Abstract
The coexistence of a large number of phytoplankton species on a seemingly limited variety of resources is a classical problem in ecology, known as ‘the paradox of the plankton’. Strong fluctuations in species abundance due to the external factors or competitive interactions leading to oscillations, chaos and short-term equilibria have been cited so far to explain multi-species coexistence and biodiversity of phytoplankton. However, none of the explanations has been universally accepted. The qualitative view and statistical analysis of our field data establish two distinct roles of toxin-producing phytoplankton (TPP): toxin allelopathy weakens the interspecific competition among phytoplankton groups and the inhibition due to ingestion of toxic substances reduces the abundance of the grazer zooplankton. Structuring the overall plankton population as a combination of nontoxic phytoplankton (NTP), toxic phytoplankton, and zooplankton, here we offer a novel solution to the plankton paradox governed by the activity of TPP. We demonstrate our findings through qualitative analysis of our sample data followed by analysis of a mathematical model.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Armstrong, R.A., McGehee, R., 1980. Competitive exclusion. Am. Nat. 115, 151–170.
Bracco, A., Provenzale, A., Scheuring, I., 2000. Mesoscale vortices and the paradox of the plankton. Proc. R. Soc. Lond. B 267, 1795–1800.
Britton, N.F., 1989. Aggregation and the competitive exclusion principle. J. Theor. Biol. 136, 57–66.
Byrne, G.D., Hindmarsh, A.C., March 1975. A polyalgorithm for the numerical solution of ODEs, ACM TOMS 1(1), 71–96.
Buskley, E.J., Stockwell, A.J., 1997. Effect of persistent “brown tide” on zooplankton population in the Laguna Madre of southern Texas. In: Smayda, T.J., Shimuzu, Y. (Eds.), Toxic Phytoplankton Bloom in the Sea. Elsevier, Amsterdam, The Netherlands, pp. 659–666.
Chattopadhyay, J., Sarkar, R.R., Elabdllaoui, A., 2002b. A delay differential equation model on harmful algal blooms in the presence of toxic substances. IMA J. Math. Appl. Med. Biol. 19, 137–161.
Chattopadhyay, J., Sarkar, R.R., Mandal, S., 2002a. Toxin-producing plankton may act as a biological control for planktonic blooms—Field study and mathematical modelling. J. Theor. Biol. 215, 333–344.
Chattopadhyay, J., Sarkar, R.R., Pal, S., 2004. Harmful algal blooms—Mathematical and stochastic modelling supported by experimental findings. Ecol. Complex. 1, 225–235.
Descamps-Julien, B., Gonzalez, A., 2005. Stable coexistence in a fluctuating environment: An experimental demonstration. Ecology 86(1), 2815–2824.
Erdman, D., Morelock, M.M., 1996. A Study of Kinetics: The Estimation and Simulation of Systems of First-Order Differential Equations, Proceedings of the tewenty-first annual SAS® users group international conference, pp. 1407–1414 (http://support.sas.com/rnd/app/papers/kinetics.pdf.)
Hallegraeff, G.M., 1993. A review of harmful algae blooms and the apparent global increase. Phycologia 32, 79–99.
Heerkloss, R., Klinkenberg, G., 1998. A long-term series of a planktonic foodweb: A case of chaotic dynamics. Verh. Int. Ver. Limnol. 26, 1952–1956.
Hassel, M.P., Comins, H.N., May, R.M., 1994. Species coexistence and self-organizing spatial dynamics. Hydrobiologia 344, 87–102.
Huisman, J., Johansson, A.M., Folmer, E.O., Weissing, F.J., 2001. Towards a solution of the plankton paradox: The importance of physiology and life history. Ecol. Lett. 4, 408–411.
Huisman, J., Van Oostveen, P., Weissing, F.J., 1999. Species dynamics in phytoplankton blooms: Incomplete mixing and competition for light. Am. Nat. 154, 46–68.
Huisman, J., Weissing, F.J., 1999. Biodiversity of plankton by species oscillation and chaos. Nature 402, 407–410.
Hulot, Florence D., Huisman, J., 2004. Allelopathic interactions between phytoplankton species: The role of heterotrophic bacteria and mixing intensity. Limnol. Oceanogr. 49, 1424–1434.
Hutchinson, G.E., 1961. The paradox of the plankton. Am. Nat. 95, 137–145.
Ives, J.D., 1961. Possible mechanism underlying copepod grazing responses to levels of toxicity in red tide dinoflagellates. J. Exp. Mar. Biol. Ecol. 112, 131–145.
Ives, A.R., May, R.M., 1985. Competition within and between species in a patchy environment: Relations between microscopic and macroscopic model. J. Theor. Biol. 115, 65–92.
Kirk, K., Gilbert, J., 1992. Variation in herbivore response to chemical defence: Zooplankton foraging on toxic cynobacteria. Ecology 73, 2208.
Kozlowsky-Suzuki, B., et al., 2003. Feeding, reproduction and toxin accumulation by the copepods Acartia bifilosa and Eurytenora affinis in the presence of the toxic cynobacterium Nodularia spumigena. Mar. Ecol. Prog. 249, 237–249.
Levins, R., 1979. Coexistence in a variable environment. Am. Nat. 114, 765–783.
Ludwig, D., et al., 1978. Qualitative analysis of an insect outbreak system: The sruce budworm and forest. J. Anim. Ecol. 47, 315.
Nielsen, T.G., Kiorboe, T., Bjornsen, P.K., 1990. Effect of Chrysochromulina polylepis sub surface bloom on the plankton community. Mar. Ecol. Prog. Ser. 62, 21–35.
Odum, E.P., 1971. Fundamentals of Ecology. Sunders, Philadelphia, PA.
Powell, T., Richerson, P.J., 1985. Temporal variation, spatial heterogeneity, and competition for resources in plankton system: A theoretical model. Am. Nat. 125, 431–464.
Richarson, P.J., Armstrong, R., Goldman, C.R., 1970. Contemporaneous disequilibrium: A new hypothesis to explain the paradox of plankton. Proc. Natl. Acad. Sci. U.S.A. 67, 1710–1714.
Rothhaupt, K.O., 1988. Mechanistic resource competition theory applied to laboratory experiments with zooplankton. Nature 333, 660–662.
Rothhaupt, K.O., 1996. Laboratory experiments with a mixotrophic and phototrophic competitors. Ecology 77, 716–724.
Roy, S., Bhattacharya, S., Das, P., Chattopadhyay, J., 2005. Interaction among nontoxic phytoplankton, toxic phytoplankton and zooplankton: Inferences from field observations (manuscript in preparation).
Roy, S., Chattopadhyay, J., 2006. Toxin-alleopathy among phytoplankton species prevents competition exclusion. J. Biol. Sys., submitted for publication.
Sarkar, R.R., Chattopadhyay, J., 2003a. Occurence of planktonic blooms under environmental fluctuations and its possible control mechanism-mathematical models and experimental observations. J. Theor. Biol. 224, 501–516.
Sarkar, R.R., Chattopadhyay, J., 2003b. The role of environmental stochasticity in a toxic phytoplankton – Non-toxic phytoplankton–zooplankton system. Environmentrics 14, 775–792.
Scheffer, M., Rinaldi, S., Gragnani, L.R. Mur, van Nes, E.H., 1997. On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology 78, 272–282.
Scheffer, M., Rinaldi, S., Huisman, J., Weissing, F.J., 2003. Why phytoplankton communities have no equilibrium: Solutions to the paradox. Hydrobiologia 491, 9–18.
Solé, J., García-Ladona, E., Ruardij, P., Estrada, M., 2005. Modelling allelopathy among marine algae. Eco. Mod. 183, 373–384.
Sommer, U., 1985. Comparison between steady state and non-steady state competition: Experiments with natural phytoplankton. Limnol. Oceanogr. 30, 335–346.
Sommer, U., 1986. Nitrate-and silicate-competition among Antarctic phytoplankton. Mar. Biol. 91, 345–351.
Steidinger, K.A., et al., 1996. Pfiesteria Piscicida, a new toxic dinoflagelate genus and species of the order Dinamoebales. J. Phycol. 32, 157–164.
Tilman, D., 1977. Resource competition between planktonic algae: An experimental and theoritical approach. Ecology 58, 338–348.
Tilman, D., 1981. Test of resource competition theory using four species of Lake Michigan algae. Ecology 62, 802–815.
Tomas, C.R., 1997. Identifying Marine Diatoms and Dinoflagellates. AP, San Diego, CA, p. 858.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Roy, S., Alam, S. & Chattopadhyay, J. Competing Effects of Toxin-Producing Phytoplankton on Overall Plankton Populations in the Bay of Bengal. Bull. Math. Biol. 68, 2303–2320 (2006). https://doi.org/10.1007/s11538-006-9109-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11538-006-9109-5