ; bl', median blood-sinus ; d, roof of the placenta (basal plate) ;
e, lower part of the epithelial prominence, known later as the placental membrane ;
e', upper part of the epithelial prominence (Salensky's ectoderm-germ) ; ./', folliculai
cavity ; fh, covering fold ; fvo, follicle-wall.
Todaro, Bakkois and Salensky, and more recently by Brooks
(No. [.), Heider (No. XIIL), and Korotneff (Nos. XX.. XX"..
and XXIa.). The following account relates chiefly to S. pinnata, a
comparatively well-known form.
Starting with the embryonic development of S. /linnntd at the
stage depicted in Fig. 217 A, we find conditions in fairly close agree-
ment with those described in connection with S. democrotica. The
embryo consists of large and of small cells. The protoplasm of the
large cells (b) breaks up in a peculiar way into polygonal portions
[See footnote, p. 423 and p. 445. — Ed.
FF
434 TUNICATA.
which must be regarded as the direct descendants of the blastomeres.
These seem to multiply little, but, up to the stage at which the
organs begin to develop, continue to be seen in the embryo (Fig. 219
A, b). The significance of these parts and their further fate are
obscure. The numerous small cells which form the greater part of
the embryo are all regarded by Salensky as immigrated follicle-cells,
but we think ourselves justified in assuming, with Todaeo, that they
are partly derived from the blastomeres and are only partly immi-
grated follicle-cells. The latter cells disintegrate, while the former
take an essential share in the formation of the embryo (p. 420 and
footnote, p. 421).*
The embryo lies in a sac (Fig. 217 A, fw) which is derived from the
union of the follicle and the dilated oviduct. The wall of this sac has
been described in .S'. democratica-mucronata as the inner lamella of the
brood-sac. At the posterior end of this sac a thickening is soon seen
in the forms now under consideration ; this becomes more and more
distinct (Fig. 217 B, bh), and is to be traced back to the transformed
wall of the follicle. While, in S. democrat ica-mucrojiata, this thicken-
ing forms the rudiment for the whole of the placenta, in S. pinnata
and related forms it represents a comparatively small part of that
organ, which does not develop further but, in later stages, breaks up
into its elements and mingles with the blood of the parent (or of
the embryo ?). This part has been called by Todaro the blood-bud
(bottone ematogene, Figs. 217 B, and 218, bk).
The embryo almost entirely fills the cavity of the brood-sac (Fig.
217, /). On one side, it appears to be continuous with the inner
lamella of the sac. According to Salensky, this side represents the
later haemal side of the body, so that we are able, even at this stage,
to orient the embryo. [According to Brooks (No. I.), this, on the
contrary, mai*ks the middle dorsal line of the embryo.]
The outer lamella of the brood-sac (Fig. 217, e and e) is derived
from the thickened part of the atrial epithelium of the parent, which
is pushed out into the atrium by the growth of the embryo beneath
it, and which is called by Salensky the epithelial prominence (p. 417).
Two parts can soon be distinguished in it. The upper part (rmol>la$tiea [the supporting
ring of t lie' placenta (Bkooks)] .
A differentiation somewhat resembling that just described in the
outer lamella is also found in the inner lamella (splanchnic layer of
the follicle) which represents the transformed epithelium of the ovi-
duct and follicle. The lower half of the lamella (Fig. 217 B, d), in
this case, becomes connected with the thickened epithelium of the
atrial cavity known as the placental membrane or supporting ring
i 't' the placenta (e), and forms the roof of the placenta (Fig. 218 A, dp),
in the centre of which the " blood-bud " is attached. The placenta
is thus hollow, its lateral walls (supporting ring, Fig. 218 A, mp)
being yielded by the epithelial prominence of the atrium, and its
roof (dp) by the inner lamella of the brood-sac, i.e., by the follicle
(placental portion of the follicle). The "blood-bud" (bk) hangs
from the roof into the cavity which is part of one of the blood-
channels of the parent. Salensky distinguishes in this cavity two
communicating sinuses, an afferent and an efferent sinus, and, be-
tween these two, a third vascular space round the " blood-bud" (Fig.
217 A, hi'), the relations and significance of which are unknown.
The placenta, which, from the first, is a greatly swollen structure,
now becomes constricted at its base (Fig. 218), and thus forms a
stalked structure on the upper surface of which the embryo rests.
It becomes saddle-shaped later, the parts lying at the sides of the
embryo growing upward. This is why, in a horizontal section (Fig.
219) only the lateral parts of the placenta (p) are seen cut through.
The actual relations of this organ are still very obscure.
While, in this way, the primary brood-sac undergoes essential
alteration, a circular fold of the atrial epithelium grows up from
the base of the epithelial prominence (Figs. 210 B, and 217, //*)
and completely overgrows the placenta and the embryo (Fig. 218, /),
and thus forms a new secondary brood-sac (embryo-sac) such as is
not found in »S'. democratica-mucronata. This is known as the cover-
in;/ fold or amnion. It continues to grow upwards as a circular fold
round the embryo, over which, however, it never fuses, but remains
separated by a variable aperture through which the embryo eventu-
ally passes out into the atrium.
There are, in the different species, characteristic variations in the form of
this fold. In S. africana-maxima, the aperture is elongate and the margins
of the fold project and take the form of a semicircular crest ; this is seen in
cross-section in Fig. 221, c ; in S.fusiformis, this crest is abruptly truncated.
In S. pinnata and S. punctata, on the contrary, such a crest is wanting.
436 TUNICATA.
We have seen that the placenta is formed from the lower parts of
the primary hrood-sac, the upper halves of the outer and inner
lamellae taking no part in it (Figs. 217 and 218). We are still quite
in the dark as to the future fate of these latter parts, which cover
the embryo like a cap. According to Barrois (No. 87) and Todaro
(No. 110), they are cast off and disintegrate.
According to Salensky, on the contrary, they are retained by the embryo,
becoming closely connected with it and participating in its formation. That
part of the outer lamella (Fig. 217, e!) of the primary brood-sac, derived from
the maternal atrial wall, which is not concerned in the formation of the
placental membrane, is said to yield the ectoderm of the embryo (Fig. 218, ec),*
and the upper half of the outer lamella, which consists of flat cells, has there-
fore been called by Salensky the ectoderm-germ. The inner lamella (Fig. 217,
fw), on the other hand, which can be traced back to the transformed epi-
thelium of the oviduct, is said to yield, together with those parts that are not
used up for forming the roof of the placenta, chiefly the mesoderm-tissue of
the embryo (Fig. 218) ; the enteric rudiments, however, are also said to
originate in this layer. We must admit that we feel sceptical as to these state-
ments. According to them, the embryo results from separate rudiments derived
from various parts of the body of the parent. The epithelium of the atrial cavity
of the latter would yield the ectoderm, the oviduct, a part of the mesoderm
and the enteric rudiments, while the rest of the embryo would be derived
from immigrated follicle-cells (for, according to Salensky, the blastomeres
take no part in the building up of the embryo, p. 421). We are inclined to
think that errors of observation or of interpretation must here have crept in.
[See editorial notes, pp. 420-425].
At the stage when we should expect the development of the germ-
layers, + and the first rudiments of the organs, there is a considerable
gap in our knowledge. We, at least, have been unable, from the very
fragmentary statements of the stages that follow those described
above, to obtain any clear idea of these processes of development
which we desire to compare with the facts known in connection
with the ontogeny of the other Tunicates or that of other animals.
* [This layer, (e') the epithelial capsule of Brooks, is apparently only a
temporary protective membrane which disintegrates at a later stage. It takes
no part in the formation of the ectoderm, which is, on the contrary, derived
from the blastomeres (Brooks, Heider and Korotnefp). — Ed.]
t In connection with the formation of the germ-layers in the Salpidae,
special stress is to be laid on a " gastrula-stage " observed by Barrois (No. 87),
in which an invagination is found on the lower side of the embryo, that turned
towards the placenta.
[According to Brooks, the stage in Salpa corresponding to the gastrula of
the Ascidians is to be sought in a stage like that given in Fig. 217, the cavity
of the follicle, which becomes the body-cavity, being the cleavage-cavity,
and the blastopore coinciding with the attachment of the central mass of
blastomeres and follicle-cells to the inner layer of the brood-chamber. The
segmentation of the egg is much retarded, but the gastrula is planned out
in follicle-cells. This view is not accepted by other observers. — Ed.]
SALPIDAE — -FOKMS WITH COVERING FOLDS.
437
In the next stages we timl ourselves on firmer ground (Fig. 218 A),
the most important organs having already developed. This stage is
characterised by the appearance of a cavity which, from its relations
to the rudiments of organs (corresponding with those described for
S. democratica-mucronata), we may regard as the body-cavity. Into
this cavity, a club-shaped mass of cells, the early rudiments of the
organs, hangs down from the upper surface <>f the embryo. The peri-
cardial rudiment (/»•) is, however, distinguished by being further
attached at its lower end.
i
a
& m \
As
Fig. 218. T\\ itogeuetic stages of Salpa pinnata (after Sai.kxskv). A, diagram-
matic median section i>t a younger stage combined from various figures by Salensky i
/!. older stage, b, blastomeres ; bk, " blood-forming bud " ; bl, blood-spaces in the
placenta ; d, atrial cavity ; d, enteric rudimeut ; dp, rout' of the placenta ; ec, ecto-
derm ; i . covering fold ; h, rudiment of In-art ; k, .nill ; m, muscle-hoops ; mp,
placenta] membrane ; n, rudiment of the uervous system ; //. placenta ; /<<•. peri-
cardial rudiment : ph, pharyngeal cavity.
This cavity has been called by Salensky the secondary follicle-
cavity. Since, according to this author, only some of the rudiments
of the internal organs (the nervous system and the pericardial
rudiments) are formed from the inner cell-mass of the embryo, the
body-wall (together with the rudiment of the intestine) being
derived from the wall of the primary brood-sac ; this cavity has, for
Salensky, the same significance as the original cavity of the primary
brood-sac (Fig. 217,/). The latter, which is called by Salensky
the primary follicle-cavity, is said completely to disappear in those
obscure stages which lead up to the stage now being considered, and
438
TTJNICATA.
A
to be replaced by a secondary follicle-cavity that appears in the same
place.*
The body-cavity (Salensky's secondary follicle-cavity) separates
the rudiments of the organs laterally and ventrally from the body-
wall. In the latter we can now distinguish an external layer, the
ectoderm (Fig. 218 A, cc), from an inner layer, the cells of which
wander into the body-cavity, filling it with a mesenchyme. We are
consequently enabled to recognise in this inner layer a part of the
mesoderm-rudiment.
If, in order to obtain a correct idea of the relative positions of the
organ-rudiments, we
examine horizontal
sections (Fig. 219), we
find in them a remark •
able cruciform figure,
the enteric rudiment
(d) forming the trans-
verse portion of the
cross, while the neural
rudiment (■«,) and the
pericardial rudiment
(pc) form the longi-
tudinal portion. It
is characteristic of
the Salps now under
consideration that the
enteric rudiment (d)
originally appears to
develop chiefly in a
transverse direction.
At the same time, it
is evident that the
first parts of the
enteric rudiment
(pharynx) to develop
are its future lateral
portions so that there
Fig. 219. — Horizontal sections through two embryos oi'
Salpa pinnata, made in the direction of the line a-a
in Fig. 218 .1 (after Sai.exsky). b, the blastomeres ;
d, enteric rudiment ; (/,', layer covering the intestine ;
ec, ectoderm ; n, middle part, n,', lateral parts of the
nerve-rudiment ; j>, lateral parts of the placenta : /»•.
pericardial rudiment; ///, l>looil-ca\ ities of the placenta.
* [Brooks considers that this second cavity is probably the original cavity
of the follicle opened a second time by the growth of the surrounding parts.
He would thus derive the body-cavity in Salpa from the primary follicular
cavity, the latter he believes to represent the cleavage-cavity of the Ascidiacea.
—Ed.]
SALPIDAE — F01JMS WITH COVERING FOLDS.
439
is at first a paired rudiment of the pharynx only slightly connected
in the median line. According to Salensky, the first recognisable
rudiments of this system of organs are found as two entirely distinct
accumulations of cells derived from the wall of the primary brood-sac
(wall of the follicle).* In a similar way, in S. dernocratica-mucronata
also, the rudiment of the pharynx develops in the form of paired
cavities (p. -426). Two layers may be distinguished in the enteric
rudiment ; an inner layer consisting of deep cylindrical cells (ento-
derm) and an external layer, the so-called covering layer of the
intestine () can still be recognised and which may perhaps be
considered as belonging to the mesoderm.
In horizontal sections the rudiment of the nervous system has at
first a curious trilobate form (Fig. 219 J), but this is less marked in
later stages. Todako (No. 107) has given to the two paired lobes
(?(,') the name of the dorsal disc,
and regards them as belonging to
the mesoderm. He considers them
to be provisional and homologous
to the chorda. The pericardial
rudiment (/><■) is distinguished by
the regular arrangement of the
blastomeres found in it, two columns
of the latter in which the cells are
arranged in pairs running through
it. Both the pericardial rudiment
and the neural rudiment project
slightly at their upper ends above
the surface of the embryo (peri-
cardial and neural projections, Fig.
220, n ) ; in later stages a dorsal
Longitudinal furrow runs between
them, but as to the significance of
these structures we are still in the
dark.
In these stages the embryo lies like a flat disc on the placenta (Fig.
218 A). Only its upper surface appears covered by the cap-like
ectoderm-layer (Fig. 221, ec). It is not clear in what way the basal
* [See footnote, p. 42G. The above account of the origin of the pharynx
appears to be quite inaccurate. In all probability the cavity described by
Salensky was the atrial cavity, but even that structure is not derived from
the wall of the follicle but from the ectodermal blastomeres. — Ed.]
■*♦!'*
»
& »"
KTV'W
mm
PlG. '220. — Horizontal section through
an embryo of Salpa pinnate (after
Salensky). d, the two atrial diverti-
cula of the enteric rudiment (gill-slits
of Brooks) ; /.-, rudiment of gill ;
//. neural rudiment : n', so-called
neural projection ; v, cells within the
lumen of the intestine (invaginateil
somatic layer of the follicle, Brooks).
440
TUNICATA.
boundary between the embryo and the placenta arises. In the stage
now being considered the body-cavity seems to be separated from the
placental cavity only by the lamella which was mentioned above as
the roof of the placenta (dp), but we do not know to what extent this
lamella participates in the formation of the embryo.
Further development leads to the complete disappearance of the
primary body-cavity which becomes filled in the way mentioned above
by a mesenchyme (Fig. 222, wis), the elements of which give origin
not only to the connective tissue but also to the blood-corpuscles, the
Fig. 221. — Transverse section through an embryo of Salpa africana-maxwia (after
Salenskt). a, epithelium of the respirators cavity of the parent; bk, ''blood-
hud " ; c, crest of the covering fold ; ec, ectoderm of the embryo ; ./', covering fold
(embryo-sac) ; k, paired fold-like rudiment of the gill ; p, upper cavity between the
placenta and the embryo; p', actual placental cavity.
body-musculature and the elaeoblast. As the embryo grows further
a marked increase in length takes place, and it thus approaches the
adult form, whereas at first its transverse diameter was greater than
its longitudinal diameter (cf. Fig. 21 S /> with Fig. 224). This change
in shape is specially connected with the change both in shape and
relation of the pharyngeal cavity. This rudiment, which may be
considered as consisting of two sacs connected by a narrow transverse
SALPIDAE — FORMS WITH COVERING FOLDS.
441
bridge, first elongates. Tin- tral>ecula, which is retained between
the two diverticula of the developing respiratory cavity (Figs. 220, d,
aiul 222, cl) that run upward, represents the rudiment of the gill (k)
which, when the diverticula unite over it, becomes detached from the
dorsal wall of the respiratory cavity.*
Fig. 222. — Median section through a later ontogenetic stage of Salpa pinnata (after
Salbnsky). <•/. atrial diverticulum of the enteric rudiment ; d, enteric rudiment
(rudiment of the respiratory cavity); ec, ectoderm; f, ciliated pit ; h, rudiment of
heart : ms, mesenchyme; it, ganglion ; pc, pericardium; />/. tissue of the placenta.
The part of the respiratory cavity which is to he regarded as t he
cloacal cavity is not, consequently, according to Salensky, derived
from an independent rudiment, but arises through the formation of
diverticula from the rudiment of the pharyngeal cavity. Todaro
:;'[The recent observations of Brooks, Heider and Korotneff are so abso-
lutely antagonistic to those of Sai.knskv. that we must now regard the above
account of the origin of the pharyngeal and atrial cavities and of the gill as
inaccurate. Eeidsr and Korotneff are fairly in agreement, and together
ilie\ differ in some important points from Brooks. All three are, however,
agreed that the atrium develops first, and is probably ectodermal in origin.
The pharynx, on the other hand, appears as a cleft in the embryonic mass
which becomes lined with entodermal blastomeres. The gill arises from the
septum between these two cavities by the breaking down of the lateral parts
of this septum, the clefts thus formed being the gill-slits. Salhnsky's view
that the gill and atrium oi Salpa arc not homologous with the similarly named
structures in the other Tunicates may be regarded as disproveh. — Ed.]
442 TUNICATA.
(No. 113), on the contrary, states that, in Salpa, the cloaeal cavity is
derived independently from the ectoderm, two ectodermal invagina-
tions that develop one after the other taking part in its formation.
An ectodermal growth first develops on the dorsal side, behind the
cerebral vesicle, and this then becomes hollow and forms a vesicle
which is the rudiment of the primary cloaeal vesicle. This vesicle
becomes applied laterally to the epithelium of the respiratory cavity
(pharyngeal cavity), but remains separated from the latter medianly
by a mass of mesenchyme. The median part becomes the future gill,
and in the lateral part, at a later stage, the two large gill-clefts break
through. Only after the gill is completely developed does a second
ectodermal invagination appear and bring about the communication
of the cloaeal vesicle with the exterior (<■/. the development of the
cloaeal cavity in S. democratica, p. 426).*
According to Salensky, the development of the gills varies considerably in
the different species of the Salpidae. In ,S'. africana and S.fusiformis the gill
develops through a median fusion of two horizontal folds which rise from
the lateral walls of the respiratory cavity (Fig. 221, A).t The figure of .S'.
africana; in which this is depicted, serves at the same time to illustrate some
other peculiarities occurring in this species. We see the upright crest (c) of
the covering fold (p. 435) in cross-section, and may observe that the connection
of the embryo with the placenta is here brought about in a manner different
from that in S. pi/rmata, a large cavity (p) here being intercalated between the
embryonic rudiment and the roof of the placenta. The origin and significance
of this cavity are, however, still somewhat obscure.
According to Salensky, the rudiment of the pharyngeal cavity is not closed
completely, but, at a certain stage, shows a dorsal aperture through which a
considerable number of mesenchyme-cells wander into the respiratory cavity
[probably entodermal blastomeres]. These partly fill the latter and become
applied to the wall of the intestine from within ; later, however, they disin-
tegrate and are absorbed (Fig. 220, z).
The development of the actual enteric canal (as an outgrowth of
the pharyngeal cavity), that of the endostyle, and of the oral and
atrial apertures, seem to take place here in the same way as in
& democratica-mucronata (p. 430).
The rudiment of the nervous system (Fig. 2 IS, u), which arises, as
we have seen (p. 439), as a trilobed cell-strand (Fig. 219 A, u, n'), now
* [Todaro's account, in its most essential features, is in accord with that of.
Brooks. — Ed.]
t [Korotnepf (No. XXIa.) supports Salensky in his account of the origin
of the gill in S. africana-maxima. — Ed.]
SALPIDAE— FORMS WITH COVERING FOLDS.
I i:i
begins to assume a simpler form (Fig. 210 B, ») ; at still ater stages
it is found as a cell-mass running obliquely downwards and forwards;
within tins mass a cavity appears which communicates anteriorly with
the respirator; cavity ( Fig. 222). The part lying nearest to the aper-
,,„,. of the central canal represents the rudiment of the ciliated pH
( f) while the blind end that is directed backward and upward forms
the ganglion proper (»). In the course of development these two-
sections of the neural rudiment become more sharply marked oft from
one another by a constriction. At the same time, in the ganglionic
part of the rudiment, the central canal becomes segmented, breaking
up into three consecutive cerebral vesicles, a condition first noticed
by Kowalevsky, and similar to that
seen in S. democratica (p. 429). In
later stages the cerebral rudiment
becomes completely separated from
the ciliated pit, and the two rudi-
ments shift apart, although they seem
still to remain connected by a nerve-
strand that runs forward from the
brain to the ciliated pit. The central
cavity of the cerebral rudiment disap-
pears, and the interior of the rudiment
then seems rilled with punctate nervous
tissue (Leydig's " Punktsubstanz ").
A process running towards the surface
leads to the development of the eyes,
in which single cells of the ganglion
become changed into elements sensi-
tive to light, while other cells of the
most superficial layer become tilled
with pigment (p. 430). No details
are known of the development of the
paired auditory vesicles which lie in
contact with the brain, and were first
observed by H. Mullek and further described by Todako (No.
107). The ciliated pit, by the folding of its walls, assumes a com-
plicated form approaching that of the same organ in the adult (Fig.
214,5,/). .
The pericardial rudiment (Figs. 2 IS, 219 pc), which is originally
a cell-strand running from above downward, divides into two parallel
strands (Figs. 223, 224 A) ; the anterior strand, near the enteric
Fig. 223. — Horizontal section
through an embryo of Salpa
pinnata (after Salensky). b,
blastomeres ; \ means of division,
may even be connected with this regeneration. The yellow body then
becomes lobate, and divides into several parts, each of which develops
into a new Ascidian. The details of these interesting processes are,
however, still unknown.
The occurrence of such far-reaching regenerative processes and the
capacity for asexual reproduction in the Tunicata at first sight seems
surprising, when we take into account their comparatively complicated
organisation and their near relationship to the Vertebrata. W e must,
however, remember that the same capacity is found in the Annelida
and the Echinoderma, groups which, in the condition of their
organisation, may at least be compared with the Tunicata.
1. Social and Composite Ascidians.
The asexual reproduction winch takes place in these groups is
usually called budding. In the Polyclinidae, however, asexual
multiplication takes place through the segmentation of the post-
abdomen. This kind of reproduction, therefore, must, strictly
speaking, be defined as transverse fission, and must be considered
as distinct from budding.
A. Reproduction through Transverse Fission.
This is the kind of multiplication which was defined by Giard
(Xo. "'7) as " bourgeonnement ovarien" and which has become better
known through the researches of Kowalevsky (No. 61) in connection
with Amaroucium prolifemtm.
[Since this description was published, further investigation of the budding
processes in the composite and tbe social Ascidians has shown us that, while
the account given in tbe following pages is correct in so far as it derives all
the important internal organs from the inner sac, yet it obscures the actual
state of affairs by always speaking of this structure as entodermal. While it
is probably true that this inner sac is derived from the entoderm in most cases,
pel in one group, the Botryllidae, if the observations of Hjoht (No. XIV.) and
Pizon (No. XXVI.) are correct, this does not appear to be the case. These
observers find that the stolon is purely ectodermal, the epicardia arising from
the peribranchial sacs of the parent which, in the first instance, i.e., in the
larva, are of ectodermal origin. From this ectodermal epicardium, the bud
arises much in the way described above. Tims we find that, in one family, all
the organs of the bud are of ectodermal origin, while, in the majority, they
arise from the entoderm. — Ed.]
GG
450
TUNICATA.
In the Mediterranean the larvae of Amaroucium hatch ont in
winter (Maurice and Schulgin, No. 39). After becoming attached,
they multiply by transverse fission, and throughout the whole summer
produce a succession of generations exclusively asexually, and in this
way the colony grows. Towards the beginning of winter the youngest
zooids cease to reproduce in this manner and develop sexual organs.
The older asexual individuals of the colony die off, and their dis-
integrated remains are, according to Maurice's observations on
Fragaroides (No. 40), taken in and digested by the mantle-cells
which function as phagocytes (p. 356).
Kowalevsky investigated the asexual reproduction that takes place
in the primary individuals of the
colony which result from the larva.
He found in them (Fig. 'I'll A) three
body-regions; thorax (a), abdomen
{!>) and post-abdomen (c). The post-
abdomen is the elongated posterior
region of the body in which the
genital organs develop in the herma-
phrodite individual (hence the term
" bourgeonnement ovarieu"). In a
cross-section (Fig. 225) through the
post-abdomen of an individual about
to commence multiplying asexually,
beneath the ectoderm, longitudinal
muscle-bundles {>n) are- seen em-
bedded in an extensive layer of
mesoderm-cells
Fig. 225. - Transverse section
through the post-abdomen of
Amaroucium (after Kowalevsky).
/), upper. V, lower blood-sinus ;
ec, ectoderm ; m, muscle-fibres in
transverse section ; ms, mesoderm-
cells ; s, partition-wall (epicardial
sac).
(»i.s),
seeming to be filled with
these latter
reserve
nutritive material. The primary body-cavity (b, b') which is con-
tinued upward into the thoi'ax and the abdomen, appears divided by
a transverse partition- wall (.s) into a doi'sal half {b) and a ventral half
(//). The partition-wall itself is hollow, and is nothing more than a
flat diverticulum of the branchial sac arising from the latter immedi-
ately behind the posterior end of the endostyle, between it and the
entrance of the oesophagus, which runs back through the whole of the
post-abdomen and ends blindly near its posterior end. Here lies the
heart (Fig. 227 A, li) curved into a crescent round the posterior end <>!"
the entodermal process just mentioned. This entodermal diverticulum
is identical with the tube in Clavelina called by van Beneden and
•Tulin (No. 1<>) the epicardial tube (see Fig. 173 C, ep, p. 375). It
ASCII)! U'KA TRAXSYKKSK FISSION.
\r>\
<■—
is also evidently tin- homologue of the entodermal or endostyle-process
in the proliferating- stolon of the Salpidae and Pyrosoma, but the rela-
tive position of the heart distinguishes this so-called epicardial tube
in the Polyclinidau. from
the similar tube in the
above-mentioned forms*
T he ti ner ana torn ical
features of this tube have
been described by Mat-
rice (No. 40) in Fraga-
roides. The tube forks at
its anterior end; the two
prongs of this fork have
been distinguished by van
Bexedex and Julix as
epicardial tubes from the
posterior undivided epi-
cardial sae (see above, p.
370). The two epicardial
tubes arise on either side
of the median line behind
the posterior end of the
endostyle from the pharynx. The posterior end of the sac is, according
to Maurice, also forked (Fig. 226 A and D, ep). It embraces the
crescent-shaped pericardial vesicle (p). In Clavelina, the epicardial
tube enters into close relation to the heart (p. 370), completing
the dorsal wall of that organ, but this is not the case, according to
Maurice, in the Polyclinidae. The heart-tube (h) in these latter is
an invagination of the outer wall of the U-shaped pericardial vesicle
(Fig. 226 C and D).
It should be mentioned that the paired apertures of the two epicardial tubes
can be recognised only in larvae and in .quite young asexually-produced
individuals. They could not be found by Kowalevsky in the adult zooid,
and M SlURICE also has recently stated that the two epicardial tubes, although
bhey approach close to the wall of the branchial sac, seem no longer to com-
municate with its cavity.
The epicardial sac in the Polyclinidae divides the body-cavity into
a dorsal and a ventral half (Fig. 225, I>, //). Through each of these
halves a blood-stream Hows, but, in the dorsal half, the direction of
the stream is opposed to that in the ventral half, the blood flowing
in the one half towards the heart and in the other from the heart to
Fig. 226. — Diagrams illustrating the condition of
the posterior end of the post-abdomen in Fraga-
rcides (after Maurice). A, side view ; /}, trans-
verse section at the level ah ; C, at the level c-d ;
h, at the level e-f. ep, epicardial sac ; h, heart ;
/i, pericardial sac : x, forked end of the epi-
cardial sac.
452 TUNICATA.
the body. Similar conditions are found in the proliferating stolon of
other Tunicates (e.g., Clavelina, p. 370). In this form also, in the
stolon, a dorsal blood-current is separated from a ventral current
flowing in the opposite direction by the epicardial sac which forms a
partition extending almost to the end of the stolon (Fig. 229, ./•). A
transverse section through the proliferating stolon of Clavelina shows,
on the whole, remarkable agreement with one through the post-
abdomen of the Polyclinidae, though important variation is found in
the position of the heart. In the Polyclinidae, the heart lies at the
posterior distal end of the post-abdomen (Figs. 226 and 227), which,
consequently, contains important organs belonging to the organisa-
tion of the parent (the heart and the genital organs). In Clavelina,
the pericardial vesicle and the heart have shifted to the point of
origin of the stolon (Fig. 173 C, p. 375). The heart lies at the
proximal end of the epicardial sac, on the ventral side of the latter,
so that the epicardial lamella, as shown above (p. 370), can be utilised
in the formation of the dorsal wall of the heart. The proliferating
stolon of Clavelina does not contain any important organ of the
parent body, but is a process of the body dedicated exclusively to a
sexual reproduction. The same is the case with the stolon of other
Tunicates (Thaliacea and Pyrosoma, etc.). We might imagine the pro-
liferating stolon as derived from the post-abdomen of the Polyclinidae,
if we chose to assume that the genital organs and the heart withdrew
to the proximal end of the post-abdomen, which then became dedicated
exclusively to the function of reproduction. Such an assumption
would satisfactorily explain the remarkable divergence in the position
of the heart above alluded to. While, in Clavelina, the heart lies on
the ventral side of the epicardial sac, in Pyrosoma it is found on the
dorsal side of the so-called endostyle-process (Fig. 253, hz, p. 485).
If, then, we assume that in these two groups the heart originally lay,
as in the Polyclinidae, at the distal end of the stolon, it is not difficult
to imagine that secondary shifting took place, in the Clavelina to the
ventral and in Pyrosomu to the dorsal side.
The ontogeny of the Pyrosoma would, indeed, rather lead us to consider
the change of position of the heart as the consequence of lateral shifting of
the oi-gans. The heart there lies originally on the right side of the entoderm-
process, and only later shifts to the dorsal side (Seeliger) ; cf. p. 493.
It is evident from the above that the asexual reproduction of the
Polyclinidae (through the segmentation of the post-abdomen) and
the stolonic budding found, for instance, in Clavelina, are related one
to the other. Giard (No. 57) has already pointed out that the
ASCIDIACEA — TRANSVERSE FISSION.
153
elongated, branched post-abdomen of many Polyclinidae (e.g., Circin-
alium), part of which creeps horizontally along the substratum, is
remarkably like the stolon of Glavelina. These two methods of
reproduction are thus connected with each other by transitional
forms.
Fig. 227. — A, young Amaroucmm before the commencement of asexual reproduction ;
/.'. Amtti-iinriiim with segmented post-abdomen (after Kowalevsky). h. thorax;
b, abdomen; c, post-abdomen; h, heart; s, partition-wall; s', anterior part of the
partition-wall ; .<•, //, separated portions of the post-abdomen : /.-. anterior swollen
end of the partition-wall in the posterior separated portion.
The commencement of asexual reproduction in the post-abdomen
of Amaroucium is marked by its elongation and the abstraction of
its soft part from the point of attachment to the rest of the body.
The heart continues to heat after the separation of the post -abdomen
from the abdomen is accomplished. Soon after, the post-abdomen
(Fig. 227 /!) breaks up, through transverse fission, into a varying
454
TUNIC ATA.
number of parts, each of which develops into a young Ascidian.
The first sign of development is shown in a widening of the proximal
end (K) of the ectoderm-tube (segment of the epicardial sac) which
lies in every segment. This proximal dilation is the rudiment of
the whole alimentary canal of the young animal. The non-dilated
part of the entoderm-tube becomes the epicardial tube of the ycung
individual. The heart of the parent-animal that has remained in
the distal segment now degenerates. Somewhat older colonies
(Fig. 228) are of a different shape. The young animals, which
originally lay in a row one behind the other, show a tendency to
Fig. 228. — Two young colonies of Amuroucium (alter Kowalevsky). .).
B, older stage. ". parent-animal ; b, an advanced bud ; c, younger buds.
shift upward within the test towards the parent-individual, and the
whole colony thus becomes broader and shorter. The parent-indi-
vidual now begins to develop, through regeneration, a new heart
and post-abdomen (Fig. 228 .1, a)'. The daughter-individuals in the
figure seem to be at different stages of development. < hie of them
(6) exhibits the almost perfect organisation of the adult Ascidian,
while the three others show the rudiments of the different parts of
the body, but these are very slightly developed. In all these young
individuals the post-abdomen is still comparatively short. 'hily
later (Fig. 228 B) does it grow out to a greater length, and come
\S( IDIACEA — STOLONIC GEMMATION.
l.M
to resemble more and more the post-abdomen of the parent before
the commencement of asexual multiplication. The anterior part of
the body of the young individual lias shifted upward. The branchial
and atrial apertures have broken through, and reproduction by means
of tranverse fission now takes place in the daughter-individuals that
have arisen as described above.
We thus find, in this case, the first rudiments of the young animal
in the portion of the post-abdomen, which becomes separated by
transverse constriction, and which, through processes of regeneration,
is able to develop into a perfect new individual. For details of these
processes, see p. 470.
Whether, in the segmentation of the post-abdomen in the Polyclinidae, we
actually have a more primitive form of asexual multiplication, from which
the stolonic gemmation of other Tunicates is to be derived, must still be
regarded as doubtful. It is also possible that the transverse division of the
Polyclinidae is to be derived from stolonic budding. A comparison with the
conditions of development of Pyrosom i shows that caution must be exercised
in such speculations. At first sight we should feel inclined to describe the
rise of the first four Ascidiozooids in the Pyrosoma embryo as transverse
fission (Fig. 193, p. 397), but more careful examination reveals the fact that
the later longitudinal axis of the Ascidiozooid is at right angles to that of the
proliferating stolon. We have, consequently, to regard the rise of these first
Ascidiozooids also as stolonic budding, which is not essentially distinguished
from the budding of the zooids that are produced later (see pp. 404 and 484).
B. Stolonic Gemmation.
The typical form of stolonic gemination is found in the so-called
social Ascidians, in Clavelina and Perophora. The single individuals
here send out a creeping proliferating stolon which branches re-
peatedly (Fig. 229), and at the end of which the buds appear as
club-shaped swellings. In structure the stolon closely resembles the
post-abdomen of the Polyclinidae. Here also we find, as has already
been shown, the blood-space of the stolon (primary body-cavity)
divided by the extension of the epicardial sac (stolonic septum, s)
into a dorsal and a ventral half, the blood circulating through these
in opposite directions. Since the partition-wall does not reach quite
to the distal end of the stolon (x) the two sinuses communicate at
this point, where also the stream of blood changes from the one
direction into the other.
The buds here originally appear in the form of bilaminate vesicles
\kn). The outer layer of the vesicle, the ectoderm of the bud, is
continuous with the ectoderm of the stolon and of the parent-
456
TUNICATA.
individual. The inner layer, the entoderm, arises as was first proved
by Kowalevsky (No. 60) for Perophora, as a diverticulum of the
stolonic septum (epicardial sac) with which it long remains connected.
Between the ectoderm and the entoderm, the primary body-cavity
of the bud appears filled with
mesenchyme - cells. We shall
presently, following the accounts
of Kowalevsky (Xos. 60 and
61), Seeliger (No. 66), and
van Beneden and Julin (No.
10), describe more in detail the
further development of the bud.
We can here merely mention
that, in Clavelina, the connection
of the bud with the stolon, and
through the latter with the other
individuals of the colony, is
usually retained even in the adult.
Not all the root-like processes of
Clavelina seem to be capable of pro-
ducing buds. Many of the ramifica-
tions seem intended merely for attach-
ment or to serve as reservoirs of blood
(Seeliger). The latter then have
no epicardial process extending into
them. A sharp distinction must be
made between these sterile body-
processes, which may be compared
with the mantle-vessels, and the
ramifications of the actual prolifer-
ating stolon.
Among the Composite Ascidians
the family of the Distomidae
belongs to the type just described,
the entoderm-vesicle of the bud
here also becoming abstricted
from a process at the posterior end
of the endostyle. In the Botryllidae, the Did&mnidae, and the
Diplosomidae, on the contrary, budding of another type occurs.
The family of the Distomidae seems to be distinguished by the fact
that its buds separate very early from the proliferating stolon. They
are then found within the common cellulose mantle scattered between
Fig. 229. — Portion of a proliferating
stolon oiPerophora (after Kowalevsky).
ec, ectoderm of the bud ; en, entoderm
of the bud ; hn, buds ; s, stolonic
septum (epicardial lamella) ; v, ramifica-
tion of the stolon.
ASCIDIACEA — STOLONIC GEMMATION.
457
the separate individuals as small, rounded bodies, each provided with
a cavity. In individual cases a longer proliferating stolon seems to
occur, as in the stalked colony of Colella pedtmculata, in which
Hkrdman found that each individual gave off into the common stalk
a body-process (evidently the proliferating stolon). On this, then,
the young buds arise and detach themselves, shifting upward in the
common mantle-substance in proportion as they develop further. In
another form belonging to this group, described by Kowalevsky.
as Diili in n a in styliferum, but which, according to Della Valle
(No. 68), belongs to the genus Distaplia, the small buds which early
become independent, arise, as Kowalevsky conjectured, on a process
Fig. 230. Free-swimming larva of Distaplia (after Della Valle). cl, atrial cavity ;
• . atrial aperture ; <«, endostyle ; hut Della Valle believes that the latter are perhaps
derived direct from the genital rudiments of the parent.
At the same time, the thoracic bud (Fig. 232 A, k') also develops
fully (Fig. 232, 11). We cannot here enter in detail into the some-
* [The genus Trididemnum is included by Herdman in the genus Didemnum
Savigny. — Ed.]
BUDDING OF THE DIDEMNIDAE AND THE DIPLOSOMIDAE.
4(il
what unsatisfactory statements of authors as to the way in which the
organs develop in this bud, but may mention thai peribranchial sacs
develop at the sides of the central enteric cavity, that gill-clefts break
through, ami that the ganglion, and the branchial and atrial apertures,
appear as rudiments. An oesophageal tube and a short rectum seem
also to appear. The former (Fig. l'-""'-' />, . rudiment of the
intestine in the bud k ; V, the same rudiment in the bud k' ; i. intestine of the parent-
individual ; /■. abdominal bud; /•'. thoracic bud; m, stomach; oe, oesophagus; x,
constricting ectoderm-ring.
thoracic bud (©') entering the rectum of the parent (7) at the point
at which the rectum of the abdominal bud (b) joins it. If, now, the
oesophagus of the thoracic bud became more closely connected with
that of the abdominal bud, and such connection were also to be
established between the intestines of the two buds, the two halves of
the daughter organism would then at last be united. But although
the alimentary canal of the bud is now completed, it still, for a long-
period, remains connected with that of the parent, both in the
oesophageal region and through the rectum (Fig. 233).*
* [For further details concerning the development of the complex buds of
the Diplosomidae and Didemnidae, see the recent works of Caulery (Nos. V.-
VII.) and Salensky (Nh. XXIX. i. Callery finds epicardial tubes in the
adults, and from these he derives the thoracic and abdominal buds. — Ed.]
462
TUNICATA.
The thoracic and the abdominal buds do not always develop equally.
In some cases only the abdominal bud develops. This leads to an
abnormality, consisting of one
branchial region with two fully
developed intestinal loops (Fig.
234 B). In such cases the intestine
of the parent may degenerate later.
This condition is regarded by Della
Valle as a rejuvenescence, and
consists in the development of an
individual, the anterior half of which
belongs to the parent, while its
posterior half develops anew (see
also Oka, No. 646). A similar
process may occur in the anterior
part of the body, when the thoracic
bud alone develops (Fig. 234 A).
The process is often still further
complicated by the appearance of
the bud-rudiments of a third genera-
tion arising from the not yet fully
developed bud. In this way
le various halves of the body are
Fin. 233. —Late stage in tlie budding
of Tridide?nnu>n(a,fter Della Valle).
The alimentary canal of the perfectly
developed bud still remains connected
with that of the parent, e, atrial
aperture; en, endostyle; i, branchial
aperture; in, stomach; n, ganglion;
lie, oesophagus ; r, rectum.
remarkable
produced.
combinations of tl
Pig. 234. — Abnormal forms resulting from the development of one hajf of the bud in
Trididemnum (alter Della Valle, simplified). A, two branchial regions connected
with one intestinal Loop; H. two intestinal loops connected with one branchial
region, e, atrial aperture; en, endostyle; i, branchial aperture; m, stomach; n,
ganglion ; oe, oesophagus; r, rectum.
ASCIDIACEA — FORMATION OK ORGANS IN THE HUD. 463
In the Diplosomidae the process of budding and bhe formation of double
individuals begins even in bhe free-swimming larva, but in the Didemnidae
this is not the case.
But for the statements made 1>\ JOURDAIN we might be tempted to derive
the remarkable budding processes in these two families from a primitive
longitudinal fission of the parent.
E. Development of the Organs in Asexually Produced
Individuals.
The development of the inner parts of the bud has been described
by Metschnikoff (No. 41), Ganin (No. 55), Kowalevsky (Nos. 60
and 61), Giard (Xo. 57), Della Valle (No. 68), Seeliger (Nos.
66 and XXXIV.), van Beneden and Julin (Nos. 10 and XVII.),
H.iort ( Nos. 59 and XVI. ), Oka (No. 64«), and in the still more recent
works of Caulery (Xo. IV.), Lefrvre (Xo. XXII.), and Ritter
(No. XXVIII.). In our account of these processes we have followed
Kowalevsky, whose careful researches have been confirmed with re-
gard to the development of the nervous system and the pericardial
vesicle by van Beneden and Julin.
The bud is at first a hollow body consisting of two or three layers
(Fig. 229, kn). The outer layer is the ectoderm (ec) which is in
continuous connection with the ectoderm of the stolon. The inner
layer, the entoderm (en), encloses the primary enteric cavity of the
bud, which, in Clavelina and the Distomidae, originated as a diverti-
culum of the epicardial sac (entodermal stolonic septum, " cloison ").*
The connection between the entoderm-vesicle of the bud and the
epicardial sac is retained in the social Ascidians (Chivelitw and Pero-
phora) for a very long time, often throughout life. According to
van Beneden and Julin, the stalk-like portion which connects the
hud with the stolonic septum represents the rudiment of the epicardial
sac and of the pericardial vesicle of the budding individual. The
primary body-cavity extends between the ectoderm and the entoderm
of the bud : into it mesoderm-elements soon immigrate, and these are
the first rudiment of the mesoderm of the bud. In many cases
(especially in the buds of the Distomidae and the Botryllidae) the
* [In Perophora, according to Rittbb (No. XXVIII.) and Lefevre (No.
XXIII.), the developing blastozooid (bud) is connected with the stolonic
septum, not by its branchial sac but by the left peribronchial sac. Hitter
expresses some doubt concerning the origin of the pericardium ; he thinks
that it arises from the inner vesicle, but even if it is produced by the aggrega-
tion of mesenchyme-cells, as Lefevre states, it is skill probable that its
ultimate source is the entoderm, since the mesenchyme-cells are probably
produced from that layer. — Ed.]
464
TUNICATA.
genital rudiments can also be distinguished at an unusually early
stage.* The above is the case in the buds of Distaplia (Kowa-
levsky's Didemniwm styliferum), which, as free bodies detached from
the stolon, are found scattered in the cellulose substance of the colony.
In the genital strand (Fig. 235, g) of the youngest of these bads,
several young egg-cells can always be recognised. These buds,
however, are capable of multiplying by fission (Fig. 235 B), and in
this case the eggs become distributed so that one occurs in each
portion of the original bud. Kowalevsky is, therefore, inclined to
regard the buds which form first as stolons which have separated
.— £C
■au
/-
Fig. 235. — A, younger, B, older stage of development of Distaplia stylifera (after
Kowalbvskt). In B, the bud is dividing into two. ec, ectoderm ; en, entoderm ;
g, genital strand ; ms, mesoderm.
from the Ascidiozooids, the parts resulting from fission alone repre-
senting the true buds, and Lahille has recently adopted this view.
The entoderm-sac is the seat of the most important transformations
through which the bud develops into the young Ascidian. This sac
increases in size and its anterior margin becomes trilobed (Fig. 236).
The middle lobe must be regarded as the rudiment of the branchial
sac (pharynx), while the two lateral parts represent the rudiments of
the peribranchial sacs. These sacs are, therefore, in the bud of
Distaplia, distinctly entodermal in their origin.
The peribranchial sacs grow round the sides of the middle ves-
icle and, at the same time, a process grows from each sac towards
* [In the Didemnidae (Pizon, No. XXVTa.) the sexual cord is continued
from the parent into the bud. — Ed.]
ASCIDIACEA FORMATION OF ORGANS IN THE BUD.
465
the dorsal middle line (Fig. 236 B, p). These processes grow
towards each other and fuse, and thus the single atrial cavity arises
(Fig. 237, <•/). In the meantime the two peribranchial sacs have
become completely disconnected from the central cavity.
The peribranchial sacs arise in a slightly different manner in Perqphora
(Kowalevsky, Ritter), in which form, instead of separating as two distinct
sacs and fusing together at a later period, a single bilobed sac separates from
the inner vesicle ; thus the definitive atrial cavity is formed at an earlier
period, the development being apparently abbreviated. Seeliger also states
that, in Clavelina, an unpaired vesicle becomes abstricted from the dorsal side
,71
V*
Fig. "236. — Two stages in the development of the buds of Distaplia stylifera (after
Kowai.kvskv). .1. younger. /!. older stage. d. alimentary canal; dr, digestive
gland ; ,/'. rudiment of the stolon ; .s%js (SfC£A ■
(^S^kSrewM
v>K) .Slip
--ft \
1 ^^'^'-^.^v/Rrtvi
Fig. 239. — Three consecutive ontogenetic stages in the so-called bud of Ama/rcmcium
(after Kowalevsky). A, dorsal view of the anterior part of the body ; B, side view
of an older stage ; C, dorsal view of a still more advanced stage, d, enteric rudi-
ment ; ec, ectoderm; en, entoderm; ej>, epicardial process; », rudiment of the
nervous system ; p, peribranchial sac.
Important observations on the condition of the pericardial vesicle
and the epicardial tube have been made by van Beneden and Julin.
Following these authors, we shall first describe the condition of a
more fully developed bud traced in a series of cross-sections. The
last section of this series (Fig. 238 F) passes through the base of the
U-shaped intestinal loop (i) and, ventral to this, the stolonic septum
(st) is seen. In anterior sections, we rind that the latter is in direct
connection with the pericardial vesicle (Fig. 238 D, pc). The heart
(h) here also has arisen through the invagination of the wall of the
pericardial sac (pc). A section cut further forward (Fig. 238 D)
shows the double or forked end of the epicardial sac (ep) of the bud,
in close contact with the pericardial vesicle. Further forward, the
pericardial vesicle decreases in size (Fig. 238 C, pc) and finally
\S( 1DIACEA FORMATION OF ORGANS IN THE BUD.
469
*J
disappears (Fig. 238 A'), while the epicardial sue (ep) can be followed
forward to the point at which its wide paired aperture (Fig. 238 A)
enters the pharynx (branchial
sac). In other words, the epi- _ '
cardial sac arises from paired
apertures situated ventrallv to
the entrance of the oesophagus
and extends backward, its forked,
blind end becoming applied to
the pericardia] vesicle. The
latter is continued direct into
the stolonic septum. At an
earlier stage, the forked end of
the epicardium is found to be
continuous with the wall of the
pericardial vesicle, and the cavity
of the epicardium of the bud
communicates at this point with
the pericardial cavity. Conse-
quently, the cavity of the
stolonic septum, the pericardial
sac and the epicardium are
merely differentiated portions of one and the same system of cavities.
In the larva, however, according to van Beneden and Julin, the
relation of the parts is different (p. 368).*
With regard to the further development of the bud, we can merely
briefly mention that the gill-clefts appear as perforations of the
contiguous walls of the pharyngeal sac and the peribranchial sacs ;
that the muscles are derived from strands of mesenchyme-cells, and
that the branchial and atrial apertures owe their origin to ectodermal
invaginations which become connected with the pharynx and the
atrium. The endostyle appears in the form of a fold of the ventral
wall of the pharynx.
FlG. li-iO. — Later ontogenetic stage of a
so-called bud of Amaroucium (after
Kiiwalevsky). <•/, atrium; (/.alimentary
canal ; e, atrial aperture ; ep, epicardium ;
es, endostyle ; i, branchial aperture ; ks,
gill-clefts ; n, nervous system ; p. peri-
branchial cavity.
* [Julin (No. XVII. | has recently investigated the origin of the pericardium
in Distaplia, and finds a condition which differs somewhat from that described
above as occurring in Clavelina. As in Clavelina, a pair of epicardial (pro-
cardial) tubes grow out from the pharynx on either side of the oesophageal
aperture : of these the left becomes divided transversely into an anterior
portion, which then fuses with the left epicardial tube to form the epicardial
sac, and a posterior portion which gives rise to the pericardium and heart.
Prom the recurved end of the right sac the primary bud is given off before
the tube fuses with that on the left to form the median epicardial sac. — Ed.]
470 TUNICATA.
< Ontogenetic processes altogether similar to those just described are
found in cases where the detached parts of the post-abdomen in the
PolycUnidae regenerate (Fig. 239). Here also the central entoderm-
vesicle is the first seat of transformation. As has already been men-
tioned (p. 454), the first change to occur is a widening of the proximal
end of the epicardial septum (Fig. 239 B). An entoderm-vesicle is
in this way formed in the proximal part of the young individual, and
this is continued backward into the part of the stolonic septum which
did not widen. The proximal dilatation is the rudiment of the whole
alimentary canal of the new individual, while from the non-widened
part are derived the epicardial sac (Fig. 239 B, ej>) and probably
also the pericardium. The entoderm-vesicle here also divides up in
the same way as in the bud into three lobes (Fig. 239 A and B), the
middle lobe being the rudiment of the branchial sac and the two
lateral lobes the rudiments of the peribronchial sacs. The complete
abstriction of the latter, their interconnection (Fig. 239 C) to form
a median impaired dorsal part (atrium), and the development of the
gill-clefts all occur in the same way as in the formation of buds.
The rudiment of the alimentary canal is here also a small, unpaired
caecum (Fig. 239 B, ) are
arranged symmetrically in two pairs,
while the other three (n, z, and m) are
unpaired. Grobben and Uljanin differ
considerably as t<> the origin and signifi-
cance of these seven strands which, with
the ectoderm that envelops them, form
the primary rudiment of the buds.
These two authors agree that two cones
grow downwards from both the pharyn-
geal and the atrial cavities of the
'•nurse" (Fig. 241, ph and cl), enclosing
between them a mesoderm-mass [m), the
origin of which has already been traced
(p. 387 ; see also Fig. 182 B, d and
ms', p. -'587). According to Uljanin,
the stolon is thus originally composed
of five strands, two pharyngeal and two
atrial strands and a middle mesoderm-
strand (Fig. 241). The number of these
strands becomes augmented to seven when the atrial strand (cl')
becomes bent on itself, its reflexed end
giving rise to a new pair of strands (el").
The fusion of this pair, according to
Ul.tanin, yields the future neural rudi-
ment (//), while the pharyngeal strand (p)
yields, by dehiscence, an unpaired middle
strand (.# ■) in which this author sees the
rudiment of the pharyngeal cavity of the
bud. The unpaired strand (m) is said to
represent the pericardial rudiment, while
the pharyngeal strands (p) change into
the genital rudiment, and the atrial
strands (k) into those of the muscle-plates.
According to Grobhen, on the con-
trary , the pharyngeal strands (/>) represent
the rudiment of the pharyngeal cavity
and intestine of the hud. the atrial strands
(/) the later rudiment of the atrium, and the unpaired mass ,
Fig. 241. — Young stage of de-
velopment of tlie proliferating
stolon (rosette-like organ) of
Doliolum Miilleri (after Ulja-
nin). cl, atrial wall of the
parent-animal ; cl', out-growth
of the atrial wall ; cl", bent
portion of the same ; m, aggre-
gation of mesoderm forming
part of the rosettedike organ ;
//. pericardial vesicle ; ph,
pharynx of the parent ; ph',
outgrowth of the wall of the
pharynx.
€C
Fig. '242. — Transverse section
through the ventral stolon or
.■I primitive bud of Doliolwm
(diagram alter Grobben and
Uljanin). ec, ectoderm ; k,
muscle-rudiments ; m, peri-
cardial rudiment ; n , neural
rudiment ; p, genital rudi-
ment ; x, pharyngeal rudi-
ment i Uljanin).
472
TUNICATA.
- - m s
-- — #13
^"U,
not
de-
the
(resulting from the fusion of paired strands) is assumed to be the
genital rudiment. The unpaired strand m is regarded as the rudi-
ment of the pericardial sac,
and the mass n, which from
the first is unpaired, as that
of the nervous system.
The buds are produced
through the transverse con-
striction of the ventral
stolon (Fig. 243, r and st),
from which they eventually
become completely de-
tached. In structure, they
resemble the stolon itself,
being composed of an ecto-
dermal envelope and the
seven strands above de-
scribed. • They are
capable, however, of
veloping further on
ventral stolon. Gkobben
has therefore regarded the
ventral stolon, which is
evidently homologous with
the proliferating stolon of
thi' other Tunicates, as a
vestigial stolon, and con-
siders the buds produced
by it as abortive.
A cross-section of the
dorsal outgrowth (Fig. 243,
st') of the " nurse " genera-
tion (hlastozooid) reveals
an essentially different
structure (Uljanin). Like
the ventral stolon, it is
covered superficially by a
layer of ectoderm, thickened
on the dorsal side, but the
interior of this outgrowth
is occupied merely by two
u.' w- /
Fig. 243. — Dorsal view of the posterior part oi the
body in a large " nurse " (blastozooid) Doliolum
.(after Barrois). /, lateral buds (gastrozooids) ;
in, median buds (phorozooids) ; ms^-ms'*, four
posterior muscle-hoops ; p, pericardium ; /'.
rosette-like organ ; st, ventral stolon ; st', dorsal
outgrowth ; u, primitive buds wandering to the
ventral side of the "nurse" ; //', primitive buds
wandering to the dorsal side ; n" , primitive
buds on the dorsal outgrowth.
DOLIOLIDAE — ASEXUAL REPRODUCTION. 473
blood-vessels separated by ;i partition-wall of connective tissue. The
transverse section of this outgrowth, indeed, strikingly recalls
sections through the stolon of certain Ascidians, although it must
be noted that, in these latter, the partition-wall is formed by an
entodermal lamella (epicardial lamella) of which nothing can be seen
in Doliolum.
The buds which develop from the dorsal outgrowth as lateral and
median buds (Fig. :243, /, m) do not arise independently from this
structure. Grobben conjectured that they were all abstricted from
a " primitive bud " found at the base of the stolon. Ulianin, on the
other hand, observed that the parts which become abstricted from the
ventral stolon are capable of wandering along the surface of the body
of the parent, and in this way reach the dorsal outgrowth (u, u').
These wandering cell-masses are the primitive buds, from which the
lateral and median buds of the dorsal outgrowth arise by constriction.
The primitive buds that first reach the dorsal outgrowth remain at
its base and, through fission, produce buds which become arranged
along each side of the stolon, developing into the lateral buds or
gastrozooids (/) : consequently the buds towards the distal end of the
row are more highly developed than those near its base. Those
primitive buds which reach the dorsal outgrowth later are distributed
along the whole of the middle dorsal line (""), and by gemmation give
rise to the median buds or phorozooids (m). These buds are arranged
in groups alternating on either side of the row of primitive buds (><").
The I tin Is of each group develop unequally, but here also there is
an advance in development towards the distal end of the stolon.
According to Uljanin, the ventral stolon is thus the only prolifer-
ating stolon of the " nurse " generation ; the dorsal outgrowth cannot
be regarded as a true proliferating stolon, but is merely a body-process
serving for the nourishment of the buds attached to it, which can be
traced hack to the mantle-vessels of the Ascidians.
The Doliolidae thus show an early detachment of the buds from the
proliferating stolon such as takes place in the Distomidae (pp. 456 and 463), in
which family also the detached buds are able to multiply further through
fission. The wandering of the primitive buds and the development of their
descendants in their secondary position in the Doliolidae are very remarkable.
The statements made mi this subject have been confirmed for Doliolum by
Baerois (No. 77), and similar processes have been observed in Anchinia and
Dolchinia, so that little room is left for doubt on this point. According to
Uljanin, the buds are able to move by means of pseudopodia-like processes
of their ectoderm-cells. According to Barrois, on the contrary, there are,
on each side of the ventral stolon of Doliolum, large amoeboid cells, arranged
474
TUNICATA.
in such a way that one pair becomes attached to each primitive bud as it
separates from the stolon (Fig. 252 A, p. 483). While these large, amoeboid
cells are attached to the surface of the primitive buds, they do not seem to
belong directly to the bud itself. According to Barrois, they are modified
test-cells concerned in the transportation of the primitive buds. Similar cells
arc found on the buds of Anchiuin and the primitive buds of Dolchinia.
,0*1
The median buds differ essentially from the lateral buds in form
and function. The lateral buds or gastrozooids (Fig. 244) are-
asymmetrical, short-stalked individuals in which, through increase in
length, the characteristic barrel -shape disappears. They may be
likened to spoons with deep concavity and
short handle. The concavity of the spoon is
formed by the pharyngeal cavity with its
wide aperture, the dorsal wall being formed
by the somewhat swollen branchial lamella.
The atrial cavity of the bud and its aperture
are so dilated as altogether to disappear.
The ^ill-clefts therefore lead from the pharyn-
geal cavity direct to the exterior. The
alimentary canal (d) is well developed, the
muscle hoops are vestigial, and the genital
rudiment found in the bud degenerates in
the further course of development. The
lateral buds are not able, after their detach-
ment from the dorsal outgrowth, to lead an
independent life, and they do not multiply in
any way. Their sole functions are the taking
in of food and respiration ; they obtain the
nutritive material for the other buds of the
dorsal outgrowth as well as for the blasto-
zooid (" nurse ") which has lost its alimentary
canal (p. 388). They correspond to the
nutritive polyps of a Siphonophoran stock (FoL) and have therefore
been called nutritive forms or trophozooids.
The median l>mh (phorozooids), on the contrary, after attaining their
full development, become detached from the dorsal stolon of the first
"nurse" (blastozooid) generation and lead a free pelagic life. These
individuals (Fig. 245 B) in the development of their body, closely
resemble the barrel-shaped sexual generation, from which they are
only distinguished by the absence of the genital organs (which here
degenerate at an early period in the hud) and by the presence of a
Fig. 244. --Lateral bud
(gastrozooid) of Dolio-
lum Mhlleri (after
Gbobbex). "». anal
aperture ; '/. alimentary
canal ; es, endostyle ;
//. ciliated arch ; ks,
'gill-clefts; it, ganglion;
//. pericardial vesicle
and heaxt;ph, pharynx.
|)OI,IOI.II)AK \sK\l\L RKI'KOIHH TION.
475
ventral process (.*/) near the posterior end of the body ; this process
is derived from the peduncle connecting the median hud with the
enr
Fig. 245.- The three generations of Doliolum Millleri (after G-ROBBEN). .1. young
"nurse" <' and C).
We have still to describe the development of the young buds after
their detachment from the primitive buds. According to Ul.tanin,
all these buds, whether lateral, median or sexual, develop more or
less in the same way, so that an account of the development of the
lateral buds will suffice. The young buds, immediately after abstric-
tion, resemble in structure the primitive bud and the ventral stolon,
consisting of an external layer of ectoderm and of the seven strands
mentioned above. We have already mentioned (p. 471) the different
views held by Grobben and Ul.ianin as to the significance of these
seven strands in connection with the further development of the bud.
We have as yet comparatively few statements as to the way in which
the young laid develops out of these seven primary rudiments, and
further investigation of this point is very desirable.
The young bud (Fig. 246 A), from the time when it becomes
detached from the primitive bud, is a completely independent organ-
ism enclosed in ectoderm, but attached externally, like a parasite,
to the body of the " nurse " or to the foster form. This attachment
is brought about by means of a thickening of the ectoderm (ec). In
the youngest buds observed by Uljanin, the body was already
elongated, and the organs, as compared with the seven cell-strands,
had already changed their positions. The dorsal side can now be
distinguished by the presence of the large rudiment of the nervous
system (n), while, on the ventral side, the pericardial rudiment (j>)
is to be observed. Between these two, the pharyngeal rudiment (ph)
can be seen, while the paired genital rudiment, forming a common
cell-mass, has shifted into the neighbourhood of the point of attach-
ment of the laid. The ectodermal invagination (<■/), behind the
nervous system, represents the rudiment of the atrium. This is one
of the principal points in which Qljanin's description differs from
that of Gbobben. According to the latter author, the atrium arises
from paired rudiments (the strands k in Fig. I'll') already present in
the primitive bud. At the two sides of the body, the muscle-plates
(///). lying in close contact with the ectoderm, have extended con-
siderablv.
478
TUNICATA.
In the course of further development a cavity forms in the pharyn-
geal rudiment and gradually enlarges (Fig. 246 B, ph) ; this soon
opens externally through an aperture (branchial aperture,/) resulting
from an ectodermal invagination which forms opposite to the atrial
aperture. The muscle-hoops which lie in the neighbourhood of the
atrial and branchial apertures now become separated from the muscle-
plates. The pharyngeal cavity gives off a pair of flat lamella-like
diverticula (I) towards the dorsal side, and these, as Grobben had
already observed, embrace the neural rudiment («) laterally. Accord-
ing to Uljanin, these diverticula are concerned principally in the
Fig. 246— Diagrams illustrating three stages in the development of the lateral buds of
Doliolwm, seen from the side(i4 and B, after Uljanin ; C, after Grobben). cl, atrium ;
d, enteric rudiment; e, atrial aperture: ec, basal ectodermal thickening; es, endo-
style-rudiment; g, genital rudiment ; i, branchial aperture ; k, gill ; I, lateral out-
growths of the pharyngeal cavity ; m, outline of the muscle-plates ; n, neural rudi-
ment ; />, pericardial rudiment; /)/'. pharyngeal rudiment.
formation of the branchial lamellae. A process (d) running back
from the pharyngeal cavity develops into the intestine of the bud, its
blind end becoming applied to the wall of the dilating atrial cavity
(cl). The latter extends specially towards the sides of the body, so
that, as Grobben observed, at a certain stage it resembles a pair of
spectacles. Its lateral extensions become applied to the wing-like
processes of the pharyngeal cavity (/). This juxtaposition of the
atrial and pharyngeal walls gives rise to the branchial lamellae (Fig.
24G C, /), in which the gill-clefts then break through. The rudiment
of the central nervous system undergoes a transformation closely
ALTERNATION OF GENERATIONS IN DOLIOLUM. 479
resembling that described above for tin- larva on leaving the egg
(p. 386). An anterior narrowed portion becomes the ciliated pit,
a posterior process changes into an unpaired nerve running from the
ganglion, while a third [tart of the rudiment develops into the gang-
lion and the sub-ganglionic body. The pericardial sac (p) and the
heart seem, as in the larva, to develop according to the type preva-
lent among all Tunicates. The genital rudiment (g) degenerates in
the lateral buds. It can still be recognised for some time to the left
side of the intestinal loop as a mass of cells. In the buds which
become sexual individuals this rudiment breaks up into two unequal
portions, the anterior smaller part developing into the ovary and the
posterior larger portion into the testis.
The later differences found in the lateral and median buds and the
sexual individuals are explained by the valued forms which these
finally attain. The median buds and the sexual individuals tend to
assume the characteristic barrel-shape, while the lateral buds increase
in height and, as mentioned above, adopt the somewhat asymmetrical
spoon-shape, owing to the dilation of the atrial aperture and
cavity.
Two more remarkable and insufficiently understood genera, Anchinia and
I ~k>lehin ia, which, in the structure of their gills, form a transition between
Pyrosoma and Doliolum, have still to be added. In these genera only parts
of detached stolons are known, the asexual " nurse " form, developed from
the egg which produced the stolon, being still undiscovered. We shall have
to compare these stolons with
the dorsal outgrowth of the first
" nurse" generation of Doliolum.
As a rule the stolon, in Anchinia
and Dolchinia, consists of a tube
which, in cross-section, is round
(the colonial tube, Fig. 247, c),
and seems to be formed of a q
Mii^le layer of flat ectoderm-cells. *
The interior of the tube is filled .,, .-,,- r.- , .. ., ,
r ic 247. — Diagrammatic cross-section through
with a gelatinous mass, in which the colonial tube (dorsal outgrowth) of
are embedded mesoderm -eel Is Dolchinia (after Korotneff). c, colonial
. m. , tube ; a, buds giving rise to tin- sexual
varying in shape. The external individuals ; -.. zooids.
surface of the ectodermal tube
which is covered by a cellulose mantle carries the various buds (a) which, in
later stages of their development, seem to grow out on stalks from thickened
parts of the ectoderm. The buds are thus here, as in Doliolum, only attached
to the exterior of the so-called stolon. They appear irregularly arranged along
the stolon, quite young buds being found among others half-developed, and
others again fully developed. In a transverse section of a stolon, however, the
480
TUNICATA.
youngest buds are found to occupy the dorsal middle line, while the older
buds shift to the sides of the stolon (Fig. 247).
Three different forms have been found in the colonies known of Anchinia,
but these are regarded by Baerois (No. 77) as fragments of the same stolon in
different stages of development.
I. There are fragments with zooids which, even when developed, remain
comparatively small, which are without genital organs and are incapable of
reproducing themselves by budding. These zooids are distinguished from
those of the sexual generation (III.)
by the absence of the three pigment-
spots and of the papilla-like pro-
cesses above the apertures of the
body. An accumulation of pigment
is found, on the other hand, at the
base of the peduncle (Fig. 248 A,
"li. pharyngeal rudiment; st, epithelium of
the colonial tube ; ./-, mass of large cells.
484 TUNICATA.
3. Pyrosoma.
Since the development of the four primary Ascidiozooids of the
Pyrosoma colony is closely connected with that of the Cyathozooid,
and takes place almost entirely within the period of embryonic life,
it has already been described above. It still remains for us to
describe the process of budding by which the other individuals
found in the adult colony are produced. These processes have been
described by Huxley (No. 72) and Kowalevsky (No. 71), and later
by Juliet (No. 73) and Seeligee (No. 76). The first development
of the proliferating stolon has also recently received some attention
from Salensky (No. 74). The chief point which we shall have to
consider is the origin of the primary organs in the proliferating stolon.
The further development of the zooids agrees so closely with that of
the four primary Ascidiozooids described above that we need only
refer to it briefly. The following account is based mainly on the
detailed observations made bv Seeligee.
A. Development of the Proliferating Stolon.
The individual zooids of Pyrosoma start budding very early, even
at a time when their individual independence is not fully attained, as
they are still connected with the stolon from which they were pro-
duced. In such a stolon (Figs. 253 and 267) the individuals increase
in size from its proximal to its distal end, those lying furthest from
the parent (Fig. 253 III) being the most developed aud exhibiting
the almost perfect organisation of a Pyrosoma zooid and the first
rudiments of the future proliferating stolon.
The first indication of this organ is an outgrowth . (d) of the
branchial or pharyngeal sac directed toward the ectoderm ; this lies
at the posterior end of the endostyle (es), ventrally to the heart (hz),
and appears surrounded by elaeoblast-tissue (eh). This structure is
known as the entoderm-tube, the entoderm-process, or, on account of its
close relation to the endostyle of the parent, the endostyle-process. It
seems probable that the stolon in every case is nothing more than the
remains of the entodermal tube which connects the entoderm-sacs of
two neighbouring buds (Fig. 253, v).
Another element which enters into the formation of the prolifer-
ating stolon is a group of closely crowded mesoderm-cells (ms)
embedded in the elaeoblast. This must be regarded as the rudiment
of tin (jnutal strand of the budding stock. Even earlier one or more
PYROSOMA DEVELOPMENT OF THE PROLIFERATING STOLON. 485
large cells are seen in it which can be recognised us young egg-cells.
The rudiment of the genital strand has, in its turn, become abstricted
Prom the genital rudiment (o, h) of the parent (<■/. ms, in individuals
// and ///).
Fig. 253. — A chain of three individuals of Pyrosoma (after Seeliger). /, youngest,
proximal bud ; //. middle and ///, oldest, distal bud (nearly fully developed). 1),
point at which the cndostyle-process of the parent enters ; d, endostyle- or entoderm-
process ; dc, rudiment of the alimentary canal ; \ rudiment
of tlh- atrial aperture; eb, elaeoblasf ; Ec, ectoderm of the parent; ec, ectoderm-
plate of the stolon-rudiment ; Es, endostyle of the parent ; es, endostyle ; fg, ciliated
pit ; :/. ganglion ; h, testis ; lid. intestine ; hz, heart ; i, rudiment of the branchial
aperture; hi, atrium ; ks, gill-clefts; //, internal longitudinal gill-bars; lm, lenti-
cular phosphorescenl organ ; m, stomach ; /«••>•, genital strand ; n, rudiment of the
nervous system; <<. ovary (egg-follicle with egg); oe, oesophagus; p, dotteil line
indicating the boundary of the peribranchial sacs ; /><■. pericardium; rz, languets ;
/. tentacle-rudiment ; u, duct connecting the enteric cavity of the second individual
with thai of the third.
These two rudiments (those of the entoderm-process and the
genital strand) ran also he recognised in a transverse section through
•Wis region of the body of the parent (Fig. 255). We then also see
that the entoderm-process is still accompanied by isolated mesen-
chyme-cells (Fig. •-'•"> J, ms). At the two sides of the process especially,
mesenehyme-cells can be seen arranged in two strands (pis). The
486
TUNICATA.
- rns
Fig. 254. — Transverse sec-
tion through the ento-
derm - process [en) of a
very young stolon-rudi-
ment of Pyrosoma (after
Seeliger). his, surround-
ing mesenchyme-cells.
strand on the right is continued as far as the pericardial vesicle of
the parent. These strands are the so-called mesoderm-strands of the
proliferating stolon mentioned above, the development of which in
the four primary Ascidiozooids was followed by Salensky (No. 74).
The part played by these mesoderm-strands in the further develop-
ment of the proliferating stolon and of the
buds is still obscure, and therefore no
further note will be taken of it.
That part of the ectoderm towards which
the entoderm-proeess is directed (Fig. 253,
ec) seems somewhat thickened even in the
early stages. The actual stolon now begins
to form in this region as a rapidly increasing
swelling. The conical process that results
(Fig. 256 A) is the stolon at the distal end
of which transverse constrictions soon lead
to the abstriction of individuals (Fig. 256 C).
In transverse sections through a developing stolon (Fig. 255), the
rudiments of the peribronchial tuhcs, (p) can already be seen at either
side of the entoderm-proeess. How these rudiments arise is not yet
accurately known, but as they are found connected by their distal
ends in a certain way
with the genital
strand, Seeliger is
inclined to derive
them from the latter.
He therefore regards
the peribranchial
tubes in the buds of
Pyrosoma as meso-
dermal structures,
although, in the
Cvathozooid and in
the first four Ascidio-
zooids, they are un-
doubtedly derived
from the ectoderm. [Judging by what is known of the development
of these organs in other Tunicates, and of the relations of the genital
rudiment in all other animals, it appears to us in the highest degree
improbable that there is any connection between the two structures,
i.e., peribranchial tube and genital strand, or between the latter and
the nervous system].
— fi,
Fig. 255. — Transverse section through two very young
stolons of Pyrosoma (after Seeliger). ec, ectoderm ;
el, elaeoblast-tissue of the parent ; en, entoderm-
proeess ; g, genital strand ; u, young egg-cell ; //.
peribranchial tubes.
PYKOSOMA DEVELOPMENT OF THE I'KOLI FERATTNG STOLON. 487
The rudiment of the nerve-tube of the stolon also, according to
Seeliger, is derived from the genital strand. In very young stolons
(Fig. 256 A) the distal end of the latter appears to bend round to
the upper side. (The lower side of the stolon is marked by the
position of the genital strand g). This upper part of the genital
strand becomes, in the further course of development, separated
from the lower part, and, according to Seeliger, becomes the
rudiment of the neural tube (Fig. 256 C, n), a lumen very soon
appearing inside it.
Seeliger thus holds that not only the genital organs of the bud
but also its peribranchial tubes, and a large part of all its mesodermal
structures, are derived from the genital strand. The group of cells,
ff
9 a ' is
Fig. "2"iti. Three stages in the development of the proliferating stolon of Pyrosoma
(after Seeliger). In C, the separation of the two individuals (/ and II) is already
indicated, if, entoderm-process ; ec, ectoderm; es, endostyle of the parent ; g,
genital strand ; ks, first gill-slits ; ni, rudiment of the alimentary canal proper; n,
rudimenl oi the neural tube.
which we described as the simple rudiment of the genital strand, has
thus, in his eyes, a far wider significance in the development of the
proliferating stolon. He has therefore designated it as the germ-
strand or the mesodermal germ-mass.
The fact that Skeliger traces back the peribranchial tubes and the neural
tube in the buds of Pyrosoma to the mesoderm cannot fail to awaken surprise
when it is remembered that the rudiments of these organs are undoubtedly
derived from the ectoderm, not only in the Cyathozooid but also in the four
primary Ascidiozooids. in our attempts to interpret the structure and sig-
nificance of the proliferating stolon, we naturally seek for agreement between
the development of its buds and that of the first four Ascidiozooids. When
we consider that the proliferating stolon must evidently be traced back to the
^S,S TUNICATA.
remains of the duct connecting each zooid with its neighbours (Fig. 196, s
p. 402 ; Fig. 253 ; v), and when we remember that in the four primary Ascid'io-
zooids continuations of the peribranchial tubes also are originally contained
in these ducts, we shall be led to ask whether, after the abstriction of those
parts of the peribranchial tubes that belong to the separate Ascidiozooids from
the ducts, remains of the tubes may not be retained in the form of incon-
spicuous cell-groups which might easily be mistaken for mesoderm, and from
which the peribranchial tubes of the stolon that develops later are derived
The rudiment of all the peribranchial tubes which .form later could in this
way be traced back to the peribranchial tubes in the Cvathozooid. Indeed
an extension of this way of viewing the matter might perhaps lead us to con-
jecture that the explanation of the many conflicting statements as to the rise
of the primary organs in the proliferating stolon in the various groups of
Tumcates is perhaps to be found in the theory that no primary organs originate
afresh m the proliferating stolon, but that they can all be traced back to corre-
sponding organs in the embryo from which thru become abstricted. Such a
conjecture receives special support from the condition of the ventral stolon
iu Doliolum.
We might well feel inclined to find some genetic relation between the peri-
branchial tubes of the Pyrosoma bud and the so-called mesoderm-strands of
the stolon mentioned above. After Salensky's statements as to the rise of
these strands (No. 74), such an assumption seems to us improbable, and we
prefer to derive the mesodermal structures of the bud from these strands.
When the stolon is perfectly developed, the typical aspect presented
by it in cross-section (which recurs also in the Salpidae) is that de-
picted in Fig. 257. The entoderm-tube (en) is cruciform, two limbs
«>f the cross extending upwards and two downwards ; the fold between
the former gives rise to the endostyle, while the two latter may already
be considered as the rudiment of the stomach and intestine. In fch_
spaces between the four outgrowths of the entoderm-tube are four
strands, three of which already possess lumina. The dorsal strand
(n) is the nerve-strand, the lateral strands are the peribranchial
tubes (p), and the ventral space is occupied by the genital strand (g).
In later stages, by the development of the primary body-cavity, these
strands become separated from the entoderm-tube; the mesoderm
(nu), at the same time, appears both as isolated mesenchyme-cells
and as cell-masses which, according to Seeligek, must to some
extent be traced back to the genital strand (Fig 255 B, g).
The breaking up of the stolon into separate individuals takes place
by means of constrictions (Fig. 25G C). Through the development
of these, the peribranchial tubes, the neural tube and the genital
strand of each individual become completely separated from the
corresponding rudiments of the adjacent buds. The enteric tube
retains its continuity longer; even in highly developed buds we find
s
e
PYBOSOMA PUBTHEB DEVELOPMENT OP THE liUDS. 489
the enteric rudiment still connected with thai of the next bud
i Fig. 258, '■)• The distal individual of the stolon is always the most
developed (<■/'. also Fig. 267). When five individuals have become
marked off on the stolon through the appearance of constrictions,
the distal individuals always seems to become detached. More
than rive individuals are consequently never found on one stolon.
B. Further Development of the Buds.
A fact already pointed out in connection with the development of
the four primary Ascidiozooids (p. 407) must again be emphasised
here, viz.. that the longitudinal axis of the stolon does not coincide
with the later longitudinal axis of the developing buds, but rather
appears to lie at right angles to it (Figs. 258, 267). The longitudinal
axis of the segments of the stolon changes into the dorso-ventral axis
of the developed bud. The axis which becomes the later longitudinal
axis of the body is one which we may imagine as cutting the
longitudinal axis of the stolon at right angles, i.e., from the neural
side to that of the genital strand. The ends of such an axis would
be indicated by the rudiments of the branchial and atrial apertures.
From the ectoderm of the stolon is developed the integument of the
laid which, on its outer surface, secretes the cellulose mantle. Accord-
ing to Seeliger, this secretion takes place here in the way described
for other Tunicates by Semper, Hertwig and others. When, there-
fore, Salensky emphasises the fact that the first rudiment of the
cellulose mantle is yielded by the Cyathozooid, the four primary
Ascidiozooids at first taking no part in the secretion of the cellulose
substance, his remark applies only to the first stages of development.
The further enlargement of the cellulose envelope proceeds from the
Ascidiozooids.
The branchial and atrial apertures (Figs. 253, 259, i) first appear as
simple ectodermal invaginations. These invaginations fuse with the
wall of the branchial sac or atrial cavity, the apertures breaking
through later at the points of fusion. Near the point at which the
branchial aperture forms, the branchial sac {i.e., the entoderm) <;ives
off the first bud-like rudiments of the crown of tentacles that en-
circles the entrance to this part of the alimentary canal (Fig. 253, t).
The entoderm-sac of the laid first forms the branchial sac or
pharynx. It has already been mentioned (p. 488) that this is cruci-
form in transverse section (Fig. '_'-">7), two of the outgrowths being
directed upward and two downward. The upward outgrowths are
separated from each other by a median fold in which can be recognised
490
TUNICATA.
the first rudiment of the endostyle (Fig. 259, es). The latter is com-
pleted later through the rise of two lateral folds, the median groove
becoming the base of the endostyle-furrow. The condition here,
according to Joliet and Seeliger, corresponds perfectly with that
described for the four primary Ascidiozooids (p. 406). The rudiment
of the endostyle originally occupies the upper or neural wall of the
branchial sac, its proximal end corresponding to the later anterior end.
The endostyle-rudiment, according to Joliet (as described on p. 418),
here passes over into the remarkable provisional structure known as
the diapharync/eal hand, which runs towards the ganglion below the
branchial aperture.
The two lower outgrowths of the branchial sac, as seen in trans-
verse section, are the rudiment of the alimentary canal proper (i.e.,
'A
Fig. 257. — Two transverse sections through the stolon of Pyrosoma (after Seeliger).
ec, ectoderm; en, entoderm; ., peribranchial tubes; sn, rudiment of the lateral
nerves.
oesophagus, stomach and intestine). These two outgrowths com-
municate at the distal end of the bud. This rudiment, which soon
becomes abstricted from the branchial sac, is thus horse-shoe-shaped.
The right portion, which retains a connection with the branchial sac,
gives rise to the oesophagus and stomach, while the left portion be-
comes the intestine, which ends blindly at first and later opens into
the atrial cavity (Fig. 253). Seeliger's account agrees fairly well
with Salensky's description given above (p. 408). The digestive
gland, which originates as an outgrowth, arises at the boundary
between the stomach and the intestine.
The lateral walls of the branchial sac are occupied by the gill-clefts.
These are at first (Fig. 256 (', ks) more or less round perforations of
PYROSOMA— FURTHER DEVELOPMENT OF THE BUDS. 191
the contiguous walls of the entoderm-sac and the peribranchial sacs
(Fig. 258, p), but they very soon become elongate (Fig. 259)
The inner longitudinal bars of the branchial sac (Fig. 253, If) now
develop at right angles to the clefts. As the slits break through
chiefly in consequence of an outgrowth of the entoderm-sac, the}
appear to be lined with entoderm.
The two peribranchial sacs, which early lost their connection with
, lu.se of the adjacent bud, by growing towards each other on the lower
side of the stolon and fusing, give rise to the unpaired atrial cavity
(Figs. 253, /•/. 259, <•/).
Finally, the outgrowths of the dorsal wall of the branchial sac
known as the languets (Fig. 253, /■:) develop.
The rudiment of the central nervous system appears at first as a tube
running along the whole length of the upper side of a stolon-segment
es h's 7i
pIG 958 — Stolon of Pyrosoma with the rudiments of two individuals, / and // (after
Sebijgeb). A, side view; B, seen from the side on which the genital strand is
situated eb rudiment of elaeoblast ; ec, ectoderm; es, endostyle-rudiment ; g,
tenital strand; hs, gill-clefts; m, rudiment of the stomach and intestine ; //.nervous
system of bud J ; n', nervous system of bud II; />. peribranchial tubes ; s, rudiment
of the lateral nerves (in /.'. seen in transverse section).
i I'm. 256, n) ; later, however, the proximal part of this tube develops
into a large vesicle, while the thinner, distal part disappears. Two
lateral outgrowths of the proximal part of the neural tube (Figs. 258, s,
259) can be seen very early (Fig. 257 A, m) ; these soon change
into hollow processes which encircle the alimentary canal and unite
on its lower side. These are the rudiments of the so-called lateral
nerves. A growth of the cells on the dorsal wall of the cerebral
vesicle yields the rudiment of the ganglion proper, which later gives
off the lateral nerves that run backward along the dorsal surface of
the adult in the form of solid strands with terminal ganglionic
swellings. The remains of the cerebral vesicle develop a connection
with the branchial sac and become transformed into the ciliated pit
492
TUNICATA.
(Fig. 253, fg). The posterior blind end of this tube gives rise to the
subneural gland.
Isolated mesenchyme-cells are early met with in the primary body-
cavity of the stolon (Fig. 257). Seeliger traces these to a great
extent to cells of the genital strand that have become independent
(Fig. 255 B). Some of these mesenchyme-cells become transformed
later into connective tissue-cells and blood-corpuscles. Others take
part in the formation of the lenticular and elongate cell-masses. The
elongate mass which belongs to the dorsal region (Fig. 253, dm) seems
to be connected with the formation of blood-cells. The cells of the
lenticular masses (Fig. 253, Im), on the contrary, contain oil globules
in their protoplasm in later stages, and are regarded as phosphorescent
organs. The elaeoblast also (Figs. 253, eb, 25S, 259) arises from an
Fig. 259.— Stolon of Pyrosoma with the rudiments of two individuals, / and // (after
Seeliger). <■/, atrium; eb, elaeoblast; ed, intestine; es. endostyle; g, genital
strand; i, branchial aperture; ks, gill-clefts; m, stomach; ■/. neural tube of bud
/, /'. rudiment of ganglion of bud // , oe, oesophagus; s, lateral nerves.
originally paired accumulation of mesenchyme-cells lying immediately
below the entoderm in the distal region of the stolon-segment, The
two halves of the elaeoblast-rudiment unite later at their upper
and lower surfaces, a perfect circle being thus formed which soon,
through deposits of nutritive material, develops the typical character
of elaeoblast-tissue.
The musculature also which, in Pyrosoma, is reduced to a few slight
strands running round the branchial and atrial apertures and in the
outer wall of the peribranchial cavity, is derived from the mesenchyme-
eells. These at first unite to form cell-strands in the peripheral parts
of which the fibrils of contractile substance first appear. As these
i,yiu)som\ i- ii; ihi;k dkvkloi'MBNT of the huds.
t93
A—
A-
Fig. 2t>0. — Two early stages in the develop-
ment of the pericardial vesicle in the buds
of Pyrosoma (after Seeliger). en, entoderm
( wall of the enteric rudiment) ; ec, ectoderm ;
p, peribranchial sac ; pc, rudiment of the
pericardia] vesicle.
fibrillae increase in size they become band-like. In transverse sec-
tion, tiny then appear radially arranged, while the centre of the
muscle-bundle is occupied by
the undifferential protoplasm
and nuclei of the cells.
The first rudiment of the
pericardial vesiclt is also traced
backj by Seeliger, toa small
group of mesenchyme-cells
which can be seen beneath the
distal end of the right peri-
branchial tube. In this cell-
group (Fig. 260, />(■) a lumen
soon appears which is the
pericardial cavity ; at a later
stage, the rudiment of the heart {hz) arises through the invagination
of that part of the wall of the pericardial vesicle which is in contact
with the wall of the intestine (Fig. 261).
The pericardial vesicle originally lies on
the right side of the bud, but wanders
later towards the median plane and thus
reaches the dorsal side of the endostyle,
process (Fig. 253, hz). It has therefore
in Pyrosoma, a position unlike that
occupied by it in the other Ascidiacea,
where, as described above (p. 370), the
heart lies on the ventral side of the
endostyle-process (epicardium) in such
a way that the epicardial lamella brings
about the closure of the cardial tube.
In each bud, the genital strand (Fig.
259, g) gives rise to the genital organs
of the individual and to the genital
strand of the stolon produced by that
individual. At an early stage, the
genital strand is found to break up into
a distal and a proximal part. The
distal part, which is embedded in the
elaeoblast-tissue (eb), becomes abstricted
and gives rise to the genital strand of
the stolon. In the proximal part, which represents the rudiment of
£
Fig. 261.— Two later stages in
tin- development of the peri-
cardial vesicle in the hud oi
Pyrosoma (utter Seeliqkr).
ec, ectoderm ; el, elaeoblast ;
i c. entoderm (wall of intes-
tine); pc, pericardial vesicle;
hz, rudiment of heart.
494 TUNICATA.
the genital organs, lies the egg-cell surrounded by smaller undif-
ferentiated cells from which the follicular epithelium is derived. A
cell-mass attached to the follicular epithelium and lying proximally
to the left of the egg-cell represents the rudiment of the testis (Fig.
253, h). In the young rudiment of this organ, a superficial epithelium-
like layer of cells can be distinguished from a central mass of cells.
The seminal duct forms as an outgrowth of the peripheral epithelial
layer. The oviduct ai-ises in a similar way from the egg-follicle, and
both ducts open into the atrium. In later stages, the rudiment of
the testis becomes lobate. Two eggs occasionally occur in the egg-
follicle, one being larger than the other. The smaller egg seems to
disintegrate later, so that only one egg is maturated in each indi-
vidual in Pyrosoma as in the Salpidae.
4. Salpidae.
The processes of budding in the Salpidae early attracted the
attention of zoologists and have been repeatedly investigated.
Eschricht, Huxley (No. 95), Leuckart (No. 98), and Vogt laid
the foundations of our knowledge of this subject, and in more recent
times it has been increased through the application of modern methods
by Kowalevsky (No. 96), Todaro (No. 107), Salensky (Nos. 101
and 102), Seeliger (No. 105) and Brooks (Nos. 92 and I.). No
very satisfactory comprehension of the ontogenetic processes has,
however, as yet been attained. Brooks was able to trace back the
budding of the Salpidae to the type observed in Pyrosoma, point-
ing out that the biserial arrangement of the buds on the stolon of the
former is the result of lateral shifting and the simultaneous rotation
of the buds round their longitudinal axis. Since this latter point was
overlooked by the other authors, we must regard with some doubt
their statements as to the rise of the organs in the buds.
In SiiIjik, the buds arise on a proliferating stolon (Fig. 262, st)
which must be regarded as in every way homologous with that of
Pyrosoma. In older embryos (Figs. 216, st, 224 B, s) this can be
seen as a conical outgrowth at the posterior end of the endostyle
growing out between it and the opening of the oesophagus rather to
the left side of the body. When the stolon grows longer, it appears
embedded in the cellulose mantle of the solitary individual. A cavity
containing the stolon develops, however, in the mantle-substance
(Fig. 262, h) and this finally opens externally (o), so that the distal
end of the stolon from which the mature buds are abstricted, projects
out freely. The position of the stolon differs in the various species.
SALPA — DEVELOPMENT OK THE STOLON.
195
lii Salpa pinnata, S. a/ffwis sfes out behind this organ. Iu
S. democratica - rmtcronata, S.
scutigera - confederata and S.
cordi/ormis - xmaria, the stolon
winds spirally round the nucleus
(Fig. 262).
The individual .buds here, as in
Pyrosoma, become marked off by
transverse constrictions which
appear on the stolon. While,
however, in Pyrosoma, the separate
parts of the stolon remain in a
single row, in the Salpidae,
secondary shifting leads to a bi-
serial arrangement. A large
number of buds consequently can
of the stolon.
dolichosoma, it is more or Less
ventral side of the body. In S.
Fig. 262. — Posterior end of the body in
a solitary form of Salpa democratica-
mucronata, from the dorsal side(after
Leuckakt). d, alimentary canal ; /'.
brood-cavity ; o, aperture of the same ;
st, proliferating stolon.
be crowded on to a short piece
A. Structure and Development of the Proliferating Stolon.
< >ur knowledge of the earliest stages of the development of the
stolon is due chiefly to Seeligek (No. 105). The stolon, as already
mentioned, is at first a small, conical
outgrowth on the left side of the
body near the posterior end of the
endostyle. Three layers can be dis-
tinguished in it : ectoderm, mesoderm
and entoderm. The ectoderm of the
stolon passes direct into that of the
parent. The entoderm-sac of the
stolon (Fig. 263, en) is a diverticulum
of the wall of the parent's branchial
sac arising immediately behind the
endostyle. This diverticulum exactly corresponds to the organ known
l'i'.. 263. — Youngest stage "I de-
velopment of the stolon in Salpa
(after Sbeligbr). <>. blood-sinus;
ectoderm : en, entoderm-
process; m, mesoderm;
mesenchj me-cells.
496
TUNICATA.
m the other Tunicate* as the entodermal, endostylic, or epicardia]
process. Between the ectoderm and the entoderm of the stolon the
primary body-cavity extends, being directly connected with that of
the parent. In it we find an accumulation of mesoderm-cells (m)
completely enveloping the entoderm-process ; these, accordino- to
Seeligee, are produced by the simple immigration of mesenchyme-
cells from the parent. Such cells (mz) are found in large numbers
at the point of origin of the stolon in the neighbourhood of the
elaeoblast-tissue.
While Seeliger considers that the mesoderm of the stolon results from
the immigration of a large number of mesenchyme-cells, Todaro (No 107)
regards it as arising from the division of certain large germ-cells (germoblasts
derived from the placental membrane (membrana germoblastoca, p 435) at
em.
tm.
bfei M'neuraltube; "• "PP- Mood-sinus; „,.„,„,,„, rudiment?* W
the cleavage of the original egg which gave rise to the solitary form Since
according to Todaro, the whole bud is derived exclusively from the descend
ants of these cells, the ectoderm and entoderm of the stolon taking no part in
the formation of the buds, these latter are to be traced back to a form of
sexual reproduction. Todaro regarded the buds (in Salpa-chains) as younger
members of the generation to which the solitary form belongs.
Transverse sections through older stolons (Fig. 264) reveal a condi-
tion deviating somewhat from that above described, but showing
great agreement with the stolon of Pyromma (Fig. 257 p 490) In
the primary body-cavity, four regularly-arranged strands have
appeared. The uppermost of these, which we will call the neural
strand or newal tube (Fig. 264, n) contains a distinct lumen The
paired lateral strands also (c) are said by authors to have Iumina
SALl'A DEVELOPMENT OF THE STOLON.
497
round which the cells are arranged like an epithelium (Fig. 265, c),
although Skelickk was not able t<> come to a definite conclusion on
this point. He called these strands the lateral strands, whereas the
other authors speak of them as the peribranchial, perithoracic or cloacal
tubes. They correspond to the peribranchial tubes in the stolon of
Pyrosoma. In the fourth, lower strand (n p. 484, the individuals
are arranged on the
Pyrosoma stolon in a
single row, one behind
the other. The orienta-
tion of each individual
resembles that of the
parent. The haemal or
ventral side of the buds
(marked by the position
of the endostyle, es) is directed towards the distal end of the stolon.
The right half of the body of every individual agrees in position with
the right side of the parent; the left half of the bud corresponds to
the left half of the parent and has been produced by the left half of
the stolon, just as the right half of the bud has been produced by
the right half of the stolon.
i
Fig. 267. — Diagrammatic longitudinal section
through the stolon of a Pyrosoma (constructed by
Brooks after Huxley and Kowalevsky). P,
parent-individual ; /, //, ///, first second and
third buds ; b, branchial-sac ; c, atrium ; d,
alimentary canal ; ec, ectoderm of the connecting
strand ; en, entoderm of the same ; es, endostyle ;
/(. nervous system; o, segment of the genital
strand; s, young stolon of the third individual. |
* [According to Bbooks (No. I.), the nerve-tube and the two peribranchial
tubes are probably derived from the ectoderm of the stolon ; the upper blood-
sinus is continuous with the cavity of the heart, and the lower sinus with the
body-cavity of the nurse-form. — Ed.]
500
TUNICATA.
If, now, the individuals of the Salpa stolon remained in the same
position as those of the Pyrosoma stolon, the stolon of the Salpidae
Fig. 268. — Diagram representing a stolon oJ Salpa as it would appear it no secondary
shifting of the individuals were to take place (after Brooks). /', solitary form
(parent-individual); /, 77, ///, first, second and third group of individuals; b, b",
b'", branchial sac (pharynx); c", c'", atrium ; d, alimentary canal ; ec, ectoderm ; el,
elaeohlast; en, entoderm (of the connecting strands); es, endostyle; g, gill; h,
heart; n, nervous system ; o", <>'", ovary.
would he accurately represented by Brooks' diagram (Fig. 268). Here
also the individuals are still arranged in a single row one behind the
other, their orientation being that of the
parent. The median plane of the stolon and
of all the individuals on it coincides with
that of the solitary form (P). The only
distinction between this stolon and that of
Pyrosoma is the larger number of indi-
viduals here present. The Pyrosoma stolon
has only a limited number of individuals
(five), but the stolon of Salpa consists of
several consecutive groups, each comprising
50 to 100 individuals all at the same stage of
development. The most distal group (///)
is the oldest, and contains the most highly
developed individuals. (For the sake of
clearness, the groups depicted in the diagram
are composed of not more than four indi-
viduals). These groups, further, are not
sharply marked off from one another. Be-
tween every two groups there are always a
few individuals which, in the degree of their
development, form transitions between the
two groups. We also find, especially in the
FlG. 269. — Diagram illus-
trating the position of
the individuals on the
stolon in the Salpa-chain.
( s, endostyle-folds ; h,
haemal or ventral side of
the buds; I, left side;
n, nervous system and
neural -or dorsal side; r,
right side ; st, remains
of stolon.
SALPA — DEVELOPMENT OF THE BUDS ON THE STOLON.
50]
younger stages, thai the distal individuals of a group are somewhal
further developed than the
proximal individuals of the
same group.
The individuals are in reality
arranged on the stolon in two
alternate rows (Fig. 269) in
such a way that the correspond-
ing individuals of the two rows
turn their ventral (haemal)
sides (h) to each other, while
their dorsal (neural) sides (,/)
are directed outward. This
arrangement can be clearly
made out in the transverse
section (Fig. 275) through an
older part of a stolon. We
thus have an arrangement of
the individuals like that de-
picted in the diagram (Fig.
269). The median plane of the
individuals docs not coincide
with that of the stolon, but
This
of the
buds results from a lateral
shifting of the segments of the
stolon which move alternately
to the right and left side.
Bach hud at the same time
rotates round its longitudinal
axis, passing through an angle
i if 90 : consequently, I he dorsal
side of the hud which origin-
ally (Fig. 268) was directed
Fig. '^70. Horizontal Longitudinal section through an advanced stolon of Salpa
(after Brooks). The individuals are cut thr >ugh obliquely, the longitudinal sei
passing through them in such a way that, in those placed mosl distallj (1, 2, etc.),
the most anterior region <>i the body is seen and, in the most proximal individuals
(20, 21, etc.), the posterior region of the body. D, distal ; P, proximal; R, right;
L, left. <>. anal aperture; ■■. atrium; el, elaeoblast; es, endostyle; g, gill; l>.
heart; hs, haemal side .>t the bud; i, intestine; lb, left hall' of tin- branchial sac;
///, opening of the oesophagus; >'. nervous system ; ns, neural side of the bud :
ovary : rh. right half of the branchial sac ; s, stomach.
lies at right angles to it.
biserial arrangement
/
502
TUNICATA.
towards the proximal end of the stolon is now turned toward the outer
side of that structure (Fig. 269), while the ventral side has passed from
its original distal position and is turned toward the median line of the
stolon. This rotation, which was pointed out by Brooks, does not
take place simultaneously throughout the whole of the bud, but
affects the posterior or ab-oral end at which the elaeoblast lies earlier
than the anterior or oral end.
If, therefore, we carefully examine
a somewhat oblique longitudinal
section through the stolon, like
that given in Fig. 270, we shall
be able to follow the process of
shifting, since the individuals are
in consequence cut through at
different planes. We find that
individuals 16-21, the posterior
ends of which arc cut through,
are already in their final position,
their arrangement being distinctly
biserial. The individuals of the
left row (16, 18, 20) have their
dorsal side directed to the left, but
the ventral side turned to the
middle line of the whole stolon.
The individuals of the right row-
show an opposite arrangement.
When, however, we examine the
buds the anterior part of which
is cut through (7-11), we find
that the biserial arrangement is
here not fully carried out, the
individuals of the left row lying
partly on the right and those of
the right row partly on the left
Fig. 271.— Diagram illustrating the
relative po.sition of the individuals 3-7
depicted in Fig. 270 (after Bkooks).
D, distal; I', proximal; R, right; L,
left (with regard to the stolon). >n,
entoderm - tube of the stolon ; hs,
haemal side of the bud ; I, left side of
the bud ; lb, left half of the branchial
sac ; n, neural side of the bud ; o, upper
blood-sinus in the stolon ; /•, right side
of the bud ; rb, right half of the
branchial sac ; u, lower blood-sinus in
the stolon.
of the stolon. The rotation also
is not complete. The endostyle (es in individuals 8) which marked
the ventral (haemal) side, is still directed distally (D). The neural
side, which is marked by the position of the ganglion (>i in individual
11), still to a certain extent retains its primary position, i.e., is still
turned towards the proximal end (P) of the stolon. We here see
very clearly the way in which the final biserial arrangement of
SALPA DEVELOPMENT OF THE BUDS ON THE STOLON.
503
the individuals on the stolon of Salpa can be traced back to the
original monoserial arrangement which is retained in the stolon of
Pyrosoma.
Special interest attaches to the condition of individuals 3-7 of
Fig. 270, diagrammatically illustrated in Fig. 271. We can here
clearly see the relation of the buds to
the stolon. The stolon itself is cut
through obliquely, the section being
intermediate between a longitudinal and
a transverse section. We can see the
entoderm-tube of the stolon {en), an
teriorly, the upper blood-sinus (o) and
posteriorly the lower blood-sinus (u, cf.
Figs. 264 and 2G5). In individual 5,
we can trace the connection between the
right (rl.) and the left (lb) halves of the
branchial sac with the entoderm-tube
(en) of the stolon. All the other indi-
viduals are cut through at a different
level. In individuals 4 and 6, for
instance, the two blood-sinuses are inter-
calated between the right and left halves
of the respiratory cavity.
We have reproduced other diagrams
by Brooks (Figs. 272 and 273) which
still further illustrate this condition.
Fig. 272 gives the upper or oral aspect of
a stolon as it would appear if the primary
position of the buds had been retained
unaltered (cf. Fig. 268). The right half
of each bud is seen to have arisen from
the right side of the stolon and the left
half of the bud from the left side of the
stolon. Fig. 273 shows the buds shifted
alternately to the two sides of the stolon,
a condition attained through the repeti-
tion of the process taking place in indi-
vidual 5 in Figs. 270 and 271. The
buds 1, 3 and 5 have moved toward the
right side of the stolon while 2, 4 and 6 have moved toward the
left side. The rotation of the individuals, however, is not yet visible.
FlG. "272. — Diagram of a stolon
of Salpa as it would appear
ii' no secondary shifting of
the individuals were to take
place (after Brooks). /'.
proximal; />, distal; R,
right ; L, left of the stolon ;
r and /, right and left sides
of the individuals ; e$, endo-
style-folds ; /<, ganglion.
504
TUNICATA.
D
1
Originally, therefore, the rudiments of the individuals (buds) are
nothing more than the consecutive segments of the stolon marked off
one from the other by transverse furrows. These furrows, as seen
from above or below, are soon no longer transverse, but run somewhat
obliquely (Fig. 274), in alternating directions, so that furrows 1, 3
and 5 are parallel on the one hand,
and furrows 2, 4 and 6 on the other.
In this oblique course of the furrows,
we see the first preparation for the
later biserial arrangement ; it is
the expression of the lateral displace-
ment of the tissues of the buds
forming the dirferent segments of
the stolon. When, therefore, in
later stages, the segments shift to
the two sides, it appears as if the
buds arose as lateral outgrowths
from the stolon. This erroneous
view of the budding of the Salpa is
actually adopted by many of the
older authors. Brooks was the first
to trace back the origin of the buds
to the transverse division of the
stolon.
The individuals become more and
more sharply marked off from one
another in proportion as they assume
their lateral positions and project out
from the stolon. They then appear
to be hanging on to the remains of
the stolon like grapes on a bunch
(Fig. 275 B). The remains of the
stolon (st\ however, are nothing
more than the consecutive strands
which connect the individuals.
These-, as may be seen from the
diagram (Fig. 272). originally ran from the haemal side of each
individual to the neural side of the next older bud. They are
originally inserted at the middle of the body. In later stages,
when the individuals have taken up the lateral position and have
undergone rotation, the connective strand forms a continuous longi-
£7?
T
Fie. 273. — Diagram of a stolon of
Sulpa after the lateral shifting of
the buds has taken place ; tin;
Sctlpae in this diagram are all repre-
sented in the position of individual
5 in Figs. 270 and 271. J', proxi-
mal ; I>, distal ; R, right ; L, left;
/•and /, right and left halves of the
buds; ((-<(, line separating one indi-
vidual from the next ; ec, ectoderm ;
en, entoderm.
SALPA — -DEVELOPMENT OF THE 1UJDS ON THE STOLON.
505
tudinal tube to which the buds adhere laterally. The blood-vessels
running in this strand, and the eutoderm-tube which persists within
it and connects the branchial sacs of the individuals,
arc of importance for the nourishment of the buds.
'Tin's longitudinal strand may be called the remains of
tlw stolon. Its position with relation to the Imds
changes, as its points of attachment wander more and
more upward, i.e., toward the branchial aperture
of the individual (Fig. 275), while the individuals sink
downward on either side of it. This change of position
can be most distinctly traced in the ganglia. The
neural tube of the stolon originally lies above the
entoderm-tube as is seen in Fig. -64. The ganglia
derived from the neural tube must consequently seem
to lie in the median line above the entodermal con-
nective canals (see diagram, Fig. 268). When, later,
the buds become marked oft' laterally, the ganglia sink
lower down, and come to lie at the sides of the con-
necting canals ; indeed, in the diagram (Fig. 268)
they appear alternately to cover the canals and to be
covered by them. Later, the ganglia and, with them,
t he individuals, sink still farther down.
The sinking down of the buds on either side of the remains of the
stolon solves a difficulty which apparently presents itself in connec-
tion with their rotation. In examining individual 5 in Fie.-. 271,
and still more in considering the diagram Fig. 273, it may occur to
the observer to wonder in what way the endostyle fold which, in
individual 5, lies on the left side, passed over to the right, since it
appears separated from the right side of the body by the entoderm-
tube of the stolon. We have tried to make this process clear by the
diagrams given in Fig. 276. The connecting strand ab, which
represents the remains of the stolon, originally runs from the neural
side of each individual to the haemal side of the next (proximal)
individual. After rotation has taken place, these strands would
assume a zig-zag course, as indicated in Fig. li T * > 1>. Later, as the
buds sink down, the connecting strands, which are already attached
near the anterior region of the body, shift further forward to a
•position quite near the branchial aperture, whereas the endostyle-
t'olds, which remain unaffected by this change, do not extend so far
forward. There is therefore no obstacle in the way to prevent the
union of the connecting strands ; by this union these strands appear
Fig. 27 i. -
Diagram il-
Lustrati n g
the course
of transverse
furrowing in
the stolon of
; oa, seen
from above.
506
TUNICATA.
as a continuous tube in which we recognise the remains of the stolon
(Fig. 276 G).
Even in later stages, the two principal blood-sinuses (Figs. 264, 275,
o and u) which appeared at an early stage within the developing
stolon (Fig. 264 B) are still to be found in the remains of that
structure. These vessels are bounded by distinct epithelial walls and
have no connection with the bud, the blood-vascular system of which
arises quite independently. The blood from the body of the parent
therefore does not pass over into the body of the bud.
Fig. 275. — Transverse section through a stolon of Salpa (after Salensky). .1, with
younger, and B, with older buds, cl, atrium ; d, enteric canal ; e, atrial aperture ;
es, endostyle ; h, connecting process (couplings) ; k, gill ; n, nervous system ; o,
upper blood-sinus ; ov, ovary ; p, pericardial vesicle ; ph, pharynx ; st, remains of
stolon ; v, lower blood-sinus.
When the buds are fully developed the remainder of the stolon
degenerates, breaking up into segments which are drawn in by the
buds and absorbed by them. The connection between these (the
individuals of the chain), originally brought about by the stolon, is
now maintained by means of integumental processes derived from
buds (the so-called connecting processes or couplings, Fig. 278, hf),
which originate as outgrowths of the integument. These processes
SALPA — DEVELOPMENT OF THE BUDS ON THE STOLON.
507
are hollow, aud each of them contains a blood-vessel. These might
be compared to the mantle-vessels of the Ascidians. The final
connection between the individuals is formed by the processes of
neighbouring individuals growing out towards one another and
fusing. Each of the individuals belonging to a chain possesses, as
a rule, eight of these processes placed in four longitudinal rows ;
two ventral and two lateral. The lateral couplings serve for attach-
ment to the individuals lying in the same longitudinal row, while the
ventral processes establish a connection between the two parallel rows
Via. 27b'. -Diagram illustrating the relations of the connecting strand (st) to the buds
on the stolon of a Salpa. .1 , represents the stolon from Fig. 268 viewed from above ;
B, shows the condition after rotation has taken place ; C, the condition after the
buds have sunk downward, a, distal end of the connecting strand, b, proximal end
of the same ; d, distal part of stolon ; es, endostyle-folds ; h, haemal or ventral side ;
n, nervous system and neural or dorsal side ; p, proximal part of stolon ; st, connect-
ing strands.
of individuals seen in the diagram (Fig. 277 A). The long axes of
the individuals are inclined somewhat obliquely to that of the chain,
a position which results from the fact that the couplings are not
inserted at the same level on the right and the left sides of the body
(Fig. 277 />')■ This oblique position may have given rise to the
horizontal one seen in Salpa fusiftyrmis. In S. {Cyclosalpd) pinnata
the individuals are found arranged in the form of a rosette, each of
the buds giving off a single process only from the ventral side which
runs towards the centre of the rosette, where all the processes meet
508
TUNICATA.
Together like the spokes of a wheel. Such an arrangement is charac-
teristic of the genus Gyclosalpa. *
This union between the individuals of the Salpa-chain must bo
regarded as colony-formation. Whereas, in the composite Ascidians
and in Pyrosoma, the individuals which arise through budding remain
connected by means of a common cellulose mantle, connection here
takes place through special connecting organs.* This connection is-
Fig. 277.— Diagram illustrating the interconnection existing between the individuals
F a. Salpa-chain. .1. the chain seen from above; B. lateral view, es, endostyle ;
em, embryo; - found in it. Its form,
in cross-section, later resembles that of the letter H, also found in a
similar section of a Pyrosoma bud (Fig. 257). In the latter, the two
portions of the tube that point upward arc connected with the
development of the endostyle-folds, while those that extend down-
ward, yield the stomach and intestine (p. 1(.»0). It is at present
impossible to say whether similar conditions prevail in tin- Salpa bud.
* [Brooks' memoir on the geuus Salpa (No. I.) should be consulted in this
connection ; he gives a full and detailed account of the development of the
chain-form, including its organogenesis. — Ed.]
510 TUNICATA.
In any case, the rudiment of the endostyle grows out as paired folds
projecting inward, while the intestinal loop (Fig. 268, d) is derived
from the lower end of the entoderm-vesicle, from which it grows out
as a blind diverticulum on the right side.
The atrial cavity of the bud (Fig. 269, c) arises, according to
Brooks, through the union of the paired peribranchial tubes (Fig.
265, c). The cavity which thus arises then occupies a dorsal position
in the posterior part of the bud. Two lateral perforations which
occur in the partition-wall extending between the atrial cavity and
the pharynx represent the rudiment of the two gill-clefts, and the
trabecula remaining between the clefts is the rudiment of the gill
(Fig. 268, g), the ventral and lateral covering of which is derived
from the entoderm, while the covering of the dorsal side is yielded
by the epithelium of the atrial cavity [ectoderm, Brooks]. Only at
a later stage do the pharyngeal and atrial cavities open externally,
ectodermal invaginations leading to the formation of the branchial
and atrial apertures.
The neural tube of the stolon becomes broken up into segments,
each of which, in the form of a spherical vesicle with thick walls,
gives rise to the central nervous system of a bud. In the young
buds, these appear remarkably large (Figs. 270, 275, n), but decrease
in size later. The vesicular rudiment which lies on the dorsal side
of the bud in the anterior region of the body, becomes divided into
two parts by a transverse furrow ; these parts at first remain con-
nected with each other, but are later completely separated. The
anterior part becomes connected with the entodermal wall of the
pharyngeal cavity and, after its lumen has broken through into that
cavity, it may be recognised as the rudiment of the ciliated pit. The
posterior part of the vesicle which soon loses its lumen is the rudi-
ment of the ganglion proper, in which a peripheral layer of ganglionic
cells and a central accumulation of punctate tissue (Leydig's Punkt-
substanz) develop. The peripheral nerve-strands also soon grow out.
A dorsal outgrowth from the ganglionic rudiment forms the rudiment
of the eyes which, in the buds, develop somewhat otherwise than in
the embryo. [See on the development of the eyes, Seeliobr (No. 105)
and Metcalf (Nos. 99, 99a, and I.).]
The mesoderm of the stolon, which is represented by a mesenchyme
filling the primary body-cavity and by the Brooks' muscle-tubes,
gives rise to the connective tissue, the blood-vessels, the pericardial
vesicle, the elaeoblast and the body -uiusculature. We are not in a
position, however, to make any more definite statements as to the
SALPA — DEVELOPMENT OF THE ORGANS IN THE BUD. 511
origin of these organs. According to Brooks, the muscle-tubes give
rise to the body-musculature. We may no doubt assume that the
paired segments of these tubes spread out on either side of the bud
and thus yield muscle-plates, which become fenestrated and then
break up into the muscle-hoops.
The rudiment of the genital organs is yielded by the genital strand
(Figs. 264, 265, r/). We have already seen (p. 497) that young egg-
cells can early be i*ecognised within this strand. These at first are
very plentiful, but many of them disintegrate later and seem to serve
as food for the developing eggs. When the genital strand is ready
to break up into segments, the eggs become arranged in such a way
that only one occurs in each division. The smaller peripheral cells
of the genital strand yield the egg-follicle, the oviduct and (according
to Seeliger) probably also the rudiment of the testis. Even in
-v*
A~"
Fig. 278. — Chain-form of Saljoa democratica-mucronata from the distal part of an
advanced stolon (after Seeliger). c, atrium ; e, atrial aperture ; eb, elaeoblast ;
es, endostyle ; fg, ciliated pit; g, ganglion ; A. rudiment of testis; hf, connecting
process ; hz, heart ; i. branchial aperture ; in, intestine ; k, gill ; m, stomach ;
oc, eye ; od, oviduct : oe, oesophagus ; ov, egg-follicle ; j>/;., pharynx.
early stages, it is evident, in cross-sections through the stolon, that
a group of cells becomes detached in each segment from the lower
part of the genital strand, and this probably is to be regarded as the
rudiment of the testis (Fig. 264, c, h).
The rudiment of the genital organs originally lies at the posterior
end of each bud. Later the egg-follicle shifts farther forward on the
dorsal side and then lies above the intestinal loop in the dorsal median
line. From this point the oviduct turns to the right with an S-shaped
curve and becomes connected on the right side of the body with the
epithelium of the atrial cavity (Fig. 278, ov and od). The watch-
glass-shaped rudiment of the testis (h) remains longer at the posterior
end of the body curved round the posterior end of the intestinal loop.
At a later stage it breaks up into separate tubes which unite to form
512 TUNICATA.
;i common efferent duct that opens out into the atrial cavity between
the intestine and the stomach on a papilla-like prominence (see
Salensky, Nos. 101 and 102, and Seeligek, No. 105). The testis
develops comparatively late in the chain-form.
5. The Interpretation of the Alternation of Generations
in the Tunicates.
Alternation of generations is found among the Tunicates in a
marked form in Pyrosoma, Doliolnm and Salpa. This fact has
long attracted the attention of zoologists, who have attempted to
explain it in many different ways. We shall adopt the view first put
forward by Leuckart (No. 98) and accepted later by Claus;: and
Grobben (No. 79) that alternation of generations in the Tunicates
must lie regarded as having arisen in consequence of the formation of
stocks through division of labour, and we shall follow Grobben's
clear exposition of this view. Among more recent descriptions we
may specially mention those of Uljanin (No. 86) and Seelicjek
(No. 106).
The Larvaeea, which are conjectured to be the most primitive of
all existing Tunicates, develop through sexual reproduction. Tins
seems to suggest that the capacity for asexual reproduction (by means
of buds) was acquired as a consequence of the attached manner of
life. Asexual reproduction is indeed very common among attached
animals. We may, with Grobben, suggest as the cause that the
abandonment of locomotion left a larger proportion of the substance
of the body available for reproduction, so that it was possible for
attached animals to introduce a new method of multiplication into
the cycle of their development. It may also, however, lie added that
when, in consequence of attachment, cross-fertilisation became more
difficult, the capacity for asexual reproduction would become of special
importance for the maintenance of the species.
It is evident that, originally, all the individuals of forms which had
developed this character were equally able to reproduce themselves
either sexually or ase.xuallv.
Asexual multiplication led to the formation of stocks, the buds
being either altogether incapable of separating from the parent or
else able to do so only incompletely. All individuals were thus at
first capable, by asexual multiplication, of increasing the size of the
colony to which they belonged, or else by sexual multiplication of
* Grundz. d. Zool. 4 Aufl.
ALTERNATION OF GENERATIONS IN THE TUNICATES. 513
founding new colonies. Such a condition is found, for example, in
the Ascidiozooids ofPyrosoma, which produce stolons and also maturate
genital products.
The distribution of these two kinds of reproduction among various
individuals of the colony must be regarded as a later, derived condi-
tion through which the first individuals arising in a colon}' then
became adapted exclusively for increasing the colony by budding,
while the lateral individuals formed new colonies by sexual reproduc-
tion. Such an arrangement, in which we see the first commencement
of alternation of generations, is found in the composite Aseidians.
Ganin, following the investigations of Krohn, established that, in
this case, the individuals developing from the egg are capable of
asexual reproduction only, and in this way lay the foundation of
the colonies, while the descendants of these individuals, produced
by budding, again develop genital products.
In Sitl [in we find this condition more marked, and established
as a regular alternation of two generations, one reproducing only
asexually and the other only sexually. At the same time the two
generations vary to a certain degree in the structure of the body.
Grobben has rightly pointed out that these variations may be
explained by the different conditions of life and the different work
to be carried out by the two generations. The points that project
at the posterior end of the " nurse" of Salpa democratica-mucronata
(Fig. 262) serve as a protection for the proliferating stolon which
occurs in that region of the body. This "nurse*' of S. democratica-
mucronata further possesses one muscle-hoop more than the sexual
animal, and this is explained on the ground that, owing to the
presence of the massive proliferating stolon, greater muscular power
is required in this case to enable the animal to swim with equal
rapidity. On the other hand, the form of the sexual indi vidua
(that belonging to a chain) may be explained by the crowding of the
buds on the chain.
It follows from the above that the solitary form and all the indi-
viduals of the chain produced by it must be regarded as members of
one and the same colony. The solitary (" nurse ") form is the
founder of the colony, while the individuals of the chain produced
asexually give rise to the foundation of new colonies in producing
sexually new solitary forms.
The heteromorphous development of the individuals of the Salpa
colony recalls the polymorphism of the Siphonophora. Polymorphism
is still more strongly marked in the Doliolidae, where we have, in
LL
514
TUNICATA.
the barrel-shaped " nurse," the lateral and the median buds of differ-
ently formed individuals of one and the same stock (pp. 388 and 474).
In Pyrosoma, the alternation of generations consists of successive
generations of Cyathozooids and Ascidiozooids. The Cyathozooid
corresponds to the solitary form of Salpa, but remains in an un-
developed condition, its development being restricted to the embryonic
period. It reproduces itself only asexually. The Ascidiozooids, on
the contrary, besides multiplying sexually, have retained the capacity
for budding, and therefore, in the cycle of generations of Pyrosoma,
one generation (Cyathozooid) produced from the egg, alternates with
several generations (Ascidiozooids) which have arisen through bud-
ding.
The alternation of generations which takes place in the Doliolidae
has already been described in detail (p. 474).
The alternation of generations in the Tunicates must therefore be
derived from colony-formation and must be regarded as a case of
division of labour (Leuckart). The only difficulty that remains to
be explained is in what way the hypothetical ancestors of the
Tunicates which became attached acquired the capacity for repro-
duction by budding. It is not easy to understand how an animal
which had always reproduced itself sexually should come to produce
buds. There is considerable evidence tending to show that, in the
Tunicates, budding developed out of fission. The asexual repro-
duction of Amaroucium especially must be regarded as an actual
process of division (p. 449). We are therefore justified in assuming
that the hypothetical ancestors of the Tunicates, besides their sexual
multiplication, at first reproduced themselves through fission, and
that the later budding and stolon-formation developed out of this
manner of reproduction.
Balfour* and Uljanin (No. 86) have tried to remove the
difficulty which arises if we regard the capacity for multiplication
by fission as acquired only after attachment, by suggesting that this
process appears first in the embryos. According to this view, the
Tunicates first acquired a capacity for dividing in the first embryonic
stages, as is the case in Lumbricus trapezoids (Vol. I., p. 281), a
capacity which was only secondarily passed on from the embryonic
stages to the adult form. But when we remember the great capacity
for regeneration possessed by the Tunicates (p. 448) we shall hardly
find it necessary to fall back on such an hypothesis. There is no
* Text-book of Comp. Embr., Vol. II., p. 34 (footnote) 2nd edit., 1885.
ALTERNATION OF GENEBATIONS IN THE TUNICATES. 515
reason why we should not assume that the capacity for division was
not possessed by the adults from the first, indeed, this capacity may
possibly have been inherited directly from older pelagic ancestors
of the Tunicates. For, even if the circumstance that the Larvacea
do not multiply asexually seems to indieate that this form of re-
production was acquired only after attachment, we are not sure that
this was the ease.
Seeliger, who attributes to the mesoderm the principal part in
the development of the proliferating stolon, and who derives the
mesoderm of the stolon, at any rate in Pyrosoma, from the genital
tissues of the parent, finds in the limitation of sexual reproduction
the cause for the development of buds, the material left in the
ovary after the production of a single egg is utilised in its plastic
capacity as the mesoderm of the stolon. But even if we make this
assumption, the manner in which budding was acquired remains
obscure.
Further confusion has been introduced into the views as to the
alternation of generations in the Tunicates by the fact that the egg
cells frequently maturate very early in the buds. They can even be
distinguished in the genital strand of the stolon in Pyrosoma and
Salpa. This has, in many cases, led to the view that the ovary
actually belongs to the solitary form and is merely deposited in the
forms composing the chain. This view, which is adopted by Brooks
(Nos. 88-91) does not seem justifiable to us. We prefer Seeliger's
view that the egg with its follicle is just as much an organ of
the individual of the chain as are all the other organs. The early
differentiation of the egg-cells is to be traced back to the effort on
the part of the organism to arrive at sexual maturity as early as
possible. The same hastening of sexual maturity is found in the
Hydroids and, indeed, in the parthenogenetic CladoCera and Aphidae
and also in the Diptera (polar cells).
P>kooks regards all the ovaries of the individuals of a Salpa-chain taken
together as the germ-gland of the solitary form shifted into the stolon. He
considers the solitary forms not as sexless but as females, while he regards the
individuals of the chain as males which have arisen from the females as buds.
The solitary form deposits an egg in each male, and this, when fertilised,
deveiup-^ into a female. Brooks therefore reduces the alternation of genera-
tions of Salpa to a kind of sexual dimorphism.
We have already stated (p. 496) that Todaro, by deriving all the buds from
certain embryonic germ-cells (germoblasts), and by tracing these latter directly
to the blastomeres of the embryo, regards the individuals of a Salpa-chain not
as the descendants of the solitary form hut merely as younger members of the
516 TUNICATA.
same generation. Todabo would, however, strictly speaking, not be justified
in assuming an asexual multiplication of the embryo in early stages of
embryonic development.
Salensky (Nos. 74 and 102) traces back the alternation of generations of
the Tunicates to metamorphosis. The acquisition of the capacity for asexual
reproduction by the larvae of the Tunicates, or, in other words, the shifting
back of this capacity originally belonging to adult forms to larval stages,
made it possible to spread out over several generations the series of trans-
formations which constitute metamorphosis. In this way we can explain the
dimorphism of the generations. Salensky consequently regards the solitary
form as a larval stage and the individuals of the chain as the adults. We,
however, with Leuckart (No. 98), hold on the contrary that we are justified
in regarding the solitary form just as much as the individual of the chain as
a fully developed individual.
III. General Considerations on the Tunicates.
If we attempt to draw from the ontogeny of the Tunicates con-
clusions of a more general nature, we are at once struck by the
difference of opinion prevailing among the various investigators of
this subject. As an example of this, we may mention that the
central nervous system in the larvae of the Ascidiacea is traced back
to an ectodermal invagination ; in the buds of the composite Ascidians,
on the contrary, according to statements made by Kowalevsky and
recently confirmed by H.iort (No. 59), it is derived from the ento-
derm of the bud.* In the Cyathozooid of Pyrosoma, and probably
also in the first four Ascidiozooids, it is derived from the ectoderm,
whereas Seeligek, in all the later-developed Ascidiozooids of the
colony, as in the buds of the Salpidnc, traces it back to the meso-
derm. Similar uncertainty prevails with regard to the development
of the peribranchial cavities and the atrium. We are also in doubt
as to howr far the ectoderm and entoderm take part in their formation
in Ascidian larvae, but in the Cyathozooid of Pyrosoma, in any case,
they are derived exclusively from the ectoderm. Nearly all authors,
however, are agreed that the peribranchial sacs become abstricted
from the central entoderm-sac in the buds of the Ascidiacea. In the
buds of the Salpidae and in the later Ascidiozooids of Pyrosoma,
Seeligek derives the peribranchial tubes from the mesoderm. It is
difficult to decide how far this difference of opinion can be accounted
for by errors of observation or to what extent actual differences exist.
We, for instance, find it difficult to assume that the buds of Pyrosoma
develop in a totally different way from those of the nearly related
* [See footnote, p. 466. — Ed.]
GENERAL CONSIDERATIONS ON THE TUNICATES. 51*S
composite Ascidians. We must await the result of farther researches
before coming to any definite conclusion.
In any case, the development of t lie buds must always lie considered
quite apart from embryonic development, since these two methods
of development are to be traced back to different principles. In
the embryo, the primary organs arise anew from an originally
undifferentiated mass of blastomeres, while in budding, which is
evidently deducible from division, parts of the most important
primary organs are taken over from the organisation of the parent
into the bud. Although the literature on the budding of the Tuni-
cates at present is far from supporting the statement that all the
more important organs in the bud or the stolon are to be derived by
abstriction from the corresponding organs of the parent, indications
are not wanting that the solution of the problem as to the origin of
the organs of the bud is to he sought in this direction (p. -1ST). It
appears, for instance, that the strands which, compose the rosette-like
organ of Doliolum are direct continuations of all the more important
organs of the parent. In the four primary Ascidiozooids of Pyrosoma
dso, the peribronchial tubes and the pericardial rudiment of the
Cyathozooid are directly continued. It may be mentioned further
that, according to Koyvalevsky, the peribranchial tubes in the stolon
of Salpa are derived from the atrium of the parent. These state-
ments which, however, are in direct contradiction to many observa-
tions on other forms suggest that none of the more important organs
airist anew in the bud, but that all the mort important rudiments of
organs pass over from the parent into the stolon and thence into the
buds, while tin actual new formation of organ-rudiments takes place
only in the embryo. The nervous system would probably have to be
considered as an exception to this rule. Since we know that the
brain of the Ascidian can be regenerated after excision, it appears
possible that it arises anew also in the buds, though probably only
from the ectoderm.
Turning to the embryonic development, we rind that the different
divisions of the Tunica ta here also vary greatly. The embryouic
development of the Salpidae is, indeed, so little understood that we
are hardly in a position to say anything definite about it. When we
see that, according to Salensky, all the species examined show
important variation in their methods of development, it is evident
that there is here an ample Held for further research.* We may.
[*See footnote, p. 123 and pp. 445-446.— Ed.]
518 TUNICATA.
however, say that in Pyrosoma, as well as in the Salpidae, the
embryonic development has undergone great coenogenetic variation.
In Pyrosoma, the accumulation of food-yolk, and, in Salpa, the fusion
of the embryo with the body of the parent as well as other conditions
have brought about such variations. In both cases, development is
direct, and, as compared with the development of the Ascidians, much
abbreviated. The suppression in the embryonic development of the
Sulpiride of so important an organ as the chorda dorsalis is of interest.
In the Cyathozooids of the Pyrosoma, also, this organ does not develop
distinctly, although Salensky thought that he found a trace of its
rudiment. The chorda-rudiment is also wanting in the buds of all
Tunicates. Salensky, indeed, regarded the elaeoblast, that pro-
visional organ of the Salp embryo, as the rudiment of the chorda,
but the fact that the elaeoblast also occurs in the buds of Pyrosoma
and Salpa, while other provisional larval organs are not found as
rudiments in these buds, throws doubt upon this view. It is found,
for example, that the nervous system in the second individuals pro-
duced by budding in the larval Diplosoma no longer show the larval
character (p. 459). The elaeoblast is wanting in the buds of the
composite Ascidians and the Doliolidae, nor does its rudiment appear
in the Cyathozooids of Pyrosoma.
Salensky maintains that, in the chief groups of the Tunicata, the
follicle-cells take part in the formation of the embryo. We are
somewhat sceptical as to these statements, which will be found more
in detail on pp. 357, 392 and 421 and think that this supposed
participation may be reduced to the absorption of the follicle-cells as
nourishment by the blastomeres [see footnote, pp. 420 and 421].
It is evident from the above that, in judging of the systematic
position and phylogeny of the Tunicates, we are dependent almost
entirely on the embryonic development and metamorphosis of the
Ascidiacea. Among these, the solitary forms and Clavelina have
yielded the most valuable material, while the eggs of the composite
forms, which are rich in yolk, show a derived condition.
Among the Tunicates now living, Appendicularia is regarded as
showing in its organisation the most primitive conditions. We must,
however, raise the question as to how far these conditions are really
primitive. The Larvacea show remarkable resemblance in their
structure to the free-swimming tailed Ascidian larvae, from which
they are distinguished chiefly by the absence of a common atrial
cavity, the anus and the two peribranchial tubes opening out
independently on the ventral side of the body. Since the abbrevia-
*
GENERAL CONSIDERATIONS ON THE TUNICATES. 519
tion of the dorsal region found in the Ascidians and the approxima-
tion of the branchial and atrial apertures thus brought ahout is
Jfraced back to attached forms, the position of the anus in the
" Larvacea, which must evidently be regarded as primitive, would
indicate thai these animals are descendants of those hypothetical
Tunicate ancestors which still retained the original pelagic life.
<>n the other hand, we find in Appendicularia a series of unmistakable
degenerative phenomena tending t<> support the assumption that we
must regard the racial form of the Larvacea as an attached Tunicate.
It is evident that they must be considered as sexually mature larval
tonus, sexual maturity being shifted continually further back to
earlier stages so that, finally, the mature adult form no longer
developed. What form can we imagine this latter to have assumed I
Was it a free swimming Ascidian form intermediate between AmphioxUs
and the Ascidian larva, or an already attached Ascidian form ' The
last assumption seems the more probable. The appearance of the
cellulose mantle and hermaphroditism and the indistinctness of the
segmentation of the body must be regarded as features acquired as
a consequence of attached manner of life. As these characters are
found in the Larvacea, we are to a certain extent justified in con-
sidering them as the sexually mature larvae of an already attached
form of Tunicate.* In any case, however, all phylogenetic specula-
tions concerning the Tmiicates must rest upon careful consideration
of the structure of Appendicularia and the Ascidian larvae.
Among the Ascidiacea the solitary forms are probably the more
primitive. The composite forms lead on to Pyrosoma, which may lie
regarded as a composite colony that has not become attached and
that is distinguished by a large common cloaca. In the interesting
family Coelocormidae we see the development of the whole colony in
a similar direction. Here also the colony is not attached but, on the
other hand, the internal cavity cannot be compared to the common
doaca of Pyrosoma (see Herdman, No. 24). Pyrosoma forms
a transition to the free-swimming Doliolidae. This was pointed out
by Huxley with reference to the structure of the gill and the
opposite position of the two apertures of the body (n true homology. Among these are : the presence of a dorsal
neural tube which, in early stages, opens externally through the
neuropore; the possession of a chorda dorsalis extending between
this and the alimentary canal ; the transformation of the anterior part
of the alimentary canal into a respiratory region perforated by lateral
gill-slits, the ventral side of which region is occupied by the hypo-
branchial groove (endostyle) ; and, finally, the transformation of 'the
posterior part of the body into a locomotors organ provided with an
unpaired marginal fin, while the intestinal rudiment at this part
degenerates. The first stages of development in these two forms
are also strikingly alike. Only recently van Beneden and Julin
(p. 349), who, however, are not supported by Davidoff, have made
statements as to the development of the mesoderm and the chorda
dorsalis winch would render the agreement between these two groups
almost complete. We are, therefore, justified in regarding the
Tunicata and the Cephalochorda which lead on to the Vertebrates,
as members of a large common group, the Chordata, and to derive
them from a common racial form (the Protochordata). We must
imagine this racial form as a pelagic, segmented animal, provided
with gill-slits and a chorda. The Tunicates, as compared with such
a form, are to some extent degenerate, this being due, on the whole,
to their attached manner of life, while, in another direction, their
organisation is more highly developed. This is the case, for instance,
in the pharyngeal region which has undergone considerable enlarge-
ment and specialisation.
Among the indications of degeneration found in the body of the
Tunicates we should first mention the loss of the coelom and the
GENERAL CONSIDERATIONS ON THE TUNICATES. 521
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region of the A.scidian larvae and of A/>jn'u'.
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63. Krohn, A. Ueber die friiheste Bildung der Botryllenstocke..
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64. Jourdain, S. Sur les Aseidies composees de la tribu des.
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66. Seeliger, O. Zur Entwicklung der Ascidien. Eibildung and
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67. Uljanin, B. Bemerkungen uber die Synascidiengattung
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68. Della Valle, A. Nuove contribuzioni alia storia naturale
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69. Della Valle, A. Sur le bourgeonnement des Didemnides et
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70. Della Valle, A. Sul rihgiovanimento delle colonie de
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Pyrosoma.
71. Kowalevsky, A. Ueber die Entwicklungsgeschichte der-
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LITERATURE. 529
72. Huxley, Th. H. Anatomy and Development of Pyrosoma.
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7.*1 Joliet, L. Etudes anatomiqu.es et embryogeniques sur le
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74. Salensky, W. Beitrage zur Entwicklungsgeschichte der
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75. Seeliger, 0. Bemerkungen zu Herrn Prof. Salensky's
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An:. Jahrg. xv. 1892.
76. Seeliger, O. Zur Entwicklungsgeschichte der Pyrosomen.
.Una. Zeitschr. f. Naturw. Bd. xxiii. 1889.
76a. Seeliger, O. Ueber die erste Bildung des Zwitterapparates
in den jungen Pyrosomenstocken. Festschrift fur Leuckart.
Leipzig, L892.
Doliolum.
77. Barrois, J. Reeherches sur le cycle genetique et le bourgeon-
nement de l'Anchinie. Journ. Anat. Phys. Pan's. Ann. xxi.
1 885.
78. Gegenbaur, C. Ueber den Entwicklungscyclus von Doliolum
nebst Bemerkungen uber die Larven dieser Tbiere. Zeitschr.
f. wiss. Zool. Bd. vii. 1856.
79. Grobben, C. Doliolum und sein Generationswechsel. Arb.
Zoo!. Inst. Wien. Bd. iv. 1882.
80. Huxley, Th. H. Remarks upon Appendicularia and Doliolum.
Phil. Trans. London. 18:11.
81. Keferstein und Ehlers. Zoologische Beitrage. Leipzig,
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82. Korotnkff, Al. de. La Dolchinia mirabilis. Mitth. Zool.
Stat. Neapel. Bd. x. 1891.
83. Korotneff, A. Die Knospung der Anchinia. Zeitschr. f.
wiss. Zool. Bd. lx. I. ssi.
84. Kowalevsky, A., et Barrois, J. Materiaux pour servir a
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85. Krohn, A. Ueber die Gattung Doliolum und ihre Arten.
Archiv.f. Naturg. Bd. xviii. 1852.
86. Uljanin, B. Die Arten der Gattung Doliolum im Golfe von
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MM
530
TUNICATA.
Salpa.
87. Barrois, J. Memoire sur les membranes embryonnaires des
Salpes. Journ. Anat. Phys. Paris. Ann. xvii. 1881.
88. Brooks, W. K. On the Development of Salpa. Bull. Mus.
Comp. Anat. Harv. Coll. Camb. Vol. iii. 1871-1876. Cf.
Archiv. fur Naturg. Bd. xlii. 1876.
89. Brooks, W. K. The Origin of the Eggs of Salpa. Stud. Biol.
Lab. Johns Hopkins Univ. Baltimore. Vol. ii. 1882.
90. Brooks, W. K. Chamisso and the Discovery of Alternation of
Generations. Zool. Anz. Jahrg. v. 1882.
91. Brooks, W. K. Is Salpa an Example of Alternation of Genera-
tions 1 Nature. Vol. xxx. 1884.
92. Brooks, W. K. The Anatomy and Development of the Salpa-
chain. Stud. Biol. Lab. Johns Hopkins Univ. Baltimore.
Vol. iii. 1886.
93. Brooks, W. K. On the Relationship between Salpa and
Pyrosoma. Johns Hopkins Univ. Circ. Vol. 9. 1890.
94. Butschli, O. Einige Bemerkungen uberdie Augen derSalpen.
Zool. Anz. Jahrg. xv. 1892.
94a. Goppert, E. Untersuchungen iiber das Sehorgan der Salpen.
Morph. Jahrb. Bd. xix. 1892.
95. Huxley, Th. H. Observations on the Anatomy and Physiology
of Salpa and Pyrosoma. Phil. Trans. 1851.
96. Kowalevsky, A. Beitrag zur Entwicklung der Tunicaten.
Nachr. kgl. Gesellsch. Wissensch. Gottingen. 1868.
97. Krohn, A. Observations sur la generation et le developpement
des Biphores. Ann. Sri. Nat. (3). Tom. vi. 1846.
98. Leuckart, R. Salpa, and Verwandte. Zool. Untersuchungen,
Heft. ii. Giessen, 1854.
99. Metcalf, M. The Anatomy and Development of the Eyes
and Subneural Gland in Salpa. Johns Hopkins Univ. Circ.
No. 97. 1892.
99a. Metcalf, M. On the Eyes, Subneural Gland and Central
Nervous System in Salpa. Zool. An::. Jahrg. xvi. 1893.
100. Salensky, W. Ueber die embryonale Entwicklungsgeschichte
derSalpen. Zeitschr. f. wiss. ZjooI. Bd. xxvii. 1876.
101. Salensky, W. Ueber die Knospung der Salpen. Morph Jahrb.
Bd. iii. 1877.
102. Salensky, W. Ueber die Entwicklung der Hoden and iiber
don Generationswechsel dor Salpen. Zeitschr. f. wiss. Zool.
Bd. xxx. Suppl. L878.
LITERATURE. 531
103. Salensky, W. Folliculare Knospung der Salpen und die
Polyeinbryonie der Pflanzen. Biol. Central bl. Bd. v. 1885.
104. Salensky, W. Neue Untersuchungen iiber die embryouale
Entwioklung der Salpen. Mitth. Zool. Stat. Neapel. Bd. iv.
1883. In two parts.
105. Seeliger, Osw. Die Knospung der Salpen. Jen. Zeitschr.
fiir Saturn:. Bd. xix. 1886.
106. Seeliger Osw. Die Entstehung des Generationswechsels der
Salpen. Jena. Zeitschr. f. Naturw. Bd. xxii. 1888.
107. Todaro, Fr. Sopra lo sviluppo e l'anatoniia delle Salpe. Atti.
R. Accad. Lincei. Trans. (2). Vol. ii. 1875.
108. Todaro, Fr. Sui primi fenomeni dello sviluppo delle Salpe.
Atti. R. Accad. Lincei. Trans. (3). Vol. iv. 1880.
109. Todaro, Fr. Sui primi fenomeni dello sviluppo delle Salpe.
2da uommunic. preliminare. [Atti. R. Accad. Lincei. Trans.
Vol. vi. 1882. (Also in Archiv. ltal, Biol. Tom. ii. 1882.)
110. Todaro, Fr. Sui primi feuomsni nello sviluppo delle Salpe.
3a comin. prelim. Atti. R. Accad. Lincei. Trans. Vol. vii.
1883. (Also in Archiv. Red. Biol. Tom. iii. 1883,)
111. Todaro, Fr. Sopra i eanali e le fessure branchiali delle Salpe.
Atti. R. Accad. Lincei. Trans. Vol. viii. 1884.
112. Todaro, Fr. Studi ulteriori sullo sviluppo delle Salpe. Atti.
R. Accad. Lincei. Mem. (4). Vol. i. 1886.
113. Todaro, Fr. Sull' omologia della branchia delle Salpe con
quella degli altri Tunicati. Atti. R. Accad. Lincei. Rend. (4).
Vol. vi. 1889. (Also in Archiv. Ltal. Biol. Tom. xi. 1889).
APPENDIX TO LITERATURE OX TUXICATA.
I. Brooks, W. K. The genus Salpa. Mem. Johns Hopkins
Univ. L893.
II. Castle, W. E. Early Embryology of Ciona intestinalis.
Butt. Mus. Harvard. Vol. xxvii. 1896.
III. Castle, W. E. On the Cell-lineage of the Ascidian egg.
Proc. Amer.Acad. Vol. xxx. 1894.
IV. Caulekv, M. Contributions a l'Etude des Ascidies com-
posees. Bull. Sri. France et Belgique. Tom. xxvii.
L895.
V. Caulery, M. Sui- la Morphologie de la Larve comjwsee
d'une Synascidie (Diplosomoides Lacazii, G-iard). C<>/n/>t.
Rend. Acad. Sci. Paris. Tom. exxv. 1897.
532 TUNICATA.
VI. Cauleky, M. Sur le Bourgeonnement des Diplosoniidae
et des Didemnidae. Gompt. Rend. Acad. Sci. Paris,
Tom. cxxi. 1895.
VII. Cauleey, M. Sur 1' Interpretation rnorphologique de la
larve, etc., du genre Diplosoma. Gompt. Rend. Acad.
Sci. Pari*. Torn. cxxi. 1895.
VIII. Cauleky, M. Sur les Synascidies du genre Colella, et le
polymorphisme de leurs bourgeons. Gompt. Rend. An id.
Sri. Paris. Tom. cxxii. 1896.
IX. Damas, D. Les Formations epicardiques chez Ciona
intestinalis. Archiv. Biol. Tom. xvi. 1899.
X. Flodebus, M. tTber die Bildung der Follikelhullen bei
den Ascidien. Zeitschr. f.wiss. Zool. Bd. lxi. 1896.
XI. Gaestang, W. Budding in Tunicata. Science Prot/ress.
Vol. iii. 1896.
XII. Giabd, A., et Cauleey, M. Sur 1'HiYernage de la
Clavelina lepadiformis. Gompt. Rend. Acad. Sci. Paris.
Tom. cxxiii. 1896.
XIII. Heideb, K. Beitrage zur Embryologie von Salpa fusi-
formis. Frankfurt, 1895. (Ahh. Senkenb. Ges. Bd.
xviii.)
XIV. Hjobt, J. Beitrage zur Keimblatterlehre und Entwick-
lungsmekanik der Ascidienknospung. Anat. An,;:. Bd. x.
1895.
X V. Hjobt, J. Ueber den Entwicklungcyclus der zusammen-
gesetzten Ascidien. Mittheil. Zool. Stat. Neapel. Bd. x.
1893.
XVI. Hjobt, J., und Bonnevie, Fe. Ueber die Knospung von
Distaplia magnilarva. Anat. Anz. Bd. x. 1895.
XVII. Julin, C. Rechercbes sur la blastogenese chez Distaplia
magnilarva et D. rosea. Gongr. Zool. Leyden. 1896.
X VIII. Kobotneff, A. Embiyonale Entwicklung der Salpa demo-
cratica. Biol. Gentralbl. Bd. xiv. 1894; and Zeitschr.
f. iris*. Zool. Bd. lix. 1895.
XIX. Kobotneff, A. Tunicatenstudien. Miff//. Zool. Stat.
Neapel. Bd. xi. 1895.
XX. Kobotneff, A. Zur Embryologie von Salpa cordiformis-
zonaria und musculosa-punctata. Mitth. Zool. Stat..
Neapel. Bd. xii. 1896.
XXa. Kobotneff, A. Zur Embryologie von Salpa runcinata-
fusiformis. Zeitschr/'. wiss. Zool. Bd. lxii. 1896.
LITERATURE. 533
XXI. Korotneff, A. Zur Entwicklung der Salpen. Biol.
Centralhl. Bd. xv. 1895.
XXIa. Korotneff, A. Zur Embryologie von Salpa maxima-
Africana. Zeitschr.f. wiss. Zool. Bd. lxvi. 1899.
XXI 1. Lefevre, G. Budding in Ecteinascidia. Anat.Anz. Bd.
xiii. ; and Joint* Hopkins Univ. Give. 1897.
XXI II. Lefevre, G. On budding in Perophora. John* Hopkins
Univ. Girc. Vol. xiv. 1895.
XXIV. Metcalf, M. The follicle-cells of Salpa. Zool. Anz.
Jahrg. xx. 1S97 ; and Johns Hopkins Univ. Giro.
1897.
XXV. Pizon, A. Contributions a l'Embryogenie des Ascidies
simples. Gompt. Rend. Acad. Sci. Pari*. Tom. cxx.
1895.
XXVI. Pizox, A. Histoire de la Blastogenese chez les Botryllides.
Aim. Sri. Nat. Tom. xiv. 1893.
XXVIa. Pizox, A. Evolution des elements sexuels chez les
Ascidiens composes. Gompt. Bend. Acad. Sci. Paris.
Tom. cxix. 1894.
XXVII. Pizon, A. Les Membranes embryonnaires et les Cellules
de rebut chez les Molgules. Gompt. Rend. Acad. Sci.
Pari*. Tom. cxxii. 1896.
XXVIII. Ritter, W. E. Budding in Compound Ascidians based
on studies on Goodsira and Perophora. Jo/irn. Morpliol.
Vol. xii. 1896.
XXIX. Salexsky, W. Beitrage zur Entwicklungsgeschichte d.
Syuascidien (Diplosoma and Didemnum). Mitth. Zool.
Stat. Neapel. lid. xi. 1895.
XXX. Salenskv, W. Morphologische Studien an Tunicaten.
Nervous system and Metamorphosis of Distaplia). Morph.
Jahrb. Bd. \x. 1893.
XXXI. Salensky, W. Ueber die Entstehung der Metagenesis bei
Tunicaten. Biol. Central hi. Bd. xiii. 1893.
XXXII. Samassa, P. Zur. Keuntniss der Furchung bei den Asci-
dien. Archiv.f. mikro. Anat. Bd. xliv. 1894.
XXXIII. Seeliger, O. Einige Beobachtungen iiber die Bildung
der auesseren .Mantels der Tunicaten. Z eitschr. f. wiss.
Zool. Bd. lvi. 1893.
XXXIV. Seeliger, 0. Ueber die Kntstehung des Peribranchial-
raums in den Embryonen der Ascidien. Tom. fit.
534 TUNICATA.
XXXV. Todaro, F. Sopra lo Sviluppo della parte anteriore del
corpo delle Salpe. Atti. R. Acad. Lincei. Rend. (3).
Vol. vi. 1897.
XXXVI. Widley, A. Studies on the Protochordata. Parts II. and
III. (nervous system, sense-organs and mouth). Quart.
Journ. Micro. Sci. Vol. xxxv. 1893.
XXXVII. Willey, A. Amphioxus and the Ancestors of the verte-
brates. London and New York. 1894.
CHAPTER XXXVI.
CEPHALOCHORDA.
Amphioxus.
The earlier statements concerning the development of Amphioxus
made by Max Schultze (No. 18), Leuckart and Pagenstecher
(No. 15) referred merely to a few of the later larval stages ; our
knowledge of the ontogeny of this form is, therefore, founded princi-
pally on the investigations of Kowalevsky (Nos. 10 and 11), and was
extended by Hatschek (Nos. 4 and 8). The metamorphosis of
Amphioxus has recently been described by Ray Lankester and
Willey (No. 13) and by Willey alone (No. 23). The develop-
ment of the genital organs has been investigated by Boveri (No. 3).
This last author (No. 2) as well as Spengel (No. 19), Ray Lankester
(No. 12) and van Wuhe have also published treatises on the anatomy
of the adult Amphioxus to which we shall have occasion to refer.*
A. Oviposition, Cleavage and Gastrulation.
The mature genital products of Amphioxus pass from the genital
chambers, through rupture of their walls, into the atrial cavity and
thence they were said to pass through the gill-clefts into the pharynx
and to be ejected through the mouth (Kowalevsky, Hatschek).
According to Ray Lankester and Willey, however, they are, in
most cases, ejected through the atriopore. Fertilisation takes place
in the surrounding water. The newly laid egg is surrounded by a
vitelline membrane at first only slightly separated from it, but, under
the influence of the sea water, the interval between the egg and the
•[More recently, Sobotta (No. XI.) and Sticht (No. XII.) have rein-
vestigated the maturation and fertilisation of the egg, and the former,
Klaatsch (No. IV.) and Macbride (No. VIII.) have re-examined the forma-
tion of the germ-layer.— Ed.]
536 CEPHALOCHORDA.
membrane becomes greater. There is no micropyle. The spermatozoa
pass through this elastic membrane to reach the egg.*
The tirst stages of development closely resemble those of the
Ascidians. Cleavage is total and almost equal (adequal type of
Hatschek). The tirst furrow is meridional and appears tirst at
the animal pole, where for some time it is deepest ; it eventually
divides the egg into two exactly equal parts (Fig. 279 B). The
second furrow, which is also meridional, is at right angles to the tirst
and leads to the rise of four blastomeres of equal size which leave free
between them a cavity open above and below ; this is the cleavage-
cavity (Fig. 279 C and D). The eight-celled stage (Fig. 279 E) is
brought about by an equatorial furrow which lies somewhat nearer
the animal than the vegetative pole and leads to the tirst differentia-
tion between the blastomeres of the animal and vegetative halves.
The embryo consists of a circle of four smaller blastomeres near the
animal pole and another circle of four larger blastomeres belonging
to the vegetative pole. Further meridional furrows divide these eight
cleavage-spheres into sixteen, the sixteen-celled stage then consisting
of a circle of eight smaller and another of eight larger blastomeres
(F^ig. 279 F).
Even at this sixteen-celled stage, according to Wilson, certain individual
differentiations are found which influence the further course of cleavage. The
regular stage described by Hatschek, in which the eight cells of the upper
circle are found resting regularly on the eight cells of the lower circle, was
comparatively rarely observed by Wilson. The blastomeres of the upper
circle often appear shifted spirally in relation to those of the lower, as is found
to be the case in the Annelida and Mollusca. Most frecpaently, however, at
the sixteen-celled stage a bilateral (or strictly speaking a biradial) symmetry
is evident in the arrangement of the blastomeres, the eight cells of the vege-
tative half being divided into four larger and four smaller cells. The four
larger cells surround the vegetative pole in regular order, while the four
smaller cells are grouped in two pairs symmetrically to the median plane.
This median plane, according to Wilson, corresponds to the first cleavage-
plaue. A similar arrangement of the blastomeres was seen in the sixteen-celled
stage of the Ascidiaus.
The thirty-two-celled stage arises, according to Hatschek, in
iinisequeiice of further equatorial furrows. It consists of four rows
of eight cells each, one super-imposed above the other. ■ The dilated
cleavage-cavity, which was hitherto open at the animal and vegetative
poles, now becomes closed at these points. In the fui'ther course of
[* Only one polar body is generally said to be present at this stage (Fig.
279), but Sobotta (No. XI.) has recently discovered the presence of a second
one. — Ed. 1
CLEAVAGE AND (JASTKULATION.
537
D
E
F
G
If
Fig. 279. — Cleavage of Aw-phioxus (after Salenskt). A, egg before cleavage, with
the polar bodj ; />'. division into twOj the two cells being still connected by a band
i>i protoplasm; < '. tour-celled stage; I), the saint- seen from the pole; I'., eight-
celled stage ; /•'. sixteen-celled stage ; 67, stage showing more rapid division at the
animal pole : one of the circles of cells is in the act of dividing ; //. the same stage
in section ; /, blastula, surface view/ A", blastula, in section.
538
CEPHALOCHORDA.
cleavage, the circle of small blastomeres divides more rapidly, while
the circle of eight larger cleavage-spheres surrounding the vegetative
pole remains longer undivided (Fig. 279 G). In later stages, the
regular arrangement of the blastomeres in circles is obliterated and
the cells form an epithelium surrounding the cleavage-cavity, the
Uast'idctrstage being reached in this way (Fig. 279 /, K). The eoo-
at this stage, is lengthened in the direction of the future gastrula-
axis, and the wall at the vegetative pole, i.e., the posterior third of
the egg, is composed of somewhat larger cells richer in yolk-granules.
This represents the entodermal region of the embryo. In it flatten-
ing occurs, and this soon passes into an invagination (Fig. 280 A)
which leads to the development of a cap-shaped gastrula. The
invagination causes the cleavage-cavity to decrease in size and finally
completely to disappear, the two primary germ-layers coming into
close contact (Fig. 280 B).
C
Fig. 280. — Three consecutive ontogenetic stages of Amphwxus (after Hatschek),
showing the invagination of the entoderm. A, 'luring invagination ; B, after the
completion of invagination, right dorsal side, left ventral side ; (J, with narrowed
gastrula-mouth, orientation as in /!.
The gastrula-stage now passes through certain phases by means of
which the bilateral symmetry which, according to Wilson, is already
evident in the stages of cleavage, becomes more distinct, while at the
same time, the embryo elongates in the direction of its definitive
longitudinal axis. The apex of the ectoderm of the gastrula corre-
sponds to the animal pole, while the vegetative pole may be said to
coincide with the centre of the at first circular aperture of invagina-
tion. This latter soon becomes oval, and the plane of symmetry is
thus established. These later stages, seen in profile (Fig. 280 £),
show a point at which the curve is more abrupt ; this point does not
coincide with the animal pole but lies somewhat excentrically, corre-
sponding to the anterior end of the later principal axis, the posterior
DEVELOPMENT OF THE MEDULLARY TUBE, ETC. 539
end coinciding' with the posterior edge of the blastopore. The
definitive principal axis thus forms an acute angle with the primary
axis. The blastopore has undergone shifting to the dorsal side of
the embryo ; it now gradually decreases in size, chiefly through a
backward growth of its dorsal or anterior border. The posterior
(ventral) edge of the blastopore, on the contrary, remains stationary
during this narrowing process. It is always marked by two larger
entoderm-cells lying symmetrically to the median plane (Fig. 280 C) \
these are claimed by Hatschek as pole-cells of the mesoderm.*
Finally, the embryo becomes more elongated. The ventral surface
is distinguished by being arched, while the dorsal side, which was
originally occupied by the blastopore, is distinctly flattened. The
posterior end of the dorsal side is occupied by the now very small
vestige of the blastopore (Fig. 280 G). Even at this stage, the
external surface of the embryo is covered with short flagella which
enable it to rotate within the egg-envelope.
In the position of the blastopore and the conditions under which it closes,
there is close resemblance between Amphioxus and the Ascidia (cf. p. 342).
In our description of the transformations undergone by the gastrula-stage,
we have for the most part followed Hatschek. A rather divergent account
has recently been given by Lwoff (No. 17) who, in dealing with the closure
of the blastopore, lays the chief stress on the independent and rapid growth
of the ectoderm at its dorsal margin. (Sti'ess should also be laid on the
protrusion of the lateral edges of the blastopore, a point which was overlooked
by Lwoff). From this rapidly growing dorsal edge, ectodermal elements are
said to be invaginated dorsally into the gastrula-cavity and there finally to
force the proper entodermal elements from the dorsal to the ventral side of
the cavity. According to this view, the cells forming the dorsal wall of the
archenteron are ectodermal and it is from this cell-layer that Lwoff derives
the chorda. Lwoff was not able to convince himself of the presence of the
primitive cells of the mesoderm which Hatschek found marking the posterior
end of the longitudinal axis of the embryo.
B. Development of the Medullary Tube, the Primitive Segments
and the Notochord.
The next ontogenetic stages of Amphioxus are characterised by the
increase in length of the whole body. The median part of the dorsal
surface, at the same time, sinks in somewhat (Fig. 281), and this
* [Sobotta (No. X.) agrees with Lwoff (No. 17) in denying that the blasto-
pore closes from before backward. They believe that it gradually diminishes
on all sides. Sobotta was unable to find the pole-cells and does not believe
that they exist, at any rate at the early stages figured by Hatschek. — Ed.]
540
CEPHALOCHORDA.
depression leads to the development of the medullary tube. The
latter is here formed, not, as in the Ascidia and many Vertebrates,
through the fusion in the middle line of
two lateral medullary folds, the process,
although it may be deduced from the
above type, being somewhat modified.
It might be described as lateral over-
growth. The medullary plate (Fig. 282
A, hi))) sinks down somewhat and its
lateral edges become detached from the
rest of the ectoderm. The ectoderm (lib)
now grows inward from either side above
the medullary plate and unites in the
middle line before the plate has become
curved into a tube (Fig. 282 B). "The
dorsal groove, although completely
covered externally, is still open within,
under the integument " (Fig. 283). Only
later does the medullary plate curve round
dorsally, and, through the fusion of its
lateral edges, form a closed tube, the
medullary tube (Fig. 284).
The union of the lateral ectodermal growth above the medullary
plate takes place from behind forward, commencing near the remains
-TOt'
nip
Fig. 281. — Embryo of Amphi-
oarus with the rudiment of
two primitive segments (after
Hatschek). mp, pole-cells
of the mesoderm ; //*/-, medul-
lary groove ; m/' medullary
tube ; its', first primitive seg-
ment ; «*■", second primitive
segment.
A
B
Fig. 282. — A, transverse section through an embryo of Amphioxus with the rudiment
oi the first primitive segment (after Hatschek, from 0. Hertwig's Text-book). /I,
transverse section through an embryo of Amphioxus, with the rudiments of five
primitive segments (after Hatschek, from O. Hertwig's Text-book), ak, ectoderm;
ch, chorda-rudiment; dh, archenteric cavity; Jib, layer of the ectoderm that grows
over the medullary plate; ik, entoderm; Ih, body-cavity; mk, primitive segment ;
m/i, medullary plate.
DEVELOPMENT OF THE MEDULLARY TUBE, ETC.
541
of the blastopore, which thus becomes covered by a layer of ectoderm
(Fig. 281). The blastopore thus does not open externally but into the
neural canal ; this connection between the intestine and the neural
tube is long retained, being known as the neurenteric canal. [See
Kopsch, Xo. V. ;
The medullary plate does not reach the most anterior end of the
embryo, but extends for about three-quarters of its length. At the
point where it stops, which lies somewhat in front of the anterior
edge of the first primitive segment, the medullary tubes retain an
external aperture which is at first wide but gradually narrows
later (neuropore, Figs. 285, 286, np). As we shall presently see,
the neuropore in Ampkioxtts
only closes in a very late stage
(Kupffer). The cells of the
medullary tube, like the other
ectodermal cells, carry rlagella.
These, which are long and ex-
ceedingly hue, project into the
lumen of the tube and are
directed backward.
The development of the
medullary tube leads to a
pressing inward of the middle
part of the dorsal wall of the
entoderm - sac (Fig. 282 A).
This median swelling is accompanied by two latero-dorsal out-
growths of the entoderm-sac (Fig. 282 B, ink). These paired
longitudinal folds, the so-called mesoderm-folds, yield the material
which becomes the mesoderm and can be traced posteriorly as far as
to the neighbourhood of the two primitive mesoderm-cells,* although
the most posterior part of the folds is indistinctly marked off from
the rest of the entoderm-sac. Segmentation very soon appears in
the anterior region, the mesoderm-folds becoming cut up by trans.
\ eise indentations, into consecutive portions, the primitive segments
(Fig. 281, us', /is"). The segments which, owing to their origin, must
be regarded as archenteric diverticula, develop regularly from before
backward. We thus see, in Fig. 281 two, in Fig. 285 five, and in
Fi-->- 7.-7- - ~S
Or, -J
XP. 771
k
/
/
JV
is "
'd
en
B
4U^
v
r so
\ nrr
d
-■*' SI)
Fig. 288.— A, larva of A mphioxus with the rudiment of the oral aperture and the first
gill-cleft, seen from the left .side (after Hatschek) ; B, anterior end of the same
larva, highly magnified, c, larval caudal tin; ch, chorda; en, neurenteric canal ;
d, alimentary canal : h, cavity caused by the transformation of the right anterior
entoderm-sac ; /.. club-shaped gland ; //. efferent portion of the same; ks, gill-cleft;
m, mouth ; mr, medullary tube ; np, neuropore ; sv, sub-intestinal vein ; w, ciliated
organ (pre-oral pit).
final condition of the chorda. In transverse section the chorda is
seen to be composed of about four cells one above the other (Fig.
284). Small, round vacuoles now appear in the protoplasm of these
cells. These vacuoles in the uppermost and undermost rows of cells
remain small, but in the two middle rows they run together to form
large vacuoles, the order at the same time becoming changed in such
a way that a large vacuole compressed from before backward alternates
with a cell. The cells of the middle layers then form partitions
between the successive large vacuoles. A similar stage of develop-
ment was described above for the chorda of the Ascidians. According
to Lwoff's researches (No. 16), the chorda-tissue' of Amphioxw
EARL! LARVAL DEVELOPMENT. 549
essentially agrees with that of the Vertebrates, consisting- of vesicular
flattened cells. The structures thai were described as choixla-plates
appear to be a kind of artifact.
Great changes also take place in the entoderm. Two lateral
diverticula first become abstricted from that anterior part of the
entoderm-sac which lies in front of the first primitive segment; these
diverticula lie beneath the cephalic process of the first primitive
segment (Fig. 286, do), and arc called by Hatschek the anterior
entoderm-sacs. This author has recently claimed them as an anterior
pair of branchial sacs (No. 8). The future fate of these two diverti-
cula, which at first resemble each other, differs greatly. The one on
the right (Fig. "JS7, ') increases considerably in size and, pressing
back the anterior end of the alimentary canal, completely Alls the
anterior cavity beneath the chorda in the snout-like prolongation of
the body (Fig. 288, h). The left diverticulum (Fig. 287, dv), on the
contrary, remains small and does not shift forward. In later stagas
it lies transversely beneath the chorda and opens outward in front of
and above the oral aperture (Fig. 288, w). A strongly ciliated efferent
portion can be distinguished from a smaller blind portion lying to the
right. This vesicle to which, later, a nerve runs, was regarded by
Kowalevsky as a peculiar sensory organ of the larva. The pre-oral
pit becomes enclosed by the developing oral hood and thus comes to
lie within the adult mouth ; the ciliated epithelium lining its efferent
section increases in extent and gives rise to the so-called wheel-organ
(Raderorgan), while its sensory organ persists in the adult as the
groove of Hatschek.
The two anterior entoderm-diverticula have been interpreted in many
different ways. We have already mentioned that Eatsi her (Xo. 8) regards
them as the most anterior pair of branchial sacs. van YVijhe (No. 22)
recently claimed the aperture of the left entoderm- vesicle as the primary
mouth (autostomai of Amphioxus, homologous with the mouth of the Tunicata.
The ciliated organ which develops from the entoderm-vesicle, together with
Hatschek's pit, has been compared by van Wijhk to the ciliated pit of the
Tunicata. The right entoderm-vesicle, on the contrary, which is not morpho-
logically the antimere of the left, corresponds to the anterior cephalic somite of
i he Selachians, from which are developed the optic muscles innervated by the
oculo motorius. Batesoe (Xo. 26) has compared the two anterior vesicles to
the proboscis-coelom of Balanoglossus and the aperture of the left vesicle to
the proboscis-pore, a conclusion with which Wiu.kv (No. XIII.) agrees.
A further derivative of the entoderm is found in the so-called club-
shaped gland, first seen by M. SCHULTZE and later by LEUCKART and
PAGENSTECHEB I Figs. 288, 289, If). This lies near the first primitive
550
CEPHALOCHORDA.
segment and arises as a transverse groove in the floor of the enteron
(Fig. 2S7, dr) specially distinct on the right side of the body and
running thence ventrally to the left side. This groove deepens and
becomes constricted off from the enteron to form an independent
tube, and then represents the club-shaped gland, the right, blind
portion of which is dilated, while the narrowed left section opens
externally in front of the oral aperture (Fig. '288, //). In later stages,
the right, blind end of this gland enters into communication with the
lumen of the intestine (Ray Lankesteb and Willey).
ds ds
A
-mr ch Jc fl
FtG. 289. — A, anterior end oJ a larva somewhat older than that depicted in Fig. 288,
•-'•cii from th.- right side ; B, posterioi end of tin- same seen from the left side", an,
anus; c, larval caudal fin ; ch, chorda; d, alimentary canal ; ds, dissepiments of the
side turned to the spectator ; ds', dissepiments of the other side;.//, ciliated band
(rudiment of the endostyle) ; /•, club-shaped gland ; ks, gill-cleft ; m, mouth; mp,
pole-cells ot the mesoderm ; mr, medullary tube : mr', posterior end of the medullary
tube : i'/'. neuropore ; sv, sub-intestinal vein ; w, ciliated organ (pre-oral pit).
Immediately in front of the club-shaped gland there is a transverse
ciliated band (Fig. 289 A, fi) which, according to Willey, is the
first rudiment of the endostyle.
The oral aperture (Fig. 289, m) forms on the left side of the body
in the region of the first segment. A disc-like thickening of the
ectoderm first appears, to the inner side of which the intestine
becomes closely applied, since, in this region, the mesoderm does not
LATER LARVAL STAGES. 55]
extend bo far ventrally. In the middle of this ectodermal thickening,
the larval oral aperture forms al first as a narrow perforation which,
however, soon widens. Consequently, the oral aperture is surrounded
by a thickened ectoderm- wall.
The fird gill-cleft forms soon after (Fig. 289, hs) in the ventral
region of the second body-segment. A small outgrowth of the ento-
derm here forms, round which the entoderm-cells become elongated
and less granular. An annular entodermal thickening is thus formed
in the middle of which is the above-mentioned depression, the cells
of which soon fuse witli the ectoderm, and a perforation, the first
gill-slit, takes place. bound the first gill-cleft, the ectoderm is not
thickened, but the entoderm forms a circular wall representing the
inner edge of the gill-cleft. The first primary gill-cleft which ai ises
in this way soon shifts to the right side of the body (Fig. 289 A).
After the mouth and the first gilt-clefts have broken through, the ciliated
organ, the pre-oral pit (derived from the left enteric vesicle), and the club-
shaped gland also open externally.
The anal apertun breaks through at the most posterior end of the
alimentary canal on the left side of the body. At the same time,
the communication between the intestine and the ventrally curved
end of the medullary tube (neurenteric canal) (Fig. 289 B) is lost.
After all these apertures have formed, the larva is capable of
taking in food.
D. Later Larval Stages.
The further development of the larva falls into three periods :—
I. Behind the first gill-slit, a series of other so-called primary tj ill-
slits (as many as fourteen, Willev) develop ; most of these shift to
'he right side of the pharynx. The metapleural folds arise and the
itrium begins to form and to close from behind. The primitive seg-
ments increase in number till the condition of the adult is in tins
respeel readied (sixty-one segments forming in A mphiojcm lanceolatus).
The unpaired fin of the adult with its cavity develops (Figs. 290, 291 ).
II. (hi the right side, above the row of primary gill-clefts, a second
row forms (secondary clefts of Willey). After the atrium has closed,
the primary gill-clefts shift to the left side, while the secondary
remain on the right side. The larval mouth becomes changed into
the velum, and the definitive mouth-aperture arises as a consequence
of the formation of paired folds, the oral hood, round the larval
mouth. The mouth shifts into the ventral median line. The oral
552 CEPHALOCHORDA.
cirri develop and the club-shaped gland degenerates. In consequence
of the development of tongue-bars in connection with the gill-slits,
the number of the latter is doubled. The hepatic caecum forms
(Figs. 292, 293, 296).
III. The larva, which in essential points now closely resembles the
adult, has given up pelagic life and buries itself in the sand. The
gill-clefts already formed, which at first were arranged metamerically,
shift nearer together, and their number is further increased by the
addition of paired tertiary clefts (Willey). These tertiary clefts
continue to increase in number throughout life.
It has already been mentioned (p. 551) that the first primary gill-
cleft which arose in the ventral median line of the second trunk-
segment soon shifts to the right side of the body. In an exactly
similar way, new gill-clefts form successively in the body-segments
that follow (Figs. 290, 291), these clefts also lying in the ventral
median line and shifting later to the right side of the body. The
row of primary clefts now lying on the right side is destined later
to take tip its final position on the left side. The number of primary
clefts which thus arise one after the other varies from twelve to
fifteen, and is usually fourteen. They have a strictly metameric
arrangement and, according to Hatschek (No. 8), are intersegmental.
The gill-clefts thus correspond to the boundaries of the segments.
Hatschek (No. 8) regards the above-mentioned entoderm-vesicles as the most
anterior pair of gill-clefts. These vesicles correspond to the posterior boundary
of the first metamere (represented by the cephalic process of the mesoderm
which Hatschek regarded as an undeveloped pair of primitive segments).
The peribranehial groove (the anterioi ciliated arch, which is homologous
with the ciliated arch of the Tunicates) was regarded by him as ihe second
pair of gill-clefts. The clefts which were described above as the first true
gill-clefts would, according to this interpretation, represent the third pair.
This pair is on the right somewhat smaller than the others; the clefts which
follow the ninth are also at first smaller than the rest and do not deviate from
their median position to the right.
The median ventral blood-vessel which, in the pharyngeal region,
constitutes the branchial alters, turns somewhat to the right in the
branchial region and then runs forward above the row of primary
gill-clefts (Figs. 292, si). We have already seen (p. -34 7) that the
course of this vessel is diverted to the right by the rudiment of the
must anterior pair of gill-clefts. The course of this vessel marks the
future ventral median line of the pharynx.
A longitudinal ridge now sunn arises above the branchial artery on
the right side of the body (Fig. 292, k) ; tins is composed of con-
LATKK LARVAL STAGES.
553
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554
CEPHALOCHORDA.
secutive connected oval thickenings. This ridge, which represents
a thickening of the pharyngeal wall, is the rudiment of a new row of
gill-clefts, the secondary clefts of Willey which remain on the right
side of the body. Their true character is soon announced by fusion
of the entodermal thickenings with the ectoderm and by the ap-
pearance of small elongated perforations in the middle of the ovals
(Fig. 292 />', I- VII). The rudiments of six secondary clefts usually
first appear, alternating in position with the primary clefts in the way
K
n
f secondary clefts increases later, one more
forming anteriorly, and several being added posteriorly, so that,
finally, they number in all seven to nine, eight being the most
common number.
The later changes in the branchial region consist of the shifting
of the row of primary gill-clefts over the ventral surface of the
pharynx from the right side of the body to the left. The oral
l.vi Ki; LARVAL STAGES.
555
aperture lias meanwhile shifted from the left side and taken up a
more anterior and ventral position. The branchial artery, which
lies beneath the rudiment of the endostyle, now occupies the ventral
middle line, while the secondary gill-clefts remain on the right side of
the body (Fig. 293). A reduction in the number of the primary
delta takes place at the same time, the most anterior and some of
the most posterior closing and completely disappearing (twelfth in
Fig. 293), so that finally the number of clefts on the right equals
that on the left. These changes have been defined as the process of
symmetrisation of the branchial region or the equalisation of the
gill-slits. They lead to a final stage in which an equal number of
clefts (seven to nine, usually eight) is found on each side. This
stage, which marks a long pause in development daring which only
the endostyle-rudiment grows further posteriorly and the clefts
I €S
F,G. 293. Ventral side of an Amphioxus larva at a later steg < er Wn lk
second, It, vestige of twelfth primary gill-.-lett ; r-VIir first eight
clefts; be, buccal cirri; eft, chorda ; es, endostyle; m, mouth ; v, velum.
increase in height, has been named by Willey the critical stage of
larval development. Wilms* points out that the number of clefts
at this stage approximately agrees with the typical number oi gill-
clefts in Vertebrates.
The -ill-clefts hitherto present were segmentally arranged, but
this relation to the hodv-segments is lost in the tertiary clefts wind,
are added later in pairs behind the clefts already formed. The most
anterior, originally segmental clefts (primary and secondary) are also
then displaced forward.
The primary clefts become early lengthened in the transverse
direction of the body, i.e., vertically ( Fig- 292, 293). The secondary
clefts, on the contrary, arc when they first appear, lengthened at
right angles to this direction and consequently parallel to the
longitudinal axis of the body (Fig. 293). Only in later stages do
they also extend vertically.
556 CEPHALOCHORDA.
While the above chauges are taking place in t lie branchial region,
the number of gill-clefts is doubled, each cleft being cut up into two
halves by the down-growth of a conical process from its dorsal edge
(Fig. 293). So long as this process (the rudiment of the secondary
or tongue-bar) does not reach the lower edge of the cleft, the latter
is horse-shoe-shaped, recalling in appearance the gill-clefts of Balano-
glossus. The process finally fuses with a prominence which rises to
meet it from the lower edge and each gill-cleft is thus divided into
two. ' In consequence of the clefts having developed in this way, we
are able to distinguish in the adult alternate series of primary and
secondary gill-bars, between which an essential anatomical distinction
exists, as has recently been pointed out by Ray Lankester (No. 12),
Spengel (No. 19), and Boveri (No. 2).* Here we can only mention
that the primary bars enclose a coelomic canal which is wanting in
the tongue-bars. The cross-bars or synapticula (Fig. 312, s), running
in an obliquely horizontal direction from one primary bar to the next,
only develop comparatively late.
While the changes just described are gradually leading to the
perfection of the pharynx, a cavity develops round this region, the
peribranchial or atrial cavity. In accordance with KowALEVSKY and
Eolph, this was formerly thought to arise through two longitudinal
folds growing completely over the region of the branchial clefts like
the branchiostegite in the Crustacea and fusing in the ventral median
line so that, finally, of the original wide aperture between the
peribranchial folds only a small median postero- ventral opening is
left. This aperture, the atriopore, serves to put the atrial cavity
into communication with the exterior. Our view of the development
of the atrial cavity has, however, recently been modified through the
researches of Ray Lankester and Willey. The first rudiment of
this cavity is, indeed, found in the form of two folds (Fig. 29+ A),
known as the lateral or metapleural folds (If and rf). Within these
folds a cavity develops (Fig. 311, of, p. -~>72), which, according to
Kowalevsky, represents an isolated part of the body-cavity. This
cavity, which is known as the metapleural canal (Hatschek's
Oberfaltenhohle), is not reckoned as belonging to the coelom by Ray
Lankester and Willey, but is regarded as a lymph-sinus (pseudo-
code). According to HATSCHEK, on the contrary, it should be
considered to belong to the myocoele.
[See Benham's more recenb work, No. I. — En.]
LATER LARVAL STM.KS.
557
The lateral folds at first lie very near together on the ventral side
of the larva (Fig. 294). They arc found in larvae in which nine or
ten primary gill-clefts have developed. Behind this region, the
lateral folds are bilaterally symmetrically placed ai the sides of the
median line. Near the gill-clefts, on the contrary, they diverge to
the righl (Fig. 294). The righl lateral fold (rf) runs forward along
the right side <>t' the body above the clefts, in front of which it again
bends toward the median line. It covers externally the upper part
of the clefts. The left lateral fold (If) is at first only slightly
developed anteriorly and runs almost along the median line in the
branchial region.
The lateral folds border a groove running along the ventral side
which is the first rudiment of the atrial cavity. The posterior part
ap
Fig. 294.— Three larval stages of Amphioxus, from the ventral aspect (after Ray
Lamkester and WlLLEY). A. the atrium is still entirely open ; B, the atrium
is partially closed posteriori} ; 0, the atrium is almost completely closed, ap,
atriopore ; /. , gill-slits; If, left metapleural fold; m, mouth; rf. right metapleural
fold : w, pre-oral pit.
of this groove closes first (Fig. 294 B), closure being effected by the
appearance of two solid ridge-like projections of the inner opposed
faces of the metapleurs (sub-atrial ridges of Ray Lankester and
Willey) ; these ridges grow out towards one another (Fig. 295
A, .•>•/) and fuse (Fig. 295 B). Through the fusion of the sub-atrial
ridges, the floor of the atrial cavity is formed, in which later that
part of the body-cavity culled by Hatschek (No. 8) the cavity of tin
lower folds appears (Fig. 311, uf, p. 572). The atrial cavity, which
is at first tubular and open at both ends, gradually extends farther
forward (Fig. 294 B and C), till, finally, the anterior part of the atrial
eavity is completely closed towards the exterior. Only in the posterior
part of it do the metapleurs still remain separate. The aperture here
558
CEPHALOCHORDA.
retained is the atriopore (Fig. 294, ap). The lateral folds are also
found in the adult as projecting ridges of the body-wall, running from
the mouth to the atriopore.
The atrial cavity thus formed is at first a tube with a compara-
tively narrow lumen (Fig. 295 B) which only secondarily widens ;
this widening, which is accompanied by a shifting apart of the meta-
pleural folds, is brought about by the lateral growth of the atrial
cavity between the wall of the intestine and the body-wall pressing
into the coelom so as almost completely to grow round the alimentary
canal (Fig. 311, p. 572), the coelom being proportionately reduced as
s/ :/
Fig. 'J'.'.'p. — Three diagrammatic transverse sections through older larval stages of
Amphioxus to illustrate the development of the atrial cavity latter Ray Lankestkk
and WlLLEY). (to, aorta; c, cutis; ch, chorda; d, enteric canal ; ./'. muscle-fascia ;
fh, dorsal fin-cavity ; m, myomere ; n, neural tube ; p, atrial cavity ; sf, metapleur;
sfh, metapleural cavity; si, sub-intestinal vein; sk. sclera-layer ; si, sub-atrial
ridge ; sp, coelom.
the atrium enlarges. Part of the outer wall of the atrial cavity (the
epipleura of Ray Lankestkk) therefore does not arise through the
formation of folds, but is a modified portion of the body- wall which
has undergone no displacement. [See also MacBride, No. VIII. >/.]
The formation of the atrial cavity iu Amphioxus recalls to some extent
that of the similarly placed cavity in the Ascidians which, as we have seen,
originated in the form of paned invaginations (p. 366) which also only
secondarily grow round the pharynx.
The outer wall of the atrial cavity cannot be homologised with the oper-
culum of the fishes, the latter being a fold which belongs exclusively to the
hyomandibular arch.
LATBK LARVAL STAGES. 559
The metapleural folds have frequently been homologised with the
primary paired lateral fins of the Vertebrata (Ray Lankestee and
Willey, Hatschbk). According to Hatschek (No. 8), they are
merely special parts of a system of ventral folds which in the most
anterior part of the body develops as the unpaired ventral tin of the
rostrum, in the oral region forms the lateral buccal wall, in the
branchial region the metapleural fold, and, finally, behind the atrio-
pore, the unpaired ventral tin which extends in front of and behind
the anus. The "cavities of the lower folds" which develop in the
sub-atrial ridges arc said to be the cavities of the unpaired ventral
tin.
We have already alluded (p. 550) to a ciliated band lying on the
right side of the pharyngeal wall in front of the club-shaped gland
(Fig. 289, fl). This ciliated band, in which a somewhat clearer inner
/one can he distinguished, resembles in shape the club-shaped gland,
so that, in the illustration, it looks like a shadow or a reduplication
of the latter. It is the rudiment of the endostyle and, even in early
stages, appears bent on itself (Fig. 292 A, e->-), being divided into a
shorter upper and a longer lower half. The endostyle-rudiment then
proceeds hack ward (Fig. 292 B) passing over the club-shaped gland
into the space between the primary and secondary clefts. It thus
comes to overlie the branchial artery. During the shifting mentioned
above as taking place in the branchial region, the endostyle-rudiment
passes from the right side of the body to the ventral median line
(Fig. 293, rs). The upper half of the bent rudiment becomes the
right ami the lower half the left part of the endostyle of the adult.
At an early stage, two ciliated arches, the peripharyngeal hands, are
to lie seen ascending from the anterior end of the endostyle-rudiment
to the dorsal side of the pharyngeal wall (Fig. 296, //), and then
continue backward on either side of the dorsal middle line as the
ciliated hyperpharyngeal (epipharyngeal) bands. The proximal part
of them corresponds to the ciliated arches (pericoronal arches or
peripharyngeal bands) of the A.scidian (Willey).
The formation of the definite oral aperture has been described in
detail by WiLLEY. The oral aperture shifts from the left side of
the body forward and ventralwards, so that it finally occupies a
median symmetrical position on the ventral side. At the same time,
it becomes grown over by a secondary fold of the body-wall (Fig. 296,
////•), the stomodaeum or oral hood being thus formed. The primary
oral aperture of the larva shifts to the hack of the buccal cavity and
its lips are retained as the velum (r) ; here the first rudiments of the
560
CEPHALOCHOEDA.
velar tentacles soon appear. There are at first four of these, two
lateral, one upper and one lower; later, the number increases to
twelve. In the lower of the two secondary oral folds, the first rudi-
ment of the cartilaginous skeleton that supports the oral cirri (Fig.
296, be) soon appears in the form of rounded thickenings of the
mesodermal tissue. Each of these cartilaginous spherules corresponds
in later stages to an outgrowth of the edge of the mouth which gives
rise to a cirrus. New cirri form in the lower lip in front of and
behind those already formed, while, from the condition of the adult,
Ray Lankestee concluded that the median cirri of the ventral edee
of the mouth were the last to arise.
1 Z fl ft p
E [G. 296.— The same stage as in Fig. 292 B seen from the left .side (after Willey). /,
2, 1.$, first, second, and fourteenth primary gill-clefts, be, buccal cirri; fi, peri-
pharyngeal ciliated band ; fh, dorsal fin-cavities ; mr, oral fold ; np, neiiropore ;
nph, nephridium oi Hatschek ; p, atrial cavity ; v, velum ; w, wheel-organ (part
of pre-oral pit).
After the oral hood has formed, those organs which opened in the
immediate proximity of the larval mouth have to open into the
secondary oral cavity. These are the club-shaped gland and the
pre-oral pit which marks the aperture of the sensory organ derived
from the left anterior entoderm-vesicle.
The lower of the two folds which form the definitive oral aperture is
continued forward without break into the unpaired fin (Ray Lankesteb).
Ray Lankestee interprets the oral folds as the anterior continuation of the
so-called epipleura (lateral walls of the atrial cavity) and Hatschek (No. 8)
has also adopted this view. According to Willey, the right half of the oral
hood arises essentially in continuity with the right metapleur. The left half,
however, is entirely independent of the left metapleur. The latter condition,
Willey thinks, may possibly be secondary.
Another view has recently been adopted by van YYijhe (No. 22), who
maintains that botli the halves of the oral hood belong exclusively to the
left side of the body. This conclusion was arrived at from a consideration of
their innervation as well as from the fact that only the cavity of the left
lateral fold is continued into the lip on the outer side of the massive external
lip-muscle. The definitive mouth of Amphioxus is thus, according to van
LATEK LARVAL STAGES. 561
WlJHE, like th<' larval mouth, an organ belonging to the left side of the body,
in spite of its apparently symmetrical position.
It is difficult, from Wii.lhy's description, to gain a clear idea of the sh if tings
which occur in the oral region. According to this author, the longitudinal axis
of the slit-like larval mouth rotates about a vertical axis through an angle of
90c. Originally it lies parallel to the axis of the body, but is at right angles
to it later. Consequently, the anterior part of the larval mouth sinks in and
passes to the right side to give rise to the right half of the velum, while the
left half of that organ is derived from the posterior corner of the mouth.
Similar shifting of the labial folds takes place.
van Wijhe maintains that the mouth of Amphioxtts is not homologous
with that of the Craniata. He also doubts the homology of the velum of
Ampkioxus with that of the (Jyclostomi. According to him the mouth of
Amphioxus is a gill-cleft lying on the left, and the club-shaped gland is the
corresponding organ on the right side of the body, van Wijhe homologises
it with the left spiracle of the Selachians aud with the left gill-cleft of
Appendicularia (.'i.
*
In the later larval stages, when eight secondary gill-clefts have
already developed and the tongue-bars have begun to form, the
club-shaped gland degenerates, and finally, as it appears, reaches
the interior of the alimentary canal where it is perhaps absorbed.
The aperture of the gland into the intestine which was mentioned
above (p. 550) seems to withstand disintegration longer than any
other part of the organ (Willey).
In these later stages an organ is found which was discovered by
Hatschek (No. 5) and was figured and described both by him and
by Kay Lankester and Willey (Nos. 12 and 23)' as the kidney
{nephridium, Fig. 290, x). This is developed only on the left side in
the form of a mesodermal ciliated funnel and canal lying in front of
the mouth in the region of the first metamere (between the pre-oral
pit and the mouth). It lengthens posteriorly later and is found, in
the adult, as a strand extending on the left side beneath the chorda
from the anterior edge of the mouth to immediately behind the
velum. Hatschek conjectured that this canal opened into the
pharynx. [See MacBride, No. VIII. a.]
This last observation has recently been confirmed by van Wijhe (No. 22)
who considers this organ, which he calls the oesophageal process, as the
remains of the original communication between the intestine and the left
anterior entoderm-diverticulum.
We have already mentioned that, in the larval stages which follow
the stage with one primary gill-cleft, the number of primitive segments
is continually increasing through the formation of new segments from
the mesoderm-folds at the posterior end of the body. At the time
oo
562 CEPHALOCHORDA.
when the mouth and the first gill-clefts form (Fig. 288), the
larval Amphioxus has fourteen primitive segments, the cavities of
which, when they arise, are in communication with the archenteric
cavity. The primitive segments that form later are yielded by the
mesoderm-folds after these have become separated from the entoderm
(p. 545). The cavities of these segments are thus from the first quite
distinct from the archenteron. The number of body-segments of the
adult Amphioxus is approximately sixty-one, and this number is
attained even before the appearance of the secondary gill-clefts
(Fig. 291).
The unpaired fin of the adult develops simultaneously with the
increase in number of the primitive segments. While the larval fin
(Figs. 288, 289, 290, c) consists of a simple thickening of the ectoderm
(see p. 544), the cells of which had a columnar form, the adult fin
(Fig. 291, c) consists of an ectodermal-fold, into which special parts
of the body-cavity (the fin-cavities) extend (Fig. 302 7, 77). Within
these fin-cavities the fin-rays develop in consequence of a thickening
of the mesoderm which grows up into the cavity from its floor, and
these project freely into the cavity (Bay Lankester).
The unpaired fin extends along the whole of the dorsal side (Fig.
291). In consequence of its development, the neuropore (np) is
pressed out of its original median position to the left side of the body
The anterior end of the unpaired fin passes round the anterior end of
the chorda, so that, in the rostral region, the fin is continued also on
to the ventral side. This anterior ventral section of the fin, according
to Ray Lankester (No. 12), is continued without break into the
right oral fold. In passing round the posterior end of the body the
unpaired fin is widened and then runs forward along the ventral side
of the body as far as to the atriopore, the anal aperture being dis-
placed by the developing caudal fin to the left side of the body
(Fig. 291).
While, in the dorsal region, the fin-rays are unpaired, in the ventral
region, between the atriopore and the anus, they are paired, though,
according to Ray Lankester, they develop in unpaired fin-cavities.
The presence of these paired fin-rays has been regarded as an indica-
tion that this part of the unpaired fin arose from the fusion of paired
folds which represent the backward continuation of the epipleural folds
(Ray Lankester, Hatschek).
The fin-cavities are divided into consecutive compartments (Figs.
292, 296, fh), about five of which in the dorsal fin, according to
Ray Lankester, belong to one muscle-segment, although a definite
LATER LARVAL STAGES.
W.i
relation of these compartments to the segmentation of the body cannot
be made out.
The anal aperture which originally lay at the posterior end of the
body shifts later further forward (Fig. 291), and this leads to the
development of the post-anal region of the body characteristic of
the Vertebrates.
We have seen above (p. 545) that the anterior end of the medullary
tube, which lies in the region of the first true primitive segment and
the so-called cephalic process of the mesoderm (anterior primitive
segment of Hatschek) is widened (Figs. 288, 289). This part,
according to Hatschek's recent statements (No. 8), becomes dif-
ferentiated, in the young Amphioxus, into three consecutive sections
which correspond to the three primary cephalic vesicles of the Craniata.
JT
izr,
tic. 297.
Fig. 2'.'7.--.l. transverse .suctions through the brain of a young Amphioxus (after
Hatschek). /. through the (primary) first ventricle; //, through the (primary)
second ventricle [aquaeductus Sylvii) ; III, through the (primary) third ventricle
i fossa rhomboidalis). B, transverse sectiou through the spinal cord.
Fig. 298.
FlG. 298. — Brain with the most anterior nerve-roots of a young Amphioxus (after
HATSCHEK). Oh, chorda dorsalis; N, ciliated pit, to the posterior wall of which
the olfactory nerve runs ; /, //. ///, the three primary ventricles (diagrammatic).
The anterior section, the primary fore-brain, shows, in transverse sec-
tion, the well-known dilation of the medullary tube which constitutes
the first primary ventricle (Figs. 297 A, /; 298 /). The anterior end
of this ventricle is continued towards the neuropore (i.e., towards the
ciliated olfactory pit) into the infundibulum (the lobus olfadorius of
Langerhans) which, in Amphioxus, is curved upward. The second
part of the brain (the mid-brain) contains within it the second
primary ventricle, winch is represented by a narrowed portion of the
564 CEPHALOCHORDA.
medullary canal (aquaeductus Si/lvii, II). In the third part (the
hind-brain) the central canal shows a narrow ventral tube, while its
dorsal portion is independently dilated so as to form a vesicle covered
by a thin membrane, the fossa rhomboidalis of Hatschek (III).
The medullary tube originally opens externally through a neuropore
bordered by closely crowded flagella. This is pressed out of the
middle line to the left through the development of the dorsal fin.
An epithelial depression forms later at this point ; this is Kolliker's
olfactory or ciliated pit (Fig. 298, «), at the base of which the neuro-
pore opens. The ciliated pit is the homologue of the olfactory organ
and of the hypophysis of the Craniata. The short, unpaired olfactory
nerve discovered by Langerhans runs from the brain to the posterior
wall of the ciliated pit. The continuation of the first ventricle towards
the neuropore corresponds, as above mentioned, to the infundibulum
of the Craniata. In Ammocoetes, the hypophysis and the olfactory
organ are still connected together, and the external aperture of the
hypophysis still retains its original dorsal position. The inner end of
the hypophysis, on the contrary, and the infundibulum have moved
to the ventral surface of the brain.
In identifying the anterior end of the medullary tube of Amphioxus with
the iufundibulum of the Craniata we have followed Hatschek. It should,
however, be mentioned that Kuppper has recently been led by his researches
on Acipenser (No. 38) to homologise the anterior end of the cranial axis of
Amphioxus with his lobus olfactorius impar which lies near the lamina
terminalis above the anterior commissure, and indicates the point where the
medullary tube remained longest in direct connection with the ectoderm
precisely as in Amphioxtis, and to regard the infundibulum as a secondary out-
growth of the ventral side of the brain.
It should here be pointed out that Kohl (No. 9) occasionally noticed, on
the right side of the head of Amphioxus, a pit resembling the olfactory pit of
the left side. Kohl is inclined to consider this as the half of an originally
paired olfactory organ in a vestigial condition. The relations of the neuropore
to the olfactory pit were denied by Kohl. The remains of the neuropore are
said to be found in an ectodermal depression lying somewhat behind the
olfactory pit.
( )ur knowledge of the important transformations that take place in
the primitive segments and the body-cavity is due chiefly to Hatschek
(No. 7). Each primitive segment becomes divided by a transverse
partition into two portions, as has already been stated (p. 547), viz.,
a dorsal portion (proto- vertebra) and a ventral part (lateral plate,
Fig. 300, / and //). Only in the dorsal portion is the primitive
segmentation retained, the adjacent walls of the segments persisting
as the transverse septa (myosepta). In the region of the lateral
LATER LARVAL STAGES.
565
plates, the septa disappear and the segmental cavities enclosed by
them flow together to form a common cavity surrounding the intestine
(splanchnocoele). The disappearance of the ventral mesentery leads
to intercommunication between the righl and left halves of the
splanchnocoele.
The proto- vertebrae enclose segmentally-arranged cavities which.
however, are not quite symmetrical in relation to the median plane
(p. 545). These are the cavities of the proto-vertebrae or the
cnyocoeles (Fig. 153, /). The walls of each proto-vertebra consists of
a parietal (/) and an inner (2) layer. The parietal layer (/), which
consists of flat cells, applies itself closely to the ectoderm, and since
Fig. 299. — Transverse section Fig. 300. — Diagrammatic render-
from the middle of the bodj ing of the same section.
of an Amphioxus larva with
five branchial clefts (after
Hatschek).
.1. epidermis; B, medullary tube ; <". chorda; Vlt inner chorda-sheath ; /'.intestinal
epithelium : E, sab-intestinal vessel. 1, cutis-layer ; 2, mnscle-layer (lateral
trunk-muscle); 3, sclera-layer ; /. boundary cells of the proto-vertebra; -5, somato-
pleure ; 6, splanchnopleure. /. myocoele ; II, splanchnocoele.
it yields the cutis of the adult, is sometimes termed the cutis-layer.
The cells of the inner layer, at the sides of the chorda and of the
medullary tube, elongate transversely and longitudinally, as described
above (p. 548), and, as they give rise to the muscle-fibres of the
myotome, this pari is spoken of as the muscle-plate.
At first, each muscle-cell contains only one fibrilla, but as the
number of fibrillae increases later they are arranged in regular order
one above the other. Several such groups of fibrillae occur in each
muscle-cell. The nuclei of the muscle-cells lie on the outer side
of the muscle layer thai turns towards the myocoele. Towards the
ventral side, the muscle-layer is continued into a pavement-epithelium
566
CEPHALOCHORDA.
in contact with the intestinal wall ; this is known as the selera-layer
and this portion of the coelom as the sclerotome ($). At the point at
which it passes over into the cutis-layer, there is a large boundary
cell (4) which, according to Boveri, is probably to be regarded as a
primitive genital cell.
In the lateral plates also, a parietal layer (•->) can be distinguished
from a median (visceral) layer. The parietal layer (somatopleure) at
first lies on the inner side of the ectoderm ; the visceral (splanchno-
Fig. 301.— Transverse section through Fig.302.— Diagrammaticrendering
a young Amphioxus, immediately of the same section.
after metamorphosis, through tin-
region between the atriopore ami the
anus (after Hatschek).
.1. epidermis; /!, medullary tube ; <\ chorda; h. aorta; E, intestinal epithelium;
F, sub-intestinal vessel. /. cutis-layer : .'. muscle-layer ; 3, fascia-layer ; 4, outer
chorda-sheath ; tf , muscle-septum ; 5, gastral continuation of the skeletogenous layer
(intercoelic membrane) ; 6, somatopleure; 7, splanchnopleure ; /. myocoele ; /„
dorsal, //f ventral fin-cavity ; //. splanchnocoele.
pleure) forms the dorsal mesentery, in connection with which the aortae
develop later, and surrounds the intestine and the sub-intestinal vessel,
running along the ventral surface of the latter. This layer yields the
uristriped muscle-layer of the alimentary canal.
In later stages (Figs. 301, 302) the muscle-plate becomes com-
pletely separated from the chorda dorsalis and the nerve-tube, in
consequence of the development of an outgrowth of that part of
the myocoele termed the sclent-layer which grows up from below
LATER LARVAL STAGES. 567
{sclerotoni'). The muscle-plate is then connected merely at its dorsal
edge by means of a mesentery-like hand to the wall of the proto-
vertebra and otherwise hangs quite freely into the cavity of the
same. Its chief points of attachment are to the dissepiments. The
inner wall of the sclerotome becomes applied to the chorda and the
medullary tube, and here forms the skeletogenous layer which yields
the outer sheath of the chorda (.'/) and the neural continuation of the
latter. The outer layer of the sclerotome becomes applied to the
inner side of the muscle-layer and forms the internal sheath or
fascia-layer (3). The lateral trunk-muscle of Amphioxus is not
entirely surrounded by fascia, since this layer only develops on its
inner Bide.
All these layers, derived through differentiation from the wall of
the proto- vertebra, shift ventrally, pressing in between the ectoderm
and the somatopleura. The cutis-layer in this way comes to lie in
the ventral middle line, where it yields the lining of the cavity of the
ventral tin (/,), and the dorsal fin-cavities (/) seem in the same way
to be lined by the cutis-layer. From the floors of these cavities, the
fin-rays grow up later. The skeletogenous and the muscular layers
also shift ventrally.
The method of formation of the layers agrees in all essential points
with that of the Craniata. In this type, beneath the epidermis, lies
the cutis-layer (/) which, in Amphioxus, retains its simple epithelial
character throughout life. This is followed by the myocoele, which
also here persists throughout life. Then conies the muscle-layer (..')
and on the inner side of the latter lies the fascia-layer (•>') : in the
( 'raniata the faseia is also developed on the outer surface of the
muscles ; then eomes the cavity of the sclerotome, and, finally, the
skeletogenous layer (4). The latter (as chorda-sheath) encloses the
chorda and also the medullary tube in the dorsal half of the body;
in the lower half, it becomes applied to the somatopleure. The two
layer- (skeletogenous layer and somatopleure) here form a delicate
partition-wall, the intercoelic membrane (5 and 6) which separates
the cavity of the primitive vertebrae from the splanchnocoele. On
the inner side of the splanchnocoele lie the splanchnopleure and the
entodermal intestinal epithelium.
In the branchial region (Fig. 311) the condition of the body-cavity
i- complicated through the development of the atrial cavity (/<). which
presses in between the splanchnocoele and the ventral part of the
myocoele. The latter then lies in the peril iranchial fold and breaks
up into sections called by Hatschek (No. 8) the upper and lower
568
CEPHALOCHORDA.
fold-cavities. The cavity of the upper fold (of) lies in the meta-
pleural folds and is also known as the metapleural cavity. In its
inner wall, which is in contact with the outer wall of the atrial cavity,
the transverse or sub-atrial muscle (mt) develops. The cavities of
the lower folds (uf) are regarded by Hatschek as the equivalent
of the ventral fin-cavities in that part' of the body which lies behind
the atriopore. The splanchnocoele is divided by the gill-clefts into an
SIX sx
Fig. -jO."!. — Side view of the lower edges of the proto-vertebrae in a young Amphioxus,
9 mm. long (after Boveri). hm. ventral muscle ; gd, genital gland ; S IX, S X ,
ninth and tenth mesodermal somites.
upper paired cavity (■•>/■, epi-branchial , suyra-pharyngeal or sub-chordal
eoelom) and an unpaired ventral cavity (ec, mdostylar coelom). These
two are connected by means of canals running within the gill-bars
(cf. p. 556 and Fig. 311, on the right side of which a primary gill-bar
with its coelomic canal is represented as cut through longitudinally).
The development of the genital organs has recently been described
by Boveri (No. 3). The genital vesicles which develop in each
FIG. 304.— Hide view of the
(alter Boveri).
jenita
urn. long
mesodermal somite from the tenth to the thirty-fifth, are abstricted
portions of the somites which may be compared to the nephrotomes
or gononephrotomes (Ruckert) of Selachian embryos. Boveri,
therefore, regards the genital chambers of Amphioxus as the homo-
logues of the canals of the primitive kidney in the Craniata. The
development of these chambers can be observed in the quite young
Amphioxus four to twelve millimetres long. In cross-sections, at the
I. villi; DAEVAL STAGES.
509
part along the ventral edgeof the protovertebrae where the cutis-layer
passes into the Bkeletogenous layer, small cells filled with deeply
staining nuclei can be made out. These are accumulations of primi-
tive genital cells which represent the rudiment of the genital gland,
and which may perhaps he traced back to Hatschek's large boundary
cells mentioned above (Fig. 299, 4, p. 565). These agglomerations of
cells arc repeated at definite intervals in series of cross-sections.
Since they are related to the dissepiments between the mesodermal
somites, they are affected by the asymmetry of those structures and,
like them, alternate on the right and left sides of the body. In
superficial views of later stages (Fig. 303), the rudiments of the
Fig. 305. Pig. 306.
Pig. 305 and 306.— Later stages of development of the genital rudiment
in Amphioxus latter (Boveki i.
Fig. 307.— Genital rudiment in
an Amphioxus, 8 mm. long
(after Boveri).
genital -land can be seen as rounded knobs (Icio.rvx
we must, in conclusion, briefly describe the renal canals discovered by
Boveri (Nos. 1 and 2) in the adult animal. These are short tubes
found in the region of the pharynx which connect the sub-chordal
coelom (Fig. 311, sc) with the atrial cavity (p). They lie on the
GENERAL CONSIDERATIONS.
571
mesial side of the sub-chordal coelomic sac, and open into the atrial
cavity at the uppermost angle where the wall that covers the outer
side of the gill-bars bends outward to
form, together with the wall of the
sub-chordal coelomic sac, the thin
partition-wall known as the ligamen-
tinn denticulatum (/,
atrial cavity : sc, sub-chordal coelom ; si, truncus arteriosus (branchial artery) :
sk, sclera-layer ; »j\ cavities of the lower folds.
type, that we may well regard it as the " primitive Vertebrate," or
at least as a form standing remarkably near the hypothetical ancestor
of the Vertebrata. We need here only refer to the primitive con-
GENERAL CONSIDERATIONS.
573
ditions of the blood-vascular system, and especially to the development
of the body-cavity which, as made known by Hatschek, yields the
key for understanding the formation of the layers in the Vertebrates.
It must further be pointed out that the development of Amphioxus
without doubt shows very primitive characters, a view to which
however, objections have been raised by Dohrn. The occurrence of
free-swimming ciliated larvae, nevertheless, can hardly be interpreted
in any other sense.
ms
m
Z -jr- nc
PIG. 312.-Dorsal portion of the left pharyngeal wall of 4^™}t7£lert2
renal canals, seen from the side (diagrammatic, ^erBmERi) Id 1 W^ntum
cavity ; s, synapticnlum ; /, primary gill-bar ; //, tongue-bar.
Considering the agreement prevailing between Amphioxus and the
Vertebrates, it is important to emphasise the distinctions between the
two forms. Amphioxus is specially distinguished by the rostrum-
like prolongation of the notochord, by the secondary increase in
number of the gill-clefts, and by the duplication of such primary clefts
through division (development of the tongue-bars), this last character-
istic recalling the multiplication of the gill-clefts in the Ascidia.
With regard to the condition of the urogenital system, we must refer
to the accounts of Boveri (No. 2), according to which the renal
canals of Amphioxus a,re to be considered as the homologue of the
proncphric canals of the Vertebrata, and the atrial cavity of
574 CEPHALOCHOBDA.
Amphioxus as that of the pronephric duct in the Craniata, while the
genital vesicle of A mphioxus is homologous with the gononephrotomes
of the Craniata and consequently also of the canals of the primitive
kidney in the latter. Even if we adopt Boveei's homologies, we
must still recognise certain distinctions between the development of
the urogenital system of Amphioxus and that of the Vertebrata,
which, however, would not then be of a fundamental character.
Through the great development of the atrial cavity which, according
to Boveei, is represented in the Craniata by the pronephric canals,
Amphioxus is linked on to the Tunicates. Among the further
peculiarities of Amphioxus, we must reckon the development of the
so-called anterior entoderm-vesicle and the club-shaped gland, organs
as to the morphological significance of which we are at the present
time unable to state anything with certainty.
The peculiarities just mentioned seem to indicate that Amphioxus,
as contrasted with the Craniata or Vertebrata, shows, in the strict
sense of the term, a certain independence in its position. It would
be difficult to find an explanation for this if Ave were to adopt the
assumptions of Dohen (p. 522), that Amphioxus is a degenerate form
derived from the Craniata. We do not deny that Amphioxus, in
consequence of its half-sedentary manner of life (burying in the sand)
may have undergone a certain degree of simplification and degenera-
tion. Above all, we might in this way explain the slight development
of the brain and the sensory organs and also the locomotory system.
It is naturally difficult to determine how far the simple structure of
Amphioxus rests upon primary peculiarities or to what extent upon
peculiarities secondarily acquired through degeneration. The majority
of the facts known to us as to the ontogeny and the anatomy of
Amphioxus seem to indicate that we have in this case actually to do
with a very primitive form.
Among the peculiarities which we regard as secondarily acquired
is the remarkable asymmetry in the structure of the body which is
specially marked in the larval forms, but is also retained to some
extent in the adult (position of the olfactory pit, of the anus, and of
the hepatic caecum, conditions of the innervation of the velum and
the definitive mouth according to van Wijhe). Willey's observation
that the Amphioxus larva lies when at rest at the bottom of the sea
on the right side of the body seems to indicate that this asymmetry
is acquired in the same way as in the PleuronecMdae*
* [According to Wiixey, our authors have misunderstood his observations on
this point. The fact that the young when kept in a glass jar sink to the
GENBBAL CONSIDEBATIONS. 575
We therefore regard Amphioxus as a very primitive chordate form
\rrv closely related to the hypothetical ancestor of t he Crauiutu, but
somewhat more distantly related to the Tunicutes. Every specula-
tion as to the origin of the Vertebrates and the Chordata must
necessarily take account of Amphioxus as the most primitive repre-
sentative and the starting-point of the whole series. Ammy all the
hypotheses* which have hitherto been advanced as to the origin
of the Chordate stock, that which derives it from the Annelida has
at present most adherents. As the founders and most eminent
upholders of this hypothesis we must name Semper (No. 46) and
Dohrx (Nos. 30 and 31), while, more recently, a whole series of
renowned zoologists have taken part in its further development. The
view that the Vertebrates are descended from Annelids rests chiefly
on the similarity in the segmentation of the body and in the produc-
tion of new segments at the posterior end of the body ; further, on
the agreement in the position of the more important organs, if we
assume that the hypothetical Annelid ancestor of the Vertebrata
underwent such a rotation round its longitudinal axis that the former
ventral side became the dorsal side, an assumption which lay at the
root of Geopfroy St. Hilaire's statement that " Insects are
Vertebrates running on their back." When such a rotation is
assumed, the ventral ganglionic chain of the Annelida corresponds
to the medullary tube of the Chordata, the ventral longitudinal
vessel of the Annelida becomes the aorta, while the dorsal vessel
corresponds to the sub-intestinal vessel. The Annelidan hypothesis
obtained its strongest support when Semper discovered a remarkable
bottom and fall on one side, is due to the physical impossibility to rest in any
other position, and not to a pressing desire or instinct to assume this position.
The asymmetry of Amphioxus is of a totally different character to that of the
Pleuronectidae. For a full account of these views, see Willey, Amphioxus
anil the Ancestry of the Vertebrates. Columbia Univ. Biol. Series, 1894. — Ed.]
* We have no intention of entering upon the much-disputed point of the
origin of the Chordata except in a passing way. A detailed investigation of
this difficult problem would require a study of vertebrate embryology which
does not fall within the scope of the present work. We have already, in the
foregoing chapter (p. 528), stated that the Tunicates contribute little to the
solution of this question. They are to be considered as degenerate members
of the Chordate stock, of which Amphioxus is to be regarded as the most
primitive form. Of the many theories on the subject of the relationship of
the Chordata we have here alluded only to those two which appear best
founded >m actual morphological facts, viz., the derivation of the Chordata
from Annelids and the assumption of relationship between the Chordata and
Balanoglossus. The hypothesis of the relationship to the Nemertines lias
been briefly alluded to above (vol. i., p. 231). We do not consider it necessarj
to refer to the relationship of the Vertebrata to the Arthropoda which has
recently been again assumed.
576 CEPHALOCHORDA.
similarity of structure between the primitive kidney-tubules of the
Selachian embryo and the segmental organs of the Annelida. Our
acceptance of this homology, however, has been recently made im-
possible by the researches of van Wijhe (No. 48), Kuckert
(No. 44), and Boveri (No. 2) which cause us to doubt the serial
homology of the pronephros with the primitive kidney and to regard
the latter as a secondary acquisition which in any case has nothing
to do with the segmental organs. From this point of view it would
be the pronephros which requires consideration.
The derivation of the Vertebrates from the Annelida is, in fact,
accompanied by certain difficulties which are not insurmountable.
The most important of these is the position of the mouth. While,
in the Annelida, the oesophagus perforates the central nervous system
at the oesphageal ring in such a way that the supra-oesophageal
ganglion comes to lie above and the ventral cord below the gut,
no such relation between the stomodaeum and the central nervous
system is to be found in the Vertebrates. The most varied hypotheses
have been suggested to obviate this difficulty. Schneider thought
that he could discover in the connection of the hypoglossal and tri-
geminal nerves an equivalent for the oesophageal ring, van Beneden
and Julin (No. 29) have assumed that, in the primitive ancestors
of the Vertebrates, the oesophagus shifted forward in the median
plane between the still unconnected cephalic lobes of the brain, while
other zoologists like Kleinenberg, Beard, No. 27, v. Kennel
(No. 35a) believe that the supra-oesophageal ganglion atrophied and
that the brain and the dorsal chord of the Vertebrates only are the
equivalents of the ventral cord of the Annelida. In connection
with this idea, we have the question as to the primitive mouth of
the Vertebrates. Under the assumption that the pro-cephalon of
the Vertebrates corresponds to the supra-oesophageal ganglion of these
Annelida, we should have to conjecture that the original vertebrate
mouth, which perforated the oesophageal ring, lias disappeared. The
definitive mouth of the Vertebrates would have to be regarded as a
secondary formation, and is by many zoologists thought to have arisen
through the fusion of gill-slits. There is actually much to support
the view that the mandibular arch is a branchial arch which has
been drawn into the mouth. This, however, does not decide the
question of the derivation of the vertebrate mouth from gill-clefts.
In the case of Amphioxus, there is no ontogenetic indication of the
derivation of the mouth from gill-clefts. The mouth here arises in a
different manner from the gill-slits (p. 550) and in a different position.
GENERAL CONSIDERATIONS. 577
Hatschek (No. 8) has therefore maintained that the velar opening
of Amphioxus is not to be regarded as a gill-slit.
The attempt has often been made, in following out these ideas
further, to discover vestiges of the primary vertebrate mouth, which
has been sought in the rhomboidal fossa, the pineal gland and the
hypophysis. Only recently, Beard (No. 27) and Kupffer (No. 38^
have pointed to the hypophysis as the primary mouth (palaeostoma)
of the Vertebi*ata. .
An altogether satisfactory solution of the difficulties connected with
all these questions is, however, at present wanting.
Attempts have been made in other directions also to find the con-
nection between the Vertebrates and the Annelida. We may recall
the discovery by Eisig of organs in the Oapitellidae comparable to
the lateral line of the Vertebrata, the homologising of the spinal
ganglia of the Vertebrates with the parapodial ganglia of the Annelida
by Kleinenberg (No. 36), the derivation of the unpaired fin of the
Selachians from fused Annelidan parapodia by P. Mayer (No. 39),
the attempt to derive the vertebrate eye from the Annelidan eye
by v. Kennel (No. 35a), etc. For its support, the Annelidan
hypothesis has required a number of sub-hypotheses. Nevertheless,
we must admit that the gap which divides the Annelida from the
Chordata is even now very considerable, and, as Balfour pointed
out, the two most typical organs of the Chordata, the notochord and
the gill-clefts, are not foreshadowed in the Annelids. Attempts have
not been wanting, it is true, to find the equivalents of these organs
in the Annelids. The origin of the mouth from paired rudiments in
the buds of Nads and Chaetoyazter (Semper) was compared to the
formation of gill-clefts, while the most varied structures in the
Annelida were regarded as homologues of the chorda. With regard
to this latter point, the view that most deserves attention is that of
Ehlers (No. 32) and Eisig (No. 33), who see in the so-called
accessory intestine of the Capitfillidae and the Eunicidae (and in
similar structures in the Gephyrea) the homologue of the notochord.
On the other hand, it should be mentioned that the researches of
Kleinenberg (No. 36) on this point did not lead to satisfactory
results. " In the development of most Annelids," says Kleinenberg,
" there is no trace of the accessory intestine ; I found it only in the
larvae of those forms which possess it when adult, viz., the Oapitel-
lidae and the Eunicidae. In a larva belonging to the last of these
families it hangs as a somewhat short loop beneath the principal
intestine and opens both anteriorly and posteriorly into the latter.
PP
578 CEPHALOCHORDA.
In the Gapitellidae, a diverticulum forms early at the most posterior
part of the archenteron and grows out anteriorly. I believe that this
is the rudiment of the accessory intestine, but am not quite certain
on this point," With regard to the origin of the gill-clefts, we may
assume that the originally blind intestinal diverticula secondarily
acquired external openings, so as to allow of the outflow of the
respiratory water. The assumption that such perforations occur
is supported by the actual presence of pores of communication at the
ends of the tentacles in the Actinia, and in the hepatic tubes of some
Aeolidae.
We are not, however, able to regard the Annelidan hypothesis as
resting on altogether certain foundations. It seems to us that we
have no convincing proof that the many points of agreement which
actually exist between the Annelida and the Chordata rest upon true
homology. The crucial point of the whole question lies in the
decision as to whether it is necessary for us to refer the similar
method of segmentation of the body in the two groups to their
derivation from a common ancestor. It is evident that, as Bateson
(No. 26) has shown, it is not a decisive objection to this assumption
that the characteristic segmentation in each of the two groups (the
Annelida and the Chordata) has arisen separately, or, in other words,
that the common ancestor of the two groups was still uusegmented.
Balfour (No. 25) in this connection wrote " that we must look for
the ancestors of the Chordata, not in allies of the present Chaetopoda,
but in a stock of segmented forms descended from the same un-
segmented types as the Chaetopoda, but in which two lateral
nerve-cords, like those of Nemertines, coalesced dorsally, instead of
ventrally to form a median nerve cord."
If, after what has just been said, we do not regard the derivation
of the Chordata from the Annelida as certainly proved, and institute
comparison with the other invertebrate groups, we are confronted first
of all by Balanoglossus which, in the possession of gill-clefts in the
pharyngeal region and the nerve-strand running dorsally shows
striking agreement with the type of the Chordata. This form was
formerly thought to be nearly related to the Chordata by Gegenbaur
and Huxley and more recently by Bateson, Haeckel, Schim-
kewitsch, Morgan, Boule and others. We are far from regarding
as established the various homologies assumed by Bateson between
Balanoglossus and Amphioxus, and on this point refer the reader to
the detailed criticism of the best qualified judge in this matter —
Spengel (No. 47, p. 721, etc.) — who denies all relationship between
GENERAL CONSIDERATIONS. 579
the Chordata and Balanoylosms. Bateson (No. 2<>) nomologists the
dorsal nerve-strand in the collar region of BcUanoglossus (the so-called
collar-cord) with the medullary tube of the Vertebrates. The anterior
intestinal diverticulum (the so-called proboscis-intestine) of Balano-
glossus (Vol. i., Fig. 165, di, p. 375), according to him and to Koehler,
is the homologue of the notochord. The rudiment of the so-called
proboscidal coelom is homologised with the anterior unpaired entoderm-
diverticulum of Amphioxus (Fig. 285 B). The external aperture of
the left anterior entoderm-diverticulum of Amphioxus is assumed to
correspond to the proboscis-pore of Balanoglossus. A posterior fold
in the collar-region, called by Bateson the "operculum," is said to
correspond to the epipleura of Amphioxus. Finally, even Gegenbaur
compared the ventral nutritive section of the pharynx in Balanoglossus
(Vol. i., Fig. 166, d, p. 377) to the endostyle of the Tunicates.
Spengel (No. 47) has pointed out the difficulties that stand in the
way of such a homology, and lays special stress on the great difference
in the position of the gills which, in Balanoglossus, are dorsal, and, in
Amphioxus, ventral — the development of the blood-vascular system
and the genital organs in the two groups. The bare fact of the
presence of gills in Balanoglossus, indeed, and their remarkable and
detailed agreement in structure and arrangement with those of
Amphioxus (U-shaped form in consequence of the growth of tongue-
bars, chitinous skeletal structures in the form of prongs, presence of
synapticula) seem to us of such significance that we cannot avoid
the thought that we have, in Balanoglossus, the only living form of
invertebrate which is closely related to the Chordata. But, if we
adopt this assumption, the Chordata naturally become somewhat
more remote from the Annelida, since Balanoglossus is only distantly
related to this last group. How far it is possible to remove the diffi-
culties which now lie in the way of establishing a stricter homology
between BcUanoglossus and Amphioxus must be decided by further
research .
The problem of the derivation of the Chordata is not solved by
assuming a relationship between them and the Enteropncusta, since
the latter themselves occupy an unusually isolated position. Only
through the structure of the Balanogi lossus larva is an indication
given of remote connection with the Echinoderma. We musl
resign ourselves to the thought that we are not at present in a
position to state from what primitive form the Chordata and, with
them, BcUanoglossus are to be derived. The origin of the Vertebrates
is lost in the obscurity of forms unknown to us.
580 CEPHALOCHORDA.
LITERATURE.
1. Boveri, Th. Ueber die Niere des Amphioxus. Miinchener
Med. Wochenschr. No. 26. 1890.
2. Boveri, Th. Die Nierenkanalchen des Amphioxus. Ein Beit-
rag zur Phylogenie des Urogenitalsystems der Wirbelthiere.
Zool. Jahrb. Abth.f. Anat. Bd. v. 1892.
3. Boveri, Th. Ueber die Bildungsstatte der Geschlechtsdrusen
und die Entstehung der Genitalkammem beim Amphioxus.
Anat. Ariz. Jahrg. vii. 1892.
4. Hatschek, B. Studien iiber Entwicklung des Amphioxus.
Ark. Zool. Inst. Wien. Bd. iv. 1881.
5. Hatschek, B. Mittheilungen iiber Amphioxus. Zool. Anz.
Jahrg. vii. 1884.
6. Hatschek, B. Zur Entwicklung des Amphioxus. Vers. D.
Naturf. Aerzte in Berlin. Tagebl. lix., p. 271. 1886.
7. Hatschek, B. Ueber den Schichtenbau von Amphioxus. Anat.
Anz. Jahrg. Hi. 1888.
8. Hatschek, B. Die Metamerie des Amphioxus und des Ammo-
coetes. Verhandl. der Anat. Gesellseh. 6. Vers, in Wien.
Anat. Anz. Jahrg. vii. 1892.
9. Kohl, C. Einige Bemerkungen iiber Sinnesorgane des Amphi-
oxus lanceolatus. Zool. Anz. Jahrg. xiii. 1890.
10. Kowalevsky, A. Eiitwicklungsgeschichte des Amphioxus
lanceolatus. Mem. Acad. Imper. St. Petersbourg (7). Tom. ii.
1867.
11. Kowalevsky, A. Weitere Studien iiber die Entwicklungs-
geschichte des Amphioxus lanceolatus. Archir. f. mikro.
Anal. Bd. xiii. 1877.
12. Lankester, E. Ray. Contributions to the Knowledge of Am-
phioxus lanceolatus Yarell. Quart. Jonm. Micro. Sci. (2).
Vol. xxix. 1889.
13. Lankester, E. Ray and Willev, A. The Development of the
Atrial Chamber of Amphioxus. Quart. Journ. Micro. Sci. (2).
Vol. xxxi. 1890.
14. Leuckart, R. und Nitsche, H. Zoologische Wandtafeln.
Cosset. Plate 72 contains a drawing of a hitherto unfigured
stage of Amphioxus. Of. also the accompanying text by
Hatschek.
15. Leuckart, R. und Pagenstecher, A. Untersuchungen iiber
niedere Seethiere. 1. Amphioxus lanceolatus. Archiv.f. Anat.
Phys. 1858.
LITERATURE. 581
16. Lwoff, B. Ueber Ban unci Entwicklung der Chorda von Amphi-
oxus. Mittheil.Zool.Stat.Neapel. Bd. ix. 1889.
17. Lwoff, B. Ueber einige wichtige Punkte in der Entwicklung
des Amphioxus. Bio/. Oentralbl. Bd. xii. 1892.
18. Schultze, M. Beobachtung j unger Exemplare von Amphioxus.
Zeitsehr.f. wiss. Zool. Bd. iii. 1851.
19. Spengel, J. W. Beitrage zur Kenntniss der Kiemen des
Amphioxus. Zool. Jahrb. Ahth. f. Anat. Bd. iv. 1890.
20. Weiss, F. E. Excretory Tubules in Amphioxus lanceolatus.
Quart. Journ. Micro. Sci. (2). Vol. xxxi. 1890.
21. van Wijhe, J. W. Die Kopfregion der Cranioten bei Amphioxus,
etc. Anat. Am. Jahrg. iv. 1889.
22. van Wijhe, J. W. Ueber Amphioxus. Anat. Am. Jahrg. viii.
1893.
23. Willey, A. The Later Larval Development of Amphioxus.
Quart. Journ. Micro. Sci. Vol. xxxii. 1891.
23a. Wilson, E. B. On Multiple and Partial Development in
Amphioxus. Anat. Anz. Jahrg. \ii. 1892.
On the Phylogeny of the Chordata.
24. Balfour, F. M. A Monograph on the Development of Elasmo-
branch Fishes. London, 1878.
25. Balfour, F. M. A Treatise on Comparative Embryology.
Vol. ii., chap, xii., p. 258. 1881.
26. Bateson, W. The Ancestry of the Chordata. Quart. Journ.
Micro. Sci. (2). Vol. xxvi. 1886.
27. Beard, J. The Old Mouth and the New. A Study in Verte-
brate Morphology. Anat. Anz. Jahrg. iii. 1888.
28. Beard, J. Some Annelidan Affinities in the Ontogeny of the
Vertebrate Nervous System. Nature. Vol. xxxix. 1889.
29. Van Beneden, E. et Julin, Ch. Recherches sur la Morpho-
logie des Tuniciers. Archie. Biol . Tom. vi. 1887.
30. Dohrn, A. Der Ursprung der Wirbelthiere und das Princip
des Functionswechsels. Leipzig, 1885.
31. Dohrn, A. Studien zur Urgeschichte des Wirbelthierkorpers.
Xos. 1 and 2 in Mittheil. Zool. Stat. Neapel. Bd. iii. 1882.
No. 3, ibid. Bd. iv. 1883. Nos. 4, 5, 6, ibid. Bd. v.
L884. Nos. 7, 8, 9, 10, ibid. Bd. vi. 1886. Nos. 11, 12,
ibid. Bd. vii. 1886-87. Nos. 13, 14, ibid. Bd. viii. 1888.
No. 15, ibid. Bd. ix. 1889-91. Nos. 16, 17, ibid. Bd. x.
1 89 1 .
582 CEPHALOCHORDA.
32. Ehlers, E. Nebendarm mid Chorda dorsalis. Nachr. Ges.
Wis*. Gbttingen. 1885.
33. Eisig, H. Monographie der Capitelliden. Fauna und Flora
ll . Nnturf. Berlin, 1897.
VI. Krause, W. Die Farbenempfindung des Amphioxus. Zonf.
Anz. Jahrg. xx. 1897.
VII. Macbride, E. W. The Relationship of Amphioxus and
Balanoglossus. Proc. Cambridge Phil. Soc. Vol. ix. 1897.
VIII. Macbride, E. W. The Early Development of Amphioxus.
Quart. Journ. Minn. Sci. Vol. xl. 1898.
Villa. MacBride, E. W. Further remarks on the development of
Amphioxus. Quart. Journ. Micro. Sri. Vol. xliii. 1900.
IX. Minot, C. S. Cephalic. Homologies. A Contribution to the
Determination of the Ancestry of the Vertebrates. Amer.
Nat. Vol. xxxi. 1897.
IX-/. Samassa, P. Studien iiber den Einfluss des Dotters auf die
GastrulatioD und die Bildung der primaren Keimblatter der
Wirbclthiere X. Amphioxus. Archiv. f. Entiv. Mech. Bd.
vii. 1898.
X. Sobotta, J. Beobachtung uber den Gastrulationsvorgang
beim Amphioxus. Ve.rh. Ges. Wurzburg (2). Bd. xxxi.
1897.
XI. Sobotta, J. Die Befruchtung des Eies von Amphioxus
lanceolatus. A>>>if. Anz. Bd. xi. 189o.
XII. Sticht, 0. VAN der. La Maturation et la fecondation de l'oeuf
d' Amphioxus lanceolatus. Bull. Acad. Bflij. (3). Tom. xxx.
1895.; and Archiv. Biol. Tom. xiv. 1896.
XIII. Willev, A. Amphioxus and the Ancestry of the Vertebrates.
Loudon and New Voik. 1894.
SUBJECTS INDEX.
A.
Acanthodrilus, 79.
Acanthoteuthidae, 235.
Acanthoteuthis, 292.
Acavus, 104. 179, 186,
191, 192, 196, 197.
Acera, 100, 160, 173.
Acipenser, 355, 564.
Acmaea, 99.
Actaeon, 100, 145, 162,
163, 224.
Aeolidae, 159, 161, 164.
Aeolis, 100, 102, 160, 164.
Amaroucium, 336, 449-
453, 468, 469, 514.
Ammocoetes, 522, 523,
564.
Animoiioidea, 235, 287,
288.
Aniphibola, 175, 182.
Amphineura, 1-21.
Amphioxus, 334, 339,
342, 343, 348-350, 353,
361, 366, 377, 520-524,
536-579.
Amusium Dalli, 71, 72.
Anchinia, 367, 479-483,
519.
Ancylus, 101, 180.
Anodonta, 23, 24, 50-54,
58, 62, 66, 72.
Anomia, 82.
Aplysia, 100, 102, 108,
112,115,117, 129,141,
145, 159-161, 164, 173.
Appendicularia, 334, 338,
355, 360, 366, 367, 448,
518-521, 561.
Area, 22, 70-72, 78, 79,
82.
Arcidae, 48.
Argonauta. 235-240, 251-
253. 257, 266, 267, 287,
294-296.
Arion, 101, 184-187.
Articulamentum, 13.
Ascidia canina, 337.
— mentula, 359.
Ascidiacea, 334.
Ascidiae Compositae,
334.
— Luciae, 334.
— Simplices, 334.
Ascidiella, 377, 378.
Ascidiozooid, 389-414.
Atlanta, 100, 102, 154-
158.
Auricula, 101, 175, 176.
Aviculidae, 37, 61.
Azygobranchia, 99.
B.
Balanoglossus, 542, 549,
575-579.
Basommatophora, 101.
Belemnites, 235, 288-295.
Belemnoteuthis, 235,
292.
Bellerophon, 188.
Belosepia, 290, 291.
Botryllidae, 372, 149.
456, 457, 460, 463.
Botryllus, 367, 377, 465,
466.
Branchiopneusta, 182.
Buccinum, 100, 103.
Bulimus, 101, 104, 105.
Bulla, 100.
Busycon, 103.
Bythinia, 100, HI, 114,
118, 121, 129, 136-141,
191-195, 204, 205, 209-
212.
C.
Cadulus, 96.
Calvptraea, 100, 152.
Capitellidae,82,577,578.
Cardium, 22, 23, 27, 30,
47, 67, 76.
Carinaria, 100, 102. 114,
154-158.
Cavolinia, 100. Ill, 167-
171.
Cephalochorda, 536-579.
Cephalopoda, 1, 235-314.
Chaetoderrna, 1, 324.
Chaetogaster, 577.
Chilina, 145.
Chiroteuthidae, 235.
Chiton, 1-18, 37. 93, 200,
208, 215, 308, 315, 319,
323, 326.
— marginatus, 5, 6.
— olivaceus, 10.
— Polii, 2, 3, 6, 8, 10.
Chromodoris, 100, 160,
164.
Ciona, 336-339, 342-346,
350, 361, 368, 377, 448.
Circinalium, 336.
Cirrhoteuthidae, 235.
Cirrhoteuthis, 265, 295.
Clausilia, 101, 105, 184,
187.
Clavelina, 335-340, 344-
351, 360-364, 367-377,
452, 463-469.
— lepadiformis, 359.
i — Rissoana, 344-351.
I Cleodora, 100, 167.
Clione, 101, 102, 115,
118, 167, 171. 172.
; Coelocormidae, 519.
I Colellapeduuculata,457.
! Cranchiidae, 235, 293.
! Crepidula, 100, 103, 107,
110, 111, 115119, 128,
129, 141.
I — convexa, 105.
— fornicata. 105.
— plana, 105.
Creseis, 100, 102,
169.
Ctenodonta, 61.
Ctenophora, 321.
Cuspidaria, 22.
Cyathozooid, 389, 393-
404.
Cyclas, 22-30. 33-35, 39-
48, 51, 55, 59, 63, 66-
76, 82, 123.
Cyclomyaria, 334, 519.
167-
586
SUBJECTS INDEX.
Cyclosalpa affinis, 495.
— dolichosoma - virgula,
416.
— pinnata, 433, 507, 508.
Cymbulia, 100, 111, 115,
167, 168-170.
Cynthia, 335, 357, 381.
D.
Daudebardia, 101.
Dentalium, 88-98, 132,
192, 200. 216, 318, 319,
329, 330.
Diazona violacea, 448.
Dibranchia, 235.
Didemnidae, 367, 372,
456, 457, 459-464.
Dimya, 71, 72.
Diotocardia, 99.
Diplosomidae, 459-463,
518.
Dissoconch, 61.
Distaplia, 339, 350, 354,
357, 364-367, 372, 457,
469.
— magnilarva, 346, 353,
457.
— stylifera, 464-466.
Distomidae, 372, 456,
457, 463, 473.
Docoglossa, 99.
Dolchinia, 473, 479, 482,
483.
Doliolidae, 470-483, 514,
518-520.
Doliolum, 334. 355, 367,
382-389, 432, 447, 470-
483, 512, 517.
— Ehrenbergii, 385.
— Mulleri, 383-387, 471,
474, 475.
Doliopsis (Anchinia),
519.
Dondersia, 1, 12, 15, 318,
326.
— banyulensis, 15, 17-19.
— festiva. 16.
Doridiae, 330.
Doridopsis, 330.
Doris, 100, 102, 159, 164.
Dosidicus, 293.
Doto, 100, 102.
Dreissensia, 23, 30, 33-
35, 39, 45, 47, 49, 61,
68.
E.
Eledone, 235-239, 251.
Elysia, 100, 159, 164.
Emarginula, 188.
Enantia spinifera, 325.
Entocolax, 153.
Entoconcha, 100, 111.
— mirabilis, 152.
Entovalva, 43, 67, 208.
— mirabilis, 23.
Ercolania, 111, 159, 164.
Eulamellibranchia, 22.
Eunicidae, 577.
Euthyneura, 146.
Fasciolaria, 100, 103,
104, 128, 209.
Filibranchia, 22.
Fiona, 100, 159, 164.
Firoloida, 100, 102, 111,
134, 153-158, 166, 200.
— Desmaresti, 114, 153,
154.
Fissurella, 99, 111, 130,
188, 189, 209, 215.
Fragaiium, 336.
Fragaroides, 450, 451.
Fulgur, 100, 102, 103,
107, 116, 120, 128, 130,
149.
Fusus, 100, 106,111, 115,
117, 121,141,149,150-
152, 205, 206.
— antiquus, 103.
G.
Gasteropteron, 100, 173,
174.
Gastrochaena, 43, 62.
Gastropoda, 1, 98-234.
Glochidium, 54-57.
Gnathobdellidae, 102.
Gonatus Fabricii, 292.
Gunda, 320.
Gymnosomata, 101, 171.
H.
Haliotis, 97, 99, 147,
188, 198, 209, 214.
Helicarion, 200.
Helicinidae, 99, 199.
Helix, 101,105,179,186,
200, 204.
— nemoralis, 201.
— pomatia,104,183,184,
213.
— Waltoni, 104, 179,
186, 191, 192, 196, 197.
Hemimvaria, 414 - 448,
519.
Heteropoda, 100, 102,
153.
Hyalea, 167.
Hyalocylix, 100, 167.
J.
Janthina, 100, 104, 120.
K.
Kalymmocytes, 336, 390,
420-424.
Lamellibranchia, 1, 22-
87, 330.
Larvacea, 334.
Lasidium, 57.
Leachia, 292.
Lepidosteus, 355.
Lima, 82.
Limacidae, 329.
Limacina, 100, 169.
Limapontia, 164.
Limax, 101, 104, 110,
111, 119, 136, 177, 179,
184-187, 191, 204, 217.
Limnaea, 101, 111, 114,
120, 132, 141, 177-183,
203, 221.
Lithonephrya, 335, 381.
Loliginidae, 235.
Loligo, 236-246, 251, 252-
277, 287, 296, 298-
301, 309.
— Pealii, 239, 241-248,
252-254, 258.
— vulgaris, 236, 252-
255, 259, 274, 282-284,
297.
Lucernaria, 520.
Lumbricus trapezoides,
574.
M.
Marsenina, 99.
Megascolex, 79.
Melania, 105.
Melibe, 330.
Michrochaeta, 79.
Mitraria larva, 18.
Modiolaria, 22, 25, 27,
30, 33, 47.
Molgula macrosipho-
nica, 382.
Molgulidae, 381, 445.
Mollusca, 1-333.
Monotocardia, 99, 147.
Montacuta, 30, 47, 68.
Mulleria, 80.
Murex, 100, 103, 200.
— brandaris, 19S.
SUBJECTS INDKX.
587
Muscidae, 874.
Myopsida, 235.
Mytilidae, 14, 37.
Mytilus, 22-25, 30, 33,
37, 39, 45, 47, 68-71.
— edulis, 22, 24, 68.
Mvzomenia, 1, 15, 19.
N.
Nais, 577.
Nassa, 100, 102, 106,
113, 116-121, 141, 149,
152, 163, 200, 208, 315.
— mutabilis, 103, 112,
116, 117. 150, 152,207.
Nassopsis, 105.
Natalina, 200.
Natica, 149.
Nautiloidea, 235.
Nautilus. 237, 268, 286-
288, 293-296, 301, 304-
308, 331.
Neaera, 22.
Nemertini, 322, 575.
Neomenia, 1.
Nephropneusta, 182.
Neritidae, 99, 199.
Neritiua, 99, 107, 110,
111, 116,118,129, 130,
133, 141.
— fluviatilis, 103, 116.
Nucleobranchia, 100,
153.
Nucula, 22, 37, 61, 63,
72, 75, 82.
Nuculidae, 48, 61.
Nudibranchia, 100.
O.
Octacnemus, 334.
Octopoda, 235.
Octopus, 236-239, 251,
253, 257, 264-267, 295.
— membranaceus, 265.
— vulgaris, 201, 252,
265.
Oigopsida, 235.
Oikopleura, 356.
Ommastrephes, 236, 267,
287, 291-293, 308.
Onchidium, 66, 101, 104,
111, 129, 133, 174-176,
329.
Onychoteuthidae, 235.
Onychoteuthis, 292.
Opisthobranchia, 100,
158.
Orthoceratidae, 288.
Ostracum. 288.
Ostrea, 22-38, 45-49, 66,
71, 80, 82, 115, 316.
- edulis, 23, 28, 33, 60.
— virginiana, 22, 25, 60.
Oxygyrus, 100. 102, 157.
Paludiua, 100, 106, 114,
121, 122, 129, 134-142,
148, 149, 151, 153, 163,
191-199, 202, 211-221,
318.
— vivipara, 105, 137,
139, 212-214, 219.
Patella, 4, 91, 99, 101,
106, 113-132, 141, 147,
148, 180, 188, 214, 318.
— rota, 198.
Pecten, 22, 24, 49, 61,
70-76, 82.
— eyes of, 64-66.
Pedicellina, 376.
Pegea bicaudata, 418.
— scutigera - confoede-
rata, 446, 495.
Peripatus, 80, 317.
Perophora, 379, 445, 456,
463, 465.
— Listeri, 379, 380.
Pballusia, 346, 357, 360,
366, 372.
— mammillata, 335, 343,
355, 356, 358, 373, 376.
— scabroides, 377, 378.
Philine, 100, 145, 164.
Philonexis, 235, 237.
Pholas, 45, 70.
Phragmocone, 288.
Phragmophora, 235.
Phyllidia, 330.
Phyllirhoe, 164.
Physa, 119.
Pilidium larva, 322.
Pinna, 82.
Pinnoctopus, 265.
Pisidium, 23-26, 29, 30,
39, 46, 47, 68, 73.
Planorbis, 101, 107, 109-
114, 117,118, 129, 141,
148, 149, 177-183, 204.
Pleurobranchea, 100.
Pleurobranchus, 100,
102, 164.
Pleuronectidae, 574.
Pleurotomaria, 99, 147,
188.
Pneumoderma, 101, 167-
172.
Polycera, 100, 164.
Polyclinidae, 335, 449,
452-455, 470.
i Prodissoconch, 61.
j Proneomenia, 1, 15, 19.
— aglaopheniae, 325.
Prosobranchia, 99. 102,
148.
Protobranchia, 22.
Pseudolamellibiaiichia,
22.
Pteropoda, 100, 102, 166,
173.
Pterotrachea, 100, 102,
111, 154-158.
Pulmonata, 101, 174,
187.
Pupa, 105.
Purpura, 100, 113, 115.
— floridana, 102.
— lapillus, 103.
Pyramidellidae, 330.
Pyrosoma, 334, 356, 367,
377, 381, 389-414, 420,
432, 451,455, 459,479,
484-500, 503, 508, 512-
520.
R.
Rossia, 236.
Rostellaria, 100, 157.
Runcina, 100.
Saccoglossa, 163.
Sagitta, 542.
Salpa, 334, 336, 381, 414-
448, 494-518.
— affinis, 495.
— africana - maxima,
417, 433, 435, 440, 442,
445.
— bicaudata, 417-419,
448.
— costata-Tilesii, 417,
495.
— democratica - mucro-
nata, 415, 420-446,495,
496, 511, 513.
— dolicbosoma - virgula,
416, 495.
— bexagona, 417, 446.
- pinnata, 416-420, 423,
433, 435-448, 495, 507.
— punctata, 417, 420,
433. 435, 445.
— runcinata-fusiformis,
433, 435, 442, 445, 507.
— scutigera - confoede-
rata, 446, 495.
588
SUBJECTS INDEX.
Salpa zonaria - cordi-
formis, 417, 495.
Salpidae, 414-448, 451,
477, 488, 494-512, 516-
520.
Scaphites, 294.
Scaphopoda, 87-98.
Scarabus, 175, 176.
Scioberetia, 45.
Scissurella, 188.
Sepia, 236-252, 272-277.
287-293, 296, 298.
— aculeata, 290.
— andreanoides, 289.
— officinalis, 238, 241-
247, 250, 273-276.
Sepiidae, 235.
Sepiola, 236, 244, 257.
Sepiolidae, 235.
Sepioteuthis, 238.
Siphonaria, 119.
Siphonodentalium, 96.
Solenoconcha, 1, 88-98,
329.
Solenogastres, 1.
Solenomya, 22. 75, 82.
Spekia, 105.
Spinalis, 100, 169.
Spirula, 235, 268, 286,
288, 293, 294.
Spirulidae, 235.
Spirulirostra, 288, 290.
Spondylus, 66, 82.
Stilifer, 100.
— Linckiae, 152.
Streptoneura, 99.
Strombus, 100, 157.
Styelidae, 372.
Styliola, 100, 167, 169.
Stylomatophora, 101,
184.
Succinea, 101, 132, 180,
187.
Synapta, 43.
— digitata, 152.
Taenioglossa, 153.
Taonius, 292.
Tectibranchia, 100.
Tegmentum, 13.
Teredo, 23-39, 42, 44, 66-
73, 80, 208, 319.
Tergipes, 100, 102.
— Edwardsii, 164, 165.
— lacinulatus, 164.
Testacella, 101.
Testacellidae, 182.
Tethys, 111, 119, 330.
Tetrabranchia, 235.
Teuthidae, 236.
Teuthis, 267.
Thalia democratica-mu-
cronata, 415, 420-446,
495, 511, 513.
Thaliacea, 334.
Thecosomata, 100.
Thyca, 100.
— entoconcha, 152.
Tiedemannia, 100, 167-
170.
Tornatella, 163.
Tremoctopus, 235, 237.
Triclada, 320.
Trididemnum, 460-462.
Trigonia, 71.
Tritonia, 100.
Trochophore, 5-7, 10, 18,
30-43, 91, 125-128, 142,
161, 167, 177, 318-326.
Trochus, 99, 198, 209,
215.
— magus, 198.
Trophozooid, 289.
Tunicata, 334-534.
Turbellaria, 108, 320.
Turbinidae, 199.
Turbo, 99, 215.
— creniferus, 198.
Typhobia, 105.
U.
Umbrella, 100, 107, 110,
111, 118-120, 129, 159.
Unio, 22-29. 38, 119.
Unionidae, 25-29, 30, 39,
49-59, 66-71, 73-76.
Urosalpinx, 103, 113,
116, 117.
V.
Vaginulidae, 175, 176.
Vaginulus, 101, 175.
Valvata, 99, 100.
Veliger larva, 130-134,
162, 169, 177.
Venus, 22.
Vermetus, 100, 105, 111,
115-122, 130-132, 148,
180, 192, 197, 200, 217.
Vitrma, 101, 105.
Yoldia, 19, 22, 63, 72.
Z.
Zygobranchia, 99.
AUTHORS INDEX.
Adams, A.
Cephalopoda, 294.
Adler, J., and Han-
cock, A.
(lastropoda, 158, 164.
Andrews, E. A.
Lamellibranchia, 64.
Appeloff, A.
Cephalopoda, 291.
B.
Baer. K. E. v.
Tunicata, 524.
Balfour, F. M.
Ccphalochorda, 577,
578.
Lamellibranchia, 50.
Tunicata, 355, 514,
522.
Barrois, J.
Tunicata, 433, 436,
445, 472-474, 480.
Barrois, Th.
Lamellibranchia, 22,
24, 66.
Bateson, \V.
Cephalochorda, 549,
578, 579.
Beard, J.
Cephalochorda, 576,
577.
Beddard, F.
Oligochaeta, 79.
Behme, Th.
Gastropoda, 213.
Beneden, Ed. van, and
JULIN, Ch.
Cephalochorda, 576.
Tunicata, 338-388, 432,
447, 450, 451, 456,
463-469, 482, 520-
522.
Beneden, P. J. van.
Cephalopoda, 236, 252.
Benham, W. B.
Cephalochorda, 583.
Bergh, R.
Gastropoda, 176.
Bergh, R. S.
Lamellibranchia, 74.
Bernard, F.
Lamellibranchia, 45.
Bloch, L.
Gastropoda, 232.
Blochmann, F.
Lamellibranchia, 30.
Gastropoda, 103-109,
111. 112, 115-118,
134, 141, 142, 158-
161.
Blumrich, J.
Amphineura, 10-12.
Boas, J. E. v.
Gastropoda, 169, 173.
BOBRETZKY, N.
Cephalopoda, 241, 248,
279, 282, 286, 298-
309.
Gastropoda, 103, 106,
112, 115-117, 120,
122, 129, 141, 149-
152, 195, 200, 205-
207.
BOUTAN, L.
Gastropoda, 130, 189.
Bouvier, E. L.
Gastropoda, 225.
Boveri, Th.
Cephalochorda, 535,
556, 566, 558-576.
Braun, M.
Gastropoda, 153, 213.
Lamellibranchia, 50,
56, 58-60, 83.
Brock, J.
Cephalopoda, 237.
Gastropoda, 220-223.
Brooks, W. K.
Cephalopoda, 252-254.
Gastropoda, 103, 113.
116, 128.
Lamellibranchia, 27,
28, 31.
Tunicata, 420, 423,
429, 433-438, 441,
443, 445-448, 494,
497-504, 508-510,
515.
Brdce, A. T.
Cephalopoda, 279.
Butschli, O.
Gastropoda, 114, 134,
138, 141, 144, 145,
153, 202, 217.
Lamellibranchia, 64-
66.
Tunicata, 429, 430.
Carpenter, W.
Gastropoda, 225.
Carriere, J.
Gastropoda, 200.
Lamellibranchia, 55,
64, 81.
Castle, W. E.
Tunicata, 336, 338-350.
Caulery, M.
Tunicata, 461, 463.
Chabry, L.
Tunicata, 338.
Chamisso, A. v.
Tunicata, 417.
Chiaje, St. Delle.
Cephalopoda, 294.
Claparede, E.
Gastropoda, 103, 133.
Clads, C.
Gastropoda, 173.
Tunicata, 415, 512.
CONKLIN, E. G.
Gastropoda, 105-108,
113, 115, 118, 123,
129, 141, 143.
Crampton, H. E.
Gastropoda, 108, 119.
D.
Dall, W. H.
Lamellibranchia, 71.
590
AUTHORS INDEX.
Damas, D.
Tunicata, 368.
Davidoff, M. v.
Tunicata, 336, 338,
350-354, 520.
Della Valle, A.
Tunicata, 448, 457-463.
Dietl, M. J.
Cephalopoda, 304.
Doderlein, L.
Cephalopoda, 313.
Dohrn, A.
Cephalochoi-da, 573,
575.
Tunicata, 522, 523.
Drew, G. A.
Gastropoda, 232.
Larnellibranchia, 19,
63.
E.
Ehlers, E.
Cephalochorda, 577.
Ehrenbaum, E.
Larnellibranchia, 61.
Eisig, H.
Cephalochorda, 577.
Gastropoda, 220, 221.
ElSMUND, J.
Cephalochorda, 583.
Erlanger, R. v.
Gastropoda, 114, 118-
122, 129, 134-136,
139, 141, 153, 179,
191-199, 204, 209-
220.
Eschricht, D. F.
Tunicata, 417, 494.
F.
Fadssek, V.
Cephalopoda, 314.
Fischer, P.
Gastropoda, 101, 199.
Fischer, H.
.^Gastropoda, 204.
Fleischmann, A.
Larnellibranchia, 81.
Flemming, W.
Larnellibranchia, 50,
53.
Floderus, M.
Tunicata, 532.
Fol, H.
Gastropoda, 102, 111,
114, 128, 153, 154,
166-187, 191, 192,
197, 200, 202.
Tunicata, 335-338, 365,
474.
Forel, F. A.
Larnellibranchia, 50,
54.
Fraisse, P.
Gastropoda, 199.
Fugita, T.
Gastropoda, 233.
Fulxarton, J. H.
Larnellibranchia, 22,
24, 49.
G.
Ganin, M.
Gastropoda, 178, 217.
Insecta, 286.
Larnellibranchia, 73,
74.
Tunicata, 379, 458, 463,
513.
Garstang, W.
Tunicata, 377.
Gegenbaur, C.
Amphineura, 12.
Cephalochorda, 578,
579.
Gastropoda, 128, 153,
155-157, 167-174,
179, 184-187.
Tunicata, 382, 459, 476,
523.
GlARD, A.
Mollusca, 332.
Tunicata, 449, 452, 458,
463.
Giard, A., and Caulery,
M.
Tunicata, 532.
Girod, P.
Cephalopoda, 285, 286,
310.
GOPPERT, E.
Tunicata, 430.
Goette, A.
Larnellibranchia, 27,
29, 50, 51.
Goodrich, E. S.
Mollusca, 327.
Graber, V.
Insecta, 286.
Graff, L. von.
Mollusca, 332.
Grenacher, H.
Cephalopoda, 236, 251,
279, 282, 286, 296-
298, 301, 303.
Grobben, C.
Cephalopoda, 304-307.
Gastropoda, 157, 173.
Larnellibranchia, 22,
78, 80.
Tunicata, 382, 388,
470-478, 512, 519.
H.
Haddon, A. C.
Gastropoda, 120, 159,
164, 193.
Haeckel, E.
Cephalochorda, 578.
Tunicata, 523.
Haller, Bela.
Amphineura, 15.
Hamman, J.
Cephalochorda, 583.
Hancock, A. See Adler
and Hancock.
Hansen, G. A.
Amphineura, 20.
Hatschek, B.
Amphineura, 11.
Cephalochorda, 535-
577.
Larnellibranchia, 23,
26-39, 63, 67.
Tunicata, 350, 522.
Heider, K.
Tunicata, 336, 416,
420, 423, 426, 433,
436, 441, 445.
Henchman, Annie P.
Gastropoda, 191, 195.
Herdman, W. A.
Tunicata, 335, 457,
460, 519, 520.
Hertwig, 0.
Cephalochorda, 540-
543.
Tunicata, 336, 356.
Hertwig, R.
Cephalochorda, 541.
Gastropoda, 173.
Tunicata, 365, 489.
Heymons, R.
Gastropoda, 118-120,
123, 159-163.
Insecta, 286.
Hilger, C.
Gastropoda, 198.
Hjort, J.
Tunicata, 361, 449,
458, 463-466, 516.
Hjort, J., and Bonne-
vie, Fr.
Tunicata, 532.
Holmes, S. J.
Gastropoda, 184.
Horst, R.
Larnellibranchia, 23-
30, 47.
AUTHORS INDEX.
591
HUBRECHT, A. A. W.
Amphineura, 15, 16.
Huxley, T. H.
Cephalochorda, 578.
Lamellibranchia, 47,
48.
Tunicata, 389, 413,
484, 494, 499, 519.
Jackson, R. T.
Lamellibranchia, 42,
47-49, 60, 61, 68.
Jacobson, L.
Laniellibranchia, 56.
Jaekel, O.
Cephalopoda, 292.
Jatta, G.
Cephalopoda, 305.
Jhebing, H. v.
Amphineura, 11, 56.
Cephalopoda, 304, 308.
Gastropoda, 147, 175,
182, 186, 213.
Lamellibranchia, 73,
82, 83.
Mollusca, 332.
Joliet, L.
Tunicata, 484, 490.
JOUBIN, L.
Cephalopoda, 237, 283,
306, 310.
JOURDAIN, S.
Gastropoda, 179, 186,
205, 208.
Tunicata, 460, 463.
Joyeux-Lafpdie, J.
Gastropoda, 133, 165,
175.
Julin. Ch. See Bene-
den and Julin.
Julin, Ch.
Tunicata, 360, 469.
K.
Kefersteix, W.
Gastropoda, 101, 158.
Tunicata, 382.
K.EFEBSTEIN, W., and
Ehlers, E.
Tunicata, 387, 413.
Kennkl, J. v.
Cephalochorda, 576,
577.
Kerr, J. Graham.
Cephalopoda, 305.
Kikner, L.
Gastropoda, 157.
Kingsi, ey, J. S.
Tunicata, 521 i.
Klaatsch, H.
Cephalochorda, 535.
Kleinenberg, N.
Cephalochorda, 576,
577.
Cephalopoda, 307.
Gastropoda, 122, 196.
Klotz, J.
Gastropoda, 220-223.
Knipowitsch, N.
Gastropoda, 115, 118.
Koehler, E.
Cephalochorda, 579.
Kolliker, A.
Cephalochorda, 564.
Cephalopoda, 241, 245,
252, 273-276, 294-
297.
Tunicata, 458.
Kofoid, C. A.
Gastropoda, 184.
Kohl, C.
Cephalochorda, 564.
Koken, E.
Gastropoda, 188.
Koren, J., and Daniels-
sen, D. C.
Gastropoda, 227.
KOROTNEFF, A.
Tunicata, 336, 420,
423-427, 432, 433,
436, 441, 442, 445-
448, 479, 482, 483.
KORSCHELT, E.
Cephalopoda, 279, 301.
Lamellibranchia, 23,
30, 47.
KOWALEVSKY, A.
Amphineura, 1-15.
Amphioxus, 334.
Cephalochorda, 535.
542, 547, 549, 556,
Cephalopoda, 297.
Gastropoda, 200.
Mollusca, 325.
Solenoconcha, 88-93,
97.
Tunicata, 335-343, 355-
358, 362-366, 373,
376, 389, 391, 395-
403, 408, 429, 443,
448 - 457, 463 - 469,
484, 494, 498, 499,
516-520.
Kowalevsky, A., and
Barrois, J.
Tunicata, 529.
Kowalevsky, A., and
Marion, A. F.
Amphineura, 20.
Krohn. A.
Gastropoda, 128, 133,
155-158, 167-173.
Tunicata, 376, 382,
417, 458, 513.
KUPFFER, C. V.
Cephalochorda, 541,
577.
Tunicata, 335 - 338,
357, 364, 372, 374,
381, 382, 521.
Lacaze-Duthiers, H.
DE.
Gastropoda, 105, 131,
199.
Lamellibranchia, 47,
68, 83.
Solenoconcha, 88, 94-
98.
Tunicata, 381.
Lacaze-Duthiers, H.
de, and Pruvot, G.
Gastropoda, 164.
Lahille, F.
Tunicata, 360, 361,
367, 372, 417, 457,
464.
Lang, A.
Gastropoda, 144-147.
Mollusca, 320, 332.
Langerhans, P.
Gastropoda, 142, 159,
160.
Tunicata, 360, 521.
Lankester, E. Ray.
Cephalochorda, 535,
556-562.
Cephalopoda, 249, 252,
279, 285, 286, 293,
296, 298, 301.
Gastropoda, 112, 114,
128, 131-134, 141,
161, 177, 180, 183,
193, 215.
Lamellibranchia, 25-
30, 40, 68, 74.
Mollusca, 320, 332.
Lankester, E. Ray, and
Willey, A.
Cephalochorda, 535,
550-553, 556-561.
Latter, O. H.
Lamellibranchia, 56.
Lea, I.
Lamellibranchia, 56.
Lee, A. B.
Tunicata, 338.
592
AUTHORS INDEX.
Lefevre, G.
Timicata, 463.
Lehmann, R.
Gastropoda, 228.
Leuckart, R.
Cephalopoda, 254.
Gastropoda, 153.
Lamellibranchia, 73.
Tunicata, 388, 417,
428, 432, 444, 494,
495, 512, 514, 516.
Leuckart, R., and Nit-
sche, H.
Cephalocliorda, 580.
Leuckart, R., and
Pagenstecher, A.
Cephalocliorda, 535,
549, 580.
Leydig, F.
Gastropoda, 134, 202.
Lamellibranchia, 50,
56, 73.
Tunicata, 510.
Lillie, F. H.
Gastropoda, 119, 143.
Lamellibranchia, 24-
29, 38, 50-54.
LOEB, J.
Tunicata, 448.
Loven, S.
Amphineura, 1, 2, 5, 6.
Gastropoda, 158.
Lamellibranchia, 22-
27, 46, 61, 66, 68.
Lwoff, B.
Cephalocliorda, 539,
544, 548.
M.
MacBride, E. W.
Cephalocliorda, 535,
542.
McMurrich, J. P.
Gastropoda, 103-107,
116, 120, 128-130,
149, 193.
Maerenthal, F. C. von.
Cephalopoda, 238.
Manfredi, L.
Gastropoda, 109, 112.
Marion, A. F.
Mollusca, 325.
Mark, E. L.
Gastropoda, 106.
Martens, E. v.
Lamellibranchia, 39.
Maurice, Ch.
Tunicata, 338, 357, 451.
Maurice, Ch., and
Schulgin, M.
Tunicata, 450.
Mayer, P.
Cephalocliorda, 577.
Mazzarelli, G.
Gastropoda, 109, 129,
159, 160, 164.
Meissenheimer, J.
Lamellibranchia, 39.
Gastropoda, 136, 179,
184, 217.
Menegaux, M.
Lamellibranchia, 73.
Metcalf, M.
Amphineura, 1-3, 6.
Tunicata, 336, 420,
429, 510.
Metschnikoff, E.
Cephalopoda. 236, 248,
286, 305.
Tunicata, 366, 458,
468.
Meuron, P. de.
Gastropoda, 179.
Milne-Edwards, H.
Tunicata, 338, 374.
Mingazzini, F.
Tunicata, 448.
Minot, C. S.
Cephalocliorda, 583.
Mitsukuri, K.
Lamellibranchia, 71.
Mobius, K.
Lamellibranchia, 23,
24.
Morgan, T. H.
Cephalocliorda, 527,
578.
Moseley, H. N.
Amphineura, 13.
Moss, E. L.
Tunicata, 367.
MULLER, F.
Lamellibranchia. 85.
Mueller, H.
Tunicata, 443.
Muller, Joh.
Gastropoda. 152, 169,
172.
Muller, W.
Tunicata, 522.
N.
Nordmann, A. v.
Gastropoda, 158, 164,
165.
0.
Oka, A.
Tunicata, 458, 462,
463.
Osborn, H. L.
Gastropoda, 209.
Owen, R.
Cephalopoda, 312.
Owsjannikow, P., and
Kowalevsky, A.
Cephalopoda, 298.
Pagenstecher. See
Leuckart and Pa-
genstecher.
Patten, W.
Gastropoda, 101, 107,
113, 114, 119-127,
141.
Lamellibranchia, 64-
66.
Pelseneer, P.
Amphineura, 14.
Cephalopoda, 304, 305.
Gastropoda, 145, 148,
169, 172, 173, 199,
215.
Lamellibranchia, 22,
37, 71, 73, 82, 83.
Mollusca, 332.
Perrier, R.
Gastropoda, 229.
Pfeiffer, C.
Gastropoda, 101.
Pizon, A.
Tunicata, 336, 338,
449, 458, 464.
Plate, L.
Gastropoda, 145, 176,
182, 216.
Scaphopoda, 97.
Poli, G. X.
Cephalopoda, 294.
Power, Mrs.
Cephalopoda, 294.
Pruvot, G.
Amphineura, 1, 15-19.
Q.
QUATREFAGES, M. A. DB.
Lamellibranchia, 86.
R.
Rabl, C.
Gastropoda, 107-110,
112, 134, 141, 176-
182.
Lamellibranchia, 29,
38, 50, 51, 54.
Rankin, W. M.
Lamellibranchia, 76,
81.
AUTHORS INDEX.
593
Rathke, H.
Lamcllibraiichia, 56.
i; wvitz, B.
Lamellibranchia, 64.
Reincke, J.
Amphineura, 11.
Rho, F.
Gastropoda, 158-160,
204.
RlEFSTAHL, E.
Cephalopoda, 289.
KlTTER, W. E.
Tunicata, 463, 465,
4(i7.
ROLPH, \V.
Cephalochorda, 556.
Rosslkk, R.
Gastropoda, 200-202.
Roulb, L.
Cephalochorda, 578.
Mollusca, 333.
Tunicata, 338.
JIouzaud, H.
( lastropoda, 220.
Ki'CKER, A.
Gastropoda, 200.
RtJCKEBT, J.
Ceplialochoi'da, 568.
Ryder, J.
Gastropoda, 230.
Lamellibranchia, 48,
60.
Sabatieb, Ad.
Tunicata, 338.
St. Hilaike, Geoffroy.
Cephalochorda, 575.
Salensky, W.
Cephalochorda, 537.
Gastropoda, 115, 122,
192, 197, 200, 217.
Tunicata, 335, 338,
356, 359, 388-448,
461, 484-489, 506,
509, 512, 516-518.
S \MASSA, P.
Tunicata, 533.
Sabasin, P.
Gastropoda, 138, 141,
191, 205, 208, 215,
217.
Sabasin, P. and P.
Gastropoda, 104, 122,
152, 179, 186, 191-
197.
Sars, M.
Gastropoda, 158.
Tunicata, 458.
SCHALFEEW, M.
Gastropoda, 217.
Schif.mknz, P.
Castropoda, 153, 223.
Lamellibranchia, 81.
Schierholz, C.
Lamellibranchia, 29,
50-60, 63.
SCHIMKEWITSCH, W.
Cephalochorda, 578.
Cephalopoda, 308, 309.
Schmidt, P.
Gastropoda, 122, 134,
184, 187, 191-195.
Lamellibranchia, 50-
59, 62, 63, 76.
Schmidt, Osc.
Gastropoda, 179.
Lamellibranchia, 86.
Schneider, A.
Cephalochorda, 576.
Gastropoda, 164.
Tunicata, 522.
Schulgin, M. See Mau-
rice and Schulgin.
Schultze, Max.
Cephalochorda, 535,
549.
Gastropoda, 158, 164.
Sedgsvick, A.
Amphineura, 1.
Seeliger, Osw.
Tunicata, 339, 349,
360-368, 374-377,
405, 406, 409, 412,
432, 451, 456, 463,
467, 484-498, 509,
512, 515, 516, 522.
Selenka, E.
Gastropoda, 102, 113.
Semon, R.
Cephalochorda, 571.
Semper, C.
Amphineura, 11.
Cephalochorda, 575-
577.
Gastropoda, 175, 176,
223.
Tunicata, 337, 338,
489.
Sharp, B.
Lamellibranchia, 86.
Sheldon, L.
Tunicata, 527.
Simuoth, H.
Amphineura, 15.
Gastropoda, 147, 220.
Mollusca, 330.
Solenoconcha, 98.
Singerfoos, C. P.
Lamellibranchia, 45.
Sluiter, C. Ph.
Lamellibranchia, 62.
QQ
Sobotta, J.
Cephalochorda, 535-
539.
Spengel, J. W.
Cephalochorda, 535,
556, 578, 579.
Gastropoda, 173, 182.
Stauffacher, H.
Lamellibranchia, 24r
25, 39.
S'l KKNSTRUP, J.
Cephalopoda, 236,292.
Steiner, J.
Cephalopoda, 305.
Steinmann, G., 294.
Stepanoff, P.
Lamellibranchia, 23-
73.
STICHT, 0. VAN DER.
Cephalochorda, 535.
Stuart, A.
Gastropoda, 231.
Thiele, J.
Amphineura, 11, 12.
Gastropoda, 234.
Lamellibranchia, 78r
80.
Mollusca, 320, 323.
Scaphopoda, 97.
Todaro, Fr.
Tunicata, 416-421, 426.
432-448, 494 - 498,
515, 516.
ToNNiGES, C.
Gastropoda, 135, 137.
Traustedt, M.
Tunicata, 417.
Trinchese, S.
Gastropoda, 158-163.
Tullberg, T.
Lamellibranchia, 61,
62.
U.
Uljanin, B.
Tunicata, 382-388, 385
471-478, 512, 514.
Ussow, M.
Cephalopoda, 236, 240
241, 244-248, 282
286, 301, 303-306.
V.
Vialleton, L.
Cephalopoda, 238-250,
273-279, 285, 286.
301, 307.
594
AUTHORS INDEX.
ViGUiER, C.
Gastropoda, 159.
Voeltzkow, A.
Lamellibranchia, 23,
43, 67.
VOGT, C.
Gastropoda, 158, 174.
Tunicata, 494.
Voigt, W.
Gastropoda, 153.
Voltz, F.
Cephalopoda, 289.
W.
Warneck, A.
Gastropoda, 106.
Watase, S.
Cephalopoda, 241-246,
285, 286.
Weiss, F. E.
Cephalochorda, 581.
Weltner, W.
Lamellibranchia, 30.
Wierzejski, A.
Gastropoda, 119, 123
184.
WlJHE, I. W. VAN.
Cephalochorda,
560. 571, 574.
WlLLEY, A.
Cephalochorda,
549, 553-561,
575.
Cephalopoda, 237
Tunicata, 350,
361, 365-369,
519-521. See
Lankester
WlLLEY.
Wilson, E. B.
Cephalochorda,
538, 549.
535,
535,
574.
359,
377,
also
and
536,
Wilson, John.
Lamellibranchia, 22,
24, 39, 47.
Witlaczil, Em.
Insecta, 286.
Wolfson, W.
Gastropoda, 114, 120.
141, 176, 178, 183,
193, 202, 208.
Z.
Zernoff, I).
Cephalopoda, 296.
Ziegler, E.
Lamellibranchia, 23-
30, 33, 39-45, 60-63,
66, 73-77, 81-83.
Zittel, K.
Cephalopoda, 291.
Gastropoda, 188.
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