Birds are better at regulating heat loss through their legs than their bills: implications for body shape evolution in response to climate.

Endotherms use their appendages-such as legs, tails, ears and bills-for thermoregulation by controlling blood flow to near-surface blood vessels, conserving heat when it is cold, and dissipating heat in hot conditions. Larger appendages allow greater heat dissipation, and appendage sizes vary latitudinally according to Allen's rule. However, little is known about the relative importance of different appendages for thermoregulation. We investigate physiological control of heat loss via bird bills and legs using infrared thermography of wild birds. Our results demonstrate that birds are less able to regulate heat loss via their bills than their legs. In cold conditions, birds lower their leg surface temperature to below that of their plumage surface, retaining heat at their core. In warm conditions, birds increase their leg surface temperature to above that of their plumage surface, expelling heat. By contrast, bill surface temperature remains approximately 2°C warmer than the plumage surface, indicating consistent heat loss under almost all conditions. Poorer physiological control of heat loss via bird bills likely entails stronger selection for shorter bills in cold climates. This could explain why bird bills show stronger latitudinal size clines than bird legs, with implications for predicting shape-shifting responses to climate change.

Hot crabs with bold choices: Temperature has little impact on behavioural repeatability in Caribbean hermit crabs.

An animal's boldness is generally considered to be influenced by genetic and developmental factors. However, abiotic factors such as temperature have profound effects on the physiology of ectothermic animals, and thus can influence the expression and measurement of this behavioural trait. We examined the relationship between temperature and behaviour in the Caribbean hermit crab (Coenobita clypeatus) using field and lab experiments. Crabs captured in the sun were bolder than crabs captured in the shade, even when measured at a common temperature, which led to bold crabs experiencing higher microhabitat temperatures. In laboratory housed conditions, crabs demonstrated highly repeatable boldness behaviours at all temperatures, and as temperature increased, the mean behavioural latencies decreased across all individuals. Bolder crabs do not seem to rely on an innately higher thermal preference, since there was no association between boldness behaviours and thermal preference in the laboratory. Instead, bolder crabs seem to exploit more open, riskier habitats than shyer crabs. Our results highlight the complex interplay between physiological and ecological factors influencing the behaviour of a widespread and ecologically important ectothermic animal.

Energetic costs of bill heat exchange demonstrate contributions to thermoregulation at high temperatures in toco toucans (Ramphastos toco).

Body temperature regulation under changes in ambient temperature involves adjustments in heat production and heat exchange rates between the animal and the environment. One mechanism involves the modulation of the surface temperature of specific areas of the body through vasomotor adjustment. In homeotherms, this thermoregulatory adjustment is essential for the maintenance of body temperature over a moderate temperature range, known as the thermal neutral zone (TNZ). The bill of the toco toucan (Ramphastos toco) has been described as a highly efficient thermal window and hypothesized to assist in the thermal homeostasis of this bird. Herein, we directly evaluated the contribution of heat exchange through the bill of the toco toucan and role of the bill in the delimitation of the TNZ. To do this, we measured metabolic rate (MR), via oxygen consumption, over a range of ambient temperatures from 0 to 35°C. MR measurements were made in birds with the bill intact and with the bill insulated. The limits of the TNZ did not differ between treatments, ranging from 10.8 to 25.0°C. The MR differed among treatments only at elevated temperatures (30 and 35°C), reaching 0.92±0.11 ml O2 g-1 h-1 (mean±s.d.) for the intact group and 1.13±0.13 ml O2 g-1 h-1 for the insulated group. These results indicate that although heat dissipation through the bill does not contribute significantly to widening of the TNZ, it may well be critically important in assisting body temperature regulation at higher temperatures extending above the upper limit of the TNZ.

Free-living Allen's hummingbirds (Selasphorus sasin) rarely use torpor while nesting.

For reproducing animals, maintaining energy balance despite thermoregulatory challenges is important for surviving and successfully raising offspring. This is especially apparent in small endotherms that exhibit high mass-specific metabolic rates and live in unpredictable environments. Many of these animals use torpor, substantially reducing their metabolic rate and often body temperature to cope with high energetic demands during non-foraging periods. In birds, when the incubating parent uses torpor, the lowered temperatures that thermally sensitive offspring experience could delay development or increase mortality risk. We used thermal imaging to noninvasively explore how nesting female hummingbirds sustain their own energy balance while effectively incubating their eggs and brooding their chicks. We located 67 active Allen's hummingbird (Selasphorus sasin) nests in Los Angeles, California and recorded nightly time-lapse thermal images at 14 of these nests for 108 nights using thermal cameras. We found that nesting females usually avoided entering torpor, with one bird entering deep torpor on two nights (2% of nights), and two other birds possibly using shallow torpor on three nights (3% of nights). We also modeled nightly energetic requirements of a bird experiencing nest temperatures vs. ambient temperature and using torpor or remaining normothermic, using data from similarly-sized broad-billed hummingbirds. Overall, we suggest that the warm environment of the nest, and possibly shallow torpor, help brooding female hummingbirds reduce their own energy requirements while prioritizing the energetic demands of their offspring.

Thermoconforming rays of the star-nosed mole.

The star-nosed mole (Condylura cristata) is renowned for its densely innervated 22 appendage star-like rostrum ('star') specialized for tactile sensation. As a northerly distributed insectivorous mammal exploiting aquatic and terrestrial habitats, these vascularized nasal rays are regularly exposed to cold water and thermally conductive soil, leading us to ask whether the star surface temperature, a proxy for blood flow, conforms to the local ambient temperature to conserve body heat. Alternatively, given the exquisite sensory nature of the star, we posited that the uninsulated rays may be kept warm when foraging to maintain high mechanosensory function. To test these hypotheses, we remotely monitored surface temperatures in wild-caught star-nosed moles. Although the tail acted as a thermal window exhibiting clear vasoconstriction/vasodilation, the star varied passively in surface temperature, with little evidence for thermoregulatory vasomotion. This thermoconforming response may have evolved to minimize conductive heat loss to the water or wet soils when foraging.

Use of crowdsourced images for determining 2D:4D and relationship to pro-environmental variables.

The primary purpose of this study was to examine whether 2D:4D ratios (a putative measure of prenatal androgen exposure) could be determined using participant-submitted hand images. The secondary purpose was to examine whether 2D:4D ratio was associated with pro-environmental behaviors, attitudes, and empathy, given the recent literature linking sex to environmental attitudes and actions. Participants (N = 1065) were asked via an online survey to submit a clear photograph of their right hand, palm side up. Participants also completed a questionnaire to assess (a) demographics, (b) dispositional empathy, and (c) environmental attitudes and behavior. A 2D:4D ratio was calculated for each participant, and the quality of each image was classified as poor, moderate, or good. We then examined the reliability of the 2D:4D image measurements, and the relationship between 2D:4D and our environmental measures. 2D:4D ratios fell somewhat outside of previously reported ranges, but the measurements did show acceptable intra-rater consistency. Although we did not find a sex difference in 2D:4D, we did find a sex by ratio interaction for both empathy and the number of pro-environmental behaviors in which individuals had engaged. Specifically, as 2D:4D ratio increased, males reported lower empathy and less engagement in pro-environmental behaviors, whereas females reported more engagement in pro-environmental behaviors (but no differences in empathy). These findings were contrary to expectations, as we anticipated that greater digit ratios (i.e., feminized) would be associated with greater empathy and pro-environmental behaviors. Overall, the findings of this study present a preliminary examination of the utility of measuring digit ratio with online samples. Furthermore, our results provide information regarding the complex relationship between sex and pro-environmental behaviors. Supplementary Information: The online version contains supplementary material available at 10.1007/s10211-022-00401-5.

Thermal adaptation best explains Bergmann's and Allen's Rules across ecologically diverse shorebirds.

Bergmann's and Allen's rules state that endotherms should be larger and have shorter appendages in cooler climates. However, the drivers of these rules are not clear. Both rules could be explained by adaptation for improved thermoregulation, including plastic responses to temperature in early life. Non-thermal explanations are also plausible as climate impacts other factors that influence size and shape, including starvation risk, predation risk, and foraging ecology. We assess the potential drivers of Bergmann's and Allen's rules in 30 shorebird species using extensive field data (>200,000 observations). We show birds in hot, tropical northern Australia have longer bills and smaller bodies than conspecifics in temperate, southern Australia, conforming with both ecogeographical rules. This pattern is consistent across ecologically diverse species, including migratory birds that spend early life in the Arctic. Our findings best support the hypothesis that thermoregulatory adaptation to warm climates drives latitudinal patterns in shorebird size and shape.

Vocalization-associated respiration patterns: thermography-based monitoring and detection of preparation for calling.

Vocal emission requires coordination with the respiratory system. Monitoring the increase in laryngeal pressure, which is needed for vocal production, allows detection of transitions from quiet respiration to vocalization-supporting respiration. Characterization of these transitions could be used to identify preparation for vocal emission and to examine the probability of it manifesting into an actual vocal production event. Specifically, overlaying the subject's respiration with conspecific calls can highlight events of call initiation and suppression, as a means of signalling coordination and avoiding jamming. Here, we present a thermal imaging-based methodology for synchronized respiration and vocalization monitoring of free-ranging meerkats. The sensitivity of this methodology is sufficient for detecting transient changes in the subject's respiration associated with the exertion of vocal production. The differences in respiration are apparent not only during the vocal output, but also prior to it, marking the potential time frame of the respiratory preparation for calling. A correlation between conspecific calls with elongation of the focal subject's respiration cycles could be related to fluctuations in attention levels or in the motivation to reply. This framework can be used for examining the capability for enhanced respiration control in animals during modulated and complex vocal sequences, detecting 'failed' vocalization attempts and investigating the role of respiration cues in the regulation of vocal interactions.

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.

Climate-associated decline of body condition in a fossorial salamander.

Temperate ectotherms have responded to recent environmental change, likely due to the direct and indirect effects of temperature on key life cycle events. Yet, a substantial number of ectotherms are fossorial, spending the vast majority of their lives in subterranean microhabitats that are assumed to be buffered against environmental change. Here, we examine whether seasonal climatic conditions influence body condition (a measure of general health and vigor), reproductive output, and breeding phenology in a northern population of fossorial salamander (Spotted Salamander, Ambystoma maculatum). We found that breeding body condition declined over a 12-year monitoring period (2008-2019) with warmer summer and autumn temperatures at least partly responsible for the observed decline in body condition. Our findings are consistent with the hypothesis that elevated metabolism drives the negative association between temperature and condition. Population-level reproduction, assessed via egg mass counts, showed high interannual variation and was weakly influenced by autumn temperatures. Salamander breeding phenology was strongly correlated with lake ice melt but showed no long-term temporal trend (1986-2019). Climatic warming in the region, which has been and is forecasted to be strongest in the summer and autumn, is predicted to lead to a 5%-27% decline in salamander body condition under realistic near-future climate scenarios. Although the subterranean environment offers a thermal buffer, the observed decline in condition and relatively strong effect of summer temperature on body condition suggest that fossorial salamanders are sensitive to the effects of a warming climate. Given the diversity of fossorial taxa, heightened attention to the vulnerability of subterranean microhabitat refugia and their inhabitants is warranted amid global climatic change.

Naked mole-rat brown fat thermogenesis is diminished during hypoxia through a rapid decrease in UCP1.

Naked mole-rats are among the most hypoxia-tolerant mammals. During hypoxia, their body temperature (Tb) decreases via unknown mechanisms to conserve energy. In small mammals, non-shivering thermogenesis in brown adipose tissue (BAT) is critical to Tb regulation; therefore, we hypothesize that hypoxia decreases naked mole-rat BAT thermogenesis. To test this, we measure changes in Tb during normoxia and hypoxia (7% O2; 1-3 h). We report that interscapular thermogenesis is high in normoxia but ceases during hypoxia, and Tb decreases. Furthermore, in BAT from animals treated in hypoxia, UCP1 and mitochondrial complexes I-V protein expression rapidly decrease, while mitochondria undergo fission, and apoptosis and mitophagy are inhibited. Finally, UCP1 expression decreases in hypoxia in three other social African mole-rat species, but not a solitary species. These findings suggest that the ability to rapidly down-regulate thermogenesis to conserve oxygen in hypoxia may have evolved preferentially in social species.

Shape-shifting: changing animal morphologies as a response to climatic warming.

Many animal appendages, such as avian beaks and mammalian ears, can be used to dissipate excess body heat. Allen's rule, wherein animals in warmer climates have larger appendages to facilitate more efficient heat exchange, reflects this. We find that there is widespread evidence of 'shape-shifting' (changes in appendage size) in endotherms in response to climate change and its associated climatic warming. We re-examine studies of morphological change over time within a thermoregulatory context, finding evidence that temperature can be a strong predictor of morphological change independently of, or combined with, other environmental changes. Last, we discuss how Allen's rule, the degree of temperature change, and other ecological factors facilitate morphological change and make predictions about what animals will show shape-shifting.

Bearded dragons (Pogona vitticeps) with reduced scalation lose water faster but do not have substantially different thermal preferences.

Whether scales reduce cutaneous evaporative water loss in lepidosaur reptiles (Superorder Lepidosauria) such as lizards and snakes has been a contentious issue for nearly half a century. Furthermore, while many studies have looked at whether dehydration affects thermal preference in lepidosaurs, far fewer have examined whether normally hydrated lepidosaurs can assess their instantaneous rate of evaporative water loss and adjust their thermal preference to compensate in an adaptive manner. We tested both of these hypotheses using three captive-bred phenotypes of bearded dragon (Pogona vitticeps) sourced from the pet trade: 'wild-types' with normal scalation, 'leatherbacks' exhibiting scales of reduced prominence, and scaleless bearded dragons referred to as 'silkbacks'. Silkbacks on average lost water evaporatively at about twice the rate that wild-types did. Leatherbacks on average were closer in their rates of evaporative water loss to silkbacks than they were to wild-types. Additionally, very small (at most ∼1°C) differences in thermal preference existed between the three phenotypes that were not statistically significant. This suggests a lack of plasticity in thermal preference in response to an increase in the rate of evaporative water loss, and may be reflective of a thermal 'strategy' as employed by thermoregulating bearded dragons that prioritises immediate thermal benefits over the threat of future dehydration. The results of this study bolster an often-discounted hypothesis regarding the present adaptive function of scales and have implications for the applied fields of animal welfare and conservation.

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.

Hot and covered: how dragons face the heat and thermoregulate.

Regulating body temperature is a critical function for many animals. Ectotherms use multiple thermoregulatory behaviours, including habitat selection, sun-shade shuttling, posture, orientation, gaping, and panting. According to thermoregulatory control theory, gaping and postural behaviours should act in coordination with microhabitat selection, providing a fine-tuned counterbalance to more costly behaviours. However, gaping and panting have also been considered indicators of stress in lizards, which would counter a homeostatic thermoregulatory interpretation, especially during expression of voluntary behaviours. Careful adjustments in rostral orientation toward warmth have been observed in bearded dragons, analogous to well-described solar gain and solar avoidance postures in the wild. Little is known about the sensory drivers of these behaviours. Although skin temperature changes faster than core, it is not uniform across the body, and is subject to evaporative cooling, and thus could be crucial to directing behavioural thermoregulatory decision making. To examine the subtle coordination between thermoregulatory behaviours, and to test if inhibiting gaping would lead to thermoregulatory compensatory behaviours, bearded dragon lizards (Pogona vitticeps) were allowed to behaviourally thermoregulate, while their ability to show spontaneous gaping behaviour was disrupted non-pharmacologically. Gaping acted in concert with thermoregulatory behaviours, although at lower rates than predicted from earlier steady-state models, suggesting that respiratory cooling mechanisms are perceived as costly. Bearded dragons enhanced their rostral orientation to heat when gaping was inhibited, while reducing their selected temperatures in a thermal gradient. Combined, these observations indicate the presence of coordination between these various thermoregulatory behaviours.

Activity analysis of thermal imaging videos using a difference imaging approach.

Infrared thermal imaging is a passive imaging technique that captures the emitted radiation from an object to estimate surface temperature, often for inference of heat transfer. Infrared thermal imaging offers the potential to detect movement without the challenges of glare, shadows, or changes in lighting associated with visual digital imaging or active infrared imaging. In this paper, we employ a frame subtraction algorithm for extracting the pixel-by-pixel relative change in signal from a fixed focus video file, tailored for use with thermal imaging videos. By summing the absolute differences across an entire video, we are able to assign quantitative activity assessments to thermal imaging data for comparison with simultaneous recordings of metabolic rates. We tested the accuracy and limits of this approach by analyzing movement of a metronome and provide an example application of the approach to a study of Darwin's finches. In principle, this "Difference Imaging Thermography" (DIT) would allow for activity data to be standardized to energetic measurements and could be applied to any radiometric imaging system.

Hydrogen sulfide exposure reduces thermal set point in zebrafish.

Behavioural flexibility allows ectotherms to exploit the environment to govern their metabolic physiology, including in response to environmental stress. Hydrogen sulfide (H2S) is a widespread environmental toxin that can lethally inhibit metabolism. However, H2S can also alter behaviour and physiology, including a hypothesized induction of hibernation-like states characterized by downward shifts of the innate thermal set point (anapyrexia). Support for this hypothesis has proved controversial because it is difficult to isolate active and passive components of thermoregulation, especially in animals with high resting metabolic heat production. Here, we directly test this hypothesis by leveraging the natural behavioural thermoregulatory drive of fish to move between environments of different temperatures in accordance with their current physiological state and thermal preference. We observed a decrease in adult zebrafish (Danio rerio) preferred body temperature with exposure to 0.02% H2S, which we interpret as a shift in the thermal set point. Individuals exhibited consistent differences in shuttling behaviour and preferred temperatures, which were reduced by a constant temperature magnitude during H2S exposure. Seeking lower temperatures alleviated H2S-induced metabolic stress, as measured by reduced rates of aquatic surface respiration. Our findings highlight the interactions between individual variation and sublethal impacts of environmental toxins on behaviour.