The Paradox of the Plankton was formulated by Hutchinson (1961 ), stating that many more plankton species co-exist in a supposedly homogeneous habitat than permitted under the competitive exclusion principle of Gause (according to which two species competing for the same resource cannot stably coexist under otherwise constant conditions, see the knol http://knol.google.com/k/klaus-rohde/competitive-exclusion-gauses-principle/xk923bc3gp4/41# ).
A detailed review of our knowledge of the paradox is available in my book Nonequilibrium Ecology (2005 ) (accessible on the website of the book: “free online support material”: Appendix 2).
Some important potential explanations of the paradox are as follows:Nonequilibrium conditions due to seasons and other environmental disturbances.Hutchinson suggested that nonequilibrium conditions might lead to the greater than expected diversity, a suggestion shown to be correct by many subsequent studies. Hutchinson himself thought that seasons and weather-induced fluctuations were responsible. In the early monograph of plankton ecology, Harris (1986 ) showed that environmental disturbances are so frequent that competitive exclusion in phytoplankton species does not occur, leading to nonequilibrium and explaining the paradox of the plankton, although strong environmental pressures such as seasonality may make patterns more predictable.Mixing does not achieve homogeneity. Scheffer et al. (2003 ) showed in their review article that homogeneity due to mixing hardly exists, and even in the open ocean meso-scale (of intermediate size) vortices and fronts result in spatial heterogeneity.Even in homogeneous and constant environments plankton may never reach equilibrium. Moreover, modelling of plankton communities has shown that even in homogeneous and constant environments plankton may never reach equilibrium, because multi-species interactions may lead to oscillations and chaos. This is supported by laboratory experiments, which have shown highly irregular and unpredictable long-term fluctuations at the species level, although total algal biomass and other indicators at higher aggregation levels may show regular patterns. Some detailed studiesA great number of experimental and field studies, especially those by a group working with Jef Huisman in the Netherlands, have provided detailed and convincing evidence for a resolution of the paradox. Here we mention only a few of these studies. Huisman and Weissing (1999 ) have shown that a resource competition model (based on a standard model for phytoplankton competition) can generate oscillations and chaos when species compete for three or more resources, which may allow the coexistence of many species competing for a few resources. Using the same resource competition model, Huisman and Weissing (2001a ) subsequently showed that when several species compete for three resources there may be several alternative outcomes. Huisman et al. (2001 ) simulated competition between many species using different physiological scenarios (such as random species parameters, physiological trade-offs) and concluded that physiological and life-history patterns are important in determining whether species interactions generate nonequilibrium with resulting increase in diversity. A very high biodiversity with sometimes more than 100 species competing for three resources, occurred in simulations with a cyclic relation between competitive abilities and resource contents.Several studies of phytoplankton (references in Huisman and Weissing 2001b ) have shown that there are other limiting resources in addition to the traditionally recognized phosphorus, nitrogen, silica and light, such as various trace metals and, during dense phytoplankton blooms, inorganic carbon. Also, limitation by two resources appears to be more common than limitation by a single one. Different plankton species may “prosper” at different light intensities, but light intensities are far from being the only factor that determines the outcome of competition for light. As shown by Engelmann (1882 ,1893a ,b , cit. Stomp et al. 2007a ,b )) and many others after him, different species of phytoplankton possess different photosynthetic pigments and can utilize different wavelengths of light. Stomp et al. (2004 ) could show theoretically and experimentally that phytoplankton species can differ in spectral characteristics allowing niche differentiation and coexistence of species in the light spectrum. Huisman et al. (2004 ) have shown that turbulence changes are important factors determining plankton composition under natural conditions, mixing depending on climatic factors such as heat exchange and wind action. Therefore, weather–induced changes in turbulence, for instance by periodic storms, may be important contributors to maintaining high biodiversity.
Future studies must consider zooplankton, predatory fish and parasites as well
Except for the brief discussion in Passarge et al. (2006 ), which does not provide experimental evidence, none of the investigations discussed above considers predators such as zooplankton and fish, or parasites such as viruses. Viruses are very abundant in the oceans and infect many hosts including bacteria and eukaryotic primary producers. We do not know how they affect the dynamics of phytoplankton communities.
Many studies, only some discussed here, have provided evidence for an amazing complexity of the supposedly homogeneous aquatic habitats and their plankton communities. Many problems need much further work, including the effects of plankton-predators and viruses. Nevertheless, we can conclude that the paradox of the plankton can be resolved as follows (Scheffer et al. 2003 ): 1) homogeneity due to mixing hardly exists, and even in the open ocean meso-scale vortices and fronts result in spatial heterogeneity; 2) aquatic habitats provide many more niches for niche differentiation than originally thought (different wave lengths of white light; additional essential resources); 3) modelling of plankton communities and experimental studies have shown that even in homogeneous and constant environments plankton may never reach equilibrium, because multi-species competition may lead to oscillations and chaos, contributing to the maintenance of a great biodiversity. Many of the predictions based on modelling have been supported by field studies. In contrast to many communities in which nonequilibrium conditions occur in largely non-saturated niche space with little interspecific competition, nonequilibrium and chaos in plankton may be caused by such competition.
I wish to thank Jef Huisman for sending me many of his papers and for critical comments on the review article on which this brief outline is based.
Hutchinson, G. E., (1961). The paradox of the plankton. American Naturalist 95, 137–145.
Rohde, K. (2005). Nonequilibrium Ecology. Cambridge University Press, Cambridge.
Harris, G.P. (1986). Phytoplankton Ecology. Structure, Function and Fluctuation. London, Chapman and Hill.
Scheffer, M., Rinaldi, S., Huisman, J. and Weissing, F.J. (2003). Why plankton communities have no equilibrium: solutions to the paradox. Hydrobiologia 491, 9-18.
Huisman, J. and Weissing, F.J. (1999). Biodiversity of plankton by species oscillations and chaos. Nature 402, 407-410.
Huisman, J. and Weissing, F.J. (2001a). Fundamental unpredictability in multispecies competition. American Naturalist 157, 488-494.
Huisman, J., Johansson, A.M., Folmer, E.O.and Weissing, F.J. (2001). Towards a solution of the plankton paradox: the importance of physiology and life history. Ecology Letters 4, 408-411.
Huisman, J. and Weissing, F.J. (2001b). Biological conditions for oscillations and chaos generated by multispecies competition. Ecology 82, 2682-2695.
Engelmann, T.W. (1882). Über Sauerstoffausscheidung von Pflanzenzellen im Mikrospectrum. Botanische Zeitschrift 40, 419– 426.
Engelmann, T.W. (1883a). Bacterium photometricum: ein Beitrag zur vergleichenden Physiologie des Licht- und Farbensinnes. Archiv für Physiologie 30, 95–124.
Engelmann, T.W. (1883b). Farbe und Assimilation. Botanische Zeitschrift 41, 1-13.
Stomp, M., Huisman, J., Vörös, L., Pick, F.R., Laamanen, M., Haverkamp, T. and Stal, L.J. (2007a). Colourful coexistence of red and green picocyanobacteria in lakes and seas. Ecology Letters 10, 290-298.
Stomp, M., Huisman, J., Stal, J.L. and Matthij, H.C.P. (2007b). Colourful niches of phototrophic microorganisms shaped by vibrations of the water molecule. The ISME Journal (in press).
Stomp, M., Huisman, J., de Jongh, F., Veraart, A.J., Gerla, D., Rijkeboer, M., Ibelings, B.W., Wollenzien, U.I.A. and Stal, L.J. (2004). Adaptive divergence in pigment composition promotes phytoplankton diversity. Nature 432, 104-107.
Huisman, J., Sharples, J., Stroom, J.M., Visser, P.M., Kardinaal, W.E.A., Verspagen, J.M.H. and Sommeijer, B. (2004). Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85, 2960-2970.
Passarge, J., Hol, S., Escher, M. and Huisman, J. (2006). Competition for nutrients and light: Stable coexistence, alternative stable states, or competitive exclusion? Ecological Monographs 76, 57-72.
For a related knol see “Evolutionär Stabile Strategien und Ungleichgewicht in Ökologischen Systemen”