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Carbon translocation from symbiont to host depends on irradiance and food availability in the tropical coral Stylophora pistillata

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Abstract

Reef-building corals live in symbiosis with dinoflagellates that translocate a large proportion of their photosynthetically fixed carbon compounds to their coral host for its own metabolism. The carbon budget and translocation rate, however, vary depending on environmental conditions, coral host species, and symbiont clade. To quantify variability in carbon translocation in response to environmental conditions, this study assessed the effect of two different irradiance levels (120 and 250 μmol photons m−2 s−1) and feeding regimes (fed with Artemia salina nauplii and unfed) on the carbon budget of the tropical coral Stylophora pistillata. For this purpose, H13CO3 -enriched seawater was used to trace the conversion of photosynthetic carbon into symbiont and coral biomass and excrete particulate organic carbon. Results showed that carbon translocation (ca. 78 %) and utilization were similar under both irradiance levels for unfed colonies. In contrast, carbon utilization by fed colonies was dependent on the growth irradiance. Under low irradiance, heterotrophy was accompanied by lower carbon translocation (71 %), higher host and symbiont biomass, and higher calcification rates. Under high irradiance, heterotrophy was accompanied by higher rates of photosynthesis, respiration, and carbon translocation (90 %) as well as higher host biomass. Hence, levels of resource sharing within coral–dinoflagellate symbioses depend critically on environmental conditions.

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References

  • Allemand D, Tambutté É, Zoccola D, Tambutté S (2011) Coral calcification, cells to reefs. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Heidelberg, pp 119–150

    Chapter  Google Scholar 

  • Anthony KRN, Fabricius KE (2000) Shifting roles of heterotrophy and autotrophy in coral energy budgets at variable turbidity. J Exp Mar Biol Ecol 252:221–253

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Anthony KRN, Connolly SR, Willis BL (2002) Comparative analysis of energy allocation to tissue and skeletal growth in corals. Limnol Oceanogr 47:1417–1429

    Article  Google Scholar 

  • Bachar A, Achituv Y, Pasternak Z, Dubinsky Z (2007) Autotrophy versus heterotrophy: the origin of carbon determines its fate in a symbiotic sea anemone. J Exp Mar Biol Ecol 349:295–298

    Article  CAS  Google Scholar 

  • Burriesci MS, Raab TK, Pringle JR (2012) Evidence that glucose is the major transferred metabolite in dinoflagellate-cnidarian symbiosis. J Exp Biol 215:3467–3477

    Article  CAS  PubMed  Google Scholar 

  • Colombo-Pallotta MF, Rodríguez-Román A, Iglesias-Prieto R (2010) Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29:899–907

    Article  Google Scholar 

  • 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 6:35–42

    Article  CAS  Google Scholar 

  • Davies PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Mar Biol 101:389–395

    Article  Google Scholar 

  • Davies PS (1991) Effects of daylight variations on the energy budgets of shallow-water corals. Mar Biol 108:137–144

    Article  Google Scholar 

  • 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 

  • Davy SK, Lucas IAN, Turner JR (1996) Carbon budgets in temperate anthozoan-dinoflagellate symbioses. Mar Biol 126:773–783

    Article  Google Scholar 

  • Dubinsky Z, Jokiel P (1994) Ratio of energy and nutrient fluxes regulates symbiosis between zooxanthellae and corals. Pac Sci 48:313–324

    Google Scholar 

  • Dubinsky Z, Falkowski PG, Porter JW, Muscatine L (1984) Absorption and utilization of radiant energy by light- and shade-adapted colonies of the hermatypic coral Stylophora pistillata. Proc R Soc Lond B 222:203–214

    Article  CAS  Google Scholar 

  • Edmunds PJ (2011) Zooplanktivory ameliorates the effects of ocean acidification on the reef coral Porites spp. Limnol Oceanogr 56:2402–2410

    Article  CAS  Google Scholar 

  • Einbinder S, Mass T, Brokovich E, Dubinsky Z, Erez J, Tchernov D (2009) Changes in morphology and diet of the coral Stylophora pistillata along a depth gradient. Mar Ecol Prog Ser 381:167–174

    Article  Google Scholar 

  • Erez J (1978) Vital effect on stable-isotope composition seen in foraminifera and coral skeletons. Nature 273:199–202

    Article  CAS  Google Scholar 

  • Falkowski PG, Dubinsky Z (1981) Light-shade adaptation of Stylophora pistillata, a hermatypic coral from the gulf of Eilat. Nature 289:172–174

    Article  Google Scholar 

  • Falkowski PG, Dubinsky Z, Muscatine L, Porter JW (1984) Light and the bioenergetics of a symbiotic coral. Bioscience 34:705–709

    Article  CAS  Google Scholar 

  • Ferrier-Pagès C, Hoogenboom M, Houlbrèque F (2011) The role of plankton in coral trophodynamics. In: Dubinsky Z, Stambler N (eds) Coral reefs: an ecosystem in transition. Springer, Heidelberg, pp 215–229

    Chapter  Google Scholar 

  • Ferrier-Pagès C, Rottier C, Béraud É, Levy O (2010) Experimental assessment of the feeding effort of three scleractinian coral species during a thermal stress: effect on the rates of photosynthesis. J Exp Mar Biol Ecol 390:118–124

    Article  Google Scholar 

  • Ferrier-Pagès C, Witting J, Tambutté É, Sebens KP (2003) Effect of natural zooplankton feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata. Coral Reefs 22:229–240

    Article  Google Scholar 

  • Ferrier-Pagès C, Gattuso JP, Cauwet G, Jaubert J, Allemand D (1998) Release of dissolved organic carbon and nitrogen by the zooxanthellate coral Galaxea fascicularis. Mar Ecol Prog Ser 172:265–274

    Article  Google Scholar 

  • Furla P, Galgani I, Durand I, Allemand D (2000) Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis. J Exp Biol 203:3445–3457

    CAS  PubMed  Google Scholar 

  • Gattuso 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 

  • Gattuso JP, Yellowlees D, Lesser M (1993) Depth- and light-dependent variation of carbon partitioning and utilization in the zooxanthellate scleractinian coral Stylophora pistillata. Mar Ecol Prog Ser 92:267–276

    Article  Google Scholar 

  • Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189

    Article  CAS  PubMed  Google Scholar 

  • 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 47:782–790

    Article  Google Scholar 

  • Hoogenboom MO, Connolly SR (2009) Defining fundamental niche dimensions of corals: synergistic effects of colony size, light, and flow. Ecology 90:767–780

    Article  PubMed  Google Scholar 

  • Hoogenboom MO, Anthony KRN, Connolly SR (2006) Energetic cost of photoinhibition in corals. Mar Ecol Prog Ser 313:1–12

    Article  CAS  Google Scholar 

  • Hoogenboom M, Rodolfo-Metalpa R, Ferrier-Pagès C (2010a) Co-variation between autotrophy and heterotrophy in the Mediterranean coral Cladocora caespitosa. J Exp Biol 213:2399–2409

    Article  PubMed  Google Scholar 

  • Hoogenboom M, Béraud É, Ferrier-Pagès C (2010b) Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa. Coral Reefs 29:21–29

    Article  Google Scholar 

  • Houlbrèque F, Ferrier-Pagès C (2009) Heterotrophy in tropical scleractinian corals. Biol Rev 84:1–17

    Article  PubMed  Google Scholar 

  • Houlbrèque F, Tambutté É, 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 269:145–166

    Article  Google Scholar 

  • Houlbrèque F, Tambutté É, Richard C, Ferrier-Pagès C (2004) Importance of a micro-diet for scleractinian corals. Mar Ecol Prog Ser 282:151–160

    Article  Google Scholar 

  • Hughes AD, Grottoli AG, Pease TK, Matsui Y (2010) Acquisition and assimilation of carbon in non-bleached and bleached corals. Mar Ecol Prog Ser 420:91–101

    Article  CAS  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c 1 and c 2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167:191–194

    CAS  Google Scholar 

  • Jokiel RL, Maragos JE, Franzisket L (1978) Coral growth: buoyant weight technique. Monogr Oceanogr Methodol (UNESCO) 5:529–542

    Google Scholar 

  • Kazandjian A, Shepherd VA, Rodriguez-Lanetty M, Nordemeier W, Larkum AWD, Quinnell RG (2008) Isolation of symbiosomes and the symbiosome membrane complex from the zoanthid Zoanthus robustus. Phycologia 47:294–306

    Article  Google Scholar 

  • Leggat W, Rees TAV, Yellowlees D (2000) Meeting the photosynthetic demand for inorganic carbon in an alga-invertebrate association: preferential use of CO2 by symbionts in the giant clam Tridacna gigas. Proc R Soc Lond B 267:523–529

    Article  CAS  Google Scholar 

  • Loram JE, Trapido-Rosenthal HG, Douglas AE (2007) Functional significance of genetically different symbiotic algae Symbiodinium in a coral reef symbiosis. Mol Ecol 16:4849–4857

    Article  CAS  PubMed  Google Scholar 

  • Mass T, Einbinder S, Brokovich E, Shashar N, Vago R, Erez J, Dubinsky Z (2007) Photoacclimation of Stylophora pistillata to light extremes: metabolism and calcification. Mar Ecol Prog Ser 334:93–102

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Muscatine L, Porter JW, Kaplan IR (1989) Resource partitioning by reef corals as determined from stable isotope composition. I. δ13C of zooxanthellae and animal tissue versus depth. Mar Biol 100:185–193

    Article  Google Scholar 

  • 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 222:181–202

    Article  CAS  Google Scholar 

  • Naumann MS, Haas A, Struck U, Mayr C, el-Zibdah M, Wild C (2010) Organic matter release by dominant hermatypic corals of the Northern Red Sea. Coral Reefs 29:649–659

    Article  Google Scholar 

  • 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 331:99–107

    Article  Google Scholar 

  • Pearse VB, Muscatine L (1971) Role of symbiotic algae (zooxanthellae) in coral calcification. Biol Bull 141:350–363

    Article  CAS  Google Scholar 

  • 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 27:17–25

    Article  Google Scholar 

  • Smith PK, Khrohn RI, Hermanson GT, Malia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  CAS  PubMed  Google Scholar 

  • Stambler N (1998) Effects of light intensity and ammonium enrichment on the hermatypic coral Stylophora pistillata and its zooxanthellae. Symbiosis 24:127–146

    Google Scholar 

  • Stimson J, Kinzie RA (1991) The temporal pattern and rate of release of zooxanthellae from the reef coral Pocillopora damicornis (Linnaeus) under nitrogen enrichment and control conditions. J Exp Mar Biol Ecol 153:63–74

    Article  Google Scholar 

  • Tambutté S, Holcomb M, Ferrier-Pagès C, Reynaud S, Tambutté É, Zoccola D, Allemand D (2011) Coral biomineralization: from the gene to the environment. J Exp Mar Biol Ecol 408:58–78

    Article  Google Scholar 

  • Tremblay P, Peirano A, Ferrier-Pagès C (2011) Heterotrophy in the Mediterranean symbiotic coral Cladocora caespitosa: comparison with two other scleractinian species. Mar Ecol Prog Ser 422:165–177

    Article  Google Scholar 

  • Tremblay P, Grover R, Maguer JF, Legendre L, Ferrier-Pagès C (2012a) Autotrophic carbon budget in the coral tissue: a new 13C-based model of photosynthate translocation. J Exp Biol 215:1384–1393

    Article  CAS  PubMed  Google Scholar 

  • Tremblay P, Fine M, Maguer JF, Grover R, Ferrier-Pagès C (2013) Photosynthate translocation increases in response to low seawater pH in a coral–dinoflagellates symbiosis. Biogeosciences 10:3997–4007

    Article  Google Scholar 

  • Tremblay P, Ferrier-Pagès C, Maguer JF, Rottier C, Legendre L, Grover R (2012b) Controlling effects of irradiance and heterotrophy on carbon translocation in the temperate coral Cladocora caespitosa. PLoS ONE 7:e44672

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge

    Google Scholar 

  • Whitehead LF, Douglas AE (2003) Metabolite comparisons and the identity of nutrients translocated from symbiotic algae to an animal host. J Exp Biol 206:3149–3157

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Cécile Rottier and Séverine Sikorski for laboratory assistance and Prof. Denis Allemand, Director of the Centre Scientifique de Monaco (CSM), for scientific support. We also thank Dr. Sylvie Tambutté for fruitful discussion on light-enhanced calcification as well as two anonymous reviewers for helpful comments. Funding was provided by the CSM, the Institut Universitaire Européen de la Mer, and the Natural Sciences and Engineering Research Council of Canada (Grant # ES D3—378797—2009 to PT).

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Correspondence to P. Tremblay.

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Communicated by Biology Editor Dr. Anastazia Banaszak

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Tremblay, P., Grover, R., Maguer, J.F. et al. Carbon translocation from symbiont to host depends on irradiance and food availability in the tropical coral Stylophora pistillata . Coral Reefs 33, 1–13 (2014). https://doi.org/10.1007/s00338-013-1100-7

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