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Effects of increased pCO2 on zinc uptake and calcification in the tropical coral Stylophora pistillata

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Abstract

Zinc (Zn) is an essential element for corals. We investigated the effects of ocean acidification on zinc incorporation, photosynthesis, and gross calcification in the scleractinian coral Stylophora pistillata. Colonies were maintained at normal pHT (8.1) and at two low-pH conditions (7.8 and 7.5) for 5 weeks. Corals were exposed to 65Zn dissolved in seawater to assess uptake rates. After 5 weeks, corals raised at pHT (8.1) exhibited higher 65Zn activity in the coral tissue and skeleton, compared with corals raised at a lower pH. Photosynthesis, photosynthetic efficiency, and gross calcification, measured by 45Ca incorporation, were however unchanged even at the lowest pH.

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References

  • Al-Horani FA, Al-Moghrabi SM, de Beer D (2003) Microsensor study of photosynthesis and calcification in the scleractinian coral Galaxea fascicularis: active internal carbon cycle. J Exp Mar Biol Ecol 288:1–15

    Article  Google Scholar 

  • Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105:17442–17446

    Article  PubMed  CAS  Google Scholar 

  • Atkinson MJ, Carlson B, Crown GL (1995) Coral in high-nutrient, low-pH seawater: a case study of corals cultured at Waikiki Aquarium, Honolulu, Hawaii. Coral Reefs 14:215–223

    Google Scholar 

  • Bertucci A, Innocenti A, Zoccola D, Scozzafava A, Allemand D, Tambutté S, Supuran CT (2009a) Carbonic anhydrase inhibitors: inhibition studies of a coral secretory isoform with inorganic anions. Bioorg Med Chem Lett 19:650–653

    Article  PubMed  CAS  Google Scholar 

  • Bertucci A, Innocenti A, Zoccola D, Scozzafava A, Allemand D, Tambutté S, Supuran CT (2009b) Carbonic anhydrase inhibitors: Inhibition studies of a secretory isoform by sulfonamides. Bioorg Med Chem 17:5054–5058

    Article  PubMed  CAS  Google Scholar 

  • Bertucci A, Tambutté E, Tambutté S, Allemand D, Zoccola D (2010a) Symbiosis-dependent gene expression in coral-dinoflagellate association: cloning and characterization of a P-type H+ATPase gene. Proc R Soc B 277:87–95

    Article  PubMed  CAS  Google Scholar 

  • Bertucci A, Zoccola D, Tambutte S, Vullo D, Suppuran CT (2010b) Carbonic anhydrases activators, the first activation study of a coral secretory isoform with amino acids and amines. Bioorg Med Chem 18:2300–2303

    Article  PubMed  CAS  Google Scholar 

  • Bruland KW (1980) Oceanographic distributions of cadmium, zinc, nickel and copper in the North Pacific. Earth Planet Sci Lett 47:176–198

    Article  CAS  Google Scholar 

  • Bruland KW (1989) Complexation of zinc by natural organic ligands in the Central North Pacific. Limnol Oceanogr 34:269–285

    Article  CAS  Google Scholar 

  • Burris JE, Porter JW, Laing WA (1983) Effects of carbon dioxide concentration on coral photosynthesis. Mar Biol 75:113–116

    Article  CAS  Google Scholar 

  • Byrne RH (2002) Inorganic speciation of dissolved elements in seawater: The influence of pH on concentration ratios. Geochemical Transactions 3:11–16

    Article  Google Scholar 

  • Caldeira K, Wickett ME (2003) Oceanography: Anthropogenic carbon and ocean pH. Nature 425:365

    Article  PubMed  CAS  Google Scholar 

  • deBoer ML, Krupp DA, Weis VM (2006) Two atypical carbonic anhydrase homologs from the planula larva of the scleractinian coral Fungia scutaria. Biol Bull 211:18–30

    Article  PubMed  CAS  Google Scholar 

  • Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication 3:191

    Google Scholar 

  • Edmunds PJ, Spencer-Davies P (1988) Post-illumination stimulation of respiration rate in the coral Porites porites. Coral Reefs 7:7–9

    Article  Google Scholar 

  • Ferrier-Pagès C, Houlbrèque F, Wyse E, Richard C, Allemand D, Boisson F (2005) Bioaccumulation of zinc in the scleractinian coral Stylophora pistillata. Coral Reefs 24:636–645

    Article  Google Scholar 

  • Furla P, Benazet-Tambutté S, Jaubert J, Allemand D (1998) Diffusional permeability of dissolved inorganic carbon through the isolated oral epithelial layers of the sea anemone, Anemonia veridis. J Exp Mar Biol Ecol 221:71–88

    Article  CAS  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

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Harland AD, Brown BE (1989) Metal tolerance in the scleractinian coral Porites lutea. Mar Pollut Bull 20:353–357

    Article  CAS  Google Scholar 

  • Houlbrèque F, Tambutté E, Ferrier-Pagès C (2003) Effect of zooplankton availability on the rates of photosynthesis, and tissue and skeletal growth in the Scleractinian coral Stylophora pistillata. J Exp Mar Biol Ecol 296:145–166

    Article  Google Scholar 

  • Jeffree RA, Warnau M, Teyssie JL, Markich SJ (2006) Comparison of the bioaccumulation from seawater and depuration of heavy metals and radionuclides in the spotted dogfish Scyliorhinus canicula (Chondrichthys) and the turbot Psetta maxima (Actinopterygii: Teleostei). Sci Total Environ 368:839–852

    Article  PubMed  CAS  Google Scholar 

  • Jury CP, Whitehead RF, Szmant AM (2009) Effects of variations in carbonate chemistry on the calcification rates of Madracis auretenra (=Madracis mirabilis sensus Wells, 1973): bicarbonate concentrations best predict calcification rates. Global Change Biol 16:1632–1644

    Article  Google Scholar 

  • Kleypas JA, Buddemeier RW, Archer D, Gattuso JP, Langdon C, Opdyke BN (1999) Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284:118–120

    Article  PubMed  CAS  Google Scholar 

  • Krief S, Hendy EJ, Fine M, Yam R, Meibom A, Foster GL, Shemesh A (2010) Physiological and isotopic responses of scleractinian corals to ocean acidification. Geochim Cosmochim Acta 74:4988–5001

    Article  CAS  Google Scholar 

  • Lacoue-Labarthe T, Martin S, Oberhansli F, Teyssie JL, Markish S, Ross J, Bustamante P (2009) Effects of increased pCO2 and temperature on trace element (Ag, Cd and Zn) bioaccumulation in the eggs of the common cuttlefish, Sepia officinalis. Biogeosciences 6:2561–2573

    Article  CAS  Google Scholar 

  • Lane TW, Morel FMM (2000) Regulation of carbonic anhydrase expression by zinc, cobalt, and carbon dioxide in the marine diatom Thalassiosira weissflogii. Plant Physiol 123:345–352

    Article  PubMed  CAS  Google Scholar 

  • Langdon C, Atkinson MJ (2005) Effects of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res 110:C09507. doi:10.1029/2004JC002576

    Article  Google Scholar 

  • Langdon C, Broecker WS, Hammond DE, Glenn E, Fitzsimmons K, Nelson SG, Peng TH, Hajdas I, Bonani G (2003) Effect of elevated CO2 on the community metabolism of an experimental coral reef. Global Biogeochem Cycles 17:11–14

    Article  Google Scholar 

  • Lohan MC, Statham PJ, Crawford DW (2002) Dissolved zinc in the upper water column of the subarctic North East Pacific. Deep-Sea Res II 49:5793–5808

    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 136A:417–426

    CAS  Google Scholar 

  • Martin JH, Gordon RM, Fitzwater S, Broenkow WW (1989) VERTEX: Phytoplankton studies in the Gulf of Alaska. Deep Sea Res 36:649–680

    Article  CAS  Google Scholar 

  • Marubini F, Ferrier-Pages C, Furla P, Allemand D (2008) Coral calcification responds to seawater acidification: a working hypothesis towards a physiological mechanism. Coral Reefs 27:491–499

    Article  Google Scholar 

  • Millero FJ, Woosley R, Ditrolio B, Waters J (2009) Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22:72–85

    Article  Google Scholar 

  • Morel FMM, Reinfelder JR, Roberts SB, Chamberlain CP, Lee JG, Yee D (1994) Zinc and carbon co-limitation of marine phytoplankton. Nature 369:740–742

    Article  CAS  Google Scholar 

  • Moya A, Tambutte S, Lotto S, Allemand D, Zoccola D (2008) Carbonic anhydrase in the scleractinian coral Stylophora pistillata: characterization, localization and role in biomineralisation. J Biol Chem 283:25475–25484

    Article  PubMed  CAS  Google Scholar 

  • Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely AF, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686

    Article  PubMed  CAS  Google Scholar 

  • Raven JA, Evans MCW, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosyn Res 60:111–149

    Article  CAS  Google Scholar 

  • Reichelt-Brushett AJ, McOrist G (2003) Trace metals in the living and nonliving components of scleractinian corals. Mar Pollut Bull 46:1573–1582

    Article  PubMed  CAS  Google Scholar 

  • Reynaud S, Leclercq N, Romaine-Lioud S, Ferrier-Pagès C, Jaubert J, Gattuso JP (2003) Interacting effects of pCO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Global Change Biol 9:1660–1668

    Article  Google Scholar 

  • Ries J, Cohen A, McCorkle D (2009) Marine biocalcifiers exhibit mixed responses to CO2 induced ocean acidification. Geology 37:1131–1134

    Article  CAS  Google Scholar 

  • Ries JB, Cohen AL, McCorkle DC (2010) A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. Coral Reefs 29:661–674

    Article  Google Scholar 

  • Rodolfo-Metalpa R, Lombardi C, Cocito S, Hall-Spencer JM, Gambi MC (2010a) Effects of ocean acidification and high temperature on the bryozoan Myriapora truncata at natural CO2 vents. Mar Ecol 31:447–456

  • Rodolfo-Metalpa R, Martin S, Ferrier-Pagès C, Gattuso JP (2010b) Response of the temperate coral Cladocora caespitosa to mid- and long-term exposure to pCO2 and temperature levels projected in 2100AD. Biogeosciences 7:289–300

    Article  CAS  Google Scholar 

  • Ruiz-Pino DP, Nicolas E, Bethoux JP, Lambert CE (1991) Zinc budget in the Mediterranean Sea: a hypothesis for non-steady-state behavior. Mar Chem 33:145–169

    Article  CAS  Google Scholar 

  • Santore RC, Mathew R, Paquin PR, Di Toro D (2002) Applications of the biotic ligand model to predicting zinc toxicity to rainbow trout, fathead minnow, and Daphnia magna. Comp Biochem Physiol C 133:271–285

    Google Scholar 

  • Schneider K, Erez J (2006) The effect of carbonate chemistry on calcification and photosynthesis in the hermatypic coral Acropora eurystoma. Limnol Oceanogr 51:1284–1293

    Article  CAS  Google Scholar 

  • Schulz KG, Zondervan I, Gerringa LJA, Timmermans KR, Veldhuis MJW, Riebesell U (2004) Effect of trace metal availability on coccolithophorid calcification. Nature 430:673–676

    Article  PubMed  CAS  Google Scholar 

  • Tambutté É, Allemand D, Bourge I, Gattuso JP, Jaubert J (1995) An improved 45Ca protocol for investigating physiological mechanisms in coral calcification. Mar Biol 122:453–459

    Article  Google Scholar 

  • Tambutté 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

    Google Scholar 

  • Tréguer P, Le Corre P (1975) Manuel d’analyses des sels nutritifs dans l’eau de mer. Laboratoire d’Océanographie chimique. Univ de Bretagne Occidentale, Brest

    Google Scholar 

  • Vallee BL, Auld DS (1990) Zinc coordination, function and structure of zinc enzymes and other proteins. Biochemistry 29:5647–5659

    Article  PubMed  CAS  Google Scholar 

  • Warnau M, Teyssié JL, Fowler SW (1996) Biokinetics of selected heavy metals and radionuclides in the common Mediterranean echinoid Paracentrotus lividus: seawater and food exposures. Mar Ecol Prog Ser 141:83–94

    Article  CAS  Google Scholar 

  • Whicker FW, Schultz V (1982) Radioecology: nuclear energy and the environment. CRC Press, Boca Raton

    Google Scholar 

  • Wood HL, Spicer JI, Widdicombe S (2008) Ocean acidification may increase calcification rates, but at cost. Proc Biol Sci 275:1767–1773

    Article  PubMed  Google Scholar 

  • Zondervan I (2007) The effects of light, macronutrients, trace metals and CO2 on the production of calcium carbonate and organic carbon in coccolithophores—A review. Deep-Sea Res II 54:521–537

    Article  Google Scholar 

Download references

Acknowledgments

The International Atomic Energy Agency is grateful to the Government of the Principality of Monaco for the support provided to its Environment Laboratories. Thanks are due to Dr J. Ries and Pr T. A. McConnaughey for their helpful comments and constructive remarks on this manuscript. We also thank Dr. M. Holcomb for fruitful discussions on calcification processes.

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Correspondence to F. Houlbrèque.

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Communicated by Environment Editor Prof. Rob van Woesik

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Houlbrèque, F., Rodolfo-Metalpa, R., Jeffree, R. et al. Effects of increased pCO2 on zinc uptake and calcification in the tropical coral Stylophora pistillata . Coral Reefs 31, 101–109 (2012). https://doi.org/10.1007/s00338-011-0819-2

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