Ecological Research

, Volume 23, Issue 3, pp 479–485 | Cite as

Phytoplankton stoichiometry

  • C. A. Klausmeier
  • E. Litchman
  • T. Daufresne
  • S. A. Levin
Special Feature Stoichiometry in Ecology


Because phytoplankton live at the interface between the abiotic and the biotic compartments of ecosystems, they play an important role in coupling multiple nutrient cycles. The quantitative details of how these multiple nutrient cycles intersect is determined by phytoplankton stoichiometry. Here we review some classic work and recent advances on the determinants of phytoplankton stoichiometry and their role in determining ecosystem stoichiometry. First, we use a model of growth with flexible stoichiometry to reexamine Rhee and Goldman’s classic chemostat data. We also discuss a recent data compilation by Hall and colleagues that illustrates some limits to phytoplankton flexibility, and a model of physiological adaptation that can account for these results. Second, we use a model of resource allocation to determine the how the optimal nitrogen-to-phosphorus stoichiometry depends on the ecological conditions under which species grow and compete. Third, we discuss Redfield’s mechanism for the homeostasis of the oceans’ nitrogen-to-phosphorus stoichiometry and show its robustness to additional factors such as iron-limitation and temporal fluctuations. Finally, we suggest areas for future research.


Phytoplankton Stoichiometry Redfield ratio Theory 



We thank Akiko Satake for the invitation to present this lecture at the Ecological Society of Japan’s 54th Annual Meeting and for the hospitality we received. We thank S. Lan Smith, and Kohei Yoshiyama for useful discussions and Jotaro Urabe for comments on the manuscript. This research was supported by NSF grants DEB-0610531 (E.L.), DEB-0610532 (C.K.), DEB-0083566 (S.A.L.), and grants from the James S. McDonnell Foundation (C.A.K. and E.L) and the Andrew Mellon Foundation (S.A.L.). This is contribution # 1458 from the Kellogg Biological Station.


  1. Aksnes DL, Egge JK (1991) A theoretical model for nutrient uptake in phytoplankton. Mar Ecol Prog Ser 70:65–72CrossRefGoogle Scholar
  2. Armstrong RA, McGehee R (1980) Competitive exclusion. Am Nat 115:151–170CrossRefGoogle Scholar
  3. Armstrong RA (1999) An optimization-based model of iron-light-ammonium colimitation of nitrate uptake and phytoplankton growth. Limnol and Oceanogr 44:1436–1446Google Scholar
  4. Badger MR, Hanson D, Price GD (2002) Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Funct Plant Biol 29:161–173CrossRefGoogle Scholar
  5. Beardall J, Roberts S, Raven JA (2005) Regulation of inorganic carbon acquisition by phosphorus limitation in the green alga Chlorella emersonii. Can J Bot 83:859–864CrossRefGoogle Scholar
  6. Berman-Frank I, Cullen JT, Shaked Y, Sherrell RM, Falkowski PG (2001) Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnol Oceanogr 46:1249–1260CrossRefGoogle Scholar
  7. Calvin M, Benson AA (1948) The path of carbon in photosynthesis. Science 107:476–480PubMedCrossRefGoogle Scholar
  8. Caperon J (1968) Population growth response of Isochrysis galbana to nitrate variation at limiting concentrations. Ecology 49:866–872CrossRefGoogle Scholar
  9. De Leenheer P, Levin SA, Sontag ED, Klausmeier CA (2006) Global stability in a chemostat with multiple nutrients. J Math Biol 52:419–438PubMedCrossRefGoogle Scholar
  10. Diehl S, Berger S, Wöhrl R (2005) Flexible nutrient stoichiometry mediates environmental influeces on phytoplankton and its resources. Ecology 86:2931–2945CrossRefGoogle Scholar
  11. Droop MR (1968) Vitamin B12 and marine ecology. IV. The kinetics of uptake, growth and inhibition in Monochrysis lutheri. J Mar Biol Assoc U K 48:689–733Google Scholar
  12. Ducobu H, Huisman J, Jonker RR, Mur LR (1998) Competition between a prochlorophyte and a cyanobacterium under various phosphorus regimes: comparisons with the Droop model. J Phycol 34:467–476CrossRefGoogle Scholar
  13. Durrett R, Levin SA (2000) Lessons on pattern formation from Planet WATOR. J Theor Biol 205:201–214PubMedCrossRefGoogle Scholar
  14. Falkowski PG (2000) Rationalizing elemental ratios in unicellular algae. J Phycol 36:3–6CrossRefGoogle Scholar
  15. Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, New JerseyGoogle Scholar
  16. Fleming RH (1940) The composition of plankton and units for reporting populations and production. Proceedings of the Sixth Pacific Science Congress 3:535–540Google Scholar
  17. Flynn KJ (2003) Modelling multi-nutrient interactions in phytoplankton: balancing simplicity and realism. Prog Oceanogr 56:249–279CrossRefGoogle Scholar
  18. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240PubMedCrossRefGoogle Scholar
  19. Geider RJ, MacIntyre HL, Kana TM (1996) A dynamic model of photoadaptation in phytoplankton. Limnol Oceanogr 41:1–15CrossRefGoogle Scholar
  20. Geider RJ, MacIntyre HL, Kana TM (1998) A dynamic regulatory model of phytoplanktonic acclimation to light, nutrient, and temperature. Limnol Oceanogr 43:679–694CrossRefGoogle Scholar
  21. Geider RJ, La Roche J (2002) Redfield revisited: variability of C:N:P in marine microalgae and its biochemical basis. Eur J Phycol 37:1–17CrossRefGoogle Scholar
  22. Goldman JC, McCarthy JJ, Peavey DG (1979) Growth rate influence on the chemical composition of phytoplankton in oceanic waters. Nature 279:210–215CrossRefGoogle Scholar
  23. Gotham IJ, Rhee G-Y (1981) Comparative kinetic studies of phosphate-limited growth and phosphate uptake in phytoplankton in continuous culture. J Phycol 17:257–265CrossRefGoogle Scholar
  24. Grover JP (1991) Resource competition in a variable environment: phytoplankton growing according to the variable-internal-stores model. Am Nat 138:811–835CrossRefGoogle Scholar
  25. Hall SR, Smith VH, Lytle DA, Leibold MA (2005) Constraints on primary producer N:P stoichiometry along N:P supply ratio gradients. Ecology 86:1894–1904CrossRefGoogle Scholar
  26. Hessen DO, Andersen T (1992) The algae-grazer interface: feedback mechanism linked to elemental ratios and nutrient cycling. Arch Hydrobiol Ergeb Limnol 35:111–120Google Scholar
  27. Hillebrand H, Sommer U (1999) The nutrient stoichiometry of benthic microalgal growth: Redfield proportions are optimal. Limnol Oceanogr 44:440–446Google Scholar
  28. Hood RR, Coles VJ, Capone DG (2004) Modeling the distribution of Trichodesmium and nitrogen fixation in the Atlantic Ocean. J Geophys Res 109:1–25CrossRefGoogle Scholar
  29. Hutchinson GE (1961) The paradox of the plankton. Am Nat 95:137–145CrossRefGoogle Scholar
  30. Huisman J, Weissing FJ (1999) Biodiversity of plankton by species oscillations and chaos. Nature 402:407–410CrossRefGoogle Scholar
  31. Jäger CG, Diehl S, Matauschek C, Klausmeier CA, Stibor H (2008) Transient dynamics of pelagic producer-grazer systems in a gradient of nutrients and mixing depths. Ecology (in press)Google Scholar
  32. Karl DM, Björkman KM, Dore JE, Fujieki L, Hebel DV, Houlihan T, Letelier RM, Tupas LM (2001) Ecological nitrogen-to-phosphorus stoichiometr at station ALOHA. Deep Sea Res II 48:1529–1566CrossRefGoogle Scholar
  33. Kato S, Urabe J, Kawata M (2007) Effects of temporal and spatial heterogeneities created by consumer-driven nutrient recycling on algal diversity. J Theor Biol 245:364–377PubMedCrossRefGoogle Scholar
  34. Klausmeier CA, Litchman E, Levin SA (2004a) Phytoplankton growth and stoichiometry under multiple nutrient limitation. Limnol Oceanogr 49:1463–1470CrossRefGoogle Scholar
  35. Klausmeier CA, Litchman E, Daufresne T, Levin SA (2004b) Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429:171–174PubMedCrossRefGoogle Scholar
  36. Klausmeier CA, Litchman E, Levin SA (2007) A model of flexible uptake of two essential resources. J Theor Biol 246:278–289PubMedCrossRefGoogle Scholar
  37. Kooijman SALM (2000) Dynamic energy and mass budgets in biological systems. Cambridge University PressGoogle Scholar
  38. Legović T, Cruzado A (1997) A model of phytoplankton growth on multiple nutrients based on the Michaelis–Menten–Monod uptake, Droop’s growth and Liebig’s law. Ecol Model 99:19–31CrossRefGoogle Scholar
  39. Lenton TM, Watson AJ (2000) Redfield revisited: 1. Regulation of nitrate, phosphate, and oxygen in the ocean. Global Biogeochem Cycles 14:225–248CrossRefGoogle Scholar
  40. Lenton TM, Klausmeier CA (2007) Biotic stoichiometric controls on the deep ocean N:P ratio. Biogeosci 4:353–367Google Scholar
  41. Leonardos N, Geider RJ (2004) Responses of elemental and biochemical composition of Chaetoceros muelleri to growth under varying light and nitrate:phosphate supply ratios and their influence on critical N:P. Limnol Oceanogr 49:2105–2114Google Scholar
  42. Leadbeater BSC (2006) The ‘Droop equation’—Michael Droop and the legacy of the ‘cell-quota model’ of phytoplankton growth. Protist 157:345–358PubMedCrossRefGoogle Scholar
  43. Levin SA (1974) Dispersion and population interactions. Am Nat 108:207–228CrossRefGoogle Scholar
  44. Litchman E, Klausmeier CA (2001) Competition of phytoplankton under fluctuating light. Am Nat 157:170–187CrossRefPubMedGoogle Scholar
  45. Litchman E, Klausmeier CA, Bossard P (2004) Phytoplankton nutrient competition under dynamic light regimes. Limnol Oceanogr 49:1457–1462CrossRefGoogle Scholar
  46. Loladze I, Kuang Y, Elser JJ (2000) Stoichiometry in producer-grazer systems: linking energy flow with nutrient cycling. Bull Math Biol 62:1137–1162PubMedCrossRefGoogle Scholar
  47. Metz JAJ, Diekmann O (1986) The dynamics of physiologically structured populations. Springer, BerlinGoogle Scholar
  48. Michaels AF, Karl DM, Capone DG (2001) Elemental stoichiometry, new production, and nitrogen fixation. Oceanography 14:68–77Google Scholar
  49. Mills MM, Ridame C, Davey M, La Roche J, Geider RJ (2004) Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429:292–294PubMedCrossRefGoogle Scholar
  50. Quigg A, Finkel ZV, Iwin AJ, Rosenthal Y, Ho T-Y, Reinfelder JR, Schofield O, Morel FMM, Falkowski PG (2003) The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425:291–294PubMedCrossRefGoogle Scholar
  51. Pascual M, Caswell H (1997) From the cell cycle to population cycles in phytoplankton-nutrient interactions. Ecology 78:897–912Google Scholar
  52. Pascual M, Levin SA (1999) From individuals to population densities: searching for the intermediate scale of nontrivial determinism. Ecology 80:2225–2236Google Scholar
  53. Rastetter EB, Shaver GR (1992) A model of multiple element limitation for acclimating vegetation. Ecology 73:1157–1174CrossRefGoogle Scholar
  54. Raven JA (2003) Inorganic carbon concentrating mechanisms in relation to the biology of algae. Photosyn Res 77:155–171PubMedCrossRefGoogle Scholar
  55. Redfield AC (1934) In: Daniel RJ (ed) James Johnstone memorial volume. On the proportions of organic derivatives in sea water and their relation to the composition of plankton. University Press of Liverpool, pp 176–192Google Scholar
  56. Redfield AC (1958) The biological control of chemical factors in the environment. Am Sci 46:205–221Google Scholar
  57. Rhee G-Y (1978) Effects of N:P atomic ratios and nitrate limitation on algal growth, cell composition, and nitrate uptake. Limnol Oceanogr 23:10–25CrossRefGoogle Scholar
  58. Rhee G-Y, Gotham IJ (1980) Optimum N:P ratios and coexistence of planktonic algae. J Phycol 16:486–489CrossRefGoogle Scholar
  59. Sarmiento JL, Gruber N (2006) Ocean biogeochemical dynamics. Princeton University Press, New JerseyGoogle Scholar
  60. Schade JD, Espeleta JF, Klausmeier CA, McGroddy ME, Thomas SA, Zhang L (2005) A conceptual framework for ecosystem stoichiometry: balancing resource supply and demand. Oikos 109:40–51CrossRefGoogle Scholar
  61. Smith SL, Yamanaka Y (2007) Optimization-based model of multi-nutrient uptake kinetics. Limnol Oceanogr 52:1545–1558Google Scholar
  62. Snyder RE (2007) Spatiotemporal population distributions and their implications for species coexistence in a variable environment. Theor Popul Biol 72:7–20PubMedCrossRefGoogle Scholar
  63. Sterner RW (1990) The ratio of nitrogen to phosphorus resupplied by herbivores: zooplankton and the algal competitive arena. Am Nat 136:209–229CrossRefGoogle Scholar
  64. Sterner RW, Elser JJ, Fee EJ, Guildford SJ, Chrzanowski TH (1997) The light:nutrient ratio in lakes: the balance of energy and materials affects ecosystem structure and process. Am Nat 150:663–684CrossRefPubMedGoogle Scholar
  65. Sterner RW, Elser JJ (2002) Ecological stoichiometry: The biology of elements from molecules to the biosphere. Princeton University PressGoogle Scholar
  66. Stumm W, Morgan JJ (1981) Aquatic chemistry: an introduction emphasizing chemical equilibria in natural waters. Wiley, New YorkGoogle Scholar
  67. Terry KL, Law EA, Burns DJ (1985) Growth rate variation of the N:P requirement ratio of phytoplankton. J Phycol 21:323–329CrossRefGoogle Scholar
  68. Tilman D (1977) Resource competition between planktonic algae: an experimental and theoretical approach. Ecology 58:338–348CrossRefGoogle Scholar
  69. Tillman D (1982) Resource competition and community structure. Princeton University PressGoogle Scholar
  70. Tyrell T (1999) The relative influences of nitrogen and phosphorus on oceanic primary productivity. Nature 400:525–531CrossRefGoogle Scholar
  71. Urabe J, Sterner RW (1996) Regulation of herbivore growth by the balance of light and nutrients. Proc Natl Acad Sci USA 93:8465–8469PubMedCrossRefGoogle Scholar
  72. Zonneveld C (1997) Modeling effects of photoadaptation on the photosynthesis-irradiance curve. J Theor Biol 186:381–388PubMedCrossRefGoogle Scholar
  73. Zonneveld C, van den Berg HA, Kooijman SALM (1997) Modeling carbon cell quota in light-limited phytoplankton. J Theor Biol 188:215–226CrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2008

Authors and Affiliations

  • C. A. Klausmeier
    • 1
  • E. Litchman
    • 1
  • T. Daufresne
    • 2
  • S. A. Levin
    • 3
  1. 1.W. K. Kellogg Biological StationMichigan State UniversityHickory CornersUSA
  2. 2.Comportement et Ecologie de la Faune SauvageInstitut National de la Recherche AgronomiqueCastanet-Tolosan CedexFrance
  3. 3.Department of Ecology and Evolutionary BiologyPrinceton UniversityPrincetonUSA

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