No 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.biodiversity ͉ coexistence mechanism ͉ functional trait ͉ population dynamics ͉ specific leaf area H ow competing species stably coexist is a long-standing ecological problem. All niche-based mechanisms for stable coexistence rely on ecological differences that enable each species to recover when perturbed to low density and thus remain in the community. Some of these coexistence mechanisms, such as differential exploitation of multiple limiting resources (1, 2) and frequency-dependent predation (3), operate independently of fluctuations in the environment. Other stable coexistence mechanisms depend critically upon environmental fluctuations that allow species to recover from low density (4). These include competition/ colonization tradeoffs in a disturbance matrix (5, 6), relative nonlinearity of competition (7) and the storage effect (8, 9). The storage effect combines species-specific responses to the environment and population-dynamic buffering by persistent life history stages in a way that results in a positive average low-density growth rate for each species. It is perhaps the dominant fluctuationdependent mechanism for organisms in variable environments. Its role has been explored for diverse groups ranging from freshwater z...

Evolutionary bet hedging encapsulates the counterintuitive idea that organisms evolve traits that reduce short-term reproductive success in favor of longer-term risk reduction. It has been widely investigated theoretically, and many putative examples have been cited including practical ones such as the dormancy involved in microbe and weed persistence. However, long-term data on demographic variation from the actual evolutionarily relevant environments have been unavailable to test for its mechanistic relationship to alleged bet hedging traits. I report an association between delayed germination (a bet hedging trait) and risk using a 22-year data set on demographic variation for 10 species of desert annual plants. Species with greater variation in reproductive success (per capita survival from germination to reproduction x per capita fecundity of survivors) were found to have lower average germination fractions. This provides a definitive test using realistic data on demographic variance that confirms the life history prediction for bet hedging. I also showed that the species with greater long-term demographic variation tended to be the ones with greater sensitivity of reproductive success to variation among years in growing-season precipitation.

A model is developed to consider the interplay between dispersibility and delayed germination in desert annuals. The model explores the effect of low levels of dispersal, considered realistic for annual plants, on optimal germination fraction. The model also demonstrates the effect of the amount and accuracy of "predictive" (responsive to the environment) dormancy on the optimal innate germination fraction (not responsive to environmental conditions).Optimal germination fraction is found to be very sensitive to changes in despersibility especially at the limited dispersibilities that are realistic for annual plants. As dispersibility increases, optimal germination fraction increases. If plants make two kinds of seeds with differing despersibility, reproduction is maximized if the low dispersal seeds have delayed germination and the high dispersal seeds have quick germination. If dormancy mechanisms permit seeds to germinate when environmental conditions allow successful maturation, and remain dormant when environmental conditions do not permit successful maturation, what fraction of seeds should remain dormant under predicted good conditions as a hedge against inaccurate prediction of the environment? If environmental cues that break dormancy are uncorrelated with environmental conditions that permit successful maturation, predictive dormancy has little or no effect on the optimal innate germination fraction. When predictive dormancy lowers the probability of germinating when environmental conditions preclude successful maturation, the optimal innate germination fraction increases with increasing germination control by predictive dormancy. With a moderate degree of germination control by predictive dormancy, the optimal innate dormancy is still sensitive to changes in dispersal in the low dispersal ranges characteristic of annual plants.Evidence is presented from plant species that have both dispersal and germination dimorphisms to support the predicted correlation of high germination fractions with high dispersal.

In bet hedging, organisms sacrifice short-term success to reduce the long-term variance in success. Delayed germination is the classic example of bet hedging, in which a fraction of seeds remain dormant as a hedge against the risk of complete reproductive failure. Here, we investigate the adaptive nature of delayed germination as a bet hedging strategy using long-term demographic data on Sonoran Desert winter annual plants. Using stochastic population models, we estimate fitness as a function of delayed germination and identify evolutionarily stable strategies for 12 abundant species in the community. Results indicate that delayed germination meets the criteria as a bet hedging strategy for all species. Density-dependent models, but not density-independent ones, predicted optimal germination strategies that correspond remarkably well with observed patterns. By incorporating naturally occurring variation in seed and seedling dynamics, our results present a rigorous test of bet hedging theory within the relevant environmental context.

SummarySeed dormancy, by controlling the timing of germination, can strongly affect plant survival. The kind of seed dormancy, therefore, can influence both population and species-level processes such as colonization, adaptation, speciation, and extinction.We used a dataset comprising over 14 000 taxa in 318 families across the seed plants to test hypotheses on the evolution of different kinds of seed dormancy and their association with lineage diversification.We found morphophysiological dormancy to be the most likely ancestral state of seed plants, suggesting that physiologically regulated dormancy in response to environmental cues was present at the origin of seed plants. Additionally, we found that physiological dormancy (PD), once disassociated from morphological dormancy, acted as an 'evolutionary hub' from which other dormancy classes evolved, and that it was associated with higher rates of lineage diversification via higher speciation rates.The environmental sensitivity provided by dormancy in general, and by PD in particular, appears to be a key trait in the diversification of seed plants.

It is widely believed that desert annual plants maintain between—year seed banks, yet few field studies actually have measured the proportion of the viable seed bank that remains dormant through a season. Dormancy and germination fractions were quantified for a guild of winter annuals on a creosote flat in the Sonoran Desert for three years. Predictions from two types of theoretical models applicable to temporally variable environments were examined: (1) the evolution of life history traits promoting persistence in the face of temporal variation and (2) the role of temporal variation in mediating species coexistence. The density of ungerminated seeds was estimated by collecting soil samples after germination, but prior to new seed set. Seedlings were followed in nearby plots to estimate the density of germinated seedlings and their reproductive success. Long—term data collected from permanent plots over a 10—yr period were used to calculate temporal variation in reproductive success for each species. Species with higher temporal variation in reproductive success had lower germination fractions and smaller seeds, consistent with the theory that seed dormancy and large seed size are partially substitutable bet—hedging strategies. The data also suggested that this system possesses traits that are necessary for temporal variation to promote coexistence. First, between—year seed banks, necessary to buffer populations in unfavorable years, were documented for 17 species. Second, there was a strong tendency for year—to—year variation in germination fractions to vary among species. Finally, plants germinated more in years of higher reproductive success. We discuss how a correlation between germination and reproductive success enhances the role of temporal variance in success hierarchies in promoting species coexistence.

Temporal variability in survivorship and reproduction is predicted to affect the evolution of life-history characters. Desert annual plants experience temporal variation in reproductive success that is largely caused by precipitation variability. We studied several populations of the desert annual Plantago insularis along a precipitation gradient. Whereas models of bet hedging in unpredictable environments generally predict one optimal germination fraction for a population, empirical studies have shown that environmental conditions during germination can cause a range of germination fractions to be expressed. In a 4-yr field study, we found that populations in historically more xeric environments had lower mean germination fractions, as is predicted by bet-hedging models. However, populations exhibited significant variation in germination among years. Two experimental studies measuring germination under several environment conditions were conducted to elucidate the source of this in situ variation. Germination fractions exhibited phenotypic plasticity in response to water availability and date within the season. Populations differed in their norms of reaction such that seeds from more xeric populations germinated under less restrictive conditions. A pattern of delayed germination consistent with among-year bet-hedging predictions arose in the field through the interaction of seed germinability and the distribution of environmental conditions during germination.