Entering hibernation is not a passive process in response to falling T a. Nor is deep hibernation a passive process or indeed a uniform state. Figure 13 shows the pattern of hibernation (as measured by the heart rate) of an arctic marmot (Marmota caligata) kept in the laboratory at a T a of 10° C for 18 days in February. Despite being inactive, every one or two days the heart rate rises abruptly, remains high for a number of days, and then falls again. These records are from an animal under laboratory conditions, but similar changes have been recorded from animals in the wild.
Most hibernators spend the winter in hibernacula or dens some feet below the ground surface. The importance of the behaviour involved in the selection and ‘engineering’ of these winter quarters is demonstrated in Figure 14, which shows the variation in external temperature in Alaska from September to May. Superimposed on these data are temperatures of the warmest and coolest burrows of arctic ground squirrels (Spermophilus undulatus). You can see the burrow temperatures vary by less than 10° C throughout these winter months, though for most of that time they are below zero (Mayer, 1960).
An exception to the rule is the dormouse (Muscardinus avellanarius), which hibernates above ground, usually amongst the leaf litter (which provides some protection) on woodland floors. The most obvious changes in deep hibernation (apart from the lowered T b) are concerned with metabolism.
Heart rates of over ten or under three beats per minute are rare. The major cause of these extremely low rates is the lengthening of the time between individual beats.
Cardiac output is also reduced, to about 1.5% of normal (a mere 1 cm3 blood min−1 in the ground squirrel).
Respiration is greatly reduced. It may take place at quite evenly spaced intervals, or long periods of apnoea (cessation of breathing) may occur followed by several deep inspirations. (The record for holding a breath in torpor is 150 minutes in a hedgehog, though the average for this species is 60 minutes.)
The lower T b of hibernating animals and the changes in the respiratory and cardiovascular performance lead to marked acidosis: the pH of arterial blood falls by 0.24–0.48 and P CO2 is increased by a factor of 2.5–4.0. The oxygen supply to the tissues is dependent upon cardiac output, haemoglobin concentration and on the shape of the oxygen dissociation curves. Figure 15 illustrates the latter for euthermic (T b 38° C) and hibernating (T b 6° C) ground squirrels.
What do you conclude from Figure 15?
The curve for the hibernating squirrel has shifted markedly to the left. Half-saturation (P50) is therefore achieved at a much lower P O2, indicating a higher oxygen affinity.
Other evidence indicates that there is also an increase in haemoglobin in the blood as an animal enters hibernation. The hibernator's tissues therefore have a high tolerance of hypoxia. These changes explain how a hibernating animal such as a hedgehog can survive the long period of apnoea that is characteristic of intermittent breathing; it draws on the increased oxygen stored in the blood.
In addition to changes in respiration and in the cardiovascular system, there are marked changes in endocrine function. Endocrine gland atrophy is characteristically found prior to the onset of hibernation; particularly atrophy of the pituitary, gonads, thyroid and adrenal glands.
The physiological state of an animal in deep hibernation is, however, dynamic (the physiological controls are still working) and not that of a passive animal made hypothermic. For example, if there is a decline in the resistance of the peripheral blood vessels and a drop in blood pressure, there follows a compensatory increase in heart rate and cardiac output. The most graphic illustration of the fact that a hibernator retains physiological control mechanisms is its response to the falling ambient temperature. If T a drops below a particular level (which depends upon the species in question), there is always a compensatory increase in heart and respiratory rate, and a rise in metabolic rate, and therefore a tendency to raise or at least preserve T b. If the carbon dioxide concentration of the inhaled air is increased, then hibernating mammals react by increasing their breathing rate. In the hedgehog, the CO2 threshold is 0.7–1.7%, at which point the periods of apnoea become shorter. Continuous breathing replaces periodic breathing at 5–9% CO2.
The evidence suggests therefore, that the hibernator is sensitive to changes in its environment and that appropriate physiological responses can still be made. If the change or response is major, then the individual rapidly begins to arouse. It is this ability of hibernators to elevate T b from 5–10° C to the euthermic level, even at T a values below zero, that puts them into a class of their own.