Skip to main content

Advertisement

SpringerLink
Log in

Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

All reef-building corals are symbiotic with dinoflagellates of the genus Symbiodinium, which influences many aspects of the host’s physiology including calcification. Coral calcification is a biologically controlled process performed by the host that takes place several membranes away from the site of photosynthesis performed by the symbiont. Although it is well established that light accelerates CaCO3 deposition in reef-building corals (commonly referred to as light-enhanced calcification), the complete physiological mechanism behind the process is not fully understood. To better comprehend the coral calcification process, a series of laboratory experiments were conducted in the major Caribbean reef-building species Montastraea faveolata, to evaluate the effect of glycerol addition and/or the super-saturation of oxygen in the seawater. These manipulations were performed in bleached and unbleached corals, to separate the effect of photosynthesis from calcification. The results suggest that under normal physiological conditions, a 42% increase in seawater oxygen concentration promotes a twofold increase in dark-calcification rates relative to controls. On the other hand, the results obtained using bleached corals suggest that glycerol is required, as a metabolic fuel, in addition to an oxygenic environment in a symbiosis that has been disrupted. Also, respiration rates in symbiotic corals that were pre-incubated in light conditions showed a kinetic limitation, whereas corals that were pre-incubated in darkness were oxygen limited, clearly emphasizing the role of oxygen in this regard. These findings indicate that calcification in symbiotic corals is not strictly a “light-enhanced” or “dark-repressed” process, but rather, the products of photosynthesis have a critical role in calcification, which should be viewed as a “photosynthesis-driven” process. The results presented here are discussed in the context of the current knowledge of the coral calcification process.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Al-Horani FA, Al-Moghrabi SM, De Beer D (2003) The mechanisms of calcification and its relationship to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar Biol 142:419–426

    CAS  Google Scholar 

  • Al-Horani FA, Al-Rousan SA, Mansrah RS, Rasheed MY (2005) Coral calcification: use of radioactive isotopes and metabolic inhibitors to study the interactions with photosynthesis and respiration. Chem Ecol 21:325–335

    Article  CAS  Google Scholar 

  • Al-Horani FA, Tabutté É, Allemand D (2007) Dark calcification and the daily rhythm of calcification in the scleractinian coral, Galaxea fascicularis. Coral Reefs 26:531–538

    Article  Google Scholar 

  • Allemand D, Furla P, Bénazet-Tambutté S (1998) Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can J Bot 76:925–941

    Article  CAS  Google Scholar 

  • Allemand D, Ferrer-Pages C, Furla P, Haulbreque F, Puverel S, Reynaud S, Tambutte E, Tambutee S, Zoccola D (2004) Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. C R Palevol 3:453–467

    Article  Google Scholar 

  • Al-Moghrabi S, Goiran C, Allemand D, Speziale N, Jaubert J (1996) Inorganic carbon uptake for photosynthesis by the symbiotic coral-dinoflagellate association. II. Mechanisms for bicarbonate uptake. J Exp Mar Biol Ecol 199:227–248

    Article  CAS  Google Scholar 

  • Barnes DJ, Chalker BE (1990) Calcification and photosyntesis in reef-building corals and algae. In: Dubinsky Z (ed) Coral reefs. Elsevier, Amsterdam, pp 109–131

    Google Scholar 

  • Chalker BE, Taylor DL (1975) Light enhanced calcification, and the role of oxidative phosphorylation in calcification of the coral Acropora cervicornis. Proc R Soc Lond B 190:323–331

    Article  CAS  PubMed  Google Scholar 

  • Chalker B, Carr K, Gill E (1985) Measurement of primary production and calcification in situ on the coral reefs using electrode techniques. Proc 5th Int Coral Reef Congr 6:167–172

    Google Scholar 

  • Cuif J-P, Dauphin Y, Gautret P (1999) Compositional diversity of soluble mineralizing matrices in some recent coral skeletons compared to fine-scale growth structures of fibres: discussion of consequences for biomineralization and diagenesis. Int J Earth Sci 88:582–592

    Article  CAS  Google Scholar 

  • Fang L-S, Chen Y-W, Chen C-S (1989) Why does the white tip of stony corals growth so fast without zooxanthellae? Mar Biol 103:359–363

    Article  Google Scholar 

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

    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 

  • Furla P, Allemand D, Shick JM, Ferrier-Pagés C, Richier S, Plantivaux A, Merle P-L, Tambutté S (2005) The symbiotic anthozoan: A physiological chimera between alga and animal. Integr Comp Biol 45:595–604

    Article  CAS  Google Scholar 

  • Gattuso J-P, Allemand D, Frankignoulle M (1999) Photosynthesis and calcification at cellular, organismal and community level in coral reefs: A review on interactions and control by carbonate chemistry. Am Zool 39:160–183

    CAS  Google Scholar 

  • Gattuso J-P, Reynaud-Vaganay S, Furla P, Romaine-Lioud S, Jaubert J (2000) Calcification does not stimulate photosynthesis in the zooxanthellae scleractinian coral Stylophora pistillata. Limnol Oceanogr 45:246–250

    Article  Google Scholar 

  • Gautret P, Cuif J-P, Freiwald A (1997) Composition of soluble mineralizing matrices in zooxanthellate and non-zooxanthellate scleractinian corals: biochemical assessment of photosynthetic metabolism through the study of a skeletal feature. Facies 36:189–194

    Article  Google Scholar 

  • Goreau T (1959) The physiology of skeleton formation on corals. I. A method for measuring the rate of calcium deposition by corals under different conditions. Biol Bull (Woods Hole) 116:59–75

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Houlbrèque F, Tambutté E, Allemand D, Ferrier-Pagès C (2004) Interactions between zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral Stylophora pistillata. J Exp Biol 207:1461–1469

    Article  PubMed  Google Scholar 

  • Iglesias-Prieto R, Matta JL, Robins W, Trench R (1992) Photosynthetic response of elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci USA 89:10302–10305

    Article  CAS  PubMed  Google Scholar 

  • Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen (BPP) 167:191–194

    CAS  Google Scholar 

  • Jury C, Whitehead RF, Szmant A (2010) Effects of variations in carbonate chemistry on the calcification rates of Madracis auretenra (= Madracis mirabilis sensu Wells, 1973): bicarbonate concentrations best predict calcification rates. Global Change Biol 16:1632–1644

    Article  Google Scholar 

  • Kawaguti S, Sakumoto D (1948) The effect of light on the calcium deposition in corals. Bull Oceanogr Inst Taiwan 4:65–70

    Google Scholar 

  • Kühl M, Cohen Y, Dalsgaard T, Jørgensen BB, Revsbech NP (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 

  • Leggat W, Hoegh-Guldberg O, Dove S, Yellowelss D (2007) Analysis of an EST library from the dinoflagellate (Symbiodinum sp.) symbiont of reef-building corals. J Phycol 43:1010–1021

    Article  CAS  Google Scholar 

  • Lesser MP (1997) Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187–192

    Article  Google Scholar 

  • Marshall AT (1996) Calcification in hermatypic and ahermatypic corals. Science 271:637–639

    Article  CAS  Google Scholar 

  • Marshall AT, Clode PL (2003) Light regulated Ca2+ uptake and O2 secretion at the surface of a Scleractinian coral Galaxea fascicularis. Comp Biochem Physiol 136:417–426

    Article  Google Scholar 

  • McConnaughey T, Whelan JF (1997) Calcification generates protons for nutrients and bicarbonate uptake. Earth Sci Rev 42:95–117

    Article  CAS  Google Scholar 

  • Moya A, Tambutté S, Tambutté É, Zoccola D, Caminiti N, Allemand D (2006) Study of calcification during a daily cycle of the coral Stylophora pistillata Implications for “light-enhanced” calcification. J Exp Biol 209:3413–3419

    Article  CAS  PubMed  Google Scholar 

  • Moya A, Ferrier-Pagés C, Furla P, Richier S, Tambutté É, Allemand D, Tambutté S (2008) Calcification and associated physiological parameters during a stress event in the scleractinian coral Stylophora pistillata. Comp Biochem Physiol A 151:29–36

    Article  Google Scholar 

  • Muscatine L (1990) The role of symbiotic algae in carbon and energy flux in coral reefs. In: Dubinsky Z (ed) Coral reefs. Elsevier, Amsterdam, pp 75–84

    Google Scholar 

  • Muscatine L, Cernichiari E (1969) Assimilation of photosynthetic products of zooxanthellae by a reef coral. Biol Bull 137:506–523

    Article  CAS  Google Scholar 

  • Muscatine L, Pool RR, Cernichiari E (1972) Some factors influencing selective release of soluble organic material by zooxanthellae from reef corals. Mar Biol 13:298–308

    Article  CAS  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 

  • Muscatine L, Goiran C, Land L, Jaubert J, Cuif J-P, Allemand D (2005) Stable isotope (δ13C and δ15N) of organic matrix from coral skeleton. Proc Natl Acad Sci USA 102(5):1525–1530

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Puverel S, Tambutté E, Zoccola D, Domart-Coulon I, Bouchot A, Lotto S, Allemand D, Tambutté S (2005) Antibodies against the organic matrix in Scleractinian: a new tool to study coral biomineralization. Coral Reefs 24:149–156

    Article  Google Scholar 

  • Rands ML, Douglas EA, Loughman BC, Ratcliffe RG (1992) Avoidance of hypoxia in a cnidarian symbiosis by algal photosynthesis. Biol Bull 182:159–162

    Article  Google Scholar 

  • Rinkevich B, Loya L (1984) Does light enhance calcification in hermatypic corals? Mar Biol 80:1–6

    Article  CAS  Google Scholar 

  • Rodríguez-Román A, Hernández-Pech X, Thomé P, Enríquez S, Iglesias-Prieto R (2006) Photosynthesis and light utilization in the Caribbean coral Montastraea faveolata recovering from a bleaching event. Limnol Oceanogr 51:2702–2710

    Article  Google Scholar 

  • Salvador JM, Inesi G, Rigaud J-L, Mata AM (1998) Ca2+ transport by reconstituted synaptosomal ATPase is associated with H+ countertransport and net change displacement. J Biol Chem 273:18230–18234

    Article  CAS  PubMed  Google Scholar 

  • Smith S, Kinsey DW (1978) Calcification and organic carbon metabolism as indicated by carbon dioxide. In: Stoddart DR, Johannes RE (eds) Coral reefs: research methods. UNESCO, Paris

    Google Scholar 

  • Tambutte É, Allemand D, Mueller E, Jaubert J (1996) A compartmental approach to the mechanism of calcification in hermatypic corals. J Exp Biol 199:1029–1041

    CAS  Google Scholar 

  • Tentori E, Allemand D (2006) Light-enhanced calcification and dark decalcification in isolates of the soft coral Cladiella sp. during tissue recovery. Biol Bull 211:193–202

    Article  CAS  PubMed  Google Scholar 

  • Vandermeulen J, Muscatine L (1972) Influence of symbiotic algae on calcification in ref. corals: critique and progress report. In: Vernberg WB (ed) Symbiosis in the sea. University of South Carolina Press, Columbia, pp 1–20

    Google Scholar 

  • Vandermeulen J, Davis N, Muscatine L (1972) The effect of inhibitors of photosynthesis on zooxanthellae in corals and other marine invertebrates. Mar Biol 16:185–191

    Google Scholar 

  • Weis VM, Allemand D (2009) What determines coral health? Science 324:1153–1155

    Article  CAS  PubMed  Google Scholar 

  • Wellington GM, Trench RK (1985) Persistence and coexistence of a non-symbiotic coral in open reef environments. Proc Natl Acad Sci USA 82:2432–2436

    Article  CAS  PubMed  Google Scholar 

  • Whitaker JR, Granum PE (1980) An absolute method for protein determination based on difference in absorbance at 235 and 280 nm. Anal Biochem 109:156–159

    Article  CAS  PubMed  Google Scholar 

  • Yamashiro H, Yamazato K (1996) Morphological studies of the soft tissues involved in skeletal dissolution in the coral Fungia fungites. Coral Reefs 15:177–180

    Google Scholar 

  • Yao W, Byrne RH (1998) Simplified seawater alkalinity analysis: Use of linear array spectrometers. Deep-sea Res 45:1383–1392

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Claudia Morera-Roman for her technical assistance and Susana Enriquez and Bob Trench for fruitful discussions. Robin Smith and Anastazia Banaszak are thanked for their editorial assistance. Helpful comments on the manuscript were provided by two anonymous reviewers. This work was funded by the Coral Reef Targeted Research program.

Author information

Authors and Affiliations

  1. Unidad Académica de Sistemas Arrecifales, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Apdo. Postal 1152, Cancún, Quintana Roo, 77500, México

    M. F. Colombo-Pallotta, A. Rodríguez-Román & R. Iglesias-Prieto

Authors
  1. M. F. Colombo-Pallotta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Rodríguez-Román
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Iglesias-Prieto
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. F. Colombo-Pallotta.

Additional information

Communicated by Biology Editor Dr. Mark Warner

Rights and permissions

Reprints and permissions

About this article

Cite this article

Colombo-Pallotta, M.F., Rodríguez-Román, A. & Iglesias-Prieto, R. Calcification in bleached and unbleached Montastraea faveolata: evaluating the role of oxygen and glycerol. Coral Reefs 29, 899–907 (2010). https://doi.org/10.1007/s00338-010-0638-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-010-0638-x

Keywords

Search

Navigation