Award Date


Degree Type


Degree Name

Doctor of Philosophy in Biological Sciences


Life Sciences

First Committee Member

Frank van Breukelen, Chair

Second Committee Member

Andrew Andres

Third Committee Member

Jeffrey Shen

Graduate Faculty Representative

Ronald Gary

Number of Pages



During the hibernation season, animals oscillate between periods of torpor and periods of interbout arousal (IBA). During torpor, body temperature is often near 0° C and metabolism is severely depressed. Oxygen consumption, a proxy for aerobic metabolism, may fall to 1% of active values. Many physiological processes including cardiovascular, respiratory, and cellular functions nearly cease. During the IBA, euthermic body temperature is restored and most systemic and cellular processes function at fully active levels. The transition period between these two physiologically dissimilar states is called arousal.

The rate of rewarming (RRW) during arousal was previously expected to progressively increase until a euthermic set point was approached. However, my data contradict this expectation. I monitored the body temperature (Tb) of goldenmantled ground squirrels (Spermophilus lateralis) housed at 4, 8, 12, and 16° C during natural arousals. The various housing temperatures facilitate manipulation of torpid Tb, since torpid Tb is usually within 1° C of ambient temperature (Ta). The maximum RRW, the time required to reach a maximum RRW, and the relative time index all demonstrated negative relationships with Ta. The Tb corresponding to maximal RRW demonstrated a positive relationship with Ta. One parameter was independent of ambient temperature. Squirrels reached maximal RRW when they had generated 30 to 40% of the heat required to reach a euthermic Tb. These data suggest that arousal is more constrained than expected and that both time and temperature influence the RRW.

Much hibernation research involving arousal has been conduced on animals that were induced to arouse prematurely. Natural arousal from torpor occurs
spontaneously with highly predictable timing. However, animals can also be induced to arouse prematurely in response to various disturbances. While many investigations have used natural and induced arousals synonymously, direct comparisons of these two types of arousal have been lacking. I addressed the question of whether natural and prematurely induced arousals are the same. I compared the effects of ambient temperature on the dynamics of natural versus induced arousals. Arousal duration, maximum rewarming rate, and the variance associated with increases in body temperature increased during induced arousals. Prematurely inducing arousal also decreased the duration of the interbout aroused (IBA) period, and the responsiveness to the induced arousal stimulus was influenced by torpor duration.

The metabolic cost of natural versus induced arousal from torpor was also investigated. Metabolic activity was estimated through indirect calorimetry and assays of metabolites in blood plasma. Although initial rates of oxygen consumption were comparable for natural and induced arousal, initial rates of carbon dioxide production and respiratory quotient values were significantly reduced during induced arousal. Plasma lactate levels were significantly elevated during induced arousal whereas glucose and free fatty acids levels were similar. Previous work has indicated oxidative stress and elevated antioxidant defenses during hibernation. However, the effectiveness of these defenses has not been as well characterized. Indicators of oxidative damage to lipids and proteins in heart, liver, kidney, and brain tissues were measured to investigate potential oxidative damage to cellular macromolecules. Lipid peroxidation products and protein carbonyl levels were low in all tissues for both types of arousal. Thus, hibernators appear to be well protected against oxidative damage.

Arousal was once regarded as a sole effort to rewarm as quickly as possible, thereby facilitating conservation of energy stores. However, data indicate that arousal is a more constrained process where animals regularly experience less than maximal rewarming rates. Further, prematurely inducing arousal alters key aspects of the rewarming process as well as metabolic activity. Considering these differences, I recommend that careful consideration be given to experimental design and data interpretation when arousing animals are utilized.


Golden-mantled ground squirrel – Hibernation; Ground squirrels; Hibernation; Rewarming


Animal Sciences | Biology | Physiology