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"Angilletta, Michael J."
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Costs and Benefits of Thermoregulation Revisited: Both the Heterogeneity and Spatial Structure of Temperature Drive Energetic Costs
In recent years, ecologists have stepped up to address the challenges imposed by rapidly changing climates. Some researchers have developed niche-based methods to predict how species will shift their ranges. Such methods have evolved rapidly, resulting in models that incorporate physiological and behavioral mechanisms. Despite their sophistication, these models fail to account for environmental heterogeneity at the scale of an organism. We used an individual-based model to quantify the effects of operative environmental temperatures, as well as their heterogeneity and spatial structure, on the thermoregulation, movement, and energetics of ectotherms. Our simulations showed that the heterogeneity and spatial structure of a thermal landscape are as important as its mean temperature. In fact, temperature and heterogeneity interact to determine organismal performance. Consequently, the popular index of environmental quality (d
e), which ignores variance and spatial structure, is inherently flawed as a descriptor of the thermal quality of an environment. Future efforts to model species’ distributions should link thermoregulation and activity to environmental heterogeneity at fine scales.
Journal Article
Configuration of the thermal landscape determines thermoregulatory performance of ectotherms
Although most organisms thermoregulate behaviorally, biologists still cannot easily predict whether mobile animals will thermoregulate in natural environments. Current models fail because they ignore how the spatial distribution of thermal resources constrains thermoregulatory performance over space and time. To overcome this limitation, we modeled the spatially explicit movements of animals constrained by access to thermal resources. Our models predict that ectotherms thermoregulate more accurately when thermal resources are dispersed throughout space than when these resources are clumped. This prediction was supported by thermoregulatory behaviors of lizards in outdoor arenas with known distributions of environmental temperatures. Further, simulations showed how the spatial structure of the landscape qualitatively affects responses of animals to climate. Biologists will need spatially explicit models to predict impacts of climate change on local scales.
Journal Article
Thermal adaptation : a theoretical and empirical synthesis
Temperature pervasively impacts the phenotypes and distributions of organisms. These thermal effects generate strong selective pressures on behaviour, physiology, and life history when environmental temperatures vary over space and time. Despite this fact, progress toward a quantitative theory of thermal adaptation has lagged behind empirical descriptions of patterns and processes. This book draws on current evolutionary paradigms (optimization, quantitative genetics, and genetic algorithms) to establish a theory of thermal adaptation. It initially focuses on simple models that describe the evolution of thermosensitivity, thermoregulation, or acclimation. Later chapters focus on more complex models describing the coadaptation of traits or the coevolution of species. Throughout the book, various lines of evidence are used to question the major assumptions of these models. Furthermore, the predictions of these models are confronted with experimental and comparative data. Empirical examples represent a wide range of taxa, including bacteria, plants, fungi, and animals. The result is a synthesis of theoretical and empirical studies of thermal biology that offers insights about evolutionary processes.
eBook
Thermoregulatory behaviour limits local adaptation of thermal niches and confers sensitivity to climate change
Summary Thermoregulation buffers environmental variation, which enables a species to persist during climate change but ultimately hinders adaptation of thermal tolerance by weakening selective pressure. We used a model of optimal thermal physiology to demonstrate how thermoregulatory behaviour limits local adaptation of thermal physiology in a widespread group of lizards, the Sceloporus undulatus complex. Empirical data for seven populations demonstrates conservatism of thermal tolerance, consistent with the model's prediction in the case of effective thermoregulation. In an eighth population, from a region where thermoregulation should be less effective, we observed greater heat tolerance and poorer cold tolerance, as predicted by our model. Biophysical modelling indicates that lizards can avoid heat stress through thermoregulation in the coming decades but will ultimately experience an abrupt decline in the effectiveness of thermoregulation. In this scenario, thermoregulators will suffer a greater loss of performance in future climates than thermoconformers will, unless heat tolerance can evolve in a few generations. Our analyses raises a concern that behavioural plasticity, while beneficial in the short term, will ultimately limit the physiological adaptation required to endure a warming climate. Lay Summary
Journal Article
Macrosystems ecology: understanding ecological patterns and processes at continental scales
Macrosystems ecology is the study of diverse ecological phenomena at the scale of regions to continents and their interactions with phenomena at other scales. This emerging subdiscipline addresses ecological questions and environmental problems at these broad scales. Here, we describe this new field, show how it relates to modern ecological study, and highlight opportunities that stem from taking a macrosystems perspective. We present a hierarchical framework for investigating macrosystems at any level of ecological organization and in relation to broader and finer scales. Building on well-established theory and concepts from other subdisciplines of ecology, we identify feedbacks, linkages among distant regions, and interactions that cross scales of space and time as the most likely sources of unexpected and novel behaviors in macrosystems. We present three examples that highlight the importance of this multiscaled systems perspective for understanding the ecology of regions to continents.
Journal Article
World Is not Flat: Defining Relevant Thermal Landscapes in the Context of Climate Change
Although climates are rapidly changing on a global scale, these changes cannot easily be extrapolated to the local scales experienced by organisms. In fact, such generalizations might be quite problematic. For instance, models used to predict shifts in the ranges of species during climate change rarely incorporate data resolved to <1 km2, although most organisms integrate climatic drivers at much smaller scales. Empirical studies alone suggest that the operative temperatures of many organisms vary by as much as 10–20°C on a local scale, depending on vegetation, geology, and topography. Furthermore, this variation in abiotic factors ignores thermoregulatory behaviors that many animals use to balance heat loads. Through a set of simulations, we demonstrate how variability in elevational topography can attenuate the effects of warming climates. These simulations suggest that changing climates do not always impact organisms negatively. Importantly, these simulations involve well-known relationships in biophysical ecology that show how no two organisms experience the same climate in the same way. We suggest that, when coupled with thermoregulatory behavior, variation in topographic features can mask the acute effect of climate change in many cases.
Journal Article
Resolving the life cycle alters expected impacts of climate change
Recent models predict contrasting impacts of climate change on tropical and temperate species, but these models ignore how environmental stress and organismal tolerance change during the life cycle. For example, geographical ranges and extinction risks have been inferred from thermal constraints on activity during the adult stage. Yet, most animals pass through a sessile embryonic stage before reaching adulthood, making them more susceptible to warming climates than current models would suggest. By projecting microclimates at high spatio-temporal resolution and measuring thermal tolerances of embryos, we developed a life cycle model of population dynamics for North American lizards. Our analyses show that previous models dramatically underestimate the demographic impacts of climate change. A predicted loss of fitness in 2% of the USA by 2100 became 35% when considering embryonic performance in response to hourly fluctuations in soil temperature. Most lethal events would have been overlooked if we had ignored thermal stress during embryonic development or had averaged temperatures over time. Therefore, accurate forecasts require detailed knowledge of environmental conditions and thermal tolerances throughout the life cycle.
Journal Article
Thermodynamic Effects on Organismal Performance: Is Hotter Better?
Despite decades of research on the evolution of thermal physiology, at least one fundamental issue remains unresolved: whether the maximal performance of a genotype depends on its optimal temperature. One school argues that warm‐adapted genotypes will outperform cold‐adapted genotypes because high temperatures inevitably accelerate chemical reactions. Yet another school holds that biochemical adaptation can compensate for thermodynamic effects on performance. Here, we briefly discuss this theoretical debate and then summarize empirical studies that address whether hotter is better. In general, comparative and experimental studies support the view that hotter is better. Furthermore, recent modeling has shown that thermodynamic constraints impose unique selective pressures on thermal sensitivity. Nevertheless, the thermodynamic effect on maximal performance varies greatly among traits and taxa, suggesting the need to develop a more sophisticated view of thermodynamic constraints.
Journal Article
Climate change expected to improve digestive rate and trigger range expansion in outbreaking locusts
Global climate change will probably exacerbate crop losses from insect pests, reducing agricultural production, and threatening food security. To predict where crop losses will occur, scientists have mainly used correlative models of species’ distributions, but such models are unreliable when extrapolated to future environments. To minimize extrapolation, we developed mechanistic and hybrid models that explicitly capture range-limiting processes, and we explored how incorporating mechanisms altered the projected impacts of climate change for an agricultural pest, the South American locust (Schistocerca cancellata). Because locusts are generalist herbivores surrounded by food, their population growth may be limited by thermal effects on digestion more than food availability. To incorporate this mechanism into a distribution model, we measured the thermal effects on the consumption and defecation of field-captured locusts and used these data to model energy gain in current and future climates. We then created hybrid models by using outputs of the mechanistic model as predictor variables in correlative models, estimating the potential distribution of gregarious outbreaking locusts based on multiple predictor sets, modeling algorithms, and climate scenarios. Based on the mechanistic model, locusts can assimilate relatively high amounts of energy throughout temperate and tropical South America; however, correlative and hybrid modeling revealed that most tropical areas are unsuitable for locusts. When estimating current distributions, the top-ranked model was always the one fit with mechanistic predictors (i.e., the hybrid model). When projected to future climates, top-ranked hybrid models projected range expansions that were 23%–30% points smaller than those projected by correlative models. Therefore, a combination of the correlative and mechanistic approaches bracketed the potential outcomes of climate change and enhanced confidence where model projections agreed. Because all models projected a poleward range expansion under climate change, agriculturists should consider enhanced monitoring and the management of locusts near the southern margin of the range.
Journal Article