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.     

Temporal organisation of hibernation in wild-type and tau mutant Syrian hamsters

The temporal pattern of hibernation was studied in three genotypes of Syrian hamsters with different circadian periodicity to assess a potential circadian control of alternating torpor and euthermy. We recorded the pattern of hibernation by measuring activity in continuous dim light and constant environmental temperature (6 +/- 1 degrees C). In spite of differences in the endogenous circadian period of three genotypes (tau +/+: approximately equals 24 h, tau +/-: approximately equals 22 h, and tau -/-: approximately equals 20 h) torpor bout duration was statistically indistinguishable (tau +/+: 86.9+/-5.3 h; tau +/-: 94.2+/-3.3 h; tau -/-: 88.8+/-6.2 h). The time between two consecutive arousals from torpor showed unimodal distributions not significantly different between genotypes. The first entry into torpor occurred within the active phase of the circadian cycle in all genotypes whereas the first arousal from torpor appeared to be timed randomly with respect to the prior circadian cycle. The amplitude of the activity rhythm was lower after hibernation compared with the amplitude before hibernation. The results suggest that in the Syrian hamster the circadian system does not control periodicity of torpor and arousal onsets in prolonged hibernation at 6 degrees C.     

Melatonin production accompanies arousal from daily torpor in Siberian hamsters

Arousal from deep hibernation is accompanied by a transient rise of melatonin (Mel) in circulation; there are no comparable analyses of Mel concentrations in species that undergo much shallower, shorter duration episodes of daily torpor. Serum Mel concentrations were determined during arousal from both natural daily torpor and torpor induced by 2-deoxy-D-glucose (2-DG) treatment (2,500 mg/kg, intraperitoneal [IP]); blood samples were drawn from the retro-orbital sinus of anesthetized Siberian hamsters. For animals kept in darkness during torpor, Mel concentrations were highest during early arousal when thermogenesis is maximal, and they decreased as body temperature increased during arousal and returned to baseline once euthermia was reestablished. In hamsters kept in the light during the torpor bout, Mel concentrations were elevated above basal values during arousal, but the response was significantly blunted in comparison with values recorded in darkness. Increased Mel concentrations were detected in hamsters only during arousal from torpor (either natural or 2-DG induced) and were not simply a result of the drug treatment; hamsters that remained euthermic or manifested mild hypothermia after drug treatment maintained basal Mel concentrations. We propose that increased Mel production may reflect enhanced sympathetic activation associated with intense thermogenesis during arousal from torpor rather than an adjustment of the circadian rhythm of Mel secretion.     

A record of hibernation on the surface of incisor teeth in the hamster Mesocricetus raddei (Nehring, 1894)

The surface of the lower incisor teeth was studied in an adult male Mesocricetus raddei hamster with a temperature logger implanted into its peritoneal cavity in June 2010. From July 2010 to March 2011, the hamster lived under natural conditions in an enclosure and overwintered in a self-made burrow. Logger data showed that, beginning from mid-August, the animal body temperature periodically dropped and then returned to the norm, with the duration and depth of hypothermia (torpor bouts) increasing and those of nor-mothermia (arousals) decreasing with time. Growth increments on the incisor surface (presumably, daily increments) were unclear in the apical and middle tooth parts but very distinct in the basal part. The number and width of basal increments generally corresponded to the number and duration of arousals. The growth of the incisors apparently continued throughout the winter season, with every arousal after a torpor bout being marked by the formation of a distinct increment on the incisor surface. Thus, it appears that the pattern of increments on the incisor surface can be used to evaluate the course of wintering in hibernating hamsters. Experiments with vital markers are needed to confirm this assumption.     

Platelet Dynamics during Natural and Pharmacologically Induced Torpor and Forced Hypothermia

Hibernation is an energy-conserving behavior in winter characterized by two phases: torpor and arousal. During torpor, markedly reduced metabolic activity results in inactivity and decreased body temperature. Arousal periods intersperse the torpor bouts and feature increased metabolism and euthermic body temperature. Alterations in physiological parameters, such as suppression of hemostasis, are thought to allow hibernators to survive periods of torpor and arousal without organ injury. While the state of torpor is potentially procoagulant, due to low blood flow, increased viscosity, immobility, hypoxia, and low body temperature, organ injury due to thromboembolism is absent. To investigate platelet dynamics during hibernation, we measured platelet count and function during and after natural torpor, pharmacologically induced torpor and forced hypothermia. Splenectomies were performed to unravel potential storage sites of platelets during torpor. Here we show that decreasing body temperature drives thrombocytopenia during torpor in hamster with maintained functionality of circulating platelets. Interestingly, hamster platelets during torpor do not express P-selectin, but expression is induced by treatment with ADP. Platelet count rapidly restores during arousal and rewarming. Platelet dynamics in hibernation are not affected by splenectomy before or during torpor. Reversible thrombocytopenia was also induced by forced hypothermia in both hibernating (hamster) and non-hibernating (rat and mouse) species without changing platelet function. Pharmacological torpor induced by injection of 5′-AMP in mice did not induce thrombocytopenia, possibly because 5′-AMP inhibits platelet function. The rapidness of changes in the numbers of circulating platelets, as well as marginal changes in immature platelet fractions upon arousal, strongly suggest that storage-and-release underlies the reversible thrombocytopenia during natural torpor. Possibly, margination of platelets, dependent on intrinsic platelet functionality, governs clearance of circulating platelets during torpor.     

Kidney proteome changes provide evidence for a dynamic metabolism and regional redistribution of plasma proteins during torpor-arousal cycles of hibernation

Hibernating ground squirrels maintain homeostasis despite extreme physiological challenges. In winter, these circannual hibernators fast for months while cycling between prolonged periods of low blood flow and body temperature, known as torpor, and short interbout arousals (IBA), where more typical mammalian parameters are rapidly restored. Here we examined the kidney proteome for changes that support the dramatically different physiological demands of the hibernator's year. We identified proteins in 150 two-dimensional gel spots that altered by at least 1.5-fold using liquid chromatography and tandem mass spectrometry. These data successfully classified individuals by physiological state and revealed three dynamic patterns of relative protein abundance that dominated the hibernating kidney: 1) a large group of proteins generally involved with capturing and storing energy were most abundant in summer; 2) a select subset of these also increased during each arousal from torpor; and 3) 14 spots increased in torpor and early arousal were enriched for plasma proteins that enter cells via the endocytic pathway. Immunohistochemistry identified α(2)-macroglobulin and albumin in kidney blood vessels during late torpor and early arousal; both exhibited regional heterogeneity consistent with highly localized control of blood flow in the glomeruli. Furthermore, albumin, but not α(2)-macroglobulin, was detected in the proximal tubules during torpor and early arousal but not in IBA or summer animals. Taken together, our findings indicate that normal glomerular filtration barriers remain intact throughout torpor-arousal cycles but endocytosis, and hence renal function, is compromised at low body temperature during torpor and then recovers with rewarming during arousal.     

Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar

Thermoregulation, energetics and patterns of torpor in the pygmy mouse lemur, Microcebus myoxinus, were investigated under natural conditions of photoperiod and temperature in the Kirindy/CFPF Forest in western Madagascar. M. myoxinus entered torpor spontaneously during the cool dry season. Torpor only occurred on a daily basis and torpor bout duration was on average 9.6 h, and ranged from 4.6 h to 19.2 h. Metabolic rates during torpor were reduced to about 86% of the normothermic value. Minimum body temperature during daily torpor was 6.8 °C at an ambient temperature of 6.3 °C. Entry into torpor occurred randomly between 2000 and 0620 hours, whereas arousals from torpor were clustered around 1300 hours within a narrow time window of less than 4 h. Arousal from torpor was a two-step process with a first passive climb of body temperature to a mean of 27 °C, carried by the daily increase of ambient temperature when oxygen consumption remained more or less constant, followed by a second active increase of oxygen consumption to further raise the body temperature to normothermic values. In conclusion, daily body temperature rhythms in M. myoxinus further reduce the energetic costs of daily torpor seen in other species: they extend to unusually low body temperatures and consequently low metabolic rates in torpor, and they employ passive warming to reduce the energetic costs of arousal. Thus, these energy-conserving adaptations may represent an important energetic aid to the pygmy mouse lemur and help to promote their individual fitness. Accepted: 2 November 1999     

Body temperature patterns before, during, and after semi-natural hibernation in the European ground squirrel

Ground squirrels undergo extreme body temperature fluctuations during hibernation. The effect of low body temperatures on the mammalian circadian system is still under debate. Using implanted temperature loggers, we recorded body temperature patterns in European ground squirrels kept in an enclosure under natural conditions. Although hibernation onset was delayed, hibernation end corresponded closely to that measured in a field population. Circadian body temperature fluctuations were not detected during deep torpor, but indications of circadian timing of arousal episodes at higher temperatures were found at the beginning and end of hibernation. One male exhibited synchronised arousals to a relatively constant phase of the day throughout hibernation. All animals first entered torpor in the afternoon. Daily body temperature fluctuations were decreased or distorted during the first days after hibernation. We hypothesise that hibernation may affect the circadian system by either decreasing the expression of the circadian oscillator, or by decreasing the amplitude of the circadian oscillator itself. possibly due to gradual, temperature dependent, internal desynchronisation. The latter mechanism may be beneficial because it might facilitate post-hibernation re-entrainment rates.     

Staying cold through dinner: cold-climate bats rewarm with conspecifics but not sunset during hibernation

For temperate endotherms (i.e., mammals and birds) energy costs are highest during winter but food availability is lowest and many mammals depend on hibernation as a result. Hibernation is made up of energy-saving torpor bouts [periods of controlled reduction in body temperature (T _b)], which are interrupted by brief periodic arousals to normothermic T _b. What triggers these arousals in free-ranging hibernators is not well understood. Some temperate bats with intermittent access to flying insects during winter synchronize arousals with sunset, which suggests that, in some species, feeding opportunities influence arousal timing. We tested whether hibernating bats from a cold climate without access to food during winter also maintain a circadian rhythm for arousals or whether cues from conspecifics in the same cluster are more important. We used temperature telemetry to monitor skin temperature (T _sk) of free-ranging little brown bats (Myotis lucifugus) hibernating in central Manitoba, Canada, where temperatures from 22 October to 22 March were too cold for flying insects. We found no evidence bats synchronized arousals with photoperiod but they did arouse synchronously with other bats in the same cluster. Thus, in the northern part of their range where flying insects are almost never available during winter, little brown bats exhibit no circadian pattern to arousals. Warming synchronously with others could reduce the energetic costs of arousal for individuals or could reflect disturbance of torpid bats by cluster-mates.     

Inhibition of NMDA-type glutamate receptors induces arousal from torpor in hibernating arctic ground squirrels (Urocitellus parryii)

J. Neurochem. (2012) 122, 934-940. ABSTRACT: Hibernation is an adaptation to overcome periods of resource limitation often associated with extreme climatic conditions. The hibernation season consists of prolonged bouts of torpor that are interrupted by brief interbout arousals. Physiological mechanisms regulating spontaneous arousals are poorly understood, but may be related to a need for gluconeogenesis or elimination of metabolic wastes. Glutamate is derived from glutamine through the glutamate-glutamine cycle and from glucose via the pyruvate carboxylase pathway when nitrogen balance favors formation of glutamine. This study tests the hypothesis that activation of NMDA-type glutamate receptors (NMDAR) maintains torpor in arctic ground squirrel (arctic ground squirrel (AGS); Urocitellus parryii). Administration of NMDAR antagonists MK-801 (5?mg/kg, i.p.) that crosses the blood-brain barrier and AP5 (5?mg/kg, i.p.) that does not cross the blood-brain barrier induced arousal in AGS. Central administration of MK-801 (0.2, 2, 20 or 200?μg; icv) to hibernating AGS failed to induce arousal. Results suggest that activation of NMDAR at a peripheral or circumventricular site is necessary to maintain prolonged torpor and that a decrease in glutamate at these sites may contribute to spontaneous arousal in AGS.     

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)     

Maintenance of biological rhythms during hibernation in Eastern woodchucks (<Emphasis Type="Italic">Marmota monax</Emphasis>)

We undertook a study to determine presence of circadian rhythms during woodchuck hibernation using continuously monitored body temperatures. Males had shorter torpor and longer euthermic periods than females. Circular statistics revealed a significant mean vector for males entering into torpor (10:21 h), but not for females. No significant mean vector was found for male or female arousal from torpor. A contingency test was applied to the torpor bout durations. All 7 males tested had significant τ’s between 24 and 26 h, while 6 of the 13 females tested had significant τ’s with a range of 22–27 h. These results implicate a free-running circadian clock during torpor bouts. Overall, the data support the existence of biological rhythms during hibernation in woodchucks, especially for males during arousals. Since entries into torpor appear to be synchronized for males, arousal periods may be used to resynchronize their circadian system. The persistence of biological rhythms during hibernation may help to insure successful mating in the spring after emergence.     

Dietary fatty acid composition and the hibernation patterns in free-ranging arctic ground squirrels

Laboratory experiments have demonstrated that the amount of polyunsaturated fatty acids (PUFAs) in the diet before hibernation influences patterns of mammalian torpor. The hibernation ability of ground squirrels is greatest (longest torpor bouts, greatest number of animals entering torpor) when the PUFA content of their fall diets is 33-74 mg/g, under laboratory conditions. The extent to which natural fall diets both (a) vary in PUFA content and (b) influence the torpor patterns of free-ranging populations of hibernating mammals is unknown, however. We conducted a 3-yr study on the diet PUFA contents and subsequent hibernation patterns of free-ranging arctic ground squirrels (Spermophilus parryii) in the Brooks Range of Alaska. We found that the PUFA contents of fall diets varied more than threefold among individuals. Our study also revealed that arctic ground squirrels that consumed a moderate-PUFA (33-74 mg/g) diet had (a) longer torpor bouts, (b) fewer arousals from torpor, (c) shorter arousal periods, (d) more days in torpor, and (e) greater probability of persisting in the population than those that consumed a high-PUFA (>74 mg/g) diet during the fall. No animals were demonstrated to have consumed a diet representing low-PUFA (<33 mg/g) values. Our study is therefore the first to demonstrate that estimated dietary PUFA levels of a free-ranging hibernator influence subsequent torpor patterns.     

Defining torpor in free-ranging bats: experimental evaluation of external temperature-sensitive radiotransmitters and the concept of active temperature

A variety of definitions involving body temperature (Tb), metabolic rate and behavior have been used to define torpor in mammals and birds. This problem is confounded in some studies of free-ranging animals that employ only skin temperature (Tsk), a measure that approximates but may not precisely reflect Tb. We assess the accuracy of Tsk in the context of a recent definition for torpor called active temperature. We compared the active temperatures of individual big brown bats (Eptesicus fuscus), which aggregate in cavities, with solitary, foliage-roosting hoary bats (Lasiurus cinereus). In captive big brown bats, we compared Tsk and core Tb at a range of ambient temperatures for clustered and solitary roosting animals, compared Tsk and Tb during arousal from torpor, and quantified the effect of flight on warming from torpor. Hoary bats had significantly lower active temperatures than big brown bats despite having the same normothermic Tsk. Tsk was significantly lower than Tb during normothermia but often greater than Tb during torpor. Flight increased the rate of warming from torpor. This effect was more pronounced for Tsk than Tb. This suggests that bats could rely on heat generated by flight muscles to complete the final stages of arousal. Using active temperature to define torpor may underestimate torpor due to ambient cooling of external transmitters or animals leaving roosts while still torpid. Conversely, active temperature may also overestimate shallow torpor use if it is recorded during active arousal when shivering and non-shivering thermogenesis warm external transmitters. Our findings illuminate the need for laboratory studies that quantify the relationship between metabolic rate and Tsk over a range of ambient temperatures.     

Plasma androgen and gonadotropin levels during hibernation and testicular maturation in golden-mantled ground squirrels

The 4-5-mo hibernation season of golden-mantled ground squirrels consists of extended torpor bouts interspersed with brief, periodic intervals of normothermic arousal. Plasma levels of testosterone (T), luteinizing hormone (LH), and follicle-stimulating hormone (FSH) and degree of scrotal pigmentation were measured in torpid and aroused male ground squirrels throughout a season of hibernation and in active animals after the termination of torpor. T was basal in torpid animals; beginning 3 weeks before torpor ended, T was elevated in normothermic males during the first half of periodic arousals but returned to basal levels before animals reentered torpor. After the last (terminal) arousal from torpor, T levels were moderately elevated for 4 wk and maximal for the next 6 wk before they returned to basal values. LH patterns were similar to those of T; however, levels of T and LH were positively correlated only in aroused or posthibernation males. FSH levels remained constant and low during most of the heterothermic season but increased in several torpid males within 3 days of terminal arousal. FSH levels peaked 2 wk after the end of heterothermy. Scrotal pigmentation developed over the first 4 wk after terminal arousal. Maturation of reproductive function occurs during the 4 wk after termination of heterothermy, but elevated levels of T during arousals and variable levels of FSH in the last days of torpor suggest that activation or increased sensitivity of the hypothalamic-pituitary-gonadal axis is important in the termination of heterothermy in ground squirrels.     

Does fear beget fear? Risk-mediated habitat selection triggers predator avoidance at lower trophic levels

Seasonal changes in weather and food availability differentially impact energy budgets of small mammals such as bats. While most thermal physiological research has focused on species that experience extreme seasonal temperature variations, knowledge is lacking from less variable temperate to subtropical climates. We quantified ambient temperature (T _a) and skin temperature (T _sk) responses by individuals from a population of New Zealand lesser short-tailed bats (Mystacina tuberculata) during summer and winter using temperature telemetry. During summer, communal roosts were more thermally stable than T _a. During winter, solitary roosts were warmer than T _a indicating significant thermal buffering. Communal roost trees were used on 83 % of observation days during summer, and individuals occupying them rarely entered torpor. Solitary roosts were occupied on 93 % of observation days during winter, and 100 % of individuals occupying them used torpor. During summer and winter, bats employed torpor on 11 and 95 % of observation days, respectively. Maximum torpor bout duration was 120.8 h and winter torpor bout duration correlated negatively with mean T _a. Torpor bout duration did not differ between sexes, although female minimum T _sk was significantly lower than males. The summer Heterothermy Index varied, and was also significantly affected by T _a. Mean arousal time was correlated with sunset time and arousals occurred most frequently on significantly warmer evenings, which are likely associated with an increased probability of foraging success. We provide the first evidence that torpor is used flexibly throughout the year by M. tuberculata, demonstrating that roost choice and season impact torpor patterns. Our results add to the growing knowledge that even small changes in seasonal climate can have large effects on the energy balance of small mammals.     

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.     

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.     

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)     

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.