Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa

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.

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

Fig. 1
Fig. 2
Fig. 3

References

  1. Anthony KRN, Hoegh-Guldberg O (2003) Kinetics of photoacclimation in corals. Oecologia 134:23–31

    Article  PubMed  Google Scholar 

  2. 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

    Google Scholar 

  3. 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

    Article  Google Scholar 

  4. 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

    Article  Google Scholar 

  5. 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

    Article  Google Scholar 

  6. Carpenter RC, Williams SL (2007) Mass transfer limitation of photosynthesis of coral reef algal turfs. Mar Biol 151:435–450

    Article  Google Scholar 

  7. 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

    Article  CAS  Google Scholar 

  8. Dennison WC, Barnes DJ (1988) Effects of water motion on coral photosynthesis and calcification. J Exp Mar Biol Ecol 115:67–77

    Article  Google Scholar 

  9. Dustan P (1982) Depth-dependent photoadaptation by zooxanthellae of the reef coral Montastrea annularis. Mar Biol 68:253–264

    Article  CAS  Google Scholar 

  10. 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

    Article  CAS  PubMed  Google Scholar 

  11. 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

    Article  PubMed  Google Scholar 

  12. 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

    CAS  Google Scholar 

  13. FitzGerald LM, Szmant AM (1988) Amino acid metabolism: adaptations to low nutrient conditions? Proc 6th Int Coral Reef Symp 3:5–9

  14. 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

    Article  Google Scholar 

  15. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world’s coral reefs. Mar Freshw Res 50:839–866

    Article  Google Scholar 

  16. 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

    Article  CAS  Google Scholar 

  17. 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

    Article  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    Article  CAS  Google Scholar 

  20. Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547

    CAS  Google Scholar 

  21. 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

    Google Scholar 

  22. 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

    Article  Google Scholar 

  23. 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

    Article  CAS  Google Scholar 

  24. Kooijman SALM (2000) Dynamic energy and mass budgets in biological systems, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  25. Kruzic P, Bencovic L (2008) Bioconstructional features of the coral Cladocora caespitosa (Anthozoa, Scleractinia) in the Adriatic sea (Croatia). Mar Ecol 29:125–139

    Article  CAS  Google Scholar 

  26. 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

    Article  Google Scholar 

  27. 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

    Article  Google Scholar 

  28. 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

    Article  CAS  Google Scholar 

  29. 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

    Google Scholar 

  30. Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal endosymbiosis shapes growth in reef corals. Science 304:1492–1494

    Article  CAS  PubMed  Google Scholar 

  31. 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

    Article  Google Scholar 

  32. 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

    Article  Google Scholar 

  33. Marshall PA, Baird AH (2000) Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155–163

    Article  Google Scholar 

  34. 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

    Article  Google Scholar 

  35. Muller-Parker G (1984) Photosynthesis-irradiance responses and photosynthetic periodicity in the sea anemone Aiptasia pulchella and its zooxanthellae. Mar Biol 82:225–232

    Article  CAS  Google Scholar 

  36. Muscatine L, McCloskey LR, Marian RE (1981) Estimating the daily contribution of carbon from zooxanthellae to coral animal respiration. Limnol Oceanogr 26:601–611

    CAS  Article  Google Scholar 

  37. 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

    Article  Google Scholar 

  38. 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

    Article  Google Scholar 

  39. 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

    Article  Google Scholar 

  40. 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

  41. 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

    Article  Google Scholar 

  42. 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

    Article  PubMed  Google Scholar 

  43. 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

    Article  Google Scholar 

  44. 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

    Article  CAS  PubMed  Google Scholar 

  45. 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

    Article  CAS  Google Scholar 

  46. Rowan R, Powers DA (1991) A molecular genetic classification of zooxanthellae and the evolution of animal-algal symbioses. Science 251:1348–1350

    Article  CAS  PubMed  Google Scholar 

  47. 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

    Article  CAS  PubMed  Google Scholar 

  48. 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

    Article  Google Scholar 

  49. Shenkar N, Fine M, Kramarsky-Winter E, Loya Y (2006) Population dynamics of zooxanthellae during a bacterial bleaching event. Coral Reefs 25:223–227

    Article  Google Scholar 

  50. Smith GJ, Muscatine L (1986) Carbon budgets and regulation of the population density of symbiotic algae. Endocytobiosis Cell Res 3:212–238

    Google Scholar 

  51. Stat M, Morris E, Gates RD (2008) Functional diversity in coral-dinoflagellate symbiosis. Proc Natl Acad Sci USA 105:9256–9261

    Article  CAS  PubMed  Google Scholar 

  52. Steen RG (1987) Evidence for facultative heterotrophy in cultured zooxanthellae. Mar Biol 95:15–23

    Article  Google Scholar 

  53. Steen RG, Muscatine L (1984) Daily budgets of photosynthetically fixed carbon in symbiotic zoanthids. Biol Bull 167:477–487

    Article  CAS  Google Scholar 

  54. 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

    Article  Google Scholar 

  55. 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

    Google Scholar 

  56. 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

    Article  Google Scholar 

  57. 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

    Article  CAS  Google Scholar 

Download references

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to M. Hoogenboom.

Additional information

Communicated by Biology Editor Dr. Clay Cook

Electronic supplementary material

Below is the link to the electronic supplementary material.

DOC 70 kb

Rights and permissions

Reprints and Permissions

About this article

Cite this article

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

Download citation

Keywords

  • Scleractinian coral
  • Photosynthesis
  • Respiration
  • Energy balance
  • Symbiosis
  • Optimality model