Hibernating Bears Run Hotter and Cleaner While Pregnant
When it comes to feats of physiology, bears are among the superstars of the mammalian world. Their endurance is legendary. During hibernation, bears regularly survive up to six full months without consuming any food at all. Hibernating bears reduce their heart rates by over 80% and decrease their metabolic rates by 50-75%, yet they actually remain conscious during this time (Laske et al. 2010; Tøien et al. 2011). Bears also manage to avoid muscle atrophy and loss of bone density, despite remaining immobile for nearly half the year. If being a couch potato were a sport, bears would dominate the hall of fame
Smaller mammals go through hibernation periods as well, albeit through slightly different methods. They typically have to drop their body temperatures drastically, but must periodically rouse themselves to rev up their metabolic engines. In contrast, bears are able to hold steady the entire time, at least within their normal body temperature cycles of 30-36° C.
Perhaps the most amazing fact about bear hibernation is that female bears gestate, give birth, and nurse their cubs all within this hibernation period. If you have ever been pregnant, or have even been around a pregnant person, imagine that entire process happening while a mother is consuming absolutely no food. Mother bears are tough, despite being professional loungers.
What metabolic adjustments are needed for a female to both preserve her own body and essentially manufacture several other bears while she is in a state of hibernation? Recently, a team of researchers from Hokkaido University addressed this question by investigating the physiology of pregnant and nonpregnant hibernating Japanese black bears (Ursus thibetanus japonicus) during hibernation. They used a series of hypothesis about metabolic processes to investigate how the reproductive status of female bears affected body temperature and blood chemistry throughout their winter hibernation period. They reported their results in a recent issue of the Journal of Mammalogy (Shimozuru et al. 2013).
In addition to comparing pregnant and nonpregnant female bears, Shimozuru and colleagues included a third category: pseudopregnant bears. Pseudopregnant females have similar progesterone levels to truly pregnant ones, yet never actually develop a placenta. This allows researchers to tease apart the effects of corpus luteum-derived pregnancy hormones (controlled by factors from the pituitary gland and ovaries) from metabolic interactions with a real placenta. Because the progesterone levels are so similar between pregnant and pseudopregnant bears, Shimozuru's team had to identify actual pregnancies using ultrasonography.
The researchers had a few predictions about what they would find. First, they predicted that pregnant bears would maintain higher and more stable body temperatures than nonpregnant ones, in order to support fetal growth. This phenomenon is common amongst mammals, but has not been systematically tested for many species. Maintaining a higher body temperature requires extra energy, so mammals that fast during pregnancy are also expected to lose body mass more quickly when pregnant.
Next, it is known that hibernating bears primarily utilize stored body fat for energy. Pregnant bears, however, must rely on glucose to support fetal development, due to limitations on the transmission of lipid byproducts (triglycerides, fatty acids, ketone bodies, and glycerol) through the placenta. In other words, fetal bears are no Atkins dieters . . . but once they’re outside the womb, it’s a different story. Bear milk is very high in fat and very low in sugar (Iibuchi et al. 2009), which allows mother bears to tamp back down on their glucose turnover. Thus, the researchers predicted that pregnant bears should have higher blood glucose levels than nonpregnant ones, but that blood glucose during lactation should be similar between the two groups.
Finally, the researchers compared levels of creatinine and urea in the blood of pregnant, pseudopregnant, and nonpregnant bears. These substances are waste produces of protein catabolism, and measuring them allowed researchers obtain a more detailed picture of the bears' metabolic processes during hibernation. They also examined triglyceride levels and concentrations of free fatty acids, ketone bodies, and glycerol (all three of which are produced by breaking down triglycerides).
Pregnant bears do indeed run hotter (37-38° C) than nonpregnant individuals (34-36° C). Their body temperatures begin to drop soon after parturition, and body temperatures of lactating and non-lactating bears are about the same. Hypothesis upheld.
Surprisingly, the pregnant bears in this study did not lose significantly more body mass than the nonpregnant bears. This may have been an artifact of a low sample size, (the study included 6 pregnant bears, 6 pseudopregnant, and 5 nonpregnant), as previous studies have shown that pregnancy leads to more weight loss during hibernation for bears. For example, Harlow et al. (2002) reports that pregnant bears lost 37% more fat every day than their nonpregnant counterparts. Shimozuru and colleagues suggest that pregnant and pseudopregnant bears could have consumed more water during hibernation, possibly masking decreases in body mass when their weight was measured . . . but the literature on bear hibernation suggests that they don't actually drink water while they're hibernating (Nelson 1980). Further research into the causes of fat loss during hibernation will help to clarify the issue.
What about pseudopregnant bears, whose bodies “think” they’re pregnant yet never actually undergo parturition? Interestingly, their body temperatures are on par with pregnant bears in early "pregnancy," and begin decline rapidly around the time they would be scheduled to give birth if they had truly been pregnant. These results indicate that changes in pituitary or ovarian-derived endocrine levels during pregnancy (or pseudopregnancy) are likely behind elevated body temperatures, since pseudopregnant bears have similar endocrine profiles to pregnant bears but no placenta or fetuses to support.
The blood chemistry results yielded insights into a key endocrinological difference between pregnant and pseudopregnant bears, however. Pregnant bears had higher blood glucose levels than their pseudopregnant counterparts, indicating that cytokines and other chemical messengers related to the placenta may be the key regulators of blood glucose during pregnancy, rather than just hormones derived from the pituitary and ovaries, such as progesterone. This result was consistent with earlier studies, which have shown that placental extracts can stimulate gluconeogenesis when injected into lab animals, but it is interesting and informative to see the effects of this on hibernation physiology in wild animals.
By January—just before the pregnant bears gave birth--a stratification emerged: pregnant bears had higher blood glucose levels that pseudopregnant ones, and nonpregnant bears had the lowest glucose levels of all. This supports the hypothesis that glucose is necessary to support fetal development, since lipids are difficult to transmit through the placenta. The results also further bolster the idea that the signals from the placenta help--although may not entirely control--regulation of glucose metabolism.
By January, pregnant and pseudopregnant bears also had lower plasma urea, creatinine, and triglyceride concentrations than nonpregnant bears, although concentrations of free fatty acids, glycerol, and ketones did not differ between groups. Both urea and triglycerides in the blood are essentially waste byproducts created by catabolism of lipids and muscle. These fascinating results tell us that pregnant bears are better than other bears at avoiding accumulation of nitrogenous wastes in their blood during fasting.
Previous work has shown that bears are better than most other hibernating mammals at recycling urea and other nitrogenous wastes to prevent muscle deterioration (Harlow et al. 2002), which is probably why they are able to avoid catastrophic muscle loss despite being sedentary for half of the year. The new study by Shimozuru and colleagues adds a fascinating new twist to the story: it seems that pregnancy enhances that adaptation even further, allowing bears to become even more efficient at recycling metabolic waste to preserve protein and prevent accumulation of metabolic "trash." Pregnant bears are building and supporting baby bears from their own tissues during hibernation, and the authors suggest that the need to synthesize extra amino acids and proteins drives the hyperefficient use of metabolic waste observed in pregnant animals.
This study may provide a springboard for further research into the roles played by placental versus ovarian endocrines in stimulating these metabolic adjustments, which will increase our understanding of hibernation physiology as well as teach us new lessons about mammalian reproductive physiology in general. For example, identifying the placental factors controlling blood glucose could contribute to our understanding of gestational diabetes in both humans and non-human mammals. In addition, figuring out how to induce more efficient recycling of metabolic waste is a crucial hurdle for endeavors such as preventing muscle atrophy in astronauts or in earthbound patients that are immobilized by injury or disease. Human lifestyles are shifting inexorably towards being more and more sedentary, so any insights into metabolic mechanisms to preserve health without much movement will also be valuable. It will be a fascinating line of research to follow!
Harlow, H. J., T. Lohuis, G. Grogan, and T. D. I. Beck. 2002. Body mass and lipid changes by hibernating reproductive and nonreproductive black bears (Ursus americanus). Journal of Mammalogy 83: 1020-1025.
Iibuchi, R. et al. 2009. Change in body weight of mothers and neonates and in milk composition during denning period in captive Japanese black bears (Ursus thibetanus japonicas). Japanese Journal of Veterinary Research. 60: 5-13.
Laske, T. G., H. J. Harlow, D. L. Garshelis, and P. A. Iaizzo. 2010. Extreme respiratory sinus arrhythmia enables overwintering black bear survival—physiological insights and applications to human medicine. Journal of Cardiovascular Translational Research 3:559-569.
Shimozuru, M., R. Iibuchi, T. Yoshimoto, A. Nagashima, J. Tanaka, & T. Tsubota (2013). Pregnancy during hibernation in Japanese black bears: effects on body temperature and blood biochemical profiles Journal of Mammalogy, 94 (3), 618-627 : http://10.1644/12-MAMM-A-246.1
Nelson, R. A. 1980. Protein and fat metabolism in hibernating bears. Fed. Proc. 39(12):2955-8.
Tøien, Ø., J. Blake, D. M. Edgar, D. A. Grahn, H. C. Heller, and B. M. Barnes. 2011. Hibernation in black bears: independence of metabolic suppression from body temperature. Science 331: 906-909. Despite the fact that pregnant bears rely on glucose to nourish their fetuses, glucose levels showed no significant shifts during gestation.