The costs and benefits of hibernation

Some animals hibernate to save energy in times of low energy intake, e.g. due to low food availability. What are the costs and benefits of hibernation? I’ll explain in this short paper.

What is hibernation?

Hibernation is defined as a torpor bout that it is maintained for periods longer than 24 hours and it is per definition only present in winter. When a mammal goes into hibernation it will diminish its metabolism and allows its body temperature to drop to a few degrees above ambient temperatures. When the body becomes too cold, the animal will actively generate heat to stay alive (Wilz and Heldmaier, 2000). Hibernation is not one single bout of torpor during winter, but the period of torpor is divided in small bouts of torpor of approximately 2 weeks by periodic arousals. In these arousals the organism actively warms up to normothermic temperature by activation of the major heat-producing mechanisms. It will remain normothermic for a few hours, in which it will predominately sleep (Daan et al. 1991). Some species, for example bats, leave their hibernaculum (hibernation place) for some time during arousals. Arousals are hypothesized as essential for hibernation because all hibernating animals show arousals, even though it comes with large energy costs. Most of the energy spent on hibernation is actually spent on the periodic arousals. If an activity has high costs, it should have high returns too, suggesting arousals during hibernation avoid deleterious effects or offer other advantages.

Advantages of hibernation

Substantial energy savings

Hibernation is the best way of reducing energy expenditure in harsh conditions, for example at ambient temperatures around or below 0 °C.
During hibernation the MR of the animal is greatly reduced. Oxygen consumption and breathing rate will also greatly diminish during hibernation. For example in the marsupial Dromiciops gliroides VO2 falls to 1% of the euthermic value and respiratory frequency falls from 370 to 2 per minute (Bozinovic et al, 2004).The energy saving is enormous: for example the edible dormouse saves up to 99.6% of its energy when hibernating at 4 ºC compared to resting at 4 ºC (Wilz and Heldmaier, 2000). Because of this low energy demand most hibernators can survive for several months on fat reserves alone. This is of enormous value for animals living in climates where the environmental conditions or temperature are too harsh to be active in, or in areas where food availability in winter is too low to sustain the organism. Without the energy saving aspects of hibernation, existence in these regions almost does not seem to be possible for those small mammal species.

Reduced risk of predation

When an animal goes into hibernation, most species will stay in their hibernaculums for 4 to 6 months. In this time the animals will not be exposed to their regular predators, for example birds of prey (Bieber and Ruf, 2009). For species were predation is one of the major causes of death, this advantage is huge.

In an evolutionary perspective, the use of hibernation by a species forces its predators to switch diet or migrate, especially if this predator is a specialist. This imposes a problem on the predators, which could result in less overall predation or less predation right after hibernation.

Disadvantages of hibernation for animals

Hibernation is shown to impose costs on animals. These costs are both in the harmful physiological effects of hibernating, as well as in the costs of being unable to respond to stimuli.

Harmful physiological effects

It has been determined that animals show poor memory retention after hibernating. When ground squirrels (Spermophilus citellus) are trained to complete a task involving spatial memory and an operant condition test, they perform poorly when tested again after hibernation compared to a control group which did not hibernate. This shows that hibernation has a negative effect on memory retention (Millesi et al. 2001).
Immunocompetence is also reduced when hibernating, making the animal vulnerable to infections and parasites during and shortly after hibernating (Luis and Hudson, 2006).

It has also been shown that nutrient absorption in the digestive tract is slowed at low body temperatures (Carey, 1989) and in reproductive females hibernation can result in slowed growth of young (Racey, 1982). Daily torpor could also be responsible for accumulation of sleep debt (Daan et al., 1991) and reduced synaptic efficacy (Strijkstra et al., 2003). In males sperm cell production is inhibited during hibernation because of low body temperatures and low MR (Racey, 1982).
It is thought that the periodic arousals are used to restore the maintenance of cells, restore immunological processes to some degree and remove deleterious substances in the brain. Since the harmful physiological effects of hibernation can still be measured, in spite of the fact that all hibernating species show arousals, those harmful effects must be quite large and pervasive.

Decreased vigilance

Hibernating animals have a decreased sensitivity to stimuli and therefore cannot quickly respond to threats. Arousal from hibernation can take several minutes to several hours. This makes them more vulnerable for predation. (Radzicki et al., 1999).

Animals that store food are susceptible to hoard pilferage because of their decreased sensitivity to stimuli and inability to quickly respond to the intruder. When the hoard is being stolen, the hibernator will almost certainly die.

Reliability on the location where hibernation takes place

A hibernator is highly reliable on the integrity and suitability of its hibernaculum (place of hibernation). When a hibernator is dispelled from its hibernaculum, exposure and the inability to find a suitable new hibernaculum soon enough cause it to almost inevitably die. Unexpected adverse circumstances in the hibernaculum can have the same effect.

Examples of the effects of hibernation on a marsupial species

The small marsupial Dromiciops gliroides “Monito del monte”

monito del monte
monito del monte

Bozinovic et al. (2004) have studied the energy saving of hibernation in the microbiotheriid marsupial Dromiciops gliroides. Dromiciops gliroides is a small (ca. 40 g.) nocturnal marsupial that is found in the northern part of the temperate forest of southern South America. It has the common name “Monito del monte” in these regions. Within the three recognized orders of marsupials in South America (the Paucituberculata, Didelphimorphia and Microbiotheria) it is the only living representative of the otherwise extinct lineage of Microbiotheres. Dromiciops gliroides inhabits humid, cool and dense forests where it lives an arboreal lifestyle. Its diet consists of fruits and small arthropods.

Dromiciops gliroides displays daily torpor as well as hibernation. Here we will focus only on hibernation, defined as torpor bouts lasting > 24 h. Wild D. gliroides where captured and kept in captivity. Measurements were taken in a closed respirometry system. Torpor was induced by depriving the animals of food.
Normothermic D. gliroides were found to have a RMR of 0.79 ± 0.01 ml O2/g/h. Body temperature was between 33.9 ºC and 36.4 ºC. When in hibernation for 5 – 6 days the VO2 fell to 1% of normothermic values, ranging from 0.03 to 0.06 ml O2/g/h at ambient temperatures of 12.5 ºC. Body temperature was 0.7 ºC above ambient temperature, 13.2 ± 0.01 ºC. Breathing rate decreased from 370 to 2 per minute.

When hibernating at 17.5 ºC, MR was slightly higher than at 12.5 ºC with a VO2 of 0.08 ml O2/g/h. This was maintained for 2 days. Hibernation at 20 ºC resulted in a VO2 of 0.12 ml O2/g/h. This means MR was 3% and 5.7 % of the normothermic value, respectively.

Figure 2 gives an overview of the oxygen consumption at rest or during hibernation at various ambient temperatures.

hibernation
Figure 2. Oxygen consumption by Dromiciops gliroides during resting and during hibernation at various ambient temperatures.