Corticosterone and glucose are correlated and show similar response patterns to temperature and stress in a free-living bird.

Glucocorticoid (GC) hormones have traditionally been interpreted as indicators of stress, but the extent to which they provide information on physiological state remains debated. GCs are metabolic hormones that amongst other functions ensure increasing fuel (i.e. glucose) supply on the face of fluctuating energetic demands, a role often overlooked by ecological studies investigating the consequences of GC variation. Furthermore, because energy budget is limited, in natural contexts where multiple stimuli coexist, the organisms' ability to respond physiologically may be constrained when multiple triggers of metabolic responses overlap in time. Using free-living spotless starling (Sturnus unicolor) chicks, we experimentally tested whether two stimuli of different nature known to trigger a metabolic or GC response, respectively, cause a comparable increase in plasma GCs and glucose. We further tested whether response patterns differed when both stimuli occurred consecutively. We found that both experimental treatments caused increases in GCs and glucose of similar magnitude, suggesting that both variables fluctuate along with variation in energy expenditure, independently of the trigger. Exposure to the two stimuli occurring subsequently did not cause a difference in GC or glucose responses compared with exposure to a single stimulus, suggesting a limited capacity to respond to an additional stimulus during an ongoing acute response. Lastly, we found a positive and significant correlation between plasma GCs and glucose after the experimental treatments. Our results add to the increasing research on the role of energy expenditure on GC variation, by providing experimental evidence on the association between plasma GCs and energy metabolism.

Modelling the role of glucocorticoid receptor as mediator of endocrine responses to environmental challenge.

Glucocorticoid hormones (GCs) modulate acute 'stress' responses in vertebrates, exerting their actions across many physiological systems to help the organism face and overcome challenges. These actions take place via binding to the glucocorticoid receptor (GR), which determines not only the magnitude of the GC-mediated physiological response but also the negative feedback that downregulates GCs to restore homeostasis. Although GR function is assumed to determine GC regulation capacity, the associations between GR abundance and individuals' coping abilities remain cryptic. We developed a dynamic model fitted to empirical data to predict the effects of GR abundance on both plasma GC response patterns and the magnitude of GC-mediated physiological response. Individuals with higher GRs showed lower GC exposure, stronger physiological responses and greater capacity to adjust this response according to stressor intensity, which may be translated into more resilient and flexible GC phenotypes. Our results also show that among-individual variability in GR abundance challenges the detectability of the association between plasma GC measurements and physiological responses. Our approach provides mechanistic insights into the role of GRs in plasma GC measurements and function, which point at GR abundance fundamentally driving complex features of the GC regulation system in the face of environmental change. This article is part of the theme issue 'Endocrine responses to environmental variation: conceptual approaches and recent developments'.

Metabolic responses to cold and warm extremes in the ocean.

Temperature influences the geographical distribution of species, but its mechanisms are much debated. A new study in PLOS Biology suggests that metabolic constrains can arise in both warm and cold waters at the geographical range limits of marine species.

Temperate species underfill their tropical thermal potentials on land.

Understanding how temperature determines the distribution of life is necessary to assess species' sensitivities to contemporary climate change. Here, we test the importance of temperature in limiting the geographic ranges of ectotherms by comparing the temperatures and areas that species occupy to the temperatures and areas species could potentially occupy on the basis of their physiological thermal tolerances. We find that marine species across all latitudes and terrestrial species from the tropics occupy temperatures that closely match their thermal tolerances. However, terrestrial species from temperate and polar latitudes are absent from warm, thermally tolerable areas that they could potentially occupy beyond their equatorward range limits, indicating that extreme temperature is often not the factor limiting their distributions at lower latitudes. This matches predictions from the hypothesis that adaptation to cold environments that facilitates survival in temperate and polar regions is associated with a performance trade-off that reduces species' abilities to contend in the tropics, possibly due to biotic exclusion. Our findings predict more direct responses to climate warming of marine ranges and cool range edges of terrestrial species.

Climate drives global functional trait variation in lizards.

A major challenge in ecology and evolution is to disentangle the mechanisms driving broad-scale variation in biological traits such as body size, colour, thermal physiology traits and behaviour. Climate has long been thought to drive trait evolution and abiotic filtering of trait variation in ectotherms because their thermal performance and fitness are closely related to environmental conditions. However, previous studies investigating climatic variables associated with trait variation have lacked a mechanistic description of the underpinning processes. Here, we use a mechanistic model to predict how climate affects thermal performance of ectotherms and thereby the direction and strength of the effect of selection on different functional traits. We show that climate drives macro-evolutionary patterns in body size, cold tolerance and preferred body temperatures among lizards, and that trait variation is more constrained in regions where selection is predicted to be stronger. These findings provide a mechanistic explanation for observations on how climate drives trait variation in ectotherms through its effect on thermal performance. By connecting physical, physiological and macro-evolutionary principles, the model and results provide an integrative, mechanistic framework for predicting organismal responses to present climates and climate change.

Contrasting patterns in phylogenetic and biogeographic factories of invasive grasses (Poaceae) across the globe.

Grasses (Family Poaceae) are among the most successful invasive plants in the world. Here we evaluate phylogenetic and biogeographic patterns of emergence of naturalized and invasive species among grasses globally. In our data, circa 19% of the grasses are currently catalogued as invasive and almost 38% are listed as naturalized; these are among the highest ratios for single families of organisms. Remarkably, most tribes of grasses contain numerous naturalized and invasive species, suggesting that the invasion success is rooted broadly in ancestral traits in the Poaceae. Moreover, the probability of invasiveness is positively related to the diversification rates in the family also suggesting a link with recent radiation events. The phylogenetic distribution of the invasive condition is neither strongly conserved nor purely random. Phylogenetic clumping levels also vary between Poaceae subclades. We postulate that this diffuse clumping could be partially attributed to the expression of labile traits that contribute to species invasiveness. In addition, floristic regions (biomes and biogeographic realms) have different proportions of invasive species, with the temperate Palearctic region having the highest ratio of invasive vs. non-invasive species. The phylodiversity of aliens across regions is also variable in space. Comparison of alien phylodiversity levels across biogeographic realms and biomes reveals regions producing highly restricted invasive lineages and others where the diversity of aliens exported is no different from global mean diversity levels in grasses. Elucidating the evolutionary patterns and drivers of invasiveness is useful for understanding and managing invasions, with the low phylogenetic structure of alien grasses warning of their overall high invasiveness potential.

Physical constraints on thermoregulation and flight drive morphological evolution in bats.

Body size and shape fundamentally determine organismal energy requirements by modulating heat and mass exchange with the environment and the costs of locomotion, thermoregulation, and maintenance. Ecologists have long used the physical linkage between morphology and energy balance to explain why the body size and shape of many organisms vary across climatic gradients, e.g., why larger endotherms are more common in colder regions. However, few modeling exercises have aimed at investigating this link from first principles. Body size evolution in bats contrasts with the patterns observed in other endotherms, probably because physical constraints on flight limit morphological adaptations. Here, we develop a biophysical model based on heat transfer and aerodynamic principles to investigate energy constraints on morphological evolution in bats. Our biophysical model predicts that the energy costs of thermoregulation and flight, respectively, impose upper and lower limits on the relationship of wing surface area to body mass (S-MR), giving rise to an optimal S-MR at which both energy costs are minimized. A comparative analysis of 278 species of bats supports the model's prediction that S-MR evolves toward an optimal shape and that the strength of selection is higher among species experiencing greater energy demands for thermoregulation in cold climates. Our study suggests that energy costs modulate the mode of morphological evolution in bats­hence shedding light on a long-standing debate over bats' conformity to ecogeographical patterns observed in other mammals­and offers a procedure for investigating complex macroecological patterns from first principles.

Oxygen limitation may affect the temperature and size dependence of metabolism in aquatic ectotherms.

Both oxygen and temperature are fundamental factors determining metabolic performance, fitness, ecological niches, and responses of many aquatic organisms to climate change. Despite the importance of physical and physiological constraints on oxygen supply affecting aerobic metabolism of aquatic ectotherms, ecological theories such as the metabolic theory of ecology have focused on the effects of temperature rather than oxygen. This gap currently impedes mechanistic models from accurately predicting metabolic rates (i.e., oxygen consumption rates) of aquatic organisms and restricts predictions to resting metabolism, which is less affected by oxygen limitation. Here, we expand on models of metabolic scaling by accounting for the role of oxygen availability and temperature on both resting and active metabolic rates. Our model predicts that oxygen limitation is more likely to constrain metabolism in larger, warmer, and active fish. Consequently, active metabolic rates are less responsive to temperature than are resting metabolic rates, and metabolism scales to body size with a smaller exponent whenever temperatures or activity levels are higher. Results from a metaanalysis of fish metabolic rates are consistent with our model predictions. The observed interactive effects of temperature, oxygen availability, and body size predict that global warming will limit the aerobic scope of aquatic ectotherms and may place a greater metabolic burden on larger individuals, impairing their physiological performance in the future. Our model reconciles the metabolic theory with empirical observations of oxygen limitation and provides a formal, quantitative framework for predicting both resting and active metabolic rate and hence aerobic scope of aquatic ectotherms.

Divergence and constraint in the thermal sensitivity of aquatic insect swimming performance.

Environmental temperature variation may play a significant role in the adaptive evolutionary divergence of ectotherm thermal performance curves (TPCs). However, divergence in TPCs may also be constrained due to various causes. Here, we measured TPCs for swimming velocity of temperate and tropical mayflies (Family: Baetidae) and their stonefly predators (Family: Perlidae) from different elevations. We predicted that differences in seasonal climatic regimes would drive divergence in TPCs between temperate and tropical species. Stable tropical temperatures should favor the evolution of "specialists" that perform well across a narrow range of temperatures. Seasonally, variable temperatures in temperate zones, however, should favor "generalists" that perform well across a broad range of temperatures. In phylogenetically paired comparisons of mayflies and stoneflies, swimming speed was generally unaffected by experimental temperature and did not differ among populations between latitudes, suggesting a maintenance of performance breadth across elevation and latitude. An exception was found between temperate and tropical mayflies at low elevation where climatic differences between latitudes are large. In addition, TPCs did not differ between mayflies and their stonefly predators, except at tropical low elevation. Our results indicate that divergence in TPCs may be constrained in aquatic insects except under the most different thermal regimes, perhaps because of trade-offs that reduce thermal sensitivity and increase performance breadth.

The biogeography of thermal risk for terrestrial ectotherms: Scaling of thermal tolerance with body size and latitude.

Many organisms are shrinking in size in response to global warming. However, we still lack a comprehensive understanding of the mechanisms linking body size and temperature of organisms across their geographical ranges. Here we investigate the biophysical mechanisms determining the scaling of body temperature with size across latitudes in terrestrial ectotherms. Using biophysical models, we simulated operative temperatures experienced by lizard-like ectotherms as a function of microclimatic variables, body mass and latitude and used them to generate null predictions for the effect of size on temperature across geographical gradients. We then compared model predictions against empirical data on lizards' field body temperature (Tb ) and thermal tolerance limits (CTmax and CTmin ). Our biophysical models predict that the allometric scaling of operative temperatures with body size varies with latitude, with a positive relationship at low latitudes that vanishes with increasing latitude. The analyses of thermal traits of lizards show a significant interaction of body size and latitude on Tb and CTmax and no effect of body mass on CTmin , consistent with model's predictions. The estimated scaling coefficients are within the ranges predicted by the biophysical model. The effect of body mass, however, becomes non-significant after controlling for the phylogenetic relatedness between species. We propose that large-bodied terrestrial ectotherms exhibit higher risk of overheating at low latitudes, while size differences in thermal sensitivity vanish towards higher latitudes. Our work highlights the potential of combining mechanistic models with empirical data to investigate the mechanisms underpinning broad-scale patterns and ultimately provide a null model to develop baseline expectations for further empirical research.

Upscaling Microclimatic Conditions into Body Temperature Distributions of Ectotherms.

Realistic projections of the biological impacts of climate change require predicting fitness responses to variations in environmental conditions. For ectotherms, this challenge requires methods to scale-up microclimatic information into actual body temperatures, Tb, while dealing with uncertainty regarding individual behaviors and physiological constraints. Here, we propose an information-theoretical model to derive microhabitat selection and Tb distributions of ectotherm populations from microclimatic data. The model infers the most probable allocation of individuals among the available microenvironments and the associated population-level Tb distribution. Using empirical Tb data of 41 species of desert lizards from three independently evolved systems-Western North America, Kalahari Desert, and Western Australia-we show that the model accurately predicts empirical Tb distributions across the three systems. Moreover, the framework naturally provides a way to quantify the importance of thermoregulation in a thermal environment and thereby a measurement for the constraint imposed by the climatic conditions. By predicting Tb distributions of ectotherm populations even without exhaustive information on the underpinning mechanisms, our approach forms a solid theoretical basis for upscaling microclimatic and physiological information into a population-level fitness trait. This scaling process is a first step to reliably project the biological impacts of climate change to broad temporal and spatial scales.

Biophysical Modeling of Water Economy Can Explain Geographic Gradient of Body Size in Anurans.

Geographical gradients of body size express climate-driven constraints on animals, but whether they exist and what causes them in ectotherms remains contentious. For amphibians, the water conservation hypothesis posits that larger bodies reduce evaporative water loss (EWL) along dehydrating gradients. To address this hypothesis mechanistically, we build on well-established biophysical equations of water exchange in anurans to propose a state-transition model that predicts an increase of either body size or resistance to EWL as alternative specialization along dehydrating gradients. The model predicts that species whose water economy is more sensitive to variation in body size than to variation in resistance to EWL should increase in size in response to increasing potential evapotranspiration (PET). To evaluate the model predictions, we combine physiological measurements of resistance to EWL with geographic data of body size for four different anuran species. Only one species, Dendropsophus minutus, was predicted to exhibit a positive body size-PET relationship. Results were as predicted for all cases, with one species-Boana faber-showing a negative relationship. Based on an empirically verified mathematical model, we show that clines of body size among anurans depend on the current values of those traits and emerge as an advantage for water conservation. Our model offers a mechanistic and compelling explanation for the cause and variation of gradients of body size in anurans.