Letter | Published:

Reduced calcification of marine plankton in response to increased atmospheric CO2

Nature volume 407, pages 364367 (21 September 2000) | Download Citation



The formation of calcareous skeletons by marine planktonic organisms and their subsequent sinking to depth generates a continuous rain of calcium carbonate to the deep ocean and underlying sediments1. This is important in regulating marine carbon cycling and ocean–atmosphere CO2 exchange2. The present rise in atmospheric CO2 levels3 causes significant changes in surface ocean pH and carbonate chemistry4. Such changes have been shown to slow down calcification in corals and coralline macroalgae5,6, but the majority of marine calcification occurs in planktonic organisms. Here we report reduced calcite production at increased CO2 concentrations in monospecific cultures of two dominant marine calcifying phytoplankton species, the coccolithophorids Emiliania huxleyi and Gephyrocapsa oceanica . This was accompanied by an increased proportion of malformed coccoliths and incomplete coccospheres. Diminished calcification led to a reduction in the ratio of calcite precipitation to organic matter production. Similar results were obtained in incubations of natural plankton assemblages from the north Pacific ocean when exposed to experimentally elevated CO2 levels. We suggest that the progressive increase in atmospheric CO2 concentrations may therefore slow down the production of calcium carbonate in the surface ocean. As the process of calcification releases CO2 to the atmosphere, the response observed here could potentially act as a negative feedback on atmospheric CO2 levels.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from $8.99

All prices are NET prices.


  1. 1.

    Production and accumulation of calcium carbonate in the ocean: budget of a nonsteady state. Glob. Biogeochem. Cycles 7, 927–957 (1993).

  2. 2.

    & Significance of ocean carbonate budgets for the global carbon cycle. Glob. Change Biol. 2, 85–95 ( 1996).

  3. 3.

    et al. (eds) Climate Change 1994: Radiative Forcing of Climate Change and an Evaluation of the IS92 Emission Scenario (Cambridge Univ. Press, Cambridge, 1995).

  4. 4.

    , , & Direct effects of CO2 concentration on growth and isotopic composition of marine plankton. Tellus 51B, 461– 476 (1999).

  5. 5.

    , , , & Effect of calcium carbonate saturation of seawater on coral calcification. Glob. Planet. Change 18, 37–46 ( 1998).

  6. 6.

    , , , , , , , & Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochem. Cycles 14, 639–654 ( 2000).

  7. 7.

    , & Coccolith production (biomineralisation) in the marine alga Emiliania huxleyi. J. Protozool. 36, 368–373 (1989).

  8. 8.

    et al. A model system approach to biological climate forcing. The example of Emiliania huxleyi. Glob. Planet. Change 8, 27–46 (1993).

  9. 9.

    , & in Coccolithophores (eds Winter, A. & Siesser, W. G.) 161–179 (Cambridge Univ. Press, Cambridge, 1994).

  10. 10.

    et al. Strategies for the study of climate forcing by calcification. Bull. Inst. Oceanogr. Monaco (Spec. Issue) 13, 37–60 (1994).

  11. 11.

    et al. A biogeochemical study of the coccolithophore, Emiliania huxleyi, in the North Atlantic. Glob. Biogeochem. Cycles 7, 879–900 (1993).

  12. 12.

    Growth, dark respiration and photosynthetic parameters of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae) acclimated to different day length-irradiance combinations. J. Phycol. 33, 818– 822 (1997).

  13. 13.

    Variation in Emiliania huxleyi coccolith morphology in samples from the Norwegian EHUX Experiment, 1992. Sarsia 79, 417–425 (1994).

  14. 14.

    , & Temporal variation in the structure of autotrophic and heterotrophic communities in the subarctic Pacific. Prog. Oceanogr. 32, 57–99 ( 1993).

  15. 15.

    & Impact of a coccolithophorid bloom on dissolved carbon dioxide in sea water enclosures in a Norwegian fjord. Sarsia 79, 379–387 (1994).

  16. 16.

    , & Marine calcification as a source of carbon dioxide: Positive feedback of increasing atmospheric CO2. Limnol. Oceanogr. 39, 458–462 ( 1994).

  17. 17.

    & in Developments in Sedimentology 48: Geochemistry of Sedimentary Carbonates (Elsevier, Amsterdam, 1990).

  18. 18.

    in Coccolithophores. (eds Winter, A. & Siesser, W. G.) 63– 82 (Cambridge Univ. Press, Cambridge, 1994).

  19. 19.

    Calcification, photosynthesis, and global cycles. Bull. Inst. Océanogr. Monaco (Spec. Issue) 13, 137–161 (1994).

  20. 20.

    & Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci. Rev. 42, 95–117 ( 1997).

  21. 21.

    Zooplankton grazing on the coccolithophorid Emiliania huxleyi and its role in inorganic carbon flux. Mar. Biol. 119, 431–439 (1994).

  22. 22.

    & A light-limited continuous culture study of Emiliania huxleyi: determination of coccolith detachment and its relevance to cell sinking. J. Exp. Mar. Biol. Ecol. 207, 127–147 (1996).

  23. 23.

    , & Marine biota effects on the compositional structure of the world oceans. J. Geophys. Res. 96, 4957–4969 (1991).

  24. 24.

    & Studies of marine planktonic diatoms. I. Cyclothella nana (Hustedt) and Detonula confervacea (Cleve). Can. J. Microbiol. 8, 229– 239 (1962).

  25. 25.

    , , , & Coulometric total carbon dioxide analysis for marine studies: maximizing the performance of an automated gas extraction system and coulometric detector. Mar. Chem. 44, 167–187 (1993).

  26. 26.

    , , & Measurements of total carbon dioxide and alkalinity by potentiometric titration in the GEOSECS program. Earth Planet. Sci. Lett. 55 , 99–115 (1981).

  27. 27.

    & New determination of carbonic acid dissociation constants in seawater as a function of temperature and salinity. Deep-Sea Res. 36, 1635– 1654 (1989).

  28. 28.

    & R. Program Developed for CO 2 System Calculations. ORNL/CDIAC-105. (Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, Tennessee, 1998).

Download references


We thank A. Dauelsberg, B. Höhnisch, A. Terbrüggen, and K.-U. Richter for laboratory assistance, F. Hinz for REM analyses, D. Crawford, M. Lipsen, F. Whitney and C. Mayfield for invaluable help at sea and C. S. Wong for providing space on RV J.P. Tully. The E. huxleyi strain PML B92/11A was generously supplied by J. Green, Plymouth Marine Laboratory, and the G. oceanica strain PC 7/1 by the CODENET Algae collection in Caen. This work was supported by the Netherlands-Bremen Cooperation in Oceanography (NEBROC).

Author information


  1. *Alfred Wegener Institute for Polar and Marine Research, P.O. Box 120161, D-27515 Bremerhaven, Germany

    • Ulf Riebesell
    • , Ingrid Zondervan
    • , Björn Rost
    •  & Richard E. Zeebe
  2. †Department of Geosciences & Department of Ecology and Evolutionary Biology, Princeton University, Princeton , New Jersey 08544, USA

    • Philippe D. Tortell
    •  & François M. M. Morel
  3. ‡Lamont-Doherty Earth Observatory, Columbia University, Palisades, New York 10964 , USA

    • Richard E. Zeebe


  1. Search for Ulf Riebesell in:

  2. Search for Ingrid Zondervan in:

  3. Search for Björn Rost in:

  4. Search for Philippe D. Tortell in:

  5. Search for Richard E. Zeebe in:

  6. Search for François M. M. Morel in:

Corresponding author

Correspondence to Ulf Riebesell.

About this article

Publication history







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.