Thermoregulation and energetics in hibernating black bears: metabolic rate and the mystery of multi-day body temperature cycles

Abstract

Black bears overwintering in outdoor hibernacula in Alaska decrease metabolism to as low as 25 % basal rates, while core body temperature (T(b)) decreases from 37 to 38 °C to a mid-hibernation average of 33 °C. T b develops cycles of 1.6-7.3 days length within a 30-36 °C range, with no circadian component. We do not know the mechanism or function underlying behind the T(b) cycles, although bears avoid T(b) of <30 °C and shorter cycles are predicted from higher rates of heat loss in colder conditions. To test this we manipulated den temperatures (T(den)) of 12 hibernating bears with body mass (BM) from 35.5 to 116.5 kg while recording T(b), metabolic rate (M), and shivering. T b cycle length (0.8-11.2 days) shortened as T den decreased (partial R(2) = 0.490, p < 0.001). Large bears with low thermal conductance (TC) showed more variation in T b cycle length with changes in T(den) than did smaller bears with high TC. Minimum T b across cycles was not consistent. At low T(den) bears shivered both during rising and decreasing phases of T(b) cycles, with minimum shivering during the fastest drop in T(b). At higher T den the T b pattern was more irregular. Mean M through T(b) cycles was negatively correlated to T den below lower critical temperatures (1.4-10.4 °C). Minimum M (0.3509 W/kg ± 0.0121 SE) during mid-hibernation scaled to BM [M (W) = 1.217 × BM (kg)(0.6979), R(2) = 0.855, p < 0.001]. Hibernating thermal conductance (TC) was negatively correlated to BM (R(2) = 0.721, p < 0.001); bears with high TC had the same T(b) cycle length as bears with low TC except at high T(den), thus not supporting the hypothesis that cooling rate alone determines T(b) cycle length. We conclude that T(b) cycling is effected by control of thermoregulatory heat production, and T(b) cycling may not be present when hibernating bears use passive thermoregulation. More intense shivering in the rising phase of cycles may contribute to the prevention of muscle disuse atrophy. Bears hibernating in cold conditions use more energy during hibernation than in warmer conditions. At T den below lower critical temperature, no extra energy expenditure results from T b cycling compared to keeping a stable T(b.)

Daily and annual cycles in thermoregulatory behaviour and cardio-respiratory physiology of black and white tegu lizards

“…Some of the hallmark traits of endothermic hibernation are a depression of body temperature (T b ) and a reduction of basal metabolic rate, accompanied by falls in ventilation and heart rate (Lyman 1982;Willis 1982;Carey et al 2003;Tøien et al 2015). While the magnitude and mechanism of metabolism and T b depression in hibernating endotherms have been well studied (Lyman 1982;Nedergaard et al 1990;Storey and Storey 1990;Carey et al 2003), the same aspects of dormancy have not been extensively studied in ectothermic hibernators.…”

Room without a view – den construction in relation to body size in brown bears

“…The large interannual variance of post-hibernation BCI shown by the most parsimonious model suggests potential impacts of interannual variations in biotic and abiotic factors on post-hibernation body condition of bears. For example, severe winter temperatures [1, 17], berry production [33, 43, 44], and snow deposition [23, 24, 45, 46] are expected to affect pre-hibernation body condition and energy loss during hibernation [9, 15, 37], thereby affecting post-hibernation body condition. Sex may affect the energy loss during hibernation, likely because females spend significantly more time in dens than males [22], and energy cost and weight loss increase with longer duration of hibernation [15].…”

“…In addition, energetic costs and weight loss in bears generally increase with the duration of hibernation [15], and the duration of denning varies depending on sex and reproductive status [7, 22, 42]. Heat loss during hibernation can be exacerbated by severe winter temperatures [17], even if the animal is hibernating in an enclosed cavity [1]. In addition, the loss of energy and body mass of bears during hibernation is highly affected by pre-hibernation body condition [9, 15, 37].…”

“…In addition, bears give birth during hibernation and the cubs are fed on milk produced from the stored fat and lean body mass [12, 14, 15]. To cope with this exclusive dependence on stored fat and protein reserves for survival and reproduction during hibernation, in addition to the slow cooling rate of the body due to their relatively small surface area to volume ratio [4], bears use metabolic inhibition independently of body temperature [13, 16, 17]. American black bears suppress their metabolism to 25% of the summer basal metabolic rate, but body temperature only decreases from 37-38 C to an average of 33 C in mid-hibernation [13].…”

“…This mechanism enables bears to reduce the thermal gradient between the body and the environment, thereby minimizing energy loss [18]. Hibernating bears shiver to produce extra heat in cold ambient and den temperatures, thereby inducing cycles of body temperatures [17]. Therefore, the use of well-insulated dens should help bears minimize energy loss during hibernation and bears should select dens optimally in relation to energy conservation [19].…”