Abstract
The effect of decreasing aragonite saturation state (ΩArag) of seawater (elevated pCO2) on calcification rates of Acropora muricata was studied using nubbins prepared from parent colonies located at two sites of La Saline reef (La Réunion Island, western Indian Ocean): a back-reef site (BR) affected by nutrient-enriched groundwater discharge (mainly nitrate), and a reef flat site (RF) with low terrigenous inputs. Protein and chlorophyll a content of the nubbins, as well as zooxanthellae abundance, were lower at RF than BR. Nubbins were incubated at ~27°C over 2 h under sunlight, in filtered seawater manipulated to get differing initial pCO2 (1,440–340 μatm), ΩArag (1.4–4.0), and dissolved inorganic carbon (DIC) concentrations (2,100–1,850 μmol kg−1). Increasing DIC concentrations at constant total alkalinity (AT) resulted in a decrease in ΩArag and an increase in pCO2. AT at the beginning of the incubations was kept at a natural level of 2,193 ± 6 μmol kg−1 (mean ± SD). Net photosynthesis (NP) and calcification were calculated from changes in pH and AT during the incubations. Calcification decrease in response to doubling pCO2 relative to preindustrial level was 22% for RF nubbins. When normalized to surface area of the nubbins, (1) NP and calcification were higher at BR than RF, (2) NP increased in high pCO2 treatments at BR compared to low pCO2 treatments, and (3) calcification was not related to ΩArag at BR. When normalized to NP, calcification was linearly related to ΩArag at both sites, and the slopes of the relationships were not significantly different. The increase in NP at BR in the high pCO2 treatments may have increased calcification and thus masked the negative effect of low ΩArag on calcification. Removing the effect of NP variations at BR showed that calcification declined in a similar manner with decreased ΩArag (increased pCO2) whatever the nutrient loading.
References
Allemand D, Ferrier-Pagès C, Furla P, Houlbrèque F, Puverel S, Reynaud S, Tambutté É, Tambutté S, Zoccola D (2004) Biomineralisation in reef-building corals: from molecular mechanisms to environmental control. Comptes Rendus Palevol 3:453–467
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
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
Atkinson MJ, Cuet P (2008) Possible effects of ocean acidification on coral reef biogeochemistry: topics for research. Mar Ecol Prog Ser 373:249–256
Atkinson MJ, Carlson B, Crow GL (1995) Coral growth in high-nutrient, low-pH seawater: a case study of corals cultured at the Waikiki Aquarium, Honolulu, Hawaii. Coral Reefs 14:215–223
Buxton L, Badger M, Ralph P (2009) Effects of moderate heat stress and dissolved inorganic carbon concentration on photosynthesis and respiration of Symbiodinium sp. (Dinophyceae) in culture and in symbiosis. J Phycol 45:357–365
Cordier E (2007) Dynamique hydrosédimentaire du récif frangeant de l’Hermitage/La Saline (La Réunion): processus physiques et flux sédimentaires. Ph.D. thesis, Université de La Réunion, p 193
Cuet P, Naim O, Faure G, Conan JY (1988) Nutrient-rich groundwater impact on benthic communities of La Saline fringing reef (Reunion Island, Indian Ocean): preliminary results. Proc 6th Int Coral Reef Symp 2:207–212
Dennison WC, Barnes DJ (1988) Effect of water motion on coral photosynthesis and calcification. J Exp Mar Biol Ecol 115:67–77
Dickson AG (1990) Standard potential of the reaction: AgCl(s) + 1/2H2(g) = Ag(s) + HCl(aq), and the standard acidity constant of the ion HSO4 in synthetic seawater from 273.15 to 318.15 K. J Chem Thermodyn 22:113–127
Dickson AG, Goyet C (1994) Handbook of methods for the analysis of the various parameters of the carbon dioxide system in seawater (Version 2). DOE (US Department of Energy) ORNL/CDIAC-74. Carbon Dioxide Information and Analysis Center, Oak Ridge, Tennesee
Doney SC, Fabry VJ, Feely RA, Kleypas JA (2009) Ocean acidification: the other CO2 problem. Annu Rev Mar Sci 1:169–192
Dubinsky Z, Stambler N, Ben-Zion M, McCloskey LR, Muscatine L, Falkowski PG (1990) The effect of external nutrient resources on the optical properties and photosynthetic efficiency of Stylophora pistillata. Proc R Soc Biol Sci Ser B 239:231–246
Eakin CM, Kleypas J, Hoegh-Guldberg O (2008) Global climate change and coral reefs: rising temperatures, acidification and the need for resilient reefs. In: Wilkinson C (ed) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville, Australia, pp 29–34
Edmunds P, Gates R (2002) Normalizing physiological data for scleractinian corals. Coral Reefs 21:193–197
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
Ferrier-Pagès C, Gattuso J, Dallot S, Jaubert J (2000) Effect of nutrient enrichment on growth and photosynthesis of the zooxanthellate coral Stylophora pistillata. Coral Reefs 19:103–113
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
Gattuso J, 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
Herfort L, Thake B, Taubner I (2008) Bicarbonate stimulation of calcification and photosynthesis in two hermatypic corals. J Phycol 44:91–98
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
Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742
Holcomb M, McCorkle DC, Cohen AL (2010) Long-term effects of nutrient and CO2 enrichment on the temperate coral Astrangia poculata (Ellis and Solander, 1786). J Exp Mar Biol Ecol 386:27–33
Holmes G (2008) Estimating three-dimensional surface areas on coral reefs. J Exp Mar Biol Ecol 365:67–73
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
Jeffrey SW, Humphrey GF (1975) New spectrophotometric equations for determining chlorophylls a, b, c 1 and c 2 in algae, phytoplankton and higher plants. Biochem Physiol Pflanz 167:191–194
Johannes RE, Wiebe WJ (1970) A method for determination of coral tissue biomass and composition. Limnol Oceanogr 15:822–824
Jury C, Whitehead R, Szmant A (2009) 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
Kleypas JA, Langdon C (2006) Coral reefs and changing seawater carbonate chemistry. In: Phinney JT, Hoegh-Guldberg O, Kleypas JA, Skirving W, Strong A (eds) Coral reefs and climate change: science and management. Coast Estuar Sci 61:73–110
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
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
Langdon C, Atkinson MJ (2005) Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J Geophys Res 110, C09S07. doi:10.1029/2004JC002576
Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations, ORNL/CDIAC-105. Carbon Dioxide Information and Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennesee. Available at: http://cdiac.esd.ornl.gov/oceans/co2rprt.html
Manzello DP (2010) Ocean acidification hot spots: spatiotemporal dynamics of the seawater CO2 system of eastern Pacific coral reefs. Limnol Oceanogr 55:239–248
Markwell MAK, Haas SM, Bieber LL, Tolbert NE (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87:206–210
Marubini F, Atkinson MJ (1999) Effects of lowered pH and elevated nitrate on coral calcification. Mar Ecol Prog Ser 188:117–121
Marubini F, Davies PS (1996) Nitrate increases zooxanthellae population density and reduces skeletogenesis in corals. Mar Biol 127:319–328
Marubini F, Thake B (1999) Bicarbonate addition promotes coral growth. Limnol Oceanogr 44:716–720
Marubini F, Ferrier-Pages C, Cuif J-P (2003) Suppression of skeletal growth in scleractinian corals by decreasing ambient carbonate ion concentration: a cross-family comparison. Proc R Soc Lond B Biol Sci 270:179–184
Marubini F, Ferrier-Pagès C, Furla P, Allemand D (2008) Coral calcification responds to seawater acidification: a working hypothesis towards a physiological mechanism. Coral Reefs 27:491–499
McConnaughey TA, Whelan JF (1997) Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci Rev 42:95–117
Naim O, Cuet P, Mangar V (2000) The Mascarene Islands. In: McClanahan TR, Sheppard CRC, Obura DO (eds) Coral reefs of the Indian Ocean: their ecology and conservation. University Press, Oxford, pp 353–381
Ohde S, Hossain MMM (2004) Effect of CaCO3 (aragonite) saturation state of seawater on calcification of Porites coral. Geochem J 38:613–621
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner G, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686
Renegar DA, Riegl BM (2005) Effect of nutrient enrichment and elevated CO2 partial pressure on growth rate of Atlantic scleractinian coral Acropora cervicornis. Mar Ecol Prog Ser 293:69–76
Reynaud S, Leclercq N, Romaine-Lioud S, Ferrier-Pages C, Jaubert J, Gattuso JP (2003) Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Global Change Biol 9:1660–1668
Ries JB, Cohen AL, McCorkle DC (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37:1131–1134
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
Roy RN, Roy LN, Vogel KM, Porter-Moore C, Pearson T, Good CE, Millero FJ, Campbell DM (1993) The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45°C. Mar Chem 44:249–267
Sabine CL, Feely RA, Gruber N, Key RM, Lee K, Bullister JL, Wanninkhof R, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng T, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305:367–371
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
Smith SV, Key GS (1975) Carbon dioxide and metabolism in marine environments. Limnol Oceanogr 20:493–495
Stambler N, Popper N, Dubinsky Z, Stimson J (1991) Effects of nutrient enrichment and water motion on the coral Pocillopora damicornis. Pac Sci 45:299–307
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
Tanaka Y, Miyajima T, Koike I, Hayashibara T, Ogawa H (2007) Imbalanced coral growth between organic tissue and carbonate skeleton caused by nutrient enrichment. Limnol Oceanogr 52:1139–1146
Tribollet A (2008) The boring microflora in modern coral reef ecosystems: a review of its roles. In: Wisshak M, Tapanila L (eds) Current developments in bioerosion. Springer, Berlin, Heidelberg and New York, pp 67–94
Wallace CC (1999) Staghorn corals of the world. A revision of the coral genus Acropora (Scleractinia; Astrocoeniina; Acroporidae) worldwide, with emphasis on morphology, phylogeny and biogeography. CSIRO Publishing, Collingwood, Australia
Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291
Weis VM, Allemand D (2009) What determines coral health? Science 324:1153–1155
Acknowledgments
The authors would like to thank Amandine Pierre and Marjorie Sawadogo for laboratory assistance, Kévin Coustaut for help with iconography and Karyne Rogers for English corrections. This research was made possible through the financial support of the Conseil Régional de La Réunion (ITUE program) and performed under collecting permit number 94/DRAM/09. The manuscript was greatly improved with help from the topic editor Mark Warner and two anonymous reviewers.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Mark Warner
Rights and permissions
About this article
Cite this article
Chauvin, A., Denis, V. & Cuet, P. Is the response of coral calcification to seawater acidification related to nutrient loading?. Coral Reefs 30, 911–923 (2011). https://doi.org/10.1007/s00338-011-0786-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-011-0786-7