Chapter 12.1

Mammalian Hibernation

Sleep and Torpor

There has been much discussion on the purpose and evolution of sleep in mammals (see Carl Sagan's book, The Dragons of Eden, for an entertaining and speculative adventure) but from the perspective of low temperature biology, we can simply consider it to be a form of energy conservation by lowering metabolism during periods when a high metabolic activity would not be helpful (e.g. during the night for animals that gather food during daylight). Most mammals lower their body temperature by 1 to 2°C during sleep, resulting in a lowering of energy metabolism by about 7-15%. Although most mammals have a diurnal cycle of waking and sleeping, those animals that live in cold climates have adapted more elaborate sleep patterns to survive the cold, when normal energy expenditures are high and food gathering becomes more difficult.

Torpor in mammals is characterized by a regulated reduction in body temperature, usually below 30°C, that requires a much longer period before normal activity can be resumed, when compared with sleep. A reduction in body temperature necessarily results in a reduction in metabolic activity, due to the temperature dependence of the rates of chemical reactions. Normal mammalian metabolism is usually considered to have a Q₁₀ of 2, although representing the metabolism of a complex organism by a simple Q₁₀ value is clearly an oversimplification.

(12.1.1)
Where R₁ and R₂ are the rates of some phenomenon at two temperatures T₁ and T₂.
This is related to an Arrhenius activation energy by the following relation:

(12.1.2)

Animals that maintain very high metabolic rates, such as hummingbirds and small rodents or marsupials, often go into daily torpor. Their body temperature drops dramatically during "sleep", so that a period of one to three hours is required to regain normal activity. These animals are referred to as heterotherms.

The large carnivores that live in subarctic and arctic regions enter a dormant state during the winter months that is commonly referred to as "hibernation". The physiologists do not use that term, as the winter dormancy of bears and their like does not resemble that of the true hibernators.

Bears overeat during the summer and autumn, accumulating body fat, until their food supply becomes scarce and hard to find. In late fall, they make an underground den and enter it for overwintering. Much of the time is spent sleeping, with a body temperature that ranges from 31°C to 35°C. Experimenters quickly realized that bears are not classic hibernators when they attempted to put thermometers inside them; bears remain alert enough to occasionally attack any invaders. The bears lose approximately 25% of their body weight during the winter sleep, but remain in good physical condition. The females are able to suckle their young without further nourishment. Bears do not normally urinate or defecate during their winter sleep, water and nitrogen being re-absorbed in the bladder. They are perfectly capable of surviving the cold winters without entering a den and are, in fact, often found taking brief sabbaticals from their den during the winter. It appears that their lethargy is simply triggered because of the lack of food.

Hibernation

Classic hibernation is defined by a deep torpor that is induced by low temperatures. It occurs in small mammals living in temperate, subarctic, or arctic regions, although it is not universal among these animals living in cold regions. Indeed, hibernation is relatively uncommon in the arctic, where the winter is so long that survival through hibernation becomes more risky than survival in the subsnow microhabitat where these rodents live. It is also not the case that all animals that are capable of hibernation enter a torpid state to overwinter. Hibernation is brought on by severe conditions; it is not triggered by photoperiod or other seasonal clues.

Hibernation is characterized by a body temperature that is within a few degrees of the ambient temperature (usually 4°C to 7°C) that is held for periods of one to several weeks at a time; the total period of hibernation occupying several months during which torpid states are interspersed with short periods of arousal and activity. The length of the torpid states increases during the depth of winter and then shortens again toward spring. There are some data that support the idea that metabolism is depressed beyond the simple lowering of body temperature, but the difficulty in extrapolating based on a naive idea such as the Q₁₀ for a whole organism makes this proposition difficult to support.

Most hibernators prepare for winter by eating excessively during the summer and autumn, laying down the excess energy in normal adipose tissue (white fat) and brown adipose tissue (brown fat). Most mammals lose their stores of brown fat as they mature to adults, although hibernators maintain the tissue lifelong. Brown fat is brown because of the high density of mitochondria (and the brown cytochromes of the respiratory chain) and the high level of vascularization. Respiration within brown adipose tissue is primarily directed toward heat generation, rather than the production of ATP, so there is little synthesis of ATP in the tissue. Heat production within brown adipose tissue (non-shivering thermogenesis) is triggered by the sympathetic nervous system.

Onset of Torpor
Prior to hibernation, most animals burrow or enter a sealed den that maintains a temperature above freezing through geothermal heating. It appears that a hormone, possibly controlled by photoperiod and other environmental cues, initiates the onset of torpor. At the beginning of hibernation, the animal reduces the activity of its sympathetic nervous system so that the normal responses to falling temperature such as shivering and non-shivering thermogenesis, and peripheral vasoconstriction are not employed to counteract the falling temperature. The temperature set-point of the hypothalamus is reduced to a few degrees above the temperature of the environment and cooling takes place over one to several days.
Physiology During Torpor
Torpor is characterized by low body temperature, low metabolic rate, and the absence of food and water intake. In non-hibernating animals, low body temperature leads to ventricular fibrillation and death, however this is not the case for hibernators. The low metabolic rate lowers the need for food intake, such that the reserves of fat that were laid down prior to the onset of hibernation are sufficient to carry the animal through the winter. The metabolism of fat also produces water that is conserved by the animal through slow breathing and the high humidity of the hibernation chamber. The total energy expenditure during torpor can be anywhere from 60% to 98% less than normal, depending on the core temperature and the size of the animal (smaller animals generally save more energy).
Sympathetic neural control is resumed during torpor to close down the peripheral vasculature. This allows the aortic blood pressure to remain at normal levels, despite the heart rate falling by almost two orders of magnitude. This allows effective perfusion of the coronary arteries so that ventricular fibrillation does not occur. The myocardium of hibernators also has a concentration of lipid droplets that allow energy production within the heart. These droplets are not present in non-hibernators. An increase in blood CO₂ decreases the pH, leading to a further decrease in metabolism (beyond that produced by a drop in temperature) although the pH is maintained within the heart and liver to support proper function.
Arousal from Torpor
Torpor is not maintained throughout the period of hibernation. The animal must wake up periodically, although the reasons for this remain largely unknown. It is likely that repair and maintenance of organs, tissues, and cells must be carried out periodically. In fact, it has been found that intensive protein synthesis occurs during periods of arousal, thus it seems likely that these periods are necessary for routine maintenance, since chemical degradation of macromolecules will accumulate over time (albeit at a slower rate with lower temperature).
The initiation of arousal is likely due to an endocrine function that measures time in torpor. The first physiological response is hyperventilation, increasing oxygen in the blood, but more importantly, reducing the CO₂ concentration in the blood. The body temperature begins to rise exponentially from non-shivering thermogenesis and shivering begins at body temperatures above 20°C, increasing the rate of warming until the animal reaches normothermy. The period of torpor is usually on the order of one to several weeks, while the period of activity between bouts of torpor is on the order of hours. As spring approaches, the period of torpor decreases and the period of activity increases until one such arousal defines the end of hibernation.

Supercooling

The arctic ground squirrel, Spermophilus parryii, is the only known endothermic organism to use supercooling of body fluids as a means to survive in a freezing environment. A colony of ground squirrels in Alaska that was monitored by telemetry reached body temperatures as low as -2.9°C (average -2°C) during natural hibernation. It appears that heat production was initiated after the temperature dropped below -1.5°C and the body temperature was maintained several degrees above the soil temperature (and was kept within a range of 1°C) during torpor. The brain and thoracic and abdominal cavities was maintained above the freezing point although peripheral temperatures and the colonic temperatures were below freezing. Blood flow was maintained to all parts of the body at subzero temperatures as evidenced by prompt bleeding when cut, even at the periphery. The blood and body fluids of the squirrel showed no thermal hysteresis, with the freezing points and melting points coinciding at -0.56°C.

These squirrels exist in a supercooled state during hibernation; a tenuous strategy since the slightest vibration or contamination (especially in the gut) with an ice nucleator would mean death. Other hibernating rodents, when artificially supercooled, can be revived with artificial warming, although spontaneous nucleation always occurs within about an hour, leading to death. The arctic ground squirrel maintained the supercooled state for periods of six weeks at a time, with no mortality noted in the experimental group (nor any indication that this is a common mode of death in nature). Extrapolating current estimates of the metabolic cost of hibernation at 0°C, it would appear that a further lowering of body temperature to -3°C would produce a further energy savings of about 10 times. Due to the necessity of a long hibernation period and a short growth period, this metabolic saving may provide a much greater chance for species survival than the cost of accidental death from ice nucleation.

Mammalian Hibernation

Sleep and Torpor

Hibernation

Onset of Torpor

Physiology During Torpor

Arousal from Torpor

Supercooling