The Role of Plankton in Coral Trophodynamics



Historically, reef-building corals have been considered to be photoautotrophs due to their symbiosis with dinoflagellates that transfer photosynthetically fixed carbon to the animal tissue. Nevertheless, corals also obtain carbon heterotrophically through capture of plankton, ingestion of suspended particulate matter, and uptake of dissolved organic compounds. This review assesses the effects of heterotrophy on coral physiology, and how strongly feeding on all of these food sources contributes to coral energy budgets. Evidence in the literature demonstrates that feeding has a positive effect on coral tissue, enhancing the growth of both partners of the symbiosis. Nevertheless, the effects of feeding are light dependent: in general, tissue quality (lipid and protein composition) is enhanced in the presence of an adequate food source only under low-light conditions or in bleached corals. On the other hand, growth rates are typically highest under conditions of high light and food availability. However, under low-light conditions, feeding can provide a mechanism to maintain skeletal growth rates even though photosynthesis is reduced. Overall, a strong interaction between autotrophy and heterotrophy is apparent for scleractinian corals. Feeding can play a central role in maintaining physiological function when autotrophy is reduced. Moreover, taking all food sources into account, heterotrophy contributes more strongly to coral energy budgets than was previously thought. Nevertheless, not all symbiotic corals can sufficiently upregulate heterotrophic feeding to compensate for reduced photosynthesis, and identifying which coral species are facultative heterotrophs should be a focus of future research.


Feeding heterotrophy photosynthesis coral physiology 


  1. Al-Moghrabi S, Allemand D, Jaubert J (1993) Valine uptake by the scleractinian coral Galaxea fascicularis characterization and effect of light and nutritional status. J Comp Physiol B 163:355–362CrossRefGoogle Scholar
  2. Al-Moghrabi S, Allemand D, Couret JM (1995) Fatty acid of the scleractinian coral Galaxea fascicularis: effect of light and feeding. J Comp Physiol B 165:183–192CrossRefGoogle Scholar
  3. Allemand D, Tambutté E, Girard JP, Jaubert J (1998) Organic matrix synthesis in the scleractinian coral Stylophora pistillata: role in biomineralization and potential target of the organotin tribulyltin. J Exp Biol 201:2001–2009Google Scholar
  4. Anthony KRN (1999) Coral suspension feeding on fine particulate matter. J Exp Mar Biol Ecol 232:85–106CrossRefGoogle Scholar
  5. Anthony KRN, Connolly SR (2004) Environmental limits to growth: physiological niche boundaries of corals along turbidity-light gradients. Oecologia 141(3):373–384CrossRefGoogle Scholar
  6. Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J Exp Mar Biol Ecol 252:221–253CrossRefGoogle Scholar
  7. Anthony KRN, Connolly SR, Willis BL (2002) Comparative analysis of energy allocation to tissue and skeletal growth in corals. Limnol Oceanogr 47:1417–1429CrossRefGoogle Scholar
  8. Bachok Z, Mfilinge P, Tsuchiya M (2006) Characterization of fatty acid composition in healthy and bleached corals from Okinawa, Japan. Coral Reefs 25:545–554CrossRefGoogle Scholar
  9. Bagdley BD, Lipschultz F, Sebens K (2006) Nitrate uptake by the reef coral Diploria strigosa: effects of concentration, water flow and irradiance. Mar Biol 149(2):327–338Google Scholar
  10. Bak RPM, Joenje M, DeJong I, Lambrechts DYM, Newland G (1998) Bacterial suspension feeding by coral reef benthic organisms. Mar Ecol Prog Ser 175:285–288CrossRefGoogle Scholar
  11. Barnes DJ, Crossland CJ (1980) Diurnal and seasonal variations in the growth of a staghorn coral measured by time-lapse photography. Limnol Oceanogr 25:1113–1117CrossRefGoogle Scholar
  12. Barnes DJ, Lough JM (1993) On the nature and causes of density banding in massive coral skeletons. J Exp Mar Biol Ecol 167:91–108CrossRefGoogle Scholar
  13. Belcher AM, Wux XH, Christensen RJ, Hansma PK, Stucky GD, Morse DE (1996) Control of crystal phase switching and orientation by soluble mollusc shell proteins. Nature 381:56–58CrossRefGoogle Scholar
  14. Bythell JC (1988) A total nitrogen and carbon budget for the elkhorn coral Acropora palmata (Lamarck). Proc 6th Int Coral Reef Symp 2:535–540Google Scholar
  15. Clayton WS Jr, Lasker KE (1982) Effects of light and dark treatments of feeding by the reef coral Pocillopora damicornis. J Exp Mar Biol Ecol 63:269–280CrossRefGoogle Scholar
  16. Clayton WS Jr, Lasker KE (1984) Host feeding regime and zooxanthellae photosynthesis in the anemone Aiptasia pallida. Biol Bull 167:590–600CrossRefGoogle Scholar
  17. Cook CB (1972) Benefit for symbiotic zoochlorella from feeding by green hydra. Biol Bull 142:236–242CrossRefGoogle Scholar
  18. Cook CB, Davy SK (2001) Are free amino acids responsible for the “host factor” effects on symbiotic zooxanthellae in extracts of host tissue? Hydrobiologia 461(1–3):71–78CrossRefGoogle Scholar
  19. Cook CB, D’Elia CF, Muller-Parker G (1988) Host feeding and nutrient sufficiency for zooxanthellae in the sea anemone Aiptasia pallida. Mar Biol 98:253–262CrossRefGoogle Scholar
  20. Coles SL (1969) Quantitative estimate of feeding and respiration of three corals. Limnol Oceanogr 14:949–953CrossRefGoogle Scholar
  21. Conover RJ (1966) Assimilation of organic matter by zooplankton. Limnol Oceanogr 11:338–345CrossRefGoogle Scholar
  22. Crossland CJ (1987) In situ release of mucus and DOC-lipid from the corals Acropora variabilis and Stylophora pistillata in different light regimes. Coral Reefs 6:35–43CrossRefGoogle Scholar
  23. Cuif JP, Gautret P (1995) Glucides et protéines de la matrice soluble des biocristaux de scléractiniaires Acroporidés. C R A S Paris II 320:273–278Google Scholar
  24. D’Elia CF (1977) The uptake and release of dissolved phosphorus by reef corals. Limnol Oceanogr 22:301–315CrossRefGoogle Scholar
  25. D’Elia CF, Cook CB (1988) Methylamine uptake by zooxanthellae-invertebrate symbioses: insights into host ammonium environment and nutrition. Limnol Oceanogr 33:1153–1165CrossRefGoogle Scholar
  26. Davies PS (1991) Effect of daylight variations on the energy budgets of shallow water corals. Mar Biol 108:137–144CrossRefGoogle Scholar
  27. Davy SK, Cook CB (2001) The relationship between nutritional status and carbon flux in the zooxanthellate sea anemones Aiptasia pallida. Mar Biol 119:999–105Google Scholar
  28. Davy SK, Withers KJT, Hinde R (2006) Effects of host nutritional status and seasonality on the nitrogen status of zooxanthellae in the temperate coral Plesiastrea versipora (Lamarck). J Exp Mar Biol Ecol 335:256–265CrossRefGoogle Scholar
  29. DiSalvo LH (1972) Bacterial counts in surface open waters of Eniwetok Atoll, Marshall Islands. Atoll Res Bull 151:1–5Google Scholar
  30. Dubinsky Z, Stambler N, Ben-Zion M, McCloskey LR, Muscatine L, Falkowski PG (1990) The effect of external nutrient resources on the optical properties and photosynthetic efficiency of Stylophora pistillata. Proc R Soc Lond B 239:231–246CrossRefGoogle Scholar
  31. Edmunds PJ, Davies PS (1986) An energy budget for Porites porites (Scleractinian). Mar Biol 92:339–347CrossRefGoogle Scholar
  32. Erez J (1978) Vital effect on stable-isotope composition seen foraminifera and coral skeletons. Nature 273:199–202CrossRefGoogle Scholar
  33. Fabricius KE, Metzner J (2004) Scleractinian walls of mouths: predation on coral larvae by corals. Coral Reefs 23:245–248CrossRefGoogle Scholar
  34. Fabricius KE, Yahel G, Genin A (1995) Herbivory in asymbiotic soft corals. Science 268:90–93CrossRefGoogle Scholar
  35. Falini G, Albeck S, Weiner S, Addadi L (1996) Control of aragonite or calcite polymorphism by mollusk shell macromolecules. Science 271:67–69CrossRefGoogle Scholar
  36. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and bioenergetics of a symbiotic coral. Bioscience 11:705–709CrossRefGoogle Scholar
  37. Farrant PA, Borowitzka MA, Hinde R, King RJ (1987) Nutrition of the temperate Australian coral Capnella gaboensis. Mar Biol 95:575–581CrossRefGoogle Scholar
  38. Felis T, Pätzold J, Loya Y, Wefer G (1998) Vertical water mass mixing and plankton blooms recorded in skeletal stable carbon isotopes of a Red Sea coral. J Geophys Res 103:731–739CrossRefGoogle Scholar
  39. Ferrier MD (1991) Net uptake of dissolved free amino acids by four scleractinian corals. Coral Reefs 10:183–187CrossRefGoogle Scholar
  40. Ferrier-Pagès C, Gattuso JP, Cawet G, Jaubert J, Allemand D (1998) Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis. Mar Ecol Prog Ser 172:265–274CrossRefGoogle Scholar
  41. Ferrier-Pagès C, Witting J, Tambutté E, Sebens KP (2003) Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22:229–240CrossRefGoogle Scholar
  42. Fitt WK, Cook CB (2001) The effects of feeding or addition of dissolved inorganic nutrients in maintaining the symbiosis between dinoflagellates and a tropical marine cnidarian. Mar Biol 139:507–517CrossRefGoogle Scholar
  43. Fitt WK, Pardy RL, Littler MM (1982) Photosynthesis, respiration, and contribution to community productivity of the symbiotic sea anemone Anthopleura elegantissima (Brandt 1835). J Exp Mar Biol Ecol 61:213–232CrossRefGoogle Scholar
  44. Furla P, Allemand D, Orsenigo MN (2000) Involvement of H + -ATPase and carbonic anhydrase in inorganic carbon uptake for endosymbiont photosynthesis. Am J Physiol 278:870–881Google Scholar
  45. Furla P, Allemand D, Shick JM, Ferrier-Pagès C, Richier S, Plantivaux A, Merle PL, Tambutté S (2005) The symbiotic anthozoan: a physiological chimera between alga and animal. Int Comp Biol 45(4):595–604CrossRefGoogle Scholar
  46. Gagan MK, Chivas AR, Isdale PJ (1996) Timing coral based climatic histories using 13C enrichments driven by synchronized spawning. Geology 24:1009–1012CrossRefGoogle Scholar
  47. Gattuso JP, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review of interactions and control by carbonate chemistry. Integr Comp Biol 39(1):160–183CrossRefGoogle Scholar
  48. Goreau TF, Goreau NI (1960) Distribution of labeled carbon in reef-building corals with and without zooxanthellae. Science 131:668–669CrossRefGoogle Scholar
  49. Goreau TF, Goreau NI, Yonge CM (1971) Reef corals: autotrophs or heterotrophs? Biol Bull 141:247–260CrossRefGoogle Scholar
  50. Grottoli AG (2002) Effect of light and brine shrimp on skeletal delta C-13 in the Hawaiian coral Porites compressa: a tank experiment. Geochim Cosmochim Acta 66:1955–1967CrossRefGoogle Scholar
  51. Grottoli AG, Rodrigues LJ, Juarez C (2004) Lipids and stable carbon isotopes in two species of Hawaiian corals, Porites compressa and Montipora verrucosa, following a bleaching event. Mar Biol 145:621–631CrossRefGoogle Scholar
  52. Grottoli A, Rodrigues L, Palardy J (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189CrossRefGoogle Scholar
  53. Grover R, Maguer JF, Reynaud-Vaganay S, Ferrier-Pagès C (2002) Uptake of ammonium by the scleractinian coral Stylophora pistillata: effect of feeding, light and ammonium concentrations. Limnol Oceanogr 47:782–790CrossRefGoogle Scholar
  54. Grover R, Maguer JF, Allemand D, Ferrier-Pagès C (2003) Nitrate uptake by the scleractinian coral Stylophora pistillata. Limnol Oceanogr 48(6):2266–2274CrossRefGoogle Scholar
  55. Grover R, Maguer JF, Allemand D, Ferrier-Pagès C (2006) Urea uptake by the scleractinian coral Stylophora pistillata. J Exp Mar Biol 332:216–225CrossRefGoogle Scholar
  56. Grover R, Maguer J-F, Allemand D, Ferrier-Pagès C (2008) Uptake of dissolved free amino acids (DFAA) by the scleractinian coral Stylophora pistillata. J Exp Biol 211:860–865CrossRefGoogle Scholar
  57. Harland AD, Navarro JC, Davies PS, Fixter LM (1993) Lipids of some Carribbean and Red Sea corals: total lipid, wax esters, triglycerides and fatty acids. Mar Biol 117:113–117CrossRefGoogle Scholar
  58. Heidelberg KB, Sebens KP, Purcell JE (2004) Composition and sources of near reef zooplankton on a Jamaican forereef along with implications for coral feeding. Coral Reefs 23:263–276CrossRefGoogle Scholar
  59. Heikoop JM, Dunn JJ, Risk MJ, McConnaughey TA, Sandman IM (2000) Separation of kinetic and metabolic effect in carbon-13 records preserved in reef coral skeletons. Geochim Cosmochim Acta 64:975–987CrossRefGoogle Scholar
  60. Herndl GJ, Velimirov B (1985) Bacteria in the coelenteron of Anthozoa: control of coelenteric bacterial density by the coelenteric fluid. J Exp Mar Biol Ecol 93:115–130CrossRefGoogle Scholar
  61. Hill R, Ralph PJ (2006) Photosystem II heterogeneity of in hospite zooxanthellae in scleractinian corals exposed to bleaching conditions. Photochem Photobiol 82:1577–1585Google Scholar
  62. Hoegh-Guldberg O (1999) Coral bleaching, climate change, and the future of the world’s coral reefs. Mar Freshwater Res 50:839–866CrossRefGoogle Scholar
  63. Hoegh-Guldberg O, Smith GJ (1989) 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 57:173–186CrossRefGoogle Scholar
  64. Hoegh-Guldberg O, Williamson J (1999) Availability of two forms of dissolved nitrogen to the coral Pocillopora damicornis and its symbiotic zooxanthellae. Mar Biol 133:561–570CrossRefGoogle Scholar
  65. Holzman R, Reidenbach MA, Monismith SG, Koseff JR, Genin A (2005) Near-bottom depletion of zooplankton over a coral reef. II. Relationships with zooplankton swimming ability. Coral Reefs 24:87–94CrossRefGoogle Scholar
  66. Houlbrèque F, Tambutté E, Ferrier-Pagès C (2003) Effects of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 296:145–166CrossRefGoogle Scholar
  67. Houlbrèque F, Tambutté E, Allemand D, Ferrier-Pagès C (2004a) Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Biol 207:1461–1469CrossRefGoogle Scholar
  68. Houlbrèque F, Tambutté E, Richard C, Ferrier-Pagès C (2004b) Importance of a micro-diet for scleractinian corals. Mar Ecol Prog Ser 282:151–160CrossRefGoogle Scholar
  69. Howe SA, Marshall AT (2001) Thermal compensation of metabolism in the temperate coral, Plesiastrea versipora (Lamarck, 1816). J Exp Mar Biol Ecol 259:231–248CrossRefGoogle Scholar
  70. Huettel M, Wild C, Gonelli S (2006) Mucus trap in coral reefs: formation and temporal evolution of particle aggregates caused by coral mucus. Mar Ecol Prog Ser 307:69–84CrossRefGoogle Scholar
  71. Johannes RE (1974) Sources of nutritional energy for reef corals. Proc 2nd Int Coral Reef Symp 1:133–137, BrisbaneGoogle Scholar
  72. Johannes RE, Tepley L (1974) Examination of feeding on the reef coral Porites lobata in situ using time lapse photography. Proc 2nd Int Coral Reef Symp 1:127–131, BrisbaneGoogle Scholar
  73. Johannes RE, Cole S, Kuenzel NT (1970) The role of zooplankton in the nutrition of some scleractinian corals. Limnol Oceanogr 15:579–586CrossRefGoogle Scholar
  74. Johnson AS, Sebens KP (1993) Consequences of flattened morphology: Effects of flow on feeding rates of the scleractinian coral Meandrina meandrites. Mar Ecol Prog Ser 1–2:99–104CrossRefGoogle Scholar
  75. Juillet-Leclerc A, Gattuso JP, Montaggioni LF, Pichon M (1997) Seasonal variation of primary productivity and skeletal δ13C and δ 18O in the zooxanthellate scleractinian coral Acropora formosa. Mar Ecol Prog Ser 157:109–117CrossRefGoogle Scholar
  76. Jokiel PL, Maragos JE, Franzisket L (1978) Coral growth: buoyant weight technique. In: Stoddart DR, Johannes RE (eds) Coral reefs: research methods. UNESCO monographs on oceanographic methodology, Paris, pp 529–542Google Scholar
  77. Kim K, Lasker HR (1998) Allometry of resource capture in colonial cnidarians and constraints on modular growth. Funct Ecol 12:646–654CrossRefGoogle Scholar
  78. Kramarsky-Winter E, Harel M, Siboni N, Ben Dov E, Brickner I, Loya Y, Kushmaro A (2006) Identification of a protist-coral association and its possible ecological role. Mar Ecol Prog Ser 317:67–73CrossRefGoogle Scholar
  79. Kramer PA, Swart PK, Szmant AM (1993) The influence of different sexual reproductive patterns on density banding and stable isotopic compositions of corals. Proc 7th Int Coral Reef Symp 1:222Google Scholar
  80. LaJeunesse TC (2001) Investigating the biodiversity, ecology and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37:866–880CrossRefGoogle Scholar
  81. Lough JM, Barnes DJ (1997) Several centuries of variation of skeletal extension, density and calcification in massive Porites colonies from the Great Barrier Reef: a proxy for seawater temperature and a background of variability against which to identify unnatural change. J Exp Mar Biol Ecol 211:29–67CrossRefGoogle Scholar
  82. Marubini F, Davies PS (1996) Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar Biol 127:319–328CrossRefGoogle Scholar
  83. Marubini F, Thake B (1999) Bicarbonate addition promotes coral growth. Limnol Oceanogr 44(3):716–720CrossRefGoogle Scholar
  84. McAuley PJ (1992) The effect of maltose release on growth and nitrogen metabolism of symbiotic Chlorella. Br Phycol J 27:417–422CrossRefGoogle Scholar
  85. McConnaughey TA (1989) 13C and 18O isotopic disequilibrium in biological carbonates: I Patterns. Geochim Cosmochim Acta 53:151–162CrossRefGoogle Scholar
  86. McConnaughey TA, Whelan FF (1997) Calcification generates protons for nutrient an bicarbonate uptake. Earth Sci Rev 42:92–117CrossRefGoogle Scholar
  87. McGuire MP, Szmant AM (1997) Time course of physiological responses to NH4 enrichment by a coral-zooxanthellae symbiosis. Proc 8th Coral Reef Symp 1:909–914Google Scholar
  88. Meyer JL, Schultz ET (1985) Tissue condition and growth rate of corals associated with schooling fish. Limnol Oceanogr 30:157–166CrossRefGoogle Scholar
  89. Miller MW (1995) Growth of a temperate coral: effects of temperature, light, depth and heterotrophy. Mar Ecol Prog Ser 122:217–225CrossRefGoogle Scholar
  90. Mills MM (2000) Corals feeding on sediments? Ingestion, assimilation, and contributions to coral nutrition. PhD thesis, University of Maryland, College ParkGoogle Scholar
  91. Mills MM, Lipschultz F, Sebens KP (2004) Particulate matter ingestion and associated nitrogen uptake by four species of scleractinian corals. Coral Reefs 23:311–323CrossRefGoogle Scholar
  92. Muller-Parker G (1985) Effect of feeding regime and irradiance on the photophysiology of the symbiotic sea anemone Aiptasia pulchella. Mar Biol 90:65–74CrossRefGoogle Scholar
  93. Muller-Parker G, Cook CB, D’elia CF (1994a) Elemental composition of the coral Pocillopora damicornis exposed to elevated seawater ammonium. Pac Sci 48:234–246Google Scholar
  94. Muller-Parker G, McCloskey LR, Hoegh-Guldberg O, McAuley PJ (1994b) Effect of ammonium enrichment on animal and algal biomass of the coral Pocillopora damicornis. Pac Sci 48:273–282Google Scholar
  95. Muscatine L (1973) Nutrition of corals. In: Jones OA, Endean R (eds) Biology and geology of coral reefs. Academic, New York, pp 77–115Google Scholar
  96. Muscatine L (1980) Productivity of zooxanthellae. In: Falkowski PG (ed) Primary productivity in the Sea. Plenum Publishing Corporation, New York, pp 381–402Google Scholar
  97. Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27:454–460CrossRefGoogle Scholar
  98. Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611CrossRefGoogle Scholar
  99. Muscatine L, Falkowski PG, Porter JW, Dubinsky Z (1984) Fate of photosynthetic fixed carbon in light- and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc Lond B 222:181–202CrossRefGoogle Scholar
  100. Muscatine L, Fallowski PG, Dubinsky Z, Cook PA, McCloskey LR (1989) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proc R Soc Lond B 236(1284):311–324CrossRefGoogle Scholar
  101. Muscatine L, Ferrier-Pagès C, Blackburn A, Gates RD, Baghdasarian G, Allemand D (1998) Cell-specific density of symbiotic dinoflagellates in tropical anthozoaires. Coral Reefs 17:329–337CrossRefGoogle Scholar
  102. Muscatine L, Goiran C, Land L, Jaubert J, Cuif J-P, Allemand D (2005) Stable isotopes (δ15N and δ13C) of organic matrix from coral skeleton. Proc Natl Acad Sci 102(5):1525–1530CrossRefGoogle Scholar
  103. Owens NJP (1987) Natural variations in 15 N in the marine environment. Adv Mar Biol 24:389–451CrossRefGoogle Scholar
  104. Palardy JE, Grottoli AG, Matthews KA (2005) Effects of upwelling, depth, morphology and polyp size on feeding in three species of Panamian corals. Mar Ecol Prog Ser 300:79–89CrossRefGoogle Scholar
  105. Palardy JE, Grottoli AG, Matthews KA (2006) Effect of naturally changing zooplankton concentrations on feeding rates of two coral species in the Eastern Pacific. J Exp Mar Biol Ecol 331:99–107CrossRefGoogle Scholar
  106. Papina M, Meziane T, Van Woesik R (2007) Acclimation effect on fatty acids of the coral Montipora digitata and its symbiotic algae. Comp Biochem Physiol B 147:583–589CrossRefGoogle Scholar
  107. Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320CrossRefGoogle Scholar
  108. Piniak G, Lipschultz F, McClelland J (2003) Assimilation and partitioning of prey nitrogen within two anthozoans and their endosymbiotic zooxanthellae. Mar Ecol Prog Ser 262:125–136CrossRefGoogle Scholar
  109. Porter JW (1974) Zooplankton feeding by the Caribbean reef-building coral Montastrea cavernosa. Proc 2nd Int Coral Reef Symp 1:111–125Google Scholar
  110. Porter JW (1976) Autotrophy, heterotrophy and resource partitioning in Caribbean reef-building corals. Am Nat 110(975):731–742CrossRefGoogle Scholar
  111. Pratchett MS (1995) Dietary overlap among coral-feeding butterflyfishes (Chaetodontidae) at Lizard Island, northern Great Barrier Reef. Mar Biol 148:373–38CrossRefGoogle Scholar
  112. Pratchett MS, Gust N, Goby G, Klanten SO (2001) Consumption of coral propagules represents a significant trophic link between corals and reef fish. Coral Reefs 20:13–17CrossRefGoogle Scholar
  113. Rahav O, Dubinsky Z, Achituv Y, Falkowski PG (1989) Ammonium metabolism in the zooxanthellate coral Stylophora pistillata. Proc R Soc Lond B 236:325–337CrossRefGoogle Scholar
  114. Rau GH, Mearns AJ, Young DR, Olson RJ, Schafer HA, Kaplan IR (1983) Animal 13C/12C correlates with trophic level in pelagic food webs. Ecology 64:1314–1318CrossRefGoogle Scholar
  115. Rau GH, Ainley DG, Bengtson JL, Torres JJ, Hopkins TL (1992) 15 N/14 N and 13C/12C in Weddell sea birds, seals, and fish: implications for diet and trophic structure. Mar Ecol Prog Ser 84:1–8CrossRefGoogle Scholar
  116. Reynaud S, Ferrier-Pagès C, Sambrotto R, Juillet-Leclerc A, Jaubert J, Gattuso J-P (2002) Effect of feeding on the carbon and oxygen isotopic composition in the tissue and skeleton of the scleractinian coral Stylophora pistillata. Mar Ecol Prog Ser 238:81–89CrossRefGoogle Scholar
  117. Ribes M, Coma R, Gili J-M (1998) Heterotrophic feeding by gorgonian corals with symbiotic zooxanthella. Limnol Oceanogr 43:1170–1179CrossRefGoogle Scholar
  118. Richman S, Loya Y, Slobodkin LB (1975) The rate of mucus production by corals and its assimilation by the coral reef copepod Acartia negligens. Limnol Oceanogr 20:918–923CrossRefGoogle Scholar
  119. Rodolfo-Metalpa R, Peirano A, Houlbrèque F, Abbate M, Ferrier-Pagès C (2008) Effects of temperature, light and heterotrophy on the growth rate and budding of the temperate coral Cladocora caespitosa. Coral Reefs 27:17–25CrossRefGoogle Scholar
  120. Rodrigues L, Grottoli AG (2007) Energy reserves and metabolism as indicators of coral recovery from bleaching. Limnol Oceanogr 52:1874–1882CrossRefGoogle Scholar
  121. Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Carribean coral Montastrea franksii. Coral Reefs 20:85–91CrossRefGoogle Scholar
  122. Rosenfeld M, Bresler V, Abelson A (1999) Sediment as a possible source of food for corals. Ecol Lett 2:345–348CrossRefGoogle Scholar
  123. Sammarco PW, Risk MJ, Schwarcz HP, Heikoop JM (1999) Cross-continental shelf trends in coral delta N-15 on the Great Barrier Reef: further consideration of the reef nutrient paradox. Mar Ecol Prog Ser 180:131–138CrossRefGoogle Scholar
  124. Sebens KP, Johnson AS (1991) Effects of water movement on prey capture and distribution of reef corals. Hydrobiologia 226:91–101CrossRefGoogle Scholar
  125. Sebens KP, Vandersall KS, Savina LA, Graham KR (1996) Zooplankton capture by two scleractinian corals Madracis mirabilis and Montastrea cavernosa in a field enclosure. Mar Biol 127:303–317CrossRefGoogle Scholar
  126. Sebens KP, Grace S, Helmuth B, Maney E, Miles J (1998) Water flow and prey capture by three scleractinian corals, Madracis mirabilis, Montastrea cavernosa, and Porites porites in a field enclosure. Mar Biol 131:347–360CrossRefGoogle Scholar
  127. Smith GJ, Muscatine L (1986) Carbon budgets and regulation of the population density of symbiotic algae. Endocyt C Res 3:212–238Google Scholar
  128. Snidvongs A, Kinzie RA (1994) Effects of nitrogen and phosphorus enrichement on in vivo symbiotic zooxanthellae of Pocillopora damicornis. Mar Biol 118:705–711CrossRefGoogle Scholar
  129. Sorokin YI (1973) Role of microflora in metabolism and productivity of Hawaiian Reefs. Oceanology-USSR 13:262–267Google Scholar
  130. Sorokin YI (1993) Coral reef ecology. Ecological studies. Springer, Berlin, p 465Google Scholar
  131. Spencer-Davies P (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101(3):389–395Google Scholar
  132. Stambler Z, Dubinsky N (1996) Marine pollution and coral reefs. Glob Change Biol 2:511–526CrossRefGoogle Scholar
  133. Stambler N, Popper N, Dubinsky Z, Stimson J (1991) Effects of nutrient enrichment and water motion on the coral Pocillopora damicornis. Pac Sci 45:299–307Google Scholar
  134. Swanson R, Hoegh-Guldberg O (1998) Amino acid synthesis in the symbiotic sea anemone Aiptasia pulchella. Mar Biol 131:83–93CrossRefGoogle Scholar
  135. Swart PK, Leder JJ, Szmant AM, Dodge RE (1996) The origin of variations in the isotopic record of scleractinian corals. II. Carbon. Geochism Cosmochim Acta 60:2871–2886CrossRefGoogle Scholar
  136. Szmant-Froelich A (1981) Coral nutrition: comparison of the fate of 14C from ingested labelled brine shrimp and from the uptake of NaH14CO3 by its zooxanthellae. J Exp Mar Biol Ecol 55:133–144CrossRefGoogle Scholar
  137. Szmant-Froelich A, Pilson MEQ (1980) The effects of feeding frequency and symbiosis with zooxanthellae on the biochemical composition of Astrangia danae Milne Edwards and Haime 1849. J Exp Mar Biol Ecol 48:85–97CrossRefGoogle Scholar
  138. Tambutté E, Allemand D, Bourge I, Gattuso JP, Jaubert J (1995) An improved 45Ca protocol for investigating physiological mechanisms in coral calcification. Mar Biol 122:453–459CrossRefGoogle Scholar
  139. Titlyanov EA, Titlyanova TV, Tsukahara J, Van Woesik R, Yamazato K (1999) Experimental increases of zooxanthellae density in the coral Stylophora pistillata elucidate adaptive mechanisms for zooxanthellae regulation. Symbiosis 26:347–362Google Scholar
  140. Titlyanov EA, Bil’ K, Fomina L, Titlyanova T, Leletkin V, Eden N, Malkin A, Dubinsky Z (2000a) Effects of dissolved ammonium addition and host feeding with Artemia salina on photoacclimation of the hermatypic coral Stylophora pistillata. Mar Biol 137:463–472CrossRefGoogle Scholar
  141. Titlyanov EA, Tsukahara J, Titlyanova TV, Leletkin VA, Van Woesik R, Yamazato K (2000b) Zooxanthellae population density and physiological state of the coral Stylophora pistillata during starvation and osmotic shock. Symbiosis 28:303–322Google Scholar
  142. Titlyanov EA, Titlyanova TV, Yamazato K, Van Woesik R (2001) Photo-acclimation of the hermatypic coral Stylophora pistillata while subjected to either starvation or food provisioning. J Exp Mar Biol Ecol 257:163–181CrossRefGoogle Scholar
  143. Treignier C, Grover R, Tolosa I, Ferrier-Pagès C (2008) Effect of light and feeding on the Fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis. Limnol Oceanogr 53(6):2702–2710CrossRefGoogle Scholar
  144. Trench RK (1979) The cell biology of plant-animal symbiosis. Ann Rev Plant Physiol 30:485–531CrossRefGoogle Scholar
  145. Verde EA, McCloskey LR (1996) Photosynthesis and respiration of two species of algal symbionts in the anemone Anthopleura elegantissima (Brandt)(Cnidaria; Anthozoa). J Exp Mar Biol Ecol 195:187–202CrossRefGoogle Scholar
  146. Wang JT, Douglas AE (1999) Nitrogen recycling or nitrogen conservation in an alga-invertebrate symbiosis? J Exp Biol 201:2445–2453Google Scholar
  147. Weiner S, Addadi L (1991) Acidic macromolecules of mineralized tissues. The controllers of crystal formation. Trends Biochem Sci 16:252–256CrossRefGoogle Scholar
  148. Wellington GM (1982) An experimental analysis of the effects of light and zooplankton on coral zonation. Oecologia 52:311–320CrossRefGoogle Scholar
  149. Wild C, Huettel M, Klueter A, Kremb SG, Rasheed MYD, Jørgensen BB (2004) Coral mucus as an energy carrier and particle trap in the reef ecosystem. Nature 428:66–70CrossRefGoogle Scholar
  150. Yahel R, Yahel G, Berman T (2005) Diel pattern with abrupt crepuscular changes of zooplankton over a coral reef. Limnol Oceanogr 50:930–944CrossRefGoogle Scholar
  151. Yamamuro M, Kayanne H, Minagawa M (1995) Carbon and nitrogen stable isotopes of primary producers in coral reef ecosystems. Limnol Oceanogr 40:617–621CrossRefGoogle Scholar
  152. Yamashiro H, Oku H, Onaga K (2005) Effect of bleaching on lipid content and composition of Okinawan corals. Fish Sci 71:448–453CrossRefGoogle Scholar
  153. Yonge CM (1930a) Studies on the physiology of corals. I. Feeding mechanisms and food. Sci Rep Great Barrier Reef Exped 1:13–57Google Scholar
  154. Yonge CM (1930b) Studies on the physiology of corals. III. Assimilation and excretion. Sci Rep Great Barrier Reef Exped 1:83–91Google Scholar
  155. Yonge CM, Nicholls AG (1931) Studies on the physiology of corals. IV. The structure, distribution and physiology of the zooxanthellae. Sci Rep Great Barrier Reef Exped 1:135–176Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Centre Scientifique de MonacoMonacoMonaco
  2. 2.Marine Environment LaboratoriesInternational Atomic Energy AgencyMonacoMonaco

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