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More than local adaptation: high diversity of response to seawater acidification in seven coral species from the same assemblage in French Polynesia

Published online by Cambridge University Press:  16 September 2021

Mathilde Godefroid*
Affiliation:
PSL Research University: EPHE-CNRS-UPVD, USR 3278 CRIOBE, BP 1013, 98729 Papetoai, Mo'orea, French Polynesia Laboratoire d'Excellence “ CORAIL”, Mo'orea, French Polynesia
Robin Arçuby
Affiliation:
PSL Research University: EPHE-CNRS-UPVD, USR 3278 CRIOBE, BP 1013, 98729 Papetoai, Mo'orea, French Polynesia Laboratoire d'Excellence “ CORAIL”, Mo'orea, French Polynesia
Yann Lacube
Affiliation:
PSL Research University: EPHE-CNRS-UPVD, USR 3278 CRIOBE, BP 1013, 98729 Papetoai, Mo'orea, French Polynesia Laboratoire d'Excellence “ CORAIL”, Mo'orea, French Polynesia
Benoit Espiau
Affiliation:
PSL Research University: EPHE-CNRS-UPVD, USR 3278 CRIOBE, BP 1013, 98729 Papetoai, Mo'orea, French Polynesia Laboratoire d'Excellence “ CORAIL”, Mo'orea, French Polynesia
Sam Dupont
Affiliation:
Department of Biological and Environmental Sciences, University of Gothenburg, Kristineberg Marine Research Station, Kristineberg 566, 45178 Fiskebäckskil, Sweden
Frédéric Gazeau
Affiliation:
Sorbonne Université, CNRS, Laboratoire d'Océanographie de Villefranche, LOV, 06230 Villefranche-sur-Mer, France
Marc Metian
Affiliation:
Environment Laboratories, International Atomic Energy Agency, 4a Quai Antoine 1er, MC-98000, Principality of Monaco, Monaco
Laetitia Hédouin
Affiliation:
PSL Research University: EPHE-CNRS-UPVD, USR 3278 CRIOBE, BP 1013, 98729 Papetoai, Mo'orea, French Polynesia Laboratoire d'Excellence “ CORAIL”, Mo'orea, French Polynesia
*
Author for correspondence: Mathilde Godefroid, E-mail: [email protected]

Abstract

Responses of corals to seawater acidification have been extensively studied. Sensitivity varies widely between species, highlighting the need to avoid extrapolation from one to another to get an accurate understanding of coral community responses. We tested the responses of seven coral species (Acropora cytherea, Acropora hyacinthus, Acropora pulchra, Leptastrea pruinosa, Montipora grisea, Pavona cactus, Pocillopora verrucosa) from the Mo'orea lagoon to a 48-day exposure to three pH scenarios (pH 7.95, 7.7 and 7.3). Tissue necrosis, mortality, growth rates, photophysiological performances and colour index were recorded. Few significant differences were noted between pH 7.95 and 7.7, but species-specific responses were observed at pH 7.3. While our data do not allow identification of the mechanisms behind this diversity in response between species inhabiting the same environment, it can exclude several hypotheses such as local adaptation, skeletal type, corallum morphology or calcification rate as sole factors determining coral sensitivity to pH.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Anderson, AJ, Kuffner, IB, Mackenzie, FT, Jokiel, PL, Rodgers, KS and Tan, A (2009) Net loss of CaCO3 from a subtropical calcifying community due to seawater acidification: mesocosm-scale experimental evidence. Biogeosciences (Online) 6, 18111823.CrossRefGoogle Scholar
Atkinson, MJ and Cuet, P (2008) Possible effects of ocean acidification on coral reef biogeochemistry: topics for research. Marine Ecology Progress Series 373, 249256.CrossRefGoogle Scholar
Bahr, KD, Jokiel, PL and Rodgers, KS (2016) Relative sensitivity of five Hawaiian coral species to high temperature under high-pCO2 conditions. Coral Reefs 35, 729738.CrossRefGoogle Scholar
Ban, SS, Graham, NAJ and Connolly, SR (2014) Evidence for multiple stressor interactions and effects on coral reefs. Global Change Biology 20, 681697.CrossRefGoogle ScholarPubMed
Barkley, HC, Cohen, AL, McCorkle, DC and Golbuu, Y (2017) Mechanisms and thresholds for pH tolerance in Palau corals. Journal of Experimental Marine Biology and Ecology 489, 714.CrossRefGoogle Scholar
Barner, AK, Chan, F, Hettinger, A, Hacker, SD, Marshall, K and Menge, BA (2018) Generality in multispecies responses to ocean acidification revealed through multiple hypothesis testing. Global Change Biology 24, 44644477.CrossRefGoogle ScholarPubMed
Barott, KL, Venn, AA, Perez, SO, Tambutté, S and Tresguerres, M (2015) Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis. Proceedings of the National Academy of Sciences USA 112, 607612.CrossRefGoogle ScholarPubMed
Bedwell-Ivers, HE, Koch, MS, Peach, KE, Joles, L, Dutra, E and Manfrino, C (2017) The role of in hospite zooxanthellae photophysiology and reef chemistry on elevated pCO2 effects in two branching Caribbean corals: Acropora cervicornis and Porites divaricata. ICES Journal of Marine Science 74, 11031112.CrossRefGoogle Scholar
Bielmyer-Fraser, GK, Patel, P, Capo, T and Grosell, M (2018) Physiological responses of corals to ocean acidification and copper exposure. Marine Pollution Bulletin 133, 781790.CrossRefGoogle ScholarPubMed
Biscéré, T, Rodolfo-Metalpa, R, Lorrain, A, Chauvaud, L, Thébault, J, Clavier, J and Houlbrèque, F (2015) Responses of two scleractinian corals to cobalt pollution and ocean acidification. PLoS ONE 10, e0122898.CrossRefGoogle ScholarPubMed
Blunden, J and Arndt, DS (2019) State of the climate in 2018. Bulletin of the American Meteorological Society 100, SiS306.CrossRefGoogle Scholar
Bopp, L, Resplandy, L, Orr, JC, Doney, SC, Dunne, JP, Gehlen, M, Halloran, P, Heinze, C, Ilyina, T, Seferian, R and Tjiputra, J (2013) Multiple stressors of ocean ecosystems in the 21st century: projections with CMIP5 models. Biogeosciences (Online) 10, 62256245.CrossRefGoogle Scholar
Burke, L, Reytar, M and Spalding, M (2011) Reefs at Risk: Revisited. Washington, DC: World Resources Institute, 115 pp.Google Scholar
Chan, NCS and Connolly, SR (2013) Sensitivity of coral calcification to ocean acidification: a meta-analysis. Global Change Biology 19, 282290.CrossRefGoogle ScholarPubMed
Cheal, AJ, MacNeil, MA, Emslie, MJ and Sweatman, H (2017) The threat to coral reefs from more intense cyclones under climate change. Global Change Biology 23, 15111524.CrossRefGoogle ScholarPubMed
Comeau, S, Edmunds, PJ, Spindel, NB and Carpenter, RC (2013) The responses of eight coral reef calcifiers to increasing partial pressure of CO2 do not exhibit a tipping point. Limnology and Oceanography 58, 388398.CrossRefGoogle Scholar
Comeau, S, Edmunds, PJ, Spindel, NB and Carpenter, RC (2014 a) Fast coral reef calcifiers are more sensitive to ocean acidification in short-term laboratory incubations. Limnology and Oceanography 59, 10811091.CrossRefGoogle Scholar
Comeau, S, Carpenter, RC, Nojiri, Y, Putnam, HM, Sakai, K and Edmunds, PJ (2014 b) Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification. Proceedings of the Royal Society B: Biological Sciences 281, 20141339.CrossRefGoogle ScholarPubMed
Comeau, S, Carpenter, RC, Lantz, CA and Edmunds, PJ (2016) Parameterization of the response of calcification to temperature and pCO2 in the coral Acropora pulchra and the alga Lithophyllum kotschyanum. Coral Reefs 35, 929939.CrossRefGoogle Scholar
Comeau, S, Cornwall, SC and McCulloch, MT (2017 a) Decoupling between the response of coral calcifying fluid pH and calcification to ocean acidification. Scientific Reports 7, 110.CrossRefGoogle ScholarPubMed
Comeau, S, Carpenter, RC and Edmunds, PJ (2017 b) Effects of pCO2 on photosynthesis and respiration of tropical scleractinian corals and calcified algae. ICES Journal of Marine Science 74, 10921102.CrossRefGoogle Scholar
Comeau, S, Cornwall, CE, DeCarlo, TM, Doo, SS, Carpenter, RC and McCulloch, MT (2019) Resistance to ocean acidification in coral reef taxa is not gained by acclimatization. Nature Climate Change 9, 477483.CrossRefGoogle Scholar
Crawley, A, Kline, DI, Dunn, S, Anthony, K and Dove, S (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biology 16, 851863.CrossRefGoogle Scholar
Davies, PS (1989) Short-term growth measurements of corals using an accurate buoyant weighing technique. Marine Biology 101, 389395.CrossRefGoogle Scholar
De Putron, SJ, McCorkle, DC, Cohen, AL and Dillon, AB (2011) The impact of seawater saturation state and bicarbonate ion concentration on calcification by new recruits of two Atlantic corals. Coral Reefs 30, 321328.CrossRefGoogle Scholar
Dickson, AG and Millero, FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Research Part A. Oceanographic Research Papers 34, 17331743.CrossRefGoogle Scholar
Dickson, AG, Sabine, CL and Christian, JR (2007) Guide to Best Practices for Ocean CO2 Measurements. Sydney: North Pacific Marine Science Organization.Google Scholar
DeCarlo, TM, Comeau, S, Cornwall, CE and McCulloch, MT (2018) Coral resistance to ocean acidification linked to increased calcium at the site of calcification. Proceedings of the Royal Society B: Biological Sciences 285, 20180564.CrossRefGoogle Scholar
Doney, SC, Fabry, VJ, Feely, RA and Kleypas, JA (2009) Ocean acidification: the other CO2 problem. Annual Review of Marine Science 1, 169192.CrossRefGoogle ScholarPubMed
Edmunds, PJ (2018) MCR LTER: Coral Reef: Long-term Population and Community Dynamics: Corals. Moorea Coral Reef LTER. Ongoing since 2005.Google Scholar
Edmunds, PJ and Burgess, SC (2016) Size-dependent physiological responses of the branching coral Pocillopora verrucosa to elevated temperature and pCO2. Journal of Experimental Biology 219, 38963906.Google ScholarPubMed
Edmunds, PJ, Doo, SS and Carpenter, RC (2019) Changes in coral reef community structure in response to year-long incubations under contrasting pCO2 regimes. Marine Biology 166, 112.CrossRefGoogle Scholar
Enochs, IC, Manzello, DP, Carlton, R, Schopmeyer, S, Van Hooidonk, R and Lirman, D (2014) Effects of light and elevated pCO2 on the growth and photochemical efficiency of Acropora cervicornis. Coral Reefs 33, 477485.Google Scholar
Erez, J, Reynaud, S, Silverman, J, Schneider, K, Allemand, D, Erez, J, Silverman, J, Schneider, K, Reynaud, S and Allemand, D (2011) Coral calcification under ocean acidification and global change. In Dubinsky, Z and Stambler, N (eds), Coral Reefs: An Ecosystem in Transition. Dordrecht: Springer, pp. 151176.CrossRefGoogle Scholar
Evensen, NR and Edmunds, PJ (2017) Conspecific aggregations mitigate the effects of ocean acidification on calcification of the coral Pocillopora verrucosa. Journal of Experimental Biology 220, 10971105.Google ScholarPubMed
Fine, M and Tchernov, D (2007) Scleractinian coral species survive and recover from decalcification. Science (New York, N.Y.) 315, 1811.CrossRefGoogle ScholarPubMed
Foster, T, Falter, JL, McCulloch, MT and Clode, PL (2016) Climate science: ocean acidification causes structural deformities in juvenile coral skeletons. Science Advances 2, e1501130.CrossRefGoogle Scholar
Frieler, K, Meinshausen, M, Golly, A, Mengel, M, Lebek, K, Donner, SD and Hoegh-Guldberg, O (2013) Limiting global warming to 2°C is unlikely to save most coral reefs. Nature Climate Change 3, 165170.CrossRefGoogle Scholar
Gabay, Y, Fine, M, Barkay, Z and Benayahu, Y (2014) Octocoral tissue provides protection from declining oceanic pH. PLoS ONE 9, 410.CrossRefGoogle ScholarPubMed
Gattuso, JP and Hansson, L (2011) Ocean Acidification. Oxford: Oxford University Press.CrossRefGoogle Scholar
Gattuso, JP, Frankignoulle, M, Bourge, I, Romaine, S and Buddemeier, RW (1998) Effect of calcium carbonate saturation of seawater on coral calcification. Global and Planetary Change 18, 3746.CrossRefGoogle Scholar
Gattuso, JP, Hoegh-Guldberg, O and Pörtner, HO (2014) Cross-chapter box on coral reefs. In Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press.Google Scholar
Gattuso, JP, Magnan, A, Billé, R, Cheung, WWL, Howes, EL, Joos, F, Allemand, D, Bopp, L, Cooley, SR, Eakin, CM and Hoegh-Guldberg, O (2015) Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science (New York, N.Y.) 349.CrossRefGoogle Scholar
Halpern, BS, Frazier, M, Potapenko, J, Casey, KS, Koenig, K, Longo, C, Lowndes, JS, Rockwood, RC, Selig, ER, Selkoe, KA and Walbridge, S (2015) Spatial and temporal changes in cumulative human impacts on the world's ocean. Nature Communications 6, 17.CrossRefGoogle ScholarPubMed
Hendriks, IE, Duarte, CM and Álvarez, M (2010) Vulnerability of marine biodiversity to ocean acidification: a meta-analysis. Estuarine, Coastal and Shelf Science 86, 157164.CrossRefGoogle Scholar
Hoegh-Guldberg, O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50, 839866.Google Scholar
Hoegh-Guldberg, O, Cai, R, Poloczanska, ES, Brewer, PG, Sundby, S, Hilmi, K, Fabry, VJ and Jung, S (2014) The Ocean. In Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press, pp. 16551731.Google Scholar
Hoegh-Guldberg, O, Jacob, D, Taylor, M, Bindi, M, Brown, S, Camilloni, I, Diedhiou, A, Djalante, R, Ebi, KL, Engelbrecht, F, Guiot, J, Hijioka, Y, Mehrotra, S, Payne, A, Seneviratne, SI, Thomas, A, Warren, R and Zhou, G (2018) Impacts of 1.5°C Global Warming on Natural and Human Systems. In Global Warming of 1.5°C. An IPCC Special Report on the Impacts of Global Warming of 1.5°C above Pre-industrial levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change, Sustainable Development, and Efforts to Eradicate Poverty. Geneva: IPCC.Google Scholar
Hofmann, GE, Barry, JP, Edmunds, PJ, Gates, RD, Hutchins, DA, Klinger, T and Sewell, MA (2010) The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism-to-ecosystem perspective. Annual Review of Ecology, Evolution, and Systematics 41, 127147.CrossRefGoogle Scholar
Hughes, TP, Baird, AH, Bellwood, DR, Card, M, Connolly, SR, Folke, C, Grosberg, R, Hoegh-Guldberg, O, Jackson, JB, Kleypas, J and Lough, JM (2003) Climate change, human impacts, and the resilience of coral reefs. Science (New York, N.Y.) 301, 929933.CrossRefGoogle ScholarPubMed
Hughes, TP, Barnes, ML, Belwood, DR, Cinner, JE, Cumming, GS, Jackson, JB, Kleypas, J, Van De Leemput, IA, Lough, JM, Morrison, TH and Palumbi, SR (2017) Coral reefs in the Anthropocene. Nature 546, 8290.CrossRefGoogle ScholarPubMed
IPCC (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva: IPCC.Google Scholar
Jokiel, PL (2011) The reef coral two compartment proton flux model: a new approach relating tissue-level physiological processes to gross corallum morphology. Journal of Experimental Marine Biology and Ecology 409, 112.CrossRefGoogle Scholar
Jokiel, PL, Rodgers, KS, Kuffner, IB, Andersson, AJ, Cox, EF and Mackenzie, FT (2008) Ocean acidification and calcifying reef organisms: a mesocosm investigation. Coral Reefs 27, 473483.CrossRefGoogle Scholar
Kennedy, EV, Perry, CT, Halloran, PR, Iglesias-Prieto, R, Schönberg, CHL, Wisshak M, Form, AU, Carricart-Ganivet, JP, Fine, M, Eakin, CM and Mumby, PJ (2013) Avoiding coral reef functional collapse requires local and global action. Current Biology 23, 912918.CrossRefGoogle ScholarPubMed
Kleypas, A, Feely, RA, Fabry, VJ, Langdon, C, Sabine, CL and Robbins, LL (2006) Impacts of ocean acidification on coral reefs and other marine calcifiers: a guide for future research. Report of a workshop held 18–20 April 2005, St. Petersburg, FL, sponsored by NSF, NOAA, and the U.S. Geological Survey, 88 pp.Google Scholar
Krief, S, Hendy, EJ, Fine, M, Yam, R, Meibom, A, Foster, GL and Shemesh, A (2010) Physiological and isotopic responses of scleractinian corals to ocean acidification. Geochimica et Cosmochimica Acta 74, 49885001.CrossRefGoogle Scholar
Kroeker, KJ, Kordas, RL, Crim, RN and Singh, GG (2010) Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecology Letters 13, 14191434.CrossRefGoogle ScholarPubMed
Kvitt, H, Kramarsky-Winter, E, Maor-Landaw, K, Zandbank, K, Kushmaro, A, Rosenfeld, H, Fine, M and Tchernov, D (2015) Breakdown of coral colonial form under reduced pH conditions is initiated in polyps and mediated through apoptosis. Proceedings of the National Academy of Sciences USA 112, 20822086.CrossRefGoogle ScholarPubMed
Langdon, C and Atkinson, MJ (2005) Effect of elevated pCO2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. Journal of Geophysical Research: Oceans 110.CrossRefGoogle Scholar
Lewis, E, Wallace, D and Allison, LJ (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105, 121.Google Scholar
McCulloch, MT, Falter, J, Trotter, J and Montagna, P (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nature Climate Change 2, 623627.CrossRefGoogle Scholar
Mehrbach, C, Culberson, CH, Hawley, JE and Pytkowicx, RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18, 897907.CrossRefGoogle Scholar
Nakamura, T, Iguchi, A, Suzuki, A, Sakai, K and Nojiri, Y (2017) Effects of acidified seawater on calcification, photosynthetic efficiencies and the recovery processes from strong light exposure in the coral Stylophora pistillata. Marine Ecology 38, e12444.CrossRefGoogle Scholar
Pandolfi, JM, Connolly, SR, Marshall, DJ and Cohen, AL (2011) Projecting coral reef futures under global warming and ocean acidification. Science (New York, N.Y.) 333, 418422.CrossRefGoogle ScholarPubMed
Pearson, PN and Palmer, MR (2000) Atmospheric carbon dioxide concentrations over the past 60 million years. Nature 406, 695699.CrossRefGoogle ScholarPubMed
Pelejero, C, Calvo, E and Hoegh-Guldberg, O (2010) Paleo-perspectives on ocean acidification. Trends in Ecology & Evolution 25, 332344.CrossRefGoogle ScholarPubMed
Pendleton, L, Comte, A, Langdon, C, Ekstrom, JA, Cooley, SR, Suatoni, L, Beck, MW, Brander, LM, Burke, L, Cinner, JE and Doherty, C (2016) Coral reefs and people in a high-CO2 world: where can science make a difference to people? PLoS ONE 11, e0164699.CrossRefGoogle Scholar
Putnam, HM, Davidson, JM and Gates, RD (2016) Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evolutionary Applications 9, 11651178.CrossRefGoogle ScholarPubMed
R Core Team (2017) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available at https://www.R-project.org/Google Scholar
Raven, J, Caldeira, K, Elderfield, H, Hoegh-Guldberg, O, Liss, P, Riebesell, U, Shepherd, J, Turley, C and Watson, A (2005) Ocean Acidification due to Increasing Atmospheric Carbon Dioxide. London: Royal Society, 68 pp.Google Scholar
Ridgewell, A and Schmidt, DN (2010) Past constraints on the vulnerability of marine calcifiers to massive carbon dioxide release. Nature Geoscience 3, 196200.CrossRefGoogle Scholar
Ries, J, Cohen, A and McCorkle, D (2009) Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37, 11311134.CrossRefGoogle Scholar
Rivest, EB and Gouhier, TC (2015) Complex environmental forcing across the biogeographical range of coral populations. PLoS ONE 10, e0121742.CrossRefGoogle ScholarPubMed
Rodolfo-Metalpa, R, Martin, S, Ferrier-Pagès, C and Gattuso, JP (2010) Response of the temperate coral Cladocora caespitosa to mid- and long-term exposure to pCO2 and temperature levels projected for the year 2100 AD. Biogeosciences (Online) 7, 289300.CrossRefGoogle Scholar
Rodolpho-Metalpa, R, Houlbrèque, F, Tambutté, E and Hall-Spencer, JM (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nature Climate Change 1, 308312.CrossRefGoogle Scholar
Ruel, JJ and Ayres, MP (1999) Jensen's inequality predicts effects of environmental variation. Trends in Ecology & Evolution 14, 361366.CrossRefGoogle ScholarPubMed
Sanford, E and Kelly, MW (2011) Local adaptation in marine invertebrates. Annual Review of Marine Science 3, 509535.CrossRefGoogle ScholarPubMed
Schleussner, CF, Lissner, TK, Fischer, EM, Wohland, J, Perrette, M, Golly, A, Rogelj, J, Childers, K, Schewe, J, Frieler, K and Mengel, M (2016) Differential climate impacts for policy-relevant limits to global warming: the case of 1.5°C and 2°C. Earth System Dynamics 7, 327351.CrossRefGoogle Scholar
Sekizawa, A, Uechi, H, Iguchi, A, Nakamura, T, Kumagai, NH, Suzuki, A, Sakai, K and Nojiri, Y (2017) Intraspecific variations in responses to ocean acidification in two branching coral species. Marine Pollution Bulletin 122, 282287.CrossRefGoogle ScholarPubMed
Shaw, EC, Munday, PL and McNeil, BI (2013) The role of CO2 variability and exposure time for biological impacts of ocean acidification. Geophysical Research Letters 40, 46854688.CrossRefGoogle Scholar
Siebeck, UE, Marshall, NJ, Kluter, A and Hoegh-Guldberg, O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25, 453460.CrossRefGoogle Scholar
Silbiger, NJ, Guadayol, O, Thomas, F and Donahue, MJ (2014) Reefs shift from net accretion to net erosion along a natural environmental gradient. Marine Ecology Progress Series 515, 3344.CrossRefGoogle Scholar
Tambutté, E, Venn, AA, Holcomb, M, Segonds, N, Techer, N, Zoccola, D, Allemand, D and Tambutté, S (2015) Morphological plasticity of the coral skeleton under CO2-driven seawater acidification. Nature Communications 6, 19.CrossRefGoogle ScholarPubMed
Vargas, CA, Lagos, NA, Lardies, MA, Duarte, C, Manríquez, PH, Aguilera, VM, Broitman, B, Widdicombe, S and Dupont, S (2017) Species-specific responses to ocean acidification should account for local adaptation and adaptive plasticity. Nature Ecology & Evolution 1, 17.CrossRefGoogle ScholarPubMed
Veron, JEN (1995) Corals in Space and Time: The Biogeography and Evolution of the Scleractinia. Ithaca, NY: Cornell University Press.Google Scholar
Vidal-Dupiol, J, Zoccola, D, Tambutté, E, Grunau, C, Cosseau, C, Smith, KM, Freitag, M, Dheilly, NM, Allemand, D and Tambutté, S (2013) Genes related to ion-transport and energy production are upregulated in response to CO2-driven pH decrease in corals: new insights from transcriptome analysis. PLoS ONE 8, e58652.CrossRefGoogle ScholarPubMed
Yuan, X, Guo, T, Cai, WJ, Huang, H, Zhou, W and Liu, S (2019) Coral responses to ocean warming and acidification: implications for future distribution of coral reefs in the South China Sea. Marine Pollution Bulletin 138, 241248.CrossRefGoogle ScholarPubMed
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