Changes in body surface temperature reveal the thermal challenge associated with catastrophic moult in captive gentoo penguins.

Once a year, penguins undergo a catastrophic moult, replacing their entire plumage during a fasting period on land or on sea-ice during which time individuals can lose 45% of their body mass. In penguins, new feather synthesis precedes the loss of old feathers, leading to an accumulation of two feather layers (double coat) before the old plumage is shed. We hypothesized that the combination of the high metabolism required for new feather synthesis and the potentially high thermal insulation linked to the double coat could lead to a thermal challenge requiring additional peripheral circulation to thermal windows to dissipate the extra heat. To test this hypothesis, we measured the surface temperature of different body regions of captive gentoo penguins (Pygoscelis papua) throughout the moult under constant environmental conditions. The surface temperature of the main body trunk decreased during the initial stages of the moult, suggesting greater thermal insulation. In contrast, the periorbital region, a potential proxy of core temperature in birds, increased during these same early moulting stages. The surface temperature of the bill, flipper and foot (thermal windows) tended to initially increase during the moult, highlighting the likely need for extra heat dissipation in moulting penguins. These results raise questions regarding the thermoregulatory capacities of penguins in the wild during the challenging period of moulting on land in the current context of global warming.

Surface temperatures are influenced by handling stress independently of corticosterone levels in wild king penguins (Aptenodytes patagonicus).

Assessing the physiological stress responses of wild animals opens a window for understanding how organisms cope with environmental challenges. Since stress response is associated with changes in body temperature, the use of body surface temperature through thermal imaging could help to measure acute and chronic stress responses non-invasively. We used thermal imaging, acute handling-stress protocol and an experimental manipulation of corticosterone (the main glucocorticoid hormone in birds) levels in breeding king penguins (Aptenodytes patagonicus), to assess: 1. The potential contribution of the Hypothalamo-Pituitary-Adrenal (HPA) axis in mediating chronic and acute stress-induced changes in adult surface temperature, 2. The influence of HPA axis manipulation on parental investment through thermal imaging of eggs and brooded chicks, and 3. The impact of parental treatment on offspring thermal's response to acute handling. Maximum eye temperature (Teye) increased and minimum beak temperature (Tbeak) decreased in response to handling stress in adults, but neither basal nor stress-induced surface temperatures were significantly affected by corticosterone implant. While egg temperature was not significantly influenced by parental treatment, we found a surprising pattern for chicks: chicks brooded by the (non-implanted) partner of corticosterone-implanted individuals exhibited higher surface temperature (both Teye and Tbeak) than those brooded by glucocorticoid-implanted or control parents. Chick's response to handling in terms of surface temperature was characterized by a drop in both Teye and Tbeak independently of parental treatment. We conclude that the HPA axis seems unlikely to play a major role in determining chronic or acute changes in surface temperature in king penguins. Changes in surface temperature may primarily be mediated by the Sympathetic-Adrenal-Medullary (SAM) axis in response to stressful situations. Our experiment did not reveal a direct impact of parental HPA axis manipulation on parental investment (egg or chick temperature), but a potential influence on the partner's brooding behaviour.

How birds dissipate heat before, during and after flight.

Animal flight uses metabolic energy at a higher rate than any other mode of locomotion. A relatively small proportion of the metabolic energy is converted into mechanical power; the remainder is given off as heat. Effective heat dissipation is necessary to avoid hyperthermia. In this study, we measured surface temperatures in lovebirds (Agapornis personatus) using infrared thermography and used heat transfer modelling to calculate heat dissipation by convection, radiation and conduction, before, during and after flight. The total non-evaporative rate of heat dissipation in flying birds was 12× higher than before flight and 19× higher than after flight. During flight, heat was largely dissipated by forced convection, via the exposed ventral wing areas, resulting in lower surface temperatures compared with birds at rest. When perched, both before and after exercise, the head and trunk were the main areas involved in dissipating heat. The surface temperature of the legs increased with flight duration and remained high on landing, suggesting that there was an increase in the flow of warmer blood to this region during and after flight. The methodology developed in this study to investigate how birds thermoregulate during flight could be used in future studies to assess the impact of climate change on the behavioural ecology of birds, particularly those species undertaking migratory flights.

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.

The metabolic cost of subcutaneous and abdominal rewarming in king penguins after long-term immersion in cold water.

Marine endotherms in the polar regions face a formidable thermal challenge when swimming in cold water. Hence, they use morphological (fat, blubber) adjustment and peripheral vasoconstriction to reduce demands for heat production in water. The animals then regain normothermia when resting ashore. In the king penguin (Aptenodytes patagonicus) metabolic rate is lower in fed than in fasted individuals during subsequent rewarming on land. This has been suggested to be a consequence of diversion of blood flow to the splanchnic region in fed birds, which reduces peripheral temperatures. However, peripheral temperatures during recovery have never been investigated in birds with different nutritional status. The aim of this study was, therefore, to measure subcutaneous and abdominal temperatures during the rewarming phase on land in fasted and fed king penguins, and investigate to which extent any different rewarming were reflected in recovery metabolic rate (MRR) after long term immersion in cold water. We hypothesized that fed individuals would have a slower increase of subcutaneous temperatures compared to fasted penguins, and a correspondingly lower MRR. Subcutaneous tissues reached normothermia after 24.15 (back) and 21.36 min (flank), which was twice as fast as in the abdomen (46.82 min). However, recovery time was not affected by nutritional condition. MRR during global rewarming (4.56 ± 0.42 W kg-1) was twice as high as resting metabolic rate (RMR; 2.16 ± 0.59 W kg-1). However, MRR was not dependent on feeding status and was significantly elevated above RMR only until subcutaneous temperature had recovered. Contrary to our prediction, fed individuals did not reduce the subcutaneous circulation compared to fasted penguins and did not show any changes in MRR during subsequent recovery. It seems likely that lower metabolic rate in fed king penguins on land reported in other studies might not have been caused primarily by increased circulation to the visceral organs.

Thermal strategies of king penguins during prolonged fasting in water.

Most animals experience periods of unfavourable conditions, challenging their daily energy balance. During breeding, king penguins fast voluntarily for up to 1.5 months in the colony, after which they replenish their energy stores at sea. However, at sea, birds might encounter periods of low foraging profitability, forcing them to draw from previously stored energy (e.g. subcutaneous fat). Accessing peripheral fat stores requires perfusion, increasing heat loss and thermoregulatory costs. Hence, how these birds balance the conflicting demands of nutritional needs and thermoregulation is unclear. We investigated the physiological responses of king penguins to fasting in cold water by: (1) monitoring tissue temperatures, as a proxy of tissue perfusion, at four distinct sites (deep and peripheral); and (2) recording their oxygen consumption rate while birds floated inside a water tank. Despite frequent oscillations, temperatures of all tissues often reached near-normothermic levels, indicating that birds maintained perfusion to peripheral tissues throughout their fasting period in water. The oxygen consumption rate of birds increased with fasting duration in water, while it was also higher when the flank tissue was warmer, indicating greater perfusion. Hence, fasting king penguins in water maintained peripheral perfusion, despite the associated greater heat loss and, therefore, thermoregulatory costs, probably to access subcutaneous fat stores. Hence, the observed normothermia in peripheral tissues of king penguins at sea, upon completion of a foraging bout, is likely explained by their nutritional needs: depositing free fatty acids (FFA) in subcutaneous tissues after profitable foraging or mobilizing FFA to fuel metabolism when foraging success was insufficient.

High peripheral temperatures in king penguins while resting at sea: thermoregulation versus fat deposition.

Marine endotherms living in cold water face an energetically challenging situation. Unless properly insulated, these animals will lose heat rapidly. The field metabolic rate of king penguins at sea is about twice that on land. However, when at sea, their metabolic rate is higher during extended resting periods at the surface than during foraging, when birds descend to great depth in pursuit of their prey. This is most likely explained by differences in thermal status. During foraging, peripheral vasoconstriction leads to a hypothermic shell, which is rewarmed during extended resting bouts at the surface. Maintaining peripheral perfusion during rest in cold water, however, will greatly increase heat loss and, therefore, thermoregulatory costs. Two hypotheses have been proposed to explain the maintenance of a normothermic shell during surface rest: (1) to help the unloading of N2 accumulated during diving; and (2) to allow the storage of fat in subcutaneous tissue, following the digestion of food. We tested the latter hypothesis by maintaining king penguins within a shallow seawater tank, while we recorded tissue temperature at four distinct sites. When king penguins were released into the tank during the day, their body temperature immediately declined. However, during the night, periodic rewarming of abdominal and peripheral tissues occurred, mimicking temperature patterns observed in the wild. Body temperatures, particularly in the flank, also depended on body condition and were higher in 'lean' birds (after 10 days of fasting) than in 'fat' birds. While not explicitly tested, our observation that nocturnal rewarming persists in the absence of diving activity during the day does not support the N2 unloading hypothesis. Rather, differences in temperature changes throughout the day and night, and the effect of body condition/mass supports the hypothesis that tissue perfusion during rest is required for nutritional needs.

Body temperature responses to handling stress in wintering Black-capped Chickadees (Poecile atricapillus L.).

Body temperature variation in response to acute stress is typically characterized by peripheral vasoconstriction and a concomitant increase in core body temperature (stress-induced hyperthermia). It is poorly understood how this response differs between species and within individuals of the same species, and how it is affected by the environment. We therefore investigated stress-induced body temperature changes in a non-model species, the Black-capped Chickadee, in two environmental conditions: outdoors in low ambient temperature (mean: -6.6°C), and indoors, in milder ambient temperature close to thermoneutrality (mean: 18.7°C). Our results show that the change in body temperature in response to the same handling stressor differs in these conditions. In cold environments, we noted a significant decrease in core body temperature (-2.9°C), whereas the response in mild indoor conditions was weak and non-significant (-0.6°C). Heat loss in outdoor birds was exacerbated when birds were handled for longer time. This may highlight the role of behavioral thermoregulation and heat substitution from activity to body temperature maintenance in harsh condition. Importantly, our work also indicates that changes in the physical properties of the bird during handling (conductive cooling from cold hands, decreased insulation from compression of plumage and prevention of ptiloerection) may have large consequences for thermoregulation. This might explain why females, the smaller sex, lost more heat than males in the experiment. Because physiological and physical changes during handling may carry over to affect predation risk and maintenance of energy balance during short winter days, we advice caution when designing experimental protocols entailing prolonged handling of small birds in cold conditions.

Individual inconsistencies in basal and summit metabolic rate highlight flexibility of metabolic performance in a wintering passerine.

Resident passerines inhabiting high latitude environments are faced with strong seasonal changes in thermal conditions and energy availability. Summit metabolic rate (maximal metabolic rate elicited by shivering during cold exposure: M(sum)) and basal metabolic rate (BMR) vary in parallel among seasons and increase in winter due to cold acclimatization, and these adjustments are thought to be critical for survival. Wintering individuals expressing consistently higher M(sum) and BMR could therefore be seen as better performers with higher chances of winter survival than those exhibiting lower metabolic performance. In this study, we calculated repeatability to evaluate temporal consistency of body mass, BMR and M(sum) within and across three consecutives winters in black-capped chickadees (Poecile atricapillus). We found that body mass was significantly repeatable both within and across winters (R 0.51-0.90). BMR (R 0.29-0.47) was only repeatable within winter while M(sum) was repeatable both among (R 0.33-0.49) and within winters (R 0.33-0.49) with the magnitude and significance of repeatability in both variables depending on the year and whether they were corrected for body mass or body size. The patterns of repeatability observed among years also differed between the two variables. Our findings suggest that the relative ranking of individuals in winter metabolic performance is affected by local ecological conditions and can change within relatively short periods of time.

How does flexibility in body composition relate to seasonal changes in metabolic performance in a small passerine wintering at northern latitude?

Abstract Small avian species wintering at northern latitudes typically show increases in basal metabolic rate (BMR) and maximal thermogenic capacity (Msum). Those are widely assumed to reflect changes in body composition, with enlargement of digestive and excretory organs resulting in elevated winter BMR and larger body muscles driving the increase in Msum. Using free-living black-capped chickadees (Poecile atricapillus) as our model species, we investigated seasonal changes in body composition and tested for relationships between mass variations of body organs and variability of both BMR and Msum. Our results confirmed the expected winter increase in mass of body muscles and cardiopulmonary organs (heart + lungs) and showed that 64% of the observed Msum variations throughout the year were explained by changes in these organs. In contrast, we found little support for an effect of the digestive organs (gizzard + intestines) on BMR seasonal changes. Instead, this variable was mainly influenced by variations in mass of body muscles and excretory organs (liver + kidney), explaining up to 35% of its variability.

Intra-seasonal flexibility in avian metabolic performance highlights the uncoupling of basal metabolic rate and thermogenic capacity.

Stochastic winter weather events are predicted to increase in occurrence and amplitude at northern latitudes and organisms are expected to cope through phenotypic flexibility. Small avian species wintering in these environments show acclimatization where basal metabolic rate (BMR) and maximal thermogenic capacity (MSUM) are typically elevated. However, little is known on intra-seasonal variation in metabolic performance and on how population trends truly reflect individual flexibility. Here we report intra-seasonal variation in metabolic parameters measured at the population and individual levels in black-capped chickadees (Poecileatricapillus). Results confirmed that population patterns indeed reflect flexibility at the individual level. They showed the expected increase in BMR (6%) and MSUM (34%) in winter relative to summer but also, and most importantly, that these parameters changed differently through time. BMR began its seasonal increase in November, while MSUM had already achieved more than 20% of its inter-seasonal increase by October, and declined to its starting level by March, while MSUM remained high. Although both parameters co-vary on a yearly scale, this mismatch in the timing of variation in winter BMR and MSUM likely reflects different constraints acting on different physiological components and therefore suggests a lack of functional link between these parameters.

Dominant black-capped chickadees pay no maintenance energy costs for their wintering status and are not better at enduring cold than subordinate individuals.

Winter requires physiological adjustments in northern resident passerines. Cold acclimatization is generally associated with an increase in physiological maintenance costs, measured as basal metabolic rate (BMR), and cold endurance, reflected by summit metabolic rate (M(sum)). However, several northern species also form social groups in winter and a bird's hierarchical position may influence the size of its metabolically active organs as well as its BMR. Winter metabolic performance in these species may therefore reflect a complex set of adjustments to both seasonal climatic variations and social environment. We studied the effect of social status on parameters of cold acclimatization (body mass, size of fat reserves and pectoral muscles, BMR and M(sum)) in free-living black-capped chickadees (Poecile atricapillus). Birds that were structurally large and heavy for their body size, mostly dominant individuals, carried more fat reserves and had larger pectoral muscles. However, social status had little effect on metabolic performance in the cold. Indeed, M(sum) was independent of social rank while mass-corrected BMR was slightly lower in dominant individuals, likely due to a statistical dilution effect caused by large metabolically inactive fat reserves. BMR and M(sum), whether considered in terms of whole-animal values, corrected for body mass or body size were nevertheless correlated, suggesting a functional link between these metabolic components. Our results therefore indicate that the energy cost of social dominance is not a generalized phenomenon in small wintering birds.