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.

  • Letter
  • Published:

Biodiversity of plankton by species oscillations and chaos

Abstract

Biodiversity has both fascinated and puzzled biologists1. In aquatic ecosystems, the biodiversity puzzle is particularly troublesome, and known as the ‘paradox of the plankton’2. Competition theory predicts that, at equilibrium, the number of coexisting species cannot exceed the number of limiting resources3,4,5,6. For phytoplankton, only a few resources are potentially limiting: nitrogen, phosphorus, silicon, iron, light, inorganic carbon, and sometimes a few trace metals or vitamins. However, in natural waters dozens of phytoplankton species coexist2. Here we offer a solution to the plankton paradox. First, we show that resource competition models6,7,8,9,10 can generate oscillations and chaos when species compete for three or more resources. Second, we show that these oscillations and chaotic fluctuations in species abundances allow the coexistence of many species on a handful of resources. This model of planktonic biodiversity may be broadly applicable to the biodiversity of many ecosystems.

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

Access options

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

Figure 1: Oscillations on three resources.
Figure 2: Chaos on five resources.
Figure 3: Bifurcation diagram, for five species competing for five resources.
Figure 4: Competitive chaos and the coexistence of 12 species on five resources.

Similar content being viewed by others

References

  1. Wilson,E. O. The Diversity of Life (Belknap, Cambridge, Massachusetts, 1992).

    Google Scholar 

  2. Hutchinson,G. E. The paradox of the plankton. Am. Nat. 95, 137–145 (1961).

    Article  Google Scholar 

  3. Hardin,G. The competitive exclusion principle. Science 131, 1292–1298 (1960).

    Article  ADS  CAS  Google Scholar 

  4. Phillips,O. M. The equilibrium and stability of simple marine biological systems. I. Primary nutrient consumers. Am. Nat. 107, 73– 93 (1973).

    Article  Google Scholar 

  5. Armstrong,R. A. & McGehee,R. Competitive exclusion. Am. Nat. 115, 151–170 (1980).

    Article  MathSciNet  Google Scholar 

  6. Grover,J. P. Resource Competition (Chapman and Hall, London, 1997 ).

    Book  Google Scholar 

  7. Leon,J. A. & Tumpson,D. B. Competition between two species for two complementary or substitutable resources. J. Theor. Biol. 50, 185–201 ( 1975).

    Article  CAS  Google Scholar 

  8. Tilman,D. Resource competition between planktonic algae: an experimental and theoretical approach. Ecology 58, 338– 348 (1977).

    Article  CAS  Google Scholar 

  9. Hsu,S. B., Cheng,K. S. & Hubbell, S. P. Exploitative competition of micro-organisms for two complementary nutrients in continuous cultures. SIAM J. Appl. Math. 41, 422–444 ( 1981).

    Article  MathSciNet  Google Scholar 

  10. Huisman,J. & Weissing,F. J. Light-limited growth and competition for light in well-mixed aquatic environments: an elementary model. Ecology 75, 507–520 ( 1994).

    Article  Google Scholar 

  11. Holm,N. P. & Armstrong,D. E. Role of nutrient limitation and competition in controlling the populations of Asterionella formosa and Microcystis aeruginosa in semicontinuous culture. Limnol. Oceanogr. 26, 622–634 (1981).

    Article  ADS  CAS  Google Scholar 

  12. Sommer,U. Comparison between steady state and non-steady state competition: experiments with natural phytoplankton. Limnol. Oceanogr. 30, 335–346 (1985).

    Article  ADS  CAS  Google Scholar 

  13. Sommer,U. Nitrate- and silicate-competition among Antarctic phytoplankton. Mar. Biol. 91, 345–351 ( 1986).

    Article  CAS  Google Scholar 

  14. Van Donk,E. & Kilham,S. S. Temperature effects on silicon- and phosphorus-limited growth and competitive interactions among three diatoms. J. Phycol. 26, 40–50 (1990).

    Article  CAS  Google Scholar 

  15. Rothhaupt,K. O. Laboratory experiments with a mixotrophic chrysophyte and obligately phagotrophic and phototrophic competitors. Ecology 77, 716–724 (1996).

    Article  Google Scholar 

  16. Huisman,J., Jonker,R. R., Zonneveld,C. & Weissing,F. J. Competition for light between phytoplankton species: experimental tests of mechanistic theory. Ecology 80, 211– 222 (1999).

    Article  Google Scholar 

  17. Monod,J. La technique de culture continue, théorie et applications. Ann. Inst. Pasteur (Paris) 79, 390– 410 (1950).

    CAS  Google Scholar 

  18. Von Liebig,J. Die organische Chemie in ihrer Anwendung auf Agrikultur und Physiologie (Friedrich Vieweg, Braunschweig, 1840).

    Google Scholar 

  19. Richerson,P. J., Armstrong,R. & Goldman, C. R. Contemporaneous disequilibrium: a new hypothesis to explain the paradox of the plankton. Proc. Natl Acad. Sci. USA 67, 1710–1714 ( 1970).

    Article  ADS  CAS  Google Scholar 

  20. Levins,R. Coexistence in a variable environment. Am. Nat. 114 , 765–783 (1979).

    Article  MathSciNet  Google Scholar 

  21. Padisák,J., Reynolds,C. S. & Sommer, U. (eds) The intermediate disturbance hypothesis in phytoplankton ecology. Hydrobiologia 249, 1– 199 (1993).

    Article  Google Scholar 

  22. Sommer,U. Phytoplankton competition in Plußsee: a field test of the resource-ratio hypothesis. Limnol. Oceanogr. 38, 838– 845 (1993).

    Article  ADS  CAS  Google Scholar 

  23. Sterner,R. W. Seasonal and spatial patterns in macro- and micronutrient limitation in Joe Pool Lake, Texas. Limnol. Oceanogr. 39, 535–550 (1994).

    Article  ADS  CAS  Google Scholar 

  24. Escaravage,V., Prins,T. C., Smaal,A. C. & Peeters,J. C. H. The response of phytoplankton communities to phosphorus input reduction in mesocosm experiments. J. Exp. Mar. Biol. Ecol. 198, 55– 79 (1996).

    Article  Google Scholar 

  25. May,R. M. Stability and Complexity in Model Ecosystems (Princeton Univ. Press, Princeton, 1974).

    Google Scholar 

  26. Tilman,D. Biodiversity: population versus ecosystem stability. Ecology 77, 350–363 (1996).

    Article  Google Scholar 

  27. Naeem,S. & Li,S. Biodiversity enhances ecosystem reliability. Nature 390, 507–509 (1997).

    Article  ADS  CAS  Google Scholar 

  28. Gilpin,M. E. Limit cycles in competition communities. Am. Nat. 109 , 51–60 (1975).

    Article  Google Scholar 

  29. May,R. M. & Leonard,W. J. Nonlinear aspects of competition between three species. SIAM J. Appl. Math. 29, 243–253 (1975).

    Article  MathSciNet  Google Scholar 

  30. Smale,S. On the differential equations of species in competition. J. Math. Biol. 3, 5–7 ( 1976).

    Article  MathSciNet  CAS  Google Scholar 

Download references

Acknowledgements

J.H. thanks J. Roughgarden at Stanford University and L. J. Stal at the Center for Estuarine and Marine Ecology for their hospitality and for providing facilities to do this research. We thank U. Sommer for comments. J.H. was supported by the Netherlands Organization for Scientific Research (NWO), and the Earth and Life Sciences Foundation (ALW), which is subsidized by NWO.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jef Huisman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huisman, J., Weissing, F. Biodiversity of plankton by species oscillations and chaos. Nature 402, 407–410 (1999). https://doi.org/10.1038/46540

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/46540

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

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