Skip to main content

Thank you for visiting 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:

Magnitude of oceanic nitrogen fixation influenced by the nutrient uptake ratio of phytoplankton


The elemental stoichiometry of sea water and particulate organic matter is remarkably similar. This observation led Redfield to hypothesize that the oceanic ratio of nitrate to phosphate is controlled by the remineralization of phytoplankton biomass1. The Redfield ratio is used universally to quantitatively link the marine nitrogen and phosphorus cycles in numerous biogeochemical applications2,3,4. Yet, empirical and theoretical studies show that the ratio of nitrogen to phosphorus in phytoplankton varies greatly with taxa5,6 and growth conditions7,8,9. Here we present a dynamic five-box ecosystem model showing that non-Redfield utilization of dissolved nitrogen and phosphorus by non-nitrogen-fixing phytoplankton controls the magnitude and distribution of nitrogen fixation. In our simulations, systems dominated by rapidly growing phytoplankton with low nitrogen to phosphorus uptake ratios reduce the phosphorus available for nitrogen fixation. In contrast, in systems dominated by slow-growing phytoplankton with high nitrogen to phosphorus uptake ratios nitrogen deficits are enhanced, and nitrogen fixation is promoted. We show that estimates of nitrogen fixation are up to fourfold too high when non-Redfield uptake stoichiometries are ignored. We suggest that the relative abundance of fast- and slow-growing phytoplankton controls the amount of new nitrogen added to the ocean.

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: The ETSP five-box ecosystem model.
Figure 2: Effects of phytoplankton nitrate/phosphate (NO3/PO4) utilization ratios on PO4 and xsPO4 in the ETSP.
Figure 3: Seasonal variation in excess PO4 (xsPO4,mmol m−3) and chlorophyll (chl, mg m−3) in the northern North Atlantic Ocean.

Similar content being viewed by others


  1. Redfield, A. C. in James Johnstone Memorial Volume (ed. Daniel, R. J.) 177–192 (Univ. Press Liverpool, 1934).

    Google Scholar 

  2. Anderson, L. A. & Sarmiento, J. L. Redfield ratios of remineralization determined by nutrient data-Analysis. Glob. Biogeochem. Cycles 8, 65–80 (1994).

    Article  Google Scholar 

  3. Gruber, N. & Sarmiento, J. L. Global patterns of marine nitrogen fixation and denitrification. Glob. Biogeochem. Cycles 11, 235–266 (1997).

    Article  Google Scholar 

  4. Moore, J. K., Doney, S. C., Kleypas, J. A., Glover, D. M. & Fung, I. Y. An intermediate complexity marine ecosystem model for the global domain. Deep-Sea Res. II 49, 403–462 (2002).

    Article  Google Scholar 

  5. Quigg, A. et al. The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425, 291–294 (2003).

    Article  Google Scholar 

  6. Arrigo, K. R. et al. Phytoplankton community structure and the drawdown of nutrients and CO2 in the Southern Ocean. Science 283, 365–367 (1999).

    Article  Google Scholar 

  7. Geider, R. J. & La Roche, J. Redfield revisited: Variability of C:N:P in marine microalgae and its biochemical basis. Eur. J. Phycol. 37, 1–17 (2002).

    Article  Google Scholar 

  8. Bertilsson, S., Berglund, O., Karl, D. M. & Chisholm, S. W. Elemental composition of marine Prochlorococcus and Synechococcus : Implications for the ecological stoichiometry of the sea. Limnol. Oceanogr. 48, 1721–1731 (2003).

    Article  Google Scholar 

  9. Klausmeier, C. A., Litchman, E., Daufresne, T. & Levin, S. A. Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429, 171–174 (2004).

    Article  Google Scholar 

  10. Deutsch, C., Sarmiento, J. L., Sigman, D. M., Gruber, N. & Dunne, J. P. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167 (2007).

    Article  Google Scholar 

  11. Anderson, T. R. & Pondaven, P. Non-Redfield carbon and nitrogen cycling in the Sargasso Sea: Pelagic imbalances and export flux. Deep-Sea Res. I 50, 573–591 (2003).

    Article  Google Scholar 

  12. Christian, J. R. Biogeochemical cycling in the oligotrophic ocean: Redfield and non-Redfield models. Limnol. Oceanogr. 50, 646–657 (2005).

    Article  Google Scholar 

  13. Chavez, F. P., Buck, K. R., Service, S. K., Newton, J. & Barber, R. T. Phytoplankton variability in the central and eastern tropical Pacific. Deep-Sea Res. II 43, 835–870 (1996).

    Article  Google Scholar 

  14. Bruland, K. W., Rue, E. L., Smith, G. J. & DiTullio, G. R. Iron, macronutrients and diatom blooms in the Peru upwelling regime: Brown and blue waters of Peru. Mar. Chem. 93, 81–103 (2005).

    Article  Google Scholar 

  15. Dandonneau, Y. et al. Seasonal and interannual variability of ocean colour and composition of phytoplankton communities in the North Atlantic, equatorial Pacific and South Pacific. Deep-Sea Res. II 51, 303–318 (2004).

    Article  Google Scholar 

  16. Garcia, H. E., Locarnini, R. A., Boyer, T. P. & Anotov, J. I. in NOAA Atlas NESDIS 64 (ed. Levitus, S.) (US Government Printing Office, 2006).

    Google Scholar 

  17. Voss, M., Bombar, D., Loick, N. & Dippner, J. W. Riverine influence on nitrogen fixation in the upwelling region off Vietnam, South China Sea. Geophys. Res. Lett. 33, L07604 (2006).

    Article  Google Scholar 

  18. Capone, D. G. et al. An extensive bloom of the N2-fixing cyanobacterium Trichodesmium erythraeum in the central Arabian Sea. Mar. Ecol. Prog. Ser. 172, 281–292 (1998).

    Article  Google Scholar 

  19. Canfield, D. E. Models of oxic respiration, denitrification and sulfate reduction in zones of coastal upwelling. Geochim. Cosmochim. Acta 70, 5753–5765 (2006).

    Article  Google Scholar 

  20. Moore, J. K. & Doney, S. C. Iron availability limits the ocean nitrogen inventory stabilizing feedbacks between marine denitrification and nitrogen fixation. Glob. Biogeochem. Cycles 21 (2007).

  21. Tagliabue, A., Bopp, L. & Aumont, O. Ocean biogeochemistry exhibits contrasting responses to a large scale reduction in dust deposition. Biogeosciences 5, 11–24 (2008).

    Article  Google Scholar 

  22. Glibert, P. M. & Bronk, D. A. Release of dissolved organic nitrogen by marine diazotrophic cyanobacteria, Trichodesmium spp. Appl. Environ. Microbiol. 60, 3996–4000 (1994).

    Google Scholar 

  23. Yamamoto-Kawai, M., Carmack, E. & McLaughlin, F. Nitrogen balance and Arctic throughflow. Nature 443, 43–43 (2006).

    Article  Google Scholar 

  24. Lochte, K., Ducklow, H. W., Fasham, M. J. R. & Stienen, C. Plankton succession and carbon cycling at 47° N 20° W during the JGOFS North-Atlantic bloom experiment. Deep-Sea Res. II 40, 91–114 (1993).

    Article  Google Scholar 

  25. Staal, M. et al. Nitrogen fixation along a north–south transect in the eastern Atlantic Ocean. Limnol. Oceanogr. 52, 1305–1316 (2007).

    Article  Google Scholar 

  26. Richardson, T. L. & Jackson, G. A. Small phytoplankton and carbon export from the surface ocean. Science 315, 838–840 (2007).

    Article  Google Scholar 

  27. Schmittner, A. Decline of the marine ecosystem caused by a reduction in the Atlantic overturning circulation. Nature 434, 628–633 (2005).

    Article  Google Scholar 

  28. Irwin, A. J. & Oliver, M. J. Are ocean deserts getting larger? Geophys. Res. Lett. 36, L18609 (2009).

    Article  Google Scholar 

  29. Codispoti, L. A. et al. The oceanic fixed nitrogen and nitrous oxide budgets: Moving targets as we enter the anthropocene? Sci. Marina 65, 85–105 (2001).

    Article  Google Scholar 

  30. Paulmier, A., Kriest, I. & Oschlies, A. Stoichiometries of remineralisation and denitrification in global biogeochemical ocean models. Biogeosciences 6, 2539–2566 (2009).

    Article  Google Scholar 

Download references


We thank G. van Dijken and B. Saenz for help coding the model and L. Thomas for help parameterizing upwelling fluxes. We are also indebted to the members of the Arrigo laboratory and to C. M. Moore for fruitful discussions on nutrient utilization ratios of different phytoplankton and for comments on the manuscript. This work was supported by NSF grant ANT 0732535 and DOE grant DE-FG02-04ER63896 to K.R.A.

Author information

Authors and Affiliations



All authors contributed equally to this work.

Corresponding author

Correspondence to Matthew M. Mills.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary Information (PDF 1687 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mills, M., Arrigo, K. Magnitude of oceanic nitrogen fixation influenced by the nutrient uptake ratio of phytoplankton. Nature Geosci 3, 412–416 (2010).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:

This article is cited by


Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

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