Intra and interspecific variation in thermal performance and critical limits in anurans from southern Chile.

The relationship between temperature and performance can be illustrated through a thermal performance curve (TPC), which has proven useful in describing various aspects of ectotherms' thermal ecology and evolution. The parameters of the TPC can vary geographically due to large-scale variations in environmental conditions. However, only some studies have attempted to quantify how thermal performance varies over relatively small spatial scales, even in the same location or consistently among individuals within a species. Here, we quantified individual and species variation in thermal sensitivity of locomotor performance in five amphibia Eupsophus species found in the temperate rainforests of southern Chile and compared their estimates against co-occurring species that exhibit a substantially more extensive distributional range. We measured critical thermal limits and jumping performance under five different temperatures. Our results suggest that thermal responses are relatively conserved along the phylogeny, as the locomotor performance and thermal windows for activity remained narrow in Eupsophus species when compared against results observed for Batrachyla taeniata and Rhinella spinulosa. Additionally, we found significant individual differences in locomotor performance within most species, with individual consistency in performance observed across varied temperatures. Further analyses explored the influence of body size on locomotor performance and critical thermal limits within and between species. Our results suggest a trade-off scenario between thermal tolerance breadth and locomotor performance, where species exhibiting broader thermal ranges might have compromised performance. Interestingly, these traits seem partly mediated by body size variations, raising questions about potential ecological implications.

Nor climate nor human impact factors: Chytrid infection shapes the skin bacterial communities of an endemic amphibian in a biodiversity hotspot.

The bacterial communities of the amphibian skin (i.e., the bacteriome) are critical to the host's innate immune system. However, it is unclear how different drivers can alter this function by modulating the bacteriome's structure. Our aim was to assess the extent to which different host attributes and extrinsic factors influence the structure of the bacterial communities of the skin. Skin bacterial diversity was examined in 148 individuals of the four-eyed frog (Pleurodema thaul) from 16 localities spanning almost 1800 km in latitude. The richness and beta diversity of bacterial families and the richness and abundance of Bd-inhibitory bacterial genera were used to describe their structure. Predictors associated with the host (developmental stage, genetic lineage, individual Batrachochytrium dendrobatidis [Bd] infection status) and the landscape (current climate, degree of anthropogenic disturbance) were used in the statistical modeling in an information theoretical approach. Bd infection and host developmental stage were the only predictors affecting bacteriome richness, with Bd+ individuals and postmetamorphic stages (adults and juveniles) having higher richness than Bd- ones and tadpoles. High diversity in Bd+ individuals is not driven by bacterial genera with known anti-Bd properties. Beta diversity was not affected by Bd infection and was mainly a consequence of bacterial family turnover rather than nestedness. Finally, for those bacterial genera known to have inhibitory effects on chytrid, Bd+ individuals had a slightly higher diversity than Bd- ones. Our study confirms an association between Bd infection and the host developmental stage with the bacterial communities of the skin of P. thaul. Unexpectedly, macroclimate and human impact factors do not seem to play a role in shaping the amphibian skin microbiome. Our study exemplifies that focusing on a single host-parasite system over a large geographic scale can provide essential insights into the factors driving host-parasite-bacteriome interactions.

Mental health and religiosity: the role of experiential avoidance in the symptoms of depression, anxiety, and stress

Several studies have considered religiosity to be a protective factor against several mental health difficulties. However, other studies suggest the opposite, that is, that religiosity is a risk factor associated with psychological symptoms. In this context, there are no studies that evaluate this relationship considering the role of experiential avoidance, which is a predictive transdiagnostic variable of various mental health disorders. This study evaluated the relationship between experiential avoidance, attitudes toward religion, and symptoms of depression, anxiety, and stress in a sample of believers using a non-experimental cross-sectional design in the city of Valdivia, Chile. Results indicate that experiential avoidance is positively related to symptoms of depression, anxiety, and stress, being the only predictor variable of the three symptomatic dimensions. Engaging in regular religious practice was not associated with religious literalness or experiential avoidance, while religious literalism was negatively associated with stress. Finally, Evangelicals showed a more regular religious practice than Catholics, while Catholics showed a higher index of religious literality; however, these differences were not associated with mental health. The clinical implications of these results are discussed (AU)

Interpopulation differences in male reproductive effort drive the population dynamics of a host exposed to an emerging fungal pathogen.

Compensatory recruitment is a key demographic mechanism that has allowed the coexistence of populations of susceptible amphibians with Batrachochytrium dendrobatidis (Bd), a fungus causing one of the most devastating emerging infectious disease ever recorded among vertebrates. However, the underlying processes (e.g. density-dependent increase in survival at early life stages, change in reproductive traits) as well as the level of interpopulation variation in this response are poorly known. We explore potential mechanisms of compensatory recruitment in response to Bd infection by taking advantage of an amphibian system where male reproductive traits are easy to quantify in free-living populations. The Southern Darwin's frog Rhinoderma darwinii is a vocal sac-brooding species that exhibits a high susceptibility to lethal Bd infection. Using a 7-year capture-recapture study at four populations with contrasting Bd infection status (one high prevalence, one low prevalence and two Bd-free populations), we evaluated whether Bd-positive populations exhibited a higher adult recruitment and a higher male reproductive effort than Bd-negative populations. We also estimated population growth rates to explore whether recruitment compensated for the negative impacts of Bd on the survival of adults. In addition, we evaluated a potential demographic signal of compensatory recruitment (i.e. positive relationship between the proportion of juveniles and Bd prevalence) in response to Bd infection using raw count data from 13 R. darwinii populations. The high Bd prevalence population exhibited the highest male reproductive effort and the highest recruitment among the four monitored populations. This led to a growing population during the study period despite high mortality of adult hosts. In contrast, males from the population with low Bd prevalence had a low reproductive effort and this population, which had the lowest adult recruitment, was declining during the study period despite adults having a higher survival in comparison to the high Bd prevalence population. We also found a demographic signal of compensatory recruitment in response to Bd infection in our broader analysis of 13 R. darwinii populations. Our study underlines the importance of interpopulation variation in life-history strategies on the fate of host populations after infectious disease emergence. Our results also suggest that an increase in reproductive effort can be one of the processes underlying compensatory recruitment in populations of Bd-susceptible amphibians.

Bioclimatic and anthropogenic variables shape the occurrence of Batrachochytrium dendrobatidis over a large latitudinal gradient.

Amphibian chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), has caused the greatest known loss of biodiversity due to an infectious disease. We used Bd infection data from quantitative real-time PCR (qPCR) assays of amphibian skin swabs collected across Chile during 2008-2018 to model Bd occurrence with the aim to determine bioclimatic and anthropogenic variables associated with Bd infection. Also, we used Bd presence/absence records to identify geographical Bd high-risk areas and compare Bd prevalence and infection loads between amphibian families, ecoregions, and host ecology. Data comprised 4155 Bd-specific qPCR assays from 162 locations across a latitudinal gradient of 3700 km (18º to 51ºS). Results showed a significant clustering of Bd associated with urban centres and anthropogenically highly disturbed ecosystems in central-south Chile. Both Bd prevalence and Bd infection loads were higher in aquatic than terrestrial amphibian species. Our model indicated positive associations of Bd prevalence with altitude, temperature, precipitation and human-modified landscapes. Also, we found that macroscale drivers, such as land use change and climate, shape the occurrence of Bd at the landscape level. Our study provides with new evidence that can improve the effectiveness of strategies to mitigate biodiversity loss due to amphibian chytridiomycosis.

Could plasticity mediate highlands lizards' resilience to climate change? A case study of the leopard iguana (Diplolaemus leopardinus) in Central Andes of Argentina.

The predicted rise of global temperatures is of major concern for ectotherms because of its direct impact on their behavior and physiology. As physiological performance mediates a species' resilience to warming exposure, physiological plasticity could greatly reduce the susceptibility to climate change. We studied the degree to which Diplolaemus leopardinus lizards are able to adjust behavioral and physiological traits in response to short periods of temperature change. We used a split cross design to measure the acclimation response of preferred body temperature (Tp), and the thermal performance curve of resting metabolic rate (RMR) and evaporative water loss (EWL). Our results showed that plasticity differs among traits: whereas Tp and EWL showed lower values in warm conditions, the body temperature at which RMR was highest increased. Moreover, RMR was affected by thermal history, showing a large increase in response to cold exposure in the group initially acclimated to warm temperatures. The reduction of EWL and the increase in optimal temperature will give lizards the potential to partially mitigate the impact of rising temperatures in the energy cost and water balance. However, the decrease in Tp and the sensitivity to the warm thermal history of RMR could be detrimental to the energy net gain, increasing the species' vulnerability, especially considering the increase of heat waves predicted for the next 50 years. The integration of acclimation responses in behavioral and physiological traits provides a better understanding of the range of possible responses of lizards to cope with the upcoming climatic and environmental modifications expected as a result of climate change.

Amphibian responses in experimental thermal gradients: Concepts and limits for inference.

The interpretation of thermal-gradient data depends on the behavioral drives reported or assumed, and on the underlying behavioral models explaining how such drives operate. The best-known example is positive thermotaxis, a thermoregulatory behavioral drive frequently linked to a dual set-point model of thermoregulation around a target range. This behavioral drive is often assumed as dominant among 'ectotherms', including amphibians. However, we argue that, because amphibians are extremely diverse, they may exhibit alternative behavioral drives in thermal gradients, and tackle this idea from two perspectives. First, we provide a historical review of original definitions and proposed limits for inference. Second, although caveats apply, we propose that a cross-study analysis of data of temperature settings of gradients and the temperatures selected by amphibians would corroborate alternative behavioral drives, including negative thermotaxis. Therefore, we analyzed published data focusing on such relationships and show that gradient temperature settings influence the temperatures selected by amphibians, with further effects of phylogeny and ontogeny. We conclude that thermal gradient experiments are outstanding tools to investigate behavioral drives, but no given drive can be assumed a priori unless additional information about thermoregulation is available. Based on the historical debate, we propose using selected temperatures and preferred temperatures as different concepts, the former merely operational and the second explicitly linked to positive thermotaxis (and thus compatible with dual set-point thermoregulation). Under this view, thermal preferences would stand for a hypothesis of a behavioral drive (positive thermotaxis) requiring formal testing. These considerations impact the scope for inference based on thermal gradient experiments, particularly ecological modeling and emerging disease.

Why disease ecology needs life-history theory: a host perspective.

When facing an emerging infectious disease of conservation concern, we often have little information on the nature of the host-parasite interaction to inform management decisions. However, it is becoming increasingly clear that the life-history strategies of host species can be predictive of individual- and population-level responses to infectious disease, even without detailed knowledge on the specifics of the host-parasite interaction. Here, we argue that a deeper integration of life-history theory into disease ecology is timely and necessary to improve our capacity to understand, predict and mitigate the impact of endemic and emerging infectious diseases in wild populations. Using wild vertebrates as an example, we show that host life-history characteristics influence host responses to parasitism at different levels of organisation, from individuals to communities. We also highlight knowledge gaps and future directions for the study of life-history and host responses to parasitism. We conclude by illustrating how this theoretical insight can inform the monitoring and control of infectious diseases in wildlife.

Geography, Temperature, and Water: Interaction Effects in a Small Native Amphibian.

Amphibian locomotor capacity is strongly linked to temperature and hydration. However, organisms in nature experience covariation of multiple environmental factors, and thus to better understand the effects of thermal and hydric conditions on physiological performance, it is critical not only to experimentally disentangle them but also to incorporate potential interactive effects due to geographic variation. To this end, we selected two populations of the small amphibian Pleurodema thaul inhabiting highly contrasting temperatures and precipitation regimens. With these two populations, we evaluated the thermal and hydric sensitivities of locomotor performance. For both factors, performance increased with temperature as well as with hydration level, although performance reached a plateau between 25° and 30°C. In addition, the influence of dehydration on performance was independent of the temperature at which it was tested. Our results also showed that the population from the warmer environment has lower sensitivity of locomotor performance to dehydration, probably as a consequence of thermal adaptation, although further studies might be required to fully understand this.

Shrinking dinosaurs and the evolution of endothermy in birds.

The evolution of endothermy represents a major transition in vertebrate history, yet how and why endothermy evolved in birds and mammals remains controversial. Here, we combine a heat transfer model with theropod body size data to reconstruct the evolution of metabolic rates along the bird stem lineage. Results suggest that a reduction in size constitutes the path of least resistance for endothermy to evolve, maximizing thermal niche expansion while obviating the costs of elevated energy requirements. In this scenario, metabolism would have increased with the miniaturization observed in the Early-Middle Jurassic (~180 to 170 million years ago), resulting in a gradient of metabolic levels in the theropod phylogeny. Whereas basal theropods would exhibit lower metabolic rates, more recent nonavian lineages were likely decent thermoregulators with elevated metabolism. These analyses provide a tentative temporal sequence of the key evolutionary transitions that resulted in the emergence of small, endothermic, feathered flying dinosaurs.

Testing the metabolic homeostasis hypothesis in amphibians.

A number of hypotheses about compensatory mechanisms that allow ectothermic animals to cope with the latitudinal decrease in ambient temperature ( TA) have been proposed during the last century. One of these hypotheses, the 'metabolic homeostasis' hypothesis (MHH), states that species should show the highest thermal sensitivity of the metabolic rate ( Q10-SMR) at the colder end of the range of TAs they usually experience in nature. This way, species should be able to minimize maintenance costs during the colder hours of the day, but quickly take advantage of increases in TA during the warmer parts of the day. Here, we created a dataset that includes Q10-SMR values for 58 amphibian species, assessed at four thermal ranges, to evaluate three predictions derived from the MHH. In line with this hypothesis, we found that: (i) Q10-SMR values tended to be positively correlated with latitude when measured at lower TAs, but negative correlated with latitude when measured at higher TAs, (ii) Q10-SMR measured at lower TAs were higher in temperate species, whereas Q10-SMR measured at higher TAs were higher in tropical species, and (iii) the experimental TA at which Q10-SMR was maximal for each species decreased with latitude. This is the first study to our knowledge showing that the relationship between Q10-SMR and latitude in ectotherms changes with the TA at which Q10-SMR is assessed, as predicted from an adaptive hypothesis. This article is part of the theme issue 'Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen'.

Natural selection on plasticity of thermal traits in a highly seasonal environment.

For ectothermic species with broad geographical distributions, latitudinal/altitudinal variation in environmental temperatures (averages and extremes) is expected to shape the evolution of physiological tolerances and the acclimation capacity (i.e., degree of phenotypic plasticity) of natural populations. This can create geographical gradients of selection in which environments with greater thermal variability (e.g., seasonality) tend to favor individuals that maximize performance across a broader range of temperatures compared to more stable environments. Although thermal acclimation capacity plays a fundamental role in this context, it is unknown whether natural selection targets this trait in natural populations. Additionally, understanding whether and how selection acts on thermal physiological plasticity is also highly relevant to climate change and biological conservation. Here, we addressed such an important gap in our knowledge in the northernmost population of the four-eyed frog, Pleurodema thaul. We measured plastic responses of critical thermal limits for activity, behavioral thermal preference, and thermal sensitivity of metabolism to acclimation at 10 and 20°C. We monitored survival during three separate recapture efforts and used mark-recapture integrated into an information-theoretic approach to evaluate the relationship between survivals as a function of the plasticity of thermal traits. Overall, we found no evidence that thermal acclimation in this population is being targeted by directional selection, although there might be signals of selection on individual traits. According to the most supported models, survival increased in individuals with higher tolerance to cold when cold-acclimated, probably because daily low extremes are frequent during the cooler periods of the year. Furthermore, survival increased with body size. However, in both cases, the directional selection estimates were nonsignificant, and the constraints of our experimental design prevented us from evaluating more complex models (i.e., nonlinear selection).

Thermal physiological traits and plasticity of metabolism are sensitive to biogeographic breaks in a rock-pool marine shrimp.

Populations of broadly distributed species commonly exhibit latitudinal variation in thermal tolerance and physiological plasticity. This variation can be interrupted when biogeographic breaks occur across the range of a species, which are known to affect patterns of community structure, abundance and recruitment dynamics. Coastal biogeographic breaks often impose abrupt changes in environmental characteristics driven by oceanographic processes and can affect the physiological responses of populations inhabiting these areas. Here, we examined thermal limits, performances for heart rate and plasticity in metabolic rate of the intertidal shrimp Betaeus emarginatus from seven populations along its latitudinal range (∼3000 km). The distribution of this species encompass two breaks along the southeastern Pacific coast of Chile: the northern break is characterized by sharp discontinuities in upwelling regimes, and the southern break constitutes a major discontinuity in water conditions (temperature, pH, dissolved oxygen and nutrients), coastline topography and divergence of main oceanographic currents. For B. emarginatus, we found higher plasticity in metabolism at the sites sampled at the biogeographic breaks, and at the site subjected to seasonal upwelling. The variation in metabolic rate was not consistent with increasing latitude and it was not affected by breaks. The lower and upper thermal limits were lower in populations around breaks, although the optimum temperature decreased towards higher latitudes. Overall, whereas thermal limits and plasticity of metabolism are related to biogeographic breaks, metabolic rate is not related to increasing latitude or the presence of breaks in the sampled range.

Intraspecific geographic variation in thermal limits and acclimatory capacity in a wide distributed endemic frog.

Intraspecific variation in physiological traits and the standard metabolic rate (SMR) is common in widely distributed ectotherms since populations at contrasting latitudes experiences different thermal conditions. The climatic variability hypothesis (CVH) states that populations at higher latitudes presents higher acclimation capacity than those at lower latitudes, given the wider range of climatic variability they experience. The endemic four-eyed frog, Pleurodema thaul is widely distributed in Chile. We examined the variation in maximum and minimum critical temperatures (CTmax and CTmin), preferred temperature (TPref), SMR and their acclimatory capacity in two populations from the northern and center of its distribution. All the traits are higher in the warmer population. The capacity for acclimation varies between traits and, with the exception of CTmax and TPref, it is similar between populations. This pattern could be explained by the higher daily thermal variability in desert environments, that increases plasticity to the levels found in the high latitude population. However, we found low acclimatory capacity in all physiological traits, of only about 3% for CTmin, 10% for CTmax and TPref, and 1% for SMR. Thus, despite the fact that Pleurodema thaul possess some ability to adjust thermal tolerances in response to changing thermal conditions, this acclimatory capacity seems to be unable to prevent substantial buffering when body temperatures rise. The low acclimatory capacity found for P. thaul suggests that this species use behavioral rather than physiological adjustments to compensate for environmental variation, by exploiting available micro-environments with more stable thermal conditions.

Exploring physiological plasticity and local thermal adaptation in an intertidal crab along a latitudinal cline.

Intertidal organisms have evolved physiological mechanisms that enable them to maintain performance and survive during periods of severe environmental stress with temperatures close to their tolerance limits. The level of these adaptive responses in thermal physiology can vary among populations of broadly distributed species depending on their particular environmental context and genetic backgrounds. Here we examined thermal performances and reaction norms for metabolic rate (MR) and heart rate (HR) of seven populations of the porcelanid crab Petrolisthes violaceus from markedly different thermal environments across the latitudinal gradient of ~3000km. Physiological responses of this intertidal crab under common-garden conditions suggest the absence of local thermal adaptation along the geographic gradient (i.e., lack of latitudinal compensation). Moreover, thermal physiological sensitivities and performances in response to increased temperatures evidenced the existence of some level of: i) metabolic rate control or depression during warm temperature exposures; and ii) homeostasis/canalization (i.e., absence or low levels of plasticity) in physiological traits that may reflect some sort of buffering mechanism in most of the populations. Nevertheless, our results indicate that elevated temperatures can reduce cardiac function but not metabolic rate in high latitude crabs. The lack of congruence between HR and MR supports the idea that energy metabolism in marine invertebrates cannot be inferred from HR and different conclusions regarding geographic differentiation in energy metabolism can be obtained from both physiological traits. Integrating thermal physiology and species range extent can contribute to a better understanding of the likely effects of climate change on natural populations of marine ectotherms.

Geographical gradients in selection can reveal genetic constraints for evolutionary responses to ocean acidification.

Geographical gradients in selection can shape different genetic architectures in natural populations, reflecting potential genetic constraints for adaptive evolution under climate change. Investigation of natural pH/pCO2 variation in upwelling regions reveals different spatio-temporal patterns of natural selection, generating genetic and phenotypic clines in populations, and potentially leading to local adaptation, relevant to understanding effects of ocean acidification (OA). Strong directional selection, associated with intense and continuous upwellings, may have depleted genetic variation in populations within these upwelling regions, favouring increased tolerances to low pH but with an associated cost in other traits. In contrast, diversifying or weak directional selection in populations with seasonal upwellings or outside major upwelling regions may have resulted in higher genetic variances and the lack of genetic correlations among traits. Testing this hypothesis in geographical regions with similar environmental conditions to those predicted under climate change will build insights into how selection may act in the future and how populations may respond to stressors such as OA.

Spatio-temporal environmental variation mediates geographical differences in phenotypic responses to ocean acidification.

Phenotypic plasticity is expected to play a major adaptive role in the response of species to ocean acidification (OA), by providing broader tolerances to changes in pCO2 conditions. However, tolerances and sensitivities to future OA may differ among populations within a species because of their particular environmental context and genetic backgrounds. Here, using the climatic variability hypothesis (CVH), we explored this conceptual framework in populations of the sea urchin Loxechinus albus across natural fluctuating pCO2/pH environments. Although elevated pCO2 affected the morphology, physiology, development and survival of sea urchin larvae, the magnitude of these effects differed among populations. These differences were consistent with the predictions of the CVH showing greater tolerance to OA in populations experiencing greater local variation in seawater pCO2/pH. Considering geographical differences in plasticity, tolerances and sensitivities to increased pCO2 will provide more accurate predictions for species responses to future OA.

Effects of amphibian phylogeny, climate and human impact on the occurrence of the amphibian-killing chytrid fungus.

Chytridiomycosis, due to the fungus Batrachochytrium dendrobatidis (Bd), has been associated with the alarming decline and extinction crisis of amphibians worldwide. Because conservation programs are implemented locally, it is essential to understand how the complex interactions among host species, climate and human activities contribute to Bd occurrence at regional scales. Using weighted phylogenetic regressions and model selection, we investigated geographic patterns of Bd occurrence along a latitudinal gradient of 1500 km within a biodiversity hot spot in Chile (1845 individuals sampled from 253 sites and representing 24 species), and its association with climatic, socio-demographic and economic variables. Analyses show that Bd prevalence decreases with latitude although it has increased by almost 10% between 2008 and 2013, possibly reflecting an ongoing spread of Bd following the introduction of Xenopus laevis. Occurrence of Bd was higher in regions with high gross domestic product (particularly near developed centers) and with a high variability in rainfall regimes, whereas models including other bioclimatic or geographic variables, including temperature, exhibited substantially lower fit and virtually no support based on Akaike weights. In addition, Bd prevalence exhibited a strong phylogenetic signal, with five species having high numbers of infected individuals and higher prevalence than the average of 13.3% across all species. Taken together, our results highlight that Bd in Chile might still be spreading south, facilitated by a subset of species that seem to play an important epidemiological role maintaining this pathogen in the communities, in combination with climatic and human factors affecting the availability and quality of amphibian breeding sites. This information may be employed to design conservation strategies and mitigate the impacts of Bd in the biodiversity hot spot of southern Chile, and similar studies may prove useful to disentangle the role of different factors contributing to the emergence and spread of this catastrophic disease.

Quantitative Genetic Modeling of the Parental Care Hypothesis for the Evolution of Endothermy.

There are two heuristic explanations proposed for the evolution of endothermy in vertebrates: a correlated response to selection for stable body temperatures, or as a correlated response to increased activity. Parental care has been suggested as a major driving force in this context given its impact on the parents' activity levels and energy budgets, and in the offspring's growth rates due to food provisioning and controlled incubation temperature. This results in a complex scenario involving multiple traits and transgenerational fitness benefits that can be hard to disentangle, quantify and ultimately test. Here we demonstrate how standard quantitative genetic models of maternal effects can be applied to study the evolution of endothermy, focusing on the interplay between daily energy expenditure (DEE) of the mother and growth rates of the offspring. Our model shows that maternal effects can dramatically exacerbate evolutionary responses to selection in comparison to regular univariate models (breeder's equation). This effect would emerge from indirect selection mediated by maternal effects concomitantly with a positive genetic covariance between DEE and growth rates. The multivariate nature of selection, which could favor a higher DEE, higher growth rates or both, might partly explain how high turnover rates were continuously favored in a self-reinforcing process. Overall, our quantitative genetic analysis provides support for the parental care hypothesis for the evolution of endothermy. We contend that much has to be gained from quantifying maternal and developmental effects on metabolic and thermoregulatory variation during adulthood.

Thermoregulation in endotherms: physiological principles and ecological consequences.

In a seminal study published nearly 70 years ago, Scholander et al. (Biol Bull 99:259-271, 1950) employed Newton's law of cooling to describe how metabolic rates (MR) in birds and mammals vary predictably with ambient temperature (T a). Here, we explore the theoretical consequences of Newton's law of cooling and show that a thermoregulatory polygon provides an intuitively simple and yet useful description of thermoregulatory responses in endothermic organisms. This polygon encapsulates the region in which heat production and dissipation are in equilibrium and, therefore, the range of conditions in which thermoregulation is possible. Whereas the typical U-shaped curve describes the relationship between T a and MR at rest, thermoregulatory polygons expand this framework to incorporate the impact of activity, other behaviors and environmental conditions on thermoregulation and energy balance. We discuss how this framework can be employed to study the limits to effective thermoregulation and their ecological repercussions, allometric effects and residual variation in MR and thermal insulation, and how thermoregulatory requirements might constrain locomotor or reproductive performance (as proposed, for instance, by the heat dissipation limit theory). In many systems the limited empirical knowledge on how organismal traits may respond to environmental changes prevents physiological ecology from becoming a fully developed predictive science. In endotherms, however, we contend that the lack of theoretical developments that translate current physiological understanding into formal mechanistic models remains the main impediment to study the ecological and evolutionary repercussions of thermoregulation. In spite of the inherent limitations of Newton's law of cooling as an oversimplified description of the mechanics of heat transfer, we argue that understanding how systems that obey this approximation work can be enlightening on conceptual grounds and relevant as an analytical and predictive tool to study ecological phenomena. As such, the proposed approach may constitute a powerful tool to study the impact of thermoregulatory constraints on variables related to fitness, such as survival and reproductive output, and help elucidating how species will be affected by ongoing climate change.