Abstract
About one-third of the carbon dioxide (CO2) released into the atmosphere as a result of human activity has been absorbed by the oceans1, where it partitions into the constituent ions of carbonic acid. This leads to ocean acidification, one of the major threats to marine ecosystems2 and particularly to calcifying organisms such as corals3,4, foraminifera5,6,7 and coccolithophores8. Coccolithophores are abundant phytoplankton that are responsible for a large part of modern oceanic carbonate production. Culture experiments investigating the physiological response of coccolithophore calcification to increased CO2 have yielded contradictory results between and even within species8,9,10,11. Here we quantified the calcite mass of dominant coccolithophores in the present ocean and over the past forty thousand years, and found a marked pattern of decreasing calcification with increasing partial pressure of CO2 and concomitant decreasing concentrations of CO32−. Our analyses revealed that differentially calcified species and morphotypes are distributed in the ocean according to carbonate chemistry. A substantial impact on the marine carbon cycle might be expected upon extrapolation of this correlation to predicted ocean acidification in the future. However, our discovery of a heavily calcified Emiliania huxleyi morphotype in modern waters with low pH highlights the complexity of assemblage-level responses to environmental forcing factors.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Rapid diversification underlying the global dominance of a cosmopolitan phytoplankton
The ISME Journal Open Access 06 February 2023
-
Eocene emergence of highly calcifying coccolithophores despite declining atmospheric CO2
Nature Geoscience Open Access 01 September 2022
-
High-CO2 Levels Rather than Acidification Restrict Emiliania huxleyi Growth and Performance
Microbial Ecology Open Access 27 May 2022
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout



Accession codes
Primary accessions
GenBank/EMBL/DDBJ
Data deposits
The GenBank accession numbers are JN098138–JN098158, JN098160 and JN098163–JN098174; their correspondence is given in the online Supplementary Information.
References
Sabine, C. L. et al. The oceanic sink for anthropogenic CO2 . Science 305, 367–371 (2004)
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)
Gattuso, J.-P., Frankignoulle, M., Bourge, I., Romaine, S. & Buddemeier, R. W. Effect of calcium carbonate saturation of seawater on coral calcification. Global Planet. Change 18, 37–46 (1998)
Kleypas, J. A. et al. Geochemical consequences of increased atmospheric carbon dioxide on coral reefs. Science 284, 118–120 (1999)
Barker, S. & Elderfield, H. Foraminiferal calcification response to glacial–interglacial changes in atmospheric CO2 . Science 297, 833–836 (2002)
Moy, A. D., Howard, W. R., Bray, S. G. & Trull, T. W. Reduced calcification in modern Southern Ocean planktonic foraminifera. Nature Geosci. 2, 276–280 (2009)
de Moel, H. et al. Planktic foraminiferal shell thinning in the Arabian Sea due to anthropogenic ocean acidification? Biogeosciences 6, 1917–1925 (2009)
Riebesell, U. et al. Reduced calcification of marine plankton in response to increased atmospheric CO2 . Nature 407, 364–367 (2000)
Iglesias-Rodriguez, M. D. et al. Phytoplankton calcification in a high-CO2 world. Science 320, 336–340 (2008)
Langer, G. M. et al. Species-specific responses of calcifying algae to changing seawater carbonate chemistry. Geochem. Geophys. Geosyst. 7, Q09006 (2006)
Langer, G., Nehrke, G., Probert, I., Ly, J. & Ziveri, P. Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosci. Discuss. 6, 4361–4383 (2009)
de Vargas, C., Aubry, M. P., Probert, I. & Young, J. in Evolution of Aquatic Photoautotrophs (eds Falkowski, P. G. & Knoll, A. H.) 251–285 (Academic, 2007)
Bollmann, J., Henderiks, J. & Brabec, B. Global calibration of Gephyrocapsa coccolith abundance in Holocene sediments for paleotemperature assessment. Paleoceanogr. 17 10.1029/2001PA000742 (2002)
Lewis, E. & Wallace, D. W. R. Program developed for CO2 system calculations. Carbon Dioxide Information and Analysis Center Report, ORNL/CDIAC-105 (1998)
Hönisch, B. & Hemming, N. G. Surface ocean pH response to variations in pCO2 through two full glacial cycles. Earth Planet. Sci. Lett. 236, 305–314 (2005)
Paasche, E. A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification–photosynthesis interactions. Phycologia 40, 503–529 (2001)
Zondervan, I. The effects of light, macronutrients, trace metals and CO2 on the production of calcium carbonate and organic carbon in coccolithophores—a review. Deep Sea Res. II 54, 521–537 (2007)
Feng, Y. et al. Interactive effects of increased pCO2, temperature and irradiance on the marine coccolithophore Emiliania huxleyi (Prymnesiophyceae). Eur. J. Phycol. 43, 87–98 (2008)
Bollmann, J. & Herrle, J. O. Morphological variation of Emiliania huxleyi and sea surface salinity. Earth Planet. Sci. Lett. 255, 273–288 (2007)
Colmenero-Hidalgo, E., Flores, J. A. & Sierro, F. J. Biometry of Emiliania huxleyi and its biostratigraphic significance in the Eastern North Atlantic Ocean and Western Mediterranean Sea in the last 20 000 years. Mar. Micropaleontol. 46, 247–263 (2002)
Anderson, D. M. & Archer, D. Glacial interglacial stability of ocean pH inferred from foraminifer dissolution rates. Nature 416, 70–73 (2002)
Buitenhuis, E. T., de Baar, H. J. W. & Veldhuis, M. J. W. Photosynthesis and calcification by Emiliania huxleyi (Prymnesiophyceae) as a function of inorganic carbon species. J. Phycol. 35, 949–959 (1999)
Berry, L., Taylor, A. R., Lucken, U., Ryan, K. P. & Brownlee, C. Calcification and inorganic carbon acquisition in coccolithophores. Funct. Plant Biol. 29, 289–299 (2002)
Mackinder, L., Wheeler, G., Schroeder, D., Riebesell, U. & Brownlee, C. Molecular mechanisms underlying calcification in coccolithophores. Geomicrobiol. J. 27, 585–595 (2010)
Zondervan, I., Rost, B. & Riebesell, U. Effect of CO2 concentration on the PIC/POC ratio in the coccolithophore Emiliania huxleyi grown under light-limiting conditions and different daylengths. J. Exp. Mar. Biol. Ecol. 272, 55–70 (2002)
Young, J. et al. A guide to extant coccolithophore taxonomy. J. Nannoplankton Res. 1 (Special Issue). 1–132 (2003)
Hagino, K. et al. New evidence for morphological and genetic variation in the cosmopolitan coccolithophore Emiliania huxleyi (Prymnesiophyseae) from the COX1b-ATP4 genes. J. Phycol. (in the press)
Gibbs, S. J., Bown, P. R., Sessa, J. A., Bralower, T. J. & Wilson, P. A. Nannoplankton extinction and origination across the Paleocene–Eocene Thermal Maximum. Science 314, 1770–1773 (2006)
Monnin, E. et al. Atmospheric CO2 concentrations over the last glacial termination. Science 291, 112–114 (2001)
Petit, J. R. et al. Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature 399, 429–436 (1999)
Acknowledgements
We thank the crew from Puerto Deseado, Atalante, Suroit and Marion-Dufresne, and D. Vaulot, L. Garczarek, M.-A. Sicre and H. Claustre for their help in collecting material for this work. The long-term OISO observational programme is supported by INSU (Institut National des Sciences de l’Univers), IPSL (Institut Pierre-Simon Laplace) and IPEV (Institut Paul-Emile Victor). We thank F. C. Bassinot for help in estimating palaeosalinities. The IMAGES programme is acknowledged for collection and curation of the cores. This work was funded by the ‘Agence National de la Recherche’ project PALEO-CTD (grant ANR-06-JCJC-0142), by the European Research Council under grant agreement 205150, by the European Funding Agencies from the ERA-net program Biodiversa, under the Biomarks project, and by the European Community’s Seventh Framework Program EPOCA (European Project on Ocean Acidification) under grant agreement 211384.
Author information
Authors and Affiliations
Contributions
On the basis of an original idea from L.B., the concept of this paper was developed in discussion between all authors. L.B., N.B., P.C. and M.G. conducted coccolith measurements, D.R.-P., N.M. and C.G. conducted modern-ocean chemistry measurements, L.B. and T.d.G.-T. computed past ocean chemistry, E.M.B., I.P. and C.d.V. performed genetic analyses, B.R., R.E.M.R. and I.P. conceptualized the physiological interpretation, L.B., I.P., D.R.-P., C.d.V. and R.E.M.R. interpreted the relationships between calcification and environment.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
This file contains Supplementary Methods, Supplementary Figures 1-7 with legends, Supplementary Tables 1-4 and additional references. (PDF 7250 kb)
Rights and permissions
About this article
Cite this article
Beaufort, L., Probert, I., de Garidel-Thoron, T. et al. Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476, 80–83 (2011). https://doi.org/10.1038/nature10295
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature10295
This article is cited by
-
Rapid diversification underlying the global dominance of a cosmopolitan phytoplankton
The ISME Journal (2023)
-
High-CO2 Levels Rather than Acidification Restrict Emiliania huxleyi Growth and Performance
Microbial Ecology (2023)
-
Malformation in coccolithophores in low pH waters: evidences from the eastern Arabian Sea
Environmental Science and Pollution Research (2023)
-
An integrated multiple driver mesocosm experiment reveals the effect of global change on planktonic food web structure
Communications Biology (2022)
-
Cyclic evolution of phytoplankton forced by changes in tropical seasonality
Nature (2022)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.