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:

Biomineralization control related to population density under ocean acidification

Abstract

Anthropogenic CO2 is a major driver of present environmental change in most ecosystems1, and the related ocean acidification is threatening marine biota2. With increasing pCO2, calcification rates of several species decrease3, although cases of upregulation are observed4. Here, we show that biological control over mineralization relates to species abundance along a natural pH gradient. As pCO2 increased, the mineralogy of a scleractinian coral (Balanophyllia europaea) and a mollusc (Vermetus triqueter) did not change. In contrast, two calcifying algae (Padina pavonica and Acetabularia acetabulum) reduced and changed mineralization with increasing pCO2, from aragonite to the less soluble calcium sulphates and whewellite, respectively. As pCO2 increased, the coral and mollusc abundance was severely reduced, with both species disappearing at pH < 7.8. Conversely, the two calcifying and a non-calcifying algae (Lobophora variegata) showed less severe or no reductions with increasing pCO2, and were all found at the lowest pH site. The mineralization response to decreasing pH suggests a link with the degree of control over the biomineralization process by the organism, as only species with lower control managed to thrive in the lowest pH.

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

Access options

Buy this article

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

Figure 1: Range in pH total scale and mean percentage of cover for Balanophyllia europaea, Vermetus triqueter, Padina pavonica, Acetabularia acetabulum and Lobophora variegata along the pCO2 gradient.
Figure 2: Scanning electron microscope images of a longitudinal section of Vermetus triqueter shell-tube.
Figure 3: Scanning electron microscope images of Padina pavonica thalli and Acetabularia acetabulum cups.
Figure 4: In situ pictures of Padina pavonica and Acetabularia acetabulum at Sites 1 and 4, showing the reduction of calcified material (white areas) with increasing pCO2.

Similar content being viewed by others

References

  1. IPCC, IPCC Special Report on Renewable Energy Sources and Climate Change Mitigation (Cambridge Univ. Press, 2011).

  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. Fabry, V. J., Seibel, B. A., Feely, R. A. & Orr, J. C. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci. 65, 414–432 (2008).

    Article  CAS  Google Scholar 

  4. Rodolfo-Metalpa, R., Martin, S., Ferrier-Pages, C. & Gattuso, J. P. Response of Mediterranean corals to ocean acidification. Biogeosciences Discuss. 6, 7103–7131 (2010).

    Article  Google Scholar 

  5. Hahn, S. et al. Marine bivalve shell geochemistry and ultrastructure from modern low pH environments: environmental effect versus experimental bias. Biogeosciences 9, 1897–1914 (2012).

    Article  CAS  Google Scholar 

  6. Barry, J. P., Hall-Spencer, J. M. & Tyrrell, T. Guide to Best Practices for Ocean Acidification Research and Data Reporting (Publications Office of the European Union, 2010).

  7. 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 

  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. Cigliano, M., Gambi, M. C., Rodolfo-Metalpa, R., Patti, F. P. & Hall-Spencer, J. M. Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents. Mar. Biol. 157, 2489–2502 (2010).

    Article  Google Scholar 

  10. 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 

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

    Google Scholar 

  12. 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 

  13. Venn, A. A. et al. Impact of seawater acidification on pH at the tissue–skeleton interface and calcification in reef corals. Proc. Natl Acad. Sci. USA 110, 1634–1639 (2013).

    Article  CAS  Google Scholar 

  14. Fantazzini, P. et al. A time-domain nuclear magnetic resonance study of Mediterranean scleractinian corals reveals skeletal-porosity sensitivity to environmental changes . Environ. Sci. Technol. 47, 12679–12686 (2013).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  16. McCandless, E. L. & Craigie, J. S. Sulfated polysaccharides in red and brown algae. Ann. Rev. Plant Physiol. 30, 41–53 (1979).

    Article  CAS  Google Scholar 

  17. Mann, S., Webb, J. & Williams, R. J. P. Biomineralization: Chemical and Biochemical Perspectives (VCH Verlagsgesellschaft, 1989).

    Google Scholar 

  18. Robbins, L. L., Knorr, P. O. & Hallock, P. Response of Halimeda to ocean acidification: field and laboratory evidence. Biogeosci. Discuss. 6, 4895–4918 (2009).

    Article  Google Scholar 

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

    Article  Google Scholar 

  20. Fabry, V. J. Marine calcifiers in a high-CO2 ocean. Science 320, 1020–1022 (2008).

    Article  CAS  Google Scholar 

  21. Johnson, V. R., Russell, B. D., Fabricius, K. E., Brownlee, C. & Hall-Spencer, J. M. Temperate and tropical brown macroalgae thrive, despite decalcification, along natural CO2 gradients. Glob. Change Biol. 18, 2792–2803 (2012).

    Article  Google Scholar 

  22. Cornwall, C. E. et al. Carbon-use strategies in macroalgae: Differential responses to lowered pH and implications for ocean acidification. J. Phycol. 48, 137–144 (2012).

    Article  CAS  Google Scholar 

  23. Hofmann, L. C., Straub, S. & Bischof, K. Competition between calcifying and noncalcifying temperate marine macroalgae under elevated CO2 levels. Mar. Ecol. Prog. Ser. 464, 89–105 (2012).

    Article  CAS  Google Scholar 

  24. Sarker, M. Y., Bartsch, I., Olischläger, M., Gutow, L. & Wiencke, C. Combined effects of CO2, temperature, irradiance and time on the physiological performance of Chondrus crispus (Rhodophyta). Bot. Mar. 56, 63–74 (2013).

    Article  Google Scholar 

  25. Cronin, G. & Hay, M. E. Effects of light and nutrient availability on the growth, secondary chemistry, and resistance to herbivory of two brown seaweeds. Oikos 77, 93–106 (1996).

    Article  CAS  Google Scholar 

  26. Rohde, S., Hiebenthal, C., Wahl, M., Karez, R. & Bischof, K. Decreased depth distribution of Fucus vesiculosus (Phaeophyceae) in the Western Baltic: Effects of light deficiency and epibionts on growth and photosynthesis. Eur. J. Phycol. 43, 143–150 (2008).

    Article  Google Scholar 

  27. Munday, P. L., Warner, R. R., Monro, K., Pandolfi, J. M. & Marshall, D. J. Predicting evolutionary responses to climate change in the sea. Ecol. Lett. 16, 1488–1500 (2013).

    Article  Google Scholar 

  28. Anderson, J. T., Inouye, D. W., McKinney, A. M., Colautti, R. I. & Mitchell-Olds, T. Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proc. R. Soc. B 279, 3843–3852 (2012).

    Article  Google Scholar 

  29. Dias, B. B., Hart, M. B., Smart, C. W. & Hall-Spencer, J. M. Modern seawater acidification: The response of foraminifera to high-CO2 conditions in the Mediterranean Sea. J. Geol. Soc. 167, 843–846 (2010).

    Article  CAS  Google Scholar 

  30. Calosi, P. et al. Distribution of sea urchins living near shallow water CO2 vents is dependent upon species acid-base and ion-regulatory abilities. Mar. Pollut. Bull. 73, 470–484 (2013).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

I. Berman-Frank helped with alkalinity measurements. B. Basile, F. Sesso, and Eolo Sub diving centre assisted in the field. F. Gizzi and G. Polimeni helped during preparation and participated in field surveys. The Scientific Diving School supplied scientific, technical and logistical support. The research leading to these results has received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP/2007-2013)/ERC Grant Agreement no. [249930 - CoralWarm].

Author information

Authors and Affiliations

Authors

Contributions

S.G., Z.D. and G.F. conceived and designed research. S.G., F.P., E.C. and B.C. collected the samples and performed the diving fieldwork. L.P., S.F., M.R. and G.F. performed the laboratory experiments. S.G., F.P., E.C., B.C., L.P., P.F., M.R., K.E.F. and G.F. analysed the data. All authors wrote the manuscript and participated in the scientific discussion.

Corresponding authors

Correspondence to Stefano Goffredo or Giuseppe Falini.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Goffredo, S., Prada, F., Caroselli, E. et al. Biomineralization control related to population density under ocean acidification. Nature Clim Change 4, 593–597 (2014). https://doi.org/10.1038/nclimate2241

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nclimate2241

This article is cited by

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