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 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.     

Communally breeding bats use physiological and behavioural adjustments to optimise daily energy expenditure

Small endotherms must change roosting and thermoregulatory behaviour in response to changes in ambient conditions if they are to achieve positive energy balance. In social species, for example many bats, energy expenditure is influenced by environmental conditions, such as ambient temperature, and also by social thermoregulation. Direct measurements of daily fluctuations in metabolic rates in response to ambient and behavioural variables in the field have not been technologically feasible until recently. During different reproductive periods, we investigated the relationships between ambient temperature, group size and energy expenditure in wild maternity colonies of Bechstein’s bats (Myotis bechsteinii). Bats used behavioural and physiological adjustments to regulate energy expenditure. Whether bats maintained normothermia or used torpor, the number of bats in the roosts as well changed with reproductive status and ambient temperature. During pregnancy and lactation, bats remained mostly normothermic and daily group sizes were relatively large, presumably to participate in the energetic benefits of social thermoregulation. In contrast, smaller groups were formed on days when bats used torpor, which occurred mostly during the post-lactation period. Thus, we were able to demonstrate on wild animals under natural conditions the significance of behavioural and physiological flexibility for optimal thermoregulatory behaviour in small endotherms.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Summer dormancy in edible dormice (Glis glis) without energetic constraints

Average longevity in free-living edible dormice (Glis glis) can reach 9 years, which is extremely high for a small rodent. This remarkable life span has been related to a peculiar life history strategy and the rarity of reproductive bouts in these seed eaters. Most females (96%) reproduce only once or twice in their lifetime, predominantly during years of mast seeding of, e.g., beech, but entire populations can skip reproduction in years of low seed availability. Surprisingly, in non-reproductive years, large fractions of populations apparently vanished and were never captured above ground. Therefore, we determined the duration of above-ground activity, and body temperature profiles in a subset of animals, of dormice under semi-natural conditions in outdoor enclosures. We found that non-reproductive dormice returned to dormancy in underground burrows throughout summer after active seasons as short as <2 weeks. Thus, animals spent up to >10 months per year in dormancy. This exceeds dormancy duration of any other mammal under natural conditions. Summer dormancy was not caused by energy constraints, as it occurred in animals in good condition, fed ad libitum and without climatic stress. We suggest that almost year-round torpor has evolved as a strategy to escape birds of prey, the major predators of this arboreal mammal. This unique predator-avoidance strategy clearly helps in explaining the unusually high longevity of dormice.     

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.     

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.     

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.     

Mushroom harvesting ants in the tropical rain forest

Ants belong to the most important groups of arthropods, inhabiting and commonly dominating most terrestrial habitats, especially tropical rainforests. Their highly collective behavior enables exploitation of various resources and is viewed as a key factor for their evolutionary success. Accordingly, a great variety of life strategies evolved in this group of arthropods, including seed harvesters, gardeners, and planters, fungus growers, nomadic hunters, life stock keepers, and slave makers. This study reports the discovery of a new lifestyle in ants. In a Southeast Asian rainforest habitat, Euprenolepis procera is specialized in harvesting a broad spectrum of naturally growing mushrooms, a nutritionally challenging and spatiotemporally unpredictable food source. While unfavorable to the vast majority of animals, E. procera has developed exceptional adaptations such as a shift to a fully nomadic lifestyle and special food processing capabilities, which allow it to rely entirely on mushrooms. As a consequence, E. procera is the most efficient and predominant consumer of epigeic mushrooms in the studied habitat and this has broad implications for the tropical rainforest ecosystem.     

Divergent evolution of feeding substrate preferences in a phylogenetically young species flock of pupfish (Cyprinodon spp.)

A fundamental question in sympatric speciation is how trophic divergence is achieved. We used an extremely young (<8,000 years) species flock of pupfish (Cyprinodon spp.) from Laguna Chichancanab in south-eastern Mexico to examine divergent evolution of preferences for different feeding substrates. In a test aquarium, we presented four feeding substrates (sand, gravel, a plastic plant, and blank bottom), but no actual food was offered. The four feeding substrates were chosen to mirror the most common substrate types in Laguna Chichancanab. Previous studies demonstrated that benthic food items prevail in the diet of most Cyprinodon species. C. beltrani preferred sand, whereas C. labiosus preferred gravel. F₁ hybrids of both species showed intermediate preferences. C. maya searched for food equally at all substrates. As the test fish were reared under identical laboratory conditions (i.e., in the absence of feeding substrates), the species-specific preferences appear to be genetically fixed, suggesting rapid divergent evolution of feeding behaviors.     

Torpor at high ambient temperature in a neotropical didelphid,the grey short-tailed opossum (Monodelphis domestica)

The grey short-tailed opossum, Monodelphis domestica, has been an established research animal for more than five decades, but relatively, little is known about its thermophysiology. Here we studied core body temperature (T _b) and metabolic rate (MR) of female adult M. domestica housed in the laboratory at an ambient temperature (T _a) of 26 °C. In expanding previous reports, the average recorded core T _b of M. domestica was 34.3 °C. The T _b of an individual M. domestica can drop below 30 °C (minimal T _b: 28.6 °C) accompanied by a reduction in MR of up to 52 % even while having ad libitum access to food. These findings demonstrate for the first time the presence of spontaneous torpor in M. domestica. Metabolic suppression at relatively high T _a and T _b furthermore broadens our perspective on the use of torpor as a metabolic strategy not just restricted to cold climates.     

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.