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 ...

University of Glasgow

Huddling can be defined as "an active and close aggregation of animals". It is a cooperative group behaviour, permitting individuals involved in social thermoregulation to minimize heat loss and thereby lower their energy expenditure, and possibly allowing them to reallocate the saved energy to other functions such as growth or reproduction. Huddling is especially important in the case of animals faced with high heat loss due to a high surface-to-volume ratio, poor insulation, or living in cold environments. Although numerous experimental studies have focused on the huddling behaviour of a wide range of species, to our knowledge, this is the first attempt to review the various implications of this widely used behavioural strategy. Huddling allows individuals to maximise energy savings by (1) decreasing their cold-exposed body surface area, (2) reducing their heat loss through warming of ambient temperatures surrounding the group, and (3) eventually lowering their body temperature through physiological processes. Huddling provides substantial energy savings and is estimated to reduce energy expenditure by between 6 and 53%. Broad variations in the energetic benefits of huddling depend on the number of individuals and species involved in huddles, the ambient temperatures to which individuals are exposed and the density of the aggregations. It has been shown that huddling individuals have increased survival, a lower food intake, a decreased body mass loss, increased growth rate, reduced water loss, and/or a more constant body temperature together with a significant reduction in metabolic rate. Though huddling has been studied widely, this review reveals the intricacies of this adaptive behaviour.

One for all and all for one: the energetic benefits of huddling in endotherms.

Within their litter, young altricial mammals compete for energy (constraining growth and survival) but cooperate for warmth. The aim of this study was to examine the mechanisms by which huddling in altricial infants influences individual heat production and loss, while providing public warmth. Although considered as a textbook example, it is surprising to note that physiological mechanisms underlying huddling are still not fully characterised.

Private heat for public warmth: how huddling shapes individual thermogenic responses of rabbit pups.

In many incubating birds, heat transfer from parent to egg is facilitated by the brood patch, an area of ventral abdominal skin that becomes highly vascularised, swells and loses its down feathers around the time of laying. Only the female develops a brood patch in most passerine species, but males of some species can incubate and maintain the eggs at similar temperatures to females even without a brood patch. Here we used a novel application of infrared thermography to examine sex differences in parental care from a physiological perspective. Using incubating male and female zebra finches (Taeniopygia guttata), a species in which the male lacks a brood patch, we measured the surface temperature of the ventral plumage overlying the abdomen and a reference area that does not contact the eggs (thorax) twice per pair. In half of the pairs, clutch size was experimentally enlarged between the two sets of measurements to increase incubation demand. We found that the temperature differential between abdomen and thorax plumage was greater in females than in males, and that abdomen plumage was warmer after clutch enlargement than before in females but not in males. These findings are consistent with morphological sex differences in brood patch development and suggest that male and female zebra finches differ in the way they regulate abdomen versus general body surface temperature in response to variation in incubation demand.

Female but not male zebra finches adjust heat output in response to increased incubation demand.

Leatherback turtles (Dermochelys coriacea) are the largest species of marine turtle and the fourth most massive extant reptile. In temperate waters they maintain body temperatures higher than surrounding seawater through a combination of insulation, physiological, and behavioural adaptations. Nesting involves physical activity in addition to contact with warm sand and air, potentially presenting thermal challenges in the absence of the cooling effect of water, and data are lacking with which to understand their nesting thermal biology. Using non-contact methods (thermal imaging and infrared thermometry) to avoid any stress-related effects, we investigated core and surface temperature during nesting. The mean±SE core temperature was 31.4±0.05°C (newly emerged eggs) and was not correlated with environmental conditions on the nesting beach. Core temperature of leatherbacks was greater than that of hawksbill turtles (Eretmochelys imbricata) nesting at a nearby colony, 30.0±0.13°C. Body surface temperatures of leatherbacks showed regional variation, the lateral and dorsal regions of the head were warmest while the carapace was the coolest surface. Surface temperature increased during the early nesting phases, then levelled off or decreased during later phases with the rates of change varying between body regions. Body region, behavioural phase of nesting and air temperature were found to be the best predictors of surface temperature. Regional variation in surface temperature were likely due to alterations in blood supply, and temporal changes in local muscular activity of flippers during the different phases of nesting. Heat exchange from the upper surface of the turtle was dominated by radiative heat loss from all body regions and small convective heat gains to the carapace and front flippers.

Core and body surface temperatures of nesting leatherback turtles (Dermochelys coriacea).

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.

Dominic McCafferty

Institute of Biodiversity,
Animal Health and Comparative Medicine,
College of Medical,
Veterinary & Life Sciences,
Institute of Biodiversity, Animal Health and Comparative Medicine, College of Medical, Veterinary & Life Sciences

University of Glasgow

Thermal Imaging to Study Stress Non-invasively in Unrestrained Birds