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Hibernation in Black Bears: Independence of Metabolic Suppression from Body Temperature

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Science  18 Feb 2011:
Vol. 331, Issue 6019, pp. 906-909
DOI: 10.1126/science.1199435

Abstract

Black bears hibernate for 5 to 7 months a year and, during this time, do not eat, drink, urinate, or defecate. We measured metabolic rate and body temperature in hibernating black bears and found that they suppress metabolism to 25% of basal rates while regulating body temperature from 30° to 36°C, in multiday cycles. Heart rates were reduced from 55 to as few as 9 beats per minute, with profound sinus arrhythmia. After returning to normal body temperature and emerging from dens, bears maintained a reduced metabolic rate for up to 3 weeks. The pronounced reduction and delayed recovery of metabolic rate in hibernating bears suggest that the majority of metabolic suppression during hibernation is independent of lowered body temperature.

Mammalian hibernation is well characterized in species such as marmots, ground squirrels, bats, and dasyurid marsupials (1). These small (<5 kg) hibernators undergo regulated decreases in core body temperature (Tb) to near or below freezing during torpor bouts that last days to weeks (25). Torpor is periodically interrupted by arousals to normothermia (35° to 38°C) that usually last for less than one day (6, 7). During torpor, metabolic rates of small hibernators decrease to 2 to 5% of basal metabolic rate (BMR) (810). However, the relative contributions of temperature-dependent (described by Q10, rate coefficient for a 10°C change in Tb) and temperature-independent mechanisms of metabolic suppression depend on the size of animals and stage of entry into torpor (11). In contrast, the relationships between Tb and metabolism in the large hibernators of the bear family Ursidae have remained unknown because technical limitations have prevented continuous, long-term monitoring in these 30 to 200 kg or larger animals. We used telemetry and respirometry to record Tb, metabolic rates, and heartbeat patterns of black bears, Ursus americanus, through their hibernation and post-hibernation recovery.

Black bears were nuisance animals captured in south-central or interior Alaska in late autumn 3 different years and transported to facilities at the Institute of Arctic Biology, University of Alaska Fairbanks. Radio transmitters for Tb and electromyogram (EMG)/electrocardiogram (ECG) were surgically implanted (12), and animals were transferred to outdoor enclosures in an isolated wooded area. Bears hibernated inside 0.8 m3 wooden nest boxes with straw for bedding and equipped with infrared cameras, activity detectors, and telemetry-receiving antennas. Food and water were not provided. Air was continuously collected from the closed hibernacula to record O2 consumption (a measure of metabolic rate). After the spontaneous emergence of bears from their dens in spring, Tb recordings were continued, and minimum metabolism after 24 hours of fasting was determined every four nights for 1 month.

Hibernating black bears kept a curled posture (Fig. 1), similar to that previously described (13), that facilitates heat preservation and water economy. Animals changed position twice a day to once every 2 days, when they stood, occasionally groomed, and rearranged bedding material. Tb, which is normally 37° to 38°C, decreased to average levels of 33.0°C (31.7° to 34.0°C, n = 4 bears) in mid hibernation (defined as 21 January to 20 February). Minimum Tb was 30.4°C (29.4° to 32.5°C, n = 4 bears). Before emergence in mid-April, Tb gradually increased over 2 to 4 weeks to 36° to 37°C (Fig. 2). Hibernating bears did not show spontaneous, periodical arousals to normothermic levels of Tb, as do small hibernators. This may be because bear Tb did not decrease below 30°C, a level that may reflect a threshold below which neural deficits, such as loss of neuronal structure (14), begin to occur that require regular returns to high Tb. Hibernating fat-tailed dwarf lemurs that are regularly warmed by the sun to above 30°C also do not show spontaneous arousals (15). Diurnal rhythms in Tb also were not evident in mid-winter; instead, there were unexpected 1.6- to 7.3-day cycles of Tb with 2° to 6°C amplitude. Cycles were shortest during coldest conditions and most regular in the smallest bear (Fig. 2B, top). Tb was higher and more stable in free-ranging black bears studied in Wyoming and Colorado, which could be due to milder ambient temperatures (16). In spring when conditions were warmer in our study, multi-day Tb cycles were also less evident (Fig. 2). High-amplitude multi-day cycles of Tb may be a feature of thermoregulation, when gradients between Tb and environmental temperatures are large. Early studies on hibernating black bears in Alaska or arctic Canada reported Tb of 32° to 35°C (17, 18) and could not reveal any multi-day patterns because of intermittent measurements.

Fig. 1

Black bear hibernating in its artificial den.

Fig. 2

Body temperature patterns of hibernating black bears. Core body temperature (Tb, black), temperature outside dens (Ta, blue), and movements (purple) recorded over 3 different years. (A) One bear. (B) Two bears. (C) Two bears. Female BB99-02F was pregnant and gave birth, indicated by the plus symbol. Implantation of Tb transmitters in (C) occurred before the EMG/ECG transmitter surgery, marked by an asterisk. Surgery (both transmitters) for the other bears took place simultaneously and before recording. Missing Tb data for BB92-01M were due to instrumentation problems.

The Tb of a female bear remained at normothermic levels through the end of January (Fig. 2C, bottom), when she gave birth to a 243-g cub that died because of a congenital diaphragmatic hernia (12). Afterwards, her Tb became more variable and decreased toward levels of other hibernating bears. High and stable Tb patterns occurred during pregnancy in a European brown bear (19). Bears have delayed implantation, and pregnancy starts in late November after denning (20). We suggest that low and fluctuating Tb may not be favorable for embryonic development, and thus, hibernating bears maintain normothermia while pregnant.

O2 consumption in hibernating bears varied from minimum levels of 0.06 ml g−1 h−1 sustained for as much as one day to brief peaks of >0.35 ml g−1 h−1 accompanied by movement (Fig. 3A). Tb declined shivering when metabolism and were minimal and increased during intense shivering and heightened metabolism. This varying pattern of endothermic thermoregulation can explain the wide range in metabolic rates found in the only previous metabolic study of hibernating bears (18). Predicted BMR for carnivores (21, 22) averages 0.228 ml g−1 h−1. Here, we show BMR (defined as overnight resting and fasting metabolic rate measured 1 month after emergence from hibernation) was 0.276 ml g−1 h−1 (range from 0.267 to 0.285 ml g−1 h−1, n = 3 bears); the mean Tb was 37.8°C. A comparison of the changes in metabolism and corresponding Tb in three nonpregnant bears (Fig. 3B) revealed that during mid-hibernation, when Tb was 32.2°C (30.9° to 33.6°C), minimum metabolic rate (12) was 0.069 (0.056 to 0.086) ml g−1 h−1, or 24.9% of BMR. A reduction to only 0.179 ml g−1 h−1 (64.9% of BMR) would be expected because of direct effects of the 5.5°C decrease in Tb, when a Q10 of 2.2 is assumed (1). When bears emerged from dens in mid-April with Tb of 36.6°C (36.1° to 37.4°C), metabolic rate averaged 0.149 (0.127 to 0.170) ml g−1 h−1 or 52.9% of BMR and stabilized at BMR levels after 2 to 3 weeks (Fig. 3B). Bears began feeding over this period, and their return to BMR may in part involve resumption of a full capacity of the digestive system. In alpine marmots, hibernation is accompanied by a 70% decrease in mass of stomach and intestines, which was reversed in spring (23). Hypothyroidism of hypothalamic origin reported in hibernating black bears (24) may also contribute to metabolic suppression.

Fig. 3

Body temperature and metabolic rate of hibernating black bears. (A) O2 consumption, EMG activity, Tb, movements, and temperature outside and inside the den of BB97-02F during a 5-day period in January. (B) Minimum O2 consumption and corresponding Tb of three bears during hibernation and during recovery from hibernation. The vertical dashed line indicates the average time of emergence, which varied by ±2 days.

Decreased metabolism in hibernating bears reduces the need for transport of blood gases and nutrients. Heart rate (HR) of three non-pregnant bears in mid-hibernation decreased from summer resting levels (Fig. 4A) of 55 (44.5 to 63.7) beats per min to 14.4 (8.9 to 20.1) beats per min, which is similar to minima of 8 to 12 beats per min in a captive hibernating black bear reported by Folk (25). Hibernating bears showed a marked variation in inter-beat intervals through the breathing cycle, encompassing a profound sinus arrhythmia (Fig. 4, B and C). Typically, a group of rapid heartbeats occurred as inspiration ended followed by interbeat intervals of 8 to 20 s after expiration. Bursts of shivering were synchronous with rapid heartbeats and breathing (Fig. 4C). At emergence, sinus arrhythmia was less pronounced, and average resting HR was 23.7 (16.1 to 31.1) beats per min. HR during hibernation was reduced to 26.2% and at emergence was 43.0% of summer levels. Similar reductions in HR during hibernation with a transition at emergence have been observed in grizzly bears (26).

Fig. 4

ECG and breathing patterns in summer and hibernating bears. (A) Representative ECG for a bear in summer. (B and C) ECG, breathing (chamber pressure), and EMG amplitude of two hibernating bears, (B) BB99-01M and (C) BB97-02F, showing increased heart rate at inspiration. The open bar marks inspiration, and the filled blue bar marks expiration. The peaks in average EMG amplitude in (C) are shivering bursts, which occurred at the end of inspiration.

Black bears share attributes of hibernation with small hibernators, including a decrease in metabolic rate, lack of diurnal Tb patterns, reduced HR, and surviving without feeding or drinking for approximately half a year. However, Tb in hibernating bears is far higher than in small hibernators, which is in part due to the estimated lower levels of thermal conductance in bears (approximately 20%) as compared with ground squirrels [supporting online material (SOM) text and table S1] (10). Whereas smaller hibernators show long torpor bouts interrupted by regular arousal episodes, black bears in Alaska exhibit distinct cyclic non-diurnal Tb patterns. Bear metabolism is reduced by 53% from BMR, even when Tb has returned to normothermic levels. These observations expand the phenotype of mammalian hibernation that occurs in diverse animals over body mass ranges from 0.005 to 200 kg. Insights into how hibernating bears achieve and cope with these reductions in energy need and Tb, as well as conservation of muscle (27, 28) and bone mass (29) despite prolonged seasonal inactivity and disuse, could lead to the development of novel clinical therapies. Current molecular and genetic approaches (28, 30) in combination with better physiological knowledge can increase our understanding of the regulation of hibernation in small and large hibernators and their evolution.

Supporting Online Material

www.sciencemag.org/cgi/content/full/331/6019/906/DC1

Materials and Methods

SOM Text

Table S1

References

References and Notes

  1. Materials and methods are available as supporting material on Science Online.
  2. This work was supported by U.S. Army Medical Research and Materiel Command grant 05178001; NSF grants 9819540, 0076039, and 0732755; NIH HD-00973; and gift funds to Stanford University, American Heart Association #0020626Z, and the Fulbright Program. We thank the Alaska Department of Fish and Game for providing bears, D. Ritter for technical assistance, and J. Kenagy and J. Duman for comments.
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