Energetics of tropical hibernation

In this field study, the energetic properties of tropical hibernation were investigated by measuring oxygen consumption and body temperature of the Malagasy primate Cheirogaleus medius in their natural hibernacula. These lemurs use tree holes with extremely varying insulation capacities as hibernacula. In poorly insulated tree holes, tree hole temperature and body temperature fluctuated strongly each day (between 12.8 and 34.4°C). The metabolic rate under these conditions also showed large daily fluctuations between about 29.0 ml O₂/h and 97.9 ml O₂/h in parallel with changes in body temperature. In well insulated tree holes in very large trees on the other hand, tree hole temperature and body temperature remained relatively constant at about 25°C. Lemurs hibernating in these tree holes showed a more constant metabolic rate at an intermediate level, but hibernation was interrupted by repeated arousals with peak metabolic rates up to 350 ml O₂/h. The occurrence of these spontaneous arousals proved that the ability for thermoregulation persists during hibernation. Arousals were energetically costly, but much less so than in temperate and arctic hibernators. Despite the decisive influence of tree hole properties on the pattern of body temperature and metabolic rate during hibernation, the choice of the hibernaculum does not seem to be of energetic importance. The overall energetic savings by tropical hibernation amounted to about 70% as compared to the active season (31.5 vs. 114.3 kJ/d). Therefore, tropical hibernation in C. medius is an effective, well-regulated adaptive response to survive unfavourable seasons.     

Seasonal and daily rhythms of body temperature in the European hamster (Cricetus cricetus) under semi-natural conditions

Body temperature of five European hamsters exposed to semi-natural environmental conditions at 47° N in Southern Germany was recorded over a 1.5-year period using intraperitoneal temperature-sensitive radio transmitters. The animals showed pronounced seasonal changes in body weight and reproductive status. Euthermic body temperature changed significantly throughout the year reaching its maximum of 37.9±0.2°C in April and its minimum of 36.1±0.4°C in December. Between November and March the hamsters showed regular bouts of hibernation and a few bouts of shallow torpor. During hibernation body temperature correlated with ambient temperature. Monthly means of body temperature during hibernation were highest in November (7.9±0.8°C) and March (8.2±0.5°C) and lowest in January (4.4±0.7°C). Using periodogram analysis methods, a clear diurnal rhythm of euthermic body temperature could be detected between March and August, whereas no such rhythm could be found during fall and winter. During hibernation bouts, no circadian rhythmicity was evident for body temperature apart from body temperature following ambient temperature with a time lag of 3–5 h. On average, hibernation bouts lasted 104.2±23.8 h with body temperature falling to 6.0±1.7°C. When entering hibernation the animals cooled at a rate of -0.8±0.2°C·h^-1; when arousing from hibernation they warmed at a rate of 9.9±2.4°C·h^-1. Warming rates were significantly lower in November and December than in January and February, and correlated with ambient temperature (r=-0.46, P<0.01) and hibernating body temperature (r=-0.47, P<0.01). Entry into hibrnation occured mostly in the middle of the night (mean time of day 0148 hours ±3.4 h), while spontaneous arousals were widely scattered across day and night. For all animals regression analysis revealed free-running circadian rhythms for the timing of arousal. These results suggest that entry into hibernation is either induced by environmental effects or by a circadian clock with a period of 24 h, whereas arousal from hibernation is controlled by an endogenous rhythm with a period different from 24 h.Abbreviations bw body weight - CET central European time - T _a ambient temperature - T _b body temperature - TTL transistor-transistor logic     

THE TEMPORAL ORGANIZATION OF DAILY TORPOR AND HIBERNATION: CIRCADIAN AND CIRCANNUAL RHYTHMS

Mammals and birds have evolved the ability to maintain a high and constant body temperature T_b over a wide range of ambient temperatures T_a using endogenous heat production. In many, especially small endotherms, cost for thermoregulatory heat production can exceed available energy; to overcome these energetic bottlenecks, they enter a state of torpor (a regulated reduction of T_b and metabolic rate). Since the occurrence of torpor in many species is a seasonal event and occurs at certain times of the day, we review whether circadian and circannual rhythms, important in the timing of biological events in active animals, also play an important role during torpor when T_b is reduced substantially and may even fall below 0°C. The two distinct patterns of torpor, hibernation (prolonged torpor) and daily torpor, differ substantially in their interaction with the circadian system. Daily torpor appears to be integrated into the normal circadian rhythm of activity and rest, although torpor is not restricted only to the normal rest phase of an animal. In contrast, hibernation can last for several days or even weeks, although torpor never spans the entire hibernation season, but is interrupted by periodic arousals and brief normothermic periods. Clearly, a day is no longer divided in activity and rest, and at first glance the role of the circadian system appears negligible. However, in several hibernators, arousals not only follow a regular pattern consistent with a circadian rhythm, but also are entrainable by external stimuli such as photoperiod and T_a. The extent of the interaction between the circadian and circannual system and hibernation varies among species. Biological rhythms of hibernators for which food availability appears to be predictable seasonally and that hibernate in deep and sealed burrows show little sensitivity to external stimuli during hibernation and hence little entrainability of arousal events. In contrast, opportunistic hibernators, which some times use arousals for foraging and hibernate in open and accessible hibernacula, are susceptible to external zeitgebers. In opportunistic hibernators, the circadian system plays a major role in maintaining synchrony between the normal day-night cycle and occasional foraging. Although the daily routine of activity and rest is abandoned during hibernation, the circadian system appears to remain functional, and there is little evidence it is significantly affected by low T_b. (Chronobiology International, 17(2), 103–128, 2000)     

Partial arousals from hibernation in hedgehogs in outdoor hibernacula

Summary Thermal properties of hibernacula and sequences of arousals have been studied in four adult hedgehogs for seven months starting in October. Departures and entries to the nesting chamber were continuously monitored together with ambient temperature and the temperature in the hibernacula.During the two first months of the experimental period nest departures were intermittently recorded, predominantly in the two females which also occasionally foraged. The longest periods spent continuously in the hibernaculum ranged from 129 to 178 days. The natural hibernation season for Danish hedgehogs was found to comprise the six months from October onwards when there is little shelter where hedgehogs normally roam.Ambient temperatures recorded were —11 to +13° C being subzero for half the total time measured. The nest temperatures generally were higher, and above 0° C during 78–99% of total time, most commonly ranging from 0° to 4° C and thus reflecting deep hibernation.Between December and May spontaneous increases in nest temperatures amounting to 7–26° C (average 18° C) and bringing these temperatures to 10–29.5° C were recorded in 58 cases. Fiftyfour arousals did not involve departure from the hibernaculum (partial arousals). In the remaining cases (full arousals) the preceding rewarming lasted 4 1/2–6 1/2 h and nest departures amounted to 10,2 and 5 min in one female hedgehog and 90 min in another.The hedgehogs showed 12–18 arousals, the mean duration of which was 34–44 h. The high energy expenditure associated with arousals however, was found to last on average 21 h during each arousal. It is hypothesized that the body temperature during arousals chiefly was below 35–37° C.The time between arousals was 3–15 days. Periods in hibernation averaged 7–8 days in the females and 9–10 days in the heavier males, being generally longest in January-February. Neither arousals nor re-entries into deep hibernation occurred at any particular time of the day. It is suggested that for undisturbed hedgehogs arousals are induced and controlled by endogenous factors. In conclusion it is stressed that future studies on hibernation should recognize the importance of individual variability in the response pattern and focus interest on the endogenous factors which govern this important process.     

The temporal organization of daily torpor and hibernation: circadian and circannual rhythms

Mammals and birds have evolved the ability to maintain a high and constant body temperature T_b over a wide range of ambient temperatures T_a using endogenous heat production. In many, especially small endotherms, cost for thermoregulatory heat production can exceed available energy; to overcome these energetic bottlenecks, they enter a state of torpor (a regulated reduction of T_b and metabolic rate). Since the occurrence of torpor in many species is a seasonal event and occurs at certain times of the day, we review whether circadian and circannual rhythms, important in the timing of biological events in active animals, also play an important role during torpor when T_b is reduced substantially and may even fall below 0°C. The two distinct patterns of torpor, hibernation (prolonged torpor) and daily torpor, differ substantially in their interaction with the circadian system. Daily torpor appears to be integrated into the normal circadian rhythm of activity and rest, although torpor is not restricted only to the normal rest phase of an animal. In contrast, hibernation can last for several days or even weeks, although torpor never spans the entire hibernation season, but is interrupted by periodic arousals and brief normothermic periods. Clearly, a day is no longer divided in activity and rest, and at first glance the role of the circadian system appears negligible. However, in several hibernators, arousals not only follow a regular pattern consistent with a circadian rhythm, but also are entrainable by external stimuli such as photoperiod and T_a. The extent of the interaction between the circadian and circannual system and hibernation varies among species. Biological rhythms of hibernators for which food availability appears to be predictable seasonally and that hibernate in deep and sealed burrows show little sensitivity to external stimuli during hibernation and hence little entrainability of arousal events. In contrast, opportunistic hibernators, which some times use arousals for foraging and hibernate in open and accessible hibernacula, are susceptible to external zeitgebers. In opportunistic hibernators, the circadian system plays a major role in maintaining synchrony between the normal day-night cycle and occasional foraging. Although the daily routine of activity and rest is abandoned during hibernation, the circadian system appears to remain functional, and there is little evidence it is significantly affected by low T_b. (Chronobiology International, 17(2), 103-128, 2000)     

Hormonal changes and energy substrate availability during the hibernation cycle of Syrian hamsters

Animals have to adapt to seasonal variations in food resources and temperature. Hibernation is one of the most efficient means used by animals to cope with harsh winter conditions, wherein survival is achieved through a significant decrease in energy expenditure. The hibernation period is constituted by a succession of torpor bouts (hypometabolism and decrease in body temperature) and periodic arousals (eumetabolism and euthermia). Some species feed during these periodic arousals, and thus show different metabolic adaptations to fat-storing species that fast throughout the hibernation period. Our study aims to define these metabolic adaptations, including hormone (insulin, glucagon, leptin, adiponectin, GLP-1, GiP) and metabolite (glucose, free fatty acids, triglycerides, urea) profiles together with body composition adjustments. Syrian hamsters were exposed to varied photoperiod and temperature conditions mimicking different phases of the hibernation cycle: a long photoperiod at 20 °C (LP20 group), a short photoperiod at 20 °C (SP20 group), and a short photoperiod at 8 °C (SP8). SP8 animals were sampled either at the beginning of a torpor bout (Torpor group) or at the beginning of a periodic arousal (Arousal group). We show that fat store mobilization in hamsters during torpor bouts is associated with decreased circulating levels of glucagon, insulin, leptin, and an increase in adiponectin. Refeeding during periodic arousals results in a decreased free fatty acid plasma concentration and an increase in glycemia and plasma incretin concentrations. Reduced incretin and increased adiponectin levels are therefore in accordance with the changes in nutrient availability and feeding behavior observed during the hibernation cycle of Syrian hamsters.     

Partial arousals from hibernation in a pair of common dormice,Muscardinus avellanarius (Rodentia,Gliridae), in their natural hibernaculum

Summary A pair of common dormice discovered while torpid in their natural hibernaculum on December 5, was studied continously outdoors, exposed to natural fluctuations in temperature and rainfall. Temperature inside and outside the nest ball and motor activity were recorded. The first emergence from hibernaculum occurred on March 4, after which the dormice were daily active, chiefly during evening and night hours. Nest departures lasted on average 10.5 h (6.5–14 h) per day.During the 88 days while the animals remained in the hibernaculum ambient temperature ranged from -5° to 8.5° C. Nest temperature never fell below zero, being chiefly 1.0°C above ambient temperature during 68 of these days and thus reflecting deep hibernation in both animals. However, on 19 occasions nest temperature was raised steeply from average 5.6°C (2.0–8.0°C) to average 23.0°C (17.5–32.5°C). These increases of nest temperature, lasting roughly 4 h (3–8 h) are interpreted as partial arousals. The total duration of partial arousals was 76 h, i.e. 3.6% of the time during which the animals remained consistently in the nest.The interarousal time varied, being 16 days at the most and 12 h at the least. The frequency of arousals increased with rising maximum values of ambient temperature, and partial arousals never were recorded on days when temperature remained below 2°C. It is believed that partial arousals correspond to the periodic or spontaneous arousals previously recorded in laboratory experiments of some other hibernating mammals. However, the energetic expenditure seems to be smaller during periodic arousals because of their shorter duration and the fact that no departure from the hibernaculum occurs.Possible mechanisms governing partial arousals are discussed. As these events chiefly occurred during night they may partly be controlled by an inherent time sense.     

Effect of Ambient Temperature on the Body Temperature Rhythm of Male Gray Mouse Lemurs (Microcebus murinus)

In order to cope with the seasonal variations in ambient temperature and food availability in the natural habitat, gray mouse lemurs (Microcebus murinus) exhibit adaptive energy-saving mechanisms similar to those in hibernating species with seasonal and daily heterothermia. To determine thermoregulatory responses, via telemetry we recorded body temperature and locomotor activity variations during the breeding season in three captive male mouse lemurs kept at ambient temperatures (T_a) ranging from 18° to 34°C. Rhythms in body temperature and locomotor activity were clearly exhibited regardless of ambient temperature. As _a increased, mean body temperature increased from 36.5 ± 0.1°C to 37.6 ± 0.3°C, with significant change in the amplitude of the body temperature rhythm when _a rose above 28°C. Effects of _a were mostly due to changes in the fall in body temperature occurring daily at the beginning of the light phase when the subjects entered diurnal sleep. The daily decrease in body temperature was not modified by exposure to ambient temperatures from 18°C to 28°C whereas it disappeared under warmer condition. Changes in locomotor activity levels only delayed the occurrence of thermoregulatory modulation. These results strongly suggest that, during the breeding season, the thermoneutral zone of mouse lemurs is close to 28°C and that the diurnal fall in body temperature could be considered as an important adaptive energy-saving mechanism adjusted to ecological constraints.     

Daily torpor and hibernation in birds and mammals

Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian‐mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (～35°) than daily heterotherms (～25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30‐fold longer, and mean torpor bout duration >25‐fold longer in hibernators. Mean minimum body temperature differed by ～13°C, and the mean minimum torpor metabolic rate was ～35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.     

Timing of torpor bouts during hibernation in European hamsters (Cricetus cricetus L.)

Body temperature (T _b) of seven European hamsters maintained at constant ambient temperature (T _a = 8 °C) and constant photoperiod (LD 8:16) was recorded throughout the hibernating season using intraperitoneal temperature-sensitive HF transmitters. The animals spent about 30% of the hibernation season in hypothermia and 70% in inter-bout normothermy. Three types of hypothermia, namely deep hibernation bouts (DHBs), short hibernation bouts (SHBs), and short and shallow hibernation bouts (SSHBs), were distinguished by differences in bout duration and minimal body temperature (T _m). A gradual development of SSHBs from the diel minimum of T _b during normothermy could be seen in individual hamsters, suggesting a stepwise decrease of the homeostatic setpoint of T _b regulation during the early hibernation season. Entry into hibernation followed a 24-h rhythm occurring at preferred times of the day in all three types of hypothermia. DHBs and SHBs were initiated approximately 4 h before SSHBs, indicating a general difference in the physiological initiation of SSHBs on the one hand and DHBs and SHBs on the other. Arousals from SHBs and SSHBs also followed a 24-h rhythm, whereas spontaneous arousals from DHBs were widely scattered across day and night. Statistical analyses of bout length and the interval between arousals revealed evidence for a free-running circadian rhythm underlying the timing of arousals. The results clearly demonstrate that entries into hypothermia are linked to the light/dark-cycle. However, the role of the circadian system in the timing of arousals from DHBs remains unclear. Accepted: 11 December 1996     

The timing of hibernation in Tasmanian echidnas: why do they do it when they do?

We investigated the patterns of hibernation and arousals in seven free-ranging echidnas Tachyglossus aculeatus setosus (two male, five female) in Tasmania using implanted temperature data loggers. All echidnas showed a ‘classical’ pattern of mammalian hibernation, with bouts of deep torpor interrupted by periodic arousals to euthermia (mean duration 1.04±0.05 (n=146). Torpor bout length increased as body temperature fell during the hibernation season, and became more variable as temperature rose again. Hibernation started in late summer (February 28±5 days, n=6) and males aroused just before the winter solstice (June 15±3 days, n=3), females that subsequently produced young aroused 40 days later (July 25±3, n=4) while females that did not produce young hibernated for a further two months (arousal Sept 27±5, n=7). We suggest that hibernation in Tasmanian echidnas can be divided into two phases, the first phase, marked by declining minimum body temperatures as ambient temperature falls, appears to be obligatory for all animals, while the second phase is ‘optional’ and is utilised to varying amounts by females. We suggest that early arousal and breeding is the favoured option for females in good condition, and that the ability to completely omit breeding in some years, and hibernate through to spring is an adaptation to an uncertain climate.     

Hibernation by tree-roosting bats

In summer, long-eared bats (Nyctophilus spp.) roost under bark and in tree cavities, where they appear to benefit from diurnal heating of roosts. In contrast, hibernation is thought to require a cool stable temperature, suggesting they should prefer thermally insulated tree cavities during winter. To test this prediction, we quantified the winter thermoregulatory physiology and ecology of hibernating tree-roosting bats, Nyctophilus geoffroyi and N. gouldi in the field. Surprisingly, bats in winter continued to roost under exfoliating bark (65%) on the northern, sunny side of trees and in shallow tree cavities (35%). Despite passive re-warming of torpid bats by 10-20 degrees C per day, torpor bouts lasted up to 15 days, although shorter bouts were also common. Arousals occurred more frequently and subsequent activity lasted longer on warmer nights, suggesting occasional winter foraging. We show that, because periodic arousals coincide with maximum roost temperatures, when costs of rewarming and normothermic thermoregulation are minimal, exposure to a daily temperature cycle could largely reduce energy expenditure during hibernation. Our study provides further evidence that models of torpor patterns and energy expenditure from hibernators in cold temperate climates are not directly applicable in milder climates, where prolonged torpor can be interspersed with more frequent arousals and occasional foraging.     

The effect of temperature on the pattern of torpor in a marsupial hibernator

Physiological variables of torpor are strongly temperature dependent in placental hibernators. This study investigated how changes in air temperature affect the duration of torpor bouts, metabolic rate, body temperature and weight loss of the marsupial hibernator Burramys parvus (50 g) in comparison to a control group held at a constant air temperature of 2°C. The duration of torpor bouts was longest (14.0±1.0 days) and metabolic rate was lowest (0.033±0.001 ml O₂·g^-1·h^-1) at2°C. At higher air temperatures torpor bouts were significantly shorter and the metabolic rate was higher. When air temperature was reduced to 0°C, torpor bouts also shortened to 6.4±2.9 days, metabolic rate increased to about eight-fold the values at 2°C, and body temperature was maintained at the regulated minimum of 2.1±0.2°C. Because air temperature had such a strong effect on hibernation, and in particular energy expenditure, a change in climate would most likely increase winter mortality of this endangered species.Abbreviationst STP standard temperature and pressure - T _a air temperature - T _b body temperature - VO₂ rate of oxygen consumption     

Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels

Golden-mantled ground squirrels (Spermophilus lateralis) undergo seasonal hibernation during which core body temperature (T(b)) values are maintained 1-2 degrees C above ambient temperature. Hibernation is not continuous. Squirrels arouse at approximately 7-day intervals, during which T(b) increases to 37 degrees C for approximately 16 h; thereafter, they return to hibernation and sustain low T(b)s until the next arousal. Over the course of the hibernation season, arousals consume 60-80% of a squirrel's winter energy budget, but their functional significance is unknown and disputed. Host-defense mechanisms appear to be downregulated during the hibernation season and preclude normal immune responses. These experiments assessed immune function during hibernation and subsequent periodic arousals. The acute-phase response to bacterial lipopolysaccharide (LPS) was arrested during hibernation and fully restored on arousal to normothermia. LPS injection (ip) resulted in a 1-1.5 degrees C fever in normothermic animals that was sustained for > 8 h. LPS was without effect in hibernating squirrels, neither inducing fever nor provoking arousal, but a fever did develop several days later, when squirrels next aroused from hibernation; the duration of this arousal was increased sixfold above baseline values. Intracerebroventricular infusions of prostaglandin E(2) provoked arousal from hibernation and induced fever, suggesting that neural signaling pathways that mediate febrile responses are functional during hibernation. Periodic arousals may activate a dormant immune system, which can then combat pathogens that may have been introduced immediately before or during hibernation.     

The functional brain state of hibernators and nonhibernators at different animals temperatures

Literature and our own data on structural and functional state of neocortex and hippocampus during both entrance in hibernation of ground squirrel (Spermophilus undulates) and Wistar rats in hypothermia were generalized. During hibernation when body temperature is about 2-4 degrees C the suppression of both bioelectrical and protein-synthesizing activity, the decrease of neuronal cell bodies and the branching of dendrites, retraction of dendritic spines, and a decrease of postsynaptic active zones of synapses were observed. Similar changes in those parameters were triggered for rats during hypoxia-hypercapnia at body temperature 17-19 degrees C. Hypoxia-hypercapnia facilitates the entrance in torpid state for hole animals. Nonhibernating animals during cooling and hypoxia-hypercapnia trigger functioning some mechanisms similar hibernators during entrance in hibernation. Similar morphological and functional changes for both hibernators and nonhibernators at low temperature state show similarity of mechanisms which induce a low level of brain activity of different animals.     

Ecology of natural hibernation in the marsupial mountain pygmy-possum (Burramys parvus)

The hibernating marsupial mountain pygmy-possum (Burramys parvus, 40 g) has to raise its slow-growing offspring during a short alpine summer. Only females provide parental care, while after mating males emigrate to marginal habitats often at lower altitudes which can sustain only low possum densities. We predicted that the hibernation strategies in mountain pygmy-possums are distinct from those of similar-sized placental hibernators, because of the developmental constraints in marsupials and because hibernation differs between the sexes. Using temperature-sensitive radio transmitters, we studied the hibernation patterns of free-living male and female mountain pygmy-possums living in a north- and a south-facing boulder field (Kosciusko National Park) for two consecutive winters. Individual possums commenced hibernation several months before the snow season. As in other hibernators, torpor in the mountain pygmy-possum was interrupted by periodic arousals which occurred most often during the late afternoon. Torpor bouts initially lasted a few days when the hibernacula temperature (T _hib) ranged from 4 to 7°C. As the hibernation season progressed, torpor bouts became longer and possum body temperatures (T _b) approached 2°C. The T _bs of females were significantly lower and torpor bouts were longer in the second half of the hibernation season than in males. Between torpor bouts, both sexes were often active and left hibernacula for periods of up to 5 days. Especially during the first months of the hibernation season, possums also frequently changed hibernacula sites probably in an attempt to select a site with a more suitable microclimate. Emergence from hibernation was closely coupled with the disappearance of snow from the possum habitat (September 1995, October 1996) and the limited fat stores probably dictate an opportunistic spring emergence. However, in 1995, spring was early and males emerged significantly earlier than females. In 1996, when snow melt was delayed, this difference vanished. Testes are regressed in males during hibernation and the time needed for testes growth and spermatogenesis favours an earlier emergence for males which was probably achieved by their preference for the more sun exposed north-facing boulder field. A sexual dimorphism in hibernation strategies and spring emergence therefore enables mountain pygmy-possums to cope with their harsh alpine environment. Received: 22 May 1997 / Accepted: 21 August 1997     

Hibernation patterns and energy expenditure in hedgehogs from semi-arid and temperate habitats

Summary Hibernation patterns, body temperature (T _b) and oxygen consumption ( ) were measured during hibernation in two hedgehog species, a desert speciesHemiechinus auritus (body mass 367 g) and a temperate habitat speciesErinaceus europaeus (body mass 598 g). A continuous ambient temperature of 11 °C was the only necessary condition for both species to enter hibernation outdoors and in the laboratory. At this temperature, hibernation could be induced at any time of the year. Hibernation bouts ofHemiechinus were regular and short (average 4.8 days), whereas those ofErinaceus lasted 5 to 27 days (average 9.3 days). The frequency of spontaneous arousals was 5.3 and 2.9 per month forHemiechinus andErinaceus, respectively. None of the hedgehogs took any food during arousal periods. Both species had the sameT _b during hibernation (12.5 °C) and during arousal (33 °C). of the hibernatingHemiechinus was twice the rate ofErinaceus (0.050 vs. 0.025 ml g^–1 h^–1), but during arousal it was the same for both. The monthly average energy expenditure for both species was 1,477 kJ per animal, which is 15% of the energy used by non-hibernating hedgehogs. The corresponding amount of fat catabolized was 37 g per month. This mass loss would limit the hibernation inHemiechinus to 3.9 months and inErinaceus to 6.5 months. Although hibernation inHemiechinus does not constitute a special adaptation to hot environments, it significantly improves the hedgehog's energy economy during the desert winter.     

Warming up for dinner: torpor and arousal in hibernating Natterer’s bats (Myotis nattereri) studied by radio telemetry

The frequency and function of arousals during hibernation in free-living mammals are little known. We used temperature-sensitive radio transmitters to measure patterns of torpor, arousal and activity in wild Natterer’s bats Myotis nattereri during hibernation. Duration of torpor bouts ranged from 0.06 to 20.4 days with individual means ranging from 0.9 to 8.9 days. Arousals from torpor occurred most commonly coincident with the time (relative to sunset) typical for bats emerging from summer roosts to forage. Bats with lower body condition indices had a shorter average duration of their torpor bouts. We found a non-linear relationship between duration of torpor bout and ambient temperature: the longest average torpor bouts were at temperatures between 2 and 4°C with shorter bouts at lower and higher ambient temperatures. One individual was radio-tracked for ten nights, remained active for an average of 297 min each night and was active for longer on warmer nights. Our results suggest that vespertilionid bats use relatively short torpor bouts during hibernation in a location with a maritime climate. We hypothesise that Natterer’s bats time arousals to maximise opportunities for potential foraging during winter although winter feeding is not the sole determinant of arousal as bats still arouse at times when foraging is unlikely.     

Tree Holes Used for Resting by Gray Mouse Lemurs (Microcebus murinus) in Madagascar: Insulation Capacities and Energetic Consequences

I studied the insulation capacity of tree holes used by gray mouse lemurs (Microcebus murinus) in a primary dry deciduous forest in western Madagascar during the cool dry season. Tree holes had an insulating effect, and fluctuations of air temperatures were less extreme inside the holes than outside them. The insulation capacity of the tree holes peaked between 0800 and 1100 hr, when ambient temperatures ranged between 25 and 30°C. To compare tree holes, I calculated the mean difference between the internal temperature )(T_i ) and the external temperature (T_e ) for each tree hole. Thus large differences indicate good insulation capacities. The mean difference of tree holes in living trees was significantly larger than that of tree holes in dead trees, which shows that insulation in living trees is more effective. During the dry season, the insulation capacity of tree holes in living trees decreased and was lowest in July, whereas the insulation capacity of holes in dead trees remained approximately constant. Physiological studies under natural temperature and light condition in Microcebus murinus reveal that daily torpor saves around 40% of the daily energy expenditure compared to normothermia. However, torpor can be maintained only up to the threshold body and ambient temperature of 28°C, whereat Microcebus murinus have to terminate torpor actively. By occupying insulating tree holes, mouse lemurs may stay longer in torpor, which increases their daily energy savings by an extra 5%.