the alimentary canal of style-bearing prosobranchs: 5. on the structure of the alimentary canal of...

THE ALIMENTARY CANAL OF STYLE-BEARING PROSOBRANCHS . 75

5 . On the Structure of the Alimentary Canal of Style-bearing Prosobranchs . By ALASTAIR GRAHAM. M.A., B.Sc., Department of Zoology. Birkbeck College. University of London * .

[Received October 20. 1938 : Read April 4. 103% J

(Text-figures 1-10.)

Iiitrotluction ................................................. Arcehseogastropoda ..........................................

Diodotoapertura ....................................... Neritecee ...............................................

Septmia .................................. T h e d o ~ ~ u v i u . t i l i s ....................................

~ c h i ~ n i o g l o e ss .......................................... LoOigepMgrandis ...................................... AnvpuUanicegigoa ....................................... Pikrovata ..............................................

Rieeoecee ............................................... Adwrbia &rinatw ................................... Riaeoaparvo ........................................... Hydrobiowntroaa ...................................... Hydrobia ienkdnad ...................................... Other Hydrobiidre ...................................... Bithyniotentacuhta .....................................

Porndias ekqans ....................................... Cerithi~ee ...............................................

Tu&k wmmunis . . ............................... Aporr?uaia ............................................. Vermetua .............................................. Tierid ................................................. Potamides (Potamides) ininimwr .......................... Potamidea(Cerithidea)dewUata ........................... Telescopizlm teleacopkum ..................................

Calyptr~ecea ............................................. Crepidulafornicata ..................................... Cdyptrzu chin+s ................................... '. . Capulua ungalrcua .......................................

Stromb~ee .............................................. RoateUoria ............................................. Pterocera .............................................. Strombua ..............................................

Opisthobranchia ........................................... Pteropode ...............................................

Discussion ................................................... References to Literature ......................................

Zeugobrsnchia ........................

&fesogeetropode ...........................................

Hydrobia (Periqio) ulve ...............................

........................................

........................................

~ U I t U R 8 ~ ...................................................

CONTENTS . Page 76 77 77 7 7 n i n i

n3 n3 83 n4 84

84

81

84

85 Ur, 85 nr, 87 87 90 90 00 !)3 93 95 !).5 !J5 !)7 !J7 !J7 !)7 97

101 104 104 104 104 104. 104 104 105 100 110

.. . .-__

* Communicated by Prof . H . G . JACKSON, DSc., F.Z.S.

76 MR. AUBYTAIR GRAHAM ON THE ALIMENTARY

INTRODUCTION The glandular areas associated with the alimentary tract of prosobmnch

gastropods are three in number : (1) salivary glands opening to the buccal ctivity ; (2) digestive diverticula leading from the stomach ; (3) lateral oesophageal pouches and homologous structures. While the two former are of almost universal occurrence the last may not be represented a t all. Recent work has in several instances elucidated the rBle of the salivary glands and the digestive gland, but the significance of the oesophageal pouches is in most cases still obscure though it is generally conceded that they produce some substance, either enzymatic or of the nature of a kinase, necessary for digestion. The present paper deals with the oesophageal region and stomach of gastropods possessing a crystalline style : lists of these may be found in Robson (1922b), Mackintosh (1925), and in Yonge (1932), and most of the more easily obtainable species recorded there have been examined alive. Through the great kindness of Mr. G. I. Crawford, of the British Museum (Natural History), I have been allowed to dissect preserved specimens of many exotic snails, an opportunity for which I am extremely grateful ; where even this was impossible descriptions of anatomy have been drawn from the original accounts. I am also indebted to Miss F. M. Haworth, Ph.D., and to Capt. C. Diver for a supply of living specimens of Pomatias and for information about, their habits ; to A. E. Ellis, Esq., and R. Winckworth, Esq., for supplies of Thmdoxus. Lastly, I would thank Prof. H. G. Jackson for his interest in the work. The work here recorded was done mainly in the Department of Zoology, Birkbeck College, University of London, but Diodora and Riseoa were dissected during a stay at the Marine Biological Station, Port Erin. In the case of British marine species the names used are those given by Winckworth (1932), in other cases Thiele (1931) has been followed. In several cases better known synonyms are given in bracketu.

Most of the animals that were available were dissected alive ; for histological details specimens were fixed in Ciaccio’s fluid or in that of Helly, and sections, 8 p thick, were stained in iron haematoxylin with toluidin blue as counterstain for mucus, or with the Champy Kull process.

In this paper I take the anterior limit of the oesophagus to be the point at which the radula sac separates from the gut proper, and its posterior limit the point where i t enters the stomach ; the former limit coincides with the junction between the ectoderm and the endoderm. In the lower prosobranchs in which there is no style the oesophagus, apart from the extreme anterior end, which resembles the buccal cavity histologically, and which I shall speak of aa the anterior oesophagus, consists of a dorsal food-channel bounded by two longitudinal folds, lined by a ciliated epithelium containing mucous cells, which constitutes a path leading to the stomach, and of two lateral glandular dilatations the surfaces of which are increased by the walls being raised either into numerous transverse folds as in Patella or villiform papillae as in Gibhh. This portion of the oesophagus I shall refer to as the mid-oesophagus. The right and left glandular areas are usually separated from one another by a ciliated median ventral fold. As I showed in the case of Patella (Graham, 1932) the ciliary currents on the walls of the gut carry the secretion of the lateral pouohes into the dorsal food-channel and bear the mixed food and secretion to the stomach. This portion of the alimentary tract is involved in the torsion of the visceral mass, with the result that the food-channel leaves the buccal cavity on the dorsal side but twists round the left side of the oesophagus to occupy a topographically ventral position ; simultaneously the ventral fold curves up the right side to a mid-dorsal position, the pouches always lying

CANAL OF STYLE-BEARING PROSOBRANCHS. 77

between the two. The exact extent of the twisted part varies from one gaatro- pod to another, but, as Amaudrut (1898) showed, its anterior limit is always clearly marked by the supra-intestinal branch of the visceral loop and its posterior limit by the cephalic aorta running forwards. Behind the mid- oesophagus lies a third motion, here referred to as the posterior mophagus, in which the lumen is always small and the walls are thrown into longitudinal folds covered with a ciliated epithelium containing mucous cells.

In higher prosobranchs, especially in such as are carnivorous, the right and left glandular areas coalesce and in some case8 may become separated from the oesophagus to form the gland of Leiblein, communicating with the topographically dorsal side of the esophagus by means of a short duct ; in herbivorous animah an arrangement similar to that found in the lower prosobranchs may still prevail.

In the courae of this work I have taken the essential characteristic of the crystalline style to be the presence of a diastatic enzyme. Some caution must be exercised in this respect aa there are one or two prosobranchs which possess a mucous rod lying in a sac attached to the distal end of the stomach the histology of which resembles that of the style-sac, the superficial appearance of the whole agreeing with that of the style and sac in several respects, but which differs from a true style in that i t contains no enzyme. This may represent a stage in the evolution of the crystalline style, but so far as the glandular equipment of the prosobranch is concerned i t cannot be regarded as a true style. Similar care must be taken over the term gastric shield, which will be limited in this paper to a cuticular structure found on the wall of the stomach against which bears a crystalline style aa defined above.

The general results of my work indicate that in prosobranchs which possess a crystalline style (with the apparent exception of Adeorbis (=Tornua) sub- curinatus, Woodward (1899)) the original type of oesophageal structure has been altered in one of two ways. On the one hand, i t may be completely suppressed ; on the other, the glandular epithelium of the lateral pouches may be replaced either by a ciliated one in which mucous and similar lubricating glands occur, or by cuticularized cells. In this case the original dilatation of the walls may still remain, forming a more or less crop-like structure. In no case that I have found is the typical prosobranch condition retained.

A systematic account of the various molluscs examined follows.

ARCHBOGASTROPODA (=DOCOGLOSSA+ RHIPIDOGLOSSA).

Zeugobranehia. DIODORA (= F’ISSURELLA) .

DIODORA APERTURA (Montagu) : examined alive. According to Haller (1888) the stomach of Diodora contains at certain

times a crystalline style which lies freely in the region from which the intestine arises. Now, as Amaudrut (1898) has shown, this mollusc posse~lses a series of msophageal pouches similar to those found in Callioetoma and Chbbula (Randles, 1905) and Haliotis (Crofts, 1929) : it thus becomes of considerable interest to ascertain whether Haller’s statement is accurate or is a misinterpretation of some other structure found in that position. I have concluded, from an examination of living specimens of D. apertura, that no style is to be found in the stomach,

78 M R . ALASTAIB GRAHAM ON THE ALIMENTARY

Text-figure 1.

d -

s. g

d. Diodora apertura.

Stomach opened from the dorsal side. Arrows indicate the direction of the ciliary currents and the thick broken line outlines the area covered with cuticle. d., ducts of the digestive gland ; f., typhlosolar fold separating the upper and lower parts of the intestine ; g., groove ; h., depression a t the base of the typhlosole ; i., intestine ; o., oesophagus ; o.a., opening of the esophagus ; r., ridged area extending on to the floor of the intestine ; s.g., spiral groove and ridge. x 15.


The stomach is a rather pear-shaped structure (text-fig. 1) lying obliquely towards the posterior end of the visceral mass, with the narrower end pointing forwards along the animal’s left side. The oesophagus (0 . ) enters it ventrally near the posterior end to the right (o.a.), whilst the intestine passes ventrally from the anterior end of the left portion. On opening i t two wide openings (d.), those of the ducts of the digestive gland, may be seen one on either side of the oesophageal aperture, a series of parallel ridges (r.) running forwards from them to the floor of the narrower anterior portion. This is split into upper and lower parts by a prominent fold (f.) arising from the left side and running along its whole length, and the ridges from the diverticular ducts run on to the floor of the lower half. On the dorsal surface of the fold, parallel to and near the free edge, runs a shallow groove (9.) containing quantities of mucus ; posteriorly this runs to a cup-shaped depression (h.) in a ridge-like extension of the fold into the posterior chamber of the stomach. This chamber contains, in the neighbourhood of the oesophageal opening, a short spiral groove (8.g.) and ridge, perhaps the homologue of the spiral czecum of other rhipidoglossa. The bulk of the walls of the posterior part, especially on the dorsal right and the anterior half of the ventral sides, is covered with a thick cuticle ; this area hau dightly raised edges. The remainder of the walls is ciliated, the direction of the currents being shown in the text-figure. In the anterior section the cilia are weak and their beat difficult to make out.

living DiaE0l.a be opened a cylindrical structure. about 1 cm. long, will be found lying in the upper half of the anterior chamber : it is semi-opaque, and of a yellowish white colour ; the outer layers white, the central ones pale brown. If i t be picked out i t pulls with it strands of whitish material from the groove on the fold (9.) and a hemispherical mass of brown matter from the posterior chamber, whilst its distal end looks as if it had been broken short, the central axis being exposed : it thus presents, so far as macro- scopic appearance goes, some of the characters of a crystalline style. When examined under the microscope it is found that the outer, whiter layers consist of concentric strands of granular mucous material, whilst the central, yellowish layers are composed of large numbers of particlea of detritus-some sand- grains and fragments of shell, occasional diatoms and pieces of plant remains, and vast numbers of sponge-spicules, most belonging to species of Halichondria. The brownish maas which clings to the posterior end of this structure has the same composition as the central layers, consisting mainly of half-digested fragments of sponge and quantities of spicules. It appears, indeed, that far from being a herbivorous animal, aa recorded by Yonge (1930, 1932), Diodora eats sponges, and although, as Millott (1937) has suggested, extracellular enzymes need not necessarily accompany this habit, it, is impossible that a style could develop under such circumstances. An observation given by Forbes and Hanley (1853) supports this idea : they record that the colour of Diodora apertura varies from “ creamy white, through various shades of yellow to a rich orange approaching scarlet, in the latter case only in such specimens as are taken from the surface of scallops incrusted with crimson sponge,” suggesting a dependence of the colour of the mollusc on that of the food it eats. Allen and Todd (1900), too, record Fieeureh reticulatu as ‘ I fairly common . . . feeding on Ascidians, Sponges, etc.” in their account of the fauna of the Salcombe estuary.

That the rod present in the stomach is not a style is also borne out by the arrangement of the ciliary currents on the walls of the stomach, which direct prtrticles into the lower half of the anterior chamber and drive the rod itself

If the stomach of

80 m. ALASTAIR a u m ON THE ALIMENTARY

Text-figure 2.

0. a.

Enuarginula r&deulata.

Stomach opened from the dorsal side. Arrows indicate the direction of the ciliary currents c.T., cuticular and the thick broken line outlines the area covered with cuticle.

ridge ; other lettera 88 in text-fig. 1. X 20.

CANAL O F STYLE-BEARING PROSOBRANCHS. 81

into the intestine ; ' by the absence of a diastatic enzyme ; and by the presence of this structure not only in the stomach but also through the greater part of the intestine, from which the gastric portion is broken on removal, as was noted above. In short, the structure is simply the first step in the formation of a faecal rod, although it is possible that from some such rod as this the style was originally elaborated.

That this is the correct interpretation of the " style " of Diodora is still further suggested by the conditions encountered in Emarginula reticukta, a mollusc belonging to the same family as Diodora, but one which has never been accused of possessing a style. As text-fig. 2 shows, the general structure of the stomach and the intestine and the arrangement of the ciliary streams on its surface are extremely reminiscent of what is found in Diodora. The posterior chamber contains an even thicker cuticle, raised a t one point into what might easily be taken for a gastric shield (c.T.), and the same whitish rod can be picked out of the elongated anterior chamber ; in this case, however, i t is obviously at first glimpse a mucous food-string which could not be mistaken for a style.

Diodora appears to be a carnivore in which extracellular digestion probably takes place, effected by enzymes secreted from the oesophageal pouches and the digestive gland, and in which the remains of a meal, consisting mainly of sponge-spicules, are compacted together into a fmal rod. Part of this seems to be accomplished by ciliary rotation of the plentiful secretion of mucus, pertly by muscular contractions of the wall of the stomach, for which the cuticular coat would be helpful.

Neritacres. SEPTARIA .

THEODOXTJS (=NERITINA).

THEODOXUS FLUVIATILIS (L.) : examined alive. The morphology of the alimentary canal of T. Jluviatilis has been fully

described by Lenssen (1899), whilst the oesophageal pouches of Nerita p h a have been described by Amaudrut (1898). In view of the remark of Bourne (1908) that Lenssen's description of Neritina (= Theodom) Jluviatilis would apply to all the Neritidae SO far as the gut is concerned, it would appear that if Thm~bms has a style SO should all the other members of the family. Seshaiya (1934) has, indeed, described a style-sac in Septaria drawidica bashad. Lenssen, however, makes no mention of astyle, and seems to have had no real idea of the cuticular secretion on the wall of the stomach acting as a gastric shield : the suggestion that style and shield were found in this mollusc appears to have been made in the first place by Yonge (1932).

Both Amaudrut and Bourne agree that the esophageal pouches are reduced to two sac-like structures lying one on either side of the oesophagus at. the posterior end of the buccal cavity in front of the region in which torsion occurs, whereas Lenssen interpret,s these as the homologue of the salivary glands of other prosobranchs and describes two ciliated and glandular grooves on the floor of the oesophagus as the vestiges of the esophageal pouches. If, as Yonge claims, T'heodozus has a style, it would stand almost alone among gastropods in possessing oesophageal pouches and style simultaneously, whichever homology turned out to be correct.

paw. ZOOL. SOC., SER. B.-l939, Q

82 MR. ALASTAIR GRAHAM ON THE ALIMENTARY

h.

Theodoxua jeuviatilia. Stomach opened from the ventral eide.

x about 20,

Arrows indicate the direction of the ciliary currents Lettering as in and the thick broken line outlines the area covered with cuticle.

text-figs. 1 and 2.

C+NAL OF STYLE-BEARING PROSOBRANCHS. 83

The difficulty of proving the absence of a crystalline style being notorious, 1 dissected five living Tluxwbw under a binocular microscope within a minute or two of their being collected from the River Cherwell, near Oxford : in no c&88 ww a style present. The part of the stomach which might be taken for a style-sac waa in each caae filled with a food-string composed of mucus, minute grains of sand and pieces of bark, full and empty diatom and desmid cases, and numerous brown spherules similar to others encountered in the cells of the digestive gland. This food-st,ring-waa continuous on the on0 hand with a less compact m w of similar material lodged in the hemispherical posterior chamber of the stomach, and on the other with the rods of faecal matter lying in the intestine. As in Diodora, the “style” of Thmdoxw appears to be a preliminary stage in the formation of the faeces.

T w having no style, the question of the homology of the pouches a t the anterior end of the alimentary canal is less pressing, but it seems from the lamellatad internal structure of each pouch and from the arrangement of the ciliary currents that Amaudrut and Bourne must be right and that they correspond to the oesophageal pouches of the other prosobranchs. No explanation can a t present be offered for the separation between the glandular and the conducting portions of the oesophagus which has taken place in this and kindred molluscs.

The structure of the stomach and the arrangement of the ciliary currents on its walls are shown in text-fig. 3. In general these seem to be similar to those which have been found in the other molluscs examined, the oesophagus opening (0.a.) on the left side t e a ciliated tract which leads along a groove (9.) to the posterior end. The apertures of the ducts of the digestive gland (d.) are wide- mouthed and flank the opening of the esophagus : from their anterior borders ciliary currents pass along grooves to a ridged area (r.) on .the floor of the intestine. Folds bound the groove leading back from the oesophageal aperture, and the right wall pwteriorly bears a cuticle elevated into a‘rolled crest. The upper part of the intestine is separated from the lower by two typhlosoles, on one of which currents run towards the anus and into the lower half of the intestine, on the other anally and into a deep sac (h.) a t the base of the typhlosole where it borders on the stomach.

The mode of working of the stomach has not been determined, but further work on the structure and function of the alimentary canal of TheaEorms is in progress in this department.

The organization of Septuria almost certainly corresponds with that of TheodoXUS.

MESOGASTROPODA ( =T.ZNIOGLOSSA) . Ar@hitaenioglossa.

LAVIGEFUA ( =NASSOPSIS).

LAVICIERIA GRANDIS Bourguignat : examined preserved. The esophagus dilates a little in the region posterior to the nerve-ring ;

apart from this it is a straight tube of narrow dimensions. Its inner surface is smooth save for a few longitudinal folds. Moore (1899 b), describing another species of this genus (as Nmsop.& nassca), stated tha.t the oesophagus was long, parrow, and simple.

0 2

84 MR. ALASTAIR GRAHAM ON THE ALIMENT9Y

AMPULLARIUS ( =AMPULLARIA in parte). AMPULLARIUS GIGAS Spix : examined alive. I have been unable to find a style in the stomach of this snail. This is in

agreement with the original observations of Bouvier (1888), who described a caecal chamber at the intestinal end of the stomach but did not mention any style. It appears to have been Robson (1922 6) who first suggested that this structure might be a style-sac, and, from his words, i t seems that he was basing the suggestion on the relations of the sac with the rest of the stomach as reported by Bouvier. Mackintosh (1925) and Yonge (1932), though they both quote Bouvier as authority for the observation that this genus has a style, are in reality merely giving a fahe air of certainty to Robson's suggestion, and actually the structure of the stomach and sac are such that it is impossible for a style to be present. The stomach possesses in part, i t is true, a thick cuticular secretion which might be taken for a gastric shield, but when the living animal is examined i t is found : first, that there is no direct communication between the assumed style-sac and the part of the stomach which bears this structure, so that if a style were present it would be impossible for it to come into contact with the shield ; secondly, that if a style were present in the sac the ciliary currents there are so arranged that it and its solution would be carried into the intestine and not into the stomach ; thirdly, that the cuticularized portion of the stomach is provided with an extremely thick layer of muscle-fibres, that the food coming down the esophagus is passed into it, and that i t appears to act as a gizzard ; and fourthly, that the animal is.provided with a pair of stout jaws by means of which i t snips off pieces of weed of such size aa to preclude the possibility of ingestion without previous digestion, an arrangement incompatible with the occurrence of a crystalline style.

I hope to give an account of the structure and function of the gut of this animal in greater detail elsewhere.

PILA (=AMPULLARXA in parte).

PILd OVATA Bolten : examined preserved. The structure of the alimentary canal was identical in general plan with

that of Ampullurius gigas, and with that of P. globosa a8 described by Prashad (1925), so that a style may be held to be absent in this genus too.

Rissoaeea. ADEORBIS ( =TORNUS).

ADEORBIS STJBCARINATUS Montagu : not examined. A description of this species has been given by Woodward (1899). From

the point of view of this investigation this is an animal of great importance, as it appears to be the sole taenioglossan with a style in which any massive structure corresponding to the crop of the rhipidoglossa has been described. According to Woodward the esophagus leads backwards from the buccal mass to a glandular enlargement, the lumen of which is split by a series of infoldings of the wall so as to appear in section as made up of several distinct tubes lying together. Woodward himself likens i t to the '' Vorderdarmdriise " described by Haller (1893) in Natica and Sigarelus. The stomach is divided into three portions, from the middle of which opens the intestine, whilst the anterior is " 8 blind diverticulum having all the relations of a crystalline style-sac, and


not unlike that described by Moore in Typhobia and other forms.” In view of the fact that this appears to be the sole case where such a type of esophageal structure coincides with the presence of a style, the anatomy and physiology of the alimentary tract of this genus require reinvestigation.

RISSOA.

RISSOA PARVA (da Costa) : examined alive. Robson (1922 b) suggested, on the basis of the figure given by Simroth (1901j.

that a style was present in the sac attached to the anterior end of the stomach. Dissection of living specimens of R. parva has shown that his suggestion wad true, a small style about two-thirds of a millimetre in length and bluish-green in colour being present in the style-sac and stomach. Oddly, the relationship between the sac and the stomach never appears to have been ascertained in this genus ; the sac lies at the anterior end of the stomach, with the intestine running along one side, between it and the esophagus ; for a little more than half their length the sac and the intestine communicate with each other by means of a slit-like space between two typhlosoles (text-fig. 4 A). Over the distal half of the length of the style-sac there is no communication, but the site of the slit is marked by the presence of a groove in the otherwise even wall lined by low ciliated cells instead of the tall cells characteristic of the rest of the wall (text-fig. 4 B). This corresponds to the groove described in other cases by Seshaiya (1929 b, 1930, 1932).

On each side of the dorso-median line in the buccal cavity projects a ciliated fold, the beginning of one of the dorsal folds ofthe food-channel ; in its epithelium ere many mucous cells. Elsewhere these are few and the cells bear no cilia. At the posterior end of the buccal cavity the lumen dilates on each aide to form a pouch-like structure, and at this level all the cells save those of the pouches are ciliated: The esophageal region is narrow in diameter throughout, is lined by ciliated epithelium containing large numbers of mucous cells, and immediately posterior to the nerve commissures twists round in the characteristic prosobranch fashion.

HYDROBIA. HYDROBIA VENTROSA (Montagu) : examined alive. HYDROBIA (PERINGIA) ULVZ Pennant : examined alive. HYDROBIA JENKINSI Smith : not examined. Owing to their minuteness I have not been able to make out the arrange-

ment of the ciliary currents on the wall of the alimentary canal of these animals with sufficient certainty to give an account of them. Of these species the first has previously been described by Robson (1922 a) under the name Palud- estrina ventrosa, the second by Henking (1894), and the last by Krull (1935). The details of structure appear so similar that a single account will serve, and I shall refer only to those points in which previous papers are lacking in sufficient detail.

Robson’s description of the esophageal region is limited to observing that it bears a “ series of diverticula in the form of deep longitudinal furrows. Behind the cerebral commissure the esophagus in most cases shows a tripartite arrangement as in Bythinella. Henking describes and figures a similar division into a median ciliated channel and two smaller lateral ones.

It is ciliated almost up to its distal extremity.”

86 MR. -STAIR GRAHAM ON THE ALtMENTARY

The threefold division is due to the fact that on the roof of the aesophagus runs the dorsal food-channel, guarded by the usual two folds which project so far as to come into contact with the opposite wall, thus dividing the lumen into a median and two lateral channels. The median channel is the food- channel, and its walls consist of the mesial surfaces of the dorsal folds and of a median strip of the ventral wall ; these regions are all lined by a ciliated columnar epithelium containing numerous mucous cells. The ciliated cells are character- ized by minute pigment granules in the distal half of the cytoplasm. The two lateral channels are the “deep longitudinal furrows ” described by Robson, but it is inaccurate to talk of a “ series ” of them : two only are to be found, one on each side of the central food-channel, and they are continuous from end to end. Their walls are formed by the outer sides of the dorsal folds and by the lateral walls of the aesophagus ; their diameter decreases steadily towards the posterior

Text-figure 4.

A B

Ris8oa p a w . Two transverse sections through the style-sac and the intestine ; A is slightly posterior

to B. g., groove ; i., intestine ; 8.8.. style-sac. x about 50.

end, and they ultimately disappear. The epithelium which lines them is different from that found on the folds : it is columnar, but the cells are only about half as tall as the others, are not ciliated, and have no pigment granules. Their cytoplasm is homogeneous, slightly vacuolated, and rather denser a t the surface of the cells than elsewhere.

The posterior cesophagus, which bears numerous longitudinal folds, one of which, a continuation of the left dorsal fold as noted by Henkinp, is larger than the others, leads back to the stomach, concerning the structure of which I have little to add to the account given by Robson of that of H. vedrosa. In addition to the structures which he mentions it might be recorded that a groove, lined by especially long cilia, runs from the base of the aesophagus towards the posterior end of the stomach and ends near the gaRtric shield which covers most of the right side of the stomach. Parallel to this groove and separated from it by a prominent bulge of the stomach wall is a second furrow running

Mucous cells do not occur here.


in a more ventral position, which passes the length of the stomach and ultimately leads into the intestine. S s this is reminiscent of what is found in several other forms (e.g., Turritellu, Graham, 1938; Calyptrza, see p. 103) i t may be conjectured that in the former groove the cilia beat aborally and that, as in the other genera described, i t leads food particles towards the style, whereas in the second groove the cilia beat in the opposite direction and conduct waste and rejected particles to the intestine.

Other Hydrobiida! . A style has been recorded previously in Bythinella dunkeri Frauenfeld by

Bregenzer (1916), in B. steinii Martens (aa Pal&trina steini Martens), Lartetia ( Vitrella) quenstedtii Wiedersheim and Lithoglyphua rusticoides de FBrussac by Krull (1935), in Potamolithus (=Lithoglyphua) lapidum (d’orbigny) by von Ihering (1885), in Hypsobia noaophora (Robson) by Robson (1921), and in Amniwlu and Mysorella wetigera Kuster by Seshaiya (1930, 1932). I have not been able to examine any of these snails, but it appears from the brief accounb referred to above that in all caws the structure of the buccal cavity and esophagus is similar to that which is found in Hydrobia. The most full description is that of Bregenzer (1916) for Bythinella dunkeri. Here the dorsal food- channel is closed ventrally by the apposition of the tips of the dorsal folds to the floor of the esophagus. The folds and the mid-ventral strip are ciliated. The remainder of the gut forms what are described aa glandular pouches one on each side of the esophagus. The histological description of these is inadequate to decide whether the cells that line them are truly glandular or whether they are like the featureless epithelium found in corresponding positions in Hydrobia. Bregenzer notes that this portion of the gut is extremely shorb and that the greater length of the passage from the buccal cavity to the etomach is occupied by the posterior esophagus (“ Vorderdarm ”), a narrow tube, the walls of which are thrown into lon,gjtudinal folds, with no glandular enlarge- ments.

BITHYNIA.

BITHYNIA TENTACULATA (L.) : examined alive. Previous accounts of the anatomy of this snail are given by Moquin-Tandon

(1855), by Seshaiya (1932) on the relation between style-sac and intestine, and by Krull (1935), who gives a figure of the stomach.

The buccal maas is of considerable size, and the median dorsal food-chaw lying between prominent folds is a conspicuous feature. Two small salivary glands open to $he buccal cavity, their ducts running along the outer sides of the anterior parts of the dorsal folds. A t the posterior end of the bum1 maas the esophagus curves ventrally, passes through the nerve-collar, and then runs back towards the stomach. Immediately posterior to the nerve-ring is the area of torsion.

When the esophagus and buccal cavity are opened it is seen that the ventra walls of the anterior esophagus are smooth, with the exception of short longitudinal folds of no great height. Alongside this area the lumen is dilated laterally into pouch-like structures which lie between the longitudinal dorsal fold above and the smooth ventral wall below. Posteriorly these extensions become smaller, and at the point where the ceaophagus penetrates the nerve-collar they have vanished, so that the dorsal fold borders the ventral tract directly. Behind

Bithynia tentacuhta. Stomach opened from the ventral side. Arrows indicate the direction of the ciliary currents

and the thick broken line outlines the gastric shield. d., duct of the digestive diverticula ; g.l, g.#, g.a, grooves as described in the text ; g.8., gastric shield ; i., intestine ; o., oesophagus ; o.u., opening of the oesophagus ; p., papilla ; T., ridge marking the boundary between stomach and intestbe ; 8.8., style-sec ; t., typhloeole. x about 20.

"HE ALIMENTARY CANAL OF STYLE-BEARING PROSOBRANCHS. 89

the region of the esophagus which is involved in torsion its diameter becomes much less, and the distinction between the dorsal and ventral parts is lost, the whole bearing longitudinal folds.

The arrangement of the ciliary streams is straightforward : on the dorsal food-channel the cilia beat towards the stomach. Anteriorly, so long as the esophagus possesses lateral extensions the cilia on the lateral margins of each of the dorsal folds beat transversely out of the pouches into the channel. On the floor of the esophagus the cilia beat posteriorly. Apart from the dorsal folds the walls of the buccal cavity are covered with cuticle.

Although, in dissection, the ventral wall of the esophagus seems to have no regular folds, in sections of fixed material two longitudinal folds run along it, almost as prominent as those of the dorsal surface. The histology of these is similar to that of the dorsal folds with the exception that they contain many more mucous cells : this is especially true of the anterior end, where the epithelium is largely composed of them. The ciliated cells in both are columnar, with basal nuclei and vacuolated cytoplasm. In the lateral pockets a second type of epithelium is found : this consists of lower cells of rather variable height with cytoplasm on the whole similar to that of the ciliated cells, but without cilia and bearing a thin cuticle instead. Mucous cells do not occur in these situations.

The esophagus (o., text-fig. 5) leads back to the stomach, which is a slightly elongated structure of some complexity, opening into it on the left side in a rather posterior position (0.a.). From the anterior end leave the intestine (i.) and the style-sac (6.5.) communicating with one another by a slit between two typhlosoles ( t . ) , as observed by Seshaiya (1932). On the right and dorsal walls lies the gastric shield (g.s.), similar in shape to those of Pomatias and Turritella. The duct of the digestive diverticula opens on the left side close to the esophageal aperture. Krull (1935) records the presence of a second duct, close to the first, but this I have not been able to verify.

The general plan of the stomach is reminiscent of both Pomatias and Turri- tells. Curving round the left margin of the gastric shield is a deep crescent- shaped groove (9.J bounded by tumid lips, that on the left having a number of parallel transverse grooves on its surface which curve on to the left wall of the stomach behind the esophageal aperture. Posteriorly the crescentic groove leads to a distinct pocket near the point where the style bears against the gastric shield, and is continued towards the origin of the intestine anteriorly. Parallel to this groove there runs a second (9.J which originates between the openings of the duct of the digestive diverticula and the esophagus and runs thence anteriorly to the left side of the intestine, curving below a prominent papilla ( p . ) a t the entrance to the latter. The papilla is the swollen end of a transverse ridge (r . ) which delimits the style-sac and intestine from the stomach. The former has smooth walls save for a series of transverse ridges which originate from the left typhlosole and run a short distance across the wall in a fashion reminiscent of the similar folds found in Anodonta (Mackintosh, 1925), so that the style is supported on bearings. Below the right typhlosole is an irregular grouping of folds and grooves on the intestinal floor. The principal of these is a groove (q.J running parallel to the typhlosole and leading to the stomach slightly to the right of the mid-line. Into this opens a series of tributary grooves, separated by ridges, from the floor of the intestine.

The arrangement of the ciliary tracts may be gathered by reference to text- fig. 6 . The general functioning of the stomach appears to be in most respects similar to what I have already suggested for Turritella (Graham, 1938), making

(30 THE ALIMENTARY CANAL OF STYLE-BEARING PROSOBRANCHS.

allowance for the fact that Bithynia appears to possess two sorting areas on the walls of the stomach, only one of which is represented in Turrite1Ea;dthaugh indications of both are found in PomatiaS. Particles are brought down the esophagus and are carried back to the pocket near the head of the style with the substance of which they are thoroughly mixed. Thence they are carried forwards along the left margin of the shield, and enter one or both of the grooves leading towards the intestine. A certain amount of selection of particles would apparently take place at this stage, and, whilst some are carried towarde the intestine, others are swept backwards along the crescent-shaped groove. Particles carried into the intestine arrive there on its left side and are brought to the series of ridges and grooves which lies on its floor. This is particularly true of particles entering by way of the extension of the crescent-shaped groove ; the others enter the intestine so far to the left as to miss almost entirely the sorting action exercised by these structures. These particles are, however, mainly from the duct of the digestive diverticula.

Larger particles are passed acroaa the grooves and ridges and continue their paseage down the intestine ; smaller ones, on the other hand, are directed along the grooves and enter the longitudinal gutter which lies ventral to the right typhlosole. Along this a strong ciliary current beats towards the stomach, which returns the smaller particles to the stomach where they are carried round the anterior margin of the shield into tracts passing back to the duct of the diverticula and to the head of the style.

Particles which leave the duct of the diverticula after digestion enter the principal rejection tract and pass directly into the intestine.

ASSIMINEA.

ASSIMINEA sp. : examined preserved. In an unidentified species of Assiminea, individuals of which I have dissected,

the cesophagus ran as a straight narrow tube from the buccal cavity to the stomach. No differentiation into regions waa possible. The relation between style-sac and intestine has been described by Seshaiya (1932). A style has been recorded in AssemunicG (=Asaiminea) gruyum Leach by Krull (1935). No further details are given.

CYCLOTOPSIS. POMATIAS ( =CYCLOSTOMA).

POMATIAS ELEGANS (Miiller) : examined alive. An earlier description of P. elegans is given by Garnault (1887). Seshaiya

(1934) records the presence of a style in CyclotopsiS subdiSc0idea. On the dorsal side of the buccal cavity lies the dorsal food-channel, the

groove appearing as a distinct light-coloured tract when the buccal mass is examined from the outer side. Lateral to it, slightly in front of the nerve-ring, open the ducts of two salivary glands, lobulated strap-shaped structures lying freely in the haemoccel one on either side of the esophagus, to which they are tied by connective tissue. Behind the nerve-ring the esophagus leaves the buccal maas and follows an approximately straight course to the stomach, exhibiting the characteristic torsion immediately behind the nerve-ring. The radula-sac is also involved and passes dorsal to the posterior end of the twisted area, curving from right to left.

On opening the oesophagus in this region it is found that the food-channel ( f . ~ . , text-fig. 6 A) with its two folds (d. f-) occupies the entire dorsal half

Text-figure 6.

A 1

j . C .

0.

B C.

C

- . c. I .

Ponaatk elegana. A. Dia rammatic transverse section through the mophagus ; the epithelium of the dorsal

food-channel is stippled. Arrows indicate the direction of the ciliary currents on the dorsal folds, and in the channel between the two circles the cilia beat towards the stomach. d.j., dorsal fold ; f.c., dorsal food-channel ; v . , ventral wall of the

B. C a l ~ ~ ~ ~ ~ d o r s a l food-channel. c., cilia ; c.t., connective tissue and muscle layem ; j., intracellular fibrillae ; mc. , mucous cell ; n.c., nucleus of ciliated cell ; p., pigment granules. x 250.

C. Cells from the ventral wall. d., dense peripheral cytoplasm ; n., nucleus of epithelial cell ; other lettering as in B.

D. Stomach opened from the ventral side. Arrows indicate the direction of the ciliary currents, and the thick broken line outlines the gastric shield. c., cacum; i.t., ingoing tract ; a t . , outgoing tract ; other lettering aa in text-fig. 6.

. x about 35.

x 250.

x 12.

92 MR. U S T A I R GRAHAM ON THE ALIMENTARY

of the gut ; as it twists backwards the extent of wall which it covers dwindles, and at the posterior end i t extends over only about a third of the wall. The morphologically ventral region of the gut (v.), which begins anteriorly a t the mouth of the radula-sac, bears no folds apart from minor irregularities of the surface ; posteriorly, where i t occupies successively right and dorsal positions, i t gradually decreases in size, and ultimately disappears, the wall of the cesophagus being then marked by longitudinal folds similar in appearance to the two dorsal ones, though less high.

A corresponding histological differentiation, which Garnault missed, exists between the dorsal and the ventral parts of the fore-gut. The dorsal folds and the groove between are lined by a ciliated epithelium (text-fig. 6 B). The cells bear numerous cilia (c.), with intracellular fibrillae (f.) embedded in the distal cytoplasm; the nucleus (n.c.) lies in the central region of the cytoplasm, and between it and the rootlets of the cilia is a zone of minute pigment granules (p . ) . The rest of the gut in this region (text-fig. 6 C) is covered with a different type of cell : a lower columnar cell, without cilia, but with a dense layer of cytoplasm (d.) on its distal surface which extends down the boundaries between neighbouring cells towards the basement membrane. The rest of the cytoplasm is fibrillar, and the nucleus of the cell (n.) is more granular than those of the ciliated cells of the food-channel. MUCOUS cells occur here too (m.c.), but less frequently than in the dorsal folds. The epithelium everywhere rests on a spongy connective tissue (c.t.). Circular and longitudinal muscles form a definite layer around the gut. lying close to the epithelium save in the regions of the dorsal folds ; the former are the more numerous.

At the posterior end of this part of the gut, where the smooth area ends and is replaced by longitudinal folds, the entire wall is covered by an epithelium Aimilar to that of the dorsal channel.

On the walls of the dorsal groove and the median halves of its limiting folds the cilia beat ahorally (text-fig. 6 A) ; on their lateral margins they have a transverse direction, beating into the groove and thus keeping the food close to the main transporting current on the gut wall. Posteriorly all the cilia beat towards the stomach.

The esophagus (o., text-fig. 6 D ) leads back to the stomach, opening into it about the middle of the left side. The stomach is elongated and is produced into a long caecal extension (c.) passing posteriorly, similar to that found in the related genus Littorim. The intestine (i.) and the style-sac (s.s.) open from the anterior end, the two communicating with each other by a fairly broad aperture between two typhlosoles ( t . ) . On the right and dorsal walls of the stomach lies a small gastric shield (g.s.), near the base of which open the ducts of the digestive diverticula @). On the left wall of the stomach, slightly anterior to the esophageal opening, lies a deep crescent-shaped groove (8.) bounded by tumid lips, and a t the opening of the intestine is a series of close-set longitudinal folds.

The longitudinal folds with which the esophageal walls are set diminish markedly in size when the stomach is reached, but they can be traced along the whole length of the wall of the caecum as a ciliated tract (i . t . ) bearing particles. from the one part to the other. Garnault's observation that no cilia occur on the stomach walls is thus without foundation. On the opposite wall of the caecum a similar but rather narrower tract (0.t.) leads forwards to the floor of the stomach, where i t loses itself in a broad tract between the gastric 'shield and the crescent-shaped depression. The rest of the caecal wells is not ciliated.

MUCOUS cells (m.c.) are abundant.

CANAL OF STYLE-BEARING PROSOBRANCBS. 93

On the folds around the crescentic groove, except on the left side, currents beat towards the intestine. On the left lip they beat into the posteriorly beating tract which leads from the esophageal opening. The folds a t the base of the intestine, the left typhlosole, and the bulk of the intestinal wall itself bear cilia which beat towards the anus ; on the right side of the intestine and on the right typhlosole they beat in an opposite direction. This typhlosolar current ie responsible for forcing the style towards the stomach, whilst transverse currents on the wall of the sac rotate it. From the openings of the ducta of the digestive diverticula currents sweep round the base of the gastric shield on to the ventral wall in the neighbourhood of the anterior end of the forward tract in the caecum. I have seen no currents beating into the ducts.

Food particles will be led into the csecum, which will act aa R store place from which they may be withdrawn by the anteriorly beating ventral tract and brought to the head of the style. This ventral tract is less rapid than the posteriorly beating dorsal one : this may help in maintaining a regular supply of food for the style if the animal does not eat sufficiently steadily to do this directly. In this way the caecum would act as a kind of valve, converting a spaamodic inflow into a continuous outflow. If, as Yonge (1932) suggests, Pomatk is R continuous feeder this may not be of importance, but the possibility of evening out irregularities in the rate a t which food is taken into the stomach by this means is important.

The crescent-shaped groove appears to act in some way as a sorting device, but its small size when compared with the homologous structure in Turritella (Graham, 1938) suggests that it is vestigial and not of great significance in the functioning of the stomach. The same may apply to the return current along the intestine. As has been Been above (p. 90) there is developed in this particular region in Bithynia a definite sorting area, and i t may be that the simple current running into the stomach from the intestine is all that represents this in Pomcaticls. The other currents present are clearly connected with emptying the stomach and the digestive diverticula of waste material or of particles unsuited for ingestion.

Cerithiaeea. TURRITELLA.

The general result of this arrangement of ciliary currents is plain.

~ R R I T E L L A COMMUNIS Risso : examined alive. A description of the alimentary tract and of the ciliary currents on its walls

is given in an earlier paper (Graham, 1938), and the structure of the stomach h w been discussed by Seshaiya (1932). The general course and structure of the esophageal region are similar to what has been described in many cases above- a straight tube with a morphologically dorsal food-channel (J.c., text-fig. 7 A) twisting behind the nerve-collar into a topographically mid-ventral position. The two folds of the dorsal food-channel (d.f.) remain slightly larger than the other folds which occur on the esophageal walls. With the exception of the most anterior part of the ventral wall all the folds and grooves are ciliated, the cilia beating aborally.

&spite the similarity in the direction of the ciliary currents there is a slight differentiation between the food-channel and its folds and the morphologically ventral half of the esophagus. The inner walls of the food-channel am covered with a tall columnar ciliated epithelium (text-fig. 7 B), the cells

Text-figure 7.

B C

m.c.

n. m. c. TurrWla mmunis.

A. Diagrammatic transverse section through the aesophague ; the epithelium of the dorsal

B. Cells from the dome1 food-channel. n.m.c., nucleus of mucous cell ; p., pipent granules ;

c. Cells from $he ventral wall, bettering 88 in B,

food-channel is stippled.

8.. spherules in secreting cell : other lettering as in text-fig. 6 B.

Lettering as in text-fig. 6 A. x about 50.

x 300. x 300.

THE ALIMENTARY CANAL OF STYLE-BEARING PROSOBRANCHS. 95

of which contain elongated oval nuclei (n.c.) in their centre and numbers of minute pigment granules (p.) in the cytoplasm between the nuclei and the intracellular fibrills of the cilia. Mucous cells abound (m.c.), with round b w l nuclei (n.m.c.). A second type of glandular cell also occurs, containing spherules (9.) of moderate size ; these stain darkly with iron hsmatoxylin and bright red with the Champy Kull stain. In the morphologically ventral portion of the esophagus (text-fig. 7 C) the general character of the epithelium L similar but with suficient difference in detail to give it a distinctly different look : it is lower, and the granules of pigment (p . ) in the ciliated cells arb larger, 80 that it appears as a dark coloured tract in the intact gut contrasting with the lighter food-channel. The other point of difference is the relative proportions of the two types of gland-cell : in the food-channel mucous cells predominate, in the ventral part the second type is commoner. The exact function of this type is unknown. It is improbable in view of the rarity of free enzymea in the gut of animals possessing a crystalline style that these are enzymatic cells, and it seems most probable that they are to be regarded as accessory lubricating or cement-glands. Their appearance and staining reactions are suggestive of the clavate glands of the intestine of Patella (Graham, 1932), which appear to have this €unction. Should they be enzymatic the enzyme cannot be a protertse (Yonge, 1930), and might therefore be a diastatic enzyme of some sort. Tests for mllulase have been negative. I am loth to accept this idea, however, as the cells are not confined to the ventral part of the esophagus but are also encountered in the food-channel, a part of the esophagus which throughout the entire prosobranch series appears to be concerned exclusively with the transport towards the stomach of food and, on occasion, of enzymes prod& ekewhere, and the sole type of gland-cell which is normally found in that position is the mucous cell or its functional equivalent.

APORRHAIS. Yonge (1937) records

that the oesophagus is straight and wide, and does not mention any glandular appendage or tract. Torsion, though not explicitly mentioned in any description, presumably occurs both here and in Verrnetua. Yonge also gives an account of the structure and ciliary currents of the stomach.

I have not examined any specimens of Aporrhais.

VERMETUS. According to Yonge (1932) the interrelationships of the various species

of this genus are incompletely known, and i t appears that it includes two quite distinct groups of animals : one, including V. n u v ~ hollandict! and an unnamed species, both ciliary feeders, and another, including the better known V. gigas and V. triquebr, which do not feed by cilia but by means of mucous traps (Boettger, 1930). I have not examined any of these species myself, and rely on Yonge’s account (1932). According to this no glandular structures occur on the esophagus, a long straight tube with thick walls bearing aborally beating cilia, so weak as to suggest that food is transported along this part of the gut by peristalsis. It may be the development of muscles in the esophageal wall for this purpose which causes its thickness.

T IARID~E (=ME L A N I I D a). Of this family I have examined preserved specimens of seven members:

Melanopsis pzmorsa (L. ) , PalwEamus sp., Melania (Melanoides) zenganw (Morelet), Tanganyicia rufoJiha (Smith), Spekia uynata (Woodward), Para- melania (Bythmerm) minor (Moore), and P. (P.) damoni (Smith). Of these a11


have been previously known to possess a style except Melanopsis. They fall naturally into two groups, the first, including Melanopsis and Melania (=Tiara, Seshaiya (1934)), representative of the subfamilies Melanopsiwe and T'iarim (=Melani im), the second containing the rest, which belong to the subfamily Paludomiwe.

The structure of the anterior end of the alimentary canal of Melanopsis and Melania is similar. Behind the region of the odontophore, where the food-channel is conspicuous, the gut dilates to form an elongated spindle- shaped crop, hetween the two regions lying the nerve-ring. Along the dorso- median line of the crop in Melanopsis runs the food-channel, distinguished externally by its lighter colour and internally by the two large folds. The rest of the wall is marked by weakly developed longitudinal folds, and there is a suggestion of an out-pouching of the walls of the lateral areas where they border on the dorsat folds. In Melania the channel is invisible externally though still conspicuous within ; the wall is marked by longitudinal folds, but there is no pouching.

In the subfamily PalwEomiwe the arrangement of this part of the gut is different, and in the case of Spekia zonatu, Tanganyieia rufofilosa, Bythoceras ( =Paramelania) sp., Bathanalia h e s i , and Typhobia ( =Tiphobia) horei has been described by Moore (1898, 1899 a, 1899 b), while accounts of Limmtroehus and Chytra have been given by Digby (1900-1902), and of Paludomus tan- schaurica by Seshaiya (1929 a) . I have not been able to dissect specimens of Bathanalia, Tiphobia, Lirnnotrochus, or Chytra, but in the other cases my results agree with those of Moore.

In Tanganyicia rufojilosa the mouth leads into a buccal cavity in which a minute odontophore is lodged. Alongside this run muscles inserted on its lateral walls, whence they diverge to the ventral body-wall. Behind the nerve- ring the oesophagus, which is a straight, narrow tube, shows twisting, but neither externally nor internally is there any trace of gland or glandular region. Moore (1899 a) was unable to decide in what way this animal fed as the radula and the odontophore are vestigial, and yet the gut of all the specimens he examined was full of sharp fragments of rock. The anterior end of the snout is produced into a somewhat bloated non-eversible proboscis with a small mouth at its tip, the whole structure appearing-in preserved specimens at least-very mobile. Moore makes no mention of the muscle-bands attached to the gut. It seems probable that the mode of feeding is suctorial, and that the muscles which run along the sides of the buccal cavity are for the purpose of dilating the cavity when feeding is taking place.

In Paludomus, Spekia zonata, Paramelania m i w , and P. darnoni the structure of the gut is similar, the snout and buccal mass being normal.

Tiphobia horei, according to Moore (1898), has a long slender oesophagus, its walls thrown into long folds and lined by ciliated and glandular cells. The nature of the latter is not disclosed, but it can probably be taken that only mucous cells are meant.

Neither Robson (1922 b), Mackintosh (1925), nor Yonge (1932) admit Bathanalia howmi to their list of prosobranchs with a style. In view of the fact that Moore (1898) makes the statement that " in its anatomical features it is so similar to Typhobia that no special description is required," and has previously described the style and style-sac of Tiphobia, i t seems illogical to conclude that Rathanalia does not also have a style. 80 far as the structure of its alimentary canal is concerned Moore's figs. 37, 40, and 42 show a slender and straight esophagus without any lateral glandular pouches in transverse section.

CANAL OF STYLE-BEARXNO PROSOBRANCHS. 97

The structure of the gut in Limnotrochus and Chytra, aa described by Digby (1900-1902), is similar to what has been given for the other members of the Paludomim.

Seshaiya (1934) records the presence of a style in Aerostoma and Stomatodon without giving any further details about the gut ; this probably agrees with other members of the family.

POTAMIDES.

POTAMIDES (POTAWDES) MINIMUS (Gmelin) : examined preserved. POTAMIDES (CERITHIDEA) DECOLLATA (L) : examined preserved. In both of these the gut posterior to the nerve-ring expands into a large

A prominent food-channel There is no trace either of folding of the lateral

thin-walled crop tapering before and behind. occupies the usual position. walls or of a mid-ventral longitudinal fold.

TELESCOPIUM ( =POTA.MOIDES).

TELESCOPIUM TELESCOPIUM (L.) : examined preserved. Seshaiya (1932) has already described the presence of a style and style-sac

The oesophagus is a straight narrow tube running backwnrds in this species. from the buccal mass ; internally the walls show slight longitudinal folding.

Calyptraeacea. CREPIDULA.

CREPIDULA FORNICATA (L.) : examined alive. A description of the anatomy of Crepidula fornicata, without mention of a

style, waa given by Haller (1892). In 1912 Orton described its ciliary feeding process ; ten years later (1922) he noted the presence of a crystalline style in the stomach, and Mackintosh (1925) described the details of the stomaah and style-sac.

The mouth lies at the tip of the dorso-ventrally flattened cephalic region, and leads into a small buccal cavity into which a small odontophore projects. From the buccal cavity a tube of narrow dimensions takes a slightly sinuous course posteriorly, alongside it in the surrounding connective tisaue lying a pair of lobulated salivary glands. Level with the anterior end of the foot the alimentary canal passes through the nerve-ring, which thue lies a considerable distance behind the buccal mass. Behind the nerve-ring the gut continues its straight course and runs back to the stomach. Although the supra-intestinal branch of the visceral loop crosses the gut immediately posterior to the nerve-collar (Bouvier, 1887), and should indicate the anterior border of the region involved in torsion, I have not found any clear indication of a twisting in the alimentary tract at any point between here and the stomach either by external or internal examination or in sections. Assuming that the original torsion indicated by the nerves had also affected the gut, this would imply that a post-torsional growth in the oesophageal wall had taken place tending to restore the original disposition of the parts.

On opening the alimentary canal in the anterior region the two folds described by Haller become visible in the part lying anterior to the nerve-collar, whitish in colour, the rest of the walls having a grey tint. His interpretation of these structures and his description of the histology of this part of the gut,

PBOO. ZOOL Sw., SEB. B 1 4 9 3 9 , B

Text-figure 8.

C C.

m.

B

C.

i t . Crep&lula fornicata.

A. Diagrammatic transverse section through the posterior buccal cavity, anterior to the nerve-ring. c.t., connective tissue and muscle layers; g., groove running along dorsal fold ; p., nerve lying at base of dorsal fold ; other lettering aa in text-fig. 6 A ; symbols as in text-fig. 6 A.

g.c., gland-cell ; other lettering as in A and text-fig. 6 B. x 250.

c., cuticle ; b.na., basement membrane ; other lettering as in A,

x about 50. B. Cells from the dorsal fold.

C. &Us from t,he dorsal and ventral areas. x 600.


however, rest on a complete misconception of its homologies, and I have found nothing to correspond with it (see, however, Calyptrza, p. 103). According to Haller the folds, which are themselves ciliated on both sides, are simple and separate a dorsal ciliated food-channel from a ventral glandular region which he homologizes with the “ crop ” or “ Vorderdarmdruse ” of other prosohranchs-that is, with the esophageal pouches. The folds certainly lie right and left, and divide the lumen into dorsal (D, text-fig. 8 A) and ventral (V) chambers, but these are histologically identical, and neither resembles the folds, which are the only ciliated tracts in this part of the gut. The two folds, which are distinctly divided themselves by a longitudinal groove (9.) along their summit, are covered by a regular columnar epithelium of ciliated cells (text-fig. 8 B) and occasional gland-cells (s.c.), not mucous, but resembling those described in the esophagus of Turritella (p. 95) in their staining reactions. Both rest on connective tissue in which run circular and longitudinal muscles (c.t.). At the base of each fold runs a nerve (n., text-fig. 8 A).

In the dorsal and ventral chambers of the gut (text-fig. 8 C ) the cells are columnar, about half the height of those on the folds. None is ciliated, but all bear a cuticle (c.) on their surface resting on a layer of dense protoplasm. Occasional gland-cells like those described above occur. The cells rest on a very thick basement membrane (b.m.), and below that lie connective tissue and muscles (c.t.).

The folds begin in the buccal cavity above the odontophore, lying one on either side of the mid-dorsal line, and extend almost as far as the nerve commissures. Just anterior to this the structure and histology of the gut-wall change : the whole wall is covered with longitudinal folds, two of them, con- tinuations of the anterior ones, standing out as slightly larger than the others, and the columnar ciliated epithelium described above is now the sole type found on the wall.

The arrangement of the ciliary currents is simple (text-fig. 8 A) : on the longitudinal folds of the gut anterior to the cerebral commissure, and especially in the groove along them, a strong current beats towards the stomach ; on the lateral margins of these folds, where they border the dorsal and ventral chambers, the cilia beat into the groove. Behind this region all the folds bear cilj 1 which beat aborally.

The correct interpretation of the anterior end of the alimentary canal of Crepidula is simple when the histology and the morphological relations of the region are considered. The two important points to bear in mind are (1) that the histology of the region in identical with that of the buccal cavity and (2) that this region all lies anterior to the nerve-ring. In Crepidulu, and to a lesser degree in Culyptrtea, the region between the posterior end of the odontophore and the nerve-collar has been extended to form the conspicuous “ neck,” and the part of the alimentary canal lying here, i. e., the anterior esophagus, has increased equally in length. The glandular part of the esophagus always lies posterior to the nerve-ring : there is thus no relation possible between this part of the gut of Crepidulaand the glandular esophagus of other prosobranchs, and Haller’s homologies and compitrisons are valueless.

The structure of the stomach and the arrangement of the ciliary currents on its walls may be gathered from text-fig. 9. They bear a close resemblance to what is seen in Calyptrtea. The style-sac (8.8.) and intestin? (i.) arise from the anterior end of the stomach, with two ducts of the digestivediverticula opening a t their base. The esophagus opens to the stomach (0.a.) on the left aide, and the wall opposite bears the gastric shield (g.s.), around the left side of

This arrangement persists to the stomach.

H2

Text-figure 9.

2

Crepidub f w n i c a t a . Stomach opened from the ventral side. Arrows indicate the direction of the ciliary currents

and the thick broken line outlines the gastric shield. f., fold from the oesophagus extending on to stomach-wall ; X, see text ; other lettering as in text-fig. 5. x about 12.


which runs a crescentic groove (9.) bounded by double folds on each side. Of these the left is a continuation of a fold arising in the esophagus ; a second oesophageal fold (f.) extends on to the left wall of the stomach for a short distance. Between the crescentic groove and the left edge of the gastric shield lies an irregularly folded area, and from the crescentic groove to the intestine the wall of the stomach bears a series of fine ridges and grooves. Two further ducts of the digestive diverticula (d.J open near the posterior end of the stomach. The style-sac and the intestine are separated from each other by a single typhlosole, on one side ( t . l ) and a double one on the other ( t . J , the head of the first fitting closely into the depression which rum along the other.

Food is carried from the esophagus to the posterior end of the stomach by the tract lying to the left of the left fold bounding the crescentic groove, and passes to the gastric shield, where it will be mixed with the style enzyme. Thence i t is carried forwards by a series of currents, the strongest lying to the right of the right fold bounding the crescentic groove. Many particles usually accumulate at the point X, whence they are borne on to the series of ridges and grooves. Strong ciliary currents there drive them into the intestine, and are joined by tributaries from the lips of the ducts of the digestive diverticula. The crescentic groove appears to act rn a sorting mechanism, but the details are not obvious, as there is not, as in Turritellu, a current leading into the groove from the anterior end ; it is probable, however, that the current leading to the left on the right fold serves to drive particles across the groove on to the left half of the left fold, whence they could join the current passing back from the aesophageal aperture ; other particles, larger in size, would be intercepted by the currents on the right halves of the two folds and flicked in each case into a stream which would lead them ultimately into the intestine. Another mechanism which appears to prevent the passage of certain particles into the intestine is provided by a posteriorly directed current on the underside of the right typhlosole ( t . l ) and by the current on the intestinal half of the left typhlosole (t..J which leads particles back to the stomach.

CALYPTRBA.

CALYPTIVEA CHINEXSIS (L.) : examined alive. Calyptrtea bears a close resemblance to Crepidula, differing from it as regards

the arrangement of the anterior end of the alimentary canal mainly in the fact that the length of the region between the buccal cavity and the cerebral corn- missure is relatively smaller.

The floor, in the anterior esophagus, is a triangular area, the apex pointing backwards and reaching a point just anterior to the nerve-ring. Here the gut has in section the figure-of-eight shape seen in Crepidulu. Behind the nerve-collar the whole gut-wall bears longitudinal folds and is laterally compressed. About aa far behind the nerve-ring as the odontophore lies in frontimmediately anterior to the point where the oesophagus penetrates the diaphragm separating the cephalic and visceral haemocelic sinuses-the oesophagus is twisted in the usual fashion.

The esophagus (o., text-fig. 10) leads to the stomach, opening into it anteriorly on the right side, which i t reaches by crossing over ventrally from the left ; the folds on its wall end a t the opening. The style-sac (8.8.) and the intest,ine (i.), communicating with each other by a slit between two typhloeoles ( t . ) , leave from the p t e r w r end, and two ducts from the digestive diverticula

On the roof of the buccal cavity lies the dorsal food-channel.


Text-figure 10.

1.

P

Colyptrza chinensis.

Stomach opened from the ventral side. Arrows indicate the direction of the ciliary currents A, P, topographically anterior and the thick broken line outlines the gastric shield.

and posterior ends ; other lettering as in text-fig. 6. x about 20.


(d.J open between the apertures of esophagus and intestine. A gastric shield (g.s.) lies on the left side, two further ducts from the diverticula (&) opening at its base on the right, and, aa in other cases, the right margin borders a pro- nounced crescent-shaped groove (9.). At the base of the style-sac lies a series of transverse folds, and a group of smaller longitudinal ones occurs near the openings of the anterior pair of ducts from the digestive diverticula. The unusual relations of the stomach imply that it has been displaced in the viscerel maas, so that its morphologically anterior end now lies in a posterior position, and that it has rotated on its long axis so that the Ieft side now lies on the right. This is further shown by the course taken by the esophagus to reach the stomach-it passes backwards slightly left of the middle line, and on nearing the stomach passes abruptly across its ventral surface to open into the right side.

Particles brought down the esophagus are passed into a tract which carries them to a pocket lying near the head of the style. where they will be mixed with its substance. A series of currents bears them forwards along the grooves and folds which border the shield on ite right margin. This takes them a t once towards the intestine and the ducts of the digestive diverticula. There is no obvious mechanism to separate large from small particles, so that it may be that the sorting of particles which takes place in the mantle-cavity (Cdyptriea being a ciliary feeder) is sufficient to ensure that only particles of appropriate size enter the gut. Currents on one typhlosole and the contiguous strip of the wall of the style-sac push the style towards the stomach ; those on the rest of the wall of the sac rotate it. On the other typhlosole I have not been able to detect any effective current, although cilia can be seen beating on its surface. From the apertures of the ducts of the diverticula a rapid current beats directly into the intestine, on the floor of which particles are passed to the anu8.

The summits and upper sides of the dorsal folds bear a columnar ciliated epithelium with mucous cells. Save for a median strip the roof of the gut is not ciliated, but consists of a columnar epithelium of cells bearing a thin cuticle. The lower sides of the dorsal folds and the triangular floor of the anterior esophagus are unciliated, and are covered by low columnar cells often arranged in groups separated from each other by clumps of smaller cells lying at the bottom of crypt-like depressions which appear to poke through interstices in the muscle layers into the surrounding blood sinuses. This may be caused by extreme contraction on the part of the underlying muscles on fixation. The cytoplasm of these small cells is homogeneous, and they do not appear to be glandular. Oddly enough this type of epithelium is reminiscent of what was described by Haller (1892) in CrepicEula fornicata, but which I was unable to verify. Its position and homologies are ab in Crepidula, and there is no relationship between i t and the typical esophageal pouchep of the prosobranchs.

CAPULUS.

The ciliary currents on its walls are shown in text-fig. 10.

CAPULUS UNGARICUS (L.) : examined preserved. The structure of the specimens dissected was sufficiently well preserved

to enable me to describe the esophageal region, but not to give any details of the stomach.

From the roof of the buccal cavity two folds hang down, one on either side of the dorso-median line, and pass back into the cesophagw, curving down behind

104 MR. ALASTAIR GRAHAM ON THE ALIMENTAFLY

the nerve-ring to the ventral side : this constitutes the dorsal food-channel. The structure of the ventral part of the gut varies. Between the nerve-ring and the anterior end of the esophagus lies a sheet of smooth epithelium ; behind the nerve-ring this part of the wall bears numerous small longitudinal folds and grooves. Posteriorly these become fewer and larger, and a t the posterior end of the cesophagus i t shows internally a series of approximately equal folds, amongst which the two of the dorsal food-channel stand out by being slightly larger and further apart than their neighbours. The transition between this folded region and the anterior unfolded one is abrupt.

In general characters the stomach resembles those of the Calyptraeidae.

Strombacea. ROSTELLARIA. PTEEOCERA. STEOMBUS.

STROMBUS sp. : examined preserved. I have been able to dissect only a single. rather badly preserved specimen

of a species of Strombus, and none a t all of Rostellaria or Ptermra, but descriptions have already been given of the alimentary canal of Strombus troglodytes and S . g igas and of Roetellaria rectirostria by Haller (1893), and Amaudrut (1898), describing R. curvirostris, remarks that the resemblances between the two are so great that one description will suffice for the two. Pterocera has been described by Woodward (1894) and Yonge (1932).

In Strombus and Rostellaria the esophagus is a narrow tube showing only a slight degree of expansion in the region lying behind the nerve-ring. Within it lies a food-channel of normal structure showing the usual twisting, the rest of the wall being thrown into longitudinal folds the edges of which are irregularly pappillated, which Amaudrut describes as probably glandular. In Pterocera the esophagus enlarges to form a crop described as tapering away to a narrow tube ; no further details of its structure are given. If, as these accounts suggest, the esophageal pouches of Strombus, Rostellaria, and Pterocera are rather less reduced than in other forms i t may be that here lies the locus of secretion of the cellulase found in Pterocera and in Strombus at least by Yonge (1932), which proved so difficult to trace. Further work on the structure and function of this part of the alimentary tract of these molluscs is desirable.

OPISTHOBRANCHIA.

Pteropoda. As both Meisenheimer (1905) and Yonge (1926 6 ) have shown the only

opisthobranchs in which a crystalline style occurs are the thecasomatous Pteropods. These animals lie outside the scope of this paper, it9 the lateral glandular areaa of the esophagus and homologous structures are a characteristically prosobranch structure of which only traces, and these stiIl uncertain, may be found in an opisthobranch. Nevertheless, most descriptions of the m o p h a p s of the thecasomatous Pteropods (e. 3., Howells, 1936) state that, it ie a tube of small dia,meter, without glandular differentiation, paming back to the stomach.

CANAL OF STYLE-BEARING PBOSOBRANCHS. 105

DISCUSSION The crystalline style is an adaptation peculiar to certain molluscs, and its

occurrence is intimately associated with a particular method of functioning of the alimentary canal. The details of this have been admirably summed up in the form of two generalizations by Yonge (1930, 1932). The first of these is that all molluscs which possess a style are microphagous herbivores without free proteolytic enzymes in the gut, and the second is that all these animals feed either by cilia or radula in such a way as to maintain an almost const,ant Atream of food along the alimentary tract.

The glandular areas associated with the prosobranch gut are three in number-buccal salivary glands, lateral oesophageal pouches, and the gastric digestive gland. Proteoclastic enzymes from any or all of these will interfere with the functioning of a crystalline style, and accordinglv their function is modified in such prosobranchs as possess that structure.

The primary function of the salivary glands appears to have been the production of mucus for the lubrication of the radula and for cementing together the food particles collected by it. Where other structures provide a lubricant, as in Turritella, the salivary glands will be reduced. In carnivores the secretion of a protease (Symtypus, Mendel and Bradley, 1905), and in herbivores that of various enzymes attacking carbohydrates (Pulmonates, Krijgs- man, 1925, 1928 ; Pterocera, Strombus, Yonge, 1932), may be superadded. In such as possess a style they usually preserve only their primitive function- that of lubrication-though in certain cases, aa in Pterocera, the secretion of amylolytic and of sucroclastic enzymes also takes place.

The digestive gland in the opisthobranchs and in some of the higher prosobranchs secretes enzymes which act in the stomach, and absorbs the products of digestion ; or it may, as in all forms with a style, assume the form of digestive diverticula (Yonge, 1926 b), organs not of secretion but for the ingestion of minute particles and for their intracellular digestion.

The functions of the glandular pouches of the esophagus are almost unknown. Graham (1932) described the production of an amylase by this part of the gut in Patella, and Weber (1927) attributed the secretion of a proteolytic enzyme to its homologue in Dolium, though the accuracy of the homology is questioned by Thiele (1935). Hirsch (1915) records the secretion of a protease from the “ Vorderdarmdriise ” of NatiCa, of a proteolytic enzyme by the “ kleine Vorder- darmdriise,” and of an amylase by the “ grosse Vorderdarmdriise ” of Murex ; these structures Amaudrut (1898) had previously shown- to be the homologues of the oesophageal pouches of the rhipidoglossa. Fretter, too (1937), had found an amylase in their homologues in chitons. Whatever the details of their function may turn out to be it is plain that they secrete some substance of importance in the digestive processes of the typical prosobranch ; their presence is an index of extracellular digestion taking place in more posterior parts of the alimentary canal. Provided that this is a digestion of carbohydrate material they may co-exist with a crystalline style, as may be the case in the Strom- bacea. It is equally plain, however, from the numerous examples described above that they have been lost in the style-bearing prosobranchs. The reason for this is not far to seek : if they secrete an amylase they are redundant in animals which have a st,vle ; if they secrete a proteolytic enzyme their activity is incompatible with the existence of a style. In both caam they are in consequence reduced, and disappear. The change in the structure of the oesophagus may take place in one of two ways. In most of the Risaoacm, the Strombaw, and the Paludomina? the original structure of the aeeophagu


is still clearly recognizable, with a ciliated dorsal food-channel and vestiges of the lateral and ventral glandular areas, provided with gland-cells not found in the food-channel, though it is clear that their function must have undergone a fundamental alteration. In others, like the remaining members of the family Tiaridae, Turritella, and, in particular, in the Calyptrsacea, the original structure of this part of the gut has been almost completely suppressed, and only in such forms as Turritella is there any trace of the former arrangement dis- cernible. This change, i t would appear, has been brought about in most cases by the abbreviation of the mid-esophageal region until the anterior esophagus passes more or less directly into the posterior. The mid-esophagus is the only part affected by the presence of the style ; the anterior and posterior regions, apart from an increase in length, are unaltered.

It thus appears that in the case of the herbivorous prosobranchs a style and a series of glandular esophageal pouches are alternative mechanisms, mutually inconsistent, for helping with the digestion of food, and this raises the question of what decides whether a given mollusc will have one or the other. Why do not the common vegetarian gastropods of the shore have a style ? This is bound up with the way in which the animal feeds and also with the habitat in which it dwells. Yonge’s second law lays down that all style-bearing molluscs are more or less continuous feeders, and if the habitats of all those prosobranchs which possess a style be examined, as Yonge has done in his list (1932), i t is found that all live in positions where this is a possibility-in fresh water or brackish water, or, if marine, low down on the beach like Rissoa, where the animal is exposed by the tide so little as not materially to affect the rate of feeding, or in places which lie in pools when the tide recedes like Pterocera ; or in deeper waters like Aporrhais, Turriklla, and Calyptrza ; or in the plai‘kton as in the case of the Pteropods. The style then is utilized by those which feed continuously by suitable mechanisms and live in a habitat where this can be carried on. It is significant to note in this connection the presence of the cscal extension of the stomach in Pma,tias and Cyclotopsis, the sole terrestrial genera with a style, which may act as a means of regulating the flow of food through the stomach. According to information kindly given to me by Dr. F. M. Haworth it is very doubtful if Yonge’s contention that Pomatias is a continuous and a subterranean feeder is correct. According to Miss Haworth Pomatias is just as much affected by external conditions such as light and, in particular, moisture as any other terrestrial snail, and, far from being an underground feeder, it comes to the surface to feed.

Diver ( in lit.) allows me to say that his experience of the behaviour of land mollusca both in nature and in vivaria is in complete agreement with Haworth’s observations. In land species feeding appears to take place only during periods of general movement controlled by the amount of moisture available. Though no doubt during its sub-surface activity soil is ingested in addition to the vegetable matter taken in during surface feeding, he considers it highly improbable that this snail could properly be described as a more or less continuous feeder. If this is the case, then the importance of the caecum 88 a regulator of the flow of food to the style cannot be exaggerated.

In contrast with a crystalline style it is the peculiarity of a gland that its secretion can be regulated and drawn upon as required by the evolution of an appropriate nervous or hormonic mechanism of control ; for this reason the esophageal pouches and not a style are to be found in those animals which have a rhythm in their feeding or to which meals come a t irregular and un- prd&d.de intervals. This will be the wee with all carnivores, and in such


herbivores as have, by reason of their feeding process, adopted a periodic mode of feeding, or, as is most frequently the case, have, by reason of their habitat, had an external rhythm imposed upon them. Amongst land-dwelling gastropods such as the pulmonates the activities of the animal are probably controlled by the day-night rhythm and the accompanying variations in tempera- tures and relative humidity, so that the molluscs feed perhaps during only one period every twenty-four hours : in this case a style is obviously inappro- priate, and, as Krijgsman (1925, 1928) has shown, the salivary glands, from which come most of the pulmonate's indubitable extracellular enzymes, show a definite secretory cycle. Amongst marine forms many have imposed upon them the rhythm of the tides, allowing them to feed during two periods every twenty-four hours, and necessitating quiescence between the two : such, too, possess glandular pouches, which, indeed, find their most characteristic expression in the common inter-tidal prosobranchs-in the Patellidae, Haliotidae, Trochids, and Lacunidae amongst herbivores, and in all the carnivores.

The possession of a style is also, but less intimately, bound up with the form in which a mollusc takes its food : it is pre-eminently the possession of microphagous forms feeding principally on unicellular or small multicellular algae, food which is easily collected by cilia or radula. The converse is not necessarily true. It does not follow that because an animal is microphagous that i t will have a style-as, for example, in Patella, which was found by Davis and Fleure (1903) and later by myself (1932) to feed on diatoms, but which has no style in the alimentary canal.

The distribution of the crystalline style amongst the prosobranchs has been dealt with by Robson (1922 h), who pointed out that it appears to have arisen in the gastropods wherever all the conditions necessary for its functioning have been fulfilled. This, however, does not appear to be the whole story : the style is not just scattered a t random through the prosobranch series, and genetic affinity is undoubtedly involved. If 'its distribution be considered it wil l be found (using the classification of Thiele (1925, 1931)) that the style is limited to a comparatively small number of the twenty-four superfamilies into which the subclass is divided. In the first place, since Diodora and Thealom prove not to have a style, that structure is a characteristically taenioglossate feature, not a primitive gastropod one. Amongst the mesogastropods, so far as is known at present, i t is confined to the superfamilies Architaenioglossa (Lavigeria only), Rissoacea (fourteen genera), Cerithiacea (seventeen genera), Calyptraeacea (three genera), and Strombacea (three genera). In connection with the Calyptraeacea it should be noted that Lebour's discovery (1937) that Capulus has an echinospira larva casts considerable doubt on its correct assignation to that group, and suggests that i t should belong to the Cypraeacea or to the Lamellariacea, both typically carnivorous groups with well-developed oesophageal pouches, of which it would be an aberrant sedentary vegetarian member. This would add a sixth superfamily to the above list. Thus, whilst Robson's contention that the style has arisen in the prosobranch series wherever conditions are suitable may be true, i t is apparently only in five or six groups, some of which, like the Calyptraeacea and the Strombacea, are admittedly closely related, that this has actually taken place, and of these none is really primitive. The simplest explanation of this is, perhaps, that only in these superfamilies have all the necessary conditions for the development of the style arisen, but the fact that numerous families within the limita of a single group possess i t must be due to a real relationship existing between them, and suggests that there may be a closer degree of affinity between all

108 MB. -STAIR GRAHABl ON THE ALIMENTLLRY

the superfamilies in which a style occurs than is usually suspected. The position of Lavigeria, which has already been discussed by Moore (1899 c), aa the sole member of its superfamily with a style, makes one wonder whether its systematic position has been correctly diagnosed and whether it would not be better retained nearer the Tiaride. The fact that the style appears to be characteristic of the higher rather than of the lower prosobranchs would suggest that it had been evolved in gastropods independently of the lamellibranchs, that i t itself is not an inheritance from a common ancestor, and emphasizes Robson’s second point, that it is not the style which has been inherited but the potency to produce one when desired. Just how far the power has been invoked among the superfamilies in which the style is known to occur awaits fuller investigation-it seems improbable that anything like a complete list of animals with a style is known ; thus, for example, the observations of Haller (1892) and of Kleinsteuber (1913) make it almost certain that the other members of the family Calyptreidae-Trochita, Crucibulum, Ergaa, Janacus-also possess a style.

In connection with the evolution of the style i t is interesting to note that the conditions found in the Archsogastropoda, especially in Diodora and Theodozus, are almost exactly parallel with those found by Yonge (1939) in the Protobranchia. In both groups the stomach appears to be concerned in its morphologically anterior portion with the breaking up and sorting out of the food particlee entering it, and in its morphologically posterior part with the elaboration of a mucous rod from which the fecal pellets will ultimately be feshioned. If this rod can be regarded as a precursor of the true style found in the higher lamellibranchs and prosobranchs it is clear that its evolution has been closely parallel in these two great molluscan groups.

The only point which calls for emphasis in the course of the alimentary canal is the structure of the stomachs which have been described in this paper and, in the case of Turritella, in a previous one (Graham, 1938). In most carnivorous gastropods, and in those herbivores in which digestion is predomin- antly extracellular, the stomach has a comparatively simple structure. In those with styles, on the other hand, the stomach becomes an important part of the alimentary tract, where the food particles are mixed with style substance, where those which can be manipulated by the cells of the digestive diverticula are separated from those which cannot, and where the indigestible matter from the diverticula is directed away from incoming food and passed into the intestine for defecation. As the animals are more or less continuous feeders all these processes must be capable of going on simultaneously, a fact which has trans- formed the stomach into a complex ciliated structure upon the successful functioning of which that of the rest of the alimentary canal depends. By referring to the figures and descriptions given above it will be seen that in all, especially in the mesogastropods, the broad outlines of their structure and of the ciliary currents on their walls coincide. The style probably, as various writers have noted in other cases, assists in the paasage of food through the stomach. At some point on the wall near the base of the intestine is an area which sorts particlea on a basis of size, the larger ones being passed directly into the intestine aa not adapted for ingestion by the cells of the digestive diverticula, the smaller ones being passed into the ducts of the digestive diverticula, although the details of this are not usually decipherable. The sorting area may be in the proximal part of the intestine (Bithynia, Pomatim) and/or in a crescent-shaped groove lying on the dorsal wall (Rithynia, Pomatias, Turritellu, Crepidulu, Calyptrzza). This appears to be homologous with the spiral cecum which is

CANAL OF STYLAE-BEARING PROSOBRANCHS. 109

found in connection with the stomach of many of the archaeogastropods (rhipidoglossa), where its exact function is still a matter of doubt.

The close resemblance which exists between the stomachs of all these style- bearing gastropods extends to the other portions of the alimentary tract. The primary function of these is the conduction of food from mouth to stomach, and again from stomach to anus, a simplicity of function which is mirrored in a simplicity of structure. Glands are reduced to lubricating cells in the former situation, and to these and others necessary for the formation of faecal m w e s in the latter. With this simplification of structure in the anterior and posterior halves of the alimentary canal, and in the complexity encountered in the stomach, which is acting as a general clearing house, the gut comes to bear a close likeness to the type found in the lamellibranchs. This is due to convergence, a morphological reflection of the fact that the presence of a crystalline style implies a given set of pre-existent physiological conditions.

SUMMARY.

In the primitive prosobranch mollusc the esophagus may be divided into

(1) Anterior a?sophagus.--lying immediately behind the point where the radula sac separates from the gut. Histologically i t resembles the buccal cavity. On its roof runs a pair of folds enclosing a g r o o v e the ciliated dorsal food-channel.

This part bears lateral glandular pouches in which digestive enzymes are secreted, and has a continuation of the dorsal food-channel on its roof in which food and mucus from the anterior esophagus is mixed with the secretion of the pouches and the mixture carried back. This region is involved in the torsion of the visceral mass.

This has no glandular pouches ; its wall bears numerous longitudinal folds, and i t carries the mixture from the food-channel to the stomach.

Tha structure of this region of the alimentary canal has been examined in eighteen genera of prosobranch gastropods in which a crystalline style in- dubitably occurs, and compared with t,he published descriptions of twenty other genera and with the thecasomatous Pteropods. In all cases (with the single exception of Ackorhi8) the pouches have lost their original secreting epithelium, and have been reduced in size or have completely disappeared. In the Rissoacea (text-fig. 6), Strombacea, and Paludominae, the original crop- like expansion of the gut persists ; in more fully adapted molluscs-Cerithiama (test-fig. 7), Calyptraacea-a11 trace of expansion has disappeared, and the anterior esophagus appears to pass directly into the posterior. In Crepeilula no torsion of the alimentary canal is visible.

The structure and the ciliary currents of the stomachs of seven animals is described and shown to be very similar (text-figs. 6,6,9,10). In all provision is made for (1) the mixing of food particles with the style substance ; (2) the sorting of small particles which can be ingested by.the cells of the digestive diverticula from larger ones which cannot ; (3) the removal of the latter and of waste from the digestive diverticula into the intestine ; (4) the rotation and paasage into the stomach of the crystalline style.

three regions :-

(2) Mid-mophagus.-Lying behind the anterior esophagus.

(3) Posterior @sophagus.-Lying behind the mid-esophagus.

110 MR. ALASTAIR ORAHABI ON TRE ALIMENTARY

The reason for the loss of the cesophageal pouches is bound up with those characteristics of style-bearing animals first expressed by Yonge (1930, 1932) : (1) that no free protease can exist in their gut, and (2) that they are continuous feeders. Prosobranchs which live in habitats where continuous feedii .; is possible can have a style ; those which, like littoral or terrestrial forms, have a rhythm in their feeding, or which, like carnivores, require a free protease in their gut, have cesophageal pouches.

The style appears to be found in only one archsogastropod and in only six superfamilies of mesogastropods, some of which are closely allied. This suggests that i t has been evolved independently in the gastropods and the lamellibranchs, and that the ability to produce it is limited among the gastropods to a few stocks, probably inter-related, within that group.

No style occura’ in Diodora, Theodom, Septaria, Ampullarim or Pila, genera in which it was once thought to be found. Diodora feeds on sponges.

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