Coevolution between heat and cold tolerance in endotherms.

Whether the heat and cold tolerance of endotherms evolve independently or correlatively remains unresolved. Both physiological trade-offs and natural selection can contribute to a coevolutionary pattern of heat and cold tolerance in endotherms. Using a published database, we tested the correlation between upper and lower thermal limits across endothermic species with multi-response generalized linear mixed models incorporating phylogenies. We found a positive correlation between upper and lower thermal limits, which suggested a coevolutionary pattern of heat and cold tolerance. Specifically, this relationship between heat and cold tolerance is phylogenetically constrained for tropical endotherms but not for temperate endotherms. The correlated evolution between heat and cold tolerance may have a significant influence on endotherms' evolution and ecology and needs to be further investigated.

Equivocal support for the climate variability hypothesis within a Neotropical bird assemblage.

The climate variability hypothesis posits that an organism's exposure to temperature variability determines the breadth of its thermal tolerance and has become an important framework for understanding variation in species' susceptibilities to climate change. For example, ectotherms from more thermally stable environments tend to have narrower thermal tolerances and greater sensitivity to projected climate warming. Among endotherms, however, the relationship between climate variability and thermal physiology is less clear, particularly with regard to microclimate variation-small-scale differences within or between habitats. To address this gap, we explored associations between two sources of temperature variation (habitat type and vertical forest stratum) and (1) thermal physiological traits and (2) temperature sensitivity metrics within a diverse assemblage of Neotropical birds (n = 89 species). We used long-term temperature data to establish that daily temperature regimes in open habitats and forest canopy were both hotter and more variable than those in the forest interior and forest understory, respectively. Despite these differences in temperature regime, however, we found little evidence that species' thermal physiological traits or temperature sensitivity varied in association with either habitat type or vertical stratum. Our findings provide two novel and important insights. First, and in contrast to the supporting empirical evidence from ectotherms, the thermal physiology of birds at our study site appears to be largely decoupled from local temperature variation, providing equivocal support for the climate variability hypothesis in endotherms. Second, we found no evidence that the thermal physiology of understory forest birds differed from that of canopy or open-habitat species-an oft-invoked, yet previously untested, mechanism for why these species are so vulnerable to environmental change.

How birds dissipate heat before, during and after flight.

Animal flight uses metabolic energy at a higher rate than any other mode of locomotion. A relatively small proportion of the metabolic energy is converted into mechanical power; the remainder is given off as heat. Effective heat dissipation is necessary to avoid hyperthermia. In this study, we measured surface temperatures in lovebirds (Agapornis personatus) using infrared thermography and used heat transfer modelling to calculate heat dissipation by convection, radiation and conduction, before, during and after flight. The total non-evaporative rate of heat dissipation in flying birds was 12× higher than before flight and 19× higher than after flight. During flight, heat was largely dissipated by forced convection, via the exposed ventral wing areas, resulting in lower surface temperatures compared with birds at rest. When perched, both before and after exercise, the head and trunk were the main areas involved in dissipating heat. The surface temperature of the legs increased with flight duration and remained high on landing, suggesting that there was an increase in the flow of warmer blood to this region during and after flight. The methodology developed in this study to investigate how birds thermoregulate during flight could be used in future studies to assess the impact of climate change on the behavioural ecology of birds, particularly those species undertaking migratory flights.

The allometry of mitochondrial efficiency is tissue dependent: a comparison between skeletal and cardiac muscles of birds.

Body mass is known to be a fundamental driver of many biological traits, including metabolism. However, the effect of body mass on mitochondrial energy transduction is still poorly understood and has mainly been described in mammals. Using 13 species of birds ranging from 15 g (finches) to 160 kg (ostrich), we report here that the mitochondrial production of ATP, and the corresponding oxygen consumption, are negatively dependent on body mass in skeletal muscles but not in the heart. Results also showed that mitochondrial efficiency was positively correlated with body mass at sub-maximal phosphorylating states in the skeletal muscle, but not in the heart. This difference between muscle tissues is potentially linked to the difference in energetic demand expandability and the heavy involvement of skeletal muscle in thermoregulation.

Effect of physiological hyperthermia on mitochondrial fuel selection in skeletal muscle of birds and mammals.

Both birds and mammals have important thermogenic capacities allowing them to maintain high body temperatures, i.e., 37 °C and 40 °C on average in mammals and birds, respectively. However, during periods of high locomotor activity, the energy released during muscular contraction can lead to muscle temperature reaching up to 43-44 °C. Mitochondria are responsible for producing the majority of ATP through cellular respiration and metabolizing different substrates, including carbohydrates and lipids, to generate ATP. A limited number of studies comparing avian and mammalian species showed preferential utilization of specific substrates for mitochondrial energy at different metabolic intensities, but authors always measured at body temperature. The present study evaluated mitochondrial respiration rates and OXPHOS coupling efficiencies at 37 °C, 40 °C and 43 °C associated with pyruvate/malate (carbohydrate metabolism) or palmitoyl-carnitine/malate (lipid metabolism) as substrates in pigeons (Columba livia) and rats (Rattus norvegicus), a well-known pair in scientific literature and for their similar body mass. The data show different hyperthermia-induced responses between the two species with (i) skeletal muscle mitochondria from rats being more sensitive to rising temperatures than in pigeons, and (ii) the two species having different substrate preferences during hyperthermia, with rats oxidizing preferentially carbohydrates and pigeons lipids. By analyzing the interplay between temperature and substrate utilization, we describe a means by which endotherms deal with extreme muscular temperatures to provide enough ATP to support energy demands.

An evaluation of a biophysical model for predicting avian thermoregulation in the heat.

Survival and reproduction of endotherms depend on their ability to balance energy and water exchange with their environment, avoiding lethal deficits and maximising gains for growth and reproduction. At high environmental temperatures, diurnal endotherms maintain body temperature (Tb) below lethal limits via physiological and behavioural adjustments. Accurate models of these processes are crucial for predicting effects of climate variability on avifauna. We evaluated the performance of a biophysical model (NicheMapR) for predicting evaporative water loss (EWL), resting metabolic rate (RMR) and Tb at environmental temperatures approaching or exceeding normothermic Tb for three arid-zone birds: southern yellow-billed hornbill (Tockus leucomelas), southern pied babbler (Turdoides bicolor) and southern fiscal (Lanius collaris). We simulated metabolic chamber conditions and compared model outputs with thermal physiology data collected at air temperatures (Tair) between 10 and 50°C. Additionally, we determined the minimum data needed to accurately model diurnal birds' thermoregulatory responses to Tair using sensitivity analyses. Predicted EWL, metabolic rate and Tb corresponded tightly with observed values across Tair, with only minor discrepancies for EWL in two species at Tair≈35°C. Importantly, the model captured responses at Tair=30-40°C, a range spanning threshold values for sublethal fitness costs associated with sustained hot weather in arid-zone birds. Our findings confirm how taxon-specific parameters together with biologically relevant morphological data can accurately model avian thermoregulatory responses to heat. Biophysical models can be used as a non-invasive way to predict species' sensitivity to climate, accounting for organismal (e.g. physiology) and environmental factors (e.g. microclimates).

Temperature, size and developmental plasticity in birds.

As temperatures increase, there is growing evidence that species across much of the tree of life are getting smaller. These climate change-driven size reductions are often interpreted as a temporal analogue of the observation that individuals within a species tend to be smaller in the warmer parts of the species' range. For ectotherms, there has been a broad effort to understand the role of developmental plasticity in temperature-size relationships, but in endotherms, this mechanism has received relatively little attention in favour of selection-based explanations. We review the evidence for a role of developmental plasticity in warming-driven size reductions in birds and highlight insulin-like growth factors as a potential mechanism underlying plastic responses to temperature in endotherms. We find that, as with ectotherms, changes in temperature during development can result in shifts in body size in birds, with size reductions associated with warmer temperatures being the most frequent association. This suggests developmental plasticity may be an important, but largely overlooked, mechanism underlying warming-driven size reductions in endotherms. Plasticity and natural selection have very different constraining forces, thus understanding the mechanism linking temperature and body size in endotherms has broad implications for predicting future impacts of climate change on biodiversity.

Understanding the relationship between dispersal and range size.

The drivers of variability in species range sizes remain an outstanding enigma in ecology. The theoretical expectation of a positive dispersal-range size relationship has received mixed empirical support, despite dispersal being one of the most prominent hypothesised predictors of range size. Here, we synthesised results from 86 studies examining the dispersal-range size relationship for plants and animals in marine, terrestrial and freshwater realms. Overall, our meta-analysis showed that dispersal positively affects range size, but its effect is dependent on the clade and dispersal proxy studied. Moreover, despite potential differences in habitat connectivity, we did not find an effect of realm on the dispersal-range size relationship. Finally, the strength of the dispersal-range size relationship was dependent on latitude, range size metric and the taxonomic breadth of the study clade. Our synthesis emphasizes the importance of developing a mechanistic understanding of the trait to dispersal to range size relationship, considering the complexity of dispersal departure, transfer and settlement, as well as evolutionary components such as time for range expansion, speciation and past geological-environmental dynamics. We, therefore, call for a more integrative view of the dispersal process and its causal relationship with range size.

Mononucleotide A-repeats may Play a Regulatory Role in Endothermic Housekeeping Genes.

Background: Coding and non-coding short tandem repeats (STRs) facilitate a great diversity of phenotypic traits. The imbalance of mononucleotide A-repeats around transcription start sites (TSSs) was found in 3 mammals: H. sapiens, M. musculus, and R. norvegicus. Principal Findings: We found that the imbalance pattern originated in some vertebrates. A similar pattern was observed in mammals and birds, but not in amphibians and reptiles. We proposed that the enriched A-repeats upstream of TSSs is a novel hallmark of endotherms or warm-blooded animals. Gene ontology analysis indicates that the primary function of upstream A-repeats involves metabolism, cellular transportation, and sensory perception (smell and chemical stimulus) through housekeeping genes. Conclusions: Upstream A-repeats may play a regulatory role in the metabolic process of endothermic animals.

Diving physiology of marine mammals and birds: the development of biologging techniques.

In the 1940s, Scholander and Irving revealed fundamental physiological responses to forced diving of marine mammals and birds, setting the stage for the study of diving physiology. Since then, diving physiology research has moved from the laboratory to the field. Modern biologging, with the development of microprocessor technology, recorder memory capacity and battery life, has advanced and expanded investigations of the diving physiology of marine mammals and birds. This review describes a brief history of the start of field diving physiology investigations, including the invention of the time depth recorder, and then tracks the use of biologging studies in four key diving physiology topics: heart rate, blood flow, body temperature and oxygen store management. Investigations of diving heart rates in cetaceans and O2 store management in diving emperor penguins are highlighted to emphasize the value of diving physiology biologging research. The review concludes with current challenges, remaining diving physiology questions and what technologies are needed to advance the field. This article is part of the theme issue 'Measuring physiology in free-living animals (Part I)'.

Food intake: an overlooked driver of climate change casualties?

Reduced voluntary food intake is a common response of endotherms to warmer temperatures. However, the implications of this are rarely considered for wild animals exposed to higher temperatures caused by climate change. We provide a conceptual model to demonstrate the potential consequences of elevated temperatures on food intake and survival.

Climate impacts on organisms, ecosystems and human societies: integrating OCLTT into a wider context.

Physiological studies contribute to a cause and effect understanding of ecological patterns under climate change and identify the scope and limits of adaptation. Across most habitats, this requires analyzing organism responses to warming, which can be modified by other drivers such as acidification and oxygen loss in aquatic environments or excess humidity or drought on land. Experimental findings support the hypothesis that the width and temperature range of thermal performance curves relate to biogeographical range. Current warming causes range shifts, hypothesized to include constraints in aerobic power budget which in turn are elicited by limitations in oxygen supply capacity in relation to demand. Different metabolic scopes involved may set the borders of both the fundamental niche (at standard metabolic rate) and the realized niche (at routine rate). Relative scopes for aerobic performance also set the capacity of species to interact with others at the ecosystem level. Niche limits and widths are shifting and probably interdependent across life stages, with young adults being least thermally vulnerable. The principles of thermal tolerance and performance may also apply to endotherms including humans, their habitat and human society. Overall, phylogenetically based comparisons would need to consider the life cycle of species as well as organism functional properties across climate zones and time scales. This Review concludes with a perspective on how mechanism-based understanding allows scrutinizing often simplified modeling approaches projecting future climate impacts and risks for aquatic and terrestrial ecosystems. It also emphasizes the usefulness of a consensus-building process among experimentalists for better recognition in the climate debate.

Dechlorane Plus Biomagnification and Transmission through Prairie Food Webs in Inner Mongolia, China.

Dechlorane Plus (DP) is found widely in the environment. It is important to study DP enrichment and biomagnification in terrestrial ecosystems to improve our understanding of the possible effects of DP on the environment and human health. A total of 90 samples, including plant and animal tissues, were collected from Xilingol Prairie in Inner Mongolia, China. The DP concentrations in different species were assessed, and transmission of DP through food webs containing ectotherms and endotherms was assessed. The compound was detected in the biotic samples (plant; range 0.133-0.422 ng/g dry wt), in animal muscle (range: not dected-5.70 ng/g lipid wt), and in animal hair (range: not dected-2.03 ng/g dry wt), indicating that DP is present in remote environments such as Xilingol Prairie. These findings suggest that DP can undergo long-distance transport in the environment. Biomagnification factors (ectotherms: range 0.146-88.0, endotherms: range 0.866-17.2) and anti-DP/total DP concentration ratios (fanti values of 0.412-0.787) for the prairie animals were calculated. Ectotherms were found to selectively enrich syn-DP, and stereoselective enrichment increased moving up the food web. Lower-trophic-level endotherms strongly stereoselectively enriched syn-DP, and higher-trophic-level endotherms stereoselectively enriched anti-DP. Environ Toxicol Chem 2021;40:413-421. © 2020 SETAC.

Comparison of natural and pharmacological hypothermia in animals: Determination of activation energy of metabolism.

The constancy of the activation energy of metabolism (E) for all living organisms is one of the most impressive, though controversial, statements of the modern metabolic theory of evolution. According to WBE-theory suggested by West, Brown, and Enquist, E should be in the range from -0.6 to -0.7 eV. However, there are many examples of significant deviations of E from the predictions of the theory. Now we have conducted a study of this value using rats in different types of pharmacological hypothermia: 1. Short-term (for several hours) hypothermia induced by anesthetic xylazine; 2. Daily torpor-like state induced by the pharmacological composition developed in our previous study. It has been found that in pharmacological daily hypothermia E = -0.56 ± 0.03 eV, which was close to that in daily heterotherms found in literature, E = -0.57 ± 0.04 eV. In short-term hypothermia E was substantially lower, E = -0.17 ± 0.071 eV. Our analysis revealed that in short-term hypothermia, changes in body temperature may lag behind changes in metabolic rate for a period Δt, affecting E. We propose an approach for estimating Δt and obtaining an adjusted E = -0.68 ± 0.17 eV, which corresponds to theoretical predictions. We assume that a similar consideration of Δt should be done when calculating E of daily heterotherms. We assume that in ectotherms, when the ambient temperature changes rapidly, changes in metabolic rate may lag behind changes in body temperature for a period (-) Δt, that should also be considered in E calculations. The proposed approach may contribute to the further development of the metabolic theory of evolution and may be useful in comparing artificial and natural hypothermia, as well as in studying the energy transformations in ecosystems.

On the Interplay among Ambient Temperature, Basal Metabolic Rate, and Body Mass.

One of the most generalized conclusions arising from studies analyzing the ecological variation of energy metabolism in endotherms is the apparent negative correlation between ambient temperature and mass-independent basal metabolic rate (residual BMR). As a consequence, ambient temperature has been considered the most important external factor driving the evolution of residual BMR. It is not clear, however, whether this relationship is size dependent, and artifacts such as the biased sampling of body masses in physiological data sets could cause us to overstate the ubiquity of the relationship. Accordingly, here we used published data on body mass (mb), BMR, and annual mean temperature (Tmean) for 458 mammal species (and/or subspecies) to examine the size dependence of the relationship between temperature and BMR. We found a significant interaction between mb and Tmean as predictors of residual BMR, such that the effect of Tmean on residual BMR decreases as a function of mb. In line with this, the amount of residual variance in BMR explained by Tmean decreased with increasing mb, from 20%-30% at body sizes of less than 100 g to almost 0 at body sizes greater than 1,000 g. These data suggest that our current understanding of the importance of broad-scale variation in ambient temperature as a driver of metabolic evolution in endotherms probably is affected by the large number of small species in both nature and physiological data sets.

Ambient temperature-mediated changes in hepatic gene expression of a mammalian herbivore (Neotoma lepida).

Herbivores regularly ingest natural toxins produced by plants as a defence against herbivory. Recent work suggests that compound toxicity is exacerbated at higher ambient temperatures. This phenomenon, known as temperature-dependent toxicity (TDT), is the likely result of decreased liver function at warmer temperatures; however, the underlying cause of TDT remains speculative. In the present study, we compared the effects of temperature and dietary plant toxins on differential gene expression in the liver of an herbivorous rodent (Neotoma lepida), using species-specific microarrays. Expression profiles revealed a greater number of differentially expressed genes at an ambient temperature below the thermal neutral zone for N. lepida (22°C) compared to one within (27°C). Genes and pathways upregulated at 22°C were related to growth and biosynthesis, whereas those upregulated at 27°C were associated with gluconeogenesis, apoptosis and protein misfolding, suggestive of a stressed state for the liver. Additionally, few genes associated with xenobiotic metabolism were induced when woodrats ingested plant toxins compared to nontoxic diets, regardless of temperature. Taken together, the results highlight the important role of ambient temperature on gene expression profiles in the desert woodrat. Temperatures just below the thermal neutral zone might be a favourable state for liver metabolism. Furthermore, the reduction in the number of genes expressed at a temperature within the thermal neutral zone indicates that liver function may be reduced at temperatures that are not typically considered as thermally stressful. Understanding how herbivorous mammals will respond to ambient temperature is imperative to accurately predict the impacts of climate change.

How low can you go? An adaptive energetic framework for interpreting basal metabolic rate variation in endotherms.

Adaptive explanations for both high and low body mass-independent basal metabolic rate (BMR) in endotherms are pervasive in evolutionary physiology, but arguments implying a direct adaptive benefit of high BMR are troublesome from an energetic standpoint. Here, we argue that conclusions about the adaptive benefit of BMR need to be interpreted, first and foremost, in terms of energetics, with particular attention to physiological traits on which natural selection is directly acting. We further argue from an energetic perspective that selection should always act to reduce BMR (i.e., maintenance costs) to the lowest level possible under prevailing environmental or ecological demands, so that high BMR per se is not directly adaptive. We emphasize the argument that high BMR arises as a correlated response to direct selection on other physiological traits associated with high ecological or environmental costs, such as daily energy expenditure (DEE) or capacities for activity or thermogenesis. High BMR thus represents elevated maintenance costs required to support energetically demanding lifestyles, including living in harsh environments. BMR is generally low under conditions of relaxed selection on energy demands for high metabolic capacities (e.g., thermoregulation, activity) or conditions promoting energy conservation. Under these conditions, we argue that selection can act directly to reduce BMR. We contend that, as a general rule, BMR should always be as low as environmental or ecological conditions permit, allowing energy to be allocated for other functions. Studies addressing relative reaction norms and response times to fluctuating environmental or ecological demands for BMR, DEE, and metabolic capacities and the fitness consequences of variation in BMR and other metabolic traits are needed to better delineate organismal metabolic responses to environmental or ecological selective forces.

Accelerated body size evolution during cold climatic periods in the Cenozoic.

How ecological and morphological diversity accumulates over geological time is much debated. Adaptive radiation theory has been successful in testing the effects of biotic interactions on the rapid divergence of phenotypes within a clade, but this theory ignores abiotic effects. The role of abiotic drivers on the tempo of phenotypic evolution has been tested only in a few lineages or small clades from the fossil record. Here, we develop a phylogenetic comparative framework for testing if and how clade-wide rates of phenotypic evolution vary with abiotic drivers. We apply this approach to comprehensive bird and mammal phylogenies, body size data for 9,465 extant species, and global average temperature trends over the Cenozoic. Across birds and mammals, we find that the rate of body size evolution is primarily driven by past climate. Unexpectedly, evolutionary rates are inferred to be higher during periods of cold rather than warm climates in most groups, suggesting that temperature influences evolutionary rates by modifying selective pressures rather than through its effect on energy availability and metabolism. The effect of climate on the rate of body size evolution seems to be a general feature of endotherm evolution, regardless of wide differences in species' ecology and evolutionary history. These results suggest that climatic changes played a major role in shaping species' evolution in the past and could also play a major role in shaping their evolution in the future.

Ambient temperature influences tolerance to plant secondary compounds in a mammalian herbivore.

Growing evidence suggests that plant secondary compounds (PSCs) ingested by mammals become more toxic at elevated ambient temperatures, a phenomenon known as temperature-dependent toxicity. We investigated temperature-dependent toxicity in the desert woodrat (Neotoma lepida), a herbivorous rodent that naturally encounters PSCs in creosote bush (Larrea tridentata), which is a major component of its diet. First, we determined the maximum dose of creosote resin ingested by woodrats at warm (28-29°C) or cool (21-22°C) temperatures. Second, we controlled the daily dose of creosote resin ingested at warm, cool and room (25°C) temperatures, and measured persistence in feeding trials. At the warm temperature, woodrats ingested significantly less creosote resin; their maximum dose was two-thirds that of animals at the cool temperature. Moreover, woodrats at warm and room temperatures could not persist on the same dose of creosote resin as woodrats at the cool temperature. Our findings demonstrate that warmer temperatures reduce PSC intake and tolerance in herbivorous rodents, highlighting the potentially adverse consequences of temperature-dependent toxicity. These results will advance the field of herbivore ecology and may hone predictions of mammalian responses to climate change.