Studies on the physiology of the giant clam Tridacna gig as linné—I. Feeding and digestion

Camp. Biochem. Phwiol. Printed in Great Britain

Vol.

78A, No.

I. pp. 95-101, 1984

0300.9629/84

53.00 f0.00

CC 1984 Pergamon Press Ltd

STUDIES ON THE PHYSIOLOGY OF THE GIANT CLAM TRIDACNA GIGAS LINNk-I. FEEDING AND DIGESTION R. G. B. REID, P. V. FANKBONER* and Department *Department

of Biology, of Biological

D. G. BRAND

University

of Victoria, Victoria, British Columbia, Canada V8W 2Y2. Telephone: (604) 477-6911 Sciences, Simon Fraser University, Burnaby, British Columbia, Canada (Receiurd 2 August 1983)

Abstract-l. The feeding behaviour of the giant clam Tridacna gigas has a marked circadian rhythm, which cues a gastric digestive rhythm. 2. Intracellular protein and starch digestion do not exhibit a digestive cycle corresponding to the feeding cycle. 3. The histoenzymatic condition of the digestive diverticula is heterogeneous at all stages of the feeding cycle. 4. The gut is of typical bivalve proportions in relation to the visceral mass. The retention of an effective digestive system in an organism which depends also upon symbiotic zooxanthellae indicates the nutritional opportunism of the species.

gested that these cells had been extruded from heatstressed corals and then filtered from the sea water by the normal feeding process. C. M. Yonge’s comment on these observations, that here was a possible source for the initial infection of young giant clams by the symbiotic algae (Yonge, personal communication) has been supported by the observations of Fitt and Trench (1981). However, Trench et al. (1981) have found undigested zooxanthellae in the gut and faeces of tridacnids maintained in aquaria with filtered sea water, and have inferred that the “reverse digestion” transfer from the blood, through the digestive diverticula to the gut. is the most likely mechanism. Emphasis on the investigation of the nutritional economy of symbiosis in giant clams has resulted in a relative neglect of their digestive physiology. Mansour (1946) proposed that giant clams received a substantial quantity of fragmentary and whole zooplanktonic material in their diet, but Mansour-Bek’s study of the enzymology of T. elongata did not support the hypothesis of a semi-carnivorous habit (Mansour-Bek, 1948). Fankboner (1971b) has studied the ultrastructure of the digestive diverticula of T. gigus and Morton (1978) has studied the cytology of the digestive cycle in T. crocea; both of these authors made inferences about the digestive process. T. crocea showed a marked diurnal cycle, reducing its feeding and phasic valve adduction at night. Given the opportunity to study T. gigus we were interested in discovering if this species showed a similar digestive cycle and, if so, in characterising its cytological and enzymological phases, while at the same time providing a general description of the physiology of the digestive system.

INTRODUCTION Tridacna gz’gm LinnC is the largest bivalve mollusc. attaining lengths of 1.37 m in some specimens (Rosewater, 1965). This large animal is sustained in a low-nutrient tropical reef environment by a symbiotic

association with unicellular algae which reside in the blood spaces of the expanded siphonal and mantle edge tissues. The nature of the nutritional association has attracted the attention of many investigators, and one of the aspects of this problem is the extent to which the zooxanthellae might be holozoically harvested and digested by the bivalve. Yonge (1936) and Mansour (1946) discovered zooxanthellae in the guts and faeces of tridacnids. Mansour studying Triducna elongata, proposed that an anatomical duct directed a flow of blood containing zooxanthellae to the alimentary tract, but Yonge suspected that the presence of gut zooxanthellae was an artifact. Morton (1978) studying Tridacna crocea observed large numbers of zooxanthellae in the diverticular blood spaces in specimens sampled at night, and proposed that these algal cells, carried by amoebocytes, were taken through the basement membranes of the digestive tubule cells and discharged into the digestive tubules, whence they passed into the gut and were voided as faeces. He also agreed with Fankboner’s earlier obthat amoebocytes transported zooservation xanthellae to the kidney and that this was an important route for the excretion of unusable residues from the symbiotic algae (Fankboner, 1971). As already reported (Fankboner and Reid, 1981) we were unable to observe the ‘reverse digestion’ process in T. gigas, and made the more parsimonious suggestions that zooxanthellae found in the guts of giant clams had an exogenous origin, and were there because they had been eaten. We also demonstrated that free algal cells, indistinguishable from the tridacnid zooxanthellae, were to be found in the natural environment, especially on a flooding tide, and sug-

MATERIALS AND METHODS Seven specimens of T. gigas were obtained in the vicinity of Mijkadrek and Kidrinen Islands in the Enewetak atoll of the Marshall Islands, and transferred to the Mid Pacific 95

R. G. B.

96 Table

1. Environmental

&ID

et

al.

data txrtainine

to feedine

Previous low water time

Location and condition when samDIed

1230

1100

Gl

1400

0808

G2 G3 G4

1400 1400 0600

0808 0808 2050

GS G6* G7

1600 1500’ I400

2050 1138’ 1258

G8 G9

1400 2400

1258 1304

Native environment; out of water Shr Quarry pool; 6 days acclimatisation As GI As Gl Quarry pool; 7 days acclimatisation As G4 Native environment* Lagoon; 3 days acclimatisation As G7 Lagoon; 4 days acclimatisation

Soecimen

number

Sampling

time

‘Warm surface water with reef detritus after low water.

passed over specimens in this location

Marine Laboratory on Enewetak Island, where some were dissected immediately and others were placed in the ‘quarry’ pool in the windward side of the reef at a depth of I .5 m at mean tide level. The tidal range being 0.7 m during the period of our investigation these specimens were covered at all times and the quarry pool was flushed with a tidal flow passing over the windward reef on each flooding tide. The animals were individually labelled G(tG6. GO was sacrificed on the day it was collected but since the lag between collecting and extraction of samples was 6 hr we did not include this specimen in the comparative study; Gl-G6 were allowed to acclimatise for six days in the quarry pool and their behaviour was recorded at different states of the tide, during both the day and night throughout the acclimatisation period. These specimens were then sacrificed over a 24-hr period as shown in Table 1. At the following spring tidal period three more animals G7-G9 were collected from the original habitat. G7 was sacrificed immediately upon collection; G8 and G9 were given a 4-day

acclimatisation in the lagoon on the leeward side of the laboratory and sacrificed as shown in Table 1. Sampling times were chosen on the basis of an assumed digestive cycle, so that the organisms would either have had some time to ingest and digest incoming particulate food or, alternatively, to have undergone a significant period of nocturnal deprivation. Some accommodation was also made for the hypothesis of the distribution of zooxanthellae proposed by the Morton study of T. crocea.

When specimens were opened the valve weights and total tissue wet weights noted. Gastric juice was extracted with a Pasteur pipet and frozen at -20°C after the volume was measured. Crystalline styles were removed and their lengths recorded. Digestive diverticula were removed and weighed. Portions were fixed in Bouin’s fixative for conventional histology, and in glutaraldehyde fixative prior to epon embedding and subsequent transmission electron microscopy. Portions of digestive diverticula were fixed in cold neutral 4% formalin for 1 hr, rinsed in distilled water and embedded in gelatin. The gelatin blocks were frozen in liquid nitrogen for cryostat sectioning and histochemical study. The remains of the digestive diverticula were frozen for enzymology. The analytical, cytological and enzymological studies of fixed and frozen material were conducted at the University of Victoria, and at Simon Fraser University. The particulate content of the sea water in the clams’ native locality and in the quarry pool and lagoon was studied by filtering the water through millipore filters (0.22 pm pore diameter) and examining the residue microscopically. The particulate material in the stomachs of specimens was examined microscopically as soon as the gastric juices were obtained. Histochemical tests for esterase and acid and alkaline

at 1430, 3 hr

phosphatase and arylamidase were conducted using these substrates: cc-naphthyl acetate (esterase); a-naphthyl phosphate (phosphatases) and L-leucyl-4-methoxy-Bnaphthylmide (arylamidase), following the procedures described by Pearse (1961) and Reid (1966). Frozen gastric juice was thawed and centrifuged at 15,OOOg for 30 min at 4°C. Two extractions of stock frozen digestive diverticula were made by homogenising in a Sorvall Omnimixer, centrifuged at 15,OOOg at 4°C for 2 hr, and supernatants were reduced in volume by freeze drying. Subsamples of the homogenates were taken for the estimation of fat-free dry weight by ether extraction and drying. The amylase activity of gastric juice and the diverticular extracts was estimated by the digestion of 1% starch solution incubated at 37°C for I hr. Following the precipitation of undigested starch with ethanol, glucose was estimated by the anthrone calorimetric method from a standard glucose curve. Results, which were corrected for pre-existing reducing sugars by the subtraction of zero time estimations, were expressed as Somogyi units: I unit releases 1 mg reducing sugar per 30min at 37°C at pH 6.9-7.0. Proteolytic activity of diverticular extracts over a pH range of 2-8 and gastric juice over a pH range of 5.5-6.5 estimated spectrophotometrically at 280 nm following 1 hr incubation with albumin substrate (Reid and Rauchert, 1972). Results, which were corrected for pre-existing amino acids and peptides by the subtraction of zero time estimations, were expressed as units per ml of gastric juice and per mg fat-free dry weight of digestive diverticula. One unit causes an absorption increase of 0.001 per min at 25°C.

RESULTS

Food and feeding behaviour In the original environment and in the quarry pool the sea water contained unidentifiable fragments of planktonic crustacea, diatoms, algal cells identical in size, shape and colour to coral and tridacnid zooxanthellae, and coral sand particles. The lagoon water lacked the algal cells and the particulate matter consisted largely of sand grains. The particulate material in the quarry pool and original environment was found in similar proportions in the stomachs of the giant clams. Tridacna gigas exhibited the nocturnal inactivity described by Morton (1978) for T. crocea. We will refer to this as the ‘nocturnal torpor’ since the inhalant and exhalant currents were weak in three specimens and undetectable in the others and no

Physiology

of Tridacna gigas Linw-I

Table 2. Characteristics Specimen number

Wet weight soft

Cl G2 G3 G4 G5 G6 G7 G8 G9

6.0 8.3 2.1 8.4 3.6 5.6 5.6 9.7 5.7

tissues (kg)

Gastric index is obtained measured.

by dividing

Animals sampled after 5-11 hr of torpor had lower gastric indices (calculated as volume in ml divided by wet weight in kg) than daylight specimens (Table 2). It must, however, be borne in mind that there were uncontrollable quantities of free mantle water associated with the large mass of tissue involved, as well as a loss of blood that increased with increasing attempts to drain off free mantle water; therefore, the gastric indices are approximations at best. The pH of the gastric juices ranged from 5.8 to 6.1 (Table 2). Gastric proteolytic activity at pH 5.5, 6.0 and 6.5 varied from zero activity in G8 at pH 6 to 200 units at pH 5.5. in G6 (Table 3). Gastric amylolytic activity ranged from 10.4 units to 21.3 units (Table 3). There was a considerable individual variation in the length of the crystalline style relative to total wet weight of soft tissues and to shell length. For example, G4 and G5 both had crystalline styles approx 3Ocm long, despite the fact that while both were collected at the same time G4 was approximately double the size of G5 in terms of wet weight of tissue.

Table 3. Gastric Gastric protein digestion (units per ml) pH 6.5 pH 5.5 pH 6.0 100 150 120 80 100 200 100 100 160

Gastric index

Gastric

13.5 20.0 60 12.5 5.5 11.4 9.8 18.0 6.2

2.25 2.41 2.85 1.49 I .53 2.04 1.75 I .86 I .09

5.9 5.9 6.0 6.1 6.0 6.0 5.x 5.8 5.8

75 175 100 125 100 100 50 0 75

PH

gastric volume in ml by total wet weight in kg. -. Not

Gastric physiology

Gl G2 G3 G4 G5 G6 G7 G8 G9

swcimens

Gastric volume (ml)

31 36 22 31 30 28

response was shown to light and tactile stimuli. A vigorous prodding produced only a slight and gradual adduction of the valves. During daylight hours, however, shadow effects, water turbulence and tactile stimuli all caused rapid multiple phasic adductions of the valves and the expulsion of large volumes of mantle water. The onset of the torpor took l-5 hr after sunset in the six specimens that we observed regularly for 5 days in the quarry pool. Recovery after sunrise took from 1 to 3 hr.

Specimen number

of individual

Crystalline style length (cm)

97

110 185 130 105 75 16 25 80 200

The condition of the crystalline styles at all sampling times was similar, firm and occupying the full length of the style sac. Digestive

diverticula

Gelatin blocks were subjected to accidental thawing and refreezing during transit between Enewetak and Victoria and cryostat sections did not reveal fine cytological detail, and we assume that the complete absence of arylamidase and the presence of alkaline phosphatase in specimen G2 only is an indication of the lability of these enzymes rather than the original enzymological condition of the specimens. Alkaline phosphatase activity, for instance, could be detected in the large pieces of digestive diverticula which remained frozen in transit because of their larger size. We describe only two cytological conditions for the tubules of the digestive diverticula since intermediate phases were not distinguishable. The two conditions that we detected are the absorptive condition, where the tubule cells are expanded and the tubule lumen small, and the holding condition where the tubule cells are reduced in size and the tubule lumen large. Both conditions were found in different proportions in all specimens, but the amount of material sectioned for histochemistry was too small to allow significant quantification of these proportions. Cells in the absorptive condition showed apical concentrations of esterase or a homogenous distribution through cytoplasm. They also possessed strong acid phosphatase activity throughout the cytoplasm. Cells in the holding condition showed weak esterase activity and weak or negative acid phosphatase staining. The distal

enzyme activity Starch digestion at pH 6.9 (Somogyi units) 11.0 16.6 20.0 14.0 21.3 10.4 17.5 11.0 7.3

Proteolytic index 146.25 253.05 214.20 149.00 119.34 214.00 78.75 46.50 98.10

Amylolytic index 24.75 40.01 47.60 20.86 32.89 21.22 30.62 20.46 7.96

Proteolytic index is the function of the gastric index and the area subtended by a graph of proteolytlc activity in the pH range 5.5--6.5. Amylolytic index is the function of the gastric index and gastric amylolytic activity expressed as units per ml.

R. G. B. &ID et al.

G2

i

I

Fig. 1. Individual profiles of protein digestion in the pH range 2-8. regions of the ciliated epithelia of the small ducts always gave a strong esterase stain and a variable acid phosphatase reaction. The ciliated epithelia of the large ducts were negative for these enzymes. Proteolytic activity in each specimen over the pH range of 2-8 is shown in Fig, 1 and Table 4. In most of the organisms a double peak appeared about pH 3, a single peak at pH U-6.5 and a single peak at pH 7.0-7.5. The alkaline peak was absent from several specimens. The strongest proteolysis occurred at the lowest pH in all specimens, but the amount of activity varied from individual to individual. Amyiolytic activity in the digestive diverticula ranged from 3X to 75 units per g of fat-free dry weight (Table 3). DISCUSSION

The presence in T. gigm of a circadian feeding rhythm consisting of a diurnal phase of active filtration and a nocturnal torpor would suggest a distinctive digestive cycle such as occurs in T. crocea (Morton, 1978). It was with this in mind that we planned our sampling regime. The vigorous diurnal filtration was indeed reflected in the larger gastric volumes in most animals sampled in daylight. However, there was no significant correlation between gastric volume and pH, nor between pH and sampling time. Crystalline style size varied greatly from one individual to another without any characteristic relationship to the other size and weight parameters of the organisms, and the crystalline styles were

always in the same firm condition; so there are no conclusions pertinent to the digestive cycle to be drawn from this observation. If results expressed simply as units per ml are examined gastric enzyme activity showed no correlation with the feeding cycle. However, if the activity per unit volume remains constant as the stomach volume increases through the ingestion of food and water then the ingestion of food must be accompanied by an active secretion of gastric enzymes (Reid, 1978). As seen in Table 3 the estimation of gastric protein digestion as a function of gastric index shows that Gl-G3 and G6, all sampled after the daylight flood tide, show increased protein digestion. The lagoon specimens from a more impoverished environment, G7-G9, have lower activity. Even so, the gastric levels of both protein digestion and starch digestion are seen to vary from clam to clam. Histochemical results showed differences between digestive tubule cells in the absorptive phase and those in the holding phase, but as Robinson et al. (1981) have pointed out, large samples of individuals, and numbers of sections taken throughout the gland, are necessary to provide reliable conclusions concerning digestive cycles. We are, nevertheless, able to conclude that there is no universal cyclical pattern involving cytological and enzymological conditions cued by the diurnal feeding activity. Langton (1975) studying Mytilus edulis, has argued that lack of synchrony in digestive cells may be due to different proportions of the food reaching different parts of the digestive diverticula. Individual intracellular variations of protein digestion in T. gigas are relevant to an unpublished study of Crassostrea gigus by Reid which relates low acid pH proteolysis to the nocturnal phase of the feeding cycle. The same study also shows individual bivalve idiosyncrasies. For example, in a pulse-feeding experiment some oysters held food in the stomach for up to 8 hr, without passing it on through the subsequent digestive processes involving the diverticula and the mid-gut, while the majority of individuals processed their food to the point of defaecation in less than 8 hr. This individuality appears in Triducna gigus: for example, G3 sampled at the same time as Gl and G2 may either have been slow to emerge from its nocturnal torpor, or, if feeding, had not passed the food beyond the gastric stage. The availability of particulate food to giant clams in nature is unlikely to be continuous, but to come instead in irregular pulses, as from the heat-extruded zooxanthellae from corals on the rising tide (Fankboner and Reid, 1981). A pulse of food may become heterogeneously distributed among the cells of the digestive diverticula, and evoke local cyclic responses, with later pulses affecting different area in different sequences. Hypothetically, a minor cycle, involving one region of the digestive diverticula could be initiated as soon as the

Table 4. Enzyme activity in the digestive diverticula Specimen number ___.._ - ___-__. Total proteolytic activity Amylolytic activity (Somogyi units per g)

Gl

G2

G3

G4

G5

G6

G7

GS

G9

160

100

90

110

290

170

280

180

160

62.5

56.8

43.2

75.0

61.5

75.0

38.0

44.0

43.2

Total proieoI~ic activity is calculated as the areas subtended by the graphs shown in Fig. 1.

Physiology

of Tridacna gigas Linnk--I

Fig. 2. Tridacna squamosa. (a) T. squamosa photographed in natural environment, mantle. (b) T. squamosa after several weeks in the dark, showing “bleached” mantle. of F. J. R. Taylor.

99

showing pigmented Photograph courtesy

100

R. G. 8.

REID

et al.

clam comes out of its nocturnal topor, and be alimentation to the extent that some are gutless (Reid terminated 8-12 hr later, while a pulse of food re- and Bernard, 1980; Felbeck et al., 1981). The districeived just before sunset might either be held for an bution of the giant clams, where they can best take indefinite period in the stomach, or processed advantage of reef detritus, expelled coral zoothrough the night. Thus a particular clam could be xanthellae, and possibly coral exudates (cf Johannes, sampled at any hour of the day or night and exhibit 1967), plus the retention of the digestive system a heterogeneous cytological condition in the digestive emphasise the opportu~stic nature of the TX+ divert&la, and an idiosyncratic overall endacnidae. zymological picture. We attempted without success to make allowances for these variables by sampling Acknowledgements-This study was funded by a grant to most of our daylight specimens at a time when the P. V. Fankboner by the U.S. Department of Energy and by maximum amount of food might have been available NSERC operating grants to R. G. B. Reid and P. V. on the flooding tide, or when a significant period of Fankboner. nocturnal starvation had occurred. While the degree of individuality in these matters REFERENCES makes it difficult to generalise about the digestive cycle it is of particular note that the proteolytic Fankboner P. V. (1971a) Intracellular digestion of symbiotic and amylolytic activities of the digestive system of zooxanthellae by host amoebocytes in giant clams (Bivalvia:Tridacnidae), with a note on the role of the T. gigas falls well within the ‘normal’ range found in hypertrophied siphonal epidermis. Bioi. Bull. mar. biol. other bivalves. Likewise, the proportions of the gut Lab., Woods Hole 141, 222-234. are ‘normal’, although there is a certain dorsoventrai flattening of the stomach which presumably preserves Fankboner P. V. (1971b) Behaviour, digestion, and the role of the zooxantheliae in giant clams~(Eulamellibranchia, the fluid dynamic conditions that are required for Tridacnidae). PhD Thesis. Universitv of Victoria. gastric sorting. The size of the gut has kept pace with Victoria, Brjtish Columbia, 116 pp. . the increase in size of the visceral mass. All of these Fankboner P. V. and Reid R. G. 8. (1981) Mass expulsion observations indicate that the digestive system conof zooxanthellae by heat-stressed reef corals: a source of tinues to have an important role in the economy of food for giant clams? Exprientia 37, 25 l-252. the organism, although the symbiotic zooxanthellae Felbeck H., Childress J. J. and Somero G. N. (1981) Calvin-Benson cycle and sulphide oxidising enzymes in are regarded by all investigators as the most imanimals from sulphide-rich habitats. Nature 293,291-293. portant contributors (Yonge, 1981). Salvat (1969, Fitt W. K. and Trench R. K. (1981) Spawning, devel1971) has described large populations of T. maxima opment, and acquisition of zooxanthellae by Triducna in closed atolls lacking phytoplankton, and Ricard squamosa. (Mollusca, Bivalvia). Biol. Bull. mar. biol. Lub., and Salvat (1977) have shown the ability of this Woods Hole 161, 213-235. species to thrive in the absence of phytopiankton. Johannes R. W. (1967) Ecology of organic aggregates in the Some hitherto unpublished independent observations vicinity of a coral reef. Limnol. Oceanogr. 12, 189-195. on the relative importance of the two nutritive Langton R. W. (1975) Synchrony in the digestive diverticula factors, symbiosis and digestion, are relevant here. of Mytilus edttlis L. J. mar. biol. Ass. U.K. 55, 221-229. Mansour K. (1946) Source and fate of the zooxanthellae of Fankboner placed specimens of T. maxima, T. squathe visceral mass of Tridacna elongata. Nature 158, 130. moss and Hippopus hippopus in dark lagoon caves. Three months later the mantle and siphonal tissues Mansour-Bek J. J. (1946) The digestive enzymes of Tridacnu eiongata Lamk and Finctada t?ulgaris L. Proc. Egypt. were colourless, indicating that the zooxanthellae had Acad. Sci. 1, 13-20. died off. Six months later the bivalves had expired. Morton B. S. (1978) The diurnal rhythm and the processes F. J. R. Taylor of the University of British Columbia of feeding and digestion in Tridacna croceu (Bihas informed us that on a collecting expedition in vaivia:Tridacnidae). J. Zool. Land. 185, 371-387. Pukat, Thailand, a specimen of Tridacna squamosa Pearse A. G. E. (1961) Histochemistrv Theoreticul and was inadvertently left in a dark holding tank in the Applied, 2nd edn: J. & A. Churchill, London. collecting vessel, for approx 6 weeks. This specimen Reid R. G. B. (1966) Digestive tract enzymes in the bivalves Lima hians bmelin and Mya arenarid L. Comp. Biochem. (Fig. 2) was also bleached but seemed otherwise Physiol. 17, 4171133. healthy. A few ~ooxanthellae had survived in the region of the siphon. While in the holding tank fresh Reid R. G. B. (1978) The systematic, adaptive and physiological significance of proteolytic enzyme distribution in sea water containing phytoplankton was circulated bivalves. Veliger 20, 260-265. past the bivalve. Taylor then placed the specimen in Reid R. 6. B. and Bernard F. R. (1980) Gutless bivalves. a lit tank with a closed circulation system containing Science 208, 609-6 IO. filtered sea water and the animal expired within 1 Reid R. G. B. and Rauchert K. (1972) Protein digestion in week. Although it is not clear to what extent the members of the genus Macoma (Mollusca:Bivalvia). Camp. Bioehem. Physiol. 41A, 887-895. animals described above were surviving by filtration Ricard M. and Saivat B. (1977)Faeces of Tridacna maxima and digestion, as opposed to living off their energy (Mollusca-Bivalvia), composition and coral reef imstores of lipid and glycogen, it is a reasonable inferportance. Proc. 3rd horal R‘eef Symp. Miami I, 496-501. ence that prolonged survival might be achieved in the Robinson W. E.. Penninet M. R. and Langton R. W. (1981) dark if adequate supplies of suspended food were Variability of’tubule &pes within the digestive glands of available. The retention of the digestive system at a Mercenaria mercenaria (L), Ostrea edulis L. and Mytiius functional level by Tridacnidae is in marked contrast eduiis L. J. e.~p. Mar. Biol. 54, 265-276. to the condition in the Solemyidae, where a de- Rosewater .I. (1965) The family Tridacnidae in the fndopendence on symbiotic chemoautotroph~c bacteria Pacific. Ind~)-Pacl~c ~ollusca 1, 347-396. Salvat B. (1969) Dominance-biologique de quelques mollusand possib!y dependence on the uptake of dissolved ques dans les atolls fermks (Tuamotu, Polynksie); PhCorganic materials has permitted the loss of normal

Physiology

of Tridacna gigas Linne-I

nomene recent-Consequences actuelles. Mulacologia 9, 187-189. Salvat B. (1971) Evaluation quantitative totale de la Faune benthique de la bordure laquanaire d’une atoll de Polynesia Francaise. C.r. hebd. S&me. Acad. Sci., Paris 272, 21 l-214. Trench R. K., Wethey D.S. and Porter J. W. (1981) Observations on the symbiosis with zooxanthellae among

101

the Tridacnidae (Mollusca:Bivalvia) Biol. Bull. mar. hiol. Lab., Woods Hole 161, 180-198. Yonge C. M. (1936) Mode of life, feeding, digestion and symbiosis with zooxanthellae in the Tridacnidae. Scient. Rep. Gt. Barrier Reef Exped. 1, 283-321. Yonge C. M. (198 1) Functional morphology and evolution in the Tridacnidae (Mollusca:Bivalvia:Cardiacea). Rec. Australian Museum 33, 735-777.