Hibernation Patterns Research Articles

Thermoregulatory variation among populations of bats along a latitudinal gradient

Most studies of hibernation physiology sample individuals from populations within a single geographic area, yet some species have large ranges meaning populations likely experience area-specific levels of energetic challenges. As well, few studies have assessed within-season variation. Since physiological adjustments often are influenced by environmental factors, and the types of environments vary with geography, we expected variance in hibernation patterns among geographically separated populations. Our specific goal was to measure intraspecific variation in torpid metabolic rate (TMR) and body temperature (T (b)) as a function of ambient temperature (T (a)) for a non-migratory and migratory species to determine whether there is a continuum in physiological responses based on latitude. We chose big brown (Eptesicus fuscus) and eastern red bats (Lasiurus borealis) as model species and sampled individuals from populations throughout each species' winter range. In both species, individuals from southern populations maintained higher TMR at cooler T (a)s and lower TMR at warmer T (a)s than those from northern populations. Big brown bats from southern populations regulated T (b) during torpor at higher levels and there was no significant difference in T (b) between populations of eastern red bats. Although metabolic responses were similar across the gradient between species, the effect was more dramatic in big brown bats. Our data demonstrate a continuum in thermoregulatory response, ranging from classic hibernation in northern populations to a pattern more akin to daily torpor in southern populations. Our research highlights the potential usefulness of bats as model organisms to address questions about within-species physiological variation in wild populations.

Formation and Contents of Yellow-Pine Chipmunk (Tamias amoenus) Winter Larders

Despite much attention to the foraging habits and hibernation patterns of food-storing mammals, little is known about the contents of winter larders under natural conditions or how animals prepare a winter larder. Here we describe the contents of 15 yellow-pine chipmunk (Tamias amoenus) winter larders from 3 different years and describe the movement of scatter-hoarded seeds into larders. We found larders by locating 14 radio-collared chipmunks in their winter dens. One additional larder was found by tracking the movement of seeds labeled with radioactive scandium-46 from scattered caches into the larder. Chipmunks formed winter dens and rapidly provisioned winter larders in the fall, just before the onset of winter. Surface caches were dynamic, with seeds residing in 1-6 cache sites (x - = 2.6, s = 1.1) before being found in the larder. Distances from scattered caches to the winter larder were 34.5 m (s = 17.1). Contents of winter larders consisted of pine and shrub seeds. In 14 of the 15 larders, pine seeds contributed most to the size and caloric content of larders. Pine seeds and other seeds found in winter larders were produced by plants 2-4 months before the onset of winter. We conclude that if yellow-pine chipmunks did not scatter-hoard seeds during summer and autumn, seeds would not have been available for use in winter larders.

Habitat differences affect life history tactics of a pulsed resource consumer, the edible dormouse (Glis glis)

AbstractWe studied flexibility of life history tactics, in terms of habitat‐dependent survival and reproduction, in a pulsed resource consumer, the edible dormouse (Glis glis). We compared capture–mark–recapture data from three subpopulations of dormice: one in a homogeneous beech forest (Forest), and two in patches of woodland (Grove/Hedge), with more constant but less energy‐rich food availability (e.g., fleshy fruits), over a period of 5 years. The general seasonal pattern of hibernation and reproduction was similar in all three subpopulations. Juveniles were born in only 3 out of 5 years at all study sites, which was paralleled by the occurrence of strong seed production in beech. Reproductive output (number of juveniles/female) was lower at the two sites with low seed tree abundance (Grove: 1.3; Hedge: 2.0) than in the Forest (4.4). Yearly survival probability of adults was significantly lower in the Forest (0.57, CI = 0.42–0.70) than in the areas Grove and Hedge (0.83, CI = 0.70–0.91). Despite their shortened lifespan, estimated lifetime reproductive success of females in the Forest was higher (6.2 young) than in the areas Grove/Hedge (4.8 young). Together, these data indicate that, in more constant habitats (Grove/Hedge), lower reproductive investment was associated with increased longevity. However, dormice apparently maximise lifetime reproductive success by a ‘sit tight’ strategy that synchronises reproduction with energy rich seed pulses in deciduous forests.

Ambient temperature and annual timing affect torpor bouts and euthermic phases of hibernating European ground squirrels (Spermophilus citellus)

The low body temperature state of hibernating mammals is interrupted regularly by short euthermic phases. The frequency of these euthermic phases changes according to the phase of hibernation. This typical pattern, common among ground squirrels (genus Spermophilus F. Cuvier, 1825), can be regulated by internal factors and affected by outside temperature. To evaluate the effects of internal annual timing and ambient temperature, we monitored nest temperatures of overwintering European ground squirrels ( Spermophilus citellus (L., 1766)) under three temperature conditions during late hibernation (9, 5, 0 °C). Our results showed that in spite of constant thermal conditions, an annual timing effect changed torpor-bout length (TBL) at 9 and 5 °C but not at 0 °C. Ambient temperature had an independent influence on TBL and euthermic phases. The loss in body mass was higher at higher ambient temperatures and was affected by TBL and euthermic phases. Thus, the hibernation pattern of European ground squirrels is regulated by both an annual timing pattern and the ambient temperature in the hibernacula.

Modification and miniaturization of Thermochron iButtons for surgical implantation into small animals

Thermochron iButtons are being used increasingly by animal physiologists to measure long-term patterns of body temperature in reptiles, birds and mammals. Typically, iButtons are surgically implanted into the intraperitoneal cavity where they measure and store body temperature together with the date and time from an onboard real-time clock. In 16-bit resolution, the DS1922L iButton can store a total of 4,096 data points over pre-determined sampling intervals. iButtons have proved invaluable in measuring patterns of torpor and hibernation in animals larger than 70 g. Weighing around 3.5 g after potting with wax, iButtons are too heavy and large to implant into animals smaller than 70 g because their weight exceeds 5% of the animal's total body weight. This paper describes how the stainless steel canister housing the DS 1922L iButton battery and circuit board can be removed to reduce the weight of the components to 1.49 g after waxing (ready for implantation) without compromising the function or battery life of the iButton. The modified iButton can be implanted into animals as small as 20-30 g. Calibration data revealed an offset of ca. 1 degrees C on average, confirming that iButtons must be calibrated prior to implantation.

Mammalian hibernation as a model of disuse osteoporosis: the effects of physical inactivity on bone metabolism, structure, and strength

Reduced skeletal loading typically leads to bone loss because bone formation and bone resorption become unbalanced. Hibernation is a natural model of musculoskeletal disuse because hibernating animals greatly reduce weight-bearing activity, and therefore, they would be expected to lose bone. Some evidence suggests that small mammals like ground squirrels, bats, and hamsters do lose bone during hibernation, but the mechanism of bone loss is unclear. In contrast, hibernating bears maintain balanced bone remodeling and preserve bone structure and strength. Differences in the skeletal responses of bears and smaller mammals to hibernation may be due to differences in their hibernation patterns; smaller mammals may excrete calcium liberated from bone during periodic arousals throughout hibernation, leading to progressive bone loss over time, whereas bears may have evolved more sophisticated physiological processes to recycle calcium, prevent hypercalcemia, and maintain bone integrity. Investigating the roles of neural and hormonal control of bear bone metabolism could give valuable insight into translating the mechanisms that prevent disuse-induced bone loss in bears into novel therapies for treating osteoporosis.

Daily rhythmicity and hibernation in the Anatolian ground squirrel under natural and laboratory conditions

We studied daily rhythmicity of body temperature (T(b)) before and during hibernation in Anatolian ground squirrels (Spermophilus xanthoprymnus) under natural and laboratory conditions using surgically implanted temperature loggers. Under both conditions, robust daily T(b) rhythmicity with parameters comparable to those of other ground squirrel species was observed before but not during hibernation. Euthermic animals had robust daily T(b) rhythms with a mean of 37.0 degrees C and a range of excursion of approximately 4 degrees C. No T(b) rhythm was detected during torpor bouts, either because T(b) rhythmicity was absent or because the daily range of excursion was smaller than 0.2 degrees C. The general patterns of hibernation that we observed in Anatolian ground squirrels were similar to those previously observed by other investigators in other species of ground squirrels.

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.

Testis development and testosterone secretion in captive European ground squirrels before, during, and after hibernation

In some hibernating species, an extended euthermic period before spring emergence has been reported during which testicular maturation occurred. In this study, we investigated whether male European ground squirrels Spermophilus citellus (Linnaeus, 1766) develop scrotal testes before or after the termination of hibernation. The course of testis development and testosterone concentrations were examined in young-of-year male ground squirrels (n = 4) before, during, and after their first hibernation. In the environmental chamber, all animals showed regular hibernation patterns with decreasing torpor bout lengths prior to the end of hibernation. Four weeks before hibernation ended, testosterone levels were elevated during spontaneous arousals. Testosterone concentrations peaked during the first 2 months post heterothermy and decreased thereafter. In 2 experimental males, testes descended from the inguinal region into the scrotum shortly before the end of heterothermy. The state of testis development and testosterone secretion corresponded to that found in semi-free-living males at spring emergence. Testis size increased in active animals to maximum widths during weeks 3 and 4 post heterothermy. Scrotal skin pigmentation was absent until heterothermy ended and developed during the first month thereafter. The data suggest that male S. citellus do not need a pre-emergence euthermic period for reproductive development.

Hibernation and emergence pattern of Tupinambis merianae (Squamata: Teiidae) in the Taim Ecological Station, southern Brazil

The emergence period and winter aggregations of a population of Tupinambis merianae from southern Brazil as well as some behavioural aspects from its post‐emergence period are examined. Fifty‐six individuals were captured and marked in 64 days (640 h) of field study. Most of the hibernacula identified were beneath human constructions. The first individuals emerged in August and the last active ones were observed in April. The population's emergence shows a protandric pattern, where males emerge before females, both in adults and juveniles. After emerging, males basked in aggregations of up to 13 individuals, in which individuals changed positions following audible resonant signals emitted by the lizards. Sibilated sounds were emitted in stress situations or in agonistic interactions. Future studies are necessary to elucidate behaviour patterns of the species in the natural environment, mainly related to the utilization of sound communication.

Hibernation patterns in mammals: a role for bacterial growth?

Summary 1 To examine the hypothesis that stimulation of immune function plays a role in periodic arousal from hibernation, bacterial growth during hibernation was estimated using a simple mathematical model of the general dynamics of bacterial abundance at body temperatures experienced during hibernation. 2 In the model, periodic arousals were important for animals infected with Salmonella at body temperatures above 7 °C, but not below. In contrast, periodic arousals appeared to be important at all temperatures examined when infected with several species of coliform bacteria and Pseudomonas, species that grow well at low temperatures. 3 The modelled outputs were compared with torpor patterns seen in captive European Ground Squirrels, Spermophilus citellus, under natural light and temperature conditions. We used maximum likelihood to estimate model parameters and show that the six bacterial species examined are consistent with the immune stimulation hypothesis. 4 Our analyses suggest that bacterial infection could be a selective force on torpor behaviour and warrants further experimental investigation.

Yellow-bellied Marmots (Marmota flaviventris) Hibernate Socially

Of 14 species of marmots (genus Marmota, Family Sciuridae), only 2, the woodchuck (M. monax) and yellowbellied marmot (M. flaviventris), have not been reported to be obligate social hibernators. There is one published report of yellow-bellied marmot juveniles hibernating together at a subalpine site, and social hibernation was reported at a single high-alpine site. Solitary hibernation is expected in woodchucks because they do not share burrows during summer, but is unexpected in yellow-bellied marmots, a harem-polygynous species where females may share burrows and have extensive home-range overlap with female kin during summer. We documented emergence patterns in 13 matrilines to determine whether adult marmots hibernate socially. We found that adult males hibernated with 1 or more adult females, and mothers hibernated with their offspring. Therefore, we conclude that yellow-bellied marmots hibernate socially. There is, however, no evidence that suggests that yellow-bellied marmots receive social thermoregulatory benefits from social hibernation. Documenting social hibernation required us to quantify patterns of emergence from hibernation. Throughout our subalpine site, emergence appears to be getting earlier; a result consistent with a previous report based on 1 colony site and which suggests the effects of global climate change are affecting hibernation patterns.

The role of energy availability in Mammalian hibernation: a cost-benefit approach.

Hibernation is widely regarded as an adaptation to seasonal energy shortage, but the actual influence of energy availability on hibernation patterns is rarely considered. Here we review literature on the costs and benefits of torpor expression to examine the influence that energy may have on hibernation patterns. We first establish that the dichotomy between food- and fat-storing hibernators coincides with differences in diet rather than body size and show that small or large species pursuing either strategy have considerable potential scope in the amount of torpor needed to survive winter. Torpor expression provides substantial energy savings, which increase the chance of surviving a period of food shortage and emerging with residual energy for early spring reproduction. However, all hibernating mammals periodically arouse to normal body temperatures during hibernation. The function of these arousals has long been speculated to involve recovery from physiological costs accumulated during metabolic depression, and recent physiological studies indicate these costs may include oxidative stress, reduced immunocompetence, and perhaps neuronal tissue damage. Using an optimality approach, we suggest that trade-offs between the benefits of energy conservation and the physiological costs of metabolic depression can explain both why hibernators periodically arouse from torpor and why they should use available energy to minimize the depth and duration of their torpor bouts. On the basis of these trade-offs, we derive a series of testable predictions concerning the relationship between energy availability and torpor expression. We conclude by reviewing the empirical support for these predictions and suggesting new avenues for research on the role of energy availability in mammalian hibernation.

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.

The effect of a linseed oil diet on hibernation in yellow-bellied marmots ( Marmota flaviventris)

The essential fatty acids (EFAs), α-linolenic acid (18:3,n-3) and linoleic acid (18:2,n-6) are known to be important for mammalian hibernation. In marmots ( Marmota flaviventris), reducing both dietary EFAs alters hibernation patterns by causing an increase in energy expenditure, but hibernation still occurs. In this study, marmots fed a diet high in α-linolenic acid, with normal linoleic acid levels, had significantly ( p < 0.05) more α-18:3 in their WAT and plasma unesterified fatty acids after 4 months than did marmots fed a control diet. During the winter, the control marmots hibernated normally while the marmots fed the α-18:3 diet did not hibernate, continued to eat, and lost less mass than the control group during the winter. These results suggest that α-18:3 may play a role in regulating normal hibernation behavior in marmots.

Sex and Age Differences in Mass, Morphology, and Annual Cycle in European Ground Squirrels, Spermophilus citellus

We collected 6 years of data (1990-1995) on survival, hibernation, body-mass changes, and morphological parameters for a suburban population of European ground squirrels (Spermophilus citellus) using censusing and capture-recapture techniques. We attempted to determine differences in sex and age in these parameters. In the focal population, sex ratios of adults and yearlings were female-biased, but the sex ratio of juveniles was balanced. Overwinter mortality was low, but losses during the active season were high in all sex and age groups. Male and female juveniles disappeared from their natal area in roughly equal proportions. Among older individuals, more males disappeared than females. Hibernation patterns were similar to other Spermophilus species, except that females began hibernation before males. Therefore, females had significantly longer hibernation periods and higher proportional overwinter losses of mass than males. All adult (greater than or equal to 2 years) but only a few yearling males were reproductively active. Yearling males emerged from hibernation with a lower mass than adults but were indistinguishable from them before subsequent immergence. Adult and yearling females reproduced and lost mass during late lactation, a pattern more pronounced in older than yearling females. Juvenile males were heavier than juvenile females before hibernation, although no difference was found at weaning. Skull size increased in the first two active seasons but did not change thereafter. Differences in sex and age resembled those of most hibernating,ground squirrels in many aspects but also showed some unusual patterns that probably have evolved due to specific environmental constraints in this species.

The influence of hibernation patterns on the critical enzymes of lipogenesis and lipolysis in prairie dogs

White-tailed prairie dogs (Cynomys leucurus) are spontaneous hibernators that enter torpor each fall, whereas black-tailed prairie dogs (C. ludovicianus) hibernate facultatively only when food- or water-stressed during the winter. The body masses of both species greatly increase during the fall feeding period, with most of this gain in the form of depot fat. Body fat is utilized during winter fasting and/or hibernation. We measured the activities of fatty acid synthase (FAS), ATP-citrate lyase (ACL), malic enzyme (ME), glucose-6-phosphate dehydrogenase (G6PDH), and hormone-sensitive lipase (HSL) in the tissues of both C.leucurus (hibernating and euthermic) and C. ludovicianus (euthermic only) under controlled conditions. The activities of FAS, ACL, and G6PDH in the liver all decreased during hibernation. The activities of ME and G6PDH in white adipose tissue (WAT) were also reduced during hibernation. Euthermic C. leucurus and euthermic C. ludovicianus differed only in brown adipose (BAT) ACL and WAT G6PDH activities. No significant differences in HSL activities were found between these two species or between euthermic and hibernating animals. These results suggest that this seasonal body fat cycle is due, at least in part, to seasonal variations in the activities of FAS, ME, ACL, and G6PDH that affect the rate of fatty acid synthesis. This study also demonstrates that spontaneous hibernators do not have a greater capacity to synthesize fatty acids during the fall than facultative hibernators, as previously suggested.

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.

Suprachiasmatic nucleus: role in circannual body mass and hibernation rhythms of ground squirrels

Female golden-mantled ground squirrels that sustained complete ablation of the suprachiasmatic nucleus (SCNx) were housed pre- and post-operatively at 23°C and then at 6.5°C for 5–7 yr. SCNx and control animals held at the higher temperature manifested circannual rhythms (CARs) in body mass. In contrast, body mass CARs were not expressed in 50% of SCNx squirrels during cold exposure; rhythm amplitude was reduced to 25–40% of pre-operative values and the interval between successive peaks in body mass fell outside the circannual range. Unlike normal squirrels that hibernate for about 6 months during each circannual cycle, these SCNx squirrels expressed bouts of torpor nearly continuously throughout 2.5 yr of cold exposure. Body mass increases were often observed during hibernation—a phenomenon never observed in control animals. The remaining SCNx squirrels that did not hibernate continuously displayed CARs in body mass within the normal range. The effects of SCN ablation on body mass rhythms presumably are related to disrupted patterns of hibernation, food intake, and metabolism. The SCN, which sustains neural and metabolic activity at low tissue temperatures, may exert greater influence on thermoregulation and metabolism during the hibernation season than at other times of year, thereby accounting for the greater effect of SCN ablation in squirrels maintained at low ambient temperatures.

Ablation of suprachiasmatic nucleus alters timing of hibernation in ground squirrels.

Hibernation patterns were monitored continuously for 2.5 years in female squirrels that were neurologically intact or in which the hypothalamic suprachiasmatic nucleus (SCN) was completely ablated (SCNx). The number of hibernation bouts in SCNx squirrels increased by 159%, total hibernation time increased by 58%, and periodic arousals from hibernation were 47% longer in SCNx than in control squirrels; the duration of individual torpor bouts was 2 days shorter and far more variable in SCNx than in control animals. Some SCNx squirrels cycled through bouts of torpor continuously for nearly 2 years. The SCN appears to be part of the mechanism that controls the duration of the hibernation season and the temporal structure of individual torpor bouts.