Physiology Of Hibernation Research Articles

Temperature alone is insufficient to understand hibernation energetics.

Energy conservation has long been a focal point in hibernation research. A long-standing assumption is that ambient temperature (Ta) largely defines the rate of energy expenditure because of well-known relationships between Ta, metabolic rate and frequency of arousal from torpor. Body condition and humidity also affect energy expenditure but are usually considered secondary factors. We held tricolored bats (Perimyotis subflavus) in captivity under multiple environmental conditions to directly compare the importance of Ta, fat mass and humidity for hibernation energy expenditure. Fat mass was the best predictor of female mass loss, followed by Ta and humidity. However, males had less fat and adopted a more energetically conservative hibernation strategy. Our results demonstrate that understanding the evolution of behavior, physiology and ecology of hibernation requires disentangling the relative contributions of multiple drivers of hibernation energetics, and that Ta is not always the most important factor driving energy expenditure.

Hibernation induces widespread transcriptional remodeling in metabolic tissues of the grizzly bear

Revealing the mechanisms underlying the reversible physiology of hibernation could have applications to both human and animal health as hibernation is often associated with disease-like states. The present study uses RNA-sequencing to reveal the tissue and seasonal transcriptional changes occurring in grizzly bears (Ursus arctos horribilis). Comparing hibernation to other seasons, bear adipose has a greater number of differentially expressed genes than liver and skeletal muscle. During hyperphagia, adipose has more than 900 differentially expressed genes compared to active season. Hibernation is characterized by reduced expression of genes associated with insulin signaling, muscle protein degradation, and urea production, and increased expression within muscle protein anabolic pathways. Across all three tissues we find a subset of shared differentially expressed genes, some of which are uncharacterized, that together may reflect a common regulatory mechanism. The identified gene families could be useful for developing novel therapeutics to treat human and animal diseases.

Sex-Dependent Phenological Plasticity in an Arctic Hibernator.

Hibernation provides a means of escaping the metabolic challenges associated with seasonality, yet the ability of mammals to prolong or reenter seasonal dormancy in response to extreme weather events is unclear. Here, we show that Arctic ground squirrels in northern Alaska exhibited sex-dependent plasticity in the physiology and phenology of hibernation in response to a series of late spring snowstorms in 2013 that resulted in the latest snowmelt on record. Females and nonreproductive males responded to the >1-month delay in snowmelt by extending heterothermy or reentering hibernation after several days of euthermy, leading to a >2-week delay in reproduction compared to surrounding years. In contrast, reproductive males neither extended nor reentered hibernation, likely because seasonal gonadal growth and development and subsequent testosterone release prevents a return to torpor. Our findings reveal intriguing differences in responses of males and females to climatic stressors, which can generate a phenological mismatch between the sexes.

Hibernation in a primate: does sleep occur?

During hibernation, critical physiological processes are downregulated and thermogenically induced arousals are presumably needed periodically to fulfil those physiological demands. Among the processes incompatible with a hypome tabolic state is sleep. However, one hibernating primate, the dwarf lemur Cheirogaleus medius, experiences rapid eye movement (REM)-like states during hibernation, whenever passively reaching temperatures above 30°C, as occurs when it hibernates in poorly insulated tree hollows under tropical conditions. Here, we report electroencephalographic (EEG) recordings, temperature data and metabolic rates from two related species (C. crossleyi and C. sibreei), inhabiting high-altitude rainforests and hibernating underground, conditions that mirror, to some extent, those experienced by temperate hibernators. We compared the physiology of hibernation and spontaneous arousals in these animals to C. medius, as well as the much more distantly related non-primate hibernators, such as Arctic, golden-mantled and European ground squirrels. We observed a number of commonalities with non-primate temperate hibernators including: (i) monotonous ultra-low voltage EEG during torpor bouts in these relatively cold-weather hibernators, (ii) the absence of sleep during torpor bouts, (iii) the occurrence of spontaneous arousals out of torpor, during which sleep regularly occurred, (iv) relatively high early EEG non-REM during the arousal, and (v) a gradual transition to the torpid EEG state from non-REM sleep. Unlike C. medius, our study species did not display sleep-like states during torpor bouts, but instead exclusively exhibited them during arousals. During these short euthermic periods, non-REM as well as REM sleep-like stages were observed. Differences observed between these two species and their close relative, C. medius, for which data have been published, presumably reflect differences in hibernaculum temperature.

Proteomics approaches shed new light on hibernation physiology.

The broad phylogenetic distribution and rapid phenotypic transitions of mammalian hibernators imply that hibernation is accomplished by differential expression of common genes. Traditional candidate gene approaches have thus far explained little of the molecular mechanisms underlying hibernation, likely due to (1) incomplete and imprecise sampling of a complex phenotype, and (2) the forming of hypotheses about which genes might be important based on studies of model organisms incapable of such dynamic physiology. Unbiased screening approaches, such as proteomics, offer an alternative means to discover the cellular underpinnings that permit successful hibernation and may reveal previously overlooked, important pathways. Here, we review the findings that have emerged from proteomics studies of hibernation. One striking feature is the stability of the proteome, especially across the extreme physiological shifts of torpor-arousal cycles during hibernation. This has led to subsequent investigations of the role of post-translational protein modifications in altering protein activity without energetically wasteful removal and rebuilding of protein pools. Another unexpected finding is the paucity of universal proteomic adjustments across organ systems in response to the extreme metabolic fluctuations despite the universality of their physiological challenges; rather each organ appears to respond in a unique, tissue-specific manner. Additional research is needed to extend and synthesize these results before it will be possible to address the whole body physiology of hibernation.

The physiology of artificial hibernation

Incomplete understanding of the mechanisms responsible for induction of hibernation prevent translation of natural hibernation to its artificial counterpart. To facilitate this translation, a model was developed that identifies the necessary physiological changes for induction of artificial hibernation. This model encompasses six essential components: metabolism (anabolism and catabolism), body temperature, thermoneutral zone, substrate, ambient temperature, and hibernation-inducing agents. The individual components are interrelated and collectively govern the induction and sustenance of a hypometabolic state. To illustrate the potential validity of this model, various pharmacological agents (hibernation induction trigger, delta-opioid, hydrogen sulfide, 5'-adenosine monophosphate, thyronamine, 2-deoxyglucose, magnesium) are described in terms of their influence on specific components of the model and corollary effects on metabolism. Relevance for patients: The ultimate purpose of this model is to help expand the paradigm regarding the mechanisms of hibernation from a physiological perspective and to assist in translating this natural phenomenon to the clinical setting.

The effects of poly-unsaturated fatty acids on the physiology of hibernation in a South American marsupial, Dromiciops gliroides

Many mammals hibernate, which is a profound lethargic state of several weeks or months during winter, that represents a transitory episode of hetherothermy. As with other cases of dormancy, the main benefit of hibernation seems to be energy saving. However, the depth and duration of torpor can be experimentally modified by the composition of food, especially by fattyacid composition. In eutherians, diets rich in unsaturated fatty acids (i.e., fatty acids with at least one double bond) lengthen torpor, reduce metabolism and permit hibernation at lower temperatures. Here we studied whether diets varying in fatty acid composition have an effect on the physiology of hibernation in a South American marsupial, Dromiciops gliroides. We designed a factorial experiment where thermal acclimation (two levels: natural versus constant temperature) was combined with diet acclimation: saturated (i.e., diets with high concentration of saturated fatty acids) versus unsaturated (i.e., diets with high concentration of unsaturated fatty acids). We measured energy metabolism in active and torpid individuals, as well as torpor duration, and a suite of 12 blood biochemical parameters. After a cafeteria test, we found that D. gliroides did not show any preference for a given diet. Also, we did not find effects of diet on body temperature during torpor, or its duration. However, saturated diets, combined with high temperatures provoked a disproportionate increase in fat utilization, leading to body mass reduction. Those animals were more active, and metabolized more fats than those fed with a high proportion of unsaturated fatty acids (=“unsaturated diets”). These results contrast with previous studies, which showed a significant effect of fatty acid composition of diets on food preferences and torpor patterns in mammals.

Phenology of hibernation and reproduction in ground squirrels: integration of environmental cues with endogenous programming

AbstractMammalian hibernation is characterized by prolonged dormancy consisting of pronounced depression of metabolism and body temperature. Though hibernation occurs in at least seven mammalian orders and several families of the order Rodentia, the ecology and physiology of hibernation in rodents has been most extensively studied in the family Sciuridae, particularly in the so‐called ground squirrels, that is, the tribe Marmotini. Early studies of these rodents demonstrated the important role of an endogenous circannual clock in the persistence of annual timing and phasing of key seasonal events, including weight gain, hibernation and reproduction. Here, we review the causes and consequences of intraspecific variation in the timing of hibernation and reproduction in these sciurids and examine the physiological mechanisms that contribute to phenotypic plasticity in seasonal timing. Although the duration, annual phasing and predictability of seasonal change in environmental conditions likely promoted the evolution of endogeneity, precision and brevity of breeding seasons in the annual cycles of sciurids, substantial intraspecific variation in hibernation and reproductive phenology exists along latitudinal and altitudinal clines, as well as among locally varying environmental micro‐conditions. We suggest that much of this variation is a function of plasticity in the physiological mechanisms controlling annual cycles. While studies of captive animals have been instrumental in establishing the role of an endogenous rhythm, a greater emphasis on experimental field manipulations is needed to better understand the function, causes and consequences of phenological shifts in wild populations. Ultimately, the capacity of hibernators to adjust their timing in response to changing environmental conditions, either through phenotypic plasticity or microevolution, will be an important determinant of the resilience of sciurid species to changing climate.

Multimodality imaging in the assessment of myocardial viability

The prevalence of heart failure due to coronary artery disease continues to increase, and it portends a worse prognosis than non-ischemic cardiomyopathy. Revascularization improves prognosis in these high-risk patients who have evidence of viability; therefore, optimal assessment of myocardial viability remains essential. Multiple imaging modalities exist for differentiating viable myocardium from scar in territories with contractile dysfunction. Given the multiple modalities available, choosing the best modality for a specific patient can be a daunting task. In this review, the physiology of myocardial hibernation and stunning will be reviewed. All the current methods available for assessing viability including echocardiography, cardiac magnetic resonance imaging, nuclear imaging with single photon emission tomography and positron emission tomography imaging and cardiac computed tomography will be reviewed. The effectiveness of the various techniques will be compared, and the limitations of the current literature will be discussed.

First direct evidence of hibernation in an eastern dwarf lemur species (Cheirogaleus crossleyi) from the high-altitude forest of Tsinjoarivo, central-eastern Madagascar

The nocturnal dwarf lemurs of Madagascar (genus Cheirogaleus) are the only primates known to be obligate hibernators. Although the physiology of hibernation has been studied widely in the western, small-bodied species, Cheirogaleus medius, no direct evidence of hibernation, i.e., body temperature recordings, has been reported for any of the three recognized eastern dwarf lemur species. We present skin temperature data collected by external collar transmitters from two eastern dwarf lemur individuals (Cheirogaleus crossleyi) captured in the high-altitude forest of Tsinjoarivo, central-eastern Madagascar. Our study species is larger in body size than western dwarf lemurs and inhabits much colder environments. We present the first evidence of hibernation in an eastern dwarf lemur species, and we compare the results with data available for the western species. Although the hibernation period is shorter in dwarf lemurs from Tsinjoarivo, minimum body temperatures are lower than those reported for C. medius. Both individuals at Tsinjoarivo showed limited passive and extended deep hibernation during which they did not track ambient temperature as observed in most western dwarf lemurs. Because ambient temperatures at Tsinjoarivo never exceed 30°C, dwarf lemurs have to experience arousals to maintain homeostasis during periods of hibernation. We show that large dwarf lemurs (>400 g) are capable of undergoing deep hibernation and suggest that cold, high-altitude forests may render hibernation highly advantageous during periods of food scarcity. This study has implications for understanding the physiology of hibernation in small-bodied lemurs.

Physiology of hibernation under the ice by turtles and frogs

Successful overwintering under ice by an air-breathing vertebrate requires either effective aquatic respiration if dissolved O(2) is available or the capacity for prolonged anaerobic metabolism if O(2) supplies are limiting. Frogs can remain aerobic for many weeks when submerged at low temperature, even at water PO(2) as low as 30 mmHg, but are unable to survive even 1 week in anoxic water. Fuel reserves of hibernating frogs limit aerobic submergence, whereas acidosis may limit anoxic submergence. Freshwater turtles can also satisfy all or most of their O(2) needs in well-aerated water at low temperature by aquatic respiration, but certain species, in particular painted and snapping turtles, can also survive for up to 4-5 months without O(2). Key adaptations of the painted turtles, and presumably snapping turtles, include metabolic depression and the exploitation of the shell and other bones to buffer lactic acid. As in frogs, glycogen and glucose are the only fuel sources during anoxia, and stores do not seem to be limiting in the painted turtle. Significant differences in anoxia tolerance exist among chelonian species that can be attributed, at least in part, to the magnitude of metabolic depression, the effectiveness of lactic acid buffering, and the size of glycogen stores.

The PULSE initiative: scientific priorities and strategic planning for resuscitation research and life saving therapies.

The Post-resuscitative and initial Utility in Life Saving Efforts (PULSE) Conference represented an initiative by leaders of the international scientific community who sought opportunities for major improvements in clinical outcomes after cardiopulmonary resuscitation and after resuscitation from serious traumatic injury.1 The experts focused on scientific research that would yield major advances in lifesaving care, including measurable increases in survival and functional recovery. However, unless research support is prioritized to address resuscitation, it is highly unlikely that these opportunities would soon be realized. We lose more than 1000 lives each day in the United States from sudden, unexpected death, a fatality rate comparable to the crash of two 747 aircraft without survivors.2–5⇓⇓⇓ Cardiovascular disease is the leading cause of death among individuals aged greater than 65 years, the second leading cause of death among individuals aged 45 to 65 years, and the 5th leading cause of death among individuals aged 1 to 9 years.4,5⇓ Traumatic injuries in the United States were responsible for 147 891 deaths and 2.6 million hospitalizations, costing over $335 000 per death and resulting in 37 million emergency department visits in 1995.6,7⇓ Trauma is the leading cause of death among children and all individuals to age 34 years, the leading cause of loss of productive life-years of any disease, with societal costs (estimated by the National Safety Council) of $469 billion dollars annually, and the third leading cause of death among individuals aged 35 to 54 years. The Conferees anticipated that the availability of new intervention strategies with more effective diagnostic methodologies in the early post-injury time interval would not only save lives but also reduce morbidity.1 Accordingly, the PULSE participants cited current restraints and/or barriers to the delivery of more effective resuscitation interventions and reaffirmed that …

Scaling of Nonpolar Lipids with Ovum Size in the Mole Salamander, Ambystoma talpoideum

PACKARD, G. C. 1997. Temperatures during winter in nests with hatchling painted turtles (Chrysemys picta). Herpetologica 53:89-95. PACKARD, G. C., S. A. FASANO, M. B. ATTAWAY, L. D. LOHMILLER, AND T. L. LYNCH. 1997. Thermal environment for overwintering hatchlings of the painted turtle (Chrysemys picta). Can. J. Zool. 75: 401-406. SAS INSTITUTE. 1999. SAS/STAT User's Guide. Rel. 7.0. SAS Institute Inc., Cary, NC. ST. CLAIR, R. C., AND P. T. GREGORY. 1990. Factors affecting the northern range limit of painted turtles (Chrysemys picta): winter acidosis or freezing? Copeia 1990:1083-1089. TROBEC, T. N., AND J. G. STANLEY. 1971. Uptake of ions and water by the painted turtle, Chrysemys picta. Copeia 1971:537-542. TUCKER, J. K., AND G. C. PACKARD. 1998. Overwinter survival by hatchling sliders (Trachemys scripta) in west-central Illinois. J. Herpetol. 32:431-434. ULTSCH, G. R. 1989. Ecology and physiology of hibernation and overwintering among freshwater fishes, turtles, and snakes. Biol. Rev. 64:435-516. WEISROCK, D. W., AND F. J. JANZEN. 1999. Thermal and fitness-related consequences of nest location in painted turtles (Chrysemys picta). Funct. Ecol. 13: 94-101. WILBUR, H. M. 1975. The evolutionary and mathematical demography of the turtle Chrysemys picta. Ecology 56:64-77.

Opioids confer myocardial tolerance to ischemia: Interaction of delta opioid agonists and antagonists

Background: Mammalian hibernation biology is now known to be mediated by delta opioids. The altered myocellular physiology of hibernation closely parallels that of hypothermic ischemia used to protect the heart for cardiac surgery. Methods and Results: The present study examined the interaction of delta opioid agonists and antagonists on myocardial tolerance to ischemia. By means of a nonhibernating isolated rabbit heart model, functional and metabolic myocardial parameters were assessed during nonischemic baseline and postischemic recovery periods. Control hearts with standard cardioplegic protection alone were compared with those with cardioplegia plus preperfusion with a delta opioid agonist, a delta opioid antagonist, or both. All hearts were then subjected to 2 hours of global ischemia. Compared with cardioplegia alone, postischemic left ventricular developed pressure, coronary flows, and myocardial oxygen consumption were all increased with administration of delta opioid agonists and decreased below baseline with delta opioid antagonists. Functional recovery of left ventricular developed pressure was improved with opioids (control hearts: 36 ± 3 mm Hg vs hearts with cardioplegia plus delta opioid agonist: 65 ± 5 mm Hg, P < .01) and inhibited with antagonists (control hearts: 36 ± 3 mm Hg vs hearts with cardioplegia plus delta opioid antagonist: 17 ± 5 mm Hg, P < .05), and true to form, the protective opioid effect was negated when combined with an antagonist (control hearts: 36 ± 3 mm Hg vs hearts with cardioplegia plus delta opioid agonist and delta opioid antagonist: 42 ± 4 mm Hg, P = not significant). Conclusions: This study demonstrates that cardiac tolerance to ischemia may be mediated by delta opioids.

The physiology of hibernation in common map turtles ( Graptemys geographica)

Map turtles from Wisconsin were submerged at 3°C in normoxic and anoxic water to simulate extremes of potential respiratory microenvironments while hibernating under ice. In predive turtles, and in turtles submerged for up to 150 days, plasma P o 2, P co 2, pH, [Cl −], [Na +], [K +], total Mg, total Ca, lactate, glucose, and osmolality were measured; hematocrit and body mass were determined, and plasma [HCO 3 −] was calculated. Turtles in anoxic water developed a severe metabolic acidosis, accumulating lactate from a predive value of 1.7 to 116 mmol/l at 50 days, associated with a fall in pH from 8.010 to 7.128. To buffer lactate increase, total calcium and magnesium rose from 3.5 and 2.0 to 25.7 and 7.6 mmol/l, respectively. Plasma [HCO 3 −] was titrated from 44.7 to 4.3 mmol/l in turtles in anoxic water. Turtles in normoxic water had only minor disturbances of their acid–base status and ionic statuses; there was a marked increase in hematocrit from 31.1 to 51.9%. This study and field studies suggest that map turtles have an obligatory requirement for a hibernaculum that provides well-oxygenated water (e.g. rivers and large lakes rather than small ponds and swamps) and that this requirement is a major factor in determining their microdistribution.

The physiology of hibernation among painted turtles: the midland painted turtle ( Chrysemys picta marginata)

Midland painted turtles from Michigan were submerged at 3°C in normoxic and anoxic water. In predive, and in turtles submerged for up to 150 days, plasma PO 2, PCO 2, pH, [Cl −], [Na +], [K +], total Mg, total Ca, lactate, glucose, and osmolality were measured; hematocrit and mass were determined, and plasma [HCO 3 −] was calculated. Anoxic turtles developed a severe metabolic acidosis, accumulating lactate from a predive value of 4.4 mmol/L to a 150-day value of 185 mmol/L, associated with a fall in pH from 7.983 to 7.189. To buffer lactate increase, total calcium and magnesium rose from 3.7 and 2.6 to 58.9 and 11.8 mmol/L, respectively. Plasma [HCO 3 −] was titrated from 39.2 to 4.8 mmol/L in anoxic turtles. Turtles in normoxic water had only minor disturbances of their acid–base and ionic statuses, associated with a much smaller increase of lactate to 23 mmol/L; there was a marked increase in hematocrit from 29.1% to 42.1%. We suggest that it is ecologic, rather than phylogenetic, relationships that determine the responses of painted turtles to prolonged submergence associated with hibernation.

Increased connexin43 gap junction protein in hamster cardiomyocytes during cold acclimatization and hibernation.

The physiology of hibernation is characterized by dramatic reductions of heart rate, respiration, metabolism, blood pressure and body temperature and by resistance to ventricular fibrillation. Gap junctions in the heart provide low resistance pathways, facilitating electrical and metabolic coupling between cardiac muscle cells for coordinated action of the heart and tissue homeostasis. The conductance of these junctions, and therefore their function, is likely to be affected by the physiological changes that take place during hibernation. Our objective was to quantitate gap junction protein levels in cold acclimatization, hibernation and arousal. We have used specific antibodies to connexins 43 and 40, in combination with confocal microscopy, to quantitatively analyze the expression of connexin protein in hamster (Mesocricetus auratus) left ventricles in four animal groups: normal controls at euthermy, cold controls (cold-exposed animals that did not undergo hibernation), hibernating animals and animals aroused from hibernation for 2 h. Connexin40 immunostaining was not detected in ventricular cardiomyocytes in any animal group but connexin43 was found in all groups. Connexin43 expression was significantly enhanced in hibernation and cold control ventricular cardiomyocytes. Total plaque area, numerical density and plaque size were higher in the cold controls and hibernating hamsters compared to normal controls and animals aroused from hibernation. It is possible that the increased size and number of connexin43 gap junction plaques in the cold controls may represent a compensatory response in order to maintain sufficient gap junction communication during physiological conditions that would reduce conductance. These changes may represent a mechanism by which the hamster avoids ventricular fibrillation during hibernation and arousal.

The physiology of hibernation among painted turtles: the Eastern painted turtle Chrysemys picta picta.

Eastern painted turtles (Chrysemys picta picta) from Connecticut were submerged at 3 degrees C in normoxic and anoxic water to simulate potential respiratory environments within their hibernacula. Those in normoxic water could survive submergence for at least 150 d, while those in anoxic water could survive for a maximum of about 125 d. Turtles in normoxic water developed a slight metabolic acidosis as plasma lactate accumulated to about 50 mM in 150 d, while anoxic turtles developed a severe lactic acidosis as plasma lactate reached about 200 mM in 125 d; there was no respiratory acidosis in either group. Plasma [Na+] changed little in either group, [Cl-] fell by about one-third in both, and [K+] increased by about fourfold in anoxic turtles but only slightly in those in normoxic water. Total plasma magnesium and calcium increased profoundly in anoxic turtles but moderately in those in normoxic water. Consideration of charge balance indicates that all major ions were measured in both groups. Plasma glucose remained unchanged in anoxic turtles until after about 75 d of submergence, when it increased and continued to increase with the duration of anoxia, with much variation among individuals; glucose remained unchanged throughout in turtles in normoxic water. Hematocrit doubled in 150 d in turtles in normoxic water; in anoxic turtles, an initial increase was no longer significant by day 100. Plasma osmolality increased markedly in anoxic turtles, largely because of accumulation of lactate, but anoxic turtles only gained about half the mass of turtles in normoxic water, who showed no increase in osmolality. The higher weight gain in the latter group is attributed to selective perfusion and ventilation of extrapulmonary gas exchange surfaces, resulting in a greater osmotic influx of water. The physiologic responses to simulated hibernation of C. picta picta are intermediate between those of Chrysemys picta bellii and Chrysemys picta dorsalis, which correlates with the severity of the winter each subspecies would be expected to encounter.

ECOLOGY AND PHYSIOLOGY OF HIBERNATION AND OVERWINTERING AMONG FRESHWATER FISHES, TURTLES, AND SNAKES

Summary1. Freshwater fishes are the most northerly of freshwater ectotherms, followed by frogs. North American freshwater snakes, turtles, and salamanders do not range farther north than southernmost Canada.2. Freezing and desiccation are the main challenges during terrestrial hibernation of ectotherms. Oxygen depletion, water balance, and ionic balance are the major problems for air breathing ectotherms that hibernate underwater.3. The importance of accumulation of energy stores for overwintering among fishes depends upon the length and severity of the winters, whether or not there is springtime reproduction, body size, latitude, and the availability and use of food during overwintering.4. Fishes can decrease energy demands during the winter by reductions in activity, metabolic depression, and entrance in semi‐torpidity.5. Adaptations for coping with hypoxia and anoxia among overwintering freshwater fishes may include metabolic depression, a decrease in blood O2affinity, microhabitat selection, air breathing, short‐distance migration, biochemical modifications aimed at adjusting glycolytic rates, and alcoholic fermentation.6. Freshwater turtles have a worldwide northern limit of approximately 50° N, which means that some species spend about half of their lives hibernating.7. Aquatic turtles normally hibernate underwater, although occasionally they hibernate on land. In water they usually hibernate in a hypoxic or anoxic (mud) environment and in relatively shallow water. Wintertime movements of unknown frequency occur in some species.8. The hatchlings of many turtle species can overwinter in the nest. Among northern species this behaviour is most common among painted turtles, whose hatchlings can withstand freezing.9. Mortality among adult turtles is probably highest during the hibernation cycle.10. Temperature appears to the most important cue for entry and exit from hibernation among freshwater turtles.11. Little is known of the energetics of overwintering turtles. Energy stores for overwintering may be more important at lower latitudes than at higher ones, due to the higher metabolic rates of overwintering, but non‐feeding, southern turtles.12. The ability of turtles to tolerate submergence is a function of temperature, degree of water oxygenation, latitude of origin, efficacy of extrapulmonary respiratory pathways, and metabolic rate.13. For turtles that hibernate in an anoxic hibernaculum, and for those without sufficient extrapulmonary uptake of O2to allow metabolism to be completely aerobic, the most important physiological perturbation is an acidosis developed from a continuing production of lactate. If sufficient O2can be obtained, the most likely factors limiting hibernation time are water balance and ion balance.14. Mechanisms of turtles for coping with acidosis include metabolic depression, integumental CO2loss, bicarbonate buffering, and changes in ion concentrations that minimize the decrease in SID (strong ion difference). The most important among the latter are a decrease in plasma [Cl‐] and large increases in plasma calcium and magnesium.15. Turtles are unique among reptiles in their ability to maintain both cardiovascular and nervous system function during prolonged anoxia.16. Turtles gain weight from water uptake during submerged hibernation, but apparently maintain some kidney function; however, osmoregulation is one of the least known areas of the physiology of hibernation.17. Recovery of turtles upon emergence commences with a rapid hyperventilatory compensation of pH, followed by a slower adjustment of ion levels. Basking speeds recovery greatly.18. While hibernation of turtles in the northern parts of their ranges is most likely very stressful physiologically, northern range limits are more likely to be determined by reproductive restraints than by the rigors of extended hibernation.19. The superior ability of turtles to tolerate anoxia may be more the result of an annual hibernation than of their diving habits during active periods of the year.20. Freshwater snakes usually hibernate on land. However, they appear to be capable of aquatic hibernation and may not do so because of the risk of death from anoxia.21. Some species of terrestrial snakes are known to hibernate underwater, and are able to do so in the laboratory for months. In the field, this behaviour is considered opportunistic, as there is no evidence to suggest that any snakes can tolerate extended anoxia.

Cardiovascular and Other Physiological Correlates of Hibernation in Aquatic and Terrestrial Turtles

Recent research has provided new insight into the physiology of hibernation in freshwater, marine, and terrestrial turtles. In this paper I review what is known about the mechanisms that permit the hearts of these turtles to withstand several months of hypoxia or anoxia. I also report new research that indicates that a terrestrial turtle, unlike freshwater and marine species, does not experience hypoxia in its winter burrow and thus does not rely on glycolysis to supply ATP, at least under moderate winter conditions.