Looking to the past to understand the future: linking evolutionary modes of response with functional and life history traits in variable environments.

In a variable world, plants must have strategies to deal with environmental conditions as they change. Understanding these strategies is critical since climate change not only affects mean conditions but also affects variability and predictability of those conditions. Doing so requires identifying how functional and life history traits interact throughout the life cycle to drive responses, as well as exploring how past variability will shape future responses. Here, I highlight relevant life history theory for predicting strategies in relation to the nature of environmental variability, relate theory to empirical studies integrating functional and life history traits to understand responses, and identify key areas for future research that will facilitate the application of this understanding toward predicting responses to climate change.

Vulnerability of grassland seed banks to resource-enhancing global changes.

Soil seed banks represent reservoirs of diversity in the soil that may increase resilience of communities to global changes. Two global change factors that can dramatically alter the composition and diversity of aboveground communities are nutrient enrichment and increased rainfall. In a full-factorial nutrient and rainfall addition experiment in an annual Californian grassland, we asked whether shifts in aboveground composition and diversity were reflected in belowground seed banks. Nutrient and rainfall additions increased exotic and decreased native abundances, while rainfall addition increased exotic richness, both in aboveground communities and seed banks. Under nutrient addition, forbs and short-statured plants were replaced by grasses and tall-statured species, both above and below ground, and whole-community responses to the treatments were similar. Structural equation models indicated that especially nutrient addition effects on seed banks were largely indirect via aboveground communities. However, rainfall addition also had a direct negative effect on native species richness and abundance of species with high specific leaf area (SLA) in seed banks, showing that seed banks are sensitive to the direct effects of temporary increases in rainfall. Our findings highlight the vulnerability of seed banks in annual, resource-poor grasslands to shifts in compositional and trait changes in aboveground communities and show how invasion of exotics and depletion of natives are critical for these above-belowground compositional shifts. Our findings suggest that seed banks have limited potential to buffer resource-poor annual grasslands from the community changes caused by resource enrichment.

The Net Effect of Functional Traits on Fitness.

Generalizing the effect of traits on performance across species may be achievable if traits explain variation in population fitness. However, testing relationships between traits and vital rates to infer effects on fitness can be misleading. Demographic trade-offs can generate variation in vital rates that yield equal population growth rates, thereby obscuring the net effect of traits on fitness. To address this problem, we describe a diversity of approaches to quantify intrinsic growth rates of plant populations, including experiments beyond range boundaries, density-dependent population models built from long-term demographic data, theoretical models, and methods that leverage widely available monitoring data. Linking plant traits directly to intrinsic growth rates is a fundamental step toward rigorous predictions of population dynamics and community assembly.

Variation in the seasonal germination niche across an elevational gradient: the role of germination cueing in current and future climates.

PREMISE: The timing of germination has profound impacts on fitness, population dynamics, and species ranges. Many plants have evolved responses to seasonal environmental cues to time germination with favorable conditions; these responses interact with temporal variation in local climate to drive the seasonal climate niche and may reflect local adaptation. Here, we examined germination responses to temperature cues in Streptanthus tortuosus populations across an elevational gradient. METHODS: Using common garden experiments, we evaluated differences among populations in response to cold stratification (chilling) and germination temperature and related them to observed germination phenology in the field. We then explored how these responses relate to past climate at each site and the implications of those patterns under future climate change. RESULTS: Populations from high elevations had stronger stratification requirements for germination and narrower temperature ranges for germination without stratification. Differences in germination responses corresponded with elevation and variability in seasonal temperature and precipitation across populations. Further, they corresponded with germination phenology in the field; low-elevation populations germinated in the fall without chilling, whereas high-elevation populations germinated after winter chilling and snowmelt in spring and summer. Climate-change forecasts indicate increasing temperatures and decreasing snowpack, which will likely alter germination cues and timing, particularly for high-elevation populations. CONCLUSIONS: The seasonal germination niche for S. tortuosus is highly influenced by temperature and varies across the elevational gradient. Climate change will likely affect germination timing, which may cascade to influence trait expression, fitness, and population persistence.

Optimal germination timing in unpredictable environments: the importance of dormancy for both among- and within-season variation.

For organisms living in unpredictable environments, timing important life-history events is challenging. One way to deal with uncertainty is to spread the emergence of offspring across multiple years via dormancy. However, timing of emergence is not only important among years, but also within each growing season. Here, we study the evolutionary interactions between germination strategies that deal with among- and within-season uncertainty. We use a modelling approach that considers among-season dormancy and within-season germination phenology of annual plants as potentially independent traits and study their separate and joint evolution in a variable environment. We find that higher among-season dormancy selects for earlier germination within the growing season. Furthermore, our results indicate that more unpredictable natural environments can counter-intuitively select for less risk-spreading within the season. Furthermore, strong priority effects select for earlier within-season germination phenology which in turn increases the need for bet hedging through among-season dormancy.

Predicting evolutionarily stable strategies from functional responses of Sonoran Desert annuals to precipitation.

For many decades, researchers have studied how plants use bet-hedging strategies to insure against unpredictable, unfavourable conditions. We improve upon earlier analyses by explicitly accounting for how variable precipitation affects annual plant species' bet-hedging strategies. We consider how the survival rates of dormant seeds (in a 'seed bank') interact with precipitation responses to influence optimal germination strategies. Specifically, we incorporate how response to resource availability (i.e. the amount of offspring (seeds) generated per plant in response to variation in desert rainfall) influences the evolution of germination fractions. Using data from 10 Sonoran Desert annual plants, we develop models that explicitly include these responses to model fitness as a function of precipitation. For each of the species, we identify the predicted evolutionarily stable strategies (ESSs) for the fraction of seeds germinating each year and then compare our estimated ESS values to the observed germination fractions. We also explore the relative importance of seed survival and precipitation responses in shaping germination strategies by regressing ESS values and observed germination fractions against these traits. We find that germination fractions are lower for species with higher seed survival, with lower reproductive success in dry years, and with better yield responses in wet years. These results illuminate the evolution of bet-hedging strategies in an iconic system, and provide a framework for predicting how current and future environmental conditions may reshape those strategies.

Increasing temperature seasonality may overwhelm shifts in soil moisture to favor shrub over grass dominance in Colorado Plateau drylands.

Ecosystems in the southwestern U.S. are predicted to experience continued warming and drying trends of the early twenty-first century. Climate change can shift the balance between grass and woody plant abundance in these water-limited systems, which has large implications for biodiversity and ecosystem processes. However, variability in topo-edaphic conditions, notably soil texture and depth, confound efforts to quantify specific climatic controls over grass vs. shrub dominance. Here, we utilized weather records and a mechanistic soil water model to identify the timing and depth at which soil moisture related most strongly to the balance between grass and shrub dominance in the southern Colorado Plateau. Shrubs dominate where there is high soil moisture availability during winter, and where temperature is more seasonally variable, while grasses are favored where moisture is available during summer. Climate change projections indicate consistent increases in mean temperature and seasonal temperature variability for all sites, but predictions for summer and winter soil moisture vary across sites. Together, these changes in temperature and soil moisture are expected to shift the balance towards increasing shrub dominance across the region. These patterns are strongly driven by changes in temperature, which either enhance or overwhelm effects of changes in soil moisture across sites. This approach, which incorporates local, edaphic factors at sites protected from disturbance, improves understanding of climate change impacts on grass vs. shrub abundance and may be useful in other dryland regions with high edaphic and climatic heterogeneity.

Rapid alignment of functional trait variation with locality across the invaded range of Sahara mustard (Brassica tournefortii).

PREMISE OF STUDY: Mechanisms by which invasive species succeed across multiple novel environmental contexts are poorly understood. Functional traits show promise for identifying such mechanisms, yet we lack knowledge of which functional traits are critical for success and how they vary across invaded ranges and with environmental features. We evaluated the widespread recent invasion of Sahara mustard (Brassica tournefortii) in the southwestern United States to understand the extent of functional trait variation across the invaded range and how such variation is related to spatial and climatic gradients. METHODS: We used a common garden approach, growing two generations of plants in controlled conditions sourced from 10 locations across the invaded range. We measured variation within and among populations in phenological, morphological, and physiological traits, as well as performance. KEY RESULTS: We found nine key traits that varied among populations. These traits were related to phenology and early growth strategies, such as the timing of germination and flowering, as well as relative allocation of biomass to reproduction and individual seed mass. Trait variation was related most strongly to variation in winter precipitation patterns across localities, though variations in temperature and latitude also had significant contributions. CONCLUSIONS: Our results identify key functional traits of this invasive species that showed significant variation among introduced populations across a broad geographic and climatic range. Further, trait variation among populations was strongly related to key climatic variables, which suggests that population divergence in these traits may explain the successful colonization of Sahara mustard across its invaded US range.

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.

Desert grassland responses to climate and soil moisture suggest divergent vulnerabilities across the southwestern United States.

Climate change predictions include warming and drying trends, which are expected to be particularly pronounced in the southwestern United States. In this region, grassland dynamics are tightly linked to available moisture, yet it has proven difficult to resolve what aspects of climate drive vegetation change. In part, this is because it is unclear how heterogeneity in soils affects plant responses to climate. Here, we combine climate and soil properties with a mechanistic soil water model to explain temporal fluctuations in perennial grass cover, quantify where and the degree to which incorporating soil water dynamics enhances our ability to understand temporal patterns, and explore the potential consequences of climate change by assessing future trajectories of important climate and soil water variables. Our analyses focused on long-term (20-56 years) perennial grass dynamics across the Colorado Plateau, Sonoran, and Chihuahuan Desert regions. Our results suggest that climate variability has negative effects on grass cover, and that precipitation subsidies that extend growing seasons are beneficial. Soil water metrics, including the number of dry days and availability of water from deeper (>30 cm) soil layers, explained additional grass cover variability. While individual climate variables were ranked as more important in explaining grass cover, collectively soil water accounted for 40-60% of the total explained variance. Soil water conditions were more useful for understanding the responses of C3 than C4 grass species. Projections of water balance variables under climate change indicate that conditions that currently support perennial grasses will be less common in the future, and these altered conditions will be more pronounced in the Chihuahuan Desert and Colorado Plateau. We conclude that incorporating multiple aspects of climate and accounting for soil variability can improve our ability to understand patterns, identify areas of vulnerability, and predict the future of desert grasslands.

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.

High water-use efficiency and growth contribute to success of non-native Erodium cicutarium in a Sonoran Desert winter annual community.

The success of non-native, invasive species may be due to release from natural enemies, superior competitive abilities, or both. In the Sonoran Desert, Erodium cicutarium has increased in abundance over the last 30 years. While native species in this flora exhibit a strong among-species trade-off between relative growth rate and water-use efficiency, E. cicutarium seems to have a higher relative growth rate for its water-use efficiency value relative to the pattern across native species. This novel trait combination could provide the non-native species with a competitive advantage in this water-limited environment. To test the hypothesis that E. cicutarium is able to achieve high growth rates due to release from native herbivores, we compared the effects of herbivory on E. cicutarium and its native congener, Erodium texanum. We also compared these two species across a range of environmental conditions, both in a common garden and in two distinct seasons in the field, using growth analysis, isotopic compositions and leaf-level gas exchange. Additionally, we compared the competitive abilities of the two Erodium species in a greenhouse experiment. We found no evidence of herbivory to either species. Physiological measurements in a common environment revealed that E. cicutarium was able to achieve high growth rates while simultaneously controlling leaf-level water loss. Non-native E. cicutarium responded to favourable conditions in the field with greater specific leaf area and leaf area ratio than native E. texanum. The non-native Erodium was a stronger competitor than its native congener in a greenhouse competition experiment. The ability to maintain relatively higher values of water-use efficiency:relative growth rate in comparison to the native flora may be what enables E. cictarium to outcompete native species in both wet and dry years, resulting in an increase in abundance in the highly variable Sonoran Desert.

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.

Phenotypic selection favors missing trait combinations in coexisting annual plants.

Trade-offs among traits are important for maintaining biodiversity, but the role of natural selection in their construction is not often known. It is possible that trade-offs reflect fundamental constraints, negative correlational selection, or directional selection operating on costly, redundant traits. In a Sonoran Desert community of winter annual plants, we have identified a trade-off between relative growth rate and water-use efficiency among species, such that species with high relative growth rate have low water-use efficiency and vice versa. We measured selection on water-use efficiency, relative growth rate, and underlying traits within populations of four species at two study sites with different average climates. Phenotypic trait correlations within species did not match the among-species trade-off. In fact, for two species with high water-use efficiency, individuals with high relative growth rate also had high water-use efficiency. All populations experienced positive directional selection for water-use efficiency and relative growth rate. Selection tended to be stronger on water-use efficiency at the warmer and drier site, and selection on relative growth rate tended to be stronger at the cooler and wetter site. Our results indicate that directional natural selection favors a phenotype not observed among species in the community, suggesting that the among-species trade-off could be due to pervasive genetic constraints, perhaps acting in concert with processes of community assembly.

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.

It is risky out there: the costs of emergence and the benefits of prolonged dormancy.

Prolonged dormancy is a stage in herbaceous perennial plants in which some individuals remain alive below ground for one or more growing seasons instead of emerging. Prolonged dormancy is puzzling, because foregoing opportunities for growth and reproduction seems costly. However, studies have shown that it buffers plants from the negative consequences associated with environmental stochasticity, suggesting that dormancy is a beneficial strategy to avoid the risks of stress above ground. If so, emergence during unfavorable conditions should have significant costs. Here, we test the hypothesis that emergence during times of stress has negative demographic consequences in a native perennial forb, Astragalus scaphoides, and investigate the potential underlying physiological mechanisms. We measured plant responses to a severe seasonal drought and an experimental defoliation to ask: (1) How do emergent plants respond to above-ground stress? (2) Do these responses have negative demographic consequences? and (3) Based on these responses, does stress increase the risk of emergence? Plants showed remarkable physiological tolerance to stress in the short term: high temperatures and low moisture did not have a strong effect on photosynthesis rates, and neither drought nor defoliation significantly impacted stored resources. However, stress did result in demographic costs for emergent plants relative to plants experiencing more favorable conditions. Drought resulted in decreased flowering probabilities relative to the long-term average and defoliation significantly increased mortality rates. These results demonstrate that the risk of emerging and experiencing stress entails considerable costs, supporting the hypothesis that prolonged dormancy is a beneficial strategy to avoid such risk.

Are dormant plants hedging their bets? Demographic consequences of prolonged dormancy in variable environments.

During the growing season, some individuals in perennial plant populations may remain alive belowground while others emerge. This phenomenon, known as prolonged dormancy, seems maladaptive, because prolonged dormancy delays growth and reproduction. However, prolonged dormancy may offer the benefit of safety while belowground, leading to the hypothesis that prolonged dormancy is a bet-hedging strategy. We evaluated this hypothesis using a 25-year demographic study of Astragalus scaphoides, an iteroparous perennial plant. First, we determined the relationship between prolonged dormancy and fitness using data from individuals in our population. This analysis showed that prolonged dormancy decreased arithmetic mean fitness and reduced variance in fitness. Geometric mean fitness was maximized at intermediate levels of prolonged dormancy. Empirical patterns of lifetime reproductive success confirm this relationship. We also compared fitness of plants in our population to hypothetical plants without prolonged dormancy, which generally revealed benefits of prolonged dormancy, even if plants could forgo prolonged dormancy without costs to other vital rates. Therefore, prolonged dormancy may indeed function as a bet-hedging strategy, but the benefits of remaining belowground outweigh the costs only for a subset of individuals. Bet hedging has been demonstrated in plants with simple life histories, such as annuals and monocarpic perennials; we present evidence that bet hedging may be important for plants with more complex life histories.

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.