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,
Eutoprocta, Crustacea, Palaeostrica. 12s.
Vol. III. — Arachnida, Pentastomidae, Pantopoda, Tardigrada,
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 w r as 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 ; (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 ; w Jt pre-oral, w IJt 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 row 7 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 7 T /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 tin 1
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< j larva as a neural plate (Figs. 15,
p. 31, 18, p., 36). This consists at first of large closely crowded cells
which, by active division, give rise to a multilaminar cell-plate.. The
upper layer of this plate which remains continuous with the body
epithelium becomes raised up, the lower cell-mass becoming detached
from it in the form of two groups of cells. These are the two halves
of the cerebral ganglion, the connecting commissures of which no
doubt arise in the same way, becoming severed from the ectoderm
(this, according to Ziegler, is probably the case in Cycla*). F.
Schmidt, indeed, has claimed for the cerebral ganglia of the
Uniunidae distinct origins and secondary connection by means of a
commissure, a condition which will lie described in connection with
the Gastropoda (Chap. XXXI 1.). In Anodonta, the two halves of the
ganglion arise near the month and are separated by the stomodaeum,
above which the commissure extends as a loop.
TIIK SENSORY ORGANS. 63
The pedal ganglia, in Oyclas and the Unionidae, according to the
somewhat similar accounts of ZlEGLER and F. SCHMIDT, with which
also that of Schierholz can be harmonised, in their formation arc
associated with the byssal gland. Shortly before the paired byssal
gland becomes invaginated (Fig. 19, ]>. 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
whi le 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 n f 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 tube s, 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*< SS -
53 Sluiter, C'. Ph. Ueber die Bildung der Kalkrbhren von Gas-
trochaena. Natarkund. Tijdschrift NederlarvUch. India. Bd. 1.
1890. .
54 Stepanoff, P. Ueber die Geschlechtsorgane u. die Entwick-
lung von Cyclas cornea. Archiv. f. Noturg. Jahrg. xxxi.
1865.
55. Thiele,Th. Die Mundlappen der Lamellibranchiaten. Zeitschr.
f wiss. Zool Bd. xliv. 1886.
56 Tullberg, T. Studien uber den Ban und .las Wachsthmn des
Hummerpanzers u. der Molluskenschalen. Kgl. Svemka
Vetenskaps-Akad. Handlingar. Bd. xix. No. 3. 1882.
57 Voeltzkow, A. Entovalva mirabilis, eine schmarotzende
Muschel aus dem Darm einer Holothurie. Zool. Jahrb.
Abth. f. Systematik, etc. Bd. v. 1890.
:,*. Weltner, W. Zur Entwicklung von Dreissensia. Zool. Anz.
.lahrg. xiv. 1891.
59. Wilson, John. On the Development of the Common Mussel
LITERATURE. 87
(Mytilus edulis L.). Fifth Annual Report of the Fishery
Board for Scotland (for the year 1886). Edinburgh, 1887.
60. Ziegler, E. Die Entwicklung von Cyclas cornea Lam. Zeitschr.
f. ioiss. Zool. Bd. xli. 1885.
APPENDIX TO LITERATURE OX
LAMELLIBRACHIA.
I. Bernard, F. Scioberetia anstralis, type nouveau de Lamelli-
brauche (Anatomy, Embryology, etc.). Bull. Sci. Frame et
Belgique. Tom. xxvii. 1896.
II. Drew, A. G. Notes on the Embryology, Anatomy and Habits
of Yoldia limatula, Say. Johns Hopkins Univ. Circ. No. 132.
1897.
III. Lillie, F. K. The Embryology of Unio complanata. Journ.
Morphol. Vol. x. 1895.'
IV. Pelseneer, P. Les yeux eephaliques chez les Lamellibranches.
Compt. Rend. Acad. Sri. Paris. Tom. cxxvii., p. 735. 1898.
V. Singerfoos, C. P. The Pholadidae. I. Note on the Early
Stages of Development. Johns Hopkins Univ. Circ 1895.
II. Note on the Organisation of the Larva and the Post-larval
Development of the Shipworm. Op. cit. 1896.
VI. Stauffacher, H. Eibildung und Furchung bei Cyclas cornea.
L. .J»n. Zeitschr. f Natunciss. Bd. xxviii. 1894.
VII. Stauffacher, H. Die Urniere bei Cyclas cornea. Zeitschr.
f. wiss. Zool. Bd. lxiii. 1898.
VIII. VIeissenheimer, J. Entwicklungsgeschichte von Dreissensia
polymorpha. Marburg. 1899. Zool. Gentralbl. Jahrg. vi.
l O'
CHAPTER XXXI.
SOLENOCONCHA (Scaphopoda).
(Dentalium.)
The ontogeny of Dentalium was investigated many years ago
(1857) by Lacaze-Duthiebs, and more recently (1883) by Kowa-
levsky with the aid of sections; the researches of Kowalevsky,
however, do not extend so far into the life of the animal as do those
of Lacaze-Duthiees, the former having been able to observe the
larva only up to the sixth or seventh day, while the latter was able
to keep the larvae alive until they were thirty-five days old. We
therefore still have to refer, for many points, to the older accounts of
Lacaze-Duthiers.
The genital products are discharged into the water through the
right renal aperture, fertilisation taking place outside of the body.
The eggs, which are not very rich in yolk, are surrounded by a thin
envelope.
1. Cleavage and Formation of the Germ-Layers.
The cleavage is total, the egg dividing into two cleavage-spheres,
one of which is somewhat larger than the other. The larger sphere
then, by division, gives rise to a new sphere, and the smaller sphere
als«. divides into two, so that we have now one macromere and three
micromeres. It is possible that additional micromeres are segmented
off from the larger sphere. The former divide repeatedly, so that
there is soon a great number of the micromeres lying upon a single
macromere which still remains rather large. This latter also finally
divides into two and then into four niaeromeres. This method of
cleavage shows considerable resemblance to that most common among
the Lamellibranchia. Further division and the formation of a
mitral cavity give rise finally to a blastula, one half of which con-
sists of small and the other of large cells (Fig. 34 .1). The animal
CLEAVAGE AND FORMATION OK THE GERM-LAYKKS.
89
J3.
pole of this blastula is therefore easily distinguished from the vege-
tative pole; the latter soon heroines somewhat flattened, its cells
becoming invaginated to form the archenteron (B). Dentalium has
thus a typical in-
vagination- gastrula pi
(C) whose trans-
verse axis is some-
what broader than
its invagination-
axis. A few large
blast omeres soon
become detached
from the outer
surface and pass
into the cleavage-
cavity (Fig. 34 C).
Here they become
arranged with bi-
lateral symmetry
and are found,
especially at later
stages, near the
blastopore. They
represent the rudi-
ment of the mesoderm {mes). This latter, which at first consists
of only a few large cells, soon takes the form of two groups of
cells which, after increasing still further in number, form the two
mesoderm-hands which lie near the archenteron.
Fig. B4..—A-C, sections through embryos of Dentalium in
the blastula and gastrula-stages (after Kowalevsky).
hi, blastopore ; mes, rudiment of the mesoderm : w, cells
of the ciliated ring; ws, ciliated tuft.
The mesoderm-rudiment, as has been mentioned, shows a bilateral
symmetry, but this is not so regular as, for instance, in Chiton (p. 4). In
>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). Tin 1 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 : —
'm 1 small mesomere.
fME
D
(left posterior
macromere).
ME 1 (right)-;
Me 1
I , p [ fM 1 mesodermal teloblast.
1 e {e 1 secondary entomere.
E 1 primary entomere.
E- primary entomere.
V- '- ' e " secondary entomere.
. ., j e \ M 2 mesodermal teloblast.
L ME 2 (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>-
( M 1 right mesodermal teloblast.
( M 2 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. Now r , 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 w T ith 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
betw r een 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, p u , 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 r eliger 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
w r as 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 T eliger 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 r eliger 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$.
fi G- 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 orga