Abstract
Tridacnid clams live on coral reefs in the Indo-Pacific, in waters containing low concentrations of inorganic nitrogen. This study examined nitrogen flux in the giant clam Tridacna gigas. Adults and juveniles of this species typically occur with symbiotic dinoflagellates of the genus Symbiodinium sp., often referred to as zooxanthellae, which live in their tissues. Intact clams took up or released dissolved inorganic nitrogen (DIN), with the direction and magnitude of the fluxes dependent on clam size. Non-symbiotic larvae and newly-settled juveniles with few zooxanthellae released ammonium. Larger juveniles and adults depleted ammonium or nitrate from seawater, when offered separately. Rates of uptake of DIN, standardized to either clam wet weight or number of zooxanthellae, were highest in small clams (1 to 5 cm in length), and decreased with increasing clam size (>5 cm). Clams maintained in seawater containing high concentrations of ammonium (ca. 20 μM) for ≥ 1 wk generally released ammonium in the dark and exhibited net uptake in the light. Freshly isolated zooxanthellae (FIZ) from small clams had higher uptake rates than FIZ from larger clams, implying that the latter may be more nitrogen-sufficient than the former. The gradient of nitrogen sufficiency in giant clams is related to zooxanthellae density, with peaks of both algal density and rates of uptake of DIN occurring in small sizes of clams, whose growth also appears to be limited by nitrogen availability.
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Braley, R. D., Sutton, D., Mingoa, S. S. M., Southgate, P. C. (1993). Passive greenhouse heating, recirculation, and nutrient addition on nursery phase Tridacna gigas: growth boost during winter months. Aquaculture, Amsterdam 108: (in press)
Cook, C. B., D'Elia, C. F. (1988). Are natural populations of zooxanthellae ever nutrient-limited? Symbioses 4: 199–211
Cook, C. B., D'Elia, C. F., Muller-Parker, G. (1988). Host feeding and nutrient sufficiency for zooxanthellae in the sea anemone Aiptasia pallida. Mar. Biol. 98: 253–262
Cook, C. B., Fitt, W. K. (1989). Nutritional status and the regulation of host/symbiont growth in the zooxanthellae hydroid Myrionema ambionense. II. The effect of feeding, starvation, and dissolved inorganic nutrients. Endocytobiology 4: 285–288
Crawford, C. M., Lucas, J. S., Munro, J. L. (1987). The mariculture of giant clams. Interdisciplinary Sci. Rev. 12: 333–340
D'Elia, C. F., Domotor, S. L., Webb, K. L. (1983). Nutrient uptake kinetics of freshly isolated zooxanthellae. Mar. Biol. 75: 157–167
Dubinsky, Z., Stambler, N., Ben-Zion, M., McCloskey, L. R., Muscatine, L., Falkowski, P. G. (1990). The effect of external nutrient resources on the optical properties and photosynthetic efficiency of Stylophora pistillata. Proc. R. Soc. Lond. B. 239: 231–246
Fisher, C. R., Fitt, W. K., Trench, R. K. (1985). Photosynthesis and respiration in Tridacna gigas as a function of irradiance and size. Biol. Bull. mar. biol. Lab., Woods Hole 169: 230–245
Fitt, W. K. 81991. Mariculture of tridacnid clams. In: Menzel, W. (ed.) The culture of estuarine and marine bivalve mollusks in temperate and tropical regions. CRC Press, Inc., Miami, Florida, p. 283–295
Fitt, W. K., Cook, C. B. (1989). Nutritional status and the regulation of host/symbiont growth in the zooxanthellae hydroid Myrionema ambionese. I. The effect of host feeding and incident light levels in nature. Endocytobiology 4: 281–289
Fitt, W. K., Heslinga, G. A., Watson, T. C. (1993) Utilization of dissolved inorganic nutrients in growth and mariculture of the tridacnid clam Tridacna derasa. Aquaculture, Amsterdam 109: 27–38
Hastie, L., Watson, T. C., Isamu, T., Heslinga, G. A. (1992) Effect of nutrient enrichment on Tridacna derase seed: dissolved inorganic nitrogen increases growth rate. Aquaculture, Amsterdam 106: 41–49
Heslinga, G. A., Fitt, W. K. (1987). The domestication of tridacnid clams. BioSci. 37: 332–339
Heslinga, G. A., Perron, F. E., Orak O. (1984). Mass culture of giant clams (f. Tridacnidae) in Palau. Aquaculture, Amsterdam 39: 197–215
Hoegh-Guldberg, O., Hinde, R. (1986). Studies on a nudibranch that contains zooxanthellae. I. Photosynthesis, respiration and the translocation of newly fixed carbon by zooxanthellae in Pteraeolidia ianthina. Proc. R. Soc. (Ser. B) 228: 493–509
Hoegh-Guldberg, O., Smith, G. J. (1989). The influence of the population density of zooxanthellae and supply of ammonium on the biomass and metabolic characteristics of the reef corals Seriatopora hystrix and Stylophora pistillata. Mar. Ecol. Prog. Ser. 57: 173–186
Liddicoat, M. I., Tibbits, I. S., Butler, E. (1975). The determination of ammonia in seawater. Limnol. Oceanogr. 20: 131–132
McCloskey, L. R., Falkowski, P. G., Dubinsky, Z., Muscatine, L., Ben-Zion, M. (1993). Effects of external nutrient resources on photosynthesis, respiration, and translocated materials in the zooxanthellae coral Stylophora pistillata. (In preparation)
Miller, D. J., Yellowlees, D. (1989). Inorganic nitrogen uptake by symbiotic marine cnidarians: a critical review. Proc. R. Soc. (Ser. B) 237: 109–125
Muscatine, L. (1980). Uptake, retention, and release of dissolved inorganic nutrients by marine alga — invertebrate associations. In: Cook, C. B., Pappas, P. W., Rudolf E. D. (eds.) Cellular interaction in symbiosis and parasitism. Ohio State University Press, Columbus, Ohio p. 229–244
Muscatine, L., D'Elia, C. F. (1978). The uptake, retention, and release of ammonium by reef corals. Limnol. Oceanogr. 23: 725–734
Muscatine, L., Falkowski, P. G., Dubinsky, Z., Cook, P. A., McCloskey, L. R. (1989). The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proc. R. Soc. (Ser. B) 236: 311–324
Onate, J. A., Naguit, M. R. A. (1989). A preliminary study on the effect of increased nitrate concentration on the growth of giant clams Hippopus hippopus. In: Zaragoza, E. C., de Guzman, D. L., Gonzales, E. P. (eds.) Culture of giant clams (Bivalvia: Tridacnidae). Australian Centre for International Agricultural Research, Canberra, p. 57–61
Rahav, O., Dubinsky, Z., Achituv, Y., Falkowski, P. G. (1989). Ammonium metabolism in the zooxanthellae coral, Stylophora pistillata. Proc. R. Soc. (Ser. B) 236: 325–337
Rees, T. A. V. (1991). Are symbiotic algae nutrient deficient? Proc. R. Soc. (Ser. B) 243: 227–233
Rees, T. A. V., Fitt, W. K., Yellowlees, D. (1993). Host glutamine synthetase activation in the giant clam symbiosis: effect of clam size, elevated ammonium and continuous darkness. (In preparation)
Summons, R. E., Boag, T. S., Osmond, F. R. S. (1986). The effect of ammonium on photosynthesis and the pathway of ammonium assimilation in Gymnodinium microadriaticum in vitro and in symbiosis with tridacnid clams and corals. Proc. R. Soc. (Ser. B) 227: 147–159
Szmant-Froelich, A., Pilson, M. E. Q. (1984). Effects of feeding frequency and symbiosis with zooxanthellae on nitrogen metabolism and respiration of the coral Astrangia danae. Mar. Biol. 81: 153–162
Watson, T. C., Heslinga, G. A. (1988). Optimal harvest age for Tridacna derasa: maximizing biological production. In: Copland, J. W., Lucas, J. S. (ed.) Giant clams in Asia and the Pacific. Australian Centre for International Agricultural Research, Canberra p. 221–224
Wilkerson, F. P., Muscatine, L. (1984). Uptake and assimilation of dissolved inorganic nitrogen by a symbiotic sea anemone. Proc. R. Soc. (Ser. B) 221: 71–86
Wilkerson, F. P., Trench, R. K. (1986). Uptake of dissolved inorganic nitrogen by the symbiotic clam Tridacna gigas and the coral Acropora sp. Mar. Biol. 93: 237–246
Wood, E. D., Armstrong, F. A. J., Richards, F. A. (1967). Determination of nitrate in seawater by cadmium-copper reduction to nitrate. J. mar. biol. Ass. U.K. 47: 23–31
Yellowlees, D., Dionisio-Sese, M. L., Masuda, K., Maruyama, T., Abe, T., Baillie, B., Tsuzuki, M., Miyachi, S. (1993a). Role of carbonic anhydrase in the supply of inorganic carbon to the giant clam-zooxanthellae symbiosis. Mar. Biol. 115: 605–611
Yellowlees, D., Rees, T. A. V., Fitt, W. K. (1993b). The effect of ammonium supplemented sea water on the glutamine synthetase and glutamate dehydrogenase activities in host tissue and zooxanthellae of Pocillopora damicornis and on the ammonium uptake rates of the zooxanthellae. (In prepration)
Yonge, C. M., Nichols, A. G. (1931). Studies on the physiology of corals. 4. The structure, distribution and physiology of zooxanthellae. Scient Rep. Gt Barrier Reef Exped. 1: 135–176
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Fitt, W.K., Rees, T.A.V., Braley, R.D. et al. Nitrogen flux in giant clams: size-dependency and relationship to zooxanthellae density and clam biomass in the uptake of dissolved inorganic nitrogen. Marine Biology 117, 381–386 (1993). https://doi.org/10.1007/BF00349313
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DOI: https://doi.org/10.1007/BF00349313