5.5 Energy budgeting – the benefits of hibernation and torpor
Studies performed on ground squirrels in the wild and in the laboratory have allowed estimates to be made of energy expenditure in hibernating and euthermic animals over similar periods (Wang, 1987). The average time spent by Richardson's ground squirrel in a periodic arousal in the wild is about 10 hours and the frequency of arousal decreases during November-March, when animals are spending more than 90% of their time in torpor. Monthly total oxygen consumption in January is about 35% of that in August, and rises again in February and March. Between July and March, entry into hibernation accounts for 27% of total energy expenditure, torpor for 33% and arousal for 40%. However, if the time between periods of torpor is taken into account, the figures are 12% for entry, 17% for torpor and 19% for actual arousal with 51% for the euthermic periods between arousals.
Entry into hibernation seems to cost little. Entry and the hibernation period together account for less than one-third of the total energy expenditure averaged over the whole 9-month period. Arousal in itself is not that expensive (less than 20%). It is the time between bouts of hibernation, when the animal is euthermic, that consumes more than 50% of the energy expended, though the amount varies between months. In December and January for example, entry and torpor account for more than 35%, and time in euthermia for about 40% of the energy expended.
We have estimates of how hibernators apportion expenditure throughout the hibernating season. But how do the figures compare with figures from similar individuals that are euthermic over the same period? Wang's estimates are given in Table 5. From August through to February, the savings due to hibernation are over 80%. Even in July and March, months in which arousal frequency is high and time in torpor is short, the savings are significant. On average over 9 months, hibernation endows a small mammal, such as this ground squirrel, with an 88% saving of energy. Over an entire year, the hibernating habit saves an animal 60% of the energy used by an individual of similar size that continuously maintains the euthermic condition.
Table 5 The reduction of metabolic cost by hibernating, in Richardson's ground squirrel
|Month||Total energy expenditure with torpor/cm3 O2 month−1||Total energy expenditure if animal remained euthermic/cm3 O2 per month||% energy saved by exhibiting torpor|
|mean for 9 months||87.8|
Note: * During parts of July and March the animal is not in hibernation, hence these values are low. When calculating the % energy saved by exhibiting torpor, it was assumed that the animals were hibernating for the equivalent of only half of these 2 months, i.e. a total of 8 months in the year.
A study of a close relation, the golden-mantled ground squirrel, showed that, during the hibernating season, energy expenditure in this particular species was also only 20% of the expected value if the animal remained euthermic. Furthermore, the energy consumption throughout the 7 months of the hibernating season was only 15% of the total annual consumption.
Both these species fit our earlier definition of obligative, deep hibernators; the picture may be a little different in facultative hibernators responding more directly to environmental cues. Using one such animal, the golden hamster (Mesocricetus auratus), the energy budgets of a whole population in the laboratory were estimated. The hibernating behaviour of individuals varied widely. The average for the group was that only 18% of the ‘hibernating season’ was spent in torpor, though this value might not be representative of a wild population. However, when in torpor their energy consumption was only 9% of normal euthermic consumption at that temperature. Overall, the group saved 23% of the energy they would have used without torpor, still quite a significant figure.
What are the disadvantages to an animal in entering torpor, or full seasonal hibernation?
The animal becomes very vulnerable to predators. A deep hibernator may take quite a long time to respond even to an alarm arousal. Also, unless the ‘cold alarm arousal’ is efficient, the T b may go below the point from which it can recover.
The energy cost of hibernation must also take into account the special requirements of females in gestating and caring for the young. Their T b fluctuations, torpor bout duration and BMR often differ from those of males of the same species. In pregnant female black bears (Ursus americanus) in the North American Rocky Mountains, the cost of winter reproduction, including gestation and lactation, was found to be 1432 kJ day−1 to produce two young. Fat provides 92% of the total energy for lactation and gestation during early winter. Consequently, these animals have 89% larger fat depots than have non-reproductive females entering hibernation. The rate of fat loss was 37% greater, and protein loss was about 2.4 times higher for reproductive females than for non-reproductive females. Protein utilization is a last resort in any hibernating animal due to the danger of nitrogen toxicity and the disadvantages of muscle weakness on arousal. However, a source of transplacental amino acids is essential even when the mother is not feeding. Black bears minimize this cost by having a shorter period of post-implantation gestation together with metabolic pathways that enable them to hydrolyse urea and recycle their nitrogen more effectively than other mammals (The openLearn course on Polar biology (S324_3) covers this in more detail).