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Research Article

Species fluctuations sustained by a cyclic succession at the edge of chaos

Elisa Benincà, Bill Ballantine, Stephen P. Ellner, and Jef Huisman
PNAS May 19, 2015 112 (20) 6389-6394; first published April 20, 2015; https://doi.org/10.1073/pnas.1421968112
Elisa Benincà
aDepartment of Aquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands;
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Bill Ballantine
bLeigh Marine Laboratory, University of Auckland, Warkworth, Northland 0941, New Zealand; and
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Stephen P. Ellner
cEcology and Evolutionary Biology, Cornell University, Ithaca, NY 14853
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Jef Huisman
aDepartment of Aquatic Microbiology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE Amsterdam, The Netherlands;
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  • For correspondence: j.huisman@uva.nl
  1. Edited by Alan Hastings, University of California, Davis, CA, and accepted by the Editorial Board March 20, 2015 (received for review November 17, 2014)

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  • Nonlinearity and chaos in ecological dynamics
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Significance

The intuitive and popular idea of a balance of nature has been criticized, because species interactions may generate nonequilibrium dynamics, such as oscillations and chaos. However, field evidence of chaos in ecosystems is rare. We report on a coastal community that has displayed striking fluctuations in the abundances of barnacles, mussels, and algae for more than 20 y. Data analysis reveals that these fluctuations reflect a cyclic succession alternating between stabilizing and chaotic dynamics during the species replacement. These results are supported by a simple patch-occupancy model, which predicts very similar dynamics when exposed to seasonal variation. Our findings provide a field demonstration of nonequilibrium coexistence of competing species through a cyclic succession at the edge of chaos.

Abstract

Although mathematical models and laboratory experiments have shown that species interactions can generate chaos, field evidence of chaos in natural ecosystems is rare. We report on a pristine rocky intertidal community located in one of the world’s oldest marine reserves that has displayed a complex cyclic succession for more than 20 y. Bare rock was colonized by barnacles and crustose algae, they were overgrown by mussels, and the subsequent detachment of the mussels returned bare rock again. These processes generated irregular species fluctuations, such that the species coexisted over many generations without ever approaching a stable equilibrium state. Analysis of the species fluctuations revealed a dominant periodicity of about 2 y, a global Lyapunov exponent statistically indistinguishable from zero, and local Lyapunov exponents that alternated systematically between negative and positive values. This pattern indicates that the community moved back and forth between stabilizing and chaotic dynamics during the cyclic succession. The results are supported by a patch-occupancy model predicting similar patterns when the species interactions were exposed to seasonal variation. Our findings show that natural ecosystems can sustain continued changes in species abundances and that seasonal forcing may push these nonequilibrium dynamics to the edge of chaos.

  • chaos
  • coexistence
  • cyclic succession
  • rock–paper–scissors dynamics
  • rocky intertidal community

Footnotes

  • ↵1Present address: Centre for Infectious Disease Control, National Institute for Public Health and the Environment, 3720 AB Bilthoven, The Netherlands, and Department of Epidemiology, Crisis Organization and Diagnostics, Central Veterinary Institute of Wageningen UR, 8200 AB Lelystad, The Netherlands.

  • ↵2To whom correspondence should be addressed. Email: j.huisman{at}uva.nl.
  • Author contributions: B.B. designed research and collected 20-year dataset; and E.B., S.P.E., and J.H. analyzed data, developed the model, and wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. A.H. is a guest editor invited by the Editorial Board.

  • See Commentary on page 6252.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1421968112/-/DCSupplemental.

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Cyclic succession at the edge of chaos
Elisa Benincà, Bill Ballantine, Stephen P. Ellner, Jef Huisman
Proceedings of the National Academy of Sciences May 2015, 112 (20) 6389-6394; DOI: 10.1073/pnas.1421968112

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Cyclic succession at the edge of chaos
Elisa Benincà, Bill Ballantine, Stephen P. Ellner, Jef Huisman
Proceedings of the National Academy of Sciences May 2015, 112 (20) 6389-6394; DOI: 10.1073/pnas.1421968112
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