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iii 


24503377736 











TEXT-BOOK 


OF THE 


EMBRYOLOGY OF INVERTEBRATES 








By Prors. KORSCHELT ann HEIDER. 


TEXT-BOOK OF THE 
EMBRYOLOGY OF INVERTEBRATES. 
Vou. I.—Porifera, Cnidaria, Ctenophora, Vermes, Enteropneusta, 

Echinodermata. 15s. 


Vou. I1.—Phoronidea, Bryozoa, Ectoprocta, Brachiopoda, 
Entoprocta, Crustacea, Palaeostrica. 12s. 


Vou. ITI.—Arachnida, Pentastomidsae, Pantopods, Tardigrada, 
Onychophora, Myriopoda, Insecta. 14s, 


Vou. IV. 188, 











vi PREFACE, 


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, 
eapecially 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, 
LT 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 
wade certain alterations in the text which appeared justified 
by recent: investigations 

T 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. ili. and iv. came into the hands of 
the translator only in 1897, and the task of bringing them out 
being necessarily somewhat lengthy. it bas been impossible 
suoner to offer the completed work to the English-speaking 
student. to whom it should be of great service. 


MARTIN F. WOODWARD. 


Rov Consus vr Sciescs. Loxpos. 
Fre, W9OU. 


CONTENTS OF VOL. IV. 


Caarren XXIX. AMPHINEURA. By E. Korscuetr. 

I. The development of Chiton . See eS 

1. Tho cleavage and the formetion of the germ-layes 

2, The development of the larval form . . 

8. The further development of the larva and metamorphosis. 

I, The development of Dondersia =. 0. ww wwe 
Literature . 





Cuarrer X LAMELLIBRANCHIA. By E. Korscurut 
1. Oviposition and care ofthe brood . . 1 7 wt 
2. Cleavage and formation of the germ-layers Ree 1S 
8. Development and structure of the Trochophore larva. 
A. The Trochophore stage ass free-swimming larva. 
B. The Trochophore stage of fresh-water Lamellibranchia . 
4. The transformation into the adult . . . . . 
Divergencies in the metamorphosis accompanying the 
Monomyarian condition. . 3 . . . 2. 
5. The development of the Unionidae. . . . 
A. Development of the early stage 
B. The development of the embryo into the parasitic larva 
C. The transition tothe adult. . . . . . 
6. The formation of the organs ‘ 
A.Thesholl. . . 1 we 
B.Thenervoussystem. .  . . 1 wee 
C. The sensory organs. ww wee 
The eyes of Pecten Bite! Loni He 8 
The otocyuts. 5 
Spengol's olfactory organs, abdominal vensory organs. 
D. The alimentary canal gs 
E.The gills. 
F. The body-cavity, the blood-vascular sytem and the 
kidney 2. 
‘The formation of the heart ee 
G. Musculature and connective tissue . . a a 
H. The genital organs. ws 
Literature . . . . ‘s 


Ss 


viii CONTENTS. 


Cuarrer XXXI. SOLENOCONCHA. By E. Korscuett . 
1, Cleavage and formation of the germ-layers . 
2. The development of the form of the larva =. . 
3. The transformation of the larva into the adult . 
Literature =. ae = . . . > + < . 


Cuapren XXXII. GASTROPODA. By E. Korscnetr . 
1. Oviposition and character of the egg-capsules and the eee 
2, Cleavage and formation of the germ-layers ‘ 
8. The formation of the germ-layers . 
The mesoderm. . 
4. The rise of the larva and its relation to the adult form . 
The ontogeny of Patella . .  . 
The Trochophore stage . .  . 
The Veliger stage. a 
The development of Paludina |. 
The primitive kidneys . ue fs 
The shape and transformation of the blastopore. . 
Considerations relating to the asymmetry of the Gastropoda 
. The development of the external form of the body in the 
different divisions of the Gastropoda 
A. Prosobranchia . . . . . . . 


Pa 





B.Heteropoda . 1 www 

!, Opisthobranchia 2  .  . 1 ee 

D. Pteropoda 6 wwe a oS 
Thecosomata oP REM St on a ces ce NS 
Gymnosomata . 5 we 


&. Pulmonata . . . 
The ontogeny of the Stylomatophorous ‘terrestrial 
Pulmonates . Fs . . . 
6. The formation of the organs. we wee 
A. The shell . . . . . . . . . 
B. The nervous system . 
(. The sensory organs . 
Theeyss . . . 
Theotocysts. 2. 0. ewe 
Theosphradium . 7 ww ee 
D. The pedal glands 
E. The alimentary canal 
F.Thegils. 9.2. : 
G, The differentiation of the mesoderm. rudiment, the 
development of the body-cavity, the nephridial and 
circulatory systems 5 ww ewe 
H, The genital organs. 
Literature . . . . . 


III, CEPHALOPODA. By E. Korscnxtt . 





CHapTeR XX: 
1. Oviposition and the constitution of the egg : 
2. Cleavage and formation of the germ-layers  . . . 





x CONTENTS. 


Cuarren XXXV. TUNICATA—continued. 
Themantle. . © . . e. $8 
The nervous system. 7 : 


The ciliated pit . 3 5 3 

The chorda . - . . . c 
Mesoderm, body-cavity, musculature * : ie 
The alimentary canal . a z . a 


Peribranchial, atrial or cloacal cavity . . . . . 
The heart, the pericardium and the epicardium . 
E. Review of the organisation of the free-swimming larva. 
F. Fixation and retrogressive metamorphosis 
‘The development of new gill-slits . . 
‘The development of the genital organs =. | 
G, The abbreviated development of the Molgulidse 
. Doliolum. . a er Ha sis! aah” VG oe 
7 Pyrosoma. . bg ia, headiee a 
4. Cleavage and formation of the germ-layers |. 
B. Development of the Cyathozooid 5 
C. Development of the primary Tetrazooid colony. 
D. Further development of the Cyathozooid 
E. Development of the four primary Ascidiozooids 
5. Tho Hemimyaria (Salpidae) . ae 
A. Forms without covering folds . . . . . . 
B. Forms with covering folds... 
General considerations on the embryonic development 
oftheSalpidsee. . . . . . 
Il. Asexual reproduction... wt ‘ 
1. Social and composite Ascidians 
‘4. Reproduction through transverse fission . 
B. Stolonic gemmation . 
C. Pallial gemmation of the Botryllidae 
D, Budding of the Didemnidse and the Diplovomidae 
E. Development of the organs in pi secrneny produced in- 
dividuals . . . . . . . 
2. Doliolidae . . Boe be As 
Alternation of generations in Doliolum . . . 
Alternation of generations in Anchinia . . . z 
Alternation of generations in Dolchinia . 
3. Pyrosoma. i 
A. Development of the proliferating stolon # 
B. Further development of the buds. 
4. Salpidae . S ‘ : 
4. Structure and development of the proliferating stolon 
B. Development of the buds on the stolon . . 
C. Development of the organs inthe bud . . 
5. The interpretation of the alternation of generations in the 
Tunicates . . . . . . . 
III. General considerations on the “punicates 
Literature 





CONTENTS. 


Cmapren XXXVI. CEPHALOCHORDA (Aeros): By K. 
HEIDER . . . . 
Amphioxus . eee eral 
A. Oviposition, cleavage and ‘gastrulation a és 
B, Development of the medullary tube, the primitive seg- 
ments and the notochord 

C. Farther development up to the time when the mouth 
and the first gill-cleft form . - . . . . 

D. Later larvalstages . . . ww 
General considerations on Amphioxus. - www. 
Literature . . . . . . . . . . . 


Susszcrs Inpex Be 
Aurnors INDEX . . . . : ots 


vi PREFACE, 


“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 great service. 


MARTIN F. WOODWARD. 


Royar CoLircr or Sciexcr, Loxpon, 
June, 1900. 


CONTENTS OF VOL. IV. 


Carrer XXIX. AMPHINEURA. By E. Korscuerr. 
I. The development of Chiton re 
1. The cleavage and the formation of the germ-layera . . 

2. The development of the larval form 
3. The further development of the larva and metamorphosis 
IL. The development of Dondersia A 
Literature . . . . . & “ 


CHapren XXX. LAMELLIBRANCHIA. By E. Korscueit 
1. Oviposition and care of the brood . 5 is 7 . 
2. Cleavage and formation of the germ-layers pea 
3. Development and structure of the Trochophore larva 
A. The Trochophore stage as 8 free-swimming larva . 
B. The Trochophore stage of fresh-water Lamellibranchia . 
4, The transformation intotheadult. . . . . 
Divergencies in the metamorphosis accompanying the 
Monomysrian condition. . 3 . . 3 . 
5. The development of the Unionidae . . * . . 
A. Development of the early stage 
B. The development of the embryo into the parasitic ‘larva 
C. The transition to the adult o 
6. The formation of the organs. ‘ 2 ts 
A. The sholl . o 
B. The nervous system . Ca as ky Ae 
©. Thesensory organs. ww ww wtt 
TheeyesofPecten . . . . . . 
The otocysts . 
Spengel's olfactory organs, abdominal sensory organs . 
D. The alimentary canal ie ts 
E. The gills . 
F. The body-cavity, the blood-vascular sytem and the 
kidney . 
The formation of the heart . . . . 
G, Musculature and connective tissue . . . . 
Hi. The genital organs . 
Literature. if 5 v “i 


» 
= 
& 
™ 


SBSSSSSE HSSSREE BRawnwwe 


o 
8 


BSERBSEB 


2 AMPHINEURA, 


I. The Development of Chiton. 


The external characters of the larva of Chiton and the develop- 
ment of the same were described many years ago by Lovin 
(No. 10), while the formation of the germ-layers and the various 
internal changes have since been investigated with the assistance 
of modern methods by Kowauevsky (Nos. 6-8).* 

Oviposition and Nature of the Eggs, The eggs pass from the genital 
duct into the mantle-groove of the female in an immature condition, 
and are there fertilised by the sperm which the male has discharged 
into the water ; after this they are deposited either singly or in groups. 
They are found floating freely in the water; but, in some cases, as 
in C. Polii, the eggs are retained, until the embryo is mature, 
within the mantle-cavity of the female. ach egg is enclosed 
within a spiny shell, the surface of which is marked out into poly- 
gonal areas, The form of these spines varies in the different species 
and genera. The egg itself does not appear to be yery rich in yolk, 


1, The Cleavage and the Formation of the Germ-Layers., 


The cleavage is total and practically equal, the egg being divided 
by two meridional grooves first into two and then into four blastomeres. 
of almost equal size. At the eight-blastomere stage, however, a 
slight differentiation of the cleavage-spheres lying at the animal pole 
takes place, four larger (vegetative) and four smaller (animal) blasto- 
meres being distinguishable. The animal pole is marked by the 
polar bodies which lie almost exactly over the point of intersection of 
the cleavage-planes. During the further course of cleavage, the 
blastomeres of the vegetative half are at first to be distinguished by 
their larger size, the smaller size of those of the animal pole being due 
to their more rapid division. In the later stages, as in the earliest, 
there is also a certain resemblance to the conditions found in the 
Gastropoda which are characterised by a stage consisting of four 
macromeres and four micromeres (Fig. 40 C’, p. 109). We find here the 


tres are Mollusca at all, According to Sepewick, the most important 
Gitterence between the Solenogastres and all other Mollusca is that in the 
former the gonad opens directly into the pericardium. This distinction does 
not appear to us to be so vital when we remember that in some Molluscs the 
gonad communicates directly with the kidney, the latter in turn opening into 
the pericardium, and further that the cavities of all three organs are parts of 
the primitive coelom.—Ep,] 

*[Mercaxx (No. L.) has since reinvestigated the embryology of Chiton, pay- 
beepers Seaton! Ne the cleavage and cell-lineage, his observations entirely 
confirming those made by Kowanevsky,—Ep.] 


THE CLEAVAGE AND THE FORMATION OF THE GERM-LAYERS. 3 


expression of a kind of radial symmetry, which is still more marked 
in the Gastropoda at a somewhat later stage (Fig. 40 D and Z), and, 
aceording to Kowavevsky's figures, is sometimes also met with in 
Chiton. At first the vells increase in unmber in a more regular 
manner than in the later stages, 

Cleavage results im the production of a somewhat flattened, and 
therefore hemispherical blastula, the vegetative pole of which consists 
of comparatively few but very large cells (Fig. 1 A.) As the cells 








: 


= sections embryos of Chiton Polit at the blastula 
2 Sain bi, blastopore ; m, rudiment of the mesoderm 
ent 0 y ring (velum]. ‘ 


divide, an invagination of the vegetative half (B) takes 
this way the cleavage-cavity, which was never large, is 
The invagination-gastrula (B) which at first is 
at depressed, now elongates in the direction of the invagina- 
‘The archenteron also grows larger. In its wall, near the 
re, there appear two cells which, as compared with the rest, 







». 1.) finds a ba 2 blastocoele which is not wholly obliterated 
ent.—Ep.) 


4 AMPHINEURA. 


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, t.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 
(Lamellibranchia, p. 29, Gastropoda, p. 117). 


2. The Development of the Larval Form. 

Even before the development of the germ-layers has progressed 
thus far, altorations 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, 
@ 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 aud 3, 2 and ws). Very similar 
embryonic stages are met with in the ontogeny of other Mollusca, ¢9., 
Patella (Fig. 50, p. 124). The pre-oral ciliated ring in the Lamelli- 
branch larvae is aleo formed of two rows of cells. Indeed, the 
ciliated ring seems usually to be biserial ; though, in Patella, there 
are three rows of cella (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 BD). 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 4). 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 4} 
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 uctual primitive mouth thus comes to lie at the 
inner end of a laterally compressed ectodermal tube which for some 


‘THE DEVELOPMENT OF THE LARVAL FORM. 5 


time longer continues to deepen (Fig. 2 A, oe). This ectodermal 
invagination, the stomodaenm, represents the rudiment of the fore-gut 
(buceal mass and oesophagus). In connection with it there appears 
later, as a ventral outgrowth, the radular sac (Fig. 2 B, 7). 


‘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. 





Pro. and 2, median longitudinal sections through embryos of Chitow Polit at 
SS Se os Tel 
‘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 (¢.9., Chiton marginatus, 

Loves). The larvae of this latter form carry a large ciliated tuft at 

the frontal pole (Fig. 3.4). The embryos of other Chitones remain 

Jonger in the egg, and before attaining free life approach more nearly 

‘the form of the adult (Fig. 3 ©). 


‘The larwne of the Chitones resemble those of the Annelida, and since a 
phore exceedingly like that of the Annelida is found in other Molluscs 
(Pigs: 1S, 51, 59), we are justified in instituting such a comparison here also, 
a gh the resemblance is not so close. We have here a pre-oral 
ting, and the origin and position of the different sections of the 
tinal canal is the same asin the Trochophore, The larva, at first, has no 
terminal segment of the alimentary canal only appears later ab 
“the posterior end of the body in the form of an ectodermal invagination, the 
oko 







6 AMPHINEURA. 


proctodaeum (Fig. 9). An organ which is of great importance in interpreting 
the larva, the apical piate, is not present in the eariy 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 Chizon Polit 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). 





Fis, 7A, larva of Chilo marginatus (after Lovés); B, embryo; and C, larva of 
Polit (after KowAanewsky) ; ; &, rudiments of sbeli-plates; in, month ; 
a spines; 1, ciliated ring wel}; ys apical ciliated tuft. 





3 The Further Development of the Larva and Metamorphosis. 


The changes that now take place in the larva are introduced by 
considerable growth of the posterior region of the body (Figs. 2 and 5), 
8 process which recalls the development of this same section in the 
Annelidan Trochophore into the trunk region of the worm (Vol. i., 
Fig. 120, p. 269; cf. also Chapter xxxiii.). In the case of Chston, 
it is especially the dorsal surface which increases in size (Fig. 5). 
In some cases, these changes take place even in the embryo, and as 


THE FURTHER DEVELOPMENT OF THE LARVA AND METAMORPHOSIS. 7 


these forms have received more attention than the others, they will 
serve for description, as these processes have a very similar course in 
all Chitones. 

To the organs which we have already found in the larva, a new 
one is udded at a somewhat early stage: this is a sac-like gland, 
opening behind the oral aperture (Fig. 2 3, fd.), According to 
Kowateysky this organ, whieh he regards as the pedal gland, is 
unpaired and originates as a thickening and depression of the 
ectoderm, but this origin has not been fully established. Structures 
corresponding to the “pedal gland” will again be met with in the 
Gastropoda. The nature of this organ in Chiton is not yet quite 
clear, and, as it appears to degenerate later, its efferent duct closing 
first, Kowanevsry regards it as a larval organ. 

As the post-oral portion of the body elongates, the intestine also 
increases in length (Fig. 5); but: its posterior end does not as yet 
communicate with the exterior. It has already been shown that, in 
the Annelidan 7'rochophore, the anus is wanting, or else the intestine 
is in @ very backward stage of development. 

The mesoderm which, as has already been described, first arose as 
two groups of cells continuous with the entoderm, and shifted later 
into the cleavage-cavity near the blastopore, has become richer in 
cells, and with the progressive growth of the larva has extended 
between the ectoderm and the entoderm. Now, as when it first 
appeared, it shows « bilateral arrangement, i., in young embryos 
(aged twelve hours or slightly older, Fig. 3 B), the mesoderm takes 
the form of two compact cell-bands situated on the ventral side of 
the embryo and lying internal to the ectoderm. We may claim 
these as mesoderm-bands, since they later undergo division into a 
splanchnic layer applied to the embryonic intestine and a somatic 

| layer lining the ectoderm (Fig. + 4 and #). The cavity lying 
between therm (coe) which is paired, is consequently to be regarded 

| ae a trne coelom. It develops earlier in the anterior than in the 
posterior part of the body. Thus, when two distinct cavities almost 
‘lined with epithelium are to be found in front, there is still a solid 
‘mass of cells in the posterior region. The reader will here doubtless 
‘reeall conditions prevailing among the Annelida. It should also be 
‘mentioned here that the regular arrangement of the mesoderm just 
described ‘is soon lost, as the mesoderm-cells grow into the primary 
in 4 manner similar to that observed in other Molluscs 

(Figs. 5, 9). A large complex of mesoderm-cells, which at first 
‘remains lying at the posterior end of the body (Fig. 5) yields later 


} 





8 AMPHINEUBA. 


the chief material for the formation of various organs (circulatory, 
excretory and genital organs) 





‘THE FURTHER DEVELOPMENT OF THE LARVA AND METAMORPHOSIS. 9 


According to the figures before us, the mesoderm in Chiton shows a specially 
primitive condition, the coelomic sacs being very Iurge, and by far the grater 
part of the mesoderm formed up to this time being related to them (Fig. 4, 4 
and §). In other Molluses they are much smaller and do not assume the 
characteristic shape found in the Annelida. As rule, the mesoderm-bands 
disintegrate very early. In the remains of thése bands, if not also in the 
Seattered portions of mesoderm, a division into layers takes place which gives 
rise to the pericardial cavity (which is thus coelomic in origin). It would be 
‘of great value to ascertain the relation of the pericardium to the first (bilateral 
and bilaminar) mesoderm-rudiment in the Amphineura, especially as in some 
of them we find very primitive conditions prevailing in that the genital glands 
are immediately connected with the pericardium and the genital products thus 
pass direct into the latter, as, in the Annelida, they pass into the body- 
cavity, and are conducted thence to the exterior by the nephridia (Soleno- 
gastres). 


The central nervous system in Chiton consists of the oesophageal 





below). The Fra, 5,—Longitustinal section thi bryoni 
© Sel earalle tre ger tied tet 
f commis- ‘matt hg, viseeral ganglion ; m, mouth ; 


geet mes, en: oe, eto Yr, 
? lular sac; vell-rudiment ; 0, cil 
from the ectoderm by — [velum); mv, & ated tuft. tee 





of cell-strands, stages of which may be seen in Fig. 4. 
4-0, pn, In. 


~ 


10 AMPHINEURA, 


We have already mentioned that we thought ourselves justified in comparing 
the radiments of the cerebral ganglia with the apical plate of the Annelidan 
Trochophore (p. 6). ‘The connection of this rudiment with the lateral 
tranks of the nervous system in the larva cannot as yet be clearly established. 
Kowanrysky speaks of the two organs as discontinuous. The cell-mass at 
the posterior end of the body described as the visceral ganglion (Fig. 5, jig) is 
(as regards its ganglionic nature) of the same significance and origin. 

Actual ganglia, indeed, are not developed in the nervous system of Chifon, 
where we find the ganglionic cells distributed along the entire length of 
the longitudinal commissures, nevertheless it appears from KowaLEvsky’s: 
ontogenetic researches that these trunks are greatly swollen both anteriorly 
and posteriorly. The transverse commissures no doubt form in the same way 
as the longitudinal trunks. 


When the embryo (Chiton Polit and C. olivaceus) has attained a 
stage somewhat like the one described above, it leaves the egg and 
becomes a free-swimming larva. At this stage, a fresh differentia- 
tion makes its appearance in the form of a segmentation affecting the 
dorsal surface. Here, seven consecutive segments may be dis- 
tinguished, separated from one another by shallow grooves (Figs. 5 
and 9), These structures are indications of the future shell ; this. 


dd 


) 
, 





BA 2 cg 
Fics. 6 and 7.—Two sections through the mantle-epithelium of Chiton Poli (after 
Buomaren). A, oe papilla without spine; B-D, papillac in various stages of 
spine-formation ; #, later of the same; bs, formative cells of the spines; ¢, 
onticular covering of the body ; «p, mantle-epithelium ; m, mantle-tissue; s¢, spines, 


eventually consists of eight plates, but the eighth segment only 
appears at a later stage. 

The ectoderinal skeleton in C/iton falls under two categories: (1) 
the eight calcareous dorsal plates and (2) isolated spines and plates. 
situated anteriorly, posteriorly and laterally to the former (Fig. 8, 
at). These spines are of special interest, being a characteristic feature 
not only of Chifon but also of all other Amphineura. 


FURTHER DEVELOPMENT OF THE LARVA AND METAMORPHOSIS. 11 


According to KowauEvsky, the spines of the larval Chiton originate 
within the cells—the cells, at those points where the spines arise 
Inter, being richly vacuolated ; within these cells, the spicula are said 
to appear as rudiments and only later break through the surface of 
the body. The description of the embryonic development of the 
spines given by Kowatnvsky is not easily reconcilable with the 
observations made by other zoologists on their formation in the adult 
Chiton (e.g., those of Reinoxs, No. 14, and recently those of 
-Buosrrtcx, No. 1), and other Amphineura (Proneomenia, Tarene, 
No, 1). According to these observers, the spines arise as cuticular 
secretious in depressions of the mantle-epithelium, the whole being 
covered by « thick cuticle (Figs. 6-8, ¢). 


In the mantle-epithelium there are papilla-like swellings (Fig. 6 4) in which 
‘at @ later period the formation of spines takes place. These papillae become 
‘differentiated in the following way: broad cells appear at their bases, and to 
these smaller cells become applied laterally (Fig. 6 B), the whole structure thus 
Assuming the character of an cotodermal depression. A special basal cell (bz) 
is said to be pre-eminently the formative cell of the spine, which is first to be 
‘recognised as a small rounded structure within the papilla, It then increases 
‘in size (Fig. 6 B), presses apart the cells of the papilla and passes out of the 
latter (C and D). As the epithelial cells round the papilla continually secrete 
cuticular substance, the spine is pressed upwards. The basal (formative) cell 
from which it formerly rose is during this process drawn out like a thread 
(Pig. 7 2), the spine for a long time remaining in connection with it. The 
base of the spine, in contradistinction to the main calcareous shaft, consists of a 
chitinous substance and surrounds the latter like a cup, the whole being now 

_far removed from the smaller papilla-cells. The latter, probably, give the 

characteristic markings, The formation of the spine is completed 

y the secretion of @ peg-like terminal knob by the formative cell, from which 

“spine then detaches itself. The neighbouring cells may also secrete 

“another chitinous ring composed of several pieces round the base of the 
actnal spine. 

‘Tt is & remarkable fact that these spines somewhat resemble in their origin 
‘the setae found in the Annelida in ectodermal depressions; this has already 
Tepentedly been pointed out (Reixcke, Suwrur, v. Jnenrnc) and Harscune 
‘and Taree have again recently laid great stress on this point. We shall refer 
to it again later (Chapter xxiv.) 


While the spines show a formation sui generis, the dorsal plates 
are comparable with the shell-structures of other Molluscs. Their 
“position on the back of the larva corresponds to that of the shell- 
gland in the larvae of the Lamellibranchia and Gastropoda (c/. Figs. 
4and 5; Figs. 56, p. 135, and 57, p. 137). As in these latter forms, 

nN first appears above the epithelium (Fig. 9, c) and, beneath 

euticle, the calcareous substance is then secreted (Fig. 9, 4). 


12 AMPHINEURA, 


Each plate begins to form independently ; the calcareous secretion 
takes place first at the anterior border of each segment, and proceeds 
backwards from this point. 5 


‘The segmentation of the shell is a peculiarity of the Chitones and does not 
occur in other Molluscs. Although the impression of segmentation is given 
(Figs. 3 C, and 9), this term is not, strictly speaking, applicable here, since there 
is no corresponding segmentation of the body. The shape of the shell is perhaps 
rather due to its mode of origin. We have already seen that the spines are 
cuticular structures, and this is of special interest since, in Molluscs as 
primitive as the Solenogastres, they are the only hard structures of the integu- 





Fic, 8.—Portion of a transverse section through a (hiton (diagrammatic, chiefly after 
BrUMgicH): a, articulamentum ; ae, aesthetes; c, mantle-cuticle; ep, ectoderm 
cavesing body and mantle, forming papillae in the mantle-region : Ay foot ; ys, cornice 

asd Banh a mantle; &, gill, with the branchial artery cut through on its left 
and the branchial vai on its right, between the two lies the lateral (visceral) uerve- 
strand (m); vity ; wm, mantle; st, spines; ¢, tegmentum, with another 
thinner and Mooctalle ‘differentiated cuticular layer above it. 


ment besides the cuticle. It has already been mentioned that the spines may 
assume a plate-like shape, and if we bear in mind the development of the 
spines in such forms as very young Dondersia (of. Fig. 10 C, p. 17), it appears 
probable that the dorsal plates of the Chitones may have developed out of such 
modified spines,* either through the broadening of individual spines or through 
the fusion of several to form a single plate. In this respect Dondersia is of 
Special interest, for this form, in which actual dorsal plates do not occur, 


* The derivation of the dorsal plates of Chiton from its spines was attempted 
by Georynave (in his Grandriss der vergl, Anatomie) as early as 1878; his 
views have recently heen adopted by BLuamicu, but THinLe assumes difforent 
origins for the dorsal plates and the spines, and attempts to explain a part of 
the former (the articulamentum) as an inner integumental skeleton, 


FURTHER DEVELOPMENT OF THE LARVA AND METAMORPHOSIS. 13 


shows, in its youth, a remarkable resemblance to Chifon in the arrangement 
of its broad, leaf-like dorsal spicula. The first appearance of the shell in the 
Molluses will be discussed further in Chapter xxxiy. 

‘The dorsal plates of Chiton consist of two layers, an upper layer which is 
continued into the thick cuticle of the mantle, the so-called tegmentum, and 
‘a subjacent calcareous layer, the articulamentum (Fig. 8, / and a), In tracing 
the origin of the shell from spines, we should have to imagine the articula- 
mentum as arising from the latter, which, as can easily be explained by their 
origin, remained lying beneath the cuticle where they became expanded, The 
cuticle above the calcareous plates which have thus arisen becomes the teg- 
mentum of the shell. The retention of single modified spines or complexes of 
spines, which is determined by the segmentation of the shell into separate 
plates, would then be explicable by the manner of life of the animal, the body 
of which, at first perhaps of considerable length, was able to roll up. 


The shell of Chiton is characterised not only by its segmenta- 
tion, but by the presence within it of cellular strands. These are 
the aesthetes (Fig. 8, ae) which may be simple or branched, and are 
accordingly composed of a smaller or a larger number of long cells. 
‘These sometimes occur in the tegmentum and extend from its outer 
surface, where each is covered by a cuticular cap, to a cornice-like 
fold of the mantle at the lateral margin of the shell (Fig. 8, gs). 
These cell-strands have developed from the epithelial cells of the 
mantle, which underwent great elongation during the secretion of 
the enticle through pressure of the surrounding cells. While that 
part of the mantle to which they belong, and which secretes the 
tegmentum, undergoes marked lateral displacement during the growth 
of the shell, they, in consequence of their length, are able to retain 
their primitive connection with the surface of the shell, and yet to 
remain attached by their bases to the epithelium of the lateral 
cornice of the mantle (Fig. 8). This latter epithelium is also partly 
concerned in the secretion of calcareous shell-substance and, in this 
way, the aesthetes appear to perforate the articulamentum which has 
in reality been secreted round their bases. These structures have 
been held to be sensory organs. They can hardly be tactile organs, 
but they may perhaps serve other sensory purposes which are un- 
known to us. The eyes discovered by Moseuey (No. 11) on the 
shell of a few exotic Chitones must doubtless be regarded as further 
modification of the aesthetes. 


‘Figs. 5-9 show cloarly that the shell of Chiton is, just like that of other 
Molluscs, a cuticular structure. While the articulamentum, in consequence 
of lying immediately above the epithelium, can readily increase in thickness, 
the tegmentum, from its position, must grow chiefly at its margin. 


14 AMPHINEURA. 


The development of the shell commences even during larval life. 
But, since some Chitons leave the egg-membrane only at a very late 
stage, the free-swimming stage is in their case of comparatively short 
duration. The commencement of metamorphosis is indicated by the 
compression and final degeneration of the cells of the ciliated ring 
which from the first were distinguished from the surrounding ecto- 
derm by their size and structure (Figs. 5 and 9 t). It must be 
further mentioned that in the older larvae, two eves are said to be 





Fic, 9—Median longitedinal section through a young CR, just emerging. from 
the larval stage (after KOWALEVSET). a, rn ; ¢, cuticle of the shell, 
darkened parts indicating, according to RowaLxvskt, those. points, at w 
formation of the shell-plates is 





the 
h the 
place ; ag, cerebral ganglion ; ecpola aod 
Praleided portion of the shell mouth nc, cnteron aes messleney edule 
sac: or, sub-radular organ ; sf. spines; w, ciliated ring. 





present, which curiously enough lie, not in the actual pre-oral section, 
i+. im front of the ciliated ring, but behind it (Fig. 3 C). These 
eyes are still to be found in the young Chiten, but, whereas they 
were at first superticial in position, they are now found beneath the 
epidermis (Fig. 4 (’) and are consequently still nearer than before 
to the lateral nerve-trunk.® 


© [Peisexeen (App. Lit. on Lamellibranchia, No. IV.) regards these 
exes of the larval Chiton as homologous with the cephalic eres which have 
recently been discovered in the adult Myfilidae under the branchial filaments. 
In the larva, they are situated outside the velar area as is the case also in 
Chiton, whereas the eves of the typical Gastropods arise within the velar area.— 





THE DEVELOPMENT OF DONDERSIA. 16 


When the larva changes into the adult, the external form is modi- 
fied not only by the continuous lengthening of the posterior region 
of the body but also by the rotation of the pre-oral region towards 
the ventral surface., A comparison of Figs. 5 and 9 shows clearly 
the beginning of this process, 

A further approximation towards the shape of the adult is bronght 
about by the development of a fold growing out on either side of 
‘the body at its dorso-lateral angle, thus giving origin to the mantle. 
At the same time, the ventral surface becomes specialised by the 
growth of its cells, which multiply and give rise to the flattened foot. 
The area between the mantle and the margin of the foot becomes 
the slightly invaginated mantle-cavity (Fig. 4 C). 

Nothing, to our knowledge, is known of the origin of the gills, but, 
considering the simplicity of their form, it is very probable that they 
arise a8 papilla-like prominences on the body-surface. In the adult 
they form on each side a row of consecutive bipectinate ctenidia. 

Among the internal changes we note the formation of an ecto- 
dermal invagination (KowaLEvsky) at the posterior end of the body ; 
this is the proctodueum which gives rise to the anus and the base 
of the intestine (Fig. 9, a). In the stomodaeum, the radular sac has 
increased considerably in size, and the radula itself has already 
appeared within it. In front of the latter another ventral outgrowth 
‘of the wall of the stomodaeum has formed ; this widens later, and at 
its base a thickened cell-mass can be recognised. We here appear to 
have the so-called sub-radular organ of the adult, which has been 
aeourately described by Hatter (No. 2). A further differentiation 
of the alimentary canal is caused by a ventral swelling of the enteron, 
which is perhaps the first indication of the liver (Fig. 9). 

The further development of the larvae of Chiton has not'as yet 
become known, but it is evident that they already resemble the 
adult in various ways, apart from the incompleteness of their 
internal organisation. 


IL The Development of Dondersia. 


The development of Dondersia banyulensis * has been investigated 
‘by Pruvor. This form is allied to Proneomenia (Fig. 147, Chap. 
xxxur, Huprecur, No. 5), possessing like the latter, a vermiform 
body (40 mm. long and 1 mm. broad) capable of coiling up spirally. 


[Smmora (Zeitschr. f, wiss, Zool., Bd. ivi., 1893) has created the genus 
Beemets Pi tis species. Ee) 


a 


16 AMPHINEURA. 


The doraal and lateral parts of the body bear spicules ; on the back, 
these are inclined towards one another and form a projecting ridge 
in the doraal-median line, elsewhere (especially at the sides) the 
apines become flattened and imbricated.* A groove is found on 
the ventral surface as in many other Solenogastres (Fig. 147 B, 
Chap. xxx.) 

Dondersia lays its egy singly. They are opaque and surrounded 
by a delicate envelope which is only developed after the egg has 
passed from the pericandium into the nephridia which serve as genital 
ducts Acconting to Pruvort. the envelope is formed by the latter, 
which ne longer possess the function of excretory organs. 

The cleavage is from the first, slightly unequal ; the egg breaks up 
iwtw tee unequal blastomeres which, through division, yield three 
stwall cleavage spheres and one lanre one (77. Lamellibranchia, Fig. 
WLC. The next stage. ane af eight cells. is reached by the biparti- 
taon af the micromeres aani the unequal division of the macromere. 
No forther monomers are cut off from the macromere. which now 
Yreaks cp into tes ani then inte four macromeres, while the seven 
primsry moomeees te in fourteen and then inte twenty-eight. 
Tn thos squge. tie errno begins and the entadenm-celis dis 
spear wks ite aa foemed by the more rapéily dividing eetoderm- 
col, Thr enter: 
The TevacTaI AC 
Time. Vie sik agg. ctuated ares arsine ac the frontal pole. o., 
Tat thssteoure Pacvor. as well as round 
Tome aia: demas WEN eocizeies the whole body 














vw Sas a conical caplike shape. the aperture of 









Thy uct + 
shoot nal war 


mar he oomneres 
suhsted ting trees 63 ibe gastric la ssc. 





lam anceramr 
mit & dew spermlly 
al The ace Hertuc, cettvimg the 
THOT leg Gece anor aku Scumat of 
yey ce we ad ak atthe ant ce wiant nes ie szectim 28 amesgimi- 
yee DAEWOT cage te note ah Te imcgem. sd que vow 





aa Qomencing af iw: srs oe 
semng and long a. 
aban tng and | 














2 Ohne eremans wlnol sor onacmeme oR embiue meu umbenamd Te 
SO aoa, RO Basar Sere ster oracee we Teron Na C2) om 
Ph Oativevanaa Tre qustur mnemis wu guiiisa 
Soap the x ment deencmmerc om she Summ, 
hes NUISRA § ScARTM nt Shenae af squther 


Veen ce nastics 













THE DEVELOPMENT OF DONDERSIA. lq 


that at first it is somewhat elongate and reaches (on the dorsal side ?) 
almost to the ciliated ring, but later becomes circular (Fig. 10 A). 
The further development of the larva, as described by Provor (4 and 
B) makes his interpretation of this depression (at least in the later 
stages) appear somewhat doubtful. 

About this stage the embryo appears to become free, for the stage 
depicted im Fig. 10 A is called by Prouvor a larval stage, The 
wperture of invagination has already narrowed, and is terminal in 


The further transformation of the larva is said to take place in the 
following way, From within the invagination a button-like structure 
gradually grows out, which corresponds to the posterior end of the 
animal (Fig. 10, 8 and C), and carries at its end the remains of the 





Fro. 10.—A-0,, stages in the metamorphosis of Dondersia banyulensis ; A and B, larva 
Shertanorpons te Pver ee ae cnerr seven ie eats 
. + dp. jo pero Pe ar 


‘calcareous spicules 
blastopore. This latter must be regarded as having been previously 
displaced inwards. With the button-like terminal region a conical 
part is also gradually evaginated (2), and this is destined to yield 
the greater part of the definitive body. On this the leaf-like spicules 
‘are already appearing (2, sp). These are said to arise, as asserted for 
Chiton (jp. 11), as intracellular secretions, only breaking out of these 
cells ax they increase in size. The conical part now grows consider- 
ably, and new spicules continue to be formed ; the anterior part of 
the larva, on the contrary, degenerates rapidly, and finally appears 
only as a small collar at its anterior end. The larva is at last no 
longer able to swim about in the water, for the cilia degenerate 
together with the cells that carry them. The two posterior rows of 
cells also (those of the third section, Fig, 10, 4 and 2) are thrown off. 
S c 


be 


18 AMPHINEURA. 


This section of the body is called by Pruvor the mantle-section in the 
older larvae (B), and this name seems to be justified by its relation 
to the adult body which is in process of formation. Between the 
process of invagination just described and the formation of the adult 
body, various other formative processes take place, but these apparently 
occur within the larval body, and have so far not yet been investi- 
guted. Essential differences are to be found between the development 
of Doudersia and that of Chiton ; although, in the latter also, it is 
chiefly the part of the larval body lying behind the ciliated ring that, 
by its elongation, becomes changed into the body of the adult. The 
pre-oral part of the larva (i.e., the part lying in front of the ciliated 
ring) is here retained, as in Chiton, and yields the corresponding part 
of the adult body. It appears that, in Donderaia banyulenais, there 
are two lobe-like projections at the anterior end of the body, and that 
these are already distinct in the young animal (Fig. 10 C). The 
mouth is said to be wanting until metamorphosis commences; the 
entoderm is present in the form of a solid mass, at the sides of which 
two mesoderm-bands lie. This latter condition would agree with 
that described for Chiton (p. 7), and is interesting inasmuch as 
the mesoderm-bands in other Molluscs are not usually so distinct. 
Unfortunately, no further details are known either of the internal or 
of the external development of Dondersia. It should, however, be 
stated that seven calcareous plates are found on the back of the young 
animal which has only just undergone metamorphosis (Fig. 10 C), 
these being formed of rectangular spicules arranged one behind another. 
The resemblance of this stage to a young recently metamorphosed 
Chiton is striking, the latter also possessiug seven such plates. In 
what way this condition can be reconciled with that of the adult 
Dondersia we do not know: this cau only be made clear by the 
investigation of transition-stages. The voung animal has lateral 
spicules which are plate-like and imbricated, and which, in the adult, 
seem to be less developed. as far at least as can be judged from the 
statements as yet made on the subject. 

The form of the larva of Dondersia, like that of the Chiten, may be 
traced back to that of the Trochuphore. We have already pointed 
out various specially striking poiuts of resemblance between the 
development of Dewiersia and that of Chiten. The elongation of 
the posterior section of the body recalls here almost more than in 
Chiten the growing of the post-oral seetion of the Annelidan Trocho- 
pho into the trunk of the worn :Vol. i, Fig. 120, p. 269. This is 
specially striking if we examine the Mirna: .. Fig. 124, 






aa darva (Vol. 


= 


THE DEVELOPMENT OF DONDERSIA. 19 


p. 276), in which the posterior end of the body is at first also sur- 
rounded by the cap-like anterior part of the larva and hidden within 
it. Since the Amphineura are very primitive representatives of the 
Molluscan type, such comparisons are not unjustifiable, although the 
‘unusual length of the body in this form alone determines a greater 
ebange in the more compact larva, We shall return to this point. 
again in diseussing the relationships of the Mollusea (Chap. xxxiv.) 


[Pavvor Pre. TL.) bas neg sider @ preliminary account of the 





stages ination- 

identical in the two forms, Similarly, Proneomenia 

Ac a divided into shses its and provided with a 
tong. flagellum. Jay tl invagination (? archen- 
Ree sceasiot corsapond 2 definitive entoderm, but gives rise to all the 
‘issues of the trunk. By the tangential division of its cells, it gives rise to a 
entodermic upon a single layer of cells; the latter in- 
oreases by the radial division of its cells and infol forming three 


; of these the middle one, which remains open, becomes the 
while the two lateral ones close and are transformed 


incontact with the proctodaeum behind. The next important change 

eee a of three ventral invaginations of the larval ectoderm, just 
circle of cilia on the middle segment; the median of these 
eeamnsirs, the stomodaeum, is merely transitory, while the two 
ones sre concerned in the formation of the ectoderm and mesoderm 
vRaleee ‘These two unite, forming a transverse band capping the anterior 
e the entodermic mass and prolonged posteriorly at two points to meet 
trunk ; this portion appears to form the muscles, 

more dorsal elements of the invagination form the cerebral ganglia. 


of the plate seem to take no in the formation of the 
Cepeda of the head ae to form entirely from 


invaginations, while that of the trunk develops from the 
¥ pos invagination. The latter is now completely evaginated, 
the provisional imbric 


Proneomenia is developed under cover of of kg ar ectoderm which 
aw 


+ the moment of meta- 










is perfectly distinct and arises quite independently of 


__A very striking resemblance, possibly of great significance, is to be noted 
etween ee and certain Lamellibranchia (Drew, 
ia, No. IL). In Foldia, we find the young, Molluse 


a pair of invaginations at the antero-ventral 








20 AMPHINEURA, 


end of the larva. As in the Solenogastres, the larval locomotory ectoderm is 
thrown off during Pheciad Fone ‘The resemblance in the early cleavage 
has been already pointed ont, These yery striking resemblances, suggesting 
as they do a connection between the Solenogastres and the Lamellibranchia, 
require further and more complete investigation.—Ep.] 


LITERATURE. 


rar 


. Buvaricn, J, Das Integument der Chiton. (With a pre- 
face by Hatschek, treating of the position of the Chitones 
or Amphineura). Zeitschr. f. wiss. Zool., Bd. Iii, 1891, A 
critical account of this treatise, with remarks on the integu- 
ment as well as on the systematic position of the Chitones, 
by Thiele. Biol, Centralbl. Bad. ii. 1891. 

2. Haier, Bena. Die Organisation der Chitonen der Adria. 
Theil. i. u. ii. Arb. Zool. Inst. Univ. Wien. Bad. iv. a. v. 
1882 u, 1884. 

3, Hansen, G. A. Neomenia, Proneomenia und Chiitoderma, 

Bergens Museums Aars beretning for 1888, Bergen 1889. 

Husrecat, A. A. W. (1) Proneomenia Sluiteri. Nederland. 

Archiv. Zool. Suppl. 1., 1881. (2) A contribution to the 
morphology of Amphineura. Quart. Journ. Micro, Sci. Vol, 
xxii. 1882. 

5. Huprecat, A.A. W. Dondersia festiva. Donders-Feestundel 
Nedert, Tijdschr. 1888, 

6, Kowanevsry, A, Ueber die Entwicklung der Chitonen, Zool. 
Anz, Jabrg. ii, 1879. 

7. Kowanevsky, A. Weitere Studien iiber die Entwicklung 
der Chitonen. Zool. Anz. Jabrg.v. 1882. 

8, Kowanevsky, A. Embryogénie du Chiton polli ayee quel- 
ques remarques sur le développement des autres Chitons. 
Ann. Mus. Hist. Nat. Marseille Zool. Tom. i. 1883. 

9. Kowanevsty, A., et Manton, A. F, Contributions a Ihistoire 
des Solénogastres. Ann. Mus, Hist. Nat. Marsville. Zool. 
Tom. iii, 1887. 

10. Lovéx, 5. Ueber die Entwicklung von Chiton. Archiv. f. 
Naturgeschichte, Jahrg. xxii. 1856. Oefversigt af Konyl. 
vetenskaps. Acad. Forhand. 1885. Translated in Ann. Mag, 
Nat, Hist. Vol. xvii. 1856. 

11. Moseney, H. N. On the presence of eyes in the shells of 

certain Chitonidae and of the structure of these organs. 

Quart. Journ. Micro. Sci. Vol. xxv. 1885. 


> 


13. 


14. 


It. 


LITERATURE. 21 


. Pruvot, G. Sur quelques Néoméniées nouvelles de la Médi- 


terranée. Archiv, Zoul expér. (2). Tom. viii., p. 22 (Notes and 
review). 1890. 3 

Pruvor, G. Sur le développement d’un Solénogastre. Comp. 
rend. Acad, Sci. Puris. Tom. cxi., p. 689. 1890. 

Reincxe, J. Beitriige zur Bildungsgeschichte der Stacheln, ete., 
im Mantelrande der Chitonen. Zeiferhr. f. wiss. Zool. Bd. 
xviii. 1868. 


APPENDIX TU LITERATURE ON AMPHINEURA. 


- Mercatr, M. M. Contributions to the Embryology of Chiton. 


Johns Hopkins Univ, Studies. Vol. v. 1893. 


. Pauvor, G. Sur l'embryogenie d’une Proneomenia. Comp. 


rend. Acad. Sei. Parix, Tom. cxiv. 1892. 
Smunots, H. In Bronn'x Klass. u. Ord. d. Thierreichs. 1892- 
94. Anatomy, Ontogeny, Phylogeny and Literature. 


CHAPTER XXX. 


LAMELLIBRANCHIA.* 


Systematic :— 

I. Prorosrancalia, gills bipectinate, branchial processes plate-like 
and not reflected, foot with creeping sole. 

Nucula, Yoldia, Solenomya. 

Il. Fivrrancai, gill-filaments distinct and reflected; solid 
interlamellar junctions, cilia forming interfilamentar junctions. 

_ Arca, Mytilus, Modiolaria, etc. 

III. PsEUDOLAMELLIBRANCHIA, the gill-filaments reflected and 
loosely connected by ciliated discs or vascular junctions, interlamellar 
junctions vascular; gills folded and filaments at base of grooves 
modified. 

Pecten, Ostrea, ete. 


IV. EvLAMELLIBRANCHLA, gill-filaments of plate-like gill con- 
nected by vascular interfilamentar and interlamellar junctions, re- 
flected. 

Cardium, Teredo, Cyclax, Unio, Venus and most Lamellibranchs. 


1. Oviposition and Oare of the Brood. 


The eggs of the Lamellibranchia may be discharged into the 
water and there fertilised (Modiolaria and Mytilus edulis, LOVEN, 
Barrois, Winson ; Ostrea riryiniana, Brooks, No. 16; and pro- 


* We have, chiefly for practical reasons, placed the Lamellibranchis be- 
fore the Gastropods, because their larval forms appear to be more primitive, 
and their further development is usually more simple. The relation of the 
Lamellibranchia to the other divisions of the Mollusce will be discussed 
later (Chap. xxx.). In the classification of the Lamellibranchs, we have 
followed PztseNeen’s recent works, but it should be mentioned that GROBBEN 
has quite recently adopted a new stand-point in classifying the Lamelli- 
branchia, and hes expressed himself as opposed to the use of the gills as the 
determining feature in their classification (Beitrige zur Kenntniss des Baues 
von Cuspidaria (Neaera) cuspidata, ete. Arb, Zool. Inst. Wien. Bd.x. 1892). 





24 LAMELLIBBANCHIA. 


2 Cleavage and Formation of the Germ-layers. 


Tn those forms in which the cleavage of the egg has been carefully 
investigated (Caio, Anodonta, Cartiam, Cyclas, 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 (Osreu 
edulix, Perten, Mytilus edulis, Méprus, Horst. Fcuartos. Barros 
and Witsox). 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 
Teredu, a corres- 
ponding differen- 
tiation is indicated 
eveu before cleav- 
age by the different 
constitution of the 
protoplasm at the 


Pro. 11.—.-F, diacrams illustrating the cleavage of the  Veeetative and at 
ewe in the Lamellibranchia The lines connecting the the animal poles 
nackei of two cells indicate that the pair has arisen from 
the division of one vel. of the ey. 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 
toa new micromere (CL The new cell then divides, and the process 
of the abstriction of a micromere from the lange cleavage-sphere is 
repeated (D) again and again. the lange cell viekling micromeres 
which then divide (£1. Finally, the micromeres. seen from the 
surface. resemble a cap placed upeo the remaius of the macromere, 
which at last also divides into two similar cells (macromeres) 

(Fig. 11 Pe 





eh is common) ¥ hed thas che entaden arses soleir from the macromeres: 
ema and thai. ai the foar- 





— 


‘OLEAVAGE 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 the one last 
formed has divided; but this does not indicate any essential deviation from 
the course above desoribed. This is also the case in the apparently divergent 
method of cleavage seen in Modiolaria and Ostrea virginiana, as was recognised 
jong ago by Lovéx, and was again pointed out by Zrecuer. In the two 
Lamellibranchs just named, during the first stages of cleavage, a very 
temarkmble process tukes 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; ata later stage, this protuberance is withdrawn into the macromere, 
‘On account of this process, which is probably determined by the relative 
‘Aistribution of the protoplasm and the yolk in the egg, the first stages of 
Mediolavia and Ostrea virginiana difier in appearance from the diagrams given 
wboye; they may, however, be referred to these, as is evident after the de- 
generation of the false blastomere. 

‘Ray Lasnesrer long ago described the cleavage of the egg in Pisidinm 
pusitlam, « form nearly related to Cyclas, into four spheres of equal size, from 
each of which a smaller cell became constricted (No. 29). Tf this is really the 
ease, this method of cleavage would not correspond to that known to cour in 
other Lamellibranchs, but would rather closely resemble the cleavage of the 
Gastropod egg (p. 108). This condition of the egg of Pisidiwm is however so 
peculiar when compared with that of other Lamellibranch eggs that it requires 
to be further 4 


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 egys is very similar, nevertheless certain differences of 
‘Internal constitution are very soon evident. In one case, a cavity, 
ee nn. soon appears between the micromeres and the 
macromeres. [In Cyelos, at the 13-celled stage, Sravrracumn.] 
“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 Cyelas, Pixidium and the Unionitae, the wall of which is not 
uniform in thickness. In other cases, the cleavage-cavity is not so 


| Tange, especially at first (Mytitus),* while in Teredo, as well as in 







to be precisely similar to that described above, but neither 
the second eee ep the salen from a vegetative 
asserted, this separati Litre, only oceurri 
i ‘and thus the entoderm arises both from the epee me 
‘Lintne suggests that the peers cleavage in Unio is due 
‘the rudiment of the immense shell-gland is to be found in 
‘and he further accounts for the minute size of the entomeres 
remains undeveloped until late stage.—Eb.] 
eae mists on Mytilus (No. 1) are only known to 
in the Jahrsberichte, but, taken together with the 
os (No. 59) are probably to be understood in the way 















26 LAMELLIBRANCHIA. 


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 
thus produced (Figs. 
12 and 14 A), such as, 
according to Lov#n, 
is found in Modiolaria 
and Cardium. In the 


last stages of cleav- 

Frc. 12—1-C, embryos of Tered» during the for- i 
mation of the germlarers after Harscutx:, The 98% the two primary 
entoderm-celisare lightly dotted. whilethemesoderm- germ-layers are 


cells are more darkly market; the unsbaded partis Sieeady 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 inragination (fresh-water Lamellibranchs, 
Ray Laswesrer, Zreccer, Livuie). In Cyclas, for instance, 
a shallow depres- 
sion forms in the: 
blastula (Fig. 13 
A) the vegeta- 
tive pole of which 
is no longer to be 
distinguished by 
the larger size of 
its cells, and. by a 
farther invagina- 
tien of the cells at 
this point. a small 
arehenteron is 
formed (Fig. 13 
Bu This is also 
the case in Pis- 
Erg peters cre pp pA 
iastopore ater ZIBGLER. NW. tlassapore: topore takes the 
Pow miewnferm : es, rudiment of the S00 Go of a slit lying 
in the median line, 

and in this way the embryo early assumes a bilateral symmetry. 
The blastopore won closes, « that the arvhenteron kees its 
connection with the exterior and lies as a closed svc in cuntact 











OLEAVAGE AND FORMATION OF THE GERM-LAYERS. a7 


with the ectoderm (Fig. 13 C), It is not known whether the 
loses from behind forward, so that its relations to 
the mouth and anus are still uncertain. [In Unio (Lannie) the 
‘blastopore is said to close by the forward growth of its posterior 
lip, the ventral plate.) 
Tp the Unionidae also there is an invagination-gastrula, but the 
arehenteron is here still smaller than in Cyclas (Gorrrs, Fig. 23 
ALC, #, p. 51). ¥ 


‘The presence of an invagination-gastrula in the Unionidae was first ob- 
served by Rape in 1876 (No, 43), and Scurernouz in 1878 (Nos. 47-49), and 
the gastrala 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 Gorrre'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. 28 4-C, sd and ¢). The subject will be discussed more 
in detail in connection with the further development of the Unionidae (p. 49). 
[Lanxzm (No. II.) has shown definitely that the large invagination observed 
‘by Rast and Scumnnoiz was the temporarily inturned shell-gland, the true 
‘erchonteron being very small.) 


Between the extreme cases of epibolic and embolic gastrulation, 
such as are offered by Cyclas on the one band and Teredo on the 
other, Ostrex 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). Hors 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 ut the vegetative pole, a depression arises in this 
region. When the macromeres now divide, a stage arises, with an 
almost triangular blastopore, which cannot be distinguished from an 
ecctns cin a. 14.8). 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 ©, «!). ‘To this and the further 
transformation of the embryo (C-£) we shall return later. 


Conditions similar to those in the Oyster are found also in the Lamelli- 


Jbranchs examined by Loviix (Modiolaria and Cardium), in which the abund- 
determines the varly ciroumerescence of the entoderm-elements, 


i a 


28 LAMELLIBRANCHIA. 


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 81). 

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 Tvredo, there are two large cells 
which, according to HaTscHEs, are to be traced back to the macro- 


@ & & 








Fro, 11. —A-E, various stages of development of the Oyster (a of Ostrea virginiana 
after BRooxs, B-£, of edulis after Honst). a, anus; bl, blastopore ; a, 
mouth ; ma, stomach ; mes, mesoderm-cells ; rk, polar bodies ; s, anal (in D, ux 
paired embryonic shell-rudiment) ; ad, shell-gland ; «v, the anterior adductor muscle; 
4o, pre-oral ciliated ring. 





meres, lying symmetrically to the median plane at the posterior 
edge of the blastopore (Fig. 12 A and #). They are soon grown 
round by ectoderm and are thus drawn into the interior of the 
embryo (Fig. 12 €). In Ostrea edulis, corresponding cells are 
found in a similar position (Fig 14 C), and conditions similar on the 
whole are also found in Cyclas.* These two cells have been assumed 
to be primitive mesuderm-cells [mesodermal teloblasts] homologous to 


*[In Cyclas, after the macromere has given origin to the last miecromere 
(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 smal] remnants of the macromeres form 
the entoderm (Sravrracuzr, No, VI),—Ep.] 


CLEAVAGE AND FORMATION OF THE GERM-LAYERS. 29 


Dieses the! Annelida, from which by repeated ‘division the meeoderm- 
bands 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 Rann and 
Harsenex. Honsr has described similar conditions in Ostrea, and ZimoLen’s 
account of Cyclas also, on the whole, agrees with the above. The latter 
author, however, does not exclude the idea of o further participation of the 
ectoderm in yielding the mesoderm-elements, and Ray LaNgesren also was 
formerly in favour of the partial derivation of the mesoderm from the ecto- 
derm {Pisidiwm). There was therefore a general inclination not to derive the 
whole of the mesoderm in the Lamellibranchia from the primitive mesoderm- 
cells. 

Unio, a form in which the mesoderm and the germ-layers in general were 
first demonstrated by Rast, although indeed not very accurately (c/, pp. 
7 and 50), shows most markedly the method of formation of the primitive 
tmesoderm-cells [mesodermal teloblasts] and the mesoderm-bands, But since 
the entodermal nature of the large invagination in the Unionidae must be 
considered as refuted, these conditions also cannot be regarded as sufficiently 
established. Rar 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 
tothe 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 Rant within the young embryo is confirmed by the later descriptions 
of Scurensonz (No. 49) and Gorrre (No. 15) (Fig. 28 4, p. 51). According 
to Gorrre's figures, these might also lie near the blastopore, since the latter 
is apparently not far removed from the shell-invagination which Rast mis- 
took forthe archenteron (Fig. 23 4). The mesoderm-bands in the Lamelli- 
branchis 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 . There are in addition certain mesoblastic cells (the larval 
mesoblast of Liztze) situated anteriorly to the archenteron, which have the 
—— and possibly form the larval adductor muscle and 


Summary. The differentiation of the germ-layers in the Lamelli- 
‘branchia takes place very early. Even during cleavage the two 
primary Jayers can be clearly distinguished, and the rudiment of 
the middle germ-layer can also be recognised very early (Figs. 
1214), After the gastrula-stage is reached, the mesoderm is found 
"tn the form of more or less massive accumulations of cells (mesoderm- 


, bands), apparently proceeding from the posterior pole, between the 


“tetoderm and the entoderm. The bilateral symmetry of the germ 
‘ 


30 LAMELLIBRANCHIA. 


ourly finds expression in the rudiment of the mesoderm and in the 
position of the blastopore. 


8. Development and Structure of the Trochophore Larva. 


There ix, in the dovelopment of the Lamellibranchia, a stage 
which more or less closely resembles the 7'rochophore larva of the 
Annolida, and which hus therefore received the same name (Ray 
Lanxestser, HaTscuek). This stage is most marked, as we should 
naturally expect, when it is represented by a free-swimming larva, 
much ax ig found among the marine Lamellibranchs (Teredo, Car- 
dium, Mytilus, Ostrea, ete.) but can be clearly recognised also in 
other forma (Cyelas, Pisidinm). In the Unionidae, the Trochophore 
tayo hax undergone much greater modification. Thus among the 
marine Lanellibranchs we find, as a rule, that the primitive larval 
form has been retained in a less specialised condition than among the 
fresh-water forma, and this affords a further confirmation of a pheno- 
menon which is very wide-spread in the animal kingdom. One fresh- 
water Lamellibranch, however, Dreissensin polymorpha (evidently in 
consequence of its late transference to fresh water) exhibits a larva 
agreoing exactly with those of the marine Lamellibranchia (Kor- 
woment, No 27, BLocumans, No. 3, Wentsgp, No. 58). 

‘Vhe structure and development of the Trochuphore larva have been 
boat investigated by Hatscnen in Teredo ; in addition, Brooxs and 
Hows have published observations upon the larva of the Oyster, 
aud Loves upon those of various other Lamellibranchs (Modiolaria, 
Cwntinn, Montacata). The TrochopAure stage of the fresh-water 
Lameltibranehs has been carefully investigated in Cycluz by ZUBGLER. 
We shall here for the mest part follow HatscHEx’s account of the 
larva of Tero, since this form, of all these as yet known, most 
clearly exhibits the Trochephoran condition. The larva of Oxrea 
aiscis which, with regant tw the furmation of the alimentary canal, 
whows (aceunting to Horst) a still simpler conditinn. agrees very 
eloeely with Tee te 


A. The Trochophore stage as a free-swimming larva. 


We have stremiy on. 25) dewnbed a few stages iz the development 
wo fest Son whieh am ett gastrula ws formed (Fiz. 12 4-c) 
Wurther chars barn by the overgrowsh of the meadern-veills bring 
at the aise of the Nastomare by the ectaiers: . tie Samer thas 
eerre encet in the ember, the Nastonwe cies im con 











‘THE TROCHOPHORE STAGE AS A FREE-SWIMMING LARVA. 31 


‘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 side seems to take place in the neighbourhood of the future 
mouth. This latter arises at a somewhat later stage in the form of 
ain ectodermal invagination (Fig. 15 A). A comparison of this stage 
with those that lead to the Trockuphore shows us that the longitu- 





rior 

by an invagination of pyc, 15.—4-C, embryos and Inrva of Teredo (after 

the ectoderm, the HATSCHEK). began entoderm-cells are lightly the 
a cells dark ; 


mesoderm 
ce etaatoe af a x nell la Meee 
mi m, mou! 
‘dlastopore thus pers ell Bishan 


stomodaecum 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 4-D). In Teredo, on the contrary, the two large entoderm-cells 
are retained for a very long time, only few smaller entoderm-cells 

abstricted from them (Fig 15 2). The development 
of the enteric cavity and its close connection with the stomodaeal 
Wwyagination thus occur later (Fig, 15 €).* Consequently, the in- 
‘testine of Teredo can only become capable of functioning at a much 


* The statement of Buoons that, in the American Oyster, the blastopore 
‘and the mouth and anus appear as new structures in no way connected 
ft, cannot be reconciled with the account given by Horst, We should 
‘@condition such as is found in the fresh-water Lamellibranchia 

| a condition would have to be regarded as a specialised one, and 

allel expect to find it in the free-swimming larvae of 


32 LAMELLIBEANCHIA. 


later stage than that of Oxfrea. The proctodaeum also seems to 
develop earlier in the latter. In 7-redo, according to HarscHex, 
the terminal portion of the intestine arises as an ectodermal invagina- 
tion ut the posterior ent of the body (proctodaeum), which afterwards 
becomes connected with the enteron (Fig. 15 C, «). 

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 somewhar 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. pp 265, ete. 

During this alteratien in the shape of the embryo. the ciliation 
characteristic of the Trwhopdore also appears, two rows of cells lying 
in froat of the mouth and encircling the cephalic area becoming 
covered with cilia (Fig. 15 4. The preoral ciliated ring consisting 
o€ a double row of cells thus aries. but, in the following ontogenetic 
stages of To~ia, this & the less distinet. as the whole body becomes 
covered with cilia, overs of which are ket again later. Then. only 
the biverial preoral ciliated ring persists, while behind the moath 
are seen the first inicatinns of a peet-oral ciated img. These are 
gradually continued towands the dorsal shie until the chowed post-oral 
universal ciliated rims  predaed Fix. IS ©. Between the two 
Yims. a wee of more delete cilia is retaimad: chis i= called by 
Hiarsommx the adural ciliated sme. Rebind the anus. ale a small 
ciisted area umd. A tuft of rene Ga of a single thick cillium, 
dounsi =m cuany Lamelitranch “arvae xz the centre of the cephalic area, 
Muaces the Skeness to the Anoeldan Fewiced 7. alreniy produced 
ay the fem cf Dady ani dembote of the cia cil more striking 

Fir is. 

Ware the nets clan mor sad the aioe wee Do doubt 











2 thas fameman it alwars found 
Preserves errae. iz which the 
Sate cay Saremerate. This important 
TAY RV ‘ 





Jew) mmr ami tae 
ermetorr cmc sct&ss = 
Tle agrerur cart -€ he Sy aera 











34 LAMELLIBRANCHIA. 


larvae of the last-named form are met with swimming freely on the surface of 
the water before a:taining the Troctupduwr stage as well as at that stage. 

Before indicating further points of resemblance between the 
Lamellibranch larvae and the Annelidan Trovhuphore connected speci- 
ally with the internal organisation. we most first draw attention to 
a character, not hitherto considered. which distinguishes these larvae 
at once from all other (non-Mollasean! larvae. This is the so-called 
shell-Nawi. At a somewhat early peried in (#¢ra, as early as the 
wastrulaetage (Fig. 14 8), in Tesi. rather later, a part of the 
ectoderm, which is smewhat thickened by the lengthening of its 
cells, forms a trough-like depression on the dorsal surface near the 
posterior pole (Fig. 15 8). This depression. which represents the 
ridiment of the shell-gland. s»a deepens considerably. so that it 
appears like a blind tube (Fixx 14 4. and 22. p. 50) It has a 

vlandular chanecter, inasmuch as its cells show the longitudinal 
striatinn characteristic of many glandular cells: it son also begins 
to secrete a substance which can be seen as a thin integument over 
the external aperture ami the margin of the shell-gland (Figs 14 C, 
amd 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 coure of development the invagination of the 
shell-gland atten: out again. first becoming redaced tw a shallow 
ciepression eovered by the rudiment of the shell (Figs. 14 D, and 23), 
waned later ppearing alteether. The shell at the same time in- 
e. am pew. Uke a siddle, covers a part of the donal 
réaces Firs 130. 14 2 ami 23. C1. By the extension 























ze-tmangin of the adult shell : it is indi- 
by ht line on the back of the 
the uiethead of of the detinitive shell in 
tained by the shell in 









The ianse size 
Ling larva is to be seen 
srorect: teyoud the body. a condition only rep- 
muatinn of the right ami left mantle-folds 
‘lace. These folds are fwmed as Lateral out- 
‘mal cells being in 
he face of the outgrowth 
<i-shaped veutral nrx~a of the larva by a 
sleet nure—the mantl-vavity (HaTScHEK’. The reader should 








= 


THE TROCHOPHORE STAGE AS A FREE-SWIMMING LanvA. 85 


compare this with the formation of the mantle in Cyclay at a later 
stage (p. 43). 

‘The shell, in the condition just described, is already a real pro- 
tection to the larva, for, on account of the contractility of the velum, 
the whole body can be withdrawn between the two valves. The 
shell increases in size as the larva grows ; in Dyeissensia concentric 
bands of growth can soon be recognised, their number increasing 
more and more with age. The growth of the larva of Dretssensia, 
and also that of the larvae 


A 2 





P16, 17, —1-C, ne Dlactyd Dreissensia polymorpha i 
various : af, surface sree thy abit 5 


B, wntero-ventral + © (older Jarva), seen 
from the side (original) ; m, oral region ; 4, shell. 
‘The velum, in Aa strongly pig. 


mented. In C, retractors are faintly seen running 
twek from the velum. 











tween the mouth and the anus, and the gill-rudi- 
ch are first indicated by papilla- or ridge-like outgrowths 
mm : but these changes will be dealt with later when 
transformation of the larva into the adult. Before 
subject, we have to describe an important char- 

lore larva itself, which marks still more strongly 
the Annelidan Trochophore. 
































ne 118 B, p.265). Fine hairs are attached 
the centre of each is a strongly refractive round 


es embedded in them, which Lovén observed in a 


larvae (¢.g., Mytilus), apparently arise at a Tutor 


cently discovered that these eyes are retained 
Arvicila, where they are situated at the base 
filament of the internal branchial lamella; 

in. They are not homologous with the larval 

. occur on the velum, and are therefore true 
sibly homologous with the larval eyes of Chiton 




























have remained only slightly differentiated, 

retained in this primitive condition for a very. 
it is evident that they contain, stored up 
nutritive material, which is gradually used up in t 
larval body ; the presence of this food renders an 
of the intestine, such as takes place in Oxtrea, unmec 
14). At first the intestine makes but a simple b 
resemble in shape that of the Anuelidan 






rudiment and its derivatives, which are, nevertheless, 
ance. According to Rann and Harscres, the symmeti 
mesoderm-bands run forward from the two primitive 1 
{mesodermal teloblasts} which at first lie near the 
afterwards (ventrally) at the sides of the anus. The 
these mesoderm-bands are, as in the Annelida, 

of the primitive mesoderm-cells, which long retain 
character of the blastomeres (Fig. 15). ‘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 leagthen, 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. 
‘Thon 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 
seom to serve chiefly for closing the shell (Harsomes), but this fune- 
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 carly in the larvae of many Lamellibranchs 
(Fig. 16, sm), 





“(According to Lrutre (No. LIL), this larval mesoderm has in Unie an 
quite distinct from the mesodermal teloblasts which form the mesoderm- 
bands. ‘The larval has more the character of a 
is situated in front of the whereas the mesodermal are 
situated behind the blasto) c| former ves ccicha 60 the Se eae 
9 and adult m is well seen in Figs. 








i 






‘The fact that this degeneration has taken 
cated form of the alimentary canal. In Cyclas and 
the Unionidae, the blastopore closes; the ectoderm then | 





Fig. eles Cyclas cornen nt the Trock- the Trochophore, 


(combined from E, ZrecuEn's Seuss) 
lion; d, enteron 








a 


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. small ciliated area extending above and below the mouth 
and at its sides. Zreater has homologised this ciliated area with the ad- 
oral ciliated zone of the Trochophore, and believes that the part of the yelam 
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 « corresponding reduction of the larval muscles. 


It has alreudy been mentioned that the larval kidney is found in 
Cyelas. Of the other Trochophoral organs, ZIEGLER was only able 


* The statements that the blastopore becomes directly transformed into 
anus (as in Pisidiwm, Ray Laxxester) require confirmation, since the more 

Aire Lamellibranchia show an entirely different relationship = 
seated account of the processes in Cyclas, emerges 
anus arises at the Lsancies end of the ditlike blastopore which has a 
ee A proctodseal invagination seems in any case to be absent in 





i 





42 LAMELIDIBRANCHTA. 


48 a hollow outgrowth of the ectoderm into which a great mass of 
mesoderm-cells find their way. 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 Cyclus), or else at the same spot is 
# single row of papillae (Mytilus, Dreiasensia 
and the Unionidae, and, acvording to Jacksox, 
in Ostrer). 

In those stages of Cyclas and Pistdiuin 
which must be regarded as the equivalents 
of the Troehophore, the foot has already 
uttained a considerable size. It oceupies 
the whole of the ventral surface between 
the mouth and anus in the form of a massive 
projection of the ectoderm (Fig. 19 f). 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 

pa — Oiler tere. of ig. 21), 

Drveissensict inonyphé 

(original). In the free-swimming larva, the foot is 

a f already of considerable size. Althongh 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 appears to make vermiform 
movements and to function as a tactile organ (Fig. 20). 








At this stage, therefore, the larva, besides its provisional lecomotory organ, 
the velum, also possesses the locomotory organ of the adult Lamellibranch, 
Farther, 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 yelum, 
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 Trockophore stage as well as Inter, 
is covered with fine cilia. At the posterior upper boundary of this 
ciliated area, in Cyclas,  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. 





| 


44 LAMELLIBRANCHIA, 


an outgrowth of the ectoderm arises (Fig, 19 mr), forming a fold 
which extends anteriorly and posteriorly over the body (Fig. 21 4, 
mr; 

vids Teredo (p. 34), the mantle extends with the shell from the 
dorsal to the ventral side, The outer lamella of the mantle is closely 
applied to the shell, while its inner lamella bounds the 
which has arisen with the growth of the mantle. per pc 
the mantle also increases more and more in size, and th two now 
enclose a large part of the body (Figs. 21 B, and 31, p, 

The siphons, where found, appear to develop at a very late stage. 
They are formed from the edges of the mantle, which become closely 
applied and fuse, the parts destined to form siphons then growing 
out into long, tabular structures. 


and B, pes op. co weet (after bp ae to = a, anus; by, byssus ; 


ment ei, mined ak m+é, stomach and liver ; wr, 
Faust of Tne vighh calcarnoue whet-ratee sad cate pe 1; wel, stomodaennt moma wi, 
velar area. 





Within the mantle-cavity another ectodermal fold appears on either 
side of the body, developing from behind forward like the mantle 
itself. This paired fold is the first rudiment of the gills (Pig. 21 
B, k), which arise in the same way in Teredo. The branchial fold 
is covered by fine cilia. Thus, in Cyelas and Teredo, the earliest gill- 
rudiment exhibits the form of a plate, and at first shows no indication 
of the slits and bars so characteristic of the adult. The further 
differentiation of the gills, resulting in the formation of the gill-slits 
and filaments, takes place from the anterior end of the fold. Starting 
from the lower free edge, a series of vertically placed parallel grooves 




















Zetete 








‘the latter, a gill-plate first appears, but 
extend to the ventral edge of the fold, 
distinct gill-filaments are not formed, but 
with slits, the gill-plate retaining its 
ow the slits 

the external form of the Lamellibranchia we 
the labial palps (oral lobes). "These, in the 
upper (anterior) and « lower (posterior) 
to ZieGLER, they arise in the following 
surrounding the mouth becomes divided 
ver portion by a groove which runs out on either 
of the mouth. ‘The first of these must be reck- 
d the second as the lower lip. These two areas 
re rise to the labial palps. At the time when 
over the upper lip, a median depression ap- 
4 similar depression is to be found in the 
s being thus divided into two lateral portions. 
out as folds, and develop into the labial 

























s the two halves of the upper and lower 
aboye 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 
Lovim that the velum of the larva may pass over directly into the adult 
palps. In the double nature of this organ Lovin finds agreement with the 
double velum of the Gastropoda, a resemblance which is strengthened by 
Yxecuen'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 Trocho- 
plore, The ciliated area of Cyclas, however, as we haye just shown, seems 
rather to correspond to the ad-oral ciliation of the Iarva (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 
({Tarere, No. 55). An exact knowledge of the fate of the entire velum, fe. 
of the pre-oral ciliated portion of the body ina 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 4), 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 Pisidium 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 Ostrec, 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 Tvochuphore larva already possesses an 








Didairigislab aed atdacKon. to the\tks valgen 
‘This adductor in Ostrea lies dorsally to the alimentary 
(ANS mcr empscaliec sence ea 







es ops gee eae 
be homologised with this latter, The adductor of 
er therefore cannot be the same as that of the adult. 

h has been. emphasised by several investigators 
ete.) by the study of the later 
panel 


which ouly one adductor musele (the anterior) is 
Perea eee etn s better developed than the 














via Pion, In the Unionidae also the anterior 
first, as, indeed, is the case in nearly all 


Retr tigd fe this reap 
we ie ntrary, according to Zimanun, the posterior adductor 
A sok e anterior, but it has already been pointed out that in the. 
F di the anterior appears first. Lacazn-Durarens (No. 28) 

rior adductor develops first in Mytilus, but this 
larval stages examined by this author as well as by 
0 old, According to Wiisow (No. 59), in the young 
adductor develops earlier than the posterior, and 
the nearly related form Preissensia (Korsennur, 






















adductor has appeared in Osxtrea, a posterior 
ly to the intestine arises in the same manner 
chs mentioned above (JACKSON). Ostrea, und 
Monomyaria as well, possess for » time two 
and a posterior) of almost equal strength, and 
the Dimyaria. era ee eetesy of these vee 


och larvac do for time possess only one ad- 
as eS 2 roe aly ome ot 
‘permanent condition of the Monomyaria as having 
of development in this direction, i., through the 
a second muscle. The Dimyaria hence do not pass 
an stage in the proper sense of the term, but the 














48 LAMELLIBRANCHTA. 


Monomyaria probably invariably possess in youth the two typical adductors 
of the Dimyarian, 

(The fact that the anterior adductor almost invariably 
‘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- 
Dranchs found in the Cambrian belong to the Nuculidae and Areidae, 
which are typically Dimyarian,] 

The young of Osfrea 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 museles, 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 (Huxney, Ryper). 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 
almost 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 Osfyea, the shell 
becomes permanently attached at the close of the free-swimming 
Trochophove stage; the foot is therefore unnecessary before fixation 


Dates in relation to Wee el the true transverse axis of the 
animal. ‘is rotation is possibly due in large measure to the degeneration 
‘of the anterior adductor muscle and of the velum.—Ep,) 





of the Unionidae. 
Unionidae differs 40 essentially from that 






attached to the gills or to the integument: 
in the Unionidae, superadded to the normal 
Ib din the marine Lamellibranchs, an 








jal form which cannot be compared with 
and which possesses characters not present 


by Fontartoy, from 
‘o. 14), we ir that 
jbranchs up to the later 
adult was not observed. 






' 


a 


50 LAMELLIBRANCHIA—UNIONIDAE. : 


The ontogeny of the Unionidae bas been studied by a number of 
zoologists. Frewantnc, Rast, Gorrre and ScureraoLz have in- 
vestigated their embryonic development, while the later stages of 
their development, which were examined by Foren (No. 13), Layne 
(No, 32), Braun (Nos. 4 and 5), Barrour, F. Soumupr (No. 50) 
and others, have recently been reinvestigated by Scniernonz and 
Gorrrr. 

[Still more recently, Laure (No. 111.) has reinvestigated the entire 


course of development in Unio complanata, paying special attention, 
however, to the cell-lineage.] 


A. Development of the Early Stage. 


It has already been mentioned that the Unionidae show an in- 
yagination-gastrula (p, 27, etc.) and that, before the latter develops, 
large mesoderm-cells bud off from the wall of the blastula and enter 
the cleavage-cavity. 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 ou the blastula 
and deepens more and 
more (Fig, 22, ad). 
This depression is 
formed by large cells 
which are granular 

o and therefore appear 

Fio, 22—Embryo of Anodonta in the vitelline mem- ark, and ite whole 
brane (after Scurenno1z) ; ase eatsinayeaene: form is such that we 
ie msglrmadl some of rich have tured nto can easily understand 
interal cells: re, posterior cilinted nrea [rentral plate). WAY it was long  mis- 
taken. for the archeu- 


teron (p. 27). This depression, however, does not occur en 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 4-C, 24 
A). This structure is therefore, as Gonrrs proved, the shell- od 





* [According to Linum (No, II1.) the entomeres which eventually become 
invaginated to form the archenteron are derived from all the four cleavage. 


— 


‘DEVELOPMENT OF THE EARLY STAGE. 51 
eon S exactly the same way as in the marine Lamellibranchs 
coro and 15, p. 81) and in Cyelas (Pig. 19, p. 40), except that 


specially large and appears very early. This early develop- 

i ee a he. ie ae 

estrada all 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 » 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 


Tater ciate area Lago Plate]. 





the most aie feature is the ciliated area (Figs, 
is evidently the last vestige of the ciliation of the 
. This ciliated area, termed the ventral plate, 


sat first supposed, correspond to a remains of the 
the whole ventral surface plus the posterior 


y, and is therefore rather to be compared with the 


the first, two divisions, that is to say, neither the first 
e-p divides the egg into an animal cell and a vege- 
Lirxrm further finds that the small archenteron 
of the malgad which latter, however, 
ner. Of the two groups of mesoderm-cells represented 
those above the at shellegiand would correspond with 
while those below this structure and behind the 

23 A, represent the adult mesoderm 

ir of mesoderm-cells. For more 
















52 LAMELLIBRANOHIA—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 Zrochuphore, 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 ZrEGLER 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. [Lroure 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 ('nionidae 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 musele-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, «). 

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. 
25 and 26, sk). 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, iv., 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 4 and B). 
‘The mantle arises in this way and ut this stage is remarkably large, 
greatly over the rest of the body, which only later 
redevelops by 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,s0); during the invagination-processes just described 
these organs lengthen and, in consequence of these changes, are then 





ae, * ent, 





Sn 


oS al de eater {4 ee OT FLEMMING, somewhat 


a 0 veil sek with he outline of the sel 
ou 3 i entoderm (arc! dimen i 
eek eral chatty oo wath pg, beneory. briatles? Wy vitae res 


found on the inner surface of the mantle. Kach of these organs 
consists of a long columnar cell which gives origin to a number of 
Jong and fine sensory bristles (at first four to ten in number, later as 
*) that perforate the thin ectodermal cuticle (FLEMMING). 
organs are apparently of importance to the larva in the 
‘attaching itself to the fish-host and are acquired at a late 













gly regard these sensory organs as differentiations 
and can hardly consider them to be related to the 

(OLY was led to believe on account of the position 
. This particular organ occupies an isolated position 
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 
hecome 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, Lroure] (Fig. 23 C, 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 


BO 








Fro, 25.—Older embryo (within the egg-envelope) and free larva (@lochidium) of Ano- 
donta (after ScurenHoLz and Roane) , larval filaments ; 9, lateral pits; s, shell ; 
sh, shell-hooks; «m, adductor muscle; 's, tufts of setae representing the sensory 
organs ; 1, ciliated wrea, 


other weaker muscles in the form of long mesoderm-cells attached in 
various directions to the ectoderm, like the muscles which, in the 
Lrochophore, bring about the contractions of the larval body. 
Scmrernouz [and Lior] ascribe to the continuous contraction of 
these muscles the withdrawal of the central part of the embryo above 
mentioned. There are also, according to Scumipt, 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 
eotoderm (Rast), It grows inwardly as a long glandular tube which 
coils several times round the adductor of the shell and secretes 4 
filament of tough substance which projects from the aperture of the 
gland (Figs. 25 B and 26 A,/'). This organ has been regarded as 


—— 


THE DEVELOPMENT OF THE EMBRYO INTO THE PARASITIC LARVA, 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 gland (Carriere, F. Scuarpr, Scurernoz), The 
glntinous 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 4). The mouth has been pressed un- 
usually far back and, like the intestinal canal (cd), now belongs to the 
small posterior part of the larva. This displacement has been traced 
to the great development of the adductor muscle (wm), bat the 

conditions of this larval stage as compared with 
the former Trochophove-like stage seem to us to require further 
elucidation. 

| Lannr (No. 111.) deseribes the thvead-gland as arising from one of 
the ells 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, Lite 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 arca and near the 
posterior angle of the valves, two ectodermal depressions are to be seen on 
| these are the so-called lateral pits, as to the significance of 
which authors are not yery clear. If we rightly understand the somewhat 
‘obsonre description given by Scurennorz, he implies that large cells at the 
of these pits (no doubt corresponding to the lateral cells of the young 
rise to the pedal ganglia. But since the pedal ganglia, as in 
the depressions which yield the byssal gland, these early- 
)may be related to the latter (?). In Cyclas also the paired rudi- 
gland sppears very early (Figs. 19 and 21). Taking these 
together with the position of the pits with relation 
ble that this interpretation of the lateral pits as the first 

glands is correct. The formation of the actual byssal 
however, seems to take place at a later stage, 










56 LAMELLIBRANCHIA— UNIONIDAB. 


When the embryo has attained the stage of organisation just 
deseribed, 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 (lochidinm. 
‘The embryos found by the older investigators (RATHKE, JACOBSON) 
Beste illest Lael esc ac sce ae 
called Glochidium parastticum, 

The remarkable fact that the Glochidia remain for a time parasitic 
on fishes was discovered by Leypic (No. 32) and then further in- 
vestigated by Braun. FP. Scummr and Scutersousz 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 « 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 Scurexmocz, 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 ¥. 
JueRine's recent observations (No, 25), in the larvae of South 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 Glochidium of Anodonta complanata, although in other respects the 
organisation of these larvae is the same as that of other Glochidia, and they 
lead « parasitic life (ScureRHOLz). 


* (It is often stated that the Glochidia are only discharged when fish are in 
the neighbourhood, but Larren (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 mative water. The Glochidia cannot swim, but 
when discharged sink to the bottom, where they lie on their dorsal beets! 
the thread streaming up into the water. In this position the Glochidinm lies 
powerless to move in any direction, and here, too, it dies unless a suitable 
“host” is brought into contact with its thread, Ep. ] 

+ We do not know of any other statements upon this subject, although ft is 
not impossible that such may exist among the mass of malacological literature 
which is difficult to review; v. Juxnic mentions that he found Unionid 
lurve on fish in South America, 


THE TRANSITION TO THE ADULT. 57 


A cyst soon forms from the tissues of the fish and encloses the 
parasitic Glochidium. A peculiar mushroom-like growth formed by 
large cylindrical cells of the embryonic mantle serves for absorbing 
the tissues of the host, and especially the fin-rays in which the shell- 
hooks are embedded, The larva is no doubt nourished in this way 
until its intestinal eanal becomes functional. 

The time during which the Glochédium 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. ScurerHonz and Braun 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 
Tn shape, so that v. JHeninG, who found these larvae within the mantle-cavity 
of the patent, 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 
Unionidae, in the outer gills, The body in the South American forms is com- 
posed of three sections: (1) 1 conical anterior portion covered with cilia; 
(2) 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 
flat band considered by v. Jn=ntxo to be the byssus. This band is almost at 
the middle of the body and is attached to the ventral surtace, from which it 
runs forward. It is somewhat broader than the body, and six to ten times as 
long. ‘anid also to be connested with the anterior part of the body. 
to the somewhat yague account given by v. Jamntne of the larva 
‘by him “Lasidium,” and.in the absence of any statements as to the 

‘of this larval form, it is at present impossible to compare it with 
the entirely different Unionid larvae ((lochidia) or with the larvae of other 
Lamollibranebs. 





©, The Transition to the Adult. 


Very soon after attachment, as early as the second day, the larval 
‘organs which enabled the Glochidiuim to establish itself on its host, =, 
the glutinous filament and the brush-like sensory organs, degenerate. 

depression of the ventral surface arises behind these 
organs as they degenerate ; this depression involyes the two lateral 
pits already present in the embryo (Fig 26 A and B, g), At this 


58 LAMELLIBRANCHIA—UNIONIDAE. 


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. Scumpr). 

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 (w), 
which was still visible 
when the foot had 
attained a considerable 
size, now disappears, 
Of the larval organs, 
the shell-hooks aud the 
large adductor muscle 
are still Lo be seen, 
The first are for the 
present retained, the 
shell in other respects 
also retaining its em- 
bryonie form until the 
young Lamellibranch. 
leaves the fish ; indeed 
the embryonic shell can 
still be made out in the 
shell of theadult. The 
longer of the two free 
= sides of the three-sided 

i: embryonic shell must 
P16, 26.—A-C, larvae of A nodonte (after Scurernowz). be considered to corre- 

Spork Ce Pes ah Pe Pian zt a spond to the anterior 

ao a aun tes sry 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 Trechophore larva. Tt is, aceord- 
ing to Braun and F, Scuimpr, merely « larval organ, and degene- 





‘THE TRANSITION TO THE ADULT. 59 


nutes completely later, so that the two adductors of the adult must 
be regarded as new formations. In opposition to this view we haye 
the statement of SchierHoLz that the larval muscle only partly 
degenerates, some of it passing over into the anterior adductor of 
the adult. ‘This latter condition would agree with the fact that the 
anterior adductor appears first in most Lamellibranchs, and for along 
time is the only adductor present (p. 48); Braun, however, has 
maintained his original view against that of ScureRHoLz. 

‘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 « very long time ; the larva either does not reyuire 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 stomodacum. At the posterior end where the entoderm 
yesicle is in contact with the ectoderm, the anus now breaks through, 
without the formation of an ectodermal invagination (F. Scratrpr, 
Scnrernonz). The formation of the other organs, in so fav 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 
hecome perfected, having lengthened very much and become geni- 
enlate. On its lower surface it carries a groove which represents the 
rudiment of the byssal gland. The latter arises, as in Cyelas, 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 

groove just mentioned. The persistent byssal gland 
of other Lamellibranchs exhibits similar morphological conditions 
to those wlready described in connection with the (Unionidae and 


Dyelas, 


ai 


i 2)! 


60 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 « secretion of the epithelium of the shell-gland (Figs. 14, 
p- 28, and 15, p. 31). This embryonic cuticular shell is retained 
and passes over into the periostracum (epidermis) of the adult shell. 
The latter arises through a secretion of granular calcareous substance ; 
this at first accumulates in two complexes lying symmetrically at the 
two sides of the body beneath the cuticular shell (Fig. 21 A, p. 44), 
which, by further increase, yield the shell-valves. These grow out 
dorsally until they meet. The dorsal part of the cuticular shell that 
lies between the two calcified shell-valves which are growing towards 
one another yields the ligament of the shell (Zrecnmr, p. 43). 
The larval shell which thus arises and which has a very simple 
structure, is retained in Ostrea, the Unionidae and, as has recently 
been proved, in a number of other Lamellibranchs (RYDER, JACKSON, 
Bravy, Scureruonz). It is found asa minute prominence on the 
umbo of the large shell when the latter has not, as is often the case 

with the Unionidae, been de- 
a. stroyed through mechanical 
causes. 


The larval shell usually differs in 
shape from the shell of the adult, 
and is even sometimes very unlike 
the latter, As a rule, the shell 
changes very much during develop- 
ment. The youngest stage of the 
bivalve shell is characterised by a 
straight hinge-line and the slight 
development of the umbones. This 
can be seen in Fig. 27 4, and still 
better in Figs. 14-16, pp. 28-33), This 





Fig. 
larval shell of Ostrea edudix, seen from 


27.—A and B, early stages of the 


the side and from behind ; (, somewhat 





later stage (‘‘ prodissoconch ") of the 
larval shell of Ostrea virginiana, oblique 
side view. ‘This particular larwa had 
just attached itself, the left shell being 


stage (Fig. 15 C, p. 81), follows 
directly upon that of the unpaired 
cuticular shell, and must be supposed 
to have arisen out of the latter by the 


already lightly fastened to the enb- 
stratmm (after JACKSON). gradual swelling and upward growth 
of the shell on either side of the dorsal 
middle line, causing a slight infolding along this line which gives origin to 
the straight hinge. This straight hinge changes, as the shell soon begins to 


* We here treat of the formation of the organs only in so far as this as not 
already been considered. 


THE FORMATION OF THE ORGANS. 61 


curve and appears more arched (Figs. 27 B and 18, p. 36), and finally the 
umbones appear. The form of the shell seems to be developed in this way in 
many Lamellibranchs, as may be seen from the figures given by Lovin and 
Jackson and other authors, Jackson (No. 22) gives a special description of 
its development in Ostrea (Fig. 27 A-C), and we were ourselves able to observe 
it rise in a very similar manner in Dreissensia (No. 27). 

It is hardly necessary for us to point out the great difference that exists in 
the two forms just named between the larval and the adult shell, and this is 
‘still more the case in such Lamellibranchs as Pecten and the Aviculidae, the 
larval shell of which resembles that depicted in Fig. 27 C. This latter form 
of shell (the prodissoconch of Jackson) * represents a stage passed through by 

many Lamellibranchs. Jackson is therefore inclined to consider this form 
Sel ax specially peitve. In keeping with this view, we find that Nucula, 
whieh, in consequence of other features may be regarded as a primitive form, 
and which is found in the lower Silurian [Ctenodonta, one of the Nuetlidae, 
sours in the Cambrian], has a shell of somewhat the same shape as the 
above. 


The young shell grows by the secretion from the mantle-cells of 
new calcareous material ; this is deposited both on its inner surface 
and at its margin. These deposits give rise to the lamellate and 
zoned character of the adult shell, In older stages, these growth- 
processes take place chiefly at the peripheral parts of the mantle. 
There appears to be no essential difference between the manner of 
formation of the inner (nacreous) and the outer (prismatic) layers of 
the shell ; the one may pass into the other. ‘The prismatic structure 
of the onter layer is apparently due to the fact that the originally 
rounded calcareous granules became polygonal through mutual 
pressure, For details as to the formation of the Lamellibranch shell 
we are indebted especially to the researches of Tunnnene (No. 56), 
Exnensavm and F, Mincer (Nos. 11 and 38). 

growth of the periostracum also takes place at the edge where 
pisses over into a fine cuticle which covers the (ectodermal) 
epithelium of the pallial margin. At the periphery, where the cal- 
careous shell ends, we thus have the same condition as is shown in 
r embryonic times by the whole shell; the shell-integument, as 

we covers the mantle-epithelium. Indeed, the whole of the 
Tamellibranch shell is to be regarded as a cuticular structure covering 


‘the mantle-epithelium. 


"In contradistinction to the adult shell (the “ dissoconch") Jackson has 
-arched form with well-developed umbones (Fig. 27 C) the 
because it usually precedes the adult form of shell, as has 


62 LAMELLIBRANCHIA, 


Tu the case of Lamellibranchs inhabiting a tube, ¢g., the Gustro- 
chaenidae, this latter is secreted in the same way as the shell; the 
free edges of the mantle bend over the wide open shell-valves and are 
thus able to form the tube (Snurrer, No. 53). The structure of the 
calcareous tube of (astrochaena seems closely to resemble that of the 
shell. 


We still have to mention the relation of the muscles to the shell. The 
adductor muscles, as is well known, are inserted into the shell and the rela- 
tion of the epithelium to these muscles is interesting. At the points of inser- 
tion, the epithelium must cither be modified or must altogether degenerate. 
EBRENBAUM assumes that it degenerates, and ascribes to the muscles them- 
selves the capacity for secreting the shell-substance (!). As the animal and 
its shell grow, the adductor muscles, especially the posterior adductor, con- 
tinually change the position of their attachments on the shell. At their 
points of insertion, a shell-substance is produced, the so-called transparent 
substance, and the presence of this substance on the inner side of the shell 
indicates the course taken by the wandering muscle, But that this substance 
is seoreted by the muscle itself is very improbable, and we therefore profer to 
follow the older necount of TuLLBERG, according to which there is, between 
the muscle and the shell, an epithelium which produces the shell-material. 


B, The Nervous System. 


All the ganglia originate as thickenings of the ectoderm, which 
subsequently become separated from the latter. The ganglia arise 
separately and become connected later by commissures. 

Tt has already been mentioned that the cerebral [cerebro-pleural] 
ganglion arises in the Trochophore 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 Ziman, is probably the case in Qyelas). FP. 
Scumipt, indeed, has claimed for the cerebral ganglia of the 
Unionidae distinct origins and secondary connection by means of a 
commissure, a condition which will be described in connection with 
the Gastropoda (Chap. XXXII.}. In Anodonta, the two halves of the 
ganglion arise near the mouth and are separated by the stomodaeum, 
above which the commissure extends as a loop. 


THE SENSORY ORGANS. 63 


‘The pedal ganglia, in Cyelas und the Unionidae, according to the 
somewhat similar accounts of ZreauER and F. Scumrpr, with which 
also that of ScutenHonz can be harmonised, in their formation are 
associnted with the byssal gland, Shortly before the paired byssal 
gland becomes invaginated (Fig. 19, p. 40), at the point where it is 
to form, 4 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 Harscuek, arises as an 
ectodermal thickening even before the foot begins to form (Fig. 18, 
wy p> 36). It occupies 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 
‘livision 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. 

Tn their manner of formation the visceral 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-visceral) commissure has its origin, 
according to Zrecner, in a cell-strand which becomes detached from 
the ectoderm in the groove between the gill and the body, and rans 
forward from the visceral ganglion, and later becomes x commissure. 

[In Nueula and the Protobranchia generally, distinct pleural 
wanglia 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.] 


©. The Sensory Organs. 


‘The Byes. Tt may be stated with some certainty that the 
simply constituted eyes of the border of the mantle, é.2., the so-called 
Jneaginations, or optic pits, and the compound ryes arise through « 
comparatively slight differentiation of the mantle-epithelium, 


lia 


64 LAMELLIBRANCHIA, 


The ineaginations, 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 m 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 acornea, The visual cells are connected with the fibres 
of anerve which is a branch of the mantle-nerve (Canine, Parren, Rawrrz). 

‘The eye which thus arises shows some similarity to the compound eye of 
the Annelida as recently described by Anpnews.* 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 Parren (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 Peeten, unlike the two modifications of the edge of the mantle 
just described in other Lamellibranchs, are highly developed orgaus (Fig. 
28). The principal constituents of the eye of Pecten areas follows: there is a 
cornea behind which lies a large lens; behind the lens comes @ 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. 25, 7), which sends out one branch to the 
base of the eye, and thence direet 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 
Canrréne, Bétsceut, Parren and Rawrrz, 


ParreEn 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, Jownal of Morphology, Vol, ¥-, 1891, 


THE SENSORY ORGANS. 65 


connective tissue-cells between the inner ectoderm-mass, this tissue 
forming a continuous layer between the two. From this, #.e., from 
mesodermal elements, the lens, according to Parren, is formed, while 
the inner ectodermal mass yields the principal constituent of the eye. 





Eee (alter Sears tae Harsonen's Teel- 


1, cornea; 2, 3, pigment stoderm ; blood- 
Pieter! wits mpertslas chnriisele tages tnd betwee 
fone Si 6, pigment-layer, with the tapetum lying in front of it; 7, optic 


‘The way in which the various layers, the ganglionic cell-layer, the 
retina, ‘argentea, and the tapetum, ete., arise out of this mass 
is described, but these difficnlt points are not made sufficiently 
clear. 

Purther details concerning the ontogeny of these very peculiar eyes aud 
especially ns to the origin of the rods are much to be desired. ‘The solution 
¥ 


a 


66 LAMELLIBRANOHIA. 


of these problems seems all the more desirable as the eye of Pecten,* in tts 
structure stands almost alone among Molluscan eyes, With regard to their 
morphological interpretation, we are inclined to agree with Birscuit (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 
integument. This vesicle must be supposed to have arisen by invagination 
and abstriction from the ectoderm, a view with which Patren's observation 
of a solid ingrowth can be reconciled. The description given by Parrmy also 
of the rise of the lens outside of the optic vesicle supports such a condition if 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 rise of 
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 in the 
Gastropoda and in some of the Cephalopoda also. The position of the rods 
is hereby explained (Bison), 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 Terelo and Anodonta, near the pedal gang 
lion as invaginations of the ectoderm which then become abstricted 
from the latter and provided with otoliths and sensory hairs (Fig. 18, 
vt, p. 36). In Cyecias, the otocysts lie at the two sides of the embryo, 
behind the lateral end of the ciliated area. [In the Protobranchia the 
otocysts retain their connection with the exterior throughout life.] 

Spengel’s olfactory organs and the abdominal sensory organs 
(TH1zLx) show, by their structure, that they are mere modifications 
of the body-epithelium, a 


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 Ostrea, for example, the archenteron is said 
to pass over direct into the definitive intestine the blastopore remain: 
ing open, while in T¢redo, as well as in Vyclas and the Unionidae, the 
blastopore closes and a true stomodaeum forms. his condition, and 


#5) jylus has eyes similar in structure to those of Pecten, The 
found on the dorsal papillae of Onchidium also resemble those of Pecten 
in so far os the rods in them are turned away from the light. We thus 
find similar complicated structures, which must have arisen in altogether 
different ways. 


THE ALIMENTARY CANAL. 67 


tts 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 Harscwex, a proctodaeal in- 
vagination, und a similar invagination is described by Vorurzkow 
as oceurring 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. 16, 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 (Lovéx, Zrecier). 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 stomodaeum of Cardium, Lovin observed a small bulging of the 
ventral wall which involuntarily recalls the radula-sac of other Molluses, 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 long 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 (Bannors). 
No statements ns 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. 


a 


68 LAMELLIBRANOHIA, 


E, The Gills. 


Tu those Lamellibranchs in which the formation of the gills has 
been studied, they are found to arise in one of two [three, ¢/. p. 45] 
different ways which are somewhat difficult to harmonise in their 
early stages. According to one method, which has already been 
described for Cyelas 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 
groove-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 
before backward. 

According to the other method of gill-formation, which has been 
observed in Mytilus, Dreissensia, Ostrea (a somewhat similar method 
being found also in the Unionidae),* a papilla arises on each side of 
the body between the mantle and the median visceral mass, and 
behind these new papillae arise (Fig. 26 C), A longitudinally 
placed row of papillae thus arises by the continued development of 
fresh papillae behind those already formed. These, by the develop- 
ment of interfilamentar junctions, form the inner branchial leaf, 
while the outer leaf is produced by a similar row of papillae which 
arise somewhat later. 

The further development of the papillae was studied by LacazE- 
Durusiers in a form belonging to the last category, viz, in 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 Lacazu-Duruimrs (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 Lovity on 
Montaouta. The filiform permanent gill, of Peefen at any rate, arises as 
papillae, and Ray Lankesrnr states that the gills of Pisidiwm a first in 
the form of papillae, although these, from the figures, at first like the 
mere swellings of a fold. These statements recall the condition in the nearly 
related genus Cyclas, in which also papilla-like structures produced by the 
splitting of a leaf are found as the rudiments of the gills. It is, however, 
possible that Pisidiwm, in the formation of its gills, may be somewhat nearer 
‘the primitive condition. 


THE GILLS. 69 


The papillae are thickened at 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 
44 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 npward parallel 
to the (now outer or descending) lamella towards the base of the 
latter, The inner lamella thus formed is at first an unbroken menm- 
brane, the slits only appearing in it when it has increased in size, 





Fin 24.—Diaeram of the development of the gills fu a Lamellibranch possessing tw 
Deeeen eves ie cork ella Th tunes cr ontor leach leaf, fost ve, mantic, 


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 papillae and when its inner or ascending lamella is 
partly formed (Fig, 29 C). The outer leaf forms on the whole in 
the same way as the inner, but, in it, papillae are said to form 

‘as well as posteriorly, and the leaf, in order to yield a 
second lamells, bends outwards and not inwards (Fig. 29 D). The 
fusions of the free edge of the inner lamella of the inner leaf and the 
buter lamella of the outer leaf with the integument of the body take 
place Tater, and vary in extent greatly in different Lamellibranchs, 
being altogether wanting in some. 


an 





70 LAMELLIBRANCHIA, 


In Mytilus, as in some other Lamellibranchs (e.g., Pecten, Arca) 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 ). A 
section of these gills has the form of a W, and thus resembles 4 section of the 
gill-leaves in the Eulamellibranchs (Fig. 30 £). The free ends of the fila 
ments seem to be connected by 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 Lamelli- 
branchs as Cyclas and Teredo [or better still, in Pholas, StsGenroos], the 
wills of which originate as leaves. There is therefore some difficulty in 
regarding, with many authors, the later filiform condition of the gill as am 
original condition, This difficulty is increased by the fact that the gills of 
Mytilus, Pecten, ete., 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 im 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. 72). 


It appears that the papillae correspond to the gill-burs 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 strue- 
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 
Lamellibranchs (Eulamellibranchs and Pseudolamellibranchs). 








THE GILLS. val 


To 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, ete.,on the other, we might at first feel inclined to regard the 
method seen in the former as the more primitive, since the formation of the 
leaf precedes that of the papillae. The gill originates ns a Jeaf, 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 4 few forms such as T'vredo 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 Dat, the gill on each side consistsof one 
row of branchial filaments (Fig, 30 2) and in Avusiwm Dalli (and as it appears 
also in Arca vctocomata) there are two such rows on each side (Fig. 30 C)." 
‘The branchial 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 

of Mytilus (p. 68), In this way the row of branchial filaments gave 
rise 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-K). The ascending (re- 
fected) lamella of the branchial leaf thus arose; the free edge of which may 
finally fuse with the mantle, as ix. the case, for example, with the ascending 
‘Jamelia of the outer branchial leaf in the Unionidaa (Pig. 30 F). 
of gill which consists of single filaments, bent back upon them- 
indicating the two lamellae of the later branchial leaf (Fig. 30 D) 
‘uns repeatedly been held to be very primitive and has been thought to repro- 
‘sent the stage succeeding that in which the gills consisted of two straight rows 
ae rs: 00). Such gills are found in rigonia (Pexseneen) and 
whieh may be considered as very old forms. The gill-leaf consisting 
‘was thought to have arisen from the union of these reflected 
To us, the reflection of the single filaments and their regular, 
‘arrangement, such as is seen in the gills of Peete and Mytitus 












the accounts given by Persesxen, Dave and MimsuKuni 
sepa of the Lamellibranch gills, It is impos- 
far these may represent primitive conditions or may to 
tion-phenom aay, for it is evident that these latter do 


72 LAMELLIBRANCHIA, 


and even in Arca, 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 im 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. 


B. cs 


ate 





ae 
“ b 
Fro, 30,—Diagrams illustrating the position of the gills in the Lamellibranchia, aay 
Foldia; B, Dimya; O, Anusinm Dali; 1, Arca none: B, Anodonta; 7, foots 
m, mantle; i, inner, ¢, outer branchial leat. 


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, 
@ condition permanently retained in the gills of Nucula and Yoldia (Fig. 30 
A, Mirscxor). 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 KODY-CAVITY, ETC. 73 


‘The leaflets by lengthening and narrowing gave rise to the filaments, The 
gill of Nucwla is further primitive in its free pointed posterior termination, and 
may without further question be directly homologised with the bipectinate 
gill of the lowest Gastropods. ‘This last view of the Lamellibraneh gill, which 
was advanced years ago by Lecernant (No. 90), bas recently, owing to the 
esearches of Persennen (Nos. 40 and 41), Menecavx (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 simultancously. 

The rise of the gills in the form of leaves, as in Teredo and Cyclas, may, 
according to the present state of our knowledge, best be compared to the pro- 
duction of the branchial filaments or papillae 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 Rav Lan- 
sesrem), 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 Lamellibranch gills, great modifications have been 
introduced which render it very difficult to form conclusions os to their 
original constitution. 


P. 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 Unionidae and in Cyclas, but are best known in the latter, Our 
information on these points is due to the investigations of Leypic, 
Srepanorr, Gantw and y. Juerixc, which have recently been ex- 
tended and supplemented by Zmauen. The bistory 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 Tvoehophure stage, i, 
ut & stage occurring between the two depicted in Figs. 19, p. 40, and 
al Zane a4. 

Trochophure there is on each side of the intestine a compact 
ia ‘mesoderm-cells (Fig. 19, mes) which ZrmGceR claims as the 
‘mesoderm-bands. In the anterior end of each of these masses, u 











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 
ainesoderm-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-eavity which 
contains the organs arises independently of the former as a pseudocoele. 
‘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. 32) 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 beeome grouped in the form of a tube, the 
lumen of which communieates with the cavity of this vesicle. This 
tube, which at first rans upwards, and then again bends downwards, 
is the rudiment of the organ af 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, »,). 

From Zircrer'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 on invagination of the ecto~ 
derm takes part in it. ZmGbEeR’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 Benou.* 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 be 
decided. 

The statements which have been made as to the rise of the kidneys as mere 
depressions of the ectoderm (Ray LanxkestER, Gaxtx) 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. Benon. Neue Beitrige zur Embryologie der Anneliden, I. Zur 
Entwicklung und Differenzirung des Keimstreifens von Lumbricus. Zeifsch. 
J. wiss. Zool. Ba, 1. 1890, 














THE PERICARDIUM AND HEART. 17 


32.A, x”). 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 A-D), the intestine having been 
previously invested by certain of the mesoderm-cells which were 
distributed in the primary body-cavity. 

The circumerescence of the intestine by the pericardial vesicles 
and the fasion of these latter, as described by Zreener, strikingly 
recalls the fusion of two primitive segments in the Annelida to form 
& 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, ¢¢., 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 cirewmerescence 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 ZreGueR 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 0). 
‘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 2-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 


rs 





ves LAMEDLIBRANCHIA, 


eavity arises which soon, by the regular arrangements of its cells into 
an epithelium, assumes the form of a vesicle, This is the paired 
vudiment 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-eavity. 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 psencdocoele. 
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. 32) 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 rans upwards, and then again bends downwards, 
is the rudiment of the organ of Bojanus (Fig, 21 A, n, p. 44). [ts 
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, »,). 

From ZixG.er’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. Zrmqnen’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 Bercu,* But since, as we shall see, in the 
Gastropoda and also in the Annelida (Vol. i., p. 297), an ectodermal 


takes part in the formation of the nephridia, this question cannot here be 
decided. 

The statements which have been made as to the rise of the kidneys as mere 
depressions of the ectoderm (Ray LanxesTer, GANtN) 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 # still closer relation of the nephridia, when forming, 
with the coelomic sacs, and such a relation will be found in the Gastropoda. 


“BR. 8S. Bencu, Neue Beitrige zur Embryologie der Anneliden. I. Zur 
Entwicklung und Differenzirung des Keimstreifens von Lumbrieus. Zeitach. 
J. wise, Zool, Bd. 1, 1890. 





ee 


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 orgaus 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 


d. v. pack 






un ; the middle segment is that portion of the kidney 
on takes place. In the Uionidae, and in other Lamelli- 
idle section is not so much coiled as in- Cyclas, but. 
secretory epithelium is increased by the formation 
- In the primitive forms (Nuewa, Solenomya), the 
‘the form of a slightly coiled tube, the inner wall 
‘no great increase of surface, 
longer, as in the Unionidae, the gills also lengthen 
us takes up @ somewhat different position. Its original 
pericardium and the posterior adductor which is illus- 












78 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 Cand D). 


‘This method of formation of the heart from the mesial walls of the pericardial 
yesicles 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 (GropsEN). Since the vessels arise distinot from the heart, such an 
origin of the latter is not in any way improbable. On the other hand she 
fact that, in the Lamellibranchia, a paired heart lving dorsally to the 
intestine, and with each half enclosed in a separate pericardium may occur 
(Area) has led to the conclusion that the unpaired heart which, in the higher 
forms, surrounds the intestine, might have arisen by the fusion of these two 
hearts (Turmux, 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 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 ecoelom 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 IL). The dorsal 
vessel is therefore paired and, as the primitive segments grow further, 
shifts towards the dorsal line (A IT. and IIL.) On this line, the two 
rudiments of the heart finally meet (A 1V,) 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 Arca shows the greatest agree- 
ment. We must suppose that, in Arca, each of the two pericardial 
sacs, by the invagination of its inner wall, developed a ventricle (Fig, 
33 B, L-IV., 1). 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 Lamellibranchs, 
on the contrary, the cireumerescence 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 C, 1,-1V.). The rise of this single ventricle from distinat 


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). 
Bat this double character may, as already mentioned, be derived 
from the connection of the formation of the heart with the paired 
evelomic 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 Arca, 





On Goo CS. iad 
020). Oc) 


the formation of the heart. A, in the Annelida, 

#, in Avon, ©, in other Lamellibranchs, (The auricles are omitted for the sake of 
intestine 4, anes rudiment of the heart (united, in A IV. and 

wv, R the two pericardial vesicles (united in CTV, to 
19, ee 4p, splanchni« layer of the coelomic sac (primi- 


‘there i is a common anterior and posterior aorta, seems to point rather 


to the sine up of an originally single heart than to the union of 
‘ distinct, hearts. The paired dorsal vessel of the Armelida often 


between the two parts,+ and this also might be a 


Lo lg ea such a view of the Lamellibranch heart, speaks 
“heey stage through an arrest of develo} 

Soo that the method of acuabon described would 
as double heart in cases in which such a heart 

to he animal, 
and Acanthodrilus show the recurrence of conneo- 
hearts. In another Acanthodrilus almost the whole 
paired and is without transverse connections, but in its 
still mcomnection. ag omg Note on the Paired Dorsal 
Proc, Roy, Phys, Soe, Edinburgh. Vol. viii 


















— 





80 TLAMELLIBRANCHIA, 


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 
gills lying at the two sides of the body (Tarene, 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 Nweniu, 
Arca and Anomia, 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 (af, Vol. ii, p. 180, and Vol. iii., 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 fannel opens as it does in the Arthropoda into the cavities of 
the primitive segments (or coelom), as the homologue 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 
hody-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. ‘This 
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 (Grossen). 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-yascular system, 
makes such a view appear possible, 








MUSCULATURE AND CONNECTIVE TISSUES. 81 


According to our present anatomical and ontogenetical knowledge, 
the communication between the pericardial 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 (Rawkry). ‘The structure of the organ itself as well as the 
direction of the cilia within it are unfavourable to such « process. 
Tndeed 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 (ZimcLER). The 
swelling of the foot, as is evident from the statements of a number of 
authors (CanmeRe, Freiscamann, Scuremenz, Ranxry, ete.), 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 
ont 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 mesodern 
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 
imusenlature 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-inass, the distri- 

a 


— 


82 LAMELLIBRANCHIA, 


bution of these in the pseudocoele, 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 gret 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 body has the same origin. 


H, The Genital Organs, 


The ontogeny of the genital organs has not as yet been sufficiently 
studied. In Cyclas, 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 (Zrecuer). A somewhat later 
stage in the development of these glands is depicted in Fig, 21 A, g, 
p. 44. At w still later stage, they form two club-shaped russes, 
the broad surfaces of which meet in the middle plane, lying above the 
cerebro-visceral commissure (Fig. 31, 7). 


From what is as yet known of these glands in the Lamellibranchs, they do 
not bear any direct relation to the pericardial sacs, i., to the epithelium of 
the secondary body-cavity, as was found to be the case in the Annelids and as 
we shall presently see that they do in other Mollusea. Our knowledge of the 
subject is far too slight to justify further conclusions, but we may suggest that 
the close relation of the coelom to the kidney has led to an alteration in the 
conditions and thus to a gradual shifting of the genital rudiment out of the 
coelom. The efferent ducts must at the same time have undergone alteration, 
but with respect to these points, ontogeny fails us and we can only draw our 
deductions from the anatomical conditions, 

The relation of the efferent genital ducts varies in the Lamellibranchia, 
Most usually, they open on the surface of the body independently of the 
nephridia. In by far the greater number of the Eulamellibranchia they open 
into the supra-branchial cavity near the external aperture of the kidneys. 
In other Lamellibranchs, they and the efferent ducts of the kidneys open into 
acommon cloaca (Area, Pinna, Ostrea, Cyclas); in others again, they emerge 
further back in the organ of Bojanus (Anomia, Spondylus, Pecten, Lima), and 
only in a few primitive forms (Nuenla, Solenomya) do the genital products 
pass into the kidney, not far from the reno-pericardial aperture (PELsENnER, 
No. 41). 

Distinct efferent ducts for the kidneys and the genital organs are found in 
such forms as, from their structure, may be considered as phylogenetically 
younger than the others, while the two organs are connected in those 

Lamellibranchs which, by their organisation and their early geological 
necurrence, are proved to he of greater age (v. Juenina). These facts indicate 





84 LAMELLIBRANCHIA. 


12. Fremminc, W. Studien in der Entwicklungsgeschichte der 
Najaden. Sifzungaber. k. Akad, Wiss, Wien. Math. Nat. 
Cl. Bd. li. Abth. iii. 1875. 

13, Foret, F. A. Beitriige zur Entwicklungsgeschichte der Najaden. 
Med. Inaug. Diss, Univ, Wirzbur7. 1867. 

14, Funzarton, J. H. On the Development of the Common Scallop 
(Pecten opercularis). Eighth Annual Report of the Fishery 
Board for Scotlaul. Part iii. Edinburgh, 1890. 

15, Gorrre, A. Bemerkungen uber die Embryonalentwicklung der 
Anodonta piscinalis. Zettsehr. 7. wie, Zool. Bd. li, 1891. 

16. Grosnen, C. Die Pericardialdriise der Lamellibranchiaten. 
Arh, Zool. Inst. Griv, en. Bd. vii. 1888. 

17. Groppen, C. (1) Die Pericardialdriise der Lamellibranchiaten 
und Gastropoden. Zool. Anz. 1886. (2) Die Pericardial- 
driise der Opisthobranchier und Anneliden, ete. Zovl. An- 
seiyer. 1887, (3) Die Pericardialdriise der chiitopoden Anne- 

liden, ete. Sitzungxber. k. Akud. Wien. Math. Nat. Cl. Bd. 
xevii. 1888. 

18, HatscHex, B. Ueber . Entwicklungsgeschichte von Teredo. 
Arb, Zool, Inst. Unir, Wien, Ba. iti, 1881. 

19. Horst, R. On the Development of the European Oyster (Ostrea 
edulis). Quart, Journ. Micro, Sei, Vol. xxii. 1882. 

20. Horst, R. Embryog¢énie de I’huitre (Ostrea edulis). Tijdschrift 
dor Nederlandsche Dierkuwliqe Vereeuiquaig. Supplement Deel 
1. 1883-84. 

21, Huxuey, T. H. Oysters and the Oyster Question.  Enjlish 
Hlustr, Muy. 1883. 

22. Jackson, R. T. The Development of the Oyster, with Remarks 
on Allied Genera, Pro. Bastin Sor, Nat. Hist. Vol. xxiii. 
188s, 

Jackson, R. T. Phylogeny of the Peleeypoda. The Avulidae 
and their Allies. Men, Boston Sor. Vat. Hist, Vol. iv. No. 

1890. See also + Studies of Pelecypoda and the 

1 Origin of Structure in Peleeypods ”. Amerivan 

Vol. xxv. (p. 1.132), and xxv. (p. 11). 1890- 





















Zur Morphologie der Niere der sog. Mollusken. 
Leiterhe 1, wis Ba. xxix 1887. 

Jrerisc. H. vo Anodonta und Glibaris, Zool. Anz. Jahn. 

i 1s91. 

26. Juprinc., Ho v. Ueber die Ontogenie von Cyclas und die Homo- 









33. 


34. 


35. 


36. 


37. 


41. 


LITERATURE. 85 


logie der Keimblatter bei den Mollusken. Zetxchr. J. wixa, 
Zool, Bd. xxvi. 1876. 


. Korscnet, E. Ueber die Entwicklung von Dreissena poly- 


morpha Pallas. Sitzwngsber. Gesellech. Naturforsch. Freunde. 
Berlin, July, 1891. 


. LacazE-Dutaiers, H. Mémoire sur le développement des 


branchies des Mollusques acéphales lamellibranches. Ann. 
Sei, Nat. Zool. (iv.) Tom. v. 1856. 


. Langester, E. Ray. Contributions to the Developmental History 


of the Mollusca. Phil. Trans. Roy. Soc. London. Vol. elxv. 
Parti. 1875. 


. Leuckart, R. Ueber die Morphologie und Verwandtechaftsver- 


haltnisse der wirbellosen Thiere. Brunswick, 1848. 


. Leypic, F. Ueber Cyclas cornea Lam. Archiv. Anat. und 


Phys, 1855. 


. Leypic, F. Mittheilung fiber den Parasitismus junger Unioni- 


den an Fischen in Noll: Tithing. Inaug.-Dissert. Frank- 
furt u, M. 1866. 

Lovén, S. Bidraytil kanned om. Utreckl. af. Moll. Acephala 
Lamellibr. Vetenxk. akud. Handl, 1848, and Archiv. f. Nuturg., 
1849. 

Martens, E. von. Eine eingewanderte Muschel. Der Zvolo- 
gieche Garten, Jahrg. vi. 1865. 

Méx&caux, 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. Bull. Suc. 
Philom, Parix, (viii) Tom. i. 1888-89, 

Mitsuxurt, K. On the Structure and Significance of some 
Aberrant Forms of Lamellibranchiate Gills. © Quart. Journ. 
Micro, Sei. Vol. xxi. 1881. 

Ménius, K. Die Auster und die Austerwirthschaft. Berlin, 
1877. 


. Miuuer, F. Ueber die Schalenbildung bei Lamellibranchiaten. 


Schneider's Zool, Beitrage. Bd. i. Breslau, 1885. 


. Partes, W. Eyes of Molluscs and Arthropods.  Mittheil. 


Zool. Stat, Neapel. Ba. vi. 1886. 


. PELSENEER, P. Sur la classification phylogénétique des Pélécy- 


podes. Bull. xi. France of Belyique (A. Giard). Tom. xx. 
1889, 

PELSENEER, P. Contributions u l'etude des Lamellibranches. 
Archiv, Biol, Tom. xi, 1891, 


46. 


47. 


LAMELLIBRANCHIA. 


2. QuaTREFAaGEs, M. A. DE. Mémoire sur l’embryogénie des 





Tarets (Teredo). Ann. Sei. Nat. Zool. (ii) Tom. xi. 1849. 





3. Rast, C. Ueber die Entwicklungsgeschichte der Malermuschel. 


Jen. Zeitachr. 7. Natur, Bd. x. 1876. 


. Rangin, W. M. Ueber das Bojanus’sche Organ der Teich- 


muschel etc. Jen. Zeitachr. 7. Naturw. Bd. xxiv. 1890. 


. Rawitz, B. Der Mantelrand der Acephalen. Jen. Zeitechr. 7. 


Nature. Bd. xxii. and xxiv. 1888 and 1890. 

Ryper, J. A. The Metamorphosis and Post-larval Stages of 
Development of the Oyster. Annu Report of the Commis- 
xioners of Fish and Fixheries for 1882. Washington, 1884. 

ScurerHouz, C. Zur Entwicklungsgeschichte der Teich- und 
Flussmuschel.  Zeitechr. f. icixx, Zool, Bd. xxxi. 1878. 


. ScHERHOLZ, C. Zur Entwicklungsgeschichte der Teich- und 


Flussmuschel. Berlin, 1878. 


. SCHIERHOLZ, C. Ueber die Entwicklung der Unioniden. 


Denkachr. k. Akad. wins. Wien. Math. Vat. Cl. Bd. xiv. 1889. 


. Scumipt, F. Beitrag zur Kenntniss der postembryonalen 


Entwicklung der Najaden. 9 Archiv. 7. Natury.  Jabrg. li. 
1885, 


. Scnapt, Osc. Ueber die Entwicklung von Cyclas caliculata. 


Archiv, f. Anat. n. Phys. 1854. 


2. SHarp, B. Remarks on the phylogeny of Lamellibranchiata. 


Ann, May. Nat. Hist. (vic) Vole ii, 1RRR, 


. SLuITER, C. Px. Ueber die Bildung der Kalkriéhren von Gas- 


trochaena. Naturkund, Tijdschrift Nederlandech, Indié, Ball. 
1890. 


. STEPANOFF, P. Ueber die Geschlechtsorgane u. die Entwick- 


lung von Cyclas comea. Archie. f Natury. Jahrg. xxxi. 
1865. 


. THIELE, TH. Die Mundlappen der Lamellibranchiaten. Zettachr. 


J. wise, Zool. Ba. xliv. 1886. 


. TULLBERG, T. Studien iiber den Bau und das Wachsthum des 


Hummerpanzers u. der Molluskenschalen.  A‘g/. Svenska 
Vetenskaps-Akal. Handlingar, Ba. xix. No. 3. 1882. 


. VorLttzkow, A. Entovalva mirabilis. eine schmarotzende 


Muschel aus dem Darm einer Holothurie. Zool. Jahrb. 
Abth. 7. Systematik, ete. Ba. v. 1890. 


.» Wextner, W. Zur Entwicklung von Dreissensia. Zool. Anz. 


Jahrg. xiv. 1891. 


. Witson, Joan. On the Development of the Common Mussel 


LITERATURE, "87 


(Mytilus edulis L.).  Fisth Annual Report of the Fishery 
Bourd sor Scotland (jor the year 1886). Edinburgh, 1887. 

60. Zrecuer, E. Die Entwicklung von Cyclas cornea Lam. Zeitschr. 
J. weiss, Zool. Bd. xli, 1885. 


APPENDIX TO LITERATURE ON 
LAMELLIBRACHIA. 


1, Bernagp, F. Scioberetia australis, type nouveau de Lamelli- 
branche (Anatomy, Embryology, etc.). Bull. Sei. France et 
belyique. Tom. xxvii. 1896. 

I. Drew, A. G. Notes on the Embryology, Anatomy and Habits 
of Yoldia limatula, Say. Johns Hopkins Univ. Circ. No. 132. 
1897, 

MI. Linure, F. K. The Embryology of Unio complanata. Journ. 
Morphol. Vol. x. 1895. 
IY, PeELsENEER, P. Les yeux cephaliques chez les Lamellibranches. 
Compt. Rend. Acad. Sei. Paria, Tom. exxvii., p. 735. 1898. 
V. Sincerroos, C. P. The Pholadidae. I. Note on the Early 
Stages of Development.  Jvhnx Hopkins Univ. Cire. 1895. 
II. Note on the Organisation of the Larva and the Post-larval 
Development of the Shipworm. Op. cif. 1896. 
VI. SraurracHEr, H. Kibildung und Furchung bei Cyclas cornea. 
L. Jen. Zeitechr. f. Naturwins. Ba. xxviii. 1894. 
Vi. Sraurracuer, H. Die Urniere hei Cyclas cornea. Zeiterhr. 
J. ties, Zool. Ba. \xiii. 1898. 
VIII. MzissennEmer, J. Entwicklungsgeschichte von Dreigsensia 
polymorpha. Marburg. 1899. Zool. Centralbl. Jahrg. vi. 


CHAPTER XXXI. 


SOLENOCONCHA (Scapuopopa). 


(DENTALIUM.) 


Tue ontogeny of Dentalinm was investigated many years ago 
(1857) by Lacaze-Dururers, 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-DuTuiers, 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 egy 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 
also 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 macromeres. This method of 





cleavage shows considerable resemblance to that most common among 
the Lamellibranchia. Further division and the formation of a 
central cavity give rise finally to a blastula, one half of which con- 
sists of small and the other of lurge cells (Fig. 34 4). The animal 








a 


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 A). 
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, 
ax is evident from a glance at Fig, 35 A. In later stages, as the larva 
grows in size and as its cells increase in number, the rows of ciliated 





Fig, 35,—A-C, three larvae of Dentadinn aged respectively 12, 24 aud 87 hours (after 
Kowarevsky). 41, blastopore ; m, mantle-fold ; moe, permanent posterior aperture 
of the mantle; p, posterior part of the hody; W, ciliated ving; a, apical ciliated 


tuft. 








cells are less conspicuous as compared with the rest of the body (Fig. 
36 A), and finally appear as 4 single though somewhat broad ciliated 
ring (Fig. 35 A-C). Meantime, the ciliated tnft at the cephalie 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 8), 

In the youngest larvae, eiz., at the gastrula-stage, the blastopore 
was terminal, i.¢., opposite to the cephalic pole (Fig, 34 C), but it 
soon changes its position, shifting forward towards the ciliated rmg 
along the future ventral surface (Fig. 35 A). 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, hus 


92 SOLENOCONCHA. 


of a certain character typical of the Molluscan larva. Thus, a dorsal 
invagination of the ectoderm (Fig. 36, «/) becomes differentiated at a 
very early stage (A), 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 frum the back on to the two sides of the body, 
but, whereas the young Lamellibranch shell soon becomes bivalve, 
the shell of Denta/ium remuins single, /.¢., it remains to a. certain 
extent at a 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 Dentulinm, 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 Jrufalinm 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. and 36 B). The definitive mouth is derived from an 
invagination lying immediately behind the ciliated ring (Fig. 36, m). 
The depression on the dorsal side which is to be regarded as the shell- 
gland (./) 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, m). 
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, 7), at the base of which the otocysts are to be 






— | 


‘THE DEVELOPMENT OF 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 neur 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 deseribed for 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. ‘Thus, two ectodermal depressions appear close to 
the ciliated tuft; these at first are shallow, but deepen more and 
more (Fig. 37 4 and &, cy) 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, direetly 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 donbt as to their 
ic 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, ax 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, 

other Mollusca. Considering the greater contractility of the Iurva, the 
Presence of such invaginations suggests a more or less temporary infolding of 
‘the surface. Kowatevsxy assumes that these ganglia first arose as a surface 
uf and explains the invagination of the ganglionic rudiment as due 
% je absence of room for surface-expansion owing to the limitation of the 
pre by the forward concentration of the ciliated ring. The develop- 
‘ment of the cerebral ganglion in Pentalinm recalls the condition which we 
‘shall find in various Gastropods, where it undoubtedly arises by invagination 
- Since, in these latter cases, we have to do with more specialised 
would be desirable, in instituting a comparison with Dentalium, to 
1 in what way the cerebral ganglion arises in the more primitive 
‘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, ete.) 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 (ef. p. 42 and Figs. 
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 (acazE-DUTHIERS). 





es 
the formation of the brain (after Kow 
Levsky). ey, rudiment of the c 

ganglion; 1, mantle ; 
x, cephalic pole; 1, pre 








‘tol 
al 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 when 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 

is therefore marked by the growth and the further 
development of rudiments already present in it. 

If we examine the larva externally (Fig. 38 B), we find that the 
shell has grown much larger. At first it was a dise-like structure 
lying on the back, 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, « parallel 
strintion can be recog- 
nised (Fig, 38 2), 
representing lines of 
growth, su that the 
growth takes place 
here in the same way 
as in the shells of the 
Lamellibranchia (Fig. 
2%, p. 60), as the gig, u8—Lormne of Denlalium, A at. the end of the 
shell increases in size, second day and A on the third or fourth day. 1, 


4 = seen from “the ventral side, B, seen somewhat obliqu ely 
‘the fusion of the the oame side (after Lacans-Durutans).. /, toot 


weil margins e-file 
comes closer, At first 
the anterior aperture of the shell is still considerably wider than the 
 & condition connected with the shape of the larva (Fig. 
38 2B), but when the velum degenerates and the shell lengthens, the 
anterior uperture 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 « later stage the shell assumes « dorsal curvature and gradually 
‘sequires the tubular conical shape found in the adult. The anterior 
gud posterior apertures, which originated through the lateral growth 





96 SOLENOCONCHA. 


and ventral fusion of the shell-plate (Fig. 39 A-and 2), 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 





=A, a larva of Dentalinn undergoing metamorphosis ; B, anterior portion of 
young Dentalivm (after Lacaze-DUTHIERS), d, intestinal canal ; 7, foot ; mor, 
posterior aperture of the mantle ; s, shell; ¢, tentacle-rudiment ; r, 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 
Dentulinm (Fig. 39 A and B, f). In spite of the early development 
of this exceedingly characteristic shape, it is not to be considered 
a primitive feature, but must be regarded rather as a later acquisi- 
tion, as it is wanting in a few genera PLATE (No. 3). In Stphono- 
dentalium and Caduus the two lateral lobes are wanting, these genera 
apparently exhibiting a more primitive form of foot. 


THE TRANSFORMATION OF THE LARVA INTO THE ADULT. 97 


At a somewhat later stage, at which the velum is still retained, the 
foot is found protruded from the shell (Fig. 39 A). This stage, 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 
ef 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-inarked channel, lined with 
‘powerfully ciliated cells (Fig. 38 and 39, 1). This ciliation is 
eonnected 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. 
Tt is here that the prominences arise which give origin to the 
tentacles (Fig. 39 6, f). According to Lacaze-Duraters, 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 
deseription given does not explain the relution 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 in the Gastropoda, 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. 


A similar view of the tentacle-filaments of the adult is taken by THrene 

a to Chapter xxxiii.}, who compares the two lobes or tentacular 
shields with the large tactile lobes of Haliotis which are beset with tufts. 
‘These Intter, if lengthened, would result in structures resembling the ten- 
teoular filaments. Quite recently PLarr (No, 3) also has accepted this view, 


ortega prominences on the head of the young animal the 


‘The radular sac arises during the later stages of larval life as an 
gutgrowth of the stomodaeum, The anus also appears in the larva 
‘6 aslight depression of the ectoderm behind the base of the foot. 
‘The enteron, according to Kowarevsxy, 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-Doratens, 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. Kowauevsky, A. Etude sur Vembryogénie du Dentale. Aun. 
Musée Hist. Nat. Murseille Zool. Tom. i. 1883, 

2. Lacaze-Duraters, H. pg. Histoire de l’organisation et du 
développement du Dentale. Ann. Sci. Nat. (4.) Tom. vi. 
and vii. 1856 and 1857. 

3. Puate, L. Ueber den Bau und die Verwandtschaftsbezichungen 
der Solenoconchen. Zool. Juhrh. Atth. f. Anut. Bd. v. 
1892. 


APPENDIX TO LITERATURE ON SOLENUCONCHA 
(SCA PHOPODA). 


I. Sumrota, H. In Bronn’s Klass. u. Ord. d. Thierreichs. 1894-95. 
Anatomy, Ontogeny, Phylogeny and Literature. 


CHAPTER XXXII. 
GASTROPODA. 


Systematic Order :— 


L Prosoprancata (Streptoneura). 
The gill or gills lie in front of the heart. The pleurovisceral 
connectives are crossed. The sexes are distinct (save in 
Vilvata, 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 
inarginal slit or row of” perforations. 

Haliotix, Fissurella, Pleurotomaria. 

(+) Azygobranchia. One ctenidium (left of Zygo- 
branchs); two auricles (right ending blindly); heart 
traversed by rectum (except in Helfeinidue); nephridium 
generally paired, operculate. 

Turbo, Trochws, Neritina (one kidney, distinct genital 
aperture). Aelicina (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), Aemaee, 


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 Valvata). The 
nerve-ganglia distinct and concentrated round oesophagus ; 
pedal commissures rare. (senital 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. 
Junthina, Murex, Buccinun, Purpura, Newa, Fulque, 
Fusux, Farciolaria, Strombus, Rostellaria, Crepidula, 
Calyptraca, Vermetus, Bythinia, Paludina, Thyea, Stilt- 
ter, Entoconcha, ete. 


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. 

Oxyyyrus, Atlanta, Pterutrachea, Carinarin, Firoloidu, 


II. Op1stHOBRANCHIA. 


The gill and auricle generally behind the ventricle (except in 
Actaeun). — Pleurovisceral commissures rarely crossed 
(Actaeonidae). Hermaphrodite, marine. 


Sub-order 1.—Tectibranchia. Shell generally present, often 
much reduced and internal, wanting in Runcina and 
Plenrobranchea ; with mantle-cavity containing a cteni- 
dium. 

Artaron, Bullu, Avera, (asteropteron, Philine, Aplusia, 
Plearobrauchus, Pleurobranchea, Umbrella. 


Sub-order 2.—Nudibranchia. Without shell in adult stage ; 
mantle, ctenidium and osphradium wanting. 
Tritonia, Doris, Chromuduris, Palyeeva, Teryipes, Rlysia, 
Arolis, Doto, Fiona, 


111. Preropopa. 


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. 
Spirinlix, Limacina, Tiedemaunia, Cymbnlia, Crvolinia, 
Hyalorylie, Styliola, Cleudurn, Cresvia, 


OVIPOSITION AND CHARACTER OF THE EGG-CAPSULES AND EGG, 10] 


Sub-order 2.—Gymnosomata. Without shell and mantle. 
Clicne, Preumodermon. 


IV. Ponmonara. 

Principally fresh-water or terrestrial. Ctenidium wanting ; 
mantle-cavity modified as a lung. The pleuroyisceral 
commissures are not crossed. Hermaphrodite, 

Sub-order 1.—Onchidiacea. Marine or littoral, without 
shell; anal and pulmonary orifice posterior, 
Ouchidivn, Vaginulus. 
Sub-order 2.—Basommatophora. Fresh-water and terres- 
trial (usually maritime) Pulmonates. Eyes at the bases 
of the tentacles. 


Limnaea, Planorhis, Ancylus, Auricula. 


Sub-order 3.—Stylommatophora. Terrestrial Pulmomates. 
Eyes at the tips of the tentacles. 
Suceinea, Vitrina, Clausitia, Bulinus, Helix, Testacella, 
Dawlebardia, Limac, Arian. 


1. Oviposition and Character of the Bgg-capsules and Egg. 


‘The Gastropoda * are mostly oviparous, but oviposition takes place 
in such « 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 ure wanting in this genus. Tt was there- 
fore possible to fertilise these eggs artificially (ParrEn, No, 52). 
Each egg is surrounded by a somewhat thick radially striated en- 
yelope which has a funnel-like projection with a wide aperture (the 
micropyle). 

Th 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 dise-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- 
is by Pyenren (No. 88). A detailed account of oviposition in 
! and notices of the literature on the subject are given by Kurer- 
ee and reneat obtained ere the treatises setecies a3 a 
account of the egg-capsules will found in 

ameraele Comic 1887.—Eb. mn = 


102 GASTROPODA. 


surrounded by a transparent membrane. In certain marine Gastro- 
poda, ¢.y., in various Opisthobranchia, this gelatinous spawn attains 
a great size, forming long, ribbon-like coils (Acol/s) 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, Pleurobrauchux, ete.). These gelatinous masses 
frequently contain a very large number of eggs, the spawn of a single 
Dorix 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 (Teryipes, according to 
Sauenxa, No. 114). 

The eggs of the Heteropoda are also laid in gelatinous masses 
which take the form of long ropes (Carinaria, Pterotrachea, Firu- 
loida) according to Fou (No. 31); only the Atlantidae (Atlanta, 
Oxrygyrus) 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 shape. 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 (Creseis aeirulata), or as round 
balls containing a large number of eggs (C/ione).* 

In Fixeurelle 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 
egy-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 (Gathobdellidar) in the cocoons of 
which several embryos are found floating in a nutritive fuid (Vol. i., 
pp. 281 and 391). The comparison becomes all the more striking 
when we find that ina few Prosobranchs, as in the Oligochaeta (p. 
281), not all the eggs ina capsule develop, but a few, or it may be 
a luge number disintegrate, and serve as food for those that survive. 
In many Prosobrinchia, however, all the es in a capsule develop, 
in Fudyur, from 12 to 14, in Nasea, from 5 to 15, ete. In Purpnra 
A sules contain many egys, all of which undergo 





Hana, the ea 





* Detailed statements as to the oviposition in the Pteropoda and also in the 
Heteropoda are found in the works of Fon (Nos. 31 and 32). 


OVIPOSITION AND CHARACTER OF THE EGG-CAPSULES AND EGG, 103 


cleavage, some of the embryos, however, develop no further, but 
perish, their remains being devoured by the other embryos, This 
ix also the case, according to McMurrics, in a few species of 
Cepidala, and in Urosalpine (BRooxs). Fasciataria lays about 200 
eggs in each capstile, but only 4 to 6 of these develop, and this is also 
the case with Buceinnm undatum. Each capsule of Purjara lapillus 
contains 400 to 600 eggs, only 10 to 16 of which develop into mature 
embryos (SenunKa). The egg-capsule of Neritina fluviatilis also 
shelters « large uumber of eggs (according to Buocnmann 70 to, 90) 
although only « single embryo in it attains complete development. 
(Ccavantpe). In this case, the unfertilised eggs divide soon after 
the polar bodies have formed, and break up into irregular heaps of 
protoplasmic spheres, being in this way distinguished from the eggs 
undergoing cleavage. 

Tn shape and structure, these egy-capsnles vary greatly. As a 
rule 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 Ner/ins. the older cocoons of whieh easily divide into 
two hemispherical halves. ‘T'o allow the brood to eseape, the capsule 
oceasionally hus an aperture closed hy a delicate membrane, situated 
opposite to the point of attachment. Several capsules are usually 
found together, as in Bucrinum wulatum, Fusus antiquus and others, 
the capsules of which are piled one upon another, thus forming an 
enormous mass of spawn, ‘They oceasignally appear laterally com- 
pressed and, in one species of Fusus observed by Bosrerzky, are 
round plano-convex dises, attached by the flattened side. The 
capsules of Busyron (Fulgur) also are leaf-like or rather dise-shaped ; 

these are arranged in « row like a roll of coins, aud are attached to a 
| common filament, ‘These capsules have an aperture opposite to the 
points of attachment for the escape of the brood. 

tn Wessa neutabilis, the capsules are cup-shaped and attached by 
the obliquely troneated end, the opposite pointed end carrying an 
aperture ut 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 (Maree), 
Here also, the aperture of the cup is closed by a membranous cover, 
Which opens when the brood is ready to hatch, In Purpura dapillus 
10 to 15 such capsules, which, however, are more flask-shaped and of 


— 





104 GASTROPODA. 


leathery consistency, are fastened to a similarly constituted, strueture- 
less membrane which, in its turn, is attached to a stone, The same 
is the case with the capsules of Fusciolaria 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 by & gelatinous albuminous substance 
and may be connected together into spawn-masses which resemble 
rows of beads (imac) 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 « 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 
which is continued into the envelope of another egg, so that the 
eggs constituting the spawn are connected into wreathlike 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-sults. A more or less thick calexreous shell 
is thus formed around the egg; this, even in Heli pomatia, is of 
somewhat firm consistency. The eggs are usually deposited in great 
numbers (60 to 80 in elie pomatia) in small holes in the ground pre- 
pared by the parent animal and are then covered over with earth. 
Species of Bulimasx which live on trees roll up leaves into the form 
of cornucopiw and Jay in these their soft-shelled eggs. 

The egys of the terrestrial Pulmonata attain a considerable size. 
Even the eggs of Helic pomtia measure 6 mm. in diameter. Those of 
the Ceylon form, Helie (Acirne) Waltout ave as large as a sparrow's 
egg (P. and F, Sarasin, No, 102), and those of an American species 


i =" 





OVIPOSITION AND CHARACTER OF THE EGG-CAPSULES AND EGG. 105 


of Brilimus which are oval, measure 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 fills the shell, having increased 
im size to this extent at the expense of the surrounding mass of 
nutrient material. 

Some Gastropods take care of their eggs. Those species of Crepn- 
dula which are immovably fixed to one spot (C. surnicata, plana, 
and conrera, McMunnion, No. 70, Consnin, No. IV) retain the egg- 
capsules, which ure attached to the substratum, under cover of 
the shell. The wall of the capsules thus protected are naturally of 
delicate nature. Verimetus attaches a few capsules to the inner sur- 
face of its shell, near the aperture of the latter (Lacaze-Duraiers), 
Tn 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 Paludina (Viviparns) vivi- 
para, the eggs of which develop in the oviduct, which functions 
‘a5 a uterus, until the form of the adult is reached. Its course of 
development, however, exactly resembles that of other Prosobranchin. 
The egg is surrounded by « conspicuous layer of albumen, which 
again is enclosed in a membrane that runs out into a twisted stalk, 
s¢ that « kind of cocoon is formed, As a rule, only one egg lies 
within this envelope, but two are sometimes found in it (Leypia, 
No. 68), the resemblance to the eggwapsules of other Prosobranchia 
‘being thus heightened. Similarly, in a few species of Melanéa [in 
Typhobie sud Nassopsis), the embryos develop in the uterus, and 
are only boru when they have attained the adult form. 

{in some species of Melania and in Spelia, the embryos develop in 
‘# special brood-pouch formed by an ectodermal invagination near 
‘the right cephalic tentacle, The viviparous habit appears to be 
hugely confined to fresh-water forms. | 

A few Pulmonata are, like the Prosobranchia above-mentioned, vivi- 
parous, the development of the embryo here also taking place in 
‘the oviduct which is transformed into a uterus, This is the case in 
“afew species of Clausitia, Pupa, Helix and Vitrina, Nearly related 


+ osnligaahtaad found to differ greatly in their methods of repro- 
ie 


ion, some being oviparous, and others viviparous (No. 102). 
1 


il 


106 GASTROPODA. 


The actual egg of the Gastropods, if not specially large, is ‘fairly 
rich in yolk which is often yellow, but occasionally of some other 
colour (blue-green in Pafell) ; this frequently renders the egy quite 
opaque. A clear protoplasmic region can frequently be distinguished 
from a more opaque region laden with yolk, the difference between 
the animal and the vegetative pole being thus indicated (Fig. 40 A 
and B). 

In some Gastropod egys there is less yolk than in others. /aln- 
dina may be cited as an extreme case on the one hand, and Vase 
and Fusux on the other. The egg itself is usually surrounded by a 
clear viscid mass which, in its turn, is again enclosed in a transparent 
envelope. It has already been mentioned that other envelopes may 
be udded, and that several egzs may be enclosed in a common 
capsule. 





2, Cleavage and Formation of the Germ-Layers. 


In spite of the great number of forms among the Gastropoda and 
the different development of the several divisions, we can, in every 
case which has been investigated, recognise a common plan in the 
cleavage of the egy, although at times this is more or less obscured 
by modifications introduced by the variations in the amount of the 
yolk present. 

In this respect we have resemblance to the Lamellibranchs, but 
the course of cleavage itself is different in the Gastropoda. The 
phenomena of cleavage have been studied in a large number of 
Gastropods and may therefore be considered as pretty accurately 
understood. As early as 1850, the cleavage of the Gastropod egg 
was described by WaknEck (No. 130), very completely, considering 
the time at which he wrote. And since then it has been investigated 
by a number of zoologists, among whom we may mention For, 
Bonretzky, Rani, Mark, Buocu Sand others (see the literature 
appended to this chapter). 

In all Gastropods, as far 
may be equal 














is known, cleavage is total; at first it 
but it very soon becomes unequal. The egg, in many 





cases, is divided up into two large blastomeres of almost equal size 
by a median groove which cuts it below the polar bodies (Fig. 40 4). 
A second furrow, which is also meridional, divides the egg into four 
almost equal blastomeres (/, /-/1). These four cells, owing to the 
nature of the second cleavage, often lie in such a way that two are 
in contact with one another in the centre of the egg and thus 





CLEAVAGE AND FORMATION OF THE GERM-LAYERS, 107 


separate the other two (Fig. 48 A, p. 120) [see Conkran, No. 1V, pp. 
44-53 on this point]. At the line of junction between the first two 
blastomeres, the transverse axis of the future embryo can already be 
seen, while the plane at right angles to this represents the sagittal 
plane of the embryo. _The position uf the axes is thus determined 
very early as was seen to be the ease in other animals.* 

An equatorial furrow cuts otf from these four cleavage-cells four 
smaller cells so that the embryo now consists of four macromeres and 
four micromeres (Fig. 40 C, L/V and J'-7V"), the latter lying at the 
animal pole. The relative size of these blastomeres varies eon- 
siderably im different Gastropods. In Patella (Parren, No. 83), 
and in Paludina, for instance, the micromeres are not much smaller 
than the macromeres, whereas in Fudyur, the micromeres in com- 
ferison with the macromeres, which are very rich in yolk, are hardly 
visible (MeMurricn, No. 70). These differences are no doubt de- 
termined by the amount of yolk present in the eggs. 

As cleavage proceeds, four moré micromeres arise (D, 1*-1V"), as 
before, from the macromeres. As a rule, this process is repeated 
once more, and in this way three generations of micromeres arise 
from the macromeres ; this, however, is not the case in all forms. 
The nuclear spindles in the macromeres depicted in Fig. 40 /, show 
Unt these cells ure preparing to divide to form the third generation 
of micromeres. In the meantime, the already formed micromeres 
have, by division, increased still further in number; sometimes, 
however, they do not multiply antil later, In Voritins, according 
to BuocuMann, the first and second generation of micromeres (/-/" 
aud 1-4) divide first, but in Planordix the twelve cleavage-spheres 
which now compose the embryo undergo almost simultaneous division 
(Rast). In the example depicted in Fig. 40 4, the twenty-four- 
celled stage is reached by a division of the first generation of 
micromeres quickly followed by the division of the second generation 
and the abstriction of the third row of micromeres from the macro- 
meres as indicated by the nuclear spindles in /’-7V" and L-JV, &. 
The macromeres, through this last division, are either considerably 


(This seems to hold good for ull those forms in which the position of the 

‘first two cleavages has been investigated in relation to the axis of the adult 

. CONKLIN, for instance (No. 25), concludes that, in Crepiduda, the first 

to the transverse axis and divides the egg into an anterior 

aod o half, while the second furrow lies in the longitudinal axis 

denotes the division of the egg into a right and a left half. Heywons 

(No. X11) finds a similar condition in Umbrella. Cf. also the position of the 
“Asis at & somewhat later stage, as given on p. 143.—Kp.] 





108 GASTROPODA, 


reduced in size (Fig. 40 #), or, as is most frequently the case, are 
retained for some time longer as specially large cells (F aud @), the 
micromeres which have arisen from them shifting towards the animal 
pole. The multiplication of the latter continues and leads to the 
development of a cap of smaller cells which lies upon the macromeres 
(F und (, ete.).* 


The great agreement of the various stages of cleavage in the Gastropoda 
with those of the Turbellaria is very striking, as may be seen from a com- 
parison of Fig. 40 with Fig. 75, Vol, i., p. 162. This is most marked in 
stages C-F of Fig. 40, but the later stages F’ and @ also show great re- 
semblance to the corresponding stages in the Turbellaria (Vol. i., Fig. 75 F 
and Z), The radial structure does not, indeed, in the Gastropoda, extend as 
far as in the Turbellaria, and cannot be directly compared with that of the 
Polyclad embryo, because the radial cells of the latter are to be regarded as 
the rudiment of the mesoderm (Vol. i., Fig. 75 C and £), while, in the 
Gastropods, they are ectodermal. The radial structure in the two cases is, 
however, only apparent, since the axes of the body can early be demonstrated 
both in the Turbellaria and the Gastropoda. In « similar way we might 

» speak of a radial symmetry in connection with the stages of cleavage of many 
other animals. Further, this radial symmetry is very soon lost in the 
Gastropod embryo by the appearance of the paired rudiment of the mesoderm 
which gives the embryo a marked bilateral character. It has, however, been 
asserted (Manvnept, No, 72), that in Aplysia, when the embryo consists of 
eight blastomeres only, the mesoderm arises as four cells through division of 
the four micromeres ; this, if true, considerably strengthens the resemblance 


"(Since this work was published, a large number of observations relating 
to the sy pee in the cleavage of the erie yea egg have been recorded, 
allof which lend additional support to the belief expressed above (p. 106) that 
4 common type or plan could be recognised in the segmentation of the egys of 
all the various divisions of the Gastropoda. 

Thus, it is possible to trace the origin cf the ectoderm in every case to three 
quartettes of micromeres which are cut off successively from the macromeres, 
complication being introduced, in some cases, by the secondary division of the 
first and second quartettes before the separation of the third and last quartette 
from the macromeres, and in other cases, by the lesser development of the 

‘olk and consequent slighter differentiation of the blastomeres, thus making 
it difficult eA identify the macromeres. woe E 

A very striking feature, common to the development of most Gastropodan 
eggs and well shown in Fig. 40 €, D and E, Pas beea tecaned abe taee 
cleavage. Thus, as carly as the third cleavage, é., the formation of the first 
quartette of micromeres, « 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 
Lercreind This “spiral" character is generally more than 
represented in Fig, 40 (, but is well shown in D in the case of the second 
uartette of micromeres, Spiral cleavage is of particular interest in view of 
the fact that, in sinistral Gastropoda, the obliquity takes the reverse inelii 
to that which is found in dextral forms (Cramprox, No, V and Houmes, No. 
XIIa). Fora oes discussion of the significances of the forms of cleavage 
in the Gastropodan egg see Conxiin (No LV, pp, 185-192),—Ep,]} 





a 





CLEAVAGE AND FORMATION OF THE GERM-LAYERS. 109 


to the Turbellaria, but the 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 
Brockasy, who investigated the ontogeny of Aplysia at the same time as 
Maxrnept, saw nothing of this process, and MazzaneLui who, quite recently, 
has made similar investigations, describes the formation of the mesoderm in 
an entirely different way, 





of the germ-layers develop, as in the Amphineura 
very early. In Planorhis, according to Raby, 


110 GASTROPODA. 


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 
off such a small cell towards the centre, so that there are now four 
small entoderm-cells (Fig. 40 #). The posterior macromere then 
divides into two large cells of about equal size (//, mes) and the other 
imacromeres also divide (H, ent). In Neritina, a similar process takes 
place, but the size and position of the cells is somewhat different (Fig. 
40 G, wes and ent). In Crepidula 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 « 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-cayity (@) or else are pressed 
into that cavity later. This latter is the case when, as in Playurbis 
(Fig. 40 H), these cells (wes) 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 results (Planorbis).* Tn 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 cleayage-cavity. In this latter case, 
however, the germi-layers may also already have appeared as rudi- 
ments. The macromeres next give off at the vegetative pole a few 
small cells (G and HH, ent) which, together with the former, repre- 
sent the rudiment of the entoderm. The rudiments of the three 
germ-layers are now visible; the ectoderm has arisen from the micro- 
meres, the entoderm 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 Limaa, and Koro 
(No. XTV) thinks that this cavity is connected with the excretory of 
the blastomeres. The cavity is most developed in those Gast in which: 
the gastrula is embolic and, during invagination, it becomes temporarily 
obliterated, but re-appears later (Planorbis, Rant, No. 90).—Ep. 

+ (It will be seen that if the interpretations given on p. 107 of the relation 
between the first and second cleavage-planes and the axis of the adult body 





CLEAVAGE AND FORMATION OF THE GERM-LAYERS. di 


‘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 
reseinblance. 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 Prosobranchia, Fissurella (No, 12), 
Neritina (No. 7), Crepidula (Nos. 24 and 25), Bythinia (Nos. 91, 
101 and 28), Vermetus (No. 99), Fusus (No. 11), Entoconeha (No. 76) ; 
among the Heteropoda, Firoloida and Pterotrachea (No. $1); among 
the Pulmonata, Plaworbis (No. 91), Limnwea (Nos. 130 and 131), 





Fr, 4. Jn the clenvage of Covolinia tridentata (A) and Aplysia ti B 
ations Rupes) Fra Tecan pane Ariveia femacina (B 
: and the polar bodies 


Limex (Nos. 130 and 73), Onchidinm (No. 51); among the Opistho- 
Dranchia, Voto, (No. 91), Ercolenia (No. 124), Tethys (No. XXVI), 
Uabrella (No, X11); among the Pteropoda, Cavolinix, Cyynebutia 
(No. 32), Clione (No. 55). 

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 Cymtuliv, 


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. [1 seems further ble that the first mesomere arises from the left 
| macromere in and from the right in sinistral Gastropoda. In 
| ;, of the large amount of evidence which is accumulating in favour 
| ‘view we must, when we consider the great difficulty in tracing the rela- 
the early cleavage-planes, wait for further observations, especially on 
rs before we finally conclude that this origin of the mesoderm is 

‘ypical of all a, See footnote, p. 119.—Kp.] 





112 GASTROPODA. - 


for instance, one of the four macromeres is markedly smaller than the 
others, although the cleavage, in other respects, follows the usnal 
course (Fig. 41 A). At the four-celled staye in Aplysia, two blasto- 
meres are distinguished by their smaller size, a difference which can 
be recognised in the later stages also (Fig. 41 2), Although the two 
smaller macromeres are still visible at this stage (8, 77. and /V.), yet 
in later ontogenetic stages, only the two larger ones are still distinet, 
and these are apparent until grown over by the micromeres (epibolic 
gastrulation, Ray LANKESTER, Chap. xxvi., Lit, No. 29; MaNrREpi, 
No. 72, Buocumann, No. 8). Another Opisthobranch, Avera, re- 
sembles Aplysia in this respect (RaBL, No. 91). 





Fig, 42,—A-£ stages of cleavage in Vasa mutabilis (after Bonnerzky from BaLvoun's 
Text-book), A-C, formation of the macromeres, on which, in, four, and in A « 
large number of micromeres lie, 


‘The first stages of cleavage, in Nassa mutabilis, are very striking 
and peculiar (Bosretzky, 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 ovam 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 
this case not attained to any great size. This condition soon dis- 





THE FORMATION OF THE GERM-LAYERS, 113 


appears, the yalk-sphere fusing with one of the blastomeres (Fig. 42 
B); 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 C) 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 dise or cap upon the four macromeres (Fig. 42 2). 
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. 
Tt 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 (Sepenna, No, 115) and in Uyo- 
ealpine (Broors, No, 17; Corgis, No, 24), forms which in their 
ontogeny seem to resemble Naas. 


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 
swith the variations in cleay- 
age. In the simplest cases, Fig, 43-—Blatalastage of Patlla (ater 
tively large cleavage-cavity 
“arises (Fig. 43). The vegetative pole of the blastula is formed by the 

1 





114 GASTROPODA. 


macromeres and consequently appears much thickened. After the 
mesoderm has become differentiated, the entomeres begin to increase 
in number (Fig. 40 H,+nt), and the whole entoderm becomes in- 
vaginated into the cleavage-cavity, and thus a typical invagination- 
gastrula forms (Planorbis, Rabu). 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, No. 83). 

In a few Gastropods, such as Bythinia and Limnuea, a cleavage- 
cavity is present at an early stage, but this soon disappears; the 





WH. 
Fic. 44 —.1-C, embryos of Firnluida Desmuresti in the stage of gastrula-formation 
(after Fou). 4. blastopore ; raf, ectoderm ; rk, polar 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 
(Ray Lankester, No. 63: Wotrson, No. 131; ERtancer, No. 
28). Gastrulation follows the same course in Paludina, with the 
distinction that, in this form, the cleavage-cavity is from the first 
very small, and the mesoderm only later becomes recognisable 
(cf. p. 134, Biirscuit, No. 18). In the Heteropoda also (Firoluida 
and Carinuria) 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 


THE FORMATION OF THE GERM-LAYERS. 115 


to the gustrula (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 C), and the archenteron thus 
represents a wide sac (Fou, 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 
A), But even here an invagination takes place. The middle ento- 





a 
45.—A and B, embryos of Clione limacina showing the formation of the germ- 
Kexrowrrsen). 61, Seep ect, hater eta ose ntoderm ; se, Pe 


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 

(Fig. 45 B). A similar process was described 
in connection with the Lamellibranchia (Ostrea, p. 27). 

“The gastrula arises by epibole in Fueus (Boprerzxy, No. 11), 
Aplysia (Buocumans, No. 8), Crepidula (Conxti, No. 24) and 
Vermetus (Savensky, No. 99). In these forms, the ectoderm, as a 
thin Tayer, surrounds the four yolk-laden macromeres, from which, 
‘at w later stage, small cells become detached, chiefly at the vegetative 
pole, that is, in the neighbourhood of the blastopore ; by the deyelop- 
‘ment of these small cells an archenteron is formed, bounded dorsally 
‘by the four macromeres and ventrally by these small cells. In Neri= 
tina, these cells form early, before the circumerescence of the macro- 





116 GASTROPODA. 


meres has proceeded so far (Fig. 40 G, ent). According to BLocuMANN 
(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 
entoderm-cells and 
partly by the mac- 
romeres. eritina 
in this point more 
nearly resembles the 
forms considered 
above, in which there 
was a transition from 
; an epibolic to an in- 
Fro. 46.—Embryo of Neritina sluciatilis in optical Vagination - gastrula. 
section (after LOCHMANS). Al, blastopore ; ert, ecto- A capofmicromeresat 
derm ; ent, entoderm ; mes, mesoderm. 
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 Uroralpins, Fulgur, Purpura and Nasea also, gastrulation takes 
place through epibole (Brooks, No» 17; McMurricn, No. 70; 
Bosretzky, 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 mutabilis 
the one of these forms which has received most attention, as well as 
in Urosalpine and Purjnra, 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 FE). When the micromeres grow out towards the vegetative pole, 
the three smaller macromeres also take part in the process of shifting 
and in so doing increase in number (Fig. 47 B, hy). 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-dise (Fig. 47 B). As far as can be seen from 





EE 


THE FORMATION OF THE MESODERM. 117 


Brooks’ description, the entoderm forms in an exactly similar way 
in Urosalpine. A mass of food-yolk is also formed in Fusus, Ver- 
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- 












A 





eel sections tl sh embryos of different ages of Nass muta- 

‘Bonnerzky, from BaLroun's Text-book). 6/, blastopore ; ap, ectoderm ; 

Sees hy, entoderm ; in, intestine ; m, mouth ; me, mesoderm ; 
shell-gland ; enteron, 


* divides, giving rise to un entomere and to the primitive meso- 
which latter eventually yields the two primitive mesoderm- 
as already shown (p. 110), These are soon pressed into the 
ity, and, by their increase in number, give rise to the 
ape eemotierns-bands. This seems also to be the case in the Ptero- 


© 8 [This coll is believed to be homologous in all Gastropods and is now desig- 
“nated D by studente of cell-lineage.— wt. J a 





118 GASTROPODA, 


poda (Clione, Kxreowrrscn, 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. Kxrrowrrscr conjectures that in those 
Pteropoda in which, according to Fon, one of the macromeres is 
distinctly smaller than the others, this smaller macromere yields the 
primitive mesoderm-cells (Fig. 41 4, ///). 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-#), 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 A). 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... it divides into two cells, one of which remains as an entomere 
in the position oecupied 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 (y. ErnancEr, No. 
28). The mesoderm rises in a similar manner in Crepidula (CONKLIN, 
No. 24) * and Neritina (Buocumann, 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 Weritina, 
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 m) 
arise through the division of one of the posterior macromeres (A and 
B). This primitive mesomere divides into two laterally placed meso- 
derm-cells (C, wm) which soon give rise to the two mesoderm-bands, 
formed of a few large cells containing yolk and other smaller cells 
(D and E£). The rise of the mesoderm from one of the posterior 


*(Conxuis (No, IV.) now finds that, in Crepidula, the mesoderm ae ae 
arise until after two further divisions, but regards this as an 
dition,—Ep,] 


120 GASTROPODA. 


the mode of formation of this layer in Nossa as given by BoprerzKy 
(No. 11) to the method described above. In sections made through 
such a stage in the egg of Nussa (Fig. 42 £), 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-vells and, since the cells 
from which they were abstricted evidently correspond to one of 
the smaller macromeres (Fig. 42 #), the mesoderm has an origin 
similar to that in the cases previously considered. The smaller 





Fie. 48.—A-#, a few stages of the cleavage and formation of the i-layers of 
Umbrella {afer Heymons). A shows the four macromeres ; F, {he ‘Uvicios of the 





fo 
ect, ectoderm ; ent, entoderin 5 Rly the: primitive mesomere ; mesoderm ; ram, the 
pained mesodermn-cells (mesodermal teloblasts) resulting from the division of #, 


mesoderm-cells at first present soon again divide (Fig. 47 A), 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 (Woursox, No. 131) and Fulgur (McMcrrice, No. 
70), and Janthina, in which form, according to Happow (No. 40) it becomes 
Separated from the macromeres at the top of the blastopore, At a stage ip 
which the ectoderm-cap has not completely grown round the macromeres, the 
peripheral macromeres yield the mesoderm-cells. Happox'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 Janthino. There are also various 
other descriptions of the origin of the mesoderm in the Gastropoda which, as 
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 (Parren, 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, however, according to 
Parren, a cell arises on each side of these four blastomeres which, 
by division, gives off into the cleavage-cavity another rather large 
cell. These two cells are regarded by Parren as mesentoderm-tells 
(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 Parren, developed with special 
regularity in Patella (Figs. 51 and 52, p. 126). 

‘The mesoderm, in the Gastropods, has generally been considered to arise in 
eonnection 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 Molluses showed no sign of the formation of enterocosles, 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, show great agreement with certain ‘ Enterocoelia," and there is no doubt 
‘that, like these, they possess a secondary body-cavity, but, in this respect, they 

‘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 cannob 
agree with the results obtained by Ertancen 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), 

y. Exnaxoen's account is as follows: From the rather wide archenteron of 
“Paiudina a bilobed outgrowth appears which gives the impression of a double 
eoelomie sac such as occurs for instance in various Echinoderms (Vol. 1., pp. 
407-409). This sac, which rises from the archenteron near the blastopore, 
‘becomes detached later from the entoderm and now represents a vesicle 
@losed on all sides and symmetrical in form, The outer and inner walls 
‘approach the ectoderm and the entoderm respectively so that at this stage 

‘speak of a somatic and a splanchnic layer, It is evident that, up 
point, the condition of the mesoderm closely resembles that of the 
sacs in otheranimals. This, however, soon changes, for the coclo- 
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 Termetus (SALENSKY, No. 99) and 
in various other Gastropods (For). 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 SaLensxy, 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. Sazensky 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. 
Sarasix (No. 101) of the origin of the mesoderm. According to SaRasix, 
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, SanasiN 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 
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 SARASLN, we 
should have to show whether, besides this distinct mesoderm-rudiment, 6 
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 P’aludina must still be regarded as undecided. In his 
most recent publication, ERLANGER (No. X.) 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. 

‘SNNIGES (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- 
arycoelom. Scuwipt (Nos. XX. and NXI.\, who has confined his attention to 
Pulmonates, finds no support for ERLAS| iews in the origin of the mero- 
derm of these forms. _An investigation on this point in some of the primitive 
Prosobranchia is very desirable. —Ep.} 




















THE RISE OF THE LARVA, ETO, 123 


bas been assumed or conjectured in connection with other forms (Annelida, 
Echinodermata) and specially for the Mollusca (cf. Cyclas, p. 29). It must be 
regarded as a striking fact that even those zoologists who, like Ertanorn, 
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,” ic, am accumulation of specially 
large ectodermal cells, pass inward so as to become distributed in the con- 
Weetive 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 various divisions are somewhat far- 
reaching, so that we are obliged to consider the different larval forms 
upart. We shall first, however, describe the development of a few 
specially forms so as to give the reader a general 
‘idea of the subject and to make possible a comparison with other 
| tlivisions of the Molinsca. 

The development of the larval form of Patella has been deseribed 
‘in detail by Parren (No. 83), and since this Prosobranch, which 
telongs 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 Parren up to a stage at which the larva is still far removed from 
‘the shape of the adult. 
of Patella shows primitive conditions in so far as 
is thrown off very early, even while cleavage is still 







fhe aboye somewhat conflicting accounts of the rise of the mesoderm, 
im cont ion with the more recent observations of ConKiin (No, IV.), 
(0 oe ), and Wrerzessk1 (No. XXVIL.), seem to render it highly 
a ae Sane aaeet layer has, in all Gastropoda, os has 
hia, a double origin: (1) from primitive 
sing oven to the lateral mesoderm-bands ; and (2) from 
stage as paired differentiations nearer the anterior 
the body.—Ep.] 




















124 GASTROPODA. 


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 
alarva. In this way, Patella resembles a Lamellibranch, but such 
early locomotion is not common among the Gastropods, most of the 
larvae hatching at a much later stage. The ingrowth of entoderm 





Flos. 49 and 50,—Embryos of Patella at the blastula-stage and at the commencement 
and comple gastrulation (after PaTTRN). 8/, blastopore ; em, mesentomere ; 
ent, entoderm ; mex, mesoderm ; sd, sbell-gland ; 17, 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 OF 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 50). In later stages, the dis- 
placement of the blastopore becomes much more striking, and recalls 
the condition already described in connection with Dentalium (Figs. 
34 and 36, p. 91). The blastopore, during this process, changes 
from its round form and becomes slit-like (Fig. 51 8). At its 





Bei eettateat petal vets can be oes ear the coeslsr Uincapore Ts Bie 

Rope agitate. Near ié cen to recognised the xndimenta of the two 

‘hind it the anal ciliated eet 

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 
earried inwards by a depression of the ectoderm, the stomodaeum, 
which occurs at this point. This depression represents the rudiment 
of the oesophagus (Fig. 50 /), the blastopore persisting as the opening 
etween the stomach and oesophagus. Out of this solid mass of 
cells, which still represents the entoderm, the enteron forms later 


be 


126 GASTROPODA. 


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. 

Parren asserts that the foot arises at a very early stage in a 
remarkable manner. It is said to be produced from two prominenees 
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 donble 
origin of which can be 
recognised even in later 
stagesthrough thepresence 
of a median groove, 

Up to this stage, the 
pre-oral region was speci- 
ally large and bell-shaped 
(Fig. 51). It is separated 
aera from the posterior section 
Mio, Pua ater Protas). "a, ciated anal PY the pre-oral ciliated 

osetia aa mesoderm ; 4, spit 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, *), now takes up # 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 aboye- 
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 eup- 








THE RISE OF THE LARVA, ETC. 127 


shaped. The somewhat swollen edge which is seeu bordering the shell 
represents the margin of the muntle, the mantle itself being covered 
‘by the thin horny shell. The enteron has considerably widened and 
is now suc-like and, connected with it posteriorly, a pointed appendage 
can be seen; this unites later with the ectoderm to form the anus. 
In the stomodaeum, which has now enlarged, an outgrowth (r) is 
visible ; this is the rudiment of the radular sac which was found to 


i 
i 





uu 
[ 


Hl 


f 





ty Fyo, 53.—Median longitudinal section through the 
Prominence and in Eat a hal ore stage (after 


4, the ciliated homey at the post 
feo Ba month mul, enteron ; mes, 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 musele-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 proper size. 

Tn 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 Tvochophore stage met with in the 


la 





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 
aleo (Ray 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 organisation 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 Crepidula, 
Fulgur, Faseivlaria and other Prosobranchia, as well as in Heteropoda, 
Opisthobranchia and Pteropoda (GEGENBAUR, Kroun, Fou, Brooks, 
McMorricu, 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,,, 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 (1): 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 (¢/. 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 im 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, Palu- 
dina, 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. Eruancer, 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 (Palwiina, Fig. 59 B, un, p. 139) 
or else longer, as in Planorbis, in which case each kidney consists 
of a V-shaped tube (Fig. 78, un, p. 177). 

Besides the primitive tubular kidney, various groups of ectoderm-cells have 
been claimed as primitive excretory organs. Bopretzky thus interpreted two 
rounded cell-growths which appear near the rudiment of the foot, Similar 
organs have been found by McMurstca in Fulgur (No. 70). Sanasin de- 
seribes, in Bythinia, ectoderm-cells of exeretory nature which are connected 
with the velum. (In Crepidula, Conxxn (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 Nerifina, such granular cells, which later give rise 
to velar cells, may be clearly distinguished even during cleavage among the mic- 
romeres (BLocuxAsn, No. 7). Two rows of granular cells which liealong the edge 
of the velum have been described in Onchidium by Joysux-Larrure (No. 51).* 


*[(Hermons describes, in Umbrella, the presence of red groups of ecto- 
dermal excretory cells, situated near the aia of ‘hen the right woop 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 
im the Prosobranchia.  Conxur (No. IV.), however, thinks that they aré 
only, since arise from totally distinct blastomeres ; the anterior 

sina eas are found in three of the great Gastropodan orders. 
“MAZ#ARELLI pe rae} who has studied the ectodermal or anal kidney of 


‘that it does not disappear, but represents the rudiment of the definitive 
Ghee internal primitive kidney is so far known to occur only in 
ees eae in two Pestonsker Esoertapelde oe) possibly in es 

concerning which Entanour is unable form us whether 
it was an uh or & Prosobranch, Thus it will be seen that this 
itive organ is found to be most highly developed in those most 
forms, the Pulmonata, and that it is only elsewhere known to 
occur in two Prosobranchs. A further search for this in some of the 
more primitive marine Prosobranchia is much needed.—Ed.) 
K 





130 GASTROPODA. 


It is only in comparatively few Gastropods that the T'rochophore is 
developed in such a pronounced manner as in Patelin, 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 
egg-shell or in the egg-capsule. The Z'vochophore stage is neverthe- 
less to be found in all Gastropods, although it is more distinet 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 T'rochophore, so that we may 
assume that it does mot undergo any further changes except those 
which are determined 
by its transformation 
into the adult. This 
also seems to be the 
case in Fisswrella as 
far as its develop- 
ment is known 
(Boutax, No. 12). 
In this Gastropod, 
the velum broadens 
somewhat and as- 
sumes « bilateral 
} form. This was also 

. A already described in 

"Sjchlemuon{f fou; ol aperture; pp para, the Lamellibranch 

ea tte iene: ad a larva, and Fiseurella 

does actually show a 

certain resemblance to the later stages of these forms (Fig. 17, p. 35), 

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 Fixsure/la is, in those Prosobranchs the eggs 
of which are rich in yolk (Neritina, Vernetus, Fulgur), evident when 
the velum first appears as a rudiment. This organ appears in the 
embryo at first in the form of two specially marked réws of cells 
(Neritina) or two curved ridges which unite only later to form the 








EE 


THE VELIGER LARVA. 131 


yelum, 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, und Pteropoda, the velum by its 
great lateral growth, assumes a bilobed form (Fig. 55 4-C), It 
hecomes 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- 


a B 





Pro, 56.—A, embryo, B and C, Velirer larvae Ch peat tn rioieg 
A, dorsal aspect; 2, ventral aspects O; lateral aspect 
fr é rudiments of the cerebral ganglia; f. foot; m, wonth; of, otocyst; op. 

{4 shell, ¢, 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 (RAY LANKESTER). ‘The 
‘great size which may be attained by the velum can be seen from 
_oapreoes represents the Veliger larva of a Prosobranch (species 





— 


132 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 eo 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 (c¢/. 
p. 146). 

The rudiment of the foot appears early and may attain large pro- 
portions in the Veliyer 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, Ray LANKESTER, 
No. 63; Succinea, F. Scumipt, 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 C, op). This is the 
operculum. The otocysts lie in close contact with the foot (B, vf). 

In the young stages of the Veliyer larva two prominences appear 
on the velur area ; these soon extend and lengthen and can be recognised 


THE VELIGBR LARVA. 133 


‘os 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 to the primary cephalic section, and it is of special 
imterest 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 deaced 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 persist near the mouth as the remains of the velum, as was 
observed by Ray LANKEsTER in Limnaea (No. 63), and Joynux- 
Lapeure in Onchidlinm (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 Veliyer 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 (WVermetus), 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 (CLararéps, 
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 
Veliger stage, suggest that it has only recently adopted a fresh-water 
existence. In other fresh-water Prosobranchs, as well as in aquatic 
and terrestrial Pulmonates, the Veliger stage is much reduced, 
Onchidium, however, among the Pulmonates, in this respect resembles 
Neritina. 

- Onchirlinm, a Pulmonate living between tide-marks, not only passes 
through a Trochophore 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 egg-shell has, on the whole, the same shape as the parent 
Goveux-Larrvir, No. 15). The condition we have just described 
would be very remarkable ina Pulmonate, did not the organisation and 
the manner of life of this form give some cause for the assumption 


ae 


134 GASTROPODA. 


that it may have been derived from a marine ancestor (possibly an 
Opisthobranch). Onchidium lives in the littoral zone, within the reach 
of the tides, hidden in rocky fissures, where it lays its gelatinous 
egg-masses, These are washed by the sea water, and JoyEux- 
Larrure 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 Veliger stage is much reduced in fresh- 
water and terrestrial Gastropods, the 7rochophore form is still more 
or less distinctly developed in them. In the Pulmonates, the 
Trochophove stage is present but is not very conspicuous (p. 177); 
in Paludina, however, it is unmistakable, although this Gastropod 
is viviparous (Fig. 56). Palwdina, 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 Leypie (No. 
68), Ray Lankester (No. 64), Biirsontr (No. 18) and vy, Exuancer 
(No. 27), and we have also observations made by Rasu (No. 92) and 
Brocumany (No. 8), Ertanaer’s account is the most recent and 
the most complete in every respect. 

The Development of Paludina. The fertilised egg of Paludina 
viciyara develops into an almost spherical blastula which becomes 
somewhat flattened later and contains a distinct cleavage-cavity. 
The flattening takes place in connection with gustrulation, the 
cleavage-cavity during this latter process being almost completely 
obliterated by the development of the archenteron, 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 
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 Bitrscutt, 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), ie., show the same condition as in other Gastropods 
(ef. 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 DEVELOPMENT 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 (Birscxt, v. Enuancer). It has, however, 
beon 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 (cf. p. 141).* A large, somewhat sunken 





Fie, 56.—A frontal and B sagittal section of two embryos of Paludina of different 


ages m, Tegion where the mouth develops at a later stage ; 


; mes, 
bands (im My and scattered mesoderm-cells (in B); sd, shell-gland ; vd, 
vy, velum, 


area, which lies dorsally in front of the blastopore and consists of 
columnar ectoderm-cells (Fig. 56 B, ed), represents the shell-gland, 
above which the chitinous shell soon appears. An ectodermal de- 
pression (1) which appears on the ventral side behind the ciliated 
ting, and 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 8). 
The mesoderm has lost its regular arrangement and has become for 


* (Téwmiers (No. XXV.), the most recent investigator of the development of 
Paludina, finds that the oval biastopore closes trom before backward, and 
‘What it does not give rise to the anus, which, as a secondary formation, appears 
‘st the point where the blastopore closes —Ep.] 


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 « 
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 sornewhat, 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 Byt/inia, this ectodermal invagination is even very 
deep and forms the longer, distal part of the primitive kidney (v, 
Exvancer). 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 eom- 
municates with the (primary) body-cavity (p. 179). v. ERLANGER 
was 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 (Bitrscxut, 
vy. ERLANGER). 

The Trochophore form of the embryo is now specially 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 Band 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. Ertancer (No. 71), however, describes an internal aperture in 
Pulmonstes. Mutssensemer (Nos, XVII. and XVII.) has made a most 
careful investigation of this point in Lima and is firm im his belief that 
there {s no internal opening in that Pulmonate. He derives the entire 
organ from the ectoderm.—Ep.] 


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 Biirsonnr 
(Fig. 57). During the further growth of the embryo, the gland 
‘becomes flattened out and its cells lose their long columnar character 





Pros. 57 and 55.—Sagittal section of two embryos of Palwdina vivipara (after Ton. 
SIGES). a, anus; enf, entoderm; /, rudiment of foot; /, rudiment of liver; m, 
{ tad, enteron ; mes, mesoderm-cells ; w/, tirst indications of the mantle-fold ; 

A sheli-gland; f, shell-groove ; v, 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 mautle-fold (Fig. 58, m/), 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 A), 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, mh). 
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 
(Bythinia, 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. Birscxri bas 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 


THE DEVELOPMENT OF PALUDINA. 139 


subject of the asymmetrical shape of the body will be alluded to 
further on (p. 143). 








vanes ina, vivipare of different (after v. Sem 
eyes foot; ear: ¥, Ser; de eft peri sac; m, mouth ; mé, 


of the mantle; na, eflerent 


eee 


It bas already been mentioned that the anal aperture lies im the 
mantlecavity. This latter has deepened during the processes just 


Aa 





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 8), and, finally, in consequence 
of its one-sided growth, becomes coiled (c/. 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 (o/) 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, op, and Fig. 
92, op). 

The tentacles arise on the yelar area as two very large swellings 
which soon increase in height and thus become conical (Fig. 59 4-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 determimed 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 yegetative pole; 
this aperture, without undergoing essential change 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 Bosrerzky for Fusus 
and by For 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 Vaxsa and Neritina (BonsetzKy and Buocumann). The pot 
at which the blastopore closes and where the adult mouth eventually 
forms, no longer corresponds to the vegetative pole, ie., 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, Palwfina and many other 
Gastropods). The slit-like blastopore closes from behind forward, © 
and its anterior end either passes direct into the mouth, as in Plan- 
orlis, Limnaea, and Patella (according to Rasy, Ray LAnKEsTer, 
Wotrson, Parren) 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 
Orpidula (BLocumany, Sanasry, y, Exvaxcer, Conxnry). 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 

x by means of the view adopted by Btrscunt, according 
te which both the mouth and anus arise by the differentiation of the 
Blastopore. Biirscxt: 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 
anus and the blastopore. v. Ertan, for instance, described the 
blastopore of Bythinia 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 
Palwdina itself it appears indisputable that the slit-like blastopore 
extends almost to the velum, #.v., 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 (Doris, Aplyxia, 
according to LancrrHans and BLocumann), 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 month 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 
Dlastopore 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 theother. 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 eondi- 
tion of Paludina may recal] 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). Tn the latter, the 
Dlastopore 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 blastopure 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 
wuimal 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 

107). The identification of these axes is by no means easy, especi- 
Wiis shape of the larva undergoes « certain amount of modifi- 
eation according to the quantity of yolk deposited in the egg, On 
this account, Fon’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 arederived 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 body. It is especially 


“(Por a review of the facts relating to the shifting of the larval axes see 
@oxxtax (No. TV.) and Lrutae (App. to Literature on Lamellibranchia, 
‘No. II).—Ep.] 





144 GASTROPODA. 


the left side that grows more actively, and this is the reason why the 
posterior parts (especially the anus and the organs surrounding it) 


B. €. 





Fro. 60,—.1-4, Diagrams illustrating the displacement of the pallial complex and the 
manner in which the asymmetry of the Gastropod body was developed {constracted 
after BOrscHit and Lana}. ‘The pallial complex shifts first to the right and then for- 
ward. In £, 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. a, anus; ao, anterior aorta; og, cerebral 
ganglion ; f, foot ; k, gills; 1m, mouth ; 1, renal aperture ; peg, pedal ganglion ; plg, 
pleural ganglion; r. edge of the mantle and shell ; tc, 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 
does not grow. These phenomena have been described by various 
zoologists who have treated of the ontogeny of the Gastropoda (P. 
Sanastx, For, Boprerzxy, ete.).* Spencer (No, 122), also, has 
made them the subject of detailed consideration in adult animals, 
and more recently Bi'rscuut especially has given a careful descrip- 
tion of them (No. 19). Lana 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 
im 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, Ci ifon-like Molluse, 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 A). 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 (Biirscan1 
and Lane). 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 (2), as in 
the Prosobranchia (including the Heteropoda), the pleuro-visceral 
commissures become crossed (chiastoneury, streptoneury, Fig. 60 £), 
@ condition not found in the two divisions mentioned above, and 
indicating a specially high degree of asymmetry.+ 


*(It is manifestly impossible in a work of this nature to review all the 
aka theories relating to the etry of the Gastropoda. The views 
adopted by our authors are those of BirscHii and Lana, but the reader should 
consult Smmorn's account of the Mollusca in Brown's Klass. u. Ordnung, d. 
Thierreichs, Ba. iii. Lief. 22 u. 23, 1896, where an excellent summary of 
both the earlier and the more recent views, including those of PersENRER and 
Puate, will be found.—Ep.) 

+[In Actazon, a form which, in spite of its uliarities, must be regarded 
Aa ee allied to the Opisthobrancha we find that pleuro-visceral 
connectives & streptoneurous condition, and in certain other forms 
also (Philine, Aplysia, foneurous condition is also found in the 


etc., a strep 
Poritoae eae Oesiina) ‘an indication of this condition is to be seen. The 
met in these forms is thought to be a highly specialised one, 
7 


— 


146 GASTROPODA. 


The cause of this asymmetry is to be sought in the manner of life of 
the Gastropoda, i.e., in the development of the foot ax a massive creeping 
organ and in the simultaneous development of the shelly covering of the 
dody. At first the visceral mass was fairly equally distributed over 
the body, which was covered only by « 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 und 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 ofthe 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, Tf 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, 
Jay 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 sae, 
and the forward displacement of the anus then follows-(¢/. 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 (ie., the Huth; are to be 
derived from the Prosobranchia after the latter attained the streptoneurous 
condition. If this is the ease, 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.—Ep.) 


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. Lane, in this way, traces back 
the absence of the organs originally forming the left purt of the 
pallial complex (the left gill and the left renal aperture, etc.) which 
is to be noticed in various Gastropods (#.y., 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 
eases (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. Lan 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 sume in the two cases. The causes that lead to the inclination 
to one side or the other are difficult to determine, indeed, at the 
present time, they are hardly known,+ 

Some of the sinistrally twisted Gastropods have their inner orgars 
arranged in the same way as the ordinary dextrally twisted forms. 
Tn 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- 
Bora, ¥. JuERtNG, Lana, No. 61). An indication of such a process 

development of the gills is very marked in Pleurotomaria, 
Uttar bere left) gill being much the shorter of the two; this is the 


sence Diseerie eg in the Monotocardia, Curiously enough the kidneys 
Hatiotis, Patella) show exactly the reverse condition 
to th iat a seen in the fees tee wile 


the right (primary left) kidney is much larger 
AE nevertheless, it is apparently the latter 

eddie which persists in the Monotocardia.—Ep.} 
+ [See footnote, p. 108, on the cleavage of the egg of sinistral Gastropods.— 






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 
(Prtseneer, 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 Planurbis 
corneus, 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 
ereeping 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 Onehidium and the 
Limacidae, 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 Trochophore 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. 

Tt has already been stated (pp. 112, 116) that the eggs of many 
Gastropods are very rich in yolk, and this influences not only tho 


* Cf. pp. 123, 131 and 134 on the development of Patella, Vermetus and 
Paludina, 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 case, for instance, in Vassx, Pasis, 
Fulgur, Natica and others. Even in Vermetus, the Veliger stage of 
which we became acquainted with (Fig. 55), the T'rochophore form is 
no longer distinctly developed. The velum appears at first in the form 
of two wavy cell-bunds 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 
& 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 toa far greater extent when the egg is still richer in yolk, 
as, for instance, in Pulgur (McMurricn, No. 70). The first rudi- 
ments of the organs are here so crowded together that we might 
almost speak of a germ-dise in contrast to the large yolk-mass of 
the egg. We should then see the commencement of processes which, 
in « fur higher degree, will be met with in the Cephalopoda. Thus 
im 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 &, 
p- 112, and Fig. 47 A and A, p. 117. If we compare these figures with 
those of the blastula and invagination-gastrula of Putel/a (Figs. 49 
and 50), Plaworbis or Paluedina, it is evident that these altered condi- 
tions must bring with them modifications in the external shape of 
the body. 

In Nossa motabilis, 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 
by cells (Figs. 61 4, b/, and 47 C, bp). This is the blastopore which 
closes later, the stomodaeum arising in this region (Fig. 47 D, m). 
Iu Fuss, the eggs of which exhibit « similar condition, the blastopore 
is said to persist and to pass over into the mouth (Bosrerzky). 
‘The foot appears very early as a broad swelling behind the blastopore, 
even before the rudiment of the velum has arisen (Fig. 61 4, /), 
Neur it lie the groups of ectoderm-cells (ez) which have been claimed 
4s an exeretory apparatus (external kidney). The velum (x) appears 
in front of the blastopore, advancing from the ventral to the dorsal 
side. 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 Vassa, in a species of Fueus examined by Boprerzky. 

Tn 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. €. 





Fra, 61.—A-#, embryos of Nasea. mutabiliv of different ages (after BOBRETZKY). 
Diastopore ; «, posterior tubnlar portion of the enteron ; dr, yolk; er, group 
ectodermal excretory cells ; /, foot ; fd, peilal gland ; A, rudiment of the heart 5 
posterior hepatic lobe, near whick can be seen, to the left, the anterior hepatic Tol 
and above the latter the intestine () and the anus ; 2, rodiment of gill; &h, 

vl 


A, 


cavity ; d, larval heart ; op, operculum ; r, margin of the shell (s) ; », velum. 


part of the embryo. This swollen part, which corresponds to the 
pre-oral section of the Tyoehophore 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, A/, and 81, 00). 
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—PROSOBRANCHIA. 151 


enteron is seen to be open towards the yolk (Figs. 47 Cand D, 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 D, and 62, md). The latter is ut first 
pérallel 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 @). Ata 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 D and £). 
Here also the pallial 
cavity arises as a sickle- 
shaped depression of the 
ectoderm, this cavity in 
Navsu being altogether 
restricted to the right 
side of the embryo. The 

seems still 
more marked here than 
in Paludina (p. 138). 
‘The shell also shares 
in this asymmetry; by 





(Fig, 61 D) The py, 62,—A, surface view, ant 8, median I tudinal 
cperoulum appears as a setion rose an entre ot er alt ci 
delicate plate in the i, liver; m, mouth; wd, enteron; mg, stomach 5 
posterior oral part of cuit; tal ees tau 
To the foot can be seen a ventral tubular ectodermal depression, 
which is no doubt the rndiment of the pedal gland (Figs. 61 F 
and D, 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 noteh 
(Fig. 61 @). It at the same time increases in size and thus assumes 
the bilobed form which we have already described in connection with 


152 GASTROPODA. 


other Gastropod larvae. Massa now shows a strong general resem- 
blance to such larvae, as is evident from Fig. 61 £. This is also the 
case with #usws, the embryos of which also at first deviate in 
several points from the usual shape and resemble those of Vassa.! 


Bosrerzky 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,” 
which has also been found in other Gastropoda (¢g., by Sacensky in 
Calypiraea, No. 98). This larval heart (Fig. 61 F, Ji) is said to be part of 
the eotoderm 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. 


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 miralili« 
described by Jon. Mi~uer 


Pe ity carhy of Span 
eeret Troe Birigs Totton, attached to the wall of the 
imagers soamictt wt ciemy intestine, ‘The only of this 
from the yolk which forms the posterior animal has the form of a long 
Pattar the embryo. cov: cepbalicvesicle;  vermiform oiled tube which 

in no way recalls that of a 

Gastropod, but its brood-cavity contains embryos very like those 

of other Prosobranchs. These have a velum (not, it is true, very 

highly developed), « spirally coiled shell, a foot with an opereulum, 
otocysts, etc. Their further development is not known, but it is 
probable that they live freely for a time, like the young Hnfovaloa 

(p. 43), and only later wander into a Holothurian. 

In explaining the remarkable transformation undergone by Enfo- 
couche in consequence of its parasitic life, two Prosobranchs described 
by P. and F. Sarasix (Zhyca entoconcha and Stilifer Linchiae) 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 case 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 
Stilifer, which has already buried itself deep in the skin. The 
external shape as well as the inner organisation finally undergo, as 
im many other parasites, such a far-reaching alteration, that there ix 
hardly any resemblance left to the former Gastropod, the parasite 
having degenerated into a mere tube, like Hnfocolax or Eutoconcha, ou 
which are devolved the functions of feeding and reproduction alone 
4{W. Votar, No. 129; Braun, No. 15; Scarmmenz, 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), GzGennaur (No. 37), Kronn (No. 
58a) and Fon (No. 31). 

We have already become acquainted with a few of the younger 
stages of the embryo of Firo/oida (Fig. 44 
A-C, p. 114), The oldest of these stages 
was an invagination-gastrula. The inner 
end of the archenteron soon assumes a 
remarkable bilobed form, which recalls the 
enterocoelie formation of the mesoderm as 
deseribed by ExuanGenr in connection with 
Palwdina (p. 121), but which is no doubt 


explained by the fact that the shell-gland Fra, 644—Embryo of Firvloide 


which arises dorsally grows as a conical — Desmmuresti (after Fou), ¢ 
the primary body-eavity ; 9, 








invagination towards ne oe archeteris a iat 
causing a depression in the latter. hen 2 {ook 5, shell gland; 
the shell-zland 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, 0). The shell-gland at first appears filled by « plug 
of brownish substance (#'); in Padudina, where « similar feature was 

or Nucleobranchia, are very generally regarded as a 


* (The 
minor branch of the Prosobranchia, being classed under the Monotocardia as 
« subdivision of the Taenioglossa.—Ev.) 


154 GASTROPODA. 


observed by Birscurt, the plug was said to be expelled before the 
actual shell formed, whereas For 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 4 prominence which widens and thus assumes the form of a plate 
(Fig. 65 B). On either side at its base, the otocysts (of) 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, corresponds. 







Fic, 65.—Embryos of Firolvida Desinavesti. « 
the ventral d, 


to the operculum of the Prosobranchia. Fine caleareous concretions 
become deposited beneath the shell-integument, and lead to the 
development of the caleareous shell. Unequal growth here also 
causes the shell soon to assume a coiled form, at least in the later 
stages. In Ftroloida and Pterotrachea, the shell has only two. 
whorls; in Carinaria and Atlanda it coils several times. 

Up to this point, the alimentary canal is without an anus. 
According to Fox, 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, ae).. 


DEVELOPMENT OF THE EXTERNAL FORM—HETEROPODA, 155 


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 7'rocho- 
plore. Tt then soon passes 
over to the Veliger stage, the 
yelum being bilobed (Iig. 66). 
This bilobed character is at first 
made evident by the mouth 
shifting into a notch of the : A, mdi 
pre-oral ciliated ring. the base of whie a i is visible ; 
So far, the course of de- the lotetantacle teat vention tartoeege 
velopment in the various peasy an aera 
Heteropoda seems to be very similar (Fou). 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 ubout 
asa free larva (Fig. 66), 
circling slowly in the water 


(Groensaur), 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. 
to Krosn, in 
Firoloida and Pterotrachea, ARE 
the yelum becomes drawn out ue 
oa each side into wo Ing Mt des el 
and very narrow streamers, rudiment of the fin; op, operculum ; 0¢, 
Raita presenting an otocyst ; s, shell ; v, velum. 
similar to that of the Veliger larva depicted in Fig. 54, 
p. 130. In At/anta, the velum is drawn out into three streamers 








156 GASTROPODA. 


(Fig. 67), which, however, are considerably shorter than those just 
mentioned. In Carinaria, again, the streamers are longer, and the 
lobes, cut up into three parts, cause this larva greatly to resemble 
that of Firoloida (GuGeNpAun and Kronn). 

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, A); 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 





Fic. 68.—Lateral aspect of a Cerinaria (after SOULKYET feces GsouxaauR}. a, aus > 
ag, sbdominal ganglion auricle; au, eye; ég, buccal ganglion; bin, 
mass; cg, cerebral ganglion; i, intestine ; /, tentacles; fl, fin; &, gill; d, liver; m, 
month vas, stomaaeh we, Kidhay t 3p, petal ganglion 'y, sucker ; sc, shell; sp, 
salivary gland ; #1, tail; tel, oesophagus ; ve, ventricle, 








approaches the form of the keel-like fin of the adult (Fig, 68, jf). 
‘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 Firvloida, is attached somewhat nearer the anterior margin, 
but in Pterofruchea somewhat further back. By degrees this also is 
drawn into the flattened fin (Krous). In some species of Atlanta, 
the fin appears from the first asa 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 OF THE EXTERNAL FORM—HETEROPODA. 157 


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, é.., 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 Oxygyrus in which it 
is independent of the fin 
and lies behind the 
latter (Fig. 69 A). We 
have here great agree- 
ment with the condition 
of some Prosobranchs 





Fie. 69.—A 


B, Strombus, each viewed 


ia, Strombus, from ihe te (er ‘SouzgvEr and Kunean), a, 

« . it iA, posterio foot 5 

Fig. 69.8), in which the $2°sifeatum's \ protoacloy a; sckess se aboll 
posterior part of the sw, tail (most ior section of the foot); #, 


Sea ibi tailor of th anterior part of the foot. 
carrier 1c 


operculum, is sharply marked off from the anterior part. This view 
corresponds on the whole with that adopted by Gr@mnsaur and 
recently especially by Groppen (No. 38), as to the significance of 
the foot in the Heteropoda, 

‘The tail found in the Heteropoda (Fig. 68, se), also arises from the 
foot, in Atlanta as a projection lying close behind the sucker (Kxouy). 
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 


158 GASTROPODA. 


side, a position which is constant in forms like Af/anfa, in which the 
operculum is retained throughout life. The operculum, however, as 
well as the shell, is frequently thrown off during the metamorphosis 

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, f). At 
the bases of the tentacles, the eyes appear. In some forms, the 
tentacles may be reduced again (Pterofrachea), 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, 68). 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 At/anta, which also as an adult possesses a shell, the 
whole animal can still be withdrawn into it. 


©. 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. Sans (Nos. 104 and 105) and 
Lovin (No, 69) established the chief features of their ontogeny, 
while at a later period ADLER and Hancock (No, 1), NorpMANN 
(No. 80), Voor (No. 127), Scuunrze (No. 113), and KerersTein 
(Nos. 52 and 53), occupied themselves principally with the develop- 
ment of the larval forms and of the shape of the body. Ray Lan- 
KESTER (Lamell. Lit., No. 29), Trinonese (No. 125), BLooHMANN 
(No. 8), Rao (No, 93), turned their attention also to the internal 
processes, especially to the earliest ontogenetic stages. References 


DEVELOPMENT OF THE EXTERNAL FORM—OPISTHOBRANCHIA. 159 


to the other authorities on this subject will be found in the literature 
asppended 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-+ The blastopore, at one 
period, is # slit of variable length (e., in Fiona and Llysta, Happon, 
No. 40; Zrcolania, TaincuEse ; Aplysid, BuocuMann). This slit 
loses 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 BLocamann, in 
Aplysia and & similar condition may, according to Voer's account, 
be found in Hlysia. In Fiona, according to Happon, 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 
finally closes. Such a condition can be gathered from the descriptions 
given by Trrncuese (No. 125) and Lanceruans (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 Buocumann. 
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 8). 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 J and J/) 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 — a this oh md have devoted themselves mainly to the 
uaa ot mymons (No. XIT.) and Vicurer (No. XXVI.). 
ens Bo. fa i y is however, made some additional observations on 


Pattee a fo. , who has investigated the early stage in the 
ontogeny of Tila, hes 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 je stages. Umbrella, in its fens me , appears to conform to 
‘the normal type, the process of ent formation is quite 
unlike that described by Buocumann in Aplysia, the yolk being equally 
distributed between the four macromeres and the entodermic epithelium 
arising in a more normal manner.—Ep.) 


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 
isa suggestion of a condition 
intermediate between an 
epibolicandan invagination- 
gastrula, as is said to be the 
case in other Gastropods 
(cf, p- 115), The closure 
of the blastopore and the 
sinking in of the stomo- 
—l of A, limacina in oy 1 alread: il 

Pest ir Beta ian ip owe ira saci 

immediately after thisstage. 
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. TrincHess, on the other 
hand, described, in the deolidac, two large and distinct primitive 
mesoderm-cells which may be traced back, like those of the mesoderm- 
rudiment found by Ruo in Chromodoris, to the macromeres. [See 
the more exact work of Huymons (No. X11.) 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 seereted. 
‘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 Lancernans in several Opisthobranchs (Acera, Aeolis, Doris) 
and had been connected with the formation of the anus; the same 





*(Mazzarecwi (No. XVI.) does not appear to have traced the ultimate fate 
of the two smaller macromeres, but one would imagine, from his ee 
that they form part of the ectoderm. He regards the small entomeres seen in 
Fig. 71 as derivatives of the two lanes macromeres and, judging Sor his Fig. 
12, Pl. x., small cells are constricted off from the macromeres. His observa- 
tions are not clear, but they seem to differ from those of BLocuMaNN.—Ep.] 


DEVELOPMENT OF THE EXTERNAL FORM—OPISTHOBRANCHIA, 161 
significance is aseribed to them by TxixcaEse in the Aeolidae 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, »). Ventrally 
bebind the mouth, the foot appears as a swelling (/); behind it can 
be recognised the wnal cells (az). The shell-integument has already 
developed further. The T'rochophore stage is here less marked than 
im many other Gastropods, as the embryo undergoes certain modifiea- 
tions in consequence of the richer supply of yolk. Such a stage, 
however, has been distinctly recognised by Ray Lankester and 
Trrvcnrse and other observers in Opisthobranchs which have been 





Fre. 71, —Two stages in the development of Apiysia dimacine (after BLOCHMANN), a3, 
Saal cells; eet, ectoderm ; ent, entoderns; #7 loot; m, mouth; mes, imesoderm ; mr, 
mmmrgin of the mantle ; 4, shell’; sf, shell-ziand ; #h, shell-integument ; e, velum, 


investigated by them. An embryo of Aplysia figured by Ray Lan- 
kesTER * shows the greatest resemblance to the embryos of Firo- 
Joida depicted in Fig. 65 A. 

‘The Trochophore stage, by the transverse extension of the velum, 
passes 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 


* (Bee Lit. to Lamellibranchia, No. 20, Pl. 8, Fig. 17.) 
M 


i 


[enna 


162 GASTROPODA. 


The two lobes of the velum are very large and give the larva » 
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 (f) develops an operculum on 
its dorsal surface. We thus find, in the Opisthobranchia, the same 
general condition already met with in the Prosobrauchia and the 
Heteropoda, Although most Opisthobranchs, as adults, are entirely 





Fig. 72.—Veliger larva of an Opisthobranch. @, anus; ad, anal gland (? probably an 
excretory organ, like »);«, alimentary canal! di, divertionlam of the stomach ; /, 
foot ; m, mouth; mm, mascle (retractor of the velum) ; op, operculum ; al, otoeyst | 
#, shell; », 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—OPISTHOBRANCHIA. 163 


withdrawn into it; the retention of the operculum as in Actaeon 
(Tornatella) is quite exceptional. According to Trrxceese, the 
larval shell in some forms (Saceoglossa) shows « 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 (whieh 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 Trinciese, falsely been regarded by several 
observers as a heart, The so-called larval heart which has been described 
iu connection with the Prosobranchia (Nassa, Fig. 61 E, lh, 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 
&s excretory organs chiefly because they are filled with strongly 
refractive concretions. They seem never to possess efferent ducts.* 

‘The views taken of the excretory organs of the Opisthobranchia seem 


‘to us to be somewhat confused. Tarxcuesz, for instance, has described a 
or unpaired sac-like gland with a longer or shorter efferent duct which 


*(r ‘appear to be ectodermal in origin (Heymons) and analogous to the 
‘ anal kidney of the Prosobranchia (p. 129 and No. XV.),—Ed.} 


am 


| 


164 GASTROPODA. 


opens out near the anus as an anal gland. In Hrcolania, this gland is un- 
paired and strongly pigmented. A glandular structure described by Ruo in 
Chromodoris is said also to open near theanus. This involuntarily recalls the 
rudiment of the kidney of the adult, a view which has recently been adopted. 
by Mazzangnui (No. 74 and No, XV.). This author derived similar structures 
from the mesoderm. Oue 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- 
Dorarers and Provor, 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 Mazzareuoi, as already mentioned, it is 
derived from the mesoderm, but Lacaze-Duruiens and Pruvor, 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 Prosobranchia, 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 Opisthobranchs are 
better known. 


Among the sensory organs of the larva, the large otocysts wt the 
base of the foot deserve special mention. As in other pelagic larvae, 
strong cilin appear at the ceutre of the velar area in various forms 
(Fiona, Polycera, Elysia, Phitine, Happow, No. 40). In the Aeotidae, 
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 ux rudiments, but are altogether wanting in many larval forms. 

The greatly modified forms found among the Opisthobranchia, 
such as the genera Limapontia and Phyllirhue, like the more primitive 
forms, have larvae with bilohed yelum and shell provided with au 
operculum (ADLER and Hancock, No. 2; Scunerper, No. 112). 

Our knowledge of the transformation of the larva into qhe adult 
rests principally upon the statements of Max Scnunrze and Norp- 
MANN made with regard to Vergipes Edwardeii and T. lacinulatus 
(Nos. 80 and 113). 

The larva of Tergipes Edwardeit, when still provided with « shell, 
already seems to have lengthened somewhat. The two velar lobes 
are unusually large and oval. On the velar area are sitnated 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. 165 


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. 
Tn the Tergipes observed by M. Scuunras, the passage frem the larva 
to the adult is somewhat different, the velum degenerating in this 
form before the shell is thrown off. In this last case, the larva must 
have adopted earlier the creeping manner of life. ‘The shell-less larvae 
of Tergipes Edwardsit, 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 @), 
which, it has been assumed, change into the labial palps. 


a. 3B. ¢. 





be Th —A-D, SEAMEN hae young 0 of the Tergipes Kéwartsit (after NompMany), 
lorsal papillae. 


‘This view of the transformation of the remains of the velum into the sensory 
organs near the mouth, has been adopted especially by Lovin, who already 
held a similar view as to the origin of the oral lobes in the Lamellibranchs 
ip. 46), Ray Lanxesrer holds that, in Limnaea, the remains of the velum 
PASS over into these subtentacular lobes ; but this point has been disputed 
iw connection with this form. It has already been stated (p. 198) that the 
observations made by Ray Lankesrer for Onchidiam were confirmed by 
Joveex-Larrvie. 

‘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 C). 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 approuches more and more 


il 


166 GASTROPODA. 


nearly to the adult form, but has first to pass through a moult 
(Norpmany), during which it remains entirely quiescent, surrounded 
by the cast skin as by a transparent sheath. This membrane is no 
loubt 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 Bp. 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 throngh 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 off the velav 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 yelum becomes more distinet, and, 
behind the mouth, the foot appears as a large outgrowth. When 
the otocysts arise near the foot and the two anal cells (whieh also 
occur in the Pteropoda) behind it, the embryo passes into the 
Trochophore 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 Gymnosomata also diverge from the other 
forms in so far as the Veliger stage gives rise to a peculiar larval 
form encircled with several ciliated rings. 


A certain differentiation in the development of the early larval stages is 
also caused by the fact (stated by For) that the order in which the organs 


167 


(velum, mouth, shell-gland, foot, ete.) appear, varies greatly in different forms. 
‘The comparison of corresponding stages is in this way rendered somewhat 
‘more difficult, but the final result is, as already stated, very similar, 

The embryonic development of a large number of Pteropoda (Cavolinia 
(Hyalea), Hyalocylix, Creseis, Styliota, Cleodora, Cymbutia, Clione) has been 
closely studied by For, who has also described the further development and 
the metamorphosis of these animals (No. $2). The phenomena connected 
with metamorphosis had previously been investigated especially by Jon. 
Mé ten, Georxeaur, and Knounin the above genera as well as in Tiedemannia 
and Preumodermon (Nos. 77-79, 37 and 58a), 


Thecosomata. The Tvochophore 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 serviug for locomotion, and posteriorly by weaker cilia 
which conduct food to the mouth 
(Greennaur, Fou). In Cleodora 
4 band of cilia appears on the velar 
area at a time when the larva is 
still at the Troekuphory stage. 
Other Pteropods, e.y., Cavolinia, 
carry on the velar area a central 
ciliated tuft, such as has been met 
with 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. 74, 
we see the velum in a slightly 
older larva of such « form. In 
Cleodora, Cymbulia, Tiedlemannia 
(Fig. 75 A and #) the velum is 
much larger, and each of the two 


DEVELOPMENT OF THE EXTERNAL FORM—PTEROPODA, 





Fre. 74.—Larva of Cavolinia tridentata, 


lobes in aguin subdivided, so that 
the whole appears to consist of 
four lobes. This condition is 
specially distinct in a larva be- 
longing to the genus Crese/x und 
described by Grosnpaun (Fig. 
7h ©), in which the velum is still 


seen from the right and veutral side 
Coles Fou, from Baurour's  Text- 

). a, anal region, with the two 
anal cells; /, mesopodium; A, heart ; 
é, intestine; 4n, contractile dorsal 


sinus; m, oral region; mb, mantle; 
me, mantle-cavity ; of, otocyst; pn, 
rudiment of fin ; 9, shell ; 1, renal sac; 
», stomach ; «, food-yolk. 


of considerable size when the shell has grown to « great length. A 
‘strong retractor starts from the anterior part of the body and is 
inserted nt the posterior end of the shell (Fig. 76 A, 1). 


— 


168 GASTROPODA. 


The shell originates from the shell-gland which has shifted towards 
the end of the body. Aceording to Fox, a plug of strongly refractive 
substance is very often to be found in the shell-yland ; in some cases, 
this plug is perhaps formed abnormally, but in Cymbutia 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 
(Cavolinia, Cleodora, ete.), or else it becomes rounded and almost 
oviform like the embryonic chamber of the Cephalopoda. This is 





Fra. 75.—Larvae of Tiedemennia (A), Cyututia Peronit (B); and Oveseis acicula (C) 
{after Kron and GeornBaun). d, operculum ; f, foot Sei fins; s, shell ; », velum, 


the case in Cress, 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 zones of growth. In this way, the large larval shell which, in the 
Cavoliniidae and Gy mnosomata is long and in the Cymbuliidas coiled 
is formed (Figs. 74, 9, 75 A-C, 76 A, #). 

In the Cavolinitdae, 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—PTEROPODA. 169 


margin, but the latter is marked off by a constriction from the part 
which represents the adult shell; here also, in Cavofinin, a transverse 
wall is seereted, after the body of the animal has withdrawn from 
the posterior part of the shell, This larval shell is afterwards lost. 
In other Cuvoliniidae, the larval shell is retained even in the adult 
(Styfiola), the posterior part of the body not being withdrawn from 
it (Cresei*). The coiled larval shell of the Limucinidae passes directly 
over into the adult shell, new coils merely being added to those 
already present (Limacina, Spivialis) In the Cymbulitdac, the 
larval shell can hardly be 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 be in any way compared to a true 
Mollusean shell (PELSENEER). 
The transformation of the shell just described is one of the most 
features among the external alterations undergone by 
the larva. In the Cavoliniidae, the shell lengthens, and, in the Cym- 
tuliidae and Limacinidae, becomes rolled up (Fig. 75 A and B). 
Even in the straight shells of the Cucoliniidae 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 
does not correspond to the ventral side, but lies dorsally, This must 
‘be connected with « twisting undergone by the posterior part of the 
body in these forms (Boas, Nos. 9 and 10). The coiled shell in any 
cause represents the more primitive condition and persists throughout 
life in the Limacinidue, which ave 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 
the middle part 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. 74, pv, and 75 A, fl) in the form of two large 
lobes, the so-called fins (Fig. 75 4, fl). The great size which may 
be attained by the fins in the further course of metamorphosis is 
already sufficiently known. The median lobe of the foot also in- 
creases in size. In the Cymbuliidar, a filiform appendage develops 
on it posteriorly, Ontogeny proves indisputably that the fins owe 
‘their origin to the foot, as was observed long ago by Jon. M0LLER 


: ie 
The Vetiver tarvn of the Pteropoda shows great agreement with 


—_— 


170 GASTROPODA, 


that of the Opisthobranchia, a fact which is specially evident in 
the forms that have « coiled shell (Figs 75 4, and 72, p. 162). The 
posterior part of the foot here also usually carries an operculum 
which, in the Limerinidee, is retained throughout life, aud in the 
Cymbuliilae, is thrown off 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 
filled 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 cacea, be- 
come the nutritive diverticula. These caeca have been supposed to 
yield the liver, but this organ, according to Fou’s statements, forms 
independently of them as an outgrowth of the archenteron. A pos- 
terior tubwlar 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 (Cavoliniidae) or 
else it lies from the first on the right side of the body (Cymbulitdae, 
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 disappeur- 
ance of the velar area leads to the yreat reduction af the large section 
of the tarcat body which lies in front uf the fact. At w 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 7'edemunnia, 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 Cuvolinitiar (according to Fou) 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 


DEVELOPMENT OF THE EXTERNAL FORM—PTEROPODA. 171 


is connected with the mantle or shell (in the Cavoliniidae) only on 
the left dorsal side. 

‘The ventral position of the mantle-cavity in the Cavoliniidae is very striking, 
as this cavity, in obher 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 the 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 in adaptation to a different manner 
of life. 

We shall not here give any special aceount of those ontogenctic 
processes such as the formation of the otocysts, the radular sao, ete., 
which take place in the sate way as in other Gastropods, 

Gymnosomata. The 7rochophor is followed by a larva provided 
with « large bilobed velum 
and a pointed foot (Fig. 
76 A, /f). The shell, which 
at first is cup-shaped but 
later oviform, as it crows 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 retain 
at this stage, in which it 
closely resembles — the 
straight-shelled — Thecoso- 
mata. The shell is thrown 


re 76 Band 77.A). In 
those larvae that develop / 
ciliated rings even before Fria. 76,— Larvae of Clione at two Afferent stages 
the disappearance of the ee itn ane ee ase: 
yelum and the casting of retractor muscle; s, shell; , velums 1, 





chiated rings. 


buted in such a Way that the most anterior ring lies between the 


a 





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 
Dear no relation to the ciliated rings. After it degenerates, the larva 
presents an appearance which, for a Molluse, is very peeuliar, recalling 
rather the Annelid larvae which are encircled with several ciliated 
rings. These also are at u stage following the Trochuphure larva, 
as already mentioned (Vol. i., p. 277), and as we were able to see 
in various polytrochan larvae. This comparison to an Annelid 
larva has already been instituted by Grcensavr, 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 Prewmodermon, two forms which seem to agree pretty closely in the 
general features of their development, as shown by Jou. Mirten, Gecexeaun, 
Kronsand Fou, Asmost of these larval Gymnosomate have not been traced to 
the adult stage, it is by uo 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 2). 
Somewhat further back, but 
in any case in front of the 
anterior ciliated ring, the rudi- 
ments of the acetabuliferous 
appendages appear (JoH. 
Miinner), (These, according 
to PEUSENEER, are derivatives 
of the proboscis,] When the 
proboscis is evaginated at a 
later stage, these seem shifted 
Fio, 77.—Two larvae of Pnenmodermm at further back, being now situ- 

dierent aged, Gucesaaces OM ated on its posterior pat 

(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 





VIS — 


DEVELOPMENT OF THE EXTERNAL FORM—PTEROPODA. 173 


be seen as very small, rounded lobes projecting from depressions in 
the body (Krowy). 

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 be found when the young animal attains its full size, 
but no doubt degenerates later. 


We must here add a few words of explanation as to the position assigned by 
us to the Pteropoda, Until recent times, the Pteropoda were often regarded. 
a 8 special elass equivalent to the Gastropoda, Cephalopoda, ete., although 
some zoologists objected to such a classification. For anatomical and onto- 
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 fins 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 (SounkYET, 
No. 121; Gnospes, No. 39), The fins have been regarded by some as epipodia, 
bat Petsesesn, on the contrary, considers them to be 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. Gnonnen, as well as Boas and Petseneer (No. 84), 
‘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 
Avera, Gasteropteron. These Opisthobranchs which, like the Ptoropoda, can 
swim freely by flapping these fin-like foot-lobes have therefore been regarded 
us the starting-point for the latter group. From such Opisthrobranchs the 
‘Thecosomata would first have to be derived, as has been done by Petsexner, 
‘who traced back the Thecosomata to forms like Acera among the Bulloidea, 
whereas he derives the Gymuosomata from forms like Aplysia, in whioh latter 
‘the swimming lobes are, as in the Gymnosomata, somewhat more dorsal in 
position. Persexxun, in his classification of the Opisthobrunchia, places the 
‘Thecosomata directly after the Bulloidea, and the Gymnosomata near the 
bag Boas also regards the Pteropoda as very nearly related to the 


1 Se ten cadcl of this view we may mention For, Spexeen, 
iN In R. Henrwie's text-book, the Lar ey 

8 Sota of the Gastropoda, and Craus also recentl 
vinallar |, Placing them after the Opisthobranchia, [ Pract. 
now class the Pteropoda with the Gastropoda and most 
according to which they find their nearest allies 
‘Opisthobranchs. PrLsexmer further separates the 
om the osomata, placing the latter with the Bulloidea 
r with the Aplyscidea (see Challenger Reports, Vol. xxiii,)— 






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 developmont 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 Gymmosomata are to be traced back to forms 
resembling the ancestors of the Theeosomata, 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 Gymmosomata, 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. Voor were really found to refer to Gasteropteron, as was con- 
jectured by Gucensavn (No. 123). This Veliger larva develops two fin-like 
structures, and yet, in consequence of various other characteristics, is nob 
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 hus been directly denied by Knons (No. 58b) who regards another larva 
‘as being that of Gasteropteron, Weare 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 
seashore, 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 Veliger larva of the Opisthobranchia. Although the adult is shell- 
Jess, the embryo has a coiled shell like that of a marine Gastropod, 


==E==E 


DEVELOPMENT OF THE EXTERNAL FORM—PULMONATA. 175 


The operculum, on the contrary, is wanting according to Jormux- 
Larevte (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 
Jovevx-Larrore can hardly be doubted, it should be pointed out 
that this organ is as a rule not found in the Pulmonates, 


The marine Amphibola, however, has an operculum showing the usual 
structure and position (i.c,, 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, 118, 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 palmonary cavity, shifts dorsally and, with the 
kidney, opens by a median aperture at the posterior end of the body. 
‘The hitherto asymmetrical anus (lying on the right side) also assumes 
median position at the posterior end of the body. Iu 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, 4 phenomenon that may also occur in other slug-like forms 
(a8 also in various Opisthobranchs). 

With regard to the further development of Ovehé lium, it need here 
only be noted that the form of the adult is attained within the egy. 

The Vaginulidas, forms usually placed near to Onchidium, no 
Jonger possess, according to Semper und y, JHERING, either the fully 
developed bilobed velum or the larval shell (No, 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. 

— Onehidinm and Vayinulus 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 « condition like that of the marine Opisthobranchs, have become 
bac ged to a terrestrial existence. The classification of Onchidinm 

nd Vayinulus among the Pulmonata which might, on account 
of the peculiarities above mentioned, appear doubtful (Joreux- 
Larrcte), has been strengthened by the more recent observations on 


a 


i 


176 GASTROPODA. 


this subject (v. Jazrine, No. 46; Stora, No. 120).* Since the 
Veliqer stage may still be found even among the undoubted Pulmon- 
ates, although usually in a somewhat reduced condition, no objection 
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 Onchicdiun 
(p. 133). 

The velum, it should be mentioned, is, according to Semper, well 
developed in some tropical forms (Auricala, Searabus No. 118); in 
the same way as in Ovchidium (R. Bara, No. 5, p. 175). Sampur 
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 
yelttm is much reduced in the Pulmonates. These puss throngh the 
invagination-gastrula stage, the manner in which this gastrnla 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, yolk-laden cells, appears at first as a massive structure 
with « narrow lumen, bit at a later stage widens out and becomes 
4 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 pomt, 
in the midst of un 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 eom- 
mences (Fon, No. 33; Rann, No. 91; Wonrson, 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 


* [Pate (Zool. Jahrb, Anat., Ba. vii., 1894) who has roan tly nee 
study of the anatomy of Onchidium, concludes that while these forms are 
true Pulmonates, they nevertheless show affinities with the Tectibranchiate 
Opisthobranchs. He places the Onchidiadae and Vaginulidae as direct 
derivatives of the primitive pulmonate on a branch quite independent of the 
Stylommatophora or Basommatophora,—Ep.] 


=== 


DEVELOPMENT OF THE EXTERNAL FORM—PuLMONATA, 177 


later, secreting the shell in the usual way; in Linaz, however, the 
shell of which is at first internal, the shell-gland is pouch-like and 
becomes ubstricted from the ectoderm (Fon). A swelling of the body 
behind the mouth 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 Planorlis, in consequence of the very much 
reduced condition of the velum, never completely unite (Fig. 78, v). 
At this stage, we may, with Ray Lanxesrer, consider the embryo 
as equivalent to the Trochophore ; occasionally, as in Limnaea, even 





a ore tecgaterd ane, een the Liimline Rast). aw, “yes m, argh 
‘enteron and ive gland (large cells); mes, mesoderm ; of, otocyst ; 
radular seo; *, shell; sd, shell-gland ; «p, apical plate ; wm, primitive kidney ; as 


; 


the external form of the Trochophore is preserved, « large pre-oral 
portion of the body being marked off from the posterior portion by 
the yelum (Ray Lasxesrer, For), A thickening at the pre-oral 
pele denotes the apical plate. That the bilobed character of the 
velum so characteristic of the Velijer larva is found here also is due 
to its mode of origin, Asa 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 s00m grows out ventrally (Fig 78, r) and the still undivided and 

e N 


a 


| 


178 GASTROPODA. 


exceedingly large archenteron (sd). 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 u 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, wn) Even at an early stage, a 
remarkably Tange cell cau be seen on each side below the dorsal part 
of the velum; these two cells yield the principal constituents of the 
primitive kidney, and have been claimed as velar cells which have 
entered the body-cavity (Wourson), 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 Rast 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 (Gani, No. 35 ; 
Rast, No. 91; Wourson, 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.—Ep.] 


DEVELOPMENT OF THE EXTERNAL FORM—PULMONATA, 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. Sarastn (No, 102) and Jourpary, as well as Mevrox 
(Nos. 50 and 75), arrived at the same result. 

The primitive kidneys of the terrestrial Pulmonates, which were 
early recognised by O. Sonmipr and GuGrnnaun, are somewhat 
differently constituted from those of the aquatie forms. They also 
have 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 (Jourparn, Meuron, SARasty). 


De Mevnon considers that, in Helix, the primitive kidney arises chiefly 
from the ectoderm, but holds also that the innermost part may be derived 
from 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 Palmonates, 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 


AY Easvascen (No, VII.) has since described the detailed structure of the 
kidney in P! isand 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 on to the exterior, this latter portion Entancur thinks may 
in the Euthyneura, while the remainder is mesodermal. In 
he finds a swollen ampulla at the junction of the two seg- 
ments, The develo] t of this organ has been more recently investigated 
Morsenvneimen (No. XVIL.), and this observer maintains that, in Limar, 
primitive kidney is wholly ectodermal, and here he is at variance with most 
observers. As he also maintains that the heart and definitive kidney 

a arise from a common ectodermal rudiment, we think that his views 
confirmation before we can accept them. Mutssexnetmen (No. 

has also given a most elaborate account of the structure of this organ 

ins he differs from EnLaxcer in one important respect, vir., he is un 
able to find any opening into the body-cavity and thinks that ExtancEr 
mistook a =H vacuole which is invariably present in the end-cell for an 


RAGES 


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 ut first appears as an unpaired swelling, is 
said to assume a bilobed form (Ray-Lanxesrer). Such a bilobed foot seems 
often to occur among the Gastropoda, We have already met with it in 
Succinea, Patella and Vermetus (p, 132). Fou also observed this later develop- 
ment of the bilobed form in the foot of Limnaea, as well as in Planorbis and 





F 4 
Fie. 79.—Older embryo of Planorbis, seen trom the side (after am, cye 
Se Sear | Fe) pedal makin oe, Sataee a 3 um, primitive 
kidney ; v, velum, 
Ancylus, though in these last two animals it was less striking. Ray Law- 


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 OF THE EXTERNAL FORM—PULMONATA, 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. 

Tt has repeatedly been stated that certain regions of the body-covering, 
those to which a large number of ‘mesoderm-cells became attached, carry on 
contractions which sometimes follow one another with considerable regularity, 
this last fact having led to their being called ‘Jarval hearts.” The cireulation 
of the body-fluid is, in any case, promoted by these contractions, but it seems 
doubtful whether they should bedlescribed as actual pulsations, Sometimes 
the movements that thus occur are somewhat irregular, and Rast 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 ing go 
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 « circulation of its own and special 
excretory organs, the velum may serve as respiratory apparatus, this func- 
tion being also exercised by it in addition to its locomotory function in the 
free-swimming larvae. In the embryos of terrestrial Pulmonates, a special 
respitatory organ develops, the caudal vesicle (podocyst), which will be further 
described below. 


The very large apical plate of the embryo has considerubly thickened 
and has become bilobed. According to Rasn, 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 
Isterully 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, 80 aw, #, of). 

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 

As the mantle eitendd further, its growth takes place more rapidly 
‘on the right than on the left side. In front of the anus an indenta- 


am 


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 
the anus and the aper- 
tures of the adult kidney. 
This cavity itself opens 
externally only through 
a narrow aperturey the 
respiratory aperture, 
which lies rather far 
forward on the right 
side of the body, 


The formation of the res- 
Fic, 80.—Older Planorbis embryo, seen from the Pitatory cavity has nlso been 
a OTe tire ee x al 
; foot ; ma, id, as ion taki ince 
eetentacles un, priitive ‘Kidneys relum; Between the margin of the 
wd, stomodacum, mantle and the body, only 
a small aperture being left, 
which, 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 (dmphibola). 'The respiratory cavity 
in the Stylommatophora has, ou 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. JnBRtNo termed the terrestrial 
Pulmonates the Nephropneusta, thus distinguishing them from the aquatic 
Pulmonates, which he named the Branchiopneusta (Nos, 45 and 46.) We 
ourselyes 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, Puate, No, 89) a sensory organ is present in it which 
corresponds to SrenGeu'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 whieh the 
embryo may be compared with the larva of other Gastropods, the 
sinuses in the head and the foot which gaye 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 distinet, 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 For and is directly refuted by 
‘Worrson. 


Fig. 81,—Embryo of Helive lafter Fox). a, 
peepee ie mouth ? md, enteron and ive gland 
iar suo; i, shel ‘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 


has, so far, referred chiefly to the development of the 


set Put especially to that of a few forms which have 
‘been particularly carefully investigated, such as Linnaea and Plan- 
‘orbis. These latter have been described in detail by Rav LankesT2r 

Wo 68), Base (No. 91), For, (No. 33), and Worrson (No. 131) to 
- whose descriptions we must refer the reader for further details. Fou 





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 Gucunsaur, 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 





Fro. treo of Heli powatia, ten a day 9 old, awe tro u the side (after Fou). a 
anus ; coat ie vesicle ; 3 md, enteron and 
aiqertive sani genre ots lan wn, ‘print kidney, 


Trochophore stage, the embryos (of Limaz, Arion, Helix, Clausilia) 
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 (id) is still very large, but 


* [See also the more recent works of Honates (No. XIII. eer ee 

Metsenaanren (No. XVIL), Scammpr (No. XX.) and Wrerzessnt ‘ eva, 

‘These deal for the pgp with the cleavage and cell-lineage. 

‘wermER's researches on Limax, however, are carried anreee Soa outa te 

= in connection with the development of the Stylommatophora. — 
D. 


THE ONTOGENY OF THE STYLOMMATOPHORA. 185 


the foot now bulges ont 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 atill 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 Limax, no traces of the velum are to be found (For). 
‘These embryos, like those of the aquatic Pulmonates, are able to 
rotate within the egg, being covered with cilia, 





¥iq. 8, —Older ombryo of Limax marinus, seen from the side (after Fou), au, eye; 
’d, yolk-material :'7, (oot; , labial palp: ima, tustle-fold : 


pele eee ve gland; of, upper lip; pd, podocyst; py, pedal gunglion ; 
rs, vadular sac; 9, shell; 1, tentacle ; wn, primitive kidney, ey Mt 


‘The position of the different organs of the embryo can be nnuder- 
‘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-gland. A pit lying near the mouth represents the 
rudiment of the radular sac which, according to Fou, arises in the 
stomodaeum, which has 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 Fon, opens outward at the posterior 
base of the foot. Almost in this region, but somewhat behind the 
foot, lies an organ described by For as the larval heart. 


The so-called larval heart (Fig. 82, /h) consists of a bulging of the ectoderm 
with which numerous mesoderm-cells become connected. This specially 
differentiated part of the coyering 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 Fo. ns 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 olub-shaped 
organ (Fig. 83), which is known as the caudal vesicle, and more 
recently has been named the podocyst (Jourpain, Sarasty), 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 podoeyst is specially large in the embryos of various species of 
MHelic (Gucennavr, v. JuexinG, Fou, Saxasin). 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. Sarasry, in describing 
a Helix (Acavus Waltoni, Fig. 
84) found im Ceylon, show that 
the podocyst covers like a cap 
the shell of the very large 
embryo in which several coils 
Ee have already developed. In this 
Fic. $1.—Eimbryo of Helix (Acaeus) form also, in which the pedal 

Pat, thie ane waite in apeially igh 

ss agg ele) veloped, pleating movenents 
4, upper, ¢’, lower tentacle. 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 








THE FORMATION OF THE ORGANS—THE SHELL, 187 


dorsally towards the viscera which are surrounded by a blood-sinus. 
A provisional circulation thus exists side by side with the definitive 
circulation. 

‘Towards the end of embryonic life, the pedal vesicle decreases in 
sive, It remains at first as an appendage to the foot, but this vestige 
also disappears, being absorbed. The foot thus assumes its final 
shape. A median invagination, which only appears at a late stage 
on the foot near the mouth and lengthens out posteriorly into a tube, 
represents the rudiment of the pedal gland (For). 

Apart from the development of these embryonic organs which are 
here specially large, the further development of the embryo resembles 
that of other Gastropods and especially of the aquatic Pulmonata. 
This also applies to the shell where this is not vestigial and internal 
as in many terrestrial Gastropods. Where there is an internal shell, 

in Limar and Arion, the shell-gland becomes disconnected from 
the ectoderm, as already explained. The shell remains internal, being 
hidden beneath the mantle, and is a vestigial structure. In Arion it 
eonsists merely of a number of disconnected calcareous granules. 

Tt is « striking fact that, in Clausilia, according to Gecunsaur, the shell 
algo ab first lies internally enclosed in the epithelium of the shell-gland, 
Only when this latter, as well as the mantle-tissue above it, disappears, does 
this internal shell become external, develop and become coiled. As far us 
we know, this somewhat inexplicable observation of GuGessaun has not been 
corroharated.* We feel inclined to explain the phenomenon described on 
the belief that there is retained a small aperture over the shell as it lies 
within the shell-gland, this gland flattening out at an unusually late stage. 


6. The Formation of the Organs. 
A. The Shell. 


We have already, in treating of the external shape of the body, 
repeatedly alluded to that of the shell, so that only a few further 
remarks need be added. The shell arises from the shell-gland, and, 
when the latter has flattened out, appears cap-like, At first, there- 
fore, there is great resemblance in this point to the Lamellibranchs. 
Here also a shell-integument forms first, beneath which the calcareous 
substance is deposited later. The further Processes are altogether like 
‘those in the Lamellibranchs as given more in detail on p. 60, The 


add ) has since confirmed Grounpavr's observations that 
she thal a Seely and later opens out again both in Clausilta 


188 GASTROPODA. 


unequal growth which leads to the coiling of the shell, has already 
been described (p. 147) and so have the special shapes assumed by 
the shell (¢.7., Pteropoda) and the partial or total loss of the shell in 
the Heteropoda, Opisthobranchia, Pteropoda and Pulmonata, 

Tt is a striking fact that a few specially low forms of Gastropoda 
such as Haljotis and still more Patella and Fiseurella, ave dis- 
tinguished by a reduction of the coils and the udoption of a flat eup- 
shaped shell. In youth, the shell was, as in other 
distinctly coiled. This can be seen particularly well in Pissurella 
(Fig. 85 A-C), The margin of the shell is at first unbroken, but a 
slit appears in it later lying above the slit which occurs in the 
mantle of these forms (Fig. 85 A). The shell-slit is of special interest 
because it is present in two of the oldest fossil Gastropods, ag., 
Pleurotomuria and Belleraphon, both of which are found in the 
Cambrian.* The ontogeny of Fissurella would suggest that these 
forms with slit shells have been derived from forms in which the 
margin is not slit. In many forms the slit is retained as such 
(Scisrurella, Emarginula, and fossil as well as recent Pleurotomariae), 
in others, as the shell grows further ; the most posterior portion of 
the slit becomes cut off by shelly matter from the rest of the slit and, 
4s this continues to take place throughout life, we find in such forms 
as Haliotis a series of consecutive apertures in the shell ; in other 
cases, the slit becomes to a great extent closed by a shell-substance 
of peculiar structure which is seen extending alung the length of the 
whorls as the slit-band. In Fisswrefla, the margin, as it grows 
further, is unbroken (Fig. 85 B). The reduction of the coiled part 
of the shell and the fairly equal growth of the whole margin leads 
finally to the slit taking up a central position near the apex of the 
adult shell (Fig. 85 C). The shell of Fixsure//a has now passed from 
a coiled form to that of a flattened cone; this change is due, as in 
other Gastropods with similarly simple shells, to the manner of life 
and, as ontogeny shows, must be regarded as a phenomenon of 
degeneration. The symmetry of the shell is thus of a secondary 
character. 


B. The Nervous System. 
The nervous system usually arises by delamination (Fig. 88, eg, 
pl, p, p- 194), but it cannot be doubted that, according to recent 


*A description of the development of the Gastro ot the different 
geological epochs has been given by Koren (No, 56). See also Zrrren’'s 
Palacontologie, 


THE FORMATION OF THE ORGANS—THE NERVOUS SYSTEM. 189° 


researches, the cerebral ganglion or part of it, is, in certain cases, 
formed by an invagination of the ectoderm. So far as is as yet 
known, the cerebral ganglion alone has such an origin; all the other 
ganglia arise as ectodermal thickenings which later split off from 
this germ-layer. 

An acourate knowledge of the structure of the nervous system of the adult 
is very desirable as a help to understanding the processes of development, 
especially as some confusion prevails as to the naming of the different parts 
of that system, one and the same ganglion sometimes bearing several different 





85.—A-C, three stages in the development of Misswrella showing the changes in 
isfiet BoorAN), ‘The anitoal’ as depicted in'O, has very nearly attained 


shell 
adult form. f, part of the foot ;'ma, mantle; ms, mantle-slit; «, shell; sn, 
sont; ap, apex of the shell; ss, shell-oleft ; ¢, tentacles. 


names, while, on the other hand, different ganglia receive similar names, 
‘We shail therefore describe side by side some of the principal types of nervous 
system found in the Gastropoda (Fig. 86 4-C). 

‘The nervous system of the Gastropoda consists of the two cerebral ganglia, 
whieh are connected by the supra-oesophageal cerebral commissure (4-C, cg). 
Below the oesophagus, and connected with the cerebral ganglia by connectives, 
lie the pedal ganglia (peg), which innervate the foot and are joined together 
by a commissure. In this way a ring corresponding to the oesophageal ring 
of the Annelida and Arthropoda is formed. The resemblance ceases when we 


a 


190 GASTROPODA, 


come to the other constituent parts of the nervous system. A large nerve 
runs back from the cerebral ganglia on each side, swelling to form two lateral 
ganglia, the pleural ganglia (A-C, ply). ‘These are connected with the pedal 
ganglia by the pleuro-pedal connectives. From the pleural ganglia, again, 
two lateral strands ran back and end in the one or two connected abdominal 
ganglia (Fig. 85 B, aby). Another lateral ganglion is formed in each of these 
lateral strands which are known as the pleuro-visceral commissures, These 
two last ganglia may be called the visceral ganglia (B and C, vg). In the 
Prosobranchia, the pleuro-visceral commissures undergo displacement in 
consequence of the twisting of the body already described (cf, p. 145 and 





go 
spp) 


Fig, $6.—A-C, Diagrams of the nervous system of a Prosobranch (4), an Opisthobranch 
(B), anda Pulmonate (€}. aby, abdominal ganglia; 4g, buccal ganglia; og, cerebral 
gunglin; d, alimentary cival diagrammatically represented a8 a etraight tbe 5 pap 
pedal ganglia; pig, plewral ganglia; sog, sub-, and spg, supra-intestinal ganglion ; 
vy, visceral ganglia. 


Fig. 60), the right commissure coming to lie above and the left commissure 
below the intestine (Fig. 86 A). The original right visceral ganglion is thus 
displaced to the left side and becomes the supra-intestinal ganglion (spg), 
while the original left visceral ganglion now lies on the right side and is 
known as the sub-intestinal ganglion (sy). The abdominal ganglia (abg), 
in consequence of the twisting, come to lie dorsally to the intestine. In 
this way arises the crossing of the pleuro-visceral commissures (chiastoneury) 
characteristic of the Prosobranchia. 

Tn the Pulmonata, the commissures are, as a rule, decidedly shorter than 
in the other divisions, and the whole of the nervous system appears con- 
centrated round the oesophagus (Fig. 86 C). 


THE FORMATION OF THE ORGANS—THE NERVOUS SYSTEM. 191 


The cerebral ganglia might at once be referred back to the apical 
plate of the Trachophore, were it not for the fact, about which authors 
seem to be fairly unanimous, that the ganglia here appear in the 
form of two distinet thickenings of the ectoderm (Fig. 68, cy) which 
only unite later by the formation of the cerebral commissure. P. 
Sanasry, indeed (No, 101), has stated for Byfhinia, that the two 
eetodermal thickenings at first are connected by a median ectodermal 
growth, and thus (in their origin at any rate) suggest a common 
rudiment, but this method of formation, which in itself is very 
probable, has been directly denied, not only for Bythinia but for the 
related form Paludina (v. ERLANGER, Nos. 27 and 28). The two 
thickenings belong to the velar area, lying laterally in it in front of 
the mouth. Even if the cerebral ganglion forms with the help of 
au invagination, its rudiment is paired, In the Pulmonata, in which 
this method of formation of the braia is best known, there are at 
first the two ectodermal thickenings which here also yield the 
principal mass of the cerebral ganglia in the usual way. Then, 
when these are already partly detached from the ectoderm, a 
depression of the ectoderm occurs at the lower edge of the posterior 
tentacles; this becomes continually deeper, and thus forms a tube 
(Sanasin’s cerebral tubes). According to P. and F. Sarasry, in 
Helix (Acavus) Walton/, there wre two such cerebral tubes on each 
side (Fig. 87 A, ct) while, in Limax, only one is found on each 
side (H=ncxman, No. 42; F. Scumrpt, No. 110). The blind ends of 
the cerebral tubes become applied to the rudiments of the cerebral 
ganglia which have become further differentiated (Fig. 87 A, ct, cg), 
and fuse with these to form that part of the brain which is known as 
the accessory lobe (Fig. 87 B, ct). They then become abstricted 
from the superficial epithelium. Their lumina can still be recognised 
as fissures (Fig. 87 B), but these soon entirely disappear, the forma- 
tion of the brain being thus practically completed. A differentiation 
of the principal part of the brain into ganglionic cells and fibrous 
tissue had already taken place. 


_ SaRAstn’s observations with regard to the cerebral tubes, which were on the 
whole confirmed by the researches of F. Scumrpt and Hexcamax, afford an 
‘explanation of the apparent contradiction involved in the two views of the 
origin of the cerebral ganglia, which were derived by one author by invagina- 
‘tion, and by another in the same or related forms by delamination, Both 
these views are founded on fact, each being observed at a different stage of 

i Tn this respect, those forms in which the brain arises as two 
depressions of the velar aroa, us is the case, according to For, in the Pteropoda, 
‘require more careful investigation. The two invaginations are no doubt 


i 


192 GASTROPODA. 


present, as we gather from Fou's description, but}the question arises whether 
they yield only a part or the whole of the cerebral ganglion, From what we 
as yet know, the latter view is the more probable, and is further rendered 
possible by the fact that in a Prosobranch (Vermetus) also, the whole of the 
cerebral ganglion originates from two invaginations (Sacensky), These first 
appear on the velar area as two thickened plates which then sink inwards, 


Fic, 87.—A and B, transverse sections through two embryos of Helix 
Waltoni, at different stages (diagrammatic after P. and F. SARAsty). 
doraal, ia, the ventral ope the ‘section is same, con 

jet, corel (in B, as the ac lobes) j 
am Seda gland ; Us, body-cavity ;'mes, pay sat? Ba 
‘the salivary ducts); s/, buccal mass (in A, 
tentacles. 





The two tubes that arise in this way unite to form the brain and become 
detached from the superficial ectoderm. The cerebral ganglia were seen to 
form in exactly the same way in Dentalium (p. 93). Tt would in any ease be 
interesting to learn in what way this condition may be reconciled with that 
described for the Pulmonata. The rise of the brain through delamination, 


ee 


THE FORMATION OF THE ORGANS—THE NERVOUS SYSTEM. 193 


which was observed in various Prosobranchs (Sanasix, Woursox, Happox, 
MeMorrtcs, vy. Extaxcen, etc.), in Heteropoda (For) and perhaps also in 
Opisthobranchs (Rar Lanxesrer) appears in any case to be the more usual. 

‘The pedal ganglia arise laterally or rather on the under surface of 
the foot, near the otocysts, the positionof which has already been 
described more than once (Fig. 88 B, p). These ganglia at first are 
not connected with each other nor with any other ganglia. The 
commissures and connectives* are secondary structures, év., they 
arise only after the detachment of the ganglia from the ectoderm as 
outgrowths of the ganglia, « point on which the statements of all 
observers agree. Where, as in the Pulmonates, the ganglia lie close 
together, the distinct ganglia, in the eourse of growth become 
connected at an enrly period. 


Besides the original commissure connecting the pedal ganglia in the 
Palmonates, second smaller commissure appears lying more posteriorly. 
Since this second commissure is also present in adults, it was thought that 
it might belong to a second pair of ganglia, but this view is not supported 
by ontogeny, as each of the two ganglia first appear as distinct structures, 
the apparent division in them arising only Secondarily (F. Senmipt), [This 
second commissure appears to be specially developed in the Opisthobranchs, 
where it is known as the parapedal commissure.) 

The commissures and connectives, so far as their origin has been traced, 
arise by the growing out of peripheral parts of the gunglia, and the same 
origin has been assumed for the peripheral nerves (SaLENskY, Hexcaumax, 
y. Earanoen, F. Souampr, etc.). P. Sanasis, indeed, as above stated, main- 
tained that the two halves of the cerebral ganglion separated as one connected 
organ from the ectoderm, and Rast assumed, as we saw (p. 181), that they 
arose from 4 common rudiment, the apical plate. It is therefore in any case 
probable that the cerebral commissure may have arisen from the middle part 
of the common ectodermal thickening. Such an origin for the commissures 
snd the cormectives is on the whole very probable, but is not supported by 
the observations so far made, indeed, in Bythinia, investigated by Sanasry, 
the common origin of the two cerebral thickenings has been denied (v. 
Extaxcen, No. 28), 

‘The buceal ganglia, ax was first shown by Sarasin and as has been 
confirmed by subsequent investigators, arise as cell-growths of the 
stomodacum, The wall of the stomodaeum becomes thickened, and 
while the cells lying on the inner side retain the eylindrical shape, a 
number of smaller cells appear on the outer side (Fig. 88 B, dg). 
These become differentiated into two swellings which lie near the 


~ Lacaze-Dvrnizns and Srenoet (No, 122), we distinguish the 

strands connect the ganglia of one and the same side as connectives 

0 ‘transverse strands which connect the right and left halves of a pair 
these latter being commissures. 


o 


— 


194 GASTROPODA. 


stomodacum and the radular sac and form the rudiments of the 
buccal ganglia. 

The formation of these ganglia recalls to some extent that of the frontal 
ganglion in the Insecta, which also arises from the stomodaeum (vol. iii., 
Pp. 328). 

The pleural ganglia form, in Paludina and Bythinia, as two lateral 
ectodermal thickenings lying somewhat ventrally behind the velum 





Fra, 88,—Transverse sections through the anterior region of two embryos of Paludina 
at the stage represented in Fig. 59, A and H, p. 139 (after v. ERLanagn). 6g, buccal 
ganglia; a7, cerebral ganglia : wes, mesodermal tissue ; os, oesophagus ; uf, otocyst ; 
p. pedal ganglia ; j/, pleural ganglion; r, radular sac; ¢, rurliment of ‘tentacle; 
us, primitive sinus: r. velum. 








(Fig. 88 A, pl), and the two visceral ganglia also arise ventrally 
and laterally, though farther back than the pleural ganglia (v. 
Ervancer). They lie near the edge of the mantle, and near the 


‘THE FORMATION OF THE ORGANS—THE NERVOUS SYSTEM. 195 


constriction which divides the visceral mass from the cephalic and 
pedal parts of the body, laterally and somewhat ventrally to the 
alimentary canal, It is important to note that these two pairs of 
ganglia, on their first appearance, are quite symmetrical, and that 
the asymmetry which is so characteristic of the Prosobranchia 
appears in them only later as a consequence of unequal growth of 
the different regions of the body, This leads to the right visceral 
ganglion shifting first dorsally and then over the oesophagus, while 
the left lies below this tube. In this way, these ganglia become 
the supra- and sub-intestinal ganglia, 


This process has already been theoretically examined, and illustrated by 
Fig. 60 A-E, p. 144. Ontogenetically, the process is similar, but is less 
distinct on account of the connecting strands of the visceral loop, which are 
either wanting or difficult to make out, Indeed, the study of the develop- 
ment of the nervous system is often rendered difficult by the fact that the 
ectodermal rudiments are so indistinctly marked off from the mesoderm, as 
may be gathered both from the text and the figures of older and more recent 
authors. This difficulty no doubt gave rise to the view thnt the nervous 
system in the Gastropoda was of mesodermal! origin, which was supported by 
Bosuerzky's observations (No. 11). 


The abdominal ganglion arises, in Paludina and Bythinéu, us an 
unpaired ectodermal thickening on the floor of the mantle-cavity at 
its posterior end, being found dorsally to the heart. 


As already mentioned, all the ganglia are said to arise independently and 
to become secondarily connected by commissures, Where, as in Bythinia, 
the ganglia lie very near each other, they are, according to Emuaxcer, more 
distinct in the embryo and only later shift nearer to one another. P. 
Sans, in these very forms, derived the pedal and intestinal ganglia as well 
as the abdominal ganglion from a common ventral ectodermal thickening, 
‘and therefore was able to compare them to the ventral chain of ganglia of 
the Annelida, whereas the prevailing opinion now is that only the pedal 
génglia or rather the pedal strands (which in some Prosobranchia are pro- 
vided with transverse connecting strands) can be considered as the true 

of the ventral cords. 

Even in the Pulmonata, in spite of the great concentration of the nervous 
‘system peculiar to this division, the ganglia appear as distinct rudiments, and 
‘only become connected later. We have repeatedly alluded to the conditions 
in the Pulmonates, which have recently been very thoroughly examined by 
A. Hexcumas and F. Scumrr, although we have dealt principally with the 
Prosobranchia, in which the processes can be more easily understood on 
account of the intervals between the ganglia being greater. The formative 
processes fn the Pulmonata agree on the whole with those in the Proso- 
branchia. 


196 GASTROPODA. 


C. The Sensory Organs. 


The appearance of the tentacles as prominences on the velar area 
has already been several times alluded to in connection with the 
external form of the body (Figs. 54, 55, 59, 78, 79, ete.). They lie 
immediately above the rudiment of the brain and, when this becomes 
detached from the ectoderm, remain as large thickenings of the latter 
(Fig. 88 B, t). In position, they correspond to the cephalic tentacles 
of the Annelida, a correspondence which would be all the more strik- 
ing if we could definitely homologise the rudiment of the cerebral 
ganglion with the apical plate. The anterior and lower tentacles in 
the terrestrial Pulmonates arise somewhat later in the closest prox- 
imity to the bases of the posterior tentacles (ophthalmophores). In 
the terrestrial Pulmonates, the cephalic region in which these organs 
originate, and where also the cephalic invagination occurs, has been 
called the sensory plate. P. and F. Sarasin found here in Helis 
(Acavus) a number of sinall bulb-like specialisations of the ectoderm 
(Fig. 39 4, s, and B) which, by the similarity of their structure to 
the lateral line organs of the Vertebrata, were shown to be sensory 
organs. On each side of the section of the embryo given in Fig. 89 
A, two of these organs can be seen in a depression, and it is possible 
that the cerebral tubes which arise at these points originate from 
them. These lateral organs are found in other parts of the body as 
well, and have also been met with in a somewhat similar form in 
adult Gastropods. It is, however, probable that the organs now 
under consideration do not persist and we must therefore regard 
them as temporary larval organs. 





A similar significance is ascribed by P. and FP. Sanasty to the cerebral 
tubes described above (p. 191) as taking part in the formation of the brain, 
these being also considered ax vanishing sensory organs. They may have 
actually functioned in the ancestors of the Gastropoda, as is assumed to be 
the case with the conjectural olfactory organ of the Annelida. They now 
give rise to part of the brain, just as in the Annelida, where the origin of the 
brain is traced to the pre-oral sensory organs (KLEINENBERG, Vol. i., p. 288). 





The eyes develop in a very simple way. They first appear almost 
simultaneously with the rudiments of the tentacles, at the ventral 
edge of which a depression takes place. This deepens to form a 
vesicle which finally becomes detached from the ectoderm and is then 
found below the integument. Each optic vesicle frequently, as in 
Paludina, lies on a prominence at the base of the tentacle. Where 
the eyes are found on the tentacles themselves, as in the posterior 





THE FORMATION OF THE ORGANS——THE SENSORY ORGANS. 197 


tentacles of terrestrial Pulmonates, they are raised up as the tentacle 
grows. The eyes are already visible when the tentacles are first 
indieated (For). 

The next step in the development of the eyes is the deposition of 
pigment in the proximal part of the optic vesicle. The cells of this 
region increase and yield the retina, while the distal part forms the 
cornea. Two structures arise within the optic vesicle as secretions 
of the cells; these are the lens and the vitreous body which are 
at first homogeneous and strongly refractive. In the latter, delicate 
fibres appear which run from the retina to the lens (v. ERLANGER, 
No. 27). 





im ‘49, —A, Transverse section through a young embryo of Melix (tcavusy Wallond, 

j. one of the Interal organs (.1, s) highly magnified (after P. and FP. Sanastn). cet, 

‘ectoderm ; mes, mesoderm ; #, lateral organs of the sensory plate ; al, posterior part 
of the bucea! mass, including transverse section of the oesophagus the mdalar 
mac; mm, sensory cells ; «¢, supporting cells. 


According to Sarensxy, the formation of the eyes, in Vermetus, is connected 
with the invagination of the cerebral ganglion. They appoar as rounded 
thickenings at the edge of the plate which later sinks in to form the brain ; 
these xeon become hollow and form vesicles similar to those described above 
‘as rudiments of the eyes, and then shift inwards in connection with the 
invagination. Only somewhat late, when the lens has already been secreted, 
do they lose their connection with the cerebral invagination. The further 
development of the eyes apparently takes the course described above. This 





198 GASTROPODA. 


method of formation of the eyes recalls the condition in those Gastropods in 
which they lie upon the brain (many Opisthobranchs), The eyes of Viermwtus, 
however, so far as we know, lie externally at the bases of the tentacles, 


B 


Fro, 0,—Byex—A, Patella rede; B, Trvchnn onus Twrtes creniferwe : 
Murex betadacias (after HILcERL by, connective tixsae ectodern: ; gf, vitreonm 


body; d, lems: a, optic nerve; p, pigment ; ¢, retina; sf, 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. Pafella, for instance, has eyes which are 
placed in the usual position, but which are mere pit-like depressions 
of the surface (Fig. 90 4). In Haliutis, Trochme, ote., the pit is deeper 


THE FORMATION OF THE ORGANS—THE SENSORY ORGANS. 199 


and becomes a vesicle which, however, remains open (Fig. 90 2). Its 
tumen is filled with a strongly refractive gelatinous mass (g/) known 
as the vitreous body. In other forms the vesicle has closed (() 
and, finally, the higher form of Gustropod eye (10) provided with 
& so-called lens and vitreous body is developed (FRaisse, No. 34; 
Hiner, No. 43; Pauseneen, No. 85). [In most Diotocardia the 
optic vesicle is open, but in the specialised Helicénidae and 
Neritidue (the Gymnopoda of Fisenen) and in the Turbinidae it is 
‘losed as in all the Monotocardia.) 

~ The first-named Prosobranchs are held on other yrounds to be 
primitive forms, and the simple stracture 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 Cannréne (No. 22), in cases where the eyes are regenerated, 
their formation takes place in the same way as when they arise ontogene- 
Hieally, 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, 
: 79), appear as depressions of the ectoderm on either side 
rudiment, near the pedal yanglion, with which, however, 
t come into any closer relation as they are innervated from 
sin (LAcazE-Durniers). When cut off from the ectoderm, 

is are still formed of long cylindrical cells which flatten 
for a time, the anterior and ventral part of the vesicles 
thick. From this part of the wall, the otolith or otoliths 

) are secreted ; these structures become detached from the 
nd rest upon the sensory hairs which have arisen on the 














‘Spengel’s (olfactory) organ (osphradium) only develops at a later 
stage (Palutina). It arises as an ectodermal thickening composed 
of several layers of cells. Where, as in Palulina, pits are found in 
the organ, these are caused by depressions in the thickened ectoderm 
& ‘Extaxoun). 

condition of this organ, which is found in many Gastropods, 
‘a similar way. The organ was originally paired and lay near 
“45 may still be the case in Zygobranchiate Diotocardia. Where 

jn the Monotocardia and the Euthyneura, this is in all cases 
connected with the asymmetry caused by the torsion of the visceral mass. 


i 






rises 





200 GASTROPODA. 


D. The Pedal Glands. 


In the larvae of various Gastropods, e.g., Nassa (Figs. 61 D and F, 68), 
Vermetus, Murex, Firoloida (Fig. 65), etc., a deep tubular or aac-like ectodermal 
depression has been described in the foot; this shows great agreement in 
position with the pedal gland found by KowaLevsxy in the embryos of Chiton. 
Such a rudiment is perhaps also present in Denfalium. In Nassa, this gland 
forms a rather long tube, and in Murer it has a similar form (BoBRETZKY, 
No. 11); in Firoloida, it is said to be much shorter and bilobed (Fo, No. 31, 
Fig. 65, fd.). Savensky 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, eo as to yield the 
glandular portion. Various glands are known in adult Gastropods also lying 
one behind the other in the sole of the foot (CanRrzreE, 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 (Barnots, No. 8), 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 
igs, ST and 82. p. 184). When the radular sac lengthens, it 
ves dorso-ventral flattening. — Its lateral margins then bend 
upw rd so that it assumes the form of a channel. the dorsally directed 

vity of which is filled with a mass of connective tissue. The wall 
of the chanel 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 R6ssLeR (No. 95), and RUcKER 
(No. 86), and others. takes place in’ the following way: The teeth 
theniselves are seereted by the cells which lie ventrally at the blind 
end. while the basal membnare upen which the teeth are bore is 











2 enormous development in the Pulmocata: 
ere the giand takes the form of a 
siong the greater part of the foot. 
ad and foot. as in Heiss, or 21 
_—Ep.” 















THE FORMATION OF THE ORGANS—THE ALIMENTARY CANAL, 201 


yielded by the lower epitheliam (Fig. 91 4). The large groups of 
tooth-forming vells (odontoblasts) form a kind of cushion or bed upon 
which the teeth are modelled (Fig. 91 4 and B). In the shape of 
this cushion, the future form of the tooth is already shown. In the 

i ‘ia and the Pulmonata, a special differentiation occurs, 
ouly « few (four to five as seen in longitudinal section) * very large cells 
undertaking the formation of one tooth (Fig. 91 B, od); the most 
waterior of these large cells is said to yield the part of the basal 
membrane that underlies the tooth now in course of formation. 








OT 


i ead we a 

Fie, 91, —A and £8, Longitudinal sections through the radular Oct 
frudgaria (a) and Helge memorutis (H) (after Réssuxu), bn, basal membrane ;-od, 
" 3% @» “pper epithelium ; arm, subsratular membrane; m, ep lower 

Hina; 2, teoth, 

The tooth thus produced fuses with the basal membrane and with 

the prolongation of the basal part of the last tooth (Fig. 91 2), 

When « tooth is thus completed, this cell-group undertakes the 





rof gach tooth, the cells being arranged in two parallel sories, so that, in a 
section, like that shown in Fig. 91, only one raw is seen at a time, 

Te 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.—Ep.} 


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 4, 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 us diverticula of that 
part of the stomodacum 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 ont posteriorly 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 uot 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 Palwiina (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, ete.). 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 


a later stage, the whole of the sac-like anterior part of the enteron is 
affected by these deposits, which, however, are always greatest on 
the ventral side, The dorsal and anterior part, with which the 

becomes connected, is marked off into a sac-like stomach, 
while the part that lies ventrally and more posteriorly, and which 
contains by far the largest amount of deutolecithal constitnents, 
yields the liver. The latter, originally spherical, soon becomes lobate, 
Ley 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 wre connected with its formation; it appears donbtful 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. Fou, 
in connection with the Hetcropoda, 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 liver, its glandular 
eharacter being soon proved by the development of several lobes. A 
ventral nutritive sac is also found in the later stages of Limnuea ; 
but it is expressly stated that this does not take part in the forma- 
tion of the liver, but that the latter arises quite independently of 
it as two small caeca which grow out at the end of the stomach 
(Wotrsox, No. 131). 


Ik is impossible to ascertain the correctness of the various statements made 
‘8s to the manner of formation of the liver. These statements differ so greatly, 
and in the present state of our knowledge are so difficult to compare with one 
another, that we are justified in assuming that more careful research will 
greatly modify them. This is all the more probable as it is evident that the 
Processes under consideration are difficult to interpret. 


In the Pteropoda also, the liver is said to arise as x finger-shaped 
outgrowth of the ventral wall at the posterior end of the stomach, 
‘near which a second outgrowth soon appears (Fo), In the Pteropod 
Jarva, the nutritive material is stored up in the cells forming the 
walls of two suc-like outgrowths of the stomach, which are at times 

from the latter by stalks. These nutritive sacs, one of 
Which is usually larger than the other, differ slightly in position in 


a 


204 GASTROPODA. 


the different forms, but generally appgar to open into the stomach at 
its postero-ventral end, so that # relation between the nutritive sacs 
and the liver seems probable. As the liver continues to develop, the 
sacs decrease in size. 

The two entodermal stomach-diverticula of different sizes are, as 
already mentioned, also found in the larvae of the Opisthobranchia 
(Fig. 72. di, p. 162). They are here said to belong rather to the 
dorsal and anterior part of the stomach (RHo, No. 93; FiscHEk, 
No. 30). According to FiscHer, they become transformed direct 
into the liver, forming the outgrowths which enter the dorsal 
papillae (cerata). The 
left diverticulum yields 
the principal lobe of 
the liver, while the 
right, in the Nudi- 
branchia, is of small 
size. 

To the Pulmonata, the 
position of the nutritive 
masses is somewhat 
different. It has been 
asserted that, in them, 
the principal mass of 
large cells filled with 
albumen lies at the 
dorsal side. The large 
dimensions attained by 
this part of the ento- 
derm is evident from 
Figs. 18-83, pp. 197-185, 
depicting the embryos 
of Planurhis, Helis and 
Limax. The entoderm- 









Fic. 02,0 amd B. embryos of Byt 
at liflerent stages catter ¥. 
. verebral ganglion ; F. foot; 


cells in other parts, 





abe ot however, remain small, 
especially ventrally and 
posteriorly, and these 
parts give rise to the 
posterior portion of the 
intestine which takes the course already deseribed. The small- 
celled portion of the entoderm spreads out further at a later 





THE FORMATION 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 are said to be dorsal in position in 
the land Pulmonates also, and the direct rise of the liver from them 
has been described (Jourparx, No. 49). It appears, however, from 
the figures of Pulmonates, especially of the land-form before us, 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- 





93.—A-C, sagittal sections of the embryos of Fuse at various stages (after 
RMR Gy ae eclks 7, tock di, cephalic vesicles 7, livers mm, month} ma, 
‘eniterou ; wg, stominch ;'4, shell; a, shell-gland ; ed, stoniodacum, 


ditions described above. The fact that the intestine, the stomach 
and the liver are not clearly marked, makes it diftioult 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. ExuancEx). 
"Phe liver appears in the form of a very wide anterior and a smaller 


= 


206. GASTROPODA, 


posterior outgrowth (Fig. 92, vl, Ai), while the stomach (my) 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 eases so far considered, the enteron bas at first 1 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 Bopretzky, 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 





= sub-velar cells, 3 
with yolk, having a small protoplasmic portion directed towards the 
mouth (Fig. 93 4). 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, thus 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, m7), 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 off (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 CANAL. 207 


albuminous cells of other Gustropods described above. The yolk- 
tmass, 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 filled with disintegrated yolk-substance (Fig. 62 B), this 
being taken up by the large entoderm-cells, which, according to 
Bowagerzky, represent the rudiment of the liver (Figs. 62, 93 and 
94,4). The large-celled “hepatic vesicle '’ may be said to form the 





Fic, 95.—A-), lougitudinal sections thre 


ey from BaLroun’ 
ra it of foot; Ay, entoderm ; in, 
‘@, shell-gland ; #f, lumen of the enteron. 





gh embryos of Noses ssilabilts ob diferent 
xt-book). bp, blastopore ; ep, ectoderm ; 
epithelium of the enteron ;'m, mesoderm ; 





dorsal and posterior part of the entoderi-sac, if the rudiment of the 
intestine is left out of consideration (Figs. 93 and 94, md). It 
ocoupies 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 « 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 
jntestine, but is gradually absorbed as development advances, 





208 GASTROPODA. 


A still further specialisation of the enteron along the lines seen in 
Fusns is found in the egy of Naxa which is still more richly supplied 
with yolk. The formation of the germ-layers in this egg has already 
been 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 Cand 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 £, 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 
further development, no doubt follows the same course as that of 
Faana, 

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 nay be modified through the 
various ways in which the nutritive mass is deposited. From the 
different conditions found, we scem 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 anux 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; Jourpain, No. 
49, ete.) speak of the development of a proctodaeum. As the latter 
is said to occur in other Molluses, ¢.7., Chiton, Teredo, Entovalva, 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 @ 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, A, p. 150. and 99 and 100, p. 214), but occasionally it 





= 


THR DIFFERENTIATION OF THE MESODERM-RUDIMENT, ETC. 209 


may be found at an earlier period on the surface of the body, as in 
Faseiolavia (Osporn, No. 81). 


Bipectinate plumose gills, a pair of which is found in Fisswredia and Hadiotis, 
are considered as the most primitive, and we may assume that the single 
monopectinate gill of the Monotocardia is to be 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 aa yet beon bestowed on the development of the gills in the Gastropoda 
that itis impossible to confirm by their ontogeny this view which in any 
case ix 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 « bilateral rudiment 
whieh 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. 96, 48, 51, 52, 56). The distinctness 
of these two cell-masses varies in the different forms; they may also 
be 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 u cavity in each of these cell-masses, 
right and left coelomic sacs are formed (Fig. 56 4 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 Bythinia 
by v. Exnancer. 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- 


*{In Trochus, the septum, which separates the two sets of leaves of the 
gill, is attached (except at the free end) to the mantle-wall along both 

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. 
are much reduced in size as compared with the set which 
t main mantle-cavity, and it is easy to see that a further stage 
this process might result in a complete fusion of the septum with the 
mantle-wall and thus cause 4 suppression of the one set of gill-leaves. There 
‘is every reason to believe that the monopectinate gill nrose in this way—Ep.} 

p 


: 


— 


210 GASTROPODA. 


ment of the pericardium ; the process is therefore very similar to 
that described (p. 74) in connection with the Lamellibranchs. The 
lumen of the saes is to be regarded, here ulso, 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; ovcasionally even vom- 
pact masses of mesoderm remain which have been distinguished as 





Pie. 96.—Dingranimatic represeutations of Rev! embryos of Bythinia tentaculata » 

A ital section; B and (*, from the right side (alter v. OER), a, anal 
Fey 3 bd, Buco ¢, coelom; ent, entoderm ; m, mouth; mes, ‘ 
rudiment ; s¢, shell-gland ; ¢. ectodermal thickening, from which the tentacles and 
the cerebral ganglion are produced ; 7, velum. 






cephalic or trank-mesoderm and from which, by delamination, somatic 
and splanchnic layers have been derived. According to this view, 
the definitive body-cavity would arise at least to some extent in 
the form of a coelom. This subject will be referred to again later 
(p. 217). Tt is generally assumed that the definitive body-cayity 
arises out of the primary body-cavity in which the cells detached 
from the mesoderm-bands become distributed, yielding comneetive 
tissue and musculature. With regard to the latter, the origin of 
the columellar muscle has been somewhat more carefully examined : 


THE DIFFERENTIATION OF THE MBSODERM-RUDIMENT, BTC. 211 


it is found to arise by the concentration of mesoderm-cells at the 
base of the foot. 

The development of the mesoderm and of the parts connected with 
it has recently been specially studied by v. Enuancer in Paludine 
and Bythinia, As vy, EXtaNeeR found that these organs developed 
here in the same way as in the Lamellibranchs, and, since the 
investigwtions of other zoologists which were less comprehensive led 
to less satisfactory results, we shall here follow principally the state- 
ments of this author. 

The two mesoderm-sacs, above mentioned, approach each other 
and come to lie ventrally between the archenteron and the ectoderm, 





Fro. 97.—Transverse section hyd the pericardial region of an embryo of Paludina 
" at the stage depicted in Fig. 59 B, p (after v. ERLANGER). /, liver ; Lh, 
i stomach ; wes, mesodermal tissue; mf, mantle-fold; mh, muntle- 
envity 7 ty nt of detinitive, n’, of abortive kidney ; na, na’, rndiments of 
efferent duets of the same; p, pericardium ; », shell. 





where they fuse. Oceasionally, in later stages, a septum is retained 
as an indication of the former partition-wall (Fig. 98 A, sp). In the 
further course of development, the right half of the sue grows much 
more vigorously than the left, and the whole sac extends dorsally to 
the 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 n’). 
These outgrowths, according to Ertanaer, are the rudiments of the 
definitive kidneys which are consequently, like the pericardial sacs, 
paired on their firstappearauce. The left rudiment soon disappears, 


212 GASTROPODA. 


while the right forms a sac (Fig. 101, ») and unites with the ecto- 
derm to form the efferent duct. In Bythinia, the kiduey can at this 
stage be recognised as a derivative of the posterior part of the peri- 
cardial sac (Fig. 92 B,n). At. 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 Palwdina, 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 





Fira, 98.—A, transverse section through the goo of an em 
Paludina vivipara. at the stage Sg rahe in . 90. B, eee ets 


mature Paludine embryo (after V. INGER). d, intestine ; = 


, liver; Uy body-cavity ; m, stomach ; mes, mesodermal tissue 
abortive kidney ; na, efferent duct of the former: ve, aperture Edy to 
the dhe porter Pp, pericardium ; sy, pericardial Spee tee are he of 


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 ranning 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, sa 
thus becomes its ureter (Figs, 59 4, and 98, na). an 


= 


THE DIFFERENTIATION OF THE MESODERM-RUDIMENT, ETC. 213 


‘The ectodermal origin of the ureter can be recognised even at a lator stage 
in its histological structure. The duct formed.as above has been distinguished, 
‘a primary 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 
Pee eee aes ie AT naan Mes age this channel partly 

closes and, becoming finally altogether detached from the wall 
iad eaptiney aunt, yields the secondary uyeter which, in the most 
oxtreme cases, such as Heli pomatia, runs alongside of the rectum and, 
with it, ends near the respiratory aperture (vy. JamRrxc, No. 46; Bravx, 
No. 14). 

The origin of the ureter as w part of the pulmonary cavity which at first 
is channel-like but closes to form a tube later, gathered with some certainty 
from the study of comparative anatomy, is entirely confirmed by ontogeny 
(Buavs, Beuwe, No, 4). The kidney, in the embryos of Heli pomatia, opens 





es embryo of Palwlina wiviy (after v. Entanogn). /, liver; wn, 
3% Velumn ; the rest of the lettering as in Fig. 100, 
‘neur the primitive kiduey in a depression of the body which represents the 
‘diment of the respiratory cavity. As this cavity deepens, the glandular 
part of the kidney and the primary ureter become differentiated. At the 
_ posterior part of the pulmonary cavity, the latter passes into o channel which 
sums through the whole cavity and ends only at the respiratory aperture. 
a broad and is distinguished by its high cylindrical 
the rest of the respiratory cavity which is lined with 
jum, The channel closes later, its edges bending together 
and fusing from behind forward, and the secondary ureter thus formed now 
ees Saeary tube which opens in the neighbourhood of the anus. 
‘The secondary tireter is a new acquisition within the division of the Stylom- 


‘ as Vv. Jaeninc has shown. It ocours only in the so-called 
Ma. Ainong these, however, in one and the same genera, forms 
possessing the secondary ureter and others exhibiting the much 


a 





214 GASTROPODA. 


more primitive conditions found in the aquatic Pulmonates, as Brion has 
shown. From this we may gather that the division of the Pulmonates into 
Branchiopneusta and Nephropneusta is not justifiable. It has already been 
shown (p. 182) that we cannot regard the pulmonary cavity us a transformed 
ureter, but must consider it as the pallial cavity, corresponding to that in 
other Gastropods, 


The kidney now enlarges considerably and its walls become folded 
(Fig. 98 8). At first only a few such folds are formed, and the renal 
cavity is still spacious, but at a later stage the lamellae almost com- 
pletely fill it. vy. ERpanGer points out that the complicated kidney 





Fro, 100.—An almost mature 






ryo of Paludina s Vivipere (after v. ERLANGER). a, 
anus; «, auricle; am, eye; f, foot; g, sential yiaw efferent genital duct ; ky, 
gill; 'm, mouth ; wel, intestine ; mg, stomach ; raptor ere edge of the 
Thantle! 2, kidney ; na, ureter: o; aperture of the unter fut the mantleenti 
e, reno-pericardial pore ; op, operculum ; ut, otocyst ; ium ; r, raduler 
sac; ap aeetippietn #/, spines on the shell ; t tae ventricle, 





of Paludina thus passes through a stage which is retained through- 
out life by the very simple kidney of Haliotis. The opening of the 
kidney into the efferent duct gradually approximates to the reno- 
pericardial pore (Fig. 100). he latter is (with some exceptions) 
known to be retained in the Gastropoda, so that the details given 
under the Lamellibranchia (p. 74, ete.) as to the connection between 
the coclom and the nephridia are applicable here. 

Most of the Gastropoda possess only one kidney, but those 
Prosobranchs that are provided with two auricles (Diotocardia, sueh 


THE DIFFERENTIATION OF TH! MESODERM-RUDIMENT, ETC. 25 


as Haliotia, Palella, Fisturella, Trockus) have a second kidney. Iv 
is an interesting fact that this original paired character still finds 
expression in the development of the kidney in Palwfine. In the 
adult, this kidney lies, as in inost 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 bedy took 
place (Fig. 100 A-2, p. 214). This view is admirably supported by 
vy. Excanoen’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 (Monotocardia) 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 (Haliotis, Fissurella, Turbo, Truchus) 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 (Perrine, No, 87). Ontogeny, however, as well 
as the fact that, in the Diotocardia, the right nephridium serves for con- 
ducting to the exterior the genital products (see below, p. 220) indicate that 
it is the left (which before torsion is the right) kidney that persists and is 
alone retained in the Monotocardia (Ray Lankesrer, No. 65; v, ERtancer, 
No. 29). 

‘The pericardial sac has several times been mentioned. ‘The term 
pericardial is here hardly correct, since the kidney also originates 
from this sac, to which, further, the /eart owes its origin. This 
organ has now become very large and has thin walls (Fig. 99). 
Dorsally, and to the left of the renal outgrowth of the pericardium, 
a channel-like invagination representing the rudiment of the heart 
(Fig. 98, 4) appears and occupies the whole length of the sac. The 
channel becomes more and more marked off from the pericardium /., 
it becomes a tube which at first still remains open toward the primury 
body-cavity. ‘This tube, by finally closing and remaining connected 
with the wall of the pericardium only at its two ends, gives rise to 
the heart which now, as a tube, lies within the pericardinm, 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 ave 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 moyement, have been assumed to be larval hearts. The 
rudiments of the vessels first appear as such blood-sinuses of different 
sizes; in Palmdlina, for instance, » large sinus is found beneath the 
intestine (Fig. 88 B, ux, p. 194). The yradual narrowing of these 
spaces, which are surrounded by i luyer 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 veiu. The other vessels arise in « 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 wudergone 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 o 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. 

Tt is an interesting fact that we have, persisting throughout life, in 
Dentalium, & condition similar to that seen in the developing heart in the 
Gastropoda, which, as we have seen, arises as an infolding of the pericardium. 
According to Prare (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 PLare as pericardium und heart, however, are but slightly developed, 
and the nephridia are not connected with the pericardium, It is well known 
that Dentalinm 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). One of the auricles, as was seen, is almost always Jost in 
the process. If the pallial complex is only displaced to the side, the 
gill lies behind the heart, the auricle behind the ventricle (this is 
notably the case in the Opisthobranchia); but, if the pallial eom- 





THE FORMATION OF THE ORGANS—THE GENITAL ORGANS. 317 


plex shifts quite to the front, the gill will be found in front of the 
heart and the auricle in front of the ventricle (Prosobranchin). 


Other descriptions of the rise of the pericardium, the kidney and the 
heart." In the formation of the pericardium as deseribed above, this organ 
Was treated as if it corresponded to the whole of the coelom, but Vv, Hntaxomn's 
observations on Paludina and Hythinia may also be interpreted as showing 
that only « part of the original coelom persists as the pericardium while the 
rest disintegrates, as we saw to be the case in the formation of the definitive 
body-cavity in the Arthropoda. Sanensicy also, at a somewhat later stage of 
the embryos of Vermetus, speaks of « somatic aud a splanchnic layer which 
&re apposed to the ectoderm and the entoderm respectively and which enclose 
@ large space as a (temporary) secondary body-cavity, The two layers of the 
mesoderm are, however, so indistinct in the Mollusca that we are unable to 
speak of them with wny certainty and, until more detailed statements are 
wads, must regard ther as only definitely differentiated in the pericardium. 
Sausinsky, who regarded this large space as the coelom, considers that the 
heart urose from it im a way similar to that above described. With this may 
be reconciled the earlier accounts of Gaxrx (No. 85), Bétsenus (No. 18) and 
especially of P. Sanasuy (No. 101) and Scaanrenw (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 
pericardium (ScuaLrxew) or at least in the neighbourhood of the latter 
(SALessky), the efferent ducts being derived from au (ectodermal) invagina- 
Hon of the mantle-cavity, but the majority of authors trace back the whole 
Kidney to an ectodermal invagination. After what hos been said above 
{p- 74) 4s Lo the formation of the nephridia in the Lamellibranchia and the 
Annelida, it cannot be doubted that the first method is the more probable. t 


H, The Genital Organs. 


‘The development of the genital organs bas been best observed in 
Paludina, a form belonging to the Prosobranchia in which the sexes 
are distinct (v. Extanexr). In these animals, the condition of the 


* The literature connected with the formation of the iaplaetaal organs is, 
like that connected with the ontogeny of the Gastropoda in general, rivh in 
\erteeaid ‘statements. Where recent researches may be considered to 

older statements, we have ignored the latter. Lack of space 


oa peateom, taking into cousideration all the published data of a 
nature. A summary of these is to be found in v. Exuancnn's 

works (Nos. 27 und 28). 
recent investigatious made by Memsennuimer (No. XVIL) on the 
tence. in Lima do not at present help to clear up the 


to their origin, as they are too startling to be accepted 
Misses aerten maintains that the heart and kidney arise from 
‘ectodermal rudiment, a condition which, so fur as we are aware, 


opps. to be quite unique.—Ep.) 


— 


218 GASTROPODA. 


genital organs is far simpler than in the hermaphrodite Pulmonates 
which have repeatedly been studied but are far from being fully 
understood, and we shall therefore consider Palwilina first. The 
first rodiment of the genital organs here appears at a time when the 
velum is still present, and the primitive kidney at its highest de 
velopment, #.*., somewhat at the stage of Fig. 99. The male and 
female genital rudiments are similar. 

The germ-gland arises as a rounded outgrowth of the pericardial 
sac near the rudiment of the (original) left kidney (Fig. 101, 9), which, 





ad 


Fra, 101,—Transvetse section through the posterior end of an embryo of Palwabinn 


in the stage depicted im Fig. 9 (after v. ERLANGEM). ay, 
iduct; d, intestine; y, ru 
tissue; mA, mantle-cavity ; 
we, ureter. 





ut of the genital gland; /, liver: wes, 
, kidney: 0, reno-pericartial pore; pr, pericnndimur ; 


as has been stated, degenerates. This outgrowth becomes separated 
from the pericardial sac as a spherical vesicle which approaches the 
efferent genital duct (a) that has now also appeared as a rudiment. 
The latter arises as an ectodermal invagination from the mantle- 
cavity, and, according to v. ERLANGER, it is very probable that the 
duct of the (original) left kidney changes direct into the genital duct. 
It grows out further (Fig. 102, ug) and becomes anited with the 
vesicular rudiment of the germ-gland (Fig. 100, g and ga), The 
genital gland and its efferent duct now increase considerably in length 


THE FORMATION OF THE ORGANS—THE GENITAL ORGANS, 219 


and begin to coil, but there is as yet no sexual differentiation save 
that this increase in growth takes place at «an earlier stage in the 
male than in the female. 

‘The male genital apparatus of Palwdina is composed of the germ- 
gland just described, 
which becomes the 
testis, of the efferent 
duct, which has also 
been to some extent 
described, and of uw 
much Jonger section, 
the vas deferens; the 
latter, which leads to 
the penis, develops in a 
somewhat different way. 
This part of the vas 
deferens arises in the 
form of « groove in the 
base of the mantle- 
cavity into which the 
previously formed : ere peo Pee youn iawn) a 


(primary) efferent duct — giferent duct: , intestine; y, rudiment. of 
opens. ‘The groove —_eetiltal gland; liver; wine, mesodermal tissue ; 


choees and, ip the form wl, mautle-cavity, 
of a tube, extends as far as the right tentacle where the penis 
develops. 

In some Prosobranchs, this seminal groove is retained throughout life and is 
continued from the male genital aperture in the mantle-cavity to the tip of 
the penis. We thus find here, as in the formation of the secondary ureter of 
the Pulmonates, conditions which are permanent in other forms appearing a8 
consecutive ontogenetic stages, 

‘The female genital apparatus of Pifui/inc does not develop as early 
as that of the male, Whereas the chief features of the latter caw 
be recognised at the end of embryonic development, those of the 
female cannot be distinctly made out \ntil several weeks after birth. 
At this stage, the rudiments of the albumen-gland appear in the 
form of eight to twelve tubular outgrowths near the point where the 
ectodermal efferent dict unites with the germ-gland. The ovary is 
still represented by a tube lined by undifferentiated opithelium. The 
short tube which extends from the ovary to the albumen-gland is 
said to be derived from the mesoderma) rudiment, like the short piece 





Fi, 102-—Pertion of mgitial section of an, embryo 


— 


220 GASTROPODA. 


which, in the male apparatus, runs from the testis to the commence- 
ment of the so-called primary (ectodermal) efferent duct. The whole 
of the remaining efferent apparatus in the female corresponds to the 
primary efferent duct in the male, and the former, like the latter, 
opens into the mantle-cavity. There is, in the female, no part corre- 
sponding to the secondary efferent apparatus of the male. Apart from 
this last portion the genital apparatus in the male and in the female 
thus agree closely in their development, the principal constituent 
parts being apparently quite homologous (v. ERLANGER). 


The relation of the germ-glands to the pericardium, which was only con- 
jectured to exist in the Lamellibranchia (p. 82), is definitely proved by v. 
ERLANGER to exist in the Gastropoda. The genital glands arise as growths 
of the pericardial wall, and thus bear to this latter the same relation as do the 
genital products in the Annelida to the peritoneal epithelium (Vol. i., p. 297). 
In this way we obtain a further support for the coelomic nature of the peri- 
cardial sac. Since, in the lower forms, the nephridia function in conducting 
tho genital products to the exterior, it appcars as if, in the Gastropoda, the 
nephridium, which no longer functions as a kidney, might become directly 
modified as the efferent genital duct. As we have seen in the Solenogastres 
{p. 9), the nephridia transmit the genital products, and even in some Proso- 
branchs (i.e. the majority of the Diotocardia) the right nephridium serves 
in addition as a genital duct; such a modification of the efferent renal ducts 
ix therefore not surprising. 





‘The hermaphrodite genital organs of the Pulmonateshave repeatedly 
been made the subject of careful ontogenetic research (Ersta, No. 26 ; 
Rouzaup, No. 94; Brock, No. 16; Simkotu, No. 119; Kiorz, No. 
54), but so far no satisfactory conclusion as to their origin has been 
arrived at. The conditions are here very complicated and obscure. 
The point of greatest importance is to ascertain the relations between 
the various ducts of the hermaphrodite forms and the simple efferent 
apparatus of the dioecious forms and finally to trace the former to the 
latter. We cannot state definitely that the separation of the sexes ix 
the primitive condition, although this seems highly probable, since the 
older Gastropods (the Diotocardia) are dioecious and the most special- 
ised forms (Opisthobranchia, Pulmonata) are hermaphrodite. As the 
accounts so far published do not enable us to obtain a clear concep- 
tion of the development of the hermaphrodite genital organs, it is 
only possible to consider them by the light of the better understood 
development of the dioecious Prosobranchia. 

At the very outset of this investigation, however, a difficulty is 








asioned by the question as to whether the genital apparatus is 
derived from one common rudiment or from two or three distinct 


THE FORMATION OF THE ORGANS—THE GENITAL ORGANS. 221 


rudiments. The whole apparatus, the yerm-gland included, has 
been derived from a single ectodermal thickening which extends and 
becomes differentiated later (RouzauD). ‘There can, however, be 
but little hesitation in at once excluding this view, inasmuch as the 
hermaphrodite gland is, in any case, yielded by the mesoderm. [The 
yonai is probably derived from the apparently undifferentiated blasto- 
meres.} With regard to the ectodermal part, i.e. the efferent ducts 
and accessory structures, there may certainly be two distinct types 
of development according as the copulatory organ lies separately 
from the female genital aperture or is united with it in a common 
atrium. In the first case, the genital apparatus would, as in the 
Prosobranchs (Paludina), consist of three parts, riz., of the germ- 
gland, of the primary (nephridial), and of the secondary (ectodermal) 
efferent ducts together with the penis. This is evidently the case in 
Linnaea, as we may conclude from the observations of Ersia and 
Kuorz. 

The genital apparatus ‘of Limnwes appears as a rudiment even 
before the hatching of the yonng animal. 
an ectodermal invagination at the 
base of the right tentacle. The 
hermaphrodite duct arises inde- 
pendently of it as a strand-like 
structure. The mesodermal 
character which has repeatedly 
been assumed for it appears doubt- 
ful. We are inclined rather to 
consider it as ectodermal, a view 
which is supported in the literature 
on the subject. This strand is of 


‘The penis appears first as 


special importance, as it splits 
later into two parts, one of which 
represents the rudiment of the 
uterus and the other that part of 
the vas deferens which is known 
us the prostate (Fig. 103, »f, w/). 
The hermaphrodite gland arises 
independently of this strand from 


the mesoderm [? primitive blastomeres} . 





ed/-- 


Fra, 103.— Diagrans representing a later 
stage in the development of the genital 
organs of a Pulmonate, alb, albumen- 
gland ; p, penis ; ra, spermetheca ; u/, 

d, vas deferens; 2, hermaph- 





te 4 Hy hermaphrodite duet ; 3 
rs ‘ant? , xenital apertures, 


A xhort process of the 


mesodermal rudiment yields the proximal portion of the efferent 
duct, while the distal part arises from the cellular strand mentioned 


above (Fig. 103, zy, Brock, Kiotz). 


The spermetheca becomes 


222 GASTROPODA. 


abstricted from the uterine portion of the common duct in a way 
similar to that in which the prostatic part of the vas deferens 
arose from it earlier. These abstrictions take place by means 
of longitudinal folds which grow into the common canal that arose 
when the strand became hollow. The albuminiparous yland arises 
in the form of a number of tubular outgrowths near the proximal 
end of the uterus (Fig. 103, ab). 


‘The origin of the male and female ducts through the division of a common 
tudiment may be demonstrated with some certainty in the various herma- 
pbrodite forms that have been investigated, When we take into consideration, 
in this connection, that, in the Opisthobranchia, the transmission of the two 
kinds of genital products takes place through « common duet (Fig. 104 B) 
and that, in the Palmonates also, their transmission takes place for a longer 
or shorter distance through the same duct, the division inte male and female 
duets occurring later (Fig. 104 C), we may with safety assume that these two 
ducts have arisen phylogenetically also through the splitting of one duct and 
that thus the Opisthobranchs exhibit the more primitive condition. If we 
then take one step further back, we may trace back the common efferent duct 
of the hermaphrodite Gastropoda to the efferent apparatus of the dioecious 
forms. We here naturally presuppose that we regard the separation of the 
sexes as the primitive condition and hermaphroditism as the derived condi- 
tion. Since also in dioecious animals, ova are often met with in the testix 
and rice versd, and, further, in other divisions of the animal kingdom in which 
separation of the sexes is the rule, hermaphroditism occurs in a few highly 
differentiated forms, such an assumption is not inadmissible. 


The question now arises how the connection is established between 
the penis and the genital aperture in those forms in which these two 
arise separately. In the Opisthobranchia, a groove runs from the 
aperture of the common duct to the introvertible penis which here 
also is found near the right tentacle (Fig. 104 8). Where the com- 
mon duct becomes divided up into a female and a male portion the 
channel starts from the aperture of the latter, and, by the closure of 
the groove and its detachment from the ectoderm, the part of the 
vas deferens arises which lies nearer the penis, the process being 
similar to the formation of the secondary vas deferens in the Proso- 
branchia (Fig. 104 C). It is in any case probable that, ontogenetic- 
ally, the formation takes place in this way, although this has not yet 
been. proved. 


In Fig, 104 4-# we have attempted to give some idea of the way in which 
these processes may have taken place. The modifications brought about by 
the earlier closing of the channel, by the later separation of the male duct, 
and by the invagination, in the course of ontogeny, of the rudiment of the 
penis (2) are self-evident, 


THE FORMATION OF THE ORGANS—THE GENITAL ORGANS. 223 


Tn cases in which, finally, the penis becomes shifted towards the 
female genital aperture, and the two join to form a common atrium, as 
in the Stylommatophora (Fig. 104 £), the rudiment of the ectodermal 
parts form from a common rudiment. In these eases, we have only 
to distinguish between the mesodermal rudiment of the hermaphro- 
dite gland (or the hermaphrodite organ) and the ectodermal rudiment 
of the primary and secondary ducts and copulatory apparatus. 


"The significance of these processes is still little understood, and it is doubt- 
ful if ontogeny will throw much light upon the subject. Summaries and 
critioal desoriptions of these ontogenetic processes are given by Rouzaun, 
Brock, Semper (No, 117), Scurmmenz (No. 107), and Kuorz (No, 54). 





Pra. 104,—.A-K, diagrams illustrating the manner in which the genital apparatus opens 
Bak ab Were’ ontogenetic stages. A, in n dioccious Gastropod; Bed, in hetma- 
Phrodite Gastropods. os, ovosemninal duct ; p, peuis; wd, vas deferens: 8 and 9 
genital apertures or the terminal portions of the corresponding efferent dnots, 


[The i of the complicated conditions met with in the herma- 

sipeclialia of the Sige saree and Pulmonata is one of those 

upon which ontogeny throws little light, We think there 

can be doubt that it will be found more profitable to leave the onto- 

side alone and accept the obvious and comparatively simple interpre- 
offered Wy the study of the comparative anatomy of these organs. 

ee existing Gast we seem to have every stage in the development of 

genil 





SSS founda many 
‘is in many of the hermaphroditic Tectibranchia, which, how- 
ever, show 


— 


224 GASTROPODA. 


groove-like vas deferens leads down to an introvertible cephalic pen' 
next change which occurs is the closure of the groove-like vas deferen: 
separation from the ectoderm asa tube. This brings us to the condition seen 
in Actaeon and then to the Basommatophorous Pulmonata, where the male 
aperture is distinct from the female. The only break in the series is that 
between the Basommatophorous and Stylommatophorous Pulmonata, due to 
the development in the latter of wascondary oviduct which extends from the 
primitive genital aperturo (now closed) down to the cephalic penis, and opens 
with that structure through an atrium. With regard to the origin of this 
secondary oviduct, two possible interpretations present themselves, one being 
that the secondary oviduct has arisen as a groove, like the vas deferens, and, 
like that structure, has secondarily closed together with the primary genital 
aperture, so that both products are discharged by a single anterior aperture. 
or it may be that the primitive genital orifice has shinies by growth down the 
xide of the body towards the penis and. finally, an atrial involution has caught 
up both these apertures, so that they now communicate with the exterior by 
common aperture. The fact that these stages are not recapitulated in the 
ontogeny is not, we think, of much importance, for we know that ontogeny 
by no means always recapitulates phylogeny, and that this is especially the 
case in forms which, like these Mollusca, have a considerable amount of yolk.— 
Ep.] 




















LITERATURE, 






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a 


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26. Exeta, H. Beitriige zur Anatomie und Entwicklungageschichte 
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Eruanagr, R. v. Zur Entwicklung der Paludina vivipara. 
Th. I. und II. Morphol. Juhrb, Bd. xvii. 1891. 

28. Eruanogr, R. v.  Beitrage zur Entwicklungsgeschichte der 
Gastropoden. Erster Theil. Zur Entwicklung von Bythinia 
tentaculata. dfitth. Zool. Stat. Neapel. Bd. x. 1892. 

29. Kruanagr, R. v. On the paired Nephridia of Prosobranchs, 
the homologies of the only remaining Nephridium, etc. 
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30. Fisongr, H. Sur le développement du foie chez les Nudi- 
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31. Fou, H. Etudes sur le développement des Mollusques. Hétéro- 
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33. Fou, H. Sur le développement des Ptéropodes. Archiv. Zool. 
exp. gen, Tom. iv. 1875. 

33. Fon, H. ftudes sur le développement des Gastéropodes 
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34. Fratssz, P. Ueber Molluskenaugen mit embryonalem Typus. 
Geitschr, f. wiss, Zool, Bd. xxxv. 1881. 

35. Ganin, M. Zur Lehre von den Keimblittern bei den Weich- 
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No.l. Zeitechr. f. wise, Zool. Bd. xxii, 1872. 

36. GrarnnauR, C. — Reitrige aur Entwicklungsgeschichte der 
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37. Quawsnaur, C. Untersuchungen iiber Pteropoden und Hetero- 
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38. Growney, C. Zur Morphologie des Fusees der Hetel len. 
Ard, Zool, Inst. Unie. Wier Bd. vii, 1888. 

39. Groregy, C. Zur Morphologie des Preropodenkirpers. 471). 
Joe, Dist. Caie, Wein, Bd. viii, 1889. 

Notes on the development of Mollusea. Qu rt. 


27. 








Porpura, ava. Map. Nas. Hie. 3). Volo sii, 1883. 

42. Hescumas is PL The origin and development of the 
central nervous system of Liman maximus, Bal, Mux Comp. 
ww. Harvari Co Volos 1290, 






LITERATURE, 227 


43. Hineer, C. Beitriige zur Kenntniss des Gastropodenauges. 
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44. Jaerive, H. von. Entwicklungsgeschichte von Helix. Jen. 
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45. Jueninc, H. vox. Vergleichende Anatomie des Nervensystems 
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46. Jwenine, H. von. Ueber den uropneustischen Apparat der 
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47. Jugrine, H, von, Die Stellung der Pteropoden. Machrichts- 
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48. Juenina, H. von. Sur les relations naturelles des Cochlides 
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49. Jourpats, 8. Sur le développement du tube digestif des 
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1834, 

50. Jourpars, 8, Sur les organes segmentaires et le podocyste des 
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51, Joveux-Larroure, J. Organisation et développement de 
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52. Kererstem, W. Malacozoa cephalophora, Sronn’s Klassen 
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53. Kurerstern, W., und Exavers, HE, Beobachtungen iiber die 
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54. Krorz, J. Beitrag zur Entwicklungsgeschichte und Anatomie 
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55. Kxrrowrrscos, N. Zur Entwicklungsgeschichte von Clione 
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56. Koxen, EB. Ueber die Entwicklung der Gastropoden von Cam- 
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57. Koren und Danterssex. On the development of the Pectini- 
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58a. Kroun, A. Beitriige cur Entwicklungsgeschichte der Hetero- 
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ai 


228 


GAB8TROPODA. 


58+. Kroun, A, Ueber die Schale u. Larven des Gasteropteron. 


59. 


60. 


61. 


64, 


66, 


7. 


72. 


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Archiv. f. Naturgesch. Jabrg. xxvi. 1860. 
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LITERATURE, 229 


74. Mazzanenut, G. Intorno al preteso occhio anale delle larve 
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79. Miter, Jon. Bemerkungen aus der Entwicklungsgeschichte 
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80, Norpmany, A. y. Essai d’une Monographie du Tergipes 
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83. Parrex, W, The embryology of Patella. Arb. Zool, Institut 
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84, Pecsenreer, P. Sur le pied et la position systématique des 
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85. Petseneer, P. Sur I'wil de quelques Mollusques Gastropodes, 
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86. Pexsexerr, P. Sur la dextrosité de certains Gastropodes dits 
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87. Perrier, R. Recherches sur l'anatomie et l'histologie du rein 
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88. Preirrer, C. Systematische Anordnung und Beschreibung 
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89. Puate, L. Studien uber opisthopneume Lungenschnecken, 
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90. Rapp, ©. Die Ontogenie der Siisswasser-Pulmonaten. Jen. 
Zeitachr. f, Naturw. Ba, ix, 1875, 


— 


280 


GASTROPODA. 


Q9la. Rasy, C. Ueber die Entwicklung der Tellerschnecke. 


Morphol. Jahrb. Bd. v. 1879. 


916. Rant, C. Ueber den ‘pedicle of invagination” u. das Ende 


92, 


93. 


94. 


95. 


101, 


103. 


los. 
is 


Wh. 


10s. 


der Furchung von Planorbis. Morphol. Jahrb. Bd. vi. 
1880. 

Rast, C. Beitriige zur Entwicklungsgeschichte der Proso- 
branchier. Sttzungeber. der k. Akad. Wiss. Wien. Bad. Ixxxvii. 
Abth. iii, 1883. 

Rao, F.  Studii sallo sviluppo della Chromodoris elegans. 
Atti R. Accnd. Sci. (2). Vol. i. Napoli, 1888. 

Rovzaup, H. Recherches sur le développement des organes 
génitaux de quelques Gastéropodes hermaphrodites. Travaux 
Lab. Zool. Faculté Sci. Montpellier, 1885. 

Résuter, R. Die Bildung der Radula bei den cephalophoren 
Mollusken. Zeitechr. f. wiex. Zool. Bd. xli. 1885. 


. Riioxgr, A. Ueber die Bildung der Radula bei Helix pomatia 


23 Ber. Oberheextsch. Gesellech. fiir Natur und Heilkunde. 
Giexsen, 1883. 


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Amer, Nat. Vol. xxiii. 1889. 

Sauensxy, W.  Beitrige zur Entwicklungageschichte der 
Prosobranchier.  Zeitechr. f. wise. Zool. Bd. xxii. 1873. 
Sauensxy, M. Etudes sur le développement du Vermet 

Archiv. Biol, Tom, vi. 1885. 





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Biel, Central, Bdov. 1885-6. 

Sarasix, P.  Entwicklungsgeschichte der Bithynia tentaculata. 
Artveit. Zool. Inst, Wurzburg. Bd. vi. 1882. 

Sarasis, P. vu. F. Aus der Entwicklungageschichte der Helix 
Waltoni.  Ergedu. Nuturi. Forsch. raf Ceylon. Bd.i. Heft. 
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Sarasix, P. cv. F. Ueber awei parasitische Schnecken. 
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Sars, M. Zur Entwicklungsgeschichte der Mollasken und 
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Sars, M. Beitras zur Entwicklumggreschichte der Moitasken. 

§ Naterwat. Rio 1840. . Supplementary paper 
 Biosi 1S. 

Swuarrepw, Mo Schimkewiteh.: Sur ie déveloprement do 
ear des Motuayres rolmeress ete. Zed de Jakeg. 
Iss. 








LITERATURE. 231 


107. Scuiemenz, P. Die Entwicklung der Genitalorgane bei den 
Gastropoden. Biol, Centralbl. Bd. vii, 1887-8. 

108, Scmremenz, P. Kritische Betrachtungen uber die parasitischen 
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109, Scusupr, F. Die Entwicklung des Fusses der Succineen. 
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110. Scuapt, F. Studien zur Entwickhingsgeschichte der Pul- 
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Nat, Gea, Univ. Dorpat. Ba, viii. 1891, Ann, and Mag. 
Nut. Hist, (6). Vol. viii. 1891, 

111. Semsnpr, O. Ueber die Entwicklung von Limax agrestis. 
Arch. f. Anat. und Phys, 1851, 

112. Scuwemer, A. Ueber die Entwicklung der Phyllirhoe 
bucephalum. Avehiv. f. Anat. und Phye, 1858, 

113. Scuunrze, Max. Weber die Entwicklung des Tergipes 
Jncinulatus, Archiv. f, Naturg. Jahrg. xv. 1849. 

114. Setenca,E, Entwicklung von Tergipes claviger. Néederldnd 
Archiv. f. Zoologie. Ba. i, 1871-3. 

115. Setenka, E. Die Anlage dér Keimblitter bei Purpura lapillus, 
Niederlind Archiv. 7. Zoologie. Bad. i, 1871-3. 

116, Semper, ©. Entwicklungsgeschichte der Ampullaria polita, 
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117, Semrer, C. Ueber Brocks Ansichten iiber Entwicklung des 
Molluskengenitalsystems. Arb, Zool. Inst. Wiirzburg. Ba. 
viii, 1887, 

118. Semper, K. Die natiirlichen Existenzbedingungen der Thiere. 
Leipziy, 1880. 

119, Sotnorx, H. Weber die Genitalentwicklung der Pulmonaten, 
etc. Zeitechr. f. wise. Zool. Bd. xlv, 1887. 

120. Stunorn, H. Ueber das Vaginulidengenus Atopos, Zeitschr, 
f- wis. Zool. Ba. li. 1891. 

121. Sounzyer, M. Hétéropodes. Voyage autour du monde 1836-7 
sur la Corvette La Bomite, etc, Tom, ii. (with atlas). Paris, 
1852. 

122. Srxnoex, J. W. Die Geruchsorgane und das Nervensystem 
der Mollusken. Zuitsehr. f. wiss. Zool. Bd. xxxv. 1881, 

1234. Sreraxor, P. Ueber Geschlechtsorgane und Entwicklung 
von Ancylus fluviatilis, Mem. Acad, Imp. St. Petersbourg (7). 
Tom. x. No, viii, 1866. 

123b, Sruanr, A. Ueber die Entwicklung einiger Opisthobranchier, 
Zeitachr, f. wits. Zool. Ba. xv. 1865, 





(A 


232 


124, 


125. 


126. 


127. 


128. 


129. 


130. 


131. 


GASTROPODA. 


TrcHesg 8. I primi momenti dell’ evoluzione nei Molluschi. 
Atti R. Accad. Lincei (3). Mem. Vol. vii. Roma, 1880. 
TrincHeEse, S. Per la funna marittima italiana. Aeolididae 
e familie affini. Atti R. Accad. Lincei (3). Mem. Vol. xi. 

Roma, 1881. 

TrincuEsE, S. Ricerche anatomiche ed embriologiche sulla 
Flabellina affinis. Mem. R. Acca. Sci. dell’ Inatituts di 
Bologn (4). Tom. viii. 1887. 

Voat, C. Recherches sur l’embryogénie des Mollusques Gaste- 
ropodes. Ann. Sci. Nat. Zool. (3). Tom vi. 1846. 

Voat, C., und Gecenpaur, C. Beitrag zur Entwicklungs- 
geschichte eines Cephalophoren. Zeitschr. f. wins. Zool. 
Bd. vii. 1856. 

Vorat, W. Entocolax Ludwigii, ein neuer seltsamer Parasit 
aus einer Holothurie. Zeitechr. f. wise. Zool. Bd. xlvii. 
1888, 

Warneck, A. Ueber die Bildung und Entwicklung des 
Embryos bei Gasteropoden. Bull. Soc. Imp. Natural. 
Moscou. Tom. xxiii. 1850. 

Woxrson, W. Die embryonale Entwicklung des Limnaeus 
stagnalis. Bull. Acud. Sci. St. Petersboury. Tom. xxvi. 1880. 


APPENDIX TO LITERATURE ON GASTROPODA. $ 


I. Buocu, L. Die embryonale Entwicklung der Radula von 
Paludina vivipara. Jew. Zeitachr. f. Nature. Bd. xxx. 
1896. 
Il. Bouran, L. Sur le développement de l’Haliotide. Compt. 
rend, Assoc. Franc. Tom, ii. 1892. 
III. Boutan, L. Sur le développement de I’Acmaea virginea. 
Compt. rend. Acad. Sri. Paris. Tom, exxvi. 1898. 
IV. Conkuin, E. G. The Embryology of Crepidula. Journ. 
Morphol. Vol. xiii. 1897. 
Vv. Crampton, H. E. Reversal of Cleavage in a Sinistral 
Gastropod. Ann. NV. York. Acad. Vol. viii. 1894. 
Vl. Drew, G. A. Some observations on the Habits, Anatomy 
and Embryology of members of the Prosobranchia. Anat. 
Anz, Bd. xv. 1899. 
VII. Ertancer, R. von. Bermerkungen zur Embryologie der 


Gasteropoden. Urnieren. Biol. Centralbl. Bd. xiii. 
1893. Bd. xiv. 1894. Bd. xviii. 1898. Also Archiv. 
Biol, Tom, xiv. 1895. : 


LITERATURE, 233 


VIL Ercaxcer R. voy. Mittheilimgen tber Bau und Entwick- 
lung einiger marinen Prosobranchier. I. Ueber Capulus 
hhungaricus. Zool. Anz. Jahrg. xv. 1892. 

1X. Brnancer, R. von. Ueber einiger abnorme Erscheinungen 
in der Entwicklung des Cassidaria echinophora. Zool. 
Anz, Jabrg. xvi. 1893. 

X. Extanomr, R. von. Zur Bildung des Mesoderms bei des 
Paludina vivipara. Morphol. Jahrb, Bd. xxii, 1894. 

XI. Fuarra, T. Preliminary note on the mesoderm formation 
of Pulmonata, Zool. May. Tokyo. Tom. vii. 1895. 

XI. Heymons, R. Zur Entwicklungsgeschichte von Umbrella 
Mediterranea. Zeitsch, f. wiss. Zool. Bd. lvi. 1893. 

XIIL, Honams, 8, J. The cell-lineage of Planorbis. Zool. Bull, 
Vol. i. 1897. XIIL a. Ancynus, Amer. Nat. 1899. 

XIV. Koror, C. A, On the early development of Limax. Bud. 
Mus. Coup, Zool, Havard. Vol. xxvii. 1895. 

XV. Mazzarenut, G. Bermerkungen iiber die Analniere der 
freilebenden Larven den Opisthobranchies. Biol. Centralbl, 
Ba. xviii, 1898. 

XVI. Mazzarenot, G. Monografia delle Aplysiidae del Golfo di 
Napoli (sistematica, biologia, anatomia, fisiologia, ed 
embriologia). Mem. Soc, Ztal, ‘Tom. ix, 1893, 

» XVIL Mzrssexnenmenr, J, Entwicklungsgeschichte von Limax 
maximus L. Theile i., und ii. Zeitschr. f wiss. Zool. 
Ba. Ixii. und Ixiii, | 1898. 

XVILL. Murssennerwen, J, Zur Morphologie der Urnieren der 
Pulmonaten, Zeitachr. f. wise, Zool. Bd. Ixy. 1899. 

XIX. Poate, L. Bermerkungen iiber die Phylogenie und die 
Entstehung der asymmetric des Mollusken. Zool. Jahrb. 
Anat, Bad. ix. 1895. 

XX. Scamipr, F. Beitrige der Entwicklungsgeschichte der 
Stylommatophoren, Zool. Jahrb, Anat. Ba. viii. 1895. 

XXL. Scmmopr, F. Die Furchung und Keimblitterbildung der 
Stylommatophoren. Zool. Jahrb, Anat, Ba. vii, 1894, 

XXIT. Smrrore, H. Mollusea, Bronn’s Klass. u, Ordn. d. Phier- 
reiehs. Bad. iii. Lief. 22 und 23. 1896, (Summary of 
all recent views on the asymmetry of the Mollusca with 
complete literature, ) 

XXIIL Siseote, H. Weber die miogliche oder wahrscheinliche 
Herleitung der asyinmetrie der Gastropoden. Biol. 
Centralbl, Bad. xviii. 1898. 





Di 


284 GASTROPODA. 


XXIV. Taree, J. Zur Phylogenie der Gastropoden. Biol. 
Centrabl. Bd. xv. 1895. 

XXV. Ténnicgs, C. Die Bildung des mesoderms bei Paludina 

vivipara. Zettechr. f. wiss. Zool. Bd. lxi. 1896. 

XXVI. Vieurer, C. Contribution a l'étude du développement 
de la Tethys fimbriata. Archiv. Zool. exper. (3). Tom. 
xvi. 1898. 

XXVIL Wierzessxi, A. Ueber die Entwicklung des Mesoderm bei 
Physa fontinalis. Biol. Centralbl. Bad. xvii. 


CHAPTER XXXIII. 


CEPHALOPODA. 


Systematic :— 

I, TerraBrancaia, with two pairs of gills, two pairs of auricles, 
two pairs of kidneys, external chambered shell and a large number 
of tentacles round the mouth. Funnel consisting of two lobes ; with- 
out ink-sac. 

1. Nautiloidea. 
2. Ammonoidea. . 

Il. Drprancuia, with one pair of gills, one pair of auricles, one 
pair of nephridia, with internal shell, the chambers of which are 
seldom distinct (Spirula, Belemnites) often reduced or absent. Round 
the month eight to ten arms. The two halves of the siphon united 
to form a tube ; an ink-sac generally present. 3 

1, Decapoda, with ten arms. 

(a) Phragmophora. 
Spirulidae. 
Belemnitidae. 
Belemnoteuthidae, 
Acanthoteuthidae. 

(B) Oigopsida. 
Ommastrephi:lae. 
Onychoteuthidae. 
Cranchitdae. 
Chiroteuthidae. 

(c) Myopsida. 
Loliginidae. 
Sepioluiae. 
Sepiidae. 

2. Octopoda, with eight arms. 
Cirrhoteuthidae, with fins. 
Philonexidae, Tremoctopus, Philonexis. 
Argonautidae. 

Octopodidae, Octopus, Eledone. 


236 CEPHALOPODA, 


1, Oviposition and the Constitution of the Egg. 


The egg of a Cephalopod, before it is mature and at the time of 
oviposition, is surrounded by « protective envelope which, in the 
different forms, may assume very various shapes. A large number 
of eggs are usually laid at one spot, forming a large mass of spawn. 

In Sepia, the eggs constituting the mass are distinct from one 
another, Each of them is surrounded by a compact, spindle-shaped, 
black capsule of leathery consistency which, at one end, runs out 
into a process, by means of which the eggs are attached close to one 
another to some firm object. The egg-capsules attain about the 
size of a hazel nut. In Rossia and Sepiola * also, the eggs are laid 
separately and are attached to some object or else to each other, 
but the envelope is less thick and is even transparent (Sepiola). 
The eggs of Lotigo, on the contrary, are laid in gelatinous tubes, 
each tube containing a large number (in Loligo vulgaris, as many 
4s eighty or more), The tubes are attached by one end to some firm 
substratum. As they stand out from their point of attachment 
radially, they form a kind of tassel. Such large tassels are found 
attached to plants, pieces of wood, stones, etc. 

The eggs composing a mass of spawn, resembling Cephalopodan 
spawn—dredged by Grenacuer off the Cape de Verde Islands and 
attributed by STEENSTRUP to one of the T'euthidae (i.¢., to a form 
something like Onvmastrephes, No. 14), are also surrounded by a 
gelatinous mass, but are not contained in distinct tubes. This spawn 
forms @ gelatinous mass 75 cm. long and 15 em. thick which 
resembles sausage. Within the gelatinous eover, the violet-coloured 
spherical eggs are arranged in fairly regular spiral coils, their number 
amounting to thousands. Each egg, as in Zoligo, is surrounded by 
a firm envelope. A similar enyelope which must be regarded as the 
chorion (p. 246) ulso surrounds the eggs of the Octopoda. 

In Octopus and Argonauta, the chorion of the oval egg is drawn 
out into a stalk. The stalks of a number of eggs become connected 
various authts (2 van evpeay Mevachnorh Uesow) flee rato to & 
species of Loligo: further obscurity being due to the fact that the masses of 


spawn found and investigated have been attributed to Cephalopods to which 
the did not belong. Hgg-masses produced by Loligo vulgaris, w are 
said to have been ascribed to Ommastrephes sagitiatus, a form to 
the group of the Oigopsida. This led to the inaccurate conclusion forms 
remote from one another in systematic position showed ut in 
their development. According to Sremysrrvr, this resemblance in 

ment is due rather to the fact that they all belong to the genus Lolago, and 
theoretical conclusions founded on this similarity would thus be of no value. 


OVIPOSITION AND THE CONSTITUTION OF THE EGG. 237 


together, large egg-bundles being thus produced, the bundles again 
uniting to form aciniform masses (Argonauta). In Hledone also, the 
threads from the chorion of the long eggs unite to form a stronger 
strand, which then becomes attached to the substratum (Jousry, No. 
21). We have ourselves found that the eggs of Eledone (apparently 
£. moschata) ave attached by their stalks to the substratum in pairs 
or in groups of two or four, A number of such groups are found in 
close juxtaposition, giving rise to a spawn-mass consisting of sixty 
to seventy eggs. The long ovate eggs of this Eledone are very large, 
measuring (including the envelope) 15 mm. in length, while those 
described by Joupin are only about half this length, 

_In Sepia, the stalks of the individual eggs become twisted together, 
the result being a rather large strand of eggs closely arranged round 
a central axis. These strands are attached to rocks, the female 
covering them with her body and, by the promotion of a continuous 
flow of water, assisting in their development (ScHMIDTLEIN).* The 
egus of Aryonuuta are still further protected by the mother, as the 
spawn is attached to the inner side of her shell and carried about by 
her. [Nautilus (Wituey, No. IV.) lays solitary eggs of great size, 
each egg-capsule measuring 45 mm. by 16 mm, and containing one 
egg 17 mm. long and very rich in yolk.—En.] 

The capsules or the gelatinous masses which surround the eggs and the 
cementing substance by means of which they are attached are secreted by 
special glandular portions of the oviducal wall and by the nidimental glands. 
Where there is no such special development of glands in the genital apparatus, 
a5 in the Octopoda, the eggs wre surrounded by the chorion alone. This latter, 
however, is also found round eggs surrounded by firm capsules or gelatinous 
masses. At the animal pole of the egg, the chorion is perforated by the 
amicropyle (Fig. 105, m). 

‘The conditions under which copulation and the fertilisation of the egg take 
place in the Cephalopoda ure so peculiar that we must devote some attention. 
ftothem, In the Octopoda, fertilisation probably takes place in the oviduct. 
‘The spermatophores are introduced by the help of the hectocotylised arm into 
the mantle-cavity or the oviduct. In Argonauta, Tremoctopus and Philonexis, 
it is well-known that the detached hectocotylised arm of the male is found in 
‘the mantle-cavity of the female. The female in the two last-mentioned forms 
possesses a receptaculum seminis in the form of an outgrowth of the oviduct 
which serves for the reception of the sperm (Brock). 

‘Tn the Oigopsida, as in the Octopoda, fertilisation takes place within the 
mantle-cavity, the spermatophores being introduced into that cavity and 
Sttached to various parts of its inner wall, Among the Myopsida, in the 


OSD ag ge Iona die rn mr und Ejablage verschiedener Seethiere. 
Zool. . Neapel, Bd, i. 1879. 


238 CEPHALOPODA. 

female of Hossia (according to the verbal statements of F. C. v. MarResrTHaL) 
there is a well-marked area near the mouth of the oviduct within which the 
spermatophores sre attached. In the nearly related Sepiola (also according 
to researches by v. MazReNTHAL not yet published), there is a pouch-like 
depression of the integument lying laterally to the mouth of the oviduct 
for the reception of the spermatophores; this has been hitherto erroneously 
regarded as s terminal portion of the oviduct itself. 

In the other Decapoda, copulation takes place in an exceedingly peculiar 
way, the spermatophores not being brought into the mantle-cavity, but 
attached near the mouth on the outer integument of the lip (buccal membrane) 
of the female. Glandular invaginations of the integument, in which the 
spermatozoa that escape from the spermatophores are stored, are found in 
this position in Sepia and Loligo (ViaLLeTox), in Sepioteuthis and no doubt 
also in the other genera (v. MazRENTHAL). 

In this last case, it is evident that fertilisation takes place only when the eggs 
are expelled through the funnel and are retained for s time near the mouth by 
the arms. The future leathery egg-capsule (of Sepia) is either still soft at 
this time and penetrable by the spermatozoa (?) or only forms after these 
have penetrated the egg (through the micropyle of the chorion), the still fluid 
glandular secretion being subsequently poured over the eggs by the funnel. 
This would then also no doubt apply to the gelatinous mass (in Loligo). It 
is an interesting fact that artificial fertilisation of mature eggs taken from 
@ female Loligo Pealii was brought sbout by means of seminal fluid found in 
the spermatophores of the buccal 
membrane (WataskE, No. 50). The 
same conditions sre found in Rossia. 


The eggs of the Cephalopoda 
are unusually rich in yolk, and 
consequently attain a considerable 
size, a point in which they are 
essentially distinguished from 
those of other Molluscs. The 
eggs of Sepia, for instance, are 
fully as large as a pea (Sepia 
officinalis). The eggs of Eledone 
may be still larger and are ex- 
ceedingly rich in yolk (p. 237). 





Fio, 105,-—The upper pole of the ogg of 
*¢Aryonauta argo in optical section. 
71, before fertilisation; 8, shortly 

after fertilixation (after Ussow). ch, 









chorion, yolk : bs, germlise; mm, 
micropyle ; pl, peripheral protoplasm : 
Ph,fpolar bellies ace 


longitudinal diameter. 


The eggs of other Cephalopods, 
such as Loligo and Octopus, are 
less rich in yolk and therefore 
distinctly smaller ; those of Aryo- 
nauta are even rather small, 
measuring, however, 1:3 mm. in 


The food-yolk, which consists of rather fine 


OVIPOSITION AND THE CONSTITUTION OF THE EGG, 239 


granules, always constitutes by far the greatest mass of the egg. The 
egg, in shape, is usually oval (Loligo, Eledone, Octopus, Argonauta) 
or spherical, as in Sepia and the Cephalopods investigated by 
GrenacuEn (p. 267). The massive food-yolk is completely invested 
by « comparatively thin layer of the formative protoplasm, which 
thickens to form a dise-shaped accumulation at the upper or future 
animal pole of the egg beneath the micropyle. This is the future 
germ-dise (Fig. 105, ks) and is sharply marked off from the food-yolk. 
In consequence of this peculiarity, and others to be described later, 
the eggs of the Cephalopoda afford the most perfect examples of 
meroblastic cleanage. 





wv 
Pro, 106,—1 tle longitudinal sections thro the egg of Loligo Peadii (after 
Warainy 5B ia mei tlt, aa oi mt ti ok 
eo re 
; While. tin food-york ia aadeL. a, decal thier ¢, ventral alder 
; 0, anterior ; /, lef ee 


A bilateral symmetry can be recognised not only in the early stages 
of cleavage but even before cleavage sets in; this symmetry bears a 
definite relation to the later development of the embryo. In the oval 
‘egys of Lolige Pealii, it is expressed not only in the form of the egg, 
‘but also in the way in which the germ-disc spreads over it (WaTASE, 
‘No. 50). The eggs of this Cephalopod appear somewhat flattened on 
one side while, on the opposite side, they are arched (Fig. 106 B). 
‘The positions of the anus and the mouth in the embryo correspond 
‘to these two sides. At the part which becomes the anterior end (vo), 
the protoplasm of the germ-dise extends further down towards the 
‘equator than on the opposite side (4). The germ-disc, however, 


ma CEPHALOPODA. 


syrenin ty right and left for an equal distance (Fig. 106 A, r and /). 
A conuparinm of Fig. 106 4 with the median sagittal sections of 
later embrymmic stages (Figs. 132, 133, p. 282) shows that the 
animal pole of the egg (¢) corresponds to the area of the dorsal 

. Murface, the vegetative pole (c), on the contrary, to the ventral 
surface, 

In the yerm-dise we find the egg-nucleus and later the first cleay- 
age-nucleus, Neither of these, however, quite coincides with the 
animal pole of the germ-dise (Fig. 105 A) but occupies a somewhat 
oxcentric position, i.«., it is slightly nearer the posterior edge of the 
dine, The nucleus appears to be surrounded by a more hyaline zone 
of protoplasm which passes externally into a more granular proto- 
plasm, The protoplasm of the germ-disc is in any case distinguished 
hy its granular character from the thin protoplasmic layer that 
surrounds the whole egg. The thickness of the disc appears to vary 
in different casos, so far as can be gathered from the statements of 
authors, This is perhaps to be accounted for by the various stages 
of development at which the disc is represented. 

A vitelline membrane is apparently never developed in the eggs of 
the Cephalopoda. The mombrane, which is perforated by the micropyle 
anc in often very tough, is secreted by the follicular epithelium (Ussow, 
ViaLLETON) and may therefore be termed the chorion. Between this 
ogg-nhell and the surface of the egg there is a somewhat wide space 
filled with clear albuminous fluid. This enables the embryo to extend 
considerably within the chorion, which is itself said to be extensible, 
and thus to admit. of further growth on the part of the embryo. 

At the animal pole, in the mature egg, there are two polar bodies, 
one of which has been observed to divide (Loligo and Argonauta) and 
ive rive to a third body (Fig. 105, rk), Such division is said by 
VIALLETON not to oceur in Sepia, but the fact that one of the two 
polar bodies possesses two nuclei shows that these bodies, even in 
Sepia, are quite normal, VIALLETON denies that there is any con- 
atant relation between the polar bodies and the first cleavage-plane, 
but the deviations from such a relation are very rare, and from his 
own figures and those of other authors this line of cleavage is seen to 
oeour in the closest proximity to the polar bodies. 


& Cleavage and Formation of the Germ-layers. 





The cleaene of the on: ts incomplete, a fact connected with the 
great abundance of the food-yolk in it and the distribution of this 





CLEAVAGE AND FORMATION OF THE GERM-LAYERS. 241 


and of the formative yolk ; cleavage is af first limited to the germ- 
dise. The conditions of this process therefore differ essentially from 
those in the other Mollusca, The principal features of these pro- 
cesses have been known for many years, being described in Kénni- 
keR’s famous work on the development of the Cephalopoda (No. 24). 
‘These investigations which, from the nature of the case are far from 
being exhaustive, appeared in 1843, and were followed by observa- 
tious made by Boprerzxy (No. 4), Ussow (Nos. 44-46), VIALLETON 
(No. 48) and more recently by WATAsE (No. 50). We shall here 
follow the last-named author, dwelling especially on the detailed 
descriptions of the processes of cleavage in Loligo Pealii as given by 
him and of Sepia officinalis as described by Vianueton, So far as 


4 B 
L I 
e ee 
Z 





Pie. 107.— Se reesiardl the polar Voalec (th after ee first (J) and second (/7) 
js at present known, cleavage seems to take place in the different 
Cephalopods in very much the same way. 

The spindle of the first cleavage-nucleus which is preparing for 
division lies with its longitudinal axis running from right to left 
(Warase), and therefore in the plane depicted in Fig. 106 4.* 
It therefore, curiously enough, does not appear to lie, according to 
the usually accepted rule, in the direction of the widest extension of 
the formative protoplasm. 

The first line of cleavage runs, in correspondence with the position 
of the spindle, from before backward, cutting the axis of the spindle 
at right angles. The first furrow thus lies in the median sagittal 


* Of. p. 239 on the bilateral symmetry of the egg before cleavage. 
R 


242 2 CEPHALOPODA, 


plane of the egg or later embryo, 7e., in the plane given in Fig. 106 
B. This first furrow (1) above which the polar bodies are, as a rule, 
found (Figs. 107 and 105 2, rh), starts from the middle part of the 
germ-disc where the cleayage-nucleus lies and is continued to the 
periphery of the disc. It cuts deepest in the centre of the dise, 
dividing the whole of the protoplasm at this point into two segments 
(Fig. 106 B), while, further back and especially beyond the actual 





Fro. 108. —1 of Lotiyo Peatii representing various stages of the cleavage of the 
-disc, the bilateral of which can be after W. a. 
Se eae ogee kath fee 


disc where it is also prolonged (Figs. 107 and 106 A), it forms 
merely « shallow groove in the formative protoplasm which vanishes 
towards the equator of the egg. The same is the ease with the next 
furrows which are like the first meridional lines of cleavage (Migs 
107 to 109), 

The second furrow runs at right angles to the first (Fig. 107 B, 
ZT). Tn consequence of the furrows passing beyond the germ-dise 





@LEAVAGE AND FORMATION OF THE GERM-LAYERS. 243 


into the thin layer of peripheral protoplasm, these first blastomeres 
as well as those that follow (Figs. 107 to 109) are not distinetly 
bounded externally but fade away into the peripheral protoplasm. 
‘This is still the with the peripheral cleavage-cells of later stages 
(Pigs. 108 @ to 111). Vianneron defines these as /asfocones ws 
opposed to the /axtomeres. 

A further step in the cleavage is marked by the breaking up of 
each of the four segments now present into two new segments (Figs. 





£™= 
Lor 





ay eS 
Pasi et ct at 

ihe sl {a directed upwards, and the posterior side downwards, ¢, leit side 

fright side; £-V, directions of the first five meridional planes of cleavage, 

109 A and 108 B). ‘Of these new furrows (J//' and JJ") only the 
anterior ones (7/7') make an angle of 45° with the median plane and 
therefore cut the two anterior segments into almost equal halves. 
‘The two posterior furrows (J//") ran somewhat parallel to the median 
plane (Figs. 105 2 and 109 4), and it thus happens that here, at the 
posterior part of the germ-disc, two narrow segments bounded by 
parallel sides are cut off. Through this course of cleavage, concerning 


he 





244 OEPHALOPODA. 


which observers are agreed, the germ-disc becomes markedly bilateral, 
a character which is retained in the later stages also (Figs. 108 and 
109 B and C, 110), the two segments mentioned above and the 
blastomeres that proceed from them retaining their characteristic 
shape, i.e., retaining their regular position with regard to the median 
plane, the other cleavage-cells also continuing to be symmetrically 
arranged with regard to that plane. 

The broad segments of the eight-celled stage (Figs. 109 A and 
108 B) are directed forward, the narrow segments, on the contrary, 
backward (Watase, Ussow). In this way the bilateral symmetry 
of the germ-dise after cleavage and the relation to the form of the 
adult animal are shown still more distinctly than in the egg before 
cleavage (cf. p. 239 and Fig. 106 4 and &). 


It should be added that ViaLLeTon also describes the striking bilateral 
symmetry of the germ-disc after cleavage which is evident from Fig. 109, but 
does not assume so definite a symmetry in the shape of the egg before cleavage. 
It may be more difficult to establish these points with certainty in the spheri- 
cal egg of Sepia. The identity of the median sagittal] line of the blastoderm 
with that-of the embryo which is emphasised by Ussow is also apparently 
assumed by VIALLETON as probable, so that, according to him also, the 
bilateral symmetry of the germ-dise after cleavage corresponds to that of 
the embryo. 

Since, in consequence of the continuous division of the cells, the shape of 
the germ-dise is less regular in the later stages (Fig. 111). it is very difficult 
to prove that the bilateral symmetry of the germ disc passes directly over 
into that of the embryo: this hax, indeed, not yet been exactly proved, so 
far as we can see. But the bilateral character of the germ-dise found in 
Cephalopods otherwise very different from one another (Loligo, Sepia, Argon- 
auta*) makes relation to the form of the embryo appear more than 
probable, and we must therefore for the present hold to the view of Watase, 
although, indeed, this seems to be somewhat conjectural. 








As cleavage advances further, an equatorial furrow cuts off from the 
two narrow posterior segments, towards the-middle of the germ-disc, 
two small blastomeres (Fig. 109 8); a continuation of this equatorial 
furrow cuts off, in Lolizo, similar blastomeres from the large segments 
in front (Fiz. 109 @). In Sepia, however, additional meridional 
furrows appear first and divide these segments into narrower sections 
(Fig. 109 B, 7V and V), after which they becéme divided by an 





* With regard to Argonauta, we have to rely on the statement repeatedly 
made by Ussow that he saw cleavage taking place, in the forms observed by 
him, in a similar manner to the above. A confirmation of these statements 
with respect to the Octopoda is, indeed, very desirable. With reference to the 
conjectural Sepiola, also investigated by Ussow, see the remarks made p. 296. 


CLEAVAGE AND FORMATION OF THE GERM-LAYERS, 245 


equatorial furrow. The two narrow posterior segments, so character- 
istic in shape and position, still remain unaltered even after this 
division, but two further blastomeres gradually become detached 
from them by equatorial division and pressed towards the centre 
(Fig. 109 €). 

The number of segments increases more and more through the 
‘ppearence of other furrows, some meridional and others equatorial 
(Figs. 108 @, 110). From the accounts of Kénntkex and ViannE- 
‘TON, it appears that the segments at the middle of the germ-dise are 
not at first in close contact with each other (Figs. 107 and 109). Ax 
cleavage advances, this space in the centre disappears. 


) ee 4 


rim 
Ah 
Fi6, 110, —Cerm-dise of Baer teal, at a later ee stars of cleavage, the bilateral sym- 








¢ blastomeres and peor ae a 
aici ae Yel ater Wotan). ry, ateror sh pnterr Pkt nates ei 


a symmetry evident up to this time and still visible in some- 
what Inter stages is still further heightened by the division of the cells taking 
place wt somewhat different times, a fact which finds expression in the 
conditions of their nuclei. Such a case is represented, for instance, 

110, in which the posterior colls lying near the middle line contain 

‘nuclei while the nuclei of all the other cells are found to be dividing. 

t is also frequent in the larger cell-complexes. The almost 
-dingrn “aspect thus produced corresponds, as Wavase expressly states, 


‘946 CEPHALOPODA, 


to the actual condition of the disc. This is also confirmed by Viatteron's 
earlier description (e.., Figs. 25 and 26, No. 48), in which the various condi- 
tions of the nuclei in symmetrical division are given. Further, whole 
complexes of cells such as the posterior cells or those of a luteral part may 
advance more rapidly in their division, whilst the division of others may. be 
retarded, this being again visible in the state of their nuclei. 

In the germ-dise depicted in Fig. 110 two complexes of segments lying 
symmetrically and marked off by the planes JJ and JJ7', are distinguished by 
the fact that the furrows lying between them are less distinct than those jp 
other parts of the germ-disc, These segments are thus shown to be connected 
together, and have most probably proceeded from the segments bounded by 
the furrows J7 and JZ7' of the stage represented in Fig. 109 4, which is passed 
through in Loligo and in Sepia in the same way (Warasr). Such a condition 
also renders the bilateral symmetry specially clear. 


bee 
bulev 





Fre. 101,—Germ f Sepia officinadie at a late stage of cleavage (after ViauuETos) 
A, blastomeres ; Ale, hlastocones ; «, yolk. 








Up to this point, the origin of the cells is clearly recognisable in 
their arrangement ; their position with regard to the middle line also 
is very regular, As cleavage proceeds further, and the blastomeres 
continually decrease in size, this regularity of form is no longer 
perceptible in the germ-disc, A certain regularity of position may at 
first be retained in the peripheral cells, especially in the blastocones, 
but even this is finally lost as the cells continue to inerease in 
number. The animal pole of the egy now appears covered by a 


CLEAVAGE AND FORMATION OF THE GERM-LAYERS. 247 


unilaminar “disc'’’* of polygonal plate-like cells (Fig. 111), The 
cells at the edge of the disc (blastocones), however, are not polygonal, 
having no outer edge (Fig. 111, b/c), but passing over into the 
remaining mass of formative yolk. In Fig. 111, a certain difference 
of size can be perceived in the blastomeres, but this apparently 
cannot yet be related with certainty to the later form of the embryo. 

The germ-dise spreads owt and increases in size as is evident in 
Figs. 107-111, at first no doubt chiefly at the expense of the formative 
yolk in contact with it; only later is the abundant food-yolk utilised 
us nourishment for the growing embryo. 





Fie, 112. —Germ-dise of Sepia officinalis at the commencement of the formation of the 
germ: fafter VIALLETON), f, yolk: ¢, unilaminar portion of the germ-dise : 
ed, (moultilaminar) portion of the yerm-dise (area opaca); #, cells in the 
act of separating from the gern-lisv. 


After the cleavage-cells have considerably increased in number, the 
peripheral cells somewhat change in shape; their free ends narrow 
and they show a tendency towards becoming detached from the 
germ-dise (Fig. 112 7). They finally become rounded off and move 
away from the disc. They are then found scattered round the latter 
at the surface of the food-yolk. It should here be mentioned that 


+ Phis so-called disc is actually a more or less arched cap. 


248 CEPHALOPODA. 


these cells, according to ViALLETON, wander beneath the cell-material 
of the germ-dise, there becoming arranged into a connected cell-layer 
which is said gradually to spread over the whole of the food-yolk. 
But this brings us to the formation of the germ-layers, and in order 
to comprehend this, we must first refer to another process and also 
mention the views which have hitherto prevailed on the subject. 

The problem of the formation of the germ-layers in the Cephalopoda 
must be regarded as exceedingly complicated. The fact that the 
significance of the different cell-layers forming in the germ has not 
been recognised and that it has not yet been possible satisfactorily to 
trace back the method of their formation to corresponding processes 
in the other Molluscs or in the members of other animal groups, is 
evidently due to the highly modified conditions under which the 
Cephalopodan egg develops on account of the large amount of food- 
yolk deposited in it and the marked distinction between the food- 
yolk and the formative yolk. 


Fra. 115.—Longita dinal section hous a an egg of mt Lali at the which the 
Sigs aete the gorm-dise becomes thickened (after frasl Teer Terk 
), ¢ peripheral cells; @ and ms, the [reser ot the | edge. 


‘The following is a brief statement of the riew hitherto held as to the formation 
of the germ-layers. The germ-dise consisting of a single layer of cells which 
at first covered only a small part of the animal pole of the egg, at a certain 
time, undergoes at the periphery a thickening of the cell-layer (Fig. 118), 
‘The layer which thus arises atid which soon gains considerably in size by the 
active increase in number of its cells, and spreads out beneath the whole of 
the upper layer of the dise, has been derived either through delamination 
from the cell-layer already present (Murscaxrxorr, Ussow) or else through 
the bending in of this layer (BosRETZKx). 

In contrast to the upper (ectodermal) cell-layer, the massive cell-accumula- 
tion has been claimed as chiefly mesodermal although the mid-gut epithelium, 
which elsewhere is always entodermal in origin, is said to be derived from this 
accumulation. Beneath the latter which, for the present, we must regard os 
mesoderm, a new layer is now found which, in its origin and relation to the 
other layers is of special interest. This is the “ vitelline membrane” of authors 
which, starting from the periphery of the germ-dise, no doubt spreads below 
the dise (and the ‘mesoderm ") as well as over the whole food-yolk, satround- 
ing it as a unilaminar cell-integument, 


CLEAVAGE AND FORMATION OF THE GERM-LAYERS. 249 


Ray LasKesrer assumes, with considerable inherent probability, that the 
vitelline membrane owes its origin to cells (or nuclei) freely distributed in the 
yolk, these being at once comparable to the yolk-cells and merocytes in the 
‘eggs of the Arthropoda and Vertebrata which are also very rich in yolk. 
These nuclei are said to shift to the surface, to become surrounded with 
protoplasm and to unite ta form the vitelline membrane. 

Other investigators (e.g., Ussow) have been inclined to derive the cells of 
the vitelline membrane rather from the deeper layers of the germ-dise, and 
thus from the “mesoderm.” Tn any case, this enveloping membrane of the 
yolk has the same significance as the vitellophags in the Arthropoda and the 
Vertebrata. As the terms vitelline membrane and yolk-integument are not 
an happy, being commonly used in another sense, we shall give this 

cellular integument another name (also applied to it by Ray LaNKesrEn), 
ealling it the yolk-epithelium. 

During the formation of the yolk-epithelium, the superficial cell-layer, the 
ectoderm, has spread over the whole of the food-yolk, which thus, beyond.the 
germ-disc, is covered by two cell-layers. Besides this, there is, as far as the 

extends, the “mesodermal” cell-mass lying between the ectoderm 
and the yolk-epithelium, The three germ-layers are thus apparently repre- 
sented, if we may for the time assume the yolk-epithelium to be the entoderm. 
The difficulty arises, however, that the yolk-epithelium is not found to be 
connected with the formation of the enteron, which owes its origin rather to 
the breaking up of the middle layer. 


Having now arrived at some comprehension of the germ-layers 
from which the Cephalopodan body is built up, we must trace the 
way in which the latter originates, as described in the most recent 
accounts. 

We traced the origin of the germ up to the point at which the 
animal pole of the egg is covered by a unilaminar plate of polygonal 
cells, and at which the irregular peripheral cells of this plate begin 
to detach themselves from it (Fig 112), Almost simultaneously with 
this process, the thickening of the edge of the plate already mentioned 
occurs, ie., the plate here becomes multilaminar through more active 
increase in number of its cells (Figs. 112, vd, and 118). This is the 
process which was described by earlier authors us the formation 
(delamination) of the mesoderm. 


Before the layer which has formed in this way loses its close connection 
with the superficial layer of the germ-disc, the cells previously detached from 
that dise undergo, uccording to Viautntos, an essential alteration, Their 
cellular character disappears, they are no longer distinetly although irregularly 
bounded, but now appear as a syncytium, ic., as nuclei lying in the thin 
Tayer of protoplasm that surrounds the food-yolk, There can be no doubt 
that we have before us, in them, the same nuclei which, according to 
Lanxesrer, give rise to the yolk-epithelium, This last significance actually 
belongs to these cellular structures which, according to VrauLeTon, arise 


a0 Cw CEPHALOPODA. ve Wet 


from the: germ-dise; they increase greatly in namber and at first unite to 
form o cell-layer which not only penetrates beneath the disc (Fig. 114 4-C, 
de), but also extends beneath the ectoderm over the whole of the yolk. The 
formation of this yolk-epithelium and the thickening of the edge of the 
dise which affects the whole of its periphery are clearly illustrated in Fig. 
114 4-C. These figures show, at the same time, how the yolk-epithelium 
Presses in towards the middle of the dise, as assumed by both VrALLeToN and 
WATASE. 





et hspreneehe ree ee », yolk-epil Sanita’ r, the the aed aaonat of = 
germ-dise, 

The separation from the superficial or ectodermal layer of the cell- 
mass, formed by the thickening of the margin of the disc, gives rise 
to the layer claimed by earlier authors as the mesoderm. So as to 
understand the real significance of this layer, we must follow its 
further fate. Since, to do so, we should have to pass on to some- 
what later stages, it will be advisable first to turn our attention to 
the external changes taking place in the germ-dise or in the whole 
blastoderm. 


3, The Development of the External Form of the Embryo. 


While the formation of the yolk-epitheliam and the simultaneous 
thickening of the edge of the germ-dise are taking place, another rapid 
increase in number of cells occurs in the superficial layer of the dise, 
and results in the gradual extension of this upper cell-layer over the 
whole egg. ‘This layer is known as the blastoderm, although this 
term is not quite correct for, apart from the fact that a differentia- 
tion of this layer has already taken place round the animal pole, it 


DEVELOPMENT OF THE EXTERNAL FORM OF 'THE EMBRYO, 251 


is soon followed in its cireumerescence of the egg by a second layer, the 
yolk-opitheliam, ‘I'wo areas can now be distinguished in the egg. 
‘The germ-dise, which forms the embryonic radiment and which now 
increases by the thickening of its margins (Figs. 112 and 113) only 
ater extends over the yolk, and a second, the yolk-sac, which at 
first is bounded by the two cell-layers, the ectoderm and the yolk- 
epithelium. A middle layer is added to the two cellular integuments 
which at first cover the yolk-sac, this third layer appearing either 
simultaneously with them or very soon after them (p, 277). 

The extension of the part known as the germ-dise over the yolk 
varies greatly in different Cephalopods. In the egg of Sepia, which 
is unusually rich in yolk, the embryonic rudiment is represented only 
by a small cup-shaped region of the spherical egg. Here, therefore, 
we can best speak of a germ-disc, and the yolk-sac is from the first 
very large. In other Cephalopods, indeed, so far as is yet known, in 
the majority, the embryonic rudiment and thus also the sv-called 
germ-dise spread over a much larger portion of the egg (Fig. 115), 
but as, at a luter stage, the embryonic rudiment again draws back 
more towards the animal pole, a yolk-sac is formed in these cases also 
(Figs. 116-118), In the Cephalopod investigated by Grexacuer, 
there is hardly any development of an external yolk-sac (Fig. 126, 
p- 270) and the yolk-mass which is comparatively small is here found 
enclosed by the embryonic rudiment at a very early stage. This 
form would thus have to stand at the end of a series, the starting 
point of which would be formed by Sepia with its unusually large 
development of yolk. ‘Transitionary forms between Sepia and the 
Cephalopod described but not identitied by GrenactEen would be 
found in such forms as Loligo, Octopus, Arqonauta, in which the yolk- 
sae is more and more reduced and the embryonic rudiment at the 
first contains the larger part of the yolk. 

‘If we may judge from the large amount of yolk in the egg (p. 297) and the 
Jarge size of the yolk-sac in older embryos (No, 26) the condition of Kledone 
‘Th this respect may resemble that of Sepia. 

Ttshould here be mentioned that the cleavage and the formation of the 
germ-loyers in forms which differ somewhat in their later development is, 80 
far as is known, yery much alike, and takes place in the way described above. 


Ta forms in which the rudiment of the embryo can early be dis- 
o.,.. from the large yolk-sac, the ectoderm, in the region of 
the germ-dise consists of cubical cells while in the yolk-region it is 
formed of flat cells. During its gradual extension over the yolk, 
the blastoderm becomes ciliated. The ciliation may extend over the 


262 CEPHALOPODA, 


whole of the blastoderm or may at first be found only at definite 
parts, appearing, for instance, especiully at the growing edge of 
‘the blastoderm (Figs, 115 and 116, p. 255). If this ciliation develops 
strongly and spreads over the whole of the blastoderm which covers 
the greater part of the yolk, as is the case in Loligo, the embryo 
rotates within the egg-integument, a phenomenon which recalls the 
free-swimming larvae in other divisions of the Mollusea. In Argo- 
nauta and Octopus, the only movement that takes place in the embryo 
is the shifting of the pole at which cleavage began away from the 
micropyle-region to that of the egg-stalk (Ray LankKEsTER). Some 
of the embryos of Octopus are, in fact, found lying at the micropyle 
end of the egg and others at the opposite pole ; in the older embryos 
examined by us the last position was the more frequent. 

The ciliation of the embryo either soon disappears, or else is 
retained for a long time, as, for instance, in Sepia, where it is found 
both in the embryonic region, which is already far developed, and on 
the yolk-sac. The embryos of Sepia, however, notwithstanding this 
ciliation, do not rotate like those of Loligo, a fact evidently due to 
the large amount of the yolk (KénnmER), 

Even before the circumerescence of the yolk by the blastoderm is 
completed, indications of the future shape of the Squid appear in the 
blastoderm or germ-dise (Figs. 115 and 116 4). We shall describe 
the rudiment and further development of the body-form at first: in 
one of those species in which the blastoderm grows round the yolk 
very early and the embryonic rudiment at first encloses the greater 
part of the yolk, The ontogeny of such « form, Loligo Peafii, was 
studied in a very thorough manner by Brooks (No. 7). Bay Lan- 
KESTER has also published investigations as to the ontogeny of 
Loligo (No. 30) and representatives of this genus, as has already been 
mentioned, were studied by earlier zoologists (P. van BungepEn, No. 
3; Merscuniorr, No. 32). Our own investigations, made with 
very rich material of Lolige oulgaris, as well as Octopus vulgaris and 
Argonouta have enabled us to supplement the discoveries of earlier 
observers. 


A. Development of the Embryonic Rudiment through its 
extension over the greater part of the egg with 
subsequent development of a Yolk-sac. 

(a) Loligo. 


In the region in which cleavage began, i.e., at the animal pole of 
the egg, 4 swelling forms in consequence of the thickening of the 


DEVELOPMENT OF THE EMBRYONIC RUDIMENT—LOLIGO. 253 


cell-layers ; this corresponds to the highest point of the dorsal side, 
as may be seen by a comparison with the later embryonic stages. 
‘This swelling, which is the rudiment of the mantle, soon becomes 
Jarge, and, in the Loligo examined by Brooks, rests like a cap upon 
the embryo (Fig. 115 A), but, in Loligo vulgaris, is less distinctly 
marked at this stage. At the stage depicted in Fig. 115 A, the 
greater part of the circular margin of this cap-like swelling has risen 
up in the form of a fold from the embryonic body (Figs. 116 and 117, 
ma), the mantle thus forming in the same way as in the other 
Mollusca, As already mentioned, the swelling lies on the dorsal side 
and a structure appears here which is comparable with the shell-gland 
‘of other Molluscs. This is an ectodermal depression (Fig. 115 B, 
and 116 A, s?) which at first is shallow but deepens later, and does 


A 





d 
Fie. 115.—Two early stages iv the development of Loligo Pealii (after Brooks). ar, 
Trotman of arma ; au, rudiment of eye; @, yolk; 4 rodiment enenary: the 
‘ciliated margin of the blastoderm ; sd, Shell land. 


not flatten ont again as in other Molluses (pp. 34, 92, 126), but 
becomes a.large pouch (Fig. 132, sd, p. 282). This peculiarity is 
connected with the fact that Loligo possesses an internal shell.* In 
those land-Pulmonates that are provided with an internal shell, we 
also found (p. 187) that such a shell-pouch formed from the shell-gland. 

‘There is a certain similarity between the swelling which becomes 
differentiated into the rudiment of the mantle and the shell-gland 
and the first indications of the eyes which also arise in the form of 
‘swellings each carrying a pit-like depression (Fig. 115 B). They lie 
t the two sides of the body below the mantle (Fig. 116 B, au). 


Of. p. 987, on the significance of the internal shell of the Cephalopoda, 






254 OEPHALOPODA, ’ 


Other much larger paired prominences are found lower down at the 
sides of the body in Loligo Pealii us the first indications of the arms 
(Fig, 115 A, av, Brooxs). It seems to be specially characteristic of 
this form that the rudiment of the embryo spreads over a very con- 
siderable portion of the egg; in other forms this is not the ease, as 
may be seen by comparing Figs. 115 A and 116 2B, 


Orientation of the Cephalopod body. A few words must be said as to the 
position in which we have represented the embryo, since it is not that formerly 
ascribed to Cephalopodan embryos, which are generally placed with the head 
and arms pointing upward. Our orientation of the embryo is in conformity 
with the now universally accepted view as to morphology of the Cephalopodan 
body, the ventral side being directed downward as is usual in other animal 
forms. If we regard the part of the body which lies between the mouth and 
the anus as the ventral surface, we have to consider by far the greater part of 
the body as the dorsal surface. That end of the body which, as opposed to 
the head appears as the posterior end must, according to this yiew, which was 
first adopted by Levckaanr (No, 81), be regarded as the apex of the dorsal 
surface. In such an assumption, according to which the ventral surface lies 
in the horizontal line, the embryo ought really to be placed obliquely, but 
this position was departed from for practical reasons and the head with the 
arms was simply directed downward. The (ascending) part of the dorsal 
surface which is directed forward will be called the antero-dorsal, and the 
(descending) part which is directed backward the postero-dorsal surface. 
These points are best illustrated by the median sagittal section of an older 
embryo (Fig. 133, p. 283) which cuts through the mouth and the anus. 


In the two ontogenetic stages of Leligo (Fig. 115 A and B) as yet 
considered, the circumerescence of the yolk by the blastoderm is not 
yet completed, although the rudiments of the mantle (m), the eyes 
(au) and indications of the arms (ur) are present, At a somewhat 
later stage, the yolk appears completely enclosed by the blastoderm 
and a number of new structures appear, especially on the ventral 
surface. Among these, the oral aperture deserves special mention ; 
this appears as a transverse oval pit somewhat in front of or between 
the optic rudiments, this pit arising like those rudiments very eurly. 
In Fig. 116 #2 the mouth is seen at a somewhat later stage. 

In front of the oral aperture a swelling appears (Fig. 116 B, ar), 
which runs right round the embryo, being divided into separate pro- 
minences. These latter are the rudiments of the arms which thus 
appear in Loligo vulgaris in x manner somewhat different from that 
described by Brooxs in the case of Loliyo Pealii. In the latter, the 
arms first appear in a very early stage as a pair of prominences, one 
on each side of the body (Fig. 165 4, ar), the individual arms 
appearing later by the breaking up of these. There is no mention of 


DEVELOPMENT OF THE EMBRYONIC RUDIMENT—LOLIGO. 255 


a circular swelling such as foreshadows the development of the arms 
in L, vulgaris (Fig. 116 2, dv). Further, in L, vu/yarts, the indi- 
vidual arms develop more distinctly in consecutive order, the first, 
which appear as button-like prominences, being those which lie next to 


A 





Fito. 116.—Various stages in the development of Loligo vulgaris (original). A, earl: 
sage st whe mich th Stee yen atid the dhell-gtand appear’ 2, on ftom tha oral alte; 
‘the anal side. J is seen obliquely from above, and for the sake of 
‘learness, rather more of the yolk-sac is shown in this figtre than is actual visible. 
te mae: € first three eats Se ey au, renee of & 
that carry the optic pits; d, yolk ; ds, yolk-sac; Mf, posterior 
; between the two branchial promivences lies the rudiment of the mond 


faeries mantle ; of, otoeysts ; r, edge of the blastoderm ; ad, sh 
at anterior funuel-fold. 








the funnel. At this period, the rudiments of various other organs are 
already visible, the most striking of these being the paired branchial 
fold (Fig. 116 @, k) which lies immediately in front of the mantle 


_— 


256 CEPHALOPODA. 


(m). In front of and somewhat laterally to these folds, a rather long 
paired ridge appears (C, Aff) running at first almost parallel with the 
branchial folds; it then passes back round the “mantle” at the 
margin of which it can be seen even on the opposite side of the embryo 
(i.e, when the embryo is viewed from the oral side, B, héf). This 
paired ridge, which appears very early, assists in the formation 
of the funnel, the chief part of which, however, is derived from a pair 
of folds which arises somewhat later more anteriorly (C, vf). These 
two pairs of ridges will be distinguished as the posterior (ht/) and 
anterior (vf/) funnel-folds. At first they are not prominent, and this 
is still the case with the anterior pair at the stage depicted in Fig. 
116 C, but they rise up more and more and then become very con- 
spicuous (Fig. 141, tr, p. 297). Between the anterior ends of the two 
posterior folds a slight curved prominence appears, apparently uniting 
the folds of the two sides (J). A very narrow superficial prominence 
now also connects the anterior folds; this latter fold is the first 
indication of the complete connection of the two anterior folds which 
takes place in later stages (Figs. 117 and 118). 

When the anterior funnel-folds appear, two vesicular depressions 
of the surface are seen behind them (Fig. 116 C, of; Fig. 141 4, 
p. 297); these are the otucysts which, when the posterior funnel-folds 
shift forward, are found lying near them (Figs. 116 D and 117 A and 
B). They lie also in the closest proximity to the large swellings 
which carry the optic pits. These swellings, which are very large 
even in an early embryonic period (Figs. 116 A and 115 B, au), 
continue to increase in size, and give the Cephalopodan embryo a 
highly characteristic appearance at the stage just described and 
especially in the following stage (Figs. 117 and 118). Only a part 
of these large projections is yielded by the eyes themselves which 
first appear on them in the form of depressions (Fig. 116 8). These 
depressions close later, a second depression then forming above the 
first (primary) optic vesicle, and the lens being secreted inwards at 
this point (cf. Figs. 142 and 143, pp. 298 and 299). 

The formative processes hitherto described affect merely a limited 
part of the egg, for the embryonic rudiment which extended earlier 
over the larger part of the egg (Fig. 115) has drawn back more 
towards the animal pole. There is therefore a part entirely free from 
the rudiments of organs, formed only of the yolk-mass and enclosed 
by several cellular integuments (Fig. 133, p. 283). This is the 
yolk-sac, which in later stages is much more distinct, the embryo 
becoming marked off from it by a constriction (Figs. 117119). The 





== 


DEVELOPMENT OF THE EMBRYONIC RUDIMENT-—LOLIGO. 257 


yolk-sac may contract (KéniiKER, Merscuntgorr) and, according 
to Ray LANKesTer, carries out rhythmical movements which are 
made possible by the fact that its envelopes do not consist, as is 
generally supposed, merely of a layer of ectodermal cells and another 
of entodermal cells, but also of « mesodermal layer intercalated 
between these (Fig. 133) which evidently contains contractile elements. 
This mesodermal layer, the presence of which in a number of other 
Cephalopods (Sepia, Sepiola, Octopus Argonauta) has been established 
through the examination of sections, seems only slightly developed 
in the forms which have smaller yolk-saes, but in those with large 
yolk-saes as, for instance, Sepiv, this layer is highly developed, long 
straight, fibre-like cells here lying one above the other. 

It appears that, by the contraction of the yolk-sac, its contents 
are pressed into the interior of the embryo, extending far into the 
embryonic rudiment (Figs, 132 and 133, p. 282). A distinction is 
therefore made between the outer and the inner yolk-sac, the latter 
extending as far as to the mantle and into the optic swellings. Here 
also it is enclosed in the ‘‘ yolk-epithelium” and does not, as has 
been assumed, stand in direct communication with the intestinal 
canal of the embryo, so that the yolk-substance can be utilised by 
the embryo only with the help of the yolk-epithelium, As the yolk- 
sac extends so far into the embryo, the surfaces are in contact over 
«very large area, a fact which explains the absorption of the yolk 
without direct communication existing with the intestine and with- 
out the intervention of special vessels. The whole embryo (including 
the yolk-sac) increases in size during development, the later stages 
being much larger than the eurlier, 

Although the great development of the external yolk-sae at first 
recalls the conditions which prevail in the Vertebrates, some difference 
is brought about in the Cephalopoda by the fact that the yolk-sac 
is Were devoid of any direct communication with the intestine. 
Special vessels also xeem to be wanting in the yolk-sae, as already 
mentioned, and it therefore enters far into the embryonic body. 
Further, the yolk-sac in the Cephalopoda is ventral, its position at 
the anterior end of the body surrounded by the arms being merely 
apparent. In reality, it lies ventrally (between the mouth and the 
anos) and a comparison of Figs. 116 4 and D, and 113, p. 248, 
shows that the mouth lies at one side of the yolk-sac (the anterior 
side) and the anus at the other (posterior) side, 

‘Tt hus already been mentioned (p. 254) that the mouth appears ws 
arndiment at an early embryonic period (Fig. 116 8). The anus 

8 





258 CEPHALOPODA. 


does not appear until later, sinking in at the middle of a slight 
prominence, the anal papilla (Fig. 116 D); the posterior part of the 
intestinal canal, starting from this point, runs towards the mantle, 
its course being externally marked by a slight rising on the surface 
(Figs. 117 and 118). 

In the embryo of Loligo Pealii, at a stage intermediate between 
those depicted in Figs. 116 B and C we find, in the oral region, 
starting from the two angles of the mouth and running first to the 
optic pits and then passing anteriorly, two rows of cilia ; these have 
been compared by Brooks with the velum, ée¢., with the pre-oral 
ciliated ring of other Molluscan larvae. We should, in this case, 
have to regard the part including the eyes and the very limited 
region between them as the pre-oral part of the body. 

Among the changes which take place on the dorsal side of the 
embryo, those that occur in the mantle exercise a special influence 
on the external form of the animal. The pit representing the shell- 
gland which, at first, is very wide (Fig. 116, «/) narrows with time, 
and in later stages is only a small aperture (Fig. 117 B) and finally 
closes entirely. The external aperture of the continually deepening 
pit becomes surrounded by a kind of circumvallation, the surface 
again sinking in, though not to any great extent (Fig. 116 D). The 
almost rhomboidal swelling (m) which surrounds this shallow de- 
pression represents the marginal part of the mantle which now 
begins to rise above the rest of the body. At a slightly later stage 
(Fig. 117 A), we find the mantle becoming marked off by the 
swelling of its margin. ‘The large depression round the circular wall 
of the shell-gland flattens out again and becomes rounded off like the 
edge of the mantle itself (Fig. 117 2). Two pointed prominences, 
the rudiments of the fins, are visible upon it (Fig. 117 4 and 8). 

Another change has taken place in the mantle-region on the 
dorsal side, the posterior funnel-folds having shifted more tovards 
the middle line, there ending in a kind of plate which is the rudiment 
of the nuchal cartilage (Fig. 117 B). The posterior funnel-folds are 
thus recognisable as the broad muscle-bands (the so-called nuchal 
muscles) which even in the adult appear as lateral continuations of 
the funnel. They run to the nuchal cartilage and become attached 
to it. 

In tracing the further development of the funnel, we find that the 
anterior folds form the essential factor in determining the alterations 
that take place in its principal parts. These anterior folds, which 
soon rise much higher than the posterior folds, become united in the 


DEVELOPMENT OF THE EMBRYONIC RUDIMENT—LOLIGO. 259 


ventral middle line (Figs. 116-117). At first they form together 
merely a slightly undulating line (Fig. 117 A), but their lateral ends 
soon bend back further (Fig, 117 #) and as the folds at the same 
time swell up more, the later form of the funnel becomes indicated 
(Fig. 118 4 and #). At the same time, the posterior funnel-folds 
become modified in shape, now appearing forked at the point where 
they come into contact with the anterior folds (Fig, 118 4). This 
is caused by the rise of a new fold at this point, which runs towards 
the mantle, This is, like the other folds, an expression of the 
greater growth of the mesodermal tissue and represents a part of the 
retractors of the funnel (muse, depressores infundibuli). 





Fre, 117.—Two in the development of Loliga oulgaris (original). A, vege from 
cpeera jsiche iby obliquely from above. ( Sights vi 116 
ree irs of arms, a, optic swelling; ds, “BAC 5 

Mp ee atoe hustled k, Ae Solas ch giles ok, masiies Sh, wate cad, 
lage 5 oe otocysts; off, anterior funnel-fold. ‘The vireular fold ont of which the 
arise can still be recognised, especially in A. In B, the long i- 

nences indicating a pair of arms Prin Bebind @,) still form part of it, The perl 
and /f) meet in the middle line. “Between the two gills (k) lies the 
anal papilla; on the mantle, are the two prominences representing the 
of the fins (¢/. Fig. 118, f). 





Tu the adult, these muscles are attached to the funnel laterally, some of 
them running further forward to end within the fannel and in its dorsal parts. 
‘This ix perhaps indicated even in the embryo (Figs. 117 and 118) by the 
course of the anterior folds, but we have hitherto been unable to make any 
careful examination of the fate of these raised parts which anteriorly become 
connected with the posterior funnel-folds, and must therefore refrain from 
‘conjectures as to their significance, 


260 CEPHALOPODA, 


It is evident from the above that not only do the anterior funnel- 
folds from the two sides unite to form a common fold but that the 
posterior folds also fuse with the anterior, At the point of junction 
of these two sets of ridges, the posterior folds appear as a mere pro- 
longation backward of the anterior (Figs. 118 and 119), By this 
process and by the simultaneous extension of the anterior folds, the 
funnel hus already approximated closely to its final shape (Fig. 119). 
The free edges of the two anterior folds become apposed, but do not 
as yet fuse (Figs. 141, fr, p. 297 and 143, #, p. 299) and the funnel 





Fie, 118.—'Two embryos of Latin ewdguri, seu from the. prsteror ge fuels 
. ital Qy-dg, ATMS; ce, Hae de, wget Jt, fins; 
ills; me, mw retractor of be funnel ; of. eee 
faunal elds.” Between the tive pills (A) ithe anal papilla 






has thus attained the stage which is retained throughout life in 
Nautilus. \n this primitive Cephalopod the funnel, though acting 
as a tube, is actually formed by the bending round posteriorly and 
the overlapping of two distinct folds. 

As development advances, the two half-tubes composing the funnel 
fuse in the middle line (Fig. 120 4); the exhalent aperture, however, 
which could already be recognised at an early stage, being retained, 
The formation of the funnel is thus completed in all essential points, 
Laterally, the posterior funnel-folds run to the nuchal cartilage (Fig. 





DEVELOPMENT OF THE EMBRYONIC RUDIMENT—LOLIGO. 261 


120 A and FB, Am). They continue to increase in breadth and 
represent the nuchal muscles (musculi collires) which, together with 
the retractors (Fig. 120 A, 7) that run backward direct to the 
mantle, form a kind of lateral chambers, not communicating with 
the actual funnel, /e., with the middle fannel-cavity. The funnel- 
valve wppears in the anterior part of the funnel, 4, in the wall 
whieh is in contact with the body, as an unpaired fold (BRooKs). 

While the changes just described 
have taken place in the funnel, 
the mantle also has undergone 
repeated modifications of form. It 
now rests like a capon the end of 
the body (Fig. 118, ma) as its 
edge has extended forward further 
and has become raised from the 
hedy. The further growth of this 
overhanging margin leads to the 
formation of the mantle-cavity, 
into which the gills are drawn, these 
not having essentially changed 
their shape (Fig. 118, 4). The 
i in size of the mantle is now 

chief feature of its develop- 
(Figs. 118-121). The fins 
its upper end also increase in 

z The optic swellings have ds 
become very Iarge. It has already P16. 119.—Oller embeyo ot Lolyyo 
wen pointed out that in this way tees oral. I era 
the enabryo wequires specially The Mo the Itong le 
charseteristic appearance which it by the overhanging margin of the 
Gelindihs leter tages uso (Figs. cet between them is the anal 

120 A and &), 

We have 86 far mentioned only the first stage in the rise ur the 
urine (p. 254). From the circular fold which runs round the whole 
embryo at the boundary line between the embryonic rudiment and 
the yolk-suc (Fig. 116 4, ar), the separate prominences which repre- 
sent the arms become differentiated, each first appearing as u long 
swelling which soon assumes a bntton-like form (Fig. 116 2-2). The 
first pairs of arms to become distinet are the two that lie nearest 
the funnel, the second pair of arms, however, in Loliyo attains a far 
higher degree of development than the first and than the one that 








262 CEPHALOPODA, 


follows it, a distinction which is retained in later stages. ‘This pair 
of arms, the prehensile arms, is soon followed by a third pair (Pig. 
116 C and JY). When the first three pairs have become distinetly 
differentiated us button-like prominences, the other two which lie 
nearest the mouth are still mere transverse swellings ; the first of 





¥ ia. 120, -Two older embryos af Lotigo vulgaris, A, seen trom the Iwunel site, Br 
from the oral side (original). aj-@,, arms; aw, eyes: ds, yolk-se ; Jf, tins ; fom, 
nuchal muscle ; ma, mantle ; rt, retractor of the funnel (tr). “In 1, the gills project 
helow the mantle ; hetween them is the anal papilla. 


these to become distinct is the fourth, then follows the fifth* As 
‘the embryo continues to develop, the arms grow in length, and the 
sucking dises appear on them. The change of shape undergone by 


* In speaking here of the first to fifth pairs of arms, they are numbered 
according to the order in which they originate in the embryo, uot 
to the order somotimes adopted (for which we can see no good reason) 
which, on the contrary, the pairof arms whieh lies furthest dorsally counts 
‘as the first and the most ventral pair as the fourth, ths pees arms being 
reckoned separntely, evidently on account of their different development, 
which seemed to give them a claim to a special position, 


DEVELOPMENT OF THE EMBRYONIC RUDIMENT—LOLIGO. 263 


the embryo in rising up from the yolk prodaces a change in the 
position of the arms which shift from the funnel-side more towards 
the oral side (Fig. 117-120). 


In Loligo Pealii, the three pairs of arms depicted in Fig. 115, ar, develop 
first and only when these have become differentiated, does the pair whieh 
hhes nearest the funnel appear (Brooks). ‘The fifth pair seems to form very 
late. The same is said to be the case in 
(Gmenxacnen’s Cephalopodan embryo (p. 271). 

The second pair of arms, the prehensile 
arms, grow with special rapidity, out- 
stripping in development not only the first 
but the other arms also (Figs. 119-121) ; 
external investigation, however, reveals no 
special peculiarity in the rudiments of these 
arms. This corresponds with the adnit 
condition in other more primitive Decapods 
(Ommastrephes). Only later, when the 
embryo hatches, are the prehensile arms 
distinguished by the fact that the basil 
part is free from suckers, this part lying in 
a depression. In younger embryonic stages 
and even in older stages (Fig. 120 4 and 
A), tive pairs of arms can easily be made 
out, but the fifth develops much less than 
the rest, so that in later stages (e.g., in 
that depicted in Fig. 121) it appears 
merely as two small cones which can hardly 
he made out. ‘This fact no doubt led to 'y, {al puter en 


rT i the posterior or fimnel-side 
the assumption that only four pairs of arms ee ete ape 
appeared as radiments in the embryo, the the necond ‘pair and. be- 





i tween them the first pair 
fifth forming later. of arms; dm, eyes; de, 
Sinde the yolk-sae occupies a ventral ‘olk-sae 5 ft, fins; &, gills; 


between the two Is is 
position (between the mouth and the anus), the anal papillu; ¢r, funnel, 


the same position must be ascribed to the Thesis Is, already 
arms that surround it. This is especially ——_phores. 

noticeable in the younger stages (Fig. 

116 BD), although it can also be recognised in older embryos 
(Fig. 120 4 and &). The mouth here still lies outside of the circle 
of arms, but seon shifts within it (Fig. 120 B) or rather is surrounded 
‘by the arms as they shift dorsally. This occurs simultaneously with 
the degeneration of the yolk-sae that now begins, The mouth finally 


264 CEPHALOPODA. 


occupies the place of the yolk-sac, /.-., is surrounded by the arms, a 
position which, as is well-known, is occupied by it in the adult. 

When the yolk-sac begins to degenerate, i.¢., in the last stages of 
development, the embryo approaches ever nearer the form of the 
adult (Fig. 121). The arms are still rather small, the eyes still 
remind us of their former condition, but the funnel, the mantle, the 
gills and the anal papilla have almost attained their final form. The 
chromatophores have already formed and they also give the embryo 
a characteristic appearance more like that of the adult. The 
chromatophores appear first on the mantle on the posterior (postero- 
dorsal) side and are only somewhat later found on the arms and on 
the head. When the embryo leaves the egg, the external yolk-sac 
has, to a great extent, disappeared. 


(b) Octopus. 


Although, systematically, Octoprux is far removed from Loligo, the 
course of development of the two forms is very similar. The em- 
bryonic rudiment extends at first over a larger part of the egg and 
later withdraws again more towards the animal pole, just as in Loliyo. 
‘The shell-yland appears very early, at a time when the blastoderm 
has not yet grown round the yolk, as a depression at the animal pole. 
This fact is of special interest, because Octopus, like most other 
Octopoda (Cirrhoteuthix perhaps forming an exception?) has no 
internal shell. The shell-gland in this case, therefore, has the 
significance of a vestigial organ. At somewhat later stages, when 
thé rudiments of the external organs appear, it can be recognised as 
a distinct depression at the apex of the rudiment of the mantle, and 
even later is perceptible (Fig. 122 4). According to Ray LANKESTER. 
it disappears without having closed. 

At a stage somewhat earlier than that illustrated in Fig. 122 4, « 
pair of small prominences appear on the mantle, resembling, in shape 
and position, the fins described in Loligo. Indeed, the aspect of the 
mantle-rudiment in Ocfopux in the younger stages closely resembles 
that of the mantle-rudiment of Lofigo. The prominences are retained 
for some time; they can be recognised in Fig. 122.4 and 8, and in 
later stages are still present, but, finally, they decrease in size and 
altogether disappear. They cannot be regarded as anything else than 
the vestiges of a pair of fins, and must be considered as an indication 
that the Octopoda originally carried fins, like the Decapoda. This 
fact affords further support to the view which in itself is probable 








DEVELOPMENT OF THE EMBRYONIC RUDIMENT—OCTOPUS. 265 


that the Octopoda must be regarded as derived and the Decapoda ax 
primitive forms. The conjecture as to the nature of these promin- 
ences is further rendered probable by the fact that fins occur in some 
adult Octopoda (Octopus membranaceux, Pinuoctopus, Cirrhoteuthia). 

The oral aperture appears in Octopus at a-very early stage and 
soon takes the shape of a semicircular groove bordering a swelling. 
The appearance of the rudiments that lie on the ventral side closely 
resembles that described for Loligo and will best be understood by 
a study of Fig. 122 A and &, and by comparing this figure with the 
illustrations of the Loliyo embryo given in Figs. 117 and 118. 

It should be noted that the funnel forms, in the Octopoda, in the 
same complicated way as in Loligo and the other Decapods. A paired 
posterior fold appoars and, in the course of development, unites with 
an anterior fold which is also paired to form the funnel and its lateral 
parts (Figs. 122 and 123, Wé/, vty and rf). 





do. 


Fic, 122 — Two embryos of Ortyyns rulguria at different ages, seen from the posterior 
de (original). ar, arm : au, optic swellings ; ds, yolle-xae : h(7, posterior fu 
; Ay gills; om, mantle ; of, otocyste; rtf, anterior funuel-fold, 





In comparing Loligo and Octopus, we are struck by the fact that, in the 
latter, the separate organs appear very early, but do not develop further with 
corresponding rapidity, so that, as contrasted with organs that appear later, 
their development is retarded. This peculiarity wax pointed out by Brooks 
(No. 7), in comparing the form examined by him (Loligo Pealiiy with 
Gresacuen’s Cephalopodan embryo. In (efopus, for instance, the rudi- 
ments of the arms appear early, their number being complete even earlier 
than the stage depicted in 122 A, but they then develop very slowly. 
With regard to the order in which the arms appear, this seemed to ux to be 
the same as in Loligo, ie. from the rudiment of the funnel towards the 
mouth, Two pairs of arms appear as slight swellings in front of the optic 











266 CEPHALOPODA. 


prominences; @ third and a fourth pair are soon added; this latter pair, iv., 
the one near the mouth, the most dorsal of the 
arms, is always the least developed. The pairs 
of arms appear very quickly one after the other, 
so that the above statements are made with a 
certain reserve, 


In the development of Octopus, it is of 
xpecial interest that the yolk-sac is some- 
what less developed than in Loltyo, as is 
evident from a comparison of Figs. 122 and 
123 with Figs. 118 and 119, p. 261. In 
earlier stages, this difference is less marked ; 
later, on the contrary, it is still more notice- 
able. In itself, this comparatively slight 
difference in the development of Octopux 

da would be hardly worthy of note, but it 
Moca, wee ‘Row te fords a transition to those forms in which 
funnel - side (original). ~— the yolk-sac develops still less (Argouutay 
ur, arms; au, optic swell- A 5 ‘ 
ings; Am, nuchal muscle; OF; indeed, is almost altogether wanting 


et, retractor muscle of the . “3 
founel (0), (GRENACHER’S Cephalopod). 





(c) Argonauta. 


Aryonauta, in its development, also closely agrees with the forms 
hitherto considered. Special interest attaches here to the appearance 
of the shell-gland at an carly embryonic stage and to its retention 
for a long period, although the shell of the adult does not develop in 
it, having another origin and significance, as will be shown later (p. 
294). The xhell-gland, as in Octopus, is said gradually to flatten out 
again (Ray La TER, No. 29; Ussow, No. 44, p. 352), and the 
Argonaut shell forms after embryonic life is over, as was shown by 
KGLLIKER in opposition to former statements (Nos. 24, 1 and 9). 

The embryos of Argonauta show, at various stages, in the rise of 
the different organs, great similarity with the Cephalopods already 
considered (cf., the late stage depicted in Fig. 124) especially with 
the embryos of Octopus and Loliqn of about the same age (Figs. 123 
and 119), but the small size of the yvolk-sac scems to determine a 
more compact form of bod. 

As in Loligo, the embryonic rudiment at first extends over a lange 
part of the egg, but becomes at a later stage more concentrated, 
withdrawing more to the animal pole, and rising from the yolk, thus 

















DEVELOPMENT WITHOUT ACTUAL YOLK-SAC. 267 


giving origin to an external yolk-sac which, however, is not nearly 
so large as in cases already mentioned 
(Fig. 124). As development advances, this 
volk-sac decreases in size, and, in mature 
embryos, at hatching, there is not any 
trace of it. 

The differences in size and shape of body 
existing between the two sexes of Argonauta, 
also find their first expression during post- 
embryonic life. No sexual dimorphism 
could be observed in any of the many 





embryos examined by us.* This applies 
also to the striking heetocotylised arm of Fic. 124. — Embryo 
i , aAryonauta argo, Wi 
the male, which in other Cephalopods funnel still incomplete! 
Lala leveloped (original), 
also, becomes differentiated only as sexual eloped (original) 
maturity is gradually attained. Mature ee ee tunnel 
at, tm, . 

embryos of Octopus, Loligo and Sepia show : 

no sign of this modification; this is the less strange as the arms 


are still far from being fully developed in these embryos. 







B. Development without actual yolk-sac. 


The description of the above forms may best be followed by that 
of the Cephalopod observed by GRENACHER (No. 14), a form the 
systematic position of which has not yet been determined. It 
probably, however, belongs to the large division of the Oigopsida, 
perhaps to the genus 7wthis, STREENSTRUP (No. 42) believes 
that it resembles Ommastrephes (see also p. 236). The eggs, unlike 
those of the forms hitherto mentioned, are spherical and distinguished 
by the violet colour of the yolk which elsewhere ix yellow. They 
are about 1 mm. in diameter, and thus much smaller than those 
of Argumuuta. ‘This is a remarkable fact since, judging from the 
quantity of spawn and the number of eggs contained in it (p. 236), 
this Cephalopod is inost probably a large animal. The small size 
of the eggs, and the small quantity of yolk contained in them afford 
an indication of the manner of development of this form, which is 
marked by an almost entire absence of the external yolk-sac. 


©The number of eggs laid by the female Argonaut is very large, so that a 
considerable number of embryos are to be found in the bunches within 
the shell. The eggs to which we had access belonged to various females and 
were at different stages of development, and, although no fully mature embryos 
were found by us, we were justified in forming the above conclusion from those 
in a late stage of development. 





| 


268 CBPHALOVODA. 


Since, in Guesacten'’s Cephalopod, we apparently have a comparatively 
ptimitive form, it has been thought that paucity of yolk might be regarded 
as the primitive condition, So long as the first ontogenetic processes are not 
known, no decided opinion can be given on this point, but the 
of this form in general shows such close similarity to that of other Cephalopods 
that a reduction of the yolk seems more probable. We may also regard the 
early appearance of the chromatophores which elsewhere appear late as 
secondary (see below), Although the Oigopsida are very primitive forms among 
the Cephalopods now living (Nautilus and Spirula excepted) they themselves 
appear highly specialised when fossil Cephalopods are taken into account. 
‘There is a great gap between them and the forms with chambered shell, and 
yet Nautilus even has large eggs rich in yolk, as is shown by examination of 
the ovary (Owen, No. 38), [The egg-capsule measures 45 x 16 mm. and the 
actual egg is 17 mm. long (WuLex, No. IV.).—Ep.] 


The earliest development seems to agree with that of the other 
Cephalopods. A blastoderm forms which, however, in this case very 
soon grows round the yolk, Kven 
beforedistinct rudiments of organs 
can be seen on the blastoderm, it 
has grown almost to the vegetative 
pole, leaving only a small portion 
of the yolk free (Fig. 125), The 
growing edge of the blastoderm is 
beset with cilia, but these do not 
lead to any rotation of the embryo, 
The first indication of organs is 
the appearance at the animal pole 
of star-like cells containing red 
pigment, which rapidly increase 
Fic. 125,— Young eubryo of Guawa- in number (Fig, 125, rf). ‘These 

oe Mio pba eeerone are the chromatophores whieh thus 
the yolk (after Gnexacksn). ch, chro- form, not asin other Cephalopods, 
matophores: yolk; v, mang of th towards the end of the embryonic 
period (Fig. 121), but, strange to 

say, arise quite at the commencement of that period. They soon 
spread over the upper third of the blastoderm, at the edge of which 
a circular fold now forms. The upper pigmented part of the embryo 
thus rises from the rest of the body as the rudiment of the mantle, 
this process beginning at the postero-dorsal surface, i.¢., in the 
neighbourhood of the future anal pit, and proceeding towards the 
antero-dorsal surface. During these differentiations, the originally 
spherical embryo becomes cylindrical. In Fiz, 126 4 and B the 





DEVELOPMENT WITHOUT AOTUAL YOLK-SAC. 269 


rudiment of the mantle is seen in a later stage thickly covered with: 
chromatophores. 

It is curious that Gresacien makes no mention of a shell-gland, as an in- 
ternal shell usually oceurs in the Oigopsida, and a shell-gland even appears 
in those Cephalopods which are devoid of the internal shell (Octopus, 
Argonauta). The region of the animal pole in general, in GrewacuEr’s 
Cephalopod, differs from the same region in the other Cephalopods con- 
sidered by us, and it appears probable that the intermediate stages were 
missed in consequence of the far from favourable conditions under which the 
observations were carried out. The mantle is rounded at its end, and the fins 
which, in Loligo, form so early, appear only at a later stage. 


We have already, in a Loligo, seen the arms arise not far from the 
vegetative pole (Fig, 115 A, p. 253). In GrRENACHER’s embryo, 
the rudiments of the first two pairs of arms appear as fold-like 
prominences directly at the edge of the blastoderm which has not 
yet completely closed, ¢.¢., quite near the vegetative pole, so that 
wt this stage and still more at a somewhat later stage, when the 
cireumerescence of the yolk by the blastoderm is completed, the 
whole yolk with the exception of a sinall portion is enclosed in the 
embryonic rudiment. But here also, later, a process takes place 
similar to that described for some other Cephalopods, viz, the 

ic rudiment withdraws to some extent from the vegetative 
pole (Fig. 126 A) a process which, in the cases before mentioned, 
led to the formation of a yolk-sac (Figs. 115 and 116, p. 253). 
Here, indeed, this takes place only to an inconsiderable eegree, and 
thus gives rise to the mere indication of a yolk-sac (Fig. 126 A and 
#B, de) which, however, becomes somewhat more distinct later (Fig. 
127, ds). At the time when this swelling, which corresponds to the 
yolk-saec of other Cephalopods, forms, and in consequence of it, the 
aperture of the blastoderm, which is still present, undergoes displace- 
ment, being pressed further away from the vegetative pole towards 
the so-called nuchal region. This part is for a long time marked by 
a ciliated area lying somewhat in front of the disappearing aperture 
(Fig. 126, w). Anteriorly, the oral aperture (m) appears as an 
vetodermal invagination. 

When considering the ontogeny of Loligo, a ciliated area lying near the 
tmouth was mentioned (p. 258). The ciliation occurring here in GneNacuen’s 
Cephalopod in the oral region recalls that area which was compared by 
Brooks to the velum of other Molluscs. A comparison of the two is, how- 
ever, inadmissible, since the ciliated area in the present case lies in front of 
or below the arms, as is evident from Fig. 126 4, and still more from Grey- 
4schmn’s figures of later stages. The ciliation thus belongs to the region of the 


| 


270 CEPHALOPODA. 


yolk-sac and consequently lies ventrally, In Loligo, on the coutrary, it is 
found between the rudiments of the arms and the eyes, 

‘The position of the oral invagination in the neighbourhood of the former 
‘aperture of the blastoderm might appear remarkable (Fig. 126 4), but may 
possibly be accidental, being caused by the great reduction{of the yolk-sno. 
We shall have to point out later that we are inclined to regard the slight 
development of a yolk-sac in Grenacner's Cepbalopod as a secondary 
phenomenon, 





Fra, 126,—Two stages of Grexacten's Cephalopod embryo, A, seen from the side 
B, from the ventral ee. pone surface (after cae My-O, AIMS; aw 
rudiment of ©) Qi Hever ch, chromatophores ; ds, valk saa i, ‘posterior 
ftunnel-fold fears gill; «, month: mu, mantle ve, apertre of the 

blastoderm ; of, otooyat (7, anterior funnelfold ; w, elliated ares. 


About the time when the rudiments of the arms appear, a large 
swelling arises behind them on cither side of the embryo, in connec- 
tion with a depression, the rudiment of the eyes (Fig. 126 A, au). 
Soon after, the rudiment of the funnel appears in the form of two 
pairs of folds. The anterior, slightly undulating folds are inclined 
‘one to the other (Fig. 126 2). They unite later, in the way already 
described for Loligo, to form the funnel (Fig, 127), The posterior 
folds, which were originally distinct from the anterior though 
running in the same longitudinal direction, fuse later with these latter, 
and in any ease yield the lateral portions of the funnel, that is, the 
so-called nuchal muscles (Figs. 126 2 and 127). At the points 
where the anterior and posterior folds fuse, a process rans inward 


a 





DEVELOPMENT WITHOUT ACTUAL YOLK-SAC, 271 


which gives rise to the retractor of the funnel. We thus sev here 
again that the funnel forms in much the same way in other forms. 
The course of development 
of the other organs, stich as 
the gills and the intestine, the 
otocysts and the eyes, can be 
made out by reference to Figs. 
126 and 127, as they resemble, 
in their origin and development, 
the similar structures in Loligo. 
The arms, on the contrary, 
must be referred to more in 
detuil, since, according to 
Gmexacuer's statement, they 
“Appear in an order somewhat 
different from that seen in 
Loligo vulgaris. We have 
ready mentioned two pairs of 
arms at an earlier stage, and 
there was some uncertainty as 


to the presence of a third pair, 
whieh in any case soon follows 
the others, Of these pairs of 
arms, those which appeared first 
are said to be the more dorsal 
in position, At the base of the 





which perhaps lead to 
‘the formation of the foarth pair ; ab, pe 
vesicle; au, rudiment of eye; oh, chro- 


_matophores: ds, Ik-aue; gu, optiv 


j Am, nuchal (collar) muscle ; 

‘teral portion of the funnel ; &, rudiment 

of gill; ma, mantle ; of, otocyst ; rt, re- 

tractor of the funvel ; fv, funnel; sk, 
“white body", 


subsequent third pair a fourth 
grows out, diverging to a certain extent from it. A fifth pair has not 
‘been observed in this Cephalopod, but probably develops later, 


‘If Gaesacuen is correct in his statements, the arms, in this Cephalopod, 
‘appear in an order the reverse of that which prevails in Loligo and Sepia, A 
certain departure from the accepted order was also found in the Loligo 
‘examined by Brooks (p. 263). We must await further observations, made 
for preference on related forms, to solve this difficulty. We shall not attempt 
to desoribe the arms of this Cephalopod embryo, although the difference in 
‘size between them and those of the embryos of Loligo in younger stages 
tp, 261) seems to demand examination, and the different result as to the order 
of appearance of the arms in Grenacuen’s embryo might thus be attained. 


Ty consequence of the small amount of yolk they contain, the 
embryos soon resemble the adult in the shape of the body more 
closely than do those of other Cephalopods. ‘The embryo depicted in 





272 - CEPHALOPODA. 


Fig. 127, for instance, resembles the adult more than do embryos of 
Loligo and Sepia at somewhat corresponding stages (Fig. 119, p. 261, 
and Fig. 129 C, p. 275). By the further growth of the mantle, 
the appearance on it of fins, 2s well as the closing of the funnel which 
is grown over by the mantle and, like the gills, partly enclosed in 
the mantle-cavity, the embryo approaches the adult form more and 
more. The eyes which, in this embryo, are very large, also decrease 
in size, as their internal structure gradually develops. The arms 
grow and become covered with suckers. The swelling between them 
(the external yolk-sac) gradually disappears, and the internal yolk- 
sac, which here also fills a large part of the embryo, is gradually 
but very slowly absorbed. The oral aperture, in consequence of this 
process of growth, shifts downward to between the arms, to take up 
its final position at the anterior end of the body. At about this 
stage, the embryo breaks through the egg-envelopes and, during the 
period of pelagic life which now ensues, assumes the final form of 
the adult. 


C. Development through the formation of the Embryonic Rudi- 
ment on a limited portion of the egg with simultaneous 
development of a large Yolk-sac. 


The type of development now to be considered has only been 
observed in the egy of Sepia (KOLLIKER, No. 24; VIALLETON, No. 
48), but may occur in other specially large Cephalopodan eggs as 
well. This forin of development is brought about by the-abundance 
of yolk in the egy, and is characterised by the restriction of the 
embryonic rudiment toa small, cap-like portion of the egg (the germ- 
dise), the rest of the yolk being enclosed merely by the thin cell- 
integuments already mentioned (ectoderm, mesoderm and entoderm, 
p. 257). There is a further difference between this form of develop- 
ment and that in which the embryonic rudiment extends over a 
considerable part of the egg, inasmuch as the embryo appears on a 
surface only slightly arched (Fig. 128 A and 8). This makes the 
processes of development somewhat more difficult to understand, but 
we are assisted in following them by comparison with the same 
processes in eggs less rich in yolk. 

The first indications of the embryo on the germ-disc take the form 
of various prominences and swellings which soon show bilateral 
symmetry in their shape and arrangement. This symmetry most 
probably corresponds to that already evident in the germ-dise during. 





DEVELOPMENT OF SEPIA. 273 


cleavage (see Fig. 109, and Fig. 110, of Loligo), The swellings 
of the surface which at first are very vague and indistinct, become 
gradually clearer and can soon be recognised as the rudiments 
of the different organs, one of the first to grow distinct being a 
cirenlar depression at the centre of the germ-dise. This becomes 
surrounded with a flat wall which is more or less pentagonal with 
rounded corners (Fig. 128 4, sd, and ma). This represents the 
rudiments of the shell-gland and the mantl-, in the early appearance 
of which Sepia resembles 


those highly developed 
structures which, in other 
Cephalopods, we regarded 
as the optic swellings. 
In Fig. 128 A, they are 
represented at a some- 
what later stage (Jt). 
‘The divergent character 
of the development of 
Sepia is specially shown 5 . 
‘in these structures, which a. | \ 
here appear on an almost 2 
Mae) curface; claowhere "1% 228. — Germdiscr with young embryonic 


they form two large and and KGutaxxn). "a, auus; ay-ay, the five pairs of 


: arms ; au, rudirents of posterior - 
very prominent swellings, fold ; X, wills; Kl, ce} m a totes bs, ich 3 
one-on ether side of the (yy MMs"! (tna fia 





‘The germ-disc, on the side opposite to the optic swellings, ix 
bordered by w narrow band-like prominence which at first is almost 
semicircular but soon extends round the greater part of the germ- 
dise and then resembles an incompletely closed circular swelling. 
‘This corresponds to the circular swelling which, in Loligo, runs round 

T 


274 CEPHALOPODA. 


the whole embryo (Fig. 116 B, ar, p. 255) and contains, here as there, 
the rudiments of the arms. Those of the two ventral pairs are to 
be seen first, becoming differentiated from the circular swelling as 
rounded prominences. These are followed very soon by a third pair. 
When these three pairs have become distinct, the swelling containing 
them is prolonged laterally as a narrow process. As this becomes 
more massive later, the fourth pair of arms develops from it, this 
being finally followed by the fifth which lies the most dorsally (Fig- 
128 4, aas). The order in which the arms arise is therefore the 
same in Sepia as in Loligo vulgaris (p. 261).* Here also the pre- 
hensile arm, as a rudiment, does not seem to be characterised in 
any special way. 

Another characteristic of the germ-dise at this early stage (Fig. 
128 A) is a pair of rather long, arched folds near the mouth, 
the later development of which leads us to recognise them as the 
posterior funnel-folds. Between these and the mantle lie two 
comma-shaped prominences, the gills. The anterior funnel-folds also 
(tf) are already present as rudiments. In their neighbourhood, lie 
the cirenlar otocysts (Fig. 128 A, of). These are the organs which 
K6LtikER, as VIALLETON pointed out, regarded as the nuchal 
cartilages. 

We have here, as in former descriptions of the first rudiments of external 
organs, repeatedly had to speak of folds (eg,, the funnel-folds), but this 
designation is not altogether justifiable, since, as WiacceTon has shown in 
sections of young Sepia embryos, these and other prominences, are, for the 
present, mere thickenings of the superficial cell-layer accompanied by slight 
bulging of the same, but these thickenings soon rise inte actual folds. This 
is especially the case in the further development of the mantle and the funnel 
in the next stages, 


While the organs mentioned have appeared as rudiments, the 
germ-dise only at first extends slightly over the yolk, occupying 
merely.a small part of it. The blastoderm also does not nearly cover 
the yolk, but appears in the form of a broad ring beneath the germ- 
disc. Over the rest of the egg, the yolk lies freely at the surface. 
The germ-dise and the blastoderm are covered with cilia which are 
also present in later stages, when the embryo has risen up from the 
yolk (Fig. 129 ©), 


* Our statements as to the rise of the arms rest upon our eal observations. 
Since the observations of Kénumer and Meet oe bes ae 
would be no need to mention this, especially as only he 
this stage were available, had not the order of devalopeaiied sraecar arms bean 
less clearly or otherwise described in other cases. 


DEVELOPMENT OF SEPIA. 275 


The development of Sepia (Fig. 128 #) consists for a time in the 
further growth of the rudiments of the organs already present. The 
edge of the mantle begins to rise from the germ-dise, and already 
covers the gills, only parts of which project from beneath it (Fig. 
128 B,k). The rudiment of the anus (a) appears between the gills. 
A depression which at first is crescent-shaped appears on the opposite 
side of the mantle, quite at the edge of the germ-disc ; this is the 
oval aperture (m). 

The funnel-folds also deserve mention. They have now united, 
sud the principal parts of the 
funnel ean already be made 
out in them, viz, the anterior 
folds (vt?) which yield the chief 
part of the funnel, the lateral 
parts (nuchal musele, Am) which 
run buck to the nuchal curtilage 
(nk) and, finally, the retractor- 
folds (vt) which run towards the 
gills, These parts are, indeed, 
for less distinct than in Loligo 
(Fig. 117 A and B, p. 259), 
‘but are nevertheless homologous 
with the similarly named struc- 
‘tures found in that genus. The 
origin of the funnel from two | 
jualves is, on the other hand, 
more distinct, that organ being 
formed here, as in Loligo, 
through the rising of the two pal side fale: Race) rae 
anterior folds which, after fm, nuchal muscle ; A(y, fonnel- 
obtaining in this way an increase real isc hens ees tn 
ann 
‘The principal part of the funnel derived from two half tubes, 
thus comes to lie in front of the mantle; its posterior aperture is 
tumed toward the latter and opens into the mantle-cavity after the 
mantle bas grown over the funnel. The narrow anterior aperture 
ix turned away from the mantle. 

In adult Cephalopods, the efferent aperture of the funnel is directed to- 
wards the mouth, for the funnel lies on the ventral surface between the anal 
and oral apertures (Figs. 120 and 121, p. 262). In the early stages of Sepia 











ae 


276 CEPHALOPODA. 


embryos, this is not self-evident, as apparently different conditions are brought 
about by the intercalation of the yolk-mass and the superficial extension of 
the germ. The efferent aporture of the funnel does not appear to be directed 
towards the mouth but rather turned away from it (Fig. 128 8). A com- 
parison with the embryos of oligo shows, however, that quite the same 
conditions prevail in the two cases. If we imagine e Loligo embryo, such as 
the one seen obliquely from above in Fig. 117 B, p. 259, spread out flat, we 
should find that the anterior aperture of the funnel is here also turned away 
from the oral aperture which lies on the further side of the mantle and, apart 
from the modifications peculiar to the Loligo embryo, we should have a view 
something like that given in Fig. 128 B. 


The further development of the *Sepia embryo is characterised by 
the fact that its superficial extension is arrested and it rises up from 
the yolk-sac, the yolk then pressing in beneath the arched embryonic 
rudiment ; in this way, an internal yolk-sac is formed as already 

i described for Loligo. The rise 

abl of the embryo from the yolk 

is very gradual, and has a fairly 
similar effect on the different 
organs. Fig. 129 A-C’ repre- 
sents a few stages in this 
Saas process. In the first two, the 
. ¢ embryo is seen from the oral 
side. The posterior funnel- 
folds (kéf) at first still lie rather 
far from the mantle, but the 
latter, by extending laterally, 
soon projects beyond them. At 
the same time, the mantle 
bends over and thus begins to 
assume its final shape. The 
embryo in its further rise from 
the yolk is also followed by 
oh the cephalic lobes and the 


Ftc. 130.—-Oler embryosof Sep eyes, organs which, as in Lolign, 
_ Tren -_ pealidde. (after K eae at this time and even later form 
be narrower. Lettering as in Fig. 129. the largest part of the embryo 

(Fig. 129 B). Fig. 129 C. 
representing the embryo at a somewhat later stage from the anal 
side, shows its great resemblance in external shape to the 

embryos of Loli at about the stage depicted in Fig. 119, p. 261. 

The gills are not yet completely grown over by the mantle; the 





FURTHER DIFFERENTIATION OF THE GERM-LAYERS, ETC. 277 


junction of the two posterior funnel-folds has taken place but these 
folds have not yet fused in the median line, On the mantle, the 
fins are visible, these apparently forming late in Sepia, The mouth 
lies at the opposite side; its position can be ascertained from 
Fig. 130 of a later stage. The yolk-suc is still very large, and is 
directly connected with the internal mass of yolk, As the yolk-sac 
is gradually absorbed, the large cephalic section decreases in size, 
approaching the final shape of the adult Sepia. By the time that 
the embryo is mature and ready to hatch, the greater part of the 
external yolk-sac has been absorbed. Only after its complete reduc- 
tion can the arms occupy their fillal position round the mouth. At 
hatching, they are still rather short, und only attain their full length 
during free life. The prehensile arms which, as rudiments in Sepia 
also, are not specially distinguished from the others (Figs, 128 and 
129), become characterised at later stages not only by their length 
(Wig. 130, a) but also by their bases sinking into the body. The 
depression thus caused is, in older embryos, visible even externally 
in the form of a horse-shoe-shaped fold lying above. the first pair 
of arms. 


4. The further differentiation of the Germ-layers and the 
formation of the Organs. 


A. The separation of the Germ-layers and the formation of the 
Yolk-epithelium and the Alimentary Canal. 

Only after the external form of the body is known is it possible to 
enter in detail into the further development of the germ-layers. 
‘These, in the Cephalopods, develop very late, or rather, they do not 
appear so distinctly here as in the other divisions of the Mollusea, 
As we have already remarked, the great accumulation of yolk in the 
embryo has, in this direction also, essentially modified the ontogenetic 
processes. 

Our description of the body-layers was interrupted at the stage at 
which there had formed, at the margin of the germ-dise which covered 
only a small part of the egg, a peripheral thickened ring (Fig 112, 
p- 247 and 131 A) and cells became detached from the edge which, 
according to the view adopted by ViALLETON, wandered beneath the 
superficial cell-layer (Fig. 114, p. 250) there to give rise to a con- 
neeted layer. ‘This lower cell-layer then extends over the whole yolk, 
and is followed by a middle layer * so that the yolk is now surrounded 


* See also p. 126, ete. 


278 CEPHALOVODA. 


by three cell-integuments, Yolk-cells are not found in the Cephalo- 
poda, and the yolk thus attains, in them, « greater independence 
than in the eggs of most Arthropoda and Vertebrata, whieh are also 
very rich in yolk. 

Very different conclusions haye been arrived at as to the signifi- 
cance of these cell-layers. We shall consider first the inner layer, 
the so-called yolk-epithelium. 

The yolk-epithelium is formed of large fattened cells which are 
swollen in the region of their nuclei, The only function of this layer 
is to yield an envelope for the yolk, and to bring about its utilisation 
by the embryo. In later stages it fs found surrounding the yolk still 
in the same state as before. The yolk, especially in the typical forms 
of Cephalopodan development in which it is plentiful, is accumulated 
principally in the external yolk-sac. This latter is directly continuous 
with the mass which lies now within the developing embryo (Fig. 
132); at a later stage, in consequence of the processes of growth 
that take place in the embryo, a constriction forms in the region of 
the arms (Fig. 120, p. 262), and a rather narrow duct here “in 
connecting the external with the internal yolk-sac (Fig. 133, a, ds, 
and #, ds). In this latter, again, various parts may be distinguished 
as lying respectively in the cephalic, the pallial, or the nuchal region, 
‘The part lying in the head gives off two outgrowths into the optic 
stalks, the nuchal portion narrows later and leads to the voluminous 
pallial portion, The embryo no doubt absorbs the yolk in the follow- 
ing way: the external yolk-sac passes on its contents to the internal 
sac, partly in consequence of the rhythmic contractions of its wall and 
partly in consequence of the processes of growth in the embryo itself, 
then the uutritive masses are conducted to the embryo from the inner 
yolk-sac through the intervention of the yolk-epithelium, Since, so 
far as we know, there are no vessels in the external sac, its dis- 
appearance cannot be accounted for in any other way. 

Tt has already been pointed out that the yolk-epithelium ix a 
closed unilaminar layer of cells extending round the whole yolk. In 
consequence of its close connection with the yolk, the yolk-epithelium 
must certainly be regarded as the inner layer of the Cephalopod 
germ. The question now arises, What is its relation to the future 
entaderm ? This latter first becomes perceptible in the following 
ways 

About the time when the first rudiments of organs appear ox- 
ternally on the embryo, there is seen, on the ventral side, contignons 
to the yolk, an epithelial plate which at first consists of only a few 


THE SEPARATION OF THE GERM-LAYERS, ETC. 279 


cells, This is the first indication of the enteron, which soon increases 
somewhat in size (Fig. 131 D, md) and finally separates from the 
yolk and appears sac-like (Fig. 132 A, md). Beneath it, the yolk- 
epithelium is now seen, which, in earlier stages, was wanting at this 
spot (KorscuEnt, No. 25). 

The sae-like rudiment of the enteron was known long ago and it 
was assumed, with great probability, that it might be connected 
with the yolk-epitheliam, and thus to a certain extent might be 
regarded as an outgrowth of the latter (Ray LANKEsTER, VIALLETON, 
Brucr). The two together would represent the entoderm, the 
vesicle being regarded as the permanent and the yolk-epithelium as 
the provisional part of the entoderm. Bosrerzky, on the other 
hand, considered that the vesicle arose as a mere differentiation of 
the lowest cell-layer of the middle layer, i.e, of the so-called 
‘mesoderm. There, indeed, appeur to be no yolk-epithelium at the 
stage when the epithelial plate above described as the first indica- 
tion of the enteron forms, either beneath that plate or in its near 
neighbourhood, and this has Jed to the assumption that the cells of 
the yolk-epithelium as well us the enteric plate arose as differentia- 
tions of a cell-layer which grew from the edge of the germ-disc 
towards its centre. 

This last view seems not without justification because it is very 
difficult to decide whether the yolk-epithelium presses beneath the 
germ-dise (Fig. 114, p. 250) or whether these cells are differentiated 
from the whole cell-mass. The cells which are directly in contact 
with the yolk actually bear a very close resemblance to those of the 
middle layer. 

These questions are of importance as determining the manner in 
which the germ-layers form. We have to imagine that the cell-mass 
pressing from the edge towards the centre of the germ-dise (Fig. 131 
A and B) represents the meso-entoderm. The whole process is then 
to be regarded as a much modified invagination. The edge of the 
germ-lisc corresponds to the blastopore which is filled by the large 
yolk-plug. The yolk-mass also fills the whole of the archenteric 
cavity (Fig. 131 2). 


In the Molluses considered earlier in this work, especially in the Gastro- 
poda, we have already found the mouth related to the blastopore, In Gnen- 
achen’s Cephalopodan embryo, we saw that the oral wperture arises in the 
neighbourhood of the aperture of the blastoderm which closes only at a very 
Tate stage (p. 270). Since we regard the latter as the blastopore, relations 
between it and the mouth may exist here also. 


280 CEPHALOPODA. 





Fie. 131. — oy illustrating the formation of the germ-layers, .1, thickening of 
the edge of the germ-lise ; B and C, differentiation of the yolk-epithelium, Further 
extension of the germ-dise over the yolk. ), differentiation of the rudiment of the 
enteron and the mesoderm; de, yolk-epithelium ; ect, ectoderm ; md, rudiment of 
enteron; wes, mesoderin ; erf (in 1), the rudiment of the cerebral ganglion, 





THE SEPARATION OF THE GERM-LAYERS, ETC. 281 


At a later stage, as already described, the lowest cell-layer, that 
which is in contact with the yolk, becomes differentiated and yields 
the provisional and the final entoderm (Fig. 171 Cand D, de, md). 
‘The cell-material which remains between these two and the ectoderm 
corresponds to the mesoderm, which, in its development is, like the 
entoderm, greatly influenced by the excessive abundance of the yolk. 
During these processes, the germ-dise has extended far over the ege 
(Fig. 131 @ and D). 

We need hardly point out that the formation of the germ-layers 
in the Cephalopoda, as compared with that in other Molluses is much 
modified ; transitions between the two types of formation may, how- 
ever, be found in the eggs of many Gastropods that are rich in yolk 
(e.g Navsa, Fig. 95, p. 207) although, in these latter cases, the 
modifications undergone by the process are not nearly so great. 
The entoderm, indeed, was there seen forming in « disconnected 
manner and the rudiment of the enteron was open towards the yolk 
(Figs. 123-135), as in the Cephalopoda, except that, in the 
latter, the yolk is still covered by the thin epithelial layer, 

The alimentary canal now develops, the enteron (Fig. 132 A, mu) 
inereasing in size and soon dividing into two parts, as is seen in Fig. 
132 C which represents « later stage. The lower part, which appears 
sac-like (#)), represents the rudiment of the ink-sac, and the upper 
part, which is open towards the yolk-epithelium, the actual stomach 
and intestine. Where this comes into contact with the ectoderm (a), 
fusion subsequently takes place and results in the anus, There is 
at this point only an inconsiderable depression of the ectoderm, and 
there is therefore no proctodaeum of any size, as is evident from the 
fact that the ink-sac, which originates from the entoderm, opens into 
the intestine in the adult quite near the anus. 

The enteron grows ont towards the apex of the yolk-sac, this 
being still more marked in later stages, It is growing toward the 
stomodaeum which is approaching it from the other side of the 
yolk-sac. This latter rudiment arose as an ectodermal depression 
‘on the opposite side of the blastoderm and farther down, é¢., more 
anteriorly. 

‘The positions of the mowth and the anus have already been meu- 
tioned and are made clearer by the sections now before us (Figs. 132 
and 133, also Figs. 116-120, pp. 255-262), The oral invagination arises 
below the ectodermal thickening depicted on the left in Fig. 131 A, 
wi. Another depression (sp), at first lying outside of the stomodaeum, 
represents the rudiment of the posterior or large salivary glands, At 


282 CEPHALOPODA. 


a later stage, the rudiment of the radudar sac is added (Figs. 132 and 
133, r), and a tubular depression, the rudiment of the anterior salivary 
glands, appears farther forward, 





Fre, 132,—Sagittal sections through embryos of Loliyo vn/gavis at various stuges, some- 
what diagrammatic (original). 3, section throught the region of the mouth. a, 
ent ; ¢, cerebral commissure ; ey, cerebral ganglion ; 
: eet, ectoderm ; ve, mouth; ma, wdge of mantle; Corea 
mes, mesoderm (indicated dia autnatically); vy, ractilar sac; aif, ; = 
salivary gland ; 4, ink-sae; ed, stomodacum, 





‘We may here summarise the development of the stomodaeum according to 
the numerous and careful investigations of Gnenacaen, Bosneraky, Ussow, 
‘Watase, Jovsrs, as follows. The rudiments of the salivary glands very soon 
divide into two branches assuming in this respect the final form of the adult 


i" _ eal 


THE SEPARATION OF THE GEHRM-LAYERS, BTC. 283 


organ. The posterior rudiment is specially large. The two branches, which 
diverge at a wide angle, carry diverticula and thus form the lobed masses of 
the lower pair of salivary glands (Grenacuer, No. 14; Jousrn, No. 22), The 
anpaired part of the rudiment, which corresponds to the common section of 





Fi, 138. ittal section through an older embryo of Loligo vulgaris, somewhat 

diogrammatic (original). «, anus; acs, external yolk-sac; ar, arm-rudiment ; bs, 

cerebral ganglion ; , Jyolk; de, yolk-epithelium ;' ect, 

art ‘ig ot yolkaast m mouth ; md, Intestine} mes 

7 mg, Fea re me of mantle; of, otocyst ; py, gun in 

radular aac ; salivary: giant idey nme) edoanal we bee: 
daecum : 1, oat ei 








the efferent duct, greatly lengthens, for, in the adult, the lower salivary glands 
lie far back, The rudiment of the radular sac also undergoes modification, 
‘the part of its wall which is turned backward and inward thickening and the 
radula being secreted in the way described above (p, 201 and Fig. 91 A). 


— 


284 CEPHALOPODA. 


Various prominences and folds appear in the epithelium of the stomodaeum 
near the mouth, and the jaws also arise here as cuticular secretions (JOUBIN. 
GrenacHER, BoBRETZEY). 


Long before the differentiation of the stomodaeum advanced to this 
point, it became united to the rudiment of the enteron, the two having 
grown up towards each other from opposite sides of the yolk, and 
having met near the apex of the inner yolk-sac, there fusing. Fig. 
133 represents a later stage, in which the enteron has dilated 
anteriorly and has thus formed the rudiments of the stomach (mg) 
and of the stomach-caecum (bx). 

At a somewhat earlier stage, the rudiment of the enteron shows a 
remarkable peculiarity, 
being wide open to- 
wards the yolk-epi- 
thelium, as is evident 
in sagittal sections 
(Fig. 132 C’) and still 
more in transverse 
sections (Fig. 134 A 
and 8). It here 
appears as a plate, a 
large part of which is 
in close contiguity to 
the yolk. The in- 
folding of the edges of 
this plate (Fig. 134 B) 
gives rise to the two 








k. a : 7 
Pio, 184.—The venteal portions of two transverse see. hepatic tubes which 
tions‘of embryos of align rnigaris at different. aj open into the enteron 
(original). @, anal region; de, yolk-epitheliu aa 
ret, ectoderm ; &, branchial rudiments; /-liver; md i the region of the 
enteron; mes, mesoderm ; r, vascular spaces in the Gaecum. 
mesoderm. . 











The wide opening 
of the enteron towards the yolk-epithelium gradually narrows, 
but can still be distinctly made out even in later stages (Fig. 
13. Below it, large cells of the yolk-epithelium can be seen 
lying, and sending off lateral processes into the yolk (Fig. 133). 
The yolk is thus completely covered by the yolk-epithelium even 
beneath these gaps in the intestinal epithelium, where a con- 
nection of the lumen of the intestine with the yolk-sac might be 
assumed, as well as below the former wide aperture of the euteron. 
There tx, therefore, no direct communication between yolk-sac and enteron. 





THE SEPARATION OF THE GERM-LAYERS, BTO. 285 


The yolk-material thus does not pass directly into the intestinal 
cavity, but hus first to puss through the yolk-epithelium. The latter 
consequently promotes the absorption of the yolk by the embryo, this 
being its principal function. A specially active inception of nutritive 
substance probably takes place at the open part of the enteron by 
means of the yolk-epithelium. This view is confirmed by the rise of 
the liver in this region, this organ showing in other Molluscs also 
a close relation to the nutritive substance of the egg, and also by 
the appearance of the large rhizopod-like cells in the yolk-epithelium 
which separate the cavity of the enteron and the yolk-sac. 

When the gap in the intestinal epithelium closes as development 
advances, the internal yolk-sac appears to lie in the body-cavity 
quite unconnected with the enteron. The external yolk-sac gradually 
decreases in size as its contents are transported to the internal sac 
whence they are absorbed and, when completely taken up, the internal 
suc itself shares the same fate, the yolk-epithelium being the last to 
disappear, its Function being now fulfilled. 

‘The function of the yolk-epithelium resembles that of the yolk-cells of the 
Arthropeda and the Vertebrates, described above. This comparison has 
already been made by Ray Lankesten, ViacceTox, Warase and others, and 
the resemblance is heightened by the fact that the yolk-cells may also appear 
as a peripheral layer, the outer merocyte-layer of the Selachians or the so- 
called periblasts of the Teleosteans. Some difference between these and the 
yolk-epithelium of the Cephalopoda still, however, remains, since, in the 
Vertebrates, these cells are at first distributed throughout the yolk and then 
collect into a continuous layer, whereas, in the Cephalopoda, the cells are 
never found in the yolk, the yolk-epithelium being produced direct from the 
cells of the germ-disc. The type of the meroblastic egg is thue specially 
marked in the Cephalopoda, 

Tn order to complete our description of the development of the 
alimentary canal, some reference must be made to the ink-sae. We 
have already seen that it arises from the rudiment of the enteron as 
a vesicular structure (Fig. 132 C, md). It soon deepens, and grows 
out asa tube which is surrounded by mesoderm-cells. In this tube, 
two sections can soon be distinguished, the inner blind end, the walls 
of which are much folded (Grrop), and the superficial part which 
opens externally and becomes greatly dilated, but remains lined with 
au simple epithelial layer. The inner part of the ink-bag represents 
the glandular secreting part, while the dilated portion which finally, 
through a long efferent duct, opens into the intestine near the anus, 
forms the reservoir for the secretion. As has already been pointed 
out (p. 281), the fact that this entodermal structure opens close to 


— 


286 CEPHALOPODA. 


the anus proves conclusively that there is here no long proctodaeum, 
Nevertheless, a very considerable part of the alimentary canal has 
actually, by some authors, been attributed to a proctodacal invagina- 
tion. Although we considered this view as disproved, we mention it 
here as having formerly been supported by the majority of authors 
(Merseunrgorr, No, 32; Grexacuer, No. 14; Ussow, No. 44; 
Gop, No. 12; Warvasn, No. 49). 


According to these authors, the structure spoken of as the enteron was 
already connected with the ectoderm from its earliest development, and, as 
this gives rise to the intestine, the latter must therefore have arisen in the 
form of an ectodermal depression, iv., as a proctodaeum, Ussow, as well as 
Girop and Watase, who later investigated this subject very thoroughly, must 
be regarded as having adopted this view, the details of which are here un- 
necessary. The hypothetical proctodaeum grows up over the yolk, becoming 
differentiated in the way described above for the enteron. As to the point to 
which the proctodaeum extends forward (or the stomodseum backward) 
opinions are divided, but according to this view, the liver, the eaecum and the 
stomach are all derived from the ectoderm, since the whole alimentary canal 
is produced by the union of the stomodaeum growing backward and the 
proctodaeum advancing forward. The whole of the entoderm is represented 
by the yolk-epithelium and is quite transitory (Warass). Similar statements 
ws to the ectodermal origin of the alimentary canal have been made in 
connection with other animals (e.g., Insects, Gantn, Wrrnaczi, Grane, 
Heywons), but are, in such cases also, altogether improbable, as is proved by 
the condition of nearly related forms. 

As opposed to the view to which we have just briefly referred, we have given 
that maintained by Ray Lanxusrer (No. 29); VIALLETON (No. 48); Bosrerexy, 
(No. 4) and confirmed by ourselves (No. 25) in much earlier stages of de- 
velopment, as, apart from its greater probability, this derivation of the 
alimentary canal seems much better founded. 


B, The Covering of the Body and the Shell. 


The ectoderm which covers the body of the embryo seems to pass, 
with only slight modifications, direct into the body-epithelium 
(epidermis) of the adult. The shell appears as the secretion of a 
specially modified part of the ectoderm. In studying the embryonic 
formation of this organ which is of such importance for the compre- 
hension of the Cephalopodan body, we are unfortunately restricted to 
those forms in which it no longer attains full development. Only in 
a few recent Cephalopods such as Nautilus and Spirula * is the shell 


* [It is very questionable if the shell of Spirula can be regarded as perfect ; 
it is almost internal and evidently much reduced —Ep.} _ 


INTERPRETATION OF THE SHELL IN RECENT OEPHALOPODS. 287 


found in its perfect form, and the development of these rare animals 
is not known, ‘The shell of Argonauta exemplifies other conditions 
which will be discussed later (p. 294). In those recent Cephalopods 
in which the development of the shell has been investigated, it lies, 
enclosed in the mantle (and is thus internal) on the antero-dorsal 
surface of the body, and either develops into the so-called pen, of a 
horny character (Onunastrephes, Loligo, and others) or consists of 
numerous calcareous layers built upon a horny foundation (Sapia). 
It forms in an invagination of the ectoderm, the shell-gland. 

In a very early embryonic period, a depression appears at the 
centre of the mantle-rudiment, this being the first indication of the 
shell-gland (Figs. 115, 116, p, 255, Fig. 131 D, p. 280), At first, in 
Loligo, this is a wide, shallow pit, but the margin of the pit soon grows 
inwards and constricts its aperture, the pit finally assuming the form 
of a sac connected with the exterior by a small opening. This sac is 

. lined with an epithelium composed of cells which, at its base, 
are specially long, and is surrounded by mesodermal tissue. The 
aperture of invagination completely closes at a later stage, and the 
shell-gland then lies internally as a closed sac, surrounded by the 
mesodermal tissue (Fig. 132 C). It extends later especially anteriorly 
and then occupies a large part of the antero-dorsal side of the mantle 
(Fig. 133). The secretion of the shell then takes place within it 
(Ussow, Borrerzky). 


The Interpretation of the Shell in Recent Cephalopods. 


There can be no doubt that we have in this case an internal shell, 
but the question remains, What is its relation to the large external 
shell met with in the (living) Vawtifus, in the Ammonites and other 
extinct forms? This is a point of importance in studying the manner 
of formation of the Cephalopodan shell and its relation to that of 
other Molluses. In solving this question it is necessary to institute 
comparisons with the shells of various extinct forms. 


The shell of the recent Dibranchia is very differently developed in the 
various forms. It occasionally consists merely of a long, narrow, horny, 
plate, shaped like » symmetrical bird’s feather, but otherwise not specially 
differentiated (e.g., in Loligo). In other cases, the plate is less simply formed, 
its posterior end forming u hollow cone, the whole shell thus being slipper- 
shaped (Ommastrephes, Fig, 140), 

The calcareous shell of Sepia (Figs. 137, 188 4) is' much more complicated 
in structure, and is composed of many calcareous layers. Its structure is still 
Hot fully understood, but it has been compared with the more highly 


a 


288 . CEPHALOPODA. 


developed Cephalopodan shells. Among the living Dibranchia, the shell 
which appears to approach most nearly to those of the extinct forms is that 
of Spirula; here we find a spirally coiled and chambered shell which, how- 
ever, is grown over and enclosed by the mantle. This approximates most 
nearly to the shell of certain Belemnites which was also an internal shell 
though, so far as its chambered portion (phragmocone) was concerned, it was 
less highly developed than that of Spirula. “ 

The shell of the Belemnite is not, like that of Nautilus or most Ammonites, 
spirally coiled, but is straight like that of the Orthoceratidae (Nautiloides). 
It is characteristic of the Belemnite that in addition to the part of it, the 
phragmocone, that may be regarded as corresponding to the actual cham. 
bered Cephalopodan shell (that of the Ammonites 
and Nautilus) there is a calcareous pointed external 
investing piece, the so-called guard or rostrum. A 
good example of this latter is afforded in the fossil 
Spirulirostra (Fig. 185) the phragmocone of which 
is curved and thus bears a certain resemblance to 
that of ‘Spirula, but has, addition, dorsally and 
late rally, a large conical rostrum. It has also been 
maintained that traces of such a rostrum are to be 
found in Spirula, although these were not found by 
us in an examination of a large number of shells.* 

The shell of the Belemnite is, as already men- 
tioned, straight. Two parts can be distinguished in 
it. The chambered part (phragmocone) is provided 
with siphon and is surrounded by the actual shell- 
wall (the ostracum); this latter becomes specially 
dilated towards the head of the animal as the su- 
called proostracum, and is not here followed by the 
phragmocone. This first portion of the shell might 
be compared with the Ammonite or Nautilus shell, 
but on the side opposite to the proostracum, sur- 

oe rounding the posterior part of the phragmocone and 

- Longitudinal i satis 3 
section through the prolonged in the same direction, there is a second 
shell of a Spiru/i- part, a very large rostrum, which is usually the 
rustra ir only part of the whole Belemnite to be preserved 
cae ithau,’ i @ fossil condition. ‘That this shell was internal. 
i,e., surrounded by the mantle, seems to be highly 
probable from observations made on forms resembling Belemnites but better 




















* The position of Spirula as a branch of the Belemnite stock connected to 
it by forms like Spirudirustra seems to us doubtful. While the position of 
the siphon and the orientation of the shell with regard to the body would 
seem to favour this view, the constitution of the shell, on the other hand. 
with its well-retained chambers and the siphon renders it improbable that 
it has undergone a process of degeneration which led to the total loss of the 
rostrum. The shells of other recent Cephalopods, in which such degeneration 
took place, underwent, iu consequence, great change of structure. We must. 
in any case, take into account the view that Spirula may have separated from 
the Decapodan stock before acquiring a rostrum. 





INTERPRETATION OF THE SHELL IN RECENT CEPHALOPODS. 


289 


preserved, and as is also shown by the so-called vascular impressions on the 


external surface of the rostrum of many 
Relemnites,* 

Attempts have been made to deduce the 
constituent parts of the shell of Sepia from 
the above parts of the Belemnite shell 
(Voutz, RigrstaHL, No. 39). The shell of 
Sepia, or, as it is generally termed, the cuttle- 
bone, is very complicated. The whole forms 
an oval shield-like structure, which, for the 
most part, is biconvex, but in the more dorsal 
region it becomes concave on its posterior 
or inner side, its shape is well shown in 
Figs. 187, 138 A. Its antero-dorsal surface 
is covered externally by a roughly calcified 
shagreen-like layer, the outer layer, under 
which is a deposit of horn-like matter (con- 
chyolin), the middle layer, the latter being 
freely exposed at the margin of the shell 
(Fig. 137, mp). Dorsally, the shell is 
produced into a small pointed structure 
(Figs. 137 and 138, k, d) which consists 
essentially of a prolongation of the outer 
calcified layer but has become covered by 8 
secondary development of horny (conchyolin) 
matter which is quite distinct from the 
horny middle layer. This calcareous spine 
may in some species project freely on to 
the exterior (8. andreanoides). On the 
posterior or internal surface of the shell is 
a prominent swelling produced by a great 
deposit of calcareous material arranged in 
thin oblique layers (Fig. 138 -1, 1), separated 
from one another by air-spaces closed by 
calcareous supporting trabeculae; this 
structure which is most developed near the 
antero-ventral portion of the shell serves as 
@ float. Dorsally this portion of the shell 
is less developed and consequently the mar- 
gins of the shield are here much more pro- 
nounced. Surrounding the posterior remnaut 
of the calcareous swelling is a modified forked 
or V-shaped area (Fig. 137, 9), the two ends 
of which are directed forward ; this ledge, 








Fio. 136,—Median longitudinal 
vection’ through the shell of 
Belerunite, somewhat diagram- 








matic, ek, embryonic chamber; 
ph, phragmocon - 
tracum ; 7, rostrum ; , siphon. 


The dotted lines indicate the 
anterior edge of the shell the 
limits of which are at present 
not accurately known, 


* We do not here follow out this point, since, for our purposes, it ix of 
no special importance that in certain Belemnites the posterior part of the 
Tostrum projects as a more or less long spine beyoud the mantle, giving the 
posterior end of the animal the shape of an arrow, an adaptation favourable 


to locomotion. 
u 


290 CEPHALOPODA. 


the posterior part of which is somewhat raised and arched forward, forms 
& cavity which in some cases (8. officinalis) is shallow, but in other species 
(S. aculeata, Fig. 137) tolerably deep. 

These parts of the Sepia shell have been homologised with those of the 
Belemnite shell in the following way. The spine, together with the outer 
calcareous plate, have been thought to correspond to the rostrum of the 
Belemnite (cf. Figs. 186 and 137) which is continued far on to the actual 
shell, almost as if the proostracum of the Belemnite were covered by an 
externa! calcareous investment connected with the rostrum, as perhaps may 
actually be the case. A similar condition is found in Spirulirostra, in which 
the rostrum embraces a large part of the shell (Fig. 185, r). - 

The actual shell of the Belemnite, i.e., the 
phragmocone and proostracum, corresponds 
to the two inner layers of the shield in Sepia, 
the prominence and the fork (Figs. 196-188, 
w and g). While the two outer layers are to 
be regarded as the wall of the shell (ostracum). 
the lamellae of the prominence may perhaps 
be considered as partition-walls between the 
chambors. These lamellae end posteriorly 
in free edges (Figs. 187 and 188); laterally, 
however, they are continued into corres- 
ponding lamellae of the forked ledge. As 
this latter rises anteriorly over the posterior 
end of the prominence and forms a rather 
deep cavity posteriorly, a structure arises 
which actually resembles the phragmocone 
of the Belemnite. If the comparison is 
carried further, the wide aperture of the 
posteriorly directed partition-walls of the 
chambers might be compared to the siphonal 
spaces in the Ammonites, which, however, 
iw aculedtt. have become very wide and in which a con- 
from the surface 
i d.spine; y, forked Siderable part of the body lies. 
dee ie donee ay th: This view seems to be supported by the 
vy promiuence,, showing ‘the CDdition of a fossil form (Belosepia) the shell 
frve edges of the lamellae. of which bears a general resemblance to that 

of Sepia but still shows the phragmocone 
fairly distinctly (Fig. 188 3 and C). In place of the siphon there is, in this 
form, a wide cavity (Fig. 188 4), and this may be regarded as marking a 
transition to the condition of Sepia. The rostrum in these forms resembles 
that of Sepia, but is still more strongly developed (Fig. 138 4 and B).* 

If the lamellae are regarded as partition-walls of the chambers, it appear~ 
remarkable that these latter extend anteriorly; that is, that the proostracum 
thus completely disappears, for the whole prominence would then correspond 


to the phragmocone. 
























* We refrain from comparing the antorior part of the shell (of which usually 
only the hind or dorsal end is retained) with the shell of Sepia, but it seems 


possible that here also resemblance can be found. 


INTERPRETATION OF THE SHELL IN RECENT CEPHALOFODS. 291 


‘The lamellae are connected by numerous delicate calcareous trabeculae, so 
that the spaces between them are not empty, as one might expect if they 
represented chambers. But this can hardly be reckoned as an argument 
against the above interpretation of the Sepia shell, as such a modification of 
the shell in adaptation to new functions (as a float) is quite explicable, 

The development of the different parts of the Sepia shell has beer investi- 
gated in detail by Arretérr, but has, so far as we know, been deseribed only 
in short Swedish treatise (No. 2) from which it is impossible to judge 
whether factors of import- 
ance for the morphological 
interpretation of the shell 
have been discovered, 

Finally, it appears neces- 
sary to point out that this 
whole comparison is still 
far from being well founded, 
although it may be con- 
sidered as extremely 
plausible, 

Other recent Gephalo- 
pods, especially those which 
are universally regarded 
as more primitive than 
Sepia, have a shell of very 
simple structure, carrying 
‘ab its end at the most a 
hollow oone (Ommastrephes, 
Fig. 140). If this structure 
is compared with the phrag- 
mocone, the rest of the 
shell would have to be 
regarded as the proostra- 
cum, and this suggests the 
idea that, in Sepia also, 
the fork which bifurcates Rae A ee i 
solerty and she con- 1854, agmatine of 
tained cavity may be ‘ville’, seen from the side; C, posterior part of the 
regarded as such a much- same, seen from the ventral side ( and C after 
Stiatepireamcoave: [he senee spe pl pliragmocone; r. rostrum ; 
whole of the part lying 
anteriorly to it (the prominence) would then have to be considered as the 
Proostracum, which has perhaps attained such a large size in adaptation 
to its present function, the diminution of the specific gravity of the body, 
‘The Iamellate stracture of the prominence would then be traceable to a 
secondary modification causing the secretion of the shell in layers, to form 
the air-cavities of the float; under these cireumstances the higher morpholo- 
ical significance could not be ascribed to it. Further light upon the subject 
of the significance of the shell of Sepia and its relation to the shells of the 








292 ‘CEPHALOPODA, 
fossil forms may be expected from detailed palacontological investigations and 
perhaps also from more comprehensive ontogenetic researches: 

A comparison of the shell of Sepia with that of Belemnites, such as was 
attempted above, suggests a relation between the Dibranchia in general and 
the Belemnitidae, This indeed seems a bold proceeding, since nothing certain. 
is known of the aoft parts of these Cephalopods, but forms like Belemnotouthis, 
a Cephalopod living in Triassic times with 
well-preserved phragmocone and arms 
carrying hooks, as well as Acanthoteuthis, a 
Decapod much nearer the recent Decapods 
and also armed with hooks (Jaren, No. 
17), indicate with coisiderable certainty 
that the Dibranchia or at least the Deca- 
~ poda are to be derived from forms resemb- 
ling the Belemnitidae. 

There can be no doubt that the shell of 
the Belemnitidae was internal and was 
almost completely enclosed in the mantle. 
Of the transitionary forms, moreover, 
Belemnoteuthis shows on the phragmocone 
which is still provided with chambers and 
siphon a large and distinctly bounded 
proostracum (Fig, 139, po) recalling, in its 
shape, the Sepia shell. The rostrum, in 
these forms, is either wanting or, when 
present, is only a slight appendix to the 
phragmocone. In this respect, these forms 
would approximate to the recent forms 
in which the shell has a posterior cup 
(Ommastrephes, Onychoteuthis, Taowius, 


pi 


Fic, 139,—Shell of Belomnoteuthis 
from the lower Lias, Lyme 
Regi somewhat Giagremarratin 

iginal).* ‘The shell is seen 
the funnel-side with the 
ink-sac lying (#) upon it. In 
the phragmocone (p/h), the most 
rior ‘is wanting aud is 
indicated by dotted lines. The 
partition-walle orn then chambers 
are seen on the surf aos owing to 
the posterior portion being 
broken away ; po, proostracum. 





Leachia). 

It is of interest that, in Ommastrephes, 
regular transverse striation is found on the 
hollow cone (Fig. 140); this is quite distinet 
from the lines of growth in other parts of 
the shell and may perhaps be regarded as 
the last vestige of the chambering of the 
phragmocone, [Genatus Fabricii, according 
to Srnexsrrur, has a series of chambers 
at the end of its horny pen.) Such « view 


does not appear unjustifiable, as Omuwmax- 
trephes is among the most primitive of the extant Cephalopoda, JamKeL 
has already pointed out (No.17) that Ommastrephes also, in the possession of 
small hooks, shows\a primitive character and recalls the hook-bearing transi- 
tionary forms mentioned above (Lelemnoteuthis, Acanthoteuthis), 


Fig. 189 represents a very instructive and as yet undescribed 
isan e collection of Dr, O, JawKer, kindly placed at our Our 
thanks are due to him also for revising the figure, 


INTERPRETATION OF THE SHELL IN RECENT CEVHALOPODS. 293 


The reduction of the shell goes still farther in other recent Cephalopods ; 
the terminal cone, in older specimens of Dovidieus, is found to be solid, 
whereas, in the younger animals, it was hollow (Stwexsrrup). In some 
Cranchiidae the hollow cone is still present at the end of the shell, in others 
it has disappeared and, in its place, there is mere solid swelling. 
Finally, @ simple horny plate develops, as in Lolig. The 

. hollow cone does not even appear ontogenetically, so far as we 
know at present, 

The above comparison seems to show with certainty that the 
shell in the Cephalopoda is internal, the manner in which it 
arose from an external shell being still exemplified in a living 
form, Spirula. Nautilus, only a small part of the mantle 
covers the exte shell, but the process of circumcrescence 
of the shell went farther, until the shell became covered, though 
incompletely, by the mantle, asin Spirula. During this process, 
the size of the shell as compared with that of the animal became 
reduced in most cases; at the same time, it changed its position 
and gradually degenerated, since it no longer functioned in the 
same way, Externally, new calcareous layers became added 
to the primitive shell, for we find that only the inner part of 
the shell of Belemnites or Sepia corresponds to the shell of 
Nautilus, the rostrum and its continuation as a covering of the 
proostracum are secondary structures, no doubt secreted by the 
mantle-sac which surrounded the shell. We are here again 
brought to the question of chief interest in connection with this 
subject, viz., the manner of formation of the shell. 

We saw above that the shell is formed in an ectodermal 
depression, the shell-gland. It would be well to discover 
whether this shell-gland is homologous with the organ of the 
game name in the Lamellibranchia and Gastropoda or not. 
This question has been raised before now by Ray Lanxestun 
(No. 28) who maintained the negative because he believed that 
the shell of Sepia corresponds to the Belemnite shell and conse- 
quently must be formed in a mantle-sac and not in the primitive 
shell-gland, Ray Lankesten was obliged to take up this 
position decisively since he considered the Sepia shell as 
homologous with the external part only of the shell of 
Belemnites and lett the phragmocone out of account. 

In deciding the question as to the significance of the shell- 
gland in the Cephalopoda, we are inclined from the first to 
ascribe to this organ which appears so early, in consequence 
of its position and development, the same significance as is 
possessed by the shell-gland in the other Mollusca, and thus 





Pia. 140.—Posterior veal of the shell of poate secre the a Sacre seen 
from the surface (original coni at D 
Peale sialk ehh voters, Aocaliy: vente Leonieting ent an the. cotical 
appendage: aE the strong horny ledges betwers which the shell consists merely of & 

membrane strengthened by ribs. 


— 


294 CEPHALOPODA. 


to consider it as fully homologous with this latter structure. The most 
natural course is to seek for a confirmation of this view in the ontogeny of 
those Cephalopods which are provided with an external shell. Since the 
development of the shell is unknown both in Nautilus and Spirula, em- 
bryos being unobtainable at present, we might turn to the only Cephalopod 
with external shell which is more accessible, viz., Argonan/a, if the conditions 
in this case were not essentially modified. 

Tt has already been shown (p, 266) that a shell-gland does indeed appear in 
the embryo of Argonauta, but that it disappears later and does not give rise 
to the shell of the adult. The latter is not formed within the egg-shell, as 
Was assumed by a few of the older authors (Port, Dette Cxraze, No. 9) but 
rises later, as was observed by Mrs. Power, Apams and Kéuumer (Nos, b 
and 24). The statements made as to the origin of the shell are somewhat 
peculiar and obscure, According to the almost universal view, the shell is 
secreted by the expanded surfaces of the dorsal arms which cover the shell 
when fully formed. ‘his view, which at first sight is rather improbable, is 
rendered still more so by the fact that the regeneration of parts of the shell 
which are lost is said to take place from within, The mantle might also be 
regarded as a source of the shell, but it is not closely connected with she 
latter and so this view also has no support. 

‘The disappearance of the shell-gland in the embryo of Argonauts shows 
that the adult shell, in this case, is not a structure which can be homologised 
with the shells of other Cephalopods, If, as is stated, the shell-gland actually 
flattens out, the shell may have arisen from a part of the mantle which 
originally corresponded to the shell-gland. The position of the animal with 
respect to the shell is the same as in the Ammonites and Nantilus, while, in 
Spirula, on the contrary, the orientation is different, the concave and not the 
convex side of the shell here corresponding to the ventral side, 

An attempt has receutly been made to derive the Argonaut shell directly 
from that of Scaplites, the external form in the two cases having a certain 
similarity (STenvmasx, No, 43). We are unable to accept such a view be- 
cause we do not regard the Argonaut shell as directly homologous with the 
Ammonite shell, apart from the fact that a long period elapsed between the 
disappearance of Scaphites and the appearance of Argonauta, the latter, more- 
over, belongs to the order Octopoda wnd is thus closely related to the other 
living Dibranchia. 

If the shell of Argonauta is to be derived from that of Scaphites, a com- 
paratively quick disappearance of the chambering of the shell without 
essential modification of the external form must be assumed, The chamber- 
ing of the shell, however, and the manner in which the animal is connected 
with it reappears in so marked a manner in all Cephalopoda (in which the 
shell is well preserved) that we are not warranted in assuming that 4rgonauta 
relinquished the chambering shell and received sea-water into the living 
chamber, a change which would involve a complete alteration of the manner 
of life of the animal. 

From what is known of the modifications undergone by the Cephalopod 
shell, it always appears to take place in the same way as in the forms with 
internal shells. Although, in them also, the significance of the shell is 
essentially modified, the chambering is retained (Belemnites) and disappears 


4 _ 


THE SENSORY ORGANS. 295 


only when the degeneration of the shell has reached its highest limit (horny 
shell of the Dibranchia). We might presuppose a similar process in the 
ancestors of Argonauta, and thus claim the shell which occura only in the 
female and is altogether wanting in the male, ax a new formation.® 

The only Cephalopod provided with an externa] shell, the ontogeny of 
which is at present known, is thus not adapted to assist in the solution of 
the problem as to the significance of the shell-gland; we are therefore 
restricted to the embryological facts concerning the forms with internal 
shell. 

Since the invagination known as the shell-gland secretes the whole shell, 
and therefore also the part of it which corresponds to the rostrum of the 
Belemnites, and as this is a part added to the primitive (Ammonite or 
Nautilus) shell, there can be no doubt that the invagination ix the equivalent 
of at least that part of the mantle-sac which covers the internal shell. The 
extraordinarily early appearance of the invagination indicates, however, that, 
in the Cephalopoda as in other Molluscs, the original shell owes its origin to 
@ shell-gland. If this is the case, we might assume that in the course of 
development the shell-gland became connected with this secondary mantle- 
sac. The position of the primitive invagination is easily reconcilable with 
this assumption. This question can be satisfactorily answered only when the 
formation of the shell in recent Cephalopods with external shell such as 
Spirula and above all Nautilus, is understood. Since the first of these forms 
is closely allied with the Decapoda and since, from the examination of the 
ovaries in the latter (OWEN, No. 33) it is known that, like other Cephalopoda, 
it has large eggs rich in yolk, it is uot too much to assume that similar 
processes of development took place in these forms also, the conditions 
of development of the shell especially being similar. 





C. The Sensory Organs. 


The sensory organs of the Cephalopoda (olfactory, auditory and 
visual organs) show much similarity in their development, all appear- 
ing first as invaginations of the ectoderm. The olfactory organs are, 
throughout life, mere ectodermal invaginations, but the auditory 
organs and especially the eyes become partly or altogether separated 
from the ectoderm and reach a high degree of development. In 
these cases also, however, traces of the connection with the ectoderm 
may be retained either as vestigial or specialised structures (as in 
the auditory organs) or by the retention of the original aperture of 
invagination, this latter condition being exhibited in the eye of 
Nautilus, 


* Cirrhoteuthis is said, unlike other Uctopoda, to possess a shell, the nature 
of which, however, is not well understood. If it isa true shell, it no doubt 
arises from  shell-gland as in the Decapoda, and we should be justified in 
assuming that forms like Octopus and .trgonauta, in which a shell-gland 
occurs, once possessed vestigial shells. The case inhabited by Argonuuta 
could then no longer be homologised with a true Cephalopodan shell. 


296 CEPHALOPODA. 


The Olfactory Organs. 


These organs, unlike the eyes and the auditory vesicles, appear in the 
embryo at a very late stage. In Sepia, in which they were observed 
by ZeRnor¥ (und previously by K6LLrKER) at a time when all the 
arms, the funnel and the chromatophores have already formed, there 
appears, behind each of the eyes, a round prominence. The edges of 
this rise and curve over towards the centre and thus an invagination 
of the ectoderm is brought about which at first is rather shallow and 
sac-like, its floor being much thickened, while the covering consists 
of thinner cell-layers. Some of the ectodermal elements in the floor 
of the olfactory sac take the form of spindle-shaped sensory cells pro- 
duced into stiff setae. This is the condition in the adult Eledone, 
while in Sepia and Loligo the intermediate and supporting epithelial 
cells become much lengthened and invested with movable cilia. The 
organ at a later stage becomes deeper and sac-like this being the 
usual adult condition. 

The papillae which, in Aryonauta, usually take the place of the 
olfactory pits, are considered by KGLLIKER. as the equivalent of 
the prominences which, in other Cephalopods, ontogenetically precede 
the invagination, this author consequently regarding them as a lower 
stage of development of the olfactory organ. 


These organs cannot be homologised with the osphradial olfactory organs 
which are so strikingly developed in the Prosobranchia, and in a lesser degree 
in many other Molluscs, since the latter are found in the mantle-cavity near 
the gills, whereas the former occur on the head near the eye. In Nautilus, 
true osphradia occur near the gills. [According to WILLEY, two pairs of 
these organs are present. This author also described two pairs of olfactory 
tentacles, the pre- and post-occular tentacles.] 


Otocysts. 


The rise of the otocysts has been observed in most of the forms. 
of which the ontogeny is known, and these organs have already been 
depicted in many of the figures here ziven (Figs. 116-118, p. 260, 1 
p. 265, 126 p. 270 and 128 p. 273). KOLLIKER examined in detai 
their (later) structure, and they were subsequently carefully studied 
by Ray LankesTER and GRENACHER. 

The position of the otocysts in the embryo may be ascertained 
from the above-mentioned figures. They form as depressions of the 
ectoderm (Fig. 141 A) which gradually deepen and become vesicular 
(Fig. 141 B and (). The aperture of invagination does not close 








THE SENSORY ORGANS—OTOCYSTS. 297 


for some time, and its connection with the sue becomes elongated 
and tubular (2 and @). This appendage, which was described by 
K6tnrmer and by GrenacHer, named Kéiorker’s duct, seems at 
first to communicate with 
the exterior, but is said 
later to become separated 
from the surface and to 
end blindly. [ts interior 
is lined with cilia directed 
towards the aperture of 
the otocyst which are in 
constant undulating move- 
ment, This appendage 
is also found in the adult. 
Baxrovr compares it with 
the recessus vestiould of the 
Vertebrates, the — blind 
appendage of the primitive 
auditory vesicle which re- 
presents its former connec- 
“tion with the point of 
invagination. 

Tn that part of the wall 
of the auditory vesicle 
which lies almost opposite 
to the point at which 
KGturken’s duct enters, 
the epithelial cells thicken 
‘to form the crista acustica, 
and it is here that the 
secretion of the otolith 
takes place (Fig. 141 D). 

The furtherdevelopment 





Fig. 141. —Sections through the funnel-region of 

of the otocysts is brought several advanced embryos of Loligo wulgurin 

r me (original). A.C, transverse sections, /), sagittal 

about by the differentiation pection, sonemtint Mingramuatic, "The yolk 

i i as been omitted. de, yolk-epithelium ; ect, 

OF the erixta: aewatica which ectoderm ; mex, mesoderm ; Hh otoeyst ; fF, 
extends fur over the wall fonnel-foltts. 


of the vesicle. The cells 

of the evista acusticn lengthen, the inner free ends developing « 
nimber of tine hairs. In this way arise the sensory epithelia which 
compose the auditory ridges described by Kowannvsky and 


i 


298 CEPHALOPODA. 


Owssannikow (and also probably the auditory plate which only 
develops later). In examining the formation of this terminal sensory 
apparatus, GRENACHER thought he could also recognise the nerves 
which give off branches to the cells in the form of delicate fibrous 
strands. 

While the internal structure of the otocysts is thus developing, 
the organs change their position, gradually shifting from a lateral 
position to below the funnel (Fig. 141 4-C) where, as large closed 
sacs, they are found in close contact with the pleuro-visceral ganglia 
(Figs. 133, of, p. 283 and 143, ac), Finally they come into close 
contact with one another and flatten hy mutual pressure, as was 
observed in GRreNAcHER's embryo and in Sepia. Their detinitive 
position being attained, the cephalic cartilage develcps round them- 


The Eyes. 


The origin of the eyes in the Cephalopoda has been carefully 
studied by Grenacner (No, 14), Ray Lankester (No. 29), and 
Boprerany (No. 4). 

Figs. 115-119, pp. 253-261 will help the reader to understand the 
orientation of the eyerudiments in the embryo. These organs 

originate in connection 

A with the large swellings 

(Fig. 115, au) as two 

lurge, rather — shallow 

ectodermal depressions 

(Fig. 142). The floor of 

eA each depression —_ s00n 

Yas thickens considerably and. 

Na Sian” its margins grow up and 

9, Trees esi Droeh ine acs ae 
of the eve in Rolige (after Ray L mu from (Fig. 142 2). A 

Seren oe ie eae ee a produced with 

a thinouterand thickened 

inner wall and this is connected with the exterior by a small aperture. 

The inner wall of this vesicle yields the retina, while the outer wall 

yields a part of the lens aud the ciliary body. 

It is an interesting fact that this stage of development is retained 
throughout life in the eye of one Cephalopod, Nawfilus (Fig. 145). 
The adult eye, in Nautilus, corresponds to the primitive optic vesicle, 
the cavity of which is lined by the retina, 7.¢., modified ectoderm, and 





THE SENSORY ORGANS—THE EYES. 299 


communicates with the exterior through an aperture. The sensory 
epithelium is consequently directly bathed by the sea water, and its 
ectodermal character thus becomes very evident. Eyes thus simply 
constituted have already been met with in a few primitive Gastropoda 
(Fig. 90, p. 198). 

In the Dibranchiate Cephalopoda, the eye reaches « higher grade 
of development. The first advance is the closing of the primitive 
optic vesicle and its abstriction from the ectoderm. Mesoderm-cells 
then press in between the latter and the outer wall of the vesicle, a 
process the commencement of which is indicated even in Fig. 142 3. 
After the abstriction of the optic vesicle, this stage may be compared 
to the permanent condition of the eye in the majority of the 
Gustropoda (Fig. 145 2). 





ve 


Fie. 143.—Tyansverse section through the head of an advanced embryo of Lotige (after 
Bonnerzxy, from Bauroun's Text-book). ae, otocyst ; adk, optic cartilage ; ak and 





y, lateral cartilage and white body ; cc, iris; /f, funnel-fold ; go, cerebral ganglion ; 
gm, membrana limitans; gfe, duct of the salivary gland ; (7.op), optic ganglion; (g.1) . 

ganglion ; rt, retina; ec, vena cava; vd, stomodaenm ; of, ciliary region 
of the eye; a, thickened ectoderm in the floor of the funnel. 





A secdnd circular ectodermal fold now rises above the optic vesicle, 
enclosing a depression which strongly resembles the primitive optic 
pit (Fig, 145.2). Almost simultaneously, the (cuticular) secretion of 
a conical structure (Fig. 143) commences on the inner surface of the 
external wall of the vesicle; this is the first indication of the /ens. 
‘This rudiment increases in size through the deposit of concentric 
layers (Fig, 144 4), 


300 CEPHALOPODA, 


The lens of the Cephalopodan eye is not yielded by the outer wall 
of the primitive optic vesicle alone, since the floor of the second 
invagination above the vesicle also takes part in its formation (Fig. 
143). From this latter is formed an anterior and ‘smaller section of 
The cell-layers formerly lying above 
the first-formed lens are in 
this way gradually used up 
(Figs. 143 and 144). 

The primitive —_ optic 
vesicle and the invagination 
lying above it also yield the 
ciliary body, the wall of the 
former, which is directed 
outward, and the floor of 
the latter uniting for its 
formation (Fig. 144 4 and 
B). The mesoderm present 
between these two ecto- 
dermal cell-layers no doubt 
gives rise tothe musculature 
‘of the ciliary body. The 
anterior or outer part of 
the invagination (or rather 
fold) becomes the iris (Figs. 
144 and 145), Mesoderm- 
elements find their way in 
large numbers into this 


the lens (Fig. 144 4 and 2). 








*\ ec Ke 

Fig. 144,—Sections through the eye of oligo 
in two stages of development (after BOBRETZRY, 
from Batvour’s Text-book). a and a’, the 
epithelium lining the anterior optic chamber ; 
af, and i, iris fold ; aq, equatorial pactllage 
cc, stall ectoderm-cells of the ciliary body ; 
gz, large cells of the ciliary body (nm); ht, 
inner part of the lens; ms, mesoderm-tissne of 
the ciliary body ; r¢, inner, r?!’, outer layer of 
the retina; sf, rods; ef, anterior part of the 
leus; , epithelium of funnel, 






anterior fold also. 

Another circular fold now 
grows over the eye at this 
stage of its development 
and gives rise to the cornea 
(Fig. 145 @). This fold, in 
many Cephalopoda  (¢.g., 
Oigopsida) does not close, 


the cornea retaining its 
aperture which is often somewhat wide and through whieh the 
sea water can enter the external optic chamber, while in others 
(eg., the Myopsida among the Decapoda and the Octopoda), the 
cornea either retains only a minute aperture or else completely closes, 
thus precluding any communication between the optic chamber and 


THE NERVOUS SYSTEM. 301 


the sea water. Another fold round the eye gives rise to the eye- 
lid found in some Cephalopoda (especially in the Octopoda, Fig. 145 
C, Int *). 





Nop 
Fre, 145,—Diagrams rey mting the eyes of Vewtilus (A), a Gastropod (4), and one 
7afte pook). Cb 


of the Oigopsida (0) (after Grenacner from Batrour's Text-h ) commen 5 
Ch.ep, epithelium of the ciliary body ; G.op, optic ganglion; [nt-Jul4, integument 
(ectoderm) ; Fr, iris ; J, lens; 7', outer section of the lens; Nop, optic nerve; N.S, 
nerve-layer of the retina ; Pal, eyelid ; RK, retina ; ©, outer layer of the retina. 





The course of development of the Cephalopod eye described above 
shows that it attains a high degree of perfection, as may indeed be 
seen from an examination of the adult eye. 


D, The Nervous System. 


All investigators of the origin of the nervous system in the Cephalo- 
poda were formerly unanimous in tracing it back to the mesoderm 
(Ray Lanxesrer, Ussow, Boprerzky). More recently, the forma- 
tion of the nervous system has been studied by ViALLETON, who found 
that the ganglia arise through the thickening of the external layer ; 
these thickenings, however, yield at the same time mesodermal tissue. 
Other similar thickenings of the ectoderm are principally formative 
centres for the mesoderm.* This view also, therefore, does not 
establish any sharp distinction between the central nervous system 
in the process of formation and the mesoderm. At the same 
time, we have to emphasise the fact that in the Cephalopoda as in 
other Molluscs, the nervous system is of purely ectodermal ovigin 
(Korscurit, No, 25). 


# See further, p. 907. 


302 CEPHALOPODA. 


‘The cerebral ganglion arises in the form of an ectodermal thicken- 
ing above the rudiment of the stomodaeum. Before the latter sinks 
in, the ectoderm above this region becomes multilaminar (Fig. 131 





Fic, 146,—Sagittal sections through embryos of Lolign of various ages, somewhat 
diagrammatic (0 is thle in the region of the mouth. a, anal 
region; a7, arn-ruliment; ¢ cerebral commnisire; of, cerebral ganglion ; 
de, yolk-epithelinm ; ert, ectoderm ; m, mouth ; ud, mantle-fold ; md, 


mesoderm (diagrammatic) ; 7, radular sac; a7, shell-gland ; sp. salivary gland; 
ink-sac ; ev, stomodaeum, 









D, ect., p. 280). ‘This ectodermal layer, which at first is thin, 
thickens greatly after the stomodacum has become.invaginated (Fig. 
146 A, cg), and a large ganglionic mass forms at this point, consisting 


THE NERVOUS SYSTEM. 303 


of two parts connected together by a commissure which at first is 
broad but .narrows later; these are the two halves of the cerebral 
yanglion, which become detached from the superficial ectodermal 
layer and, in sagittal section (Fig. 146 8, cg), appear as spindle- 
shaped bodies. The ectoderm, at the formative centre of the 
cerebral ganglia (above the mouth) is now again a thin layer (Fig. 
146 Band C). In the median section (C’), the cerebral commissure 
(c) can here be recognised. 

The paired rudiment of the cerebral ganglion was early observed 
(by the above-named zoologists as well as by GRENACHER). The 
two ganglia greatly increase in size and finally fuse together. In 
consequence of processes of growth, the relative position of the 
cerebral ganglion and the mouth is modified in a striking manner 
(Fig. 133, p. 283). 

The optic ganglia also form as massive thickenings of the ectoderm 
in the cephalic region. They are directly connected with the ecto- 
dermal thickenings which become the cerebral ganglia and soon press 
in below the optic vesicles, a process which evidently gave rise to the 
statement that the optic ganglion arises on the posterior side of the 
optic vesicle, from the mesodermal cell-elements there present. The 
optic ganglion soon shows a close connection with the optic vesicle, 
a connection which leads to the formation of the optic nerve. 

The pedal and the pleuro-visceral ganglia, like the other ganglia, 
are said to originate through differentiation of the cell-masses lying 
between the ectoderm and the alimentary canal. In reality they are 
due to ectodermal thickenings in the ventral part of the embryo. 
The pleuro-visceral and pedal ganglia, like the cerebral ganglion, are 
each composed of two parts of distinct origin. The two cell-mnasses 
which yield the pleuro-visceral ganglion lie behind the otocyst, aud 
the masses that produce the pedal ganglion in front of that vesicle 
(Bosretzky, Ussow, Fig. 133, p. 283). 

During the course of development, the three ganglia just mentioned 
gradually shift nearer one another and, as the yolk-sac disappears, 
move towards the stomodacum, where they finally fuse, the pleuro- 
visceral and pedal ganglia uniting to form the sub-oesophageal mass 
which is connected with the cerebral ganglion by two short com- 
missures, a broad posterior and a narrow anterior commissure. 

The anterior section of the sub-oesophageal mass, which is, to a 
certain extent, marked off from the rest, and into which the narrow 
commissure enters, is distinguished as the brachial ganglion. This 
part becomes differentiated from the pedal ganglion at a time when 


304 CEPHALOPODA. 


the latter has not yet fused with the visceral ganglion (PELSENEER). 
According to the above author, who is confirmed by Bopretzky, 
the buccal ganglia originate in the same way, becoming abstricted 
from the cerebral ganglia and shifting forward, but Ussow states that 
they have a separate origin like the principal ganglia, and unite with 
these only at a later period. A similar origin is claimed by Ussow 
for the splanchnic and the stellate ganglia. 

The ganglia can easily be recognised by the fact that, soon after 
their appearance, a differentiation into an outer cellular layer and 
a central fibrous mass takes place. 

The connection of the ganglia with the sensory organs and the 
peripheral parts of the body takes place only at a somewhat later 
stage. Ussow assumes that the cells of the layer which produced the 
ganglia lengthen and thus yield the nerve-fibres, as described above 
(p. 193) for the Gastropoda. 


The above interpretation of the nervous system is not accepted by all 
anatomists. The anterior part of the sub-oesophageal mass, the brachial 
ganglion, has been regarded as e part of the cerebral ganglion, which in con- 
sequence of the great lateral extension of its anterior section, finally stretched 
below the oesophagus, fused here in the middle line, the anterior part being 
constricted off and remaining connected only by a commissure with the 
cerebral ganglion (v. JHERING, Gropeen, No. 16). 

The brachial ganglion supplies the arms with nerves; some of these nerves, 
however, are said not to arise from the brachial ganglion but to pass into 
the cerebral ganglion through the anterior commissure (DieTL, No. 10). This 
connection and the conditions found in Nautilus have led to the view that 
the brachial ganglion belongs to the brain. In Nautilus, the majority of 
the tentacle-nerves spring from the part of the middle oesophageal ring which 
might be indicated as the pedal ganglion, but some originate above the roots 
of the optic nerves, and are thus thought to be cerebral in origin. According 
to this interpretation, the part of the oesophageal mass known as the pedal 
ganglion would then also have to be reckoned as belonging to the cerebral 
ganglion, since we cannot claim some of the tentacle-nerves as cerebral 
nerves and the others as pedal nerves. 

This question is of importance in connection with the interpretation of the 
arms which, if innervated from the brain, would have to be regarded as 
cephalic appendages, while, if they derived their nerves from the pedal 
ganglion, they would have to be considered as parts of the foot. Some of the 
facts of ontogeny and comparative anatomy have recently been shown to be 
opposed to the first of these views and to favour the second. According to 
Perseneer, as already mentioned, the brachial ganglion at first forms by 
abstriction from the pedal ganglion, and is thus not in any way closely 
connected (as assumed) with the cerebral ganglion. 

Before the brachial ganglion separated from the pedal ganglion, a nerve- 
strand ran from the anterior part of the (primitive) pedal ganglion to the 


THE GILLS. 306 


arms, a similar strand running from the posterior part of the ganglion to the 
funnel, The latter, the pedal nature of which can hardly be doubted, thus 
{according to PxiseNuEn), at this early stage, receives its nerve-elements front 
the same ganglion as the arms. 

Another argument in favour of the pedal nature of the arms is found in the 
statement of Jarta (No. 18) that the brachial nerves have their roots in the 
pedal gunglion and that they do not pass into the cerebral ganglion as has 
been stated, Prrsexern further rightly points out that the arms in their 
origin (and also in the manner of their innervation) are clearly ventral 
organs, and those that assume a dorsal position only reach it in a late stage 
of development (p. 263). Only as the arms are displaced anteriorly, and to 
some extent dorsally, does the part of the central nervous system innervating 
them and originally belonging to the pedal ganglion shift in » dorsal direc- 
tion (PeLsenzen, No. 38). J. Srerwer's physiological researches,” according 
to which the destruction of the pedal ganglion led to paralysis of the arms 
and thus proved them to belong to the foot-region, are also significant in this 
connection. 

We thus have strong reason for regarding the arms, not* as cephalic ap- 
pendages, but rather as greatly modified parts of the foot (of. Chap. XXXIV.).t 


B. The Cartilaginons Skeleton. 


The various parts of the cartilaginous skeleton are regarded by some 
authors (Merscuniorr, Ussow) as ectodermal structures which have gradu- 
ally shifted inward. Bosrerzky's figures of the optic cartilage seem to 
confirm this method of origin which at first sight is surprising. Around each 
eye (Fig. 143 ad, adk), the ectoderm is seen to become greatly thickened; these 
thickenings, in consequence of the development of the folds described above, 
come to lie deeper, Even if these figures appear convincing, we must not 
exclude the conjecture that some part of the superficial cell-layers may 
have already become differentiated, und in this case might be reckoned as 
mesoderm. 


P. The Gills. 


The gills were found to arise as papilla-like prominences in front 
of the mantle near the anal region (Fig, 85 C and D, &, p. 189), to 
be gradually grown over by the latter (Figs. 87 and 88 &, p. 194), 


* Sitz.-Ber. Akad. Berlin, 1890, 
iad recently Kenn (No. 11.) has opposed the pedal nature of the arms of 
2 and reverted to the older view of Grousen that they are cephalic. 
While ad ing several weighty arguments against some of the evidence 
which has been put forward regarding their pedal nature, he practically gives 
‘no striking reasons in favour of their cephalic nature and we think that at 
epee at any rate, we cannot unhesitatingly accept his conclusions, 
question seems to rest on the justification of the attempts to homologise 
the anterior sub-oesophageal ganglionic mass of the Cephalopoda with one of 
the highly differentiated ganglia of the Prosobranchia,.—Ep.] 
x 


306 CEPHALOPODA. 


and thus eventually to lie within the mantle-cavity. They had 
previously become flattened, and their surfaces folded in such a 
way as to produce the bipectinate gills characteristic of so many 
‘Molluscs (pp. 72 und 208). | 

The development of the gills in Seva was very carefully studied 
by Jounin (No. 20). Further foldings of the leaflets take place, 
and as these processes ure repeated in the secondary leaflets, a some- 
what complicated gill is produced consisting of three systems of folds 
one above the other ; this is peculiar to the Cephalopoda. 

According to Jounrn, the mesoderm is the chief factor in the 
development of the gills which, by its own increase, determines the 
growth of these organs and the modifications in their shape. The 
gill-rudiment, when still papilla-like, was composed of the superficial 
ectoderm-layer and a massive mesoderm (Fig. 134, &, p. 284). The 
young gill, also, when only slightly differentiated, consists largely 
of mesodermal tissue, in which, at a later stage, the cavities of the 
blood-vessels form in the usual way, through the moving apart of 
the cells. Only the larger vessels develop walls of their own. The 
afferent (venous) and efferent (arterial) vessels, lying in the axis of 
the gill (the middle lamella) become connected with the principal 
blood-vessels of the body, and the afferent vessel of each gill is 
said at its base to give rise to au auricle, In other Molluscs we saw 
the auricles form from the coelomic sacs, like the ventricles ; we must 
therefore accept these statements with caution. 


G, The Mesodermal Structures. 


The rise of the mesoderm, and of the organs derived from it, is 
still very imperfectly known in the Cephalopoda, and can therefore 
only be briefly noticed, We shall have to follow chiefly the older 
researches of Bosrerzky and Ussow, and shall have repeatedly to 
refer to the conditions found in the adult animals. 

We have already described the first rudiment of the mesoderm 
as being contained in the peripheral thickening of the germ-dise 
(Figs. 112-114, p. 247, ete., and Fig. 131, p. 280), and as lying, after 
the differentiation of the entoderm, between it and the ectoderm, 
Thus at first it forms a circular thickened layer, which then extends 
both towards the centre of the germ-dise and towards its edge, In 
this way it attains a size which, as compared with that of the 
other layers (ectoderm and entoderm), is very considerable (Figs. 131 
and 132). 


THE MESODERMAL STRUCTURES. 307 


According to the view of ViacceTox, which has already been mentioned, 
a delamination of the mesodermal part from the outer layer takes place even 
at the time when, according te the account here given, the germ-layers have 
long been differentiated. At a much later stage also, when the rudiments 
of the organs have appeared and have to some extent developed, the ecto- 
derm continues to yield mesodermal cell-material. ViauceTon compares this 
process with the development of mesoderm in the Annelida as described by 
Keersessens (Vol, i., p. 286), and refuses to acknowledge this mesoderm as 
the equivalent of a distinct germ-layer. Such a yiew can best be understood 
in connection with the Cephalopoda in which the formation of the germ- 
layers is evidently greatly influenced by the large amount of yolk in the 
egg, the distinction between the layers appearing almost obliterated, but in 
this onse, as in that of the alimentary canal and the nervous system, we 
must postpone a decision until further light is thrown upon the matter. 


Tn the Cephalopoda, especially in Vautilua and the Decapoda, the 
secondary body-cavity (the coelom) is very well developed and sur- 
rounds the heart with its afferent and efferent vessels, the branchial 
hearts, the pericardial glands, the genital organs and the stomach, 
4nd is connected with the cavities of the nephridia (Groppen, No. 
15). The last two organs lie in the posterior section of the body- 
cavity which is incompletely separated from an anterior section by 
a septum, 


In the Octopoda the body-cavity is much reduced, being represented 
merely by a system of narrow canals formerly claimed as a water-vascular 
‘system. In consequence of its slight development, the coslom no longer 
surrounds the heart, the branchial hearts and the stomach (Gropary), 

As the condition of the coelom in the Cephalopoda is so primitive, we 
are led to expect the coelomic sacs to appear distinctly in their ontogeny. 
But the conditions of the formation of the mesoderm above described seem 
im this respect to be unfavourable. A splitting of the mesoderm into a 
somatic and a splanchnic layer has indeed been asserted by Ussow, but 
is not noticed by other observers and, in any case, does not lead to the 
formation of coelomic and pericardial sacs such as were met with in the 
Gastropoda or such as we might expect in connection with the well-developed 
eoclom of the adult Cephalopod. We may observe in passing that there 
‘are reasons for believing that structures of this sort may yet be found in 
the 

The kidneys, in the Cephalopoda, show the same primitive condition as in 
other Molluscs. In the Octopoda, they are represented by two sacs lying 
symmetrically; in the Decapoda these have united to form a single sac. 
The renal sacs open out through ureters on either side of the anus. 

A comparison of the Cephalopodan kidney with the nephridia of the 
segmented animals seems specially suitable on account of two pairs of rena! 
sacs being found in Nawtilus, each pair opening out through a distinct 
aperture. One of these pairs, however, is without an aperture into the 
coelom, and its significance as a true nephridium is therefore doubtful; we 





308 CEPHALOPODA. 


must rather imagine it to be a new structure formed from the posterior pair 
(which alone is originally present), This process may have been connected 
with the development of four gills, which some believe fo be a secondary con- 
dition and which has led to the assumption that the Tetrabranchia (Nartilts) 
were derived from Dibranchia (v. Jaenixc, No. 19), Although Nautilus is, 
without doubt, a very ancient and primitive form, there are certain signs (¢.9., 
the degeneration of the efferent genital duct) that it was already specinlised 
ima definite direction, and thus might have acquired a second pair of gills. 
The same argument would apply in the case of the kidney. This view would 
find some support from the fact that, in other Mollusca, only one pair of 
nephridia and, with the exception of Chiton, only one pair of gills are present, 

‘The certain information we possess as to the development of the kidneys 
is as yet too scanty to enable us to settle this question. It was shown by 
Bosretzky that, in Loligo, the kidneys arise directly under the covering of 
the postero-dorsal surface as two distinct sacs in the mesoderm, and only 
later unite, and assume the close relation to the veins which they show in 
the adult. The inner wall of the kidneys is much folded, and thus yields the 
aciniform structures known as venous appendages (GRonaEN). 

Our knowledge of the development of the genital organs also is still very 
incomplete. The genital glands arise as thickenings of the pericardial 
epithelium near the heart (Bonretzky, Scuukewrrsca). This primitive 
relation to the pericardium or coelom is preserved by them throughout life, 
but at a later period a (genital) capsule is formed round the glands by a 
peritoneal fold ; the cavity of this capsule, however, remains permanently in 
connection with the body-cavity, and thus forms a part of the latter (Brock, 
Grospen). 

The efferent ducts, of which there is one pair, are connected with the 
eapsule. When, asin most Dibranchia, there is only one efferent duct, this 
must be considered as due to degeneration, as is proved by the presence of 
paired ducts in the Octopoda, in Ommastrephes (x Decapod) and in Nautilus, 
this latter form having one functional and one reduced oviduct. 

This relation of the efferent genital ducts suggests that they are modified 
uephridia (see Vol, iii, p. 42 footnote), and the question thus again arises 
whether the Cephalopoda possessed two pairs of nephridia and in this respect 
& segmentation (which, however, would be incomplete). Such a view is by 
no means justified by what is known of those Molluses which on the whole 
show conditions more primitive than those of the Cephalopoda. These 
Molluscs afford no convincing evidence of segmentation. We must therefore 
regard efferent ducts as having formed independently of the nephridia, or else 
as derived by fission from nephridia, but cannot consider them ns independent 
nephridia. 

The blood-vascular system. Even in the case of this system of organs, so 
well developed in the Cephalopoda, very little is known ontogenotically,* and 


*Bosrerzxy appears to have studied the development of the 
apparatus in detail, but as his work is in Russian, we are limited to the 
descriptions of the figures and a short abstract in Anat. Hofmann 
and Schwalbe, Bd. vii., 1878, and this applies also to our former references to 
his observations, . 


kL =— 


THE MESODERMAL STRUCTURES. 309 


we must content ourselves with a brief summary of the accounts given of its 
origin. 

According to Bosrerzky, the arterial heart is derived from two sac-like 
ergans which first appear as cavities in the massive mesoderm near the 
radiment of the intestine and the yolk-snc. Round these, the cells become 
regularly arranged, and the two sacs or vesicles thus produced then unite to 
form the heart, The formation of the auricles has already been mentioned 
(p. 806). 

‘The arteries arise as canals in the mesoderm, their limits being marked by 
the regularity of arrangement in the cells; at a very early period blood is 
driven through them, in consequence of the commencing pulsations of the 
heart. After the two sacs have united to form the heart, the two pericardial 
sacs are said to extend towards the latter, so as to enclose the heart in the 
same way as in other Molluscs (Scammewrrscn). The branchial hearts abut 
on that part of the body-cavity which encloses the heart, and are also covered 
by the peritoneum. The pericardial glands (the so-called branchial appen- 
dage) develop from the latter as growths of the epithelium; these glands are 
connected with the branchial hearts and are held to be excretory organs. 
The branchial hearts are said to be differentiated from the mesoderm at the 
broad bases of the gills, and the whole venous system, the venae cavae (chiefly 
the anterior vena cava) being specially noticeable in the embryo, arises as 
Incunar spaces in the mesoderm, some of these spaces changing into actual 
veins and others into irregular blood-sinuses (BosreTaxy). 

Scarm«kewrrsce attributes the origin of the blood-corpusecle to the increase 
in number and migration of cells of the yolk-epithelium in the posterior part 
of the body, and thus assumes for them an origin similar to that of the blood- 
cells in the Arachnida, the latter being formed from migrating yolk-cells 
(Vol. iii., p.88). We refrain for the present from expressing an opinion on 
these somewhat improbable statements. 


Chromatophores, subcutaneous tissue, musculature. ‘The layers of 
the mesoderm lying beneath the ectoderm become transformed into 
the so-called fibrous layer, while the deeper layers yield the con- 
nective tissue and musele-fibres of the cutis and also, iu any case, the 
muscles of the external organs. The chromatophores, also, are said 
by nearly all authors to originate here, but a somewhat different view 
of their origin has recently been propounded. 

The time of the appearance of the chromatophores in the different 
forms varies greatly (¢/. Figs. 120 and 121, p. 263). In Loligo, for 
instance, they uppear very late, but in the Cephalopod described by 
GW®ENACHER at an early stage, before the circumcrescence of the 
yolk by the blastoderm is completed and before the organs have 
appewred (Fig. 125, p. 268). In the last case, a very early differen- 
tiation of these mesoderm-layers seems to have taken place. 

The chromatophores are said to be derived from mesoderm-vells 

. Which are distinguished from the surrounding cells by their large 


ee 


310 CEPHALOPODA, 


size and by the early deposit of pigment in their protoplasm (Gmop, 
No. 13). Ata later stage, they are covered by a thick envelope; 
the cells in the neighbourhood stretch out into spindles and become 
connected with the chromatophoral cells. In this way arises the 
well-known appearance of the (contractile) fibre-bundles connected 
radially with the chromatophoral cells, The change of shape in the 
pigment-cells which is accompanied by change of colour was usually 
attributed to the contractility of these bundles, é¢., they have been 
regarded as muscle-fibres, while some authors have aseribed a capacity 
for contraction to the pigment-cells themselves, the radial fibres being 
considered as merely connective tissue which, it was assumed, held 
the actual chromatophores in position (Grrop). 

Another account of the origin of the chromatophores has recently 
been given (Joupin, No. 23). According to this view, the ectoderm- 
cells, which are especially distinguished by their size, sk inwards 
through a funnel-like depression. In the large cell at the base of 
the depression, the protoplasm becomes differentiated and, later, pig- 
ment appears, ‘The cell then loses its connection with the ectoderm, 
A number of mesoderm-cells which could be scen even earlier regularly 
arranged below it, and which soon multiply still further, yield the 
radial fibres. The chromatophores would thus be due to the com- 
bined action of the outer and the middle germ-layers (Joust), 


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45. 


46. 


47. 


48. 


49. 


LITERATURE. 313 


. PELSENEER, P. Sur la valeur morphologique des bras et la 


composition du systtme nerveux central des Céphalopodes. 
Arch, de Biologie. Tom. viii. 1888. 


. Pevsenger, P. Sur la nature pédieuse des bras des Céphalo- 


podes. Ann. Suc. Roy. Malacolog. de Belgique. ‘Yom. xxiv. 
1289. 


. Rrerstany, E. Die Sepienschale und ihre Beziehungen zu den 


Belemniten. Palaeontographica. Bd. xxxii. 1886. 


. ScuimkEwrtTscH, W. Note sur le développement des Céphalo- 


podes. Zool. Anz. Bd. ix. 1886. 


. Stzenstrup, J. De Ommatostrephagtige Blackspruthers ind- 


byrdes Forhold. Om Ommatostrephernes Aeglaegning og 
Udvikling. Oversigt over ud. k. Danske Vidensk. Selsk. 
Forhawil. 1880. 

Sreenstrup, J. Zur Orientirung iiber die embryonale Ent- 
wicklung verschiedener Cephalopoden-Typen. Biol. Centrathl. 
Bd. ii, 1884-5. 

Sremmann, G., u. Dopervein, L. Elemente der Palaonto- 
logie. Leipzig, 1890. 

Ussow, M. Zoologisch-embryologische Untersuchungen. Die 
Kopffiissler. Arch. 7. Natury. Jahrb. xl. 1874. 

Ussow, M. On the Development of the Cephalopoda. (Russian, 
with abstract in German by Stieda.) Jzryext. imp. Obxhch. 
lyubit. extesty, Antrop. i Ethnog. Moxcow, 1879. 

Ussow, M. Untersuchungen iiber die Entwicklung der Cephalo- 
poden. Arch. de Biol. Tom. ii. 1881. 

ViatteTon, L. Sur la fécondation chez les (éphalopodes. 
Comptes rent. Acai. Sei. Paris. Tom, ci. 1885, 

ViaLLeton, Iu, Recherches sur les premiéres phases du dé- 
veloppement de Ia Seiche (Sepia officinalis). daw. ai, nat. 
(7). Zool. Tom. vi. 188%. 

Watase, S. Observations on the development of Cephalopods : 
Homology of the germ-layers. Stu. Biol, Lah. Johns Hopkinx 
Univ. Baltimore. Vol. vi. 1888. 





50. Wartase, S. Studies on Cephalopods. 1. Cleavage of the Ovum. 


Journ. Morphol, Vol. iv. 1891. 


. ZErnorr, D. Ueber dasx (eruchsorgan der Cephalopoden. 


Bull. de la Soc. imp. d. Naturatlister de Moxcou. Tom. xii. 
1869. 


. Zrrrer, K. Handbuch der Paliiontologie. Bl. i. Cephalopoda. 


Munchen unt Leipzig, 1884. 


314 CEPHALOPODA. 


APPENDIX TO LITERATURE ON CEPHALOPODA. 


I, Fausser, V. Zur Cephalopodentwicklung. Zool. Anz. Jahrg. 
xix. 1896. i! : 
II. Kerr, J. Granam. On some points in the Anatomy of Nautilus 
pompilius. Proc. Zool. Soc. London. 1895. 
III. Korscnevt, E. Ueber den Laich und die Embryonen von 
Eledone. Sifzungsber. Gra. Naturf. Berlin. 1893 (1894). 
IV. Wrutey, A. The Oviposition of Nautilus macromphalus. Proc. 
Roy. Soc. London. Vol. ix. 1897. 


CHAPTER XXXIV. 
General Considerations on the Mollusca.” 


Tn attempting to combine into one yeneral scheme the de- 
velopmental phenomena described in the preceding chapters, in 
connection with the different divisions of the Mollusca, we cannot, of 
course, take into account all the very different ontogenetic processes, 
but can only select from among them those that are of the more 
general significance. 

Even in the cleavage of the egg, great variety prevails, Thus we 
find, on the one hand, that the meroblastic type of cleavage attains 
its highest development among the Mollusca (Cepbalopoda) but, on 
the other, that total and, at first equal, but soon after unequal 
cleavage is still more common in eggs of this phylum (Chifon, 
Gastropoda), and so also is a type of cleavage which from the first is 
wnequal (Solenogastres, Lamellibranchia, Solenoconehae), The cause 
of this difference is to be songht in the varying amount of yolk 
contained within the eggs but, even among eggs showing total 
cleavage, there are some that, through a secondary separation of the 
yolk-mass from the blastomeres, lead us to the meroblastic method 
of cleavage (Vassa). The latter is to be explained as due to the 
extraordinarily large amount of yolk in the egg, and this same 
peculiarity further determines so great a modification of the early 
ontogenetic phenomena in the Cephalopoda, that this division must 
be left almost entirely out of account in our comparative review. 
Within each separate division of the Mollusca, the phenomena of 
cleavage are very similar and very regular. 

‘The formation of the primary germ-layers takes place through the 
invagination of a blastulu with a more or less wide cleavage-cavity, 
or, where the latter is wanting, and the egg is richer in yolk, through 
epibole. These two processes are found in nearly related forms, or 


* See note, p. 1. 


316 GENERAL CONSIDERATIONS ON THE MOLLUSCA. 


else an invagination-gastrula appears as a stage following the epibolic 
gastrula, as, for instance, in Osfrea and various Gastropods, in which 
a cleavage-cavity arises only at a later stage, and the macromeres 
which are continuing to multiply press in towards it. There is also 
no essential difference between these two types of formation of the 
germ-layers. In the Cephalopoda also the germ-layers may be traced 
back to the same processes, although these are influenced in a marked 
manner by the large amount of yolk in the egg. 

The middle germ-layer arises in a very similar way in all those 
forms in which it has been investigated. It originates in two 
primitive mesoderm-cells derived from one of the macromeres (primary 
entoderm). In the Gastropoda, in which this point has been best 
examined, the formation of the primitive mesoderm-cells from the 
macromeres was found to be very regular.* The large primary cells 
of the mesoderm have been discovered to exist in all the following 
divisions of the Mollusca: the Amphineura, the Lamellibranchia, the 
Solenoconchac and the Gastropoda. In the Cephalopoda, on the 
contrary, the development of the mesoderm has been considerably 
modified by the conditions mentioned above. 

The two mesoderm-bands arise through the multiplication of the 
primitive mesoderm-cells. [t has repeatedly been stated that 
mesodermal tissue is not due to the multiplication of these cells, but 
is yielded later partly by the ectoderm, as described for the Annelida. 
The first of these views, i.., the derivation of the mesoderm from the 
primary cells is, so far, the more probable, but the other view should 
not be summarily dismissed, and in any case deserves more careful 
investigation.+ 

It is very characteristic of the Mollusca that the mesoderm-bands 
are retained for only a short time. They soon disintegrate, single 
cells separating from them and becoming distributed in the cleavage- 
cavity as the so-called mesenchyme. Before this happens, however, 
or else during this process, a cavity appears in each of the mesoderm- 
bands : this is bounded by a more or less regular epithelial wall and 
is thus recognisable as the coelom. ‘This process is the same already 
met with in the Annclida (Vol. i., p. 290), and Arthropoda (Vol. iii.. 
p. 413). In these latter it leads to the formation of two mesodermal 
layers, one applied to the ectoderm and the other applied to the 
entoderm ; these are the somatic and splanchnic layers. This seems 











* [See footnote, p. 119, Ep.] t [See p. 29, Ep.] 


GENERAL CONSIDERATIONS ON THE MOLLUSCA. 317 


likewise to be the case in the Chitons which in other respects also- 
appear to be very primitive animals (Fig. 4 4 and B, p. 8); they 
do not, however, show any suggestion of the segmentation of the 
mesoderm (formation of the primitive segments) so characteristic of 
the segmented animals, 

The Amphineura, even as adults, show the secondary body-cavity 
well preserved. It is still very large, and contains the principal 
organs, such as the alimentary canal, the liver and the heart. In the 
higher Mollusca (Lamellibranchia and Gastropoda) it is much more: 
veduced im comparison with the primary bedy-cavity and is even 
quite small. The primary body-cavity with the mesenchymatous 
tissue distributed in it is very large and becomes the definitive body- 
cavity, just as in the Arthropoda (Vol. iii., p. 423). In spite of this, 
the Molluses have been regarded as typical Schizocoelata, Ae, as forms 
devoid of a true coelom. Such a true coelom, however, is retained 
by them, though only slightly developed. 

While in the Arthropoda, the coelomic sacs (primitive segments) 
nsnally completely disintegrate or at the most persist to a small 
extent in the genital glands (Peripatus, Myriopoda) the coelom of the 
Mollusca is always retained in the form of the pericar/ium from which 
the wephridia and the genital glands are formed (Gastropoda) in a 
manner recalling the primitive conditions in the Annelida, Where 
the connection between the kidneys, the genital organs and the- 
pericardium has not yet been made evident in the embryo in conse- 
qnence of insufficient investigation, or else where, in consequence of 
secondary modifications in the forms examined, it can no longer be 
demonstrated, the anatomical condition of the systems of organs 
clearly proves such a connection. In various Molluses, the cavity of 
the genital glands is directly connected with the pericardial cavity 
(Amphineura, Cephalopoda), the nephridia entering the latter through 
an open funnel, a condition which recalls the open connection existing 
between the nephridia of the Annelida and the secondary body- 
cavity (Amphineura, Lamellibranchia, Gastropoda, Cephalopoda). 
There can consequently no longer be any doubt that the pericardium of 
the Mollusea should tw regarded as the secondary body-eavity ; and, 
apart from the absence of segmentation, the resemblance in this point 
to the Annelida is very great. 

The condition of the mesoderm and the structures belonging to 
it is thus evidently of great importance in interpreting the Mollusea 5 
it has therefore been considered in connection with the early onto- 
genetic processes. Hardly less important, however, is the larval 


ie 


. 
318 GENERAL CONSIDERATIONS ON THE MODLUSCA. 


_form which also in several ways throws light upon the relationships 
‘of the Molluses. 

Although the larvae of the different divisions, e.y., those of the 
Amphineura, the Solenoconchae, the Lamellibranchia, and perhaps 
also those of the Heteropoda and the Opisthobranchia appear with 
very different forms, all of them may without any difficulty be traced 
back to the Trochophore, the typical form of which was met with 
in the Annelida. In some cases, such, for instance, as the larvae of 
Dondersia and Dentalium (Figs. 10, pp. 17 and 138, p. 291) as well as 
in those of a few Gastropoda (perhaps of the Gymnosomatons Ptero- 
poda, Fig. 77, p. 172) this is less evident, while in the larvae of other 
Gastropods such as Patella, Paludina and most Lamellibranchia, the 
resemblance is exceedingly striking (Figs. 51-53, p. 127; 56, p. 135; 
14, p. 28; 18, p. 36), But even in larvae in which the resemblance 
is not so great (Figs. 66 and 67, p. 155; 72, p. 162; 75, p. 168), eom- 
parison with other forms or the examination of the younger stages 
enable us easily to trace back the larval form to the T'rochophore 
(Figs, 64 and 65, pp. 158 and 154; see also p. 166). In the greatly 
modified ontogeny of the Cephalopoda, traces of the larval form have 
hitherto not been established with certainty, 

The development of the Molluscan Trochophore closely resembles 
that of the Annelidan larva, It arises from the gastrula-stage, 
several rows of cells at the anterior region becoming covered with 
strong cilia and thus yielding the pre-oral ciliated ring, the velum 
of the Molluscan larva. The blastopore, which at first lies at the 
posterior end, usually becomes slit-like ; it probably closes from 
behind forward and generally, at its anterior end, passes into the 
mouth through the formation of an ectodermal depression, the 
stomodaeum, A post-ovw/ ciliated ring appearing behind the mouth 
heightens the resemblance to the typical 7'rochophore, the external 
form of the Molluscan larva now also agreeing with that of the 
latter, the anterior end being much widened and the posterior 
narrowed. 

At the posterior end of the body, and thus at the point where the 
Dlastopore at first lay and from which its closure commenced, the 
anus now forms. It thus appears as if it also bore some relation 
to the blastopore ; indeed, an attempt has been made to prove this 
to be the case in some Molluscs (¢.g., the Opisthobranchia), and in 
another Gastropod, Palwline, the direct transformation of the blasto~ 
pore into the anus has been assumed. We thus find in the Mollusca 
conditions altogether similar to those met with in the Annelida and 


Lb al 


GENERAL CONSIDERATIONS ON THE MOLLUSOA. 319 


the Arthropoda, in which also relations were proved to exist between 
the mouth and the anus on the one hand and the blastopore on the 
other, 

The intestine, which like the oesophagus, is usually formed by an 
ectodermal invagination in the Invertebrata, appears to be derived 
entirely from the entoderm in the Mollusca; thus the enteron 
usually fuses direct with the ectoderm, without any depression of 
the latter. This has been regarded as an important peculiarity in 
the organisation of the Mollusca, and much stress has been laid 
upon it, but if, as has been stated, an ectodermal intestine actually 
occurs in a few Molluses (Chiton, Tervdo, ete., pp- 15, 66, 208), the 
usual absence of the proctodaeum cannot be considered as a dis- 
tinctive feature. 

At the opposite end of the larval body, i.¢., at the cephalic pole, 
and in the midst of the velar area, an ectodermal thickening known 
aa the apical pinte is found, occupying the same position as in many 
other pelagic larvae. In the Annelida, the supra-oesophageal ganglion 
is thought to originate from the apical plate, and in the Mollusca 
also the cerebral ganglion is said to arise from it (Chifon, Lamelli- 
branchia) or else to bear some relation to it (Dentalium). In the 
Gastropoda, indeed, the cerebral ganglia originate as two ectodermal 
thickenings of the pre-oral part of the bedy, but these also do not 
differ much in position from the apical plate, so that even here there 
may be some relation to the latter. 

An organ of special importance in comparing the Molluscan 7'rocho- 
phore with other larval forms is the primitive kidney. This arises 
from cells derived from the mesoderm-bands,* in the same way as 
in the Annelida, as a tubular paired structure. Its relations to the 
primary body-cavity also seem to be the same as those met with in 
the Annelida and in the case of the adult excretory organ of the 
Plathelminthes. 

It is evident from the above that the resemblance of the Molluscan 
larva with the Trochophore of other animal phyla, and especially 
with that of the Annelida is exceedingly striking not only in external 
form but in internal structure. Attempts have been made to account 
for this resemblance by the supposition that the larvae of these 
phyla gradually assumed the same organisation as a consequence 
of similarity in their manner of life. We do not share this view, 
and can only explain the remarkable external and internal similarity 


* [See footnote, p. 179. Ep.) 


320 GENERAL CONSIDERATIONS ON THE MOLLUSCA- 


through actual relationship to one another of all those groups which 
have the 7yevhophore as their larval form. 

If we accept this latter view, there can be no doubt as to the 
significance to be attributed to the larval form. Its reappearance in 
the development of phyla so different as the Annelida, the Mollusca, 
and the Molluscoida, points to a racial form haying this structure. 
This brings us to the difficult and much diseussed question of the 
origin of the Mollusca.* 

Of the theories as to the origin of'the Mollusca, two seem to us 
to demand our special attention, these being the theory that the 
Mollusca are derived from Turbellaria-like forms and that which | 
derives them from a 'rochophore-like ancestor. 

The derivation of the Mollusea from Turbellaria-like forms has much 
in its favour, especially as it affords a partial explanation of the 
perplexing conditions of the nervous system. The pedal strands, 
according to this view, would correspond to the ventral longitudinal 
nerves of the Turbellaria, while the plearo-visceral strands correspond 
to the lateral nerves. The resemblance is specially striking in the ner- 
vous system of the Amphineura (forms which somewhat resemble the 
‘Turbellaria in shape) which consists of four longitudinal strands with 
connecting commissures. A similar ladder-like nervous system with 
a ventral and a lateral strand on each side occurs in the Turbellaria 
(Triclada and especially Gunda). The anus, which is wanting in the 
Turbellaria, was acquired later, and so was the blood vaseular system. 
The coelom is to be explained by the dilation of the genital glands, 
for the genital products originate, as was shown, from its epithelial 
wall, The shell, an important component part of the Molluscan 
organisation, arose for the protection of the body in the form of 
a cuticular secretion of the dorsal surface in which were deposited 
calcareous concretions. The foot, an equally essential part of the 
organism, resulted from the transformation of the ventral surface of 
the body, which was used for creeping, into a muscular sole, or else 
is assumed to be a modification of the ventral sucker. 


* A great deal has been written on the relationships of the Mollusca, Pu 
vefrain from discussing the different and often opposite views which have been 
propounded on this subject as they would merely add length to our 
and make it the lessclear. We shall only allude in passing to the 
theory adopted by Ray LankesTer and still more ardently by HatscHek, and 
to Lano’s theory of the derivation from Turbellaria-like forms. ‘list of the 
most important works on the subject will be found at the end of deeien 
Lasa's view has recently been published in his Text-book of Comparative 

Anatomy (Engl. Trans., Vol. ii.). 

+THrexe, like Lac, derives the Mollusca. from Turbellaria-like forms and 

regards the ventral sucker of the Polyclada as the organ from which, without 


Lk __ al 


GENERAL CONSIDERATIONS ON THE MOLLUSOA. 321 


The above may, on the whole, be described as possible, but this 
origin has the disadvantage of starting from very highly differentiated 
animals ; and, a point which appears to us as very important, affords 
no clear explanation of the striking resemblance existing between the 
larvae of the Mollusca and those of the Annelida, This resemblance 
is made possible if we go back farther, to a form from which may be 
derived both the Trochophore and the ancestors of the Turbellaria, 
Since, in such speculations, it is only right to try to start from existing 
forms, the common ancestral form of the Trochophore and the Tur- 
bellaria has been sought among the Ctenophora, but it is impossible 
to construct from them the desired ancestor without unduly forcing 
the comparisons, It is true that the Ctenophora, on account of their 
locomotion by means of cilia, their possession of the apical plate and 
the condition of the entoderm and mesoderm may be brought into 
relation with the Turbellaria and perhaps even with the T'rochophore, 
but it appears to us still more certain that in them we have forms 
already strongly specialised in a definite direction and thus no longer 
suited to serve as the ancestral forms of the Mollusca. Instead then 
of attempting to derive these forms from known and specialised groups, 
it seems to us simpler and at least equally justifiable to fall back 
upon some form with a more primitive organisation. 

In considering the ontogeny of the Annelida, we started from a 
gastrula-like form, ciliated all over, which developed at the cephalic 
pole « ciliated tuft, and in which also the locomotory cilia were 
specially arranged in the form of a ring running round the body (the 
later pre-oral ciliated ring or velum). The primitive mouth (blasto- 
pore), originally lying at the posterior end of the body, becomes dis- 
placed forward owing to the development of a ciliated apparatus in 
this very limited region ; thus the mouth shifts towards the locomotory 
wpparatus which at the same time serves for conducting food to the 
mouth, a8 is still seen to be the case with the ad-oral zone and the 
poat-oral ring of the Trochophore, 1n the primary body-cavity of this 
form, mesodermal elements are already found; among these lie the 
gonads which no doubt are derived from the entoderm as well as from 
the mesoderm [probably from distinct blastomeres which are neither 
mesodermal nor entodermal but are the germ-teloblasts}, and which 


— 


322 GENERAL CONSIDERATIONS ON THE MOLLUSGA. 


ure either still connected with the gastral cavity or already open 
externally through special efferent ducts (nephridia t). A specially 
important organ of this hypothetical form which ulso lies in the 
primary body-cavity is the excretory organ, the origin of which is 
one of the most difficult points to explain. Since we see the ex- 
eretory organs rising from the mesoderm, and are inclined to derive 
this latter from the entoderm, we hold it as most probable that the 
primitive excretory organ was a diverticulum of the entoderm which 
became secondarily connected with the ectoderm. At a later stage, 
it loses its connection with the entoderm and thus becomes the 
structure known as the primitive kidney (protonephridium), | 

From a form possessing such an organisation, the Plathelminthes 
also nay be derived. Their excretory system remiains on the level 
of the protonephridium, merely branching and extending further 
through the body. Their larval form corresponds more or less to 
that described, but does not possess a primitive kidney. The Pilidiwm 
of the Nemertini already shows a certain similarity to the T'roche- 
phore, ond it has been pointed out that transition forms between it 
and the MGLvER's larva of the Turbellaria are to be found (Volei., 
p- 168). The Pilidiwm is distinguished, like the Troehophore, by the 
possession of an apical plate. 

Through the coucentration of the ciliated apparatus and the 
acquisition of an anus, the ancestral form ascended to the level of 
the Trochophore, and then became the starting-point for the 
Rotatoria, the Mollusca, and the Molluscoida, Its relation to the 
Rotatoria and the Annelida, é.c., its ascent to the level of the latter, 
has already been discussed (Vol. i., p. 342). The most important 
features in this process are the appearance of segmentation and the 
rise of the coelom, the latter being perhaps explicable through the 
enlargement of the gonads ‘of the primitive form, As 
mentioned, the genital products originate from the epithelial wall 
of the eoelom, a fact which fayours such an origin, The Mollusea 
exhibit, on the whole, similar conditions, but show an important 
difference in the absence of segmentation, remaining in this respect 
more like the primitive form. 

We therefore assume that the Molluscan larva (Z'rochophore) still 
closely resembles the ancestral form; it already shows, however, 
some new characters which clearly indicate differentiation in a certain 
direction, two of these, the shell and the foot, being specially dis- 
tinctive of the whole organisation of the Mollusca. The first of these, 
especially, can very early be recognised through the appearance of 


i a 


GENERAL CONSIDERATIONS ON THE MOLLUSCA. 323 


the shell-gland on the dorsal surface of the larva, and thus gives the 
larva the special character of the Molluse without at first affecting its 
general appearance (Figs. 14, 15, 18, pp. 28, 31 and 36; Figs. 51 and 
56, pp. 125 and 135), Somewhat later, but also ata very early stage, 
the foot appears on the ventral side of the larva, The very early rise 
of this organ which may in « few cases be found even before the 
Trochophore form fully develops, must be regarded as a shifting back 
to an early period of embryonic development of this feature which was 
only a recent acquisition. It is all the more easy to admit this, as the 
shell-gland is found to arise exceptionally early in those forms, the 
development of which show marked specialisation, as, for instance, in 
the Unionidae (Fig. 22, p. 50) and in the Cephalopoda (Figs. 116 
A, p, 255 and 131 D, p. 280). The shifting back of the shell to the 
earliest poasible embryonic period can easily be explained by its im- 
portance as a protection to the larva, a fact which may be observed 
in every Lamellibranch or Gastropod larva whether young or old ; 
the slightest disturbance causes the animal rapidly to retreat into its 
shell and thus to sink to the bottom of the water. 

‘The larvae of the Amphineura have no true shell-gland, a peculiarity 
that would increase the resemblance between them and the Annelida 
if their organisation were better understood. It must at present be 
confessed that the larvae of the higher Molluses are far more like those 
of the Annelida than are the larvae of these more primitive forms, in 
which we should expect a closer resemblance. The shell-plates of 
Chiton, further, arise in the same region as the typical shell of the 
higher forms (Fig. 5, p. 9). 

‘The manner in which the shell appears in the embryo favours the 
view that it is derived phylogenetically from « cuticular dorsal cover- 
ing, within and beneath which caleareous concretions were deposited. 
‘The shell-plates of Chiton have, indeed, with some probability, been 
traced buck to the transformed spines of this animal (p. 12), but on 
the whole it seems more likely that the Chiton shell, which consists 
of a number of plates, arose in consequence of a secondary distribution 
(determined by the manner of life of the animal) of an originally 
continuons dorsal carapace.* From this flattened, bowl-shaped shell 


* The shell has also been regarded as a partly internal dermal skeleton in 
consequence of its condition in Chifon, where it is traversed by strands of 
connective tissue (Fig. 8, p. 12), and the retractors of the body inserted into 
it have been thought to an important part in its development (Tarete, 
No. 20). This last factor is in any case of importance in connection with the 
‘various modifications of the shell (where the latter is already present), 


324 GENERAL CONSIDERATIONS ON THE MOLLUSOA. 


were derived later all the varied shapes of shell met with ih the 
different divisions of the Mollusca, 

‘The protective dorsal covering which became the shell was, in any 
case, of great significance for the further development of the Mollusca. 
Since, starting from the back, the shell had to cover a large part of 
the body so as to be able to shelter it as completely as possible, the 
locomotory organ could only develop on the ventral surface, the 
ereeping manner of life leading to the development of the foot, an 
equally important organ and one highly characteristic of all the 
Mollusea. 

It has already been mentioned that attempts have been made to 
derive the foot of the Mollusca from the ventral sucker of the 
Polyclada, but it appears to us that the exclusive use of the ventral 
surface ag creeping sole, simultaneously with the development of the 
dorsal shell which necessitated a firmer adhesion to the sub-stratum, 
alone suffices to explain the greater development of the ventral part 
of the body into a muscular foot. Ina few Annelida and Annelidan 
larvae, there is a ventral ciliated area extending between the mouth 
and the anus which evidently assists the animal in creeping. Such 
a differentiation may in any case be ascribed to the primitive form, 
and this, together with a strengthening of the ventral musculature, 
led to the formation of the foot when the primitiye form became 
adapted to a creeping manner of life, an adaptation which, again, 
was connected with the development of a shell. 

In the Solenogastres, which are elongated and evidently very 
lowly Molluscs, the foot is only slightly developed and appears 
as a ciliated ridge lying in the ventral longitudinal groove. This 
gtoove, which is represented in Fig. 147 A and B, might be compared 
with the ciliated area mentioned above as occurring in the Annelida, 
in some forms becoming depressed in such a way as to produce.» 
ventral ciliated groove. In C/uetoderma, there are no signs of either 
a ventral groove or a foot, and we are much tempted to regard these 
elongated worm-like creatures (Fig. 147 4) which are totally devoid of 
shell, as worms rather than as Molluscs, a view which has repeatedly 
been adopted. In any case, it appears possible that they are tramsi- 
tion-forms between the Vermes and the Mollusca, this view being 
supported by the fact that the formation of the spines in the 
Amphineura shows great similarity to that of the setae in the 
Annelida. 

Although there cannot be any doubt that we have, in the Am- 
phineura, forms which stand very low among the Mollusca, we may 


\ 
ete — | 


GENERAL CONSIDERATIONS ON THE MOLLUSOA. 325 


hesitate to attribute to them the significance of transitionary forms. 
We have already pointed out that the spines which cover the body 
of the Amphineura (Figs. 147 B, and 6-8, p. 10) show striking agree- 
ment in their origin with the setae of the Chaetopoda and it was” 
mentioned that some authors had regarded this as proving relation- 
ship between the Amphineura and the Annelida. We do not attach 
wny great importance to this resemblance, since these spines are 
found irregularly distributed over the body, while the setae of the 
Amnelida are, as is well known, very regularly and segmentally 
arranged. Spines also occur in some forms while the related forms 


A 





dies the anterior ends the tos." skerorsadothe sae gta 
from the vewtral side, and showing the oral aperture and, behind it, the apertare of 

Uhe pedal gland and the ventral groove (after KowaLevsxy and Manqon), 
show no such structures. As an example of this we would recall the 
Turbellarian described by v. Grave, Enantia spinifera. Here we 
have true cuticular spines which can only be considered as analogous 
to those of other animals, but in connection with the origin of such 
structures this illustration is of interest. 

Tn comparing the spines of the Amphinevira with the setae of the 
Annelida it must be remembered that we ean certainly not derive 
the Mollusca from such highly developed forms as the Chaetopoda, 
‘The most primitive Annelida, however (the Archi-Annelida), have no 
‘setae, but even these are certainly too much differentiated to serve as 


Ma 


326 GENBRAL CONSIDERATIONS ON THE MOLLUSCA, 


starting points for the Mollusca in which segmentation is altogether 
wanting, 

The temptation is certainly very great to derive the elongate, 
‘worm-like Solenogastres which are provided with a coelom and 
nephridia (Fig, 47 A) from the Annelida, but they also show no 
segmentation. Either segmentation or the distinct remains of it 
must, however, be found if they are really to be more nearly related 
tothe Annelida. We are thus inclined to regard the elongate forns 
of ‘the Solenogastres rather as a secondary phenomenon and to oon- 
sider as such also the growing out of the posterior part of the larva 
into the adult body which recalls similar processes in the Annelida 
(Vol. i., p. 268). It is possible that the development of the Soleno- 
gastres, when better known, will throw further light upon their origin. 
In the young Dundersia, seven calcareous plates are said to cover the 
back, as in Ch/fou. This stage thus resembles that of Chifon and 
this perhaps supports the conjecture that we have in the Amphineura 
a less primitive form than was assumed a priori. The absence of 
the shell also would no longer have to be regarded as a primitive 
feature, nor would the slight development or absence of the foot. 
We still indeed have to take into account the important fact that 
the shell is wanting in these forms. The covering of the body with 
spines and the very primitive internal organisation in any case 
indicate that the Solenogastres are very primitive forms. If we 
actually have, in them, merely an aberrant branch of the Molluscan 
stock, ‘this branch in any case diverged very near the root. © 

If we are unable to find any direct relations between the Solenc- 
gastres and the Annelida, such might perhaps be found between 
them and other divisions of the Vermes, such as the Turbellaria or 
the Nemertini. The coclom, that very important part of the internal 
organisation might, as above shown, with some probability be derived 
from the dilation of the gonads in these forms, The conditions of 
the coelom in the Mollusca agree iu such a striking manner with 
those in the Annelida that it is difficult to believe that two stractures 
so remarkably alike arose in different ways; in this case we should 
have to derive both the Mollusca and the Annelida from Turbellaria 
or some similar form. This brings us, however, buck to our former 
view as to the racial form of the Mollusca made in ion with 
the Trochophore larva (p. $21) which, however, was wt tv to 
the derivation of the latter from the Turbellaria, 

Starting from a creature still more simple in organisation: ‘hss 
Trochophore, we arrived at the form of the latter and traced the 


L _— | 


GENERAL CONSIDERATIONS ON THE MOLLUSCA. 327 


acquisition of those characters which determine the typical Molluse. 
We then touched chiefly upon features of the outer organisation, but 
some points of internal organisation were also pointed out, such as 
the supposed rise of the coelom from the gonads of the primitive form 
and the primary exeretory organ, the primitive kidney. A further 
important characteristic of the Mollusea is the occurrence of the 
(adult) nephridia and their connection with the coelom (pericardium). 

We bolieve the origin of the adult nephridia to be the same as 
in the Annelida, ie., we derive them from the protonephridium. 
Although nothing is known ontogenetically on this subject, the adult 
nephridia, like the primitive kidney, are derived from the middle 
germ-layer, a faet which, indeed, indicates a common origin, if only 
because the mesoderm originally distributed in the body-eavity 
(mesenchyme) and the coelomic mesoderm (the former gonads) had 
im any case the same origin, 4+, were derived from the entoderm. 
‘The connection now existing between the nephridia and the coelom 
is secondary, for it is wanting in the primitive kidney. ‘The nepbridia 
took over the transmission to the exterior of the genital products, 
when special efferent ducts for them were not developed.* 

‘The circulatory system of the Mollusca, like the coelom and the 
nephridia, shows great resemblance to that of the Annelida, a fact 
which inclines us to ascribe it to the primitive form from which the 
two stocks are derived. The simplest form of circulatory system was, 
im any case, that of a contractile sac open at one end and lying 
dorsally. The heart belonged to the primary body-cavity. Where 
the coelomic sacs were specially large it was found squeezed in 
between them and the intestine, dorsally to the latter. The rise of 
the heart between the entoderm and the splanchnic layer of the 
mesoderm, still characteristic of many forms, and which, in the 
Lamellibranchia, even leads to its development round the intestine 
(Figs. 31-33, p. 75), led some authors to trace back the heart to one 
of the blood-sinuses which encircles the intestine.+ According to 
this view, the blood-sinus would have to be located dorsally to the 
intestine. The blood passed into the muscular sac which represented 
the primitive heart and which carried on rhythmical contractions, by 
means of which the blood was again driven out. There were no 
vessels, but the blood ran through spaces und slits in the mesodermal 


“(Seo footnote p. 179 and Goonricn, (Quart. Jour, Micro, Sci. Vol, 
XXXVIL—Ep.} 

+ This view which was adopted by Gronben has been discussed in con- 
nection with the formation of the heart in the Lamellibranchia (p. 79). 


328 GENERAL CONSIDERATIONS ON THE MOLLUSCA. 


tissue of the primary body-cavity, a condition which is still passed 
through by the embryos of the Mollusca, in which the heart arises 
independently of the vessels (pp. 77 and 216). 

The blood-vessels must have first arisen when the gills developed. 
These later, in any case, arose as very simple leaf-like or tubular out- 
growths of the body-wall, such as are found as the most primitive 
gills in the Aunelida, the Arthropoda and the Eehinoderma, Au 
increase of surface soon took place and led to the bipeetinate gill, 
the so-called cfenidium so characteristic of the Mollusca, This gill 
was paired, i.¢., a ctenidium was found on either side of the body 
concealed in a cavity formed by a fold of the integument. The fold 
is the mantle which grew out on each side from the back, and de- 
veloped simultaneously with the shell and the gills. As the primitive 
Molluse we must thus imagine an animal somewhat flattened dorso- 
ventrally, whose back was covered by a bowl-shaped shell while its 
ventral side formed a muscular and slightly projecting creeping sole. 
Beneath the lateral parts of the shell lay the mantle enclosing the 
pallial cavity and within this the gills. On the pre-oral part of the 
body (the head) there were perhaps also the eyes and two tentacles, 
corresponding to the cephali¢ feelers of the Archi-Annelida., In the 
oesophagus, the radular sae with the radula became differentiated as 
outgrowths, these occurring even in the most primitive of known 
Molluses (Amphineura, Solenogastres), The anus lay at the posterior 
end, the nepbridia opening out at either side of it. These latter 
opened inwardly into the coelomic saes with which the genital glands 
were connected. ‘The two coelomic sues, dorsally to the intestine, held 
the heart between them. The primary body-cavity was traversed 
by mesodermal tissue, which became differentiated into connective 
tissue and muscles. 

From such u simple form of Molluse can be derived the types 
represented in the different divisions known to us. Nearest to it 
stand the Chitones, the characteristics of which have been drawn upon 
for the above description. The somewhat aberrant conditions of the 
Amphineura have already been described above (p, 326). After the 
Chitones come the most primitive Gastropods (Diotocardia), the 
Chitones themselves being for a long time regarded as Gastropods, 

‘The foot of the Gastropoda, apart from exceptions to be mentioned 
presently, has the primitive form of the creeping sole. ‘The marked 
development of the head which carries the tentacles and eyes is 
characteristic of most Gastropoda. The shell also has attained higher 
development and is a constant feature of the Gastropoda; where it 


‘ _— | 


GENERAL CONSIDERATIONS ON THE MOLLUSCA. 329 


is wanting, it has evidently degenerated. To the actual shell, the 
operculum has been added. ‘The position of this latter is like that of 
the shell itself, 4., it lies on the dorsal side of the foot at the point 
where the latter passes over into the back. The shifting of the anus 
makes it difficult to establish the origin of the operculum. It has 
been snggested that it arose through abstriction from the shell, but 
its independent development and position in the embryo point rather 
to an independent origin. 

The simple bowl-shaped shell, assumed by us for the primitive 
form is no longer retained in this form in the Gastropoda, for the 
shell has become twisted. This condition is connected with the 
asymmetry of the body which, again, is the result of the one-sided 
development of the visceral sac, a feature which is specially character- 
istic of the Gastropoda. This one-sided development brings about 
displacements of both external and internal organs, and leads to- 
processes of degeneration (¢.g., in the gills, the kidneys, parts of the 
circulatory and nervous systems) ; these now occur on one side of the 
body only and thus still further increase its asymmetry.* In forms 
which lead a pelagic life, such as the Pteropoda, or in creeping forms 
that have lost the shell (Onchidiun, Opisthobranchia, Limacidae, ete.) 
there is a more or less complete return to the symmetrical shape. 

In the form of the gills, the paired character of the kidneys and 
the auricles, the relations of the coelom and of the nephridia, the 
Diotocardia are among the forms most nearly resembling the primitive 
Molluse, but they appear essentially differentiated from it, as the 
asymmetry of the body is already found in them. 

The relation of the Gastropoda to the primitive form is easier to 
trace than is that of the other great branches of the Molluscan stock 
(the Solenoconchae, the Lamellibranchia and the Cephalopoda). 

‘The Solenoconchae may be derived from the primitive form by the 
extension of the body in a dorsal direction ; the head is much reduced 
but develops a large number of tentacular filaments. The foot 
becomes the long burrowing foot, the mantle is found to be influenced 
by the above-mentioned growth of the body, but on the whole 
exhibits the usual features, except that it retains an aperture at its 
dorsal apex. In the same way also we can explain the shape of the 
shell which resembles a tube open at both ends. According to the 
most recent investigations as to the structure of Dentalium it seems 
most probable that this form is related to the Gastropoda, the 


* Cf. on the asymmetry of the body, Chapter XXXIL,p. 148. 


supposed relation to the Lamellibranchia and the Cephalopoda being 
untenable.* The Solenoconchae are an aberrant although insignificant 
branch of the Molluscan stock, certain resemblances between them 
and the Lamellibranchia are to be explained by the fact that 
both branched off from the same primitive form. , , 

‘The Lamellibranchia also are much specialised, but may still, 
through their lowest representatives, be related to the primitive form, 
The Protobranchia, for instance, still possess a foot with a creeping 
sole, as well as bipectinate gills. The foot and the gills in the 
higher forms, however, though modified, may still be traced back to 
the fundamental type. The creeping sole is, in any ease, lost in 
consequence of their burrowing habit, bot, on the other hand, one of 
the pedal glands which are found in the different divisions of the 
Mollusca develops into the byssal apparatus. 

The reduction of the head and absence of the radula, structures 
which are such constant features in nearly all other Molluscs, are 
characteristic of the Lamellibranchia. It has been said, no doubt 
rightly, that the radula has been lost ; it is oceasionally also wanting 
in other forms whose relations possess it as, for instance, im various 
Opisthobranchia (Phyllidia, Doridinm, Doricopsis, Tethys, ete)A 

‘The shell of the Lamellibranchia has a specially. typical -develop- 
ment. At first it is shaped like « shallow bowl, lying apon the back, 
like the shell assumed to have been possessed by the primitive form ; 
later, however, it bends over on the two sides, calcifies as two pieces, 
and thus assumes the typical bivalve form, The formation of the 
mantle corresponds to that of the shell, 

Aniong the internal organs, the nervous system, the circulatory 
apparatus, the pericardium (coelom) and the nephridia form in the 
way usual among the Mollusea, and this probably also may be said of 
these organs in the Cephalopoda, 

‘The Cephalopoda. Of the external organs of this elass, the mantle 
and gills also resemble those of other Molluscs. ‘The shell too may 
be derived from a simpler form, as is evident from the rounded 
chambers found in the embryo. The highly complicated form of the 


* Prats, in his recent work on the anatomy of Dentalinm, gives a: 

account of the relationships of these forms (see Literature to 

XXXL, No. 3, p. 98). re UG 
+ According to Sumorn (No. 17), Tethys (and the related form Melibe), for 

instance, does not require the radula because its food is soft. A Proso 

also (Magilus) has no radula. It lives ins tube covered by corals and feeds 

‘on the offal of these animals. (The Prosobranch families and 

Eulimidoe are also devoid of radulae.—Ep). 


GENERAL CONSIDERATIONS ON THE MOLLUSGA. 331 


chambered shell of Vautifus, the highest development of the Mollus- 
can shell, was attained later. 

The head, in the Cephalopoda as in the Gastropoda, is well de- 
veloped. The arms, which surround the mouth, at first sight appear 
to belong to it, and yet, according to the results of more reeent re- 
search, another significance must be ascribed to them, ie., they must 
be regarded us parts of the foot. A fact which causes surprise and, 
at first sight, is unfavourable to this view, is that some of the arms 
shift to the dorsal side of the head, being here found. behind the 
mouth. This makes it difficult to understand how the foot could 
have become transformed in this way, but when we see how extremely 
plastic it is, judging from different transformations which it has 
undergone in the Lamellibranchia, the Prosobranchia, the Hetero- 
poda and the Pteropoda, further modification is not so inconceivable, 
especially when we find thut the lateral parts of the foot in certain 
Prosobranchia (Diotocardia) even develop tentacular’ structures, 

Another part of the foot of the Cephalopoda has at any rate be- 
come changed into the fannel, which at first is paired, The pedal 
character of this structure has never been doubtful, its origin being 
at once betrayed by its position between the mouth and the anus. 
The change undergone by the foot in yielding the funnel is also very 
great, We cannot here enter into the question as to whether, as has 
been assumed, we have in this case to do with epipodia. The eom- 
parison of the different parts of the foot known as the propodium, 
mesopodium, metapodium, parapodium and epipodium becomes very 
difficult in modified forms, the inter-relationships of which alone pre- 
sent great difficulties. The conditions of transformation and adapta- 
tion may, in the various forms, have developed and modified very 
different parts of the foot. 

In the Cephalopoda, the organisation of the Mollusca has attained 
its highest development. In the structure of the adult the most far- 
reaching differentiation has taken place and thus also in its ontogeny 
we have the greatest complications found in the Molluscan stock, the 
greatest departure being made from those features (total cleavage 
of the egg, larval forms, ete.) which we have learnt to regard as 
primitive in the lower as well as the higher representatives of the 
Mollusca, 


16. 


17. 


LITERATURE. 333 


Rouue, L. Considération sur l’embranchement des Trochozo- 
aires. Ann. Sci. Nat. (7). Zool. Tom. xi. 1891. 

StumnotH, H. Ueber einige Tagesfragen der Malacozoologie, etc. 
Zeitechr. f. Naturw. Bd. |xii. Halle, 1889. 


. Spenaex, J. W. Die Geruchsorgane und das Nervensystem 


der Mollusken. Zeittschr. f. wiss. Zool. Bd. xxxv. 1881. 


. TareLE, J. Ueber Sinnesorgane der Seitenlinie und das Nerven- 


system von Mollusken. Zeitschr. f. wiss. Zool. Bd. xlix. 
1890. 


. THrELE, J. Die Stammesverwandtschaft der Mollusken, etc. 


Jen. Zeitachr. f. Naturw. Bd. xxv. 1891. 


CHAPTER XXXV. 


TUNICATA. 


Systematic (after Herpman) :— 
Order I. Larvacea (Appendicularia). 
Order II. Ascidiacea. 
1. Ascidiae Simplices. 
2. Ascidiae Compositae. 
3. Ascidiae Luciae (Pyrosoma). 
Order IIT. Thaliacea. 
1. Cyclomyaria (Duliolum). 
2. Hemimyaria (Sulpa, Octacnemus). 


IL. Sexual Reproduction. 
1. Larvacea (Appendiculuria). 


Very little is as yet known as to the development of Appendi- 
cularia, since the small eggs which are discharged into the surround- 
ing water are not easy to obtain and exceedingly difficult to examine. 
Fou (No. 1) and KowaLEvsky (treatise on Amphioxus) have, how- 
ever, stated that the development of this form closely resembles that 
of the Ascidiacea. The paired respiratory tubes of Appendicularia 
are formed in the same way as the first gill-slits of the Ascidian 
larvae (p. 366), an ectodermal invagination appearing at each side and 
a diverticulum of the pharynx growing out to meet it until the blind 
ends come into contact, perforation taking place at the point of 
junction. 


2. Ascidiae Simplices and Compositae. 
A. Oviposition, Fertilisation and Egg-envelopes. 


The eggs of most of the solitary Ascidians, soon after passing from 
the oviduct into the atrial (peribranchial) cavity, are ejected into the 


ASCIDIAE SIMPLICES AND COMPOSITAE. 335 


surrounding water where they pass through their embryonic develop- 
ment, being supported at the surface by the large, foam-like follicle 
cells (Fig. 149, ¢). Fertilisation usually takes place either in the 
peribranchial (atrial) cavity or after the egg is laid, but exceptions 
to this rule are found in the genera Cynthia and Lithonephrya 
(Gtarp), these forms passing through their embryonic development 





148.— Three stages in the development of the apy of Mhalducia wean witlata 
WALEVSKY, adapted from Kuryrer, For and others). basal membrane of the 
le; b su layer of peversent-epitheliua ; , follicle-cella; , chorfon ; 


4 tontcelld ; /, eug-cel 
within the peribranchial cavity of the mother. In Clavelina also, 
and in all composite Ascidians, development up to the time when 
the free-swimming, tailed larva is hatched takes place in the peri- 
branchial cavity of the mother, or else in peculiar divertioula of 
this cavity known as brood-spaces. The composite Ascidians differ 
from the solitary forms in the large amount of yolk contained in 
the ogg. Savensky (No. 49) recently observed in a few Polyclinidae 


336 TUNIOATA. 


(Amaroucium, Circinalium, Fragarium) a fusion of the embryo with 
the atrial wall of the mother. At this spot a thickening, the placenta, 
is formed, derived in part from the atrial wall (placenta. materna), 
from the follicle-epithelium enveloping the embryo and from an 
accumulation of test-cells (/alymmocytes). 

These Ascidiacea are hermaphrodite. Self-fertilisation seems, in- 
deed, to be prevented, in most, cases, by the maturation at different 
times of the male and the female genital products, but is not im- 
possible in other cases, in which both products ripen simultaneously. 
{In Ciona (Casrtx, No. I1,), although the products ripen at the same 
time, self-fertilisation does not occur.) 

The mature eggs are surrounded, at the commencement of em- 
bryonic development, by a complicated system of envelopes, which 
‘we are inclined to regard as derivatives of the original egg-follicle- 
In this respect we agree with KowaLEysky, whose views were con- 
firmed later by Van Benepen and Junt (No. (0) as well as by 
Moraan (No. 46), but we must point out that the origin of these 
enyelopes is still an epen question. This poimt will be further dis- 
cussed in the section on the formation of the egg under the heading 
of general considerations. 

Very young eggs, while still in the ovary, appear to be surrounded 
by a pavement-epithelium consisting of flattened cells (Fig. 148 A, ¢). 
The elements of this primary follicular epithelium (0) are derived 
from undifferentiated cells of the ovary (VAN Benepen and Juni). 
A structureless basal membrane (a) seems to be secreted early at the 
surface of the follicular epithelium, The follicle-cells multiply by 
division, and soon lose their flattened form and become cubical; a 
few of these cells are displaced inwards (Fig. 148 B, ¢) in such a 
way as to become deposited on the surface of the egg into which 
they may even find their way, passing into the most superficial layer 
of the vitellus, These cells, which can usually be distinguished by 
their yellow colour, have been called fest-elis (e) because it was 
erroneously supposed that they gave rise to the cells of the cellulose 
mantle (test) of the adult Ascidian, a view which was refuted by 
0. Herrwic (No. 25).* These test-cells, which soon increase very 

iphones 3{ more resent Eathors. ‘Toote seme be ba Saal esata 


moc 

‘about the fate of these cells. Sanensky (No. XXIX.), from his 

on the compound Ascidians, regards them as giving rise bets the ne p 
356) whereas the similarly ‘named cells of Salpa et tephra os 
nutritive structures (Hetpen, No. XIII; Kor XVII; 


No. XXIV. ; Pizox, No. XXVIL), the most recent “orga oh oa 


the follicle- and test-eella seams to agree with the given above,—Ep.] 


ASCIDIAE SIMPLICES AND COMPOSITAE. 337 


greatly in number, at first form an inner epithelial layer over the 
surface of the egg known as the fes/-cell-luyer (Fig. 148 C,e). In 
later stages they undergo a process of degeneration. 
the regularity of their arrange- 
ment and are found embedded 
separately in a gelatinous mass 
secreted over the surface of the 
egg. Their original cellular 
character is then less distinct 
and has been altogether denied 
by some authors (SEMPER, Fot). 
After the development of the 
test-cell-layer, a structureless 
membrane (Figs. 148, 149, «/) 
is secreted between it and the 


They then lose 





actual follicular epithelium, and 
this, being derived from the 
follicle-cells, may be described 
as the chorion, 


Fig, 149.—Mature egg from the oviduct 
of Ascidia canina* (after KUPFFER). c¢, 
follicle-cells (foain-like cells) ; «, chorion ; 
e, test-cells; /, egg-cell; +, gelatinous 
substance, 


In the meantime, a delicate erternal puvement-cpithelium (Fig. 
148 C, 4) has developed on the outer surface of the follicle which 
is in close contact with the basal membrane : this epithelium is pro- 
bably to be regarded as an outer layer of follicle-cells. Like the 
basal membrane, it seems to disappear, not being found in eggs after 
they have been laid. 

In the free eggs of the solitary Ascidians, the cells of the actual 
follicle-layer, at a later stage, assume a peculiar character. Their 
protoplasm becomes filled with numerous vacuoles (Fig. 148 C, 149, c) 
and thus resembles foam. The cells, which increase in size and form 
papilla-like structures (Fig. 149, c), are concerned in supporting the 
egg as it floats in the water. 

The mature Ascidian egg thus possesses the following envelopes, 
reckoned from without inwards :— 

(a) T= basal membrane of the follicle. 

(6) The external pavement-epithelium. 

(c) The actual follicle-epithelium (layer of foam-like cells). 

(@) The chorion. 

(e) The layer of test-cells (kalymmocytes, abortive eggs]. 


* ( =Ciona intestinalis, rar.—Ep.] 


Z 


338 TUNICATA. 


According to Cuasry (No. 13), another fine. structureless membrane cover- 
ing the external surface of the test-cells should be added to the above. In 
the solitary Ascidians, after the egg is laid, the interspace between the chorion 
and the surface of the egg is increased (Fig. 149) through imbibition of water 
and consequent swelling of the gelatinous matter secreted at the surface of 
the egg. 

We must here briefly allude to views as to the origin of the egg-envelopes 
which differ from those given above. According to SaBaTiER, Fo (No. 21), 
and Route (No. 47) the follicle-cells are produced by the egg itself. For and 
Rocze think that this is brought about by a process of budding from the 
germinal vesicle, but SaBatrer considers that the follicle-cells arise through 
free cell-formation in the yolk.# It seems to be fairly established that an 
ejection of chromatin-elements actually takes place from the nucleus of the 
ovum but we incline to the view that this process has nothing to do either 
with the rise of the follicle-cells or with that of the test-cells. Such an 
origin was assumed for the latter by Route, DaviporF (No. 14), and P1zox 
(No. XXVIL.), while a number of other authors (Semper, Fou, Sabatier and 
others, following Kcerrer, No. 34) thought that the test-cells formed freely 
in the protoplasm of the egg. 

It is of interest to note that the eggs of Appendicularia also are enveloped 
while in the ovary by a follicle (A. B. Lee, DaviporF). When laid, however, 
they are without covering, and only after fertilisation has taken place in the 
water do they become surrounded by a delicate vitelline membrane (Fol. 
No. 21). 





B. Cleavage. 


The free-swimming, tailed Ascidian larvae were known to the older 
authors and were carefully described by Mitye-Epwarps, P. J. 
vAN BENEDEN, and others. Our first knowledge of the embryonic 
development of the Ascidians, however, was due to the researches of 
Kowatevsky (Nos. 29 and 30), which were soon supplemented by 
the accounts of Kuprrer (Nos. 34 and 35) and MeTscuntxorF (No. 
41). Among later workers we must mention SEELIGER (No. 50) and 
van BENEDEN and Jubtn (Nos. 7-10); the eggs of the Ascidiae 
compositae which are rich in yolk have been investigated by Mauricr 
and Scrutatn (No. 39) and DaviporF (No. 14).+ 

The cleavage of the Ascidian egg is total, and, seeing that the 
blastomeres at first differ only to an inconsiderable extent iMsize and 
structure, may be described as almost equal. The term ‘ adequal 


* [As we have already stated, free cell-formation is now generally discredited 
by cytologists.—En.] 

+(Still more recently, SaLeNsKY (No. XXIX.) has worked at the develop- 
ment of the Ascidiae compositae. CastLE (No. II.) has worked at Ciona 
intestinalis. The work of the last-mentioned observer is very important and 
exhaustive.—Ep.] 





ASOIDIACEA—CLEAVAGE. 339 


cleavage,’ which was applied by Harsonex to the process in the 
egg of Amphiowus, is equally suited to the very similar processes met 
with in the Ascidians. Certain characteristic irregularities are, indeed, 
to be observed, antl these are referable to the early foreshadowing of 
certain important differentiations. 

The furrow which appears first and divides the egg into two equal 
halyes corresponds to the plane of bilateral symmetry, and the two 
blastomeres that result from this division represent the right and 
left: halves of the body (SeELIcER, van Benepe, Junin and Castim). 
From this stage onward throngh all the other stages of development, 
the bilateral symmetry of the embryo is clearly recognisable, The 





Fira. 150,—"Two a the cleavage of Clavelina (after gre LIGER). «A, four-celled 
stage, seen eeotienrsbore . The two smaller cells v rej to Sie: 
the anterior half of the body, and the larger cells Rergerees i. B, Intera! 
view of the cight-celled stage ; a, blastomeres of the Sain hal halt 6, blastomeres of 
the vegetative half, 


next furrow is also meridional and cuts the first at right angles. The 
four blastomeres thus produced (Fig. 150 A) are not of exactly the 
same xize, two being larger (/) and two smaller (v).* According to 
the most usually adopted orientation of the cleavage-stages in these 
forms, the plane of cleavage now under consideration has a transverse 
direction so that (according to vAN BenepEN and Juris) the two 
Jarger blastomeres represent the future anterior half of the body and 
the two smaller the later posterior half, but SeEniGER takes an 
exactly opposite view (Fig. 149 4). In Distaplia, according to 
Daviporr, the four blastomeres are exactly equal in size. 

“(In Ciona (Casrur, No. IT.) no difference in size is to be seen between the 


Ay the four-celled stage. The polar bodies are found to corre- 
spond to the future vegetative pole—Ev.] 


a 


340 


a 


TUNICATA, 


The third plane of cleavage is equatorial and, in the eight-celled 
stage that follows (Fig. 150 #), separates four smaller cleayage-spheres 


from four larger. 


ee 


A 


Fie. 151. Oy cant pgver chorea tnd 
SBELIGER). 4. ula-stage 5 e 
= sah G, ‘after 





According to all observers, the later ventral half 


of the body ig thus divided from 
‘the dorsal half. The four smaller 
spheres (2) which lie near the 
animal pole, and are said to 
represent the ventral surface of 
the body, are purely ectodermal 
in character, while the four larger 
blastomeres (2) which belong to 
the vegetative half (the future 
dorsal half) are said by vax 
Brnnpen and Juni to show a 
mixed character, They give rise, 
through division, to the large 
entoderm-cells, smaller eetoderm- 
elements being 


simultaneously 
-abstricted from them, these latter 


then joining with those of the 
ectodermal half of the body. 
According to SEELIGER and 
Davroorr, these cells are, on the 
contrary, purely entodermal.* 
Even at this stage, certain 
displacements of the blastomeres: 
can be observed, and these inter- 
fere with the regularity of the 
later course of the sleavage. 
This regularity is also disturbed 
by the fact that the ectoderm- 
cells, from this time onwards, 
divide more rapidly than the 
entodermal elements, It is, 
however, possible to distinguish 
a sixteen-cell stage ‘brought 
about by meridionial furrows, « 
thirty-two-cell stage caused by 
equatorial division, and a later 


* [According to both Castrx (Nos. IL. and ITT.) and Samassa 
nie roi and Jun, together with SeELicen, were Pen 


ee 


lll 


ASOCIDIACEA—FORMATION OF THE GERM-LAYERS, 341 


sixty-four-cell stage. For further details as to the cleavage we must 
refer the reader to the works of SeeticeR (No. 50), van BeneDEn 
and Sutin (No. 8), Cuanry (Nos. 12 and 13) [and especially Casi 
(No. IL.)). 

Even at the four-celled stage a cleavage-cayity is found open at 
both the animal and vegetative poles (Fig. 150). This cavity, at the 
sixteen-celled stage, appears to be closed on all sides, In later stages 
it disappears (Fig. 151 A, ) in consequence of a flattening of the 
embryo, which begins at the poles and which is specially marked 
in the entodermal half of the body; this flattening precedes the 
invagination of the entodermal cell-layer which results in the 


gastrula-stage. 


©. Formation of the Germ-layers. Appearance of the Medullary 
Tube and the Notochord. 


Through the changes just described, the embryo passes from the 
blastula-stage into a stage which we may, with Birsouts, call the 
plaeula (Fig. 151 A). The lens-shaped embryo is now composed of 
two layers, an entodermal layer (en) consisting of large high cells 
and a small-celled ectodermal layer (ec) which already covers the 
former like a cap.* In a fissure (f) between these two layers, we 
recognise the remains of the much compressed cleavage-cavity. The 
gastrulation which now takes place (Figs. 151 B, and 152) is due 
essentially to the curvature of the bilaminar embryo, the flattened 
area of entoderm-cells becoming invaginated in this process, while 
the ectodermal layer continues to spread out over the surface of the 


orientation of the Ascidian egg. CastTL concludes that SeeuicEn determined 
the dorsal and yentral sides of the egg correctly, but reversed the anterior and 
jor ends in all his figures of the carly stages. vas Buwepes and JUcin 
‘were correct in their determination of the anterior and posterior ends, but 
reversed the dorsal and ventral surfaces in all stages prior to the forty-four- 
celled Lat In consequence, the latter authors state that the four small cells 
of the eight-celled stage give rise to ectoderm only, while the four larger cells 
produce both entoderm and ectoderm ; whereas, as « matter of fact, neither 
group produces ectoderm exclusively. It is the four larger, not the four smaller 
cells, which give riso to the greater portion, perhaps the whole, of the ectoderm, 
‘The vegetative pole, which is marked by the polar bodies and the four smaller 
blastomeres, is dorsal, while the animal pole with the four larger cells is 
ventral. The future mesoderm arises from both primary layers. CasTun's 
work is so complete, and he traces the cell-lineage in such detail, that his 
interpretation must, we think, be accepted in preference to the above,—Ep.} 
* (The large cells at this stage would not, according to CasTLE, correspond 
with the e cells of the eight- and sixteen-celled stage; the latter by their 
more rapid division have become gradually smaller, whereas the originally 
«mailer cells, by their slower division, have not decreased in size to the same 
_oxtent and are now the larger of the two.—Ep.] 


se 


342 TUSICATA. 


eubrry. Gastrulation in the Ascidians has omsequently frequently 
been dexribed as transitional tetween the typical epibolic and 
embolic conditions. 

The gatrela-stam that thus arises (Fig. 151, ("is saucer-shaped. 
The arched surface of the embryo is covered with the small ectoderm- 
cells, while the flattened side of the body is occupied by the large, 
round blastopore. This side is said to change into the later dorsal 
surface of the embryo. while the arched side bhecomex the ventral 
surface. 


If we take as the principal axis of this gastrula-stage (Fig. 152 4) that 
which connects the animal] with the vegetative pole of the egg in the first 
mages of cleavage (a-b.. we find that this axis passes through the apex of the 
arched portion on the one hand and through the centre of the blastopore on 
the other. The future longitudinal axis of the body. on the contrary, would 
lie at right angles t this principal axis, since, according to all observers, the 
blastopore corresponds to the later dorsal surface. We should then havea 
condition differing from that of other Bilateralia, in which the primary axis 
corresponds approximately to the longitudinal axis of the adult. It seems 
probable that the blastopore shifts secondarily from the vegetative pole of the 
embryo, at which the posterior end of the body now develops to # position on 
the dorsal surface. According to this orientation, the dorsal and ventral 
surfaces would, as in the first ontogenetic stages of most of the Bilateralia, 
occupy a meridional position. After what has been stated above, we may 
conjecture that, in Ascidians, the displacement of the blastopore to the dorsal 
side of the body is first brought about by shifting caused by growth in the 
later gastrula-stages such as is indicated by the orientation adopted in Fig. 
152 A-C. A comparison with the ontogeny of Amphiorus to a certain extent 
supports this supposition (Chap. XXXVI). According to this view, the 
orientation of the cleavage-stages given by some authors, in which the animal 
pole of the body is said to be related to the future ventral half and the 
vegetative to the later dorsal half, does not appear altogether suitable, and 
can only be admitted with certain reservations,* 





Bilateral symmetry can be recognised in the gastrula-stage, even 
at the first, by the distribution of the cells. In later stages this 


*(CasTLe, in his work on Ciona, supports the latter view, that is, he finds 
that the vegetative pole with the entoderm and blastopore is always dorsal in 
position. The apparent shifting of the blastopore is due to the fact that it 
closes more rapidly from the anterior margin and from the sides than from 
behind. Consequently it comes to lie in the posterior portion of the dorsal 
surface of the embryo. He is therefore in agreement with Samassa (No. 
XXXIL) when ho states that there is no rotation of the axes during gastrula- 
tion as conjectured on theoretical grounds by KorscHELT and HEIpeR, but 
that the primitive axis corresponds with the vertical axis of the larva and 
the longitudinal axis is at right angles to this. According to this inter- 
pretation, the orientation of Fig. 152 is incorrect, since the blastopore, in 
each of the threo stages, is represented on a different surface, whereas it ix 
always dorsal in its position.—Ep.] 


ASCIDIACEA—FORMATION OF THE GERM-LAYERS, 


‘343 


symmetry is still more marked, the future anterior end of the body 


becoming swollen in consequence 
of the increased curvature of its 
two layers (Fig. 152 8). This 
arching is connected with the 
gradual narrowing of the blastopore 
which takes place on the dorsal 
side of the embryo in such a way 
that its last vestige lies near the 
posterior end of the body (Fig. 
153 C). Originally, the blastopore 
is a wide oval aperture, but in 
later stages it is pear-shaped, and 
it finally becomes a small posterior 
wperture (Fig. 153, 6-4"). This 
narrowing of the blastopore is 
caused principally by the inward 
growth of its anterior and lateral 
margins, the posterior edge re- 
maining unchanged. We have 
here conditions exactly similar to 
those in Amphioous, and we may 
assume a continuous closure from. 
befgre backward of the blastopore 
which originally extended along 
the whole length of the dorsal 
surface. 

During these stages even, the 
embryo becomes somewhat elon- 
gated in the direction of the 
longitudinal axis (Fig. 152 C). 
The dorsal side is recognisable by 
its flatter condition, and shows, at 
its posterior end, the remains of 
the blastopore (p); the ventral 
side, on the contrary, is arched, 
van Bryepen and Junin have 
pointed out that the posterior end 
of the body, at the gastrula-stage, 
is always marked by the presence 





F1G, 152.—Three consecutive gastrula- 
stages of Phaldusia wmumoidata (after 
Kowaxnysky). A, the invagination 
commencing ; B, appearance of the 
bilateral symmetry; C, narrowing of 
the blastopore ; «2, principal axis of 
the gastrula-stage ; ee", later lougi- 
tudinal axis of the body; d, dorsal 

side; cc, ectoderm ; en, entoderm ; /, 

cloavage-cavity; p,  blastopore; |v, 
ventral side, 


of two small wedge-shaped ectoderm-cells lying at the edge of the 


pire ‘TUNICATA. ' 


blastopore and representing the boundary between the ectoderm and 
the entoderm (Fig. 154, w). 4 
In these later gastrule-stages the commencement of histological 
: differentiation is already evident. 
This does not consist merely in 
the distinction between the eeto- 
dermal and the entodermal elements, 
although the latter are larger, : 
strongly granular and darker in 
colour; but differentiations are 
already. to be found within these 
germ-layers. ‘The ectoderm-cel 
which bound the blastopore, 
instance (Fig. 154 A, 
tinguished by the lange 
nuelei, their greater 7 
carmine stain, and their | 
shape from the other ectoderm-cells, which soon become 
‘This ring of cells is the first rudiment of the central nervon 
and, as the blastopore closes more and more, changes ix 











iq, 153.—Dorsal aspect of an embry 
of Claveline (after SERLIOER), 


bY, 
4”, outlines of the blastopore at 
consecutive stages of development. 





« 

Fro, 154.—Gastrula-stage of Clawlina Risswaie (after VAN BRNRDEN Jv 

A, dorsal area wadion sagittal section. 4, blastopora: ee, ectodern a 
ontoderm ; m, cells of the nerve-ring ; ic, small, wedge-shaped cells, + ae 


lll 


ASCIDIACEA—FORMATION OF THE GERM-LAYERS. 345 


medullary plate* This radiment, when it first appears, consists, at 
the sides of the still open blastopore, of a single row of cells, while, 
in front of the blastopore, it is composed of several rows of cells. 
Tu later stages (Fig. 154), as the blastopore narrows, the part of 
the medullary plate in front of it extends more and more, and, at the 
time when the blastopore is represented by merely a small aperture 
(Fig. 155), is a large and slightly depressed area, ‘The medullary 
groove thus formed, which is open anteriorly, is bounded by two 


teen thar 

dorsal aspect; 5, median sagittal Dlastoy ch, Peace ot 
5 B, n , ; 

chorda; ec, ectoderm ; em, entoderm ; m, Malaherpaonnn ar cells of the nerve- 





Jateral swellings (medullary swellings, m) which pass into one another 
behind the blastopore, thus forming a semicircle, 

A differentiation similar to the above is evident in the entoederm 
(Fig. 158). The cells of the latter, as a rule, are large and turgid, 
but in the region of the dorsal wall smaller cells appear which are 
originally arranged so as to form a ring encircling the blastopore, one 


af to Casrie (No. IL.), the cells lying behind the blastopore aud 
edn ta Pigs 154 and 155 are not part of the rudiment of the central 
ees, ‘as stated by Juni and vas Bennpny, but are in reality 
The rudiment of the nervous system is situated entirely in 
front of the blastopore. In Ciona the posterior margin of the blastopore 
Pied ed forward over the blastopore, coveriug in the medullary canal, as 
by VAN Beweven and Jutes in the case of Clavelina.—Ep.} 


i 























ASCIDIACEA—FORMATION OF THE GERM-LAYERS. 347 


stages as a narrow slit, The entoderm-cells also, in this latter form, do not jong 
retain their unilaminar arrangement, but become distributed in a radial direc- 


the formation of the 
3 the cell-boundaries drawn are 





nenropore, still very large. 
tion, the entoderm thus becoming multilaminar. The gastrula-stage is here 
im reality reached through epibole (Fig. 
156), In the anterior region of the body 
this overgrowth is especially marked, while in 
the posterior half, a small pit-like depression 
(Fig. 156 B) indicates the Inst remains of an 
invagination-cavity. This cavity, however, 
completely disappears after the blastopore has 
closed, The entoderm then represents a solid 
mass, the cells of which are soon found to 
vary in size. The position of the blastopore 
is occupied by the neural plate (7). 


During these stages, the medullary 
plate, which isalready somewhat invagin- yy, yg9 
ated, changes into a closed medullary hohe “i 
tube, its lateral walls, the medullary Tous: a pS mcrae the 


folds, growing towards one another and chord jec, ectoderm ; ca, ento- 





derm ; ma, lerm-~diverti 
. 160) 1; m0, folds 
ee ae aes 


The medullary tube develops from behind forward, a special part being 
taken in the process by the fold which connects the two medullary swellings 


— 


348 TUNICATA. 


posteriorly in the form of a semicircle (Figs. 155 and 158). It then appears, 
especially in longitudinal sections (Fig. 158 B), as if the medullary tube was 
formed solely by the posterior lip of the blastopore growing over the anterior 
lip. We must, however, bear in mind that, as this posterior medullary fold 





Fic, 160,—Transverse sections through an embryo of Clavelina Riswuna, at the same 
stage as in Fig. 158 (adapted from vaX BENRDEX and JULES) A, through the 
anterior, B, through the middle, and C, through the posterior part of the body. 
ch, chorda ; d, lumen of intestine : en, entoderm; #, medullary plate ; wr, medullary 
tube. 





grows forwards, the lateral medullary swellings are drawn into it, so that the 
posterior fold does not actually represent the lip of the blastopore, but « purely 
ectodermal! fold lying at this point; in this way, after the medullary tube has 
developed, its roof (n’) which is derived from the inner layer of the folds is 
also to be regarded as ectodermal. This is a point which deserves to be 
emphasised in opposition to the view of METscaNiKorF (No. 42). [Cf. foot- 
note, p. 345.) 





etxe sections through an embryo of Clacelina Risen, at the same 

162 (adapted from VAN BENEDEN and JULIS). ‘through the 
anterior, 8, through the middle, and C, through the posterior section of the body. 
ch, chorda; rn, eutodermn : ms, mesoderin : ar, medullary tube; ., cells which com 
plete the dorsal wall of the intestinal ¢ 














We shall see (Chap. NNXVL.) that, in mphiosus, the medullary tube forms 
by the sinking in of the somewhat depressed medullary plate and its separa- 
tion as such from the ectoderm; hence it is only covered by a single 
of cells, Only at a later stage does the plate curl round under the ectoderm 
toformatube. This manner of formation is probably @ moditication of the 





ASCIDIACEA—FORMATION OF THE GERM-LAYERS, 349 


origin from folds and is stated by SzeLiGeR (No. 50) as occurring in Clavelina 
also, but his observations on this subject were not confirmed by van BuwepEn 
and Juri (No. 10). These latter authors also do not agree in SEELicEn’s 
view that the medullary groove, at the time when it appears, lengthens 
posteriorly beyond the blastopore, - 

At the time when the medullary tube develops, the blastopore has not com- 
pletely closed, The remains of it, which originally lie in the floor of the de- 
veloping medullary groove, are retained for some time longer as the meurenteric 
canal and form # communication betweeen the lumen of the intestine and the 
central canal of the medullary tube (Fig. 158 B). 


Fre, 162.—Stage at which, in Olavelina Rissoena, the trunk- begins to separate 
from the caudal region (after VAN BENEDEN and JULIN). tae erteal sation; 
B, lateral aspect. ch, chorda; @, archenteric cavity; ec, ectoderm ; en, entoder 
on, snb-chordal entoderm-strand ; ms, anterior portion of the tmesoderm-bands 
composed of small cells; ms’, Roars jor portion of the same composed of large calls ; 
np, neuropore; nr, medullary tube 





As the medullary tube develops from behind forward, the aperture 
at its anterior end, known as the newropore (Fig. 162, mp), is retained 
for a long time. The separation of the mesoderm from the chorda 
dorsalis takes place simultaneously with the development of the 
medullary tube. These two rudiments arise, as may be ascertained 
from the detailed accounts of van BenepEN and Juni, essentially 
through the same processes of development as in Amphiowus, although 
the conditions are in this case not so evident, and seem specially 
modified in the posterior region of the body. The embryo soon 
assumes « long, pear-shaped form (Fig. 162), the posterior, narrowed 


a : 


350 ‘TUNICATA, 


region corresponding to the future tail of the larva. Tn the anterior, 
dilated region, the mesoderm arises through the development of 
paired diverticula of the archenteron (Figs. 159, 4, ms), the lumens 
_ of these sacs very soon disappear and the cells of their walls, 
which originally were arranged in two layers (the somatic and the 
splanchnic layers), then appear irregularly distributed between the 
ectoderm and the entoderm. Between the two coelomic diverticula, 
the roof the archenterie wall is completed by entoderm-cells (Figs. 
159, 160 A, 161 A, ch) which represent the rudiment of the chorda, 
At a later stage, these cells become shifted into closer proximity, and 
thus form a solid strand which, in cross-section, is round. ‘The fact 
that this strand is to be traced back toa median fold of the arch- 
enteron is proved by transverse sections through the most anterior 
part of the rudiment of the chorda (Figs. 160 4, 161 A), where the 
infolding of the cell-plate which represents the rudiment of the | 
chorda can actually be seen (van BenepEen and Juni, No. 10). 


In Amphiocus, according to HarscHex, the median fold of the intestinal 
wall is not completely absorbed in the formation of the chorda. Its lateral | 
cells, which are in contact with the coelomic diverticula, yield the cells which 
complete the dorsal wall of the intestine after the chorda has separated from 
the mesoderm. van BenepEeN and Juin conjecture that similar conditions 
exist in the anterior part of the chorda-rudiment in the Ascidians (ef, Fig- 

161 A, 2). 

A certain guarantee of the accuracy of the observations made by vay 
Benepe and Jur seems to be afforded by the striking resemblance to the 
formation of the mesoderm in Amphiowus. Their observations, however, 
have not been confirmed either by Daviporr (No, 14), who investigated the 
formation of the mesoderm in Clavelina and Distaplia or by Witney (No. 
54a), According to the former author, the mesoderm-cells become abstrigted: 
from definite entoderm-cells at the margin of the blastopore (mesoderm- 
gonads), and become arranged in an originally single layer below the 
entoderm, This would be a kind of mesoderm-formation by delamination. 
Davrporr was unable to find coelomic diverticula. The “mesoderm-gonads* 

‘ave said to remain in connection with the entoderm, and, after the mesoderm 
has been produced, some of them are said to take part in the formation of the 
chorda and others in that of the alimentary canal. * 


In the posterior region of the body (the future caudal region), the 


condition appears to be modified through the early disappearance of 
the lumen of the intestine (Fig, 160 @), The strand-like chorda is 


*([In Ciona, the mesoderm-cells form temporarily of the wall of the 
archenteron between the chorda and the entoderm, Eventually they become 


displaced outwardly and the entoderm and chorda come into contact, 
soning to Ciexcs (No. J) thera dose ‘not appeal Seiad setae SS 
formation in this genus.—E.] 


t ill 








ASCIDIACEA—FORMATION OF THE GERM-LAYERS. 351 


here pressed inward by the developing medullary tube, so that it 
then fills the whole lumen of the intestine. The lateral cells of the 
wall of the enteron, three of which are usually seen on either side 





Fro, 163 — — Hater tae of development of Clavelina Rixsoene (after Yay BENEDEN and 





JULEN) , median angittal section ; B, lateral aspect. , chord: 
on, 3 en’, subchordal entoderm-strand in the caudal region; me, anterior 
celled of the mesoderm-bands; ms’, posterior large-celled caudal 


weotion of the aamo; vp, neuropore; mr, medullary tube, 


in cross-section, pass directly into the large mesoderm-elements 
which cover the chorda laterally and subsequently yield the caudal 
musculature, There then still remain the entoderm-cells that lie 


_ 








352 TUNICATA. 


in the ventral middle line (Figs. 160 Cand 161 C, en) ; these, which 
are arranged in two parallel rows, retain the character of ordinary 
entoderm-cells and form a permanent cell-strand connected with the 
intestine, in which we recognise the vestiges of a caudal section of 
the alimentary canal (Fig. 162 A, 163 A, en’). 





Fic. 184.—Median sagittal sections of two stages of development of Distaplia magui- 
Jarta (after Davivorr), ¢, rudiment of the caudal section of the intestine; cA, 
rudiment of the chorda;: ‘d, enteric cavity; ec, ectoderm; en, entoderm; *. 
medullary plate; ap, neuropore; 7, medullary tube. 


In the caudal region, the separation of the mesoderm and the chorda takes 
place in a vory simple way, the archenteron merely breaking up into the two 
rudiments. These structures, however, are probably to be derived in & way 
similar to that described above for the anterior region of the body. We 


ASCIDIACEA—FORMATION OF THE GERM-LAYERS. 363 


shall have here to assume (with vAN BENEDEN and JuLin) in these regions, 
the presence of a lumen of the archenteron compressed through the growth of 
the chorda-rudiment to the shapo of @ crescent. The question here arises 
whether the mesoderm-layer of the caudal section is‘to be referred to the 
splanchnic or the somatic layer of the former mesoderm-rudiment. van 
Benepex and Juuin incline to the first assumption, and SEELIGER (No. 50) 
has also pointed out the resemblance of the mesoderm-cells of the caudal 
section to to the cells of the inner layer of the mesoderm in the anterior 
region of the body. : 





Fio. 165, —A later stage in the development of istaplia maynilarce (after DavIDOFF). 

¢, caudal prolongation of the alimentary ; ch. rudiment of the chorda ; 
vity ; ee, ectoderm; en, entodermn ; /, adhesive papillae; ma, mesen- 
; ar, medullary tube. : 





The mesoderm and the chorda are therefore derivatives of the 
primary entoderm.* Their origin can be traced back to the form of 
folding which is also found in Amphiocus. The principal distinction 
between the process here and in Amphiorns seems to be that, in the 
mesoderm-rudiment of the Ascidians, no trace is to be found of the 
segmentation which appears so early in Amphiorus, In the Ascidians 
the mesoderm-bands appear composed of two different parts (Figs. 
162 B, 163 B); an anterior part (ms), consisting of several layers of 
small cells, which has arisen through folding in the anterior part of 
the archenteron, and a posterior part composed of a single layer of 
large cells (ms’) belonging to the caudal region. The anterior part of 
the mesoderm, at a later stage, forms 2 mesenchyme filling the 


® [See footnote, p. 340.—Ep.} 
AA 


354 : TUNICATA. 


primary body-cavity (Fig. 167, ms) which yields the blood-corpuseles, 
the connective tissue, the body-musculature, as well as the genital and 
excretory organs, while the posterior part gives rise to the larval 
caudal musculature (Fig. 168 B, m). 

In Distaplia, in which, after the closure of the blastopore, the 
entoderm forms a solid cell-mass (Figs. 157, 164 A), the enteric 
cavity arises only later through the shifting apart of these cells (Fig. 
164 8). In this way posterior part of the body is marked off; in 
this the cells of the entoderm separate into the rudiment of the 
chorda (Fig. 164, ch) and into that of the solid sub-chordal enteric 
process (c), while the large entoderm-cells in the anterior region of 
the body (Fig. 165, en) mix later with the mesenchyme and probably 
disintegrate. In other respects there is no essential ditference be- 
tween the development of Distaplia as described by Daviporr (No. 
14) and that of other Ascidians. It should be pointed out that the 
elements of the food-yolk here appear equally distributed in all the 
tissues (the ectoderm, the mesoderm and the entoderm). 


D. Development of the free-swimming larva. 


External form of the body. We have already pointed out that, 
at the time when the medullary tube develops, the embryo becomes 
elongate and pear-shaped. In this way a broader anterior section is 
inarked off from a narrower posterior section (Fig. 162) which gives 
rise to the tail of the larva. This latter part of the body next grows 
yreatly in length, less, as SEELIGER points out, by the multiplication 
than by the elongation of the cells composing it. At the same time, 
it becomes more distinctly constricted from the anterior section and 
curves round ventrally (Fig. 163). As the tail, which is now bent 
downwards and forwards, increases in length, its posterior end not 
only reaches the anterior end of the body but even grows upwards 
again at the right side of the latter. In this proccss, the tail be- 
comes twisted on its longitudinal axis, so that the nerve-tube appears 
shifted to the left side of the embryo (Fig. 170, p. 368). 

The anterior region of the body, which at first appears more or less 
spherical, lengthens later, and in the larva is ovate (Figs. 167 and 
168). ‘Three prominences, arising as thickenings of the ectoderm, 
can soon be seen at its anterior end; these are the rudiments of the 
papillae for attachment (Figs. 167, 168, 170, 4), through which, by 
means of a secretion yielded by the glandular epithelium, the fixation 
of the larva takes place. 


ASCIDIACEA—DEVELOPMENT OF THE FREE-SWIMMING LARVA. 3565 


Baxrour has pointed out that, since a similar attaching apparatus is found 
in Amphibian larvae and (in front of the mouth) in the larvae of many 
Ganoids (Acipenser, Lepidosteus) we may perhaps have here an inherited 
feature common to the Chordata. It seems doubtful, however, to what ex- 
tent these structures are really homologous and not merely analogous. 





After the egg-envelope has burst, the larva straightens out. The 
tail then forms a direct posterior continuation of the longitudinal 
axis of the body (Figs. 167 and 173 A, p. 375). 





Fro. 166,—Transverse section through an attached larva of Phallusia mammillate 
(after Kowaevsky). a, mesenchyme-cells in the act of passing through the 
ectoderm ; 4, mexeuchyme-cells in the cellulose mantle; d, alimentary canal ; 
ec, ectoderm; ms, inexenchyme-celln; of, otolith ; s, transverse section” through 
the sensory vesicle; f, cellulove mantle, 









The mantle, The ectoderm-cells, which originally were somewhat 
cubical but assumed a more flattened form, at the time when the 
caudal region develops, secret, at their outer surface, a homogeneous 
cuticular layer which, from its first appearance, gives a cellulose 
reaction. This is the first rudiment of the Ascidian test or tunic. 
In the caudal region, this layer grows out to form a median dorsal 
and a ventral fin (Fig. 169, ff, p. 363). While, in Doliolum and 
Appendicularia, such a simple, homogeneous cuticular layer is 
retained throughout life, in the Ascidiacea and Hemimyaria it is 
considerably thickened, single cells immigrating into the cellulose 


356 TUNICATA. 


layer. It has hitherto been believed that, as O. Hertwia (No. 25) 
maintained, the cells that wandered into the cellulose substance came 
from the ectoderm, but Kowauevsky (No. 32) has recently proved * 
that the mantle-cells were derived from the mesoderm, being meso- 
dermal cells which traverse the ectoderm and thus migrate outwards 
(Fig. 166). Subsequently, in the cellulose substance, they assume 





Fic, 167.—Embryos of Phallusie wammillate at a later stage (after Kowal 
al, lateral aspect ; 8, dorsal aspect. a, eye; eh, chorda: cl, cloacal vesicle; , 
rudiment of the alimentary canal; ex, entoderm- ciliated pit ; h, 
papillae; é, mouth ; ms, mesenchyme-cells ; trunk-section, 
section of the medullary tube ; sb, sensory oI sub-chordal 
strand; r, vacuoles between the cells of the chorda, 















the character of star-shaped connective-tissue cells. We have to 
regard the mantle of the Tunicates as a cuticular gelatinous secretion 
permeated by phagocytes (mesoderm-cells).+ When, in the composite 
Ascidians, some of the individuals disintegrate, the phagocytes of the 


* SALENSKY's recent statements as to Pyrosoma (No. 74) fully agree with this 
observation (see below, p. 401). 

[tSreticer (No. XXXIII) agrees with Kowavgvsxy that the true test- 
cells are mesodormal. In Qikopleura, howover, the cells of the “ Haus” are 
ectodermal. --Ep.] 


ASCIDIACEA—DEVELOPMENT OF THE FREE-SWIMMING LARVA, 357 


mantle play an important part in the process (Maurtox, No, 40). 
The histological character of the mantle-tissue may undergo further 
modification, such as the vesicular transformation of the mantle-cells 
in. Phallusia, and the appearance of fibrillae in the ground-substance 
in Cynthia. 

Since the surface of the embryo is, from the earliest stage, surrounded by 
@ gelatinous covering, in which lie embedded the yellow test-cells, it was 
formerly thought that this layer was to be regarded as the rudiment of the 
future mantle (KowaLevsky, Kurrrer), an error to which the test-cells owe 
their name, Zoologists were inclined to consider the mantle of the Ascidians 
as a persisting embryonic envelope. ©, Huntwic first proved that the test- 
cell-layer is lost and that the mantle arises from the ectoderm. The im- 
migration of the mantle-cells was only recently ol by Kowanavsxy. 
Sanensxy, however, in a recent treatise (No. 49, also No. XXIX.) has returned 
to the older view, ascribing to the test-cells (kalymmoocytes) in Distaplia the 
principal part in the formution of the cellulose mantle [see footnote, p. 836.] 

The nervous system. ‘he rudiment of the central nervous system 
which has hitherto been called the medullary tube, from the early 
stages onward, shows a dilatation of its anterior section (Fig. 163, 
nr, p. 351). In the later stages which lead to the development of 
the free-swimming larva, this dilated anterior part gives rise to a 
vesicle, the so-called cerebral or sensory vesicle (Fig. 167, sb, vésieule 
antéricure ou vérébrale of vas Bexepen and Junin) while the 
posterior, narrowed part yields the caudal section (région caudate) of 
the nerve-cord (4). These two parts appear connected by a middle 
part (r) with » narrow central canal and thickened wall which 
Kowarervsky (No. 30) has called the trunk-ganglion (portion viscérale 
du myelencéphale of VAX Brxupex and Junin). The former con- 
nection between the neural tube and the exterior (the neuropore) 
completely closes even before the appearance of the oral aperture, 
whieh lies near the same point. 

The cerebral or sensory vesicle represents the most anterior part of 
the medullary tube swollen out into a vesicle by the dilatation of its 
central canal. [ts walls consist for the most part of pavement- 
epithelium, but the dorsul wall is thickened and divided into a right 
and a left awelling by a median furrow (VAN Beyepen and Junty, 
No. 7). The two organs known as the eye and the ofocyat (au and ot, 
Fig. 168) soon appear in the form of accumulations of pigment. ‘The 
eye, which is derived from the right dorsal swelling (Fig. 168 8), is 
4 cup-like deposit of pigment at the inner ends of several radially 
placed columnar cells, the cavity being occupied by « lens with a 
superimposed meniscus (Fig. 168). 


, 








ASCIDIACEA—-DEVELOPMENT OF THE FREE-SWIMMING LARVA. 359 


the ventral wall of the vesicle while the free ond carries a pigment: 
cap. This view of the formation of the auditory organ is supported 
by Koprrer’s statement (No. 35) that the cells of the ventral wall 
of the sensory vesicle which surround the otolith-cell and which 
differ somewhat in histological character from the rest, are provided 
with fine, stiff setae projecting towards the otolith-cell, According 
to Kuprrer, « vesicular cavity is found in the crista acustica 
directly below the otolith-cell, oa 


According to KowAuevs«y, the otolith-cell, on its first appearance, is 
situated on the dorsal wall of the sensory vesicle and only shifts later ovey 
its right side to the ventral surface. Our knowledge of the structure and 
development of both the sensory orguns is, however, very inadequate.* 


The frank-vection of the nervous system (Figs. 167 and 168, r) 
(the trunk-ganglion) is, according to vAN BenepEn and Junin, 
the direct continuation backward of the left dorsal swelling of the 
sensory vesicle. The cells of the wall of this swelling show the same 
histological character as those which, in a single layer, line, like an 
epithelinm, the narrow central canal of the trunk-ganglion, On 
these cells, however, on the ventral side, there is superimposed a 
great mass of ganglion-cells (Fig. 171). According to the distri- 
bution of these cells we can recognise the division of the trank- 
yanglien into an anterior and a posterior section, the anterior section 
being still included by Kurrrer in the cerebral sensory vesicle as 
4 ganglionic portion. In the posterior section, the ganglion-cells 
enclose a nucleus of nerve-fibrillae, The trunk-region of the nerve- 
cord lies above the most anterior end of the chorda (Fig. 168 4) 


* [According to Waunex (No, XXXVL) who has investigated the develop- 
ment of these organs in dscidia mentula and Clavelina lepadiformis, the first 
indication of these sensory organs consists in the deposition of black pigment- 
grapules in the dorsal wall of the cerebral vesicle. The most anterior of the 
cells containing nt-granules becomes distinguished by the larger size 
of its granules and the swollen nature of the cell itself. This pigment-cell 
soon separates itself from the others and becomes gradually transferred by 
a differential growth of the wall of the vesicle down the right wall to its 


‘final ‘ion on the ventral side of the vesicle. This cell is the otocyst, and 
the pi granules become consolidated together to form the otolith, The 
other pigment-cells of the dorsal wall of the vesicle collect themselves 


er and form a slight protuberance in the right dorso-lateral corner 
of the vesicle, The pigment-granules become concentrated toward the cavity 
‘of the vesicle. Subsequently two or three cells from the adjoining wall of 
the yesiole take up a position, one above the other, in front of the mass of 
pigment and by an alteration of their contents give rise to the lens of the 
eye. The original pigment-producing cells constitute the retina, which retains 
its primitive position as of the epithelial wall of the brain. See also 
Sauessky (No, XXX,).—Ep.) 


360 TUNICATA. 


According to vaAN BENEDEN and Junin, however, the chorda does 
uot reach so far forward in Clucelina as in Phallusia. 

The cdudal section of the nerve-cord (Figs. 167 and 168, s) is a 
tube the walls of which consist of a simple pavement-epithelium. 
Tn cross-section (Fig. 169, nr, p. 363), four cells are usually found, 
two lying laterally, one dorsally and one ventrally. 


This section extends to the postgrior end of the body. The reduction of 
the lumen of the alimentary canal in the caudal region of the embryo is 
accompanied by the obliteration of the neurenteric canal which represented 
the posterior continuation of the central canal of the nerve-cord. 


KupFFer observed the important fact that, in the larva of decidia 
mentula, lateral bundles of fibrillae are given off by the caudal 
section of the spinal cord; these we may claim as spinal nerves. 
The first pair of these was found on the boundary between the 
trunk and caudal regions, and the following two pairs at intervals 
more or less corresponding to the length of a caudal muscle-cell. 

We nay regard this as an indication of the segmentation of the 
caudal region, The same significance may be attributed perhaps 
to those cell-groups found by LaniLie (about ten in number) in 
the caudal nerve-cord of the Distaplia larva, and also occurring in 
alppendientaria (Noctse, LANGERHANS, and others). 

The ciliated pit. In connection with the central nervous system, 
we must deseribe a ciliated diverticulum which opens into the dorsal 





wall of the anterior section of the alimentary canal (branchial sae 
or pharynx) and which has been claimed as a homologue of the 
Aupophysis corchri of the Vertebrates. In adult Ascidians its form 
is more complicated. A 0 glandular mass, the sub-neural yland 
talamb -hypophysnire or sub-anglionic bedy) can then be recognised 
in close proximity to the brain. and an efferent duet runs forwant 





to enter the pharynx through a complicated apparatus, the doral 
tuberele. iu the doral middle line between the two ciliated bands 
(Mons yo weds which run upwards from the endostyle. The 
opening of this duct has erroneously been assumed to be an olfactory 
orgn (olfactory tuberele. see TuLts, Nos, 26 and 27), 

According tov. and Juris (No. 7) aud SEBLIGER 
(No. 50), the first rudiment of this ciliated diverticulum arises quite 
independently of the nervous system pit-like invagination of 
the entodermal wall of the pharynx. At a later stage. the blind 
end of this diverticulum is said to become closely applied laterally 
to the sensory vesiel on the side which is tumed away 


























ASCIDIACEA—DEVELOPMENT OF THE FREE-SWIMMING LARVA. 361 


from the eye, te., as a rule, on the left side, although LaHILLE 
(No. 37) considers that this condition varies in the different forms. 

Lanitte (No. 37), SHELDON (No. 52), Wiuvey, (No. 54), and 
Hyorr (No. 59), on the contrary, have been led by their researches. 
to confirm m almost all points the older observations of KowaLev- 
SKY as to the rise of the ciliated pit, ie., to regard it, in its origin, 
as much more closely connected with the central nervous system. 
After the neuropore has completely closed, the most anterior section 
of the cephalic vesicle lengthens and fuses with an ectodermal 
depression, the stomodaeum (rudiment of the larval mouth, branchiak 
aperture). At this point perforation takes place (Figs.-167 A, 168 
A, 7), so that now the cephalic cavity, by means of this short tube 
which represents the rudiment of the ciliated pit, communicates with 
the most anterior ectodermal section of the alimentary canal. Only 
in later stages when, after the fixation of the larva, the larval 
nervous system degenerates, is the connection between the ciliated 
pit and the nervous system lost. The pit then forms a blind in- 
testinal diverticulum contiguous with the definitive ganglion (Fig. 
173 4).* 

According to these statements, the ciliated pit opens into the ectodermat 


or stomodaeal portion of the branchial sac, and we thus have a condition 
agreeing with that of the hypophysis in the Vertebrata, 


The chorda. The chorda arises through the transformation of a 
plate-like rudiment (Fig. 159, ch), which originally formed the roof 
of the archenteron, into a cell-strand which, in cross-section, is 
round (cf. Figs. 160 and 161, ch). We have seen above (p. 348) 
that we must suppose this to have been brought about by the forma- 
tion of a groove (as in .Amphiorus). In cross-section, the chorda-strand 
is originally composed of several cells. Both in lateral (Fig. 162 4) 
and in dorsal aspect. it appears composed of two rows of cells, the 
ends of which dove-tail with one another. This dove-tailing of 
the cells denotes the commencement of a change of position which in 
most cases leads to the chorda-cells appearing arranged one behind 
the other in a single row like a roll of coins (Fig. 163 1). In those 


*[Witury (No. XXXVI.) has recently reinvestigated this point both in 
Ciona and Clavelina. He is convinced that van BENEDEN and JULIN were 
quite mistaken in their interpretation of the origin of the hypophysial tube 
in Clavelina. The whole is derived essentially from the neural tube, and 
thus the lumen of the hypophysis is at first in direct communication with 
the lumen of the central nervous system, the opening of this structure into. 
the pharynx being, according to WILLY. a reopening of the neuropore.— 

‘D.) 


362 TOUNICATA. 


later stages which ure connected with a lengthening of the caudal 
section, the cells of the chorda-strand also lengthen (Figs. 167 4, 
170, ch). The chorda then begins to undergo a transformation which, 
at its commencement, is comparable to the changes in the chorda 
of Amphiorus, but, in the Ascidians, leads to peculiar modifications in 
this organ. Between cach two consecutive cells there appears a 
vacuole filled with a gelatinous substance (Fig. 167, v; ¢f. also Fig. 
170). These vacuoles, which, at first, lie in the axis of the chorda- 
strand, as they enlarge, compress the chorda-cells in such a way that 
the latter soon assume the biconcave form of fish-vertebrae and, as 
the gelatinous mass extends further, can be recognised merely as 
thin vepta between its different sections. These sections soon come 
into contact and fuse, and in this way a strand of homogeneous 
gelatinous substance arises which at first resembles a string of beads 
but is later uniform and cylindrical (Fig. 168 A), while the chorda- 
cells which are pressed out to its surface surround it as a kind of 
sheath (KowaLEvsky, KupFFER, SEELIGER. and others). 


‘The transformation of the chorda is not, in all Ascidians, so complete. 
Avconding to SEELIGER, in Clurelina, it does not advance beyond the stage in 
which the chonda-cells assume the form of transverse septa. 





Mesoderm, body-cavity, musculature. The two mesoderm-bands 
accompauy the chorda along its whole length and project a little 
beyond it anteriorly. Two parts can be distinguished in them (Figs. 
182 4.163 4). Lathe posterior part (aie) where they consist of a single 
layer of large cells arminged in three longitudinal rows, they yield 
the musculature of the larval tail, The cells of this part lengthen 
in later stag. 
while. on th 
fibrils of contractile substamee 1Fix. 188. 











af development (Fig. [6S 2, ma) becoming hexagonal, 
inner ant outer surfaces they produce longitudinal 
1 which appear to lie 
somewhat obliquely to the lonzitudinal axis of the bedy in such a 
way that che fibres of the inner Liver emes these of the outer layer 
at an acute angle (SEE 














ada] musculature of the larva 
tmuusverse striation. 
mes sierm-bands consist of 
vely crowded together (Figs. 
Myer which ties neat to 
the myoblast-larer of 
asfomuations as the 





ASCIDIACEA—DEVELOPMENT OF THE FREE-SWIMMING LARVA. 363 


somewhat loosened ; they assume a spherical form and constitute a 
mesenchyne which fills the primary body-cavity of the trunk-section 
(Fig. 168, ms). 

We have seen (p. 350) that, according to VAN BENEDEN and JuLIN, 
the mesoderm in this anterior part becomes detached from the arch- 
enteron in the form of paired coelomic 
diverticula (Figs. 159 and 160 A). The 
true coelom that arises in this way 
belongs, however, merely to the earliest 
embryonic stages, and disappears even 
as early as the time when the mesoderm 
completely separates from the entoderm. 
The mesoderm then fills the space 
between the ectoderm and the entoderm, 
which, in later stages, becomes consider- 
ably widened and, as it appears, filled 
with a gelatinous mass ; this forms the 
yround - substance of the mesenchyme 
that arises through the transformation 
of this anterior portion of the mesoderm. 
The lacunae which arise later in this 
mesenchyme must be regarded, like 
the blood-vessels (which, according to 
vaN BENEDEN and Jurin are entirely 
devoid of an endothelial wall) as the 
pseudococle. 

The mesenchyme of the trunk-region, 
which is derived in the above way, yields 





Fis. 
through the caudal portion of 


169, — Transverse section 


the mesodermal organs of the adult 
Ascidian. Its histological differentiation 
gives rise to the connective tissue, ax 
well as to the pigmented clements, 
and to the body-musculature of the 
adult which appears arranged in radial 
and circular muscles surrounding the 


the free-swimming larva of 
Clarelina (after SRELIGER), ch. 
chorda ; er, ectoderm; fl, 
median’ fin; m, _ cellulose 
mantle ; mf, muscle-tibrillae in 
transverse section ; mz, muscle- 
celle; ur, neural tube; s, sub- 
chordal entoderm - strand ; + 
mantle cells, 








inhalent and exhalent orifices as well as into longitudinal muscles 
of the trunk, etc. Single cells of the mesenchyme, which become 
free and reach the pseudococle, become changed into blood- 
corpuscles. We shall see later (p. 380) that the genital organs 
also, with their efferent ducts, and the urinary organs originate in 
the mesoderm. 


364 TUNICATA. 


It must be mentioned that at a later stage (especially during the transforma- 
tion connected with fixation) the mesenchyme becomes apparently enriched 
by elements which, when the entodermal strand (Fig. 169, s) and the larval 
nervous system disintegrate, become free. KowaLEvsky thought that these 
cells became changed into blood-corpuscles, and later, SEELIGER (No. 50) 
utilised this fact in constructing his theory of the budding in compound 
forms. It, however, appears doubtful to us whether these elements take any 
part whatever in the formation of the organs of the adult or of their buds or 
whether they do not rather, after reaching the blood, undergo degeneration. 

The alimentary canal. The rudiment of the alimentary canal is 
derived from the archenteron by the separation of the mesodenn 
bands and the chorda-strand. In early embryonic stages (Figs. 162, 
163, p. 351) it consists of an anterior pre-chordal dilatation (en) and, 
following this, of a narrowed purt lying already below the chorda but 
still belonging to the trunk-region. This narrowest part is directly 
continued into the sub-chordal entoderm-strand of the caudal region 
(en') which must be regarded as the intestinal rudiment of this 
part of the body. 

Since the mesoderm and the chorda (as seen above, p. 350) arise 
by a process of folding from the dorsal wall of the archenteron, the 
dorsal wall of the intestine is defective at this point; this gap be 
comes closed in later stages by certain cells as described above 
(p. 350). This defect is only found in the trunk-region in the 
posterior narrowed part of the alimentary canal, as the rudiment of 
the caudal region undergoes no further advance in form and, on the 
other hand, the pre-chordal section of the intestine takes no part in 
the foldings which give rise to the mesoderm and the chorda. This 
narrowed sub-chordal trunk-portion of the intestine, after the gap 
just mentioned has closed, forms a blind diverticulum projecting 
backward (Fig. 167 .1, ¢, p. 356), the end of which, according to 
Kowavevsky, at those stages in which the caudal section becomes 
more sharply marked off from the trank, bends slightly towards the 
dorsal side, thus severing its connection with the cellular entoderm- 
band of che caudal region (xe). In this way is introduced the de- 
generation of this last part of the intestine mentioned above, which 
leads to the cells of this band becoming disconnected and assuming 
a resemblance to blood-corpuscles. We then tind, beneath the chorda 
in the caudal region, a cavity apparently filled with blood-corpuscles 
and in direct communication with the spaces of the pseudocoele. 

According to KowaLevsky, with whom the majority of later 
authors (KUPFFER, SEELIGER) agree, the branchial sac or pharynx 
is derived from the pre-chordal dilatation of the intestinal rudiment, 





ASCIDIACEA—DEVELOPMENT OF THE FREE-SWIMMING LARVA. 365 


while the sub-chordal diverticulum, which is directed backward (d), 
yields, through simple growth, the other parts of the alimentary 
canal (the oesophagus, the stomach and the intestine proper). This 
diverticulum, as the larva lengthens, is said to form a coil in which 
we can distinguish a right descending portion, a ventral connecting 
piece, and a left ascending part which ends blindly. The right 
portion is said to give rise to the oesophagus, the connecting piece 
to the stomach and the left ascending portion to the intestine (ef. 
Fig. 168, ¢ and e/ with Fig. 170, of, m, and ed). The anus only 
arises later, during larval life, by the blind end of the intestine be- 
coming connected with one of the two so-called cloacal vesicles (that 
on the left), these latter being ectodermal invaginations which will 
be described further later. 

The account given by VAN BENEDEN and Junin (No. 10) differs 
from that given above in so far as they derive only the descending 
portion of the intestinal coil (consisting of the oesophagus and the 
stomach) through direct growth from the posterior diverticulum 
mentioned above, while they believe that the intestine proper arises 
from the ventral surface of the dilated stomach as a secondary out- 
growth. The point of origin of this secondary caecum, which is 
directed to the left and upward, is said to lie somewhat far forward, 
4e., to be almost pre-chordal. We shall see below (p. 521) that these 
authors ascribe some significance to this observation. 

The oral aperture of the larva (which gives rise to the inhalent or 
branchial aperture of the adult) is formed only shortly before the 
larva hatches. The anterior pointed end of the alimentary canal, 
just before reaching the sensory vesicle, bends dorsally. It there 
comes into contact with an invagination which has arisen from a 
thickened dise of ectoderm-cclls. By the apposition of these two 
structures and a breaking down or separation of the cells, the oral 
aperture is formed (Figs. 167 and 168, p. 358). 

The endoxtyle develops as a ciliated furrow in the antero-ventral 
region of the branchial sac (pharynx), owing to the formation of two 
lateral longitudinal swellings. We cannot here enter further into 
the histological details of this structure, but must refer the reader 
for these to the treatises of R. Hertwie, Fou and SEELIGER (No. 
50). We may, however, mention that this furrow is not purely 
ventral in position, its anterior portion extending up towards the 
dorsally placed oral aperture (Fig. 170, es). According to a recent 
treatise by Wiubry (No. 54a), the rudiment of the endostyle 
originally lies in the most anterior part of the branchial sac in which 





366 TUNICATA. 


it has a dorso-ventral position. Only later does it shift farther back 
and come to lie ventrally. This observation is of importance in 
connection with the condition of this organ in Amphtoxrus, where 
it undergoes a similar displacement. 

The digestive or pyloric gland arises as a caecal outgrowth at the 
boundary between the stomach and the intestine; it, however, soon 
branches repeatedly, and these ramifications extend over the surface 
of the intestine where, by anastomosing, they form a network (Fig. 
175 A, dr, p. 379). It has been homologised by WiuLeEy (No. 54a) 
with the hepatic caecum of Amphiorus. 

Peribranchial, atrial, or cloacal cavity. The first rudiments which 
lead to the development of the peribranchial cavity are found, shortly 
before the larva hatches, in the forin of a pair of ectodermal invagina- 
tions lying dorsally at the boundary between the sensory vesicle and 
the trunk-ganglion, called by MEerscHNIkorF, who was the first to 
observe them, the cloacal vesicles (Fig. 167, cl, p. 356). Two 
diverticula grow out from the pharynx towards these invaginations, 
one on each side, and fuse with them, thus giving rise to the first 
gill-slits (Fig. 168, %, p. 358). According to KowALEvsky, a second 
pair of these slits (k”) soon forms in Phallusia behind the other in 
the same way. If the interpretations of KowALEvsky and SEELIGER 
are correct, the cloacal vesicles, by enlarging, give rise to the paired 
halves of the peribranchial cavity. In this case, the latter would be 
lined throughout with ectoderm, and the wall of the pharynx, which 
is perforated by the gill-slits, would on its inner side be covered with 
entoderm and on its outer with ectodermal epithelium. We should 
then perhaps be justified in homologising the peribranchial cavity of 
the Ascidians with the atrium of Amphiorus: we can hardly, in any 
case, doubt the homology of the gill-slits in these two groups. 
Another view has, however, been adopted by vaN BENEDEN and 
Jur (Nos. 9 and 10). According to these observers, the first gill- 
slit arises through the fusion of a rather long entodermal diverticulum 
with the cloacal vesicle of the same side which, according to these 
authors, is never very large. The Ascidian larva at this stage is 
exactly in the condition in which Appendicularia remains through- 
out life, the pharynx, in the latter, communicating through a 
branchial passage on either side with the exterior. These passages 
represent a pair of gill-slits, and this pair, in the Ascidian ax in 
Appendicularia, remains the only pair. In the Ascidian, the branchial 
passages are considerably enlarged secondarily, and in this way the 
peribranchial or atrial cavity arises. Since these passages, according 


ASCIDIACEA—DEVELOPMENT OF THE FREE-SWIMMING LARVA. 367 


to vAN Benepen and Junin, are for the most part of entodermak 
origin, a large although not sharply marked portion of the peri- 
branchial cavity must be lined with entoderm. These observers 
therefore maintain that these spaces cannot be homologised with the 
atrial cavity of Amph/owus, and the future perforations in their inner 
walls can in no way be homologised with the gill-slits of Amphiorus 
and the Vertebrates, and are therefore distinguished from true gill- 
slits by these authors as branchial stigmata. We have some hesita- 
tion in accepting the view of vAN Buyepxn and Jens. The origin 
of the peribranchial cavities in the Ascidians does not appear to us 
sufficiently understood to justify its utilisation in the formation of 
such important conclusions, It should be pointed out that, in the 
embryo of Pyrosoma, the purely ectodermal origin of the peribranchial 
eavities can hardly be doubted (see below, p. 394), and this seems 
also to apply to Doliolum (see the statements as to the Anchinia buds, 
p. 481). Again, we are probably not justified in concluding without 
further evidence that the condition of Appenlicularia is primitive. 
Since an Appendieularian was found by Moss (No. 5) possessing 
many gill-clefts like those of Doliofwm, we may have to regard the 
apparently simple respiratory organs of other Larvacea as degenerate. 

We shall have to speak of the further transformations in the 
branchial region when describing the metamorphosis of the attached 
larva, although, in some cases, the multiplication of the gill-slits 
commences in the free-swimming larva (Botryllus, Distaplia, Fig. 
230, p. 457), 

Laninee (No, 38) and Wittey (No. 54a) have both recently expressed their 
belief in the purely ectodermal origin of the peribranchial sacs. According to 
Lanu.e, they arise, in the Didemnidae, through the enlargement of the 
cloacal vesicles. Their outer aperture then disappears and an unpaired 
ectodermal invagination appears on the dorsal side; this is the cloacal in- 
yagination proper, which only secondarily becomes connected with the 
peribranchial sacs. Wrotry (No, 54a) observed, in Clavelina, as the pre- 
cursor of the cloacal vesicle, a longitudinal furrow, from the posterior end of 
which the cloacal vesicle develops. Wruuny is therefore inclined to assume 
Shat the peribranchia!l cavity of the Ascidians is homologons with that of 
Amphionus. 

The outer apertures of the two peribranchial spaces (Fig. 231, 
p. 460) shift continually towards each other and towards the dorsal 
middle line till they meet and fuse. In this way arises the cloacal, 
atrial or inhalent orifice (Fig. 230, ¢). van Benepen and Jou 
(No. 9) have pointed ont that, during this fusion, the part of the 
ectoderm which lies between the two apertures becomes depressed 


i 


368 TUNICATA. 


and this depression gives rise to the true cloacal cavity, i.e. to the 
unpaired part which connects the two peribranchial cavities and 
which is thus lined with ectoderm. 

The terminal portion of the intestine which had, at an earlier 
stage, become connected with the left cloacal vesicle (see above, 
p- 365) now opens into the common peribranchial cavity. 

The heart, the pericardium and the epicardium. We owe to 
SEELIGER the proof that the heart and the pericardium of the 
Ascidians are entodermal structures, the first rudiment of which can 
be recognised in the form of an outgrowth from the pharynx arising 
between the posterior end of the endostyle and the entrance to the 
oesophagus. A vesicle which becomes abstricted from this caecum 





es ep we 
Taevline obey (attet SEELIGER). 01, e) 
hor xhalent aritive ; «/, . epivardial outgrowth : es, endost 
7, iufolding of the body-snttace in anticipation of the rotation that takes pl 
fixation h. adhering papillae; é iuhaleut oritive; de, gill 
esophagus: 4, anditory ong 
; sh, sensory vesicle, 














Lett lateral asp 





















(Fig. 170, pe) is the common rudiment of the pericardiam and the 
heart. The remainder of the caecum (4) has been named by vay 
Bexepes and Junin the egveardium.*® These authors were able 
essentially to contirm the statements of SEELIGER, although they 
Aly ditfer from him in points of detail. They also recognised 
titicance of the epicardium in connection with budding, and 
the originally double rudiment of these structures, 

The tirst rudiment of these org: observed in the form of two 
solid cell-strands which ran side by side in close contiguity to the 











repute 
the 


















aS Ww 





*(Dastas (No. IX.) finds that in Ciona the epicardium has a paired origi: 
and opens by two distinct orifices into the pharynx.—ED.] 











ASCIDIACEA—DEVELOPMENT OF THE FREE-SWIMMING LARVA. 369 


ventral wall of the alimentary canal near the point at which the 
oesophagus enters the pharynx. The origin of these cell-strands 
(procardium) is less clearly stated. vax Brnepen and Juin have 
no doubt that they become detached from the entodermal intestinal 
epithelium. Wuttey has recently (No. 54a) made the same observa- 
tion, finding, however, that the procardial rudiment is unpaired and 
also not entirely agreeing with vay BeyepEN and Juni with regard 
to its further development. The left procardial strand always appears 
stronger than the right. The strands soon develop lumina and thus 
become tubes, In later stages, the posterior ends of these tubes fuse, 
while, anteriorly, they open into the branchial sac, ‘The whole rudi- 





Pip, 171.—Pares comeoutvy franaveres sections throng the trunk: region of a Clare 
(diagrammatic, after VAN BewEDEN aud JuLIN). A, shows the pe | 
ind nacre branchial auc or pharynx with the apertures of 


epicardial tubes (~p.0). 8, shows the connection hetween the epicardial Sire 
isha he the nde rete (os ©, shows the blind ends’ of the epicardial 
¥ 





ip tctoterm |, 
teas e °, Pina en ends of the plonrdial tabex 
wear their ‘openings os the TX; thy heart; m, pte wntle ; m, neural 





inent now consists of wn unpaired posterior caecum (Fig. 171 B, ep 
and pe), which forks anteriorly into two tubes that open separately 
into the branchial sac (Fig. 171 4, ep). From the posterior 
caecum, a vesicle becomes abstricted (Fig. 171 C, pe) and this 
represents the common rudiment of the heart and the pericardium. 
The lumen of this vesicle (pe) is the future pericardial cavity. 
form of the yesicle is complicated in consequence of the invagina- 
tion of its dorsal wall as a furrow running along its whole length ; 
this makes the vesicle crescent-shaped in cross-section, The lumen 
of this invagination is the future cavity of the heart (4). The in- 
BB 






















‘TUNICATA, = 
vaginated part of the wall of the vesicle 
‘ ‘the noninvaginated part | 


Th tn tt hn in 


and 4, p. hoo age it ceates tans Sea 
ventral wall is drawn in to close the dorsal aperture of 


duction of the buds. By extending farther and f 
reaches the stolon (Fig. 173 C, st) in which it fo 
partition. Th  thiv' process it becomes \so! minal 





of the stolon (Fig. 229, 2, p. 456,) the two bloo 
each other at this point. Werrhall hers tose 


oats tetova Wace aah ri 
vertebrate pericardium. In later stages, the cell 
the heart secrete, on the surface turned to the lu 


ASCIDIACEA—ORGANISATION OF THE FREE-SWIMMING LARVA. 371 


muscle-fibrils in which transverse striation can be distinctly seen. 
An endocardium is wanting in the Ascidian heart, and its yessela 
have no endothelial lining. 


E. Review of the Organisation of the Free-swimming 
Larva (Pigs. 168-173 A). 


It should be mentioned that there is considerable variation in the 
degree of development attained by the organisation at the moment 
of hatching in the different species and even in the individuals of the 
same species. 

The form of the larva, the development of which has just been 
traced in detail, recalls somewhat that of a tadpole. Anteriorly, 
there is an oral region (cephalic and trunk-region) the end of which 
carries the three adhesive papillae (Fig. 173, hp); this region is 
followed by a long, flatly compressed swimming tail. This latter, 
which shows markings like those of fin-rays (Fig. 173 A) attains its 
characteristic form through the great development of the mantle- 
substance (Fig. 169, #) which further covers the whole surface of 
the body, even passing over the oral and cloacal apertures. 

The axis of the tail is oceupied by the chorda which extends 
anteriorly into the trunk-region. Above it lies the neural tube, 
while a cell-strand that runs below it and soon disintegrates repre- 
sents the remains of that part of the intestine which belongs to the 
caudal region. Running along this part of the body and extending 
along its whole length, are the massive muscle-bands. 

In the anterior region, the neural tube swells out to form a sensory 
vesicle (Fig. 173, s+) and a swollen trunk-section (1) immediately 
following the latter. The primitive enteron gives rise to the 
pharynx or branchial sac, the oesophagus, the stomach and the 
intestine. The oral aperture (or inhalent orifice, ‘) is established 
and is distinguished by its dorsal position. Near it, the ciliated pit 
(A), which extends as far as the base of the sensory vesicle, opens 
into the pharynx. The intestine opens into the atrial cavity which 
has formed by the union of the two originally separate peribranchial 
sacs. There is now a single atrial aperture (or exhalent orifice, e). 
The number of gill-slits which have at this stage developed varies 
in different species. 

The heart (}, the pericardium and the epicardium (ep) have 
developed. The heart already pulsates ; the endostyle (hypobranchial 
groove) has developed. The mesenchyme becomes differentiated into 


ASCIDIACEA—FIXATION AND METAMORPHOSIS. 373 


(Fig. 173 B), to which they are then appended as # short truncated 
process. The internal organs of the caudal region are retracted more 
and more into the trunk (Fig. 172). They there coil up spirally, but 
the separate elements (the chorda, the muscle-bands, the neural tube) 
which compose this coiled strand retain for a long time their relative 





Fic, 172.--Degeneration of the candal region during metamorphosis in the larva of 
Phatlusie mummillate (atter KOWALBVSKY). itudinal section through an 
early stage’; B, posterior portion of a longi ction through an older stage. 

-cells ; ¢c, ectoderm ; eva, invaginated epidermis of the tail; me, mesen- 
chyme-cells in the act of passing through the ectoderm ; mt, cellulose mantle ; ms, 
inuscle-cells of the tail : #1, nerve-cells of the caudal section ;’ns, neural tube, 








positions (cf. Fig. 172 B, 2, where the strand is cut through trans- 
versely). The degeneration of the chorda commences, according to 
KowaLevsky's most recent researches (No. 32), by the disappearance 
of its gelatinous substance, while its cells (Fig. 172, ch) again become 


374 TUNIOATA, 


arranged into a simple strand, The degeneration of the chorda-cells 
which are distinguished by their granular contents, is finally brought 
about by phagocytosis. This is also the case with the musele-cells. 
The ectoderm-cells, as the caudal section shortens, become larger 
(Fig. 172 A), and spherical, strongly refractive bodies appear in 
them, so that they come to resemble the so-called granulated spheres 
of the pupa of the Muscidae (Vol. iii., p. 379), When the internal 
organs of the caudal section have teat completely taken up into 
the body-cavity of the trunk, the ectoderm is invaginated (Fig. 172 
B, ens), This invagination soon becomes completely abstrieted from 
the epidermis of the larva and then forms a closed vesicle lying 
within the body-cavity ; the cells of this vesicle soon lose their 
cohesion, the lumen disappears, und finally nothing remains but 
a mass of detached and gradually disintegrating granular cells. The 
gelatinous envelope (Fig, 173 ©, ss) of the caudal region is, finally, 
lost either by being simply absorbed aceording to Kuprrer’s obser- 
vations, or thrown off, as SkEnIGER and Munr-Epwarps agree in 
maintaining. f 
Since the attachment of the larva is accomplished by means of the 
anterior end of the body, the oral aperture (inhalent orifice) appears 
to lie near the point of attachment (Fig. 173 B). In the adelt 
Ascidian, on the contrary, the oral aperture lies at the end of the 
principal axis of the body opposite to the point of attachment (Fig, 
173 C). ‘This shifting of the position of the oral aperture is the 
result of a rotation made by the body round its transverse axis 
after attachment, during which the part of the body between the 
mouth and the point of attachment lengthens, This lengthening, in 
Clavelina, according to SEELIGER, is made possible by the develop- 
ment of a deep infolding of the surface of the body (Figs. 170, 173 
A and B, f) whieh slightly separates a pre-oral portion carrying the 
adhering papillae from the rest of the body. This pre-oral region 
represents the basal section of the young Clavelina from which the 
branching stolon soon grows out. The folding just mentioned 
renders it possible for the Clavelina, which originally was placed 
with its longitudinal axis at right angles to the basal plane (surface 
of attachment), first to bend sharply towards this plane and then 
to lie with its longitudinal axis parallel to it, finally however, to 
rise up from it in such a way that the oral aperture comes to 
lie opposite to the point of attachment. During this rotation round 
the transverse axis, which was pointed out first by Kurrrer and 
later by SeexicER, the angle passed through is one of almost 180." 


a 


ASCIDIACEA—FIXATION AND METAMORPHOSIS. 875 





picardial 
th at , heart; i, adhering papillae; i, bra H 
By cavity; r, trunk-portion of the medullary tube; s, partition-wall of the 


376 TUNICATA. 


It is interesting to compare the transformations undergone by the 
Ascidian larva after attachment with that of the Cirripedia and the 
Pedicellinn larvae, in which to some extent analogous conditions 
prevail. 

A degeneration similar to that undergone by the organs of the 
caudal region algo takes place in the larval nervous system. The 
anterior sensory vesicle breaks down, its elements become spherical 
and lose their connections. For some time after the sensory organs 
have disappeared a mass of pigment remaining from them may be 
“observed in the body-cavity of the young Ascidian. The degenerated 
elements. later reach the latory system, where they probably 
completely disintegrate (p. 364). A similar disintegration is suffered 
by the tissue on the ventral side of the trunk-ganglion which consists 
of large ganglionic cells. The central nervous system of the young 
Ascidian, according to VAN BENEDEN and JULIN (No. 9), consists of 
those elements which surround the central canal in the region of the 
trunk-ganglion, and are continued anteriorly on to the left swelling 
of the sensory vesicle. The elements derived from the cephalic vesicle 
thus yield the definitive ganglion, while the elements of the trunk- 
ganglion produce aganglionic cell-strand (rordonganglionnaire viscéral) 
discovered by vAN BENEDEN and Juin, which, first running back- 
ward in the dorsal median line, becomes applied to the dorsal wall of 
the pharynx but then diverges to the left, runs along the left side of 
the oesophagus and ends between the two hepatic diverticula, After 
the gelatinous cover has been perforated by the apertures of ingestion 
and egestion, the admission of water and of food into the alimentary 
canal becomes possible. 

In the further development of the Granchial network, the chief im- 
portance attaches to the appearance of new slits, each of which, as a 
rule, arises through the fusion of a shallow diverticulum growing out 
from the entodermal wall of the pharynx with the lining of the atrial 
cavity. At the point of fusion, the slit is first visible as a very small 
aperture. In this way, according to KowauEvsky, in Phallusio 
mammillata, after the first gill-slit has formed, a second appears 
behind it (Fig. 168, 4”) this being apparently of the same size as 
the first. Later, nccording to Kroun (No. 33), two new slits appear 
between these two and behind the last slit (the second in order of 
formation) one more. In this way five primary gill-slits form in a 
longitudinal row. Each of the trabeculae between every two gill-slits 
contains a blood-sinus (branchial vessel, Fig. 168, 4). Above and be- 
low this primary row of slits, other rows are said to form later, the 











ASCIDIACEA—FIXATION AND METAMORPHOSIS. 317 


number being then further increased by the intercalation both of new 
slits and new rows between those already formed. ‘The gill-slits are 
at first elongated in the transverse direction, but their shape changes 
later, as they lengthen longitudinally. 

According to van Brenepen and Junin (No. 9) the formation of 
the additional gill-slits in Phadlusia (Ascidiella) scabroides follows an 
entirely different rule. A longitudinal.row of six primary slits here 
first forms (Fig. 174 A, 1-6). Of these, the fourth (4) in the row is 
suid to appear first, the first in position (1) being the second to form. 
The fifth (5) forms next and then the second (2), while those that 
oceupy the third and sixth positions (3 and 6) form last. These six 
primary gill-slits ure markedly elongate transversely (Fig. 174 B) 
and each becomes divided by projecting outgrowths of the trabeculae 
lying between them, In this way the six primary slits give rise to 
six rows of secondary slits. In later stages, new slits are said to 
break through between these. 

Tn Clavelina, according to SkrcicEeR, two transverse rows of gill-slits are 
found even in the free-swimming larva (Pig. 173 A). A new row forms in 
front of these and behind them another is added after fixation. In this case 
the number of slits is increased by the appearance of new independent perfora- 
tions (and thus not by the division of those already present), This is also the 
case, acoording to GansTana (No. 21a) with the buds of Bofryllus, while, in 
the larva, the number of slits is increased through the division of thoxe 
formed first. According to this author also, Pyrosoma, with its transversely 
elongated slits in a single row, represents a specially primitive condition. 

The rise of the six primary gill-slits (Fig. 174 A, 1-6) has recently 
been carefully examined in Ciona by Witney (No. 54a). Slits 1 and 
4 arise first, simultaneously and apparently independently of one 
another. Wuinney is inclined to regard these two as parts of a single 
slit separated as in Amphiorus by a tongue-bar, The next slits to 
appear (2 and 3) form by abstriction from | and 4, while 5 and 6 
arise independently. Witory thus regards slits 1-4 as parts of a 
single primary slit separated by abstriction. The stage depicted in 
Fig. 174 4 would then possess only three actual primary slits. As 
the six slits present divide in the manner stated by VAN BENEDEN 
and Jur, six transverse rows of slits are formed, these all at first 
being elongated transversely but later lengthening longitudinally 
(parallel to the endostyle). Further division of the apertures leads 
to the intercalation between these six rows of other transverse rows 
(Witxey). 

‘Even at an early stage, an entodermal fold can be seen projecting 
inward on the imner side of the branchial region between every two 


Ui 





= | 


* 378 TUNICATA, 


primary slits (Fig, 174, tr). These folds are the rudiments of the 
transverse bars; prominences (p) form on them both anteriorly 





p 


Fie, 174.—Two young stages of Phallusia (Ascidietla) idles (after Wax 
and JULIN, somewhat altered), 1-6 in A, the six primary gill-elefts, in B, the 
of gill-clefis derived from them, cl, atri 5 





and posteriorly and give rise to papillae. The papillae on the eon- 
secutive branchial arches lie so near each other as to come into 


i — | 


ASCIDIACEA—FIXATION AND METAMORPHOSIS. 879 


contact and fuse, giving rise to the internal longitudinal bars (Ir) 
of the branchial region. 

At an early stage, the first rudiment of the pericoronal circle 
(peripharyngeal bands, ciliated arch, Fig. 174 A, 6), as well as that of 
the coronal circle, which lies in front of it and is beset with tentacles, 
can be seen. The arrangement of the tentacles when they first appear 
is bilateral. 

The development of the genital organs has still to be described. 
In the compound Ascidians, the individual that develops from the egg 
has no genital organs, but multiplies exclusively through budding. 
This is also the case with the social Ascidians (GaNrn). In studying 
the development of the genital organs we are consequently restricted 
to the simple Ascidia if we wish to study their origin in a sexually 





Fio, 175.—.1, dorsal aspect of the intestinal coil in the bud of Perophora Listeri with 
the rudiment of the genital organs; B, somewhat older genital vesicle (after VAN 
BeNngnes and Juuty). g, genital vesicle ; gs, yenital strand ; dr, digestive gland ; 
ve, oesophagus; a, stomach ; é, intestine, 


produced embryo, otherwise we must trace their rise in the asexually 
produced buds of other Ascidians. The course of development in 
these two cases is, however, so uniform that we may take as our 
example the buds of Perophora which were examined with special 
reference to this point by vAN BEenEDEN (No. 10). 

The Ascidians are hermaphrodite. The male and female genital 
rudiments, however, are derived from a common rudiment which is 
always unpaired and lies on the intestinal loop medianly and dorsally 
(Figs. 174 B, gs’, 238 EZ, g). This is found at the point at which the 
efferent duct of the digestive gland firat branches (Fig. 175 A). It 
consists of an accumulation of cells indistinguishable from ordinary 


THE ABBREVIATED DEVELOPMENT OF THE MOLGULIDAR. 38% 


comes into contact with it. At the same time, the vas deferens has 
been gradually split off from the oviduct so that finally the two 
canals enter the cloaca separately, The male and female genital 
rudiments have thus become altogether distinct. The further de- 
velopment of the genital glands manifests itself chiefly in the con- 
tinuous formation of lobes. In the epithelium lining the ovary, the 
eggs can soon be distinguished from the surrounding undifferentiated 
cells, which form the follicular epithelium. As the eggs increase in 
size, they shift, enveloped in their respective follicles, into the 
surrounding stroma, so that, finally, they are only connected, like 
the grapes on a bunch, by means of the thin efferent ducts of the 
follicles with the ovarian epithelium. 

The urinary vesicles (Fig. 174 B, rs) form in the same way as the 
first rudiment of the genital organs as accumulations of mesenchyme- 
cells in which a cavity appears, containing at first only serous fluid, 
but, later, urinary concretions (VAN BENEDEN and Jury, No. 9). 


G. The Abbreviated Development of the Molgulidae. 


The development of those forms the eggs of which up to the time 
when the tailed larva hatches remain within the body of the mother 
(Ascidiae compositac, Cynthia, Lithonephria) is, in many ways, some- 
what modified and abbreviated. One of the Molgulidae which lays 
its eggs affords us, however, curiously enough, the most marked 
example of abbreviation of development. The caudate larval stage, 
in this case, is ultogether omitted (Lacaze-Durnrers, No. 36; and 
Kurrrer, No. 35); even the chorda does not appear to develop, In 
other respects, the ontogeny of this form, so far as it is known, does. 
hot seem essentially to differ from that of other Ascidians, After the 
cleavage of the very opaque egg has taken place, the thick-walled 
primary enteric vesicle can be recognised inside the embryo, and near 
it an accumulation of large cells filled with reserve nutritive material. 
This accumulation ean be seen for a long time, as development pro- 
ceeds, lying near the posterior end of the body (Fig. 177, r). It may 
perhaps be regarded as the equivalent of the suppressed larval tail and 
may be compared to the claeoblast of Pyrosoma and Salpa. As the 
internal organs develop, five finger-shaped outgrowths appear on the 
surface (Fig. 177, f); these vary greatly in size and position and 
degenerate later, They do not serve, as might be supposed, for the 
fixation of the embryo. The nervous system (mn) seems to develop 
from an ectodermal depression. The primary enteric vesicle repre- 


S| 


382 TUNICATA. 


sents the rudiment of the branchial sac (pharynx). The rest of the 
alimentary canal (d) develops as an outgrowth at the posterior dorsal 





Fig, 177.—Embryo of Molgula spb a tere (after ae 
alimentary pal es, endastyle ; ae Inet Of the of the imhalen 
orifice; m, nervous system ; 7, spherules Chtcamereaettiaale 


angle of the primary enteric vesicle. The inbalent and exhalent 
orifices, the endostyle, the gill-slits, ete., develop as in other Ascidians, 


3. Doliolum. 


The development of the egg in Doliolum seems to form a direct 
sequence to that in other Ascidians. As in the latter, a larval form 
occurs which propels itself by means of a swimming tail. ‘This larva 
was first described by Kron (No. 85), and later by GEGENBAUR 
(No. 78), Kerensrety and Exuers (No. 81), Gronpen (No. 79), and 
Unsanin (No. 86), To the latter author we owe, further, almost 
the only statements we have as to the embryonic development of 
Doliolum, which is very insufficiently known. 

‘The mature egg of Dotiolum, surrounded by follicle-cells, reaches 
the atrial cavity of the mother from which it is soon ejected inte the 
surrounding water. Occasionally, however, part of the embryonic 
development seems to take place within the atrial cavity. As a rule, 
the egg is fertilised only after its expulsion, and then surrounds 
itself with a homogeneous membrane. This membrane (Fig. 178, =) 
which soon rises up from the surface of the egg in such @ way 
that a space filled with fluid can be seen between it and the egg, 


: al 


DOLIOLUM—CLEAVAGE, 383 


has been called the vitelline membrane by ULsanty, and for a long 
time shows, on the external surface, remains of the original follicular 
epithelium (f). Since, however, both Grospen and Fon (No. 21) 
observed within this membrane cells which without doubt correspond 
to the test-cells of the Ascidiacea we may perhaps rather regard it 
as the equivalent of the chorion of the Ascidian egg. 





Fro. eet er eae, ee of meer Miilleri Lali d rd rls 
Ree icecths os ons toat (cncciosys ovr, menor sw totinon! or tha eevee 


Cleavage is total and almost equal, and closely resembles that 
described above in connection with the solitary Ascidians. The 
blastala and invagination-gastrula (Fig. 178 A) observed by Unsantn 
were comparable to the similar stages in the Ascidiacea. 

We have very incomplete accounts of the subsequent stages, At 
the next stage observed by Utsaniw and depicted in Fig. 178 B, 
the embryo is pear-shaped, and within it we can see three distinct 
rudiments. A large dorsal cell-mass (m) is regarded by Unsantn as 











a... 


384 TUNICATA, 


the rudiment of the central nervous system, which here does not take 
the form of a tube but of a solid ectodermal growth, while 4 ventral 
cell-mass (eh) is assumed to be the rudiment of the chorda and a 
posterior mass the mesoderm (ms). According to Unsanry, the arch- 
enteron is used up in the formation of the chorda and the mesoderm ; 
the rudiment of the adult intestine on the contrary owes its origin 
to an independent ectodermal invagination which occurs later. 

In the next stage (Fig. 178 C), the embryo appears to be folded 
several times within the egg. A dilated anterior region principally 





Fie, 179. = ire sorcalled larval’ stagos of Zoliofwm Allert iter (aoe Uist ay 
pase B, older stage, ch, chorda ; cl, atrial : 
heart ; 2m, Ser eet ahle ma’, anterior mesodernt-1 vadtaheee ma", :, 
ridiment; 1, nervous system ; p, pharynx ; x, mesodermal rut imeut of the stalon ; 
yy mesoderm-masses, 


occupied by the large ganglionic rudiment (w) can be distinguished 
from a caudal region bent back upon itself, in which the chorda (ch) 
is seen to be already developed. ‘wo lateral mesoderm-bands (ma) 
run along the whole length of these two regions of the body. Similar 
stages were also observed by Fon (No. 21). 

In the stages which follow (Fig, 179 A), the embryo straightens 
itself out within the egg-shell and is now able to raise itself from 
the bottom of the sea on which the egg rests and to swim about 


«a 


DOLIOLUM—LARVAL DEVELOPMENT. 385 


by means of its long caudal region, und is therefore usually called 
a farve although it is still enveloped in the much-distended egg-shell 
(m) iu which traces of the follicle-cells ean be found, We do not 
know for certain when this egg-shell is cast off, During these pelagic 
ontogenetic stages in which the Doéfolum resembles the Ascidian 
larva, the body is elongate (Fig. 179 4) and the middle of it is 
occupied by a vesicular ectodermal swelling (¢4) caused by the 
accumulation of a clear fluid. ‘This vesicle divides the body into a 
posterior and an anterior region. ‘I'he anterior develops into the 
young Doliolum (the first asexual or “nurse” form, the /aatozaoid) 
while the ectodermal vesicle and the caudal region must be regarded 


nm 





Fic. 130.—Young “nurse” form of Lotiolum Khrenbergii, with remains of the larval 
tail (after Unsaxrn). ch, chorda ; dé, so-called dorsal stolon ; ¢, endostyle ; A, heart 
and pericardium ; m, egg-shell ; #, nervous system ; +, rosette-shaped organ (rudi- 
ment of the weutral stolon). 

as provisional larval organs and degenerate later (Figs, 179 #, and 

180). The structure of the caudal region corresponds to that of 

the same region in the Ascidian larva. It consists of a chorda and, 

laterally, of muscle-plates derived from the mesoderm-bands. At the 
anterior end of the caudal region, a part of the mass of mesoderm- 
cells (Fig. 179, ms’) is not transformed into spindle-shaped muscle- 
fibres. ‘I'wo cell-masses (y) are subsequently given off from this into 
the ectodermal vesicle, where they break up and change into blood- 
corpuscles. 

The anterior region of the body contains the very large rudiment 
of the central nervous system (Fig. 179 A, ”) and the anterior 

co 


F 


386 TUNICATA. 


portion of the lateral mesoderm-bands (ms) which also give off into 
the ectodermal vesicle from their posterior ends elements that change 
into blood-corpuscles. An ectodermal invagination can also be seen 
forming ventrally (p) and from this is derived the whole intestine 
of the ‘‘ nurse” form. This invagination first gives rise by its dilata- 
tion to the pharyngeal cavity (Fig. 179 B, p), while the intestine 
proper is derived from a solid cone of cells which develops at the 
base of the invagination. This cone very soon develops a lumen at 
first closed at both ends, and this becomes differentiated into the 
esophagus, the stomach and the intestine, the rudiment of the 
digestive gland also becoming visible. ‘The rudiment of the intestine 
opens only later into the atrial cavity (cl). The latter develops later 
than the pharyngeal cavity from an independent dorsal ectodermal 
invagination (Fig. 181, c/) which, as it enlarges, comes into close 
contact with the posterior wall of the pharynx. In this way the 
transverse and somewhat diagonally-placed branchial lamella arises, 
in which the four pairs of gill-clefts found in this generation (Fig.. 
245, p. 475) soon appear in the form of small round perforations. 
According to Unsanrn, the two pairs that lie dorsally develop before 
those that lie ventrally. 









um Maileri (after ULAsINi. 7. 
lion; 1d, branchial uerve. 


181, -Dersal region of an older lar 
atrium : 77, ciliated pit; 0, uuscle-ho« 





Only the middle part of the rudiment of the central nervous system 
(Fig. 181, 7) retains its original massive character, while the anterior 
and posterior ends soon become narrower In the anterior narrowed 
portion, an irregular cavity develops and breaks through into the 
pharyna. At this point, the ciliated pit (7) appears and a delicate 

connects it with the sub-ganglionic body (the homologue of 
‘ylanle hypophysaire” of the Ascidians). From the middle 
swelling of the neural rudiment, the actual ganglion and the sub- 
ganglionic body develop, while the posterior narrowed portion gives 
rise to an unpaired nerve which runs back wards (nernus branchialis, 9. 





DOLIOLUM—LARVAL DEVELOPMENT. 387 


Unsanty) in which we perhaps have the homologue of the ganglionic 
cell-strand discovered by van BeyepeN and Joan in the Ascidians 
(p. 376), ‘The peripheral nerves and the sensory organs develop 
later, and among these the vesicular auditory organ which belongs 
to the left side of the body deserves special mention (Fig. 245 A, ot); 
the vesicle itself urises as an ectodermal invagination into which a 
cell wanders and develops into the otolith. According to Unsantn, 
the auditory organ of Doliolum AMfilleri remains throughout life a 
mere cup-shaped ectodermal invagination, 


ae 








‘Pie. 182.— Transverse section through two outogenetic stages of Doliolum (after 
ULsantx). A, section through anterior ion of the body at a stage somewhat 
holder tan that depicted in Fig. 179 4; 2, section through an older stage.  d, 
Bester ee corer ee iach rotitents av tre hears ond pertains 
ya, mesoderm; max’, mesoderm of the ventral stolon; a, rudiment of the nervous 
system ; p, pharynx, 
The mesoderm of the anterior region of the body gives rise 

principally to the musele-hoops (Fig. 181, m), the pericardial rudi- 

ment (Fig. 182 B, hk) and the mesoderm-mass (ms’) of the ventral 
proliferating stolon of the “nurse” stage (the rosetie-skaped organ 
of Kerersrein and Exvers), Two cell-groups become separated 
posteriorly und ventrally from the mesoderm-layer which envelops 
the pharyngeal cavity like a mantle ; one of these, in close contact to 
the ectoderm, becomes the mesoderm of the ventral stolon (ms’), 
while the other, near the rudiment of the alimentary canal, changes 
into the pericardial vesicle (A), a cavity appearing within it round 
which the cells become arranged into an epithelium, As in other 
‘Tunicates, the heart is derived from a dorsal invagination of this 


388 TUNICATA. 


vesicle.* It should here be mentioned that the dorsal closure of the 
cardiac tube is brought about by a histologically differentiated lamella 
(the “ mittelfeld” of GRoBBEN) as to the development of which, how- 
ever, we have no detailed information, but we are reminded of the 
participation of the epicardial lamella in the formation of the heart 
in the Ascidians (vAN BENEDEN and Juuin, p. 370). 

The muscle-hoops develop in the way described by Leuckarr for 
Salpa democratica (see p. $31), through the fenestration of the meso- 
dermal lamella, these perforations separating one muscle-hoop from 
another. 

In this way, the general course of the most important systems of 
organs occurring in the first ‘‘nurse” generation is indicated (Figs. 
180, 243, 245, p. 475). To these, two stolons connected with the 
formation of buds have to be added. One of these (Figs. 180, r, and 
245 A, rs) lies behind the fifth muscle-hoop, close to the posterior 
end of the pericardial vesicle; this we shall call the ventral stolun 
(the rosette-shaped organ). The second or dorsal stolon (Figs. 180, d, 
245, ds) + arises from the dorsal surface in the seventh intermuscular 
space and forms a geniculate process pointed posteriorly, into the 
base of which an open coil of the seventh muscle-hoop extends (Fig. 
243, st’). We shall have to enter into the details of the structure 
and development of these stolons and of their relation to the forma- 
tion of the subsequent generations later (p. +70). 

After the young barrel-shaped ‘“ nurse” has developed fully, the 
provisional larval orgaus gradually atrophy. While the internal 
parts undergo futty degeneration and the cells become mixed with 
the blood, the ectodermal envelope yradually shortens so that the 
ectodermal vesicle and the larval tail soon form merely a rounded 
prominence on the body of the nurse”. This outgrowth strikingly 
resembles an embryonic organ consisting of reserve nutrition found 
in the Thaliacea, the so-called elaeoblast, a fact which makes the 
derivation of the latter from the transformed tail of the Ascidian 
larva, attempted by SALENSKy, appear somewhat probable (see below 
p. 432) : 

The first “nurse” generation of Doliolum, at a later period, as 
Fou first pointed ont, undergoes a remarkable metamorphosis, the 


*GRoBBEN’s statements as to the formation of the heart in the larval 
Doliolwm have been misunderstood and misrepresented by ULsanin. 

+ (This is better termed the dorsal outgrowth, as it does not itself give rise 
to buds, but receives those structures in rudiment from the ventral stolon and 
only gives attachment to them (pp. 472-476).—Eb.} 


PYROSOMA—EMBRYONIO DEVELOPMENT. 389 


gills, the endostyle and the whole of the alimentary canal degenerat- 
ing completely, while the muscle-hoops considerably increase in size, 
and the neryous system develops correspondingly. ‘The “nurse” 
then, like a swimming bell of a Siphonophoran stock, carries out the 
locomotory function, while the nutritive and respiratory functions 
of the whole stock are fulfilled by certain laterally- placed buds (tropho- 
avoids) on the dorsal outgrowth. 


4, Pyrosoma, | 


The development of Pyrosoma from the egy resembles in many 
respects that of the Thaliacea, Embryonic development takes place, 
as in them, within the body of the mother and is consequently direct 
or abbreviated. It even takes place, as at first in the Thaliacea, 
within the egg-follicle. Pyrosoma is, however, specially distinguished ; 
(1) by the large amount of food-yolk in the egg, which leads to a 
discoidal cleavage and the development of a germ-dise and (2) by 
the early asexual multiplication of the embryo, The primary indi- 
vidual which develops from the embryo and which has been called 
the Cyathorooil by Huxuery, at an early embryonic stage, gives rise 
by a kind of transverse fission to four more individuals, the first 
Ascidiozooids of the colony (Fig, 193, ete), 

We owe our knowledge of the embryonic development of Pyrosoma 
ebiefly to Huxney (No. 72), Kowanevsxy (No. 71), and SALeNsky 

N. 74). 


A. Cleavage and Formation of the Germ-Layers. 


Only a single egg matures in the genital rudiment of the Axscidio- 
zooid which has arisen through budding, as also is the case in the 
Thaliacea. Part of the remaining cell-material of the so-called genital 
strand becomes arranged round the egg as the follicle, while another 
part is used up in forming the rudiment of the testes and of the 
oviduct which appears as an outgrowth of the follicle. The egw 
wrows greatly by the addition of food-yolk, so that finally the forma- 
tive yolk and the germ-vesicle within it form «# mere prominence 
upon the large yolk-sphere (Fig. 183 A). After the oviduct has 
hecome connected with the atrial cavity, spermatozoa pass into it 
and remain in it until the egy is ready for fertilisation ile the 
oviduct partly degenerates, At the same time, an active immigra- 
tion of follicle-cells takes place into the space extending between 
the surface of the egg und the folliculur epithelium (Fig. 183 A, 2). 





| 


390 TUNICATA. 
These cells, which have been called by Kowangvsky inner follicular 
cells and by Sauensky kalymmocytes, aud as to the det of 


which from the follicle-cells there can be no doubt, are homol 
with the test-cells of the Ascidiaus and the inner follicle-cells of the 
Thaliacea (SALENSKY's gonoblasts). According to SauEnsiky, they 
take a certain part in the formation of the embryo here as in the 
Thaliacea, The statements on this subject, however, appear ty us 
somewhat inconclusive. 

An epithelial lamella further becomes separated from that part 
of the inner surface of the follicle which lies next the oviduct (Pig. 
184, ds); this covers the germ-dise like a cap und represents a 
secondary germ-envelope that takes no further part in the develop 
ment of the embryo, ‘This has been called by SaneNsky the cover 
ing layer. 





Fic. 183.—A, lateral aspect of the ogg of Pyrosonut, showing the first ane, 
the germ-line of Pyronoma at the sit-oellad stage, viewed. from eae eee eae 


LEVSKY), ft, inner follicle-cells. 


The cleavage of the egg of Pyrosoma, first made known through 
the investigations of Kowatevsky, is discoidal and recalls that of 
the Teleostei. The first stages seem to have a fairly regular course, 
the germ becoming divided into two, four and eight blastomeres by 
the successive appearance of meridional furrows (Fig. 36). ‘The stage 
of three blastomeres observed by SALENSKY and that of six found by 
Kowaueysky (Fig. 183 2) must be regarded as accidental 
larities. We have no further details as to the course of cleavage, 
but its result is a so-called morula-stage (Fig. 184 B) in whieh the 
yerm-prominence is composed of blastomeres apparently irregu 
arranged and already forming several layers. 

‘The numerous inner follicle-cells (kalymmocytes) wander by imeans of 


amoeboid movements into the spaces between the blastomeres 
and are even able to penetrate the cell-substance of the latter, 





- il 


PYROSOMA—CLEAVAGE OF THE EGG. 391 


bethe case, however, only in the first stages of cleavage and to have no further 
significance, since the follicle-cells, as it appears, do not remain inside the 
blastomeres. Many inner follicle-cells, as cleavage advances are, however, 
found scattered between the blastomeres (Fig. 184 2B, fe) and, as the distinc- 
jon of size between the two kinds of cells disappears when the blastomeres 
divide further, and the original histological character of the inner follicle-cells 
canalso no longer be recognised, it is finally impossible to distinguish the follicle- 
cells from the actual germ-cells or blastomeres. For this reason, and because 





Pie, 184. —Sections of two germ-dises of Pyrosoma (diagrammatic after SALENSKY), 
he aight celled stage ; B, older sage. 6, blastomeres ; do, food-yolk ; dx, covering 
layer ; dz, yolk-cells ; f, egg-follicle ; fs, immigrated follicle-cells ; ar, oviduct. ri 


Sanensky was unable to find follicle-cells showing the commencement of dis- 
integration, this author concluded that the inner follicle-cells take part in the 
formation of the embryo, a view resembling that held by him in connection 
with the Thaliacea (p. 420). We consider it to be more probable that the 
embryo here; as in the Thaliacea, is produced solely by the blastomeres, and 
that the follicle-cells which wander in between the blastomeres undergo final 
disintegration, [See footnotes, pp. 420 and 421}. 


392 TUNICATA. 


Mention must now be made of cells which, in the later stages of 
cleavage, are found in large numbers in the yolk, near the point at 
which the germ-dise lies on it, and which may be called yolk-cells 
(Fig. 184, dz). Sauensky, who traced back these cells to follicle- 
cells that had immigrated into the yolk, has named them the yolk- 
kalymmocyter. Since, however, as we shall see below (p. 395), these 
yolk-cells take part in the formation of the intestinal wall, we are 
inclined to regard them as blastomeres belonging to the entoderm-part 
of the germ-mass. We here have a repetition of the conditions found 
in the meroblastic egg of the Vertebrata, in which also volk-cells (to 
be considered as entoderm) are said to take a similar part in the 
formation of the intestinal gland-cells. 

For information as to the formation of the germ-layers in Pyrosoma 
we are dependent entirely on SaLeNsky's statements. The embryo, 
after a number of cell- 
divisions, lies on the yolk 
as & prominence composed 
of uniform polygonal cells 
which are irregularly distri- 
buted. This prominence 
soon becomes bilaterally 
symmetrical, the largest 
mass of cells collecting in 
the posterior half of the 
germ-dise, so that the pos- 

ities terior slope is more abrupt 
do foods te velkells than the anterior (Fig. 183). 
terior : r, anterior. According to SALENSKY, the 





separation of the germ-layers 
takes place throngh delunination, the most superficial cell-layer (er) 
first becoming arranged inte an cpithelium (ectoderm) ; the mass that 
remains (the meso-entoderm) then undergoes a similar transformation, 
the lowest layer, that in contact with the yolk, becoming separated 
as the intestinal epithelium (entoderm). Between the ectoderm and 
the entoderm the mesoderin extends, being greatly developed in the 
posterior half of the germ-dise while, in the anterior half, it is want- 
ing or elxe is represented merely by a few cells (Fig. 186.1 and &). 








Taking into account the process of formation of the germ-layers in the 
meroblastic eggs of the Vertebrata, we may perhaps be allowed to conjecture 
that in Pyrosoma also the separation of the germ-layers is not an actusl 
delamination, but an invagination or infolding of the posterior edge of the 
germ-dise, such as, for instanc ‘urs in the Selachians. 








= 


PYROSOMA—DEVELOPMENT OF THE CYATHOZOOID, 393, 


At the time when the separation of the germ-layers takes place 
three systems of cavities appear in the mesoderm (SaLENsKy) these 
being connected with invaginations on the lower (entodermal) surface 
of the germ-dise. One of these invaginations is rather large and lies 
near the posterior edge of the germ-dise (Fig. 185, ch), It is con- 
nected with a system of cavities ranning forward in the median line 
of the disc. The two other (paired) invaginations (Fig. 186 4, «) 





Fie. 186.—Two transverse sections through a young rin-dise of Pyrosome (after 
SabeNeky), A, through the posterior, and 4, through the anterior region. 6, coclom ; 
oh, cavity of the chordn ; ec, ectoderm ; en, entoderm ; ms, mesoderm ; u, nervous 
system. 

lie laterally and somewhat in front of the first and probably com- 
municate with the lateral system of cavities.* These are regarded 
hy Saensky as the rudiments of the coelomic sncs, and the axial 
system of cavities as the equivalent of the chorda, SabENsky was 
unable to decide whether there are here a number of separate spaces 
serjally arranged or a continuous, but somewhat bent longitudinal 
canal. 


B. Development of the Uyathozooid. 


The next changes to be noticed in the germ-lisc are the appearance 
of the rudiment of the nervous system of the Cyathozooid and the 
development of the peribranchial sacs. The nervous system arises as 
an ectodermal thickening in the anterior part of the germ-dise (Fig. 
187, n), which later becomes depressed us a furrow, and in this way 

* [Savensky figures the paired coelomic invaginations at an earlier stage 
than that shown in Fig. 186 A, and further he regards the depression seen on 


the right of the swelling containing ch as the coelomic invagination, and in 
his figure, of which the above is a copy, letters it as such.—Ep.] 





— 





394 TUNICATA. 


orms the vesicular rudiment of the ganglion. In enoss-seetions this 
anterior part of the germ-<disc is seen to be bilaminar (Fig. 186 2), 
as the mesoderm of the germ-dise does not extend so far forward, 





Fic, 187.— Two germ-dises of Pyrosoma (after Kowanevsky). ”, radi of the 
hervous system ; 0, aperture of one rats peribranchial tubes ; p, peribranchial 


cavity (tube). 
The two peribranchial sues or tubes appear as ectodermal invagina- 
tions (Fig. 187 4, p) directed from before backward, which seo 
lengthen (Fig. 187 /) and show, at the anterior end, the original 
aperture of invagination (9). 
The two anterior ends with 
their apertures unite in. 
front of the rudiment of 
the nervous system (x) 
(Kowaneysky), and thus 
give rise to the atrial 
aperture (Fig. 189, ef) of 
the Cyathozooid. Aceord= 
ing to Savensky, on the 
contrary, the latter is pro~ 
duced by an unpaired ecto 


dermal invagination with 
which the anterior ends of 





Fro, 188,—‘Trausverse sections through the germ- ; z 
\lise of Pyriwmn, ut the stage depicted in the peribranchial tubes 


Fig. 187 1 (after Sanensky), A, through the ii 
auterlor part of the disc, with théxudiment of °Ome into, contaay the | 


the nervons system ; 2, through the zladiaae original apertures of 
ity; 


withthe peribranchial snes, dh, enteric em 3 
ds, yolk-cells ; ec, ectoderm ; ev, entoderm; n, ttbes having closed 


rndimant of the nervous system ; », invagina- the formation of the 
tions of the peribranchial sacs. 
(SALENSKY), 





PYROSOMA—DEVELOPMENT OF THE CYATHOZOOID. 395. 


In the meantime the germ-dise has separated somewhat from the 
surface of the food-yolk (Fig. 188). The cavity thus formed is the enteric 
cavity, which originally appears covered by the entoderm (e) only on 
its upper surface. At a later stage the entoderm covers the whole of 


el 


pe 





Fra, 189.—Germ-dise of Pyrimona with the atrial otilice sleveloped (after Kowa- 
LBVSKY). cloaca ; en, endostyle ; x, nervous system ; p, peribrauchial tubes ; 
pe, pericardial snc ; pe’, the posterior tubular continustion of the same, 


the cavity, its lateral edges bending downward and growing towards 
one another (KowaLevsky). According to SaLensky, the yolk-cells 
also take part in this ventral closure of the enterie rudiment (Fig. ” 
188, dz) by coming to the surface of the food-yolk and changing into 





Pig, 190. —Transverse section through the eeaeinaat region a germ-ise at the stage 

apes in Fig. 189 (after Savenskr). ch, enteric envity ; ec, ectoderm ; en, entox 

A ef inet if the ‘erslontyle i Muay, meeodormn ; po, paribranchlal Gabo | pc; 
parla tube, 

‘epithelial cells of the entoderm (p. 392). While the enteric rudiment 

in this way becomes a tube closed on all sides (Fig. 190), a median 

Gnfolding, the rudiment of the endosty/e (es) becomes visible in the 


Posterior half of its upper wall. 





Mi 





396 TUNICATA. 


‘The transformations undergone, in the further course of develop- 
ment, by the paired coelomic snes, the lumina of which had become 












Fic. 191.—Three 
cavity ; 3, 1 
Py peribranchial t va 
connected posteriorly, are of importance, Only the rig] 
sac is retained (Fig. 191, re), while the left * undergoes di 
(ig, 191 4-C), its lumen becoming smaller and its cells Tos 


8 


-tlises of 1 diagrammatic (afer Sabey 
Samos fa ‘a it fei wa einen of the 
ial sae = ve, Tight enelomic sae, 





wo embryos of Myrosene (after KowaLeveky), 
il. em, endostyle-fol tern 5 
"ut tube; pr, per eee 
ith y dial aac ; 2, posterior part of thes germ: 
the surface of the egg (rudiment of the stalon); =, cell-some, 









"The terms " right” and “left refer to the arrangement of | 
‘the adult Cyathozovid, in which the atrial aperture denotes the | 
‘of the body. As, in our orientation of the germ-dise, the atrial | 
at the anterior edge of the disc, the right and left organs to 
Onur orientation of the germ-dise is, however, intentional (p. 404), 
apenas: in accordance with the views of authors, since ox 

id also lead to certain difficulties in describing the procosses (és 
jn connection with the development of the ‘Ascidionsnid), 





PYROSOMA—DEVELOPMENT OF THE CYATHOZOOID. 397 


epithelial continuity, so that finally, only a mass of irregularly 
arrange cells remains to take part in the formation of the mesenchyme 
which is developing in the primary body-cavity. A similar disin- 
tegration is undergone by the median strand which was regarded as 
the equivalent of the chorda, and which, after the disappearance of 
its lumen, retains its independence only for a short time, and is called 
by SALENSKY the axial mesoderm-strand, ‘The right coelomic sac 
gives rise to the pericardial rudiment (Figs. 192 C, 189, 190, po), 





thozooids with their tirst-formed buds (utter KoWALEVSKY, some- 
I straight stolon; 2, with curved stolon ; the Cyathozooid 
from the surface of the food-yolk (id), cf, atrial aperture ; , 
. rudiment of the endostyle ; 2, body-cavi ¢ Cyathozooid |p; 
vathozooi 









3 comme 
food-yolk ; 
peribranchial tubes; yc, perivardial sav of the 





which soon becomes club-sxhaped, a dilated, anterior, sac-like part 
changing into the pericardial vesicle of the Cyathozooid, while the 
tube that runs backward from this part does not develop further but 
soon loses its lumen : the connection of its cells then becomes loosened. 
It appears that these elements then mingle with the mesenchyme 
and assist in the formation of the mesoderm of the Ascidiozooid. In 
the pericardial sac of the Cyathozooid the surface adjacent to the 
intestinal wall is seen to thicken, this part then becoming invaginated 
and forming the rudiment of the heart proper. 




















body-cavity of the Cyathozooid (Fig. 193 B, 2). 
up into separate islands (Fig. 194, 2) which are 
visible near the surface of the food-yolk. Kowa 
the elements of this cell-zone took no further i 
of the embryo, or at the most changed into bloo 
‘SADENSKY axeribes to them a very important part 
of the mesoderm of the Ascidiozooid (see below, p 



































©, The Development of the Primary T 


The edge of the germ-dise, by continu 
the yolk-sphere (Figs. 193 B, 194), which 
merely by the follicular epithelium. The fo 
comes to lie inside the Cyathozooid, i.e, in 
part is taken in this circumerescence, howe 
of the elongated dise (Fig. 192 B, x), Tt 
vows out into a long sac-like appendage (Fig. 
by transverse furrows into four sections (1 
the tape-worm); these sections are ede 
Aseidiorovids. This chain of Ascidiozooids, 
stolon, and is evidently homologous with the m 
and Salpa, is originally straight, lying parallel to t 
of the Cyathozooid (Fig. 193 4). Later, howe 
it curves and finally lies equatorially (Figs, 194, 
the Ascidiozooids form a ring surrounding the 
Cyathozooid. The individual Ascidiozooids at t 
their positions ; at first they lay with their k 
same direction as that of the whole stolon (Fig. 
is a tendency for these axes to lie purallel to the pr 
Cyathozooid (Fig. 196). The stolon then, as a 
of zig-zags, as the thin, drawn ont trabeculae 
necting the individual Ascidiozooids lie obliquely, a: 
posterior end of one zooid to the anterior end of 


YROBOMA—THE PRIMARY TETRAZOOID COLONY. 399 


While the four Aastdioacias continue to increase in size and develop 
the structure of the adult individual (Figs. 194-196), the Cyathozooid 
whieh lies in the midst of them gradually utrophies (Fig. 196, ¢). 
Only now (Fig. 196 B) does the colony, which is enveloped in « large, 
common cellulose mantle, attain an independent existence. It passes 
out of the parental brood-sac into the cloaca of the colony, and thence 
to the exterior, The youngest free colonies of Pyrosoma are only 
found at considerable depths (Cuun), but older and larger stocks are 
met with at the surface of the water. 





Ftc, 194,—T'wo staze> in the development of the colony of /yrosum (after Kawa~ 
Levsky). In A, the yolk-mass (do) is partly surrounded by the Cyathozooid (¢), 
while, in B, it Hes entirely orth the body-cavity of the latter. ¢; Cynthozooid : 
el, atrial pore ot the Cyathozooid ; d, alimentary canal of the Cyathozooid ; do, 
io ; el, elacoblast ; en, endostyle of the Ascidiozooid ; 1, olllated 
snglion of ibe Cyaan: i, imhalent orifice of the Asoidiouoaid ; a, gill- 

oer ae of id ‘Cyathozooid ; m, cellulose mantle ; m, nervous system of 

MNORSSIA Pe ribranchial cavity ; sn, Interal nerve ; 0, eutodermal canal 

ee the Ascidiozooids with one another ; 2, remains of the cell-zone. 


The organ-rudiments of the young Ascidiozooid chain are, originally, 
direct continuations of the imperfectly developed organ in the Cyatho- 
woid (Figs. 192 8, 193). The ectoderm of the chain is in continuity 
with that of the germ-disc, The intestine of the Cyathozooid is 
continued into the enteric rudiment of the Ascidiozooid, and the 
endostyle-fold also proceeds direct from the rudiment of this fold in 
the germ-dise (Figs. 192,193,en). In a similar way the peribranchial 


400 TUNICATA, 


tubes (p) on either side of the intestine, and, on the right side of the 
body, the pericardial tube (Fig. 192, pc), are continued direct from 
the Cyathozooid into the chain of Ascidiozovids. The central nervous 
system, on the contrary, arises independently in the Ascidiozovids 
(SaLENsky). From this point the development of the Cyathozooid 
and that of the Ascidiozooids will be treated separately. 


D. Further Development of the Cyathozooid. 


The structure of the Cyathozooid is fairly simple. One of the poles 
of the body is marked by the presence of an ectodermal invagination, 
the atrial invagination (Fig. 193 B, 194, cl) which occupies the most 
anterior end of the germ-dise (Fig. 189, cl), and the origin of which 
has already been discussed (p. 394). This invagination originally 
communicates with the peribranchial tubes (Figs. 189, 192 B, 393 
A, p). Very soon, however, that part. of these tubes which lies in the 
Cyathozooid degenerates and completely disappears (Fig. 193 8). 
The atrial invagination, on the contrary, in which a narrow thick- 
walled portion can be distinguished later from a thin-walled portion, 
the actual cloaca, becomes connected with the alimentary canal of 
the Cyathozooid, the lamellae that separate the two cavities being 
perforated (Fig. 194). he alimentary canal (Fig. 194, d) of the 
Cyathozooid is a simple thin-walled sac, narrowed in the shape of 
a funnel posteriorly, which adopts a somewhat curved position in 
accordance with the curving of the stolon in later stages. — Its 
posterior, narrowed end passes over into the enteric rudiment of 
the Ascidiozooids. There is no sign of endostyle-folds in the intestine 
of the Cyathozooid, that part of the organ in which, in the germ-dise, 
the rudiments of these folds appeared (Fig. 189 ¢2) being nsed up 
in the formation of the Ascidiozooids (Fig. 193, e7). 

The rudiment of the nervous system of the Cyathozooid, whieh is 
derived from an ectodermal invagination lying close behind the atrial 
rudiment near the anterior margin of the germ-dise (Fig. 189, 1) is 
originally a somewhat long and completely closed vesicle which, when 
the alimentary canal changes its position, in consequence of the 
curvature of the stolon, also shifts from its original position. The 
posterior end of the neural vesicle now enters into open communica 
tion with the enteric cavity (Figs. 194 B, y, and 197). This is the 
rudiment of the ciliated pit (ff). The anterior part of the vesicle 
now becomes divided by a farrow from that part which is used for 
the formation of the ciliated pit: it swells and changes into the rudi- 















PYROSOMA—FURTHER DEVELOPMENT OF THE CYATHOZOOID, 401 


ment of the ganglion (y). This part gives off two lateral processes, 
the rudiments of the lateral nerves (sv) which clasp the enteric canal 
(d) laterally and end in the lower wall of the atrial invagination. 
Within the ganglionic rudiment of the Cyathozooid there is never any 
development of punctated nervous tissue (Punktsubstanz), 

The development of the 
heart has already been de- 
scribed (Fig. 193, pe). 

The cetoderm of the 
Cyathozooid yields the cel- 
lulose test of the young 
colony, The secretion of 
this layer begins even before 
the ciroumeresence of the 
yolk-sphere by the Cyatho- 
zooid is fully completed 
(Fig. 194 4, m). The area 
occupied by the Cyathozooid 
is then indicated by the 
extension of the cellulose 
mantle which, at a later 
period, encloses the four 
primary Ascidiozooids (Figs. 
194, 195). ‘The ectoderm 
of the Asoidiozooids does 
not, according to SALENsKy, 
take part in the formation 





. Fi, 195,—Later ontogenetic stage of a tetrazooid 
of the cellulose investment colony of Pyrosowa (after SaLensxy). The 


of the young colony, which mn calelies mantle Gf the thetheoaa kas 
is yielded exclusively by the grown round the Ascidiozooids. ci, atrial 
Cyathowoid. ‘The process ual en, euostle 1, inion? orice ES 
by which this mantle is gill-clefts ; m, mantle ; x, cell-lamellae of the 


cellulose mantle ; =, remains of the cell-rone, 
secreted agrees pretty 


closely with that described by Kowaxevsy for the Ascidiacea (p, 355), 
According to Sanansky, single mesoderm-cells (mesenchyme-cells), 
wandering through the ectoderm, come to lie on its external surface 
(Fig. 198, ms) and are the cells found later in the test. The secretion 
of the latter which now takes place proceeds from the ectoderm-cells 
(ec), each cell giving off externally a perpendicular plate-like process, so 
that the cellulose layer which is secreted seems broken up by these 


processes into separate prisms. At the same time, the mantle-cells 
DD 


ae 
















‘TUNICATA. 


(wandering mesoderm-eells) become arranged in a 
way in Pyresoma. ‘They form rows, which are note 
‘way as to produce hexagona] areas (Figs. 195, 1 pers 
later stages the processes of the ectoderm-cells 
test are again withdrawn. ‘The hexagonal p 
by the arrangement of the mesoderm-cells is, | 10 
some time. 





Fig, 196.—Two later ont 
KoWAaLevsky).  ¢, 


Boao oni 

, lnnguets ; +, youn! ive strand 
ery sand 4”, Gunectins versus Veerouaaae ene 
of the cell-zone. 


According to Sanensky, the ectoderm of = 
capable of secreting cellulose substance on its 
accounts for the fact that the ground sultans 
which fills a part of the primary body-cavity is 
the development of this -intermediate layer, 
becomes removed « considerable distance from 
Cyathozooid. 
The simplicity of structure of the Cyatho : 
we consider that its sole function is to give asi y 
four primary Ascidiozooids, As soon as these 


PYROSOMA—FURTHER DEVELOPMENT OF THE CYATHOZOOID, 403 


degree of development, the Cyathozooid begins gradually to degenerate, 
[t can then be seen as an oval body (Fig. 196, ¢) gradually decreasing 
in size, at the centre of the young tetrazooid colony. — Its atrial 


wperture (ef) closes, and it is gradually 
absorbed till not a trace of it is left. 
Kowavevsky thought that the atrial cavity 
of the Cyathozooid persisted as the common 
cloacal cavity of the whole colony; this, 
however, is in opposition to the above 
account by Sauensky. In accepting the 
latter account we must assume that the 
common cloacal cavity of the colony repre- 
sents a depression of the surface of the 
cellulose mantle which appears later. 

We have still briefly to describe the way 
in which the structure of the Cyathozooid 
is to be interpreted and to compare it with 
that of a typical Tunicate (Fig. 199), and 
in connection with this we must explain 
why, together with KowaLevsky and 
Savensky, we regard the ectodermal depres- 
sion in the Cyathozooid just mentioned as 
the atrial cavity (c). The fact that the 
peribranchial tubes open into this cavity is 
in favour of interpreting it in this way, and 
this view is still further confirmed by the 
system with relation to this invagination. 





Big). d, Ge ne 
sea sole 
a 


position of the nervous 
If it is to be regarded as 


the inhalent aperture, the ciliated pit (/l) of the central nervous 


system would have to 
be directed towards it, 
but this is not the 
case. The ciliated pit 
forms the part of the 
central nervous system 





(g) which is turned Fic, 198.—Transverse section through the developing 
test of the Cyathozooid in the stage depicted in ns 


away from the invagi- 195 (after SateNsKY), 


¢, cellulose substance ; eo, ecto- 


nation. Acomparison — derm; ms, mesenchyme-cells ; ma’, mesenehyme-cells 


of a diagram illustrat- 


forming hexagonal pattern in test (of. Fig. 196). 


ing the relative positions of the most important organs in the body 
of a solitary Salp (Fig. 199 #) with a diagram of a Cyathozooid 


ie 














one representing the intestinal tube, the — 
consecutive individuals, and the two lateral 
tubes (p). These tubes are originally 

ions of the corresponding org: 
192 B). When, at a later period, 


PYROSOMA—THE FOUR PRIMARY ASCIDIOZOOIDS. 405 


become more markedly constricted from one another, these rud 
ments also are cut up into sections corresponding to the different 
individuals. The peribranchial tubes become completely dissevered 
at the boundaries of the individuals (Fig. 193 2), each Ascidiozooid 
then containing a pair of lateral closed sacs, the peribranchial cavities 
(p). The remains of the peribranchial tubes in the Cyathozooid, as 
already mentioned (p. 400) then atrophy. The enteric rudiment, 
however, does not at first undergo such complete constriction 
between the individual Ascidiozooids, but a canal is retained in the 
connecting trabeculae which establishes communication between the 
consecutive individuals (Fig. 194 B, »). This canal does not dis- 
integrate until. the Ascidiozooids separate completely on attaining 
their full development. A vestige of it plays an important part in 
‘the later development of buds, changing into the so-called endostyle- 
process or entoderm-process of the stolou (SEEDIGER, p. 486). 

The rudiment of the endostyle-furrow was recognisable in the 
primary enteric rudiment of the Cyathozooid even before the chain 
of Ascidiozooids began to form (Figs. 189, 190, en). That part of 
the alimentary canal of the Cyathozooid which was distinguished by 
the presence of the endostyle-rudiment was the ‘part which, by 
lengthening, changed into the common enteric rudiment of the 
four primary Ascidiozooids, Consequently, the endostyle-rudiment 
originally runs through all the four Ascidiozooids (Fig. 193, en). At 
‘a later stage, however, only the posterior part of it is retained in each 
individual (Figs. 194, en, 200, es), becoming the definitive endostyle 
of the zooid, In cross-section, the endostyle-rudiment originally has 
the form of a broad fold projecting into the lumen of the intestine 
(Fig. 203 A), the lateral part of which shows epithelial thickenings 
which, in a surface view, appear as dark bands. The depression 
between them flattens out later, but, on either side, the paired 
endostyle-folds project inwards (Fig, 203 B, es). It is not yet 
clearly understood in what way these lateral endostyle-folds together 
with the middle part yield the endostyle of the adult. 

Tn front of the anterior end of the endostyle-rudiment there is, in 
the developing Ascidiozooid, a pit-like ectodermal depression (Figs. 
194, 200, #), the rudiment of the inhalent or branchial aperture. 
‘The space in front of this is occupied by the rudiment of the central 
nervous system (Figs. 194, 200, n). 

The lateral walls of the branchial sac of the Ascidiozooid are in 
contact with the peribranchial tubes (Fig. 193, p). Here the gill-slite 
(ks) break through (Fig. 200), a small entodermal outgrowth fusing 


a 


406 TUNICATA, 


on either side with the wall of the peribranchial sacs, and the 
perforation then taking place in the base of the outgrowth. The 
entodermal lamella thus takes a more active part in the development 
of the gill-slits than does the ectodermal wall of the peribranchial 
sac, The vertical bars between the adjacent gill-slits whieh, in 
cross-section, are almost quadrangular, are not merely covered on 
their inner surfaces with entoderm, but their lateral surfaces also 
which are turned towards the slits belong to the entoderm. Only 
the covering of the external surface is derived from the ectodermal 





Fic, 200,—Diagramumatic views of an Ascidiozooid at the depicted in Fig. 1% | 
(iollowing SaukNsky). 4A, viewed from above; B, from I thy i | 
x (branchial sae) ; éd, rectum ; el elaeoblast ; ia rudiment of is 
pha at inhalent ot branchial aperture; ‘ka,’ gill-slits ; stomach ; #, 

oe, oesophagus ; p, peribranchial sacs; pe, vesicle; me, 


7 
rudiment of the lateral nerves. 


wall of the peribranchial cavities, The gill-slits in Pyrosoma, acoorl- 

ing to SALENSKY, appear in order from before backward, the most 

anterior slit forming first. After the gill-slits have broken through, | 

they very soon lengthen ; those of Pyrosoma, indeed, are distinguished 

for their length. The internal longitudinal bars, which cross the 

slits at right angles and give rise to the characteristic latticelike 

appearance of the branchial wall, develop later as independent in- 

growths from the vertical bars which become secondarily connected. 
The gill-slits, as Servicer has pointed out, seem always to lie 

at right angles to the endostyle (Fig, 201, 4s and ¢s), Since the 

endostyle of the Ascidiozooids originally runs horizontally, as may 

be seen in the diagram Fig. 201 4, and then later adopts a vertical 

position (Fig. 201 C) the gill-slits pass gradually from a vertical t9 | 


PYROSOMA—THE FOUR PRIMARY ASCIDIOZOOIDS, 407 


an oblique position and finally lie horizontally. This leads us to the 
general changes of form which characterise the development of the 
Ascidiozooid, The longitudinal axis of the adult Ascidiozooid (Fig, 
201 C) seems to be marked by the branchial and atrial apertures (i) ; 
in the bud, however, these two apertures do not lie at the ends 





! 4 
Fig, 201,—Three consecutive ontogenetic stages of two Ascidiozoolds, side view, 
diagrammatic (following Saumnsky). cl, atrium; @, alimentary canal; ¢, atrial 
apertnre; ¢s, endostyle ; i, branchial aperture ; ks, gill-clefts; m, nervous system ; 
p, peribranchial cavity. 
of the longitudinal axis (Fig, 201 4). This shows that through the 
changes brought about by growth during the course of development, 
the longitudinal axis of the bud is replaced by a new one running 
at right angles to it. The longitudinal axis of the young Ascidio- 
zovid, the two poles of which are represented by trabeculae join- 
ing one Ascidiozooid to another becomes, later, the transverse axis of 


i 


PYROSOMA—THE FOUR PRIMARY ASIDIOZOOIDS, 409 


cavity. The rudiment of the stomach and intestine is found on the 
lower surface of the entoderm-tube in the form of a blind horseshoe- 
shaped diverticulum (Fig. 200 B) closely bent upon itself, the free 
ends being directed anteriorly, The two limbs of the horseshoe are 
seen cut through in the cross-section given in Fig. 204 (o¢ and ed), 
One limb (ed) of this rudiment separates early from the entoderm-sac 
and, as a blind diverticulum, represents the rudiment of the intestine, 
while the other gives rise to the stomach and oesophagus. The com- 
munication between this latter limb and the pharyngeal cavity is re- 
tained as the entrance to the oesophagus (oe). Only in later stages 
does the blind end of the intestine become connected with the atrial 
cavity and the alimentary canal attains complete development with 
the appearance of the so-called digestive gland, 





The central nervous system arises in the most anterior region of 
the Ascidiogooid as an ectodermal invagination (Fig. 202, n) on the 
upper surface of the body, which soon becomes separated from the 
ectoderm as an elongate closed vesicle. This, at a later stage, becomes 
triangular (Fig. 200, n). The anterior part * of this vesicle forms the 
rudiment of the ganglion proper principally by a growth of its upper 
wall. From this region, two lateral hollow processes arise (Fig 200, 
mm) which, at a later period, grow and embrace the sides of the ali- 
mentary canal. These are the rudiments of the lateral nerves which 
thus arise here in a way similar to that described by SeenicER for 
the later buds of Pyrovoma, The narrowed portion of the neural 
rudiment whieh is directed towards the branchial aperture becomes 
connected with the ectoderm of the alimentary canal, and, by a per- 


ce in relation to the long axis of the bud, posterior in the adult.— 
























ia clotoeaa cae nella ane ; 
a bn OEM EE eee 
| which is to some extent derived from inner 
but for the greater part from elements of the disit 
sac, is the principal source of the whole of th 
diozooids, It must indeed be pointed out tl 


as x prolongation of the pericardial rudiment 
breaking up into separate cells, may also co 









Ascidiozooids in the cell-zone which, in its tu 
from the elements of the disintegrated left co 
gration of the mesoderm into the germ-stock ( 
zooids) takes place first in the form of an 
cell-masses, Later, when the cell-zone has b 
islands, detached cell-groups or single elen 
hody-cavity of the Ascidiozooids. 
The mesodermal elements become distribute 
cavity of the Ascidiozooids. Two groups of the 
up a definite position in the posterior region of 
side of the body, and their elements are found 


AN 


PYROSOMA—THE FOUR PRIMARY ASCIDIOZOOIDS. 


411 


layers, the external layer (Fig. 203 A, e/) being the rudiment of the 
elacoblast, and the inner that of the so-ealled pericardial strands, 
which must not be confounded with the pericardial tube mentioned 
above, an organ that disappears at an early stage (Fig. 203 A, pe and 
pe’). The cells of the elacoblast-rudiment soon increase in size and 


form a rather high eylindrical 
epithelium. At a later stage, 
they are less regular in their 
arrangement, vacuolesdevelop 
within them and they change 
into large elements, resem- 
bling vegetable parenchyma- 
cells, and thus assume the 
features characteristic of the 
elacoblast-tissue (Fig. 203 C/). 
The elacoblast is here at first 
paired and consists of rounded 
groups of cells lying in the 
posterior part of the body 
which cause the surface of 
the body to bulge out some- 
what (Figs. 194 and 200 ed). 

The inner layer of the 
paired mesodermal rudiment 
just described gives rise to 
two cell-strands which develop 
differently (Fig. 203, pe, pc’). 
The strand to the right 
extends somewhat further 
forward than the other, and 
its anterior end becomes 
transformed into a closed 
vesicle, the pericardial vesicle 
(Fig. 203 # and C, pe). The 
heart develops through the 
thickening of that wall of the 
vesicle which is in contact 





Fic, 203.—Transverse sections through the 
distal region of an Ascidiozooid of 
in three consecutive stages of development 


(after Sacessky), 
ment of elaeoblast; en, entoderm; es, paired 
endostyle-folds; g, genital strand ; pc, right 
pericardial strand, or pericardial vesicle ; 
pe, left pericardial strand. 


ec, ectoderm ; el, rudi- 


with the alimentary canal and its invagination into the vesicle, 
The heart consequently forms here in the same way as in all other 


Tunicates. 


The right pericardial strand (Fig. 203, ye) is not completely used 


i 


a 


412 TUNICATA. 


up in the formation of the pericardial vesicle, but is continued pos- 
teriorly. This mesodermal strand and the corresponding strand of 
the left side (the so-called left pericardial strand, Fig. 203, pe’) do 
not for the present develop further, but at a later stage, when the 
Ascidiozooid has become independent and prepares to give rise to 
fresh buds, these strands pass over into the proliferating stolon which is 
developing and, on either side of the endostyle-process (entoderm-tube) 
that is also continued into the stolon, form the mesoderm-rudiment 
of the latter structure (SALENSKY), According to SALENSEY, there- 
fore, the paired pericardial strands of the Ascidiozooid give rise, on 
the right, to the pericardial vesicle of the Ascidiozooid, ancl, in their 
further course, to the to mesoderm-strands of the proliferating stolen 
(p. 486). 

By the development of the peribranchial sacs and the above-men- 
tioned mesoderm-formation in the lateral parts of the embryo, the 
primary body-cavity is divided into two longitudinal sinuses, ont 
above and the other below the alimentary canal (Fig. 203), called by 
SALENsKy the supra-intestinal and the sub-intestinal blood-vinuses 
In the region of the sub-intestinal sinus the mesenchyme-cells collect 
(Fig. 203 4, g) and unite to form the genital strand belonging to the 
posterior region of the Ascidiozooid. In later stages, according to 
SALENSKY, a lumen appears in this strand (Fig. 203 €, g), = 
which the cells become arranged 
like an epithelium, but the lumen 
disappears again in the course of 
further development. The genital 
strand not only represents the 
genital rudiment of the Ascidio- 
zooid in which it appears, but gives 
rise to the genital strand of the 
proliferating stolon of this zooid, 
as will be described later (p. 484), 
The rise of the genital organs in 
the first four Ascidiozooids has 7 - 
recently been deseribed in detail beter earn est Boose 
by SeRLIgER (No. 76a). As it — SpeGNeeth ai 
resembles that of the corresponding hee 
organs in the zooids that develop branebial ca > 
later we must refer the reader to 
the description given on p. 493, merely adding here hanya 
first four Ascidiozooids, the ovary degenerates, It was well-known te 





PYROSOMA—THE FOUR PRIMARY ASCIDIOZOOIDS. 413 


KowAatevsky that the small Pyrosoma colonies contained only male 
zooids, females being found in the large colonies, 

Auteriorly the supra-intestinal blood-sinus surrounds the rudiment 
of the central nervous system, Further back it is continued into the 
furrow which seems to be formed by the infolding of the endostyle- 
rudiment. Since, between the nervous system and the endostyle- 
rudiment the branchial aperture occurs, the stream of blood would 
be interrupted but for a peculiar adaptation for conducting it further, 
the upper wall of the intestine becoming folded in at this point 
somewhat in the manner of a typhlosole (Figs. 204, 205, dh), This 
fold within which the blood now rans becomes completely separated 
from the dorsal wall of 
the intestine, and then 
forms a tube ranning 
freely through the intes- 
tine from the neural 
rudiment (Fig. 205, n) 
to the beginning of the 
endostyle - furrow (en), 
This peculiar structure, 
which has been called 
by Sanensky the pha- 
bps greene P26. — Longa tion Shrvagh ay Asc 

yy Huxney the diapha- of Pyrosomne MALENSKY). db, diapha- 
ryngeal band, may be Sansui apeciers snp stomach? “ei spl De 
compared with che gil mutt orn se eno oop 
of the Thaliacea with 

which SALENSKY even homologises it, although topographically it is 
clearly only an analogous structure. The diapharyngeal band is 
merely a provisional adaptation which atrophies in the further 
course of development. 

‘Two structures, the significance of which is obscure, the clongate and the 
lenticular cell-masses (Kerersteix and Extmrs) are to be traced back to the 
mésoderm. The lenticular masses are paired and symmetrical accumulations 
‘of cells lying at the entrance to the branchial sac between the wall of the 
peribranchial cavities and the entoderm (Figs. 196, 1, and 106, lm, p). 
Sauenskr considers that they are to be derived from the kalymmocytes 
{inner follicle-cells), They are said to be phosphorescent organs, The 
elongate masses, which lie on the neural side “near the gills in the blood- 
sinus,” form later from an unpaired accumulation of mesoderm-cells which 
originally lies below the so-called languets of the entoderm (Figs. 196, d, 
106, cm). 





Mi 





THE HEMIMYARIA (SALPIDAE). 416 


points, such as the cleavage, the formation of the germ-layers and the 
development of the placenta, the recorded investigations are ineom- 
plete and contradictory, and we have statements which we must 
hesitate to accept because they are at variance with all that is known 
of the development of other Tunicates (and of animals in general). 
Tm our account we shall have these difficulties to contend with 
and must restrict ourselves to giving a brief survey of what at the 
present time seems to be fairly well established. We cannot enter 
upon the many contradictory uud obsenre points in connection with 
this subject. 

Among the Sadpidae, the sexual individuals (the forms belonging 
to the chain) are hermaphrodite, but the time of maturation of the 
male and female products differs. The individuals of the young 
chain set free from the stolon of the “nurse” generation (solitary 





FiG, 206,—Side-view of democraticu-mucronata (combined after con a 
‘SALENSKY), a a) es trial aperture ; end, eudostyle ; 


band ; i, brand ‘gill; n, nerv ion} niu, Hud! 
en -folllele) ; gare cavity 


ov, (conslating of a 
the oviduct. 

form) are at first female; they are fertilised by the individuals of 

another chain, and each develops one embryo, Only as this develops, 

do the testes become functional. 

The Salpidae, as a rule, develop only one egg, The whole ovary 
(Fig. 206, ov) consists, in such cases, of a single follicle which con- 
tains the egg and is connected with the epithelium of the atrial 
cavity * by a strand-like oviduct in which two portions can be dis- 













% nperture of 


"(Owing to the peculiar relations existing between the pharynx and the 
ssi scanty fn Salva, i it becomes extremely difficult to do their limits ; 
ratory Eoertanite (Athemhdhle) in commonly loosely applied to the 
Aree chamber. We have, however, thought it za isable to d: 
and to use in its stead the more specific terms atrial cavity anc 
8 cavity in those cases in which we were able to determine the 
‘of the general cavity which was being referred to.—Ep.] 


i 


| 


416 TUNICATA. 


tinguished (Fig. 207). One of these (st) is directly connected with 
the follicle and consists of a single row of cells (the so-called stalk 


of 
narrowed 





of the follicle) and the other is a dilated efferent portion (od), with 
a distinct lumen. The egg-follicle lies at the base and to the right 


ll 





THE HEMIMYARIA (SALPIDAE). 417 


of the nucleus near the oesophagus (Fig. 206) and is surrounded by 
ramifications of the circumvisceral network of blood-vessels. The 
oviduct also appears to be accompanied until near its aperture by 
a vascular network (Fig. 207 B, 4). The point at which the oviduct 
opens (Fig. 206, x) is found on the right side of the body behind the 
penultimate musele-hoop above the nucleus. Round the aperture, 
the epithelinm of the atrial cavity is thickened into a shield (Fig. 
207 A, ep) and projects slightly inward (Fig. 207 B, ep). This 
swelling is the rudiment of the epithelial prominence of SALENSKY 
which Toparo calls the uterus. 


The question now arises whether the members of a Salpa-chain, after the 
birth of the mature embryo, remain sterile or are able to produce a new ovary 
which may yield a new embryo, Some of Savunsky’s observations seem to 
favour the latter yiew. The individuals composing a chain grow consider- 
ably in size while the embryo is developing within them, so that the largest 
individual contains the most advanced embryo, Savensky, in such a large 
individual, found the remains of a placenta, 
which indicated the previous expulsion of 
an embryo and, side by side with this, « 
mature egg or a quite young embryo. 

Exceptions to the rule that each individual 
of a chain produces only one embryo are 
found in Salpa zonaria (Ouasisso and Escu- 
micut), S. Thilesii (Known) and S. heragona 
(Travstept), in which several embryos 
develop simultaneously, although they are 
not all at the same stage of development, 
In consequence of this and of the presence 
of a special point of attachment for each 
embryo, Lxuckarr (No. 98) concluded that 
several egg-follicles with distinct ducts must 
bé present, These forms have recently been 
united to form the genus Jasis (LAnILLE, 
No. 38), the above feature being one of its 
yeneric characters. 

In many of the Saipidae (S. maxima, 8. 
pinnata, 8. punctata) the, follicle appears to < 
he incompletely divided by a longitudinal ~omal 
Seem Oy) inisstwo chambers, one waaoiais euien eee 
of which (the ovarian sac, ov) contains the, which this Cnt 
egg during the stages of its maturation, while 
the other (the embryonic sac, em) receives it 
during the first embryonic stages. In many 
forms (¢.7., S. maxima) the embryonic sac is 
continued into a pointed process (s) which 
soon degenerates. The remains of this process, in later stages, whew | 

RR 








—— 








416 TUNICATA. 


tinguished (Fig. 207). One of these (st) is direetly connected with 
the follicle and consists of a single row of cells (the so-called stalk 









Fro, 207.—Female genital apparatus, .t, of Salpa pinata (after 
‘Saipa wirgula (after Toano}. a, epithelium lintng 


ipa vingula ( ( an 

nt animal; 0, blood-sinus; ¢, egg-cell ; em, embryonic chamber; 
Tromivenoe 7 fllicle; m, aparfure of the oviduct oj distal diladale i 
oviduct ; ov, ovarian chamber; a, process of the pote ‘ehaunber 5 
part of the oviduct (so-called stalk of the follicle). 


of the follicle) and the other is a dilated efferent portion (od), with 
The egg-follicle lies at the base and to the right 


a distinct lumen. 


<li 








THE HEMIMYARIA (SALPIDAE). 417 


of the nucleus near the oesophagus (Fig. 206) and is surrounded by 
ramifications of the circumvisceral network of blood-vessels. The 
oviduct also appears to be accompanied until near its aperture by 
a vascular network (Fig. 207 B, 4). The point at which the oviduct 
opens (Fig. 206, ») is found on the right side of the body behind the 
penultimate muscle-hoop above the nucleus, Round the aperture, 
the epithelium of the atrial cavity is thickened into a shield (Fig. 
207 A, ¢p) wnd projects slightly inward (Fig. 207 B, ep). This 
swelling is the rudiment of the eptthelial prominence of SALENSKY 
which Toparo calls the uterus. 


The question now arises whether the members of a Salpa-chain, after the 
birth of the mature embryo, remain sterile or are able to produce a new ovary 
which may yield a new embryo, Some of Satensky’s observations seem to 
favour the latter view. The individuals composing a chain grow consider- 
ably in size while the embryo ix developing within them, so that the largest 
individual contains the most advanced embryo. Savensky, in such a large 
individual, found the remains of a placenta 
which indicated the previous expulsion of 
an embryo and, side by side with this, « 
mature egg or a quite young embryo, 

Exceptions to the rule that each individual 
of a chain produces only one embryo are 
found in Salpa zonaria (Camisso and Escu- 
ricut), S, Thilesii (Kroax) and 8. heragona 
(Travstep?), in which several embryos 
develop simultaneously, although they are 
not all at the same stage of development. 
In consequence of this and of the presence 
of a special point of attachment for each 
embryo, Levckarr (No. 98) concluded that 
several egg-follicles with distinct ducts must 
be present. These forms have recently been 
united to form the genus Jasis (Lanmux, 
No, 38), the above feature being one of its 
generic characters. 

Tn many of the Salpidae (S. maxima, 5. 
pinnata, 8. punctata) the follicle appears to 
be incompletely divided by a longitudinal je 999 Dorsal aspect of Sal 
furrow (Fig. 207 8), into two chambers, one bicaudata (' ). @, point 
of which (the ovarian sac, ov) contains the aia Sea oie 
egg during the stages of its maturation, while {Cane idin  ateial sere 
the other (the embryonic sac, em) receives it end, endostyle ; /, periphar- 
during the first embryonic stages. In many _YPSeal band; g, genital tubs; 

M +, branchial aperture ; &, gill; 
forms (¢.g., 3. maxima) the embryonic sac is nm, nerve-ganglion ; wi, nuolews. 
eontinwed into a pointed process (s) which 
soon degenerates. The remains of this process, in later stages, when the 

EE 





418 TUNICATA. 


embryonic sac, in consequence of the shortening of the oviduct, shifts towards 
the epithelial prominence, serves for attaching the sac to the epithelium. 
The development of the female genital apparatus of Salpa (Pegea) bicaw- 
data ix quite exceptional. Here (Fig. 208) at about the middle of the body 
of the individual of the chain, at the right side, there is an outgrowth of the 
body-wall with a somewhat curved end (genital tubv, g. SaLExsKy. No. 10H. 








sin the development of Sipe bicandata (after SALBSSKY). 1 
ined figure 3 SKY), the embryo ¢ still lies at the hase of the 
T ovi In B; the embryo, at a more advance! 

ae «c, wall of the respite: 





















forming 1 . umbilical cont 
venbryn and the placenta): ¢ embryo in the dilated ovituct 
xenital fold ; 7, ciliated pit: y, genital tube: 






erture of the > mit, Mantle; 4, net 


2 pe perivardinn ; sf, stolon. 
The lumen of this tube communicates with the atrial cavity (Fig. 209 4). 
The short oviduct opens fur back in the base of this tube between two epithelial 
folds projecting into the lumen of the genital tube (incubatory folds, f. Iv 
spite of this peculiar arrangement, which must be regarded as a modification 
of the part of the atrial wall surrounding the aperture of the oviduct, it seem= 


THE HEMIMYARIA (SALPIDAE)—CLEAVAGE. 419 


(SaLENsKY) that the embryonic development of Salpa bicaudata does not, in 
essentials, diverge greatly from that of other forms. The greater the increane 
in size of the embryo and of the placenta which has attached itself at the base 
of the tube, the shorter does the tube become. The embryo finally passes into 
the atrial cavity of the parent through the opening of the tube (Fig. 209 B). 


The first change in the genital apparatus which precedes the 
fertilisation of the egg, occurs in quite young Salps, in the act of 
detaching themselves from the stolon of the “nurse” or just after 
detachment. It consists of a continuous shortening of the oviduct, 
especially affecting the part that has been described as the stalk of 
the follicle, the cells of which shift towards each other in such a way 
that they soon form several layers, while a lumen appears, so that 





Fig. 210. —Two aegonetie stages of Supa pinnate (ufter SALENSKY). In uf, the 
embryo consists of four blastomeres, two of which are cut through in the 

is of a larger number of blastomeres and of numerous smaller cells, kz, 
tt, blood-sinus ; ¢, epithelial prominence ; ¢, moditied part of the 

K's ectoderm-gerin) ;,/A, enveloping fold ; fin, follicle- 

wlls, kalymmocytes ; £2, smaller celle of the embryo 

(SALENSK Y's, qenlantay ¢ », shortened oviduct. 

























the oviduct is now hollow throughout its whole length. During this 
abbreviation of the oviduct (Fig. 210) the egg, together with the 
follicle, shifts continually nearer the aperture of the duct, the process 
suggesting that seen in the descent of the mammalian testes. 

Through the now open oviduct the spermatozoa obtain access to 
the follicle, and fertilisation takes place. According to Toparo (No. 
112), the spermatozoon enters the egg and the male pronucleus 
develops after the expulsion of the first polar body and before the 
development of the second. 

Cleavage is total (Figs. 210 4,211 A and B). Egys have been 
observed divided into two and into four and also in the later stages 


FF 


420 'TUNICATA, 


of cleavage; we are, however, fur from having obtained a clear 
insight into the details of the process. In individual cases, cleay- 
age seems to be unequal, Sanensky figured the embryo of Salpa 
mucronata in the four-celled stage consisting of four equal blasto- 
meres, but both he and Toparo observed an inequality of the 
blastomeres in S. pinnata and 8. punctata at this stage. [Judging 
from recent investigations (Nos. XIII. and XXIa,), unequal segmenta- 
tion is the rule rather than the exception in Sa/pa-] 

‘The processes of cleavage are here specially difficult to follow in 
detail because of the cells which become detached from the wall 
of the follicle and become applied to the embrydénie mass (Fig. 210 4, 
fs), and even wander in between the blastomeres; these cells are 
known as the follicle-cells or kalymmocytes. This immigration of 
cells, which we may compare to the test-cells of the Ascidiacen (jp. 336) 
and the inner follicle-cells of Pyrosome (p. 390), is so profuse that 
the blastomeres at the later stages of cleavage seem actually enveloped 
in them (Fig, 210 B), appearing to be embedded in u matrix of 
gonoblasts (as SALENSKY terms them, No. 104), Topano, who was the 
first to notice this multiplication and immigration of the follicle-cells 
(Nos. 108 and 109), described them as yolk-cells (cel/ulew lMcitiches) 
and holds that they serve for the nourishment of the embryo which 
forms from the blastomeres. ‘Uhey are said to undergo granular dis- 
integration, to be taken in and assimilated by the blastomeres, and, 
finally, to disappear altogether. Sanensky (No. 104), on the contrary. 
sees in these cells the actual constituent elements of the future 
embryo and therefore calls them gonoblasts.* According to him, 
the large blastomeres, the protoplasm of which soon bevomes divided 
up in a peculiar way, do not subdivide further and are, in general, 
incapable of any special further development, They are said finally 


* (The recent and exhaustive investigations made by Brooxs 
Heer (No, XIII), Konornerr (Nos. XVIUL-XXIc.), and 
XXIV.), prove undoubtedly that Sanmysky was in error when he 
a formative role to the kalymmocytes, since, however much these 
differ from one another in detail, they were all that the 
embryo are eventually wholly formed from the the v 
majority being that. the Bais aD ao play an entirely passive rile 
development of the embryo, being merely nutritive structures. 

The account given in the following is largely based upon § 
work on the development of Sapa. Unfortunately, the conclus 
at by this observer have, in many cases besides the one n i 
not confirmed by subsequent investigators, This renders out 
incomplete and, in some particulars, inaccurate, so that the 
well to consult the original monographs of Hmrpen, Konorxerr m 
‘We have, however, endeavoured, in footnotes, to draw attention to | 


serious error.—Ep.) 












THE HEMIMYARIA (SALPIDAE)—CLEAVAGE, 421 


to disintegrate, while the embryo is built up by the gonoblasts which 
form the greater part of all the later rudiments of organs. SALENSKY, 
therefore, considers the embryonic development of the Sa/pidae as 
4 process intermediate between the development of an egg and 
budding, beginning with a regular cleavage, but the resultant blaste- 
meres play no further part in the development, the embryo being 
for the greater part built up out of derivatives of the egg-follicle. 
SALENsKyY consequently describes the embryonic development of the 
Salps as follicular tudding. A priori, SauEnsky’s view as to the 
part taken by the follicle cells in the embryonic development of the 
Salpidae must be regarded us extremely improbable ; it is also by no 
means proved by what SALENSKY says of the decisive stages. We 
must therefore for the present accept Topano’s views as the more 
probable. * 


We have already seen (p. 390) that Savensky also ascribes a considerable 
part in the building up of the embryo of Pyrosoma to the immigrated follicle- 
cells or kalymmocytos, and he has recently attributed to these cells a share 
in the development of the cellulose mantle of Distaplia (No. 49, see also 
p- 357). 


The shortening of the oviduct mentioned above (Fig. 210) is not 
due merely to the dilation of its lumen and the consequent shifting 
of the cells of its wall, but is also directly connected with the immigra- 
tion of cells already described. In this way, a large amount of cell- 
material is given off by the wall of the oviduct and the follicle to the 
embryo. In its abbreviated condition, the oviduct forms a short wide 
chamber (Fig. 211 A) communicating with the follicle through a 
harrow aperture which, however, soon widens. The two cavities 
finally unite to form a single capsule, the lumen of which is almost 


{According to Brooks and Mrtcany (Nos. I. and XXIV.) these kalym- 
mocytes first block out the embryonic tissues and organs, but are eventually 

blastomeres, after which the former degenerate and probably serve 
a5 food-material for the latter cells. Even at an early stage Taivacidovied 
degenerate and their nuclei migrate into the large blastomeres, forming the 
so-called Si bgt Hetper (No. XIII.), while agreeing that the kalym- 
mooytes are taken up by the blastomeres, thinks that the entire cell, not merely 
its nucleus, enters the protoplasm of the latter, Korornerr (Nos. XXa. and 
XXIa.), however, regards the masses seen in the blastomeres as true yolk- 
masses and not degenerating kalymmocytes. The last two observers regard 
the latter cells as playing « passive rdle in the development and do not agree 
with Baoox’s view that the embryonic organs are blocked out in kalymmocytes. 
According to these two authors, the embryo is made up of Jarge and small 
blastomeres und kalymmocytes, the small blastomeres being indistinguish- 
able from the latter and hence, they suppose, Brooxs’ and SALENSsKY's error 
arose, the cells which the latter took to be kalymmocytes being in reality 
small blastomeres.—Ep,} 


| ae 


—7 


422 TUNICATA. 


completely filled by the embryo (Fig. 211 8). The wall of this 
capsule, which is produced by the union of the oviduet and the 
follicle is from this time called (although not very accurately) the 
Solticular epithelium. 

During the aboye changes, the shield-like thickening of the epi- 
thelium round the aperture of the oviduct has risen up more and 
more, and now forms a mound-like swelling (epithelial prominence, 
Fig. 210, e, 211, a) projecting into the posterior portion of the atrial 
cavity. As the oviduct continues to shorten, the follicle, with the 
embryo, is brought into ever closer proximity to this prominence and 
finally passes into it. At later stages, the prominence becomes con- 
stricted at its base (Fig. 213), remaining connected with the wall of 
the atrial cavity only by a thin stalk. ‘The embryo now, enclosed in 
a kind of brood-sac, projects into the interior of the atrial cavity. 


a B 









e 

aller Saueneaeh 
In A, the embryo undergoing cleavage still lies in the atte tn 
embryo has need into the cavity of the oviduct (O ‘The follicular ‘tai > 
i ¢ placenta, a later 
uinence = outer lamella of the broods 

cof the bmood-sac 5 S Ciicila SS = 

7 JF blastomeres ; 5, immigrated follicle-cells (not represented tn A 


The wall of this brood-suc, which, as we shall see, is merely proe- 
visional, is double. The external wall (Fig. 211 C, a) is a modified 
portion of the epithelium of the atrial cavity, and, in the inner wall 
(Fig. 211 C, 4) we recognise the follicular epithelium. It appears 
that, in this stage, the opening of the oviduct into the atrial cavity 
has completely closed. 

After cleavage has ended, the embryo forms a solid, rounded body 
composed of numerous cells which, according to SALENSKY, are 
mostly derived from the follicular epithelium, but, to 
Topano, have been produced by fission from the blastomeres, We 
shall for the present adopt the latter view as the more 


lll 


* [See editorial note, p. 421). 





SALPIDAE—FORMS WITHOUT COVERING FOLDS. 423 


According to Toparo, the cells derived from the follicle-epithelinm 
which are fated to disintegrate, can still be distinguished between 
these embryonic cells, It should, indeed, be mentioned that 
SaLENsKY was able to find within the embryo, long after cleavage 
had ended, at a time when the first rudiments of organs grow dis- 
tinet, a few large blastomeres definitely arranged. The significance of 
these is obscure, and we are altogether in the dark as to those stages 
in the development of Salpa which lie between cleavage and the be- 
ginning of the formation of the organs, i.¢, the stages in which we 
should expect the germ-layers toform.* ‘The cleavage-cavity appears 
to be wanting in all Salpidae [Savensky, Heer and Korotnerr]. 
Brooks, however, suggests that the follicular cavity may be thus 
interpreted. 

Certain divergencies ave found in the different species of Sadpa in 
the further processes of development, but these apparently are not 
due to any fundamental difference. The development of most: species 
being as yet only very partially known, we shall restrict ourselves to 
# closer account of the two forms which haye been best investigated, 
viz., 8. democratica-mucronata and 8. pinnata. These represent two 
types of development which are to be distinguished by the absence 
or presence of a covering fold and by the stracture of the placenta.+ 











A. Forms without Covering Folds. 


The embryo of Salpa (Thalia) democratica-mucronata, in the stages 
that mark the completion of the cleavage-processes (Fig. 211 C) pro- 
jects in the form of a cone into the atrial cavity of the parent. It 
lengthens later and becomes more cylindrical, its end being rounded 
(Fig. 212 B). It is still surrounded by the two walls of the brood- 


*(Recent investigations tend to show that germ-layers, as we understand 
them in other animals, cannot be said to exist in Salpa, since the various 
ls, which give rise to the different organs, appear to be mixed in an 
way throughout the germ-mass. Gradually, however, certain of the 
blastomeres take up definite positions, and, from what is known of their sub- 
sequent history, can now be definitely stated to give rise to certain tissues. 
‘The first of these rudiments to be yh ee is the ectoderm ; this takes the 
form of certain large blastomeres which migrate to the surface tee the 
laconta and there give rise to the ectoderm and its derivatives. Other large 
Eiimomeres which remain nearer the placenta have been found to give rise to 
* the entoderm and possibly some erm; the latter layer, however, appears 
to arise largely from the smaller blastomeres which, with the kalymmocytes, 
make up the main mass of the germ.—Ep.) 
+(Konorserr (No. XVIIL) expresses grave doubts as to the advisability of 
Oe can be no doubt from recent invest tions saat 
development ferences between these two divisions have n tly 
‘exnggerated.—Ep.} bo 


— x 








SALPIDAE—FORMS WITHOUT COVERING FOLDS. 4265 


It appears that the inner lamella of the brood-sac is very soon 
reduced (Fig. 212 2) and completely degenerates. This degeneration 
at first affects a zone running obliquely round the embryo, leaving 
only a cap of the lamella covering the anterior end of the embryo and 
a posterior cup-like portion connected with the rudiment of the 
placenta, which completely unites with the latter at a subsequent 
period ; the anterior cap appears soon to disintegrate. The embryo 
is then covered by only one envelope, the outer lamella of the brood- 
mac (a). 


The above is in accordance with SALENSKY'S earlier description of the fate 
of the inner lamella (No. 100). The more recent statements of this author 
suggest that the inner lamella does not disintegrate, but enters into close con- 
nection with the embryo, finally changing into the ectoderm of the latter. 
The ectoderm in S. democratica-mucronata would then have to be traced 
back to the transformed epithelium of the oviduct, a view which is a priori 
improbable, and less in accordance with our own investigations than the older 
statements. [The ectoderm, like the other embryonic organs, is now generally 
regarded as arising from the blastomeres. See footnote, p. 424, aud KoRoTNEFY 
(No, XVIII.) on S. democratica.) 


In the next stage (Fig. 212 2) important differentiations are evident 
in the embryo. The mesoderm (m) has appeared between the ecto- 
derm and the entoderm in the form of a cell-accumulation, which 
spreads out like a germ-layer to right and left over the sides of the 
embryo, The central nervous system (n) is algo found as a cell- 
growth proceeding from the ectoderm. Its position marks the plane 
of symmetry and the anterior end of the body in the embryo.* 
Diametrically opposite to it is another cell-accumulation (/), which 
SALENSKY also traces back to the ectoderm, and which seems to be 
the first rudiment of the elaeoblast. That part of the ectoderm which 
is in contact with the rudiment of the placenta is already distinguished 
by the large size and the height of its cells (x). This is the rudiment 
of the lunella, which takes part in the formation of the epithelium 
covering the placenta. 

The fundamental features of the organisation of the embryo of 
Salpa, which are thus already sketched out, appear still more dis- 
tinctly in the following stage (Fig. 213), in consequence of the 
development of a system of cavities. The inuer cell-mass severs 


* [Kororsrrr believes that the nervous system ix formed as a closed vesicle, 
which lies at first quite independently in the mesoderm without any relation 
w the ectoderm or to the pharynx. The elacoblast also arises from the 
cinbryonic blastomeres and not from follicular cells, ax SALENSKY stated — 
Ep.) 





THE HBMIMYARIA (SALPIDAE)—OCLEAVAGE, 421 


to disintegrate, while the embryo is built up by the gonoblasts which 
form the greater part of all the later rudiments of organs. SaLENSKY, 
therefore, considers the embryonic development of the Salpidae as 
#& process intermediate between the development of an egg and 
budding, beginning with a regular cleavage, but the resultant blasto- 
meres play no further part in the development, the embryo being 
for the greater part built up out of derivatives of the egg-follicle. 
SaLEnsky consequently describes the embryonic development of the 
Sulps as follicular budding, <A priori, Saumnsky's view us to the 
part taken by the follicle cells in the embryonic development of the 
Salpidae must be regarded us extremely improbable ; it is also by no 
means proved by what SALENSKY says of the decisive stages. We 
must therefore for the preseut accept Topano’s views us the more 
probable * 


We have already seen (p. 390) that Sacensky also ascribes a considerable 
part in the building up of the embryo of Pyrosoma to the immigrated follicle- 
cells or kalymmocytes, and he has recently attributed to these cells a share 
in the development of the cellulose mantle of Distaplia (No. 49, see also 
p. 357). 


The shortening of the oviduct mentioned above (Fig, 210) is not 
due merely to the dilation of its lumen and the consequent shifting 
of the cells of its wall, but is also directly connected with the immigra- 
tion of cells already described. In this way, « large amount of cell- 
material is given off by the wall of the oviduct and the follicle to the 
embryo. Iu its abbreviated condition, the oviduct forms a short wide 
chamber (Fig. 211 A) communicating with the follicle through « 
harrow aperture which, however, soon widens. The two cavities 
finally unite to form a single capsule, the lumen of which is almost 


* (According to Brooxs and Mrcacy (Nos. I. and XXIV.) these kalym- 
mocytes first block out the embryonic tissues and organs, but are eventually 
replaced by blastomeres, after which the former degenerate and probably serve 
Lneey oat the latter cells. ere a ye stage Mets coy 

and their nuclei migrate into the large blastomeres, forming the 
so-called yolk-particles. Hen (No. XITI.), while agreeing that the vl: 
mocytes are taken up by the blastomeres, thinks that the entire cell, not merely 
its nucleus, enters the protoplasm of the latter. Kororxnry (Nos. XXa. and 
XXIa.), however, regards the masses seen in the blastomeres as true yolk- 
masses and not de erating kalymmocytes. The last two observers regard 
the latter cells as playing « passive rdle in the development and do not agree 
with Buoor’s view that the embryonic organs are blocked out in kalymmocytes, 

to these two authors, the embryo is made up of large and small 
blastomeres und kalymmocytes, the small blastomeres being indistinguish- 
able from the latter and hence, they suppose, Brooks’ and SaLensxky's error 
arose, the cells which the latter took to be kalymmocytes being in reality 
small blastomeres.— Ep, | 


SALPIDAR—FORMS WITHOUT COVERING FOLDS. 423 


According to Toparo, the cells derived from the follicle-epithelium 
which are fated to disintegrate, can still be distinguished between 
these embryonic cells. It should, indeed, be mentioned that 
Sauensky was able to find within the embryo, long after cleavage 
had ended, at a time when the first rudiments of organs grow dis- 
tinct, a few large blastomeres definitely arranged. ‘The significance of 
these is obscure, and we are altogether in the dark as to those stages 
in the development of Sadpa which lie between cleavage and the be- 
ginning of the formation of the organs, i. the stages in which we 
should expect the germ-layers to form.* The cleavage-cavity appears 
to be wanting in all Salpidae [Savensky, Herper and KororNerr]. 
Brooks, however, suggests that the follicular cavity may be thus 
interpreted. 

Certain divergencies are found in the different species of Sa/pa in 
the further processes of development, but these apparently are not 
due to any fundamental difference. The development of most species 
being as yet only very partially known, we shall restrict. ourselves to 
a closer account of the two forms which have been best investigated, 
viz., 8. democratica-mueronata and S. pinnata. These represent two 
types of development which are to be distinguished by the absence 
or presence of a covering fold and by the structure of the placenta.+ 


A. Forms without Covering Folds. 


The embryo of Salpa (Thalia) democratica-neucronata, in the stages 
that mark the completion of the cleavage-provesses (Fig. 211 C) pro- 
jects in the form of a cone into the atrial cavity of the parent. It 
lengthens later and becomes more cylindrical, its end being rounded 
(Fig. 212 4). It is still surrounded by the two walls of the brood- 


*[Recent investigations tend to show that germ-layers, as we understand 
them in other animals, cannot be said to exist in Salpa, since the various 
-cells, which give rise to the different organs, appear to be mixed in an 
irregular way throughout the germ-mass. Gradually, however, certain of the 
blastomeres take up definite positions, and, from what is known of their sub- 
sequent history, can now be definitely stated to give rise to certain tissues, 
‘The first of these rudiments to be ised is the ectoderm; this takes the 
form of certain large blastomeres which migrate to the surface oppocite the 
lacenta and there give rise to the ectoderm and its derivatives. Other large 
jlastomeres which remain nearer the placenta have been found to give rise vo 
* the entoderm and possibly some waestenn ; the latter layer, however, appears 
to arise largely from the smaller blastomeres which, with the kalymmocytes, 
make up the main mass of the germ.—Ep.)} 
+[Konorserr (No. XVILI.) expresses grave doubts as to thé advisability of 
this subdivision, and there can no doubt from recent investigations that 
the developmental differences between these two divisions have Sse greatly 
exaggerated.—Ep.] 


SALPIDAB—FORMS WITHOUT COVERING FOLDS. 495 


It appears that the inner lamella of the brood-sac is very soom 
reduced (Fig. 212 2) and completely degenerates. This degeneration 
at first affects a zone running obliquely round the embryo, leaving 
only a cap of the lamella covering the anterior end of the embryo and 
a posterior cup-like portion connected with the rudiment of the 
placenta, which completely unites with the latter at a subsequent 
period ; the anterior cap appears soon to disintegrate. The embryo 
is then covered by only one envelope, the outer lamella of the brood- 
sno (a). 


The above is in accordance with SaLexsky's earlier description of the fate 
of the inner lamella (No. 100), The more recent statements of this author 
suggest that the inner lamella does not disintegrate, but enters into close con- 
nection with the embryo, finally changing into the ectoderm of the latter. 
‘The ectoderm in S. democratica-mucronata would then have to be traced 
back to the transformed epithelium of the oviduct, a view which is a priori 
improbable, and less in accordance with our own investigations than the older 
statements. [The ectoderm, like the other embryonic organs, is now generally 
regarded as arising from the blastomeres. See footnote, p, 424, aud Konorserr 
(No. XVITL) on S. democratica.) 


In the next stage (Fig. 212 8) important differentiations are evident 
in the embryo. The mesoderm (m) has appeared between the ecto- 
derm and the entoderm in the form of a cell-accumulation, which 
spreads out like a germ-layer to right and left over the sides of the 
embryo. The central nervous system (n) is also found as a cell- 
growth proceeding from the ectoderm. [ts position marks the plane 
of symmetry and the anterior end of the body in the embryo.* 
Diumetrically opposite to it is another cell-accumulation (/), which 
SavENsky also traces back to the ectoderm, and which seems to be 
the first rudiment of the elaeoblast. ‘That part of the ectoderm which 
is in contact with the rudiment of the placenta is already distinguished 
by the large size and the height of its cells (x), This is the rudiment 
of the lamella, which takes part in the formation of the epithelium 
covering the placenta, 

The fundamental features of the organisation of the embryo of 
Salpa, which are thus already sketched out, appear still more dis- 
tinetly in the following stage (Fig, 213), in consequence of the 
development of a system of cavities, The inner cell-mass severs 


*(Konorserr belioves that the nervous system is formed as a closed vesicle, 
whieh lies at first quite independently in the mesoderm without any relation 
to the ectoderm or to the pharynx. The elacoblast also arises ‘from the 
embryonic blastomeres ard not from follicular cells, as SALeNsKy stated.— 


SALPIDAE—FORMS WITHOUT COVERING FOLDS, 427 


a tube, the inner cells being transformed into blood-corpuscles which 
pass into the blood. 

Before passing on to describe the other changes that take place in 
the embryo we must dwell for a moment on the degeneration of the 
brood-sac and the development of the placenta, After the inner 
lamella of the brood-sae has degenerated as described above, the 
embryo remains surrounded solely by the very thin epithelium of the 
outer lamella (Fig. 212 8, a), which consists of a differentiated part 
of the atrial epithelium of the parent. This outer lamella is unable 
to keep pace with the further increase in size of the embryo ; it 
becomes ruptured at the point at which the aperture of the oviduct 
was originally situated and shrinks downwards over the embryo (Fig. 
213). In consequence of this contraction of the outer lamella the 
embryo, which originally lay in the follicle (Fig. 211 4), and then 
shifted forward into the dilated oviduct (Fig. 211 4), protrudes 
into the atrial cavity of the parent, in which from this time it lies 
freely. - 

We have already seen (p, 424) that a compact cell-mass is attached 
to the lower surface of the embryo (Fig. 212, p); this, which 
represents the first rudiment of the placenta, is derived from the 
transformed cell-material of the egg-follicle. The outer lamella of the 
brood-sac now shrinks completely back over this cell-mass, and finally, 
as a constricted funnel-like annulus, surrounds and strengthens the 
connection between the rudiment of the placenta and the parent (Fig. 
214, a), The placenta-rudiment would lie exposed, after the with- 
drawal of the outer lamella, were it not covered by « thin ectodermal 
layer of the embryo (Fig. 214, ee), which develops as the brood-sac 
‘is withdrawn. Through this cireumerescence of the placenta by an 
ectodermal lamella, which was not observed by Sauensky, but of 
which we were able clearly to convince ourselves, the placenta is 
incorporated in the embryo and then appears enclosed in a capsule 
derived from the ectoderm of the embryo, The lateral walls of this 
capsule are formed by the thin lamella just mentioned ; its upper 
wall or the so-called roof (Fig. 213, ¢), on the contrary, is yielded by 
the thick ectoderm-layer, the origin of which was traced above (p. 425), 
[This is of follicular origin according to Konornerr (No. XXe.).] On 
its under side the ectodermal capsule of the placenta possesses an 
aperture through which the placental cavity communicates with the 
blood-vascular system of the parent. The placental cavity arises in 
the form of gaps or clefts in the placental tissue, which thus assumes 
a loose structure. Some of the cells of this originally compact tissue 


latin 


SALPIDAE—FORMS WITHOUT COVERING FOLDS. 429 


the brvod-sac which can still be recognised for some time as x kind 
of corpus luteum. The embryo, at birth, passes out through the 
atrial aperture of the parent. 

The development of the final shape of the body goes hand in hand 
with the development of the placenta. The embryo at first formed 
4 cone projecting into the atrial cavity of the mother (Fig. 212), its 
principal axis corresponding to the future dorso-ventral axis, It now 
lengthens at right angles to this axis, é.¢., in accordance with its 
future longitudinal axis (Fig. 214). It soon becomes cylindrical and, 
after the cellulose mantle has developed, resembles a tetragonal prism. 
The mantle-substance develops in just the same way as in the 
Ascidians (p. ). It arises on the outer surface of the ectoderm 
aga secretion into which single cells soon wander. Finally, the two 
conical processes characteristic of Salpa democratica (solitary form) 
develop (Fig. 262, p. 495). 

The nervous system has been seen to arise as a solid ingrowth of 
the ectoderm.* ‘This soon severs its connection with the latter, a 
cavity develops within it, and it becomes a vesicle characterised by 
its size and the thickness of its walls (Fig. 214, »). KowALEvsky 
(No. 96) was aware of the fact that this vesicle lengthens later and 
is indistinctly divided by constrictions into three consecutive parts 
which show a certain resemblance to the primary cercbral vesicles 
of the vertebrate embryo (Fig. 214 8B, n). The anterior vesicle 
becomes closely connected anteriorly with the adjacent wall of the 
pharynx, and this connection which is at first solid soon develops 
a lumen which puts the neural cavity into communication with the 
pharyngeal cavity. The canal thus formed is the first rudiment of 
the future ciliated pit (Fig. 216, 4). While this organ develops 
further, the walls of the ganglionic vesicle thicken, it shortens, its 
lumen disappears and the vesicular rudiment thus gradually assumes 
the character of the definitive ganglion of the adult. A conical 
process rising on the dorsal side of the ganglion on which three 
accumulations of pigment appear represents the rudiment of the 
eye, 





Further details as to the development of the eye have recently been pub- 
lished by Mercanr (No. 99) and Biirscuti (No. 94).+ ‘The eyes seem to develop 
differently, not only in the different species but also in the solitary and the 
colonial forms of the same species. According to Bé-Tacutt, the simplest form 


* [See footnote, p. 425.—En.] 


t[See also Mxrcan® in Brooks’ Monograph (No. I.), and 
No. 94a).—Ep.] 





a 


430 TUNICATA. 


of eye is a mound-like swelling of the brain (Fig, 215 4); at the sides of this 
swelling are arranged the pigment-cells while, from the centre, closely packed 
rod-bearing cells are found radiating 

towards the surface, the nerve-fibres A r 
being connected with the inner ends of 

the rods. In this eye, the rods are 

therefore turned directly towards the P 
source of light, In other forms, the 
rudiment of the eye becomes differenti- 

ated into three parts which either remain 

united in the shape of a horse-shoe, or 

form three entirely distinct eyes, the 
unpaired median eye retaining the B 
original simple condition (Fig. 216 B, «) 

while the two latetal eyes are formed 

on the plan of an inverse eye (b), i.c., the 

rods are directed away from the surface 

and the nerve-fibres are connected with 

their outer ends, Bérscrur, assuming 

an optic vesicle which cannot be observed, 
homologised the median non-inverted 

eye with the cephalic eye of the Verte- Ft oe iteeens eee 
brates, and the lateral inverted eyes with single eye; J, typical 

the paired eyes of the Vertebrates, but, ts niet yi 6 a 
independent of this theoretical vesicle, iagthent-eclie sy title y 
the structure of the lateral eye of the 

Ascidian larva seems directly to suggest the paired vertebrate eyes by thr 
fact that the rods are directed towards the cerebral cavity (see, however, the 
objections raised by Metcary, No, a, and Gérrxnt, No, 94a). 


‘The first rudiment of the pharynx and the development of the gill 
have already been described (p. 426). The wall of the pharyngeal 
cavity is formed by a simple epithelium, the cells are either eubieal 
or somewhat flattened. The rudiment of the endostyle (hypobranehial 
furrow) appears in the form of paired folds of this epithelium origin 
ating at some distance from each other (Fig. 216, es); these shift 
towards one another later and then form the boundaries of # hypo- 
branchial furrow which runs from the peripharyngeal bands to near 
the entrance of the oesophagus. The rudiments of the 
bands which ran towards the anterior end of the gill from the anterior 
end of the endostyle, encircling the aperture of the respiratory cavity, 
first appear as similar prominences. ‘The rudiments of the branchial 
and atrial apertures (Fig. 216, i and ¢) appear only in later stages 
in the form of transverse depressions of the ectoderm which break 
through into the pharynx and atrial cavities, ‘The rudiment of the 
atrial aperture originally lies almost at the centre of the dorsal side 


~ 


_— 


SALPIDAE—FOKMS WITHOUT COVERING FOLDS. 431 


of the body (Fig. 216), but later, as the part of the body known as the 
nucleus decreases in size, it shifts further back. 

The radiment of the alimentary canal, in the strict sense of the 
term (Fig. 214 4, d), originally forms a posteriorly directed diverti- 
culum of the pharynx, This caecum becomes divided later by two 
folds rising into it from below into three spaces (Fig. 216, oe, m, ed), 
the anterior space being the rudiment of the oesophagus, while the 
posterior space represents the intestine. The middle spuce is the 
rudiment. of the stomach-caecum. The intestine curves upward 


fio, 216,—Later embryonic stage of Safpa democrution-mucronata (aftr SALENSKY). 
¢, atrial aperture ; ¢, elavol 1, intestine ; ex, ondosty! , ciliated pit; 


Trauchial (oral) apertuice ; gill; m, stomnach-eaecunt ; #, ganglion | v7, oesophh fag: 
2 per rial sac; pol, placenta ; xf, stolon; f, so-called ‘root of the placenta (basal 





towards the left, till its blind end comes into contact with the 
atrial wall, perforation leading later to the formation of the anal 
aperture. 

Tt has been shown that the mesoderm (Fig. 213 B, ms) spreads out 
over the right and left sides of the embryo in the form of two lamellae 
ju close contact with the entoderm. These lamellae, according to 
Levoxart, yield the ruscle-hoops, a kind of fenestration taking place 
in the lamellae and separating the mesoderm-bands which correspond 
to the different hoops. The transversely striated contractile substance 
develops later in the muscles. The heart also, according to SALENSKY, 


432 TUNICATA. 


owes its origin to the mesoderm, i.¢., to the lamella lying on the 
right side of the body, which is continued back over the posterior end 
of the wall of the branchial cavity, and there forms a vesicle (Fig. 
216, p) in which we recognise the first rudiment of the pericardial 
vesicle.* A swelling of the thickened dorsal wall of the vesicle. 
which projects into its lumen, and which, though at first solid 
becomes hollow later, is the rudiment of the heart proper; this con- 
sequently develops in just the same way as in the Ascidiacea (p. 370). 
The blood-vessels apparently arise as spaces within the gelatinous 
connective-tissue which, in later stages, fills the primary body-cavity. 
It should be mentioned that, in the Salpidae, as Toparo has pointed 
out and figured, the blood-vessels seem to be lined throughout with 
w cellular intima (Fig. 207 3B, 4). In this respect this group 
would seem to differ from the Ascidiacea, in which, according to 
van BENEDEN and Junin, such an intima is wanting (qf. pp. 363 
and 371). 

The elaeoblast (Fig. 216, eb), the rudiment of which has already 
been described (p. 425), attains its full development only in the later 
stages of embryonic life, and, after the birth of the embryo, under- 
yoes gradual degeneration [by phagocytosis, according to KoroTNEFF 
(No, XIX.)]. It is a mass of large polygonal cells, which are filled 
with reserve nutrition. The remarkable resemblance between the 
claeoblast and the degenerating larval tail of Doliolum (p. 388) caused 
SALENSKY to assume that this problematical organ is the homologue 
of the tail and the chorda of the Ascidian larva. But the presence 
of the rudiment of the claeoblast, as we shall see in the buds of the 
Nalpidae and of Pyrosoma, is not very favourable to this view. 
Physiologically, the elacoblast is probably, as Leuckart suggests. 
aqeservoir of food-material, which is gradually used up as the 
embryo develops. 

At a later stage of development the rudiment of the stolon can 
be seen (Fig. 216, st). This consists first of a diverticulum of the 
pharyngeal wall lying at the posterior end of the endostyle, and is 
turned toward the left side of the body. The ectoderm soon bulges 
over this entodermal diverticulum. The space between the two 
layers is, according to SEELIGER (No. 105), filled with mesenchyme: 
cells, the short conical stolon thus consisting of three germ-layer 
(p. 495). 





* According to Konorserr (No. XVIIL), the pericardium arises as in other 
Tunicates as a diverticulum of the pharynx.—F: 





8ALPIDAE—FORMS WITH COVERING FOLDS, 433 


B. Forms with Covering Folds. 


The development of the forms belonging to this type (5. (Cyclosapa) 
pinnata, 8, africana-macima, S. runcinata-fusiformis, S. prunetata) 
differs in many essential points from that of S. democratica-mucronata_ 
The principal distinction consists in the presence in the former of an 
external covering which after the degeneration of the primary brood- 
sac (present also in WS. democratica-mucronata), forms a secondary sac 
investing the embryo, and in the peculiar development of the placenta, 
The development of the organs also appears to follow another type. 
The forms just mentioned seem to agree fairly well in their develop- 
ment, which has been studied by many soologists, especially by 





Fra, 217.—Two ontogenctlo stages of Salpe pinnate (after Saueveny) forming 


sequence to Fig. 210 8. }, blastomeres ; bk, ‘* blood-forming bud"; Af, blogd- 

cavities in the ta; BY, median hlood-sinus’; of, roof of the placenta (tusal late) = 

¢, lower part of the epithelial prominence, known {ater as the placental membrane s 

#, upper part of the epithelial prominence (SALENSKY's ectoderm-gerin) ; /, follicular 

cavity ; fA, covering fold ; fiw, follicle-wall. 

Topako, Barrors and Savensxy, and more recently by Brooks 
(No, I.), Herpzr (No, XIII.), and Korotyerr (Nos. XX., XXa., 
and XXIa.). The following account relates chiefly to 8, pinata, a 
comparatively well-known form, 

Starting with the embryonic development of S. pinnata at the 
stage depicted in Fig, 217 A, we find conditions in fairly close agree- 
ment with those described in connection with 8, democratiea. The 
embryo consists of large and of small cells. ‘The protoplasm of the 
large cells (6) breaks up in a peculiar way into polygonal portions 





* (See footnote, p.423 and p, 445,—Eb.] 
FF 










aA 


‘The embryo lies in a sac (Fig. 217 A, fw) 
union of the follicle and the dilated oviduct. 
been deseribed in 8. demoeratica-mueronata 
brood-sac. At the posterior end of this sac a 
in the forms now under consideration ; this 
distinet. (Fig. 217 2, 4h), and is to be traced | 
wall of the follicle. While, in S. demoe 
ing forms the rudiment for the whole of the p 






























the embryo?). This part has been called by 
(bottone ematogene, Figs. 217 B, and 218, bk). 
The embryo almost entirely fills the cavity 
217, /). On one side, it appears to be 
lamella of the sac. According to SALENSKY, 
later haemal side of the body, so that we are. 
to orient the embryo. [According to Bi 
contrary, marks the middle dorsal line of the | 
The outer lamella of the brond-sas (Fig: 3 
from the thickened part of the atrial epitheliu 
is pushed out into the atrium by the growth o 
it, and which is called by SAnENsKY the epitl 
‘Two parts can soon be distinguished in it. ' 
covers the greater part of the embryo, co 
cells, while the lower part (e) is composed 
This latter yields later the lateral walls of the p 
Ep ay ee ee that the embry 


sists of two kinds of Blastomores 4. Tang nd 
appearance indistinguishable from the ke 


SALPIDAE—FORMS8 WITH COVERING FOLDS. 435 


by Topaxo the placental membrane or germoblastica [the supporting 
ring of the placenta (Brooxs)]. 

A differentiation somewhat resembling that just deseribed in the 
outer lamella is also found in the inner lamella (splanchnic layer of 
the follicle) which represents the transformed epithelium of the ovi- 
duct and follicle. The lower half of the lamella (Fig, 217 2, @), in 
this case, becomes connected with the thickened epithelium of the 
atrial cavity known as the placental membrane or supporting ring 
of the placenta (e), and forms the roof of the placenta (Fig. 218 A, dp), 
in the centre of which the ‘ blood-bud ” is attached. The placenta 
is thus hollow, its lateral walls (supporting ring, Fig. 218 A, mp) 
being yielded by the epithelial prominence of the atrium, and its 
roof (dp) by the inner lamella of the brood-sac, “e., by the follicle 
(placental portion of the follicle). The “ blood-bud” (#4) hangs 
from the roof into the cayity which is part of one of the blood- 
channels of the parent. SALENsKyY distinguishes in this cavity two 
communicating sinuses, au afferent and an efferent sinus, and, be- 
tween these two, a third vascular space round the “‘ blood-bud ” (Fig. 
217 A, 41), the relations and significance of which are unknown. 

The placenta, which, from the first, is a greatly swollen structure, 
now becomes constricted at its base (Fig. 218), and thus forms a 
stalked structure on the upper surface of which the embryo rests. 
Tt becomes saddle-shaped later, the parts lying at the sides of the 
embryo growing upward. This is why, in a horizontal section (Fig. 
219) only the lateral parts of the placenta (p) are seen cut through, 
The actual relations of this organ are still very obseure. 

While, in this way, the primary brood-sac undergves essential 
alteration, a circular fold of the atrial epithelium grows up from 
the base of the epithelial prominence (Figs. 210 B, and 217, fh) 
and completely overgrows the placenta and the embryo (Fig. 218, /), 
and thus forms a new secondary brood-sac (embryo-sac) such as is 
not found in 8. democratica-mucronata, ‘This is known as the cover- 
ing fold or amnion. It continues to grow upwards as a circular fold 
round the embryo, over which, however, it never fuses, but remains 
Separated by a variable aperture through which the embryo eventu- 
ally passes out into the atrium. 


There are, in the different species, characteristic variations in the form of 
this fold, In S, africana-marima, the aperture is elongate and the margins 
of the fold project and take the form of a semicircular crest; this is seen in 
eross-section in Fig. 221, c; in S. fusiformis, this crest is abruptly truneated. 
Tn S, pinnata and 8. punctata, on the contrary, such a crest is wanting. 


a | 


We haye seen that the placenta is formed from the lower parts of 
the primary brood-sac, the upper halves of the outer and inner 
lamellae taking no part in it (Figs. 217 and 218). We are still quite 
in the dark as to the future fate of these latter parts, which cover 
the embryo like a cap. According ta Haxnars (NG 187) Sienna 
(No. 110), they are cast off and disintegrate. 


According to Sanmnsmy, on the contrary, they are pepnaigy gs! 
becoming closely connected with it and participating in its formation. That 
part of the outer lamella (Fig. 217, e’) of the primary brood-sac, derived from 
the maternal atrial wall, which is not concerned in the formation of the 
placental membrane, is said to yield the ectoderm of the embryo (Fig, 218, ¢),* 
and the upper half of the outer lamella, which consists of flat cells, has there- 
fore been called by Satunsny the ectoderm-germ. The inner lamella (Fig. 217, 
fr), on the other hand, which can be traced back to the transformed epi- 
thelium of the oviduct, is said to yield, together with those parts that are not 
used up for forming the roof of the placenta, chiefly the mesoderm-tissue of 
the embryo (Fig. 218); the enteric rudiments, however, are also said 
originate in this layer. We must admit that we feel sceptical as to these state- 
ments. According to them, the embryo results from separate rudiments derived 
from various parts of the body of the parent, The epithelium of the atrial cavity 
of the latter would yield the ectoderm, the oviduct, a part of the mesoderm 
and the enteric rudiments, while the rest of the embryo would be derived 
from immigrated follicle-cells (for, according to Sanensxy, the blastomeres 
take no part in the building up of the embryo, p, 421). We are inclined to 
think that errors of observation or of interpretation must here basen in, 
[See editorial notes, pp. 420-425]. 


At the stage when we should expect the development of the germ 
layers,+ and the first rudiments of the organs, there is a considerable 
gap in our knowledge, We, at least, have been anable, from the very 
fragmentary statements of the stages that follow those described 


ubove, to obtain any clear idea of these processes of development 
which we desire to compare with the facts known im connection 


with the ontogeny of the other Tunicates or that of other animals. 


* (This layer, (¢') the epithelial capsule of Buooxs, is o 
temporary protective membrane which disintegrates at a later stage. 
no part in the formation of the ectoderm, which is, on the contrary, 

from the blastomeres (Brooks, Herprr and Kororserr).—Eb.] 


+In connection with the formation of the Ftc in the | 
special stress is to be laid on a “ gastrula-stage" by 
in which an invagination is fan on the lower side of the embryo, n 


towards the placenta. Fi 
‘According to Brooks, the ye in Salpa co to ie pat 
ns cording is to be sought nae stage ike | that given in 217, the cavi 
of the follicle, which becomes the posrearart being the 
and the blastopore coinciding with the attachment of the ce 
blastomeres and follicle-cells to the inner layer of the 
segmentation of the egg is much retarded, but the 
in follicle-cells. This view is not accepted by other 


h 









SALPIDAE—FORMS WITH COVERING FOLDS, 437 


In the next stages we find ourselves on firmer ground (Fig. 218 4), 
the most important organs having already developed. This stuge is 
characterised by the appearance of a cavity which, from its relations 
to the rudiments of organs (corresponding with those described for 
S. democratica-mucronata), we may regard as the body-cavity. Into 
this cavity, a club-shaped mass of cells, the early rudiments of the 
organs, hangs down from the upper surface of the embryo. The peri- 
cardial rudiment (pe) is, however, distinguished by being further 
attached at its lower end. 





Pia, 218. Two oiitogeictic stage of Salo pinata (after Sauk). A; lingram 
matic median soction of a younger stage combined from various figures hy SaueNsky + 
Holes 4, blastomeres ; bi, ™ blood-forming hud."” ; Bl, blood-spaces in the 

, atrial cavity ; d, enteric rudiment ; te roof of the placenta ; #2, ecto- 


covering fold; h, rudiment of heart gill; m, mnscle-hoopa mp, 
fred membrane; a, rndimont of the nervous system ; p, placenta Tee pat 
cardia} rudiment ; pls, pharyngeal cavity. 


This cavity has been called by SALENSKY the secondary follicle- 
cavity. Since, according to this author, only some of the rudiments 
of the internal organs (the nervous system and the pericardial 
rudiments) are formed from the inner cell-mass of the embryo, the 
body-wall (together with the rudiment of the intestine) being 
derived from the wall of the primary brood-sac; this cavity has, for 
SALENsKY, the same significance as the original cavity of the primary 
brood-sae (Fig. 217, f). The latter, which is called by Sauensky 
the primary follicle-cavity, is said completely to disappear in those 
obscure stages which lead up to the stage now being considered, and 


438 TUNIOATA. 
to be replaced by a secondary follicle-cavity that appears im the sate 
place.* 


The body-cavity (Sanensiy’s secondary follicle-cavity) 
the rudiments of the organs laterally and ventrally from the 





wall. In the latter we can now distinguish an external layer, the 
ectoderm (Fig. 218 A, ec), from an inner layer, the cells of whieh 
wander into the body-cavity, filling it with a mesenchyme. We are 
consequently enabled to recognise in this inner layer a part of the 
mesoderm-rudiment, 

Tf, in order to obtain a correct idea of the relative positions of the 





¥'1G, 219,—Horizontal sections through two embryos of a ie 
Salpa pinnata, wade jo the direction of the Tt first parts of the 


‘ig. 218 A'(after SALENSKY). 6, the blastomeres ; 
i, enteric rudiment; @’, layer Ceres the intestine ; enteric rudiment 
ec, sotoderm ; 1, slip lateral parts of the (pharynx) to develop 
ts of the placenta § 7, is its fat ‘Antoni! 






nerye-rudiment ; 


P, 
pericardial rudiment; pl, blood wavities of the placenta, a 


*[Brooxs considers that this second cavity is probably the ori al avity 
of the follicle opened a second time by the growl of of the r . 
He would thus derive the body-cavity in Salpa from the , 
cavity, the latter he believes to represent the cleavage-cavity 
—Ep.j 








SALPIDAE—FORMS WITH COVERING FOLDS, 439 


is at first a paired rudiment of the pharynx only slightly connected 
in the median line. According to SaLEnsxy, the first recognisable 
rudiments of this system of organs are found as two entirely distinct 
accumulations of cells derived from the wall of the primary brood-sac 
(wall of the follicle). Ina similar way, in 8. democratica-mucronata 
also, the rudiment of the pharynx develops in the form of paired 
cavities (p. 426). Two layers may be distinguished in the enteric 
rudiment ; an inner layer consisting of deep cylindrical cells (ento- 
derm) and an external layer, the so-called covering layer of the 
intestine (d’), in which a few larger blastomeres (enteric blastomeres, 
Fig. 219 A, 6) can still be recognised and which may perhaps be 
considered as belonging to the mesoderm. 

In horizontal sections the rudiment of the nervous system has at 
first a curious trilobate form (Fig. 219 4), but this is less marked in 
later stages. Toparo (No. 107) has given to the two paired lobes 
(n’) the name of the dorsal cise, 
and regards them as belonging wo 
the mesoderm. He considers them 
to be provisional and homologous 
to the chorda. The pericardial 
rudiment (pc) is distinguished by 
the regular arrangement of the 
blastomeres found in it, two columns 
of the latter in which the cells are 
arranged in pairs running through 
it. Both the pericardial rudiment 
and the neural rudiment project 
slightly at their upper ends above 
the surface of the embryo (peri- Fi, 250 — Hortoontal section through 
cardial and neural projections, Fig. pared ob ave reenate (ate 
220, n'); in later stages a dorsal cula of the enteric rudiment (gill-slits 
longitudinal furrow runs between ef Backes Beer tS ti 
them, but as to the significance of iy Projection j 2, ‘ol wiht 
these structures we are still in the somatic layer of the follicle, BRooxs). 
dark, 

In these stages the embryo lies like a flat disc on the placenta (Fig. 
218 A). Only its upper surface appears covered by the cap-like 
ectoderm-layer (Fig. 221, ¢c). Lt is not clear in what way the basal 

. 

met be ule Inaconsabe-als ail probably tas arly exisoed ay 


e atrial cavity, but even that structure is not derived from 
the wall of the follicle but from the ectodermal blastomeres,—Ep. } 





al 





SALPIDAE—FORMS WITH COVERING FOLDS. 44d 


bridge, first elongates. The trabecula, which is retained between 
the two diverticula of the developing respiratory cavity (Figs. 220, d, 
and 222, cl) that run upward, represents the rudiment of the gill (4) 
which, when the diverticula unite over it, becomes detached from the 
dorsal wall of the respiratory cavity. 





Fia, 222.—Median section through « later ontogenetic stage of Salpa pinnate (after 
Saukysky). ef, wtrinl diverticulum of the enteric rudiment; #, enteric rudiment 
frodimoent of the respiratory eavliyy no, ectoderm ; /, ciliated pit; 4, rndiment of 

wart; me, mesenchyme; 7, ganglion : pe, pericardium ; pl, tissue of the placenta. 


The part of the respiratory cavity which is to be regarded as the 
cloacal cavity is not, consequently, according to Sauensky, derived 
from an independent rudiment, but arises through the formation of 
diverticula from the rudiment of the pharyngeal cavity. Toparo 


* (The recent observations of Brooks, Herper aud Konornere are so abso- 
lutely antagonistic to those of SALENSKY, that We must now regard the above 
account of the origin of the pharyngeal and atrial cavities and of the gill as 
inaccurate. Heapsn and Kororxerr are fairly in agreement, and together 
they differ in some important points from Brooxs. All three however, 
that the atrium develops first, and is probably ectodermal in origin. 
The pharynx, on the other hand, appears as a cleft in the embryonic mass 
which becomes lined with entodermal blastomeres. The gill arises from the 
septum between these two cavities by the breaking down of the lateral parts 
of this septum, the clefts thus fanned. being the gill-slits. Saumnaky’s view 
that the gill and atrium of Sapa are not homologous with the similarly named. 
structures in the other Tunicates may be regarded as disproven,—Ep.} 











SALPIDAE—FORMS WITH COVERING FOLDS. 443 
begins to assume a simpler form (Fig. 219 B, m) ; at still later stages 
it is found as a cell-mass running obliquely downwards and forwards ; 
within this mass a cavity appears which communicates anteriorly with 
the respiratory cavity (Fig. 222). The part lying nearest to the aper- 
ture of the central canal represents the rudiment of the ciliated pit 
(/), while the blind end that is directed backward and upward forms 
the ganglion proper (n). In the course of development these two 
sections of the neural rudiment become more sharply marked off from. 
one another by a constriction. At the same time, in the ganglionic 
part of the rudiment, the central canal becomes segmented, breaking: 
up into three consecutive cerebral vesicles, a condition first noticed 
by Kowavevsky, and similar to that 
seen in S. demoeratica (p. 429). In 
later stages the cerebral rudiment: 
becomes completely separated from 
the ciliated pit, and the two radi- 
ments shift apart, although they seem 
still to remain connected by a nerve- 
strand that runs forward from the 
brain to the ciliated pit. The central 
cavity of the cerebral rudiment disap- 
pears, and the interior of the rudiment 
then seems filled with punctate nervous 
tissue (Leypia’s “ Punktsubstanz ”). 
A process running towards the surface 
leads to the development of the eyes, 


in which single cells of the ganglion 
become changed into elements  sensi- 
tive to light, while other cells of the 
most superficial layer become filled 
with pigment (p. 430). No details 
are known of the development of the 
paired auditory vesicles which lie in 





228. — Horlzontal | setion 
through an embryo of Solpa 
inmeta (after SALBNSKY), 5, 

d, enteric rudi- 

ment ; m, mesenchyme-cells ; 1, 
rudiment’ of the nervous system | 


Fra, 


wh, neural cavity; pe, pericardial 
rudiment; a, stib* pericardial 
coll-strand ; £, cells in the lumen. 
ofthe pharynx (atrium, BRooKs). 


vontact with the brain, and were first 
observed by H. Mtinrer and further described by Toparo (No. 
107). The ciliated pit, by the folding of its walls, assumes a com- 
plicated form approaching that of the same organ in the adult (Fig. 
24, B, fl). 

The pericardial rudiment (Figs. 218, 219 pe), whieh is originally 
4 cell-strand running from above downward, divides into two parallel 
strands (Figs. 223,224 4); the anterior strand, near the enteric 


THE EMBRYONIC DEVELOPMENT OF THE SALPIDAE. 445 


eavity appears within each of the developing muscle-hoops and these 
cavities have been compared by SALeNSKyY with those in the primitive 
muscle-plates of the Vertebrates (cavities of the primitive segments). 

The elacoblast (Fig, 224, eb) seems to be derived trom cells of the 
mesenchyme. 

The development of the other species of Salpa that are provided 
with the enveloping fold (S. africana, S. fusiformis and S. punctata) 
seems to follow essentially the same course as that of §, pinnata, 
Judging from the very fragmentary statements as to the ontogeny 
of these forms (Barrors, No. 87, Savensky, No. 104), however, there 
appears to be considerable variation in points of detail [see Hemmer 
(No, XIIL) and Konornerr (Nos. XX., XXa., and XXIa.)}. 


General Considerations on the Embryonic Development of 
the Salpidae. 


{The embryonic development of the Salpidae is still, in spite of the recent 
investigations of Brooks, Hemer and Korornerr, anything but satisfactorily 
understood. The confusion arising from the immigration of the kalymmo- 
cytes and the difficulty of discriminating between these cells and the smaller 
formative blastomeres of Hemer and Korornerr, still requires to be swept. 
away before we can make any satisfactory comparisons of the development of 
Salpa with that of other Tunicates. When, further, we compare the mono- 
graphs of the two last authors with that of Brooxs, we must {sel that additional 
confirmation of one or other of the views put forward by these writers is 
necessary before one of them is finally accepted, It is obvious, however, that 
we are dealing with a highly speci form of development which has 
possibly arisen in connection with the viviparous habit of Salpa and has been 
further complicated in connection with the peculinr life-history of this form.] 





The embryo undergoes direct development in accordance with its 
retention during the whole embryonic and larval periods within the 
body of the parent. We have already seen a similar omission of 
metamorphosis among the Ascidiacea in the Molgubidae. The Salpidae 
in this respect show a more specialised condition in so far as the 
embryo becomes closely connected with the tissues of the parent, 
and a placenta develops for its nourishment, Since we may, with 
some probability, derive the Salpidae from the attached Aseidialike 
forms, we might be tempted to trace back the fixation of the embryo 
on the wall of the respiratory cavity of the parent to this original 
attached manner of life, 

[Considerable stress was formerly laid upon the ontogenetic differences 
described by SALENSRY as occurring in the various species of Salpa, especially 


on the presence or absence of covering folds and on the structure of the 
placenta. According to Sauunsky, the covering folds were completely wanting 


THE EMBRYONIC DEVELOPMENT OF THE SALPIDAE. 447 


ment, is nevertheless very remarkable, this organ having been con- 
sidered as the typical feature of the Tunicate plan of organisation. 
To explain this fact, we might be tempted to assume that there are, 
among the Tunicates, forms only slightly removed from some primi- 
tive ancestor which did not possess a chorda, and in which, conse- 
quently, the development of this organ is not sufficiently established 
aus a constant feature.* 

Sanensky holds that a rudiment of the larval tail is found in the 
Salp embryo in the elaeoblast, that problematicul provisional organ 
(p. 432) to which Tovaxo (No. 107) no doubt erroneously attributes 
such a great significance in comection with the development of the 
proliferating stolon. The significance of this structure as a vestige 
of the larval tail seems to be rendered somewhat probable by a 
comparison with the tailed embryos of Doliolum. [During the 
development of this organ, however, there is no suggestion of an 
entodermal origin, if anything an ectodermal one is suggested. 
Functionally, the elaeoblast appears to be nutritive. ] 

Turning to the rudiments of organs, we must first trace the deyelop- 
ment of the respiratory cavity. In this we can always distinguish 
‘two separate cavities divided from one another by the gill which runs 
between them obliquely (Fig. 224, &). The anterior and ventral 
eavity known as the pharyngeal cavity (ph) is considered as the 
equivalent of the respiratory cavity of the Ascidian, while the pos- 
terior cavity which lies dorsally to the gill is regarded as the atrial 
cavity (c/). The two large apertures through which these two 
cavities communicate on either side of the gill are regarded as un- 
usually dilated gill-clefts. In this view, which is favoured by the 
condition of the gill in Doliolum, this one pair of gill-clefts occurring 
in the Salpidae has been thought to arise by the fusion together 
of several smaller clefts, This view is opposed by vAN BeNepEN and 
Juni (No. 10), according to whom only one pair of true gill-clefts 
develops in the Ascidiwns also, the many perforations of the wall of 
the gill which develop later being secondary structures (branchial 
stigmata, p. 367). ‘The Salpidae in this case would, like the Larvacea, 
exhibit a very primitive character in the presence of a single pair 
of gill-clefts. Toparo (No. 113), who adopts this view on the whole, 
has extended it by explaining certain ciliated invaginations which 
are found arranged im rows at the sides of the gill in some Sulps 


® We must, however, bear in mind that the body of the Thaliacean represents 
principally the pre-chordal region of the Ascidian larva, 


448 TUNICATA. 


(S. pinnata, S. bicaudata, etc.), us the homologue of the secondary 
gill-clefts in the Ascidians (branchial stigmata). We do not think 
there are sufficient grounds for such an explanation, since these 
invaginations, which were already known to Fou, may also be 
secondary acquisitions resulting from the need for increasing the 
respiratory surface. We have pointed out above that the condition 
of Appendicularia is probably not to be regarded as primitive. 

Some statements as to the occurrence of a true coelom in the 
embryos of the .yalpidae have still to be noticed. TopaRo (No. 107) 
considers that the coelomic sacs originated through dehiscence taking 
place in a mesodermal layer surrounding the intestine. According to 
SALENSKY, a cavity first arises in cach of the already distinct muscle- 
hoops, and this cavity also is considered as the equivalent of the coelom 
in the Vertebrates (#.¢., of the cavities in the primitive segment plates, 
p. 445).* = 

The origin of the pericardial sac may perhaps, according to 
SALENSKY, be traced back to the mesoderm, whereas, in the 
Ascidiacea, it is of entodermal origin (p. 368). [Entodermal accord- 
ing to Korornerr, see footnote, p. 432]. 


II. Asexual Reproduction. 


Asexual reproduction, both by fission and budding, is of wide 
occurrence among the Tunicata, and frequently leads to the forma- 
tion of stocks. Before describing these reproductive processes, we 
must point out that the capacity for regeneration also occurs to & 
large extent in this class. The experiments made by LoEn and con- 
tinued by Mrncazzixi have shown that solitary Aseidians (Ciont 
intestinalis) are capable of regenerating distinct portions of the body. 
If, for example, the central nervous system is removed artificially, it 
can be regenerated. In some cases, sinilar processes of regeneration 
Hy. This was observed by DELLA VALLE (No. 
zona violacea, in which, under unfavourable con- 








seem to occur nom 
70) in colonies of Di 
ditions, the anterior part of the body (the branchial sac and other 
organs) degenerate in the individuals of the colony. There is then 
found in this region an accumulation of yellow mesoderm-cells filled 
with nutritive material. The organs of the posterior half of the body 











*(Brooxs (No. L) considers the transitory body-cavity of Salpa as a r- 

. opening of the follicular cavity, and this latter he attempts to homologise with 

the cleavage-cavity of the normal gastrula, He thus regards the body-cavity 

of Salpa as the equivalent of the primary body-cavity (cleavage-cavity), and 

not as the secondary body-cavity (coelom’ proper). The cavity becomes filled 
later with mesenchyme-cells from which the muscle-hoops arise.—Ep.] 


ASOIDIACEA— TRANSVERSE FISSION. 449 


(the intestinal loop and the heart) remain unaffected by degeneration, 
and, should the conditions of existence again become more favourable, 
this posterior half is able to regenerate the anterior part. An increase 
in the number of individuals forming the colony, by means of division, 
may even be connected with this regeneration. The yellow body then 
becomes lobate, and divides into several parts, each of which develops 
into a new Ascidian. The details of these interesting processes are, 
however, still unknown. 

The occurrence of such far-reaching regenerative processes and the 
capacity for asexual reproduction in the Tunicata at first sight seems 
surprising, when we take into account their comparatively complicated 
organisation and their near relationship to the Vertebrata. We must, 
however, remember that the saine capacity ix found in the Annelida 
and the Echinoderma, groups which, in the condition of their 
organisation, may at least be compared with the Tunicata. 


1. Social and Composite Ascidians. 


The asexual reproduction which takes place in these groups is 
usually called budding. In the Polyelinidae, however, asexual 
multiplication takes place through the segmentation of the post- 
abdomen, This kind of reproduction, therefore, must, strictly 
speaking, be defined as transverse fission, and must be considered 
as distinct from budding. : 


A. Reproduction through Transverse Fission. 


This is the kind of multiplication which was defined by Giarp 
(No. 57) as “ bourgeonnement ovarien ” and which has become better 
known through the researches of KowaLevsky (No, 61) in conncetion 
with Amearoucium proliferun, 


[Since this description was published, further investigation of the budding 
processes in the composite and the social Ascidians has shown us that, while 
the account given in the following pages is correct in so far as it derives all 
the important internal organs from the inner sac, yet it obscures the actual 
state of affairs by always speaking of this structure ag entodermal. While it 
is probably true that this inner sac is derived from the entoderm in mort cases, 
yet, in one group, the Botryllidae, if the observations of Hsont (No. XIV.) and 
Pizon (No. XXVI.) are correct, this does not appear to be the case. Thexe 
observers find that the stolon is purely ectodermal, the epicardia arising from 
the peribranchial sacs of the parent which, in the first instance, ic., in the 
larva, are of ectodermal origin. From this ectodermal epicardium, the bud 
arises much in the way described above. Thus we find that, in one family, all 
the organs of the bud are of ectodermal origin, while, in the majority, they 
arise from the entoderm.—Ep.] 





Ga 

























primary b 
ee od uineiie aia 
4 transverse partition-wall (s) into a dorsal 
(#). The partition-wall itself is hollow, 
flat diverticulum of the branchial sac. 
ately behind the posterior end of the eu 
entrance of the oesophagus, which runs bh 

en and ends blindly near its 
heart (Fig. 227 A, A)ourved into cl 
the entodermal process just 
is identical with the tube in Clavslinais 
Junin (No. 10) the epicardial tube (see F 


ASCIDIACEA—TRANSVERSE PISSION. 451 


is also evidently the homologue of the entodermal or endostyle-process 
in the proliferating stolon of the Salpidae and Pyrosoma, but the rela- 
tive position of the heart distinguishes this so-called epicardial tube 
in the Polyelinidae from 

the similar tube in the Bie PE vcigg 
above-mentioned — forms: 
The finer anatomical 
features of this tube have 





been described by Mavu- a A 
RICE (No. 40) in Fraga- 

roides, The tube forks at a 
its anterior end; the two 

prongs of this fork huve D 

been distinguished by vax A 
Benaven and Juum as 

epicardial tubes from the 7 
posterior undivided epi- y 
cardial sac (see above, p. 1G. 226.—Dingrams illustrating the condition of 
370). The two Mploardial bs! ai te PA aide view ps 


tubes arise on cither side — “Termparetion atthe level ab 0 atthe leva cas 


of the median line behind Pp Lite sac; x, forked end of the epl- 
J cardial sac. 

the posterior end of the 

endostyle from the pharynx. The posterior end of the sac is, according 
to Maurice, also forked (Fig. 226 d and D, ep). [t embraces the 
ereacent-shaped pericardial vesicle (p). In Clavelina, the epicardial 
tube enters into close relation to the heart (p, 370), completing 
the dorsal wall of that organ, but this is not the case, according to 
Mavnicg, in the Polyclinidae. The heart-tube (/) in these latter is 
an invagination of the outer wall of the U-shaped pericardial vesicle 
(Fig. 226 © and D). 


It should be mentioned that the paired apertures of the two epicardial tubes 
ean be recognised only in larvae and in jquite young asexually-produced 
individuals, They could not be found by Kowacevsry in the adult xooid, 
and Maurice also has recently stated that the two epicardial tubes, although 
they approach close to the wall of the branchial suc, seem no longer to com- 
municate with its cavity. 


‘The epicardial sac in the Polyclinidae divides the body-cavity into 
a dorsal and a ventral half (Fig. 225, 4, 4’). Through each of these 
halves a blood-stream flows, but, in the dorsal half, the direction of 
the stream is opposed to that in the ventral half, the blood flowing 
in the one half towards the heart and in the other from the heart to 


452 TUNICATA. 


the body. Similar conditions are found in the proliferating stolon of 
other Tunicates (¢.g., Clavelina, p. 370). In this form also, in the 
stolon, a dorsal blood-current is separated from a ventral current 
flowing in the opposite direction by the epicardial sac which forms a 
partition extending almost to the end of the stolon (Fig. 229, x). A 
transverse section through the proliferating stolon of Clavelina shows, 
on the whole, remarkable agreement with one through the post- 
abdomen of the Polyclinidue, though important variation is found in 
the position of the heart. In the Polyclinidae, the heart lies at the 
posterior distal end of the post-abdomen (Figs. 226 and 227), which, 
consequently, contains important organs belonging to the organiss- 
tion of the parent (the heart and the genital organs). In Clavelina, 
the pericardial vesicle and the heart have shifted to the point of 
origin of the stolon (Fig. 173 C, p. 375). The heart lies at the 
proximal end of the epicardial sac, on the ventral side of the latter, 
so that the epicardial lamella, as shown above (p. 370), can be utilised 
in the formation of the dorsal wall of the heart. The proliferating 
stolon of Clavelina does not contain any important organ of the 
parent body, but is a process of the body dedicated exclusively to a 
sexual reproduction. The same is the case with the stolon of other 
Tunicates (Thaliacea and Pyrosuma, etc.). We might imagine the pro- 
liferating stolon as derived from the post-abdomen of the Polyclinidae, 
if we chose to assume that the genital organs and the heart withdrew 
to the proximal end of the post-abdomen, which then became dedicated 
exclusively to the function of reproduction. Such an assumption 
would satisfactorily explain the remarkable divergence in the position 
of the heart above alluded to. While, in Clavelina, the heart lies on 
the ventral side of the e 
dorsal side of the so-called endostyle-process (Fig. 2 
If, then, we assuine that in these two groups the heart origin: 
as in the Polycl/nidae, at the distal end of the stolon, it is not difficult 
to imagine that secondary shifting took place, in the Clarelina to the 
ventral and in Pyrosom to the dorsal side. 


icardial sac, in Pyrosoma it is found on the 








The ontogeny of the Pyrosoma would, indeed, rather lead us to consider 
the change of position of the heart as the consequence of lateral shifting of 
the organs. The heart there lies originally on the right side of the entoderm- 
process, and only later shifts to the dorsal side (SEELIGER) ; cf. p. 493. 





It is evident from the above that the asexial reproduction of the 
Polyclinidae (through the segmentation of the post-abdomeu) and 
the stolonic budding found, for instance, in Clavelina, are related one 
to the other. Giarp (No. 57) has already pointed out that the 


ASOIDIACEA—TRANSVERSE FISSION. 458 


elongated, branched post-abdomen of many Polyclinidae (e.g., Circin- 
alium), part of which creeps horizontally along the substratum, is 
remarkably like the stolon of Clavelina. These two methods of 
reproduction are thus connected with each other by transitional 





Fra. 227.—.1, young Amaroucium before the commencement of asexual reproduction ; 
B, Amaroucium with segmented bdomen (after Kowauevaky). a, thorax; 
8,'abdomen ; ¢, post-abdomen ; A, heart; », partition-wall ; s', anterior part of the 

i y. separated portions of the post-abdomen ; &, anterior swollen 

-wall in the posterior separated portion. 







The commencement of asexual reproduction in the post-abdomen 
of Amaroucium is marked by its elongation and the abstriction of 
its soft part from the point of attachment to the rest of the body. 
The heart continues to beat after the separation of the post-abdomen 
from the abdomen is accomplished. Soon after, the post-abdomen 
(Fig. 227 B) breaks up, through transverse fission, into a varying 


a 


454 TUNICATA, 


number of parts, each of which develops into a young Aseidian. 
The first sign of development is shown in a widening of the proximal 
end (A) of the ectoderm-tube (segment of the epicardial sac) which 
lies in every segment. his proximal dilation is the rudiment of 
the whole alimentary canal of the young animal. The non-dilated 
part of the entoderm-tube becomes the epicardial tube of the yeung 
individual. The heart of the parent-animal that has remained in 
the distal segment now degenerates. Somewhat older colonies 
(Fig. 228) are of a different shape. The young animals, which 
originally lay in a row one behind the other, show a tendency to 





Fie, 228.—Two young colonies of Amermuetum (after RowALkvakY), A, younger. 
B, older stage. a, parent-animal ; 4, an advanced bud; ¢ younger 


shift upward within the test towards the parent-individual, and the 
whole colony thus beeomes broader and shorter, The parent-indi- 
vidual now begins to develop, through regeneration, a new heart 
and post-abdomen (Fig. 228 4, a). The danghter-individuals in the 
figure seem to be at different stages of development. One of thew 
(6) exhibits the almost perfect organisation of the adult Aseidian, 
while the three others show the rudiments of the different parts uf 
the body, but these are very slightly developed, Tn all these young 
individuals the post-abdomen is still comparatively short. Only 
later (Fig. 228 8) does it grow out to a greater length, and come 


bh ay 


ASCIDIACEA—STOLONIO GEMMATION. 455 


to resemble more and more the post-abdomen of the parent before 
the commencement of asexual multiplication. The anterior part of 
the body of the young individual has shifted upward. The branchial 
and atrial apertures have broken through, and reproduction by means 
of tranverse fission now takes place in the daughter-individuals that 
have arisen as described above. 


We thus find, in this case, the first rudiments of the young animal 
im the portion of the post-abdomen, whieh becomes separated by 
transverse constriction, and which, through processes of regeneration, 
is able to develop into a perfect new individual. For details of these 
processes, see p. 470. 

Whether, in the segmentation of the post-abdomen in the Polyclinidac, we 
actually have a more primitive form of asexual multiplication, from which 
the stolonic gemmation of other Tunicates is to be derived, must still be 
regarded as doubtful, It is also possible that the transverse division of the 
Polyclinidae is to be derived from stolonic budding, A comparison with the 
conditions of development of Pyrosoma shows that caution must be exercised 
in such speculations, At first sight we should feel inclined to describe the 
rise of the first four Ascidiozooids in the Pyrosoma embryo as transverse 
fission (Fig. 193, p. 397), but more careful examination reveals the fact that 
the later longitudinal axis of the Ascidiozooid is at right angles to that of the 
proliferating stolon. We have, consequently, to regard the rise of these first 
Ascidiozooids also as stolonic budding, which is not essentially distinguished 
from the budding of the zooids that are produced later (see pp. 404 and 484). 


B. Stolonic Gemmation. 


The typical form of stolonic gemmuation is found in the so-called 
social Ascidians, in Clavelina and Perophora, The single individuals 
here send out a creeping proliferating stolon which branches re- 
peatedly (Fig. 229), and at the end of which the buds appear as 
club-shaped swellings. In structure the stolon closely resembles the 
post-abdomen of the Polyclinidae. Here also we find, as has already 
been shown, the blood-space of the stolon (primary body-cavity) 
divided by the extension of the epicardial sac (stolonic septum, s) 
into a dorsal and a ventral half, the blood circulating through these 
in opposite directions. Since the partition-wall does not reach quite 
to the distal end of the stolon (s) the two sinuses communicate at 
this point, where also the stream of blood changes from the one 
direction into the other. 

The buds here originally appear in the form of bilaminate vesicles 
tén). The outer layer of the vesicle, the ectoderm of the bud, is 
continuous with the ectoderm of the stolon and of the parent- 





456 TUNICATA. 


individual. The inner layer, the entoderm, arises as was first proved 
by Kowauevsky (No. 60) for Perophora, as a diverticulum of the 
stolonic septum (epicardial sac) with which it long remains connected. 
Between the ectoderm and the entoderm, the primary body-cavity 
of the bud appears filled with 
mesenchyme - cells, We shall 
presently, following the accounts 
of Kowatevsky (Nos. 60 and 
61), SeEticER (No. 66), and 
vaN BENEDEN and Juuin (No. 
10), describe more in detail the 
further development of the bud. 
We can here merely mention 
that, in Clavelina, the connection 
of the bud with the stolon, and 
through the latter with the other 
individuals of the colony, is 
usually retained even in the adult. 


Not all the root-like processes of 
Clavelina seem to be capable of pro- 
ducing buds. Many of the ramifica- 
tions seem intended merely forattach- 
ment or to serve as reservoirs of blood 
(SKELIGER). The latter then have 
no epicardial process extending into 
them. A sharp distinction must be 
made between these sterile body- 
processes, which may be compared 
with the mantle-vessels, and the 
ramifications of the actual prolifer- 
ating stolon. 





Among the Composite .\scidians 

Flu, 229,—Portion of n_ proliferating the family of the Dixtomidae 

atolon of Pecophuca (after Kowatevsk¥). belongs to the type just described, 
ee, ectoderm of the bud ; en, entoderm ha 

. the entoderm-vesicle of the bud 


of the bud; kn, buds 
septum (epicardial lamella} here also becoming abstricted 


tion of the stolon, 








from a process at the posterior end 

of the endostyle. In the Botryllidae, the Didemnidac, and the 
Diplosomidae, on the contrary, budding of another type occurs. 

The family of the Déstomidae seems to be distinguished by the fact 

that its buds separate very carly from the proliferating stolon. They 

are then found within the common cellulose mantle scattered bet ween 





ASCIDIACEA—STOLONIC GEMMATION, 457 


the separate individuals as small, rounded bodies, each provided with 
acavity. In individual cases a longer proliferating stolon seems to 
occur, as in the stalked colony of Colella pedyneniata, in which 
Hexpman found that each individual gave off into the common stalk 
a body-process (evidently the proliferating stolon). On this, then, 
the young buds arise and detach themselves, shifting upward in the 
common mantle-substance in proportion as they develop further. In 
another form belonging to this group, described by KowAnevsky 
as Didemnum styliferum, but which, according to Denna Vane 
(No, 68), belongs to the genus Distaplia, the small buds which early 
become independent, arise, as KowALEVSKY conjectured, on a process 






eK 


280, —Freeswimming larva of Déstaplia (utter Data VALLE). cl, atrial cavity; 
¢, atrial aperture ; en, endostyle ; hit, intestine ; 4, branchial aperture ; , detached 
Hud; &, bud in the avt of dividing ;'m, stomach! n, ganglion ; oe, 4 






adhering organ ; sf, stolon ; <r, larval tail, 


directed posteriorly, which must evidently be regarded as a pro- 
liferating stolon, This is also the case, according to LAHMmLE (No. 
38), with the individuals of Distaplia magnilaroa, but Denna VALLE 
(No. 68) assumes thut these processes are merely mantle-vessels. 
‘The special characteristic of the Distomidae is the early detachment 
of the small buds within the still free-swimming larva (Fig. 230). The 
large larvae of Distaplia magnilarva. in which, according to Denia 
Vane, the organisation of the adult Ascidian is almost perfectly 
attained while the animal swims about freely, also show, between the 
endostyle and oesophagus, a short proliferating stolon (st), from which 
small buds that multiply by division (4, 4’) are abstricted. 


lai 





BUDDING OF THE DIDEMNIDAE AND THE DIPLOSOMIDAE. 459 


individuals are arranged in such a way that their atrial apertures turn towards 
each other, In this way commences the union of the individuals round a 
common cloaca (Kroux, No. 63). This young tetrazooid colony shows con- 
siderable resemblance to the youngest Pyrosoma colonies. The individuals 
which are produced later by budding are always given off by the parent 
laterally, and thus occupy the spaces between the parent-individuals. They 
themselves are very soon capable of multiplying in their turn. The daughter- 
individuals at first lie somewhat away from the common cloaca, towards which 
they only shift later. Systems consisting of two concentric cycles may thus 
develop, the inner cycle containing the parent-individuals and the outer the 
doughter-individuals, While the latter shift to positions round the common 
cloaca, the individuals of the inner cycle disintegrate (Jourpars). The 
common cloaca is nothing more than a pit-like depression of the outer surface 
of the common cellulose mantle. This is also the case with the common 
cloaca in Pyrosoma (cf. p. 408). 

New circular systems are produced in the Bofryllidae, when one of the buds 
belonging toa cycle does not shift towards the common cloaca, but moves 
away from it. This individual, by reproducing itself through budding, 
becomes the founder of a new cycle. 


D. Budding of the Didemnidae and the Diplosomidae. 


The conditions of budding in the families of the Didemnidae and 
the Diplosomidae are very peculiar. Since, in these fathilies, the 
buds remain vonnected with the parent until fully developed, re- 
markable double individuals are produced whieh long since attracted 
the attention of zoologists. Since, further, in the Diplosomitie, the 
first budding process takes place during larval life, free-swimming 
and still caudate larvae are found in which two branchial sacs are 
well developed. On closer inspection, it is not difficult to distinguish 
the branchial sac of the larva from that of the bud. In the brain of 
the primary individual, moreover, the larval sensory organ can be 
recognised, while in the bud it is wanting. 

Budding, in these two families, follows the type defined by Garp 
(No. 57) as “ bourgeonnement pylorique."’ According to GaGENBAUR, 
Gants (No. 55), Denia Vanue (No. 68) and other authors who have 
investigated this method of budding, the newly formed individual 
here arises through the concrescence of two originally distinct buds 
(Fig. 85), one of which (the thoracic bud, k’) yields the branchial 
region with its organs, the peribranchial sacs, and the pharynx, while 
the other (the abdominal bud, k) gives rise to the intestinal loop, the 
genital organs and the heart. The first rudiment of the abdominal 
bud (Fig. 232 A, 4) is found as an outgrowth of the oesophagus of 
the parent; the thoracic bud, on the contrary (4’) lies further down 
on a level with the stomach, on the right side of the body and, 


—— 


460 TUNICATA. 


according to DeLLa VALLE, is derived from a simple outgrowth of 
the body-wall (consisting of ectoderm and the parietal layer of the 
wall of the peribranchial sac), and thus arises in the way described 
above for the buds of the Botryllidar. JourDAIN (No. 64) has 
recently stated that these two buds (the thoracic and the abdominal 
buds) arise through the division of an original single bud, and that 
the connection between the two halves is still maintained for some 
time. No further details, however, are known on this point. G1agp 
(No. 58) holds that the first rudiment of the bud can here also be 
traced back to the epicardial tube. 

The «atdominal Ind (Fig. 232 A, &) is thus at first apparently an 
outgrowth of the oesophagus of the parent which, however, soon 
becomes more sharply marked off (Fig. 231 4 and 2) in such a way 
that it then forms a caecum connected with the oesophagus only at 
its anterior end (Fig. 231 C'), this becomes U-shaped and can now 
be recognised as the rudiment of a new intestinal loop, in which the 







ophageal bud of Trufidenswn ® (after 
y AL bud: ae, stomach. 


tomach, intestine) become differentiated. 
y-formed intestinal loop is connected with 
of the parent (4+). The intestine of the bud becomes 
at of the parent (Fig. 


Various parts (oesophagus, 


The oesophagus of the new 





the oesophagu 








B, 4) and enters into com- 
munication with it. The parent-individual now possesses two fully 


applied tot 


developed intestinal loops, with continuous lumina. It is not yet 
clearly known how the heart and the genital rudiments of the bud 
develop, but Detta VacLce believes that the latter are perhaps 
derived direct from the genital rudimeuts of the parent. . 

At the 
fully (Fis: 





sue time, the thorneie hud (Fig. 232 1. &) alse develops 





2. 8). We cannot here enter in detail into the some- 





Tire genus Trididemnum is included by HinpMax in the genus Didemnum 
Savigny.—Ep.] 


BUDDING OF THE DIDEMNIDAE AND THE DIPLOSOMIDAE. 461 


what unsatisfactory statements of authors ns to the way in which the 
organs develop in this bud, but may mention that peribranchial sacs 
develop at the sides of the central enteric cavity, that gill-clefts break 
through, and that the ganglion, and the branchial and atrial apertures, 
appear as rudiments. An oesophageal tube and a short rectum seem 
also to appear. The former (Fig. 232 2, a) now becomes connected 
with the oesophagus of the parent (o-) near the point at which the 
oesophageal tube of the abdominal bud («) enters it. At this one 
point, therefore, three oesophageal tubes seem to be connected, viz., 
that of the parent and those of the two buds. This is also the case 
with the rectum, the short rudiment of that organ belonging to the 








Fig, 232,—Budding in Trididemnin (after DELLA VALLE). 





intestinal loop of the 
dividual with the rudiment of the abdominal (4), and thoracic (A’) buds ; 


pare 

Bh individual with the tyo buds at Tater stage of developinent, oesophageal 
rudiment of the bud &; «’, oesophageal rudiment of the bud 4’; 4, rudiment of the 
intestine in the bud &; 6’, the sane rudiment in the bud A” fntetine af the pore 
individual; &, abdominal bud ; 4. thoracic bud ; w, stomach ; o, oesophagu 
constricting ectoderm-ring, 














thoracic bud (/') entering the rectum of the parent (¢) at the point 
at which the rectum of the abdominal bud (4) joins it. If, now, the 
oesophagus of the thoracic bud became more closely connected with 
that of the abdominal bud, and such connection were also to be 
established between the intestines of the two buds, the two halves of 
the daughter organism would then at last be united. But althongh 
the alimentary canal of the bud is now completed, it still, for a long 
period, remains connected with that of the parent, both in the 
oesophageal region and through the rectum (Fig. 233).* 


* [For further details concerning the development of the complex buds of 
the Diplosomidae and Didemmidae, see the recent works of CacLERY (Nos, V.- 
VII.) and SaLeNsky (No. XXIX.). Cauzery finds epicardial tubes in the 
adults, and from these he derives the thoracic and abdominal buds.—Ep.] 


462 


TUNICATA. 


The thoracic and the abdominal buds do not always develop equally. 
In some cases only the abdominal bud develops. This leads to an 





Fic. 233, —Late stage in the budding 
vrid idemnni (ater DELLA VALLB). 
The alimentary canal of the perfectly. 
developed bud still remains connected 
with that of the parent. ¢, atrial 
aperture ; en, endostyle ; é, branchial 
aperture: m, stomach ; ‘x. ganglion ; 
or, oesopliagus ; r, rectum, 














abnormality, consisting of one 
branchial region with two fully 
developed intestinal loope (Fig. 
234 B). In such cases the intestine 
of the parent may degenerate later. 
This condition is regarded by Datta 
VALLE as a rejuvenescence, and 
consists in the development of an 
individual, the anterior halfof which 
belongs to the parent, while its 
posterior half develops anew (see 
also Oxa, No. 646). A similar 
process may occur in the anterior 
part of the body, when the thoracic 
bud alone develops (Fig. 234 A). 
The process is often still further 
complicated by the appearance of 
the bud-rudiments ofa third genera- 
tion arising .from the not yet fully 
developed bud. In this way 


remarkable combinations of the various halves of the body are 


produced. 


Vauue, simplified). 
B, two intestin: 











ASCIDIACEA—FORMATION OF ORGANS IN THE BUD. 463 


In the Diplosomidae the process of budding and the formation of double 
individuals begins even in the free-swimming larva, but in the Didemnidae 
this is not the case. 

But forthe statements made by Jourpain we might be tempted to derive 
the remarkable budding processes in these two families from a primitive 
Jongitudinal fission of the parent, 


E. Development of the Organs in Asexually Produced 
Individuals. 


The development of the inner parts of the bud has been described 
by Merscanrkorr (No, 41), Gants (No. 55), KowALevsny (Nos. 60 
and 61), Grarp (No. 57), Dena Vane (No. 68), SEELicER (Nos. 
66 and XXXIV.), vay Bewxepen and Juvin (Nos, 10 and XVIL), 
Hyorr (Nos. 59 and XVI), Oxa (No. 642), and in the still more recent 
works of Caunery (No. IV.), Lerivee (No. XXIL.), and Rirrer 
(No. XXVIIL). In our account of these processes we have followed 
Kowatevsky, whose careful researches have been confirmed with re- 
gard to the development of the nervous system and the pericardial 
vesicle hy vaN Bsnepen and Junin. 

The bud is at first a hollow body consisting of two or three layers 
(Fig. 229, kn). The outer layer is the ectoderm (ee) which is in 
continuous connection with the ectoderm of the stolon, The inner 
layer, the entoderm (en), encloses the primary enteric cavity of the 
bad, which, in Claveltna and the Distonidae, originated as a diyerti- 
culun of the epicardial sac (entodermal stolonic septum, ‘ cloison ").* 
The connection between the entoderm-vesicle of the bud and the 
epicardial snc is retained in the social Ascidians (Clavelina and Pero- 
phora) for « very long time, often throughout life. According to 
vAN Bexepen and Juuis, the stalk-like portion which connects the 
bud with the stolonic septum represents the rudiment of the epicardial 
sue und of the pericardial vesicle of the budding individual. The 
primary body-cavity extends between the ectoderm and the entederm 
of the bud ; into it mesoderm-elements soon immigrate, and these are 
the first rudiment of the mesoderm of the bud. In many cases 
(expecially in the buds of the Distomidae and the Botryllidae) the 


*{In Perophora, according to Rirrun (No. XXVIII.) and Lerkver (No, 
XXIIL), the developing blastozooid (bud) is connected with the stolonic 
septum, not by its branchial sae but by the left peribranchial sac. Rrrren 
expresses some doubt concerning the origin of the pericardium; he thinks 
that it arises from the inner vesicle, but even if it is produced by the aggrega- 
tion of mesenchyme-cells, as Larivan states, it is still probable that its 
ultimate source is the entoderm, since the mesenchyme-cells are probably 
produced from that layer.—Ep.]} 








464 TUNICATA. 


genita] rudiments can also be distinguished at an unusually early 
stage.* The above is the case in the buds of Distaplia (Kowa- 
LEvsky’s Didemnium styliterum), which, as free bodies detached from 
the stolon, are found scattered in the cellulose substance of the colony. 
In the genital strand (Fig. 235, 7) of the youngest of these buds, 
several young egg-cells can always be recognised. These buds, 
however, are capable of multiplying by fission (Fig. 235 4), and in 
this case the eggs become distributed so that one occurs in each 
portion of the original bud. KowALevsky is, therefore, inclined to 
regard the buds which form first as stolons which have separated 





Fig, 235.—.1, younger, #, older stage of development of Distaplia stylivera (afer 
Kowacevsky). In B, the bud is dividing into two. e¢, ectoderm ; ex, entoderm; 
7. genital strand ; ms, mesoderm, 

from the Ascidiozsoids, the parts resulting from fission alone repre- 

senting the true buds, and Laninue has recently adopted this view. 
The entoderm-sac is the seat of the most important transformations 

through which the bud develops into the young Ascidian. This sac 

increases in size and its anterior margin becomes trilobed (Fig. 236). 

The middle lobe must be regarded as the rudiment of the branchial 

sac (pharynx), while the two lateral parts represent the rudiments of 

the peribranchial sacs. These sacs are, therefore, in the bud of 

Distaplia, distinctly entodermal in their origin. 

The peribranchial sacs grow round the sides of the middle ves- 
icle and, at the same time, a process grows from each sac towards 





No. XXVla.) the sexual cord is continued 


*[In the Didemnidae (Piz 
D.) 


from the parent into the bud. 





ASCIDIACEA—FORMATION OF ORGANS IN THE BUD, 465 


the dorsal middle line (Fig. 236 4, »). These processes grow 
towards each other and fuse, and thus the single atrial cavity arises 
(Fig. 237, cl). In the meantime the two peribranchial sacs have 
become completely disconnected from the central cavity. 





The peribranchial sacs arise in a slightly different manner in Perophora 
(Kowatrvsky, Ritter), in which form, instead of separating as two distinct 
sacs and fusing together at a later period, o single bilobed sac separates from 
the inner vesicle ; thus the definitive atrial cavity is formed at an earlier 
period, the development being apparently abbreviated. SFELIGER also states 
that, in Clarelina, an unpaired vesicle becomes abstricted from the dorsal side 





Fie, 236.—Two stages in the development of the buds of Dixtaplia atylifera (after 
Kowa: -l. younger, B, older stage. «, alimentary canal ; dr, digestive 
gland ; 7, rudiment of the stolon ; 7, genital rudiments ; «, nerve-tube; p, right 
peribrainchial sac. 





of the enteric sac, which persists as the atrium and, growing round the sides 
of the pharynx, forms the peribranchial sacs. Hort (No. 59) again, recently 
stated that, during the budding of Botryllus, a saddle-shaped vesicle becomes 
separated from the inner vesicle of the bud and gives rixe to the atrial cavity 
and the paired peribranchial sacs. 





At the time when the peribranchial sacs form, an unpaired caecum 
grows out from the posterior end of the entoderm-vesicle (Fig. 236 
A, d); this soon bends to the left and thus becomes the rudiment. 
of the intestinal loop (Fig. 236 4, /) in which latter the different 
sections (vesophagus, stomach and intestine) can be more distinctly 
made out. A diverticulum (dr), rising from the pyloric region, 
develops into the rudiment of the so-called digestive gland (Fig. 237). 






L 


is 


The rudiment of the genital organs appears dorsally to the intee 
tinal loop immediately below the nerve-strand (Figs. 238 £, g, and 
237, g). The strictly median position of this rudiment is specially 
distinct in the buds of Clavelina, where it appears only in later 
stages. It apparently takes its rise as an agglomeration of closely 
crowded mesenchyme-cells, in which a cavity nevertheless soon 
appears ; this is the primary genital cavity round which the cells — 
become grouped like an epithelium. For the development of the 
male and female genital organs from this uniform rudiment we must 
refer the reader to p. 379. | 


468 TUNICATA, 





Fig. 239.—Three consecutive ontogenetic stages in the so-calli 
(after Kowangvsky), 4, dorsal view of the anterior part of 
of an older stage ; C, dorsal view ofa still more advanced. vanced stage. 
ment; ec, ectoderm ; ea, entoderm ; ” epicardial process; m, 
nervous system ; p, peribranchial adc 


bud of 4 


Important observations on the condition of the pericardial yesiele | 
and the epicardial tube have been made by vaw Benepen and Junin. | 
Following these authors, we shall first deseribe the condition of « 
more fully developed bud traced in a series of cross-sections, 
last section of this series (Fig. 238 7) passes through the 
U-shaped intestinal loop (i) and, ventral to this, the stolonie 
(st) is seen, In anterior sections, we find that the latter 
connection with the pericardial vesicle (Fig. 238 D, pe). 4 
(%) here also has arisen through the invagination of the 
pericardial sac (pe). A section cut further forward (J 
shows the double or forked end of the epicardial sae 
im close contact with the pericardial vesicle. Further 
pericardial vesicle decreases in size (Fig, 238 C@, pe) 











ASCIDIACEA—FORMATION OF ORGANS IN THE BUD. 469 


disappears (Fig. 238 B), while the epicardial sac (¢p) can be followed 
forward to the point at which its wide paired aperture (Fig, 238 4) 
enters the pharynx (branchial 
sac). In other words, the epi- 
cardial sac arises from paired 
apertures situated ventrally to 
the entrance of the oesophagus 
and extends backward, its forked, 
blind end becoming applied to 
the pericardial vesicle. The 
latter is continued direct into 
the stolonic septum, At an 
earlier stage, the forked end of 
the epicardium is found to he 
continuous with the wall of the 
pericardial vesicle, and the cavity 
of the epicardium of the bud 
communicates at this point with 
the pericardial cavity. Conse. — Kow. 
quently, the cavity of the cenit: Piseeial Hewes ks, 
stolonic septum, the pericardial pa Pic Arata SIMO. PPE 
sac and the epicardium are 

merely differentiated portions of one and the same system of cavities, 
Tn the larva, however, according to vaN BexepEN and Jucr, the 
relation of the parts is different (p. 368).* 

With regard to the further development of the bud, we can merely 
briefly mention that the gill-clefts appear as perforations of the 
contiguous walls of the pharyngeal sae and the peribranchial sacs ; 
that the muscles are derived from strands of mesenchyme-cells, and 
that the branchial and atrial apertures owe their origin to ectodermal 
invaginations which become connected with the pharynx and the 
atrium. ‘The endostyle appears in the form of « fold of the ventral 
wall of the pharynx. 





Fio, 240,—] 
so-onlledd 






* [Jou (No. XVIL) has recently investigated the origin of the pericardium 
in Distaplia, and finds a condition which differs somewhat from that described 
above as occurring in Clavelina. As in Clavelina, a pair of epicardial (pro. 
cardia!) tubes prow out from the pharynx on either side of the oesophageal 
Aperture; of these the left becomes divided transversely into an anterior 
portion, which then fuses with the left epicardial tube to form the epicardial 
sac, and a posterior portion which gives rise to the pericardium and heart. 
From: the recurved end of the right sac the primary bud is given off before 
the tube fuses with that ou the left to form the median epicardial sac, —Ep.] 


470 TUNICATA. 


Ontogenetic processes altogether similar to those just described are 
found in cases where the detached parts of the post-abdomen in the 
Polyclinidae regenerate (Fig. 239). Here also the central entoderm- 
vesicle is the first seat of transformation. As has already been men- 
tioned (p. 454), the first change to occur is a widening of the proximal 
end of the epicardial septum (Fig. 239 8). An entoderm-vesicle is 
in this way formed in the proximal part of the young individual, and 
this is continued backward into the part of the stolonic septum which 
did not widen. The proximal dilatation is the rudiment of the whole 
alimentary canal of the new individual, while from the non-widened 
part are derived the epicardial sac (Fig. 239 B, ep) and probably 
also the pericardium. The entoderm-vesicle here also divides up in 
the same way as in the bud into three lobes (Fig. 239 A and 8), the 
middle lobe being the rudiment of the branchial sac and the two 
lateral lobes the rudiments of the peribranchial sacs. The complete 
abstriction of the latter, their interconnection (Fig. 239 C) to form 
a median unpaired dorsal part (atrium), and the development of the 
gill-clefts all occur in the same way as in the formation of buds 
The rudiment of the alimentary canal is here also a small, unpaired 
caecum (Fig. 239 B, d), which grows out at the dorsal side in the 
posterior part of the entoderm-vesicle and curves into the shape of 
the letter U. In the development of the more important systems 
of organs, we thus have here complete agreement with the pmcees 
of gemmation. 


2 Doliolidae. 





We have already mentioned (p. 385) that two stolons are apparently 
found in the * nurse” (blastozeoid) generation of Ddidaae. one ventral 
(es) and the other dorsal (Ze. the dorsal outgrowth de i 
much greater size than the true ventral stolen, and finally 
to hetermorphous individuals kuown as lateral 
(the gastrozovids and phorozooids:. The two st 





si usiidle bunks 








nS Vary xTeatiy in 
structure. As will be seen later. the scalled dorsal stok 









to the buds derived from the true ventral p 
it is better to restrict the tern stelon te 
speak of the dorsal structure as the dora 
The ve ntea std Figs. ISO, rp) B83: Bo: oe. foreriy 
kuown as the neette-like onnin, and first reeounised by GBOS REN 
Tein its true charmeter as proliferating << 

















DOLIOLIDAE—AS8EXUAL REPRODUCTION, 


471 


shaped projection rising from an ectodermal depression ; in cross- 
section, this is found to be composed of seven parallel cell-strands 


(Fig. 242) four of which (4 and ») are 
arranged symmetrically in two pairs, 
while the other three (a, z, and m) are 
unpaired. Groppen and Unsaniy differ 
considerably as to the origin and signifi- 
eance of these seven strands which, with 
the ectoderm that envelops them, form 
the primary rudiment of the | buds. 
These two authors agree that two cones 
grow downwards from both the pharyn- 
geal and the atrial cavities of the 
“nurse” (Fig. 241, ph and cl), enclosing 
between them a mesoderm-mass (we), the 
origin of whieh has already been traced 
(p. 387; see also Fig. 182 B, 1 and 
ms’, yx 387). According to Unsanin, 
the stolon is thus originally composed 
of five strands, two pharyngeal and two 
atrial strands and a middle mesoderm- 
strand (Fig. 241). The number of these 


NIN). 
ut-anitul ; ct’, out 
‘all 


weynx of the paren 
Satgrowth of the wall of the 


pharynx. 





strands becomes augmented to seven when the atrial strand (c/’) 


becomes bent on itself, its reflexed end 
giving rise to a new pair of strands (c/"). 
The fusion of this pair, according to 
Unsanty, yields the future neural rudi- 
ment (x), while the pharyngeal strand ( p) 
yields, by dehiscence, an unpaired middle 
strand (#) in which this author sees the 
rudiment of the pharyngeal cavity of the 
bud. The unpaired strand (7) is said to 
represent the pericardial rudiment, while 
the pharyngeal strands (») change into 
the genital rudiment, and the atrial 
strands (4) into those of the muscle-plates. 

According to Grospgy, on the con- 
‘trary, the pharyngeal strands (») represent 
the rudiment of the pharyngeal cavity 
and intestine of the bud, the atrial strands 





Fic. 242,—Transverse section 
through the ventral stolon or 
a primitive bud of Juliolun 
( m after Gnoppes and 
UIJANIN).  ¢¢, ectoderm ; h, 
rwusole-rudiments ; i, peri- 
cardial radiment ; a, newral 
rudiment; p, genital rudi- 
mont, pharyngeal rmdi- 
ment (UisANIN). 


(&) the later rudiment of the atrium, and the unpaired mass x 


bi 


472 TUNICATA. 


(resulting from the fusion of paired strands) is assumed to be the 


genital rudiment. 








wn ¢ 
Fic, 243,- Dorsal view of the posterior part of the 
body in a large * nurse" (blastozooid) Dulinfua 
(after BaRRots). 7, lateral Inds (gastrozooids) ; 
im, median buds (phorozooids) ; mss", four 
posterior muscle-hoops ;p, perieardinm ; r. 





Tosette-like organ ; sf, ventral stolon ; at’, dorsal 
outgrowth ; 4, primitive buds wandering to the 
ids. 


veutral side of the “* nurse"; 1’, primitive 
wandering to the dorsal side: 1, prin 
bads on the dorsal outgrowth, 








The unpaired strand m is regarded as the rudi- 


ment of the pericardial sac, 
and the mass n, which from 
the first is unpaired, as that 
of the nervous system. 

The buds are produced 
through the transverse con- 
striction of the ventral 
stolon (Fig. 243, r and st), 
from which they eventually 
become completely de- 
tached. In structure, they 
resemble the stolon itself, 
being composed of an ecto- 
dermal envelope and the 
seven strands above de 
scribed. They are not 
capable, however, of de- 
veloping further on the 
ventral stolon. GROBBEN 
has therefore regarded the 
ventral stolon, which is 
evidently homologous with 
the proliferating stolon of 
the other Tunicates, as a 
vestigial stolon, and con- 
siders the buds produced 
by it as abortive. 

A cross-section of the 
dorsal outgrowth (Fig. 243, 
at’) of the “nurse” genera 
tion (blastozooid) reveals 
an essentially — different 
structure (Unsantn). Like 
the ventral stolon, it is 
covered superticially by a 
layer of ectoderta, thickened 
on the dorsal side, but the 
interior of this outgrowth 


fis occupied merely by two 


DOLIOLIDAE—ASEXUAL REPRODUCTION. 473 


blood-vessels separated by a purtition-wall of connective tissue. The 
transverse section of this outgrowth, indeed, strikingly recalls 
sections through the stolon of certain Ascidians, although it must 
be noted that, in these latter, the partition-wall is formed by an 
entodermal lamella (epicardial lamella) of which nothing can be seen 
in Doliolum. ; 

The buds which develop from the dorsal outgrowth as lateral and 
median buds (Fig. 243, /, m) do not arise independently from this 
structure. GROBRBEN conjectured that they were all abstricted from 
a “primitive bud” found at the base of the stolon. Uxsanin, on the 
other hand, observed that the parts which become abstricted from the 
ventral stolon are capable of wandering along the surface of the body 
of the parent, and in this way reach the dorsal outgrowth (wu, x’). 
These wandering cell-masses are the primitive buds, from which the 
lateral and median buds of the dorsal outgrowth arise by constriction. 
The primitive buds that first reach the dorsal outgrowth remain at 
its base and, through fission, produce buds which become arranged 
along each side of the stolon, developing into the lateral buds or 
gastrozooids (/) ; consequently the buds towards the distal end of the 
row are more highly developed than those near its base. Those 
primitive buds which reach the dorsal outgrowth later are distributed 
along the whole of the middle dorsal line (w’’), and by gemmation give 
rise to the median buds or phorozooids (m). These buds are arranged 
in groups alternating on either side of the row of primitive buds (w”). 
The buds of each group develop unequally, but here also there is 
an advance in development towards the distal end of the stolon. 

According to Unsantn, the ventral stolon is thus the only prolifer- 
ating stolon of the ‘ nurse” generation ; the dorsal outgrowth cannot 
be regarded as a true proliferating stolon, but is merely a body-process 
serving for the nourishment of the buds attached to it, which can be 
traced back to the mantle-vessels of the Ascidians. 


The Doliolidae thus show an early detachment of the buds from the 
proliferating stolon such as takes place in the Distomidae (pp. 456 and 463), in 
which family also the detached buds are able to multiply further through 
fission. The wandering of the primitive buds and the development of their 
descendants in their secondary position in the Doliolidue are very remarkable. 
The statements made on this subject have been confirmed for Doliolum by 
Barkols (No. 77), and similar processes have been observed in Anchinia and 
Dolchinia, so that little room is left for doubt on this point. According to 
Uxsanty, the buds are able to move by means of pseudopodia-like processes 
of their ectoderm-cells. According to Barkors, on the contrary, there are, 
ou each side of the ventral stolon of Doliolum, large amoeboid cells, arranged 


DOLIOLIDAE—ASEXUAL REPRODUCTION. 475 


ventral process (s/) near the posterior end of the body ; this process 
is derived from the peduncle counecting the median bud with the 





Fie, 245.—The three generations of Doliotum Millleri (utter GKONBEN). A, young 
“nurse” or blastozooid; 14, the phorozooid ; C, sexually mature individual or 
gonorooid. d, alimentary canal; as, dorsal outgrowth of the “nurse” form; 4 
endostyle; #, peripharyngeal band; y, buds of the sexual generation; h, testi 
Aa, integumental sensory organ; hx, gill-clefts; , ganglion ; of, auditory organ ; 
wm, ovary; p, pericardial vesicle and heart; «/, peduncle for the attachment of the 
onosoolds (7) to the phorozooid ; ex, ventral stolon of the nurse’ form (so-called 
rosette-like organ). 








476 TUNICATA. 


dorsal outgrowth of the “nurse,” and carries the buds of the sexual 
generation or gonozooids (g). The latter was formerly thought to be 
produced from the phorozooid itself, and these buds, when free, were 
consequently known as the second “nurse” generation. The sexual 
generation, however, is produced from a primitive bud which has 
become attached to the base of the peduncle of the phorozooid. This 
bud, according to Uxsanry, is not yielded by the phorozooid itself, 
but is a direct descendant of the primitive buds (Fig. 243, «”) which 
wandered over to the dorsal outgrowth of the first “nurse "’ genera- 
tion. Utsantn therefore regards the median bud merely as the foster- 
mother of the buds which develop into sexual animals. 

There is thus, according to Unsantn, in the whole cycle of genera- 
tions of Doliolum, only a single true proliferating stolon, viz., the 
ventral stolon, which alone is capable of producing primitive buds. 
All the individuals derived from these primitive buds which attain 
development represent, according to this author, only the heterv- 
morphous forms of one and the same generation, the sexual gener- 
tion either, as nutritive animals or as foster forms, losing their genital 
organs, or else changing into actual sexual animals (Fig. 245 €). 

According to GRoBBEN, on the contrary, who practically follows 
GEGENKAUR, the cycle of generations of Doliolum consists of two 
successive asexual generations and one sexual generation. GROBBEN 
consequently regards the form yielded by the egg, which differs 
essentially from the sexual animal, as the first “nurse” form 4. 
This gives rise to the two heteromorphous forms (lateral buds Z, ant 
median buds ./): of these. the median buds, in their capacity of 
second “nurse ” generation, produce the sexual generation 4G. The 
abortive buds yielded by the ventral stolon represent a lateral branch 
of the eyele of generations (A). These two opposite views may be 
tabulated as follows :- 


Alternation of Generations in Doliolum. 


GROBRED's view : Tianis’s view : 
A (first “nurse ” form) A ("nurse ” form) 
K- 
L. = M (second * nurse ~ form) Lo + M + G (sexual generation! 


1 
G (sexual individual) 

We see from the above that if ULranty’s view is contirmed. the 

alternation of generations in Defiolun closely resembles that in the 


ALTERNATION OF GENERATIONS IN DOLIOLUM. 477 


Salpidae, consisting in both cases of an asexual generation followed 
by a sexual generation. The only difference between the two would 
be that the primitive buds produced by the asexual generation, 
in Doliolum, multiply by fission, and that the sexual generation 
develops in three different forms (L, M and G). In this way also 
the fact that the median buds entirely agree in structure with the 
sexual generation would be explained (Fig. 245 2 and C). 

We have still to describe the development of the young buds after 
their detachment from the primitive buds. According to Unsanin, 
all these buds, whether lateral, median or sexual, develop more or 
less in the same way, so that an account of the development of the 
lateral buds will suttice. The young buds, immediately after abstrie- 
tion, resemble in structure the primitive bud and the ventral stolon, 
consisting of an external layer of ectoderm and of the seven strands 
mentioned above. We have already mentioned (p. 471) the different 
views held by GRoBBEN and ULJANIN as to the significance of these 
seven strands in connection with the further development of the bud. 
We have as yet comparatively few statements as to the way in which 
the young bud develops out of these seven primary rudiments, and 
further investigation of this point is very desirable. 

The young bud (Fig. 246 4), from the time when it becomes 
detached from the primitive bud, is a completely independent organ- 
ism enclosed in ectoderm, but attached externally, like a parasite, 
to the body of the “nurse “ or to the foster form. This attachment 
is brought about by means of a thickening of the ectoderm (ec). In 
the youngest buds observed by Unsanix, the body was already 
elongated, and the organs, as compared with the seven cell-strands, 
had already changed their positions. The dorsal side can now be 
distinguished by the presence of the large rudiment of the nervous 
system (n), while, on the ventral side, the pericardial rudiment (p) 
is to be observed. Between these two, the pharyngeal rudiment (ph) 
can be seen, while the paired genital rudiment, forming a common 
cell-mass, has shifted into the neighbourhood of the point of attach- 
ment of the bud. The ectodermal invagination (el), behind the 
nervous system, represents the rudiment of the atrium. This is one 
of the principal points in which Unsantn’s description differs from 
that of GRoBBEN. According to the latter author, the atrium arises 
from paired rudiments (the strands & in Fig. 242) already present in 
the primitive bud. At the two sides of the body, the muscle-plates 
(m), lying in close contact with the ectoderm, have extended con- 
siderably. 








478 TUNICATA. 


In the course of further development a cavity forms in the pharyn- 
geal rudiment and gradually enlarges (Fig. 246 B, ph) ; this soon 
opens externally through an aperture (branchial aperture, ¢) resulting 
from an ectodermal invagination which forms opposite to the atrial 
aperture. The muscle-hoops which lie in the neighbourhood of the 
atrial and branchial apertures now become separated from the muscle. 
plates. The pharyngeal cavity gives off a pair of flat lamella-like 
diverticula (2) towards the dorsal side, and these, as GROBBEN had 
already observed, embrace the neural rudiment (n) laterally. | Acoord- 
ing to Uxsantn, these diverticula are concerned principally in the 










Fro, 246 --Diagrams illustrating three st 
Dotiolum, seen from the side(.1 and B, 
d, enteric rudiment ; 
atyle-rudiment; 9 
growths of the 
ment > 


in the development of the lateral buds of 
ter ULJANIN ; C, after GROBBEN), ¢/, atrium; 
ectodermal thickening ; es, endo- 
enital ruc é rat || aperture ; &, gill; 7, Interal out- 
ine of the muscle-phites ; 2, neural rudi- 
rudiment ; ph, pharyngeal rudiment. 












formation of the branchial lamellae. A process (d) running back 
from the pharyngeal cavity develops into the intestine of the bud, its 
blind end becoming applied to the wall of the dilating atrial cavity 
(el). The latter extends specially towards the sides of the body, 80 
that, as GROBBEN observed, at a certain stage it resembles a pair of 
spectacles. Its lateral extensious become applied to the wing-like 
processes of the pharyngeal cavity (/). This juxtaposition of the 
atrial and pharyngeal walls gives rise to the branchial lamellae (Fig. 
246 C,é), in which the gill-clefts then break through. The rudiment 
of the central nervous system undergoes a transformation closely 





ALTERNATION OF GENERATIONS IN DOLIOLUM. 479 


resembling that described above for the larva on leaving the egg 
(p. 386). An anterior narrowed portion becomes the ciliated pit, 
4% posterior process changes into an unpaired nerve running from the 
ganglion, while a third part of the rudiment develops into the gang- 
lion and the sub-ganglionic body. The pericardial sac (p) and the 
heart seem, as in the larva, to develop according to the type preva- 
Jent among all Tunicates. The genital radiment (y) degenerates in 
the lateral buds. It can still be recognised for some time to the left 
side of the intestinal loop as a mass of cells. In the buds which 
become Sexual individuals this rudiment breaks up into two unequal 
portions, the anterior smaller part developing into the ovary and the 
posterior lurger portion into the testis. 

The later differences found in the lateral and median buds and the 
sexual individuals are explained by the varied forms which these 
finally attain. The median buds and the sexual individuals tend to 
assume the characteristic barrel-shape, while the lateral buds increase 
in height and, as mentioned ubove, adopt the somewhat asymmetrical 
spoon-shape, owing to the dilation of the atrial aperture and 
cavity. 


‘Two more remarkable and insufficiently understood genera, Anchinia and 
Dolehinia, which, in the structure of their gills, form a transition between 
Pyrowoma and Doliolum, have still to be added, In these genera only parts 
of detached stolons are known, the asexual “nurse” form, developed from 
the egg which produced the stolon, being still undiscovered. We shall have 
to compare these stolons with 
the dorsal outgrowth of the first 
“nurse” generation of Doliolum. 
Asa rule the stolon, in Anchinia 
and Dolchinia, consists of a tube 
which, in cross-section, is round 
{the colonial tube, Pig. 247, ¢), 
und seems to be formed of a 
‘single layer of flat ectoderm-cells. 
The Interior of the tube is filled Fre, 247.— matic oroar-section through 
with a gelatinous mass, in which the colonial tube (dorsal outgrowth) of 
ase embedded. mesoderm -cells Dolchinia (atter Konorxery), ¢, colonial 
varying insbape, Ths external ‘via’ tan’ "© the 8 
surface of the ectodermal tube 
which is covered by a cellulose mantle carries the various buds (2) which, in 
later stages of their development, seem to grow out on stalks from thickened 
parts of the ectoderm. The buds are thus here, as in Doliolum, ouly attached 
to the exterior of the so-called stolon. They appear irregularly arranged along 
the stolon, quite young buds being found among others half-developed, and 
others again fully developed, In a transverse section of a stolon, however, the 





480 TUNICATA. 


youngest buds are found to occupy the dorsal middle line, while the older 
buds shift to the sides of the atolon (Fig. 247). " 

Three different forms have been found in the colonies known of Anchinia, 
but these are regarded by Barrois (No. 77) as fragments of the same stolon in 
different stages of development. 

I. There are fragments with zooids which, even when developed, remain 
comparatively small, which are without genital organs and are incapable of 
reproducing themselves by budding. These zooids are distinguished from 
those of the sexual generation (III.) 
by the absence of the taree pigment- 
spots and of the papilla-like pro- 
cesses above the apertures of the 
body. An accumulation of pigment 
is found, on the other hand, at the 
base of the peduncle (Fig. 248 4, 
pda). On the dorsal side of the tube 
which bears these zooids a slightly 
coiled thread is found ranning longi- 
tudinally (Fig. 249, st); this consists 
apparently of ectoderm and ento- 
derm (Fig. 249 B), and is assumed 
by Barros to be the actual pro- 
liferating stolon, from which the 
buds of this generation grow out 
laterally. 

I. Fragments with zooids re- 
sembling in shape the sexual forms 
(III.) in which also the rudiment» 
of genital organs appear. The-e 
rudiments. however, degenerate 
later. These zooids, which may 
be compared to the phorozooids of 
Doliolum, do not seem to reproduce 
themselves either sexually or asexu- 
ally. They do not, however, directly 
nourish the buds of the sexual 
eration Of generation, for these grow out inde- 
; By sexual generation (after ri 
ii alimentary. vanals +s, pendently on the colonial tube. In 

o jk. gill; p, papilla above the — the tube on which thexe zvoids are 

branchial ‘aperture; ‘p’, papilla above found, the structure above described 

the atrial aperture ; 7,’ peduncle. : Apa ig 
as the proliferating stolon is ne 
longer to be seen ; but there are clusters of very smal] buds which Barrot: 
holds to be derived from the disintegrated proliferating stolon. 

III. Fragments with sexually mature zooids (Fig. 249 3). Each of thee 
zovids ix distinguished by the possession of a papilla-like process ;p, p') above 
the branchial and atrial apertures, that over the latter being specially large. 
On these processes, there are accumulations of pigment ; a third pigment-spet 
ovcupies the middle of the body. These zooids are further distinguished by 
the great depth of the body and the abbreviation of the endostyle (es). The 



















ALTERNATION OF GENERATIONS IN ANOHINIA, 481 


young buds from which they are derived are found scattered between the 
developed zooids on the colonial tube. 

Barpots compares the zooids of type I, to the lateral buds of Doliolum, and 
those of the second type to the phorozooids or foster forms of Doliolum, The 
three different forms of the asexually produced generation are believed to 
develop in succession in the colony of Anchinia, the one replacing the other. 
On the youngest stolons, zooids of the first type develop; later, when the 
proliferating stolon proper breaks up into portions, only zooids of type TI. 
develop, and these finally are replaced by the sexually mature forms. 

The budding of Anchtwia has been described most in detail by Bannots 
(No. 77) and is in many respects of great interest, It appears that the develop- 
mont of the three types of buds takes place as a rule in a very aniform manner, 
although considerable 
variety prevails in the m 
time and manner of de- 
velopment of the organs 
into which we cannot 
here enter further. In 
Doliolum, the prolifer- 
ating stolon is composed 
of & number of longi- 
tndinal strands and, ¢ 
consequently, even the 
youngest buds show the 
separate rudiments of 
the most important 
organs, bub the stolon 
of Anchinia (Fig. 249 1) = 
is composed merely of B 
ectoderm and an inner 
cell-mass called by atin 
Bangows entoderm. The rs beer os stolon of ante iB, oe of 
mame structure is ex- Im PROTON AIRE SOLE; OES “CURA Ly . 
hibited by the very Toke tuitions, ethene a 
smal] or youngest buds liferating stolon. 
in which an ectodermal 
Jayer and a central cell-mass can be distinguished. The latter becomes 
differentiated, in a way as yet insufficiently known, into the nervous system, 
the enteric canal (pharynx + intestine), the pericardial vesicle and (in 
types II. and IIL.) into the rudiment of the genital organs which appears 
very early, Certain features of the later development of type I. are of special 
interest, as showing close resemblance to the manner of development of the 
Ascidian embryo, ‘The nervous system is found in the form of a tube running 
along the whole dorsal side of the bud (Fig. 250 A,n). The anterior part 
of this tube gives rise to the ganglion and the ciliated pit, while the posterior 
part changes into an unpaired nerve-strand (Fig. 250 B) which runs back- 
ward and ends in a visceral ganglion. This nerve no doubt corresponds to 
the strand observed by Unsaxry in Doliolwm and called the branchial nerve, 
Tt may be regarded as the homologue of the “ cordon ganglionnaire viscéral " 

1 


wt A 








recall the atrial vesicles of the Ascidian larva and | 
in the embryo of Pyrosoma. These paired ectoder: 








Fie. 251.—Portion of « colonial tube of 
Dolehinia with its 2ooids (after Konor- 
NEFF). a, points of attachment of older 
nooids; c, colonial tube; y, buds giving 
rise to the sexual individuals ; g’, priiuitive 
bnd of the sexaal gemmae; v, wandering 
primitive buds; 2, z00id. 








ALTERNATION OF GENERATIONS IN DOLCHINIA. 483. 


pf the endostyle (es). From this diverticulum, the pericardial vesicle becomes 
separated in late stages. It is probable that a part of the diverticulum is 
retained here as an epicardium (p 368,). 

Of the form known as Dolchinia (Kornornerr, No. 82), the only colonies 
which have been found have zooids corresponding to types Il, and IIL. of 
Anchinia (i.c., foster-forms and sexual gemmae, Fig. 251). The individuals 
belonging to type Il. (phorozooids) are here closely crowded on the common 
colonial tube, while the sexual gemmae (g) develop on the peduncles of the 
foster forms (in the'same way, therefore, as in Doliolum). These foster forms 
(phorozooids) of Dolchinia (2) become very easily detached from the colony 
and then lead an independent pelagic existence. In the same way, the sexual 
individuals sever themselves from the phorozooids. Migrating primitive buds 
(u) may be seen on the colonial 
tube. These are able to move 2 A a 
from place to place (as was 
stated by Barrors for Doliolum 
and Anchinia) by means of 
large, amoeboid cells (c) adher- 
ing externally to the bud on 
each side (Fig. 952 A,a), Small 
secondary portions (b) become 
detached from the primary 
primitive buds by fission, and 
these either attach themselves 
to the colonial tube itself and 
grow into foster forms (phoro- 
sooids), or else settle on the 
peduncle of one of the develop- 
ing foster forms and there 
change into primitive buds of 
the sexual gemmae carried by 


that individual (Fig. 251, 9). bac Foapeey eign sag is of Dolchinia 
( two. deta ds (b); J, Transverse 
The primitive bud seems to ection throngh an attached tnd of Dolehowia 
produce only sexual gemmao, after Konorxnyy). a, primitive bud; }, 
and does not itself develop letached buds; ¢, amoeboid transporting 
further, For the further de. “M81, ¢¢ eotoderm'; m, muscle-rudiments ; 
. ph, pharyngeal rudiment; st, epithelium of 
velopment of the buds, which the colonial tube ; , mass of large cells. 


has not been made out quite 
clearly, we must refer the reader to the statements of Koxorxnvy (No. 82), 
Here also only an outer and inner layer of cells can at first be dis- 
tinguished. In the latter, a mass of large cells (Fig. 251 B, x) soon 
from a mass of small cells. The large cells are said to be the 
rudiment of the nervous system and the genital organs, while the mass com- 
posed of small cells breaks up into three strands, the median strand (ph) 
representing the rudiment of the pharynx, while the lateral strands are 
thought to represent the muscle-rudiments. The atrium arises as an ecto- 
dermal invagination, and the pericardial vesicle as a diverticulum of the 
pharynx. 











PYROSOMA—DEVELOPMENT OF THE PROLIFERATING STOLON. 485 


large cells are seen in it which can be recognised as young egg-cells. 
The rudiment of the genitul strand has, in its turn, become abstrieted 
from the genital rudiment (0, 1) of the parent (of. ma, in individuals 
1 and I), 





Fra, 258-—A clin of three individuals of Pyrowma (after Sunuione), 1; youngest, 


proximal bud ; 7?, middle and Z/7, oldest, distal bud (nearly fully developed). 2, 
point at which the endostyle-process of the parent enters ; d, endostyle- or entoderm- 
process ; de, rudiment of the alimentary canal ; dm, elongate cell-mnass ; ¢, rudiment 
of the atrial aperture ; eb, elaeoblast ; Hc, ectoderm of the parent ; ec, ‘ectoderm- 
plate of the stolon-rudiment ; #s, endostyle of the parent ; es, endostyle ;” fy, ciliated 
pit g, ganglion ; fh, teatis; hd 'intostine ; As, heart; iy rudiment of thé branchial 
aperture ; &i, atrium ; ks, gill-clefts ; {f, internal longitudinal gill-bars ; Zm, lenti- 
cular phosphorescent organ ; m, stomach ; ma, genital strand ; n, rudiment of the 
nervous system ; 0, ovary (égg-follicle with egg); oe, oesophagus ; p, dotted line 
indicating the boundary of the peribranchial sacs ; pe, pericardium ; rz, languets ; 
¢, tentacle-rudiment ; 0, duot connecting the enteric cavity of the second’ individual 
with that of the third. + 


These two rudiments (those of the entoderm-process and the 
genital strand) can also be recognised in a transverse section through 
this region of the body of the parent (Fig. 255). We then also see 
that the entoderm-process is still accompanied by isolated mesen- 
chyme-cells (Fig. 254, ms). At the two sides of the process especially, 
mesenchyme-cells can be seen arranged in two strands (ms). The 


486 TUNICATA. 


strand on the right is continued as far as the pericardial vesicle of 
the parent. These strands are the so-called mesoderm-strands of the 
proliferating stolon mentioned above, the development of which in 
the four primary Ascidiozooids was followed by SaLENsky (No. 74). 
The part played by these mesoderm-strands in the further develop- 


@o 


rs 


Fia, 254.—Transverse sec- 
tion through the ento- 
derm - process (en) of a 
very young stolon-rudi- 
ment of Pyrasoma (al 
SBRIIGRR). m4, xurrou 
ing mesenchyme-cells, 








ment of the proliferating stolon and of the 
buds is still obscure, and therefore no 
further note will be taken of it. 

That part of the ectoderm towards which 
the entoderm-process is directed (Fig. 253. 
ec) seems somewhat thickened even in the 
early stages. ‘I'he actual stolon now begins 
to form in this region as a rapidly increasing 
swelling. The conical process that results 
(Fig. 256 A) is the stolon at the distal end 
of which transverse constrictions soon lead 


to the abstriction of individuals (Fig. 256 C). 
In transverse sections through a developing stolon (Fig. 255), the 
rudiments of the peribranchial tubes (p) can already be seen at either 
side of the entoderm-process. How these rudiments arise is not yet 
accurately known, but as they are found connected by their distal 
ends in a certain way 
with the — genital 
strind, SEELIGER is 
inclined to derive 
them from the latter. 
He therefore reganls 
the peribranchial 
tubes in the buds of 
AS meso 
structures, 
although, in the 
Cyathozooid and in 
the first four Aseidio- 
zooids, they are un 
doubtedly derived 
SIudging by what is known of the development 
of these organs in other Tunicates, and of the relations of the senital 
rudiment in all other animals, it appears to us in the highest degree 
improbable that there is any connection between the two. structures. 
‘ey peribranchial tube and genital strand, or between the latter amd 
the nervous system]. 


Pyrowma 


dermal 







ction through two very young 
Of Pyrosona (after SEBLIGER), 





genital strand; 0. voung wgeeell: p. 
branchial tubes, 


from the ectoderm. 


PYROSOMA—DEVELOPMENT OF THE PROLIFERATING STOLON. 487 


The rudiment of the nerve-twhe of the stolon also, according to 
Seevicer, is derived from the genital strand. In very young stolons 
(Fig. 256 A) the distal end of the latter appears to bend round to 
the upper side, (The lower side of the stolon is marked by the 
position of the genital strand y), This upper part of the genital 
strand becomes, in the further course of development, separated 
from the lower part, and, according to Seenicer, becomes the 
rudiment of the neural tube (Fig, 256 C, n), a lumen very soon 
appearing inside it. 

SeeiGex thus holds that not only the genital organs of the bud 
but also its peribranchial tubes, and a large part of all ita mesodermal 
structures, are derived from the genital strand. The group of cells, 





Fe, 266,—Th ih in the dod ment of the proliferating stolon of Pyrvmma 
(uttar Su nC) the separation of the two individuals (7 and 21) is already 
indicated. ppt , ectoderm ; es, endostyle of the parent; gy 

strand ; hs, first cr m, rudiment of the alimentary canal proper 5 ™, 
rudiment of the neural tube, 

which we described as the simple rudiment of the genital strand, has 

thus, in his eyes, a far wider significance in the development of the 

proliferating stolon. He has therefore designated it as the germ- 
strand or the mesodermal germ-mass. 


‘The fact that SreriGER traces back the peribranchial tubes and the neural 
tube in the buds of Pyrosoma to the mesoderm cannot fail to awaken surprise 
when it is remembered that the rudiments of these organs are undoubtedly 
derived from the ectoderm, not only in the Cyathozooid but also in the four 
primary Ascidiozooids. In our attempts to interpret the structure and sig- 
nificance of the proliferating stolon, we naturally seek for agreement between 
the development of its buds and that of the first four Ascidiozooids. When 
we consider that the proliferating stolon must evidently be traced back to the 











PYROSOMA—FURTHER DEVELOPMENT OF THE BUDS, 489 


the enteric rudiment still connected with that of the next bud 
(Fig. 258, »). The distal individual of the stolon is always the most 
developed (¢f. also Fig. 267). When five individuals have become 
marked off on the stolon through the appearance of constrictions, 
the distal individuals always seems to become detached. More 
than five individuals are consequently never found on one stolon. 


B. Purther Development of the Buds. 


A fact already pointed out in connection with the development of 
the four primary Ascidiozooids (p. 407) must again be emphasised 
here, viz., that the longitudinal axis of the stolon does not coincide 
with the later longitudinal axis of the developing buds, but rather 
appears to lie at right angles to it (Figs. 258, 267). The longitudinal 
axis of the segments of the stolon changes into the dorso-ventral axis 
of the developed bud. The axis which becomes the later longitudinal 
axis of the body is one which we may imagine as cutting the 
longitudinal axis of the stolon at right angles, é.e., from the neural 
side to that of the genital strand, The ends of such an axis would 
be indicated by the rudiments of the branchial and atrial apertures. 

From the ectoderm of the stolon is developed the integument of the 
bud which, on its outer surface, secretes the cellulose mantle. Accord- 
ing to SEELIGER, this secretion takes place here in the way described 
for other Tunicates by Semper, Herrwic and others. When, there- 
fore, SALENSKY emphasises the fact that the first rudiment of the 
cellulose mantle is yielded by the Cyathozooid, the four primary 
Ascidiozooids ut first taking no part in the secretion of the cellulose 
substance, his remark applies only to the first stages of development. 
‘The further enlargement of the cellulose envelope proceeds from the 
Ascidiozooids. 

The branchial and atrial apertures (Figs. 253, 259, ¢) first appear as 
4imple ectodermal invaginations. These invaginations fuse with the 
wall of the branchial sac or atrial cavity, the apertures breaking 
through later at the points of fusion, Near the point at which the 
branchial aperture forms, the branchial sac (7.¢., the entoderm) gives 
off the first bud-like rudiments of the crown of tentacles that en- 
circles the entrance to this part of the alimentary canal (Fig. 253, ¢). 

The entoderm-sac of the bud first forms the Aranchial sac or 
pharynx. It has already been meutioned (p. 488) that this is cruci- 
form in transverse section (Fig. 257), two of the outgrowths being 
directed upward and two downward. The upward outgrowths are 
separated from each other by a median fold in which ean be recognised 








PYROSOMA—FURTHER DEVELOPMENT OF THE BUDS. 491 


the contiguous walls of the entoderm-sac and the peribranchial sacs 
(Fig. 258, p), but they very soon become elongate (Fig. 259) 
The inner longitudinal bars of the branchial sac (Fig. 253, (/) now 
develop at right angles to the clefts. As the slits break through 
chiefly in consequence of an outgrowth of the entoderm-sac, they 
wppear to be lined with entoderm. 

‘The two peribranchial sacs, which early lost their connection with 
those of the adjacent bud, by growing towards each other on the lower 
side of the stolon and fusing, give rise to the unpaired atrial cavity 
(Figs. 253, kl, 259, el), 

Finally, the outgrowths of the dorsal wall of the branchial sac 
known as the /anguets (Fig. 253, r2) develop. 

The radiment of the central nervous system appears at first as a tube 
running along the whole length of the wpper side of « stolon-segment 





Fig, 258,—Stolon of Pyrosoma with the rudiments of two individuals, 2 and 27 (after 
Swesicer). .1, side view; 2B, seen from the side on which the ital strand ix 
«i eb, rudiment of elueoblast; ec, ectoderm ; ex, endostyle-rudiment; g, 
genital strand ; As, gill-clefts ; m, rudiment of the stomach ane intestine; 1, nervous 

of bud J; 2’, nervous system of bud 27; p, peribranchial tubes ; s, rudiment: 
the lateral nerves (in B, seen in transverse section). 





(Fig. 256, 2); later, however, the proximal part of this tube develops 
into « large vesicle, while the thinner, distal part disappears, Two 
lateral outgrowths of the proximal part of the neural tube (Figs. 258, , 
259) can be seen very early (Fig. 257 A, sn); these soon change 
into hollow processes which encircle the alimentary canal and unite 
on its lower side. ‘These are the rudiments of the so-called /ateral 
nerves. A growth of the cells on the dorsal wall of the cerebral 
vesicle yields the rudiment of the ganglion proper, which later gives 
off the lateral nerves that run backward along the dorsal surface of 
the adult in the form of solid strands with terminal ganglionic 
swellings. The remains of the cerebral vesicle develop a connection 
with the branchial sac and become transformed into the ciliated pit 


PYROSOMA—FURTHER DEVELOPMENT OF THE BUDS. 493 


fibrillae increase in size, they become bund-like. In transverse sec- 
tion, they then appear radially arranged, while the centre of the 


musele-bundle is oecupied by 
the undifferential protoplasm 
and nuclei of the cells. 

The first rudiment of the 
pericardial vesicle is also traced 
back, by SEELIGER, toa small 
group of mesenchyme-cells 
which can be seen beneath the 





distal end of the right peri- yy, 260—Two early stages in the du 
branchial tube. In thie cell. ment of the rcepen teeny! in the bu 


{after SEKLIORR). “ev, entoderm 


group (Fig. 260, pe) a lumen (wall of the enteric rudiment); ec, ectoderm ; 


soon appears which is the 
pericardial cavity; at a later 


Line reper hae Pe, rudiment of the 


vesicle, 


stage, the rudiment of the heart (/z) arises through the invagination 
of that part of the wall of the pericardial vesicle which is in contact 


with the wall of the intestine (Fig. 261). 
The pericardial vesicle originally lies on 
the right side of the bud, but wanders 
later towards the median plane and thus 
reaches the dorsal side of the endostyle, 
process (Fig. 253, iz). It has therefore 
in Pyrosoma, a position unlike that 
oceupied by it in the other Ascidiacea, 
where, as deseribed above (p. 370), the 
heart lies on the ventral side of the 
endostyle-process (epicardium) in such 
way that the epicardial lamella brings 
about the closure of the cardial tube, 

Tn each bud, the genital strand (Fig. 
209, g) gives rise to the genital organs 
of the individual and to the genital 
strand of the stolon produced by that 
individual, At an carly stage, the 
genital strand is found to break up into 
a distal and a proximal part. The 
distal part, which is embedded in the 
elacoblast-tissue (c+), becomes abstricted 
and gives rise to the genital strand of 





de 
fe 


Fic, 261,—wo later stages in 
the development of the peri- 
cardial vesicle in the bud of 
Pyvosoma (after Seettoer). 
ec, ectoderm ; ef, elaeoblast ; 
en, entoderm (wall of intes- 
tine) 5 ed pericardial vesicle ; 
he, ridiment of heart, 


the stolon. In the proximal part, which represents the rudiment of 





SALPA—DEVELOPMENT OF THE STOLON. 495, 


In Salpa pinnata, 8. affinis and S. dolichosoma, it is more or less 
straight and runs forward along the ventral side of the body, In 8. 
vuncinata-fusiformis and costata- 
Tilesit, it at first rans forward on 
the ventral side, but then bends 
round and runs backward on the 
left side of the nucleus, and only 
passes out behind this organ. In 
S. democratica - mucronata, 8. 
acutigena - confederata and WS, 
cordliformis - zonaria, the stolon 
winds spirally round the nucleus 
(Fig. 262). 

The individual buds here, as in 
Pyrosoma, become marked off by 
transverse constrictions — which 
appear on the stolon. While, 


however, in Pyrosoma, the separate — yry4, 469 — Posterior end of tha body in 
parts of the stolon remain in a « solitary form of ipa ie 

* + vy mucronate, from the dorsal side (after 
single row, in the Salpidae, Lavckan). ¢, alimentary canal; h, 
secondary shifting leads to a bi- Pees ae el 
serial arrangement. A large : 

number of buds consequently can be crowded on to a short piece 
of the stolon. 





A. Structure and Development of the Proliferating Stolon. 


Our knowledge of the earliest stages of the development of the 
stolon is due chiefly to Spmnrcer (No, 105), The stolon, as already 
mentioned, is at first a small, conical 
outgrowth on the left side of the 
body near the posterior end of the 
endostyle. Three layers can be dis- 
tinguished in it ; ectoderm, mesoderm 
and entoderm. ‘The ectoderm of the 
stolon passes direct into that of the 51, 963, —Youngest. stage of de- 
parent. The entoderm-sac of the velopment of the stolon in. Sapa 
stolon (Fig, 263, en) is adivertioutum — {Mer Swartcnu) f, Dlood-ainus 
of the wall of the parent's branchial Process; mm; mesoderm ; ms, 

Ae 7 mesenoliyme-vells. 
sac arising immediately behind the 
endostyle. This diverticulum exactly corresponds to the organ known 








SALPA—DEVELOPMENT OF THE STOLON. 497 


round which the cells are arranged like an epithelium (Fig. 265, ¢), 
although SEELIGER was not able to come to a definite conclusion on 
this point. He called these strands the /ateral strands, whereas the 
other authors speak of them as the peribranchial, perithoracic or cloacal 
tubes, ‘They correspond to the peribranchial tubes in the stolon of 
Pyrosoma. In the fourth, lower strand (g), young egg-cells early 
appear, and it must therefore be called the genetal strand. Besides 
these strands, scattered mesenchyme-cells are found in the primary 
hody-cavity (Fig. 264, mz). 

In later stages of develop- 
tment of the stolon (Figs. 264 
B and C, 265), we find, 
farther, two large blood- 
sinuses lined with an endo- 
thelium, one lying above (0) 
and the other below (u) the 
entoderm-tube, Since this 
tube does not reach as far as 
to the end of the stolon, com- 
imunication between the two 
sinuses is possible, At this 
point the blood flows from 
one sinus to the other. 

Another constituent  ele- 
ment of the stolon in Sadpa 
has been pointed out by — Fi, 265,—Transvorse section through « youn; 
Buooxs, who found, om either HoH of et (ates, MS a clen 
side of the stolon, between tube; g, genital strand, im, muselo-tubes ; 
the peribranchial tubes and epee: Ns Ea a OSes 
the ectoderm, another tube 
which, he considers, gives rise to the muscular system. ‘These tubes 
Brooks culls the musowlar tubes (Fig. 265, m). 

In these six longitudinal strands running through the stolon we 
have the rudiments of the most important organs of the buds, ‘The 
ventral ontoderm-tube (em) yields the rudiment of the branchial sac 
(pharynx) and of the alimentary canal ; the neural tube yields the 
ganglion and the ciliated pit, while from the peribranchial tubes (c) 
the single atrial cavity arises, from the genital strand (7) the genital 
organs, and from the muscle-tubes (m) the body-musculature, When, 
later, through transverse constriction, the separate individuals (buds) 


begin to detach themselves from the stolon, the longitudinal strands 
KK 





SALPA—DEVELOPMENT OF THE BUDS ON THE STOLON. 499 


ectoderm of the stolon must, however, be considered probable for the 
neural tube. We should add that the examination of these onto- 
genetic processes in the stolon is exceedingly difficult.* 


B. Development of the Buds on the Stolon. 


Tt has already been shown (p. 495) that the buds arise through 
transverse constriction of the stolon (Fig. 266). The stolon is in this 
way cut up by a kind of transverse fission into a series of consecutive 
individuals which continuously increase in size while remaining con- 
nected together by the narrowed parts of the stolon, The buds thus 
arise in Salpa in exactly the same way as in Pyrvsoma (Figs. 253 
and 256 C), Only in later stages do the buds of the Salpidae undergo 
important changes of position which lead to their biserial arrangement 
on the stolon, In order 
clearly to understand 
these changes, we must 
first recall the condition 
of the Pyrosoma stolon, 
According to the more 
detailed account given 
on p. 484, the individuals 
are arranged on the 
Pyrosoma stolon in a 


single row, one behind — pio, a6. — Disgsamimatio longitudinal section 


Jentae _ through the stolou of a Pyrvioma (constructed b 

the other. ‘The orienta- Boggs after Huxuay ad Kowauevart), 2 
tion of each individual —— parent-individual; J, JJ, 117, tirst second and 
Slab Shat ok third buds; 6, ‘branchial-sd; c ateigim; of, 
resembles that of the alimentary Cana; , eetoderm of the connecting 
strand ; em, entoderm of the same; es, endostyle ; 

parent’: The haemal or m, nervous system; o, segment of the genital 
ventral side of the buds strand ; s, young stolon of the third individual. 


(marked bythe position 

of the endostyle, ««) is directed towards the distal end of the stolon, 
‘The right half of the body of every individual agrees in position with 
the right side of the parent; the left half of the bud corresponds to 
the left half of the parent and has been produced by the left half of 
the stolon, just as the right half of the bud has been produced by 
the right half of the stolon. 





*[According to Brooxs (No. I.), the nerve-tube-and the two peribranchial 
tubes are probably derived from the ectoderm of the stolon; the upper blood- 
sinus is continuous with the cavity of the heart, and the lower sinus with the 
body-cavity of the nurse-form.—Ep.) 


SALPA—DEVELOPMENT OF THE BUDS ON THE sroroN. 401 


younger stages, that the distal individuals of a group are somewhat 
further developed than the 
proximal individuals of the 
same group. 

The individuals are in reality 
arranged on the stolon in two 
alternate rows (Fig. 269) in 
such a way that the correspond- 
ing individuals of the two rows 
turn their ventral (haemal) 
sides (A) to each other, while 
their dorsal (neural) sides (n) 
are directed outward, This 
arrangement can be clearly 
made out in the transverse 
section (Fig, 275) through an 
older part of a stolon. We 
thus have an arrangement of 
the individuals like that de- 
picted in the diagram (Fig. 
269). The median plane of the 
individuals does not coincide 
with that of the stolon, but 
lies at right angles toit. This 
biserial arrangement of the 
bads results from a lateral 
shifting of the segments of the 
stolon which move alternately 
to the right and left side. 
Each bud at the same’ time 
rotates round its longitudinal 
axis, passing through an angle 





of 90° ; consequently, the dorsal H € 
side of the bud which origin- 
ally (Fig, 268) was directed F 


Fw. 270,—Horizontal longitudinal section through an advanced stolon of Sade 
{after Brooxs), ‘The individuals are out through obliquely, the longitnetinal section 
Pasting through them. in such a way that, in those placed most distally (1, 2, ete-) 
the most anterior region of the body is seen and, in the most proximal indi als 
(20, 21, etc.), the posterior region of the body. J», distal; P, proximal; #, right; 

, left. a, anal aperture; c, atrium; ef, elaeoblast; es, endostyle; y, gill; h, 
heart; As, hasmal side of the bud ; é, intestine ; 2, loft half of the branchial ao > 
im, opening of the oesophagus; 1, nervous system; as, neural side of the bud; o, 
ovary ; rh, right half of the branchial sae ; #, storaaeh, 












SALPA—DEVELOPMENT OF THE BUDS ON THE STOLON. 


the individuals on the stolon of Sal/pa can be traced back to the 
original monoserial arrangement which is retained in the stolon of 
Pyrosoma. 

Special interest attaches to the condition of individuals 3-7 of 
We can here 


Fig. 270, diagrammatically illustrated in Fig. 271. 


clearly see the relation of the buds to 
the stolon. The stolon itself is cut 
through obliquely, the section being 
intermediate between a longitudinal and 
4 transverse section. We can see the 
entoderm-tube of the stolon (en), an 
teriorly, the upper blood-sinus (0) and 
posteriorly the lower blood-sinus (wu, ¢/. 
Figs. 264 and 265), In individual 5, 
we ean trace the connection between the 
right (72) and the left (/0) halves of the 
branchial sac with the entoderm-tube 
(en) of the stolon, All the other indi- 
viduals are cut through at a different 
level. In individuals 4 and 6, for 
instance, the two blood-sinuses are inter- 
calated between the right and left halves 
of the respiratory cavity, 

We have reproduced other diagrams 
by Brooks (Figs. 272 and 273) which 
still further illustrate this condition. 
Fig. 272 gives the upper or oral aspect of 
« stolon as it would appear if the primary 
position of the buds had been retained 
unaltered (¢/. Fig. 268). The right half 
of each bud is seen to have arisen from 
the right side of the stolon and the left 
half of the bud from the left side of the 
stolon, Vig. 273 shows the buds shifted 
alternately to the two sides of the stolon, 
x condition attained through the repeti- 
tion of the process taking place in indi- 
vidual 5 in Figs. 270 and 271. The 
buds 1, 3 and 5 have moved toward the 





Fo, 272 — 
of Salpa as it would ay 
if no secondary shifting of 
the individuals were to take 
place (after Brooks), J’, 
pro: iD, di it 
right; ZL, left of the stolon ; 
rand /, right and left aides 
of the individuals; es, endo- 
style-folds; , ganglion, 








right side of the stolon while 2, 4 and 6 have moved toward the 
left side. The rotation of the individuals, however, is not yet visible. 


504 TUNICATA. 


Originally, therefore, the rudiments of the individuals (buds) are 
nothing more than the consecutive segments of the stolon marked off 
one from the other by transverse furrows. These furrows, as seen 
from above or below, are soon no longer transverse, but run somewhat 
obliquely (Fig. 274), in alternating directions, yo that furrows 1, 3 
and 5 are parallel on the one hand, 
and furrows 2, 4 and 6 on the other. 
In this oblique course of the furrows, 
we see the first preparation for the 
later biserial arrangement; it is 
the expression of the lateral displace- 
ment of the tissues of the buds 
forming the different segments of 
the stolon. When, therefore, in 
later stages, the segments shift to 
the two sides, it appears as if the 
buds arose as lateral ontgrowths 
from the stolon. This erroneous 
view of the budding of the Scdpt ix 
actually adopted by many of the 
older authors. Brooks was the first 
to trace back the origin of the buds 
to the transverse division of the 
stolon. 

The individuals become more and 
more sharply marked off from one 
another in proportion as the june 
their lateral positions and project out 





Diagram of a stolon or ftom the stolon, ‘They then appear 


Nepa after the lateral shifting of to be hanging on to the remains of 

the buds hast place; the einer 

Nepme in this diagram are all repre. the stolon like grapes on a bunch 

jou of individual Seay iehca . 

yulivictwil (Fig. 275 8). ‘The remains of the 

nies len stolon (xt), however, are nothing 

halves of the 5 

ating one indi- more than the consecutive strands 

or, ectoderm 5 
















RB. right ; 
1 


which connect the — individuals. 


en, entoderm, 


These, as may be seen from the 
diagram (Fig. 272), originally ran from the haemal side of each 
individual to the neural side of the next older bud. They are 
originally inserted at the middle of the body. In later stages, 
when the individuals have taken up the lateral position and bave 
undergone rotation, the connective strand forms a continuons longi- 


SALPA—DEVELOPMENT OF THE BUDS ON THE STOLON. 505 


tudinal tube to which the buds adhere laterally. The blood-vessels 
running in this strand, and the entoderm-tube which persists within 
it and connects the branchial sacs of the individuals, 

are of importance for the nourishment of the buds. 

This longitudinal strand may be called the remains of 

the stolon. Its position with relation to the buds 
changes, as its points of attachment wander more and 

more upward, ie, toward the branchial aperture 

of the individual (Fig. 275), while the individuals sink 
downward on either side of it. This change of position 

can be most distinetly traced in the ganglia. The 

-neural tube of the stolon originally lies above the 
entoderm-tube as ix seen in Fig. 264. The ganglia 

derived from the neural tube must consequently seem 

to lie in the median line above the entodermal con- 

neetive canals (see diagram, Fig. 268). When, Inter, Fra, 2 
the buds become marked off laterally, the ganglia sink [nstrating 
lower down, and come to lie at the sides of the con- hee oh oures 
necting canals; indeed, in the diagram (Fig. 268) _ furrowing in 
they appear alternately to cover the canals and tobe Mazel 
covered by them. Later, the ganglia and, with them, from above. 
the individuals, sink still farther down. 











The sinking down of the buds on either side of the remains of the 
stolon solves a ditticulty which apparently presents itself in connee- 
tion with their rotation. In examining individual 5 in Fig. 271, 
and still more in considering the diagram Fig. 273, it may oceur to 
the observer to wonder in what way the endostyle-fold which, in 
individual 5, lies on the left side, passed over to the right, since it 
appears separated from the right side of the body by the entoderm- 
tube of the stolon. We have tried to make this process clear by the 
diagrams given in Fig. 276. The connecting strand a4, which 
represents the remains of the stolon, originally rans from the neural 
side of each individual to the hacmal side of the next (proximal) 
individual. After rotation has taken place, these strands would 
assume a zig-zag course, as indicated in Fig. 276 2. Later, as the 
buds sink down, the connecting strands, which are alrendy attached 
near the anterior region of the body, shift further forward to a 
pesition quite near the branchial aperture, whereas the endostyle- 
folds, which remain unaffected by this change, do not extend so far 
forward. ‘here ix therefore no obstacle in the way to prevent the 
union of the connecting strands ; by this union these strands appear 


SALPA—DEVELOPMENT OF THE BUDS ON THE sTOLON. 507 


sare hollow, and each of them contains a blood-vessel. These might 
be compared to the mantle-vessels of the Ascidians, The final 
connection between the individuals is formed by the processes of 
neighbouring individuals growing out towards one another and 
fusing. Each of the individuals belonging to a chain possesses, as 
a rule, eight of these processes placed in four longitudinal rows ; 
two ventral and two lateral. The lateral couplings serve for attach- 
ment to the individuals lying in the same longitudinal row, while the 
‘ventral processes establish a connection between the two parallel rows 


i 





Bg 

Fro, 276. —Diagram illustrating the relatious of the connecting strand (st) to the bads 
‘on the stolon of a Salpa, A, represents the stolon from Fig. 268 viewed from above ; 
B, shows the condition after rotation has taken place ; C, the condition after the 
buds have sunk downward. a, distal end of the counecting strand, 4, proximal end 
of the same; a, distal part of stolon ; es, endostyle-folds ; , hactal or ventral side ; 
nm, wervons system and neural or dorsal side ; », proximal part of stalon ; sf, connect- 
ing strands. 


of individuals seen in the diagram (Fig. 277 A). The long axes of 
the individuals are inclined somewhat obliquely to that of the chain, 
a position which results from the fact that the couplings are not 
inserted at the same level on the right and the left sides of the body 
(Fig. 277 B). This oblique position may have given rise to the 
horizontal one seen in Salpa fusiformis. In S. (Cyelosalpa) pinnata 
the individuals are found arranged in the form of a rosette, each of 
the buds giving off a single process only from the ventral side which 
runs towards the centre of the rosette, where all the processes meet 


508 TUNICATA. 


together like the spokes of a wheel. Such an arrangement is charac 
teristic of the genus Cyclosalpa. 

This union between the individuals of the Salpa-chain must be 
regarded as colony-formation. Whereas, in the composite Ascidians 
and in Pyrosome, the individuals which arise through budding remain 
connected by means of a common cellulose mantle, connection here 
takes place through special connecting organs.* This connection is 





lustrating the interconnection existing between the individuals 
in seen trom above; B, lateral view. re, etudostyle ; 
lateral connecting’ processes ; A, Ventral processes 






not very close. When the fully developed chain passes ont from the 
cavity in the cellulose inantle of the parent and separates from the 
proliferating stolon, it very easily breaks up into smaller portions: 
individuals even become de 





hed from the chain and continue their 
existence independently. 


C. Development of the Organs in the Bud. 


In the above account of the relation of the buds to the stolon we 
have in all points followed the short but important deseription given 


hy Brooks (No. 92). The most important investigations made in 





* See [1 





Kant’s description, No. 28. 


SALPA—DEVELOPMENT OF THE ORGANS IN THE BUD. 509 


coonnection with the development of the organs in the bud are those 
of SaLEensky (Nos. 10] and 102) and SEELIGER (No. 105). Although 
the researches of these investigators yield much valuable material for 
working out the organogenesis of the buds of Sadpa, yet, owing to the 
fact that these observers did not recognise the rotation of the bud 
round its longitudinal axis, as made out by Brooks, their observations 
are somewhat vitiated through the adoption of an erroneous orienta- 
tion of the bud, taken from its later stages and applied in describing 
the earlier stages. SALENSKY and SEELIGER hold that the buds 
arise simply by the lateral shifting of the segments of the stolon, 
According to them the dorsal part of the bud develops from one of 
the lateral surfaces of the stolon, while its ventral side corresponds 
to the opposite side of the stolon, According to Brooks, on the 
contrary, the right side of the stolon gives rise to the right half of 
the body of the bud and the left side of the stolon to the left half. 
In the following account we shall merely give a brief outline of the 
genesis of the organs in Nadpa which probably closely resembles that 
in Pyrosoma.* 

[t must once more be pointed out that we have the first rudiment 
of the bud in a transverse segment of the stolon. The proximal 
parts of this segment become the dorsal side of the bud, and the 
distal parts its ventral side. From the upper region of the stolon is 
developed the anterior part of the body of the bud, while its posterior 
end develops from the lower region (see diagram, Fig. 268). The 
organs of the bud are formed from sections of the tubes and longi- 
tudinal strands which are to be seen in the transverse section of the 
atolon (Fig. 265). 

That part of the central entoderm-tube found in cach segment of 
the stolon gives rive to the pharynx of the bud. The entoderm-tube, 
in a cross-section through the stolon, bears some resemblance to the 
expanded wings of a butterfly (Fig. 264 (), an upper and a lower 
indeutation and two lateral indentations being found in it. Its form, 
in cross-section, later resembles that of the letter H, also found in a 
similar section of a Pyrosoma bud (Fig. 257). [In the latter, the two 
portions of the tube that point upward are connected with the 
development of the endostyle-folds, while those that extend down- 
wand, yield the stomach and intestine (p. 490). It is at present 
impossible to say whether similar conditions prevail in the Salpa bud. 














*(Brooxs’ memoir on the genus Salpa (No. I.) should be consulted in this 
connection ; he gives a full and detailed account of the development of the 
ohain-form, including its organogenesis.—E.} 


SALPA—DEVELOPMENT OF THE ORGANS IN THE BUD. 511 


origin of these organs, According to Brooks, the muscle-tubes give 
rise to the body-musculature. We may no doubt assume that the 
paired segments of these tubes spread out on either side of the bud 
and thus yield musele-plates, which become fenestrated and then 
break up into the musele-hoops. 

The rudiment of the genital organs is yielded by the genital strand 
(Figs. 264, 265, g). We have already seen (p. 497) that young egg- 
cells can early be recognised within this strand, These at first are 
very plentiful, but many of them disintegrate later and seem to serve 
as food for the developing eggs. When the genital strand is ready 
to break up into segments, the eggs become arranged in such & way 
that only one oceurs in each division. The smaller peripheral cells 
of the genital strand yield the egg-follicle, the oviduct and (according 
to SEELIGER) probably also the rudiment of the testis. Even in 





Fie. 278.—Chain-form of Salpa democraticn-mucronata from the distal part of an 
advanced stolon (after Skeutasr), ¢, atrinm ; ¢, atrial aperture; eh, elacoblast ; 
4s, endostyle; fy, cilinted pit: y, ganglion ; h, radiment of tostis': hy; connecting 
Prvoens | Ks, heart; ¢ branchial aperture : sm, tatesting ; &, gill me, stomachs 
oc, eye; od, oviduct ; v¢, oesophagus ; on, ogg-follicle ; ph, pharynx, 

early stages, it is evident, in cross-sections through the stolon, that 

group of cells becomes detached in each segment from the lower 

part of the genital strand, and this probably is to be regarded as the 

rudiment of the testis (Fig. 264, c, A). 

The rudiment of the genital organs originally lies at the posterior 
end of each bud. Later the egg-follicle shifts farther forward on the 
dorsal side and then lies above the intestinal loop in the dorsal median 
line. From this point the oviduct turns to the right with an S-shaped 
curve and becomes connected on the right side of the body with the 
epithelium of the atrial cavity (Fig. 278, ov and od). The wateh- 
glass-shaped rudiment of the testis (4) remains longer at the posterior 
end of the body curved round the posterior end of the intestinal loop. 
At a later stage it breaks up into separate tubes which unite to form 


612 TUNICATA. 


a common efferent duct that opens out into the atrial cavity between 
the intestine and the stomach on a puapilla-like prominence (see 
Savensky, Nos. 101 and 102, aud SEELIGER, No. 105). The testis 
develops comparatively late in the chain-form. 


5. The Interpretation of the Alternation of Generations 
in the Tunicates. 


Alternation of generations is found among the Tunicates in 
marked form in Pyrosomea, Doliolum and Salpa. This fact has 
long attracted the attention of zoologists, who have attempted to 
explain it in many different ways. We shall adopt the view first put 
forward by Leuckart (No. 98) and accepted later by Craus* and 
GropsEN (No. 79) that alternation of generations in the Tunicates 
must be regarded as having arisen in consequence of the formation of 
stocks through division of labour, and we shall follow GropBEs’s 
clear exposition of this view. Among more recent descriptions we 
may specially mention those of Unsantn (No. 86) and SgELIGER 
(No. 106). 

The Larvacea, which are conjectured to be the most primitive of 
all existing Tunicates, develop through sexual reproduction. This 
seems to suggest that the capacity for asexual reproduction (by means 
of buds) was acquired as a consequence of the attached manner of 
life. Asexual reproduction is indeed very common among. attached 
animals. We may, with GroBBEN, suggest as the cause that the 
abandonment of locomotion left a larger proportion of the substance 
of the body available for reproduction, so that it was possible for 





attached animals to introduce a new method of multiplication inte 
the cycle of their development. It may also, however, be added that 
when, in consequence of attachment, cross-fertilisation became mor 
difficult, the capacity for asexual reproduetion would become of special 





importance for the maintenance of the species. 

It is evident that, originally, all the individuals of forms which had 
developed this character were equally able to reproduce themselves 
cither sexually or asexually. 

Asexual multiplication led to the formation of stocks. the bud» 
being either altogether incapable of separating from the parent or 
else able to do so only incompletely, All individuals were thus at 
first capable, by asexual multiplication, of increasing the size of the 
colony to which they belonged, or else hy sexual multiplication ot 


* Grundz. d. Zool. 4 Aufl. 


ALTERNATION OF GENERATIONS IN THE TUNICATES. 513 


founding new colonies. Such a condition is found, for example, in 
the Ascidiozooids of Pyrosoma, which produce stolons and also maturate 
genital products. 

The distribution of these two kinds of reproduction among various 
individuals of the colony must be regarded as a later, derived condi- 
tion through which the first individuals arising in a colony then 
beeame adapted exclusively for increasing the colony by budding, 
while the lateral individuals formed new colonies by sexual reproduc- 
tion. Such an arrangement, in which we see the first commencement 
of ulternation of generations, is found in the composite Ascidians. 
Ganiy, following the investigations of Krom, established that, in 
this case, the individuals developing from the egg are capable of 
asexual reproduction only, and in this way lay the foundation of 
the colonies, while the descendants of these individuals, produced 
by budding, again develop genital products. 

In Salpa we find this condition more marked, and established 
as a regular alternation of two generations, one reproducing only 
asexually and the other only sexually, At the same time the two 
generations vary to a certain degree in the structure of the body. 
Gropsen bas rightly pointed ont that these variations may be 
explained by the different conditions of life and the different work 
to be carried out by the two generations. The points that project 
wt the posterior end of the “ nurse’ of Salpa democrativa-mucronata 
(Pig. 262) serve as a protection for the proliferating stolon which 
cceurs in that region of the body. This nurse” of S. demveratioa- 
mucroneta. further possesses one muscle-hoop more than the sexual 
animal, and this is explained on the ground that, owing to the 
presence of the massive proliferating stolon, greater muscular power 
is required in this case to enable the animal to swim with equal 
rapidity. On the other hand, the form of the sexual individua 
(that belonging to a chain) may be explained by the crowding of the 
buds on the chain, 

It follows from the above that the solitary form and all the indi- 
viduals of the chain produced by it must be regarded as members of 
one and the same colony. The solitary (“nurse”) form is the 
founder of the colony, while the individuals of the chain produced 
asexually give rise to the foundation of new colonies in producing 
sexually new solitary forms. 

‘The heteromorphous development of the individuals of the Salpa 
colony recalls the polymorphism of the Siphonophora. Polymorphism 


is still more strongly marked in the Dolioltdae, where we have, itv 
LL 


ALTERNATION OF GENERATIONS IN THE TUNICATES. 515 













why we should not assume that the capacity for division was 
possessed by the adults from the first, indeed, this capacity may 
ibly have been inherited directly from older pelagic ancestors 
the Tunicates. For, even if the circumstance that the Larvacea 
not multiply asexually seems to indicate that this form of re- 
luction was acquired only after attachment, we are not sure that 
this was the case, 

SketiGeR, who attributes to the mesoderm the principal part in 
development of the proliferating stolon, and who derives the 
of the stolon, at any rate in Pyrosoma, from the genital 
ues of the parent, finds in the limitation of sexual reproduction 
cause for the development of buds, the material left in the 
after the production of a single egg is utilised in its plastic 
ity as the mesoderin of the stolon. Bnt even if we make this 
ption, the manner in which budding was acquired remains 
obscure, 

Farther confusion has been introduced into the views as to the 
alternation of generations in the Tunicates by the fact that the exgg- 
cells. frequently maturate very early in the buds. They can even be 
4 distinguished in the genital strand of the stolon in Pyrosoma and 

Salpa. This has, in many cases, led to the view that the ovary 

actually belongs to the solitary form and is merely deposited in the 

forms composing the chain, This view, which is adopted by Brooxs 

Nos. 88-91) does not seem justifiable to us. We prefer SEELIGER’s 

view that the egg with its follicle is just as much an organ of 

the individual of the chain as are all the other organs. The early 

differentiation of the egg-cells is to be traced back to the effort on 

the part of the organism to arrive at sexual maturity as early as 
| possible. The same hastening of sexual maturity is found in the 
Hydroids and, indeed, in the parthenogenetic Cladocera and Aphidae 
and also in the Diptera (polar cells). 


Bnooxs regards all the ovaries of the individuals of a Salpa-chain taken 
together as the germ-gland of the solitary form shifted into the stolon. He 
considers the solitary forms not as sexless but as females, while he regards the 
individuals of the chain as males which have arisen from the females as buds, 
‘The solitary form deposits an egg in each male, and this, when fertilised, 
develops inton female. Bnooxs therefore reduces the alternation of genera- 
tions of Salpa to a kind of sexual dimorphism. 

We have already stated (p. 496) that Tonaro, by deriving all the buds from 
certain embryonic germ-cells (germoblasts), and by tracing these latter directly 
to the blastomeres of the embryo, regards the individuals of a Salpa-chain not 
as the descendants of the solitary form but merely as younger members of the 


GENEBAL CONSIDERATIONS ON THE TUNICATES. 517 


composite Ascidians. We must await the result of further researches 
before coming to any definite conclusion, . 

Tn any case, the development of the bude must always be considered 
quite apart from embryonic development, since these two methods 
of development are to be traced back to different principles. In 
the embryo, the primary organs arise anew from an originally 
undifferentiated mass of blastomeres, while in budding, which is 
evidently deducible from division, parts of the most important 
primary organs are taken over from the organisation of the parent 
into the bud. Although the literature on the budding of the Tuni- 
cates at present is far from supporting the statement that all the 
more important organs in the bud or the stolon are to be derived by 
abstriction from the corresponding organs of the parent, indications 
are not wanting that the solution of the problem as to the origin of 
the organs of the bud is to be sought in this direction (p. 487). It 
appears, for instance, that the strands which compose the rosette-like 
organ of Doliolum ave direct continuations of all the more important 
organs of the parent. In the four primary Ascidiozvoids of Pyrosonut 
also, the peribranchial tubes and the pericardial rudiment of the 
Cyathozovid are directly continued. It may be mentioned further 
that, according to Kowavevsky, the peribranchial tubes in the stolou 
of Salpa are derived from the atrium of the parent. These state- 
ments which, however, are in direct contradiction to many observa- 
tions on other forms suggest that none of the more important organs 
arise anew in the bud, but that all the more important rudiments of 
organs pruxs over from the parent into the xtolon and thence into the 
buds, while the actual new formation of organ-rudiments takes place 
andy in the embryo. The nervous system would probably have to be 
considered as an exception to this rule. Since we know that the 
brain of the Ascidian can be regenerated after excision, it appears 
possible that it arises anew also in the buds, though probably only 
from the ectoderm. 

Turning to the embryonir development, we tind that the different 
divisions of the Tunicata here also vary greatly. ‘The embryonic 
development of the Sa/pidae is, indeed, so little understood that we 
are hardly in a position to say anything definite about it. When we 
see that, according to SALENSKY, all the species examined show 
important variation in their methods of development, it is evident 
that there ix here an ample field for further research.* We may, 


[* See footnote, p. 423 and pp. 445-446.—Ep.] 


GENERAL CONSIDERATIONS ON THE TUNICATES, 519 


tion of the dorsul region found in the Ascidians and the approxima- 
tion of the branchial and atrial apertures thus brought about is 
traced buck to attached forms, the position of the anus in the 
Larvacea, which must evidently be regarded as primitive, would 
indicate that these animals are descendants of those hypothetical 
Tunicate ancestors which still retained the original pelagic life. 
On the other hand, we find in Appendicu/aria a series of unmistakable 
degenerative phenomena tending to support the assumption that we 
must regard the racial form of the Larvacea as an attached Tunicate. 
It is evident that they must be considered as sexually mature larval 
forms, sexual maturity being shifted continually further back to 
earlier stages so that, finally, the mature adult form no longer 
developed. What form can we imagine this latter to have assumed ? 
Was ita free-swimming Ascidian form intermediate between Amphiorus 
and the Ascidian larva, or an already attached Ascidian form? The 
last assumption seems the more probable. The appearance of the 
eollulose mantle and hermaphroditism and the indistinctness of the 
segmentation of the body must be regarded as features acquired as 
& consequence of attached manner of life. As these characters are 
found in the Larvacea, we are to a certain extent justified in con- 
sidering them as the sexually mature larvae of an already attached 
form of Tunicate.* In any case, however, all phylogenetic specula- 
tions concerning the Tunicates must rest upon careful consideration 
of the structure of Appendicularia and the Axscidian larvae. 

Among the Ascidiacea the solitary forms are probably the more 
primitive. ‘The composite forms lead on to Pyrosoma, which may be 
regarded as a eomposite colony that has not become attached and 
that is distinguished by a large common cloaca. In the interesting 
family Coelocormidae we see the development of the whole colony in 
w similar direction. Here also the colony is not attached but, on the 
other hand, the internal cavity cannot be compared to the common 
clouwea of Pyrosoma (see Herxoman, No. 24).  Pyrosoma forms 
4 transition to the free-swimming Doliolidae. This was pointed out 
by Huxuey with reference to the structure of the gill and the 
opposite position of the two apertures of the body (uf. also Gnopuen, 
No. 79). The Dotiolidue (Cyclomyaria), among which Doliopsis 
(Anchinia) exhibits the most primitive characters, must be regarded 
as phylogenetically the oldest Thaliacea. The Salpidae (Hemimyaria) 
must be considered as derived from them, We shall, therefore, have 


*Witiey (No. 54a) also has lately maintained that the Larvacea are 
degenerate forms. 


GENERAL CONSIDERATIONS ON THE TUNICATES, 521 


disappearance of the segmentation of the body. Only in the caudal 
region of the Ascidian larvae and of Appendicudaria are there any 
traces of the segmentation which must have been present in their 
ancestors. [n the caudal portion of the nervous system in the 
Ascidian larva, spinal nerves are given off segmentally, as KuprFER 
first noticed, In Appendicularia these are connected with paired 
ganglionic swellings in the dorsal cord, LanGERHANs (No, 2), by 
the use of reagents, was further able to prove that the caudal musen- 
lature breaks up into ten consecutive muscle-segments (myomeres) 
which are provided with segmentally arranged pairs of motor nerves. 
To individual cases Lancuraans (No. 2) found that, in the posterior 
caudal region of Appendicularia, the spinal nerves of the left side 
have shifted somewhat forward as compared with the corresponding 
nerves of the right side, A similar condition is found in Amphioaus. 
In the anterior region of the body, on the contrary, no traces of 
segmentation are retained. 

Although we must recognise a great general agreement in struc- 
ture and development between Amphiorus and the Tunicates, it is 
very difficult to establish exactly in detail the homologies between 
the organs of the two groups. A special attempt of this kind was 
made by vAN Brewepen and Juni, but we are not able to regard all 
their deductions as convincing. Starting from the view that, in the 
‘Tanieates, a large part of the alimentary canal (in the caudal seetion) 
hus degenerated, VAN BENEDEN and JucIn regard the rectum and the 
aval wperture of the Tunicates as new acquisitions which are not 
homologous with the homonomous structures of Amphiorus. They 
find the homologue of the rectum of the Tunieates in the ‘ club. 
shaped gland” of Amphiorus, which belongs to the first trunk-metamere 
(p- 549) and opens ont near the mouth.* Consequently the whole of 
the precaudal part of the body in the Ascidian larva corresponds 
to only the small anterior region of Amphionus, viz., to the anterior 
cephalic part—the first trunk-segment. This view leads these 
authors further logically to deny the strict homology of the endostyle 
with the hypobranchial groove of Amphionus. Since, however, in the 
Cephalochorda and the Vertebrata also, the anal aperture has evidently 
undergone a secondary shifting forward and the eandal section of the 
alimentary canal degenerates, there is nothing which compels us to 
doubt either the homology of the rectum throughout the Chordata, 


*(Wittey (No. XXXVIL) regards the club-shaped gland as the right 
primary gill-slit,—Ep,) 





GENERAL CONSIDERATIONS ON THE TUNICATES. 519 


tion of the dorsal region found in the Ascidians and the approxima- 
tion of the branchial and atrial apertures thus brought about is 
traced back to attached forms, the position of the anus in the 
Larvacea, which must evidently be regarded as primitive, would 
indicate that these animals are descendants of those hypothetical 
Tunieate ancestors which still retained the original pelagic life. 
On the other hand, we find in Appendicu/aria a series of unmistakable 
degenerative phenomena tending to support the assumption that we 
must regard the racial form of the Larvacea as an attached Tunicate. 
It is evident that they must be considered as sexually mature larval 
forms, sexual maturity being shifted continually further back to: 
earlier stages so that, finally, the mature adult form ne longer 
developed. What form can we imagine this latter to have assumed ? 
Was ita free-swimming Ascidian form intermediate between Amphiorus 
and the Ascidian larva, or an already attached Ascidian form? The 
lust assumption seems the more probable. The appearance of the 
cellulose mantle and hermaphroditism and the indistinctness of the 
segmentation of the body must be regarded as features acquired as 
4 consequence of attached manner of life. As these characters are 
found in the Larvacea, we are to a certain extent justified in con- 
sidering them as the sexually mature larvae of an already attached 
form of ‘Tanicate.* In any case, however, all phylogenetic specula- 
tions concerning the Tunicates must rest upon careful consideration 
of the structure of Appendicularia and the Ascidian larvae. 

Among the Aseidiacea the solitary forms are probably the more 
primitive. The composite forms lead on to Pyrosoma, which may be 
regarded as a composite colony that has not become attached and 
that is distinguished by a large common cloaca. In the interesting 
family Coclocormidae we see the development of the whole colony in 
«similar direction. Here also the colony is not attached but, on the 
other hand, the internal cavity cannot be compared to the cormmon 
cloaca of Pyrosoma (see Hirpman, No. 24).  Pyrosoma forms 
a transition to the free-swimming Doliolidac. This was pointed out 
by Hoxney with reference to the structure of the gill and the 
opposite position of the two apertures of the body (77. also Gronuen, 
No. 79). The Dotiolidae (Cyclomyaria), among which Doliopsis 
(Anchinia) exhibits the most primitive characters, must be regarded 
ws phylogenetically the oldest Thaliacea. The Salpidae (Hemimyaria) 
must be considered as derived froin them. We shall, therefore, have 


*Witiey (No. Sda) ulso has lately maintained that the Larvacen are 
degenerate forms. 








GENERAL CONSIDERATIONS ON THE TUNICATES. 521 


disappearance of the segmentation of the body. Only in the caudal 
region of the Ascidian larvae and of Appendiewaria are there any 
traces of the segmentation which must have been present in their 
ancestors. In the caudal portion of the nervous system in the 
Ascidian larva, spinal nerves are given off segmentally, as Kurrrer 
first noticed. In Aypendiewlaria these ave connected with paired 
vanglionic swellings in the dorsal cord. LanGERHANs (No. 2), by 
the use of reagents, was further able to prove that the caudal museu- 
lature breaks up into ten consecutive muscle-segments (myomeres) 
which are provided with segmentally arranged pairs of motor nerves. 
In individual cases Lancrrnans (No. 2) found that, in the posterior 
caudal region of Appendicularia, the spinal nerves of the left side 
have shifted somewhat forward as compared with the corresponding 
herves of the right side, A similar condition is found in Amphioxus. 
In the anterior region of the body, on the contrary, uo traces of 
segmentation are retained, 

Although we must recognise a great general agreement in struc- 
ture and development between Amphiowus and the Tunicates, it is 
very difficult to establish exactly in detail the homologies between 
the organs of the two groups. A special attempt of this kind was 
made by van Benepen and Juni, but we are not able to regard all 
their deductions us convincing. Starting from the view that, in the 
‘Tunicates, a large part of the alimentary canal (in the caudal section) 
has degenerated, vax BENEDeN and Junty regard the rectum and the 
anal aperture of the Tunicates as new acquisitions which are not 
homologous with the homonormous structures of Amphiorus. They 
find the homologue of the rectum of the Tunicates in the “ club- 
shaped gland” of Amphionus, which belongs to the first trunk-metamere 
(p- 549) and opens out uear the mouth.* Consequently the whole of 
the precaudal part of the body in the Ascidian lurva corresponds 
to only the small anterior region of Amphiorus, viz, to the anterior 
vephulic part—the first trunk-segment. This view leads these 
authors further logically to deny the strict homology of the endostyle 
with the hypobranchial uroove of Amphiorus. Since, however, in the 
Cephalochorda and the Vertebrata ulso, the anal aperture has evidently 
undergone a secondary shifting forward and the caudal section of the 
alimentary canal degenerates, there is nothing which compels us to 
doubt either the homology of the rectum throughout the Chordata, 


*(Wineey (No. XXXVIL) mgards the club-shaped gland as the right 
primary gill-slit.—Ep.} 





GENERAL CONSIDERATIONS ON THE TUNICATES. 521 


disappearance of the segmentation of the body. Only in the caudal 
region of the Ascidian larvae and of Appendicularia are there any 
traces of the segmentation which must have been present in their 
ancestors. [In the caudal portion of the nervous system in the 
Ascidian larva, spinal nerves are given off segmentally, as KupFFER 
first noticed. In Appendicn/uria these are connected with paired 
ganglionic swellings in the dorsal cord. LanGErnans (No. 2), by 
the use of reagents, was further able to prove that the caudal muscu- 
lature breaks up into ten consecutive muscle-segments (myomeres) 
which are provided with segmentally arranged pairs of motor nerves. 
In individual cases LaNGeRHans (No. 2) found that, in the posterior 
caudal region of Appendicularia, the spinal nerves of the left side 
have shifted somewhat forward as compared with the corresponding 
nerves of the right side. A similar condition is found in Amphious. 
In the anterior region of the body, on the contrary, no traces of 
seginentation are retained. 

Although we must recognise a great general agreement in stru 
ture and development between mphiorux and the Tunicates, it is 
very difficult to establish exactly in detail the homologies between 
the organs of the two groups. A special attempt of this kind was 
made by vAN BENEDEN and Jury, but we are not able to regard all 
their deductions as convincing. Starting from the view that, in the 
Tunicates, a large part of the alimentary canal (in the caudal section) 
has degenerated, vaN BENEDEN and JuLIN regard the rectum and the 
anal aperture of the Tunicates as new acquisitions which are not 
homologous with the homonomous structures of Amphiorus. They 
find the homologue of the rectum of the Tunicates in the ‘“ club- 
shaped gland” of Amphiorus, which belongs to the first trunk-metamerce 
(p. 549) and opens out near the mouth.” Consequently the whole of 
the precaudal part of the body in the Ascidian larva corresponds 
to only the small anterior region of Amphiorus, viz., to the anterior 
cephalic part—the first trunk-segment. This view leads these 
authors further logically to deny the strict homology of the endostyle 
with the hypobranchial groove of Amphiorus, Since, however, in the 
Cephalochorda and the Vertebrata also, the anal aperture has evidently 
undergone a secondary shifting forward and the caudal section of the 
alimentary canal degenerates, there is nothing which compels us to 
doubt either the homology of the rectum throughout the Chordata, 











VIL) regards the club-shaped gland as the right 





522 TUNICATA. 


or the derivation of the anterior region of the body in the Tunicate 
larva through fusion from a large number of trunk-metameres. 

We have already mentioned (p. 367) that vaN BENEDEN and JuLix 
deny the homology of the branchial slits and the peribranchial or 
atrial cavity in the Tunicates with those of other Chordata. Only 
the two clefts which form first in the Tunicates are really to be 
regarded as true gill-slits. This view results from the ascription by 
these authore to the entoderm of a considerable part in the develop- 
ment of the peribranchial sacs. In the same way, VAN BENEDEN 
and Junin doubt the homology of the heart in the Tunicates with 
the heart of the Vertebrata. We shall only be able to judge of this 
last view, which indeed receives decided support from the absence of 
the heart in the Amphiocus, when the way in which this organ arises 
in the Tunicates is fully established. While SEELIGER, like va‘ 
BeNepEN and Junin, derives the pericardial sac in the Ascidian 
larva from the entoderm, most of the statements of other writers 
seem to render its mesodermal origin probable. We must, however, 
constantly bear in mind that an actual endocardium is altogether 
wanting in the heart of the Tunicata. 

This view, shared by many of the more recent writers (BALFOUR, 
van BENEDEN and Juin, HatscHEk) that the Tunicates and the 
Cephalochorda, to which the Vertebrates are allied, represent distinct 
branches of the Chordate type connceted together only at their roots, 
is opposed to that of Donrx (Nos. 15-19), who regards the Tuni- 
cates as degenerate fish. The ¢ 
author thought to repress 





clostoma and Amphiarus are by this 
distinct in the series of degenera- 
tive processes through which the organisation of the Tunicates is to 
be derived from that of the fishes. This view rests principally upon 
the proof which Dour attempted to establish that the hypobranchial 
groove (endostyle) as well as the peripharynyeal ciliated bands of the 
Tunicates, the homologue of which was discovered by SCHNEIDER in 
Ammocortes, ave to be regarded as transformed gill-clefts, and the 
thyroid-gland, the homology of which with the hypobranchial groove 
had been maintained by W. MiLLER was said to represent a branchial 
sac lying between the spiracle and the first branchial cleft, while the 
ciliated arch is the homologue of the spiracular cleft (the pseudo- 
Iranch of the Teleosteans).* The endostyle and the ciliated arch 





teas 














* (Done stands alone in his belief that the pseudobranch of the Teleosteans 
ix formed from the anterior wall of the original spiracular cleft and that, by 
the later suppression of the cleft, the pseudobranch comes to lie in the first 
branchial cleft. Most vertebrate imorphologists regard this pseudobranch as 





GENERAL CONSIDERATIONS ON THE TUNICATES, 523 


would thus be met with in the Tunieates in a secondarily modified 
form, This view rests especially on observations of the development 
of the homologous structures in A mmocoetes. 

Even though it appears to us that Donn carries these homologies 
too far, since we are not inclined to assume direct genetic relations 
between the Fishes and the Tunicata, and still less to regard the two 
groups as independent branches derived from a common, primitive 
racial form (Protochordata), we consider that it entirely justifies the 
conviction that the Tunicates cannot be utilised to bridge over the 
gap existing between the Chordata and the other branches of the 
animal kingdom. Haroxen and GEGENBAUR have been specially 
prominent in their advocacy of this view. The hypothetical primitive 
form of the Tunicates is represented as a typical Chordate with all 
the features generally ascribed to that type. But no characteristics 
are to be found either in the anatomy or the ontogeny of the Tunicata. 
which ally them directly to any one branch of the Invertebrata. The 
Tunicates appear to us no more nearly related to the Invertebrata 
than are Amphiorus or the Vertebrata. The specially striking 
features in the Tunicates, viz., the absence of segmentation, of the 
coelom and the nephridia, the occurrence of asexual reproduction are 
all characters which we cannot regard as primitive. They have been 
newly acquired in connection with the attached manner of life. ‘The 
way in which we have to reconstruct for ourselves the primitive 
Chordata (the common hypothetical racial form of the Tunicata, the 
Cephalochorda and the Vertebrata) can only be discovered through 
careful comparison of the ontogeny and anatomy of these three 
groups, and in this we are convinced that the chief stress must be 
laid on Amphiorns. Such a reconstruction is at present specially 
diffioult, indeed is rendered almost impossible by the fact that our 
knowledge is as yet too fragmentary to enable us to establish exactly 
the homologies of the different organs in the three groups of the 
Chordata, In illustration of this it may be mentioned that our 
knowledge of the origin of the peribranchial cavities in the Tunicates 
is still incomplete, and the question as to the homology of the ciliated 
pit in the Tunicates with the hypophysis cerebri and other problems 
are as yet also insoluble, 


a development of the anterior wall of the first branchial cleft in no way con- 
nected with the spiracular cleft or with the pseudobranch of Elasmobranchs. 
Consequently, if there is any truth in the compurison given above it would be 
More in aé-ordance with the generally accepted homologies to read 
branchiae of Elasmobranchs for pseudobranchiae of Teleosteans.—Ep. 














GENERAL CONSIDERATIONS ON THE TUNICATES. 519 


tion of the dorsal region found in the Ascidians and the approxima- 
tion of the branchial and atrial apertures thus brought about is 
traced back to attached forms, the position of the anus in the 
Larvacea, which must evidently be regarded as primitive, would 
indivate that these animals are descendants of those hypothetical 
Tunieate ancestors which still retained the original pelagic life. 
On the other hand, we find in Appendicu/aria a series of unmistakable 
degenerative phenomena tending to support the assumption thar we 
must regard the racial form of the Larvacea as an attached Tunicate. 
It is evident that they must be considered as sexually mature larval 
forms, sexual maturity being shifted continually further back to 
earlier stages so that, finally, the mature adult form no longer 
developed. What form can we imagine this latter to have assumed ? 
Was it a free-swimming Ascidian form intermediate between Amphiowus 
und the Asvidian larva, or an already attached Ascidian form? The 
lust assumption seems the more probable. The appearance of the 
cellulose mantle and hermaphroditism and the indistinctness of the 
segmentation of the body must be regarded as features acquired as 
@ consequence of attached manner of life. As these characters are 
found in the Larvacea, we are to a certain extent justified in con- 
sidering them as the sexually mature larvae of an already attached 
form of Tunicate.* In any case, however, all phylogenetic specula- 
tions concerning the Tunicates must rest upon careful consideration 
of the structure of Appendicularia and the Ascidian larvae. 

Among the Ascidiacea the solitary forms are probably the more 
primitive. The composite forms lead on to Pyrosoma, which may be 
regarded as a composite colony that has not become attached and 
that is distinguished by a large common cloaca. In the interesting 
family Coelocormidae we see the development of the whole colony in 
uw similar direction, Here also the colony is not attached but, on the 
other hand, the internal cavity cannot be compared to the common 
clouea of Pyrosoma (see Herpmax, No. 24). Pyrosoma forms 
4 transition to the free-swimming Doliolidae. This was pointed out 
by Huxney with reference to the structure of the gill and the 
opposite position of the two apertures of the body (¢f. also GrosBEN, 
No. 79). The Doliolidae (Cyclomyaria), among which Doliopsis 
(Anchinia) exhibits the most primitive characters, must be regarded 
us phylogenetically the oldest Thaliacea. The Sadpidae (Hemimyaria) 
must be considered as derived from them, We shall, therefore, have 


"Winter (No. 54a) also has lutely maintained that the Larvacea are 
degenerate forms. 








GENERAL CONSIDERATIONS ON THE TUNICATES. 521 


disappearance of the segmentation of the body. Only in the caudal 
region of the Ascidian larvae and of Appendicularia are there any 
traces of the segmentation which must have been present in their 
ancestors. In the caudal portion of the nervous system in the 
Asecidian larva, spinal nerves are given off segmentally, as Kuprren 
first noticed. In Appensicwlaria these are connected with paired 
ganglionic swellings in the dorsal cord. Lancerans (No. 2), by 
the use of reagents, was further able to prove that the caudal musen- 
lature breaks up into ten consecutive muscle-segments (myomeres) 
which are provided with segmentally arranged pairs of motor nerves. 
tn individual eases Lancerans (No. 2) found that, in the posterior 
caudal region of Apperdécularin, the spinal nerves of the left side 
have shifted somewhat forward as compared with the corresponding 
nerves of the right side. A similar condition is found in Amphionus. 
In the anterior region of the body, on the contrary, no traces of 
segmentation are retained. 

Although we must recognise a great general agreement in struc- 
ture and development between Amphiorns and the Tunicates, it is 
very difficult to establish exactly in detail the homologies between 
the organs of the two groups. A special attempt of this kind was 
made by van Bexepen and Juni, but we are not able to regard all 
their deductions as convincing. Starting from the view that, in the 
‘Tunicates, a large part of the alimentary caual (in the caudal section) 
has degenerated, vaN BENEDEN and Jucrn regard the rectum and the 
anal aperture of the Tunicates as new acquisitions which are not 
homologous with the homonomous structures of Amphiorus, They 
find the homologue of the rectum of the Tunicates in the ‘ club. 
shaped gland” of Amphiorns, which belongs to the first trank-metamere 
(p. 549) and opens out near the mouth.* Consequently the whole of 
the precandal part of the body in the Ascidian larva corresponds 
to only the small anterior region of Amphiowus, yiz., to the anterior 
cephalic part—the first trunk-segment. This view leads these 
authors further logically to deny the strict homology of the endostyle 
with the hypobranchial groove of Amphionus, Since, however, in the 
Cephalochorda and the Vertebrata also, the anal aperture has evidently 
undergone a secondary shifting forward and the caudal section of the 
alimentary canal degenerates, there is nothing which compels us to 
doubt either the homology of the rectum throughout the Chordata, 


“(Witter (No. 
primary gill-slit.—! 





XXVIL) regards the club-shaped gland as the right 
a) 





528 TUNICATA. 


57..Giarp, A. Recherches sur les Synascidies. Archiv. Zod. 
expér, Vol. i. 1872. 

58, GiarD, ALFR. Sur le bourgeonnement des larves d'Astellium 
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59. Hsort, J. Zum Entwicklungscyclus der zusummengesetzten 
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60. Kowabevsky, A. Sur le bourgeonnement du Perophora Listeri. 
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61. Kowavevsky, A. Ueber die Knospung der Ascidien. Arrhir. 
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62. Kroan, A. Veber die Fortpflanzungsverhaltnisse der Botryl- 
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63. Krony, A. Ueber die friheste Bildung der Botryllenstécke. 
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64. Jourpary, S. Sur les Ascidies composées de la tribu dex 
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644. Oxa, A. Die periodische Regencration der oberen K6rperhalfte 
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65. Pizon, A. Sur la blastogénése chez les Botryllides. Bull. 
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6. SernicerR, O. Zur Entwicklung der Ascidic 
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67. Unrasix, B. Bemerkungen uber die Synascidiengattuy 
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68. Denia Vanue, A. Nuove contribuzioni alla: storia naturale 
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70. Deuba Vane, A. Sul ringievanimento delle colonie de 

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Volkov. D884. 

















Kibildung unt 
unysher, Aewl, 


























Pyrosoma. 


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LITERATURE. 529 


72. Huxuey, To. H. Anatomy and Development of Pyrosoma. 
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73. Joumt, L. Btudes anatomiques et embryogéniques sur le 
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74. Sanensky, W. Beitriige zur Entwicklungsgeschichte der 
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Bd. v. 1892. 

75. Seenicer, O. Bemerkungen zu Herrn Prof. Salensky’s 
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76. Sennicer, O. Zur Entwicklungsgeschichte der Pyrosomen. 
Jena. Zeitschr. f. Nature. Bd. xxiii. 1889. 

76a. Seericer, O, Ueber die erste Bildung des Zwitterapparates 
in den jungen Pyrosomenstocken. Festschrift fiir Leuekart. 
Leipaig, 1892. 


Doliolum. 

77. Barros, J. Recherches sur le cycle génétique et le bourgeon- 
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78. Geornpaur, C. Ueber den Entwicklungscyclus von Doliolum 
nebst Bemerkungen tiber die Larven dieser Thiere. Zeitschr. 
J. wiss. Zool. Ba. vii, 1856. 

79. Gropgen, ©. Doliolum und sein Generationswechsel. Ayd. 
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80. Huxiey, Ta. HH. Remarks upon Appendicularia and Doliolum. 
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81. Kererstem unp Enters. Zoologische Beitrage. Leipziy, 
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82. Korotnerr, Au, pe. La Dolchinia mirabilis. Mitth, Zool. 
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83. Korotnerr, A. Die Knospung der Anchinia. Zeitsehr. f. 
wiss, Zool. Bd. Ix. 1884. 

84. Kowanevsxy, A., er Barrors, J. Matériaux pour servir a 
Vhistoire de l'Anchinie. Journ. Anat. Phys. Paris, Tom. 
xix. 1883, 

85. Kromn, A. Ueber die Gattung Doliolum und ihre Arten. 
Archiv. ¢. Natury. Ba. xviii. 1852. 

86. Unsanin, B, Die Arten der Gattung Doliolum im Golfe von 


Neapel. Fauna und Flora wn Neapel. Monogr x. 1884. 
MM 


530 TUNICATA. 


Salpa. 

87. Barnois, J. Mémoire sur les membranes embryonnaires des 
Salpes. Journ. Anat. Phys. Paris. Ann. xvii. 1881. 

88. Brooxs, W. K. On the Development of Salpa. Bull. Mus. 
Comp. Anat. Harv. Coll. Camb. Vol. iii. 1871-1876. Cf. 
Archiv. fiir Naturg. Bd. xlii. 1876. 

89. Brooxs, W. K. The Origin of the Eggs of Salpa. Stud. Biol. 
Lab. Johns Hopkins Univ. Baltimore. Vol. ii. 1882. 

90. Brooxs, W. K. Chamisso and the Discovery of Alternation of 
Generations. Zool. Anz. Jahrg.v. 1882. 

91. Brooxs, W. K. Is Salpa an Example of Alternation of Genera- 
tions? Natwre. Vol. xxx. 1884. 

92. Brooxs, W. K. The Anatomy and Development of the Salpa- 
chain. Stud. Biol. Lab. Johns Hopkins Univ. Baltimore. 
Vol. iii. 1886. 

93. Brooks, W. K. On the Relationship between Salpa and 
Pyrosoma. Johns Hopkins Univ. Cire. Vol. 9. 1890. 

94. Biscuur, O. Kinige Bemerkungen uber die Augen der Salpen. 
Zool. Anz. Jahrg. xv. 1892. 

94a. GoprErRt, E. Untersuchungen iiber das Sehorgan der Salpen. 
Morph. Jahrb, Bd. xix. 1892. 

95. Huxuey, Tu. H. bservations on the Anatomy and Physiology 
of Salpa and Pyrosoma, Phil. Trans. 1851. 

96. Kowavevsky, A. 
Machy, kyle 

97. Knoxy, A. Observations sur la géncration et le developpement 
des Biphores. dun. Se/, Not. (3). Tom. vi. 1846. 

gx. Leuckart, R. Salpa und Verwandte. Zool, Untersuchungen, 
Heft. ii. Giessen, 1854. 

99. Metcatr, M. The Anatomy and Development of the Eyes 
and Subneural Gland in Salpa. Johuws Hopkins Ouie. Cire. 
No. 97. 1892. 

99a. Mercaur, M. On the Eyes, Subneural Gland and Central 
Nervous System in Salpa. Zool. Anz. Jahrg. xvi. 1893. 

100. Sanensky, W. Ueber die embryonale Entwicklungsgeschichte 
der Salpen,  Zeitsehr, f, miss, Zool. Bd. xxvii. 1876. 

101. SaLtensky, W. Ueberdie Knospung der Salpen, Morph Jala}. 
Bad. 1877. 

102. Satensky, W. Ueber die Entwicklung der Hoden und uber 
den Generations we 





Beitrag zur Entwicklung der ‘Tunicaten. 
Useh. Wissenseh. Gottingen. 186%. 















sel der 
Bd. xxx. Suppl. 1878. 


alpen. Zeitschr. f. wise, Zool. 


LITERATURE, 531 


103. Sanensky, W. Folliculare Knospung der Salpen und die 
Polyembryonie der Pflanzen. Bini. Centralbl. Bd. v. 1885, 

104. Sanensky, W. Neue Untersuchungen iiber die embryonale 
Entwicklung der Salpen, Mitth, Zool, Stat. Neapel, Ba. iv. 
1883, In two parts, 

105, Szeuicer, Osw. Die Knospung der Salpen. Jen. Zeitschr. 
fiir Naturw, Bad. xix. 1886. 

106, Szenicer Osw. Die Entstehung des Generationswechsels der 
Salpen. Jena. Zeitschr. f. Naturw. Bd. xxii. 1888. 

107. Toparo, Fr. Sopra lo sviluppo ¢ l’anatomia delle Salpe. Atti. 
R. Accad. Lincet. Trans. (2). Vol. ii. 1875. 

108, Toparo, FR Sui primi fenomeni dello sviluppo delle Salpe, 
Atti. R. Accad. Lincei. Trans. (3). Vol. iy. 1880, 

109. Toparo, Fr. Sui primi fenomeni dello sviluppo delle Salpe. 
24 communic. preliminare. Atti, R. Accad. Lincei. Trans. 
Vol. vi. 1882. (Also in Archiv. Ital. Biol. Tom. ii, 1882.) 

110, Toparo, Fr. Sui primi fenomeni nello syiluppo delle Salpe. 
3* comm. prelim. Atti. R. Accad. Lineei. Trans. Vol. vii. 
1883. (Also in Archiv. Ital. Biol. Tom. iii, 1883.) 

111. Topaxo, Fx. Sopra i canali e le fessure branchiali delle Salpe. 
Atti, R. Accad. Lincei. Trans, Vol. viii. 1884. 

112, Toparo, Fr. Studi ulteriori sullo sviluppo delle Salpe. Atti, 
R. Avead. Lineei. Mem. (4). Vol. i. 1886. 

113. Toparo, Fr. Sull’ omologia della branchia delle Salpe con 
quella degli altri Tunicati, Afi. R. Accad. Lincei. Rend. (4). 
Vol. vi, 1889. (Also in Archiv, Ital, Biol, Tom. xi, 1889), 


APPENDIX 70 LITERATURE ON TUNICATA, 


I. Brooks, W. K. The genus Salpa. Mem. Johns Hopkins 
Univ, 1893. 
Il. Casrozn, W. B. Early Embryology of Ciona intestinalis. 
Bull, Mus, Harvard. Vol. xxvii. 1896. 
Ifl. Castne, W. BE. On the Cell-lineage of the Ascidian egg. 
Proc. Amer. Acad. Vol. xxx. 1894. 
TV. Caununy, M. Contributions a l'Btude des Ascidies com- 
posées. Bull. Sei, France et Belgique. Tom. xxviie 
1895, 
V. Caunery, M. Sur la Morphologie de la Larve composée 
dune Synascidie (Diplosomoides Lacazii, Giard). Compt. 
Rend. Acad. Sci. Paris, Tom. exxv. 1897. 


532 TUNICATA. 


VI. Cauuery, M. Sur le Bourgeonnement des Diplosomidae 
et des Didemnidae. Compt. Rend. Acad. Set. Paris 
Tom. cxxi. 1895. 

VII. Cautery, M. Sur I'Interprétation morphologique de la 
larve, etc., du genre Diplosoma. Compt. Rend. Acad. 
Sci. Paris. Tom. cxxi. 1895. 

VII. Caunery, M. Sur les Synascidies du genre Colella, et le 
polymorphisme de leurs bourgeons. Compt. Rend. Acad. 
Sei, Paris, Tom. exxii. 1896. 

IX. Damas, D. Les Formations épicardiques chez Cions 
intestinalis. Archiv. Biol. Tom. xvi. 1899. 

X. Fuoperus, M. ‘ber die Bildung der Follikethiillen bei 
den Ascidien. Zeitechr. f. wise. Zool. Bd. lxi. 1896. 

XI. Garstanc, W. Budding in Tunicata. Setence Progress. 
Vol. iii. 1896. 

XII. Grarp, A., ET CaunERy, M. Sur I'Hivernage de la 
Clavelina lepadiformis. Compt. Rend, Arad. Sci. Parix. 
Tom. cxxiii, 1896. 

XIN. Herper, K.  Beitrage zur Embryologie von Salpa fusi- 
formis. Frankfurt, 1895. (bh. Senkenb. Gea. Bd. 
XV. 

XIV. Pile J.  Beitrage zur Keimblitterlehre und Entwick- 
lungsmekanik der Ascidienknospung. Anat. Anz. Bd. x. 
1895. 

XV. Hyort, J. Ueber den Entwicklungcyelus der zusammen- 
gexetzten Ascidien. Mittheil. Zool. Stat. Neapel. Bd. x. 
1893. 

XVI. Hyort, J., uxp Bonneviz, Fr. Ueber die Knospung von 
Distaplia magnilarva. Anat. Anz. Bd. x. 1895. 

XVI. Juni, GC. Recherches sur la blastogéntse chez Distaplia 
magnilarva et D. rosea. Congr. Zool. Leyden. 1896. 

XVII. Korotserr, A. Embryonale Entwicklung der Salpa demo- 
eratica. Biol, Contralbl, Ba. xiv. 1894: and Zettarhr 
foaiss, Zool, Ba. lix. 1895. 

XIX. Korotnerr, A. Tunicatenstudien. Mitth. Zool. Stat. 
Neupel. Ba. xi. 1895, 

XX. Korotyerr. A. Zur Embryologie von Salpa cordiformis- 
zonaria und musculosa-punetata, — Mitth. Zool. Stat. 
Noupel. Ba. xii. 1896. 

XXa. Korotyerr, A. Zur Embryologie von Salpa runcinata- 
fusiformis. Zeitschy #. miss, Zool. Bd. Ixii. 1896. 











XXL 


XXIa. 


XXII. 


XXIIL, 


XXIV. 


XXY. 


LITERATURE, 533 


Kororyerr, A. Zur Entwicklung der Salpen. Biol. 
Centralbl. Bd. xv. 1895. 

Kororyerr, A, Zur Embryologie von Salpa maxima- 
Africana, Zeittschr. f. wiss. Zool, Bad, Ixvi, 1899. 

Lerevrr, G. Budding in Ecteinaseidia. Anat. Anz. Bd. 
xiii. ; and Johns Hopkins Uwiv, Cire. 1897, 

Lereven, G. On budding in Perophora. Jolns Hopleins 
Univ. Cire, Vol. xiv, 1895, 

Mercatr, M. The follicle-cells of Salpa. Zool. Anz. 
Jabrg. xx. 1897; and Jvhns Hopkins Unio. Cire. 
1897. 

Pizon, A. Contributions a I'Embryogénie des Ascidies 
simples, Compt. Rend. Acad. Sei. Paris, Tom. exx. 
1895. 


XXVI. Przon, A. Histoire de la Blastogénése chez les Botryllides. 


XXVIa. 


XXVIL. 


XXVIII. 


XXIX, 


XXX. 


XXXL. 


XXXII, 


XXXII. 


XXXIV, 


Ann. Sei. Nat. Tom. xiv. 1893. 

Pizox, A. Evolution des elements sexuels chez les 
Ascidiens composts. Compt. Rend. Acad, Sei, Paris, 
Tom. exix. 1894. 

Pizon, A. Les Membranes embryonnaires et les Cellules 
de rebut chez les Molgules, Compt, Rend. Acad, Sci. 
Pavis. Tom. exxii, 1896, 

Rirrer, W. E. Budding in Compound Ascidians based 
on studies on Goodsira and Perophora. Journ. Morphol. 
Vol. xii, 1896. 

Sauensky, W. Beitrige zur Entwicklungsgeschichte a. 
Synascidien (Diplosoma and Didemnum). Mitth. Zool. 
Stat. Neapel. Bd. xi. 1895. 

Sauenscy, W. Morphologische Studien an Tunicaten, 
(Nervous system and Metamorphosis of Distaplia). Morph. 
Jahrb. Ba. xx. 1893. 

Sauensky, W. Ueber die Entstehung der Metagenesis bei 
Tunicaten. Biol. Centralbl. Ba. xiii, 1893. 

Samassa, P, Zur. Kenntniss der Furchung bei dem Asei- 
dien. Arch mikro. Anat. Ba. xliy. 1894, 

Szerioer, O. Kinige Beobachtungen iiber die Bildung 
der auesseren Mantels der Tunicaten. Zeitschr. f. wise. 
Zool. Bad. li. 1893. 

Srzticer, O. Ueber die Entstehung des Peribranchial- 
raums in den Embryonen der Ascidien. Tom. eit. 





534 TUNIOATA. 


XXXV. Toparo, F. Sopra lo Sviluppo della parte anteriore del 
corpo delle Salpe. Atti. R. Acad. Lincei. Rend. (3). 
Vol. vi. 1897. 

XXXVI. Wingy, A. Studies on the Protochordata. Parts IL and 
III. (nervous system, sense-organs and mouth). Quart. 
Journ. Micro, Sci. Vol. xxxv. 1893. 

XXXVII. Wimuey, A. Amphioxus and the Ancestors of the verte- 
brates. London and New York. 1894, 


CHAPTER XXXVI. 


CEPHALOCHORDA. 


Amphioxus. 


Tux earlier statements concerning the development of Amphiorus 
made by Max Scnruttze (No. 18), Leuckart and PAGENSTECHER 
(No. 15) referred merely to a few of the later larval stages; our 
knowledge of the ontogeny of this form is, therefore, founded princi- 
pally on the investigations of KowaLevsky (Nos. 10 and 11), and was 
extended by HarscHek (Nos. 4 and 8). The metamorphosis of 
Amphiorus has recently been described by Ray LankesTER and 
Wiuey (No. 13) and by Wiuvey alone (No. 23). The develop- 
ment of the genital organs has been investigated by Bovert (No. 3). 
This last author (No. 2) as well as SPENGEL (No. 19), Ray LANKESTER 
(No. 12) and van W1sHE have also published treatises on the anatomy 
of the adult Amphiorus to which we shall have occasion to refer.* 


A. Oviposition, Cleavage and Gastrulation. 


The mature genital products of Amphtorus pass from the genital 
chambers, through rupture of their walls, into the atrial cavity and 
thence they were said to pass through the gill-clefts into the pharynx 
and to be ejected through the mouth (KowaLEvsky, HatscHEk). 
According to Ray LankEsTER and WILLEY, however, they are, in 
most cases, ejected through the atriopore. Fertilisation takes place 
in the surrounding water. The newly laid egg is surrounded by a 
vitelline membrune at first only slightly separated from it, but, under 
the influence of the sea water, the interval between the egg and the 


*[More recently, Soporra (No. XI.) and Sticut (No. XII) have rein- 
vestigated the maturation and fertilisation of the egg, and the former, 
Kuaatscn (No. LV.) and Macsripr (No. VIIL) have re-examined the forma- 
tion of the germ-layer.—Ep.] 





636 CEPHALOCHORDA. 


membrane becomes greater. ‘I'here is no micropyle. The spermatowa 
pass through this elastic membrane to reach the egg.* 

‘The first stages of development closely resemble those of the 
Ascidians. Cleavage is total and almost equal (adequal type of 
Harscuxk). ‘The first furrow is meridional and appears first at 
the animal pole, where for some time it is deepest; it eventually 
divides the egy into two exactly equal parts (Fig. 279 8). The 
second furrow, which is also meridional, is at right angles to the first 
and leads to the rise of four blastomeres of equal size which leave free 
between them a cavity open above and below ; this is the cleavage- 
cavity (Fig. 279 C and D). The eight-celled stage (Fig. 279 £) is 
brought about by an equatorial furrow which lies somewhat nearer 
the animal than the vegetative pole and leads to the first differentia- 
tion between the blastomeres of the animal and vegetative halves. 
‘The embryo consists of a circle of four smaller blastomeres near the 
animal pole and another circle of four larger blastomeres belonging 
to the vegetative pole. Further meridional furrows divide theve eight 
cleavaye-spheres into sixteen, the sixteen-celled stage then conxisting 
of acirele of eight smaller and another of eight, larger blastomeres 
(Fig. 279 F). 

Even at this sixteen-celled stage, according to WILSON, certain individual 
differentiations are found which influence the further course of cleavage. The 
regular stage described by Hatscuex, in which the eight cells of the apper 
cirvle are found resting regularly on the eight cells of the lower 
comparatively rarely observed by Witsos. The blastom 
cance often appear shifted spirally in relation to those of the 
to be the ease in the Annelida and Mollu 
the sixteen-celled stage a bilateral (or strictiy speaking a sirad: a. 
is evident in the armingement 0 
tate haif be 
larger cells 
sma 
















ang divided into four 


Tove 


CLEAVAGE AND GASTRULATION. 537 













pol 
more rapid « 
he act of ng; II, the same stage 
blastula, in section 


5. divin 
of protoplaam ;'(, four-celled stage 
colled stage sixteonsrollod stage 
animal pole: one of the circles of cells 
in section ; /, blaxtula, surface view ; 





=f 
















axis, and the wall at ‘he vegetative pole, /.e., the p 

the egg, is composed of somewhat larger cells richer i 
‘This represents the entodermal region of the embryo. 
ing occurs, and this soon passes into an invagination: 
which leads to the development of « cap-shaped 
invagination causes the cleavage-cavity to decrease in s 
completely to disappear, the two primary g ! 
close contact (Fig. 280 2). 














The gastrula-stage now passes through certain phas 
which the bilateral symmetry which, according to Wi 
evident in the stages of cleavage, becomes more distit 
same time, the embryo elongates in the direction 
longitudinal axis. The apex of the ectoderm of the 
sponds to the animal pole, while the vegetative pole 
coincide with the centre of the at first circular ap 


show a point at which the curve is more abrupt ; 
coincide with the animal pole but lies somewhat ey 
sponding to the anterior end of the later pri 


DEVELOPMENT OF THE MEDULLARY TUBE, ETC. 539 


end coinciding with the posterior edge of the blastopore. The 
definitive principal axis thus forms an acute angle with the primary 
axis. The blastopore has undergone shifting to the dorsal side of 
the embryo ; it now gradually decreases in size, chiefly through a 
backward growth of its dorsal or anterior border. The posterior 
{ventral) edge of the blastopore, on the contrary, remains stationary 
during this narrowing process. It is always marked by two larger 
entoderm-cells lying symmetrically to the median plane (Fig. 280 @) ; 
these are claimed by Harscuex as pole-cells of the mesoderm.* 
Finally, the embryo becomes more elongated. The ventral surface 
is distinguished by being arched, while the dorsal side, which was 
originally oecupied by the blastopore, is distinctly fattened. The 
posterior end of the dorsal side is occupied by the now very small 
vestige of the blastopore (Fig. 280 @). Even at this stage, the 
external surface of the embryo is covered with short flagella which 
enable it to rotate within the egg-envelope. 

Tn the position of the blastopore and the conditions under which it closes, 
there is close resemblance between Ampiiorus and the Ascidia (cf, p. 342). 
_ Inour description of the transformations undergone by the gastrula-stage, 
we have for the most part followed Hatscnex. A rather divergent account 
has recently been given by Lworr (No. 17) who, in dealing with the closure 
of the blastopore, lays the chief stress on the independent and rapid growth 
of the ectoderm at its dorsal margin. (Stress should also be laid on the 
protrusion of the lateral edges of the blastopore, a point which was overlooked 
by Lworr), From this rapidly growing dorsal edge, ectodermal elements are 
said to be invaginated dorsally into the gastrula-cavity and there finally to 
force the proper entodermal elements from the dorsal to the ventral side of 
the cavity. According to this view, the cells forming the dorsal wall of the 
archenteron are ectodermal and it is from this cell-layer that Lworr derives 
the chorda. Lworr was not able to convince himself of the presence of the 
primitive cells of the mesoderm which Hatscu@x found marking the posterior 
end of the longitudinal axis of the embryo. 


B. Development of the Medullary Tube, the Primitive Segments 
and the Notochord. 


The next ontogenetic stages of Anmphiorue are characterised by the 
increase in length of the whole body, The median part of the dorsal 
surface, at the same time, sinks in somewhat (Fig. 281), and this 


* (Sonorra (No. X.) agrees with Lworr (No. 17) in denying that the biasto- 
pore closes from before backward. They believe that it gradually diminishes 
on allsides. Sonorra was unable to find the pole-cells and does not believe 
that they exist, at any rate at the early stages figured by Harscuex.—Ep,] 





540 CEPHALOOQHORDA, 


depression leads to the development of the medullary tube, The 
latter is here formed, not, as in the Ascidia and many Vertebrates, 
through the fusion in the middle line of 
two lateral medullary folds, the process, 
although it may be deduced from the 
above type, being somewhat modified. 
It might be described us lateral over 
growth. The medullary plate (Fig, 282 
A, mp) sinks down somewhat and its 
lateral edges become detached from the 
rest of the ectoderm. The ectoderm (/}) 
now grows inward from either side above 
the medullary plate and unites in the 
middle line before the plute hus become 
curved into a tube (Fig. 282 8). “The 
c . dorsal groove, although completely 
wiead with the reduaeny of covered externally, ia still /opadiieTiaa 
eee aera iti, under the integument” (Fig. 283). Only 
Henn je later does the medullary plate curve round 
tube; ws’, first primitiveseg- dorsally, and, through the fusion of itt 
ee Primitive Jateral edges, form a closed tube, the 
medullary tube (Fig. 284). 

The union of the lateral ectodermal growth above the medulliry 
plate takes place from behind forward, commencing near the remains 








Fig, 282. —A, transverse section through au embryo of a 
of the first primitive segment (after ATCHIRK, {hom 0, 
transverse section through an embryo of Amy 
primitive segments (after Hatsenes, from 0, 
ch, chorda-rudiment ; dh, archenteric cavity ; Ab, lay 

the medullary plate; i, entoderm ; fh, body. 
medullary plate, 





DEVELOPMENT OF THE MEDULLARY TUBE, ETO. 541 


of the blastopore, which thus becomes covered by a layer of ectoderm 
(Fig. 281). The blastopore thus does not open externally but into the 
neural canal; this connection between the intestine and the neural 
tube is long retained, being known as the neurenterie canal. [See 
Korscn, No. V.] 

The medullary plate does not reach the most anterior end of the 
embryo, but extends for about three-quarters of its length. At the 
point where it stops, which lies somewhat in front of the anterior 
edge of the first primitive segment, the medullary tubes retain an 
external aperture which is at first wide but gradually narrows 
later (neuropore, Figs. 285, 286, up), As we shall presently see, 
the neuropore in Amphioxue 
only closes in a very late stage 
(Kurrrer). The cells of the 
medullary tube, like the other 
ectodermal cells, carry flagella. 
These, which are long and ex- 
ceedingly fine, project into the 
lumen of the tube and, are 
directed backward, 

The development of the 
medullary tube leads to a Fic. 283.—Tvansverse section through an 
pressing inward of the middle Ss — Bae papa 
part of the dorsal wall of the oor from 0. Henrwio's Text- 
entoderm - sac (Fig. 282 A). 

This median swelling is accompanied by two latero-dorsal out- 
growths of the entoderm-sac (Fig. 282 3B, mic). hese paired 
longitudinal folds, the so-called mesoderm-folds, yield the material 
which becomes the mesoderm and can be traced posteriorly as far as 
to the neighbourhood of the two primitive mesoderm-cells,* although 
the most posterior part of the folds is indistinctly marked off from 
the rest of the entoderm-sac. Segmentation very soon appears in 
the anterior region, the mesoderm-folds becoming cut up by trans. 
verse indentations, into consecutive portions, the primitive segments 
(Fig. 281, ws’, ue"). The segments which, owing to their origin, must 
be regarded as archenteric diverticula, develop regularly from before 
backward, We thus see, in Fig. 281 two, in Fig. 286 five, and in 
Fig. 286 nine segments distinctly marked off. Later, the primitive 
segments become completely cut off from the entoderm-sae, and they 





[* See footnote, p. 539.—Ep.] 


1 


DEVELOPMENT OF THE MEDULLARY TUBE, ETO. 543 


contact in the median line dove-tail into one another. The rudiment, 
of the chorda is then a solid strand-like thickening of the dorsal 
entoderm-wall, from which it soon becomes severed as an independent 
strand (Fig. 284, ch). In the meantime the cells of this rudiment 
press between each other in such a way that each cell finally extends 
transversely across the entire rudiment. 

The chorda develops, on the whole, from before backward. It 
commences to develop in the region of the primitive segments. The 
anterior part of the chorda, which extends above the first primitive 
segment towards the anterior end of the body, only develops later, 





Fig, 286.—Eimbryo of Amphiccus with tive pairs of primitive segmonts (after HaTscren, 

from 0, Hxntwro's Tevt-book), A, lateral aspect; , viewed from the dorsal side. 

; om, neurenteric canal; dh, enteric cavity; ik, ectoderm; mh, 

mesoderm-fold ; #, neural tube; wd, archenteron; ws’, first primitive segment; ws, 
cavity of primitive segment; V, anterior, 1, posterior, 


and then not through the independent growing out of the already 
developed rudiment, but through « separation of cells at the most 
wnterior part of the archenteron from which no primitive segment is 
abstricted, 

The whole of the entoderm-plate which lies between the mesoderm- 
folds is not, however, used up for the formation of the chorda, but only 
the median part of it, the lateral parts, according to HaTsoneK, 
being utilised for the completion of the dorsal wall of the alimentary 


EARLY LARVAL DEVELOPMENT. 545 


288, 290, ©) does not arise as an epithelial fold, but as a simple 
thickening due to the ectoderm-cells increasing greatly in height. 

The medullary tube (Fig, 288, mr), in the central canal of which 
backwardly directed cilia can still be seen, has an anterior swelling, 
in which not only are the walls thicker but the central canal wider. 
Even in very young stages a pigment-spot is found in the ventral 
wall of the medullary tube in the fifth metamere (Fig. 288), Later, 
a similar spot, functioning as an eye-spot, appears at the anterior end 
of the cerebral swelling (Figs. 289, 290). ‘The posterior end of 
the medullary tube uppears dilated (Fig. 288), and this swelling 
contains the undifferentiated material which, as growth advances, 
continually produces new parts of the medullary tube, This dilated, 
posterior end is bent round the posterior end of the chorda, At this 
point the communication with the alimentary canal is found (nenren- 
terie canal, Fig. 288, en). 

In cross-sections, the medullary tube is found to consist of a 
single layer of cells (Fig. 234, »), the first perceptible nerve-fibres 
being found in the ventro-lateral corners, in contact with the chorda. 

The rudiment of the mesoderm consists of the series of consecutive 
primitive segments (Fig. 286, us’, ux") and of a posterior unsegmented 
region, the mesoderm-folds (mf) which (according to Harscnex) 
terminate in the pole-cells of the mesoderm (mp). In this posterior 
region, the coelom is still for a time in communication with the 
enteric cavity. Later, however, the mesoderm-folds become com- 
pletely separated from the entoderm-sac, and, as the posterior end of 
the chorda-rudiment becomes similarly abstricted from the alimentary 
canal, the neurenteric canal, in later stages, forms a simple communica- 
tion between the ventrally-curved posterior end of the medullary tube 
and the most posterior end of the intestine. 

Even in the stage with eight primitive segments, we find indica- 
tions of that asymmetry which affects the later development of the 
body. The primitive segments of the right side of the body lie 
somewhat further back than those of the left (¢/. the boundaries of 
segments fully outlined with those in dotted outline in Fig. 287). 
‘This asymmetrical shifting of the primitive segments takes place to 
such an extent that the junction between two segments on one side 
coincides with the centre of a segment on the opposite side, 

In the stage with nine primitive segments, the most anterior 
segment sends off dorsally, at the side of the chorda-rudiment, a 
hollow process (Fig. 286, m) which gradually grows forward to the 
anterior extremity of the body. This cephalic process of the mesoderm 

NN 


546 CEPHALOCHORDA. 


yields the mesodermal structures in the anterior region of the body. 
It has recently been regarded by HaTscHEK (No. &) as the rudiment 
of an independent pair of primitive segments, in which case, the 
segment hitherto called the first would actually be the second. 

The walls which separate the consecutive segments, the so-called 
dissepiments, at first run straight from the dorsal to the ventral side 
(Fig. 285, 4). Later, they curve backward (Fig. 286) and finally 
they develop the characteristic angulation at the level of the upper 
part of the chorda dorsalis (Figs. 287, 288). 





ec om 


Fic. 286.—Stage iu the development of Amphiv.cus in which there are nine primitive 
segments (after HaTscHek). In the fifth, sixth and seventh primitive segments, 
the muscle formative cells (2) are clearly marked. du, anterior entoderm-divert- 
culum ; rc, ectoderm ; en, entoderm; m, cephalic process of the first primitive 
segment ; mf, mesoderm-folds ; mp, pole-cells of the mesoderm ; m3, muscle 
formative cells ; 1p. neuropore ; us’, first primitive segment; we”, second primitive 
segment. 





The primitive segments origi 





ally lie dorsally above the alimentary 
canal (Fig. 283, wk). Later, they extend ventrally and thus grow 
round the alimentary canal (Fig. 284). Those parts of the coelom 
also which surrounded the canal are originally distinet from one 
another, but at the stage in which the mouth forms, the ventral part 
of the dissepiments degenerate 








and consequently the originally 
distinct coelomic cavities run together and form the splanchnocorle, 
which, enclosed by the lateral plates, rans through the whole length of 
the body as a continuous cavity. The right half of the splanchno- 
coele is in Open communication with the left half below the alimentary 
canal. According to HaTscHEK, previous to this union of the ventral 
part of the primitive segments that grow down on either side, 4 
simple ventral lamella is formed which extends between the ectodenu 
and the alimentary canal. [n this ventral lamella the rudiment of 
the first recognisable blood-vessel, the swh-(ntestinal vessel appears, 
a vessel w 





ich lies later on the ventral side of the alimentary canal 
covered by the splanchnopleure. The first rudiment of this vessel 


EARLY LARVAL DEVELOPMENT, 547 


can be followed forward from the posterior end of the body as a cloar 
canal (Figs. 288, 289, av). Near the second segment it is deflected 
to the right side of the body by the first gillaudiment forming in the 
ventral median line, and ends, apparently blindly, near the club- 
shaped gland. The origin of this vessel is still obsenre. KoWALEVSKY 
derives it from cells lying free in the body-eavity which form a solid 
strand that becomes hollowed out later. 

As the cavities of the primitive segments gradually increase in size 
the cells of their walls become more and more flattened. This does 
not apply, however, to the cells in contact with the sides of the noto- 
chord which, on the contrary, become greatly elongated as columnal 
or club-shaped cells and form the rudiment of the lateral trunk-museles 
(Fig. 284). These cells contain nuclei in their free club-shuped ends, 
while the basal portion, that is turned to the chorda, becomes trans- 
formed into muscular tissue. Each of these musele-cells traverses the 






te be 


Fig, 287,75! of Amphiorus with thirteen primitive segments (aftr HaTscHek). 
The boundaries of the segmecuts of the left sida are iodicated by uninterrupted lines, 
and those on the tight by dotted lines. om, ueurenteric canal ; dr, rudiment of the 
club-shaped gland, de’, right, de”, left, anterior entoderm-divertioulum ; np, 
neuropore, 


whole length of the primitive segment to which it belongs (Fig. 286, 
mz), and its axis lies in a line with the corresponding cells of the 
neighbouring primitive segments. The muscle-fibres formed by these 
cells fuse together and ran continuously through the consecutive 
segments. Each muscle-fibre is thus formed from a series of con. 
secutive muscle-cells. Transverse striation can early be made out 
in the fibres. The fact that the walls of the primary gut-pouches 
(enterocoeles) give vise not only to the lining of the body-cavity but 
also to the trunk-muscles, has caused some observers to speak of the 
primary cavities as the myocoelomic pouches, At an early period 
after the ventral extension of the mesodermal somite described above, 
its cavity becomes divided into two by the formation of a horizontal 
partition which separates a ventral splanchnocoele from a dorsal 
myocoele (see pp. 564 and 565), 





EARLY LARVAL DEVELOPMENT, 549 


essentially agrees with that of the Vertebrates, consisting of vesicular 
flattened cells. The structures that were described as chorda-plates 
appear to be a kind of artifact. 

Great changes also take place in the eatoderm, Two lateral 
diverticula first become abstricted from that anterior part of the 
entoderim-sac which lies in front of the first primitive segment ; these 
diverticula lie beneath the cephalic process of the first primitive 
segment (Fig. 286, do), and are called by Harsoren the anterior 
entoderm-sacs. This wuthor hus recently claimed them as an anterior 
pair of branchial saes (No. 8). The future fate of these two diverti- 
cula, which at first resemble each other, differs greatly. The one on 
the right (Fig. 287, dv) increases considerably in size and, pressing 
back the anterior end of the alimentary canal, completely fills the 
anterior cavity beneath the chorda in the snout-like prolongation of 
the body (Fig. 288, A). The left diverticulum (Fig. 287, dv), on the 
contrary, remains small and does not shift forward. In later stages 
it lies transversely beneath the chorda and opens outward in front of 
and above the oral aperture (Fig. 288, 1), A strongly ciliated efferent 
portion can be distinguished from a smaller blind portion lying to the 
right. This vesicle to which, later, « nerve runs, was regarded by 
Kowa.evsry as « peculiar sensory organ of the larva. The pre-oral 
pit becomes enclosed by the developing oral hood and thus comes to 
lie within the adult mouth ; the ciliated epithelium lining its efferent 
section increases in extent and gives rise to the so-called wheel-organ 
(Raderorgan), while its sensory organ persists in the adult as the 
groove of HaTscHEK. 


The two anterior entoderm-diverticula have been interpreted in many 
different ways. We have already mentioned that Harscuek (No. 8) regards 
them as the most anterior pair of branchial sacs, vas Wise (No, 22) 
recently claimed the aperture of the left entoderm-vesicle as the primary 
mouth (autostoma) of Amphionus, homologous with the mouth of the Tunicata. 
The ciliated organ which develops from the entoderm-vesicle, together with 
Hatscuen's pit, has been compared by van WisHe to the ciliated pit of the 
Tunicata. The right entoderm-vesicle, on the contrary, which is not morpho- 
logically the antimere of tho left, corresponds to the anterior cephalic somite of 
the Selachians, from which are developed the optic museles innervated by the 
culo motorius. Baresox (No. 26) las compared the two anterior vesicles to 
the proboscis-coelom of Balanogiossus and the uperture of the left vesicle to 
the proboscis-pore, a conclusion with which Wiuny (No. XIIT.) agrees. 


A further derivative of the entoderm is found in the so-called eld 
shaped gland first seen by M. Scauntze and later by Lauckarr and 
PagenstecHeR (Figs. 288,289, /). This lies near the first primitive 





550 CEPHALOCHOEDA. 


seginent and arises as a trausverse yrouve in the cher oi the enteno 
(F 87, dr) specially distinct on the right side of the teodiy and 





running thence ventrally to the left side. This gmevve leepen: and 
becornes constricted off fran the enteron to form an independent 
tube, and then represents the club-shaped gland. the right, bind 
portion of which is dilated, while the narrowed left section opens 
externally in front of the oral aperture (Fig. 288, 2°). In later stages, 
the right, blind end of this yland enters into communication with the 
Iumen of the intestine (Ray Laskester and WILEY. 





dota larva somewhat older than that depicted im Fig. 238, 
end of the same seen trom th 
; d, alimentary canal ; de, di: 
dissepiments of the other side 
, club-shaped gland ; ka, gill-cleft : mm. mouth ; sp, 
‘mr, medullary tube ; my, posterior end of the medullary 
fube sap. neuropore ; xr, sub-intestinal vein ; 1, ciliated organ ipre-oral pith. 
















lhumediately in front of the club-shaped gland there is a transverse 
ciliated band (Fig. 289 A, fl) which, according to WILLEy, is the 
first rudiment of the endoxtyle. 

The oral aperture (Fig. 289, 1) forms on the left side of the bedy 
in the region of the first segment. A dise-like thickening of the 
ectoderm first appears, to the inner side of which the intestine 
becomes closely applied, since, in this region, the mesoderm does not 





LATER LARVAL STAGES. “651 


extend so far ventrally. In the middle of this ectodermal thickening, 
the larval oral aperture forms at first as a narrow perforation which, 
however, soon widens. Consequently, the oral aperture is surrounded 
by a thickened ectoderm-wall. 

The first gill-cleft forms soon after (Fig. 289, kx) in the ventral 
region of the second body-segment. A small outgrowth of the ento- 
derm here forms, round which the entoderm-cells become elongated 
and less granular. An annular entodermal thickening is thus formed 
in the middle of which is the above-mentioned depression, the cells 
of which soon fuse with the ectoderm, and a perforation, the first 
gill-slit, takes place. Round the first gill-cleft, the ectoderm is not 
thickened, but the entoderm forms a circular wall representing the 
inner edge of the gill-cleft. The first primary yill-cleft which arises 
dn this way soon shifts to the right side of the body (Fig. 289 4). 

After the mouth and the first gill-clefts have broken through, the ciliated 
organ, the pre-oral pit (derived from the left enteric vesicle), and the elnb- 
shaped gland also open externally. 

The anal aperture breaks through at the most posterior end of the 
alimentary canal on the left side of the body. At the same time, 
the communication between the intestine and the ventrally curved 
end of the medullary tube (neurenteric canal) (Fig. 289 2) is lost. 

After all these apertures have formed. the | 
taking in food. 





va is capable of - 


D. Later Larval Stages. 





The further development of the larva falls into three periods :—- 

I. Behind the first yill-slit, a series of other so-called primary yill- 
xlitx (ax many as fourteen, WILLEY) develop ; most of these shift: to 
the right side of the pharynx. The metapleural folds arise and the 
atrinm begins to form and to close from behind. The primitive seg- 
nents increase in number till the condition of the adult is in’ this 
rexpect reached (sixty-one segments forming in Amphiocus lanceolatue), 
The unpaired tin of the adult with its cavity develops (Figs. 290, 291). 

Il. On the right side, above the row of primary gill-clefts, a second 
row forms (xeronlary clefts of WILLEY). After the atrium has closed, 
the primary gill-clefts xhift to the left side, while the secondary 
remain on the right side. The larval mouth becomes changed into 
the velum, and the definitive mouth-aperture arises as a consequence 
of the formation of pnired folds, the oral hood, round the larval 
mouth. The mouth shifts into the ventral median line. The oral 





32 CEPEALOCRORDA 





eirr: feveing ami the cbit-+hapert siami deyenerates. In consequence 
o€ che jeveinpment xf >art—bers im oamectie sith the gill-diw, 
the aumber of the latter » ienbled. The hepatic caecum form» 
(Figs. 292, 293, 255. 

TIL The iarva, which in cwential points now chwely resembles the 
adtoit. has Sven ap jeiagie ite ami baries itself in the aand. The 
gillclef=- sirewiy éemei. whieh at tirst were arranged metamerically, 
shift nearer «gether. ami their number is further increased by the 
additing of painal *-;tin-, ters (Writer). These tertiary clefts 
evatinie t) inerease in camber throagbout life. 

Tt has alrewiy been mentinoed (pp 351) that the first primary yill- 
deft which aree in the ventral median line of the second truank- 
segment ~»n shifts t» the right side of the body. In an exactly 
similar was. oew yill-elefts form successively in the body-segments, 
that follow : Fizs. 290. 291), these clefts also lying in the ventral 
median line ami shifting later to the right side of the body. The 
row of préwary clefts now lying on the right side is destined later 
to take up its tinal position en the left side. The number of primary 
clefts which thus arise one after the other varies from twelve to 
fifteen. and ix usually fourteen. They hare a strictly metameric 
orranpwent aml, aceoniing to Hatscaer (No. 8), are intersegmental. 
The gill-clefts thus correspond to the boundaries of the segments. 





HatscHEeK No. >) regards the above-mentioned entoderm-vesicles as the most 
ft... Thexe vesicles correspond to the posterior boundary 
reirepresented by the cephalic process of the mesoderm 
as au undeveloped pair of primitive segments). 
ithe anterion ciliated arch, which is homologous 
Tunicates) was regarded by him as the second 
> which were described above as the first true 
rdin. to this interpretation, represent the third pair. 
somewhat smaller than the others: the clefts which 
int. are ai at first smalier than the rest and do not deviate from 
their median position to tie right. 











With the i 
pair of 
gill-clefts would a 
This pair ison 
follow the 








The median ventral blooLvessel which, in the pharyngeal region, 
constitutes the branchial artery, turns sumewhat to the right in the 
branchial region and then runs forward above the row of primary 
will-clefts (Fi wr). We have ly seen (p. ) that the 
course of this vessel is diverted to the right by the rudiment of the 
Inost anterior pair of gill-clefts. The course of this vessel marks the 
future ventral median line of the pharyns. 

A longitudinal ridge now soon 














ss above the 





rauchial artery on 


the right side of the body (Fig. 292, 4); this is composed of con- 





LATER LARVAL, STAGES. 





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fn Soups 'p fay qepnw aaniadap “2: we pepnes wasn ‘9 jods-oe ‘ma : euodonly Tt (MATTE 
pu waLSHASY] AVY “amqyn) sqrianizes-Spoq JO (ono-Saxys) coquane yp) 949 AP Ap "162 “OL 








d x ——— a SS er ae e 
aa SCOTT TTT IH AMT OAT 
~ Se er eer 


eee I PED e, 














Sarnypraqdon § AaHOSLY A sys gid yuso-aad ‘a ‘ gaodoxnan “dS yy 
qmamypna) pumg poanytio “af = qwaws ce come ‘p ! mpsoyo ‘yo ay [wpnVa Tn 
Aawontad 99a) 840 “ST “(ATLA PUY BALSTANT AVY ay) ‘squmuities-Apoq, Xt 





LATER LARVAL STAGES, 355 


aperture has meanwhile shifted from the left side and taken up a 
more anterior and ventral position. The branchial artery, which 
lies beneath the rudiment of the endostyle, now ocenpies the ventral 
‘middle line, while the secondary gill-clefts remain on the right side of 
the body (Fig. 293). A reduction in the number of the primary 
clefts takes place at the same time, the most anterior and some of 
the most posterior closing and completely disappearing (twelfth in 
Fig. 293), so that. finally the number of clefts on the right equals 
that on the left. These changes have been defined as the process of 
symmetrisation of the branchial region or the equalisation of the - 
gill-slits. They lead to a final stage in which an equal number of 
clefts (seven to nine, usually eight) is found on each side. This 
stage, which marks « long pause in development during which only 
the endostyle-rudiment yrows further posteriorly and the clefts 





Fic. 293,—Ventral side of an Amphionws lurve wt o later stage (after WILLEY), 2, 
second, 12, vestige of twelfth prnery gill-cleft; F-VITI, first eight secondary 
lefts; be, bnecal cirri: of, chordn ; ex, endostyle: m, mouth; v, velum. 








increase in height, has been named by Winey the critical stage of 
larval development. Wurnrey points out that the number of clefts 
at this stage approximately agrees with the typical number of gill- 
clefts in Vertebrates. 

The gill-clefts hitherto present were segmentally arranged, but 
this relation to the body-segments is lost in the tertiary clefts which 
are added later in pairs behind the clefts already formed. The most. 
anterior, originally seginental clefts (primary and secondary) are also 
then displaced forward. 

The primary clefts become early lengthened in the transverse 
direction of the body, #., vertically (Figs. 292, 293). . The secondary 
cleits, on the contrary, are, when they first appear, lengthened at 
right angles to this direction and consequently parallel to the 
longitudinal axis of the body (Fig. 293). Only in later stages do 
they also extend vertically. 





LATER LARVAL STAGES, 557 


The ateral folds at first lie very near together on the ventral side 
of the larva (Fig. 294). They are found in larvae in which nine or 
ten primary gill-clefts have developed. Behind this region, the 
lateral folds are bilaterally symmetrically placed at the sides of the 
median line. Near the gill-clefts, on the contrary, they diverge to 
the right (Fig. 294). The right lateral fold (xf) runs forward along 
the right side of the body above the clefts, in front of which it again 
bends toward the median line. It covers externally the upper part 
of the clefts. The left lateral fold (Jf) is at first only slightly 
developed anteriorly and rans almost along the median line in the 
branchial region. 

The lateral folds border a groove running along the ventral side 
which is the first rudiment of the atrial cavity. The posterior part 





op 
Fic: 204.—'Three larval stages of Amphiowus, from the ventral aspect (after Ray 
LANKgSTER and Writey). A, the atrium is still entirely open; B, the ae 


in ly closed CG, the atrium is almost compl 
fk gill ates 4 Teh 'raclaplenral fds me, mouths ay; rete moterlened 


of this groove closes first (Fig. 294 B), closure being effected by the 
appearance of two solid ridge-like projections of the inner opposed 
faces of the metapleurs (sub-atrial ridges of Ray Lankester and 
Wittey); these ridges grow out towards one another (Fig. 295 
A, sl) and fuse (Fig. 295 B), Through the fusion of the sub-atrial 
ridges, the floor of the atrial cavity is formed, in which later that 
part of the body-cavity called by Harsonmx (No. 8) the cavity of the 
lower folds appears (Fig, 311, uf, p. 572). The atrial cavity, which 
is at first tubular and open at both ends, gradually extends farther 
forward (Fig. 294 B and C), till, finally, the anterior part of the atrial 
cavity is completely closed towards the exterior, Only in the posterior 
part of it do the metapleurs still remain separate. The aperture here 


558 CEPHALOCHORDA. 


retuined is the atriopore (Fig. 294, ay). The lateral folds are also 
found in the adult as projecting ridges of the body-wall, running from 
the mouth to the atriopore. 

The atrial cavity thus formed is at first a tube with a compara 
tively narrow lumen (Fig. 295 8) which only secondarily widens ; 
this widening, which is accompanied by a shifting apart of the meta- 
pleural folds, is brought about by the lateral growth of the atrial 
cavity between the wall of the intestine and the body-wall pressing 
into the coelom so as almost completely to grow round the alimentary 
canal (Fig. 311, p. 572), the coelom being proportionately reduced as 





us to illustrate the 
¥). ao, aorta; ¢, 

Ph, dorsal fin-cavity ; m, myomere ; , neural tube; p, atrial cavity 
‘fh, metaploural cavity; “si, sub-iutestinal vein! sk, selera: 
ridge ; sp, voelom. 





7, metapleur; 
pal, suleatrial 





the atrium enlarges. Part of the outer wall of the atrial cavity (the 
epipleura of Ray LankestTeR) therefore does not arise through the 
formation of folds, but is a modified portion of the body-wall which 
has undergone no displacement. [See also MacBripg, No, VIL. «.] 


The formation of the atrial cavity in Amphiorus recalls to some extent 
that of the similarly placed cavity in the Ascidians which, as we have seen. 
originated in the form of paired invaginations (p. 366) which also o 
secondarily grow round tho pharynx. 

The outer wall of the atrial cavity cannot be homologised with the oper- 
culum of the fishos, the latter being a fold which bolongs exclusively to the 
hyomandibular arch. 












LATER LARVAL STAGES. 559 


The metapleural folds have frequently been homologised with the 
primary paired lateral fins of the Vertebrata (Ray Lankester and 
Wiuury, Harscuek). According to HatscHek (No. &), they are 
merely special parts of « system of ventral folds which in the most 
anterior part of the body develops as the unpaired ventral fin of the 
rostrum, in the oral region forms the lateral buecal wall, in the 
branchial region the metapleural fold. and, finally, behind the atrio- 
pore, the unpaired ventral fin which extends in front of and behind 
the anus. The “cavities of the lower folds” which develop in the 
sub-atrial ridges are said to be the cavities of the unpaired ventral 
fin. 

We have already alluded (p. 550) to a ciliated band lying on the 
right side of the pharyngeal wall in front of the club-shaped glud 
(Fig. 289, fl). This ciliated band, in which a somewhat clearer inner 
zone can be distinguished, resembles in shape the club-shaped gland, 
so that, in the illustration, it looks like a shadow or a reduplication 








of the latter. It is the rudiment of the endostyle and, even in early 
stages, appears bent on itself (Fig. 292 A, ex), being divided into a 
shorter upper and a longer lower half. The endostyle-rudiment then 
proceeds backward (Fig. 292 B) passing over the club-shaped gland 
into the space between the primary and secondary clefts. It thus 
comes to overlie the branchial artery. During the shifting mentioned 
above as taking place in the branchial region, the endostyle-rudiment 
passes from the right side of the body to the ventral median line 
ig. 293, -x). The upper half of the bent rudiment becomes the 
right and the lower half the left part of the endostyle of the adult. 
At an early stage, two ciliated arches, the peripharyngeal bands, are 
to be seen ascending from the anterior end of the eudostyle-rudiment 
to the dorsal side of the pharyngeal wall (Fig. 296, #1), and then 
continue backward on either side of the dorsal middle line as the 
ciliated hyperpharyngeal (epipharyngeal) bands. The proximal part 
of them corresponds to the ciliated arches (pericoronal arches or 
peripharyngeal bands) of the Ascidian (W1ILLEY). 

The formation of the definite oral aperture has been described in 
detail by Wiiuey. The oral aperture shifts from the left side of 
the body forward and ventralwards, so that it finally occupies a 
median symmetrical position un the ventral side. At the same time, 
it becomes grown over by a secondary fold of the body-wall (Fig. 296, 
mr), the stomodaeum or oral hood being thus formed. ‘The primary 
oral aperture of the larva shifts to the back of the buccal cavity and 
its lips are retained as the velumn (r) : here the first rudiments of the 











LATBR LARVAL STAGES, 561 


Wine, like the larval mouth, an organ belonging to the left side of the body, 
in spite of its apparently symmetrical position. 

It is difficult, from Wiuury’s description, to gain a clear idea of the shiftings 
which occur in the oral region. According to this author, the longitudinal axis 
of the slit-like larval mouth rotates about a vertical axis through an angle of 
90". Originally it lies parallel to the axis of the body, but is at right angles 
to it later. Consequently, the anterior part of the larval mouth sinks in and 
passes to the right side to give rise to the right half of the velum, while the 
left half of that organ is derived from the posterior corner of the mouth. 
Similar shifting of the labial folds takes place. 

VAN WisHE maintains that the mouth of Amphiorus is not homologous 
with that of the Craniata. He also doubts the homology of the velum of 
Amphiorus with that of the Cyclostomi. According to him the mouth of 
Amphiorus is a gill-cleft lying on the left, and the club-shaped gland is the 
corresponding organ on the right side of the body. van WisHe homologises 
it with the left spiracle of the Selachians and with the left gill-cleft of 
Appendicularia (2. 








In the later larval stages, when eight secondary gill-clefts have 
already developed and the tongue-bars have begun to form, the 
elub-shaped gland degenerates, and finally, as it appears, reaches 
the interior of the alimentary canal where it is perhaps absorbed. 
The aperture of the gland into the intestine which was mentioned 
above (p. 550) seems to withstand disintegration longer than any 
other part of the organ (Wi1zy). 

In these later stages an organ is found which was discovered by 
Harscuek (No. 5) and was figured and described both by him and 
by Ray LankEsTER and Winury (Nos. 12 and 23) as the kidney 
(nephridium, Fig. 290, x). This is developed only on the left side in 
the form of a mesodermal ciliated funnel and canal lying in front of 
the mouth in the region of the first metamere (between the pre-oral 
pit and the mouth). It lengthens posteriorly later and is found, in 
the adult, as a strand extending on the left side beneath the chorda 
from the anterior edge of the mouth to immediately behind the 
velum. HAaTSCHEK conjectured that this canal opened into the 
pharynx. [See MacBrrpe, No. VIIL. «.] 


This last observation has recently been confirmed by vAN WisHE (No. 22) 
who considers this organ, which he calls the oesophageal process, as the 
remains of the original communication between the intestine and the left 
anterior entodorm-diverticulum. 


We have already mentioned that, in the larval stages which follow 
the stage with one primary gill-cleft, the number of primitive segments 
is continually increasing through the formation of new segments from 


the mexoderm-folds at the posterior end of the body. At the time 
00 


LATER LARVAL STAGES, 563 


relation of these compartments to the segmentation of the body cannot 
be made out. — 

The anal aperture which originally lay at the posterior end of the 
body shifts later further forward (Fig. 291), and this leads to the 
development of the post-anal region of the body characteristic of 
the Vertebrates, 

We have seen above (p. 545) that the anterior end of the medullary 
tude, which lies in the region of the first true primitive segment and 
the so-called cephalic process of the mesoderm (anterior primitive 
segment of HatscnEx) is widened (Figs. 288, 289). This part, 
according to HarscHex’s recent statements (No. 8), becomes dif- 
ferentiated, in the young Amphioxs, into three consecutive sections 
which correspond to the three primary cephalic vesicles of the Craniata, 





Fig. 297.—A, transverse sections en glen the brain of a young Amphiowue (after 
Hatscuek). /, through the (primary) first ventricle ; ah through the (primary) 
second ventricle (aquaeductus Syivii); HH, through the (primary) third ventricle 
(fossa rhombnidalis). B, transverse section through the spinal ord, 





Fie. 298. 
Fic. 298.—Brain with the most anterior nerve-roots of a ike J Amphioxus (after 


Harscnex), Ch, chorda dorsalis; N, ciliated pit, to the wall of which 
the olfactory nerve runs ; £, 7, 12, the three primary ventricles (diagrammatic), 


The anterior section, the primary fore-brain, shows, in transverse sec- 
tion, the well-known dilation of the medullary tube which constitutes 
the first primary ventricle (Figs. 297 4, 7; 298 J). The anterior end 
of this ventricle is continued towards the neuropore (é.c., towards the 
ciliated olfactory pit) into the infundibulum (the lobus olfactorius of 
LAnGeruans) which, in Amphiorus, is curved upward. The second 
part of the brain (the mid-brain) contains within it the second 
primary ventricle, which is represented by a narrowed portion of the 


564 CEPHALOCHOERDA. 


medullary canal (aquaeductus Sylvit, II). In the third part (the 
hind-brain) the central canal shows a narrow ventral tube, while its 
dorsal portion is independently dilated so as to form a vesicle covered 
by a thin membrane, the fossa rhombowlalis of HatscnEk (111). 

The medullary tube originally opens externally through a neuropore 
bordered by closely crowded flagella. This is pressed out of the 
middle line to the left through the development of the dorsal fin. 
An epithelial depression forms later at this point ; this is KOnLIKER's 
olfactory or ciliated pit (Fig. 298, x), at the base of which the neuro- 
pore opens. The ciliated pit is the homologue of the olfactory organ 
and of the hypophysis of the Craniata. The short, unpaired olfactory 
nerve discovered by LANGERHANS runs from the brain to the posterior 
wall of the ciliated pit. The continuation of the first ventricle towards 
the neuropore corresponds, as above mentioned, to the infundibulum 
of the Craniata. In Ammuocoetes, the hypophysis and the olfactory 
organ are still connected together, and the external aperture of the 
hypophysis still retains its original dorsal position. The inner end of 
the hypophysis, on the contrary, and the infundibulum have moved 
to the ventral surface of the brain. 

In identifying the anterior end of the medullary tube of Amphiorus with 
the infundibulum of the Craniata we have followed HatscHex. It should, 
however, be mentioned that Kuprrer has recently been lod by his researches 
on Acipenser (No. 38) to homologise the anterior end of the cranial axis of 
Amphiorus with his lobus olfactorins impar which lies near the lamina 
terminalis above the anterior commissure, and indicates the point where the 
medullary tube remained longest in direct connection with the ectodenn 
precisely as in Amphiocus, and to regard the infundibulum as a secondary out- 
growth of the ventral side of the brain. 

It should here be pointed out that Kout (No. 9) occasionally noticed, on 
the right side of the head of .Lmphioxus, a pit resembling the olfactory pit of 
the left side. Konu is inclined to consider this as the half of an originally 
paired olfactory organ in a vestigial condition. The relations of the neuropore 
to the olfactory pit were denied by Kout, The remains of the neuropore are 
said to be found in an ectodermal depression lying somewhat behind the 
olfactory pit. 

Our knowledge of the important transformations that take place in 
the primitive segments and the body-cavity is due chiefly to HATSCHEK 
(No.7). Each primitive segment becomes divided by a transverse 
partition into two portions, as has already been stated (p. 547), viz.. 
a dorsal portion (proto-vertebra) and a ventral part (lateral plate, 
Fig. 300, / and J/). Only in the dorsal portion is the primitive 
segmentation retained, the adjacent walls of the segments persisting 
as the transverge septa (myosepta). In the region of the lateral 


LATER LARVAL STAGES. 565 


plates, the septa disappear and the segmental cavities enclosed by 
them flow together to form a common cavity surrounding the intestine 
(splanchnocoele). The disappearance of the ventral mesentery leads 
to intercommunication between the right and left halves of the 
splanchnocoele. 

The proto-vertebrae enclose segmentally-arranged cavities which, 
however, ure not quite symmetrical in relation to the median plane 
(p. 545). These are the cavities of the proto-vertebrae or the 
myococles (Fig. 153, Z). The walls of each proto-vertebra consists of 
a parietal (7) and an inner (2) layer. The parietal layer (/), which 
consists of flat cells, applies itself closely to the ectoderm, and since 





Fic. 299.—Transverxe section Fig, 300,— Diagrammat 
from the middle of the body ing of the same sec 
of an .tinphiocus larva with 
five branchial clefts (after 
HaTScHEK). 





A, epidermis; 8, medullary tube; (, chorda; (, 
epithelium ; #, sub-intestiual’ vessel. is-layer: 2, muscle-layer (lateral 
‘trunk-muac! 3 sclera-layer ; }. boundary cells of the proto-vertebra ; 6, somato- 
plenre; 4, splanchnopleure. -/, myocoele ; 77, splanchnocoele, 


inner chorda-sheath ; /), intestinal 














it yields the cutis of the adult, is sometimes termed the cutis-layer. 
The cells of the inner layer, at the sides of the chorda and of the 
medullary tube, elongate transversely and longitudinally, as described 
above (p. 548), and, as they give rise to the muscle-tibres of the 
myotome, this part is spoken of ax the muscle-plate. 

At first, each muscle-cell contains only one fibrilla, but as the 
number of fibrillae increases later they are arranged in regular order 
one above the other. Several such groups of fibrillae occur in each 
muscle-cell. The nuclei of the muscle-cells lie on the outer side 
of the muscle-layer that turns towards the myocoele. Towards the 
ventral side, the muscle-layer is continued into a pavement-cpithelium 








LATER LARVAL STAGES, 567 


(selerotome). The musele-plate is then connected merely at its dorsal 
edge by means of a mesentery-like band to the wall of the proto- 
vertebra and otherwise hangs quite freely into the cavity of the 
same. Its chief points of attachment are to the dissepiments. The 
inner wall of the selerotome becomes applied to the chorda and the 
medullary tube, and here forms the skelefogenous layer which yields 
the outer sheath of the chorda (4) and the neural continuation of the 
Jatter, The outer layer of the selerotome becomes applied to the 
inner side of the muscle-layer and forms the internal sheath or 
Juscia-layer (3). The lateral trank-muscle of Amphiocus is not 
entirely surrounded by fascia, since this layer only develops on its 
inner side. 

All these layers, derived through differentiation from the wall of 
the proto-vertebra, shift ventrally, pressing in between the ectoderm 
and the somatopleura. he cutis-layer in this way comes to lie in 
the ventral middle line, where it yields the lining of the cavity of the 
ventral fin (7,,), and the dorsal fin-cavities (/.) seem in the same way 
to be lined by the cutislayer. From the floors of these cavities, the 
fin-rays grow up later. The skeletogenous and the muscular layers 
also shift ventrally. 

The method of formation of the layers agrees in all essential points 
with that of the Craniata. In this type, beneath the epidermis, lies 
the cutis-layer (1) which, in Amphioxus, retains its simple epithelial 
character throughout life. This is followed by the myocoele, which 
also here persists throughout life. Then comes the muscle-layer (#) 
and on the inner side of the latter lies the fascia-layer (3) ; m the 
Craniata the fascia is also developed on the outer surface of the 
muscles ; then comes the cavity of the sclerotome, and, finally, the 
skeletogenous layer (4). The latter (as chorda-sheath) encloses the 
chorda and also the medullary tube in the dorsal half of the body ; 
in the lower half, it becomes applied to the somatopleure. ‘The two 
layers (skeletogenous layer and somatopleure) here form a delicate 
partition-wall, the intercoelic membrane (5 and 6) which separates 
the cavity of the primitive vertebrae from the splanchnocoele, On 
the inner side of the splanchnocoele lie the splanchnopleure and the 
entodermal intestinal epithelium. 

In the branchial region (Fig. 311) the condition of the body-cavity 
is complicated through the development of the atrial cavity (p), which 
presses in between the splanchnocoele and the ventral part of the 
myocoele. The latter then lies in the peribranchial fold and breaks 
up into sections called by HarscneK (No. 8) the upper and lower 





LATER LARVAL STAGES. 569 


part along the ventral edge of the protovertebrac where the cutis-layer 
passes into the skeletogenous layer, small cells filled with deeply 
staining nuclei can be made out. These are accumulations of primi- 
tive genital cells which represent the rudiment of the genital gland, 
and which may perhaps be traced back to HaTscHEx’s large boundary 
cells mentioned above (Fig. 299, 4, p. 565). These agglomerations of 
cells are repeated at definite intervals in series of cross-sections. 
Nince they are related to the dissepiments between the mesodermal 
somites, they are affected by the asymmetry of those structures and, 
like them, alternate on the right and left sides of the body. In 
superficial views of later stages (Fig. 303), the rudiments of the 








Fre. 305, Fic, 306, 
—Later stages of developmeut of the genital rudiment 
(after (BovEnt). 











307, Ge 
an Lmphiorus 
{after Bovert). 


ital rudiment in 
» Samm. long 








genital gland can be seen as rounded kuobs (gd) lying in small 
outgrowths in the posterior lower angles of the myocoeles (rudi- 
ments of the genital pouches). 

Examination of the genital rudiment in the youngest stages reveals 
that it arises as a modified part of the epithelium on the anterior 
wall of each myococle (Fig 304). is epithelial growth then forms 
a hernia-like invagination into the cavity of the preceding segment 
(Figs. 305, 306), and in this way constitutes a knob which at first is 
hollow but is provided later with a himen (Fig. 307), and which is 
covered superficially with an epithelium derived from the posterior 
wall of the segment into which the knob projects, the latter being 























Ftc, 309,—Two consecutive yenital vesicles of an 
BOVERI). 












So as to complete our deseription of the 
we must, in conclusion, briefly deseribe the re 
Bovent (Nos. 1 and 2) in the adult animal. 
found in the region of the pharynx which 
coelom (Fig. 311, sc) with the atrial eavi 


GENERAL CONSIDERATIONS. 571 


mesial side of the sub-chordal coelomic sac, and open into the atrial 
cavity at the uppermost angle where the wall that covers the outer 
side of the gill-bars bends outward to 
form, together with the wall of the 
sub-chordal coelomic sac, the thin 
partition-wall known as the ligamen- 
tum denticulatum (/d). This latter, in 
the primary gill-bars, extends further 
down than in the secondary (Fig. 312, 
7 and ZJ). The nephridial canals 
recur regularly in the pharyngeal 
region and open on the tongue-bars 
(Fig. 312). In each canal (nt) an 
anterior ascending branch can be 
distinguished from a short posterior 
branch. Each of these branches 
opens at its end into the sub-chordal 

coelomic cavity (nc, funnel), and in Pours aeraoerrioeciae 
the course of the canal three or four the represented in Fig. 309 
other apertures occur. Round these on Pag esl fy 
apertures (nc) the cells of the walls of etnct land; ee bee 
the sub-chordal coelom are peculiarly ‘ Mid ts 
modified. Highly refractive spherical cells are found in the body- 
cavity connected with the apertures by means of delicate filaments 
(thread-cells), Round the nephridial canals, the upper ends of the 
branchial vessels, by anastomosing, form a vascular network which 
we may call the glomerulus (Fig. 311, g@). 

Bovent regarded these canals as homologues of the pronephros of the 
Craniata, and the atrial cavity of Amphiorus as the homologue of the 
pronephric duct of the Vertebrata. For further details on these points we 
must refer the reader to the works of this author. Nothing is as yet known 
of the development of these renal canals, We are also in the dark as to their 
relation to the larval organ mentioned above and described by HaTscHek as 
the nephridium, but it should be mentioned that the figure of this organ given 
by Harsousx (No. 14) shows a certain similarity to the canals discovered by 
Bovent, Objections have recently been raised to Bovent’s generalisations by 
Semon and van WisHe (No. 22). 





General Considerations. 


With regard to the systematic position of Amphiorus, we adopt 
the view now accepted by most zoologists that this animal is to be 
regarded as the representative of a very primitive group which served 


GENERAL CONSIDERATIONS. 
ditions of the blood-vascular system, and especially to the development 
of the body-cavity which, as made known by Harscunx, yields the 
key for understanding the formation of the layers in the Vertebrates, 
Tt must further be pointed out that the development of Amphiorus 
without doubt shows very primitive characters, a view to which 
however, objections have been raised by Donrn. The occurrence of 
free-swimming ciliated larvae, nevertheless, can hardly be interpreted 
in any other sense. 








T Ir I ia T 
eg rete ete ge 

Se lpr at entfael ontg' Gs toe eal Oe Sense 

cavity De synaptionlum ; Z, primary Mite Te tongue-bar. 

Considering the agreement prevailing between Amphioxrus and the 
Vertebrates, it is important to emphasise the distinctions between the 
two forms. Amphioxus is specially distinguished by the rostrum- 
like prolongation of the notochord, by the secondary increase in 
number of the gill-clefts, and by the duplication of sueh primary clefts 
through division (development of the tongue-bars), this last character- 
istie recalling the multiplication of the gill-clefts in the Ascidia. 
With regurd to the condition of the urogenital system, we must refer 
to the accounts of Bovert (No. 2), according to which the renal 
canals of Amphioxus are to be considered as the homologue of the 
pronephric canals of the Vertebrata, and the atrial cavity of 






























kidney in the latter. sates dates. 
must still recognise certain distinctions be 






whieh, however, would not then be of a fi 
‘Through the great development of the atrial 






assumptions of Doxrn (p. 522), that A 
derived from the Craniata. We do not deny th 
consequence of its half-sedentary manner of life 
may have undergone a certain degree of 
tion. Above all, we might in this way explai 
of the brain and the sensory organs and also omo 
It is naturally difficult to determine how far the simple st 
Amphinens vests upon primary peculiarities o 
peculiarities secondarily acquired through deg 
of the facts known to us as to the ont 1 
Amphiorus seem to indicate that we have in- 
with a very primitive form. 










specially marked in the larval forms, but is also 
extent in the adult (position of the olfactory pi 
the hepatic caecum, conditions of the Vv 

the definitive mouth according to van Wisner). Wr 
that the Amphiorus larva lies when at rest at | 
on the right side of the body seems to ind 
is acquired in the same way as in the 


dpe ‘Witney, ith 
this point, fot toad the yood, whan Ranh 7 


GENERAL CONSIDERATIONS, 575 


We therefore regard Amphioxus as a very primitive chordate form 
very closely related to the hypothetical ancestor of the Craniata, but 
somewhat more distantly related to the Tunicates. Every specula- 
tion as to the origin of the Vertebrates and the Chordata must 
necessarily take account of Amphiocus as the most primitive repre- 
sentative and the starting-point of the whole series. Among all the 
hypotheses* which have hitherto been advanced as to the origin 
of the Chordate stock, that which derives it from the Annelida has 
at present most adherents. As the founders and most eminent 
upholders of this hypothesis we must name Semprrr (No, 46) and 
Dourn (Nos. 30 and 31), while, more recently, a whole series of 
renowned zoologists have taken part in its further development. The 
view that the Vertebrates are descended from Annelids rests chietly 
on the similarity in the segmentation of the body and in the produc- 
tion of new segments at the posterior end of the body; further, on 
the agreement in the position of the more important organs, if we 
assume that the hypothetical Annelid ancestor of the Vertebrata 
underwent such a rotation round its longitudinal axis that the former 
ventral side became the dorsal side, an assumption which lay at the 
root of Gxorrroy Sr. Hruare’s statement that ‘* Insects are 
Vertebrates running on their back.” When such a rotation is 
assumed, the ventral ganglionic chain of the Annelida corresponds 
to the medullary tube of the Chordata, the ventral longitudinal 
vessel of the Annelida becomes the aorta, while the dorsal vessel 
corresponds to the sub-intestinal vessel. The Annelidan hypothesis 
obtained its strongest support when Sxarsr discovered a remarkable 


bottom and fall ou one side, is due to the physical impossibility to rest in any 
other position, and not to a pressing desire or instinct to assume this position, 
The asymmetry of Amphioxus is of a totally different character to that of the 
Plouronectidae. For a full account of these views, see Wiumy, Amphioxua 
and the Ancestry of the Vertebrates. Columbia Univ. Biol. Series, 1894.—Ep. J 
* We have no intention of entering upon the much-disputed point of the 
origin of the Chordata except in a way. A detailed investigation of 
this difficult problem would require a study of vertebrate embryology which 
does not fall within the scope of the present work. We have already, in the 
foregoing chapter (p. 523), stated that the Tumicates contribute little to the 
solution of this question. cay ose to be considered as degenerate members 
of the Chordate stock, of which Amphiorus is to be regarded as the most 
primitive form. Of the many theories on the subject of the relationship of 
the Chordata we have here alluded only to those two which appear best 
founded on actual morphological facts, viz., the derivation of the Chordata 
from CASA and the assumption of relationship between the Chordata and 
The hypothesis of the relationship to the Nemertines has 
been briefly Parkidea Soveowe (vol. i., p. 291). We do not consider it nec 
to refer to the relationship of the ertebrata to the Arthropoda which has 
recently been again assumed. 


576 CEPHALOCHORDA, 


similarity of structure between the primitive kiduey-tubules of the 
Selachian embryo and the segmental organs of the Annelida. Our 
acceptance of this homology, however, has been recently made ian- 
possible by the researches of vAN WusHE (No. 48), Rickert 
(No. 44), and Boverr (No. 2) which cause us to doubt the serial 
homology of the pronephros with the primitive kidney and to regard 
the latter as a secondary acquisition which in any case has nothing 
to do with the segmental organs. From this point of view it would 
be the pronephros which requires consideration. 

The derivation of the Vertebrates from the Annelida is, in fact, 
accompanied by certain difficulties which are not insurmountable. 
The most important of these is the position of the mouth. While, 
in the Annelida, the oesophagus perforates the central nervous system 
at the oesphageal ring in such a way that the supra-ocsophageal 
ganglion comes to lie above and the ventral cord below the gut, 
no such relation between the stomodaeum and the central nervons 
system is to be found in the Vertebrates. The most varied hypotheses 
have been suggested to obviate this difficulty. ScHNEIDER thought 
that he could discover in the connection of the hypoglossal and tri- 
geminal nerves an equivalent for the oesophageal ring. vAN BENEDEN 
and Junin (No. 29) have assumed that, in the primitive ancestors 
of the Vertebrates, the oesophagus shifted forward in the median 
plane between the still unconnected cephalic lobes of the brain, while 
other zoologists like KLEINENBERG, BEarp, No. 27, v. KENNEI. 
(No. 35a) believe that the supr-vesophageal ganglion atrophied and 
that the brain and the dorsal chord of the Vertebrates only are the 
equivalents of the ventral cord of the Annelida. In connection 
with this idea, we have the question as to the primitive mouth of 
the Vertebrates. Under the assumption that the pro-cephalon of 





the Vertebrates corresponds to the supra-oesophageal ganglion of these 
Annelida, we should have to conjecture that the original vertebrate 
mouth, which perforated the oesophageal ring, has disappeared. The 
definitive mouth of the Vertebrates would have to be regarded as a 
secondary formation, and is by many zoologists thought to have arisen 
through the fusion of gill-slits. ‘There is actually mueh to support 
the view that the mandibular arch is a branchial arch which has 
been drawn into the mouth. This, however, does not decide the 
question of the derivation of the vertebrate mouth from gill-clefts. 
In the case of Amphiorns, there is no ontogenetic indication of the 
derivation of the mouth from gill-clefts. The mouth here arises in a 
different manner from the gill-slits (p. 550) and in a different position. 


GENERAL CONSIDERATIONS. 577 


Harscuex (No. 8) has therefore maintained that the velar opening 
of Amphioxus is not to be regarded as a gill-slit. 

The attempt has often been made, in following out these ideas 
further, to discover vestiges of the primary vertebrate mouth, which 
has been sought in the rhomboidal fossa, the pineal gland and the 
hypophysis, Only recently, Brarp (No. 27) and Kurrrer (No. 38) 
have pointed to the hypophysis as the primary mouth (palaeostoma) 
of the Vertebrata. 

An altogether satisfactory solution of the difficulties connected with 
all these questions is, however, at present wanting. 

Attempts have been made in other directions also to find the con- 
nection between the Vertebrates and the Annelida. We may recall 
the discovery by Eisia of organs in the Capitellidae comparable to 
the lateral line of the Vertebrata, the homologising of the spinal 
ganglia of the Vertebrates with the parapodial ganglia of the Annelida 
by KiLEiNenberc (No. 36), the derivation of the unpaired fin of the 
Selachians from fused Annelidan parapodia by P. Mayer (No. 39), 
the attempt"to derive the vertebrate eye from the Annelidan eye 
by v. Kennet (No. 35a), etc. For its support, the Annelidan 
hypothesis has required a number of sub-hypotheses. Nevertheless, 
we must admit that the gap which divides the Annelida from the 
Chordata is even now very considerable, and, as BaLFrour pointed 
out, the two most typical organs of the Chordata, the notochord and 
the gill-clefts, are not foreshadowed in the Annelids. Attempts have 
not been wanting, it is true, to find the equivalents of these organs 
in the Annelids. The origin of the mouth from paired rudiments in 
the buds of Nais and Chastogaster (SkmPER) was compared to the 
formation of gill-clefts, while the most varied structures in the 
Annelida were regarded as homologues of the chorda. With regard 
to this latter point, the view that most deserves attention is that of 
Exvers (No. 32) and E:ste (No, 33), who see in the so-called 
accessory intestine of the Cwpitellidae and the Kunietdae (and in 
similar structures in the Gephyrea) the homologue of the notochord. 
On the other hand, it should be mentioned that the researches of 
Kreierserc (No, 36) on this point did not lead to satisfactory 
results. “In the development of most Annelids,” says KLEINENBERG, 
“there is no trace of the accessory intestine; I found it only in the 
larvae of those forms which possess it when adult, viz., the Caprfel- 
Ndae and the Hunicrdae. Ina larva belonging to the last of these 
families it hangs as a somewhat short loop beneath the principal 


intestine and opens both anteriorly and posteriorly into the latter. 
PP 


578 CEPHALOCHORDA. 


In the Capitellidae, a diverticulum forms early at the most posterior 
part of the archenteron and grows out anteriorly. I believe that this 
is the rudiment of the accessory intestine, but am not quite certain 
on this point.” With regard to the origin of the gill-clefts. we may 
assume that the originally blind intestinal diverticula secondarily 
acquired external openings, so as to allow of the outtlow of the 
respiratory water. The assumption that such perforations occur 
is supported by the actual presence of pores of communication at the 
ends of the tentacles in the Actinia, and in the hepatic tubes of some 
Acolidue. 

We are not, however, able to regard the Annelidan hypothesis as 
resting on altogether certain foundations. It seems to us that we 
have no convincing proof that the many points of agreement which 
actually exist between the Annelida and the Chordata rest upon true 
homology. The crucial point of the whole question lies in the 
decision as to whether it is necessary for us to refer the similar 
method of segmentation of the body in the two groups to their 
derivation from a common ancestor. It is evident that, as BaTEson 
(No. 26) has shown, it is not a decisive objection to this assumption 
that the characteristic segmentation in each of the two groups (the 
Annelida and the Chordata) has arisen separately, or, in other words, 
that the common ancestor of the two groups was still unsegmented. 
Batrovr (No. 25) in this connection wrote “that we must look for 
the ancestors of the Chordata, not in allies of the present Chactopoda, 








bat in a stock of segmented forms descended from the same un- 
segmented types as the Chaetopoda, but in which two lateral 
nerve-cords, like those of Nemertines, coalesced dorsally, instead of 
ventrally to form a median nerve cord.” 

If, after w tid, we do not regard the derivation 
of the Chordata from the Annelida as certainly proved. and institute 





has just been 


comparison with the other invertebrate groups, we are confronted first 
of all by Balanuylossus which, in the possession of gill-clefts in the 
phi 
striking agreement with the type of the Chordata. This form was 
formerly thought to be nearly related to the Chordata by GEGENBAUR 
and Huxvey and more recently by Bateson, HaEcKEL, ScHi- 
kKewrrscH, MoxGas, Route and others. We are far from regarding 
as established the various homologies assumed by BaTEsoN between 
ad on this point refer the reader to 
isin of the best qualified judge in this matter— 
EL (No. 47, p. 721, ete.) who denies all relationship between 


vnygeal region and the nerve-strand ronning dorsally shows 














Balsnoglossus and Amphiorus, 
the detailed crit 
Ss 








GENERAL CONSIDERATIONS. 579 


the Chordata and Balanoyloxsux. Bateson (No. 26) homologises the 
dorsal nerve-strand in the collar region of Balanoglossus (the so-called 
collar-cord) with the medullary tube of the Vertebrates. The anterior 
intestinal diverticulum (the so-called proboscis-intestine) of Bulano- 
gloxsus (Vol. i., Fig. 165, di, p. 375), according to him and to KozHLER, 
is the homologue of the notochord. The rudiment of the so-called 
proboscidal coelom is homologised with the anterior unpaired entoderm- 
diverticulum of Amphiocus (Fig. 285 B). The externil aperture of 
the left anterior entoderm-diverticulum of Amphiocus is assumed to 
correspond to the proboscis-pore of Bi/nugloxsux. A posterior fold 
in the collar-region, called by BaTEson the “operculum,” is said to 
correspond to the epipleura of Amphiorus. Finally, even GEGENBAUR 
compared the ventral nutritive section of the pharynx in Balanoyloseus 
(Vol. i., Fig. 166, d, p. 377) to the endostyle of the Tunicates. 
SpenGEx (No. 47) has pointed out the difficulties that stand in the 
way of such a homology, and lays special stress on the great difference 
in the position of the gills which, in Bu/anoglossus, are dorsal, and, in 





Amphiorns, veutral—the development of the blood-vascular system 
and the genital organs in the two groups. The bare fact of the 
presence of gills in Ba/anoglossus, indeed, and their remarkable and 
detailed agreement in structure and arrangement with those of 
Amphiocus (U-shaped form in consequence of the growth of tongue- 
bars, chitinous skeletal structures in the form of prongs, presence of 
synapticula) seem to us of such significance that we cannot avoid 
the thought that we have, in Ba/anoglossus, the only living form of 
Invertebrate which is closely related to the Chordata. But, if we 
adopt this assumption, the Chordata naturally become somewhat 
more remote from the Annelida, since Bulanoglossus is only distantly 
related to this last group. How far it is possible to remove the dithi- 
culties which now lie in the way of establishing a stricter homology 
between Balunoglosxux and Amphiorns must be decided by further 
research. 

The problem of the derivation of the Chordata is not solved by 
assuming a relationship between them and the Enteropneusta, since 
the latter themselves occupy an unusually isolated position. Only 
through the structure of the Ba/anoygloxsus larva is an indication 
given of remote connection with the Echinoderma. We must 
resign ourselves to the thought that we are not ut present in a 
position to state from what primitive form the Chordata and, with 
them, Balanglossus are to be derived. The origin of the Vertebrates 
is lost in the obscurity of forms unknown to us. 











580 


1, 


=, 


4. 


10. 


11. 


12. 


13. 


14. 


CEPHALOCHORDA. 


LITERATURE. 


Bovert, Tx. Ueber die Niere des Amphioxus. Miinchener 
Med. Wochenschr. No. 26. 1890. 

Bovert, Tu. Die Nierenkanalchen des Amphioxus. Ein Beit- 
rag zur Phylogenie des Urogenitalsystems der Wirbelthiere. 
Zovl. Jahrb. Abth. f. Anat. Bd. v. 1892. 

Boveri, To. Ueber die Bildungsstiitte der Geschlechtsdriisen 
und die Entstehung der Genitalkammern beim Amphiorus. 
Anat, Anz, Jahrg. vii. 1892. 

Hartscaex, B. Studien iiber Entwicklung des Amphioxus. 
Arb, Zool. Inst. Wien. Bd. iv. 1881. 

Hartscuex, B. Mittheilungen tiber Amphioxus. Zool. Anz. 
Jahrg. vii. 1884. 


. Harscnex, B. Zur Entwicklung des Amphioxus. Vers. D. 


Naturf. Aerzte in Berlin, Tagebl. lix., p. 271. 1886. 


. Harscuex, B. Ueber den Schichtenbau von.Amphioxus. Anat. 





Anz, Jabrg. iii, 1888. 





. Harscuer, B. Die Metamerie des Amphioxus und des Ammo- 


coetes. Verhandl. der Anat. Gesellech. 6. Vers. in Wien. 
Anat. Anz. Jahrg. vii. 1892. 


. Kort, C. Einige Bemerkungen iiber Sinnesorgane des Amphi- 


oxus lanceolatus. Zool. Anz. Jahrg. xiii. 1890. 

Kowaevsky, A. Entwicklungsgeschichte des Amphioxus 
lanceolatus. Mém. Acad. Impér. St. Pétershourg (7). Tom. ii. 
1867. 

Kowauevsky, A. Weitere Studien iiber die Entwicklungs- 
geschichte des Amphioxus lanceolatus.  Archir. 7. mikro. 
Anat. lid. xiii, 1877. 

Lanxester, E, Ray. Contributions to the Knowledge of Am- 
phioxus lanceolatus Yarell. Quart. Journ. Micro. Sei. (2). 
Vol. xxix. 1889. 

Lanxester, E. Ray anp WinueEy, A. The Development of the 
Atrial Chamber of Amphioxus. Quart. Journ. Micro. Sci. (2). 
Vol. xxxi. 1890. 

Leuckart, R. unp NitscHe, H. Zoologische Wandtafeln. 
Cassel, Plate 72 contains a drawing of a hitherto unfigured 
stage of Amphioxus. Cf. also the accompanying text by 
Harscnek. 


. Leuckart, R. unp PaGenstecHER, A. Untersuchungen iiber 


niedere Seethiere. 1. Amphioxuslanceolatus. Archiv. f. Anat. 
Phys. 1858, 








LITERATURE. 581 


16. Lworr, B. Ueber Bau und Entwicklung der Chorda von Amphi- 
oxus, Mittheil. Zool. Stat. Neapel. Bad, ix. 1889, 

17. Lworr, B. Ueber einige wichtige Punkte in der Entwicklung 
des Amphioxus. Biol. Centraldl. Bad. xii, 1892. 

18. ScnunTz", M. Beobachtung junger Exemplare von Amphioxus. 
Zeitschr. f. wise, Zoot. Ba. iii, 1851. 

19. Spencen, J. W.  Beitrage zur Kenntniss der Kiemen des 
Amphioxus. Zool. Juhrb. Abth. f. Anat. Bd. iv. 1890. 

20. Wass, F. E. Kxeretory Tubules in Amphioxus lanceolatus, 
Quart. Journ, Micro. Sei. (2). Vol. xxxi. 1890. ~ 

21, van Wuue,J,W. Die Kopfregion der Cranioten bei Amphioxus, 
ete. Anat, Anz. Jahrg. iv. 1889. 

22. van Wune, J. W. Ueber Amphioxus. Anat. Anz. Jahrg. viii. 
1893. 

23. Wituny, A. The Later Larval Development of Amphioxus. 
Quart. Journ, Micro. Sei. Vol. xxxii. 1891. 

23a, Witsoy, E. B. On Multiple and Partial Development in 
Amphioxus. Anat. Anz. Jahrg. vii, 1892. 


On the Phylogeny of the Chordata, 
24. Banrour, F.M. A Monograph on the Development of Elasmo- 
branch Fishes. London, 1878. 

25. Baurour, F/M. A Treatise on Comparative Embryology- 
Vol. ii., chap. xii, p. 258. 1881. 

26, Barzson, W. The Ancestry of the Chordata, Quart, Journ. 
Micro. Sci.(2). Vol. xvi. 1886. 

27. Buarp, J. The Old Mouth and the New. A Study in Verte- 
brate Morphology. Anat. Anz, Jabrg. iii, 1888, 

28. Buarp, J. Some Annelidan Affinities in the Ontogeny of the 
Vertebrate Nervous System. Nature. Vol. xxxix. 1889. 

29. Van Benepen, BE. er Junin, Cx. Recherches sur la Morpho- 
logie des Tuniciers. Archiv. Biol. Tom. vi. 1887. 

30. Donry, A. Der Ursprung der Wirbelthiere und das Prineip 
des Functionswechsels. Leipzig, 1885. 

31. Donen, A. Studien zur Urgeschichte des Wirbelthierkérpers. 
Nos, 1 and 2 in Mittheil. Zool. Stat. Neapel, Ba. iii, 1882. 
No. 3, ibid, Bd. iv, 1883, Nos. 4, 5, 6, ibid. Bd, v. 
1884. Nos. 7, 8, 9, 10, tid. Bd. vi, 1886. Nos. 11, 12, 
ibid. Bd. vii. 1886-87. Nos, 13, 14, hid. Bd. viii. 1888. 
No. 15, ibid, Bd. ix. 1889-91. Nos, 16, 17, ddd. Bd. x. 
18v1. 











582 CEPHALOCHORDA. 


82. Envers, E. Nebendarm und Chorda dorsalis. Narhr. Gea. 
Wiss. Gottingen. 1885. 

33. Erste, H. Monographie der Capitelliden. Fauna und Flora 
dex Golfea von Neapel. Monogr. xvi. 1887. 

34. Hagcken, E. Anthropogenie. Aufl. iv. Letpziy, 1891. 

35. Husrecut, A. A. W. The Relation of the Nemertea to the 
Vertebrata. Quert. Journ, Micro. Sri. (2). Vol. xxvii. 
1887. 

35a. v. Kennet, J. Die Ableitung der Vertebratenaugen von den 
Augen der Anneliden. Dorpat, 1891. 

36. KiEINENBERG, N. Die Entstehung des Annelids aus der Larve 
von Lopadorhynchus, ete. Zeitachr. f. wise, Zool. Bd. xliv. 
1886. 

37. Kornver, R. Sur la parenté du Balanoglossus. Zool. Anz. 
Jahrg. ix. 1886. 

38, Kuprrer, C. von. Studien zur vergl. Entwicklungsgeschichte 
des Kopfes der Cranioten. Heft. i. Miinchen Leipziy, 1883. 

39. Mayer, P. Die unpaaren Flossen der Selachier. Mitthet!. Zool. 
Stat. Neapel. Bd. vi. 186. 

40. Mayer, P. Ueber die Entwicklung des Herzens und der grossen 
Gefiisstiimme bei den Selachiern. AMitthe. Zool. Stat. 
Neapel. Ba. vii. 1887. 

41, Morgan, T. H. The Growth and Metamorphosis of Tornaria. 
Journ, Morph. Vol. vy. 1891. 

42. Rovie, L. Les attinités zoologiques des Vertébrés. Rene 
Srieutiriyue. Tom. xlix, 1892. 

43. Rickert, J. Ueber die Entstehung der endothelialen Anlagen 
des Herzens und der ersten Gefi 
Biol, Centralhl, Ba. viii. 1888, 

44. Rickert, J. Ueber die Entstehung der Excretionsorgane bei 
Selachiern. Archiv, Anat. Phys. Anat, Abth. 1888, 

45, ScuimKewirscH, W. Ueber die morpholog. Bedeutung der 
Organsysteme der Enteropneusten. Anat, Anz. Jahrg. v. 
1890. 

46. Semper, ©. Die Stanmverwandschaft der Wirbelthiere und 
Wirbellosen. Arh. Zool, Inst, Wiirzhurg. Bd. ii. 1875. 

47. Spexcen, J. W. Monographie der Enteropneusten. Fauna nnd 
Flora dos Golfes ron Neapel. Monogr. x 1893. 

48. van Wong, J. V Veber die Mesodermseginente des Rumpfes 
und die Entwicklung des Exeretionssystems bei Selachiern. 
Archiv. f. mikro, Anat, Ba. xxxiii, 1888. 





se bei Selachier-Embryonen. 

















LITERATURE. 583 


49. van Wine, J. W. Ueber die Entwicklung des Excretions- 
systems und anderer Organe bei Selachiern. Anat. Anz. 
Jabrg. iii. 1888. 


APPENDIX TO LITERATURE ON CEPHALOCHORDA. 


I. Bennam, -W. B. The Structure of the Pharyngeal Bars of 
Amphioxus. Quart. Journ. Micro. Sei. Vol. xxxv. 1898. 

Il. Ersmenp, J. Zur Ontogenie der Amphioxus lanceolatus. 
Biol, Centralbl. Ba. xiv. 1894, 

IIL. Hawmay, J. A. Zur Kenntniss der Lebenentwickehing bei 
Amphioxus. Anat. Anz. Bd. xiv. 1897-98. 

IV. Kvaatscn, H. Bemerkungen uber die Gastrula des Amphioxus. 
Morph. Jahrb. Ba, xxv. 1897, 

V. Kopscu, G. Ueber Bildung und Bedeutung der canalis 
neurentericus.  Sifzangxber. Gesell, Nating. Berlin, 1897. 

VI. Kravse, W. Die Farbenempfindung des Amphioxus. Zool, 
Anz Jahrg. xx. 1897. 

VII. Macsripg, E. W. The Relationship of Amphioxus and 
Balanoglossus. Pree, Cambridge Phil. Soe. Vol. ix. 1897. 

VII. Macnripr, E. W. The Early Development of Amphioxus. 
Quart. Journ, Miro, Sei. Vol. xl. 1898, 

Villa, MacBrivg, E. W. Further remarks on the development of 
Amphioxus. Quart. Journ. Micro, Sei, Vol. xliii. 1900. 

IX. Minor, C. 8. Cephalic Homologies. A Contribution to the 
Determination of the Ancestry of the Vertebrates. Amer. 
Nat. Vol. xxxi. 1897. 

IXa. Samassa, P. Studien iiber den Einfluss des Dotters auf die 
Gastrulation und die Bildung der primiren Keimbliitter der 
Wirbelthiere N. Amphioxus. Archiv, f. Entiv, Mech. Bd. 
vii, 1898, 

X. Sonorra, J. Beobachtung uber den (Gastrulationsvorgang 
beim Amphioxus. Verh. Gex. Wurzburg (2). Bd. xxxi, 
1897. 

XI. Sonorta, J. Die Befruchtung des Kies von Amphioxus 
lanceolatus. Anat, Anz. Bd. xi, 1895. 

XII. Sticut, O. van DER. Ln Maturation et la fécondation de Pouf 
W@Amphioxus lanceolatus, Bull. Acad. Belg. (3). Tom. xxx, 
1895; and Archir, Biol. Tom, xiv. 1896. 

XIII, Winey, A. Amphioxus and the Ancestry of the Vertebrates. 
London and New York, 1894. 





SUBJECTS INDEX. 


AL 


Acanthodrilus, 79, 
Acanthoteuthidae, 235, 
Acanthoteuthis, 292. 
Acavus, 104, 179, 186, 
191, 192, 196, 197. 
Acera, 100, 160, 173. 
Acipenser, 355, 564. 
Acmaca, 99, 
Actaeon, 100, 145, 162, 
163, 294, 


Avolidae, 159, 161, 164. 
‘Aeolis, 100, 102, 160, 164, 


Ammonoidea, 235, 287, 
288, 


Amphibola, 175, 182. 
Stophiness, 1-21. 
Sy ener S34, 389, 
348-850, 958, 
or 366, 377, 520-524, 
536-579. 
Amusium Dalli, 71, 72. 
Saree 367, 479-483, 


Aaya, 101, 180, 

Anodonta, 23, 24, 50-54, 
58, 62, 66, 72. 

Anomia, 82, 

Aplysia, 100, 102, 103, 
112, 115, 117, 129, 141, 
145, 159-161, 164, 173. 


—_ 29," 70-72, ‘78, 79, 


Arniiae, 48. 
uta, 235-240, 251- 
, 257, 266, 267, 287, 
‘294-296. 


Arion, 101, 184-187. 
Articulamentum, 13. 
Ascidia canina, 337, 
— mentula, 359, 





Ascidiacea, 334, 
a Compositae, 





Atlanta, 100, 102, 154- 
158. 


Auricula, 101, 175, 176. 
Aviculidae, 37, 61, 
‘Aaygobranchia, 99, 


B 
bpd pet 542, 549, 
5T5-5i 
Raeeecaamtoee 101. 
Belemnites, 235, 288-295. 
Belemnoteuthis, 235, 
292, 


Bellerophon, 188, 
Belosepia, 290, 291, 
Botryllidae, 372, | 449, 
456, 457, 460, 463. 
Botryitus, 467, 877, 465, 


Beeauhionancene 182, 
Buccinum, 100, 103, 
Bulimus, 101, 104, 105. 
Bulla, 100. 

Busycon, 103. 
Bythinis, 100, 111, 114, 
118, 121, 129, 136- = 
191-195, 204, 205, 209 
212, 


c. 
Cadulus, 96. 
Oulyptruca, 100, 152. 
Capitellidae,82, 577, 578. 
30, 
Carinaria, 100, 102, 114, 
1 
Cavotinia, 100, 111, 167- 


Cophilochorda, 536-579. 





Chiton, 1-18, 87, 98, 200, 
top eae 215, 308, 315, 319, 


Angee 5, 6 

— olivaceus, 10, 

— Poli, 2, 3, 6, 8, 10. 

Chromodoris, 100, 160, 
164. 


Cirrhoteuthidae, 235, 

Cirrhoteuthis, 265, 295. 

Clausilia, 101, 105, 184, 
187. 

Clavelina, 386-340, 344- 
351, 360-364, 367-377, 
452, 463-469, 

— le; 


liformis, 359. 

ma, 344-351, 

Cleodora, 100, 167. 

Clione, 101, 102, 115, 
118, 167, 171, 172. 

‘Coelocormidae, 519, 

Coletia pedunciilata, 457. 

Cranchiidae, 235, 293. 

Crepidula, 100, 108, 107, 
110, 111, 115-119, 128, 
129, 141, 

— conyexa, 105. 

— fornicata, 105. 

— plana, 


105. 
Cress, ‘100, 102, 167- 


Oyclomyaria, 394, 519. 


586 


Cyclosalpa affinis, 495. 

— dolichosoma - virgula, 
416. 

*— pinnata, 433, 507, 608. 

Cymbulia, 100, 111, 115, 
167, 168-170. 

Cynthia, 335, 357, 381. 


D. 


Daudebardia, 101. 

Dentalium, 88-98, 182, 
192, 200, 216, 318, 319, 
329, 330. 

Diazona violaces, 448. 

Dibranchia, 235. 


Didemnidae, 367, 372, 


pins 457, 459-464, 





518, 








357, 364-367, 872, 457, 
469. 

— magnilarva, 346, 353, 
457. 


= veslifera, 464-466. 

Distomidae, 372, 
457, 463, 473. 

Docoglossa, 99. 

Dolchinia, 473, 479, 482, 
483, 


456, 


Doliolidac. 470-483, 514, 
51s. 
Doliolum. 





355, 367, 
447, 470- 










4 
— banyule enisis, 15, 17-19. 


— festive. 

Doridia: . 
Doridopsis, 330. 

Doris. 100, 102, 159, 164. 








Dosidicus, 
Doto, 100, 1 
sis 30, BB. 


9, 45, 47. 49, 61, 


K 


Eledone, 235- 
Elysia, 100, 1 
Emarginula, 18k. 





SUBJECTS INDEX. 


Enantia spinifera, 325. | 
| Entocolax, 153. | 
Entoconcha, 100, 111. 
— mirabilis, 152. | 
Entovalva, 43, 67, 208. 
: — mirabilis, 23. | 
Ercolania, 111, 159, 164. 
Eulamellibranchia, 22. , 
Eunicidae, 577. ; 
Euthyneura, 146. 

| 





F. 


Fasciolaria, 100, 
104, 128, 209. 

. Filibranchia, 22. 

Fiona, 100, 159, 164. 

' Firoloida, 100, 102, 111, 
134, 153-158, 166, 200. 

— Desmaresti, 114, 158, j 
154. 


108, | 





| Fissurella, 99, 111, 180, 
i 188, 189, 209, 215, 
Fragarium, 336. 
Fragaroides, 450, 451. 
Fulgur, 100, 102, 103, 
107, 116, 120, 128, 180, ; 
149. i 
Fusus, 100, 106, 111, 115, 
117, 121, 141, 149, 150: 
152, 205, 206. 
— antiquus, 103. 1 


G. 

Gasteropteron, 100, 173, 
174. 

Gastrochaena, 43, 6: 
Gastropoda, 1, ¢ 
Glochidium, 
Gnathobdellida 
Gonatus Fabricii, 2 
Gunda. 320. 


Gymmosomata, 101, 171. 
















H. 


97, 99, 
3 2i4. 


Haliotis, 
18s, 194, 

Helicarion, 200. 

Helicinidae, 99, 199. 

Helix, 101, 105. 179, 186, 
200, 204. 

—nemoralis, 201, 

— pomatia, 104 185,184, 

13. 


147, | 





eAvaliani 104, 179, 
186, 191, 192, 196, 197. 


' Hemimyaria, 414-448, 
519. 

i Heteropoda, 100, 102, , 
153. 


Hyalea, 167. 
Hyalocylix, 100, 167. 


J. 
Janthina, 100, 104, 120. 


K. 


Kalymmocytes, 336. 390, 
420-424. 


L. 


Lamellibranchia, 1, 22- 
87, 380. 

Larvacea, 834. 

Lasidium, 57. 

Leachia, 292. 

Lepidosteus, 355. 

Lima, 82. 

Limacidue, 329. 

Limacina, 100, 169. 

Limapontia, 164. 

Limax, 101, 104, 110, 
111, 119, 186, 177, 179, 
184-17, 191. 204, 217. 

Limneea, 101, 111, 114, 
120, 132, 141, 177-183, 
203, 221. 

Lithonephrya, 885, 381. 

Loliginidae, 235. 

Loligo, 236-246, 251, 252- 
277, 287, 296, 298- 





. Lucernaria, 520. 


Lumbricus’ trapezoides, 
574. 


M. 


Marvenina, 99. 
Megascolex, 79. 
Melania, 105. 
Melibe, 330. 
Michrochaeta, 79. 
Mitraria larva, 18. 
Modiolaria, 23, 25, 27, 
30, 33, 47. 










Molgula— macrosipho- 
nica, 382. 
Molgulidae, 381, 445. 


Mollusca, a 
Monotocardia, 99, 147. 
Montacuta, 30, 47, 64. 
Miilleria, 80. 

Murex, 100, 103, 200. 
— brandaris, 198. 





Muscidae, 374. 





ytilui 

87, 89, 45, 47, 68-71. 
— edulis, 22, 24, 68. 
Myzomenia, 1, 15, 19. 





N. 


Nais, 577. 

Nassa, 100. 102, 106, 
118, 116-121, 141, 149, 
152, 163, 200, 208, 315. 

— mutabilis, 108, 112, 


116, 117, 150, 152, 207. | 


Nassopsis, 105. 
Natalins, 200. 

Natica, 149. 
Nautiloidea, 285, 
Nautilus, 287, 268, 286- 








Nemertini, $22 
Neomenia, 1. 
Nephropneusta, 182. 
Neritidae, 99, 199, 
Neritina, 99, 107, 110, 
111, 116, 118, 129, 180, 
138, 141. 
— fluviatilis, 103, 116, 
Nucleobranchia, 100, 
158. 
Nucula, 22, 37, 61, 63, 
72, 75, 82. 
Nuculidae, 48, 61. 
Nudibranchia, 100. 





oO. 


Octacnemus, 334. 
Octopoda, 235. 
Octopus, ' 236-289, 251, 
253, 257, 264-267, 295. 
— membranaceus, 265. 
—yulgaris, “201, 252, 


Oigoncid, 235. 
copleura, 356. 
Ontneieni, 236, 267, 
287, 291-298, 308. 

Onchidium, 66, 101, 104, 
111, 129, 138, 174-176, 
329. 

* Onychoteuthidae, 235. 
Onychoteuthis, 292. 
Opisthobranchia, 

158. 





100, 


Orthoceratidae, 268, 
Ostracum, 288. 


SUBJECTS INDEX. 


Ostrea, 22-38, 45-49, 66, 
TA, 80, 82, 115, 316. 
— edulis, 28, 28, 38, 60. 
— virginiana, 22, 26, 60. 
Oxygyrus, 100, 102, 157. 


P. 


Paludina, 100, 106, 114, 
121, 122, 129, 134-142, 
148, 149, 151, 153, 163, 
191-199, 202, 211-221, 
318. 

— vivipara, 


105, 187, 


139, 212-214, 219. 
99, 101, 


Patella, 4, 91, 





— oyes of, 64-66. 
Pedicellina, 376. 
Pegea bicaudata, 418. 


—seutigera - confoode- | 


rata, 446, 495. 
Peripatus, 80, 317. 
Perophora, 379, 445, 456, ; 

463, 465. 

879, 380. 
346, 357, 360, 





366, 372. 
— mammillata, 335, 348, 
355, 356, 358, 373, 376. 
— scabroides. 377, 378. 
Philine, 100, 145, 164. 
Philonexis, 235, 287. 
Pholas, 45, 70. 
Phragmocone, 288. 
Phragmophora, 235. 
Phyllidia, 330. 
Phyllithoe, 164. 
Physa, 119. 
Piliditan larva, 322. 
Pinna, 82. 

Pinnoctopus, 265. 
Pisidium, 23-26, 29, 30, 
39, 46. 47, 68, 73. 
Planorbix, 101. 107, 109- 

114, 117, 118, 129, 141, 
148, 149, 177-183, 204. 
Pleurobranchea, 100. 
Pleurobranchus, 100, 
102, 164. 
Pleuronectidae, 574. 
Pleurotomaria, 99, 147, 
188. 
Pneumoderma, 101, 167- 
172. 
Polycers, 100, 164. 





587 


, Polyclinidae, 995, 449, 
452-455, 470. 
Prodissoconch, 61. 
Proneomenia, 1, 15, 19. 
aglaopheniae, 325. 
| Pr Prcusbrenehias 99, 102, 
48. 


Protebranchia, 22. 
Pseudolamellibranchia, 


Praropoda, 100, 102, 166, 


Preroeianses 100, 102, 


111, 154-158. 
Pulmonata, 101, 174, 
| 187. 
| Pups, 105, 
Purpura, 100, 118, 115. 
— floridana, 102. 
— lapillus, 108. 


Pyramidollidae, 330. 

Pyrosoma, 334, 356, 367, 

| 377, 381, 389-414, 420, 
482, 451, 455, 459, 479, 

| 484-500. 508, 508, 512- 
520. 


R. 


| Rossia, 28 
Foanctiora: 100, 157. 
| Runcina, 100. 


Ss. 


i Saccoglossa, 168. 
' Sagitta, 54: 
, Salpa, 334, 336, 881, 414- 
| 448, 494-518. 
— affinis, 495. 
, — africana - maxima, 
| 417, 483, 485, 440, 442, 
445, 





i — bicaudata, 
448. 

— costata-Tilesii, 
495. 

, — demovratica - mucro- 
nata, 415, 420-446, 495, 
496, 511, 513. 

— dolichosoma - virgula, 
416, 495. 

— hexagona, 417, 446. 

— pinnata, 416-420, 423, 
433, 435-448, 495, 507. 

— punctate, 417, 420, 
433, 435, 445. 

— runcinata-fusiformis, 
438, 435, 442, 445, 507. 

| —scutigera - confoede- 

rata, 446, 495. 


417-419, 
417, 


588 


Salpa zonaria - cordi- | 


formis, 417, 495. 

Salpidee, 414-448, 451, 
477, 488, 494-512, 516- 
520, 


Scaphites, 294. 

Scaphopoda, 87-98. 

Bearabue, 175, 176. 

Scioberetia, 45. 

Scissurella, 188. 

Sepia, 236-252, 272-277, 
287-298, 296, 298. 

— aculeata, 290. 

— andreanoides, 289. 

— officinalis, 238, 241- 
247, 250, 273-276, 

Sepiidas, 235. 

Sepiola, 236, 244, 257, 

Sepiolidae, 235. 

Sepioteuthis, 238. 

Siphonaria, 119. 

Siphonodentalium, 96. 

Solenoconcha, 1, 88-98, 
829. 


Solenogastres, 1. 
Solenomya, 22. 75, 82. 
Spekia, 105. 
Spirialis, 100, 169. 
Spirula, 235, 268, 286, 
288, 298, 204. 
Spirulidae, 235. 
Spirulirostra, 288, 290. 
Spondylus, 66, 82. 
Stilifer, 100. 
— Linckiae, 152. 
Streptoneura, 99. 
Strombus, 100, 157. 
Styelidae, 372. 
Styliola, 100, 167, 169. 
Stylomatophora, 101, 
184. 





SUBJECTS INDEX. 


Succinea, 101, 192, 180, 
187. 


Synapta, 43. 
— digitata, 152. 


T. 


Taenioglossa, 158. 

Taonius, 292. 

Tectibranchia, 100. 

Tegmentum, 13. 

Teredo, 23-39, 42, 44, 66- 
78, 80, 208, 819. 

Tergipes, 100, 102. 

— Edwardsii, 164, 165. 

— lacinulatus, 164. 

Testacella, 101. 

Testacellidae, 182. 

Tethys, 111, 119, 830. 

Tetrabranchia, 235. 

Teuthidse, 236. 

Teuthis, 267. 

Thalia democratica-mu- 
cronata, 415, 420-446, 
495, 511, 518. 

Thaliacea, 334. 

Thecosomata, 100. 

Thyca, 100. 

— entoconcha, 152. 

Tiedemannia, 100, 167- 
170. 

Tornatella, 163. 

Tremoctopus, 235, 287. 

Triclada, 320. 

Trididemnum, 460-462. 

Trigonia, 71. 

Tritonia, 100. 


 Trochophore, 5-7, 10, 18, 





30-43, 91, 125-128, 142, 
161, 167, 177, 326. 


; Urosalpinx, 





Trochus, 99, 198, 200, 


magus, 198. 
Trophezocid, 289. 
Tunicata, 384-534. 
Turbellaria, 108, 320. 
Turbinidae, 199. 

Turbo, 99, 215. 
— creniferus, 198. 
Typhobia, 105. 
Uw. 
Umbrella, 100, 107, 110, 
111, 118-120, 129, 159. 
Unio, 22-29, 38, 119. 
Unionidae, 25-29, 30, 39, 
49-59, 66-71, 73-76. 


108, 113, 
116, 117. 


v. 


Vaginulidae, 175, 176. 
Vaginulus, 101, 175. 
Vaivata, 99, 100. 

Veliger ‘larva, 130-134, 
162, 169, 177. 

Venus, 22. 

Vermetus, 100, 105, 111, 
115-122, 130-132, 148, 
180, 192, 197, 200, 217. 

Vitrina, 101, 105. 


¥; 
Yoldia, 19, 22, 63, 72. 
Z. 


Zygobranchia, 99. 








AUTHORS INDEX. 


A. 


Apams, A. 
Cephalopoda, 294. 
Apter, J. and Han- 
ook, A. 
Gastropoda, 158, 164, 
Awsprews, E. A. 
Lamellibranchia, 64. 


APPELOFF, 
Oapaaiipetes 291. 


B. 


Bakr, K, E. v. 
Tunicata, 524. 
Baurour, F. M. 
fay eS 577, 


Latnelibrenshis, 50, 
Tunicata, 955, 514, 
522. 
Barnors, J. 
Tunicata, 433, 
445, 472-474, 480. 
Basnots, TH, 
Lamellibranchia, 22, 
24, 66. 
Barrson, W. 
Cephalochorda, 649, 
578, 579. 
Brann, J, 
Cephalochorda, 576, 
577. 
Brppanp, F. 
Oligochaeta, 79. 
Brune, Ta. 
Gastropoda, 213. 
Bexepes, Ep. vas, and 
Junin, On. 
Cephalochorda, 576. 
Tunicata, 338-388, 432, 
447, 450, 451, 456, 
465-469, 482, 520- 
$22, 





Beno, R. 


Gast 176. 





Buror, R. 8. 
Lamellibranchia, 74. 

Bernarp, F, 
Tasnallibranchis, 45. 


Lamellibranchia, 30. 

Gastropoda, 105-109, 
111, 112, 115-118, 
134, 141, 149, 158- 
161, 


Bromnron, J. 
Amphineura, 10-12. 
J.B. y. 


ropoda, 114, 134, 
138, 141, 144, 145, 


153, 202, 217. 
oarpr he a 64- 
Tunicata, 429, 430, 





Cephalopoda, 241, 248, 
Tro, sea, ba6, "208! 


309. roe 

Gastropoda, 103, 5 
112, 115-117, 120, 
122, 129, 141, 149- 
152, 195, 200, 205- 
207, 


Booran, L. 
Gastropoda, 130, 189. 
Bouvirn, B. Le 
Gastro) 225. 
Bovest, 
Oepbaloaerdiy 535, 
556, 566, 568-576. 
Braon, M. 


Gastropoda, 153, 213, 
Lamellibranchia, 60, 
56, 58-60, 83, 
Gophat poda, 237, 
Cephalo; 
Gastropi 220-223, 


Cephalopoda, 252-254. 

Gastropoda, 103, 118, 
116, 128, 

Lamellibranchia, 7, 
98, 1. 


Tunicata, 420, 423, 








Cephalopoda, 294, 
CLapanior, B. 


» 178. 
Jone 415, 612, 
Coreen 


cornea 108, 119. 


D. 


Dart, W. H. 
Lamellibranchia, TL, 


590 


Damas, D. 
Tunicata, 368. 
Davivorr, M. v. 


54. 
Tunicata, 386, 388, | Faatssz, P. 


| Fuaita, T. 


350-354, 520. 
Detua VauLE, A. 
Tunicate, 448, 457-463, 
Diett, M. J. 
Cephalopoda, 304. | 
Dopverueiy, L. | 
Cephelopoda, 318. 
Dourn, A. | 
Cephalochorda, 573, | 


575. 
Tunicata, 522, 528. | 
Drew, G. A. 
Gastropoda, 232. 
Lamellibranchia, 
63. 


19, + 


| 
E. 
EHLERS, 
Cephelochorda, 577. 
Exnrenpauy, E. 
Lamellibranchia, 61. 
Eists, H. 
Cephalochorda, 577. 
Gastropoda, 220, 221. 
E1smunp, J. 
Cephalochorda, 583. 
Ervaneer, R. v. 
Gastropoda, 114, 118- 
122, 129, 184-136, 
139, 141, 153, 179, 
191-199, 204, 209- 
220. 
Escuuicut, D. F. 
Tunicata, 417, 494. 


| 
: 





tropuda, 101, 
cen, H. 
Gastropoda, 201, 
FLmIscHMANN, A. 
Lamellibranchia, 81. 
Fresaixc, W. 
Tamellibranchia, 50, 


199, 














Frop d 

Tunicata, 532. 

Fou. H. 

Gastropoda, 102, 111, 
114, 128, 153, 154, 
166-187, 191, 192, 
197, 200, 202 

Tunicata, 335-338, 365, 
474. 


| Garstana, W. 


a ee ee poo 


AUTHORS INDEX. 


Foret, F. A. 
Lamellibranchis, 50, 


Gastropoda, 199. 


Gastropoda, 283. 
Forranton, J. H. 
Lamellibranchia, 22, 
24, 49. 


G. 


Ganis, M. 
Gastropoda, 178, 217. 
Insecta, 286. 
Lamellibranchia, 73, 

74. 
Tunicata, 379, 458, 463, 
513. 


Tunicata, 377. 

GeGenaaur, C. 
Amphineura, 12. 
Cephalochorda, 578, 

579. 

Gastropoda, 128, 158, 
155-157, | 167-174, 
179, 184-187. 

sarees 459, 476, 


Sian a 
Mollusca, 382. 
Tunicata, 449, 452, 458, 








463. 
Garp, A.,und CaULERy, 
M 
Tunicata, 532. 
Girop, P. 
Cephalopoda, 285, 286, 
310, 
Goren 
Tunic 
Gorter, A. 






27, 


Goopnicn, 
Molluse 
Graper, V. 
Thsecta, 
Gare, L1. von. 
Mollusca, 3: 
GRENACHER, H, 
Cephalopoda, 















Grosnen, C. 
Cephalopoda, 304-307. 
Gastropoda, 157, 173. 
Lamellibranchia, 22, , 

78, 80. i 


Tunicate, 362, 388, 
470-478, 512, 519. 


H. 


Happon, A. C. 

Gastropoda, 120, 159, 
164, 193. 

Haxcket, E. 
Cephalochorda, 578. 
Tunicata, 523. 

Hauer, Beta. 
Amphineura, 15. 

Hamman, J. 
Cephalochorda, 588. 

Hancock, A. See ADLER 

and Haxcock. 

Hansen, G. A. 
Amphineura, 20. 

Harscuex, B. 
Amphineura, 11. 
Cephalochorda,  535- 

577. 

Lamellibranchia, 23, 
26-39, 63, 67. 

Tunicata, 350, 522. 

Heer, K. 

Tunicata, 336, 416, 
420, 423, 426, 433, 
436, 441, 445. 

HEncuMay, ANNIE P. 
Gastropoda, 191, 195. 

Herpman, W. 





Tunicata, , 457, 
460, 519, 520. 
HERTWIG, O. 
540- 


Cephalochorda, 
543. 





33 

Herrwic, R. 
Cephalochorda, 541. 
Gastropoda, 173. 
Tunicata, 3 

Hermoss, R. 
Gastropoda, 








118-120, 





Gastropoda, 198. 
Hyont, J. 

Tunicata, 361, 449, 
458, 463-466, 516, 
Horr, and Boxne- 

vig, Fr. 
Tunicata, 532. 
Hotes, 3. J. 
Gastropoda, 184. 
Horst, R. 
Lamellibranchia, 
30, 47. 








23- 


Huprecar, A. A. W. 
Amphineura, 15, 16. 

Hoxzey, T. H. | 
Cephalochorda bit 





Tunicata, $89, 413, 
484, 494, 499, 519. 


J. 


Jackson, R. T. 
Lamellibranchia, 42, 
47-49, 60, 61, 68. ‘ 

Jaconson, L. 
Lamellibranchia, 56. 

JARKEL, O. 
Cephalopoda, 292. 

data, G. 
Cephalopoda, 305. 

Juxnina. H. 
‘Amphineure, 1, 56. | 
Cephalopoda, 304, 368. 
Gastropoda, 147, 175, ' 

182, 166, 218. I 
Lamellibranchia, 78, 
82, 83. 





Mollusca, 332. 
Jouixt, L. 

Tunicata, 484, 490. 
Jounin, L. 

Cephalopoda, 237, 283, 

306, 310. 

Jourparn, S. 

Gast yoda, 179, 186, | 





Tonkate 460, 463. ' 
Joreux-Larrurm, J. 
Gastropoda, 133, 165, \ 
175. i 
Juux, Ci. See Bane: | 
DEN and JUIN. 
Juuin, CH. 
Tunicata, 860, 469. 
K. 
Kerenstetn, W. 
Gastropoda, 101, 158. 
Tunicata, 382. 
Kererstery, W., and 
Eu.ens, EB. 1 
_ Tunicata, 387, 413. 
J. Ve 
lochorda, 








576, 





Kerr, J. Grawan. 
Cephalopoda, 305. 

Krener, L. 

_ Gastropoda, 157. 











Tunicata, 526. 


AUTHORS INDEX. 


Kuaatscu, H. 
Cephalochorda, 535. 
KLEINENBERG, N. 
Cephalochorda, 
577. 
Cephalopoda, 307. 
Gastropoda, 122, 196, 
Kuorz, J. 
Gastropoda, 220-228, 
Kuirowrtscn, N. 
Gastropoda, 115, 118. 
Korurer, R. 
Cophalochorda, 579. 
KOLLIKER, A. 
Cephalochorda, 564. 
Cephalopoda, 241, 245, 
252, 273-276, 204- 
297. 
Tunicata, 458. 
Kororp, C. A. 
Gastropoda, 184. 
Kou, C. 
Cephalochorda, 564. 
Koken, E. 
Gastropoda, 188. 
Konen, J., and Dante.s- 
sen, D.C. 
Gastropoda, 227. 
Konorserr, A. 
Tunicate, 336, 420, 
423-427, 432, 433, 
436, 441, 442, 445- 
448, 479, 482, 483. 
Koxscuenr, K. 
Cephalopoda, 279, 801. 


576, 











Lamellibranchia, 28, 
30, 47. . 
1. 

535. 

542, 547, 549, . 556, 





Cephalopoda, 297. 
Gastropoda, 200. 
Mollnsea, 825. 
Solenoconcha, 88-98, 





376, 389, “391, 395- 
403, 408, 429, 443, 


448-457, 463 - 469, 
484, 494, 498, 499, 
516-520. 

Kowanevsxy, 
Bannows, J. 

Tunicate, 529. 

Kowanevsky, A., 

Marton, A. F. 
Amphineura, 20. 


A, and’ 


and | 





591 


Kroun, A. 
Gastropoda, 128, 188, 
155-158, 167-173. ° 
Tunicata, 376, 382, 
417, 458, 513. 


Koprres, C. v. 
Cephalochorda, 541, 
577. 
Tunicata, 335 - 388, 


357, 364, 372, 874, 
381, 382, 521. 


P L. 


Lacaze-Dutuiers, 
DE. 
Gastropoda, 105, 131, 
199. 


H. 


Lamellibranchia, 47, 


Solenoconcha, 88, 94- 
§ 

Tunicata, 381. 

Lacaye-Durarmas, H, 
pn, and Pavvor, G. 
Gastropoda, 164. 
Lanier, F. 

Tunicata, 360, 361, 
367, 372, 417, 457, 
464. 

Lana, A. 
Gastropoda, 144. at: 
‘Mol sca, 3 3: 







Gastropoda, 142, 159, 
160. 
Tunicata, 360, 521. 
Lankester, E. Ray. 
Cephalochorda, 585, 
556-562. 
Cephalopoda, 249, 252, 
}, 285, 286, 298, 
296, 301. 
Gastropoda, 112, 114, 
128, 191-1834, 141, 
161, 177, 180, 183, 
193, 215. 
Lamellibranchia, 25- 
30, 40, 68 74 
Mollusca, 820, 332. 
Lankester, K. Ray, and 
WILury, A. 
Cephalochorda, 535, 
550-553, 556-561. 
Latter, O. H. 
Lamellibranchia, 56. 
Lea, I. 
Lamellibranchia, 56. 
Ler, A 
Tunicata, 388. 





Rarakn, H. 
‘Lamellibranchia, 56, 

Rawitz, B, 
Lamellibranchia, 64. 





Mollusca, 388. 


Cephalochorda, 568, 
Rypver, J. 
Gastro 230. 
Lamellibranchia, 48, 
60. 
5. 
Sapatinr, Ap. 
Tunicata, 338. 
Sr, Hiarre, GEorrroy. 
Cephalochorda, 575. 
Savensky, W. 
Cephalochorda, 587. 
Gastropoda, 115, 122, 
192, 197, 200, 217. 
Tunicata, 835, 338, 


Saaassa, P,’ 


141, 
215, 


Sanasin, P. and F, 
Gastropoda, 104, 
152, 179, 186, 

197. 


Sars, M, 
Gastropoda, 158. 
Tunicata, 458, 

Scuanreerw, M, 
Gastropoda, 217, 





122, 
191- | 


Amphineura, 1. 
Seecicer, Osw. 
. 339, 


405, 
= 


5T5- 
caatropds, 175, 176, 
anteate, 337, 338, 
489. 


Snarp, B. 
Lamellibranchia, 86. 

Suxxpon, L. 
quia 527. 


Smoove, 
‘Amphineura, 1b, 
Gestecpoti, 147, 220, 


StxcErroos, C. P. 
Lamellibranchia, 45, 
Suurres, 0, Pa, 
ellibranchia, 62, 
QQ 





Toparo, 

Tunicata, 416-421, 426, 
432-448, 494-498, 
515, 516. 

Ténsices, 0. 
aera 185, 187. 


Tunicata, a. 
‘TRINCHESE, 
ecnenee® 158-168. 
Tuiusena, T. 
Lamellibranchia, 61, 
Uv. 
Ursasiy, B. 
‘Tunicata, 382-388, 385 


471-478, 512, 514. 
Ussow, M. 


Ge) 240, 
Br Beads 302 
286, 801, 303-306. 

Vv. 
Ve RS 


“ti Fs 


594 


ViautER, C. 
Gastropoda, 159. 

VoErLtTzKow, A. 
Lamellibranchia, 28, 


Voar, C. 
Gastropoda, 158, 174. 
Tunicata, 494. 


Cephalopoda, 289. 


WwW. 


‘Wakneck, A. 
Gastropoda, 106. 

Watasg, 8. 
Cephalopoda, 241-246, 


Wuues, F. E. 
Cephalochorda, 581. 


AUTHORS INDEX. 


| Wettner, W. Wirson, Jour. 


| “Lamellibranchia, 30. !  Lamellibranchia, 2, 
Wirrzrsski, A. 24, 39, 47. 
| Gastropoda, 119, 128, ° Wrrtacziz, Em. 
184. Insecta, 286. 
Wisue, I. W. van. Wotrsox, W. 


Cephalochorda, 535, Gastropoda, 114, 120. 


| 860, 571, 574. 141, 176, 178, 183, 
| Winury, A. 198, 202, 908. 
Cephalochorda, 585, - 
549, 558-561, 574. a 
575. : on 

Cephalopoda, 287. “y ), 

Tunicata, 350, $59, PCephalipe 26. 
361, 365-969, 377. | pod, 
519-521. See also | ZIEGLER, KE. 

q igreo. Lamellibranchia, 23- 
Lankesten = and) “59°80 Gg gs GOSR 
tag anna 66, 73-77, 81-83. 
; bi ter nar | Zrrren, K. 
‘ephalocho 536, ' 
jerry Cephalopoda, 291. 


Gastropoda, 188. 


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