Nightly reductions in body temperature and effect of transmitter attachment method in free-living welcome swallows (Hirundoneoxena).

Small birds and mammals face similar energetic challenges, yet use of torpor to conserve energy while resting is considered less common among birds, especially within the most specious order Passeriformes. We conducted the first study to record the natural thermoregulatory physiology of any species from the family Hirundinidae, which we predicted would use torpor because of their specialised foraging by aerial pursuit of flying insects, that are less active during cold or windy weather. We used temperature telemetry on wild-living welcome swallows (Hirundo neoxena, 13 to 17 g) and found that skin temperature declined during nightly resting by an average by 5 °C, from daytime minima of 41.0 ± 0.8 °C to nightly minima of 36.3 ± 0.8 °C, and by a maximum of 8 °C to a minimum recorded skin temperature of 32.0 °C. The extent of reduction in skin temperature was greater on cold nights and following windy daytime (foraging) periods. Further, we found that transmitters glued directly to the skin between feather tracts (i.e., an apterium) provided a less variable and probably also more accurate reflection of body temperature than transmitters applied over closely trimmed feathers. A moderate decrease in skin temperature, equivalent to shallow torpor, would provide energy savings during rest. Yet, deeper torpor was not observed, despite a period of extreme rainfall that presumedly decreased foraging success. Further studies are needed to understand the resting thermoregulatory energetics of swallows under different environmental conditions. We advocate the importance of measuring thermal biology in wild-living birds to increase our knowledge of the physiology and ecological importance of torpor among passerine birds.

The impact of elevated aestivation temperatures on the behaviour of bogong moths (Agrotis infusa).

Bogong moths are an iconic Australian insect. They migrate annually in spring from low elevation locations in southern Australia to the Australian Alps where they aestivate during summer. As summer ends they make their return journey to the breeding grounds where they mate, lay eggs, and die. Given the moth's extreme behaviour in seeking out cool alpine habitat and with the knowledge that average temperatures at their aestivation sites are rising because of climate change, we first asked whether increased temperatures affect bogong moth activity during aestivation. We found that moth behaviour patterns changed from showing peaks at dawn and dusk with supressed activity during the day at cooler temperatures to near-constant activity at all times of day at 15 °C. Second, we asked whether moth mass changes after aestivating at different temperatures for a week due to dehydration or consumption of body energy reserves. We found that moth wet mass loss increased with increasing temperature, but found no difference in dry mass among temperature treatments. Overall, our results suggest that bogong moth aestivation behaviour changes with temperature and that it may be lost at around 15 °C. The impact of warming on the likelihood of individuals to complete their aestivation in the field should be investigated as a matter of priority to better understand the impact of climate change on the Australian alpine ecosystem.

Survivable hypothermia or torpor in a wild-living rat: rare insights broaden our understanding of endothermic physiology.

Maintaining a high and stable body temperature as observed in endothermic mammals and birds is energetically costly. Thus, it is not surprising that we discover more and more heterothermic species that can reduce their energetic needs during energetic bottlenecks through the use of torpor. However, not all heterothermic animals use torpor on a regular basis. Torpor may also be important to an individual's probability of survival, and hence fitness, when used infrequently. We here report the observation of a single, ~ 5.5 h long hypothermic bout with a decrease in body temperature by 12 °C in the native Australian bush rat (Rattus fuscipes). Our data suggest that bush rats are able to rewarm from a body temperature of 24 °C, albeit with a rewarming rate lower than that expected on the basis of their body mass. Heterothermy, i.e. the ability to withstand and overcome periods of reduced body temperature, is assumed to be an evolutionarily ancestral (plesiomorphic) trait. We thus argue that such rare hypothermic events in species that otherwise appear to be strictly homeothermic could be heterothermic rudiments, i.e. a less derived form of torpor with limited capacity for rewarming. Importantly, observations of rare and extreme thermoregulatory responses by wild animals are more likely to be discovered with long-term data sets and may not only provide valuable insight about the physiological capability of a population, but can also help us to understand the constraints and evolutionary pathways of different phenologies.

Thermal energetics and behaviour of a small, insectivorous marsupial in response to the interacting risks of starvation and predation.

Central to understanding animal ecology is how prey cope with the interacting risks of starvation and predation. This trade-off is modulated by the energy requirements of prey, yet relatively few studies have incorporated physiological mechanisms for energy savings when considering the behavioural response of prey to predation risk. In our study, we aimed to determine individual variation in behaviour, resting metabolism, body temperature and response to 24-h starvation within a captive population of fat-tailed dunnarts (Sminthopsis crassicaudata; 15-g insectivorous marsupials), and then, using semi-outdoor enclosures, test whether foraging effort and thermal energetics are adjusted in response to manipulation of ground cover, which for small mammals can simulate predation risk. We found that, under the low cover (high predation risk) treatment, dunnarts consumed less food and employed a greater daily reduction in body temperature between their active and rest phase. This result supports the hypothesis that rest-phase thermoregulatory energy savings are employed, even when food is available, if predation risk is perceived to increase the cost of foraging. Individuals exhibited correlated variation along two orthogonal axes incorporating the measured behavioural and metabolic variables, but these differences were not correlated with responses to starvation and predation risk. Our experiment demonstrates that flexibility in daily energy requirements provided by heterothermy can have important consequences for how small mammals respond to both starvation and predation risks. Such challenges are amplified in degraded habitat with introduced predators, making the capacity for heterothermy an even more important mechanism for survival.

Author Correction: Effects of aging on timing of hibernation and reproduction.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Nocturnal torpor by superb fairy-wrens: a key mechanism for reducing winter daily energy expenditure.

Many passerine birds are small and require a high mass-specific rate of resting energy expenditure, especially in the cold. The energetics of thermoregulation is, therefore, an important aspect of their ecology, yet few studies have quantified thermoregulatory patterns in wild passerines. We used miniature telemetry to record the skin temperature ( Tskin) of free-living superb fairy-wrens ( Malurus cyaneus, 8.6 g; n = 6 birds over N = 7-22 days) and determine the importance of controlled reductions in body temperature during resting to their winter energy budgets. Fairy-wrens routinely exhibited large daily fluctuations in Tskin between maxima of 41.9 ± 0.6°C and minima of 30.4 ± 0.7°C, with overall individual minima of 27.4 ± 1.1°C (maximum daily range: 14.7 ± 0.9°C). These results provide strong evidence of nocturnal torpor in this small passerine, which we calculated to provide a 42% reduction in resting metabolic rate at a Ta of 5°C compared to active-phase Tskin. A capacity for energy-saving torpor has important consequences for understanding the behaviour and life-history ecology of superb fairy-wrens. Moreover, our novel field data suggest that torpor could be more widespread and important than previously thought within passerines, the most diverse order of birds.

Effects of aging on timing of hibernation and reproduction.

Small hibernators are long-lived for their size because seasonal dormancy greatly reduces predation risk. Thus, within a year, hibernators switch between states of contrasting mortality risk (active season versus hibernation), making them interesting species for testing the predictions of life-history theory. Accordingly, we hypothesized that, with advancing age and hence diminishing reproductive potential, hibernators should increasingly accept the higher predation risk associated with activity to increase the likelihood of current reproductive success. For edible dormice (Glis glis) we show that age strongly affects hibernation/activity patterns, and that this occurs via two pathways: (i) with increasing age, dormice are more likely to reproduce, which delays the onset of hibernation, and (ii) age directly advances emergence from hibernation in spring. We conclude that hibernation has to be viewed not merely as an energy saving strategy under harsh climatic conditions, but as an age-affected life-history trait that is flexibly used to maximize fitness.

Torpor reduces predation risk by compensating for the energetic cost of antipredator foraging behaviours.

Foraging activity is needed for energy intake but increases the risk of predation, and antipredator behavioural responses, such as reduced activity, generally reduce energy intake. Hence, the mortality and indirect effects of predation risk are dependent on the energy requirements of prey. Torpor, a controlled reduction in resting metabolism and body temperature, is a common energy-saving mechanism of small mammals that enhances their resistance to starvation. Here we test the hypothesis that torpor could also reduce predation risk by compensating for the energetic cost of antipredator behaviours. We measured the foraging behaviour and body temperature of house mice in response to manipulation of perceived predation risk by adjusting levels of ground cover and starvation risk by 24 h food withdrawal every third day. We found that a voluntary reduction in daily food intake in response to lower cover (high predation risk) was matched by the extent of a daily reduction in body temperature. Our study provides the first experimental evidence of a close link between energy-saving torpor responses to starvation risk and behavioural responses to perceived predation risk. By reducing the risk of starvation, torpor can facilitate stronger antipredator behaviours. These results highlight the interplay between the capacity for reducing metabolic energy expenditure, optimal decisions about foraging behaviour and the life-history ecology of prey.

Late-born intermittently fasted juvenile garden dormice use torpor to grow and fatten prior to hibernation: consequences for ageing processes.

Torpor is thought to slow age-related processes and to sustain growth and fattening of young individuals. Energy allocation into these processes represents a challenge for juveniles, especially for those born late in the season. We tested the hypothesis that late-born juvenile garden dormice (Eliomys quercinus) fed ad libitum ('AL', n = 9) or intermittently fasted ('IF', n = 9) use short torpor bouts to enhance growth and fat accumulation to survive winter. IF juveniles displayed more frequent and longer torpor bouts, compared with AL individuals before hibernation. Torpor frequency correlated negatively with energy expenditure and water turnover. Hence, IF juveniles gained mass at the same rate, reached similar pre-hibernation fattening and displayed identical hibernating patterns and mass losses as AL animals. We found no group differences in relative telomere length (RTL), an indicator of ageing, during the period of highest summer mass gain, despite greater torpor use by IF juveniles. Percentage change in RTL was negatively associated with mean and total euthermic durations among all individuals during hibernation. We conclude that torpor use promotes fattening in late-born juvenile dormice prior to hibernation. Furthermore, we provided the first evidence for a functional link between time spent in euthermy and ageing processes over winter.

Social dominance is associated with individual differences in heart rate and energetic response to food restriction in female red deer.

Energy expenditure is a key mechanism underlying animal ecology, yet why individuals often differ in metabolic rate even under identical conditions remains largely unexplained. Individual variation in metabolism might be explained by correlations with other behavioral and physiological traits, with individual syndromes having environment- or state-dependent costs and benefits to fitness. We tested whether social rank within herds of female red deer is associated with individual differences in resting heart rate, an index of metabolic rate, and energetic response to monthly periods of food restriction during winter in a large outdoor enclosure near Vienna, Austria. Social rank had a strong positive effect on average daily heart rate, independent of the effects of food intake, air temperature, body temperature, and body mass. Subordinate individuals had lower heart rates than dominants, and consequently they suffered lower rates of body mass loss during periods of restricted pellet food supply. A greater capacity to minimize energy requirements might benefit the survival of subdominant female red deer during periods of negative energy balance in winter. Our study provides empirical support in a large mammal for linkages in behavior and metabolism within individuals that have environment-dependent consequences to the energy budget.

Seasonal variation in telomere length of a hibernating rodent.

Small hibernating rodents have greater maximum lifespans and hence appear to age more slowly than similar-sized non-hibernators. We tested for a direct effect of hibernation on somatic maintenance and ageing by measuring seasonal changes in relative telomere length (RTL) in the edible dormouse Glis glis. Average RTL in our population did not change significantly over the hibernation season, and a regression model explaining individual variation in post-hibernation RTL suggested a significant negative effect of the reduction in body mass over the inactive hibernation period (an index of time spent euthermic), supporting the idea that torpor slows ageing. Over the active season, RTL on average decreased in sub-adults but increased in adults, supporting previous findings of greater telomere shortening at younger ages. Telomere length increase might also have been associated with reproduction, which occurred only in adults. Our study reveals how seasonal changes in physiological state influence the progress of life-history traits, such as somatic maintenance and ageing, in a small hibernating rodent.

Daily torpor is associated with telomere length change over winter in Djungarian hamsters.

Ageing can progress at different rates according to an individual's physiological state. Natural hypothermia, including torpor and hibernation, is a common adaptation of small mammals to survive intermittent or seasonal declines in environmental conditions. In addition to allowing energy savings, hypothermia and torpor have been associated with retarded ageing and increased longevity. We tested the hypothesis that torpor use slows ageing by measuring changes in the relative telomere length (RTL) of Djungarian hamsters, Phodopus sungorus, a highly seasonal rodent using spontaneous daily torpor, over 180 days of exposure to a short-day photoperiod and warm (approx. 20°C) or cold (approx. 9°C) air temperatures. Multi-model inference showed that change in RTL within individuals was best explained by positive effects of frequency of torpor use, particularly at low body temperatures, as well as the change in body mass and initial RTL. Telomere dynamics have been linked to future survival and proposed as an index of rates of biological ageing. Our results therefore support the hypothesis that daily torpor is associated with physiological changes that increase somatic maintenance and slow the processes of ageing.

High survival during hibernation affects onset and timing of reproduction.

The timing of reproduction is one of the most crucial life history traits, with enormous consequences for the fitness of an individual. We investigated the effects of season and timing of birth on local survival probability in a small mammalian hibernator, the common dormouse (Muscardinus avellanarius). Local monthly survival probability was lowest in the early active season (May-August, ϕ(adult) = 0.75-0.88, ϕ(juvenile) = 0.61-0.68), increased during the late active season (August-October), and highest during hibernation (October-May, ϕ(adult) = 0.96-0.98, ϕ(juvenile) = 0.81-0.94). Consequently, dormice had an extremely high winter survival probability. We observed two peaks in the timing of reproduction (June and August/September, respectively), with the majority of juveniles born late in the active season. Although early investment in reproduction seems the better life history tactic [survival probability until onset of reproduction: ϕ(born early) = 0.46, 95% confidence interval (CI) 0.28-0.64; ϕ(born late) = 0.19, 95% CI = 0.09-0.28], only females with a good body condition (significantly higher body mass) invest in reproduction early in the year. We suggest the high over-winter survival in dormice allows for a unique life history pattern (i.e., combining slow and fast life history tactics), which leads to a bimodal seasonal birth pattern: (1) give birth as early as possible to allow even the young to breed before hibernating, and/or (2) give birth as late as possible (leaving just enough time for these young to fatten) and enter directly into a period associated with the highest survival rates (hibernation) until maturity.

Hibernation is associated with increased survival and the evolution of slow life histories among mammals.

Survival probability is predicted to underlie the evolution of life histories along a slow-fast continuum. Hibernation allows a diverse range of small mammals to exhibit seasonal dormancy, which might increase survival and consequently be associated with relatively slow life histories. We used phylogenetically informed GLS models to test for an effect of hibernation on seasonal and annual survival, and on key attributes of life histories among mammals. Monthly survival was in most cases higher during hibernation compared with the active season, probably because inactivity minimizes predation. Hibernators also have approximately 15 per cent higher annual survival than similar sized non-hibernating species. As predicted, we found an effect of hibernation on the relationships between life history attributes and body mass: small hibernating mammals generally have longer maximum life spans (50% greater for a 50 g species), reproduce at slower rates, mature at older ages and have longer generation times compared with similar-sized non-hibernators. In accordance with evolutionary theories, however, hibernating species do not have longer life spans than non-hibernators with similar survival rates, nor do they have lower reproductive rates than non-hibernators with similar maximum life spans. Thus, our combined results suggest that (i) hibernation is associated with high rates of overwinter and annual survival, and (ii) an increase in survival in hibernating species is linked with the coevolution of traits indicative of relatively slow life histories.

Regulation of heart rate and rumen temperature in red deer: effects of season and food intake.

Red deer, Cervus elaphus, like other temperate-zone animals, show a large seasonal fluctuation in energy intake and expenditure. Many seasonal phenotypic adjustments are coordinated by endogenous signals entrained to the photoperiod. The cues determining variation in the resting metabolism of ungulates remain equivocal, however, largely because of the confounding effects of food intake and thus the heat increment of feeding. To distinguish endogenous seasonal and environmental effects on metabolism, we subjected 15 female red deer to two feeding treatments, 80% food restriction and low/high protein content, over two winter seasons in a cross-over design experiment. We used rumen-located transmitters to measure heart rate and rumen temperature, which provided indices of metabolism and core body temperature, respectively. Our mixed model (R²=0.85) indicated a residual seasonal effect on mean daily heart rate that was unexplained by the pellet food treatments, activity, body mass or air temperature. In addition to an apparently endogenous down-regulation of heart rate in winter, the deer further reduced heart rate over about 8 days in response to food restriction. We found a strong correlation between rumen temperature and seasonal or periodic variation in heart rate. An effect of lowered rumen (and hence core body) temperature was enhanced during winter, perhaps owing to peripheral cooling, which is known to accompany bouts of hypometabolism. Our experimental results therefore support the hypothesis that a reduction in body temperature is a physiological mechanism employed even by large mammals, like red deer, to reduce their energy expenditure during periods of negative energy balance.

Senescence is more important in the natural lives of long- than short-lived mammals.

BACKGROUND: Senescence has been widely detected among mammals, but its importance to fitness in wild populations remains controversial. According to evolutionary theories, senescence occurs at an age when selection is relatively weak, which in mammals can be predicted by adult survival rates. However, a recent analysis of senescence rates found more age-dependent mortalities in natural populations of longer lived mammal species. This has important implications to ageing research and for understanding the ecological relevance of senescence, yet so far these have not been widely appreciated. We re-address this question by comparing the mean and maximum life span of 125 mammal species. Specifically, we test the hypothesis that senescence occurs at a younger age relative to the mean natural life span in longer lived species. METHODOLOGY/PRINCIPAL FINDINGS: We show, using phylogenetically-informed generalised least squares models, a significant log-log relationship between mean life span, as calculated from estimates of adult survival for natural populations, and maximum recorded life span among mammals (R2=0.57, p<0.0001). This provides further support for a key prediction of evolutionary theories of ageing. The slope of this relationship (0.353+/-0.052 s.e.m.), however, indicated that mammals with higher survival rates have a mean life span representing a greater fraction of their potential maximum life span: the ratio of maximum to mean life span decreased significantly from >10 in short-lived to approximately 1.5 in long-lived mammal species. CONCLUSIONS/SIGNIFICANCE: We interpret the ratio of maximum to mean life span to be an index of the likelihood an individual will experience senescence, which largely determines maximum life span. Our results suggest that senescence occurs at an earlier age relative to the mean life span, and therefore is experienced by more individuals and remains under selection pressure, in long- compared to short-lived mammals. A minimum rate of somatic degradation may ultimately limit the natural life span of mammals. Our results also indicate that senescence and modulating factors like oxidative stress are increasingly important to the fitness of longer lived mammals (and vice versa).

Introducing mother's curse: low male fertility associated with an imported mtDNA haplotype in a captive colony of brown hares.

Mitochondrial DNA mutations create variation in the efficiency of the oxidative phosphorylation pathway and therefore cellular energy production. Mildly deleterious mutations may reduce the performance of sperm cells in particular, due to their high energy requirements and low number of mitochondria, yet have little or no effect on the viability of somatic cells or ova. Mutations will be maintained in the population, despite the fitness cost for males, because mtDNA is passed down the female line. We looked for this so-called mother's curse effect in our captive colony of European brown hares. Significantly reduced male reproductive success was detected for a divergent haplotype that could be traced back to hares imported from a remote population. Median reproductive success for these hares was 0.17 compared to 0.49 for the indigenous haplotypes (Wilcoxon rank-sum, P = 0.002). No difference was detected for female reproductive success, nor were we able to find a nuclear DNA component to variation in male fertility. Our data are strong evidence for a mother's curse effect persisting despite multiple crossings over seven generations. These data raise important issues relating to the reproductive fitness of small or intermixing populations and have particular implications for the management of populations for conservation.

Hibernation and daily torpor minimize mammalian extinctions.

Small mammals appear to be less vulnerable to extinction than large species, but the underlying reasons are poorly understood. Here, we provide evidence that almost all (93.5%) of 61 recently extinct mammal species were homeothermic, maintaining a constant high body temperature and thus energy expenditure, which demands a high intake of food, long foraging times, and thus exposure to predators. In contrast, only 6.5% of extinct mammals were likely heterothermic and employed multi-day torpor (hibernation) or daily torpor, even though torpor is widespread within more than half of all mammalian orders. Torpor is characterized by substantial reductions of body temperature and energy expenditure and enhances survival during adverse conditions by minimizing food and water requirements, and consequently reduces foraging requirements and exposure to predators. Moreover, because life span is generally longer in heterothermic mammals than in related homeotherms, heterotherms can employ a 'sit-and-wait' strategy to withstand adverse periods and then repopulate when circumstances improve. Thus, torpor is a crucial but hitherto unappreciated attribute of small mammals for avoiding extinction. Many opportunistic heterothermic species, because of their plastic energetic requirements, may also stand a better chance of future survival than homeothermic species in the face of greater climatic extremes and changes in environmental conditions caused by global warming.

Hibernation by a free-ranging subtropical bat (Nyctophilus bifax).

Knowledge about torpor in free-ranging subtropical bats is scarce and it is widely believed that low and stable ambient temperatures are necessary for prolonged torpor. We present temperature-telemetry data from free-ranging male (n = 4) and female (n = 4) subtropical vespertilionid bats, Nyctophilus bifax (approximately 10 g), exposed to pronounced daily fluctuations of ambient temperature. All bats used torpor on every day in winter and both males and females exhibited multi-day torpor bouts of up to 5.4 days. Although females were larger than males, patterns of torpor were similar in both sexes. Torpor use was correlated with prevailing weather conditions and, on days when bats remained torpid, maximum ambient temperature was significantly lower than on days when bats aroused. Moreover, the duration of interbout normothermic periods at night increased with increasing average nightly ambient temperature. Skin temperature of torpid bats varied by 10.2 +/- 3.6 degrees C day(-1) (n = 8, N = 47) and daily minimum skin temperature was positively correlated with the daily minimum ambient temperature. Our study shows that prolonged torpor is an important component of the winter ecology of a subtropical bat and that torpor and activity patterns of N. bifax predominantly reflect prevailing weather conditions.

Timing of the daily temperature cycle affects the critical arousal temperature and energy expenditure of lesser long-eared bats.

Daily patterns of body temperature (T(b)) and energy expenditure in heterothermic endotherms are affected by changes in ambient temperature (T(a)) and selection of suitable microclimates, yet most laboratory studies employ constant T(a) to measure metabolic rates. In particular, exposure to a daily temperature cycle, even within rest shelters, may be important in timing of torpor and arousal and determining resting energy costs in wild animals. We tested how captive bats (Nyctophilus geoffroyi; 7 g) exposed to a diurnal T(a) fluctuation (between 13 degrees C and 27 degrees C), similar to natural conditions in their summer tree roosts, adjusted the timing of daily arousals. To distinguish the effects of T(a) and passive rewarming from time of the day, we shifted the heating phase to commence at 06:00 h, 09:00 h or 12:00 h on each day. Bats entered torpor overnight and aroused the next day at a time corresponding to rising T(a) and passive rewarming. The critical T(a) (and torpid T(b)) for arousal was not fixed, however, but was lower when heating occurred later in the rest phase, providing the first evidence that the critical arousal T(a) is affected by time of the day. Bats re-entered torpor in response to cooling late in the afternoon, yet always aroused at lights off. A period of normothermic thermoregulation was therefore closely synchronised with maximum daily T(a), indicating a trade-off between the benefits and energetic costs of normothermia during resting. Our experiment clearly shows that a daily T(a) cycle affects the thermoregulatory behaviour and energetics of these small bats. More generally, these results demonstrate the critical influence of behavioural decisions on the daily energy expenditure of small heterothermic mammals.