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Coral resilience to ocean acidification and global warming through pH up-regulation

Nature Climate Change volume 2, pages 623–627 (2012)Cite this article

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Abstract

Rapidly rising levels of atmospheric CO2 are not only causing ocean warming, but also lowering seawater pH hence the carbonate saturation state of the oceans, on which many marine organisms depend to calcify their skeletons1,2. Using boron isotope systematics3, we show how scleractinian corals up-regulate pH at their site of calcification such that internal changes are approximately one-half of those in ambient seawater. This species-dependent pH-buffering capacity enables aragonitic corals to raise the saturation state of their calcifying medium, thereby increasing calcification rates at little additional energy cost. Using a model of pH regulation combined with abiotic calcification, we show that the enhanced kinetics of calcification owing to higher temperatures has the potential to counter the effects of ocean acidification. Up-regulation of pH, however, is not ubiquitous among calcifying organisms; those lacking this ability are likely to undergo severe declines in calcification as CO2 levels increase. The capacity to up-regulate pH is thus central to the resilience of calcifiers to ocean acidification, although the fate of zooxanthellate corals ultimately depends on the ability of both the photosymbionts and coral host to adapt to rapidly increasing ocean temperatures4.

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Figure 1: Plot of pHT relative to pHcf, determined from boron isotope systematics3 (see Supplementary Information) of aragonitic corals and calcitic foraminifera17.
Figure 2: Percentage change in calcification rates (relative to seawater Ω=4.6) plotted against seawater aragonite saturation state (Ωar).
Figure 3: Future and historical projections of changes in internal saturation state and % changes in coral calcification rates.

References

  1. Kleypas, J. et al. Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284, 118–120 (1999).

    Article  CAS  Google Scholar 

  2. Langdon, C. & Atkinson, M. J. Effect of elevated p CO 2 on photosynthesis and calcification of corals and interactions with seasonal change in temperature/irradiance and nutrient enrichment. J. Geophys. Res. 110, C09S07 (2005).

    Article  Google Scholar 

  3. Trotter, J. A. et al. Quantifying the pH ‘vital effect’ in the temperate zooxanthellate coral Cladocora caespitosa: Validation of the boron seawater pH proxy. Earth Planet. Sci. Lett. 303, 163–173 (2011).

    Article  CAS  Google Scholar 

  4. Howells, E. J. et al. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nature Clim. Change 2, 116–120 (2012).

    Article  Google Scholar 

  5. Pandolfi, J. M., Connolly, S. R., Marshall, D. J. & Cohen, A. L. Projecting coral reef futures under global warming and ocean acidification. Science 333, 418–422 (2011).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Hoegh-Guldberg, O. et al. Coral reefs under rapid climate change and ocean acidification. Science 318, 1737–1742 (2007).

    Article  CAS  Google Scholar 

  8. Silverman, J., Lazar, B., Cao, L., Caldeira, K. & Erez, J. Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys. Res. Lett. 36, 1–5 (2009).

    Article  Google Scholar 

  9. Marubini, F., Barnett, H., Langdon, C. & Atkinson, M. J. Dependence of calcification on light and carbonate ion concentration for the hermatypic coral Porites compressa. Mar. Ecol. Prog. Ser. 220, 153–162 (2001).

    Article  CAS  Google Scholar 

  10. Gattuso, J. P., Frankignoulle, M., Bourge, I. & Romaine, S. Effect of calcium carbonate saturation of seawater on coral calcification. Glob. Planet. Change 18, 37–46 (1998).

    Article  Google Scholar 

  11. Rodolfo-Metalpa, R., Martin, S., Ferrier-Pages, C. & Gattuso, J. P. 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 7, 289–300 (2010).

    Article  CAS  Google Scholar 

  12. Al-Horani, F. A., Al-Moghrabi, S. M. & de Beer, D. The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis. Mar. Biol. 142, 419–426 (2003).

    Article  CAS  Google Scholar 

  13. Cohen, A. L. & McConnaughey, T. A. in Biomineralization (eds Dove, P. M., Weiner, S. & de Yoreo, J. J.) Ch. 6, 151–187 (Reviews in Mineralogy & Geochemistry, Vol. 54, Mineralogical Society of America, 2003).

    Book  Google Scholar 

  14. Allemand, D., Tambutté, E., Zoccola, D. & Tambutté, S. in Coral Reefs: An Ecosystem in Transition Vol. III (eds Dubinsky, Z. & Stambler, N.) 119–150 (Springer, 2011).

    Book  Google Scholar 

  15. Venn, A., Tambutté, E., Holcomb, M., Allemand, D. & Tambutté, S. Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS ONE 6, e20013 (2011).

    Article  CAS  Google Scholar 

  16. Ries, J. B. A physicochemical framework for interpreting the biological calcification response to CO2-induced ocean acidification. Geochim. Cosmochim. Acta 75, 4053–4064 (2011).

    Article  CAS  Google Scholar 

  17. Rae, J. W. B., Foster, G. L., Schmidt, D. N. & Elliott, T. Boron isotopes and B/Ca in benthic foraminifera: Proxies for the deep ocean carbonate system. Earth Planet. Sci. Lett. 302, 403–413 (2011).

    Article  CAS  Google Scholar 

  18. Lowenstam, H. A. & Weiner, S. On Biomineralization (Oxford Univ. Press, 1989).

    Google Scholar 

  19. Burton, E. A. & Walter, L. M. Relative precipitation rates of aragonite and Mg calcite from seawater: Temperature or carbonate ion control? Geology 15, 111–114 (1977).

    Article  Google Scholar 

  20. Holcomb, M., Cohen, A. L., Gabitov, R. I. & Hutter, J. L. Compositional and morphological features of aragonite precipitated experimentally from seawater and biogenically by corals. Geochim. Cosmochim. Acta 73, 4166–4179 (2009).

    Article  CAS  Google Scholar 

  21. Fine, M. & Tchernov, D. Scleractinian coral species survive and recover from decalcification. Science 315, 1811 (2007).

    Article  CAS  Google Scholar 

  22. Gattuso, J-P., Allemand, D. & Frankignoulle, M. 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 (1999).

    Article  CAS  Google Scholar 

  23. Schneider, K., Levy, O., Dubinsky, Z. & Erez, J. In situ diel cycles of photosynthesis and calcification in hermatypic corals. Limnol. Oceanogr. 54, 1995–2002 (2009).

    Article  Google Scholar 

  24. Jokiel, P. & Coles, S. Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar. Biol. 43, 201–208 (1977).

    Article  Google Scholar 

  25. Marshall, A. T. & Clode, P. Calcification rate and the effect of temperature in a zooxanthellate and azooxanthellate scleractinian reef coral. Coral Reefs 23, 218–224 (2004).

    Google Scholar 

  26. Cooper, T. F., O’Leary, R. & Lough, J. M. Growth of Western Australian corals in the anthropocene. Science 335, 593–596 (2012).

    Article  CAS  Google Scholar 

  27. Moy, A. D., Howard, W. R., Bray, S. G. & Trull, T. W. Reduced calcification in modern Souther Ocean planktonic foraminifera. Nature Geosci. 2, 276–280 (2009).

    Article  CAS  Google Scholar 

  28. McCulloch, M. T. et al. Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature 421, 727–730 (2003).

    Article  CAS  Google Scholar 

  29. Leggat, W., Buck, B. H., Grice, A. & Yellowlees, D. The impact of bleaching on the metabolic contribution of dinoflagellate symbionts to their giant clam host. Plant Cell Environ. 26, 1951–1961 (2003).

    Article  CAS  Google Scholar 

  30. Chalker, B. E. & Taylor, D. L. Light-enhanced calcification and the role of oxidative phosphorylation in calcification of the coral Acropora cervicornis (Lamarck). Proc. R. Soc. Lond. B 190, 323–331 (1975).

    Article  CAS  Google Scholar 

  31. Marubini, F., Ferrier-Pagès, C. & Cuif, J-P. Supression of growth in scleractinian corals by decreasing ambient carbonate ion concentration: A cross-family comparison. Proc. R. Soc. Lond. B 270, 179–184 (2002).

    Article  Google Scholar 

  32. Reynaud, S. et al. Interacting effects of CO2 partial pressure and temperature on photosynthesis and calcification in a scleractinian coral. Glob. Change Biol. 9, 1660–1668 (2003).

    Article  Google Scholar 

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

    Article  Google Scholar 

  34. Ries, J. B., Cohen, A. L. & McCorkle, D. C. A nonlinear calcification response to CO2-induced ocean acidification by the coral Oculina arbuscula. Coral Reefs 29, 661–674 (2010).

    Article  Google Scholar 

  35. Anthony, K. R. N., Kline, D. I., Diaz-Pulido, G., Dove, S. & Hoegh-Guldberg, O. Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc. Natl Acad. Sci. USA 105, 17442–17446 (2008).

    Article  CAS  Google Scholar 

  36. Ohde, S. & Hossain, M. M. Effect of CaCO3 (aragonite) saturation state of seawater on calcification of Porites coral. Geochem. J. 38, 613–621 (2004).

    Article  CAS  Google Scholar 

  37. Broecker, W. S., Langdon, C., Takahashi, T. & Peng, T-S. Factors controlling the rate of CaCO3 precipitation on the Grand Bahama Bank. Glob. Biogeochem. Cycles 15, 589–596 (2001).

    Article  CAS  Google Scholar 

  38. Langdon, C. et al. Effect of calcium carbonate saturation state on calcification rate of an experimental coral reef. Glob. Biogeochem. Cycles 14, 639–654 (2000).

    Article  CAS  Google Scholar 

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Acknowledgements

The authors are grateful for financial support from the Australian Research Council Discovery grant DP0986505 awarded to M.M. and J.T. and to the Australian Research Council Centre of Excellence for Coral Reef Studies for support to J.F. and M.M. P.M. is grateful for financial support from the Marie Curie International Outgoing Fellowship (MEDAT-ARCHIVES) and M.M. is supported by a Western Australian Premiers’ Fellowship. This is ISMAR-CNR scientific contribution no. 1745.

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Authors and Affiliations

  1. The UWA Oceans Institute and School of Earth and Environment, University of Western Australia, Crawley, Western Australia 6009, Australia

    Malcolm McCulloch, Jim Falter & Julie Trotter

  2. ARC Centre of Excellence for Coral Reef Studies, University of Western Australia, Crawley, Western Australia 6009, Australia

    Malcolm McCulloch & Jim Falter

  3. Laboratoire des Sciences du Climat et de l’Environnement, Av. de la Terrasse, 91198, Gif-sur-Yvette, France

    Paolo Montagna

  4. Institute of Marine Sciences, Bologna 40129, Italy

    Paolo Montagna

  5. Lamont Doherty Earth Observatory of Columbia University, 61 Route 9W, Palisades, New York 10964, USA

    Paolo Montagna

Authors
  1. Malcolm McCulloch
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  4. Paolo Montagna
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Contributions

M.M. and J.T. designed the study and J.F., M.M. and P.M. carried out the model simulations. M.M. led the writing with contributions from all authors to the analysis of the results and writing the manuscript.

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Correspondence to Malcolm McCulloch.

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McCulloch, M., Falter, J., Trotter, J. et al. Coral resilience to ocean acidification and global warming through pH up-regulation. Nature Clim Change 2, 623–627 (2012). https://doi.org/10.1038/nclimate1473

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