It's cool to be stressed: body surface temperatures track sympathetic nervous system activation during acute stress.

The acute stress response can be considered the primary evolutionary adaptation to maximise fitness in the face of unpredictable environmental challenges. However, the difficulties of assessing physiology in natural environments mean that comparatively little is known about how response variation influences fitness in free-living animals. Currently, determining acute stress physiology typically involves blood sampling or cardiac monitoring. Both require trapping and handling, interrupting natural behaviour, and potentially biasing our understanding toward trappable species/individuals. Importantly, limits on repeated sampling also restrict response phenotype characterisation, vital for linking stress with fitness. Surface temperature dynamics resulting from peripheral vasomotor activity during acute stress are increasingly promoted as alternative physiological stress indicators, which can be measured non-invasively using infrared thermal imaging, overcoming many limitations of current methods. Nonetheless, which aspects of stress physiology they represent remains unclear, as the underlying mechanisms are unknown. To date, validations have primarily targeted the hypothalamic-pituitary-adrenal axis, when the sympathetic-adrenal-medullary (SAM) system is likely the primary driver of vasomotor activity during acute stress. To address this deficit, we compared eye and bill region surface temperatures (measured using thermal imaging) with SAM system activity (measured as heart rate variability via electrocardiogram telemetry) in wild-caught captive house sparrows (Passer domesticus) during capture and handling. We found that lower body surface temperatures were associated with increased sympathetic nervous system activation. Consequently, our data confirm that body surface temperatures can act as a proxy for sympathetic activation during acute stress, providing potentially transformative opportunities for linking the acute stress response with fitness in the wild.

Trends and knowledge gaps in field research investigating effects of anthropogenic noise.

Anthropogenic noise is a globally widespread sensory pollutant, recognized as having potentially adverse effects on function, demography, and physiology in wild animals. Human population growth and associated changes in urbanization, transportation, and resource extraction all contribute to anthropogenic noise and are predicted to increase in the coming decades. Wildlife exposure to anthropogenic noise is expected to rise correspondingly. Data collected through field research are uniquely important in advancing understanding of the real-world repercussions of human activity on wildlife. We, therefore, performed a systematic review of literature published from 2008 to 2018 that reported on field investigations of anthropogenic noise impacts. We evaluated publication metrics (e.g., publication rates and journal type), geographical distribution of studies, study subject, and methods used. Research activity increased markedly over the assessment period. However, there was a pronounced geographical bias in research, with most being conducted in North America or Europe, and a notable focus on terrestrial environments. Fewer than one-fifth of terrestrial studies were located in rural areas likely to experience urbanization by 2030, meaning data on ecosystems most likely to be affected by future changes are not being gathered. There was also bias in the taxonomic groups investigated. Most research was conducted on birds and aquatic mammals, whereas terrestrial mammals, reptiles, amphibians, fish, and invertebrates received limited attention. Almost all terrestrial studies examined diurnal species, despite evidence that nocturnality is the prevailing animal activity pattern. Nearly half the studies investigated effects of road or urban noise; the bulk of research was restricted to functional, rather than physiological or demographic consequences. Few experimental studies addressed repercussions of long-term exposure to anthropogenic noise or long-term postexposure effects, and multiple noise types or levels were rarely compared. Tackling these knowledge gaps will be vital for successful management of the effects of increasing wildlife exposure to anthropogenic noise.

Tendencias y Vacíos de Conocimiento en el Trabajo de Campo que Investiga los Efectos del Ruido Antropogénico Resumen El ruido antropogénico es un contaminante sensorial con amplia distribución global. Se le reconoce como un contaminante con efectos adversos potenciales sobre la función, demografía y fisiología de la fauna silvestre. El crecimiento de las poblaciones humanas y los cambios asociados a la urbanización, transporte y extracción de recursos contribuyen al ruido antropogénico y se pronostica que todos incrementarán en las siguientes décadas. Se espera que la exposición de la fauna al ruido antropogénico aumente en correspondencia. Los datos recolectados por medio del trabajo de campo tienen una importancia única en el avance del entendimiento de las repercusiones reales de la actividad humana en la fauna. Por lo tanto realizamos una revisión sistémica de la literatura publicada de 2008 a 2018 en la que se reportaron investigaciones en campo de los impactos del ruido antropogénico. Evaluamos las medidas de publicación (p. ej.: las tasas de publicación y el tipo de revista), la distribución geográfica de los estudios, el sujeto del estudio y los métodos que se utilizaron. La actividad de investigación aumentó de manera marcada a lo largo del periodo de evaluación. Sin embargo, hubo un sesgo geográfico pronunciado en las investigaciones pues la mayoría se realizó en América del Norte o en Europa y hubo un enfoque notable sobre los ambientes terrestres. Menos de la quinta parte de los estudios terrestres estuvieron ubicados en áreas rurales con una probabilidad de sufrir urbanización para el 2030, lo que significa que no se están recopilando datos para los ecosistemas con mayor probabilidad de ser afectados en el futuro. También hubo un sesgo en los grupos taxonómicos investigados. La mayoría de las investigaciones se realizó en aves y en mamíferos acuáticos, mientras que los mamíferos terrestres, los reptiles, los anfibios, los peces y los invertebrados recibieron una atención limitada. Casi todos los estudios terrestres trabajaron con especies diurnas, a pesar de la evidencia existente de que los hábitos nocturnos son el patrón prevaleciente de actividad animal. Casi la mitad de los estudios investigaron los efectos del ruido urbano o de las carreteras; el grueso de las investigaciones estuvo restringido a las consecuencias funcionales y no tanto a las fisiológicas o demográficas. Pocos estudios experimentales trataron el tema de las repercusiones a largo plazo de la exposición al ruido antropogénico o el de los efectos post-exposición a largo plazo. Tampoco encontramos muchos estudios en los que se compararan los tipos o niveles de ruido. Será vital lidiar con estos vacíos de conocimiento para el manejo exitoso de los efectos de la creciente exposición de la fauna al ruido antropogénico.

A comprehensive overview of the effects of urbanisation on sexual selection and sexual traits.

Urbanisation can affect mating opportunities and thereby alter inter- and intra-sexual selection pressures on sexual traits. Biotic and abiotic urban conditions can influence an individual's success in pre- and post-copulatory mating, for example through impacts on mate attraction and mate preference, fertilisation success, resource competition or rival interactions. Divergent sexual selection pressures can lead to differences in behavioural, physiological, morphological or life-history traits between urban and non-urban populations, ultimately driving adaptation and speciation. Most studies on urban sexual selection and mating interactions report differences between urban and non-urban populations or correlations between sexual traits and factors associated with increased urbanisation, such as pollution, food availability and risk of predation and parasitism. Here we review the literature on sexual selection and sexual traits in relation to urbanisation or urban-associated conditions. We provide an extensive list of abiotic and biotic factors that can influence processes involved in mating interactions, such as signal production and transmission, mate choice and mating opportunities. We discuss all relevant data through the lens of two, non-mutually exclusive theories on sexual selection, namely indicator and sensory models. Where possible, we indicate whether these models provide the same or different predictions regarding urban-adapted sexual signals and describe different experimental designs that can be useful for the different models as well as to investigate the drivers of sexual selection. We argue that we lack a good understanding of: (i) the factors driving urban sexual selection; (ii) whether reported changes in traits result in adaptive benefits; and (iii) whether these changes reflect a short-term ecological, or long-term evolutionary response. We highlight that urbanisation provides a unique opportunity to study the process and outcomes of sexual selection, but that this requires a highly integrative approach combining experimental and observational work.

Passing rail traffic reduces bat activity.

Rail transport is expanding, with a global increase in infrastructure of up to one-third predicted by 2050. Greater reliance on rail is expected to benefit the environment at a planetary level, by mitigating transport-related carbon emissions. However, smaller-scale, more direct consequences for wildlife are unclear, as unlike roads, railway impacts on animal ecology are rarely studied. As a group, bats frequently interact with transport networks due to their broad distribution and landscape-scale movements. Additionally, their nocturnality, and use of echolocation mean bats are likely to be affected by light and noise emitted by trains. To investigate whether passing trains affect bat activity levels, we monitored the two most abundant UK species using ultrasonic detectors at 12 wooded rail-side sites in southern England. Activity fell by ≥ 30-50% each time a train passed, for at least two minutes. Consequently, activity was reduced for no less than one-fifth of the time at sites with median rail traffic, and two-thirds or more of the time at the busiest site. Such activity changes imply repeated evasive action and/or exclusion from otherwise favourable environments, with potential for corresponding opportunity or energetic costs. Hence, disturbance by passing trains may disadvantage bats in most rail-side habitats.

Eye region surface temperature dynamics during acute stress relate to baseline glucocorticoids independently of environmental conditions.

Reactions to acute stressors are critical for survival. Yet, the challenges of assessing underlying physiological processes in the field limit our understanding of how variation in the acute stress response relates to fitness in free-living animals. Glucocorticoid secretion during acute stress can be measured from blood plasma concentrations, but each blood sample can only provide information for one point in time. Also, the number of samples that can be extracted from an individual in the field is usually limited to avoid compromising welfare. This restricts capacity for repeated assessment, and therefore temporal resolution of findings within- and between-acute stress responses - both of which are important for determining links between acute stress and fitness. Acute stress induces additional body surface temperature changes that can be measured non-invasively, and at high frequencies using thermal imaging, offering opportunities to overcome these limitations. But, this method's usefulness in the field depends on the extent that environmental conditions affect the body surface temperature response, which remains poorly understood. We assessed the relative importance of individual physiology (baseline glucocorticoid concentrations) and environmental conditions (air temperature and relative humidity) in determining the eye region surface temperature (Teye) response to acute stress, in wild blue tits (Cyanistes caeruleus) during trapping, handling and blood sampling. When controlling for between-individual baseline variation, Teye initially dropped rapidly below, and then recovered above baseline, before declining more slowly until the end of the test, 160 s after trap closure. One measure of the amplitude of this response - the size of the initial drop in Teye - was dependent on environmental conditions, but not baseline corticosterone. Whereas, two properties defining response dynamics - the timing of the initial drop, and the slope of the subsequent recovery - were related to baseline corticosterone concentrations, independently of environmental conditions. This suggests inferring the acute stress response using thermal imaging of Teye will be practical under fluctuating environmental conditions in the field.

Eye region surface temperature reflects both energy reserves and circulating glucocorticoids in a wild bird.

Body temperature of endotherms shows substantial within- and between-individual variation, but the sources of this variation are not fully understood in wild animals. Variation in body temperature can indicate how individuals cope with their environment via metabolic or stress-induced effects, both of which may relate to depletion of energy reserves. Body condition can reflect heat production through changes to metabolic rate made to protect energy reserves. Additionally, changes in metabolic processes may be mediated by stress-related glucocorticoid secretion, which is associated with altered blood-flow patterns that affect regional body temperatures. Accordingly, both body condition and glucocorticoid secretion should relate to body temperature. We used thermal imaging, a novel non-invasive method of temperature measurement, to investigate relationships between body condition, glucocorticoid secretion and body surface temperature in wild blue tits (Cyanistes caeruleus). Individuals with lower body condition had lower eye-region surface temperature in both non-breeding and breeding seasons. Eye-region surface temperature was also negatively correlated with baseline circulating glucocorticoid levels in non-breeding birds. Our results demonstrate that body surface temperature can integrate multiple aspects of physiological state. Consequently, remotely-measured body surface temperature could be used to assess such aspects of physiological state non-invasively in free-living animals at multiple life history stages.

Surface temperature elevated by chronic and intermittent stress.

Stress in homeothermic animals is associated with raised body core temperature and altered patterns of peripheral blood flow. During acute stress, peripheral vasoconstriction causes a short-lived drop in surface temperature that can be detected non-invasively using infrared thermography (IRT). Whether and how skin temperature changes under chronic stress, and hence the potential of IRT in chronic stress detection, is unknown. We explored the impact of withdrawing environmental enrichments and intermittent routine handling on long-term skin temperature in laying hens (Gallus gallus domesticus). Immediately following enrichment withdrawal, comb, face and eye temperature dropped, suggesting this was acutely stressful. In the 3 weeks that followed, barren-housed hens displayed behavioural markers of frustration. Whilst control birds, housed in enriched conditions, showed a decline over weeks in both comb temperature and baseline corticosterone levels, barren-housed hens had no change in comb temperature and an increase in corticosterone. By the trial end, comb temperature (but not corticosterone) was significantly higher in barren-housed hens. This change in parameters over time may reflect cumulative impacts of enrichment withdrawal in barren pens and/or, as hens were young and maturing, age-related changes in controls. Comb, face and eye temperature were also higher on days following routine handling, and comb temperature higher on other days in hens that were regularly handled for blood sampling than for a less intensive weighing protocol. Together, these data support comb, face and eye surface temperature increase as a long-term marker of stress exposure in laying hens. It is important to recognise that the strength and even direction of these effects may vary with thermoregulatory and energetic context. However, in laboratory and indoor-reared farm animals that live in carefully managed environments, IRT of the skin can potentially be used to non-invasively monitor chronic and intermittent stress exposure.

Thermal Imaging to Study Stress Non-invasively in Unrestrained Birds.

Stress, a central concept in biology, describes a suite of emergency responses to challenges. Among other responses, stress leads to a change in blood flow that results in a net influx of blood to key organs and an increase in core temperature. This stress-induced hyperthermia is used to assess stress. However, measuring core temperature is invasive. As blood flow is redirected to the core, the periphery of the body can cool. This paper describes a protocol where peripheral body temperature is measured non-invasively in wild blue tits (Cyanistes caeruleus) using infrared thermography. In the field we created a set-up bringing the birds to an ideal position in front of the camera by using a baited box. The camera takes a short thermal video recording of the undisturbed bird before applying a mild stressor (closing the box and therefore capturing the bird), and the bird's response to being trapped is recorded. The bare skin of the eye-region is the warmest area in the image. This allows an automated extraction of the maximum eye-region temperature from each image frame, followed by further steps of manual data filtering removing the most common sources of errors (motion blur, blinking). This protocol provides a time series of eye-region temperature with a fine temporal resolution that allows us to study the dynamics of the stress response non-invasively. Further work needs to demonstrate the usefulness of the method to assess stress, for instance to investigate whether eye-region temperature response is proportional to the strength of the stressor. If this can be confirmed, it will provide a valuable alternative method of stress assessment in animals and will be useful to a wide range of researchers from ecologists, conservation biologists, physiologists to animal welfare researchers.

Skin temperature reveals the intensity of acute stress.

Acute stress triggers peripheral vasoconstriction, causing a rapid, short-term drop in skin temperature in homeotherms. We tested, for the first time, whether this response has the potential to quantify stress, by exhibiting proportionality with stressor intensity. We used established behavioural and hormonal markers: activity level and corticosterone level, to validate a mild and more severe form of an acute restraint stressor in hens (Gallus gallus domesticus). We then used infrared thermography (IRT) to non-invasively collect continuous temperature measurements following exposure to these two intensities of acute handling stress. In the comb and wattle, two skin regions with a known thermoregulatory role, stressor intensity predicted the extent of initial skin cooling, and also the occurrence of a more delayed skin warming, providing two opportunities to quantify stress. With the present, cost-effective availability of IRT technology, this non-invasive and continuous method of stress assessment in unrestrained animals has the potential to become common practice in pure and applied research.