ABSTRACT At a global scale, thermal physiology is correlated with climatic variables such as temperature and aridity. There is also evidence that thermoregulatory traits vary with fine-scale microclimate, but this has received less attention in endotherms. Here, we test the hypothesis that avian thermoregulation varies with microclimate and behavioural constraints in a non-passerine bird. Male and female southern yellow-billed hornbills ( Tockus leucomelas ) experience markedly different microclimates while breeding, with the female sealing herself into a tree cavity and moulting all her flight feathers during the breeding attempt, becoming entirely reliant on the male for provisioning. We examined interactions between resting metabolic rate (RMR), evaporative water loss (EWL) and core body temperature ( T b ) at air temperatures ( T a ) between 30°C and 52°C in male and female hornbills, and quantified evaporative cooling efficiencies and heat tolerance limits. At thermoneutral T a , neither RMR, EWL nor T b differed between sexes. At T a >40°C, however, RMR and EWL of females were significantly lower than those of males, by ∼13% and ∼17%, respectively, despite similar relationships between T b and T a , maximum ratio of evaporative heat loss to metabolic heat production and heat tolerance limits (∼50°C). These sex-specific differences in hornbill thermoregulation support the hypothesis that avian thermal physiology can vary within species in response to fine-scale microclimatic factors. In addition, Q 10 for RMR varied substantially, with Q 10 ≤2 in some individuals, supporting recent arguments that active metabolic suppression may be an underappreciated aspect of endotherm thermoregulation in the heat.

ABSTRACT Mammals in drylands are facing not only increasing heat loads but also reduced water and food availability as a result of climate change. Insufficient water results in suppression of evaporative cooling and therefore increases in body core temperature on hot days, while lack of food reduces the capacity to maintain body core temperature on cold nights. Both food and water shortage will narrow the prescriptive zone, the ambient temperature range over which body core temperature is held relatively constant, which will lead to increased risk of physiological malfunction and death. Behavioural modifications, such as shifting activity between night and day or seeking thermally buffered microclimates, may allow individuals to remain within the prescriptive zone, but can incur costs, such as reduced foraging or increased competition or predation, with consequences for fitness. Body size will play a major role in predicting response patterns, but identifying all the factors that will contribute to how well dryland mammals facing water and food shortage will cope with increasing heat loads requires a better understanding of the sensitivities and responses of mammals exposed to the direct and indirect effects of climate change.

ABSTRACT If fitness optima for a given trait differ between males and females in a population, sexual dimorphism may evolve. Sex-biased trait variation may affect patterns of habitat use, and if the microhabitats used by each sex have dissimilar microclimates, this can drive sex-specific selection on thermal physiology. Nevertheless, tests of differences between the sexes in thermal physiology are uncommon, and studies linking these differences to microhabitat use or behavior are even rarer. We examined microhabitat use and thermal physiology in two ectothermic congeners that are ecologically similar but differ in their degree of sexual size dimorphism. Brown anoles ( Anolis sagrei ) exhibit male-biased sexual size dimorphism and live in thermally heterogeneous habitats, whereas slender anoles ( Anolis apletophallus ) are sexually monomorphic in body size and live in thermally homogeneous habitats. We hypothesized that differences in habitat use between the sexes would drive sexual divergence in thermal physiology in brown anoles, but not slender anoles, because male and female brown anoles may be exposed to divergent microclimates. We found that male and female brown anoles, but not slender anoles, used perches with different thermal characteristics and were sexually dimorphic in thermal tolerance traits. However, field-active body temperatures and behavior in a laboratory thermal arena did not differ between females and males in either species. Our results suggest that sexual dimorphism in thermal physiology can arise from phenotypic plasticity or sex-specific selection on traits that are linked to thermal tolerance, rather than from direct effects of thermal environments experienced by males and females.

ABSTRACT Incubating birds trade off self-maintenance for keeping eggs warm. This causes lower incubation temperature in more challenging conditions, with consequences for a range of offspring traits. It is not yet clear how low developmental temperature affects cold tolerance early in life. This is ecologically important because before full thermoregulatory capacity is attained, precocial chicks must switch between foraging and being brooded when their body temperature declines. Hence, we studied how cold tolerance during conditions similar to a feeding bout in the wild was affected by incubation temperature in Japanese quail ( Coturnix japonica ). Cold-incubated (35.5°C) chicks took the longest to develop, hatched at a smaller size, and remained smaller during their first week of life compared with chicks incubated at higher temperatures (37.0 and 38.5°C). This was reflected in increased cooling rate and reduced homeothermy, probably on account of reductions in both heat-producing capacity and insulation. Lower cold tolerance could exacerbate other temperature-linked phenotypic effects and, hence, also the trade-off between future and current reproduction from the perspective of the incubating parent.

ABSTRACT Coping with stressors can require substantial energetic investment, and when resources are limited, such investment can preclude simultaneous expenditure on other biological processes. Among endotherms, energetic demands of thermoregulation can also be immense, yet our understanding of whether a stress response is sufficient to induce changes in thermoregulatory investment is limited. Using the black-capped chickadee as a model species, we tested a hypothesis that stress-induced changes in surface temperature ( T s ), a well-documented phenomenon across vertebrates, stem from trade-offs between thermoregulation and stress responsiveness. Because social subordination is known to constrain access to resources in this species, we predicted that T s and dry heat loss of social subordinates, but not social dominants, would fall under stress exposure at low ambient temperatures ( T a ), and rise under stress exposure at high T a , thus permitting a reduction in total energetic expenditure toward thermoregulation. To test our predictions, we exposed four social groups of chickadees to repeated stressors and control conditions across a T a gradient ( n =30 days/treatment/group), whilst remotely monitoring social interactions and T s . Supporting our hypothesis, we show that: (1) social subordinates ( n =12), who fed less than social dominants and alone experienced stress-induced mass-loss, displayed significantly larger changes in T s following stress exposure than social dominants ( n =8), and (2) stress-induced changes in T s significantly increased heat conservation at low T a and heat dissipation at high T a among social subordinates alone. These results suggest that chickadees adjust their thermoregulatory strategies during stress exposure when resources are limited by ecologically relevant processes.

ABSTRACT Insensible evaporative water loss (EWL) at or below thermoneutrality is generally assumed to be a passive physical process. However, some arid zone mammals and a single arid zone bird can control their insensible water loss, so we tested the hypothesis that the same is the case for two parrot species from a mesic habitat. We investigated red-rumped parrots ( Psephotus haematonotus ) and eastern rosellas ( Platycercus eximius ), measuring their EWL, and other physiological variables, at a range of relative humidities at ambient temperatures of 20 and 30°C (below and at thermoneutrality). We found that, despite a decrease in EWL with increasing relative humidity, rates of EWL were not fully accounted for by the water vapour deficit between the animal and its environment, indicating that the insensible EWL of both parrots was controlled. It is unlikely that this deviation from physical expectations was regulation with a primary role for water conservation because our mesic-habitat parrots had equivalent regulatory ability as the arid habitat budgerigar ( Melopsittacus undulatus ). This, together with our observations of body temperature and metabolic rate, instead support the hypothesis that acute physiological control of insensible water loss serves a thermoregulatory purpose for endotherms. Modification of both cutaneous and respiratory avenues of evaporation may be involved, possibly via modification of expired air temperature and humidity, and surface resistance.

ABSTRACT Because most desert-dwelling lizards rely primarily on behavioral thermoregulation for the maintenance of active body temperature, the effectiveness of panting as a thermoregulatory mechanism for evaporative cooling has not been widely explored. We measured changes in body temperature ( T b ) with increasing air temperature ( T a ) for 17 species of lizards that range across New Mexico and Arizona and quantified the temperatures associated with the onset of panting, and the capacity of individuals to depress T b below T a while panting, and estimated the critical thermal maxima (CT max ) for each individual. We examined these variables as a function of phylogeny, body mass and local acclimatization temperature. We found that many species can depress T b 2–3°C below T a while panting, and the capacity to do so appears to be a function of each species' ecology and thermal environment, rather than phylogeny. Panting thresholds and CT max values are phylogenetically conserved within groups. Understanding the functional significance of panting and its potential importance as a thermoregulatory mechanism will improve our understanding of the potential for species' persistence in an increasingly warmer world.

ABSTRACT Flexibility in heat generation and dissipation mechanisms provides endotherms the ability to match their thermoregulatory strategy with external demands. However, the degree to which these two mechanisms account for seasonal changes in body temperature regulation is little explored. Here, we present novel data on the regulation of avian body temperature to investigate how birds alter mechanisms of heat production and heat conservation to deal with variation in ambient conditions. We subjected dark-eyed juncos ( Junco hyemalis ) to chronic cold acclimations of varying duration and subsequently quantified their metabolic rates, thermal conductance and ability to maintain normothermia. Cold-acclimated birds adjusted traits related to both heat generation (increased summit metabolic rate) and heat conservation (decreased conductance) to improve their body temperature regulation. Increases in summit metabolic rate occurred rapidly, but plateaued after 1 week of cold exposure. In contrast, changes to conductance occurred only after 9 weeks of cold exposure. Thus, the ability to maintain body temperature continued to improve throughout the experiment, but the mechanisms underlying this improvement changed through time. Our results demonstrate the ability of birds to adjust thermoregulatory strategies in response to thermal cues and reveal that birds may combine multiple responses to meet the specific demands of their environments.

ABSTRACT It is generally assumed that the body temperature of large animals is less likely to change because of their large body size, resulting in a high thermal inertia and a smaller surface area to volume ratio. The goal of this study was to investigate the stability of body temperature in large fish using data from field experiments. We measured the muscle temperatures of free-ranging whale sharks ( Rhincodon typus ), the largest extant fish globally, and investigated their ectothermic physiology and the stability of their body temperature. The muscle temperature changed substantially more slowly than the water temperature fluctuations associated with vertical movements, and the whole-body heat-transfer coefficients (HTCs) of whale sharks estimated using heat-budget models were lower than those of any other fish species measured to date. The heat-budget models also showed that internal heat production does not contribute to changes in muscle temperature. A comparative analysis showed that the HTC at cooling in various fish species including both ectothermic and endothermic species ranging from 10 −4 to 10 3 kg was proportional to body mass −0.63 . This allometry was present regardless of whether the fish were ectothermic or endothermic, and was an extension of the relationship observed in previous studies on small fish. Thus, large fish have the advantage of body temperature stability while moving in environments with large temperature variations. Our results suggest that the large body size of whale sharks aids in preventing a decrease in body temperature during deep excursions to more than 1000 m depths without high metabolic costs of producing heat.

ABSTRACT Animals in seasonal environments must prudently manage energy expenditure to survive the winter. This may be achieved through reductions in the allocation of energy for various purposes (e.g. thermoregulation, locomotion, etc.). We studied whether such trade-offs also include suppression of the innate immune response, by subjecting captive male Svalbard ptarmigan ( Lagopus muta hyperborea ) to bacterial lipopolysaccharide (LPS) during exposure to either mild temperature (0°C) or cold snaps (acute exposure to −20°C), in constant winter darkness when birds were in energy-conserving mode, and in constant daylight in spring. The innate immune response was mostly unaffected by temperature. However, energy expenditure was below baseline when birds were immune challenged in winter, but significantly above baseline in spring. This suggests that the energetic component of the innate immune response was reduced in winter, possibly contributing to energy conservation. Immunological parameters decreased (agglutination, lysis, bacteriostatic capacity) or did not change (haptoglobin/PIT54) after the challenge, and behavioural modifications (anorexia, mass loss) were lengthy (9 days). While we did not study the mechanisms explaining these weak, or slow, responses, it is tempting to speculate they may reflect the consequences of having evolved in an environment where pathogen transmission rate is presumably low for most of the year. This is an important consideration if climate change and increased exploitation of the Arctic would alter pathogen communities at a pace outwith counter-adaption in wildlife.

ABSTRACT During winter at temperate and high latitudes, the low ambient temperatures, limited food supplies and short foraging periods mean small passerines show behavioural, morphological and physiological adaptations to reduce the risk of facing energy shortages. Peripheral tissues vasoconstrict in low ambient temperatures to reduce heat loss and cold injury. Peripheral vasoconstriction has been observed with food restriction in captivity but has yet to be explored in free-ranging animals. We experimentally food restricted both wild and captive great tits ( Parus major ) during winter months and measured surface temperatures of the bill and eye region using thermal imaging, to investigate whether birds show rapid local heterothermic responses, which may reduce their thermoregulatory costs when facing a perceived imminent food shortage. Our results of a continuously filmed wild population showed that bill temperature was immediately reduced in response to food restriction compared with when food was available ad libitum , an apparent autonomic response. Such immediacy implies a ‘pre-emptive’ response before the bird experiences any shortfalls in energy reserves. We also demonstrate temporal variation in vasoconstriction of the bill, with bill temperature gradually rising throughout the food restriction after the initial drop. Eye-region temperature in the wild birds remained at similar levels throughout food restriction compared with unrestricted birds, possibly reflecting the need to maintain steady circulation to the central nervous and visual systems. Our findings provide evidence that birds selectively allow the bill to cool when a predictable food supply is suddenly disrupted, probably as a means of minimising depletion of body reserves for a perceived future shortage in energy.

ABSTRACT The capacity to get rid of excess heat produced during hard work is a possible constraint on parental effort during reproduction [heat dissipation limit (HDL) theory]. We released hard-working blue tits ( Cyanistes caeruleus ) from this constraint by experimentally removing ventral plumage. We then assessed whether this changed their reproductive effort (feeding rate and nestling size) and levels of self-maintenance (change in body mass and innate immune function). Feather-clipped females reduced the number of feeding visits and increased levels of constitutive innate immunity compared with unclipped females but did not fledge smaller nestlings. Thus, they increased self-maintenance without compromising current reproductive output. In contrast, feather clipping did not affect the number of feeding visits or innate immune function in males, despite increased heat loss rate. Our results show that analyses of physiological parameters, such as constitutive innate immune function, can be important when trying to understand sources of variation in investment in self-maintenance versus reproductive effort and that risk of overheating can influence innate immune function during reproduction.

ABSTRACT Seasonal changes in maximal thermogenic capacity ( M sum ) in wild black-capped chickadees suggests that adjustments in metabolic performance are slow and begin to take place before winter peaks. However, when mean minimal ambient temperature ( T a ) reaches −10°C, the chickadee phenotype appears to provide enough spare capacity to endure days with colder T a , down to −20°C or below. This suggests that birds could also maintain a higher antioxidant capacity as part of their cold-acclimated phenotype to deal with sudden decreases in temperature. Here, we tested how environmental mismatch affected oxidative stress by comparing cold-acclimated (−5°C) and transition (20°C) phenotypes in chickadees exposed to an acute 15°C drop in temperature with that of control individuals. We measured superoxide dismutase, catalase and glutathione peroxidase activities, as well as lipid peroxidation damage and antioxidant scavenging capacity in pectoralis muscle, brain, intestine and liver. We generally found differences between seasonal phenotypes and across tissues, but no differences with respect to an acute cold drop treatment. Our data suggest oxidative stress is closely matched to whole-animal physiology in cold-acclimated birds compared with transition birds, implying that changes to the oxidative stress system happen slowly.

ABSTRACT The fact that body temperature can rise or fall following exposure to stressors has been known for nearly two millennia; however, the functional value of this phenomenon remains poorly understood. We tested two competing hypotheses to explain stress-induced changes in temperature, with respect to surface tissues. Under the first hypothesis, changes in surface temperature are a consequence of vasoconstriction that occur to attenuate blood loss in the event of injury and serve no functional purpose per se; defined as the ‘haemoprotective hypothesis’. Under the second hypothesis, changes in surface temperature reduce thermoregulatory burdens experienced during activation of a stress response, and thus hold a direct functional value: the ‘thermoprotective hypothesis’. To understand whether stress-induced changes in surface temperature have functional consequences, we tested predictions of these two hypotheses by exposing black-capped chickadees ( n =20) to rotating stressors across an ecologically relevant ambient temperature gradient, while non-invasively monitoring surface temperature (eye region temperature) using infrared thermography. Our results show that individuals exposed to rotating stressors reduce surface temperature and dry heat loss at low ambient temperature and increase surface temperature and dry heat loss at high ambient temperature, when compared with controls. These results support the thermoprotective hypothesis and suggest that changes in surface temperature following stress exposure have functional consequences and are consistent with an adaptation. Such findings emphasize the importance of the thermal environment in shaping physiological responses to stressors in vertebrates, and in doing so, raise questions about their suitability within the context of a changing climate.

ABSTRACT Like all birds, penguins undergo periodic molt, during which they replace old feathers. However, unlike other birds, penguins replace their entire plumage within a short period while fasting ashore. During molt, king penguins ( Aptenodytes patagonicus ) lose half of their initial body mass, most importantly their insulating subcutaneous fat and half of their pectoral muscle mass. The latter might challenge their capacity to generate and sustain a sufficient mechanical power output to swim to distant food sources and propel themselves to great depth for successful prey capture. To investigate the effects of the annual molt fast on their dive/foraging performance, we studied various dive/foraging parameters and peripheral temperature patterns in immature king penguins across two molt cycles, after birds had spent their first and second year at sea, using implanted data-loggers. We found that the dive/foraging performance of immature king penguins was significantly reduced during post-molt foraging trips. Dive and bottom duration for a given depth were shorter during post-molt and post-dive surface interval duration was longer, reducing overall dive efficiency and underwater foraging time. We attribute this decline to the severe physiological changes that birds undergo during their annual molt. Peripheral temperature patterns differed greatly between pre- and post-molt trips, indicating the loss of the insulating subcutaneous fat layer during molt. Peripheral perfusion, as inferred from peripheral temperature, was restricted to short periods at night during pre-molt but occurred throughout extended periods during post-molt, reflecting the need to rapidly deposit an insulating fat layer during the latter period.

ABSTRACT The torpor-assisted migration hypothesis posits that migration is facilitated in bats by the use of torpor during stopover roosting periods, and predicts that at stopover, bats regulate time in torpor facultatively so that daily energy expenditure is independent of ambient roosting temperature. Energy savings can thus be directed to migratory movement. However, direct measurements of total roosting energy expenditure in relation to ambient and body temperature are lacking. We captured migratory silver-haired bats ( Lasionycteris noctivagans ; ∼11 g) at Long Point, ON, Canada, in spring and autumn 2016. We used quantitative magnetic resonance analysis to measure body composition change and energy expenditure over a 12 h roosting period in a ventilated incubator at 10, 17 and 25°C. We assessed the effects of season, body mass, sex and age on energy expenditure. We found that daily energy expenditure was independent of roosting temperature, and that this was achieved by flexible use of torpor. Variation in body mass at capture was driven mainly by differences in fat, and the amount of body fat was negatively related to torpor use, particularly in spring. Season, sex and age also affected torpor use and energy expenditure, notably with pregnant females being generally fatter and using less torpor than males in spring. We estimate that stopover contributes only 15–20% to the total energy costs of migration in bats compared with 70% or more in typical birds. This study provides support for the torpor-assisted migration hypothesis, and furthers our understanding of the energy budgets of migratory bats.

ABSTRACT In severe hypoxia, most vertebrates increase anaerobic energy production, which results in the development of a metabolic acidosis and an O 2 debt that must be repaid during reoxygenation. Naked mole rats (NMRs) are among the most hypoxia-tolerant mammals, capable of drastically reducing their metabolic rate in acute hypoxia while staying active and alert. We hypothesized that a key component of remaining active is an increased reliance on anaerobic metabolism during severe hypoxia. To test this hypothesis, we exposed NMRs to progressive reductions in inspired O 2 (9–3% O 2 ) followed by reoxygenation (21% O 2 ) and measured breathing frequency, heart rate, behavioural activity, body temperature, metabolic rate, and also metabolic substrates and pH in blood and tissues. We found that NMRs exhibit robust metabolic rate depression in acute hypoxia, accompanied by declines in all physiological and behavioural variables examined. However, blood and tissue pH were unchanged, and tissue concentrations of ATP and phosphocreatine were maintained. NMRs increased their reliance on carbohydrates in hypoxia, and glucose was mobilized from the liver to the blood. Upon reoxygenation, NMRs entered into a coma-like state for ∼15–20 min, during which metabolic rate was negligible and body temperature remained suppressed. However, an imbalance in the time taken for the rates of O 2 uptake ( V̇ O 2 ) and CO 2 production ( V̇ CO 2 ) to return to normoxic levels during reoxygenation hint at the possibility that NMRs do utilize anaerobic metabolism during hypoxia but have a tissue and/or blood buffering capacity that masks typical markers of metabolic acidosis, and that the synthesis of glucose from lactate, rather than lactate oxidation, is prioritized during recovery.

ABSTRACT Parasites alter their host behaviour and vice versa as a result of mutual adaptations in the evolutionary arms race. One of these adaptations involves changes in host thermoregulation, which has the potential to harm the parasite and thereby act as a defence mechanism. We used a model of the brown trout ( Salmo trutta ) experimentally parasitised with glochidia ectoparasitic larvae from the endangered freshwater pearl mussel ( Margaritifera margaritifera ) to reveal whether parasitisation alters fish behavioural thermoregulation. A study using radiotelemetry temperature sensors was performed during almost one year of the M. margaritifera parasitic stage. Glochidia-infested S. trutta altered their thermoregulation through active searching for habitats with different thermal regimes. The general preference for temperatures in infested fish varied and was either above or below the temperature preferred by uninfested individuals. Infested fish also preferred different temperatures across localities, whereas uninfested fish maintained their thermal preference no matter which stream they inhabited. Glochidia further induced the expression of a behavioural syndrome among S. trutta personality traits, suggesting that it might increase the probability that the fish host would occur in the glochidia temperature optimum. Our findings present the first evidence that thermoregulation plays a fundamental role in the relationship of affiliated mussels and their fish hosts. Incorporating thermoregulation as a factor in the study of this relationship can help to interpret results from previous behavioural studies, as well as to optimise management measures related to endangered mussels.

ABSTRACT Terrestrial anurans often experience fluctuations in body temperature and hydration state, which are known to influence evaporative water loss through the skin (EWL Skin ) and lungs (EWL Resp ). These effects arise from associated changes in skin permeability, metabolism and lung ventilation. Herein, we determined the rates of EWL Skin and EWL Resp in the terrestrial toad Rhinella diptycha at different temperatures and hydration states. We measured oxygen uptake rates to verify whether alterations in the partitioning between EWL Skin and EWL Resp were associated with metabolism-induced changes in pulmonary gas exchange. We also measured the influence of hydration and temperature on water uptake (WU) through the skin. Finally, as estimates of skin resistance to evaporation ( R s ) are usually inferred from total evaporative water loss (EWL Total ), under the assumption of negligible EWL Resp , we calculated the potential error in accepting this assumption for different temperature and hydration states. EWL Skin and EWL Resp increased with temperature, but this response was greater for EWL Resp , which was attributed to the temperature-induced elevation in metabolism and lung ventilation. Dehydration caused a decrease in the relative contribution of EWL Skin to EWL Total , mirrored by the concurrent increase in the contribution of EWL Resp , at all temperatures. Thus, R s increased with dehydration. WU rates were dictated by dehydration with little influence of temperature. The partitioning between EWL Skin and EWL Resp was affected by both temperature and hydration state and, under some conditions, considering EWL Resp as negligible led to significant errors in the assessment of skin resistance to evaporation.

ABSTRACT Physiological plasticity allows organisms to respond to diverse conditions. However, can being too plastic actually be detrimental? Malagasy common tenrecs, Tenrec ecaudatus , have many plesiomorphic traits and may represent a basal placental mammal. We established a laboratory population of T. ecaudatus and found extreme plasticity in thermoregulation and metabolism, a novel hibernation form, variable annual timing, and remarkable growth and reproductive biology. For instance, tenrec body temperature ( T b ) may approximate ambient temperature to as low as 12°C even when tenrecs are fully active. Conversely, tenrecs can hibernate with T b of 28°C. During the active season, oxygen consumption may vary 25-fold with little or no change in T b . During the austral winter, tenrecs are consistently torpid but the depth of torpor may vary. A righting assay revealed that T b contributes to but does not dictate activity status. Homeostatic processes are not always linked, e.g. a hibernating tenrec experienced a ∼34% decrease in heart rate while maintaining constant body temperature and oxygen consumption rates. Tenrec growth rates vary but young may grow ∼40-fold in the 5 weeks until weaning and may possess indeterminate growth as adults. Despite all of this profound plasticity, tenrecs are surprisingly intolerant of extremes in ambient temperature (<8 or >34°C). We contend that while plasticity may confer numerous energetic advantages in consistently moderate environments, environmental extremes may have limited the success and distribution of plastic basal mammals.