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.     

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.     

How do weather conditions affect the huddling behaviour of emperor penguins?

Huddling allows emperor penguins to conserve energy and survive their long winter fast while facing harsh climatic conditions. Here we report the first investigation into the effects of changes in wind speed and ambient temperature on different components of penguin huddling behaviour. We attached light and temperature recorders to male emperor penguins at the Pointe Géologie colony, Antarctica, which recorded huddling events. We then compared the frequency, duration, occurrence and intensity of huddling bouts, with ambient air temperatures and wind speeds. Huddling occurrence increased with lower ambient temperatures and higher wind speeds, whereas huddling intensity was mainly enhanced by lower ambient temperatures. Moreover, huddling group movements were linked to wind direction and its global density to lower ambient temperatures. Hence, emperor penguins complex huddling behaviour was modulated differently depending on these two parameters. Weather conditions may then affect emperor penguins ability to save energy and survive their winter fast.     

Energetics and geometry of huddling in small mammals

Huddling in small mammals appears as an efficient response to low ambient temperatures with important consequences in thermoregulatory energy savings. These energy savings have been ascribed to a decrease in the exposed area in relation to the animal's volume. It has been proposed that during huddling reductions in the exposed area and in the metabolic rate are equal functions of the number of grouped individuals with a common exponent of -1/3. However, reported data shows a great variability of this exponent. In this paper we present a geometrical and energetic analysis on several huddling efficiencies in small mammals and in geometric bodies. Our theoretical analysis shows a variability in the efficiency of huddling, depending on the morphological characteristics of the geometric bodies. At the same time original and literature information show an analogous interspecific variability in small mammals. Finally, a general mathematical expression is proposed which represents and explains the energetic and geometric specific variations of huddling in small mammals.     

Dynamic thermal balance in the leaf-eared mouse: the interplay among ambient temperature,body size,and behavior

Endotherms maintain constant body temperature through physiological and behavioral adjustments. Behavioral thermoregulation is an important factor influencing energy balance. We exposed the leaf-eared mouse, Phyllotis darwini, to temperatures corresponding to its natural thermal range and studied two forms of behavioral thermoregulation: diminishing surface to volume ratio by huddling and heat dissipation by increasing physical contact with the substrate (flattening). We predicted that at low ambient temperatures (T(a)) huddling would be used as a heat conservation mechanism and at high T(a) flattening would be used for heat loss. We simultaneously measured oxygen consumption (VO2) and flattening, in response to three independent factors: huddling, T(a), and body mass. Each experiment was a 6-h VO2 trial where five virgin females were measured at constant T(a). We performed this protocol for two body mass groups, small (ca. 40 g) and large (ca. 70 g), in a metabolic chamber. Treatments were groups with and without the ability to huddle at five different T(a), ranging from 5 degrees to 35 degrees C. A significant interaction between all three factors was found. Huddling and flattening were used as strategies for conserving or dissipating heat, respectively, and the shift between both strategies occurred at the lower limit of thermoneutrality. At T(a) below thermoneutrality, huddling was a more effective way of reducing metabolic requirements and was more efficient (H(E)) in small individuals than large individuals. So, by huddling, small individuals save more energy. At high T(a), flattening appeared to be an equally useful mechanism for heat loss, for both large and small animals.     

Heterothermy, and the energetic consequences of huddling in small migrating passerine birds

The success of migration of small passerine birds depends largely on effective refueling at stopover sites. In our previous studies, we found that hypothermia facilitates accumulation of fuel at the beginning of a stopover. Later we found that blackcaps, Sylvia atricapilla, might further reduce their energy expenditure by huddling while at rest. Here, we report experimental results supporting our hypothesis that huddling is beneficial to small migrating passerines both from energetic and thermoregulatory points of view. To test this hypothesis we measured metabolic rates and body temperatures of seven blackcaps placed in respirometry chambers overnight, either solitarily or in groups of three or four at ambient temperatures of 5, 10, and 15°C. Concurring with our predictions, huddling blackcaps maintained higher body temperatures than did solitary birds, but had mass-specific metabolic rates lower by ～30% than those of solitary individuals. Based on our previous studies, we estimated energy savings through huddling to be comparable to energy savings through hypothermia in solitary blackcaps and suggest that huddling may be an important way of saving energy for small passerine birds resting at migratory stopovers. At the same time it might offer the additional benefit of lower risk of predation. In this light, we predict that huddling occurs frequently in nature, leading to significant savings of energy, faster accumulation of fuel, presumably lower risk of becoming a prey, more successful migration, and eventually increased fitness.     

The automated analysis of clustering behaviour of piglets from thermal images in response to immune challenge by vaccination

An automated method of estimating the spatial distribution of piglets within a pen was used to assess huddling behaviour under normal conditions and during a febrile response to vaccination. The automated method was compared with a manual assessment of clustering activity. Huddling behaviour was partly related to environmental conditions and clock time such that more huddling occurred during the night and at lower ambient air temperatures. There were no positive relationships between maximum pig temperatures and environmental conditions, suggesting that the narrow range of air temperatures in this study was not a significant factor for pig temperature. Spatial distribution affected radiated pig temperature measurements by IR thermography. Higher temperatures were recorded in groups of animals displaying huddling behaviour. Huddling behaviour was affected by febrile responses to vaccination with increased huddling occurring 3 to 8 h post-vaccination. The automated method of assessing spatial distribution from an IR image successfully identified periods of huddling associated with a febrile response, and to changing environmental temperatures. Infrared imaging could be used to quantify temperature and behaviour from the same images.     

Behavioural Thermoregulation in a Small Neotropical Primate

The maintenance of body temperature in endothermic animals imposes considerable metabolic costs that vary with air temperature fluctuations. To minimise these costs, endotherms can adopt certain behaviours to adjust the pattern of heat transfer between their bodies and the environment. In this study, we evaluated whether a small Neotropical primate, the black‐fronted titi monkey (Callicebus nigrifrons), living in a seasonal environment can use behavioural mechanisms to cope with fluctuations in the air temperature. We monitored the air temperature and the titi monkeys’ behaviour over 1 yr. When the animals were inactive, we recorded the microhabitat used, the huddling between individuals and the body postures adopted. The monkeys primarily responded to air temperature fluctuations through microhabitat selection: they spent more time in sunny places and used higher strata of forest under lower temperatures. Moreover, they used sunny microhabitats during the first hour of their active period after colder nights. The monkeys did not huddle or change body postures in response to air temperature fluctuations. Huddling behaviour seemed to be primarily influenced by social interactions, and body postures were more energy conserving, regardless of temperature. Titi monkeys, however, used more energy‐conserving postures and huddling behaviour under cloudy conditions than sunny conditions, suggesting that these behaviours may be important when they are unable to thermoregulate by microhabitat selection. We concluded that fluctuations in air temperature can promote significant changes in the behaviour of titi monkeys and can impose important restrictions on mammals’ activities, even in tropical regions.     

温度与聚群对三种仔兽热能代谢的影响

仔兽出生以前,是在相对稳定而安全的母兽子宫内生活的,出生以后,仔兽的营养条件与环境温度即起了根本的变化。新生仔兽是如何适应新环境的?仔兽在新环境中的生活能力怎样?环境温度与食物条件对新生仔兽的存活率、生长与发育的影响如何?环境温度和聚群行为与能量代谢的关系怎样?这是一系列的基础理论问题,尤其是毛皮动物饲养业所关心的实际问题。     

Metabolic and thermoregulatory consequences of social behaviors between Microtus townsendii

1. Townsend voles responded to each other by raising their core temperatures. 2. Increments of temperature increases that accompanied hostile reactions between voles, were proportional to the intensity of the behavioral displays. 3. Amicable behaviors (huddling) were also associated with higher body temperatures that were proportional to group size. 4. Huddling voles conserved metabolic energy expenditure by reducing their metabolic rates and thermal conductances. 5. Such conservation required 1 or more days of amicable behavior to develop, and to be reversed. 6. The degree of metabolic rate reduction that accompanied amicable huddling behavior and the associated reduction of thermal conductance was independent of group size.     

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.     

秦岭川金丝猴个体间团抱模式及其影响因素

团抱行为作为保持体温与增进社会关系的一种有效途经在非人灵长类中广泛存在,受环境和社会因素影响在各物种间呈现出多样的模式。本研究自2007 年9 月至2008 年4 月间,运用焦点动物取样法和瞬时扫描取样法对秦岭北坡周至国家级自然保护区内的一群秦岭川金丝猴的团抱模式进行了1 637 回次的扫描,结果表明研究群内的个体回避单独休息,倾向于形成团抱,团抱主要发生在2 个或3 个个体之间,较少形成4 个或4 个以上个体的团抱;团抱主要由青少年个体和成年雌性组成,成年雄性和携婴雌性多参与小的团抱,青少年猴更频繁地出现在3 个个体的团抱中,未携婴雌性在4 个和4 个以上个体团抱中比例明显增加;秦岭川金丝猴各年龄性别组的个体对团抱伙伴的选择有各自的偏好,大多数团抱由成年雄性和未成年个体发起,但获得较少的团抱;雌性和携婴雌性较少主动发出但获得较多的团抱,这显示出雌性作为团抱的主体具有很高的社会亲和力;此外团抱模式还存在季节性的变化,冬季寒冷期团抱的频率和大小都会增加,并且个体选择在距离地面较近的区域团抱以保持体温,春季生育期个体倾向于在树冠层团抱以获得新鲜的食物并且避免婴猴被捕食。秦岭川金丝猴的团抱行为是物种在其独特的社会组织形式下对山地极端环境的一种适应,在进化中以行为模式获得更高适合度的具体策略。     

Huddling house sparrows remain euthermic at night,and conserve body mass

An advantage of huddling in the cold is that the individual animals involved can maintain body temperature while saving energy. Since house sparrows Passer domesticus biblicus store little fat, but inhabit relatively cold climates, we tested the hypothesis that they huddle at night. While recording body temperature and body mass of 18 house sparrows when they were either caged individually, or free in an aviary, we observed that when free in the aviary, the sparrows huddled at low ambient temperatures and more birds huddled, in tighter and tighter formation, as ambient temperature decreased. However, their body temperatures were not significantly different from when they spent the night individually caged. When free to huddle, the birds lost significantly less body mass during the course of a day than when individually caged. This reduction in body mass loss may be of particular importance during periods of adverse environmental conditions, especially for small birds that manage their energy budgets on a daily basis.     

Lower critical temperature and cold-induced thermogenesis of lean and overweight humans are inversely related to body mass and basal metabolic rate

It is colloquially stated that body size plays a role in the human response to cold, but the magnitude and details of this interaction are unclear. To explore the inherent influence of body size on cold-exposed metabolism, we investigated the relation between body composition and resting metabolic rate in humans at thermoneutrality and during cooling within the nonshivering thermogenesis range. Body composition and resting energy expenditure were measured in 20 lean and 20 overweight men at thermoneutrality and during individualized cold exposure. Metabolic rates as a function of ambient temperature were investigated considering the variability in body mass and composition. We observed an inverse relationship between body size and the lower critical temperature (LCT), i.e. the threshold where thermoneutrality ends and cold activates thermogenesis. LCT was higher in lean than overweight subjects (22.1 ± 0.6 vs 19.5 ± 0.5 °C, p < 0.001). Below LCT, minimum conductance was identical between lean and overweight (100 ± 4 vs 97 ± 3 kcal/°C/day respectively, p = 0.45). Overweight individuals had higher basal metabolic rate (BMR) explained mostly by the higher lean mass, and lower cold-induced thermogenesis (CIT) per degree of cold exposure. Below thermoneutrality, energy expenditure did not scale to lean body mass. Overweight subjects had lower heat loss per body surface area (44.7 ± 1.3 vs 54.7 ± 2.3 kcal/°C/m²/day, p < 0.001). We conclude that larger body sizes possessed reduced LCT as explained by higher BMR related to more lean mass rather than a change in whole-body conductance. Thus, larger individuals with higher lean mass need to be exposed to colder temperatures to activate CIT, not because of increased insulation, but because of a higher basal heat generation. Our study suggests that the distinct effects of body size and composition on energy expenditure should be taken in account when exploring the metabolism of humans exposed to cold.     

The costs of keeping cool in a warming world: implications of high temperatures for foraging,thermoregulation and body condition of an arid‐zone bird

Recent mass mortalities of bats, birds and even humans highlight the substantial threats that rising global temperatures pose for endotherms. Although less dramatic, sublethal fitness costs of high temperatures may be considerable and result in changing population demographics. Endothermic animals exposed to high environmental temperatures can adjust their behaviour (e.g. reducing activity) or physiology (e.g. elevating rates of evaporative water loss) to maintain body temperatures within tolerable limits. The fitness consequences of these adjustments, in terms of the ability to balance water and energy budgets and therefore maintain body condition, are poorly known. We investigated the effects of daily maximum temperature on foraging and thermoregulatory behaviour as well as maintenance of body condition in a wild, habituated population of Southern Pied Babblers Turdoides bicolor. These birds inhabit a hot, arid area of southern Africa where they commonly experience environmental temperatures exceeding optimal body temperatures. Repeated measurements of individual behaviour and body mass were taken across days varying in maximum air temperature. Contrary to expectations, foraging effort was unaffected by daily maximum temperature. Foraging efficiency, however, was lower on hotter days and this was reflected in a drop in body mass on hotter days. When maximum air temperatures exceeded 35.5 °C, individuals no longer gained sufficient weight to counter typical overnight weight loss. This reduction in foraging efficiency is likely driven, in part, by a trade‐off with the need to engage in heat‐dissipation behaviours. When we controlled for temperature, individuals that actively dissipated heat while continuing to forage experienced a dramatic decrease in their foraging efficiency. This study demonstrates the value of investigations of temperature‐dependent behaviour in the context of impacts on body condition, and suggests that increasingly high temperatures will have negative implications for the fitness of these arid‐zone birds.     

Bioenergetic benefits of huddling by deer mice (Peromyscus maniculatus)

Both short photoperiod and communal social living conserve metabolic energy by deer mice held in thermal neutral ambient temperatures. Initial socialization was energetically more costly than solitary living, but huddling behaviors reduced thermal conductance and mass specific metabolic rate by 30% within 5 days. While short photoperiod reduced metabolic energy expenditure by decreasing thermoregulatory demand, huddling mediated behavioral conservation was achieved with hyperthermic core temperatures.     

That’s hot: golden spiny mice display torpor even at high ambient temperatures

Golden spiny mice (Acomys russatus) living in the Judean desert are exposed to extended periods of food and water shortage. We investigated their thermal and metabolic response to three weeks of 50 % food reduction at ambient temperatures of 23, 27, 32 and 35 °C by long term records of metabolic rate and body temperature in the laboratory. At all ambient temperatures, A. russatus responded to starvation by a reduction of daily energy expenditure. At 32 and 35 °C, this metabolic adjustment fully compensated the reduced food availability and they maintained their energy balance at a slightly reduced body mass. At lower ambient temperatures, they could not fully compensate for the reduced food availability and kept a negative energy balance. The reduction of daily energy expenditure was largely achieved by the occurrence of daily torpor. Torpor even occurred at high ambient temperatures of 32 and 35 °C during which metabolic depression was not associated with a marked decrease of body temperature. The results show that the occurrence of daily torpor is not necessarily linked to cold exposure and the development of a pronounced hypothermia, but may even occur as depression of metabolic rate in a hot environment.     

Radiant heat affects thermoregulation and energy expenditure during rewarming from torpor

The high expenditure of energy required for endogenous rewarming is one of the widely perceived disadvantages of torpor. However, recent evidence demonstrates that passive rewarming either by the increase of ambient temperature or by basking in the sun appears to be common in heterothermic birds and mammals. As it is presently unknown how radiant heat affects energy expenditure during rewarming from torpor and little is known about how it affects normothermic thermoregulation, we quantified the effects of radiant heat on body temperature and metabolic rate of the small (body mass 25 g) marsupial Sminthopsis macroura in the laboratory. Normothermic resting individuals exposed to radiant heat were able to maintain metabolic rates near basal levels (at 0.91 ml O(2) g(-1) h(-1)) and a constant body temperature down to an ambient temperature of 12 degrees C. In contrast, metabolic rates of individuals without access to radiant heat were 4.5-times higher at an ambient temperature of 12 degrees C and body temperature fell with ambient temperature. During radiant heat-assisted passive rewarming from torpor, animals did not employ shivering but appeared to maximise uptake of radiant heat. Their metabolic rate increased only 3.2-times with a 15- degrees C rise of body temperature (Q(10)=2.2), as predicted by Q(10) effects. In contrast, during active rewarming shivering was intensive and metabolic rates showed an 11.6-times increase. Although body temperature showed a similar absolute change between the beginning and the end of the rewarming process, the overall energetic cost during active rewarming was 6.3-times greater than that during passive, radiant heat-assisted rewarming. Our study demonstrates that energetic models assuming active rewarming from torpor at low ambient temperatures can substantially over-estimate energetic costs. The low energy expenditure during passive arousal provides an alternative explanation as to why daily torpor is common in sunny regions and suggests that the prevalence of torpor in low latitudes may have been under-estimated in the past.     

Huddling relationships in night sleeping groups among wild Japanese macaques in Kinkazan Island during winter

Huddling groups at sleeping sites, and allogrooming and proximity in the daytime during winter, were examined in a wild Japanese macaque (Macaca fuscata) troop on Kinkazan Island in the non-snowy district of northern Japan. All sleeping groups, defined as a cluster in which individuals huddle at sleeping sites, were formed on the ground. Their sizes tended to increase when the temperature was lower. The number of adults with mutual physical contact in sleeping groups increased when the size of sleeping groups increased. These results suggest that the physiological function of huddling is protection from low temperatures, and that macaques select the ground as sleeping sites to form large sized groups. Huddling was performed most frequently among kin dyads. Non-related dyads which appeared to be affiliative in the daytime also huddled frequently at sleeping sites. Even non-related dyads which showed affiliative behavior less frequently in the daytime exhibited huddling, at night, however, they did so less often than those of kin dyads and affiliated dyads. It appears that huddling at night by pairs that did not normally affiliate in the daytime was made possible by the increased tolerance of individuals responding to colder temperatures at night in winter. Furthermore, huddling, grooming, and proximity were exhibited at greater frequency between kin dyads, and between high-ranking males and specific females of kin groups, although the dyads of individuals older than 15 years often were involved only in huddling. These results suggest that two types of social bonds exist at sleeping sites in winter. One is the social bond common to both the daytime and nighttime, the other is peculiar to nighttime. Consequently, the social function of huddling is that, troop integration might increase at sleeping sites in winter as close social relationships among adults are extended more widely than those in daytime.     

晚成性哺乳动物体温调节能力的胎后发育

按照体温调节能力的发育情况,哺乳动物的生长发育可分为早成性、晚成性和未成熟性3类。本文主要综述了晚成性哺乳动物体温调节能力的发育特点。这类动物的幼体出生时一般身体裸露,热传导率较高,产热能力较差,不能进行有效的体温调节。当环境温度低于热中性区时,单独的个体不能维持较高的恒定体温。但晚成性幼体也具有一定的体温调节能力,当受低温刺激时,即使新生幼体也会具有增加代谢率的反应;同时结合亲体关怀和幼体之间的聚群效应以及巢的保温作用等方式,仍能使其体温维持在一个较高的水平。晚成性幼体生理性产热的不足,也可看作是一种有利的特点,这样可以减少能量在体温调节方面的消耗,从而增加用于生长发育的能量。文章最后对可能的发展方向进行了展望。