Torpor and activity in a free-ranging tropical bat: implications for the distribution and conservation of mammals?

Bats are most diverse in the tropics, but there are no quantitative data on torpor use for energy conservation by any tropical bat in the wild. We examined the thermal biology, activity patterns and torpor use of two tree-roosting long-eared bats (Nyctophilus geoffroyi, 7.8?g) in tropical northern Australia in winter using temperature telemetry. Bats commenced activity about 20?min after sunset, ended activity about 2.5?h before sunrise and entered torpor everyday in the early morning even when minimum ambient temperatures (T _a) were as high as 23°C. On average, bats remained torpid for almost 5?h, mean minimum skin temperature (T _skin) measured was 22.8?±?0.1°C and daily T _skin minima were correlated with T _a. Our study shows that even in the tropics, torpor is frequently employed by bats, suggesting that worldwide most bat species are heterothermic and use torpor for energy conservation. We propose that the ability of employing torpor and the resulting highly plastic energy requirements may partially explain why these small insectivorous bats can inhabit almost the entire Australian continent despite vastly different climatic and likely trophic conditions. Reduced energy requirements also may permit survival in degraded or modified habitats, reduce the need for foraging and reduce exposure to predators. Thus, the ability to employ torpor may be one important reason for why most Australian bats and other heterothermic mammals have not gone extinct whereas many obligatory homeothermic mammals that cannot employ torpor and have high energy and foraging requirements have suffered high rates of extinctions.     

Photoperiod affects daily torpor and tissue fatty acid composition in deer mice

Photoperiod and dietary lipids both influence thermal physiology and the pattern of torpor of heterothermic mammals. The aim of the present study was to test the hypothesis that photoperiod-induced physiological changes are linked to differences in tissue fatty acid composition of deer mice, Peromyscus maniculatus (∼18-g body mass). Deer mice were acclimated for >8 weeks to one of three photoperiods (LD, light/dark): LD 8:16 (short photoperiod), LD 12:12 (equinox photoperiod), and LD 16:8 (long photoperiod). Deer mice under short and equinox photoperiods showed a greater occurrence of torpor than those under long photoperiods (71, 70, and 14%, respectively). The duration of torpor bouts was longest in deer mice under short photoperiod (9.3 ± 2.6 h), intermediate under equinox photoperiod (5.1 ± 0.3 h), and shortest under long photoperiod (3.7 ± 0.6 h). Physiological differences in torpor use were associated with significant alterations of fatty acid composition in ∼50% of the major fatty acids from leg muscle total lipids, whereas white adipose tissue fatty acid composition showed fewer changes. Our results provide the first evidence that physiological changes due to photoperiod exposure do result in changes in lipid composition in the muscle tissue of deer mice and suggest that these may play a role in survival of low body temperature and metabolic rate during torpor, thus, enhancing favourable energy balance over the course of the winter.     

Fat and fed: frequent use of summer torpor in a subtropical bat

A widely held view is that torpor is avoided by mammals whenever possible because of potential costs associated with reduced body temperatures and slowed metabolic processes. We examined this hypothesis by quantifying use of torpor in relation to body condition of free-ranging northern long-eared bats (Nyctophilus bifax, approximately 10 g), a species known to hibernate, from a subtropical region during the austral summer when insects were abundant. Temperature-telemetry revealed that bats used torpor on 85% of observation days and on 38% of all nights. Torpor bouts ranged from 0.7 to 21.2 h, but the relationship between duration of torpor bouts and ambient temperature was not significant. However, skin temperature of torpid bats was positively correlated with ambient temperature. Against predictions, individuals with a high body condition index (i.e., good fat/energy reserves) expressed longer and deeper torpor bouts and also employed torpor more often during the activity phase at night than those with low body condition index. We provide the first evidence that use of torpor in a free-ranging subtropical mammal is positively related with high body condition index. This suggests that employment of torpor is maximised and foraging minimised not because of food shortages or low energy stores but likely to avoid predation when bats are not required to feed.     

Torpor and basking in a small arid zone marsupial

The high energetic cost associated with endothermic rewarming from torpor is widely seen as a major disadvantage of torpor. We tested the hypothesis that small arid zone marsupials, which have limited access to energy in the form of food but ample access to solar radiation, employ basking to facilitate arousal from torpor and reduce the costs of rewarming. We investigated torpor patterns and basking behaviour in free-ranging fat-tailed dunnarts Sminthopsis crassicaudata (10 g) in autumn and winter using small, internal temperature-sensitive transmitters. Torpid animals emerged from their resting sites in cracking soil at ∼1000 h with body temperatures as low as 14.6°C and positioned themselves in the sun throughout the rewarming process. On average, torpor duration in autumn was shorter, and basking was less pronounced in autumn than in winter. These are the first observations of basking during rewarming in S. crassicaudata and only the second direct evidence of basking in a torpid mammal for the reduction of energetic costs during arousal from torpor and normothermia. Our findings suggest that although overlooked in the past, basking may be widely distributed amongst heterothermic mammals. Therefore, the energetic benefits from torpor use in wild animals may currently be underestimated.     

Torpor in free-ranging antechinus: does it increase fitness?

Antechinus are small, insectivorous, heterothermic marsupial mammals that use torpor from late summer to early winter and reproduce once a year in late winter/early spring. Males die after mating, most females produce only a single litter, but some survive a second winter and produce another litter. As it is not known how these females manage to survive the second winter after the energetically demanding reproductive period and then reproduce a second time, we aimed to provide the first data on thermal biology of free-ranging antechinus by using temperature telemetry. Male Antechinus stuartii and Antechinus flavipes rarely entered torpor in autumn/early winter in the wild, expressing only shallow bouts of <2 h. Female A. stuartii used torpor extensively, employing bouts up to 16.7 h with body temperatures as low as 17.8 °C. Interestingly, although first and second year females used similar torpor patterns, torpor occurrence was almost twofold in second year (93 % of days) than first year females (49 %), and the proportion of the overall monitoring period animals spent torpid was 3.2-fold longer in the former with a corresponding shorter activity period. Our study suggests that intensive use of torpor is crucial for second year females for autumn and winter survival and production of a second litter. We provide the first evidence of an age-related pattern in daily torpor expression in free-ranging mammals and show that torpor use is a complex process that is affected not only by the current energy availability and thermal conditions but also by the reproductive history and age of individuals.     

Torpor use during gestation and lactation in a primate

Torpor is an energy-saving mechanism that allows endotherms to overcome energetic challenges. Torpor should be avoided during reproduction because of potential incompatibility with offspring growth. To test if torpor can be used during gestation and lactation to compensate for food shortage, we exposed reproductive female grey mouse lemurs (Microcebus murinus), a heterothermic primate, to different levels of food availability. Torpor use was characterised by daily skin temperature profiles, and its energetic outcome was assessed from changes in body mass. Food shortage triggered torpor during the end of the gestation period (n = 1), ranging from shallow in response to 40% food restriction to deep daily torpor in response to 80% restriction. During the early period of lactation, females fed ad libitum (n = 2) or exposed to a 40% restriction (n = 4) remained normothermic; but 80% food restricted females (n = 5) gave priority to energy saving, increasing the frequency and depth of torpor bouts. The use of torpor was insufficient to compensate for 80% energetic shortage during lactation resulting in loss of mass from the mother and delayed growth in the pups. This study provides the first evidence that a heterothermic primate can use torpor to compensate for food shortages even during reproduction. This physiological flexibility likely evolved as a response to climate-driven fluctuations in food availability in Madagascar.     

The key to winter survival: daily torpor in a small arid-zone marsupial

Mammalian hibernation, which lasts on average for about 6 months, can reduce energy expenditure by >90% in comparison to active individuals. In contrast, the widely held view is that daily torpor reduces energy expenditure usually by about 30%, is employed for a few hours every few days, and often occurs only under acute energetic stress. This interpretation is largely based on laboratory studies, whereas knowledge on daily torpor in the field is scant. We used temperature telemetry to quantify thermal biology and activity patterns of a small arid-zone marsupial, the stripe-faced dunnart Sminthopsis macroura (16.9 g), in the wild and to test the hypothesis that daily torpor is a crucial survival strategy of this species in winter. All individuals entered torpor daily with the exception of a single male that remained normothermic for a single day (torpor on 212 of 213 observation days, 99.5%). Torpor was employed at air temperatures (T _a) ranging from approximately −1°C to 36°C. Dunnarts usually entered torpor during the night and aroused at midday with the daily increase of T _a. Torpor was on average about twice as long (mean 11.0 ± 4.7 h, n = 8) than in captivity. Animals employed sun basking during rewarming, reduced foraging time significantly, and occasionally omitted activity for several days in sequence. Consequently, we estimate that daily torpor in this species can reduce daily energy expenditure by up to 90%. Our study shows that for wild stripe-faced dunnarts daily torpor is an essential mechanism for overcoming energetic challenges during winter and that torpor data obtained in the laboratory can substantially underestimate the ecological significance of daily torpor in the wild.     

To use or not to use torpor? Activity and body temperature as predictors

When food is limited and/or environmental conditions are unfavourable, many mammals reduce activity and use torpor to save energy. Nevertheless, reliable predictors for torpor occurrence, especially in the wild, are currently not available. Interrelations between torpor use and other energy conserving strategies are also poorly understood. We tested the hypothesis that reductions in normothermic body temperature (T _b) and the period of activity before torpor events could be used as predictors for torpor occurrence in sugar gliders, Petaurus breviceps (body mass, ∼125 g), known to display daily torpor in the wild. Occurrence of torpor was preceded by significant (∼10–25%) reductions of the duration of the activity phase. Moreover, the normothermic resting T _b fell by an average of 1.2°C over 3 days before a torpor event, relative to individuals that did not display torpor. Our new findings suggest that before entering torpor, sugar gliders, which appear to use torpor as an emergency measure rather than a routine energy saving strategy, systematically reduce activity times and normothermic resting T _bs to lower energy expenditure and perhaps to avoid employing torpor. Thus, reduced activity and normothermic T _b may provide a predictive tool for the occurrence of daily torpor in the wild.     

Deep, prolonged torpor by pregnant, free-ranging bats

Many mammals save energy during food shortage or harsh weather using controlled reductions in body temperature and metabolism called torpor. However, torpor slows offspring growth, and reproductive individuals are thought to avoid using it because of reduced fitness resulting from delayed offspring development. We tested this hypothesis by investigating torpor during reproduction in hoary bats (Lasiurus cinereus, Vespertilionidae) in southern Canada. We recorded deep, prolonged torpor bouts, which meet the definition for hibernation, by pregnant females. Prolonged torpor occurred during spring storms. When conditions improved females aroused and gave birth within several days. Our observations imply a fitness advantage of torpor in addition to energy conservation because reduced foetal growth rate could delay parturition until conditions are more favourable for lactation and neonatal survival.     

Coping with chaos: unpredictable food supplies intensify torpor use in an arid-zone marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata)

The severity, duration and amplitude of extreme weather events are forecast to intensify with current climate trends, over both long (e.g. seasonal) and short (e.g. daily) time-scales. As such, the predictability of food supplies for many small endotherms is likely to become increasingly important. Numerous small mammals and birds combat food shortages using torpor, a controlled reduction in metabolic rate and body temperature that helps lower their daily energy requirements. As such, torpor often has been cited as a key feature allowing some small endotherms to survive highly unpredictable climates, such as tropics or dry deserts, but mensurative demonstrations of this are lacking. We have shown here that when a small desert marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata), is offered unpredictable levels of daily food, they increase frequency of daily torpor and length of bouts compared with animals offered ad libitum food, but this was not found for animals offered a 70% food-restricted diet. Our data suggest that simple food restriction may not be sufficient for evaluating the efficacy of torpor as a strategy for managing unpredictable climates.     

Was basking important in the evolution of mammalian endothermy?

The first mammals were small, nocturnal, and presumably had low metabolic rates and were therefore probably unable to maintain a constant high body temperature throughout cool nights. How these animals, without sufficient heat production for endogenous rewarming, were able to become warm and active again before the next activity period remains unresolved. However, we discovered that, similar to reptiles, the carnivorous marsupial mammal Pseudantechinus macdonnellensis (body mass 30.8LJ.0 g) uses the morning sun to rewarm from low (26.3dž.5°C) body temperatures during torpor. Our findings provide the first evidence of basking during rewarming from torpor in mammals and may provide an alternative explanation as to how ancestral mammals could have become nocturnal to avoid diurnal predators despite their small size and a low endogenous heat production.     

Yearlong hibernation in a marsupial mammal

Many mammals hibernate each year for about 6 months in autumn and winter and reproduce during spring and summer when they are generally not in torpor. I tested the hypothesis that the marsupial pygmy-possum (Cercartetus nanus), an opportunistic nonseasonal hibernator with a capacity for substantial fattening, would continue to hibernate well beyond winter. I also quantified how long they were able to hibernate without access to food before their body fat stores were depleted. Pygmy-possums exhibited a prolonged hibernation season lasting on average for 310 days. The longest hibernation season in one individual lasted for 367 days. For much of this time, despite periodic arousals after torpor bouts of ∼12.5 days, energy expenditure was reduced to only ∼2.5% of that predicted for active individuals. These observations represent the first report on body-fat-fuelled hibernation of up to an entire year and provide new evidence that prolonged hibernation is not restricted to placental mammals living in the cold.     

Vertebrate diet decreases winter torpor use in a desert marsupial

One of the energetic benefits of daily torpor over prolonged hibernation is that it enables animals to regularly forage and, therefore, replenish food reserves between bouts of torpor. However, little is known about the diet of predators undergoing torpor or whether differences in prey composition among individuals influence torpor characteristics. Here, we test the hypothesis that prey composition affects winter torpor use and patterns of a population of carnivorous marsupial, the brush-tailed mulgara (Dasycercus blythi), in the Great Sandy Desert, Australia. Mulgaras in the study population captured a wide range of prey including vertebrates (mammals, reptiles, birds), seven insect orders, spiders and centipedes. The proportion of vertebrates in the diet was negatively correlated with both frequency of torpor use and maximum bout duration. This variation in torpor use with diet can be explained by the higher energetic content of vertebrates as well as their larger size. Even assuming uniform intake of prey biomass among individuals, those that subsisted on an invertebrate-dominated diet during winter apparently suffered energetic shortages as a result of the scarcity of invertebrate taxa with high energy content (such as insect larvae). Our study is the first to demonstrate a link between diet composition and daily torpor use in a free-ranging mammal.     

Sexual differences in food preferences in the white stork: an experimental study

Sex differences in the foraging ecology of monomorphic species are poorly understood, due to problems with gender identification in field studies. In the current study, we used experimental conditions to investigate the food preferences of the white stork Ciconia ciconia, an opportunistic species in terms of food, but characterised by a low level of sexual dimorphism. During a 10-day experiment, 29 individuals (20 females and 9 males) were studied by means of a ‘cafeteria test’ in which the storks’ diet consisted of mammals, birds, fish, amphibians, insects and earthworms. The storks preferred food characterised by high calorific and protein values such as mammals, birds and fish. Sexes differed strongly in their preferences; males preferred mammals, whereas females preferred birds. Moreover, females consumed insects and earthworms less often than males. Interestingly, males spent significantly less time foraging than females. We have demonstrated that the white stork exhibits clear sexual differences in food preferences which are mostly attributable to differences in parental duties, physiology and anatomy.     

Behavioural and physiological consequences of male reproductive trade-offs in edible dormice (Glis glis)

Testosterone mediates male reproductive trade-offs in vertebrates including mammals. In male edible dormice (Glis glis), reproductivity linked to high levels of testosterone reduces their ability to express torpor, which may be expected to dramatically increase thermoregulatory costs. Aims of this study were therefore to analyse behavioural and physiological consequences of reproductive activity in male edible dormice under ecologically and evolutionary relevant conditions in the field. As we frequently encountered sleeping groups in the field, we hypothesized that social thermoregulation should be an important measure to reduce energy expenditure especially in sexually active male edible dormice. Our results revealed that the occurrence of sleeping groups was negatively influenced by male body mass but not by reproductive status or ambient temperature. In reproductive as in non-reproductive males, the number of individuals huddling together was negatively influenced by their body mass. Thus in general males with a high body mass were sitting in smaller groups than males with a low body mass. However, in reproductive males group size was further negatively affected by ambient temperature and positively by testes size. Thus breeders formed larger sleeping groups at lower ambient temperatures and males with larger testes were found in larger groups than males with smaller testes. Measurements of oxygen consumption demonstrated that grouping behaviour represents an efficient strategy to reduce energy expenditure in edible dormice as it reduced energy requirements by almost 40%. In summary, results of this field study showcase how sexually active male edible dormice may, through behavioural adjustment, counterbalance high thermoregulatory costs associated with reproductive activity.     

Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): a comparison of dry and wet forests

Many endotherms save energy during food and water shortage or unpredictable environment using controlled reductions in body temperature and metabolism called torpor. In this study, we measured energy metabolism and water turnover in free-ranging grey mouse lemurs Microcebus murinus (approximately 60 g) using doubly labelled water during the austral winter in the rain forest of southeastern Madagascar. We then compared patterns of thermal biology between grey mouse lemurs from the rain forest and a population from the dry forest. M. murinus from the rain forest, without a distinct dry season, entered daily torpor independent of ambient temperature (T _a). There were no differences in torpor occurrence, duration and depth between M. murinus from the rain and dry forest. Mouse lemurs using daily torpor reduced their energy expenditure by 11% in the rain forest and by 10.5% in the dry forest, respectively. There was no significant difference in the mean water flux rates of mouse lemurs remaining normothermic between populations of both sites. In contrast, mean water flux rate of individuals from the dry forest that used torpor was significantly lower than those from the rain forest. This study represents the first account of energy expenditure, water flux and skin temperature (T _sk) in free-ranging M. murinus from the rain forest. Our comparative findings suggest that water turnover and therefore water requirement during the austral winter months plays a more restricting role on grey mouse lemurs from the dry forest than on those from the rain forest.     

Torpor in the Patagonian opossum (Lestodelphys halli): implications for the evolution of daily torpor and hibernation

Hibernation and daily torpor are two distinct forms of torpor, and although they are related, it is not known how and in which sequence they evolved. As the pattern of torpor expressed by the oldest marsupial order the opossums (Didelphimorphia) may provide insights into the evolution of torpor, we aimed to provide the first quantitative data on the thermal biology and torpor expression of the rare Patagonian opossum (Lestodelphys halli). It is the opossum with the southernmost distribution, has a propensity of autumnal fattening, and therefore, is likely to hibernate. We captured two male Lestodelphys, which while in captivity displayed strong daily fluctuations of body temperatures (T_b) measured with implanted miniature data loggers even when they remained normothermic. In autumn and early winter, torpor was expressed occasionally when food was available, but cold exposure and food withdrawal increased torpor use. The mean T_b throughout the study was 32.2?±?1.4 °C, the minimum T_b measured in torpid Lestodelphys was 7.7 °C, average torpor bout duration was 10.3 h, and the maximum torpor bout duration was 42.5 h. Thus, the pattern of torpor expressed by Lestodelphys was intermediate between that of daily heterotherms and hibernators suggesting that it may represent an ancestral opportunistic torpor pattern from which the derived patterns of daily torpor and seasonal hibernation diverged.     

Trace metal concentrations in hairs of three bat species from an urbanized area in Germany

Metal-contaminated soils and sediments are widespread in urbanized areas due to atmospheric deposition close to emission sources. These metals are bio-available for organisms, e.g., insects, and accumulate in food chains of insectivorous mammals. Especially bats, which live in urban regions and ingest large amounts of food relative to their body mass, are at risk of being poisoned due to the accumulation of trace metals. To determine species-specific trace metal contents in bats from urban environments, hair samples were analyzed by ICP-OES. Observed trace metal concentrations were related to species-specific foraging habitat, prey spectrum and degree of synanthropy. The species studied were Pipistrellus pipistrellus, Myotis daubentonii and Nyctalus noctula. P. pipistrellus showed the highest concentrations of lead and zinc and slightly higher concentrations of cadmium than the other two species, which was related to its high degree of synanthropy with foraging habitat mostly located in cities. In contrast, N. noctula displayed the highest contents of manganese and copper. The reason might be found in its prey spectrum, as N. noctula feeds mainly on beetles that are caught in cultured areas. Trace metal concentrations determined in hair samples of M. daubentonii ranged between the values of P. pipistrellus and N. noctula, probably reflecting an intermediate level of synanthropy. Positive correlations were observed between the concentrations of cadmium and lead and those of manganese and copper. Hair samples from bats are suitable monitoring tools to study trace metal exposure and can be used to determine differences in trace metal levels between species.     

Roost type influences torpor use by Australian owlet-nightjars

Australian owlet-nightjars (Aegotheles cristatus; ～50?g) are one of only a few avian species that roost in cavities year-round and regularly enter torpor. Cavity roosts act as thermal buffers, and roost type likely affects energy expenditure of small birds. We used radiotelemetry to locate diurnal winter roost sites of owlet-nightjars in central Australia and to measure body (T (b)) and skin (T (skin)) temperature. We also recorded ambient temperature inside (T (IN)) and outside roosts. Individual owlet-nightjars used one to seven different roosts (tracking time 3-10?weeks), selecting either rock crevices (four birds) or tree hollows (four birds), or switching between the two roost types (seven birds). Rock crevices (T (IN) +9°C to +33°C) were warmer and thermally more stable than tree hollows (T (IN) -4.0°C to +37°C). Torpor, often expressed by a reduction of T (skin)/T (b) by >10°C for 3-4?h at dawn, was influenced by roost selection; torpor use in tree hollows was almost twice that in rock crevices. Despite the potential energy savings accrued from roosting in well-insulated cavities, owlet-nightjars roosted in tree hollows more often (65% bird days, n?=?398) than in rock crevices (35% bird days, n?=?211). Lower costs of arousal from torpor via passive rewarming and basking and decreased risk of predation are two possible explanations for the preference to roost in tree hollows. We provide the first evidence for the influence of cavity roost selection on torpor use in a free-ranging bird and show that roost selection and thermal biology are strongly interrelated in determining energy expenditure.     

Optional strategies for reduced metabolism in gray mouse lemurs

Among the order of primates, torpor has been described only for the small Malagasy cheirogaleids Microcebus and Cheirogaleus. The nocturnal, gray mouse lemur, Microcebus murinus (approx. 60 g), is capable of entering into and spontaneously arousing from apparently daily torpor during the dry season in response to reduced temperatures and low food and water sources. Mark–recapture studies indicated that this primate species might also hibernate for several weeks, although physiological evidence is lacking. In the present study, we investigated patterns of body temperature in two free-ranging M. murinus during the austral winter using temperature-sensitive data loggers implanted subdermally. One lemur hibernated and remained inactive for 4 weeks. During this time, body temperature followed the ambient temperature passively with a minimum body temperature of 11.5°C, interrupted by irregular arousals to normothermic levels. Under the same conditions, the second individual displayed only short bouts of torpor in the early morning hours but maintained stable normothermic body temperatures throughout its nocturnal activity. Reduction of body temperature was less pronounced in the mouse lemur that utilized short bouts of torpor with a minimum value of 27°C. Despite the small sample size, our findings provide the first physiological confirmation that free-ranging individuals of M. murinus from the humid evergreen littoral rain forest have the option to utilize short torpor bouts or hibernation under the same conditions as two alternative energy-conserving physiological solutions to environmental constraints.