Beyond pairwise mechanisms of species coexistence in complex communities

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.

[1]  Robert A. Laird,et al.  Competitive Intransitivity Promotes Species Coexistence , 2006, The American Naturalist.

[2]  D. Mason,et al.  Compartments revealed in food-web structure , 2003, Nature.

[3]  P. Chesson Mechanisms of Maintenance of Species Diversity , 2000 .

[4]  R. May,et al.  Nonlinear Aspects of Competition Between Three Species , 1975 .

[5]  J. Vandermeer,et al.  Interspecific competition: a new approach to the classical theory , 1975, Science.

[6]  Ricard V. Solé,et al.  On structural stability and chaos in biological systems , 1992 .

[7]  G. E. Hutchinson,et al.  The Balance of Nature and Human Impact: The paradox of the plankton , 2013 .

[8]  Anna Eklöf,et al.  Species loss and secondary extinctions in simple and complex model communities. , 2006, The Journal of animal ecology.

[9]  Stefano Allesina,et al.  Food web models: a plea for groups. , 2009, Ecology letters.

[10]  W. Worthen,et al.  Higher-Order Interactions and Indirect Effects: A Resolution Using Laboratory Drosophila Communities , 1991, The American Naturalist.

[11]  H. A. BEAGLEY,et al.  Objective evaluation of auditory evoked EEG responses , 1974, Nature.

[12]  Carsten F Dormann,et al.  Experimental evidence rejects pairwise modelling approach to coexistence in plant communities , 2005, Proceedings of the Royal Society B: Biological Sciences.

[13]  T. Steinlein,et al.  The role of growth form and correlated traits in competitive ranking of six perennial ruderal plant species grown in unbalanced mixtures , 1998 .

[14]  S. Pimm,et al.  The structure of food webs. , 1979, Theoretical population biology.

[15]  J. Timothy Wootton,et al.  Indirect Effects and Habitat Use in an Intertidal Community: Interaction Chains and Interaction Modifications , 1993, The American Naturalist.

[16]  Nathan J B Kraft,et al.  Plant functional traits and the multidimensional nature of species coexistence , 2015, Proceedings of the National Academy of Sciences.

[17]  L. Stone,et al.  Conditions for a Species to Gain Advantage from the Presence of Competitors , 1991 .

[18]  Richard A. Lankau,et al.  Mutual Feedbacks Maintain Both Genetic and Species Diversity in a Plant Community , 2007, Science.

[19]  Jordi Bascompte,et al.  The architecture of mutualistic networks minimizes competition and increases biodiversity , 2009, Nature.

[20]  Peter B Adler,et al.  A niche for neutrality. , 2007, Ecology letters.

[21]  Dmitriĭ Olegovich Logofet,et al.  Matrices and Graphs Stability Problems in Mathematical Ecology , 1993 .

[22]  S. Schreiber,et al.  Preemption of space can lead to intransitive coexistence of competitors , 2010 .

[23]  Stephen H. Levine,et al.  Competitive Interactions in Ecosystems , 1976, The American Naturalist.

[24]  R. Hilborn,et al.  Status and Solutions for the World’s Unassessed Fisheries , 2012, Science.

[25]  Hilary G. Morrison,et al.  Reproducible Community Dynamics of the Gastrointestinal Microbiota following Antibiotic Perturbation , 2009, Infection and Immunity.

[26]  J. Silvertown,et al.  Hydrologically defined niches reveal a basis for species richness in plant communities , 1999, Nature.

[27]  Stephen P. Hubbell,et al.  Neutral theory in community ecology and the hypothesis of functional equivalence , 2005 .

[28]  P. Morin,et al.  Competition Between Aquatic Insects and Vertebrates: Interaction Strength and Higher Order Interactions , 1988 .

[29]  J. Hofbauer,et al.  Evolutionary game dynamics , 2011 .

[30]  Stefano Allesina,et al.  Modularity and stability in ecological communities , 2016, Nature Communications.

[31]  Stefano Allesina,et al.  The Effect of Intra- and Interspecific Competition on Coexistence in Multispecies Communities , 2016, The American Naturalist.

[32]  Nathan J B Kraft,et al.  Intransitivity is infrequent and fails to promote annual plant coexistence without pairwise niche differences. , 2017, Ecology.

[33]  Ricard V Solé,et al.  Press perturbations and indirect effects in real food webs. , 2009, Ecology.

[34]  Stephen P Ellner,et al.  How to quantify the temporal storage effect using simulations instead of math. , 2016, Ecology letters.

[35]  ROBERT M. MAY,et al.  Will a Large Complex System be Stable? , 1972, Nature.

[36]  Erik E. Westlund,et al.  Ecological Networks over the Edge: Hypergraph Trait-Mediated Indirect Interaction (TMII) Structure. , 2016, Trends in ecology & evolution.

[37]  Jeff Gore,et al.  Community structure follows simple assembly rules in microbial microcosms , 2016, Nature Ecology &Evolution.

[38]  Stephen P. Ellner,et al.  Species fluctuations sustained by a cyclic succession at the edge of chaos , 2015, Proceedings of the National Academy of Sciences.

[39]  Eyal Bairey,et al.  High-order species interactions shape ecosystem diversity , 2016, Nature Communications.

[40]  R. Macarthur,et al.  The Limiting Similarity, Convergence, and Divergence of Coexisting Species , 1967, The American Naturalist.

[41]  John Vandermeer,et al.  The Competitive Structure of Communities: An Experimental Approach with Protozoa , 1969 .

[42]  Franz J. Weissing,et al.  BIOLOGICAL CONDITIONS FOR OSCILLATIONS AND CHAOS GENERATED BY MULTISPECIES COMPETITION , 2001 .

[43]  Carlos J. Melián,et al.  The nested assembly of plant–animal mutualistic networks , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Ricard V. Solé,et al.  Complexity and fragility in ecological networks , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[45]  Ted J. Case,et al.  Higher Order Interactions in Ecological Communities: What Are They and How Can They be Detected? , 1994 .

[46]  Stefano Allesina,et al.  A competitive network theory of species diversity , 2011, Proceedings of the National Academy of Sciences.

[47]  Peter A. Abrams,et al.  Arguments in Favor of Higher Order Interactions , 1983, The American Naturalist.

[48]  J. Bascompte,et al.  Compartmentalization increases food-web persistence , 2011, Proceedings of the National Academy of Sciences.

[49]  M. Feldman,et al.  Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors , 2002, Nature.

[50]  Michael Lässig,et al.  Biodiversity in model ecosystems, I: coexistence conditions for competing species. , 2005, Journal of theoretical biology.

[51]  J. Vandermeer Indirect and difuse interactions: Complicated cycles in a population embedded in a large community , 1990 .

[52]  Janis Antonovics,et al.  Parasite–grass–forb interactions and rock–paper– scissor dynamics: predicting the effects of the parasitic plant Rhinanthus minor on host plant communities , 2009 .

[53]  J. Huisman,et al.  Biodiversity of plankton by species oscillations and chaos , 1999, Nature.

[54]  D. Tilman Resource competition and community structure. , 1983, Monographs in population biology.

[55]  W. Morris,et al.  A General Test for Interaction Modification , 1994 .

[56]  Nathan J B Kraft,et al.  Functional Traits and Niche-Based Tree Community Assembly in an Amazonian Forest , 2008, Science.

[57]  L. Buss,et al.  Competitive Networks: Nontransitive Competitive Relationships in Cryptic Coral Reef Environments , 1979, The American Naturalist.

[58]  Peter B. Adler,et al.  Large niche differences emerge at the recruitment stage to stabilize grassland coexistence , 2015 .

[59]  James Justus Ecological and Lyapunov Stability* , 2008, Philosophy of Science.

[60]  R. Paine,et al.  Ecological Determinism in the Competition for Space: The Robert H. MacArthur Award Lecture , 1984 .

[61]  P. Keddy,et al.  Competitive hierarchies in herbaceous plant communities , 1989 .

[62]  Si Tang,et al.  Stability criteria for complex ecosystems , 2011, Nature.

[63]  E. Lamb,et al.  Plant competitive ability and the transitivity of competitive hierarchies change with plant age , 2011, Plant Ecology.

[64]  M. Pomerantz Do "Higher Order Interactions" in Competition Systems Really Exist? , 1981, The American Naturalist.

[65]  ALAN ROBERTS,et al.  The stability of a feasible random ecosystem , 1974, Nature.

[66]  J. Grace,et al.  The Examination of a Competition Matrix for Transitivity and Intransitive Loops , 1993 .

[67]  Werner Ulrich,et al.  Intransitive competition is widespread in plant communities and maintains their species richness. , 2015, Ecology letters.

[68]  Richard A. Lankau Genetic Variation Promotes Long‐Term Coexistence of Brassica nigra and Its Competitors , 2009, The American Naturalist.

[69]  B. Sinervo,et al.  The rock–paper–scissors game and the evolution of alternative male strategies , 1996, Nature.

[70]  William E. Neill,et al.  The Community Matrix and Interdependence of the Competition Coefficients , 1974, The American Naturalist.

[71]  N. J. Ouborg,et al.  Early Root Overproduction Not Triggered by Nutrients Decisive for Competitive Success Belowground , 2013, PloS one.

[72]  L W Buss,et al.  Competitive intransitivity and size-frequency distributions of interacting populations. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Alexandra Weigelt,et al.  Identifying mechanisms of competition in multi‐species communities , 2007 .

[74]  B. Goh Global Stability in Many-Species Systems , 1977, The American Naturalist.

[75]  Colin Fontaine,et al.  Stability of Ecological Communities and the Architecture of Mutualistic and Trophic Networks , 2010, Science.

[76]  Daniel B. Stouffer,et al.  Origin of compartmentalization in food webs. , 2010, Ecology.

[77]  P. Yodzis The Indeterminacy of Ecological Interactions as Perceived Through Perturbation Experiments , 1988 .

[78]  L. Stone Some problems of community ecology: processes, patterns and species persistence in ecosystems , 2017 .

[79]  Daniel B. Stouffer,et al.  Higher-order interactions capture unexplained complexity in diverse communities , 2017, Nature Ecology &Evolution.

[80]  N. Gotelli,et al.  Matrix models for quantifying competitive intransitivity. , 2014, Oikos.

[81]  P. Amarasekare,et al.  Eco-Evolutionary Dynamics Enable Coexistence via Neighbor-Dependent Selection , 2011, The American Naturalist.

[82]  Jane Memmott,et al.  Tolerance of pollination networks to species extinctions , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[83]  Rudolf P. Rohr,et al.  On the structural stability of mutualistic systems , 2014, Science.

[84]  Shuichi Matsumura,et al.  Ancient DNA from the First European Farmers in 7500-Year-Old Neolithic Sites , 1975, Science.

[85]  P. Adler,et al.  A meta‐analysis of biotic resistance to exotic plant invasions , 2004 .

[86]  Franck Jabot,et al.  Bitrophic interactions shape biodiversity in space , 2012, Proceedings of the National Academy of Sciences.

[87]  B. Shipley A Null Model for Competitive Hierarchies in Competition Matrices , 1993 .

[88]  M. Uriarte,et al.  Trait-mediated assembly processes predict successional changes in community diversity of tropical forests , 2014, Proceedings of the National Academy of Sciences.

[89]  Jordi Bascompte,et al.  Non-random coextinctions in phylogenetically structured mutualistic networks , 2007, Nature.

[90]  J. Bascompte,et al.  The modularity of pollination networks , 2007, Proceedings of the National Academy of Sciences.

[91]  Ted J. Case,et al.  Invasion resistance, species build‐up and community collapse in metapopulation models with interspecies competition , 1991 .

[92]  René Thom,et al.  Structural stability and morphogenesis , 1977, Pattern Recognit..

[93]  Serguei Saavedra,et al.  A structural approach for understanding multispecies coexistence , 2017 .