Offspring polymorphism and bet hedging: a large-scale, phylogenetic analysis.

Offspring polymorphism is a reproductive strategy where individual organisms simultaneously produce offspring that differ in morphology and ecology. It occurs across the Tree of Life but is particularly common among plants, where it is termed seed (diaspore) heteromorphism. The prevalence of this strategy in unpredictably varying environments has resulted in the assumption that it serves as a bet-hedging mechanism. We found 101 examples of this strategy in southwestern North America. We provide phylogenetically informed evidence for the hypothesis that the occurrence of seed heteromorphism increases with increasing environmental variability, though this pattern was only significant for aridity, one of our two rainfall variability metrics. We provide a strong test of bet hedging for a large, taxonomically diverse set of seed heteromorphic species, lending support to the hypothesis that bet hedging is an important mechanistic driver for the evolution of seed heteromorphism.

Functional trait trade-off and species abundance: insights from a multi-decadal study.

Phylogenetically informed trait comparisons across entire communities show promise in advancing community ecology. We use this approach to better understand the composition of a community of winter annual plants with multiple decades of monitoring and detailed morphological, phenological and physiological measurements. Previous research on this system revealed a physiological trade-off among dominant species that accurately predicts population and community dynamics. Here we expanded our investigation to 51 species, representing 96% of individual plants recorded over 30 years, and analysed trait relationships in the context of species abundance and phylogenetic relationships. We found that the functional-trait trade-off scales to the entire community, albeit with diminished strength. It is strongest for dominant species and weakens as progressively rarer species are included. The trade-off has been consistently expressed over three decades of environmental change despite some turnover in the identity of dominant species.

Frequency-dependent seed predation by rodents on Sonoran Desert winter annual plants.

Numerous mechanisms may allow species to coexist. We tested for frequency-dependent predation, a mechanism predicted by theory and established as a foraging behavior for many types of animals. Our field test included multiple prey species exposed in situ to multiple predator species and individuals to determine whether the prey species experienced predation patterns that were frequency dependent. The prey were seeds of three species of Sonoran Desert winter annual plants while the predator species were a guild of nocturnal seed foraging heteromyid and murid rodents that co-occur naturally in the same community as the desert annuals at Tumamoc Hill near Tucson. Seeds of one species were much preferred over the other two. Nonetheless, we found the net effect of rodent foraging to be positively frequency dependent (the preference for each species is higher when it is common than when it is uncommon) as has been previously hypothesized. This frequency-dependent predation should function as a species coexistence promoting mechanism in concert with the storage effect that has been previously demonstrated for this system.

Within-and among-year germination in Sonoran Desert winter annuals: bet hedging and predictive germination in a variable environment.

In variable environments, organisms must have strategies to ensure fitness as conditions change. For plants, germination can time emergence with favourable conditions for later growth and reproduction (predictive germination), spread the risk of unfavourable conditions (bet hedging) or both (integrated strategies). Here we explored the adaptive value of within- and among-year germination timing for 12 species of Sonoran Desert winter annual plants. We parameterised models with long-term demographic data to predict optimal germination fractions and compared them to observed germination. At both temporal scales we found that bet hedging is beneficial and that predicted optimal strategies corresponded well with observed germination. We also found substantial fitness benefits to varying germination timing, suggesting some degree of predictive germination in nature. However, predictive germination was imperfect, calling for some degree of bet hedging. Together, our results suggest that desert winter annuals have integrated strategies combining both predictive plasticity and bet hedging.

The contribution of germination functional traits to population dynamics of a desert plant community.

Early life-cycle events play critical roles in determining the population and community dynamics of plants. The ecology of seeds and their germination patterns can determine range limits, adaptation to environmental variation, species diversity, and community responses to climate change. Understanding the adaptive consequences and environmental filtering of such functional traits will allow us to explain and predict ecological dynamics. Here we quantify key functional aspects of germination physiology and relate them to an existing functional ecology framework to explain long-term population dynamics for 13 species of desert annuals near Tucson, Arizona, USA. Our goal was to assess the extent to which germination functional biology contributes to long-term population processes in nature. Some of the species differences in base, optimum, and maximum temperatures for germination, thermal times to germination, and base water potentials for germination were strongly related to 20-yr mean germination fractions, 25-yr average germination dates, seed size, and long-term demographic variation. Comparisons of germination fraction, survival, and fecundity vs. yearly changes in population size found significant roles for all three factors, although in varying proportions for different species. Relationships between species' germination physiologies and relative germination fractions varied across years, with fast-germinating species being favored in years with warm temperatures during rainfall events in the germination season. Species with low germination fractions and high demographic variance have low integrated water-use efficiency, higher vegetative growth rates, and smaller, slower-germinating seeds. We have identified and quantified a number of functional traits associated with germination biology that play critical roles in ecological population dynamics.

Maternal adjustment of offspring provisioning and the consequences for dispersal.

Phenotypic plasticity in seed provisioning is a widespread phenomenon in plant populations that is often manifested as environmentally induced maternal effects. Environmental maternal effects can be beneficial if they influence population dynamic functions of seeds in a way that increases fitness, such as escaping from crowding. Using the winter annual plant, Dithyrea californica, we studied the response of seed provisioning to the maternal competitive environment and the associated seed dispersal consequences. We measured the average size of seeds produced by plants experiencing different competitive environments in order to test the hypothesis that mother plants respond to crowding by providing fewer resources to each offspring. We also hypothesized that smaller seeds produced by crowded mothers would benefit from greater dispersal away from their high-density natal habitat. We marked seeds with fluorescent paint while still attached to the mother plant, recorded seed diameter, and followed them for nine months after dispersal, recording the distance they moved from the mother plant. Plants that experienced more competition produced smaller seeds that dispersed farther from their mother plant. Larger seed diameter was previously shown to be'associated with greater competitive ability in D. californica. Thus the production of smaller seeds in more competitive environments implies a possible trade-off between competitive ability and dispersal arising from an environmentally driven aspect of phenotype. Fitness consequences of this trade-off in the context of the year-to-year variation in rainfall and density are uncertain.

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.

The evolution of seed dormancy: environmental cues, evolutionary hubs, and diversification of the seed plants.

Seed 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.

One hundred and six years of change in a Sonoran Desert plant community: Impact of climate anomalies and trends in species sensitivities.

A major restriction in predicting plant community response to future climate change is a lack of long-term data needed to properly assess species and community response to climate and identify a baseline to detect climate anomalies. Here, we use a 106-year dataset on a Sonoran Desert plant community to test the role of extreme temperature and precipitation anomalies on community dynamics at the decadal scale and over time. Additionally, we tested the climate sensitivity of 39 desert plant species and whether sensitivity was associated with growth form, longevity, geographic range, or local dominance. We found that desert plant communities had shifted directionally over the 106 years, but the climate had little influence on this directional change primarily due to nonlinear shifts in precipitation anomalies. Decadal-scale climate had the largest impact on species richness, species relative density, and total plant cover, explaining up to 26%, 45%, and 55% of the variance in each, respectively. Drought and the interaction between the frequency of freeze events and above-average summer precipitation were among the most influential climate factors. Increased drought frequency and wetter periods with frequent freeze events led to larger reductions in total plant cover, species richness, and the relative densities of dominant subshrubs Ambrosia deltoidea and Encelia farinosa. More than 80% of the tested species were sensitive to climate, but sensitivity was not associated with a species' local dominance, longevity, geographic range, or growth form. Some species appear to exhibit demographic buffering, where when they have a higher sensitivity to drought, they also tend to have a higher sensitivity to favorable (i.e., wetter and hotter) conditions. Overall, our results suggest that, while decadal-scale climate variation substantially impacts these desert plant communities, directional change in temperature over the last century has had little impact due to the relative importance of precipitation and drought. With projections of increased drought in this region, we may see reductions in total vegetation cover and species richness due to the loss of species, possibly through a breakdown in their ability to demographically buffer climatic variation, potentially changing community dynamics through a change in facilitative and competitive processes.

Water-use efficiency and relative growth rate mediate competitive interactions in Sonoran Desert winter annual plants.

PREMISE OF THE STUDY: A functional approach to investigating competitive interactions can provide a mechanistic understanding of processes driving population dynamics, community assembly, and the maintenance of biodiversity. In Sonoran Desert annual plants, a trade-off between relative growth rate (RGR) and water-use efficiency (WUE) contributes to species differences in population dynamics that promote long-term coexistence. Traits underlying this trade-off explain variation in demographic responses to precipitation as well as life history and phenological patterns. Here, we ask how these traits mediate competitive interactions. • METHODS: We conducted competition trials for three species occupying different positions along the RGR-WUE trade-off axis and compared the effects of competition at high and low soil moisture. We compared competitive effect (ability to suppress neighbors) and competitive response (ability to withstand competition from neighbors) among species. • KEY RESULTS: The RGR-WUE trade-off predicted shifts in competitive responses at different soil moistures. The high-RGR species was more resistant to competition in high water conditions, while the opposite was true for the high-WUE species. The intermediate RGR species tended to have the strongest impact on all neighbors, so competitive effects did not scale directly with differences in RGR and WUE among competitors. • CONCLUSIONS: Our results reveal mechanisms underlying long-term variation in fitness: high-RGR species perform better in years with large, frequent rain events and can better withstand competition under wetter conditions. The opposite is true for high-WUE species. Such resource-dependent responses strongly influence community dynamics and can promote coexistence in variable environments.

Understanding past, contemporary, and future dynamics of plants, populations, and communities using Sonoran Desert winter annuals.

Global change requires plant ecologists to predict future states of biological diversity to aid the management of natural communities, thus introducing a number of significant challenges. One major challenge is considering how the many interacting features of biological systems, including ecophysiological processes, plant life histories, and species interactions, relate to performance in the face of a changing environment. We have employed a functional trait approach to understand the individual, population, and community dynamics of a model system of Sonoran Desert winter annual plants. We have used a comprehensive approach that connects physiological ecology and comparative biology to population and community dynamics, while emphasizing both ecological and evolutionary processes. This approach has led to a fairly robust understanding of past and contemporary dynamics in response to changes in climate. In this community, there is striking variation in physiological and demographic responses to both precipitation and temperature that is described by a trade-off between water-use efficiency (WUE) and relative growth rate (RGR). This community-wide trade-off predicts both the demographic and life history variation that contribute to species coexistence. Our framework has provided a mechanistic explanation to the recent warming, drying, and climate variability that has driven a surprising shift in these communities: cold-adapted species with more buffered population dynamics have increased in relative abundance. These types of comprehensive approaches that acknowledge the hierarchical nature of biology may be especially useful in aiding prediction. The emerging, novel and nonstationary climate constrains our use of simplistic statistical representations of past plant behavior in predicting the future, without understanding the mechanistic basis of change.

Variation in photosynthetic response to temperature in a guild of winter annual plants.

How species respond to environmental variation can have important consequences for population and community dynamics. Temperature, in particular, is one source of variation expected to strongly influence plant performance. Here, we compared photosynthetic responses to temperature across a guild of winter annual plants. Previous work in this system identified a trade-off between relative growth rate (RGR) and water-use efficiency (WUE) that predicts species differences in population dynamics over time, which then contribute to long-term species coexistence. Interestingly, species with high WUE invest in photosynthetic processes that appear to maximize carbon assimilation, while high-RGR species appear to maximize carbon gain by increasing leaf area for photosynthesis. In high-WUE species, higher rates of carbon acquisition were associated with increased investment into light-driven electron transport (J(max)). We tested whether such allocation allows these plants to have greater photosynthetic performance at lower temperatures by comparing the temperature sensitivity of photosynthesis across species in the community. Six species were grown in buried pots in the field, allowing them to experience natural changes in seasonal temperature. Plants were taken from the field and placed in growth chambers where photosynthetic performance was measured following short-term exposure to a wide range of temperatures. These measurements were repeated throughout the season. Our results suggest that high-WUE species are more efficient at processing incoming light, as measured by chlorophyll fluorescence, and exhibit higher net photosynthetic rates (A(net)) than high-RGR species, and these advantages are greatest at low temperatures. Sampling date differentially affected fluorescence across species, while species had similar seasonal changes in A(net). Our results suggest that species-specific responses to temperature contribute to the WUE-RGR trade-off that has been shown to promote coexistence in this community. These differential responses to environmental conditions can have important effects on fitness, population dynamics, and community structure.

Fitness and physiology in a variable environment.

The relationship between physiological traits and fitness often depends on environmental conditions. In variable environments, different species may be favored through time, which can influence both the nature of trait evolution and the ecological dynamics underlying community composition. To determine how fluctuating environmental conditions favor species with different physiological traits over time, we combined long-term data on survival and fecundity of species in a desert annual plant community with data on weather and physiological traits. For each year, we regressed the standardized annual fitness of each species on its position along a tradeoff between relative growth rate and water-use efficiency. Next, we determined how variations in the slopes and intercepts of these fitness-physiology functions related to year-to-year variations in temperature and precipitation. Years with a relatively high percentage of small rain events and a greater number of days between precipitation pulse events tended to be worse, on average, for all desert annual species. Species with high relative growth rates and low water-use efficiency had greater standardized annual fitness than other species in years with greater numbers of large rain events. Conversely, species with high water-use efficiency had greater standardized annual fitness in years with small rain events and warm temperatures late in the growing season. These results reveal how weather variables interact with physiological traits of co-occurring species to determine interannual variations in survival and fecundity, which has important implications for understanding population and community dynamics.

Macroevolutionary chemical escalation in an ancient plant-herbivore arms race.

A central paradigm in the field of plant-herbivore interactions is that the diversity and complexity of secondary compounds in plants have intensified over evolutionary time, resulting in the great variety of secondary products that currently exists. Unfortunately, testing of this proposal has been very limited. We analyzed the volatile chemistry of 70 species of the tropical plant genus Bursera and used a molecular phylogeny to test whether the species' chemical diversity or complexity have escalated. The results confirm that as new species diverged over time they tended to be armed not only with more compounds/species, but also with compounds that could potentially be more difficult for herbivores to adapt to because they belong to an increasing variety of chemical pathways. Overall chemical diversity in the genus also increased, but not as fast as species diversity, possibly because of allopatric species gaining improved defense with compounds that are new locally, but already in existence elsewhere.

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.

Differences in the timing of germination and reproduction relate to growth physiology and population dynamics of Sonoran Desert winter annuals.

PREMISE OF THE STUDY: Trait differences can promote distinct survival and fecundity responses to environmental fluctuations. In a Sonoran Desert winter annual plant community, we have identified a tradeoff between relative growth rate (RGR) and water-use efficiency (WUE) that predicts interannual variation in reproductive success. Here we test the hypothesis that traits underlying RGR and WUE differences are linked to seasonal phenology. METHODS: We use long-term demographic data and finer-scale, short-term data to investigate timing of germination, reproduction, and death of several winter annual species in multiple years in open and under-shrub habitats. We hypothesized that species with high WUE and less interannual demographic variability would have life cycle transitions early in the winter to spring growing season. This would be due to an ability to use small amounts of rain and photosynthesize at low temperatures. By contrast, we hypothesized that species with low WUE whose survival and reproductive rates vary greatly from year to year would have life cycle transitions later in the season. KEY RESULTS: In any given year, species with high WUE germinated and reproduced earlier in the season than species with low WUE, whereas low-WUE species germinated later and had shorter reproductive phases. CONCLUSIONS: Our results demonstrate a direct relationship between phenology and physiological trait differences. This link between phenology and physiology is of interest because it clarifies the mechanism by which trait differences determine species' relative abundances.

Hydrothermal sensitivities of seed populations underlie fluctuations of dormancy states in an annual plant community.

Plant germination ecology involves continuous interactions between changing environmental conditions and the sensitivity of seed populations to respond to those conditions at a given time. Ecologically meaningful parameters characterizing germination capacity (or dormancy) are needed to advance our understanding of the evolution of germination strategies within plant communities. The germination traits commonly examined (e.g., maximum germination percentage under optimal conditions) may not adequately reflect the critical ecological differences in germination behavior across species, communities, and seasons. In particular, most seeds exhibit primary dormancy at dispersal that is alleviated by exposure to dry after-ripening or to hydrated chilling to enable germination in a subsequent favorable season. Population-based threshold (PBT) models of seed germination enable quantification of patterns of germination timing using parameters based on mechanistic assumptions about the underlying germination physiology. We applied the hydrothermal time (HTT) model, a type of PBT model that integrates environmental temperature and water availability, to study germination physiology in a guild of coexisting desert annual species whose seeds were after-ripened by dry storage under different conditions. We show that HTT assumptions are valid for describing germination physiology in these species, including loss of dormancy during after-ripening. Key HTT parameters, the hydrothermal time constant (θHT ) and base water potential distribution among seeds (Ψb (g)), were effective in describing changes in dormancy states and in clustering species exhibiting similar germination syndromes. θHT is an inherent species-specific trait relating to timing of germination that correlates well with long-term field germination fraction, while Ψb (g) shifts with depth of dormancy in response to after-ripening and seasonal environmental variation. Predictions based on variation among coexisting species in θHT and Ψb (g) in laboratory germination tests matched well with 25-yr observations of germination dates and fractions for the same species in natural field conditions. Seed dormancy and germination strategies, which are significant contributors to long-term species demographics under natural conditions, can be represented by readily measurable functional traits underlying variation in germination phenologies.

Seed dispersal of desert annuals.

We quantified seed dispersal in a guild of Sonoran Desert winter desert annuals at a protected natural field site in Tucson, Arizona, USA. Seed production was suppressed under shrub canopies, in the open areas between shrubs, or both by applying an herbicide prior to seed set in large, randomly assigned removal plots (10-30 m diameter). Seedlings were censused along transects crossing the reproductive suppression borders shortly after germination. Dispersal kernels were estimated for Pectocarya recurvata and Schismus barbatus from the change in seedling densities with distance from these borders via inverse modeling. Estimated dispersal distances were short, with most seeds traveling less than a meter. The adhesive seeds of P. recurvata went farther than the small S. barbatus seeds, which have no obvious dispersal adaptation. Seeds dispersed farther downslope than upslope and farther when dispersing into open areas than when dispersing into shrubs. Dispersal distances were short relative to the pattern of spatial heterogeneity created by the shrub and open space mosaic. This suggests that dispersal could contribute to local population buildup, possibly facilitating species coexistence. Overall, these results support the hypothesis that escape in time via delayed germination is likely to be more important for desert annuals than escape in space.

Photosynthetic resource-use efficiency and demographic variability in desert winter annual plants.

We studied a guild of desert winter annual plants that differ in long-term variation in per capita reproductive success (lb, the product of per capita survival from germination to reproduction, l, times per capita reproduction of survivors, b) to relate individual function to population and community dynamics. We hypothesized that variation in lb should be related to species' positions along a trade-off between relative growth rate (RGR) and photosynthetic water-use efficiency (WUE) because lb is a species-specific function of growing-season precipitation. We found that demographically variable species have greater RGR and greater leaf carbon isotope discrimination (Delta, a proxy inversely related to WUE). We examined leaf nitrogen and photosynthetic characteristics and found that, in this system, variation in Delta is a function of photosynthetic demand rather than stomatal regulation of water loss. The physiological characteristics that result in low Delta in some species may confer greater photosynthetic performance during the reliably moist but low temperature periods that immediately follow winter rainfall in the Sonoran Desert or alternatively during cool periods of the day or early growing season. Conversely, while species with high Delta and high RGR exhibit low leaf N, they have high biomass allocation to canopy leaf area display. Such trait associations may allow for greater performance during the infrequent conditions where high soil moisture persists into warmer conditions, resulting in high demographic variance. Alternatively, high variance could arise from specialization to warm periods of the day or season. Population dynamic buffering via stress tolerance (low RGR and Delta) correlates negatively with buffering via seed banks, as predicted by bet-hedging theory. By merging analyses of population dynamics with functional trait relationships, we develop a deeper understanding of the physiological, ecological, and evolutionary mechanisms involved in population and community dynamics.

Bet hedging via seed banking in desert evening primroses (Oenothera, Onagraceae): demographic evidence from natural populations.

Bet hedging is one solution to the problem of an unpredictably variable environment: fitness in the average environment is sacrificed in favor of lower variation in fitness if this leads to higher long-run stochastic mean fitness. While bet hedging is an important concept in evolutionary ecology, empirical evidence that it occurs is scant. Here we evaluate whether bet hedging occurs via seed banking in natural populations of two species of desert evening primroses (Oenothera, Onagraceae), one annual and one perennial. Four years of data on plants and 3 years of data on seeds yielded two transitions for the entire life cycle. One year was exceptionally dry, leading to reproductive failure in the sample areas, and the other was above average in precipitation, leading to reproductive success in four of five populations. Stochastic simulations of population growth revealed patterns indicative of bet hedging via seed banking, particularly in the annual populations: variance in fitness and fitness in the average environment were lower with seed banking than without, whereas long-run stochastic mean fitness was higher with seed banking than without across a wide range of probabilities of the wet year. This represents a novel, unusually rigorous demonstration of bet hedging from field data.