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.

Enhanced biological carbon consumption in a high CO2 ocean

Nature volume 450, pages 545–548 (2007)Cite this article

Abstract

The oceans have absorbed nearly half of the fossil-fuel carbon dioxide (CO2) emitted into the atmosphere since pre-industrial times1, causing a measurable reduction in seawater pH and carbonate saturation2. If CO2 emissions continue to rise at current rates, upper-ocean pH will decrease to levels lower than have existed for tens of millions of years and, critically, at a rate of change 100 times greater than at any time over this period3. Recent studies have shown effects of ocean acidification on a variety of marine life forms, in particular calcifying organisms4,5,6. Consequences at the community to ecosystem level, in contrast, are largely unknown. Here we show that dissolved inorganic carbon consumption of a natural plankton community maintained in mesocosm enclosures at initial CO2 partial pressures of 350, 700 and 1,050 μatm increases with rising CO2. The community consumed up to 39% more dissolved inorganic carbon at increased CO2 partial pressures compared to present levels, whereas nutrient uptake remained the same. The stoichiometry of carbon to nitrogen drawdown increased from 6.0 at low CO2 to 8.0 at high CO2, thus exceeding the Redfield carbon:nitrogen ratio of 6.6 in today’s ocean7. This excess carbon consumption was associated with higher loss of organic carbon from the upper layer of the stratified mesocosms. If applicable to the natural environment, the observed responses have implications for a variety of marine biological and biogeochemical processes, and underscore the importance of biologically driven feedbacks in the ocean to global change.

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

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

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

Figure 1: Growth conditions in experimental mesocosms.
Figure 2: Development of dominant phytoplankton groups.
Figure 3: CO 2 sensitivity of carbon consumption and carbon loss.

References

  1. Sabine, C. L. et al. The oceanic sink for anthropogenic CO2 . Science 305, 367–371 (2004)

    Article  ADS  CAS  Google Scholar 

  2. Feely, R. A. et al. Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305, 362–366 (2004)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  4. Langdon, C. et al. Effect of elevated CO2 on the community metabolism of an experimental coral reef. Glob. Biogeochem. Cycles 17, 1011 (2003)

    Article  ADS  Google Scholar 

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

    Article  ADS  Google Scholar 

  6. Riebesell, U. & Zondervan, I. Rost, B. Tortell, P. D., Zeebe, R. E. & Morel, F. M. M. Reduced calcification in marine plankton in response to increased atmospheric CO2 . Nature 407, 634–637 (2000)

    Google Scholar 

  7. Redfield, A. C., Ketchum, B. H. & Richards, F. A. in The Sea 2nd edn (ed. Hill, M. N.) 26–77 (Wiley, New York, 1963)

    Google Scholar 

  8. Volk, T. & Hoffert, M. I. in The Carbon Cycle and Atmospheric CO2: Natural Variations Archean to Present (eds Sunquist, E. T. & Broecker, W. S.) Monograph Vol. 32 99–110 (Am. Geophys. Union, Washington DC, 1985)

    Google Scholar 

  9. Gruber, N. & Sarmiento, J. L. in The Sea: Biological–Physical Interactions in the Oceans Vol. 12 (eds Robinson, A. R., McCarthy, J. J. & Rothschild, B. J.) 337–399 (Wiley, New York, 2002)

    Google Scholar 

  10. Houghton, J. T. et al. Climate Change 2001: The Scientific Basis (Cambridge Univ. Press, Cambridge, UK, 2001)

    Google Scholar 

  11. Raven, J. et al. Ocean acidification due to increasing atmospheric carbon dioxide. Policy Document 12/05. Roy. Soc. Rep. 12, (2005)

  12. Antia, N. J., McAllister, C. D., Parsons, T. R., Stephens, K. & Strickland, J. D. H. Further measurements of primary production using a large-volume plastic sphere. Limnol. Oceanogr. 8, 166–183 (1963)

    Article  ADS  Google Scholar 

  13. Sambrotto, R. N. et al. Elevated consumption of carbon relative to nitrogen in the surface ocean. Nature 363, 248–250 (1993)

    Article  ADS  CAS  Google Scholar 

  14. Banse, K. Uptake of inorganic carbon and nitrate by marine plankton and the Redfield ratio. Glob. Biogeochem. Cycles 8, 81–84 (1994)

    Article  ADS  CAS  Google Scholar 

  15. Engel, A., Thoms, S., Riebesell, U., Rochelle-Newall, E. & Zondervan, I. Polysaccharide aggregation as a potenial sink of marine dissolved organic carbon. Nature 428, 929–932 (2004)

    Article  ADS  CAS  Google Scholar 

  16. Engel, A. Direct relationship between CO2 uptake and transparent exoploymer particles production in natural phytoplankton. J. Plankton Res. 24, 49–53 (2002)

    Article  CAS  Google Scholar 

  17. Heemann, C. Phytoplanktonexsudation in Abhängigkeit von der Meerwasserkarbonatchemie. Thesis, Univ. Bremen. (2002)

    Google Scholar 

  18. Hein, M. & Sand-Jensen, K. CO2 increases oceanic primary production. Nature 388, 526–527 (1997)

    Article  ADS  CAS  Google Scholar 

  19. Engel, A. et al. Testing the direct effect of CO2 concentration on a bloom of the coccolithophorid Emiliania huxleyi in mesocosm experiments. Limnol. Oceanogr. 50, 493–504 (2005)

    Article  ADS  CAS  Google Scholar 

  20. Woods, H. A. et al. Temperature and the chemical composition of poikilothermic organisms. Funct. Ecol. 17, 237–245 (2003)

    Article  Google Scholar 

  21. Diehl, S., Berger, S. & Wörhl, R. Flexible algal nutrient stoichiometry mediates environmental influences on phytoplankton and its abiotic resources. Ecology 6, 2931–2945 (2005)

    Article  Google Scholar 

  22. Broecker, W. S. Ocean geochemistry during glacial time. Geochim. Cosmochim. Acta 46, 1689–1705 (1982)

    Article  ADS  CAS  Google Scholar 

  23. Toggweiler, J. R. Carbon overconsumption. Nature 363, 210–211 (1993)

    Article  ADS  Google Scholar 

  24. Körtzinger, A., Koeve, W., Kähler, P. & Mintrop, L. C:N ratios in the mixed layer during the productive season in the Northeast Atlantic Ocean. Deep-sea Res. I 48, 661–688 (2001)

    Article  Google Scholar 

  25. Sterner, R. W. & Elser, J. J. Ecological Stoichiometry (Princeton Univ. Press, Princeton, 2002)

    Google Scholar 

  26. Wanninkhof, R. & Thoning, K. Measurement of fugacity of CO2 in surface water using continuous and discrete sampling methods. Mar. Chem. 44, 189–205 (1993)

    Article  CAS  Google Scholar 

  27. Gran, G. Determination of the equivalence point in potentiometric titrations of seawater with hydrochloric acid. Oceanol. Acta 5, 209–218 (1952)

    Google Scholar 

  28. Johnson, K. M., Williams, P. J., Brandstrom, L. & Sieburth, J. McN. Colometric total carbon analysis for marine studies: automation and calibration. Mar. Chem. 21, 117–133 (1987)

    Article  CAS  Google Scholar 

  29. Barlow, R. G., Cummings, D. G. & Gibb, S. W. Improved resolution of mono- and divinyl chlorophylls a and b and zeaxanthin and lutein in phytoplankton extracts using reverse phase C-8 HPLC. Mar. Ecol. Prog. Ser. 161, 303–307 (1997)

    Article  ADS  CAS  Google Scholar 

  30. Mackey, M. D., Mackey, D. J., Higgins, H. W. & Wright, S. W. CHEMTAX — a program for estimating class abundances from chemical markers: application to HPLC measurements of phytoplankton. Mar. Ecol. Prog. Ser. 144, 265–283 (1996)

    Article  ADS  CAS  Google Scholar 

  31. Hansen, H. P. & Koroleff, F. in Methods of seawater analysis 3rd edn (eds Grasshoff, K., Kremling, K. & Ehrhardt, M.) 159–228 (Wiley VCH, Weinheim, 1999)

    Book  Google Scholar 

  32. Holmes, R. M., Aminot, A., Kérouel, R., Hooker, B. A. & Peterson, B. J. A simple and precise method for measuring ammonium in marine and freshwater ecosystems. Can. J. Fish. Aquat. Sci. 56, 1801–1808 (1999)

    Article  CAS  Google Scholar 

  33. Qian, J. & Mopper, K. Automated high-performance, high-temperature combustion total organic carbon analyser. Anal. Chem. 68, 3090–3097 (1996)

    Article  CAS  Google Scholar 

  34. Delille, B. et al. Response of primary production and calcification to changes of during experimental blooms of the coccolithophorid Emiliania huxleyi . Glob. Biogeochem. Cycles 19, GB2023 (2005)

    Article  ADS  Google Scholar 

  35. Kuss, J. & Schneider, B. Chemical enhancement of the CO2 gas exchange at a smooth seawater surface. Mar. Chem. 91, 165–174 (2004)

    Article  CAS  Google Scholar 

  36. Zeebe, R. E. & Wolf-Gladrow, D. CO2 in seawater: equilibrium, kinetics, isotopes. Elsevier Oceanogr. Ser. 65, (Elsevier, Amsterdam, 2001)

    Google Scholar 

  37. Oschlies, A. Model-derived estimates of new production: new results point towards lower values. Deep-Sea Res. 48, 2173–2197 (2001)

    ADS  CAS  Google Scholar 

  38. Maier-Reimer, E., Mikolajewicz, V. & Winguth, A. Future ocean uptake of CO2: interaction between ocean circulation and biology. Clim. Dynam. 12, 711–721 (1996)

    Article  ADS  Google Scholar 

Download references

Acknowledgements

We thank the participants of the Pelagic Ecosystem CO2 Enrichment study (PeECE III, http://peece.ifm-geomar.de). We acknowledge J. Egge, J. Nejstgaard and the staff of the Espegrend Marine Biological Station for helping to organize and set up the mesocosms. This work was supported by the EU projects CARBOOCEAN ‘Marine carbon sources and sinks assessment’ (GOCE), CABANERA and University of Bergen (LOCUS) funding.

Author information

Authors and Affiliations

  1. Leibniz Institute of Marine Sciences, IFM-GEOMAR, 24105 Kiel, Germany ,

    U. Riebesell, K. G. Schulz, M. Botros, P. Fritsche, M. Meyerhöfer, A. Oschlies, J. Wohlers & E. Zöllner

  2. Bjerknes Centre for Climate Research,,

    R. G. J. Bellerby, C. Neill & G. Nondal

  3. Geophysical Institute, University of Bergen, Allégaten 70, 5007 Bergen, Norway ,

    R. G. J. Bellerby & G. Nondal

Authors
  1. U. Riebesell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. G. Schulz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. G. J. Bellerby
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Botros
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. P. Fritsche
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Meyerhöfer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. C. Neill
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. G. Nondal
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. A. Oschlies
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. J. Wohlers
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. E. Zöllner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to U. Riebesell.

Supplementary information

Supplementary Information

The file contains Supplementary Figures S1-S4 with Legends. (PDF 112 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Riebesell, U., Schulz, K., Bellerby, R. et al. Enhanced biological carbon consumption in a high CO2 ocean. Nature 450, 545–548 (2007). https://doi.org/10.1038/nature06267

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06267

This article is cited by

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.

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