The maintenance of a high body temperature is a considerable cost for small endothermic animals. Small animals have a relatively large surface to volume ratio resulting in high heat loss during cold exposure, high mass-specific BMR in thermo-neutrality, high mass-specific energy expenditure during locomotion and a relatively small capacity for fat storage (Geiser et al. 2006). So especially in periods where ambient temperatures are low small animals face higher energetic costs. Thermoregulatory costs account for 40 to 60 % of total daily energy expenditure for small endotherms (Bozinovic et al. 2004). To reduce this energy loss, animals have evolved many different adaptations, for example daily torpor.
What is torpor?
Daily torpor is defined as a controlled reduction in body temperature and metabolic rate for less than 24 hours (Geiser, 2004), accompanied by inactivity and absence of locomotion. Most animals go into torpor in the coldest parts of the night, approximately from 03.00 a.m. to sunset. When not in torpor the energy requirements for thermoregulation would be highest in this period because of the large difference between body and ambient temperatures. So daily torpor is a way to combine metabolic down regulation with a change in circadian activity rhythm to reduce energy expenditure for thermoregulation at times when these energy requirements would be the highest.
Daily torpor is a widespread phenomenon. It is found in at least eleven mammalian orders including marsupials (Heldmaier and Elvert, 2004) and in six avian families (McKechnie and Lovegrove, 2002).
Advantages of torpor for animals
Substantial energy savings
The energy that is saved during daily torpor is substantial. During torpor most mammals have a metabolic rate (MR) of 10 to 20% of their normothermic MR. The energy that is saved by employing daily torpor is between 80% and 90% of the energy that is used by normothermic thermoregulation at the same ambient temperatures (Song et al. 1995; Geiser, 2004).
Modularity
Whether or not an animal will show torpor is for most species dependent on the energy demand, body weight, and energy intake, and can be varied on a daily basis (Körtner and Geiser, 2000). Generally an animal will show torpor at a specific time of day in a specific season. The duration of torpor can be varied according to food availability and environmental conditions (Christian and Geiser, 2007). This gives the animal the opportunity to fit the number and duration of torpor bouts nicely with its individual energy balance.
Disadvantages of torpor for animals
Harmful physiological effects
Many animal species limit the time they spent in torpor whenever it is energetically possible (Humphries et al., 2003). Sugar gliders for example will show more torpor when ambient temperature is low and rainfall is high, but will skip torpor sessions when food is plenty or the environmental conditions are accommodating (Christian and Geiser, 2007). This avoidance of torpor suggests that there are costs associated with it. There is an indication that torpor reduces immunological abilities, postpones maintenance and repair processes, increases vulnerability to predation (Radzicki et al., 1999) and could impair memory formation and/or memory maintenance (Millesi et al. 2001). It has also been shown that nutrient absorption in the digestive tract is slowed at low body temperatures (Carey, 1989). Daily torpor could also be responsible for accumulation of sleep debt (Daan et al., 1991), reduced synaptic efficacy (Strijkstra et al., 2003) and in reproductive females it can result in slowed growth of young (Racey, 1982). Therefore it is thought that increased torpor usage is associated with decreased fitness (Grinevitch et al., 1995).
Harmful ecological effects
Because torpid individuals are inactive and show a decreased and slowed response to stimuli, it cannot avoid predation when detected by a predator. Therefore daily torpor can increase the risk of predation (Radzicki et al., 1999).
Studies of daily torpor in two species
Here we present two representative studies that illustrate the dynamics of daily torpor and the energy saved by employing it in two species of marsupials. * n = number of observed torpid animals, N = number of occasions torpor was observed.
Torpor in the Sugar glider (Petaurus breviceps)
Christian and Geiser (2007) have measured the torpor pattern of sugar gliders in the field. Sugars gliders (Petaurus breviceps) are small (ca. 130 g.) nocturnal marsupials. This species lives an arboreal lifestyle in the open forests of Australia. The diet is mostly composed of arthropods and animal and plant exudates. In winter sap production of eucalyptus trees and arthropod abundance declines while cold and wet weather dominates. These factors make foraging in winter energetically expensive. To reduce the amount of weight loss in winter, sugar gliders can reduce their activity, reduce normothermic body temperature or use daily torpor (Christian and Geiser, 2007).
The measurements of torpor in wild sugar gliders in open eucalypt/acacia woodland in Australia show that sugar gliders use torpor in the colder parts of the night, especially when it also rains. Minimal body temperature fell as low as 14.1 ºC (normothermic temperature: 36 ºC) and averaged 24.0 ± 1.3°C (n = 9; N = 34)* with bouts lasting (393.4 ± 35.8 min; n = 9; N = 34) in ambient temperatures between 8 and 15 °C (Christian and Geiser, 2007). In torpor bouts (defined as body temperature lower than 24.0 ºC) energy loss is minimized because MR can be reduced to ~20% of the normothermic values in sugar gliders (Fleming 1980; Christian and Geiser, 2007).
Fat-tailed dunnart (Sminthopsis crasicaudata)
Another study by Holloway and Geiser (1995) describes the energy expenditure of Sminthopsis crasicaudata in the laboratory. Sminthopsis crasicaudata or fat-tailed dunnart is a small (16 g.) nocturnal dasyurid marsupial. It is found in the mesic to arid regions of central and southern Australia and displays daily torpor both in the wild and in the laboratory. Its diet mostly consists of small arthropods.
Metabolic rates where measured as the rate of oxygen consumption (VO2). The animals were individually housed in a respiratory vessel without food or water during the measurements and VO2 was continually monitored. Holloway and Geiser (1995) found normothermic body temperature displayed a large variation ranging from 30.1 ºC to 37.8 ºC with a mean value of 33.8 ºC. When in torpor, the body temperature ranged from 14.3 ºC at ambient temperatures of 10 ºC to 29.6 ºC at ambient temperatures of 18 ºC.
The oxygen consumption at different temperatures and different activity are presented in figure 1. RMR during the daylight hours where 3.82 ± 0.09 ml g/hr at 18 ºC and 5.00 ± 0.04 ml g/hr at 12 ºC. After the onset of darkness MR increased to maxima of 6.49 ± 0.21 ml g/hr at ambient temperatures of 18 ºC and 7.74 ± 0.19 ml g/hr at ambient temperatures of 12 ºC because of nocturnal activity. These rates where generally maintained until the animal entered torpor between 03.00 and 05.00 in the morning. When no torpor occurred the MR stayed up until morning, where it went back to RMR. Torpor bouts where marked by a steady decline in MR to 0.72 ± 0.11 ml g/hr at ambient temperatures of 18 ºC and 0.41 ± 0.10 ml g/hr at ambient temperatures of 12 ºC. This represents a decrease from the resting values of 81.2% at 12 ºC and 91.8% at 18 ºC. Upon arousing from torpor MR was drastically increased to 7.76 ± 0.43 ml g/hr at 18 ºC and 8.51 ± 0.29 ml g/hr at 12 ºC before returning to resting levels. The duration of these arousals ranged from 0.81 ± 0.09 hr at 18 ºC to 0.67 ± 0.06 hr at 12 ºC. Figure 1 provides an overview of the oxygen consumption at 12 ºC and 18 ºC.
When the costs of arousal, activity and torpor are added and compared to energy expenditure at days without torpor, energy saving is approximately 30 – 50% for a torpor bout of 10 hr. The mean torpor duration of 5 hr results in a 16% reduction of average daily metabolic rate at 12 ºC and a 12% reduction at 18 ºC. When comparing VO2 from onset of a 5 hr torpor bout until arousal with the RMR at the same interval, savings amount up to 43%.
From these two studies, it can be concluded that daily torpor can reduce daily energy expenditure by 12% to 16% in Sminthopsis crasicaudata to ~20 % in Petaurus breviceps. Other animals that show torpor are expected to have similar energy savings, but this is of course also depended on the duration of torpor bouts.
