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Beyond pairwise mechanisms of species coexistence in complex communities

Nature volume 546, pages 56–64 (2017)Cite this article

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Abstract

The tremendous diversity of species in ecological communities has motivated a century of research into the mechanisms that maintain biodiversity. However, much of this work examines the coexistence of just pairs of competitors. This approach ignores those mechanisms of coexistence that emerge only in diverse competitive networks. Despite the potential for these mechanisms to create conditions under which the loss of one competitor triggers the loss of others, we lack the knowledge needed to judge their importance for coexistence in nature. Progress requires borrowing insight from the study of multitrophic interaction networks, and coupling empirical data to models of competition.

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Figure 1: Coexistence mechanisms that emerge only with more than two competitors.
Figure 2: A competitive network and an extinction cascade.
Figure 3: A data-driven approach to modelling species dynamics.

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References

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

    Google Scholar 

  2. Chesson, P. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol. Syst. 31, 343–366 (2000).

    Google Scholar 

  3. Barabás, G., Michalska-Smith, M. J. & Allesina, S. The effect of intra- and interspecific competition on coexistence in multispecies communities. Am. Nat. 188, E1–E12 (2016). This paper investigates how the specific arrangement of competition coefficients in a network structure affects stability.

    PubMed  Google Scholar 

  4. Hubbell, S. P. Neutral theory in community ecology and the hypothesis of functional equivalence. Funct. Ecol. 19, 166–172 (2005).

    Google Scholar 

  5. Kraft, N. J. B., Valencia, R. & Ackerly, D. D. Functional traits and niche-based tree community assembly in an Amazonian forest. Science 322, 580–582 (2008).

    CAS  PubMed  ADS  Google Scholar 

  6. Allesina, S. & Levine, J. M. A competitive network theory of species diversity. Proc. Natl Acad. Sci. USA 108, 5638–5642 (2011). This paper uses mathematical theory to show how intransitive competitive loops emerge and stabilize coexistence in diverse competitive networks.

    CAS  PubMed  ADS  Google Scholar 

  7. Billick, I. & Case, T. J. Higher order interactions in ecological communities: what are they and how can they be detected? Ecology 75, 1529–1543 (1994).

    Google Scholar 

  8. Friedman, J., Higgins, L. M. & Gore, J. Community structure follows simple assembly rules in microbial microcosms. Nature Ecol. Evol. 0109 (2017).

  9. Thébault, E. & Fontaine, C. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329, 853–856 (2010).

    PubMed  ADS  Google Scholar 

  10. Stouffer, D. B. & Bascompte, J. Compartmentalization increases food-web persistence. Proc. Natl Acad. Sci. USA 108, 3648–3652 (2011).

    CAS  PubMed  ADS  Google Scholar 

  11. Montoya, J. M., Woodward, G., Emmerson, M. C. & Solé, R. V. Press perturbations and indirect effects in real food webs. Ecology 90, 2426–2433 (2009).

    PubMed  Google Scholar 

  12. Solé, R. V. & Montoya, J. A. Complexity and fragility in ecological networks. Proc. R. Soc. B 268, 2039–2045 (2001).

    PubMed  Google Scholar 

  13. Memmott, J., Waser, N. M. & Price, M. V. Tolerance of pollination networks to species extinctions. Proc. R. Soc. B 271, 2605–2611 (2004).

    PubMed  Google Scholar 

  14. Rezende, E. L., Lavabre, J. E., Guimarães, P. R., Jr, Jordano, P. & Bascompte, J. Non-random coextinctions in phylogenetically structured mutualistic networks. Nature 448, 925–928 (2007).

    CAS  PubMed  ADS  Google Scholar 

  15. Case, T. J. Invasion resistance, species build-up and community collapse in metapopulation models with interspecies competition. Biol. J. Linn. Soc. 42, 239–266 (1991).

    Google Scholar 

  16. Stone, L. & Roberts, A. Conditions for a species to gain advantage from the presence of competitors. Ecology 72, 1964–1972 (1991).

    Google Scholar 

  17. Kerr, B., Riley, M. A., Feldman, M. W. & Bohannan, B. J. M. Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors. Nature 418, 171–174 (2002). This paper shows how a rock–paper–scissors competitive loop can stabilize the dynamics of multiple strains of E. coli in the laboratory.

    CAS  PubMed  ADS  Google Scholar 

  18. Wootton, J. T. Indirect effects and habitat use in an intertidal community: interaction chains and interaction modifications. Am. Nat. 141, 71–89 (1993).

    Google Scholar 

  19. Padilla, F. M. et. al. Early root overproduction not triggered by nutrients decisive for competitive success belowground. PLoS ONE 8, e55805 (2013).

    CAS  PubMed  PubMed Central  ADS  Google Scholar 

  20. May, R. M. Will a large complex system be stable? Nature 238, 413–414 (1972).

    CAS  PubMed  ADS  Google Scholar 

  21. Yodzis, P. The indeterminancy of ecological interactions as perceived through perturbation experiments. Ecology 69, 508–515 (1988).

    Google Scholar 

  22. Allesina, S. & Tang, S. Stability criteria for complex ecosystems. Nature 483, 205–208 (2012).

    CAS  PubMed  ADS  Google Scholar 

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

    MathSciNet  MATH  Google Scholar 

  24. Levine, S. H. Competitive interactions in ecosystems. Am. Nat. 110, 903–910 (1976).

    Google Scholar 

  25. Vandermeer, J. Indirect and diffuse interactions: complicated cycles in a population embedded in a large community. J. Theor. Biol. 142, 429–442 (1990).

    MathSciNet  Google Scholar 

  26. Hofbauer, J. & Sigmund, K. Evolutionary game dynamics. Bull. Am. Math. Soc. 40, 479–519 (2003).

    MathSciNet  MATH  Google Scholar 

  27. Laird, R. A. & Schamp, B. S. Competitive intransitivity promotes species coexistence. Am. Nat. 168, 182–193 (2006).

    PubMed  Google Scholar 

  28. Huisman, J. & Weissing, F. J. Biodiversity of plankton by species oscillations and chaos. Nature 402, 407–410 (1999).

    ADS  Google Scholar 

  29. Benincà, E., Ballantine, B., Ellner, S. P. & Huisman, J. Species fluctuations sustained by a cyclic succession at the edge of chaos. Proc. Natl Acad. Sci. USA 112, 6389–6394 (2015).

    PubMed  ADS  Google Scholar 

  30. Edwards, K. & Schreiber, S. Preemption of space can lead to intransitive coexistence of competitors. Oikos 119, 1201–1209 (2010).

    Google Scholar 

  31. MacArthur, R. & Levins, R. The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101, 377–385 (1967).

    Google Scholar 

  32. Pimm, S. L. The structure of food webs. Theor. Popul. Biol. 16, 144–158 (1979).

    CAS  PubMed  Google Scholar 

  33. Krause, A. E., Frank, K. A., Mason, D. M., Ulanowicz, R. E. & Taylor, W. W. Compartments revealed in food-web structure. Nature 426, 282–285 (2003).

    CAS  PubMed  ADS  Google Scholar 

  34. Olesen, J. M., Bascompte, J., Dupont, Y. L. & Jordano, P. The modularity of pollination networks. Proc. Natl Acad. Sci. USA 104, 19891–19896 (2007).

    CAS  PubMed  ADS  Google Scholar 

  35. Allesina, S. & Pascual, M. Food web models: a plea for groups. Ecol. Lett. 12, 652–662 (2009).

    PubMed  Google Scholar 

  36. Guimerà, R. et. al. Origin of compartmentalization in food webs. Ecology 91, 2941–2951 (2010).

    PubMed  Google Scholar 

  37. Grilli, J., Rogers, T. & Allesina, S. Modularity and stability in ecological communities. Nature Commun. 7, 12031 (2016).

    CAS  ADS  Google Scholar 

  38. Bascompte, J., Jordano, P., Melián, C. J. & Olesen, J. M. The nested assembly of plant–animal mutualistic networks. Proc. Natl Acad. Sci. USA 100, 9383–9387 (2003).

    CAS  PubMed  ADS  Google Scholar 

  39. Bastolla, U. et. al. The architecture of mutualistic networks minimizes competition and increases biodiversity. Nature 458, 1018–1020 (2009).

    CAS  PubMed  ADS  Google Scholar 

  40. Sinervo, B. & Lively, C. M. The rock–paper–scissors game and the evolution of alternative male strategies. Nature 380, 240–243 (1996).

    CAS  ADS  Google Scholar 

  41. Lankau, R. A. & Strauss, S. Y. Mutual feedbacks maintain both genetic and species diversity in a plant community. Science 317, 1561–1563 (2007). This paper shows how genetic diversity in a species of mustard helps to stabilize between-species coexistence through an intransitive competitive relationship.

    CAS  PubMed  ADS  Google Scholar 

  42. Lankau, R. A. Genetic variation promotes long-term coexistence of Brassica nigra and its competitors. Am. Nat. 174, E40–E53 (2009).

    PubMed  Google Scholar 

  43. Buss, L. W. & Jackson, J. B. C. Competitive networks: nontransitive competitive relationships in cryptic coral reef environments. Am. Nat. 113, 223–234 (1979).

    Google Scholar 

  44. Buss, L. W. Competitive intransitivity and size-frequency distributions of interaction populations. Proc. Natl Acad. Sci. USA 77, 5355–5359 (1980).

    CAS  PubMed  ADS  Google Scholar 

  45. Paine, R. T. Ecological determinism in the competition for space: the Robert H. MacArthur Award lecture. Ecology 65, 1339–1348 (1984).

    Google Scholar 

  46. Keddy, P. A. & Shipley, B. Competitive hierarchies in herbaceous plant communities. Oikos 54, 234–241 (1989).

    Google Scholar 

  47. Grace, J. B., Guntenspergen, G. R. & Keough, J. The examination of a competition matrix for transitivity and intransitive loops. Oikos 68, 91–98 (1993).

    Google Scholar 

  48. Shipley, B. A null model for competitive hierarchies in competition matrices. Ecology 74, 1693–1699 (1993).

    Google Scholar 

  49. Diez, H., Steinlein, T. & Ullmann, I. The role of growth form and correlated traits in competitive ranking of six perennial ruderal plant species grown in unbalanced mixtures. Acta Oecol. 19, 25–36 (1998).

    ADS  Google Scholar 

  50. Cameron, D. D., White, A. & Antonovics, J. Parasite–grass–forb interactions and rock–paper scissor dynamics: predicting the effects of the parasitic plant Rhinanthus minor on host plant communities. J. Ecol. 97, 1311–1319 (2009).

    Google Scholar 

  51. Zhang, S. & Lamb, E. G. Plant competitive ability and the transitivity of competitive hierarchies change with plant age. Plant Ecol. 231, 15–23 (2012).

    Google Scholar 

  52. Tilman, D. Resource Competition and Community Structure (Princeton Univ. Press, 1982).

    Google Scholar 

  53. Ulrich, W., Soliveres, S., Kryszewski, W., Maestre, F. T. & Gotelli, N. J. Matrix models for quantifying competitive intransitivity from species abundance data. Oikos 123, 1057–1070 (2014).

    PubMed  PubMed Central  Google Scholar 

  54. Soliveres, S. et. al. Intransitive competition is widespread in plant communities and maintains their species richness. Ecol. Lett. 18, 790–798 (2015).

    PubMed  PubMed Central  Google Scholar 

  55. Abrams, P. A. Arguments in favor of higher-order interactions. Am. Nat. 121, 889–891 (1983).

    Google Scholar 

  56. Golubski, A. J., Westlund, E. E., Vandermeer, J. & Pascual, M. Ecological networks over the edge: hypergraph trait-mediated indirect interaction (TMII) structure. Trends Ecol. Evol. 31, 344–354 (2016).

    PubMed  Google Scholar 

  57. Bairey, E., Kelsic, E. D. & Kishony, R. Higher-order species interactions shape ecosystem diversity. Nature Commun. 7, 12285 (2016). This paper uses mathematical models to show that higher-order interactions can cause communities with greater diversity to be more stable than their species-poor counterparts, contrary to classic theory that is based on pairwise interactions.

    CAS  ADS  Google Scholar 

  58. Vandermeer, J. H. A further note on community models. Am. Nat. 117, 379–380 (1981).

    Google Scholar 

  59. Mayfield, M. M. & Stouffer, D. B. Higher-order interactions capture unexplained complexity in diverse communities. Nature Ecol. Evol. 1, 0062 (2017).

    Google Scholar 

  60. Vandermeer, J. H. The competitive structure of communities: an experimental approach with protozoa. Ecology 50, 362–371 (1969).

    Google Scholar 

  61. Neill, W. E. The community matrix and interdependence of the competition coefficients. Am. Nat. 108, 399–408 (1974).

    Google Scholar 

  62. Worthen, W. B. & Moore, J. L. Higher-order interactions and indirect effects: a resolution using laboratory Drosophila communities. Am. Nat. 138, 1092–1104 (1991).

    Google Scholar 

  63. Morin, P. J., Lawler, S. P. & Johnson, E. A. Competition between aquatic insects and vertebrates: interaction strength and higher order interactions. Ecology 69, 1401–1409 (1988).

    Google Scholar 

  64. Pomerantz, M. J. Do 'higher order interactions' in competition systems really exist? Am. Nat. 117, 583–591 (1981).

    MathSciNet  Google Scholar 

  65. Adler, F. R. & Morris, W. F. A general test for interaction modification. Ecology 75, 1552–1559 (1994).

    Google Scholar 

  66. Dormann, C. F. & Roxburgh, S. H. Experimental evidence rejects pairwise modelling approach to coexistence in plant communities. Proc. R. Soc. B 272, 1279–1285 (2005).

    PubMed  Google Scholar 

  67. Weigelt, A. et. al. Identifying mechanisms of competition in multi-species communities. J. Ecol. 95, 53–64 (2007).

    Google Scholar 

  68. Vandermeer, J. H. A further note on community models. Am. Nat. 117, 379–380 (1981).

    Google Scholar 

  69. Huisman, J. & Weissing, F. J. Biological conditions for oscillations and chaos generated by multispecies competition. Ecology 82, 2682–2695 (2001).

    Google Scholar 

  70. Vasseur, D. A., Amarasekare, P., Rudolf, V. H. W. & Levine, J. M. Eco-evolutionary dynamics enable coexistence via neighbor-dependent selection. Am. Nat. 178, E96–E109 (2011).

    PubMed  Google Scholar 

  71. Bastolla, U., Lässig, M., Manrubia, S. C. & Valleriani, A. Biodiversity in model ecosystems, I: coexistence conditions for competing species. J. Theor. Biol. 235, 521–530 (2005).

    MathSciNet  PubMed  Google Scholar 

  72. Jabot, F. & Bascompte, J. Bitrophic interactions shape biodiversity in space. Proc. Natl Acad. Sci. USA 109, 4521–4526 (2012).

    CAS  PubMed  ADS  Google Scholar 

  73. Lasky, J. R., Uriarte, M., Boukili, V. K. & Chazdon, R. L. Trait-mediated assembly processes predict successional changes in community diversity of tropical forests. Proc. Natl Acad. Sci. USA 111, 5616–5621 (2014).

    CAS  PubMed  ADS  Google Scholar 

  74. Kraft, N. J. B., Godoy, O. & Levine, J. M. Plant functional traits and the multidimensional nature of species coexistence. Proc. Natl Acad. Sci. USA 112, 797–802 (2015).

    CAS  PubMed  ADS  Google Scholar 

  75. Chu, C. & Adler, P. B. Large niche differences emerge at the recruitment stage to stabilize grassland coexistence. Ecol. Monogr. 85, 373–392 (2015). This paper describes state-of-the-art approaches for combining observational data with mathematical models to project the importance of particular coexistence mechanisms in nature.

    Google Scholar 

  76. Godoy, O., Stouffer, D. B., Kraft, N. J. & Levine, J. M. Intransitivity is infrequent and fails to promote annual plant coexistence without pairwise niche differences. Ecology http://dx.doi.org/10.1002/ecy.1782 (2017).

  77. Ellner, S. P., Snyder, R. E. & Adler, P. B. How to quantify the temporal storage effect using simulations instead of math. Ecol. Lett. 19, 1333–1342 (2016).

    PubMed  Google Scholar 

  78. Antonopoulos, D. A. et. al. Reproducible community dynamics of the gastrointestinal microbiota following antibiotic perturbation. Infect. Immun. 77, 2367–2375 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Costello, C. et. al. Status and solutions for the world's unassessed fisheries. Science 338, 517–520 (2012).

    CAS  PubMed  ADS  Google Scholar 

  80. Eklof, A. & Ebenman, B. Species loss and secondary extinctions in simple and complex model communities. J. Anim. Ecol. 75, 239–246 (2006).

    PubMed  Google Scholar 

  81. Levine, J. M., Adler, P. B. & Yelenik, S. G. A meta-analysis of biotic resistance to exotic plant invasions. Ecol. Lett. 7, 975–989 (2004).

    Google Scholar 

  82. Silvertown, J., Dodd, M. E., Gowing, D. J. G. & Mountford, J. O. Hydrologically defined niches reveal a basis for species richness in plant communities. Nature 400, 61–63 (1999).

    CAS  ADS  Google Scholar 

  83. Adler, P. B., HilleRisLambers, J. & Levine, J. M. A niche for neutrality. Ecol. Lett. 10, 95–104 (2007).

    PubMed  Google Scholar 

  84. Goh, B. S. Global stability in many-species systems. Am. Nat. 111, 135–143 (1977).

    Google Scholar 

  85. Roberts, A. The stability of a feasible random ecosystem. Nature 251, 608–609 (1974).

    ADS  Google Scholar 

  86. Vandermeer, J. H. Interspecific competition: a new approach to the classical theory. Science 188, 253–255 (1975).

    CAS  PubMed  ADS  Google Scholar 

  87. Stone, L. Some Problems of Community Ecology: Processes, Patterns and Species Persistence in Ecosystems. PhD thesis, Monash Univ. (1988).

    Google Scholar 

  88. Logofet, D. O. Matrices and Graphs: Stability Problems in Mathematical Ecology (CRC, 1992).

    Google Scholar 

  89. Case, T. J. An Illustrated Guide to Theoretical Ecology (Oxford Univ. Press, 2000).

    Google Scholar 

  90. Rohr, R. P., Saavedra, S. & Bascompte, J. On the structural stability of mutualistic systems. Science 345, 1253497 (2014).

    PubMed  Google Scholar 

  91. Justus, J. Ecological and Lyapunov stability. Philos. Sci. 75, 421–436 (2008).

    MathSciNet  Google Scholar 

  92. Thom, R. Structural Stability and Morphogenesis (Addison-Wesley, 1994).

    Google Scholar 

  93. Solé, R. V. & Valls, J. On structural stability and chaos in biological systems. J. Theor. Biol. 155, 87–102 (1992).

    Google Scholar 

  94. Saavedra, S. et. al. A structural approach for understanding multispecies coexistence. Ecol. Monogr. http://dx.doi.org/10.1002/ecm.1263 (2017).

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Acknowledgements

Comments from the Plant Ecology group at ETH Zürich improved the manuscript. We thank R. Freckleton for feedback on the limitations of relative-yield approaches and A. Ferrera for insightful discussions on stability. Conversations with S. Pacala, S. Levin, A. Hastings and A. Ives helped to clarify our thoughts on higher-order interactions. J.M.L. is supported by US National Science Foundation (NSF) grant 1644641, J.B. is funded by the European Research Council through an Advanced Grant, P.B.A. is supported by NSF grant 1353078 and S.A. is supported by NSF grant 1148867.

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Authors and Affiliations

  1. Department of Environmental Systems Science, Institute of Integrative Biology, ETH Zürich, Zürich, 8092, Switzerland

    Jonathan M. Levine

  2. Department of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, 8057, Switzerland

    Jordi Bascompte

  3. Department of Wildland Resources and the Ecology Center, Utah State University, Logan, 84322, Utah, USA

    Peter B. Adler

  4. Department of Ecology and Evolution, University of Chicago, Chicago, 60637, Illinois, USA

    Stefano Allesina

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Author Contributions All authors researched the literature to assemble the review. J.M.L. assembled the first draft of the paper, with all authors contributing individual sections and revisions.

Reviewer Information Nature thanks A. Golubski, E. Thebault and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Levine, J., Bascompte, J., Adler, P. et al. Beyond pairwise mechanisms of species coexistence in complex communities. Nature 546, 56–64 (2017). https://doi.org/10.1038/nature22898

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