Endotherms trade body temperature regulation for the stress response.

Responding to perceived threats is energetically expensive and can require animals to curtail somatic repair, immunity, and even reproduction to balance energy ledgers. In birds and mammals, energetic demands of thermoregulation are often immense, yet whether homeostatic body temperatures are also compromised to aid the stress response is not known. Using data sourced from over 60 years of literature and 24 endotherm species, we show that exposure to non-thermal challenges (e.g. human interaction, social threats) caused body temperatures to decrease in the cold and increase in the warmth, but particularly when species-specific costs of thermoregulation were high and surplus energy low. Biophysical models revealed that allowing body temperature to change in this way liberated up to 24% (mean = 5%) of resting energy expenditure for use towards coping. While useful to avoid energetic overload, these responses nevertheless heighten risks of cold- or heat-induced damage, particularly when coincident with cold- or heatwaves.

Within-Generation and Transgenerational Plasticity of a Temperate Salmonid in Response to Thermal Acclimation and Acute Temperature Stress.

AbstractThe rise in temperature associated with climate change may threaten the persistence of stenothermal organisms with limited capacities for beneficial thermal acclimation. We investigated the capacity for within-generation and transgenerational thermal responses in brook trout (Salvelinus fontinalis), a cold-adapted salmonid. Adult fish were acclimated to temperatures within (10°C) and above (21°C) their thermal optimum for 6 mo before spawning, then mated in a full factorial breeding design to produce offspring from cold- and warm-acclimated parents and bidirectional crosses between parents from both temperature treatments. Offspring from families were subdivided and reared at two acclimation temperatures representing their current (15°C) and anticipated future (19°C) habitat temperatures. Offspring thermal physiology was measured as the rate of oxygen consumption (Mo2) during an acute change in temperature (increase of 2°C h-1) to observe their Mo2-temperature relationship. We recorded resting Mo2, peak (highest achieved, thermally induced) Mo2, and critical thermal maximum (CTM) as performance metrics. Although limited, within-generation plasticity was greater than transgenerational plasticity, with offspring warm acclimation elevating CTM by 0.5°C but slightly lowering peak thermally induced Mo2. Transgenerational plasticity was evident as a slightly elevated resting Mo2 and a shift of the Mo2-temperature relationship to higher rates overall in offspring from warm-acclimated parents. Furthermore, offspring whose parents were warm acclimated were in worse condition than those whose parents were cold acclimated. Both parents contributed to offspring thermal responses; however, the paternal effect was stronger. Despite the existence of within-generation and transgenerational plasticity in brook trout, it is unlikely that these will be sufficient for coping with long-term changes to environmental temperatures.

Stress-induced changes in body surface temperature are repeatable, but do not differ between urban and rural birds.

Urbanisation can alter local microclimates, thus creating new thermal challenges for resident species. However, urban environments also present residents with frequent, novel stressors (e.g., noise, human interaction) which may demand investment in costly, self-preserving responses (e.g., the fight-or-flight response). One way that urban residents might cope with this combination of demands is by using regional heterothermy to reduce costs of thermoregulation during the stress response. In this study, we used black-capped chickadees (nurban = 9; nrural = 10) to test whether known heterothermic responses to stress exposure (here, at the bare skin around the eye): (1) varied consistently among individuals (i.e., were repeatable), and (2) were most pronounced among urban individuals compared with rural individuals. Further, to gather evidence for selection on stress-induced heterothermic responses in urban settings, we tested: (3) whether repeatability of this response was lower among birds sampled from urban environments compared with those sampled from rural environments. For the first time, we show that heterothermic responses to stress exposures (i.e. changes in body surface temperature) were highly repeatable across chronic time periods (R = 0.58) but not acute time periods (R = 0.13). However, we also show that these responses did not differ between urban and rural birds, nor were our repeatability estimates any lower in our urban sample. Thus, while regional heterothermy during stress exposure may provide energetic benefits to some, but not all, individuals, enhanced use of this response to cope with urban pressures appears unlikely in our study species.

Using mass spectrometry to investigate fluorescent compounds in squirrel fur.

While an array of taxa are capable of producing fluorescent pigments, fluorescence in mammals is a novel and poorly understood phenomenon. A first step towards understanding the potential adaptive functions of fluorescence in mammals is to develop an understanding of fluorescent compounds, or fluorophores, that are present in fluorescent tissue. Here we use Fourier transform-ion cyclotron resonance mass spectrometry (FT-ICR MS) of flying squirrel fur known to fluoresce under ultraviolet (UV) light to identify potentially fluorescent compounds in squirrel fur. All of the potentially fluorescent compounds we identified were either present in non-fluorescent fur or were not present in all species of fluorescent flying squirrel. Therefore, we suggest that the compounds responsible for fluorescence in flying squirrels may also be present in non-fluorescent mammal fur. Some currently unexplained factor likely leads to excitation of fluorophores in flying squirrel fur. A recently suggested hypothesis that fluorescence in mammals is widely caused by porphyrins is consistent with our findings.

Changes in Body Surface Temperature Play an Underappreciated Role in the Avian Immune Response.

AbstractFever and hypothermia are well-characterized components of systemic inflammation. However, our knowledge of the mechanisms underlying such changes in body temperature is largely limited to rodent models and other mammalian species. In mammals, high dosages of an inflammatory agent (e.g., lipopolysaccharide [LPS]) typically leads to hypothermia (decrease in body temperature below normothermic levels), which is largely driven by a reduction in thermogenesis and not changes in peripheral vasomotion (i.e., changes in blood vessel tone). In birds, however, hypothermia occurs frequently, even at lower dosages, but the thermoeffector mechanisms associated with the response remain unknown. We immune challenged zebra finches (Taeniopygia guttata) with LPS, monitored changes in subcutaneous temperature and energy balance (i.e., body mass, food intake), and assessed surface temperatures of and heat loss across the eye region, bill, and legs. We hypothesized that if birds employ thermoregulatory mechanisms similar to those of similarly sized mammals, LPS-injected individuals would reduce subcutaneous body temperature and maintain constant surface temperatures compared with saline-injected individuals. Instead, LPS-injected individuals showed a slight elevation in body temperature, and this response coincided with a reduction in peripheral heat loss, particularly across the legs, as opposed to changes in energy balance. However, we note that our interpretations should be taken with caution owing to small sample sizes within each treatment. We suggest that peripheral vasomotion, allowing for heat retention, is an underappreciated component of the sickness-induced thermoregulatory response of small birds.

New migration and distribution patterns of Atlantic walruses (Odobenus rosmarus rosmarus) around Nunavik (Québec, Canada) identified using Inuit Knowledge.

Environmental changes are affecting the Arctic at an unprecedented rate, but limited scientific knowledge exists on their impacts on species such as walruses (Odobenus rosmarus). Inuit Traditional and Local Ecological Knowledge (Inuit TEK/LEK) held by Inuit walrus harvesters could shed light on walrus ecology and related environmental changes. Our main objective was to study spatial and temporal changes in Atlantic walrus (Odobenus rosmarus rosmarus) distribution in Nunavik (northern Québec, Canada) using Inuit TEK/LEK. To do so, we documented the knowledge and observations of 33 local hunters and Elders as part of a larger project on Atlantic walruses in Nunavik. We first gathered information on changes in Inuit land use patterns and harvesting practices through time and space, which was a crucial step to avoid potential biases in interpreting local observations on walrus distribution. We found that walrus hunters are now covering smaller hunting areas over shorter time periods, reducing in space and time their observations of Atlantic walruses around Nunavik. While clearly taking these limitations into account, we learned from interviews that some areas abandoned by Atlantic walruses in the past were now being re-occupied. Importantly, Atlantic walruses, which migrate following the melting ice, are now traveling along the eastern coast of Nunavik one month earlier, suggesting that Atlantic walrus migration has changed due to variations in sea-ice coverage around Nunavik. Our study not only highlighted important changes in Atlantic walrus distribution and migration in Nunavik, but also sheds light on the importance of documenting temporal and spatial changes in Inuit land use patterns and harvesting practices to understand the ecology of Arctic species using Inuit Knowledge. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00300-021-02920-6.

Body temperature is a repeatable trait in a free-ranging passerine bird.

Body temperature (Tb) affects animal function through its influence on rates of biochemical and biophysical reactions, the molecular structures of proteins and tissues, and, ultimately, organismal performance. Despite its importance in driving physiological processes, there are few data on how much variation in Tb exists within populations of organisms, and whether this variation consistently differs among individuals over time (i.e. repeatability of a trait). Here, using thermal radio-frequency identification implants, we quantified the repeatability of Tb, both in the context of a fixed average environment (∼21°C) and across ambient temperatures (6-31°C), in a free-living population of tree swallows (Tachycineta bicolor, n=16). By experimentally trimming the ventral plumage of a subset of female swallows (n=8), we also asked whether the repeatability of Tb is influenced by the capacity to dissipate body heat. We found that both female and male tree swallow Tb was repeatable at 21°C (R=0.89-92), but female Tb was less repeatable than male Tb across ambient temperature (Rfemale=0.10, Rmale=0.58), which may be due to differences in parental investment. Trimmed birds had on average lower Tb than control birds (by ∼0.5°C), but the repeatability of female Tb did not differ as a function of heat dissipation capacity. This suggests that trimmed individuals adjusted their Tb to account for the effects of heat loss on Tb. Our study provides a first critical step toward understanding whether Tb is responsive to natural selection, and for predicting how animal populations will respond to climatic warming.

Infrared thermography as a technique to measure physiological stress in birds: Body region and image angle matter.

In vertebrates, changes in surface temperature following exposure to an acute stressor are thought to be promising indicators of the physiological stress response that may be captured noninvasively by infrared thermography. However, the efficacy of using stress-induced changes in surface temperature as indicators of physiological stress-responsiveness requires: (1) an understanding of how such responses vary across the body, (2) a magnitude of local, stress-induced thermal responses that is large enough to discriminate and quantify differences among individuals with conventional technologies, and (3) knowledge of how susceptible measurements across different body regions are to systematic error. In birds, temperature of the bare tissues surrounding the eye (the periorbital, or "eye," region) and covering the bill have each been speculated as possible predictors of stress physiological state. Using the domestic pigeon (Columba livia domestica; n = 9), we show that stress-induced changes in surface temperature are most pronounced at the bill and that thermal responses at only the bill have sufficient resolution to detect and quantify differences in responsiveness among individuals. More importantly, we show that surface temperature estimates at the eye region experience greater error due to changes in bird orientation than those at the bill. Such error concealed detection of stress-induced thermal responses at the eye region. Our results highlight that: (1) in some species, bill temperature may serve as a more robust indicator of autonomic stress-responsiveness than eye region temperature, and (2) future studies should account for spatial orientation of study individuals if inference is to be drawn from infrared thermographic images.

Limited transgenerational effects of environmental temperatures on thermal performance of a cold-adapted salmonid.

The capacity of ectotherms to cope with rising temperatures associated with climate change is a significant conservation concern as the rate of warming is likely too rapid to allow for adaptative responses in many populations. Transgenerational plasticity (TGP), if present, could potentially buffer some of the negative impacts of warming on future generations. We examined TGP in lake trout to assess their inter-generational potential to cope with anticipated warming. We acclimated adult lake trout to cold (10°C) or warm (17°C) temperatures for several months, then bred them to produce offspring from parents within a temperature treatment (cold-acclimated and warm-acclimated parents) and between temperature treatments (i.e. reciprocal crosses). At the fry stage, offspring were also acclimated to cold (11°C) or warm (15°C) temperatures. Thermal performance was assessed by measuring their critical thermal maximum (CTM) and the change in metabolic rate during an acute temperature challenge. From this dataset, we also determined their resting and peak (highest achieved, thermally induced) metabolic rates. There was little variation in offspring CTM or peak metabolic rate, although cold-acclimated offspring from warm-acclimated parents exhibited elevated resting metabolic rates without a corresponding increase in mass or condition factor, suggesting that transgenerational effects can be detrimental when parent and offspring environments mismatch. These results suggest that the limited TGP in thermal performance of lake trout is unlikely to significantly influence population responses to projected increases in environmental temperatures.

One hundred research questions in conservation physiology for generating actionable evidence to inform conservation policy and practice.

Environmental change and biodiversity loss are but two of the complex challenges facing conservation practitioners and policy makers. Relevant and robust scientific knowledge is critical for providing decision-makers with the actionable evidence needed to inform conservation decisions. In the Anthropocene, science that leads to meaningful improvements in biodiversity conservation, restoration and management is desperately needed. Conservation Physiology has emerged as a discipline that is well-positioned to identify the mechanisms underpinning population declines, predict responses to environmental change and test different in situ and ex situ conservation interventions for diverse taxa and ecosystems. Here we present a consensus list of 10 priority research themes. Within each theme we identify specific research questions (100 in total), answers to which will address conservation problems and should improve the management of biological resources. The themes frame a set of research questions related to the following: (i) adaptation and phenotypic plasticity; (ii) human-induced environmental change; (iii) human-wildlife interactions; (iv) invasive species; (v) methods, biomarkers and monitoring; (vi) policy, engagement and communication; (vii) pollution; (viii) restoration actions; (ix) threatened species; and (x) urban systems. The themes and questions will hopefully guide and inspire researchers while also helping to demonstrate to practitioners and policy makers the many ways in which physiology can help to support their decisions.

Experimental evidence that hyperthermia limits offspring provisioning in a temperate-breeding bird.

In many vertebrates, parental care can require long bouts of daily exercise that can span several weeks. Exercise, especially in the heat, raises body temperature, and can lead to hyperthermia. Typical strategies for regulating body temperature during endurance exercise include modifying performance to avoid hyperthermia (anticipatory regulation) and allowing body temperature to rise above normothermic levels for brief periods of time (facultative hyperthermia). Facultative hyperthermia is commonly employed by desert birds to economize on water, but this strategy may also be important for chick-rearing birds to avoid reducing offspring provisioning when thermoregulatory demands are high. In this study, we tested how chick-rearing birds balance their own body temperature against the need to provision dependent offspring. We experimentally increased the heat dissipation capacity of breeding female tree swallows (Tachycineta bicolor) by trimming their ventral feathers and remotely monitored provisioning rates, body temperature and the probability of hyperthermia. Birds with an experimentally increased capacity to dissipate heat (i.e. trimmed treatment) maintained higher feeding rates than controls at high ambient temperatures (greater than or equal to 25°C), while maintaining lower body temperatures. However, at the highest temperatures (greater than or equal to 25°C), trimmed individuals became hyperthermic. These results provide evidence that chick-rearing tree swallows use both anticipatory regulation and facultative hyperthermia during endurance performance. With rising global temperatures, individuals may need to increase their frequency of facultative hyperthermia to maintain nestling provisioning, and thereby maximize reproductive success.

Maternal glucocorticoid levels during incubation predict breeding success, but not reproductive investment, in a free-ranging bird.

The hormone corticosterone (CORT) has been hypothesized to be linked with fitness, but the directionality of the relationship is unclear. The 'CORT-fitness hypothesis' proposes that high levels of CORT arise from challenging environmental conditions, resulting in lower reproductive success (a negative relationship). In contrast, the CORT-adaptation hypothesis suggests that, during energetically demanding periods, CORT will mediate physiological or behavioral changes that result in increased reproductive investment and success (a positive relationship). During two breeding seasons, we experimentally manipulated circulating CORT levels in female tree swallows (Tachycineta bicolor) prior to egg laying, and measured subsequent reproductive effort, breeding success, and maternal survival. When females were recaptured during egg incubation and again during the nestling stage, the CORT levels were similar among individuals in each treatment group, and maternal treatment had no effect on indices of fitness. By considering variation among females, we found support for the CORT-adaptation hypothesis; there was a significant positive relationship between CORT levels during incubation and hatching and fledging success. During the nestling stage CORT levels were unrelated to any measure of investment or success. Within the environmental context of our study, relationships between maternal glucocorticoid levels and indices of fitness vary across reproductive stages.

Social hierarchy reveals thermoregulatory trade-offs in response to repeated stressors.

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 (Ts), 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 Ts and dry heat loss of social subordinates, but not social dominants, would fall under stress exposure at low ambient temperatures (Ta), and rise under stress exposure at high Ta, 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 Ta gradient (n=30 days/treatment/group), whilst remotely monitoring social interactions and Ts 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 Ts following stress exposure than social dominants (n=8), and (2) stress-induced changes in Ts significantly increased heat conservation at low Ta and heat dissipation at high Ta among social subordinates alone. These results suggest that chickadees adjust their thermoregulatory strategies during stress exposure when resources are limited by ecologically relevant processes.

Reframing conservation physiology to be more inclusive, integrative, relevant and forward-looking: reflections and a horizon scan.

Applying physiological tools, knowledge and concepts to understand conservation problems (i.e. conservation physiology) has become commonplace and confers an ability to understand mechanistic processes, develop predictive models and identify cause-and-effect relationships. Conservation physiology is making contributions to conservation solutions; the number of 'success stories' is growing, but there remain unexplored opportunities for which conservation physiology shows immense promise and has the potential to contribute to major advances in protecting and restoring biodiversity. Here, we consider how conservation physiology has evolved with a focus on reframing the discipline to be more inclusive and integrative. Using a 'horizon scan', we further explore ways in which conservation physiology can be more relevant to pressing conservation issues of today (e.g. addressing the Sustainable Development Goals; delivering science to support the UN Decade on Ecosystem Restoration), as well as more forward-looking to inform emerging issues and policies for tomorrow. Our horizon scan provides evidence that, as the discipline of conservation physiology continues to mature, it provides a wealth of opportunities to promote integration, inclusivity and forward-thinking goals that contribute to achieving conservation gains. To advance environmental management and ecosystem restoration, we need to ensure that the underlying science (such as that generated by conservation physiology) is relevant with accompanying messaging that is straightforward and accessible to end users.

Heat dissipation capacity influences reproductive performance in an aerial insectivore.

Climatic warming is predicted to increase the frequency of extreme weather events, which may reduce an individual's capacity for sustained activity because of thermal limits. We tested whether the risk of overheating may limit parental provisioning of an aerial insectivorous bird in population decline. For many seasonally breeding birds, parents are thought to operate close to an energetic ceiling during the 2-3 week chick-rearing period. The factors determining the ceiling remain unknown, although it may be set by an individual's capacity to dissipate body heat (the heat dissipation limitation hypothesis). Over two breeding seasons we experimentally trimmed the ventral feathers of female tree swallows (Tachycineta bicolor) to provide a thermal window. We then monitored maternal and paternal provisioning rates, nestling growth rates and fledging success. We found the effect of our experimental treatment was context dependent. Females with an enhanced capacity to dissipate heat fed their nestlings at higher rates than controls when conditions were hot, but the reverse was true under cool conditions. Control females and their mates both reduced foraging under hot conditions. In contrast, male partners of trimmed females maintained a constant feeding rate across temperatures, suggesting attempts to match the feeding rate of their partners. On average, nestlings of trimmed females were heavier than controls, but did not have a higher probability of fledging. We suggest that removal of a thermal constraint allowed females to increase provisioning rates, but additionally provided nestlings with a thermal advantage via increased heat transfer during maternal brooding. Our data provide support for the heat dissipation limitation hypothesis and suggest that depending on temperature, heat dissipation capacity can influence reproductive success in aerial insectivores.

No island-effect on glucocorticoid levels for a rodent from a near-shore archipelago.

Island rodents are often larger and live at higher population densities than their mainland counterparts, characteristics that have been referred to as "island syndrome". Island syndrome has been well studied, but few studies have tested for island-mainland differences in stress physiology. We evaluated island syndrome within the context of stress physiology of white-footed mice (Peromyscus leucopus) captured from 11 islands and five mainland sites in Thousand Islands National Park, Ontario, Canada. Stress physiology was evaluated by quantifying corticosterone (a stress biomarker), the primary glucocorticoid in mice, from hair and its related metabolites from fecal samples. White-footed mice captured in this near-shore archipelago did not display characteristics of island syndrome, nor differences in levels of hair corticosterone or fecal corticosterone metabolites compared with mainland mice. We suggest that island white-footed mice experience similar degrees of stress in the Thousand Islands compared with the mainland. Although we did not find evidence of island syndrome or differences in glucocorticoid levels, we identified relationships between internal (sex, body mass) and external (season) factors and our hormonal indices of stress in white-footed mice.

Evidence that stress-induced changes in surface temperature serve a thermoregulatory function.

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.

Exposure of Avian Embryos to Cycling Incubation Temperatures Reduces Adult Bactericidal Ability.

In birds, the temperature at which eggs are incubated shapes many aspects of hatchling phenotype, but long-term effects are less studied. We studied the effect of incubation temperature and pattern on the subsequent development of innate immune function in Japanese quail (Coturnix japonica). We incubated quail eggs in one of three replicated treatments: control (37.5°C), low (36.0°C), and cyclical incubation. The cyclical treatment had the same average temperature as the low-temperature treatment (36.0°C) and an upper temperature that was the same as the control. When individuals were 5, 20, and 55 d of age (i.e., adults), we measured the ability of blood plasma to kill Escherichia coli. Throughout development there was a nonsignificant trend for immune function to be lower in the cycling treatment. In adulthood, however, individuals incubated at cycling temperatures had significantly lower immune function than control birds but did not differ from individuals incubated at constant low temperatures. Males and females responded similarly to the incubation treatment, but females developed a greater plasma bactericidal ability than males. We conclude that variation in innate immune function of adult birds is shaped by temperature fluctuations experienced during incubation.

Impacts of environmental matching on the routine metabolic rate and mass of native and mixed-ancestry brook trout (Salvelinus fontinalis) fry.

The environment an organism experiences during early development can impact its physiology and survival later in life. The objective of this study was to determine if temperatures experienced at embryonic life stages of brook trout (Salvelinus fontinalis) affected mass and routine metabolic rate (RMR) of a subsequent life stage (free-swimming fry). As part of this, we assessed the contributions and importance of hierarchical levels of biological organization [ancestral type (native vs. hatchery-introgressed), population, and family] to variability in mass and RMR of fry. As embryos and alevin, individuals were reared at either natural environmental (5°C) or elevated (9°C) temperatures and then acclimated to either matched or mismatched temperature treatments once yolk sacs were resorbed. Mass differences among fry were strongly influenced by population of origin as well as initial rearing and final acclimation temperatures. Variation in mass-adjusted RMR of fry was also strongly accounted for by source population, acclimation temperature, and individual mass. A significant interaction between population RMR and final acclimation temperature indicated that not all brook trout populations responded the same way to temperature changes. In contrast to expectations, the highest ancestry category (native vs. introgressed) did not significantly influence mass or mass-adjusted RMR.