HPAIV outbreak triggers short-term colony connectivity in a seabird metapopulation.

Disease outbreaks can drastically disturb the environment of surviving animals, but the behavioural, ecological, and epidemiological consequences of disease-driven disturbance are poorly understood. Here, we show that an outbreak of High Pathogenicity Avian Influenza Virus (HPAIV) coincided with unprecedented short-term behavioural changes in Northern gannets (Morus bassanus). Breeding gannets show characteristically strong fidelity to their nest sites and foraging areas (2015-2019; n = 120), but during the 2022 HPAIV outbreak, GPS-tagged gannets instigated long-distance movements beyond well-documented previous ranges and the first ever recorded visits of GPS-tagged adults to other gannet breeding colonies. Our findings suggest that the HPAIV outbreak triggered changes in space use patterns of exposed individuals that amplified the epidemiological connectivity among colonies and may generate super-spreader events that accelerate disease transmission across the metapopulation. Such self-propagating transmission from and towards high density animal aggregations may explain the unexpectedly rapid pan-European spread of HPAIV in the gannet.

Breaking the fast: first report of dives and ingestion events in molting southern elephant seals.

Southern elephant seals (SES) experience a 'catastrophic molt', a costly event characterized by the renewal of both hair and epidermis that requires high peripheral vascular circulation. Molting animals are therefore constrained by high metabolic heat loss and are thought to fast and remain on land. To examine the ability of individuals to balance the energetic constraints of molting on land we investigate the stomach temperature and movement patterns of molting female SES. We find that 79% of females swam and 61% ingested water or prey items, despite the cost of cold-water exposure while molting. This behavior was related to periods of warm and low wind conditions, and females that dived and ingested more often, lost less body mass. We conclude that the paradigm of fasting during the molt in this species, and the fitness consequences of this behavior should be reconsidered, especially in the context of a changing climate.

Body surface temperature of rats reveals both magnitude and sex differences in the acute stress response.

Understanding how biological markers of stress relate to stressor magnitude is much needed and can be used in welfare assessment. Changes in body surface temperature can be measured using infrared thermography (IRT) as a marker of a physiological response to acute stress. While an avian study has shown that changes in body surface temperature can reflect the intensity of acute stress, little is known about surface temperature responses to stressors of different magnitudes and its sex-specificity in mammals, and how they correlate with hormonal and behavioural responses. We used IRT to collect continuous surface temperature measurements of tail and eye of adult male and female rats (Rattus norvegicus), for 30 minutes after exposure to one of three stressors (small cage, encircling handling or rodent restraint cone) for one minute, and cross-validated the thermal response with plasma corticosterone (CORT) and behavioural assessment. To obtain individual baseline temperatures and thermal responses to stress, rats were imaged in a test arena (to which they were habituated) for 30 seconds before and 30 minutes after being exposed to the stressor. In response to the three stressors, tail temperature initially decreased and then recovered to, or overshot the baseline temperature. Tail temperature dynamics differed between stressors; being restrained in the small cage was associated with the smallest drop in temperature, in male rats, and the fastest thermal recovery, in both sexes. Increases in eye temperature only distinguished between stressors early in the response and only in females. The post stressor increase in eye temperature was greater in the right eye of males and the left eye of females. In both sexes encircling may have been associated with the fastest increase in CORT. These results were in line with observed behavioural changes, with greater movement in rats exposed to the small cage and higher immobility after encircling. The female tail and eye temperature, as well as the CORT concentrations did not return to pre-stressor levels in the observation period, in conjunction with the greater occurrence of escape-related behaviours in female rats. These results suggest that female rats are more vulnerable to acute restraint stress compared to male rats and emphasise the importance of using both sexes in future investigations of stressor magnitude. This study demonstrates that acute stress induced changes in mammalian surface temperature measured with IRT relate to the magnitude of restraint stress, indicate sex differences and correlate with hormonal and behavioural responses. Thus, IRT has the potential to become a non-invasive method of continuous welfare assessment in unrestrained mammals.

Non-invasive assessment of positive affective state using infra-red thermography in rats.

With recent increased focus on positive welfare in animal welfare science, there is demand for objective positive welfare indicators. It is unclear whether changes in body surface temperature can be used to non-invasively identify and quantify positive states in mammals. We recorded continuous measurements of tail surface temperature using infra-red thermography (IRT) and concurrent behavioural observations in male and female Wistar rats (Rattus norvegicus). If tail surface temperature can differentiate between positive and negative experiences, we expect a qualitatively different response compared to negative experiences. Three groups of rats were presented with increasing magnitudes of food rewards (neutral/none, one and three rewards). The rats were placed in an arena to which they were habituated and filmed for 30 s before and 30 min after exposure to different rewards. Tail temperature initially decreased from the pre-reward baseline and subsequently returned towards baseline temperature. The overall pattern of the change was the same as for rats subjected to negative stimuli in previous studies. Nevertheless, dynamic changes in tail temperature, specifically the rate of recovery and the behavioural response (exploration), differed between neutral and rewarded rats but failed to distinguish reward magnitude. Sex differences were found in both thermal and behavioural responses, unrelated to reward magnitudes. Female rats exhibited a greater initial response with a slower recovery than male rats, emphasising the value of using of both sexes in animal welfare research. This study improves our understanding of the effects of positive emotions induced by food reward on peripheral body temperature and behaviour.

Evaluation of a Novel Infrared Thermography Projection to Assess Udder Health in Primigravid Dairy Heifers.

Heifer mastitis in early lactation impacts negatively on animal welfare, milk production and longevity. A major challenge for the prevention and control of mastitis in dairy heifers is to establish when intramammary infection occurs because pre-partum secretum sampling is risky. We evaluated a ventrodorsal projection to capture thermal images of the entire udder of primigravid and compared results against caudocranial projection, which is used in lactating cattle. Based on the analysis of 119 heifers and images taken at 2 months and 2 weeks pre-partum, a very strong positive correlation (r = 0.91 and r = 0.96, respectively) was shown between caudocranial and ventrodorsal projections of hind quarters. Quarter maximum gradient temperatures were consistently greater on ventrodorsal projection than on caudocranial projection, and less variable than minimum gradient temperatures. The collection of ventrodorsal images is a simple one-step method involving the imaging of the entire udder in a manner safe for both the cattle and handlers. Together, these results demonstrate that a single projection can be used to scan the entire udder of primigravid dairy heifers in commercial farm conditions, with the potential to implement this as a routine method for the early detection of intramammary infection based on udder surface temperature.

Experimental warming during incubation improves cold tolerance of blue tit (Cyanistes caeruleus) chicks.

Climate change and increasing air temperature may alter environmental conditions for developing birds, with a range of phenotypic consequences for offspring. The thermal environment during incubation may affect the trade-off between growth and thermoregulation, but the effects of temperature on the ontogeny of endothermy are not fully understood. Therefore, we experimentally tested whether heating the nest cup of Eurasian blue tits (Cyanistes caeruleus) during incubation would influence cold tolerance of the chicks after hatching. Chicks from both heated and control nests showed a decrease in cooling rate with age as they became increasingly endothermic and homeothermic. However, chicks from previously heated nests cooled at a lower rate per unit surface area and from across the whole body. These chicks also had a greater body mass during the first 12 days of life compared with chicks from control nests. Lower cooling rates in heated chicks may reflect greater thermogenic capacity or a reduced surface area to volume ratio owing to a greater body mass. Future projections for climate change predict rising air temperature and increased likelihood of heatwaves, even in temperate regions. Our results indicate that nest microclimate can affect thermoregulation in offspring, and thus may be used to predict some of the future physiological responses of birds to climate change during breeding.

Metabolic heat loss in southern elephant seals (Mirounga leonina) differs with stage of moult and between habitats.

The moult in southern elephant seals (Mirounga leonina) represents an especially energetically demanding period during which seals must maintain high skin temperature to facilitate complete replacement of body fur and upper dermis. In this study, heat flux from the body surface was measured on 18 moulting southern elephant seals to estimate metabolic heat loss in three different habitats (beach, wallow and vegetation). Temperature data loggers were also deployed on 10 southern elephant seals to monitor skin surface temperature. On average, heat loss of animals on the beach was greater than in wallows or vegetation, and greater in wallows than in vegetation. Heat loss across all habitats during the moult equated to 1.8 x resting metabolic rate (RMR). The greatest heat loss of animals was recorded in the beach habitat during the late moult, that represented 2.3 x RMR. Mass loss was 3.6 ± 0.3 kg day-1, resulting in changes in body condition as the moult progressed. As body condition declined, skin surface temperature also decreased, suggesting that as animals approached the end of the moult blood flow to the skin surface was no longer required for hair growth.

Avian red blood cell mitochondria produce more heat in winter than in autumn.

Endotherms in cold regions improve heat-producing capacity when preparing for winter. We know comparatively little about how this change is fueled by seasonal adaptation in cellular respiration. Thus, we studied the changes of mitochondrial function in red blood cells in sympatric Coal (Periparus ater), Blue (Cyanistes caeruleus), and Great (Parus major) tits between autumn and winter. These species differ more than twofold in body mass and in several aspects of their foraging ecology and social dominance, which could require differential seasonal adaptation of energy expenditure. Coal and Great tits in particular upregulated the mitochondrial respiration rate and mitochondrial volume in winter. This was not directed toward ATP synthesis, instead reflecting increased uncoupling of electron transport from ATP production. Because uncoupling is exothermic, this increased heat-producing capacity at the sub-cellular level in winter. This previously unexplored the route of thermogenesis in birds should be addressed in future work.

Plumage development and environmental factors influence surface temperature gradients and heat loss in wandering albatross chicks.

Young birds in cold environments face a range of age-specific thermal challenges. Studying the thermal biology of young birds throughout ontogeny may further our understanding of how such challenges are met. We investigated how age and environmental parameters influenced surface temperature gradients across various body regions of wandering albatross (Diomedea exulans) chicks on Bird Island, South Georgia. This study was carried out over a 200 d period during the austral winter, from the end of the brood-guard period until fledging, bridging a gap in knowledge of surface temperature variation and heat loss in developing birds with a long nestling stage in severe climatic conditions. We found that variation in surface temperature gradients (i.e. the difference between surface and environmental temperature) was strongly influenced by chick age effects for insulated body regions (trunk), with an increase in the surface temperature gradient that followed the progression of plumage development, from the second set of down (mesoptiles), to final chick feathers (teleoptiles). Environmental conditions (primarily wind speed and relative humidity) had a stronger influence on the gradients in uninsulated areas (eye, bill) than insulated regions, which we interpret as a reflection of the relative degree of homeothermy exhibited by chicks of a given age. Based on biophysical modelling, total heat loss of chicks was estimated to increase linearly with age. However, mass specific heat loss decreased during the early stages of growth and then subsequently increased. This was attributed to age-related changes in feather growth and activity that increased surface temperature and, hence, metabolic heat loss. These results provide a foundation for further work on the effects of environmental stressors on developing chicks, which are key to understanding the physiological responses of animals to changes in climate in polar regions.

Increased Metabolic Rate of Hauled-Out Harbor Seals (Phoca vitulina) during the Molt.

AbstractHarbor seals (Phoca vitulina) live in cold temperate or polar seas and molt annually, renewing their fur over a period of approximately 4 wk. Epidermal processes at this time require a warm skin; therefore, to avoid an excessive energy cost at sea during the molt, harbor seals and many other pinnipeds increase the proportion of time they are hauled out on land. We predicted that metabolic rate during haul-out would be greater during the molt to sustain an elevated skin temperature in order to optimize skin and hair growth. To examine this, we measured post-haul-out oxygen consumption (V˙O2) in captive harbor seals during molt and postmolt periods. We recorded greater V˙O2 of seals while they were molting than when the molt was complete. Post-haul-out V˙O2 increased faster and reached a greater maximum during the first 40 min. Thereafter, V˙O2 decreased but still remained greater, suggesting that while metabolic rate was relatively high throughout haul-outs, it was most pronounced in the first 40 min. Air temperature, estimated heat increment of feeding, and mass also explained 15.5% of V˙O2 variation over 180 min after haul-out, suggesting that the environment, feeding state, and body size influenced the metabolic rate of individual animals. These results show that molting seals have greater metabolic rates when hauled out, especially during the early stages of the haul-out period. As a consequence, human disturbance that changes the haul-out behavior of molting seals will increase their energy costs and potentially extend the duration of the molt.

Body surface rewarming in fully and partially hypothermic king penguins.

Penguins face a major thermal transition when returning to land in a hypothermic state after a foraging trip. Uninsulated appendages (flippers and feet) could provide flexible heat exchange during subsequent rewarming. Here, we tested the hypothesis that peripheral vasodilation could be delayed during this recovery stage. To this end, we designed an experiment to examine patterns of surface rewarming in fully hypothermic (the cloaca and peripheral regions (here; flippers, feet and the breast) < 37 °C) and partially hypothermic (cloaca at normothermia ≥ 37 °C, but periphery at hypothermia) king penguins (Aptenodytes patagonicus) when they rewarmed in the laboratory. Both groups rewarmed during the 21 min observation period, but the temperature changes were larger in fully than in partially hypothermic birds. Moreover, we observed a 5 min delay of peripheral temperature in fully compared to partially hypothermic birds, suggesting that this process was impacted by low internal temperature. To investigate whether our laboratory data were applicable to field conditions, we also recorded surface temperatures of free-ranging penguins after they came ashore to the colony. Initial surface temperatures were lower in these birds compared to in those that rewarmed in the laboratory, and changed less over a comparable period of time on land. This could be explained both by environmental conditions and possible handling-induced thermogenesis in the laboratory. Nevertheless, this study demonstrated that appendage vasodilation is flexibly used during rewarming and that recovery may be influenced by both internal temperature and environmental conditions when penguins transition from sea to land.

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

During winter at temperate and high latitudes, the low ambient temperatures, limited food supplies and short foraging periods mean small passerines show behavioural, morphological and physiological adaptations to reduce the risk of facing energy shortages. Peripheral tissues vasoconstrict in low ambient temperatures to reduce heat loss and cold injury. Peripheral vasoconstriction has been observed with food restriction in captivity but has yet to be explored in free-ranging animals. We experimentally food restricted both wild and captive great tits (Parus major) during winter months and measured surface temperatures of the bill and eye region using thermal imaging, to investigate whether birds show rapid local heterothermic responses, which may reduce their thermoregulatory costs when facing a perceived imminent food shortage. Our results of a continuously filmed wild population showed that bill temperature was immediately reduced in response to food restriction compared with when food was available ad libitum, an apparent autonomic response. Such immediacy implies a 'pre-emptive' response before the bird experiences any shortfalls in energy reserves. We also demonstrate temporal variation in vasoconstriction of the bill, with bill temperature gradually rising throughout the food restriction after the initial drop. Eye-region temperature in the wild birds remained at similar levels throughout food restriction compared with unrestricted birds, possibly reflecting the need to maintain steady circulation to the central nervous and visual systems. Our findings provide evidence that birds selectively allow the bill to cool when a predictable food supply is suddenly disrupted, probably as a means of minimising depletion of body reserves for a perceived future shortage in energy.

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.

Environmental and physiological determinants of huddling behavior of molting female southern elephant seals (Mirounga leonina).

While endotherms can rely on their insulation to reduce heat loss to adapt to cold environments, renewing of fur during molt impairs insulation while they have to perfuse the periphery to support epidermal tissues. The southern elephant seal Mirounga leonina undertakes an annual catastrophic molt while fasting on land in a wet, windy and cold environment. However, southern elephant seals show characteristic aggregation patterns that are predicted to reduce high metabolic costs during the molt. Between 2012 and 2016, 59 female elephant seals were tracked on land during their molt to study their aggregation behavior in relation to molt stage, habitat type and local weather conditions. Infrared thermography and stomach temperature loggers were used to observe variation in body surface and internal temperature in relation to molt stage and aggregation behavior. We found that thermal constraints varied during the molt, with a peak in surface temperature during the mid-stage of the molt. Wallows (mud pools) appear as favorable habitat to aggregate while molting. Indeed, wallows offered a warmer microclimate with greater ground temperature and lower wind speed. Moreover, there was a greater proportion of aggregated seals and larger group size in wallows. These aggregation patterns in wallows were influenced by local weather such that a greater proportion of seals were located in the center of the aggregation, and larger group size occurred during days of unfavorable meteorological conditions. We also observed a higher proportion of seals at mid-stage of molt amongst aggregated seals compared to isolated individuals. This aggregation behavior may reduce the cost of thermogenesis as surface body temperature and stomach temperature were cooler by 1.0 °C and 1.5 °C, respectively, in aggregated compared to isolated seals. As a consequence, huddling behavior may be thermally advantageous for female southern elephant seals during the molt.

Local weather and body condition influence habitat use and movements on land of molting female southern elephant seals (Mirounga leonina).

Southern elephant seals (Mirounga leonina) are known to move and aggregate while molting, but little is known about their behavior on land during this time. In this study, 60 adult females were monitored (23 with GPS tags) during four molting seasons, between 2012 and 2016 at Kerguelen Archipelago, Indian Ocean. Population surveys were recorded each year (N = 230 daily counts), and habitat use was analyzed in relation to the stage of the molt and local weather. Based on stage of molt, habitat use, and movements on land, we classified the molt of elephant seals into three phases: (1) a "search phase" at the initial stage of molt when grass and wallow habitats were used and characterized by greater mean distances travelled on land per day compared with the two other phases; (2) a "resident phase": during initial and mid-stage of molt when animals were found in grass and wallow habitats but with less distance moved on land; and (3) a "termination phase" at the final stage of molt where grass and beach habitats were occupied with no change in distances. Windchill and solar radiation influenced individual distances moved per day (mean 590 ± 237.0 m) at the mid- and final stage of molt such that animals travelled greater distances on days of low windchill or high solar radiation. Individual variation in distance moved and relative habitat use were also linked to body mass index (BMI) at arrival on the colony, as females with higher BMI moved less and preferred beach habitat. Moreover, the individual rate of molt increased with the use of wallows. Aggregation rate tended to be negatively correlated with distances moved. We therefore suggest that individuals face an energetic trade-off while molting, balancing energy expenditure between movement and thermoregulation.

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.

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.

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.