Functional tradeoffs determine species coexistence via the storage effect

How biological diversity is generated and maintained is a fundamental question in ecology. Ecologists have delineated many mechanisms that can, in principle, favor species coexistence and hence maintain biodiversity. Most such coexistence mechanisms require or imply tradeoffs between different aspects of species performance. However, it remains unknown whether simple functional tradeoffs underlie coexistence mechanisms in diverse natural systems. We show that functional tradeoffs explain species differences in long-term population dynamics that are associated with recovery from low density (and hence coexistence) for a community of winter annual plants in the Sonoran Desert. We develop a new general framework for quantifying the magnitude of coexistence via the storage effect and use this framework to assess the strength of the storage effect in the winter annual community. We then combine a 25-year record of vital rates with morphological and physiological measurements to identify functional differences between species in the growth and reproductive phase of the life cycle that promote storage-effect coexistence. Separation of species along a tradeoff between growth capacity and low-resource tolerance corresponds to differences in demographic responses to environmental variation across years. Growing season precipitation is one critical environmental variable underlying the demographic decoupling of species. These results demonstrate how partially decoupled population dynamics that promote local biodiversity are associated with physiological differences in resource uptake and allocation between species. These results for a relatively simple system demonstrate how long-term community dynamics relate to functional biology, a linkage scientists have long sought for more complex systems.

[1]  A. Hastings Disturbance, coexistence, history, and competition for space , 1980 .

[2]  D. Aplin,et al.  Plant Strategies, Vegetation Processes, and Ecosystem Properties , 2002 .

[3]  J. Ehleringer,et al.  Field water relations of Sonoran Desert annuals. , 1984 .

[4]  L. Tevis A Population of Desert Ephemerals Germinated by Less than One Inch of Rain , 1958 .

[5]  Peter Chesson,et al.  Quantifying and testing coexistence mechanisms arising from recruitment fluctuations. , 2003, Theoretical population biology.

[6]  G. Tullock,et al.  Competitive Exclusion. , 1960, Science.

[7]  P. Chesson Multispecies Competition in Variable Environments , 1994 .

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

[9]  Robert P. Gendron,et al.  Models and Mechanisms of Frequency-Dependent Predation , 1987, The American Naturalist.

[10]  R. Levins,et al.  Regional Coexistence of Species and Competition between Rare Species. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[11]  C. E. Pake,et al.  Is Coexistence of Sonoran Desert Annuals Mediated by Temporal Variability Reproductive Success , 1995 .

[12]  Mark W. Chase,et al.  Evolution of the angiosperms: calibrating the family tree , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[13]  I. Noy-Meir,et al.  Desert Ecosystems: Environment and Producers , 1973 .

[14]  Campbell O. Webb,et al.  Bioinformatics Applications Note Phylocom: Software for the Analysis of Phylogenetic Community Structure and Trait Evolution , 2022 .

[15]  C. Cáceres,et al.  Temporal variation, dormancy, and coexistence: a field test of the storage effect. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[16]  P. Chesson,et al.  Environmental Variability Promotes Coexistence in Lottery Competitive Systems , 1981, The American Naturalist.

[17]  J. HilleRisLambers,et al.  Climate variability has a stabilizing effect on the coexistence of prairie grasses , 2006, Proceedings of the National Academy of Sciences.

[18]  T. Huxman,et al.  Linking growth strategies to long‐term population dynamics in a guild of desert annuals , 2007 .

[19]  D. Tilman Plant Strategies and the Dynamics and Structure of Plant Communities. (MPB-26), Volume 26 , 1988 .

[20]  J. P. Grime,et al.  Plant Strategies, Vegetation Processes, and Ecosystem Properties , 2006 .

[21]  Thomas W. Schoener,et al.  Resource Partitioning in Ecological Communities , 1974, Science.

[22]  Howard Griffiths,et al.  Carbon isotopes and water use efficiency: sense and sensitivity , 2008, Oecologia.

[23]  K. Wiegand,et al.  Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments , 2004, Oecologia.

[24]  F. Valladares,et al.  Unity in Diversity : Reflections on Ecology after the Legancy of Ramon Margalef , 2008 .

[25]  Mathew A. Leibold,et al.  Metacommunities: Spatial Dynamics and Ecological Communities , 2005 .

[26]  James R. Runkle,et al.  Synchrony of Regeneration, Gaps, and Latitudinal Differences in Tree Species Diversity , 1989 .

[27]  P. Chesson,et al.  Short-term instabilities and long-term community dynamics. , 1989, Trends in ecology & evolution.

[28]  E. Dietz Permutation Tests for Association Between Two Distance Matrices , 1983 .

[29]  William M. Schaffer,et al.  Plant strategies and the dynamics and structure of plant communities , 1989 .

[30]  J. Ehleringer,et al.  Carbon Isotope Discrimination and Photosynthesis , 1989 .

[31]  B. Enquist,et al.  Rebuilding community ecology from functional traits. , 2006, Trends in ecology & evolution.

[32]  D. L. Venable Bet hedging in a guild of desert annuals. , 2007, Ecology.

[33]  T. Huxman,et al.  Photosynthetic resource-use efficiency and demographic variability in desert winter annual plants. , 2008, Ecology.

[34]  F. Stuart Chapin,et al.  Evolution of Suites of Traits in Response to Environmental Stress , 1993, The American Naturalist.

[35]  Campbell O. Webb,et al.  Phylomatic: tree assembly for applied phylogenetics , 2005 .

[36]  J. Lovett-Doust,et al.  Plant strategies, vegetation processes, and ecosystem properties , 2002 .

[37]  P. Chesson,et al.  DIFFERENCES IN SEED BIOLOGY OF ANNUAL PLANTS IN ARID LANDS: A KEY INGREDIENT OF THE STORAGE EFFECT , 2005 .