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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)

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.

An increasing number of marine animals are equipped with biologgers, to study their physiology, behaviour and ecology, often for conservation purposes. To minimise the impacts of biologgers on the animals’ welfare, theRefinementprinciple from the Three Rs framework (Replacement,Reduction,Refinement) urges to continuously test and evaluate new and updated biologging protocols. Here, we propose alternative and promising techniques for emperor penguin (Aptenodytes forsteri) capture and on-site logger deployment that aim to mitigate the potential negative impacts of logger deployment on these birds. We equipped adult emperor penguins for short-term (GPS, Time-Depth Recorder (TDR)) and long-term (i.e. planned for one year) deployments (ARGOS platforms, TDR), as well as juvenile emperor penguins for long-term deployments (ARGOS platforms) in the Weddell Sea area where they had not yet been studied. We describe and qualitatively evaluate our protocols for the attachment of biologgers on-site at the colony, the capture of the animals and the recovery of the devices after deployment. We report unprecedented recaptures of long-term equipped adult emperor penguins (50% of equipped individuals recaptured after 290 days). Our data demonstrate that the traditional technique of long-term attachment by gluing the biologgers directly to the back feathers causes excessive feather breakage and the loss of the devices after a few months. We therefore propose an alternative method of attachment for back-mounted devices. This technique led to successful year-round deployments on 37.5% of the equipped juveniles. Finally, we also disclose the first deployments of leg-bracelet mounted TDRs on emperor penguins. Our findings highlight the importance of monitoring potential impacts of biologger deployments on the animals and the need to continue to improve methods to minimize disturbance and enhance performance and results.

The overall study was funded by the IPEV (Program 1037 HEnergES), doctoral fellowships of French Ministry of Higher Education and Research, the University of St Andrews, the Marine Alliance for Science and Technology for Scotland (MASTS) and the Carnegie Trust for the Universities of Scotland. 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. Postprint

International audience; Social facilitation of reproduction occurs in humans and animals, and may represent one of the bases of reproductionin groups. However, its underlying physiological mechanisms remain largely unexplored. Here, we found ina colonial bird, the Adélie penguin (Pygoscelis adeliae), that the number of parental interactions (nest relief ceremonies)performed by breeding individuals on the colony was positively related to prolactin levels in otherbreeding individuals exposed to these interactions (i.e. focal individuals). As prolactin is typically involved inthe expression of parental behaviour in birds, this suggests that parental interactions by conspecifics representsocial cues that might increase parental motivation in focal individuals. Moreover, parental interactions werenot related to corticosterone levels in focal individuals, suggesting that these social cues were not stressful forpenguins. However, social stimulation still had a cost for focal individuals, as itwas negatively related to their antioxidantdefences (a component of self-maintenance). As social stimulationwas also positively related to prolactinlevels, this highlights the fact that social stimulation acts on the trade-off between reproduction and selfmaintenance.For the first time, the results of the current study shed light on the physiological factors potentiallyunderlying social facilitation of parental care. Importantly, they suggest that, even though social facilitation of parentalcare may increase breeding performance, it can also negatively affect other fitness components.

Defining reliable demographic models is essential to understand the threats of ongoing environmental change. Yet, in the most remote and threatened areas, models are often based on the survey of a single population, assuming stationarity and independence in population responses. This is the case for the Emperor penguin Aptenodytes forsteri, a flagship Antarctic species that may be at high risk continent-wide before 2100. Here, using genome-wide data from the whole Antarctic continent, we reveal that this top-predator is organized as one single global population with a shared demography since the late Quaternary. We refute the view of the local population as a relevant demographic unit, and highlight that (i) robust extinction risk estimations are only possible by including dispersal rates and (ii) colony-scaled population size is rather indicative of local stochastic events, whereas the species' response to global environmental change is likely to follow a shared evolutionary trajectory., Delimiting populations is crucial for conserving threatened species. Using genome-wide data from the whole of Antarctica, Cristofari et al. show that Emperor penguins are organised into a single global population that have shared demography since the late Quarternary.

SUMMARYThis paper investigates the energy savings of male emperor penguins Aptenodytes forsteri linked to their huddling behaviour, the key factor that allows them to assume their incubating task while undergoing a long fast. Drawing on new studies by our team, this review examines the energetic benefits accrued from huddling and estimates the respective contributions of wind protection, exposure to mild ambient temperatures,reduction in cold-exposed body surfaces and body temperature adjustments in these energy savings. The metabolic rate of `loosely grouped' birds(restrained in small groups of 5–10 individuals, which are unable to huddle effectively) is reduced by 39% compared to metabolic rate of `isolated'birds, with 32% of these energetic benefits due to wind protection. In addition, metabolic rate of `free-ranging' emperors, i.e. able to move freely and to huddle, is on average 21% lower than that of `loosely grouped' birds. Exposure to mild ambient temperatures within the groups and reduction in cold-exposed body surfaces while huddling, though overestimated, would represent a 38% metabolic reduction. About two thirds of metabolic lowering is attributable to the reduction in cold-exposed body surfaces and one third to the mild microclimate created within the groups. Moreover, body temperature adjustments contribute to these energetic benefits: maintaining body temperatures 1°C lower would represent a 7–17% reduction in energy expenditure. These processes, linked together, explain how huddling emperors save energy and maintain a constant body temperature, which ensures a successful incubation in the midst of the austral winter.

International audience; : Evaluating the demographic trends of marine top predators is critical to understanding the processes involved in the ongoing rapid changes in Antarctic ecosystems. However, the remoteness and logistical complexity of operating in Antarctica, especially during winter, make such an assessment difficult. Satellite imaging is increasingly recognised as a valuable method for remote animal population monitoring, yet its accuracy and reliability are still to be fully evaluated. We report here the first ground visit of an emperor penguin colony first discovered by satellite, but also the discovery of a second one not indicated by satellite survey at that time. Several successive remote surveys in this coastal region of East Antarctica, both before and after sudden local changes, had indeed only identified one colony. These two colonies (with a total of ca. 7,400 breeding pairs) are located near the Mertz Glacier in an area that underwent tremendous habitat change after the glacier tongue broke off in February 2010. Our findings therefore suggest that a satellite survey, although offering a major advance since it allows a global imaging of emperor penguin colonies, may miss certain colony locations when challenged by certain features of polar ecosystems, such as snow cover, evolving ice topology, and rapidly changing habitat. Moreover our survey shows that this large seabird has considerable potential for rapid adaptation to sudden habitat loss, as the colony detected in 2009 may have moved and settled on new breeding grounds. Overall, the ability of emperor penguin colonies to relocate following habitat modification underlines the continued need for a mix of remote sensing and field surveys (aerial photography and ground counts), especially in the less-frequented parts of Antarctica, to gain reliable knowledge about the population demography and dynamics of this flagship species of the Antarctic ecosystem.

Northwestern European populations of White Storks (Ciconia ciconia) have been restored by settling young birds which, after having been maintained captive for 3 years, do not migrate when released. Since they are still supplied with food, the question we address here is how settled White Storks would cope with a fast resulting from a cold spell if food were no longer available. We therefore measured daily body mass loss, nitrogen excretion and daily energy expenditure under natural photoperiod and climatic conditions in six captive White Storks exposed to 5 days of food deprivation during winter. Daily ambient temperature ranged between -10 and 17 degrees C. After an initial decrease in both daily body mass loss and nitrogen excretion during the first day of fasting, these two parameters stabilized at low values. Lipids were the main fuel energy source (91%) and body proteins accounted for the remainder (9%). The rate of CO(2) production, measured with the doubly labeled water method, decreased significantly (P0.001) during fasting when compared to the ad libitum value. Our data show that the metabolic adjustments of White Storks facing starvation are similar to those found in birds well-adapted to long-term fasting. From the determination of lipid and protein stores and of lipid and protein depletion rates, we conclude that White Storks would be able to survive at least during 4 weeks, a period of time twice as long as the duration of cold spells usually occurring in the Alsace region.

International audience; The 18 penguin species are exclusively and widely distributed in the Southern hemisphere, from the Equator to the Antarctic continent, and are thus submitted to various ecological constraints in their reproductive strategy. This results in a high variability in all aspects of the breeding biology of the different species. Although penguins appear primarily adapted for a marine existence, they remain dependent on land for breeding, rearing young and moulting. Here we describe and compare the breeding cycle of all the penguin species highlighting the characteristics of each species in terms of breeding range, population status, threats induce by environmental changes, duration of the different phases of the breeding cycle, mate fidelity, body mass, body height, egg mass and duration of egg formation. We also focus on the breeding cycle of the genus Aptenodytes since it largely differs from the breeding cycle of most of the other penguin species.

Emperor penguins Aptenodytes forsteri are able to survive the harsh Antarctic climate because of specialized anatomical, physiological and behavioural adaptations for minimizing heat loss. Heat transfer theory predicts that metabolic heat loss in this species will mostly depend on radiative and convective cooling. To examine this, thermal imaging of emperor penguins was undertaken at the breeding colony of Pointe Géologie in Terre Adélie (66°40′ S 140° 01′ E), Antarctica in June 2008. During clear sky conditions, most outer surfaces of the body were colder than surrounding sub-zero air owing to radiative cooling. In these conditions, the feather surface will paradoxically gain heat by convection from surrounding air. However, owing to the low thermal conductivity of plumage any heat transfer to the skin surface will be negligible. Future thermal imaging studies are likely to yield further insights into the adaptations of this species to the Antarctic climate.

Background: 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.\ud \ud Methodology/Principal Findings: The brown adipose tissue (BAT) contribution to energy output was assessed as a function of the ability of rabbit (Oryctolagus cuniculus) pups to huddle (placed in groups of 6 and 2, or isolated) and of their thermoregulatory capacities (non-insulated before 5 days old and insulated at ca. 10 days old). BAT contribution of pups exposed to cold was examined by combining techniques of infrared thermography (surface temperature), indirect calorimetry (total energy expenditure, TEE) and telemetry (body temperature). Through local heating, the huddle provided each pup whatever their age with an ambient “public warmth” in the cold, which particularly benefited non-insulated pups. Huddling allowed pups facing a progressive cold challenge to buffer the decreasing ambient temperature by delaying the activation of their thermogenic response, especially when fur-insulated. In this way, huddling permitted pups to effectively shift from a non-insulated to a pseudo-insulated thermal state while continuously allocating energy to growth. The high correlation between TEE and the difference in surface temperatures between BAT and back areas of the body reveals that energy loss for non-shivering thermogenesis is the major factor constraining the amount of energy allocated to growth in non-insulated altricial pups.\ud \ud Conclusions/Significance: By providing public warmth with minimal individual costs at a stage of life when pups are the most vulnerable, huddling buffers cold challenges and ensures a constant allocation of energy to growth by reducing BAT activation.

International audience; Infrared thermography (IRT) is a technique that determines surface temperature based on physical laws of radiative transfer. Thermal imaging cameras have been used since the 1960s to determine the surface temperature patterns of a wide range of birds and mammals and how species regulate their surface temperature in response to different environmental conditions. As a large proportion of metabolic energy is transferred from the body to the environment as heat, biophysical models have been formulated to determine metabolic heat loss. These models are based on heat transfer equations for radiation, convection, conduction and evaporation and therefore surface temperature recorded by IRT can be used to calculate heat loss from different body regions. This approach has successfully demonstrated that in birds and mammals heat loss is regulated from poorly insulated regions of the body which are seen to be thermal windows for the dissipation of body heat. Rather than absolute measurement of metabolic heat loss, IRT and biophysical models have been most useful in estimating the relative heat loss from different body regions. Further calibration studies will improve the accuracy of models but the strength of this approach is that it is a non-invasive method of measuring the relative energy cost of an animal in response to different environments, behaviours and physiological states. It is likely that the increasing availability and portability of thermal imaging systems will lead to many new insights into the thermal physiology of endotherms.

International audience; Age-related changes in breeding performance are likely to be mediated through changes in parental foraging performance. We investigated the relationship of foraging performance with age in female little penguins at Phillip Island, Australia, during the guard phase of the 2005 breeding season. Foraging parameters were recorded with accelerometers for birds grouped into three age-classes: (1) young, (2) middle age and (3) old females. We found the diving behaviour of middleaged birds differed from young and old birds. The dive duration of middle age females was shorter than that of young and old birds while their dive effort (measure for dive and post-dive duration relation) was lower than that of young ones, suggesting middle-aged birds were in better physical condition than other ones. There was no difference in prey pursuit frequency or duration between age classes, but in the hunting tactic. Females pursued more prey around and after reaching the maximum depth of dives the more experienced they were (old . middle age . young), an energy saving hunting tactic by probably taking advantage of up-thrust momentum. We suggest middle age penguins forage better than young or old ones because good physical condition and foraging experience could act simultaneously.

SUMMARY Foraging strategies play a key role in breeding effort. Little is known, however, about their connection with hormonal and nutritional states, especially when breeding constraints vary. Here, we experimentally increased foraging costs and thus breeding constraints by handicapping Adélie penguins (Pygoscelis adeliae) with dummy devices representing 3–4% of the penguins' cross-sectional area. We examined food-related stress (via plasma corticosterone concentration) and nutritional state (via metabolite levels). Concurrently, we investigated the use of ecological niches via the isotopic signature of red blood cells indicating the trophic position (δ15N) and the spatial distribution (δ13C) of penguins. Handicapped birds performed ∼70% longer foraging trips and lost ∼60% more body mass than controls and their partners. However, corticosterone levels and the nutritional state were unchanged. The isotopic signature revealed that males and females differed in their foraging behaviour: upper trophic levels contributed more in the males' diet, who foraged in more pelagic areas. Handicapped and partner birds adopted the same strategy at sea: a shift towards higher δ13C values suggested that they foraged in more coastal areas than controls. This change in foraging decisions may optimize feeding time by decreasing travelling time. This may partly compensate for the presumed lower foraging efficiency of handicapped birds and for the energetic debt of their partners who had to fast ∼70% longer on the nest. We propose that this flexible use of ecological niches may allow birds facing increased breeding constraints to avoid chronic stress and to minimize the impact on their body condition.

The alternation of short/coastal and long/pelagic foraging trips has been proposed as a strategy for seabirds to reconcile self-feeding and parental care. Both types of foraging trips may result in different foraging efforts and diet qualities, and consequently are likely to modify the oxidative status of seabirds. We examined the relationship between the oxidative status of Adélie penguins and (i) the duration of their foraging trips and (ii) their plasma δ 13 C values reflecting their spatial distribution. The oxidative status did not correlate with the foraging trip duration but with the δ 13 C values: high values being associated with high levels of oxidative damage. This relationship is likely to be related to the prey properties of penguins as both parameters are largely determined by the diet. Two non-exclusive hypotheses can be proposed to explain this relationship: (i) penguins foraging in coastal areas feed on a diet enriched in 13 C and depleted in antioxidant compounds; (ii) birds with low antioxidant capacity are constrained to forage in coastal areas. Our study is the first to show that the adoption of different foraging strategies is associated with different levels of oxidative stress. However, further studies are needed to investigate the underlying mechanisms of this intriguing relationship.

International audience; As emperor penguins have no breeding territories, a key issue for both members of a pair is not to be separated until the egg is laid and transferred to the male. Both birds remain silent after mating and thereby reduce the risk of having the pair bond broken by unpaired birds. However, silence prevents finding each other if the pair is separated. Huddles—the key to saving energy in the cold and the long breeding fast— continuously form and break up, but not all birds are involved simultaneously.We studied the behaviour of four pairs before laying. Temperature and light intensity measurements allowed us to precisely detect the occurrence of huddling episodes and to determine the surrounding temperature. The four pairs huddled simultaneously for only 6 per cent of the time when weather conditions were harshest. Despite this asynchrony, the huddling behaviour and the resulting benefits were similar between pairs. By contrast, the huddling behaviour of mates was synchronized for 84 per cent of events. By coordinating their huddling behaviour during courtship despite the apparent confusion within a huddle and its ever-changing structure, both individuals save energy while securing their partnership.

International audience; Huddling is considered as a social strategy to reduce thermal stress and promote growth in newborn altricial mammals. So far, the role of huddling on the allocation of saved energy has not been quantified nor have the related impacts on body temperature rhythms. To determine the energy partitioning of rabbit pups either raised alone or in groups of eight, four, or two individuals, when thermoregulatory inefficient (TI) and efficient (TE), we first investigated their total energy expenditure and body composition. We then monitored body temperature and activity rhythms to test whether huddling may impact these rhythms, centered on the suckling event. Pups in a group of eight utilized 40% less energy for thermogenesis when TI than did pups alone and 32% less energy when TE. Pups in groups of eight and four had significantly lower thermoregulatory costs in the TI period, whereas pups in groups of two, four, and eight had lower costs during the TE period. Huddling pups could therefore channel the energy saved into processes of growth and accrued more fat mass (on average 4.5 +/- 1.4 g) than isolated pups, which lost 0.7 g of fat. Pups in groups of four and eight had a body temperature significantly higher by 0.8 degrees C than pups in groups of two and one when TI, whereas no more differences were noted when the TE period was reached. Moreover, pups alone showed an endogenous circadian body temperature rhythm that differed when compared with that of huddling pups, with no rise before suckling. Thus huddling enables pups to invest the saved energy into growth and to regulate their body temperature to be more competitive during nursing, particularly at the early time when they are TI.

International audience; Although huddling was shown to be the key by which emperor penguins (Aptenodytes forsteri) save energy and sustain their breeding fast during the Antarctic winter, the intricacies of this social behavior have been poorly studied. We recorded abiotic variables with data loggers glued to the feathers of eight individually marked emperor penguins to investigate their thermoregulatory behavior and to estimate their "huddling time budget" throughout the breeding season (pairing and incubation period). Contrary to the classic view, huddling episodes were discontinuous and of short and variable duration, lasting 1.6+/-1.7 (S.D.) h on average. Despite heterogeneous huddling groups, birds had equal access to the warmth of the huddles. Throughout the breeding season, males huddled for 38+/-18% (S.D.) of their time, which raised the ambient temperature that birds were exposed to above 0 degrees C (at average external temperatures of -17 degrees C). As a consequence of tight huddles, ambient temperatures were above 20 degrees C during 13+/-12% (S.D.) of their huddling time. Ambient temperatures increased up to 37.5 degrees C, close to birds' body temperature. This complex social behavior therefore enables all breeders to get a regular and equal access to an environment which allows them to save energy and successfully incubate their eggs during the Antarctic winter.

International audience; Huddling is the key energy-saving mechanism for emperor penguins to endure their 4-mo incubation fast during the Antarctic winter, but the underlying physiological mechanisms of this energy saving have remained elusive. The question is whether their deep body (core) temperature may drop in association with energy sparing, taking into account that successful egg incubation requires a temperature of about 36 degrees C and that ambient temperatures of up to 37.5 degrees C may be reached within tight huddles. Using data loggers implanted into five unrestrained breeding males, we present here the first data on body temperature changes throughout the breeding cycle of emperor penguins, with particular emphasis on huddling bouts. During the pairing period, core temperature decreased progressively from 37.5 +/- 0.4 degrees C to 36.5 +/- 0.3 degrees C, associated with a significant temperature drop of 0.5 +/- 0.3 degrees C during huddling. In case of egg loss, body temperature continued to decrease to 35.5 +/- 0.4 degrees C, with a further 0.9 degrees C decrease during huddling. By contrast, a constant core temperature of 36.9 +/- 0.2 degrees C was maintained during successful incubation, even during huddling, suggesting a trade-off between the demands for successful egg incubation and energy saving. However, such a limited drop in body temperature cannot explain the observed energy savings of breeding emperor penguins. Furthermore, we never observed any signs of hyperthermia in huddling birds that were exposed to ambient temperatures as high as above 35 degrees C. We suggest that the energy savings of huddling birds is due to a metabolic depression, the extent of which depends on a reduction of body surface areas exposed to cold.

Sea birds play a major role in marine food webs, and it is important to determine when and how much they feed at sea. A major advance has been made by using the drop in stomach temperature after ingestion of ectothermic prey. This method is less sensitive when birds eat small prey or when the stomach is full. Moreover, in diving birds, independently of food ingestion, there are fluctuations in the lower abdominal temperature during the dives. Using oesophageal temperature, we present here a new method for detecting the timing of prey ingestion in free-ranging sea birds, and, to our knowledge, report the first data obtained on king penguins (Aptenodytes patagonicus). In birds ashore, which were hand-fed 2-15 g pieces of fish, all meal ingestions were detected with a sensor in the upper oesophagus. Detection was poorer with sensors at increasing distances from the beak. At sea, slow temperature drops in the upper oesophagus and stomach characterized a diving effect per se. For the upper oesophagus only, abrupt temperature variations were superimposed, therefore indicating prey ingestions. We determined the depths at which these occurred. Combining the changes in oesophageal temperatures of marine predators with their diving pattern opens new perspectives for understanding their foraging strategy, and, after validation with concurrent applications of classical techniques of prey survey, for assessing the distribution of their prey.