Feeding processes of members of the genus Macoma (Mollusca:Bivalvia)

ROBERT G. B. &ID AND ALISON REID Department of Biology, University of Victoria, Victoria, British Columbia

Received October 23, 1968

REID, R. G. B. and REID, A. 1969. Feeding processes of members of the genus Macoma (Molluscs: Bivalvia). Can. J. Zool. 47: 649-657.

The eight species of Mamma examined fall into ihree feeding categoria: two are deposit feeders, five are suspension feeders. and onc rccds on the surface films of bacteria on sand grains. The type of particle which is found in thc stomach depend? on the behav~or of the siphons, the quality or quant~ty of mucus secreted by the gills and Iabial palps. and, to some extent, on hes sorting function of the labial palps. The labial palps ~ c t as supplemen tar? filtering mechanisms. The stomach of M. sccm, which ingests sand grains, 1s adapted to thiq diet bv the enlargement of the gastric shield. but in the other specres there is no obvious relationship bttwcen diet and stomach morphology.

Introduction The genus Macoma has 13 northeast Pacific

species, including the recently established Ma- coma elimata (Dunnill and Coan 1968). As a possible taxonomic criterion, the esterase zymo- grams of eight species of the genus have been examined by Reid and Dunnill (1969) and that study brought to light several interesting, in- cidental factors. It was found that there were specific differences in the amount of extracellular esterolysis, and that there were specific dif- ferences in diet.

That these animals differed in what they ate, and how they digested it, suggested a partial solution to an ecological curiosity concerning the benthic members of the genus. This was that as many as eight species could be taken in a single 0.1 m2 Van Veen grab sample (Dunnill and Ellis 1968). Was each species occupying a distinct ecological niche, or were they co- existing in ignorance of Gause's principle?

The observations on diet raised the problem of how the different types of food were obtained. There were several possible answers. Firstly, the siphons might function differently, sweeping the bottom deposits or inhaling suspended material. Yonge (1949) described the Tellinacea as deposit feeders on the whole, but Braefield and Newel1 (1961) demonstrated that Macoma balthica can be both a deposit feeder and a sus- pension feeder. Alternatively, the sorting mech- anisms of ,the mantle cavity might be respon- sible for the ingestion of different types of food. Accordingly, feeding behavior and the mor- phology, histology, and sorting mechanisms of the pallial organs were studied.

A third section of the work deals with the stomachs of the animals. The bivalve stomach

is a complex structure concerned with the re- jection of dense inorganic particles, and the retention of potential food material until it is partly digested, or rendered into a finely divided suspended form suitable for assimilation by the tubule cells of the digestive diverticula (Reid 1965). The fate of ingested material depends upon the sorting mechanisms of the stomach, and so observations on the functional morphology of the stomachs of the species under study were deemed relevant to the present work. Previous observations on the stomach of the genus have been sparse, partly because Macoma balthica (Yonge 1949) is the only readily available European species, and partly because of the disarray of the taxonomy of the Pacific species before the production of a key by Dunnill(1968). However, the work of Yonge (1949) and Pur- chon (1960) on related genera is useful, and rel- evant.

While the stomach of Macoma secta was under study it emerged that the sand-grain epiflora might be signscant, and so the work was extended to include an examination of this bacterial component of the diet, as well as further general observations on stomach con- tents.

Materials and Methods Eight species are included in the present survey: the

littoral species Macoma nasuta (Conrad), Macoma secta (Conrad), Macoma inquinata (Deshayes), and the benthic species Macoma brota (Dall), Macoma calcarea (Gmelin), Maroma elimata (Dunnill and Coan), Macoma incongrua (von Martens), and Macoma lipara (Dall).

M. secra and M. nasuta were obtained at low water neap level from Mount Douglas beach, Victoria; the former from a depth of 15 to 50 cm, the latter from 10 to 15 cm, in clean sand. M. inquinata was found at a depth of 10 cm in silty gravel on the seaward side of

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650 CANADIAN JOURNAL OF ZOOLOGY. VOL. 47. 1969

Esquimalt Lagoon, Victoria. The five benthic species were obtained by dredging at a depth of 40 m off Moresby Island, at the mouth of Satellite Channel, S.E. Vancouver Island, where they occur in silt.

Substrate samples were obtained from each locality. To observe siphon orientation and behavior in burrowed animals, six individuals of each species were placed in the appropriate substrate, in containers submerged in an aquarium table, and seawater was slowly circulated over the table. The siphon activity was observed several times a day over 3 weeks. Eventually specimens were dug up to discover the position which the animals had assumed.

The movement of fluid and particles in the mantle cavity was observed by removing the left valve and mantle lobe and introducing carmine suspension, or line (20 p) or coarse (120 p) carborundum particles.

Histological examination of the labial palps and gills was made after fixation in Gilson's and embedding in paraplast. Sections were cut at 6 p. For demonstration of general microanatomy, sections were stained with Heidenhain's iron haematoxylin and orange G, and to show the distribution of mucous cells other sections were treated with Alcian blue (Steedman 1950) and orange G.

The stomach form of each species was elucidated by opening the visceral mass from the left side. Dissection from this side interferes little with the internal structures of the stomach. Fine and coarse carborundum particles were used in the study of general ciliation and sorting mechanisms in the stomach.

To establish the diet the stomach contents of several individuals of each species were examined microscopical- ly within a few hours of collection. This was done in May and again in August, 1968. The importance of bacterial colonies on sand grains was investigated by plating out sand grains from the top 2 mm at Mount Douglas beach on 1.5% seawater agar, with 1 % glucose. The sand grains were first washed four times in sterile seawater, then were pipetted on to a pad of sterile filter paper, with care being taken todisperse the grains as much as possible. After excess water was absorbed, the filter paper was pressed against the surface of the plated agar, and then peeled off, leaving the sand grains dispersed on the gel. The plates were examined after 24 hours. To compare the sand grain flora before and after exposure to the alimentary processes, sand grains from the rejection tracts of the stomach of M. secta were also plated out, in the same way.

Results

Siphon Behavior A11 species were able to burrow when placed

on the appropriate substrate, the two largest species M. secta and M. nasuta being less skessful than the others, having a failure rate of 50%.

M. brota-This species, as do all the species examined, with the exception of M. inquinata, lies on its left valve. The siphons are held vertically in a small, conical depression, and

usually lie flush with the surface of the silt, or a few millimeters above it. On three occasions the protrusion of the siphons above the surface extended to 2 cm, the siphons bending over slightly. On several occasions the inhalant siphon was seen to rotate within the depression, dislodging small amounts of surface material which were drawn in to the siphon.

M. calcarea-The inhalant siphon of this species commonly lies extended on the surface to a length of up to 3 cm, but was also seen in a vertical position. The open mouth of the siphon was seen to touch the surface of the substrate, drawing in particulate material.

M. elimata, M. incongrua, M. inquinata- These were almost invariably seen with the inhalant siphon held vertically, extended to lengths of 1.5 cm, 2 cm, and 2.5 cm respectively. M. inquinata apparently burrows with the antero- posterior axis vertical.

M. secta-This species exhibits the type of behavior described by Yonge (1949) as typical of deposit-feeding Tellinidae, in that the very long inhalant siphon lies on the substrate while the exhalant remains just level with it. The in- halant siphon moves around continuously, and periodically its aperture is pressed down on to the sand, and small amounts of surface matter are drawn in.

FIG. 1 . Macoma lipara, left valve and mantle lobe removed to show the organs of the mantle cavity. AA, anterior adductor muscle; C, cruciform muscle; ES, exhalant siphon; F, foot; G, "food groove" of gill; ID, inner demibranch; IS, inhalant siphon,; LP, labial palp; M, mouth; MF, mantle fold; ML, nght mantle lobe; OD, outer demibranch; PA, posterior adductor muscle; RV, right valve; V, visceral mass.

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FIG. 2. (a) Transverse section of the ridges of the labial palp of Macoma secta. Dark-staining portions at the bases of the ridges are mucus cells, stained with Alcian blue. (b) Transverse section of the labial palp food groove of Macoma inquinata. Mucus cells are densely stained with Alcian blue. (c) Transverse section of the gill of Macoma lipam. Mucus cells are darkly stained with Alcian blue.

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REID AND REID: FEEDING PROCESSES OF MACOMA 651

M. lipara-This species is usually seen with the inhalant siphon extended up to 3 cm and lying on the surface. The behavior described above for M. secta was seen once; the rotating of the end of the siphon within a depression was also noted once.

M. naruta-The inhalant siphon is held semivertically to a length of about 3 cm.

Ciliary Mechanisms in the Mantle Cavity The overall pattern of particle movement in the

mantle cavity was identical for each of the eight species and resembles that figured and described by Kellogg (1915) for M. secta and by Yonge (1949) for M. balthica. M. lipara is illustrated as a typical example (Fig. 1). Note that the gill is of the reflected type (Atkins 1937a; Yonge 1949), which is common to the Tellinidae, and thus there is no free collecting surface on the outer face of the outer dernibranch.

In all species, material passes from the in- halant siphon to the gill, where certain particles are bound together into mucous strings and pass anteroventrally along the filaments to the mar- ginal "groove", along which they are carried anterodorsally to the palps. Atkins (1937b) assumed that a food groove occurred in the Tellinacea. Yonge (1949) has stated that M. balthica and other Tellinidae lack a true food groove on the ventral margin of the inner demi- branch, there being only a flattening. Longi- tudinal sections of the gill filaments of the eight species show that there is no true food groove. But the ventral margin bears a ciliated notch up to 50 p deep, whose cilia probably aid in passing the mucous strings anteriorly. Large dense particles, which fail to cohere to the mucous strings, are rejected off the ventral margin of the inner demibranch. When the mantle is intact, waste currents (Kellogg 1915) carry the rejected material to the '*pocket" ventral to the mantle fold, which partially separates the internal openings of the siphons, and there farms part of the pseudofaeces. Material arriving at the palps in the form of mucous strings is carried ventrally toward the mouth in the food groove between the two palps. Masses of mucus-bound material may break away from the food strings at the posterior or at the anterior ends of the labial palp food groove. Such material is carried ventrally along the unridged margins of the palps and rejected

at the tip. Particles which are introduced on to the ridged inner faces of the palps may be carried anterodorsally at right angles to the ridges, by the cilia on the crests of the ridges, to the food groove. Between the palp ridges there are two ciliated grooves (Fig. 2a), one deep groove and one formed by an aboral shelf. Particles which enter either of these grooves are carried posterodorsally. These grooves terminate in the food groove in the anterior half of the palp, and at the posterior margin in the posterior half of the palp. The general microanatomy of the palp ridges is similar in all the species; in the anterior portion of the palps the aboral shelves are small and the grooves narrow; in the posterior portion of the palp the aboral shelves are large and the grooves wide. In general, particles which enter the grooves in the posterior region of the palp are rejected, and those which enter the grooves in the anterior region are accepted. M. secta is exceptional in that it accepts large, dense par- ticles in large quantities into the food groove.

Despite the uniformity of the pattern of the ciliary tracts the eight species differ considerably in the size and density of the particles which they accept or reject. M. secta is the most catholic and will form mucous strings with sand grains, coarse and fine carborundum, and carmine. As pointed out by Kellogg (1915) the digestive system of this species is usually full of sand. None of the other species is capable of forming mucous strings with sand; M. inquinata alone is capable of accepting even small quantities of coarse carborundum. All species form mucous strings from carmine suspension, and M. nasuta, M. inquinata, and M. elirnata can also form clumps with fine carborundum and thus transfer is from the gills to the palp food groove. M. calcarea accepts only the finest carmine particles and rejects larger particles of even this light material.

That there should be such differences in par- ticle seIection, despite the similarity of the ciliary tracts, indicated that differences in the quantity or quality of mucus secreted by the gilts and labial palps might occur. In our investigation of the distribution of mucus cells we found that the labial palp food grooves of all the species were well supplied with mucus cells (Fig. 2b). This was also true of the unridged margins of the palps. In the ridged regions of the palps only

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652 CANADIAN JOURNAL OF ZOOLOGY. VOL. 47. 1969

M. secta (Fig. 2a) and M. calcarea showed promi- nent mucus cells. But since these two speciesareat opposite extremes in particle selection, such a datum was of little value to the hypothesis that amounts of mucus secretion might be respon- sible for specific differences in selection. More- over, the distribution of mucus cells in the gills (Fig. 2c) seemed identical in each species.

Diet Observations on diet largely confirm those

of Reid and Dunnill (1969). M. lipara-Mainly portions of diatom frustule

smaller than 20 p; small diatoms including Fragilaria; many small flagellates smaller than 10 p.

M. brota-Similar to M. lipara; relatively more diatoms.

M. calcarea-A few small diatoms smaller than 20 p; many flagellates; many small silt particles and organic debris smaller than 10 p.

M. elimata-Diatoms the most numerous organism, chains of Melosira up to 100 p long, solitary diatoms up to 45 p; many flagellates.

FIG. 3, Stomach of M w m a secru, opcnd from the left side. A, anterodorwl tmct; DC, duct caecum; G . gastric shield; H, dorsal hood; I, intestenal groove; LP, left pouch; 0, opening of the oesophagus; P, posterior "sorting area"; PC, groove or the posterior sorting arm: RG, rejecary groove; SS, stylc sac; T, major typhlo~ole,; r , mmor typhlosole; V, ventral lip of oesoph- a y s opening.

M. incongrua-Similar to M. elimata; some solitary diatoms, Coscinodiscus, up to 125 p.

M. inquinata-Mainly diatoms, average size 50 p; some flagellates.

M. nmuta-Sim,ilar to M. inquinata. M. secta-Many sand grains, average size

300 p, together with relatively small numbers of diatoms similar to those found in M. nasuta from the same habitat; some naked flagellates.

The sand grain plating experiment was performed twice, with similar results each time. Within 24 h, at room temperature, the surface sand-grains from the beach were each surrounded by a colony of bacteria whose diameter was three times larger than the diameter of the sand grains. The sand grains taken from the posterior sorting area of the stomach of M. secta also developed colonies, but these were only half the size of the "undigested" sand grain colonies.

Stomach Functional Morphology Macoma possesses a type V stomach (gastro-

pemptan), in which the major typhlosole extends two flaps in the caeca containing the openings of the ducts of the digestive diverticula (Purchon 1960). The features common to the eight species examined and which are distinctive are these: (a) the posterior sorting area has little sorting function, and is much simpler than that of most other bivalves, (b) there is a rejectory groove which begins at the tip of the dorsal hood and which joins the intestinal groove at the opening of the right duct caecum.

M. secta (Fig. 3) has the most distinctive stomach. Its most prominent feature is a very large gastric shield (G) which lines a capacious, hemispherical concavity, lying on the left of the stomach in a posterior position. This region receives the head of the crystalline style and contains a large quantity of sand grains. The posterior sorting area (P) forms a pouch and its thick walls are ridged and grooved. A shallow groove whose cilia beat towards the dorsal hood (H) extends from the posterior sorting area into the dorsal hood. In the hood region all the cilia beat towards the tip of the hood, save those in the rejectory groove (RG), whose cilia beat towards the intestinal groove (I). The intestinal groove, which follows the distal edge of the flaps of the major typhlosole (T) broadens posteriorly, providing a large rejectory tract. The left pouch (LP) is a pocket underlying the

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REID AND REID: FEEDING PROCESSES OF MACOMA 653

gastric shield, and it contains four small em- bayments into which a number of divesticular ducts open, Frequently, when the stomach of a freshly collected animal is opened, strands of mucus-bound organic matter, containing rel- atively few sand grains, are found stretching from the dorsal hood and from the left pouch to the head of the crystalline style. The portion of the crystalline style within the stomach is much thinner than the portion within the style sac, and this is presumably caused by the ab- rasion of the many large sand grains contained in the posterior embayment of the stomach. At the openings of the oesophagus (0) there is a ventral Iip which projects our over the openings of the duct caeca (DC). The stomachs of the other seven species

examined are sufficiently similar for a single general description to sufice. The major dserences between these seven and M. secra are firstly, the possession of an appendix, which Yonge (1949) called a "postero-dorsal caecum," and secondly, the extent of the gastric shield; the shield is not so extensive as in M. secta.

FTG. 4. Stomach of Momma liparn, opencd from the left side. A, anterodorsal tract; DC, dudt caecum; G, gastric shield; H, dor.wl hood; T, intestinal groove; LP, lcft pouch; 0, opening of oesophagus; P, posterior sorting area goow; RG, lejcftory groove; SI, sccond;lry intestinal groove; SS, style sac; ST, shield tract: 'T. major typhlosole; t, rnlnor typhlosole; X, appendix; XO, opening of app~ndlx.

In the illustration of the stomach of M. lipara (Fig. 4) the position of the appendix (X) can be seen. This is an unciliated elastic sac which is sometimes packed with sand grains, but is sometimes empty, even in freshly collected animals.

The form of the posterior sorting area is simpler in M. lipara and the other species than in M. secta, having no ridged and grooved area. Another difference i s a secondary intestinal pave (SI) in the region of the posterior sorting area which leads directly to the intestinal groove. The secondary intestinal groove is also present in M. elimata and M. incongrun but is absent from M. nmra, M. brora, M. calcarea, and M. inquinata.

M. lipara, like M. brota and M. inquinata, has a distinctly grooved shield tract (S), but this tract has no sorting function.

The ciliary beat and hence the circulation of material in all of the species examined is es- sentially the same.

Discussion

Siphon Behavior From our laboratory observations on siphons,

it seems that M. secta, M. lipara, and M. cab carea are the only clear-cut deposit feeders. Each of these species was seen with the siphons at times lying on the surface inhaling, and at such times could be taking suspended material into the mantle cavity, but more typically the siphons of these animals moved around on the surface, sucking up masses of the surface par- ticles. M. elinrara, M. inqwinaia, M. nasuta, and M. incongrua never allowed the siphon open- ing to come into contact with the substrate, and held their inhalant siphons vertically, or semi- vertically. From this evidence alone these animals might be judged suspension feeders. M. brota also tended to spend most of the time suspension feeding, but was also observed to take in finely divided deposit material. The interruption of siphon activity for long periods probably allows the sorting mechanisms of the mantle and stomach to function without clogging with excess material.

Mantle Ciliary Mechanisms In general there is a marked difference be-

tween M. secta, which is not selective with respect to the particulate material which is

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659 CANADIAN JOURNAL OF ZOOLOGY. VOL. 47. 1969

subjected to mantle processing, and the other seven snecies studied, and there are minor diEerences among these latter seven species. The differences are not, however, reflected in any gross or even in any microanatomical differences. In M. secta large dense particles are bound together into mucus strings on the gills, and there is little rejection of material from the gills. In the other species the mucous strings are less cohesive, and large dense particles tend to become detached at the edges of the gills and labial palps, to become pseudofaeces. It was demonstrated that the differences in the cohesiveness of the mucous strings could not be explained in terms of the relative numbers of mucus cells in the labial palps and gills. The possibilities remain that relative rates of mucus secretion differ, or that the physical properties of the mucus differ among the species. Un- fortunately the investigation of these two pos- sibilities is beyond the scope of the present study.

Two anatomical features of the mantle cavity are of general interest, the relatively small reflected gills, and the large labial palps. The muscularity of the labial palps, which makes them curl up when the mantle lobes are re- moved, suggests that in their normal state they are pressed apart, providing a channel though which passes an anteriorly directed current created by the cilia on the crests of the palp ridges. Tltis water movement must contribute significantly to the inhalant stream. Alsa, the palps must act as a filtering device just as im- portant as the gills, considering their large surface area. Thus in this genus, and possibly

FIG. 5. Generalized mantle cavity of Macorna showing ciliary currents (whole arrows) and countercurrents (broken arrows). C, ctendium; ES, exhalant siphon; IS, Inhalant siphon; LP, labial palp; MF, mantle fold.

in other members of the Tellinidae, the labial palps are important filtering organs. The usual explanation that the function of the palps is to sort further the material selected by the gills is unsatisfactory. Particles selected by the @Is are mucus-bound by the time they reach the palp food groove, and the onIy possibility of their coming under the influence of the sorting mechanisms of the ridges is if they accumulate excessively, whereupon they are rejected, not sorted.

Since the gills are reflected, the exhalant chamber is smaller than in other bivalves, thus the overall circulation in the mantle cavity must differ from the classical inhalantlexhalant pat- tern. The cilia which move the mantle water are dorsally situated, on the gills and labial palps, and proximal to the visceral mass. The comple- mentary countercurrents are presumably distal and ventral. If so, an obvious function of the mantle folds (Fig. 1) which lie between the bases of the siphons is to channel the distal, pos- teriorly directed countercurrents towards the exhalant siphon. This hypothetical circulatory pattern is shown in Fig. 5.

Diet The stomach contents of the members of the

genus Macoma reflect the activity of the siphons and mantle cavity. There are three main groups: firstly, the fine deposit feeders which include M. calcarea and M. lipara; the average size of particles in their stomachs was less than I0 p and nutrients must be obtained from bacteria, flagellates, small dinoflagellates and diatoms, and detritus particles. The second group includes the suspension feeders M. nasuta, M. inquinata, M. elimata, and M. incongrua. These derive most of their nutrients from flagellates and diatoms. M. brota falls between the two groups, but according to our observations spends more time as suspension feeder. M. secta is the sole member of the third group. Most of its nutrients must come from microbial colonies on the large sand grains which it ingests. Meadows and Anderson (1968) have shown that colonies of microorganisms tend to occur in depressions on sand grains, rather than forming a complete film. These authors imply, however, that the less exposed a beach is, the more extensive will be the colonies on the surface of the sand grains. In any case the abrasion to

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REID AND REID: FEEDING PROCESSES OF MACOMA 655

which sand grains are exposed in the stomach of M. secta is much more vigorous than that which would normally occur on sheltered Mount Douglas beach, and the freeing of colonies in depressions is probably assisted by the gastric enzymes. AIong with the sand grains it takes in settled diatoms and flagellates. These are abraded along with the sand grains, so that the stomach fluid contains few particles larger than 50 p. The importance of bacterial f lms in the diet of deposit feeders has already been stressed by Newel1 (1965), who concluded that the large surface area of fine deposit particles must support a microflora which has more nutritive importance than the deposit particles themselves, Although the surface area of the sand grains ingested by M. secta is proportionately smalIer than that of fine deposit particles, the sand grains must support a microflora of suficiently high nutritive value for the species to have undergone marked adaptations in its particle selection and in its functiona1 morphology.

Stomach Functional Morphology In its gastric morphological features M. secta

is again the outstanding species. Its main features are adaptations to the diet of sand

FIG. 6. Generalized stomach of Mhcoma sectn showing ciliary currents (whole arrows) and countwcurrents Ibrokm arrows). CS, crystalline style; DC, duct caecum; H, dorsal hood; I, intestinal groove; LP, left pouch; .O, opening of oesophagus; S, sand; SS, style sac; T, major typhlosole.

grains. These include the large gastric shield embayment and the lip at the oesophagus open- ing which shields the duct caeca. The species had lost the appendix, which seems to be an archaic structure.

The mode of functioning of the intact stomach can only be deduced by envisaging the -int&r- relationships of structures and tracts, which were examined individually in two-dimensional display. Our deduction is as follows. Masses of mucus-bound sand grains together with their epiflora, detrital particles, and small diatoms enter the stomach and pass directly from the oesophagus to the shield embayment, and there they are ground together by the revolving of the style. It is unlikely that the style exerts any direct abrasive effect by rt~bbing the sand grains against the gastric shield. The function of the shield is to protect the stomach epithelia from abrasion. The grinding-together of the sand grains frees the bacterial films, which pass into suspension in the gastric juice, and there must also be some breaking-down of detrital particles and diatoms. As the amount of material in the shield embayment is added to from the oesoph- agus there is overspill into the region of the posterior sorting area. Small light particles go into suspension and are circulated throughout the stomach (Fig. 6). Dense sand grains and masses of lighter material which impinge against the stomach wall are carried into the dorsal hood. The dorsal hood has a type B sorting function (Reid 1965) and is thus analogous to the sorting caecum of the type I11 (gastrotriteian) stomach. Dense particles can enter the re- jectory groove and leave the stomach via the intestinal groove. Larger masses of material cannot normally fit the rejectory groove and are retained. Presumably when such lighter material has accumulated in the dorsal hood, it once more comes under the iduence of the rotating tip of the crystalline style, and goes through the whole cycle once more. Fine particles in suspension un- dergo partial digstion and finally enter the duct caeca or the left pouch, to enter the ducts of the digestive diverticula and be phagocytosed.

Not all of the material ingested necessarily passes through the cycle described above. As noted, the intestinal groove is broad posteriorly and must siphon off some unprocessed material, particularly when the stomach is full. Also, spontaneous muscular activity was observed in

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656 CANADIAN JOURNAL OF ZOOLOGY. VOL. 47. 1969

the right wall of the stomach, suggesting that the rejectory grooves can be expanded mus- cularly. The ciliation of the other species exam- ined is similar to that of M. secta, and so the general circulation of material in their stomachs must also be similar. All the animals except M. secta possess an appendix. Observations and hypotheses concerning this organ are reviewed by Reid (1965). In Lima hians the apparent function of the appendix is to act as a store for unusually large particles which the stomach normally has no means of rejecting and which would impede function if retained in the main lumen. A ciliary tract exists to transport such particles into the appendix. However, in Macoma the function of the appendix is enigmatic, since the cilia of the anterodorsal tract (A), adjacent to the appendix, beat away from the appendix mouth. Yonge's explanation that the appendix acts as a safety valve to take excess material which might impede normal stomach function is the one which seems most relevant to Macoma.

Among the species which possess the appendix there are no differences in structure or function which seem to relate to differences in diet.

General Conclusions The grouping of the eight species of Macoma

under discussion into three feeding types is j u s ~ e d by the observations on siphon behavior, mantle selection, stomach morphology, and stomach contents. Thus on the basis of feeding processes there are three niches which members of the genus can occupy. However, this still does not solve the ecological question raised by Dunnill and Ellis (1968) concerning the large number of species of this genus which can be found in one place. The question might rather be rephrased: in the benthos there are two feeding niches, one for deposit feeders and one for suspension feeders; why should two species of the same genus occupy the former, and three species of the same genus occupy the latter?

Different types of diet are likely to have given rise to different modes of digestion. In a survey of suspension-feeding bivalves, Reid (1968) pro- posed that a general evolutionary trend in such animals is towards an increase in the amount of extracellular digestion, and that this is advan- tageous because it allows a speeding-up of the

digestive process, and reduces the volume of cells devoted to intracellular digestion. Owen (1956) quggested that extracellular digestion is of particular advantage to non-selective deposit feeders such as the nuculids, since much of the ingested material is inorganic. Owen argued that it would be inefficient and possibly harmful for the digestive cells to assimilate such material. It has been demonstrated by Reid and Dunnill (1968) that there is as much extracellular estero- lysis in M. secta as there is intracellular. Among the other species less distinctive differences occur in esterase distribution. Currently a quantitative study of the distribution of pro- teolytic enzymes in Macoma is underway. It may be that the genus will provide in microcosm, answers to questions concerning the intracellular and extracellular distribution of enzymes, which are relevant to other invertebrate groups.

Acknowledgments This work was supported by a grant of the

National Research Council of Canada to R. G. B. Reid.

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