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.

Temperature-dependent Developmental Plasticity and Its Effects on Allen's and Bergmann's Rules in Endotherms.

Ecogeographical rules, describing common trends in animal form across space and time, have provided key insights into the primary factors driving species diversity on our planet. Among the most well-known ecogeographical rules are Bergmann's rule and Allen's rule, with each correlating ambient temperature to the size and shape of endotherms within a species. In recent years, these two rules have attracted renewed research attention, largely with the goal of understanding how they emerge (e.g., via natural selection or phenotypic plasticity) and, thus, whether they may emerge quickly enough to aid adaptations to a warming world. Yet despite this attention, the precise proximate and ultimate drivers of Bergmann's and Allen's rules remain unresolved. In this conceptual paper, we articulate novel and classic hypotheses for understanding whether and how plastic responses to developmental temperatures might contributed to each rule. Next, we compare over a century of empirical literature surrounding Bergmann's and Allen's rules against our hypotheses to uncover likely avenues by which developmental plasticity might drive temperature-phenotype correlations. Across birds and mammals, studies strongly support developmental plasticity as a driver of Bergmann's and Allen's rules, particularly with regards to Allen's rule. However, plastic contributions toward each rule appear largely non-linear and dependent upon: (1) efficiency of energy use (Bergmann's rule) and (2) thermal advantages (Allen's rule) at given ambient temperatures. These findings suggest that, among endotherms, rapid changes in body shape and size will continue to co-occur with our changing climate, but generalizing the direction of responses across populations is likely naive.

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.

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.

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.