Functional tradeoffs determine species coexistence via the storage effect

Abstract

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.

Fig. 1.

Interspecific tradeoff between growth capacity (relative growth rate, RGR, in g·g⁻¹·day⁻¹) and low-resource tolerance (intrinsic water-use efficiency, assayed by leaf carbon isotope discrimination, Δ, ‰). Species abbreviations are the first two letters of the genus and specific epithet given in Materials and Methods. Asterisks (*) denote 2 naturalized species.

Fig. 2.

Annual per germinant fecundity (survivorship to reproduction, l, times fecundity, b) for each species (left axis, lines) and decomposition of the species-by-year interaction for per germinant fecundity into effects for each species and year after subtracting species and year main effects and sampling error (right axes, black bars). If the species-by-year interaction effects are positive, then lb was greater than expected based on the main effects of species and year alone. (Lower) Interannual variation in growing season precipitation (total precipitation from the first germination-inducing rain until the final reproductive census each year).

Fig. 3.

Species differences in response to yearly variation are correlated with differences in position along the first principal component of variation in 5 key functional traits that underlie a growth capacity/low-resource tolerance tradeoff (leaf mass ratio, maximum electron transport capacity, specific leaf area, relative growth plasticity and leaf nitrogen content) (A) and differences in position along the first principal component constructed using relative growth rate and intrinsic water-use efficiency alone (B). Each point represents the pairwise squared difference between 2 species. Significance was tested with Mantel permutation tests to account for non-independence of data points.