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

Abstract

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.

Body surface temperature responses to food restriction in wild and captive great tits

“…The relatively long duration the bill was at a lower temperature on food restricted days compared to food available days indicates that vasoconstriction of the bill was not driven by an acute stress response triggered by the experiment. If so, we would have expected to see a considerably faster return to before-food restriction values than in this study, based on the timeline of the thermal response to an acute stressor in periorbital skin in the closely related blue tit (Cyanistes caeruleus) (Jerem et al, 2019). This provides evidence for selective vasoconstriction of the bill as opposed to a global drop in peripheral temperature as is expected in response to an acute stressor (e.g., Herborn et al, 2015;Nord and Folkow, 2019;Robertson et al, 2020).…”

What are you actually measuring? A review of techniques that integrate the stress response on distinct time‐scales

“…Stress can increase body temperature, known as hyperthermia (Oka, Oka, & Hori, 2001). These increases can occur in as little as 10 s (Bouwknecht, Olivier, & Paylor, 2007; Jerem, Jenni‐Eiermann, McKeegan, McCafferty, & Nager, 2019) and are tuned to stressor intensity (Herborn et al., 2015). Body temperature also appears to be sensitive to longer term factors including personality and time of day (Carere & Van Oers, 2004).…”

“…Body temperature also appears to be sensitive to longer term factors including personality and time of day (Carere & Van Oers, 2004). Finally, eye temperature has been shown to be correlated to baseline circulating glucocorticoids, suggesting it may be a useful biomarker for underlying physiology (Jerem et al., 2018, 2019). Body temperature has promise as a noninvasive indicator of physiological responses to both short (detection within minutes, if not seconds, of stressor onset) and mid‐term stressors (stressor duration up to several days; Figure 1; Table S1), although more validation work is needed.…”

A temperate endotherm trades thermoregulation for self-preservation: stress-induced changes in surface temperature as thermoregulatory trade-offs

“…shivering and non-shivering thermogenesis in cold, and evaporative cooling in heat; costs reviewed in McKechnie et al, 2016), in favour of self-preservation. Supporting the Thermoprotective Hypothesis, numerous studies have reported an influence of ambient temperature on both the magnitude and direction of stress-induced thermal responses at the skin (Jerem, Jenni-Eiermann, McKeegan, McCafferty, & Nager, 2019;Nord & Folkow, 2019;Robertson et al, 2020;Yokoi, 1966). These studies suggest that such changes may indeed be leveraged for thermoregulatory purposes.…”