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.

Biologging of emperor penguins-Attachment techniques and associated deployment performance.

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, the Refinement principle 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.

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.

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.

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.

Socially-induced variation in physiological mediators of parental care in a colonial bird.

Social facilitation of reproduction occurs in humans and animals, and may represent one of the bases of reproduction in groups. However, its underlying physiological mechanisms remain largely unexplored. Here, we found in a 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 other breeding individuals exposed to these interactions (i.e. focal individuals). As prolactin is typically involved in the expression of parental behaviour in birds, this suggests that parental interactions by conspecifics represent social cues that might increase parental motivation in focal individuals. Moreover, parental interactions were not related to corticosterone levels in focal individuals, suggesting that these social cues were not stressful for penguins. However, social stimulation still had a cost for focal individuals, as it was negatively related to their antioxidant defences (a component of self-maintenance). As social stimulation was also positively related to prolactin levels, this highlights the fact that social stimulation acts on the trade-off between reproduction and self-maintenance. For the first time, the results of the current study shed light on the physiological factors potentially underlying social facilitation of parental care. Importantly, they suggest that, even though social facilitation of parental care may increase breeding performance, it can also negatively affect other fitness components.

Full circumpolar migration ensures evolutionary unity in the Emperor penguin.

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.

Emperors in hiding: when ice-breakers and satellites complement each other in Antarctic exploration.

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.

The different breeding strategies of penguins: a review.

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 induced 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.

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

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. 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. 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.

Does foraging performance change with age in female little penguins (Eudyptula minor)?

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 middle-aged 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.

Foraging in an oxidative environment: relationship between delta13C values and oxidative status in Adelie penguins.

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 delta(13)C values reflecting their spatial distribution. The oxidative status did not correlate with the foraging trip duration but with the delta(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.

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

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.

Emperor penguin mates: keeping together in the crowd.

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.

Energy saving processes in huddling emperor penguins: from experiments to theory.

This 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 degrees 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.

Role of huddling on the energetic of growth in a newborn altricial mammal.

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.

Body temperature changes induced by huddling in breeding male emperor penguins.

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.

Huddling behavior in emperor penguins: Dynamics of huddling.

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.