Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Coral and mollusc resistance to ocean acidification adversely affected by warming

Nature Climate Change volume 1, pages 308–312 (2011)Cite this article

Subjects

Abstract

Increasing atmospheric carbon dioxide (CO2) concentrations are expectedto decrease surface ocean pH by 0.3–0.5 units by 2100 (refs 1, 2), lowering the carbonate ion concentration of surfacewaters. This rapid acidification is predicted to dramatically decrease calcification in many marine organisms3,4. Reduced skeletal growth under increased CO2 levels has already been shown for corals, molluscs and many other marine organisms4,5,6,7,8,9. The impact of acidification on the ability of individual species to calcify has remained elusive, however, as measuring net calcification fails to disentangle the relative contributions of gross calcification and dissolution rates on growth. Here, we show that corals and molluscs transplanted along gradients of carbonate saturation state at Mediterranean CO2 vents are able to calcify and grow at even faster than normal rates when exposed to the high CO2 levels projected for the next 300 years. Calcifiers remain at risk, however, owing to the dissolution of exposed shells and skeletons that occurs as pH levels fall. Our results show that tissues and external organic layers play a major role in protecting shells and skeletons from corrosive sea water, limiting dissolution and allowing organisms to calcify10,11. Our combined field and laboratory results demonstrate that the adverse effects of global warming are exacerbated when high temperatures coincide with acidification.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Species transplanted along a pH gradient near volcanic CO2 vents off Ischia, Italy.
Figure 2: Gross calcification of M. galloprovincialis measured in aquaria over a three-week period at pHT 7.4 and 8.1.
Figure 3: Calcification of P. caerulea measured in aquaria at pHT 6.8 and 8.0.
Figure 4: Underwater and scanning electron microscopy images of B. europaea transplanted along a CO2 gradient off Ischia.
Figure 5: Calcification rates of corals transplanted along a CO2 gradient off Ischia.

Similar content being viewed by others

References

  1. Caldeira, K. & Wickett, M. E. Anthropogenic carbon and ocean pH. Nature 425, 365 (2003).

    Article  CAS  Google Scholar 

  2. Orr, J. C. et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681–686 (2005).

    Article  CAS  Google Scholar 

  3. Kleypas, J. A. et al. Impact of Ocean Acidification on Coral Reefs and Other Marine Calcifiers: A Case Guide for Future Research (Report of a workshop held 18–20 April 2005, St. Petersburg, FL, sponsored by NSF, NOAQA, and US Geological Survey, 2006).

  4. Kroeker, K., Kordas, R. L., Crim, R. N. & Singh, F. G. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419–1434 (2010).

    Article  Google Scholar 

  5. 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 

  6. Silverman, J. et al. Coral reefs may start dissolving when atmospheric CO2 doubles. Geophys. Res. Lett. 36, L05606 (2009).

    Article  Google Scholar 

  7. Gazeau, F. et al. Impact of elevated CO2 on shellfish calcification. Geophys. Res. Lett. 34, L07603 (2007).

    Article  Google Scholar 

  8. Fabricius, K. E. et al. Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations. Nature Clim. Change 1, 165–169 (2011).

    Article  CAS  Google Scholar 

  9. Cohen, A. L. et al. Morphological and compositional changes in the skeletons of new coral recruits reared in acidified seawater: Insights into the biomineralization response to ocean acidification. Geochem. Geophys. Geosyst 10, Q07005 (2009).

    Article  Google Scholar 

  10. Ries, J., Cohen, A. & McCorkle, D. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 37, 1131–1134 (2009).

    Article  CAS  Google Scholar 

  11. Tunnicliffe, V. et al. Survival of mussels in extremely acidic waters on a submarine volcano. Nature Geosci. 2, 344–348 (2009).

    Article  CAS  Google Scholar 

  12. Wood, H. L., Spicer, J. I. & Widdicombe, S. Ocean acidification may increase calcification rates, but at a cost. Proc. R. Soc. B 275, 1767–1773 (2008).

    Article  Google Scholar 

  13. Jury, C. P., Whitehead, R. F. & Szmant, A. M. Effects of variations in carbonate chemistry on the calcification rates of Madracis auretenra (= Madracis mirabilis sensu Wells, 1973): Bicarbonate concentrations best predict calcification rates. Glob. Change Biol. 16, 1632–1644 (2009).

    Article  Google Scholar 

  14. Krief, S. et al. Physiological and isotopic responses of scleractinian corals to ocean acidification. Geochim. Cosmochim. Acta 74, 4988–5001 (2010).

    Article  CAS  Google Scholar 

  15. Rodolfo-Metalpa, R., Martin, S., Ferrier-Pagès, 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. Biogeosciences 7, 289–300 (2010).

    Article  CAS  Google Scholar 

  16. Ries, J. 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. Trotter, J. 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 

  18. Al-Horani, F. A., Al-Moghrabi, S. M. & de Beer, D. Microsensor study of photosynthesis and calcification in the scleractinian coral, Galaxea fascicularis: Active internal carbon cycle. J. Exp. Mar. Biol. Ecol. 288, 1–15 (2003).

    Article  Google Scholar 

  19. McConnaughey, T. A. & Gillikin, D. P. Carbon isotopes in mollusk shell carbonates. Geo-Mar. Lett. 28, 287–299 (2008).

    Article  CAS  Google Scholar 

  20. Venn, A. et al. Live tissue imaging shows reef corals elevate pH under their calcifying tissue relative to seawater. PLoS ONE 6, 1–9 (2011).

    Article  Google Scholar 

  21. Hall-Spencer, J. M. et al. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454, 96–99 (2008).

    Article  CAS  Google Scholar 

  22. Rodolfo-Metalpa, R. et al. Effects of ocean acidification and high temperatures on the bryozoan Myriapora truncata at natural CO2 vents. Mar. Ecol. 31, 447–456 (2010).

    CAS  Google Scholar 

  23. Thomsen, J. et al. Calcifying invertebrates succeed in a naturally CO2-rich coastal habitat but are threatened by high levels of future acidification. Biogeosciences 410, 3879–3891 (2010).

    Article  Google Scholar 

  24. Porzio, L., Buia, M. C. & Hall-Spencer, J. M. Effects of ocean acidification on macroalgal communities. J. Exp. Mar. Biol. Ecol. 400, 278–287 (2011).

    Article  CAS  Google Scholar 

  25. Lejeusne, C. et al. Climate change effects on a miniature ocean: The highly diverse, highly impacted Mediterranean Sea. Trends Ecol. Evol. 25, 250–260 (2010).

    Article  Google Scholar 

  26. Diaz-Pulido, G. et al. High CO2 enhances the competitive strength of seaweeds over corals. Ecol. Lett. 14, 156–162 (2011).

    Article  Google Scholar 

  27. Manzello, D. P. et al. Poorly cemented coral reefs of the eastern tropical Pacific: Possible insights into reef development in a high-CO2 world. Proc. Natl Acad. Sci. USA 105, 10450–10455 (2008).

    Article  CAS  Google Scholar 

  28. Dickson, A. G., Sabine, C. L. & Christian, J. R. (eds) in Guide to Best Practices for Ocean CO2 Measurements (PICES Special Publication 3, 2007); available at http://cdiac.ornl.gov/oceans/Handbook_2007.html.

  29. Pierrot, D. E. & Wallace, D. W. MS Excel Program Developed for CO 2 System Calculation ORNL/CDIAC-105a (Carbon Dioxide Information Analysis Center, 2006).

  30. Tambutté, É. et al. An improved 45Ca protocol for investigating physiological mechanisms in coral calcification. Mar. Biol. 122, 453–459 (1995).

    Article  Google Scholar 

Download references

Acknowledgements

We thank all collaborators from Stazione Zoologica ‘A. Dohrn’ for their help during fieldwork, D. Allemand and C. Ferrier-Pagès for helpful discussions, and J-F. Comanducci, F. Oberhänsli and J-L. Teyssié for their help during radiotracer experiments. Comments by P. Mumby and J. Ries improved this manuscript. This work was funded by the Prince Albert II of Monaco Foundation, the International Atomic Energy Agency (IAEA-NAML, Monaco, which is grateful to the Government of the Principality of Monaco for the support provided to its Environment Laboratories), Save our Seas Foundation, an EU MARES studentship and the EU ‘Mediterranean Sea Acidification under a changing climate’ project (MedSeA; grant agreement 265103). The work contributes to the European Project on Ocean Acidification (EPOCA; grant agreement 211384).

Author information

Author notes

  1. F. Houlbrèque

    Present address: Present addresses: Centre IRD, 98848, Noumea, Nouvelle-Caledonie, France (F.H.); School of the Environment, Faculty of Science, University of Technology, NSW 2007 Sydney, Australia (R.J.),

Authors and Affiliations

  1. International Atomic Energy Agency—Marine Environment Laboratories, 4 Quai Antoine 1er, 98000 Monaco, Principality of Monaco

    R. Rodolfo-Metalpa, F. Houlbrèque, F. Boisson & R. Jeffree

  2. Marine Institute, Marine Biology and Ecology Research Centre, University of Plymouth, Plymouth PL4 8AA, UK

    R. Rodolfo-Metalpa, C. Baggini, A. Foggo & J. M. Hall-Spencer

  3. Centre Scientifique de Monaco, Avenue Saint Martin, 98000 Monaco, Principality of Monaco

    É. Tambutté

  4. Stazione Zoologica ‘A. Dohrn’, Functional and Evolutionary Ecology Laboratory, Punta S. Pietro, 80077 Ischia (Naples), Italy

    F. P. Patti

  5. The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan 52900, Israel

    M. Fine

  6. Interuniversity Institute for Marine Science, Eilat 88103, Israel

    M. Fine

  7. INSU-CNRS, Laboratoire d’Océanographie de Villefranche, B.P. 28, 06234 Villefranche-sur-mer Cedex, France

    J-P. Gattuso

  8. UPMC University of Paris 06, Observatoire Océanologique de Villefranche, 06230 Villefranche-sur-mer, France

    J-P. Gattuso

Authors
  1. R. Rodolfo-Metalpa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Houlbrèque
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. É. Tambutté
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Boisson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. Baggini
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. F. P. Patti
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R. Jeffree
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. M. Fine
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. A. Foggo
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. J-P. Gattuso
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. J. M. Hall-Spencer
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

R.R-M. and F.B. designed the study. Most experiments were performed by R.R-M., who wrote the paper in collaboration with F.H., J.M.H-S., M.F. and J-P.G. Coral radiotracer incorporation was performed by F.H. Scanning electron microscopy was performed by E.T. on corals and C.B. on mussels. A.F. performed the statistical analysis. All authors read and commented on the manuscript.

Corresponding author

Correspondence to R. Rodolfo-Metalpa.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 50045 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rodolfo-Metalpa, R., Houlbrèque, F., Tambutté, É. et al. Coral and mollusc resistance to ocean acidification adversely affected by warming. Nature Clim Change 1, 308–312 (2011). https://doi.org/10.1038/nclimate1200

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate1200

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing