Fires have occurred throughout history, including those associated with the meteoroid impact at the Cretaceous-Palaeogene (K-Pg) boundary that eliminated many vertebrate species. To evaluate the recent hypothesis that the survival of the K-Pg fires by ancestral mammals was dependent on their ability to use energy-conserving torpor,we studied body temperature fluctuations and activity of an egg-laying mammal, the echidna ('Tachyglossus aculeatus'), often considered to be a 'living fossil', before, during and after a prescribed burn. All but one study animal survived the fire in the prescribed burn area and echidnas remained inactive during the day(s) following the fire and substantially reduced body temperature during bouts of torpor. For weeks after the fire, all individuals remained in their original territories and compensated for changes in their habitat with a decrease in mean body temperature and activity. Our data suggest that heterothermy enables mammals to outlast the conditions during and after a fire by reducing energy expenditure, permitting periods of extended inactivity. Therefore, torpor facilitates survival in a fire-scorched landscape and consequently may have been of functional significance for mammalian survival at the K-Pg boundary.

Although storms provide an extreme environmental challenge to organisms and are predicted to increase in frequency and intensity due to climate change, there are no quantitative observations on the behaviour and physiology of animals during natural disasters. We provide the first data on activity and thermal biology of a free-ranging, arboreal mammal during a storm with heavy rain and category 1 cyclone wind speeds. We studied a population of sugar gliders ('Petaurus breviceps'), a species vulnerable to bad weather due to their small body size and mode of locomotion, in a subtropical habitat during spring when storms are common. Although torpor is generally rare in this species, sugar gliders remained inactive or reduced foraging times during the storm and further minimized energy demands by entering deep torpor. All animals survived the storm and reverted to normal foraging activity during the following night(s). It thus appears that heterothermic mammals have a crucial adaptive advantage over homeothermic species as they can outlast challenging weather events, such as storms and floods, by reducing metabolism and thus energetic needs.

The recent observation that torpor plays a key role in post-fire survival has been mainly attributed to the reduced food resources after fires. However, some of these adjustments can be facilitated or amplified by environmental changes associated with fires, such as the presence of a charcoal-ash substrate. In a previous experiment on a small terrestrial mammal the presence of charcoal and ash linked to food restriction intensified torpor use. However, whether fire cues also act as a trigger of torpor use when food is available and whether they affect other species including arboreal mammals remains elusive. To evaluate whether smoke, charcoal and ash can act as proximate triggers for an impending period of food shortage requiring torpor for mammals, we conducted an experiment on captive sugar gliders (Petaurus breviceps), a small, arboreal marsupial, housed in outside aviaries under different food regimes and natural ambient conditions. When food was available, fire simulation via exposure to smoke and charcoal-ash substrate caused a significant earlier start of activity and a significant decrease in resting body temperature. In contrast, only when food was withheld, did smoke and charcoal-ash exposure significantly enhance torpor depth and duration. Thus, our study not only provides evidence that fire simulation does affect arboreal and terrestrial species similarly, but also suggests that smoke and ash were presumably selected as cues for torpor induction because they indicate an impending lack of food.

The capacity for nonshivering thermogenesis (NST) plays an important role during arousal from torpid states. Recent data on heterotherms inhabiting warmer regions, however, suggest that passive rewarming reduces the need of metabolic heat production during arousal significantly, leading to the question: to what extent do subtropical or tropical heterotherms depend on NST? The African lesser bushbaby, 'Galago moholi', enters torpid states as an emergency response only, but otherwise stays normothermic throughout the cold and dry winter season. In addition, this species shows unusual rewarming difficulties during arousal from torpor on cold days. We therefore examined the seasonal adjustments of the capacity for NST of naturally acclimatized G. moholi by stimulation with noradrenaline (NA) injection. Dissection of two adult female bushbabies revealed that 'G. moholi' possesses brown adipose tissue, and NA treatment (0.5 mg kg-1, s.c.) induced a significant elevation in oxygen consumption compared with control (saline) injection. However, the increase in oxygen consumption following injection of NA was not significantly different between winter and summer. Our results show that the ability to produce heat via NST seems to be available throughout the year and that 'G. moholi' is able to change NST capacity within a very short time frame in response to cold spells. Together with results from studies on other (Afro-)tropical heterotherms, which also indicate low or even absent seasonal difference in NST capacity, this raises the question of whether the definition of NST needs to be refined for (Afro-)tropical mammals.

Hibernation and daily torpor are energy- and water-saving adaptations employed to survive unfavourable periods mostly in temperate and arctic environments, but also in tropical and arid climates. Heterothermy has been found in a number of mammalian orders, but within the primates so far it seems to be restricted to one family of Malagasy lemurs. As currently there is no evidence of heterothermy of a primate outside of Madagascar, the aim of our study was to investigate whether small primates from mainland Africa are indeed always homeothermic despite pronounced seasonal changes in weather and food availability. Methodology/Principal Findings: One of the nearest relatives of Malagasy lemurs, the African lesser bushbaby, 'Galago moholi', which inhabits a highly seasonal habitat with a hot wet-season and a cold dry-season with lower food abundance, was investigated to determine whether it is capable of heterothermy. We measured skin temperature of free-ranging individuals throughout the cool dry season using temperature-sensitive collars as well as metabolic rate in captured individuals. Torpor was employed by 15% of 20 animals. Only one of these animals displayed heterothermy in response to natural availability of food and water, whereas the other animals became torpid without access to food and water. Conclusions/Significance: Our results show that 'G. moholi' are physiologically capable of employing torpor. However they do not use it as a routine behaviour, but only under adverse conditions. This reluctance is presumably a result of conflicting selective pressures for energy savings versus other ecological and evolutionary forces, such as reproduction or territory defence. Our results support the view that heterothermy in primates evolved before the division of African and Malagasy Strepsirhini, with the possible implication that more primate species than previously thought might still have the potential to call upon this possibility, if the situation necessitates it.

Ecosystems can change rapidly and sometimes irreversibly due to a number of anthropogenic and natural factors, such as deforestation and fire. How individual animals exposed to such changes respond behaviourally and physiologically is poorly understood. We quantified the phenotypic plasticity of activity patterns and torpor use - a highly efficient energy conservation mechanism - in brown antechinus ('Antechinus stuartii'), a small Australian marsupial mammal. We compared groups in densely vegetated forest areas (pre-fire and control) with a group in a burned, open habitat (post-fire). Activity and torpor patterns differed among groups and sexes. Females in the post-fire group spent significantly less time active than the other groups, both during the day and night. However, in males only daytime activity declined in the post-fire group, although overall activity was also reduced on cold days in males for all groups. The reduction in total or diurnal activity in the post-fire group was made energetically possible by a ~3.4-fold and ~2.2-fold increase in the proportion of time females and males, respectively, used torpor in comparison to that in the pre-fire and control groups. Overall, likely due to reproductive needs, torpor was more pronounced in females than in males, but low ambient temperatures increased torpor bout duration in both sexes. Importantly, for both male and female antechinus and likely other small mammals, predator avoidance and energy conservation - achieved by reduced activity and increased torpor use - appear to be vital for post-fire survival where ground cover and refuges have been obliterated.

Behavioral and physiological adaptations are common and successful strategies used by small endothermic species to adjust to unfavorable seasons. Physiological adaptations, such as heterothermy, e.g., torpor, are usually thought to be more effective energy-saving strategies than behavioral adjustments. The African lesser bushbaby, 'Galago moholi', is physiologically capable of torpor but expresses heterothermy only under conditions of extreme energy limitation, suggesting that it has evolved alternative strategies to compensate energetic bottlenecks. We hypothesized that 'Galago moholi' survives the unfavorable winter period, without-or only rarely-employing torpid phases to save energy, by using behavioral thermoregulation. We compared the ecology and behavior of 'Galago moholi' in summer and winter by telemetric tracking and examined food availability by determination of arthropod and gum availability. We found a significant increase in huddling behavior and a significant increase in the use of enclosed and insulated sleeping sites during winter, as well as a reduction in nightly activity. 'Galago moholi' hunted for insects significantly less in winter than in summer, and increased gum intake in winter, when gum showed an increase in energy content. The availability of high-quality food, albeit in low quantities, presumably enables 'Galago moholi' to stay normothermic throughout the cold, dry period and to focus on reproduction activities. We propose that 'Galago moholi' favors ecological and behavioral adjustments over torpor because these are sufficient to meet energy requirements of this species, and their advantages (flexibility, unrestricted activity, and reproduction) outweigh the energetic benefits of heterothermy.

Huddling and torpor are widely used for minimizing heat loss by mammals. Despite the questionable energetic benefits from social heterothermy of mixed groups of warm normothermic and cold torpid individuals, the heterothermic Australian sugar glider ('Petaurus breviceps') rests in such groups during the cold season. To unravel why they might do so, we examined torpor expression of two sugar glider groups of four individuals each in outside enclosures during winter. We observed 79 torpor bouts during 50 days of observation and found that torpor bouts were longer and deeper when all individuals of a group entered torpor together, and therefore infer that they would have saved more energy in comparison to short and shallow solitary torpor bouts. However, all gliders of either group only expressed torpor uniformly in response to food restriction, whereas on most occasions at least one individual per group remained normothermic. Nevertheless, the presence of warm gliders in mixed groups also appears to be of energetic advantage for torpid individuals, because nest box temperature was negatively correlated with the number of torpid gliders, and normothermic individuals kept the nest temperature at a value closer to the threshold for thermoregulatory heat production during torpor. Our study suggests that mixed groups of torpid and normothermic individuals are observed when environmental conditions are adverse but food is available, leading to intermediate energy savings from torpor. However, under especially challenging conditions and when animals are starving, energy savings are maximized by uniform and pronounced expression of torpor.

Increased habitat fragmentation, global warming and other human activities have caused a rise in the frequency of wildfires worldwide. To reduce the risks of uncontrollable fires, prescribed burns are generally conducted during the colder months of the year, a time when in many mammals torpor is expressed regularly. Torpor is crucial for energy conservation, but the low body temperatures (Tb) are associated with a decreased responsiveness and torpid animals might therefore face an increased mortality risk during fires. We tested whether hibernators in deep torpor (a) can respond to the smell of smoke and (b) can climb to avoid fires at Tbs below normothermic levels.Our data show that torpid eastern pygmy-possums ('Cercartetus nanus') are able to detect smoke and also can climb. All males aroused from torpor when the smoke stimulus was presented at an ambient temperature (Ta) of 15 °C (Tb ~18 °C), whereas females only raised their heads. The responses were less pronounced at Tₐ 10 °C. The first coordinated movement of possums along a branch was observed at a mean Tb of 15.6 °C, and animals were even able to climb their prehensile tail when they reached a mean Tb of 24.4 °C. Our study shows that hibernators can sense smoke and move at low Tb. However, our data also illustrate that at Tb ≤13 °C, 'C. nanus' show decreased responsiveness and locomotor performance and highlight that prescribed burns during winter should be avoided on very cold days to allow torpid animals enough time to respond.