Hibernation Patterns Research Articles

Frequency-modulated timer regulates torpor–arousal cycles during hibernation in distinct small mammalian hibernators

Hibernation allows mammals to endure harsh seasons by reducing their basal metabolism and body temperature (Tb) to minimize energy expenditure. During hibernation in small animals such as Syrian hamsters and 13-lined ground squirrels, Tb decreases to an ambient level ( < 5 °C) and remains constant for days to weeks in a physiological condition termed deep torpor. Torpor is interrupted by periods of arousal, during which Tb recovers to a euthermic level (approximately 37 °C), and these torpor–arousal cycles are repeated multiple times during hibernation. However, little is known about the mechanisms governing Tb fluctuations during hibernation. In this study, we employed an unbiased model selection approach to Tb data and revealed that a model incorporating frequency modulation quantitatively reproduced Tb fluctuation during hibernation in Syrian hamsters. We found that an unexpectedly long period of 120–430 days modulates a shorter period of several days. In addition, the aforementioned model reproduced Tb fluctuation in 13-lined ground squirrels, which can undergo repeated hibernation according to intrinsic circannual rhythms in constant laboratory conditions. This is the first quantitative study to demonstrate the concerted action of two endogenous periods, one lasting a few days and the other lasting a year, in the torpor–arousal cycles of distinct mammalian hibernators. We anticipate that our theoretical analysis of Tb fluctuation will be a starting point for quantitative comparisons of hibernation patterns across various hibernating species. Furthermore, quantification of Tb data using models will foster our understanding of the molecular mechanisms of hibernation by revealing the biological processes operating within these periods.

Physiological and behavioural adaptations by big brown bats hibernating in dry rock crevices.

Winter energy stores are finite and factors influencing patterns of activity are important for overwintering energetics and survival. Hibernation patterns (e.g., torpor bout duration and arousal frequency) often depend on microclimate, with more stable hibernacula associated with greater energy savings than less stable hibernacula. We monitored hibernation patterns of individual big brown bats (Eptesicus fuscus; Palisot de Beauvois, 1796) overwintering in rock-crevices that are smaller, drier, and less thermally stable than most known cave hibernacula. While such conditions would be predicted to increase arousal frequency in many hibernators, we did not find support for this. We found that bats were insensitive to changes in hibernacula microclimate (temperature and humidity) while torpid. We also found that the probability of arousal from torpor remained under circadian influence, likely because throughout the winter during arousals, bats commonly exit their hibernacula. We calculated that individuals spend most of their energy on maintaining a torpid body temperature a few degrees above the range of ambient temperatures during steady-state torpor, rather than during arousals as is typical of other small mammalian hibernators. Flight appears to be an important winter activity that may expedite the benefits of euthermic periods and allow for short, physiologically effective arousals. Overall, we found that big brown bats in rock crevices exhibit different hibernation patterns than conspecifics hibernating in buildings and caves.

An evaluation of the macro anatomy of the Hazel Dormouse’s (Muscardinus avellanarius Linnaeus, 1758) (Rodentia: Mammalia) skeletal system in Türkiye

Muscardinus avellanarius, one of the thirty species of the Gliridae family, is found in areas covered with deciduous forests, with a range stretching from Bursa (Uludağ) to Trabzon in Türkiye. Hazel Dormouse, classified as an endangered species and characterized by their deep hibernation patterns, possess significant value as bioindicators of environmental change. In this study, a macro-anatomical evaluation of the skeletal structure of forty-six specimens collected from the Eastern and Western Black Sea Regions between 1979 and 1983 were conducted. The evaluation revealed that the whole skeleton of Muscardinus avellanarius consisted of 225 bones. The morphometric variances and variations between the Eastern Black Sea and Western Black Sea specimens were detected by defining the skull and baculum bones that hold taxonomic value.

Effects of climate change on life‐history traits in hibernating mammals

Abstract Animals can respond to climate change through changes in behaviour, morphology or life‐history traits. Changes in life‐history traits do not occur independently, as they trade off or co‐evolve with other traits. Hibernation is a life‐history trait used to cope with periods of low resource availability. The energetic and survival benefits of hibernation depend on environmental conditions. Climate change‐induced changes in hibernation patterns are therefore likely to affect other life‐history traits through trade‐offs. We systematically reviewed the literature to: 1) identify studies testing for associations between climatic variables and life‐history traits in mammalian hibernators; and 2) assess variation in responses between species. Air temperature was the most commonly measured climatic variable, and phenology of hibernation emergence was the most commonly studied life‐history trait. In most studies and species, emergence date became earlier, litter size increased and the number of interbout arousals increased with increasing air temperature. Despite being considered key life‐history traits due to their potential to influence population dynamics, our search returned no studies on the effects of climatic variables on the age of primiparity or on the age distribution of reproduction. Directions of associations between climatic variables and life‐history traits often differed between species, and both species‐ and sex‐specific variations occurred in response to climatic variables for some traits. We highlight the importance of long‐term, species‐specific research, and the need for further studies on indirect effects of climatic cues on co‐adapted traits to understand the potential for mammalian hibernators to respond to ongoing and future climate change.

Characterization of Pseudogymnoascus destructans conidial adherence to extracellular matrix: Association with fungal secreted proteases and identification of candidate extracellular matrix binding proteins.

Pseudogymnoascus destructans is the etiological agent of white-nose syndrome (WNS), a fungal skin infection of hibernating bats. Pathophysiology of the disease involves disruption of bat metabolism and hibernation patterns, which subsequently causes premature emergence and mortality. However, information on the mechanism(s) and virulence factors of P. destructans infection is minimally known. Typically, fungal adherence to host cells and extracellular matrix (ECM) is the critical first step of the infection. It allows pathogenic fungi to establish colonization and provides an entry for invasion in host tissues. In this study, we characterized P. destructans conidial adherence to laminin and fibronectin. We found that P. destructans conidia adhered to laminin and fibronectin in a dose-dependent, time-dependent and saturable manner. We also observed changes in the gene expression of secreted proteases, in response to ECM exposure. However, the interaction between fungal conidia and ECM was not specific, nor was it facilitated by enzymatic activity of secreted proteases. We therefore further investigated other P. destructans proteins that recognized ECM and found glyceraldehyde-3-phosphate dehydrogenase and elongation factor 1-alpha among the candidate proteins. Our results demonstrate that P. destructans may use conidial surface proteins to recognize laminin and fibronectin and facilitate conidial adhesion to ECM. In addition, other non-specific interactions may contribute to the conidial adherence to ECM. However, the ECM binding protein candidates identified in this study highlight additional potential fungal virulence factors worth investigating in the P. destructans mechanism of infection in future studies.

Elevated plasma phospholipid n-3 docosapentaenoic acid concentrations during hibernation.

Factors for initiating hibernation are unknown, but the condition shares some metabolic similarities with consciousness/sleep, which has been associated with n-3 fatty acids in humans. We investigated plasma phospholipid fatty acid profiles during hibernation and summer in free-ranging brown bears (Ursus arctos) and in captive garden dormice (Eliomys quercinus) contrasting in their hibernation patterns. The dormice received three different dietary fatty acid concentrations of linoleic acid (LA) (19%, 36% and 53%), with correspondingly decreased alpha-linolenic acid (ALA) (32%, 17% and 1.4%). Saturated and monounsaturated fatty acids showed small differences between summer and hibernation in both species. The dormice diet influenced n-6 fatty acids and eicosapentaenoic acid (EPA) concentrations in plasma phospholipids. Consistent differences between summer and hibernation in bears and dormice were decreased ALA and EPA and marked increase of n-3 docosapentaenoic acid and a minor increase of docosahexaenoic acid in parallel with several hundred percent increase of the activity index of elongase ELOVL2 transforming C20-22 fatty acids. The highest LA supply was unexpectantly associated with the highest transformation of the n-3 fatty acids. Similar fatty acid patterns in two contrasting hibernating species indicates a link to the hibernation phenotype and requires further studies in relation to consciousness and metabolism.

Hypothesis and Theory: A Two-Process Model of Torpor-Arousal Regulation in Hibernators.

Hibernating mammals drastically lower their metabolic rate (MR) and body temperature (Tb) for up to several weeks, but regularly rewarm and stay euthermic for brief periods. It has been hypothesized that the necessity for rewarming is due to the accumulation or depletion of metabolites, or the accrual of cellular damage that can be eliminated only in the euthermic state. Recent evidence for significant inverse relationships between the duration of torpor bouts (TBD) and MR in torpor strongly supports this hypothesis. We developed a new mathematical model that simulates hibernation patterns. The model involves an hourglass process H (Hibernation) representing the depletion/accumulation of a crucial enzyme/metabolite, and a threshold process Hthr. Arousal, modelled as a logistic process, is initiated once the exponentially declining process H reaches Hthr. We show that this model can predict several phenomena observed in hibernating mammals, namely the linear relationship between TMR and TBD, effects of ambient temperature on TBD, the modulation of torpor depth and duration within the hibernation season, (if process Hthr undergoes seasonal changes). The model does not need but allows for circadian cycles in the threshold T, which lead to arousals occurring predominantly at certain circadian phases, another phenomenon that has been observed in certain hibernators. It does not however, require circadian rhythms in Tb or MR during torpor. We argue that a two-process regulation of torpor-arousal cycles has several adaptive advantages, such as an easy adjustment of TBD to environmental conditions as well as to energy reserves and, for species that continue to forage, entrainment to the light-dark cycle.

Trans-2-hexenal downregulates several pathogenicity genes of Pseudogymnoascus destructans, the causative agent of white-nose syndrome in bats.

White-nose syndrome is an emergent wildlife disease that has killed millions of North American bats. It is caused by Pseudogymnoascus destructans, a cold-loving, invasive fungal pathogen that grows on bat tissues and disrupts normal hibernation patterns. Previous work identified trans-2-hexenal as a fungistatic volatile compound that potentially could be used as a fumigant against P. destructans in bat hibernacula. To determine the physiological responses of the fungus to trans-2-hexenal exposure, we characterized the P. destructans transcriptome in the presence and absence of trans-2-hexenal. Specifically, we analyzed the effects of sublethal concentrations (5 μmol/L, 10 μmol/L, and 20 μmol/L) of gas-phase trans-2-hexenal of the fungus grown in liquid culture. Among the three treatments, a total of 407 unique differentially expressed genes (DEGs) were identified, of which 74 were commonly affected across all three treatments, with 44 upregulated and 30 downregulated. Downregulated DEGs included several probable virulence genes including those coding for a high-affinity iron permease, a superoxide dismutase, and two protein-degrading enzymes. There was an accompanying upregulation of an ion homeostasis gene, as well as several genes involved in transcription, translation, and other essential cellular processes. These data provide insights into the mechanisms of action of trans-2-hexenal as an anti-fungal fumigant that is active at cold temperatures and will guide future studies on the molecular mechanisms by which six carbon volatiles inhibit growth of P. destructans and other pathogenic fungi.

Heterothermy as the Norm, Homeothermy as the Exception: Variable Torpor Patterns in the South American Marsupial Monito del Monte (Dromiciops gliroides).

Hibernation (i.e., multiday torpor) is considered an adaptive strategy of mammals to face seasonal environmental challenges such as food, cold, and/or water shortage. It has been considered functionally different from daily torpor, a physiological strategy to cope with unpredictable environments. However, recent studies have shown large variability in patterns of hibernation and daily torpor (“heterothermic responses”), especially in species from tropical and subtropical regions. The arboreal marsupial “monito del monte” (Dromiciops gliroides) is the last living representative of the order Microbiotheria and is known to express both short torpor episodes and also multiday torpor depending on environmental conditions. However, only limited laboratory experiments have documented these patterns in D. gliroides. Here, we combined laboratory and field experiments to characterize the heterothermic responses in this marsupial at extreme temperatures. We used intraperitoneal data loggers and simultaneous measurement of ambient and body temperatures (TA and TB, respectively) for analyzing variations in the thermal differential, in active and torpid animals. We also explored how this differential was affected by environmental variables (TA, natural photoperiod changes, food availability, and body mass changes), using mixed-effects generalized linear models. Our results suggest that: (1) individuals express short bouts of torpor, independently of TA and even during the reproductive period; (2) seasonal torpor also occurs in D. gliroides, with a maximum bout duration of 5 days and a mean defended TB of 3.6 ± 0.9°C (one individual controlled TB at 0.09°C, at sub-freezing TA); (3) the best model explaining torpor occurrence (Akaike information criteria weight = 0.59) discarded all predictor variables except for photoperiod and a photoperiod by food interaction. Altogether, these results confirm that this marsupial expresses a dynamic form of torpor that progresses from short torpor to hibernation as daylength shortens. These data add to a growing body of evidence characterizing tropical and sub-tropical heterothermy as a form of opportunistic torpor, expressed as daily or seasonal torpor depending on environmental conditions.

The Spiritual Life of Teleilat Ghassul and Building 78

This article explores the spiritual life of the community at Chalcolithic Teleilat Ghassul through a reinterpretation of the frescoes within Building 78 on Tell 3. The building itself was likely used as a “lineage house” and a center of ritual activity, which is evidenced through the frescoes (the bird fresco and spook masks), numerous cornets, and 200–300 years of phasing. This article argues, through ethnographic and ecological evidence, that the bird fresco represents a moorhen, symbolizes spiritual liminality, and is tied to cyclical symbolism through the location of Teleilat Ghassul on a major migration route. Furthermore, the spook masks can be interpreted as hedgehogs that are also tied to a cyclical symbolism through their hibernation patterns. This reinterpretation may allow us to posit the types of rituals that occurred in Building 78, for example, harvest or coming-of-age rituals.

Hibernation Patterns in Grey Collared Chipmunks ( Neotamias cinereicollis )

Animals living in natural environments face daily and seasonal variation in environmental and ecological conditions. Winter is a major energetic challenge to temperate and arctic endotherms, as snow cover and low ambient temperature simultaneously reduce resource availability and increase resource requirements. Possible strategies that animals use to cope with these challenges include torpor and/or hibernation, when animals profoundly reduce body temperature and metabolic rate for several hours or weeks at a time. Chipmunks are small diurnal rodents considered to be facultative hibernators. Although western chipmunks (Neotamias spp) are represented by 23 species, most of our knowledge on chipmunk physiology and behavior comes from the Eastern chipmunk (Tamias striatus). Therefore, the aim of this study is to investigate the presence and patterns of hibernation in the grey collared chipmunk (Neotamias cinereicollis), a representative of the genus Neotamias. Also, we investigate the relationship between hibernation patterns and environmental conditions in a species assumed to be a facultative hibernator. We predict chipmunks display hibernation and that low temperatures and snow cover will be good predictors of hibernation length and onset. Grey collared chipmunks (n=7) were implanted intraperitoneally with body temperature loggers (iButtons: DS1922; Maxim) and housed in outdoor seminatural enclosures for a year where they experienced the natural weather regime but had access to food and water ad libitum. During this period, environmental variables were recorded (HOBO U30; Onset; Bourne-MA), including ambient temperature and snow cover. All chipmunks displayed hibernation starting late fall/early winter. Body temperature recordings indicated that chipmunks spend on average 81±29.5 days hibernating. During hibernation, torpor bouts averaged 3.17±2 days with the longest bout of torpor lasting for 10.1 days. During the hibernation season, average body temperature varied from 36.4±0.5C when euthermic to 5.6±3.6C during torpor bouts. The lowest body temperature recorded was -0.5C. Further analyses are being conducted to describe interrelationships among snow cover, ambient temperature and patterns of hibernation displayed by the chipmunks. Understanding hibernation patterns and their relationship with climate is important, as changes in climate and resource availability are expected to be major stressors for organisms, potentially leading to species decline.

Retrospective analysis of hibernation parameters and breeding success in captive Vancouver Island marmots (Marmota vancouverensis): 1997-2018.

Vancouver Island marmots (Marmota vancouverensis) have been managed in a captive-breeding program since 1997, as in situ conservation efforts were insufficient in raising the numbers of this critically endangered species. The success of captive-breeding programs centers on sustainable reproduction and survival of individuals once released into the wild. Captive-born Vancouver Island marmots released to the wild have lower survival rates than their wild-born counterparts; this difference may arise from compromised hibernation patterns or behaviors. Hibernation duration, body weight over the hibernation season, and reproductive success of captive Vancouver Island marmots were reviewed to assess the effect of these variables on each other. Data from a total of 1782 hibernations and 456 breeding attempts were compiled from 1997 to 2018. The number of winters spent in captivity, the origin of the marmot (captive-born or wild-born), the facility at which hibernation occurred, and the body weight all had a significant effect on hibernation length (all p < .001). Increased weight was associated with increased hibernation length by 0.4 ± 0.1 day/kg on average (p = .0015). Captive, wild-born marmots hibernated for significantly longer than their captive-born counterparts by about 21 ± 2 days (p < .001). The odds of successful breeding were significantly increased with increasing hibernation length by approximatively 20% for every 10 additional days of hibernation. This study provides information on the intrinsic relationship between body weight, reproduction, and hibernation in captive Vancouver Island marmots.

Is There a Record of Hibernation on the Surface of Incisors in the Common Hamster (Cricetus cricetus, Rodentia, Cricetidae)?

As was shown earlier, in some hibernating rodents the patterns of hibernation are recorded by tooth dentine and can be revealed in stained or ground sections of the incisors, as well as on the incisor surface. Hibernation in the common hamster, Cricetus cricetus, can be described as facultative with great individual variability of the body temperature dynamics during the winter. To investigate the records of hibernation on the incisor surface of this species, we studied the lower incisors of hamsters that had wintered with implanted temperature data loggers under natural conditions in a city park of Simferopol, Crimea (two animals); in semi-natural conditions in the village of Khunzakh, Dagestan (two animals); and using 19 hamsters from a natural population found dead in Simpferopol or its environs during late winter or early spring. Previous studies of eight hamsters that were kept under laboratory conditions and that had received tetracycline injections confirmed the daily formation of the increments on the incisor surface. This data allowed us to find the part of the incisor that could have been formed during hibernation in the hamsters with implanted loggers. In three of four of them, the typical pattern of daily increments was disrupted in the parts presumably formed during hibernation. The patterns of disruption varied in different animals, and it was impossible to interpret them as a record of hibernation. Those hamsters revealed no sequences of narrow and clearer increments characteristic of the records of hibernation on incisors. Such a sequence was seen on incisors of only one of 19 hamsters from the natural population. Consequently, no unambiguous record of the periods of hypothermia was found on the surface of incisors in the common hamster. According to the data published earlier, hibernation records on incisors were found in other hamsters of the subfamily Cricetinae (the genera Allocricetulus and Mesocricetus, in particular). A comparison of the dynamics of body temperature during hibernation in these hamsters and in the common hamster allow us to surmise that the formation of narrow increments can be determined in part by the depth and duration of hypothermia, but it mainly depends on the duration of normothermia and the feeding habits of animals during hibernation.

Hibernation Patterns of the European Hedgehog, Erinaceus europaeus, at a Cornish Rescue Centre.

Simple SummaryPopulations of the European hedgehog, Erinaceus europaeus, are declining in the UK. This small mammal is frequently admitted to rescue centres in the UK to be treated for a variety of illnesses or injuries. With many spending the winter in captivity, clear guidelines about how to look after hedgehogs during their hibernation would be very useful. We studied 35 hedgehogs over two winters to learn about their sleeping behaviour and how they change weight. We measured the total length of hibernation and the periods during hibernation when hedgehogs are more active (called spontaneous arousals). There were three main results. (1) The longer the hibernation, the more weight was lost. (2) Previous studies show that arousal is energetically expensive. Despite this, weight-loss was more related to the amount of time spent sleeping than to the number of times the hedgehog woke up, perhaps because they could easily feed each time they woke up. (3) Larger hedgehogs lost proportionally less weight per day, perhaps because they woke up and fed more often than did smaller hedgehogs. Behaviour by hibernating hedgehogs in captivity differs from that in the wild. Patterns revealed in this study are used to make some recommendations for guidelines that can be adapted for individual hedgehogs according to their size and behaviour during hibernation.The European hedgehog, Erinaceus europaeus, is frequently admitted to rescue centres in the UK. With many overwintering in captivity, there is cause to investigate hibernation patterns in order to inform and improve husbandry and monitoring protocols. Thirty-five hedgehogs were studied over two winters. Weight change during hibernation for the first winter was used to test for effects of disturbance on different aspects of hibernation, including total duration, frequency and duration of spontaneous arousals. There was no significant difference between the two winters for any of the four aspects studied. Significant positive correlations demonstrated that weight-loss increased with the duration of the hibernation period and with percent of nights spent asleep, but not with the number of arousal events. Thus, weight-loss appears more strongly associated with the proportion of time spent asleep than with the number of arousal events. This was surprising given the assumed energetic expense of repeated arousal and was potentially due to availability of food during arousals. In contrast with previous studies, larger hedgehogs lost less weight per day than did smaller hedgehogs. They also woke up more often (i.e., had more opportunities to feed), which may explain the unexpected pattern of weight-loss. Hibernatory behaviour in captivity differs from that in the wild, likely because of non-natural conditions in hutches and the immediate availability of food. This study provides a basis for further research into the monitoring and husbandry of hedgehogs such that it can be adapted for each individual according to pre-hibernation weight and behaviour during hibernation.

Hibernation Records on the Incisor Surface in the Turkish Hamster (Mesocricetus brandti) (Rodentia, Cricetidae)

The teeth of an adult female of the Turkish hamster (Mesocricetus brandti) after hibernation in semi-natural conditions were examined to reveal a relationship between the hibernation pattern on the incisor surface and the data of a temperature logger. The female spent the winter in a burrow prepared by herself inside a wintering cage from October 2018 till May 2019. A temperature logger was implanted to the animal intraperitoneally to record body temperature at 20-min intervals. Regular bouts of hypothermia started in mid-October. The longevity of each hypothermia bout increased whereas the minimum body temperature decreased and reached its lowest value in March. Later, the process proceeded backwards until the end of the heterothermia period. In the apical region of the incisor, daily increments were wide and well-distinguished which indicates that they had formed before the onset of the heterothermal period. In the basal region, closer to the growth zone, the increments were narrow and distinct, and their number corresponded in general to the number of normothermia episodes bouts. At the very base of the incisor as well as at its apical part, typical daily increments were revealed again. However, no correlation between the longevity of normothermia bouts and the width of increments was found. These data varied greatly from two other hamsters. In the Ciscaucasian hamster (Mesocricetus raddei) the number and character of increments comply with the number and duration of normothermia bouts, in the Common hamster (Cricetus cricetus), the “hibernation zone” was not recorded on the incisor surface. The Turkish hamster demonstrate an intermediate pattern, which we explain by quite different hibernation conditions of these species.

Calcium homeostasis during hibernation and in mechanical environments disrupting calcium homeostasis.

To maintain calcium homeostasis during physical inactivity, precise coordination is necessary between different organs of the body. There are a number of factors which alter an organism's calcium balance, such as growth, aging, physical inactivity and acquired or inherited disorders which ultimately lead to bone loss. In non-hibernating mammals, physical inactivity causes bone loss which may not be completely recoverable during the lifespan of an individual despite a resumption of activity. Extreme physical inactivity and nutritional deprivation are two other important factors that lead to bone loss in non-hibernating mammals. The mechanism of bone loss is still poorly understood, however, there is some evidence which shows that during hibernation, smaller mammals (ground squirrels, bats, and hamsters) undergo bone loss. While on the other hand, hibernating bears do not show any sign of bone loss and retain their bone structure and strength. This may be due to differences in their hibernation patterns, as smaller mammals may excrete calcium throughout the hibernation period, which ultimately leads to bone loss, whereas bears seem to have a more developed and advanced mechanism to prevent calcium loss and maintain their bone structure. In this review, we summarize calcium homeostasis and its adaptive mechanisms with reference to bone loss in hibernating as compared to non-hibernating mammals. We also review the effect of microgravity and simulated microgravity on bone physiology and subsequent adaptation.

The effect of seasonal variation on the activity patterns of the American black bear: an ecological niche modeling approach

AbstractThe American black bear (Ursus americanus) has very plastic activity patterns that maximize its ability to adapt to changing environments. Hibernation length is positively correlated with latitude, where northern populations remain in hibernation for up to 5 months during the winter; however, the species may not hibernate at all in its southern range. Several studies have focused on the description of the species’ ecology from specific locations; however, the macroecological perspective of the seasonal activity in black bears has not been explored. Using ecological niche models and temporal climate transfers, we tested for a correlation between the 971 monthly activity records we obtained for this species within its whole distribution and monthly climatic conditions. We observed that there was a high degree of geographic overlap among the monthly potential transferred areas and the monthly presence locality records. Thus, we suggest that climate is one of the main factors affecting the cycles of activity of this species and explains its hibernation patterns.

A pharmacological composition for induction of a reversible torpor-like state and hypothermia in rats

AimsTo initiate a state of artificial torpor we suggested a pharmacological multi-targeting strategy for simulation of the physiological pattern of natural hibernation including a significant reduction in heart rate, respiratory rate, body temperature and oxygen consumption as well as a decline in brain activity known as torpor. Materials and methodsWe have developed a composition which initiates a pharmacologically induced torpor-like state (PITS-composition), made up of eight therapeutic agents, inert gas xenon and lipid emulsion served as a drug vehicle. Key findingsAfter a single intravenous injection to rats, PITS-composition causes a rapid decline in heart rate followed by a steady decrease in body temperature from about 38.5 °C to 31.5 °C, at ambient temperature of 22 °C–23 °C. The hypothermic state may continue on average for 16–17 h with the subsequent spontaneous return of heart rate and body temperature to the initial values. In the open field test at torpor the motility, rearing and grooming were suppressed but 4–8 days later they were restored. SignificanceSuspended animation states, including natural hibernation or pharmacologically induced synthetic torpor are of special attention of medicine, since it may improve survival rate after cardiac arrest, brain hemorrhage and ischemia, and during long-term space traveling. The suggested here multi-targeting strategy made possible to develop the pharmacological composition able, after a single intravenous injection, to initiate long, stable and reversible hypothermia and torpor at room temperature. After the torpor, animals were able to spontaneously restore both physiological parameters, and behavioral reactions.

Dietary Lipids Affect the Onset of Hibernation in the Garden Dormouse (Eliomys quercinus): Implications for Cardiac Function.

Dietary lipids strongly influence patterns of hibernation in heterotherms. Increased dietary uptake of n-6 polyunsaturated fatty acids (PUFAs), particularly of linoleic acid (LA, C18:2 n-6), enables animals to reach lower body temperatures (Tb), lengthens torpor bout duration, and results in lower energy expenditure during hibernation. Conversely, dietary n-3 PUFA impacts negatively on hibernation performance. PUFA in surrounding phospholipids (PLs) presumably modulate the temperature-dependent activity of the sarcoplasmic reticulum (SR) Ca2+ ATPase 2 (SERCA2) and thus determine the threshold Tb still allowing proper heart function during torpor. We tested the effect of diets enriched with 10% of either corn oil (“CO,” high n-6 PUFA, e.g., LA) or menhaden oil [“MO,” long-chain n-3 PUFA, e.g., docosahexaenoic acid (DHA)] on hibernation performance and SERCA2 activity levels during torpor in garden dormice, an insectivorous, fat-storing hibernator. Prior to hibernation, individuals fed the MO diet showed an almost nine-times higher DHA levels and 30% lower LA proportions in white adipose tissue (WAT), reflecting the fatty acid composition of SR membranes, compared to CO-diet fed animals. When fed the MO diet, dormice significantly delayed their mean onset of hibernation by almost 4 days (range: 0–12 days), compared with CO-diet fed animals. Hibernation onset correlated positively with WAT-DHA levels and negatively with WAT-LA proportions prior to hibernation. Subsequently, hibernating patterns were similar between the two dietary groups, despite a significant difference in WAT-LA but not in WAT-DHA levels in mid-hibernation. SR-PL fatty acid composition and SERCA2 activity were identical in torpid individuals from the two dietary groups in mid-hibernation. In line with our previous findings on Syrian hamsters, a granivorous, food-storing hibernator, SERCA2 activity correlated positively with LA and negatively with DHA levels of SR-PL in torpid dormice, although SERCA2 activity was about three-times higher in garden dormice than in Syrian hamsters at similar PL-DHA proportions. Similarly, minimal Tb during torpor decreased as SERCA2 activity increased. We conclude that: (1) fatty acid composition of SR membranes modulates cardiac SERCA2 activity, hence determining the minimum Tb tolerated by hibernators, and (2) high DHA levels prevent hibernators from entering into torpor, but the critical levels differ substantially between species.

Sex-specific effects of food supplementation on hibernation performance and reproductive timing in free-ranging common hamsters

Hibernation is characterized by reduced metabolism and body temperature during torpor bouts. Energy reserves available during winter play an important role for hibernation and some species respond to high energy reserves with reduced torpor expression. Common hamsters are food-storing hibernators and females hibernate for shorter periods than males, probably related to larger food stores. In this study, we provided free-ranging common hamsters with sunflower seeds shortly before winter and recorded body temperature using subcutaneously implanted data loggers. We compared hibernation patterns and body mass changes between individuals with and without food supplements and analysed reproductive onset in females. Supplemented males delayed hibernation onset, hibernated for much shorter periods, and emerged in spring with higher body mass than unsupplemented ones. Additional food did not affect hibernation performance in females, but supplemented females emerged earlier and preceded those without food supplements in reproductive onset. Thus, males and females differently responded to food supplementation: access to energy-rich food stores enabled males to shorten the hibernation period and emerge in better body condition, probably enhancing mating opportunities and reproductive success. Females did not alter hibernation patterns, but started to reproduce earlier than unsupplemented individuals, enabling reproductive benefits by an extended breeding period.