D. Lawrence Venable

Delayed germination and dispersal in desert annuals: escape in space and time.

SummaryA 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.

SEED BANKS IN DESERT ANNUALS: IMPLICATIONS FOR PERSISTENCE AND COEXISTENCE IN VARIABLE ENVIRONMENTS'

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 envi- ronments 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

BET HEDGING IN A GUILD OF DESERT ANNUALS

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.

Size-number trade-offs and the variation of seed size with plant resource status

I develop a general treatment of the effects of parental resource status on optimal offspring size. The model shows that even when there is a resource trade-off between size and number of offspring within individuals, positive correlations between size and number may occur among individuals due to individual variation in resources. Such positive correlations imply that parental resource status affects the fitness-maximizing offspring size, in contrast to the predictions of the standard Smith-Fretwell model. I show that parental resource status affects the fitness-maximizing offspring size whenever the size-number fitness function is nonhomogeneous in offspring number. This condition implies some sort of density-dependent interactions among offspring, although it is possible to have either positive or negative sib interactions in fitness functions that are homogeneous in offspring number. In the latter case offspring size should be insensitive to parental resource status. I explore several cases including linear (Smith-Fretwell), nonlinear but homogeneous, and nonhomogeneous seed-number functions with independent size and number effects, as well as models with interacting offspring size-number effects. I briefly review the plant literature on offspring density dependence and seed-size variation with parental resource status. Some suggestions for testing the ideas with plants and some alternative explanations of positive seed-size/plant-size and seed-size/seed-number correlations are discussed.

Diversity and temporal change in the effective pollinators of Asclepias tuberosa

Although pollination effectiveness is a central process underlying the evo- lution of plant and pollinator traits, it is difficult to measure and has rarely been reported for a diverse spectrum of visitors under natural conditions. We measured the effectiveness of all common flower visitors to Asclepias tuberosa (butterfly weed) at a site in southeastern Arizona, in terms of visitation rate, per-visit rate of pollinia removal and insertion, and pollinia load. Bombus and Apis (Hymenoptera) were the most effective pollinators, counter to predictions that A. tuberosa is butterfly-pollinated. We also documented large differences between 2 yr in the pollination effectiveness of visitors, primarily due to changes in vis- itation rate. Bombus were the most frequent and effective pollinators in 1992. In 1993, Apis were equivalent to Bombus. Battus (Lepidoptera) were the second most effective pollinators in 1992, but were scarce in 1993. Thus, conclusions about the identity of effective pollinators based on floral traits, casual observations of visitation, or even precise measurement of effectiveness in a single season are all potentially suspect. We compare our results to those of previous studies of Asclepias pollination.

EVOLUTIONARY ECOLOGY OF SEED-BANK ANNUALS IN TEMPORALLY VARYING ENVIRONMENTS

The production of long-lived seeds by annual plants introduces a unique form of age structure. In a temporally varying environment the dormant seed may experience many years with different weather, whereas the germinating individual experiences only the weather conditions of a single growing season. Natural selection operates on both the between-year dormancy and on non-seed-bank traits that affect the degree of specialization to conditions pertaining in different year types. We have used an integrated model that permits these two aspects of the life history to evolve simultaneously. This leads to predictions that are not attainable by considering the evolution of each in isolation. Changes in the survival probability of the between-year seed bank select for reinforcing changes in between-year dormancy and specialization. Changes in the probability of occurrence of different year types select for damping changes in between-year dormancy and specialization. Across a gradient in environmental quality, we predict that most change will occur in between-year dormancy, with little change in specialization. If between-year dormancy is fixed, however, a greater change in specialization should occur. The predictions of the model are discussed in terms of environmental gradients, seed-bank versus non-seed-bank annuals, and a variety of plant traits modeled elsewhere that may be involved in specialization to different types of years.

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.

Is Coexistence of Sonoran Desert Annuals Mediated by Temporal Variability Reproductive Success

Models of annual plants with a persistent seed bank have shown that temporal variation can promote coexistence if the reproductive success of species is favored in different environments determined by temporally variable conditions. This study investigates whether this mechanism may explain the coexistence of three Sonoran Desert species (Pectocarya recurvata, Plantago patagonica, Schismus barbatus). In a 2—yr experiment, factors that vary across years (water and seedling density) were manipulated. In addition, the dominant spatial feature, presence or absence of Larrea cover, was also included as a factor. Our aim was to document fitness hierarchies in different types of years. Seedlings were mapped monthly for survival and reproductive success. To compare species, we used 10 yr of data to calculate the average value that seeds of different species have for population growth. Shifts in fitness hierarchies were found for two species pairs (Pectocarya—Schismus and Pectocarya—Plantago), depending on density and either the year or the water level. Surprisingly, all species had higher survival at higher densities in one or another treatment. Habitats were not important to the fitness hierarchies; all species had higher mean survival and fitness in the open than under shrubs.

Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment

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.

DORMANCY AND GERMINATION IN A GUILD OF SONORAN DESERT ANNUALS

To investigate bet hedging and species coexistence in a guild of Sonoran Desert winter annuals, we subjected seeds of eight species to factorial combinations of summer treatments (varying temperature and precipitation), germination conditions (representative of early, middle, and late germination season temperatures and day lengths), and experiment trial dates (spanning the germination season). In keeping with bet hedging theory, we found that many viable seeds would not germinate in response to any combination of treatments (germination usually <50%). In keeping with the storage effect model, we found that these coexisting species differed in their germination response to our experimental manipulations and also differed in how the experimental variables interact. Field germination data from a long-term project on population and community dynamics of this guild show that germination fractions are similar between field and growth chamber and that species that tend to germinate under early season conditions in the growth chamber also tend to do so under unmanipulated field conditions. Some species are nondormant during the summer and only acquire dormancy at the onset of the autumn germination season, while others appear to have either innate or conditional dormancy until the onset of the germination season.