Abstract
This study quantified variation in net photosynthetic carbon gain in response to natural fluctuations in symbiont density for the Mediterranean coral Cladocora caespitosa, and evaluated which density maximized photosynthetic carbon acquisition. To do this, carbon acquisition was modeled as an explicit function of symbiont density. The model was parameterized using measurements of rates of photosynthesis and respiration for small colonies with a broad range of zooxanthella concentrations. Results demonstrate that rates of net photosynthesis increase asymptotically with symbiont density, whereas rates of respiration increase linearly. In combination, these functional responses meant that colony energy acquisition decreased at both low and at very high zooxanthella densities. However, there was a wide range of symbiont densities for which net daily photosynthesis was approximately equivalent. Therefore, significant changes in symbiont density do not necessarily cause a change in autotrophic energy acquisition by the colony. Model estimates of the optimal range of cell densities corresponded well with independent observations of symbiont concentrations obtained from field and laboratory studies of healthy colonies. Overall, this study demonstrates that the seasonal fluctuations, in symbiont numbers observed in healthy colonies of the Mediterranean coral investigated, do not have a strong effect on photosynthetic energy acquisition.
References
Anthony KRN, Hoegh-Guldberg O (2003) Kinetics of photoacclimation in corals. Oecologia 134:23–31
Anthony KRN, Hoogenboom MO, Grottoli A, Middlebrook R, Maynard J (2009) Energetics approach to predicting mortality risk from environmental stress: a case study of coral bleaching. Funct Ecol 23:539–550
Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141
Bellwood DR, Hoey AS, Ackerman JL, Depczynski M (2006) Coral bleaching, reef fish community phase shifts and the resilience of coral reefs. Global Change Biol 12:1587–1594
Brown BE, Dunne RP, Ambarsari I, LeTissier MDA, Satapoomin U (1999) Seasonal fluctuations in environmental factors and variations in symbiotic algae and chlorophyll pigments in four Indo-Pacific coral species. Mar Ecol Prog Ser 191:53–69
Carpenter RC, Williams SL (2007) Mass transfer limitation of photosynthesis of coral reef algal turfs. Mar Biol 151:435–450
Davy SK, Cook CB (2001) The relationship between nutritional status and carbon flux in the zooxanthellate sea anemone Aiptasia pallida. Mar Biol 139:999–1005
Dennison WC, Barnes DJ (1988) Effects of water motion on coral photosynthesis and calcification. J Exp Mar Biol Ecol 115:67–77
Dustan P (1982) Depth-dependent photoadaptation by zooxanthellae of the reef coral Montastrea annularis. Mar Biol 68:253–264
Fagoonee I, Wilson HB, Hassell MP, Turner JR (1999) The dynamics of zooxanthellae populations: a long term study in the field. Science 283:843–845
Fitt WK, Cook CB (2001) Photoacclimation and the effect of the symbiotic environment on the photosynthetic response of symbiotic dinoflagellates in the tropical marine hydroid Myrionema amboinense. J Exp Mar Biol Ecol 256:15–31
Fitt WK, McFarland FK, Warner ME, Chilcoat GC (2000) Seasonal patterns of tissue biomass and densities of symbiotic dinoflagellates in reef coral and relation to coral bleaching. Limnol Oceanogr 45:677–685
FitzGerald LM, Szmant AM (1988) Amino acid metabolism: adaptations to low nutrient conditions? Proc 6th Int Coral Reef Symp 3:5–9
Gatusso J-P, Jaubert J (1990) Effect of light on oxygen and carbon dioxide fluxes and on metabolic quotients measured in situ in a zooxanthellate coral. Limnol Oceanogr 35:1796–1804
Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866
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 57:173–186
Howe SA, Marshall AT (2001) Thermal compensation of metabolism in the temperate coral, Plesiastrea versipora (Lamarck, 1816). J Exp Mar Biol Ecol 259:213–248
Iglesias-Prieto R, Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser 113:163–175
Jacques TG, Marshall N, Pilson MEQ (1983) Experimental ecology of the temperate scleractinian coral Astrangia danae II. Effect of temperature, light intensity and symbiosis with zooxanthellae on metabolic rate and calcification. Mar Biol 76:135–148
Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547
Jeffery SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194
Jones RJ, Yellowlees D (1997) Regulation and control of intracellular algae (equals zooxanthellae) in hard corals. Philos Trans Roy Soc London B Biol Sci 352:457–468
Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U (1998) Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zooxanthellae. Plant Cell Environ 21:1219–1221
Kooijman SALM (2000) Dynamic energy and mass budgets in biological systems, 2nd edn. Cambridge University Press, Cambridge
Kruzic P, Bencovic L (2008) Bioconstructional features of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic sea (Croatia). Mar Ecol 29:125–139
Kuhl M, Cohen Y, Dalsgaard T (1995) Microenvironment and photosynthesis of zooxanthellae in scleractinian corals studied with microsensors for O2, pH and light. Mar Ecol Prog Ser 117:159–172
LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Mar Ecol Prog Ser 248:147–161
Leggat W, Buck BH, Grice A, Yellowlees D (2003) The impact of bleaching on the metabolic contribution of dinoflagellate symbionts to their giant clam host. Plant Cell Environ 26:1951–1961
Leletkin VA, Titlyanov EA, Dubinsky Z (1996) Photosynthesis and respiration of the zooxanthellae in hermatypic corals habitated on different depths of the Gulf of Eilat. Photosynthetica 32:481–490
Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbiosis shapes growth in reef corals. Science 304:1492–1494
Loh WKW, Loi T, Carter D, Hoegh-Guldberg O (2001) Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific. Mar Ecol Prog Ser 222:97–107
Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Lett 4:122–131
Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163
Muller EM, Rogers CS, Spitzack AS, van Woesik R (2008) Bleaching increases likelihood of disease on Acropora palmata (Lamark) in Hawksnest Bay, St John, US Virgin Islands. Coral Reefs 27:191–195
Muller-Parker G (1984) Photosynthesis-irradiance responses and photosynthetic periodicity in the sea anemone Aiptasia pulchella and its zooxanthellae. Mar Biol 82:225–232
Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611
Muscatine L, Porter JW, Kaplan IR (1989a) Resource partitioning by reef corals as determined from stable isotope composition. I. 13C of zooxanthellae and animal tissue vs depth. Mar Biol 100:185–193
Muscatine L, Falkowski PG, Dubinsky Z, Cook PA, McCloskey LR (1989b) The effect of external nutrient resources on the population dynamics of zooxanthellae in a reef coral. Proc Roy Soc London B 236:311–324
Peirano A, Abbate M, Cerrati G, Difesca V, Peroni C, Rodolfo-Metalpa R (2005) Monthly variations in calix growth, polyp tissue, and density banding of the Mediterranean scleractinian Cladocora caespitosa (L.). Coral Reefs 24:404–409
R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org
Rodolfo-Metalpa R, Richard C, Allemand D, Bianchi CN, Morri C, Ferrier-Pages C (2006a) Response of zooxanthellae in symbiosis with the Mediterranean coral Cladocora caespitosa and Oculina patagonica to elevated temperatures. Mar Biol 150:45–55
Rodolfo-Metalpa R, Richard C, Allemand D, Ferrier-Pages C (2006b) Growth and photosynthesis of two Mediterranean coral, Cladocora caespitosa and Oculina patagonica, under normal and elevated temperatures. J Exp Biol 209:4546–4556
Rodolfo-Metalpa R, Reynaud S, Allemand D, Ferrier-Pages C (2008a) Temporal and depth responses of two temperate corals, Cladocora caespitosa and Oculina patagonica from the North Mediterranean Sea. Mar Ecol Prog Ser 369:103–114
Rodolfo-Metalpa R, Huot Y, Ferrier-Pages C (2008b) Photosynthetic response of the Mediterranean zooxanthellate coral Cladocora caespitosa to the natural range of light and temperature. J Exp Biol 211:1579–1586
Rossi S, Tsounis G (2007) Temporal and spatial variation in protein, carbohydrate, and lipid levels in Corallium rubrum (Anthozoa, Octocorallia). Mar Biol 152:429–439
Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–1350
Sampayo EM, Ridgway T, Bongaerts P, Hoegh-Guldberg O (2008) Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proc Natl Acad Sci USA 105:10444–10449
Schiller C (1993) Ecology of the symbiotic coral Cladocora caespitosa (L.)(Faviidae, Scleractinia) in the Bay of Piran (Adriatic Sea): II. Energy Budget. PSZNI Mar Ecol 14:221–238
Shenkar N, Fine M, Kramarsky-Winter E, Loya Y (2006) Population dynamics of zooxanthellae during a bacterial bleaching event. Coral Reefs 25:223–227
Smith GJ, Muscatine L (1986) Carbon budgets and regulation of the population density of symbiotic algae. Endocytobiosis Cell Res 3:212–238
Stat M, Morris E, Gates RD (2008) Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci USA 105:9256–9261
Steen RG (1987) Evidence for facultative heterotrophy in cultured zooxanthellae. Mar Biol 95:15–23
Steen RG, Muscatine L (1984) Daily budgets of photosynthetically fixed carbon in symbiotic zoanthids. Biol Bull 167:477–487
Stimson J (1997) The annual cycle of density of zooxanthellae in the tissues of field and laboratory-held Pocillopora damicornis (Linnaeus). J Exp Mar Biol Ecol 214:35–48
Titlyanov EA, Titlyanova TV, Tsukahara J, van Woesik R, Yamazoto K (1999) Experimental increases of zooxanthellae density in the coral Stylophora pistillata elucidate adaptive mechanisms for zooxanthellae regulation. Symbiosis 26:347–362
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 195:187–202
Visram S, Wiedenmann J, Douglas AE (2006) Molecular diversity of symbiotic algae of the genus Symbiodinium (zooxanthellae) in cnidarians of the Mediterranean Sea. J Mar Biol Assoc UK 56:1281–1283
Acknowledgments
This work was supported by funding from the government of the Principality of Monaco to the Centre Scientifique de Monaco. We thank R. Rodolfo-Metalpa for coral collection and C. Rottier for assistance with coral culture.
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Hoogenboom, M., Beraud, E. & Ferrier-Pagès, C. Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa . Coral Reefs 29, 21–29 (2010). https://doi.org/10.1007/s00338-009-0558-9
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DOI: https://doi.org/10.1007/s00338-009-0558-9