Journal of Coastal Development ISSN: 1410-5217 Volume 5, Number 3, June 2002 : 101-110 Accredited: 69/Dikti/Kep/2000

Review

CALCULATING THE CONTRIBUTION OF TO GIANT CLAMS RESPIRATION ENERGY REQUIREMENTS

Ambariyanto*) Marine Science Department, Faculty of Fisheries and Marine Sciences, Diponegoro University, Semarang . Email: [email protected]

Received: April 24, 2002 ; Accepted: May 27, 2002

ABSTRACT

Giant clams (Tridacnidae) are known to live in association with photosynthetic single cell commonly called zooxanthellae. These algae which can be found in the mantle of the clams are capable of transferring part of their photosynthates which become an important source of energy to the host ( apart from filter feeding activity). In order to understand the basic biological processes of the giant clams , the contribution of zooxanthellae to the clam’s energy requirement need to be determined. This review describes how to calculate the contribution of zooxanthellae to the giant clam’s energy requirement for the respiration process.

Key words: Giant clams, tridacnidae, zooxanthellae CZAR

*) Correspondence: Tel. 024-7474698, Fax. 024-7474698, Email: [email protected]

INTRODUCTION One of the important aspects of the biology of giant clams is the existence Giant clams (Family: Tridacnidae) are of zooxanthellae which occupy the mantle large bivalves that are commonly found in of the clams as endosymbiotic reef especially in the Indo- dinoflagellate algae (Lucas, 1988). These Pacific region. This family consists of two zooxanthellae have a significant role, genera ( and ) and eight especially in the energy requirements of : Tridacna gigas, T. derasa, T. giant clams, since they are capable of squamosa, T. maxima, T. crocea, T. translocating part of their photosynthetic tevoroa, Hippopus hippopus, and H. products to their host. This is why as a porcellanus (Braley, 1992). As well as member of bivalves giant clams do not being prominent members of healthy coral only supply their energy demand from reef ecosystems they are important to the filter feeding process, but also from the people of South East Asia and the Pacific energy translocation from zooxanthellae region as a source of food (meat) and (Klumpps et al., 1992). building material (shells). These clams This review aims to describe how have recently become an important export to calculate the contribution of commodity in several countries in this zooxanthellae to the daily respiration region (Tacconi and Tisdell, 1992; Tisdell energy requirements of giant clams. et al., 1994).

101

Journal of Coastal Development ISSN: 1410-5217 Volume 5, Number 3, June 2002 : 101-110 Accredited: 69/Dikti/Kep/2000

predominates in , whilst in Zooxanthellae-Giant Clams Association culture there is alternation between the motile and non-motile (coccoid) stage Zooxanthellae are 'yellow-brown' dino- (Muscatine, 1980; Domotor and D'Elia, flagellate algae (Pyrrophyta) which live as 1986). Motile stages are reported to be in many marine phototactic and occur only for a short invertebrate species (Brandt, 1881). Taylor period of approximately 0.5 hour (Taylor, (1974) listed four different species of 1969a; Domotor and D'Elia, 1986). Fitt et zooxanthellae: (1) Gymnodinium (Symbio- al. (1981) demonstrated different motility dinium) microadriaticum (Freudenthal, patterns of zooxanthellae collected from 1962) which lives in protozoans, jellyfish (C. xamachana, C. frondosa), sea coelenterates, molluscs; (2) Amphidinium anemones (Aiptasia tagetes, A. pallida) chattonii in some coelenterates; and (3) A. and a giant clam (T. gigas) cultured in klebsii in platyhelminthes and (4) identical conditions. Amphidinium sp. in some protozoans. Schoenberg and Trench (1980a,b) microadriaticum reported differences in isoenzyme patterns, was originally isolated from the jellyfish soluble protein, size, and the structure of Cassiopeia sp (Freudenthal, 1962). Later the cell wall of zooxanthellae collected Taylor (1971) proposed that zooxanthellae from different hosts. Using be placed in the Gymnodinium electrophoresis, Schoenberg and Trench because the free-living stage had great (1980a) investigated 40 cultures from 17 affinities to this genus. Loeblich and host species representing 12 strains and Sherley (1979) later suggested the use of found a unique combination of four Zooxanthella microadriatica when they isoenzyme patterns in each strain. Later found that the zooxanthellae isolated from Chang et al. (1983) found differences in Cassiopea xamachana differed slightly the photoadaptive mechanisms of three from Zooxanthella nutricula from the strains of zooxanthellae collected from a order Zooxanthellales (Brandt, 1881). clam (T. maxima), an anemone (A. Schoenberg and Trench (1980b), however, pulchella) and a coral (Montipora argued that the latter name was verrucosa). Similarly, Blank and Trench inappropriate, because the pyrenoids of the (1985a,b) showed several differences in algae described by Brandt (1881) are the number of chromosomes, chloroplasts, traversed by chloroplast thylakoids pyrenoid stalks, mitochondria, (Hollande and Carre, 1974), which is not chromosome volumes, nuclear volumes the case in S. microadriaticum from and thylakoid arrangements of Cassiopeia sp. zooxanthellae isolated from jellyfish Further work revealed that (Cassiopeia xamachana and C. frondosa), Symbiodinium microadriaticum are not anemone (Heteractis lucida) and coral (M. monospecific. Morphological, physio- verrucosa). These zooxanthellae were logical, biochemical and genetic reported to maintain their differences differences among S. microadriaticum when cultured in similar conditions. collected from different hosts are now The existence of these variations more the norm than the converse among zooxanthellae collected from (Schoenberg and Trench, 1980a,b; Blank different hosts suggests that zooxanthellae and Trench, 1985 a,b). There are represent dozens, perhaps even hundreds differences in the life cycle of of species. By investigating the zooxanthellae in symbiosis and in culture biochemical, physiological, conditions. The coccoid, non-motile stage morphological, and behavioural

102

Journal of Coastal Development ISSN: 1410-5217 Volume 5, Number 3, June 2002 : 101-110 Accredited: 69/Dikti/Kep/2000 differences, Trench and Blank (1987) existence of a tubular system associated introduced three new species into the with zooxanthellae within giant clams, genus Symbiodinium. These are S. goreauii previously reported by Mansour (1946). , S. kawagutii and S. pilosum isolated Norton et al. (1992) concluded that from the Caribbean sea anemone Ragactis zooxanthellae in clams are located in a lucida, stony coral Montipora verrucosa branched tubular structure, with a single and the Caribbean zoanthid Zoanthus layer of thin cells separating zooxanthellae sociatus respectively. Rowan and Powers and haemolymph (Rees et al., 1993). (1991, 1992) found 6 distinct differences There are two mechanisms by in small subunit RNA (ssRNA) genes of which zooxanthellae appear in the next zooxanthellae collected from 16 cnidarians generation of their symbiotic host. using the polymerase chain reaction (PCR) Zooxanthellae can be acquired by direct method. They could not distinguish any parental transmission via their , or by differences in the symbionts from direct acquisition from the environment. In individual of the same species, but giant clams, however, zooxanthellae are they found that different species of corals not being passed to the larvae (LaBarbera, have algae with unique sRNA sequences. 1975; Jameson, 1976; Fitt et al., 1984; However, multiple populations of 1986). This is proved by the fact that zooxanthellae have been reported from zooxanthellae are not found in the individual coral, Montrastea annularis, M. trochophore stage (Fitt and Trench, 1981). faveolata, and M. Franksi (Rowan and Giant clams larvae acquire zooxanthellae Knowlton 1995). de novo from the environment, soon after In more recent papers Baker and metamorphosis (Jameson, 1976; Fitt et al., Rowan (1997) reported genetic differences 1984). In the hatchery, zooxanthellae among zooxanthellae isolated from various isolated from adult clams are introduced to corals species collected from the veliger stages in order to promote a rapid Caribbean and Eastern Pacific. They found transition to the new stage (Gwyther and three different clades among those Munro, 1981; Fitt et al., 1984; Trinidad- zooxanthellae which were then termed as Roa, 1988). clade A, B, and C. All strains of Symbiodinium sp. are ingested by clams. Only a specific Zooxanthellae-Giant Clam Relationship strain, however, will eventually dominate a particular host (Fitt and Trench, 1981; Fitt, Giant clams are known to live in 1985b; Fitt et al., 1986). Strain selection association with symbiotic zooxanthellae by the clams entirely depends on how a (the term symbiosis being used throughout particular strain can grow, survive and this paper is to describe the mutualistic compete with other strains within the host interaction between zooxanthellae and the tissue (Fitt et al., 1986). host). In giant clams these zooxanthellae are extracellular, unlike hermatypic corals Contribution of Zooxan-Thellae to where zooxanthellae are located Giant Clams Respiration intracellularly. Initially it was agreed that zooxanthellae in giant clams are located Zooxanthellae have been found in the freely in the haemal sinuses of the stomach, digestive gland (Morton, 1978; siphonal tissue which expand along the Frankboner and Reid, 1981; Heslinga and dorsal surface of the clams (Yonge, 1953; Fitt, 1987) and faeces of clams (Trench et Frankboner, 1971; Trench et al., 1981). al., 1981; Fitt et al., 1986). Since they Norton et al,. (1992), however, found the were morphologically intact, photo-

103

Journal of Coastal Development ISSN: 1410-5217 Volume 5, Number 3, June 2002 : 101-110 Accredited: 69/Dikti/Kep/2000 synthetically functional and viable, Trench measured, respiration in the light is et al. (1981) suggested that the currently difficult, if not impossible to zooxanthellae cannot be digested by clams measure accurately (Muscatine et al., as was previously thought (Frankboner, 1981). Therefore, the first assumption that 1971; Frankboner and Reid, 1981). has to be made is that respiration in the Zooxanthellae are capable of dark and in the light are the same. In transferring part of their photosynthetic addition, zooxanthellae respiration must be products to the host (Muscatine, 1967; distinguished from respiration. Goreau et al., 1973; Taylor, 1974; Zooxanthellae respiration can be measured Streamer et al., 1988; Fitt, 1993). Their directly in vitro, but may not represent the contribution depends primarily on the light real respiration rate of zooxanthellae intensity (via ) and on clam within the host (Hoegh-Guldberg and size, both of which affect the proportion of Hinde, 1986; Muscatine, 1990). zooxanthellae reached by the light Morphological and physiological changes (Heslinga and Fitt, 1987). in zooxanthellae occur soon after they are Several approaches to the study of isolated from their host (Trench, 1979). the photosynthetic contribution of The second assumption proposed by zooxanthellae have been used. Muscatine Muscatine et al. (1981), is that the ratio of et al. (1981) outlined CZAR (the zooxanthellae and host respiration is Contribution of Zooxanthellae to Animal proportional to their respective biomass. Respiration). CZAR can be calculated as Although this method has been used for a follows: large number of studies it should be noted that the assumption that the host and

symbiont have similar metabolic [PZ net (24 h)] (%Tr) CZAR = ------intensities (that is, respiration at the same R (24 h) rate per gram of tissue) has not been a directly tested (Hinde, 1989).

In order to calculate the value of where: CZAR for a symbiosis, several parameters PZ net (24 h) = net carbon assimilated by have to be measured. These include the zooxanthellae during pho- zooxanthellae specific growth rate, tosynthesis over 24 h zooxanthellae carbon content, % Tr = the percentage of the pho- zooxanthellae and host protein content, tosynthates translocated daily carbon fixation by zooxanthellae and by zooxanthellae to the carbon respired by zooxanthellae and the host host. Ra (24h) = carbon respired by animal Zooxanthellae specific growth rate over 24 h can be calculated by first isolating zooxanthellae from the host and CZAR is based on the determining the mitotic index of the algae measurement of the production (photo- (the ratio of dividing cells in 1000 cells at synthesis) and consumption (respiration) the time when the sample is taken). This of oxygen which are then converted into index then can be converted to specific units of organic carbon (Muscatine, 1980a; growth rate using the following equation, Muscatine et al., 1981). Respiration is the for phased mitotic indices (Wilkerson et sum of the respiration of the host and al., 1981; Muscatine et al., 1984): zooxanthellae. Although the respiration rate under total darkness can be easily µ = 1/td ln(1+f)

104

Journal of Coastal Development ISSN: 1410-5217 Volume 5, Number 3, June 2002 : 101-110 Accredited: 69/Dikti/Kep/2000

the hosts (Muscatine and Porter, 1977). where: Muscatine (1980, review) found that with

µ = specific growth rate a mean translocation of 63% in P. td = duration of paired cell stage in hour damicornis and of 69% in Fungia scutaria f = the maximum value of mitotic index with different values of photosynthetic and respiration quotients and respiration ratios td is difficult to measure directly from of algae, coral and animal, CZAR could symbiotic algal populations. A range of range from 41% - 136% and 36% - 180% studies, however, have estimated that td respectively. Hoegh-Guldberg et al. (1986) lies somewhere around 0.46 d (Wilkerson reported potential seasonal differences in et al., 1983; Hoegh-Guldberg et al., 1986). the contribution of zooxanthellae to the It can also be shown that CZAR is host, Pteraeolidia ianthina (Nudibranchia) relatively insensitive to quite large and found that high densities of symbionts variation in td (Muscatine et al., 1981). contributed 79%, 121% and 173% to the The carbon content of the host in winter, spring and summer zooxanthellae can be determined based on respectively. Muscatine et al. (1984) the cell diameter and volume using the reported a higher CZAR in light-adapted following equation (Strathmann, 1967): pistillata (143%) compared

with shaded colonies (58%). Similarly, McCloskey and Muscatine (1984) showed log C = - 0.314 + 0.712 log V that CZAR in S. pistillata was 78% at 35

m and 157% at 3 m depth. where: The CZAR for zooxanthellae in C = carbon giant clams also depends on the percentage V = volume translocation by zooxanthellae. Using the value of 40% and 95% translocation, the The carbon content of mean values of CZAR of Tridacna gigas zooxanthellae can then be used to convert were 83% and 197%, respectively (Fisher information about the number of cells et al., 1985). Moreover, CZAR values in produced each day into a measure of the Hippopus hippopus were reported to vary carbon retained by zooxanthellae. between 7% and 137% depending on the Algal protein content can be photosynthetic and respiratory rates and measured by analysing the protein content the percentage translocation (assumed to of a known number of zooxanthellae be 40% and 98%, respectively; Fitt et al., isolated from the host. The total protein 1985). When the percentage translocation content of the host is usually analysed value of 95% is used, the CZAR values are using the Lowry method (1951). likely above 100% for T. gigas (Fisher et The daily net carbon fixation of al., 1985; Mingoa, 1988; Klumpp et al., zooxanthellae can be calculated from the 1992), and T. derasa and T. tevoroa photosynthetic rates of the algae and the (Klumpp and Lucas, 1994). daily irradiance. The oxygen produced by Trench et al. (1981) showed that photosynthesis then can be converted to the zooxanthellae from Tridacna maxima carbon multiplying the weight of oxygen can contribute more than 50% of the produced with 0.375 per PQ (photo- clam’s respiratory carbon requirements, synthetic quotient; Muscatine et al., 1981). which range from 62% up to 84% CZAR in the coral Pocillopora (assuming 40% translocation) on cloudy damicornis can be as high as 86.8%, by versus sunny days respectively. The assuming 40% translocation from algae to importance of the availability of light was

105

Journal of Coastal Development ISSN: 1410-5217 Volume 5, Number 3, June 2002 : 101-110 Accredited: 69/Dikti/Kep/2000 also reported by Mingoa (1988) who found Research Institute, Balboa, that the CZAR value of shade-reared Panama. P: 1295-1300 juveniles of T. gigas (mean value of 91.9%) was significantly higher than the Blank, R.J., Trench, R.K. (1985a). CZAR from unshaded clams (mean value Symbiodinium microadriaticum: a of 72.9%). The lower value of CZAR from single species?. Proc. 5th Int. unshaded clams can be explained by the Cong. 6: 113-117. lower PR ratio, indicating less fixed carbon produced and available to the host. Blank, R.J., Trench, R.K. (1985b). Mingoa (1988) also found that the value of Speciation and symbiotic photosynthetic efficiency (a) and . Science. 229: 656- maximum photosynthetic rate (Pmax) from 658. shade-reared clams were significantly lower than those of unshaded clams. Braley, R.D. (1992). The Giant Clams: A The phototrophic and hatchery and nursery culture heterotrophic contributions, through the manual. ACIAR Monograph No. translocation of photosynthate by 15. Canberra. p: 144. zooxanthellae and filter feeding, respectively, to the nutrition of giant clams Brandt, K. (1881). Ueber das have been investigated by Klumpp et al., zusammenleben von thieren und (1992), Klumpp and Griffiths (1994) and algen. Verhanddlungen der Klumpp and Lucas (1994). These Physiologischen Gesellschaft zu contributions are size- and species- Berlin. 1881-1882: 22-26. dependent. Filter feeding becomes less important with increasing size of the Chang, S.S., Prezelin, B.B., Trench, R.K. clams. For example, filter feeding provides (1983). Mechanisms of photo- 65 % and 35 % of total carbon needed by adaptation in three strains of the small and large Tridacna gigas symbiotic dinoflagellate respectively (Klumpp et al., 1992). In all Symbiodinium microadriaticum. species the value of CZAR increases with Mar. Biol. 76: 219-229. increasing the size of the clams (Klumpp Domotor, S.L., D'Elia, C.F. (1986). Cell- and Griffiths, 1994). These authors size distributions of zooxanthellae concluded that phototrophy is an important in culture and symbiosis. Biol. source of energy to the host for any size Bull. 170: 519-525. and species of giant clams.

Fisher, C.R., Fitt, W.K., Trench, R.K.

(1985). Photosynthesis and

respiration in Tridacna gigas as a REFERENCES function of irradiance and size. Biol. Bull. 1969: 230-245. Baker, AC. and Rowan, R.(1997). Diversity of symbiotic Fitt, W.K. (1985). Effect of different dinoflagellates (zooxanthellae) in strains of the zooxanthella scleractinian corals of the Symbiodinium microadriaticum on Caribbean and Eastern Pacific. In. growth and survival of their Proc. 8th. Int. Coral Reef Symp. coelenterate and molluscan hosts. Vol. 2. (eds. HA. Lessions. & IG. Proceedings of the Fifth International Macintyre). Smithsonian Tropical Coral Reef Congress. 6: 131-136.

106

Journal of Coastal Development ISSN: 1410-5217 Volume 5, Number 3, June 2002 : 101-110 Accredited: 69/Dikti/Kep/2000

nutritional role of the hyper- Fitt, W.K., Chang, S.S., Trench, R.K. throphied siphonal epidermis. (1981). Motility patterns of Biol. Bull. 141: 222-234. different strains of the symbiotic dinoflagellate Symbiodinium Frankboner, P.V. Reid, R.G.B. (1981). (Gymnodinium) microadriaticum Mass expulsion of zooxanthellae (Freudenthal) in culture. Bull. by heat-stressed reef corals: a Mar. Sci. 31: 436-443. source of food for giant clams?. Experentia 37: 251-252. Fitt, W.K., Fisher, C.R. Trench, R.K. (1984). Larval biology of Goreau, T.F., Goreau, N.I., Yonge, C.M. tridacnid clams. . 39: (1973). On the utilization of 181-195. photosynthetic products from zooxanthellae and of a dissolved Fitt, W.K., Fisher, C.R. Trench, R.K. amino acid in Tridacna maxima f. (1986). Contribution of the elongata (: ). J. symbiotic dinoflagellate Zool. London. 169: 147-454. Symbiodinium microadriaticum to the nutrition, growth and survival Gwyther, J. Munro, J.L. (1981). Spawning of larval and juvenile tridacnid induction and rearing of larvae of clams. Aquaculture 55: 5-22. tridacnid clams (Bivalvia : Tridacnidae). Aquaculture. 24: Fitt, W.K., Heslinga, G.A., Watson, T.C. 197-217. (1993a). Utilization of dissolved inorganic nutrients in growth and Heslinga, G.A., Fitt, W.K. (1987). mariculture of the tridacnid clam Domestication of tridacnid clams. . Aquaculture Bioscience. 37: 332-339. 109: 27-38 Hinde, R. (1989). Carbon budgets for Fitt, W.K., Rees, T.V.A., Braley, R.D., algal-invertebrate symbioses: the Lucas, J., Yellowlees, D. (1993b). problem of respiration. In: Nitrogen flux in giant clams: size Endocytobiology IV. Nardon, P., dependency and relationship to Gianinazzi-Pearson, V., Grenier, zooxanthellae density and clam A.M., Margulis, L., Smith, D.C. biomass in the uptake of dissolved (eds). 4th International inorganic nitrogen. Mar. Biol. Colloquium on Endocytobiology 117: 381-386. and Symbiosis.

Fitt, W.K., Trench, R.K. (1981). Spaw- Hoegh-Guldberg, O., Hinde, R. (1986). ning, development and acquisition Studies on a nudibranch that of zooxanthellae by Tridacna contains zooxanthellae I. squamosa (Mollusca, Bivalvia). Photosynthesis, respiration and the Biol. Bull. 161: 213-235. translocation of newly fixed carbon by zooxanthellae in Frankboner, P.V. (1971). Intracellular Pteraeolidia ianthina. Proc. R. digestion of symbiotic zoo- Soc. Lond. B. 228: 493-509. xanthellae by host amoebocytes in giant clams (Bivalvia: Hoegh-Guldberg, O., Hinde, R., Tridacnidae), with a note on the Muscatine, L. (1986). Studies on

107

Journal of Coastal Development ISSN: 1410-5217 Volume 5, Number 3, June 2002 : 101-110 Accredited: 69/Dikti/Kep/2000

a nudibranch that contains squamosa Bivalvia: (Tridacnidae). zooxanthellae II. Contribution of Malacologia. 15(1): 69-79. zooxathellae to animal respiration (CZAR) in Pteraeolidia ianthina Loeblich, A.R., Sherley, J.L. (1979). with high and low densities of Observations on the theca of the zooxanthellae. Proc. R. Soc. Lond. motile phase of free living and B. 228: 511-521. symbiotic isolates of Zooxanthellae microadriaticum Hollande, A., Carre, D. (1974). Les (Freudenthal) comb. nov. J. mar. xanthelles des radiolaires biol. Ass. U.K. 59: 195-205. sphaerocollides, des acanthaires et de Velella velella: Infrastructure- Lowry, O.H., Rosebrough, N.J., Farr, A.L., cytochimie-taxonomie. Randall, R.J. (1951). Protein Potistologia 10: 573-601. measurement with Folin-phenol reagent. J. biol. Chem. 193:265- Jameson, S.C. (1976). Early life history of 275. the giant clams Lamarck, Tridacna maxima Lucas, J.S. (1988). Giant Clams: (Roding) and Hippopus hippopus Description, Distribution and Life (Linnaeus). Pac. Sci. 30(3): 219- History. In: Copland, J.W., Lucas, 233. J.S. (eds). Giant Clams in Asia and the Pacific. ACIAR. Canberra. p: Klumpp, D.W., Bayne, B.L., Hawkins, 21-32. A.J.S. (1992). Nutrition of the giant clam Tridacna gigas (L.). I. Mansour,K. (1946). Communication Contribution of filter feeding and between the dorsal edge of the photosynthates to respiration and mantle and the stomach of growth. J. Exp. Mar. Biol. Ecol. Tridacna. Nature. 157: 844. 155: 105-122. McCloskey, L.R., Muscatine, L. (1984). Klumpp, DW., Griffiths, C.L. (1994). Production and respiration in the Contributions of phototrophic and Red Sea coral heterotrophic nutrition to the as a function of depth. Proc. R. metabolic and growth Soc. Lond. B 222: 215-230. requirements of four species of giant clam (Tridacnidae). Mar. Mingoa, S.S.M. 1988. Photoadaptation in Ecol. Prog. Ser. 115: 103-115. juvenile Tridacna gigas. In: Copland, J.W., Lucas, J.S. (eds). Klumpp, D.W., Lucas, J.S. (1994). Giant Clams in Asia and the Nutritional ecology of the giant Pacific. ACIAR Monograph No. 9. clams Tridacna tevoroa and T. p: 145-150. derasa from Tonga: influence of light on filter-feeding and Morton, B. (1978). The diurnal rhythm photosynthesis. Mar. Ecol. Prog. and the processes of feeding and Ser. 107: 147-156. digestion in Tridacna crocea (Bivalvia:Tridacnidae). J. Zool. LaBarbera, M. (1975). Larvae and larval Lond., 185: 371-387. development of the giant clams Tridacna maxima and Tridacna

108

Journal of Coastal Development ISSN: 1410-5217 Volume 5, Number 3, June 2002 : 101-110 Accredited: 69/Dikti/Kep/2000

Muscatine, L. (1967). Glycerol excretion Norton, J.H., Shepherd, M.A., Long, H.M , by symbiotic algae from corals and Fitt, W.K. (1992). The zooxan- Tridacna and it's control by the thellal tubular system in the giant host. Science 156: 516-519. clam. Biol. Bull. 183: 503-506.

Muscatine, L. (1980a). Productivity of Rees, T.A.V., Fitt, W.K., Yellowlees, D. zooxanthellae. In:. Falkowski, (1993). The haemolymph and its P.G. (ed). Primary Productivity in temporal relationship with the Sea. Plenum Press. p: 381-402. zooxanthellae in the giant clam symbiosis. In: Fitt, Muscatine, L. (1980b). Uptake, retention, W.K. (ed.) Biology and of and release of dissolved inorganic mariculture of Giant Clam. nutrients by marine alga- ACIAR Proc. 47: 41-45. invertebrate associations. In: Cook., C.B., Pappas, P.W., Rowan, R., Knowlton, N. (1995). Rudolph, E.D. (eds.). Cellular Intraspecific diversity and interactions in symbiosis and ecological zonation in coral-algal parasitism. Columbus: Ohio State symbiosis. Proc. Natl. Acad. Sci. Univ. Press. p: 229-244. USA. 92:2850-2853.

Muscatine, L. (1990). The role of Rowan, R., Powers, D.A. (1991). symbiotic algae in carbon and Molecular genetic identification of energy flux in reef corals. In: symbiotic dinoflagellates Dubinsky, Z. (ed). Coral Reefs. (zooxanthellae). Mar. Ecol. Prog. Ecosystems of the World 25. Ser. 71: 65-73. Elsevier. p: 75-87. Rowan, R., Powers, D.A. (1992). Muscatine, L., Falkowski, P.G., Porter, Ribosomal RNA sequences and J.W., Dubinsky, Z. (1984). Fate of the diversity of symbiotic photosynthetic fixed carbon in dinoflagellates (zooxanthellae). light- and shade-adapted colonies Proc. Natl. Acad. Sci. USA. of the symbiotic coral Stylophora 89:3639-3643. pistillata. Proc. R. Soc. Lond. B 222: 181-202 Schoenberg, D.A., Trench, R.K. (1980a). Genetic variation in Symbiodinium Muscatine, L., McCloskey, L.R., Marian, (Gymnodinium) microadriaticum, R.E. (1981). Estimating the daily Freudenthal and specifity in its contribution of carbon from symbiosis with marine inver- zooxanthellae to coral animal tebrates. I. Isoenzyme and soluble respiration. Limnol. Oceanogr. protein patterns of axenic cultures 26(4): 601-611. of S. microadriaticum. Proc. R. Soc. Lond. B. 207: 405-427. Muscatine, L., Porter, J.W. (1977). Reef corals: Mutualistic Symbioses Schoenberg, D.A., Trench, R.K. (1980b). adapted to nutrient-poor II. Morphological variation in S. environments. BioScience 27(7): microadriaticum. Proc. R. Soc. 454-460. Lond. B 207: 429-444.

109

Journal of Coastal Development ISSN: 1410-5217 Volume 5, Number 3, June 2002 : 101-110 Accredited: 69/Dikti/Kep/2000

Strathmann, R.R. (1967). Estimating the Trench, R.K. (1979). The cell biology of organic carbon content of plant-animal symbioses. Ann. Rev. from cell volume or Plant Physiol. 30: 485-531. plasma volume. Limnol. Oceanogr. 12: 411-418. Trench, R.K., Blank, R.J. (1987). Symbiodinium microadriaticum Streamer, M., Griffiths, D.J., Thinh, L. Freudenthal S. goreauii sp. nov, S. (1988). The products of kawagutii sp. nov. and S. pilosum photosynthesis by zooxanthellae sp. nov: Gymnodinioid (Symbiodinium microadriaticum) dinoflagellate symbiosis of marine of Tridacna gigas and their invertebrates. J. Phycology 35: transfer to the host. Symbiosis. 6: 469-481. 237-252. Trench, R.K., Wethey, D.S., Porter, J.W. (1981). Some observations on the symbiosis with zooxanthellae Tacconi, L., Tisdell, C. (1992). Exports among the tridacnidae (Mollusca: and exports markets for giant clam Bivalvia). Biol. Bull. 161: 180- meat from the South Pacific Fiji, 198. Tonga and Western Samoa. In: Tisdell, C. (ed). Giant Clam in the Trinidad-Roa, M.J. (1988). Spawning and Sustainable Development of the larval rearing of giant clams in South Pacific. ACIAR Monograph Pangasinan, . In: 18. Copland, J.W., Lucas, J.S. (eds). Giant Clams in Asia and the Taylor, D.L. (1969a). Identity of Pacific. ACIAR Monograph no. 9 zooxanthellae isolated from some Canberra. p: 120-124. Pacific Tridacnidae. J. Phycology.

5: 336-340. Wilkerson, F.P., Parker, G.M., Muscatine

Taylor, D.L. (1971). Ultrastructure of L. (1983). Temporal patterns of 'zooxanthella' Endodinium cell division on natural chattonii in situ. J. mar. biol. populations of endosymbiotic Assoc. U.K. 51: 227- 234. algae Limnol. Oceanogr. 28(5): 1009-1014. Taylor, D.L. (1974). Symbiotic marine algae: and biological Wilkinson, C.R., Williams, D. McB, fitness. In: Vernberg, W.B. (ed.). Sammarco, P.W., Hogg, R.W., Symbiosis in the sea. Univ. South Trott, L.A. (1984). Rates of Carolina Press. p: 245-261. nitrogen fixation on coral reefs across the continental shelf of the Tisdell, C. , Shang, Y.C., Leung, P. central . Mar. (1994). Economics of Biol. 80: 255-262. Commercial Giant Clam Mariculture. ACIAR Monograph Yonge, C.M. (1953). Mantle chambers and 25. 306 p. water circulation in the Tridacnidae (Mollusca). Proc. Zool. Soc. (Lond.) 123: 551-561

110