Hibernation and Torpor in Tropical and Subtropical Bats in Relation to Energetics, Extinctions, and the Evolution of Endothermy

Integrative and Comparative Biology, volume 51, number 3, pp. 337–348 doi:10.1093/icb/icr042 SYMPOSIUM Hibernation and Torpor in Tropical and Subtropical Bats in Relation to Energetics, Extinctions, and the Evolution of Endothermy Fritz Geiser1 and Clare Stawski Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale NSW 2351, Australia 1 E-mail: Synopsis Torpor, the most effective means of energy conservation available to endotherms, is still widely viewed as a specific adaptation in a few high-latitude, cold-climate endotherms with no adaptive function in warm regions. Nevertheless, a growing number of diverse terrestrial mammals and birds from low latitudes (0–308), including species from tropical and subtropical regions, are heterothermic and employ torpor. Use of torpor is especially important for bats because they are small, expend large amounts of energy when active, rely on a fluctuating food supply, and have only a limited capacity for storage of fat. Patterns of torpor in tropical/subtropical bats are highly variable, but short bouts of torpor with relatively high body temperatures (Tb) are most common. Hibernation (a sequence of multiday bouts of torpor) has been reported for free-ranging subtropical tree-dwelling vespertilionids, cave-dwelling hipposiderids, and house-dwelling molossids. The observed range of minimum Tb is 6–308C, and the reduction of energy expenditure through the use of torpor, in comparison to normothermic values, ranges from 50 to 99%. Overall, torpor in the tropics/ subtropics has been reported for 10 out of the currently recognized 18 bat families, which contain 1079 species, or 96.7% of all bats. Although it is unlikely that all of these are heterothermic, the large majority probably will be. Frequent use of torpor, including hibernation in diverse groups of tropical/subtropical bats, suggests that heterothermy is an ancestral chiropteran trait. Although data especially from the field are still scarce, it is likely that torpor, highly effective in reducing requirements for energy and water even under warm conditions, plays a crucial role in the long-term survival of the majority of small tropical and subtropical bats. Discovering how bats achieve this provides numerous opportunities for exiting new research. Introduction Why, one might ask, should bats in the tropics and subtropics employ torpor? Torpor is usually defined as a controlled and pronounced reduction in body temperature (Tb) and metabolic rate (MR) (Lyman et al. 1982; Geiser and Ruf 1995; Speakman and Thomas 2003) and traditionally it is viewed as an adaptation exclusively used at low ambient temperatures (Ta) or when food is severely limited. Exposure to cold requires a large increase in endogenous heat production to maintain a constant, high Tb and therefore necessitates access to energy in the form of food (Lyman et al. 1982; Withers 1992; Geiser and Ruf 1995; Speakman and Thomas 2003). The tropics and subtropics are relatively warm and at least do not expose bats to thermal challenges near or below Ta 08C that are often associated with torpor. While torpor is viewed as most effective for energy and water conservation in temperate-zone mammals and birds (Lyman et al. 1982; Hosken and Withers 1997; Thomas and Geiser 1997; Boyer and Barnes 1999; Geiser 2004), tropical and subtropical regions are viewed as thermally too benign to require energy to be conserved via a substantial reduction of Tb, as that achieved during torpor. It has even been argued that hibernation especially (sequence of multiday bouts of torpor, interspersed by periodic arousals) is impossible in tropical/subtropical habitats (Henshaw 1970; McNab 1974). Advanced Access publication June 22, 2011 ß The Author 2011. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: . From the symposium ‘‘Environment, Energetics, and Fitness: A Symposium Honoring Donald W. Thomas’’ presented at the annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2011, at Salt Lake City, Utah. 338 Methods Data on thermal biology, use of torpor, and torpor patters were derived mainly from the primary literature (Table 1) for as many bat families as possible. We also included unpublished work from a recent study on ghost bats (Megadermatidae) because data on low Tb in this family are especially scarce. Data on climate of sites where bats occur or the origin of bats and the body mass were used as provided by the original sources. Most data came from individuals living at low elevations; only two species were identified from high elevations. When quantitative field and laboratory data were both available, the field data were preferentially used because laboratory studies often underestimate the ecological significance of torpor use under natural conditions (Geiser et al. 2000). In some of the older literature, low Tb in bats was induced by exposure to low Ta. However, most of these studies do not provide data on endothermic rewarming from torpor at low Ta. Therefore, it is unclear whether bats became hypothermic (i.e., fall in Tb simply a failure in thermoregulation and bats forced to reduce Tb because of excessive cold) or whether the bats in fact entered torpor (i.e., the reductions of Tb and MR were controlled and reversible processes) (see Henshaw 1970; Lyman et al. 1982 for definitions). Thus, data on low Tb in bats without data on endothermic rewarming were either excluded or were clearly identified. The familial systematics and the number of bat species used here are based on Wilson and Reeder (2005). Torpor in tropical and subtropical bats Torpor has been observed in diverse tropical and subtropical bats both in captivity and under natural conditions (Table 1). Of the total 18 chiropteran families worldwide, 10 include species that express torpor in the tropics/subtropics. Several of the other eight families are either not found in the tropics or subtropics, or there are no data on torpor use in these groups [for example: New-World (Thyropteridae) and Old World (Myzopodidae) sucker-footed bats, or leaf-chinned bats (Mormoopidae)]; rather than that heterothermy does not occur. Even without knowledge about these low-diversity families, the total number of species of chiropteran families containing known heterothermic bats from tropical/subtropical regions represents the vast majority. The 10 families containing heterothermic species, which are distributed into the tropics/subtropics number 1079 or 96.7% of the currently recognized 1116 species (Wilson and Reeder 2005). Obviously, not all of these species are likely to be heterothermic, and only 35 species have been confirmed to be, but based on current data a large number of tropical/ subtropical bats are likely to employ torpor for conserving energy. Webb et al. (1996) have shown that temp (...truncated)