Hibernating black bears suppress their metabolic rate to 25% of normal, but only slightly reduce their body temperature.

During hibernation in Arctic ground squirrels ( Spermophilus parryii), O₂consumption and plasma leukocyte counts decrease by >90%, whereas plasma concentrations of the antioxidant ascorbate increase fourfold. During rewarming, O₂consumption increases profoundly and plasma ascorbate and leukocyte counts return to normal. Here we investigated the dynamic interrelationships among these changes. Plasma ascorbate and uric acid (urate) concentrations were determined by HPLC from blood samples collected at ∼15-min intervals via arterial catheter; leukocyte count and hematocrit were also determined. Body temperature, O₂consumption, and electromyographic activity were recorded continuously. Ascorbate, urate, and glutathione contents in body and brain samples were determined during hibernation and after arousal. During rewarming, the maximum rate of plasma ascorbate decrease occurred at the time of peak O₂consumption and peak plasma urate production. The ascorbate decrease did not correlate with mouth or abdominal temperature; uptake into leukocytes could account for only a small percentage. By contrast, liver and spleen ascorbate levels increased significantly after arousal, which could more than account for ascorbate clearance from plasma. Brain ascorbate levels remained constant. These data suggest that elevated concentrations of ascorbate {[Asc]} in plasma {[Asc]_p} provide an antioxidant source that is redistributed to tissues during the metabolic stress that accompanies arousal.

Hibernation is an adaptive strategy to survive in highly seasonal or unpredictable environments. The molecular and genetic basis of hibernation physiology in mammals has only recently been studied using large scale genomic approaches. We analyzed gene expression in the American black bear, Ursus americanus, using a custom 12,800 cDNA probe microarray to detect differences in expression that occur in heart and liver during winter hibernation in comparison to summer active animals.

Although hypoxia tolerance in heterothermic mammals is well established, it is unclear whether the adaptive significance stems from hypoxia or other cellular challenge associated with euthermy, hibernation, or arousal. In the present study, blood gases, hemoglobin O₂ saturation (So₂), and indexes of cellular and physiological stress were measured during hibernation and euthermy and after arousal thermogenesis. Results show that arterial O₂ tension (PaO₂) and So₂ are severely diminished during arousal and that hypoxia-inducible factor (HIF)-1α accumulates in brain. Despite evidence of hypoxia, neither cellular nor oxidative stress, as indicated by inducible nitric oxide synthase (iNOS) levels and oxidative modification of biomolecules, was observed during late arousal from hibernation. Compared with rats, hibernating Arctic ground squirrels ( Spermophilus parryii) are well oxygenated with no evidence of cellular stress, inflammatory response, neuronal pathology, or oxidative modification following the period of high metabolic demand necessary for arousal. In contrast, euthermic Arctic ground squirrels experience mild, chronic hypoxia with low So₂ and accumulation of HIF-1α and iNOS and demonstrate the greatest degree of cellular stress in brain. These results suggest that Arctic ground squirrels experience and tolerate endogenous hypoxia during euthermy and arousal.

Torpor in hibernating mammals defines the nadir in mammalian metabolic demand and body temperature that accommodates seasonal periods of reduced energy availability. The mechanism of metabolic suppression during torpor onset is unknown, although the CNS is a key regulator of torpor. Seasonal hibernators, such as the arctic ground squirrel (AGS), display torpor only during the winter, hibernation season. The seasonal character of hibernation thus provides a clue to its regulation. In the present study, we delivered adenosine receptor agonists and antagonists into the lateral ventricle of AGSs at different times of the year while monitoring the rate of O₂ consumption and core body temperature as indicators of torpor. The A₁ antagonist cyclopentyltheophylline reversed spontaneous entrance into torpor. The adenosine A₁ receptor agonist N⁶-cyclohexyladenosine (CHA) induced torpor in six of six AGSs tested during the mid-hibernation season, two of six AGSs tested early in the hibernation season, and none of the six AGSs tested during the summer, off-season. CHA-induced torpor within the hibernation season was specific to A₁AR activation; the A₃AR agonist 2-Cl-IB MECA failed to induce torpor, and the A_2aR antagonist MSX-3 failed to reverse spontaneous onset of torpor. CHA-induced torpor was similar to spontaneous entrance into torpor. These results show that metabolic suppression during torpor onset is regulated within the CNS via A₁AR activation and requires a seasonal switch in the sensitivity of purinergic signaling.

Ecologists need an empirical understanding of physiological and behavioural adjustments that animals can make in response to seasonal and long-term variations in environmental conditions. Because many species experience trade-offs between timing and duration of one seasonal event versus another and because interacting species may also shift phenologies at different rates, it is possible that, in aggregate, phenological shifts could result in mismatches that disrupt ecological communities. We investigated the timing of seasonal events over 14 years in two Arctic ground squirrel populations living 20 km apart in Northern Alaska. At Atigun River, snow melt occurred 27 days earlier and snow cover began 17 days later than at Toolik Lake. This spatial differential was reflected in significant variation in the timing of most seasonal events in ground squirrels living at the two sites. Although reproductive males ended seasonal torpor on the same date at both sites, Atigun males emerged from hibernation 9 days earlier and entered hibernation 5 days later than Toolik males. Atigun females emerged and bred 13 days earlier and entered hibernation 9 days earlier than those at Toolik. We propose that this variation in phenology over a small spatial scale is likely generated by plasticity of physiological mechanisms that may also provide individuals the ability to respond to variation in environmental conditions over time.