Amy L. Angert

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.

Disentangling the drivers of context‐dependent plant–animal interactions

Summary 1. A fundamental goal of ecology is to predict how strongly one species affects the abundance of another. However, our ability to do so is hindered by the fact that interaction outcomes are notoriously variable in space and time (i.e. context-dependent) and we lack a predictive understanding of the factors that drive this context-dependence. Determining whether abiotic factors, in particular, predictably shift the outcome of species interactions is of critical importance for many contemporary problems, from forecasting climate change impacts to predicting the efficacy of weed biocontrol. 2. In this essay, we highlight the context-dependent nature of interactions between plants and their pollinators and herbivores. We advocate for approaches that will identify whether particular abiotic factors predictably shift how strongly these interactions influence plant abundance and/or population growth. We review long-standing theory that describes how abiotic context should influence the selective impacts of pollinators and herbivores on plants and articulate why this theory requires modification to predict population-level effects. 3. Finally, we propose several empirical approaches to address gaps in existing knowledge: (i) experiments across broad abiotic gradients to determine whether the outcome of interactions between pollinators or herbivores and plants varies consistently with changing abiotic conditions; (ii) experiments that manipulate the underlying environmental gradient to elucidate whether the abiotic factor that correlates with interaction outcome is causal; and (iii) seed addition studies to explore how strongly seedling recruitment correlates with seed input (as affected by pollen limitation or herbivory) and to quantify how the strength of the seed-to-seedling linkage is influenced by the underlying abiotic gradient. 4. Synthesis. Our understanding of the underlying drivers of context-dependent plant–animal interactions is currently not well developed. Progress in this area is essential to better predict when and where species interactions will alter the responses of plant populations to environmental changes as well as to develop more robust theory. Experiments aimed at explicitly exploring the role of abiotic factors in mediating the population-level impact of pollen limitation and herbivory could determine the extent to which variation in the abiotic environment predictably shifts the outcome of these interactions.

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.

Growth and leaf physiology of monkeyflowers with different altitude ranges.

Every species is limited both geographically and ecologically to a subset of available habitats, yet for many species the causes of distribution limits are unknown. Temperature is thought to be one of the primary determinants of species distributions along latitudinal and altitudinal gradients. This study examined leaf physiology and plant performance under contrasting temperature regimes of sister species of monkeyflower, Mimulus cardinalis and Mimulus lewisii (Phrymaceae), that differ in altitude distribution to test the hypothesis that temperature is the primary determinant of differences in fitness versus altitude. Each species attained greatest aboveground biomass, net photosynthetic rate, and effective quantum yield of photosystem II when grown under temperatures characteristic of the altitudinal range center. Although both species exhibited greater stem length, stomatal conductance, and intercellular CO2 concentration in hot than in cold temperatures, these traits showed much greater reductions under cold temperature for M. cardinalis than for M. lewisii. Survival of M. lewisii was also sensitive to temperature, showing a striking decrease in hot temperatures. Within each temperature regime, the species native to that temperature displayed greatest growth and leaf physiological capacity. Populations from the altitude range center and range margin of each species were used to examine population differentiation, but central and marginal populations did not differ in most growth or leaf physiological responses to temperature. This study provides evidence that M. cardinalis and M. lewisii differ in survival, growth, and leaf physiology under temperature regimes characterizing their contrasting low and high altitude range centers, and suggests that the species’ altitude range limits may arise, in part, due to metabolic limitations on growth that ultimately decrease survival and limit reproduction.

Quantifying the Impact of Gene Flow on Phenotype- Environment Mismatch: A Demonstration with the Scarlet Monkeyflower Mimulus cardinalis

Geographic range margins offer testing grounds for limits to adaptation. If range limits are concordant with niche limits, range expansions require the evolution of new phenotypes that can maintain populations beyond current range margins. However, many species’ range margins appear static over time, suggesting limits on the ability of marginal populations to evolve appropriate phenotypes. A potential explanation is the swamping gene flow hypothesis, which posits that asymmetrical gene flow from large, well-adapted central populations prevents marginal populations from locally adapting. We present an empirical framework for combining gene flow, environment, and fitness-related phenotypes to infer the potential for maladaptation, and we demonstrate its application using the scarlet monkeyflower Mimulus cardinalis. We grew individuals sampled from populations on a latitudinal transect under varied temperatures and determined the phenotypic deviation (PD), the mismatch between phenotype and local environment. We inferred gene flow among populations and predicted that populations receiving the most temperature- or latitude-weighted immigration would show the greatest PD and that these populations were likely marginal. We found asymmetrical gene flow from central to marginal populations. Populations with more latitude-weighted immigration had significantly greater PD but were not necessarily marginal. Gene flow may limit local adaptation in this species, but swamping gene flow is unlikely to explain its northern range limit.

THE EVOLUTION OF ENVIRONMENTAL TOLERANCE AND RANGE SIZE: A COMPARISON OF GEOGRAPHICALLY RESTRICTED AND WIDESPREAD MIMULUS

The geographic ranges of closely related species can vary dramatically, yet we do not fully grasp the mechanisms underlying such variation. The niche breadth hypothesis posits that species that have evolved broad environmental tolerances can achieve larger geographic ranges than species with narrow environmental tolerances. In turn, plasticity and genetic variation in ecologically important traits and adaptation to environmentally variable areas can facilitate the evolution of broad environmental tolerance. We used five pairs of western North American monkeyflowers to experimentally test these ideas by quantifying performance across eight temperature regimes. In four species pairs, species with broader thermal tolerances had larger geographic ranges, supporting the niche breadth hypothesis. As predicted, species with broader thermal tolerances also had more within‐population genetic variation in thermal reaction norms and experienced greater thermal variation across their geographic ranges than species with narrow thermal tolerances. Species with narrow thermal tolerance may be particularly vulnerable to changing climatic conditions due to lack of plasticity and insufficient genetic variation to respond to novel selection pressures. Conversely, species experiencing high variation in temperature across their ranges may be buffered against extinction due to climatic changes because they have evolved tolerance to a broad range of temperatures.

Climate change and species interactions: ways forward.

With ongoing and rapid climate change, ecologists are being challenged to predict how individual species will change in abundance and distribution, how biotic communities will change in structure and function, and the consequences of these climate‐induced changes for ecosystem functioning. It is now well documented that indirect effects of climate change on species abundances and distributions, via climatic effects on interspecific interactions, can outweigh and even reverse the direct effects of climate. However, a clear framework for incorporating species interactions into projections of biological change remains elusive. To move forward, we suggest three priorities for the research community: (1) utilize tractable study systems as case studies to illustrate possible outcomes, test processes highlighted by theory, and feed back into modeling efforts; (2) develop a robust analytical framework that allows for better cross‐scale linkages; and (3) determine over what time scales and for which systems prediction of biological responses to climate change is a useful and feasible goal. We end with a list of research questions that can guide future research to help understand, and hopefully mitigate, the negative effects of climate change on biota and the ecosystem services they provide.

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.

Microhabitat Use and Thermal Biology of the Collared Lizard (Crotaphytus collaris collaris) and the Fence Lizard (Sceloporus undulatus hyacinthinus) in Missouri Glades

Abstract Collared lizards, Crotaphytus collaris, live in isolated populations on Missouri glades. Anecdotal observations suggest that another lizard species, Sceloporus undulatus, is rare on glades where C. collaris is present. Possible causes of scarcity of S. undulatus in the presence of C. collaris include competition, predation, and unsuitable thermal conditions. We characterized thermal biology and habitat partitioning in these two species by measuring body and air temperatures, and microhabitat use, at three glades. Sceloporus undulatus maintains lower body temperatures than C. collaris and shifts from open rock perches to shady tree perches during the middle of its activity season. Crotaphytus collaris microhabitats are rockier and more open than those of S. undulatus, which tend to have more branches, leaves, and trees nearby. These data indicate that areas of glades hot enough for use by C. collaris are too hot for S. undulatus. Although we cannot rule out competition or predation, constraints of the thermal environment may be an important factor in the apparent scarcity of S. undulatus on glades.

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

UNLABELLED 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.