Skip to main content
Log in

Resource partitioning by reef corals as determined from stable isotope composition

I. δ13C of zooxanthellae and animal tissue vs depth

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The pattern of resource partitioning vs depth by corals collected in February 1983 from Jamaica and the Red Sea was determined from their stable carbon isotope composition. Observations were made on isolated zooxanthellae and corresponding algae-free animal tissue from eight species at four depths over a 50 m bathymetric range. Zooxanthellae δ13C was high in shallow water and became lower as depth increased. This trend correlated significantly with the anual integrated photosynthetic rate. The trend is interpreted according to a “depletion-diffusion” hypothesis; in shallow water, at high rates of photosynthesis, metabolic CO2 is nearly depleted and the supply of CO2 from seawater bicarbonate is limited by diffusion. Since most of the available CO2 is fixed, isotope fractionation is minimal. In deeper water, at lower rates of photosynthesis, metabolic CO2 is ample, and isotope fractionation is greater. Animal tissue δ13C was slightly lower than corresponding zooxanthellae values in shallow water. As depth increased the difference between zooxanthellae and animal tissue δ13C increased and the latter approached the δ13C of oceanic particulate organic carbon. These data suggest that carbon is translocated at all depths and that deep-water corals draw significantly on allocthonous sources of carbon.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature cited

  • Appleby, G., Colbeck, J., Holdworth, E. S., Wadman, H. (1980). β-carboxylation enzymes in marine phytoplankton and isolation and purification of pyruvate carboxylase from Amphidinium carterae (Dinophyceae). J. Phycol. 16: 290–295

    Google Scholar 

  • Battey, J. F., Patton, J. S. (1984). A reevaluation of the role of glycerol in carbon translocation in zooxanthellae-coelenterate symbiosis. Mar. Biol. 79: 27–38

    Google Scholar 

  • Battey, J. F., Patton, J. S. (1986). Glycerol translocation in Condylactis gigantea. Mar. Biol. 95: 37–46

    Google Scholar 

  • Beardall, J., Mukerji, D., Glover, H. E., Morris, I. (1976). The path of carbon in photosynthesis by marine phytoplankton. J. Physcol. 12: 409–417

    Google Scholar 

  • Benedict, C. R. (1978). Nature of obligate photoautotrophy. Ann. Rev. Plant Physiol. 29: 67–93

    Google Scholar 

  • Benedict, C. R., Wong, W. C., Wong, J. H. H. (1980). Fractionation of the stable isotopes of inorganic carbon by seagrasses. Plant Physiol. 65: 512–517

    Google Scholar 

  • Black, C. C., Bender, M. M. (1976). 192-1 values in marine organisms from the Great Barrier Reef. Aust. J. Plant Physiol. 3: 25–32

    Google Scholar 

  • Black, C. C., Burris, J. E. (1983). Diurnal carbon-14 partitioning between zooxanthellae and the coral animal tissue of intact Seriatopora hystrix colonies. Mar. Biol. 75: 117–120

    Google Scholar 

  • Burris, J. E., Porter, J. W., Laing, W. A. (1983). Effects of carbon dioxide concentration on coral photosynthesis. Mar. Biol. 75: 113–116

    Google Scholar 

  • Cummings, C. E., McCarty, H. B. (1982). Stable carbon isotope ratios in Astrangia danae: evidence for algal modification of carbon pools used in calcification. Geochim. et Cosmochim. Acta 46: 1125–1129

    Google Scholar 

  • Davies, P. S. (1984). The role of zooxanthellae in the nutritional energy requirements of Pocillopora eydouxi. Coral Reefs 2: 181–186

    Google Scholar 

  • Degens, E. T., Guillard, R. R. L., Sackett, W. M., Hellebust, J. A. (1968). Metabolic fractionation of carbon isotopes in marine plankton. I. Temperature and respiration experiments. Deep-Sea Res. 15: 1–9

    Google Scholar 

  • Degens, E. T., Behrend, M., Gotthardt, B., Repmann, E. (1968). Metabolic fractionation of carbon isotopes in marine plankton. II. Data on samples collected off the coasts of Peru and Ecuador. Deep-Sea Res. 15: 11–20

    Google Scholar 

  • Deines, P. (1980). The isotopic composition of reduced organic carbon. In: Fritz, P., Fontes, J. (eds.) Handbook of environmental isotope geochemistry, Vol. 1. Elsevier, Amsterdam, p. 329–406

    Google Scholar 

  • D'Elia, C. F., Domotor, S. L., Webb, K. L. (1983). Nutrient uptake kinetics of freshly isolated zooxanthellae. Mar. Biol. 75: 157–167

    Google Scholar 

  • De Niro, M. J., Epstein, S. (1978). Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 42: 495–506

    Google Scholar 

  • Dennison, W. C., Barnes, D. J. (1987). Effects of water motion on coral photosynthesis and calcification. J. exp. mar. Biol. Ecol. (in press)

  • Descolas-Gros, C., Fontugne, M. R. (1985). Carbon fixation in marine phytoplankton: carboxylase activities and stable carbon isotope ratios; physiological and paleoclimatological aspects. Mar. Biol. 87: 1–6

    Google Scholar 

  • Deuser, W. G. (1970). Isotopic evidence for diminishing supply of available carbon during diatom bloom in the Black Sea. Nature, Lond. 225: 1069–1071

    Google Scholar 

  • Deuser, W. G., Degens, E. T. (1967). Carbon isotope fractionation in the system CO2(gas)−CO2(aqueous)−HCO3 -(aqueous). Nature, Lond. 215: 1033–1035

    Google Scholar 

  • Deuser, W. G., Degens, E. T., Guillard, R. R. L. (1968). Carbon isotope relationships between plankton and sea water. Geochim. Cosmochim. Acta 32: 657–660

    Google Scholar 

  • Deuser, W. G., Hunt, J. M. (1969). Stable isotope ratios of dissolved inorganic carbon in the Atlantic. Deep-Sea Res. 16: 221–225

    Google Scholar 

  • Edmunds, P. J., Spencer Davies, P. (1986). An energy budget for Porites porites (Scleractinia). Mar. Biol. 92: 339–347

    Google Scholar 

  • Edwards, G., Walker, D. A. (1983). C3, C4: mechanisms, and cellular regulation, of photosynthesis. Blackwell, Oxford

    Google Scholar 

  • Erez, J. (1977). Influence of symbiotic algae on the stable isotope composition of hermatypic corals: a radioactive tracer approach. Proc. 3rd int. Symp. coral Reefs 2: 563–569. [Taylor, D. L. (ed.) School of Marine and Atmospheric Sciences, University of Miami, Miami]

    Google Scholar 

  • Falkowski, P., Dubinsky, Z., Muscatine, L., Porter, J. W. (1984). Light and the bioenergetics of a symbiotic coral. BioSci 34: 705–709

    Google Scholar 

  • 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. 169: 230–245

    Google Scholar 

  • Goreau, T. F. (1961). Problems of growth and calcium deposition in reef corals. Endevour 20: 32–39

    Google Scholar 

  • Goreau, T. J. (1977a). Coral skeletal chemistry: physiological and environmental regulation of stable isotopes and trace metals in Montastrea annularis. Proc. R. Soc. Lond. B. 196: 291–315

    Google Scholar 

  • Goreau, T. J. (1977b). Carbon metabolism in calcifying and photosynthetic organisms: theoretical models based on stable isotope data. Proc. 3rd. int. Symp. coral Reefs 2: 395–401

    Google Scholar 

  • Graham, D., Smillie, R. M. (1976). Carbonate dehydratase in marine organisms of the Great Barrier Reef Aust. J. Plant Physiol 3: 113–119

    Google Scholar 

  • Hames, E. B., Montague, C. L. (1979). Food sources of estuarine invertebrates analyzed using 13C/12C ratios. Ecology 60: 48–56

    Google Scholar 

  • Hofmann, D. K., Kremer, B. P. (1981). Carbon metabolism and strobilation in Cassiopea andromeda (Cnidaria: Scyphozoa): significance of endosymbiotic dinoflagellates. Mar. Biol. 65: 25–33

    Google Scholar 

  • Kerby, N. W., Raven, J. A. (1985). Transport and fixation of inorganic carbon by marine algae. Adv. bot. Res. 11: 71–123

    Google Scholar 

  • Kokke, W. C. M. C., Epstein, S., Look, S. A., Rau, G. H., Fenical, W., Djerassi, C. (1984). On the origin of terpenes in symbiotic associations between marine invertebrates and algae (zooxanthellae). J. Biol. Chem. 259: 8168–8173

    Google Scholar 

  • Kremer, B. P., Berks, R. (1978). Photosynthesis and carbon metabolism in marine and freshwater diatoms. Z. Pflanzenphysiol. 87: 149–169

    Google Scholar 

  • Land, L. S., Lang, J. C., Smith, B. N. (1975). Preliminary observations on the carbon isotopic composition of some reef coral tissues and symbiotic zooxanthellae. Limnol. Oceanogr. 20: 283–287

    Google Scholar 

  • Land, L. S., Lang, J. C., Barnes, D. J. (1977). On the stable carbon and oxygen isotopic composition of some shallow water, ahermatypic, scleractinian coral skeletons. Geochim. Cosmochim. Acta 41: 169–172

    Google Scholar 

  • Lewis, J. B. (1976). Experimental tests of suspension feeding in Atlantic reef corals. Mar. Biol. 36: 147–150

    Google Scholar 

  • Lewis, J. B. (1977). Suspension feeding in Atlantic reef corals and the importance of suspended particulate material as a food source. Proc. 3rd int. Symp. coral Reefs 1: 405–408. [Taylor, D. L. (ed.) School of Marine and Atmospheric Scienes, University of Miami, Miami]

    Google Scholar 

  • Meyers, P., Porter, J. W., Chad, R. L. (1978) Depth analysis of fatty acis in two Caribbean reef corals. Mar. Biol. 49: 197–202

    Google Scholar 

  • Meyers, P. (1979). Polyunsaturated fatty acids in coral: indicators of nutritional sources. Mar. Biol. Lett. 1: 69–75

    Google Scholar 

  • McCloskey, L. R. and L. Muscatine (1984). Production and respiration in the Red Sea coral Stylophora pistillata as a function of depth. Proc. R. Soc. Lond. B. 222: 215–230

    Google Scholar 

  • Minegawa, M., Winter, D. A., Kaplan, I. R. (1984). Comparison of Kjeldahl and combustion methods for measurement of nitrogen isotope ratios in organic matter. Anal. Chem. 56: 1859–1861

    Google Scholar 

  • Mook, W. G., Bommerson, J. C., Staverman, W. H. (1974). Carbon isotope fractionation between dissolved bicarbonate and gaseous carbon dioxide. Earth Plan. Sci. Lett. 22: 169–176

    Google Scholar 

  • Morris, I. (1980). Paths of carbon assimilation in marine phytoplankton. In: Falkowski, P. G. (ed.) Primary productivity in the sea. Plenum, New York, p. 139–157

    Google Scholar 

  • Muscatine, L. (1980). Productivity of zooxanthellae. In: Falkowski, P. G. (ed.) Primary productivity in the sea. Plenum, New York, p. 381–402

    Google Scholar 

  • Muscatine, L., Porter, J. W. (1977). Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Biosci. 27: 454–460

    Google Scholar 

  • Muscatine, L., Falkowski, P., Porter, J. Dubinsky, Z. (1984). Fate of photosynthetic-fixed carbon in light and shade-adapted colonies of the symbiotic coral Stylopora pistillata. Proc. R. Soc. Lond. B. 222: 181–202

    Google Scholar 

  • Muscatine, L., McCloskey, L. R., Loya, Y. (1985). A comparison of the growth rates of zooxanthellae and animal tissue in the Red Sea coral Stylophora pistillata. Proc. 5th int. coral Reef Congr. 6: 119–123. [Gabrie, C. et al. (eds.) Antenne Museum-EPHE, Moorea, French Polynesia]

    Google Scholar 

  • O'Leary, M. H. (1981). Carbon isotope fractionation in plants. Phytochemistry 20: 553–567

    Google Scholar 

  • Pardue, J. W., Scalan, R. S., Van Baalen, C., Parker, P. C. (1976). Maximum carbon isotope fractionation in photosynthesis by blue-green algae and a green alga. Geochim. Cosmochim. Acta 40: 309–312

    Google Scholar 

  • Porter, J. W. (1974). Zooplankton feeding by the Caribbean reef-building coral Montastrea cavernosa. Proc. 2nd int. Symp. coral Reefs 1: 111–125. [Cameron, A. M. et al. (eds.) Great Barrier Reef Committee, Brisbane]

    Google Scholar 

  • Porter, J. W. (1976). Autotrophy, heterotrophy and resource partitioning in Caribbean reef-building corals. Am. Nat. 110: 731–742

    Google Scholar 

  • Porter, J. W. (1980). Primary productivity in the sea: reef corals in situ. In: Falkowski, P. (ed.) Primary productivity in the sea. Plenum, New York, p. 403–410

    Google Scholar 

  • Porter, J. W. (1985). The maritime weather of Jamaica: its effects on animal carbon budgets of the massive reef-building coral Montastrea annularis. Proc. 5th int. coral Reef Congr. 6: 362–367. [Gabrie, C. et al. (eds.) Antenne Museum-EPHE, Moorea, French Polynesia]

    Google Scholar 

  • Porter, J. W., Muscatine, L., Dubinsky, Z., Fakowski, P. G. (1984). Primary production and photoadaptation in light and shadeadapted colonies of the symbiotic coral Stylophora pistillata. Proc. R. Soc. Lond. B 222: 161–180

    Google Scholar 

  • Rau, G. (1981). Hydrothermal vent clam and tube worm 13C/12C: further evidence of nonphotosynthetic food sources. Science, N.Y. 213: 338–339

    Google Scholar 

  • Rau, G., Anderson, N. H. (1981). Use of 13C/12C to trace dissolved and particulate organic matter utilization by populations of an aquatic invertebrate. Oecologia 48: 19–21

    Google Scholar 

  • Rau, G. H., Sweeney, R. E., Kaplan, I. R. (1982). Plankton 13C/12C ratio changes with latitude: differences between northern and southern oceans. Deep-Sea Res. 29: 1035–1039

    Google Scholar 

  • Rau, G., Mearns, A. J., Young, D. R., Olson R. J., Shafer, H. A., Kaplan, I. R. (1983). Animal 13C/12C correlates with trophic level in pelagic food webs. Ecology 64: 1314–1318

    Google Scholar 

  • Rinkevich, B., Loya, Y. (1983). Oriented translocation of energy in grafted reef corals. Coral Reefs 1: 243–247

    Google Scholar 

  • Sackett, W. M., Eckelmann, W. R., Bender, M. L., Bé, A. W. H. (1965). Temperature dependence of carbon isotope composition in marine plankton and sediments. Science, N.Y. 148: 235–237

    Google Scholar 

  • Schmitz, K., Kremer, B. P. (1977). Carbon fixation and analysis of assimilates in a coral-dinoflagellate symbiosis. Mar. Biol. 42: 305–313

    Google Scholar 

  • Smith, F. A., Walker, N. A. (1980). Photosynthesis by aquatic plants: effects of unstirred layers in relation to assimilation of CO2 and HCO3 - and to carbon isotopic discrimination. New Phytol. 86: 245–259

    Google Scholar 

  • Streamer, M., McNeil, Y., Yellowlees, D. (1986). The short-term partitioning of carbon-14 assimilate between zooxanthellae and polyp tissue in Acropora formosa. Mar. Biol. 90: 565–573

    Google Scholar 

  • Ting, I. P. (1976). Malate dehydrogenase and other enzymes of C4 acid metabolism in marine plants. Aust. J. Plant Physiol. 3: 121–127

    Google Scholar 

  • Trench, R. K., Wethey, D. S., Porter, J. W. (1981). Observations on the symbiosis with zooxanthellae among the Tridacnidae (Mollusca, Bivalvia). Biol. Bull. 161: 180–198

    Google Scholar 

  • Trench, R. K., Fisher, C. R. (1983). Carbon dioxide fixation in Symbiodinium microadriaticum: problems with mechanisms and pathways. Endocytobiology 2: 659–673

    Google Scholar 

  • Troughton, J. H. (1979). 193-1 as an indicator of carboxylation reactions. In: Gibbs, M., Latzko E. (eds.) Encyclopedia of plant physiology (new series). Photosynthesis, Vol. II, p. 140–149, Springer, Berlin

    Google Scholar 

  • Tytler, E. M., Trench, R. K. (1986). Activities of enzymes in β-carboxylation reactions and of catalase in cell-free preparations from the symbiotic dinoflagellates Symbiodinium spp. from a coral, a clam, a zoanthid and two sea anemones. Proc. R. Soc. Lond. B. 228: 483–492

    Google Scholar 

  • Weber, J. N., Deines, P., Weber, P. H., Baker, P. (1976). Depth related changes in the 13C/12C ratio of skeletal carbonate deposited by the Caribbean reef-frame building coral Montastrea annularis: further implications of a model for stable isotope fractionation by scleractinian corals. Geochim. et Cosmochim. Acta 40: 31–39

    Google Scholar 

  • Wefer, G., Killingley, J. S. (1986). Carbon isotopes in organic matter from a benthic alga Halimeda incrassata (Bermuda): Effects of light intensity. Chem. Geol. 59: 321–326

    Google Scholar 

  • Weil, S. M., Buddemeier, R. W., Smith, S. V., Kroopnick, P. M. (1982). The stable isotope composition of coral skeletons: control by environmental variables. Geochim. Cosmochim. Acta 45: 1147–1153

    Google Scholar 

  • Weis, V. M., Smith, G. J., Muscatine, L. (1988). A “CO2 supply” mechanism in zooxanthellae cnidarians: Role of carbonic anhydrase. Mar. Biol. (present issue)

  • Williams, P. M., Gordon, L. I. (1970). Carbon-13: carbon-12 ratios in dissolved and particulate organic matter in the sea. Deep-Sea Res. 17: 19–27

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by P. C. Schroeder, Pullman

Contribution No. 436 of the Discovery Bay Marine Laboratory of the University of the West Indies

Rights and permissions

Reprints and permissions

About this article

Cite this article

Muscatine, L., Porter, J.W. & Kaplan, I.R. Resource partitioning by reef corals as determined from stable isotope composition. Marine Biology 100, 185–193 (1989). https://doi.org/10.1007/BF00391957

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00391957

Keywords

Navigation