The importance of temporal heterothermy in bats

Abstract

Animals must balance their energy budgets even when confronted with periodic food shortages and/or adverse environmental conditions. Especially, small endothermic animals require large amounts of energy to maintain high and stable body temperatures (Tb) via endogenous heat production. To deal with energetic challenges, many small endotherms are heterothermic, abandon regulation of high Tb and enter a state of torpor resulting in large energy savings. Torpor is used by many bat species because they are small, have high rates of heat loss and rely on fluctuating food resources (e.g. insects, fruit, nectar). Many bats use torpor all year, but the expression of temporal heterothermy can be strongly seasonal especially for temperate and subtropical species, which may hibernate for long periods. Recent advances in our understanding of torpor expression in bats have been made using temperature telemetry for remote data collection of Tb in free-ranging wild individuals from all climate zones. This new knowledge on free-ranging bats has revealed the importance of torpor expression not only for energy conservation but also for other benefits, such as reduction of extrinsic mortality (e.g. predation). On the contrary, dense clustering during hibernation, important for minimizing energy and water loss, may also expose bats to infectious disease. An emerging, cold-tolerant fungal pathogen of bats causes a new disease called white-nose syndrome (WNS), which is devastating populations of multiple species in eastern North America. Given the importance of temporal heterothermy to their biology, and links between torpor expression and mortality from WNS, it is becoming increasingly important to understand the ecology and physiology of torpor in this largely understudied and cryptic mammalian group. Here, we review past and current literature to summarize the importance and evolution of heterothermy in bats.

Thermoregulation by captive and free-ranging Egyptian rousette bats (Rousettus aegyptiacus) in South Africa

“…Despite body mass loss of up to ~16 % of ad libitum feeding body mass, none of the captive bats decreased T b below 33.4 °C, a value only slightly above the minimum of 32.0 °C observed in wild bats in the field study. These laboratory data hence support the view that medium sized pteropodids are generally not heterothermic and that the physiological capacity for torpor may have been lost in larger members of this family (Stawski et al 2014). …”

“…Torpor is used by various bats to offset energetic constraints, but most investigations have focused on insectivorous species with body mass < 40 g (Stawski et al 2014). Fruit-and nectar-feeding bats might also be expected to face seasonal energy shortages when these foods are in short supply.…”

“…There is growing evidence that torpor is a plesiomorphic trait widespread in basal lineages (Geiser 2008), especially among species with smaller body sizes. Laboratory studies have established that several small (16-18 g) pteropodids express daily torpor with T b falling as low as 17.2 °C, especially when food is restricted (Bartels et al 1998;Geiser et al 2001;McNab and Bonnacorso 2001; reviewed by Stawski et al 2014). In contrast, most medium sized tropical and semi-tropical pteropodids (50-200 g) appear not to use torpor (Bartholomew et al 1970;McNab and Bonnacorso 2001;Riek et al 2010;Downs et al 2012;but see McNab 1989), suggesting that the energetic demands of medium-sized bats in the tropics may not be stringent enough to warrant the use of torpor.…”

Summit metabolism and metabolic expansibility in Wahlberg's epauletted fruit bats (Epomophorus wahlbergi): seasonal acclimatisation and effects of captivity

“…The high M sum and ME we observed in both wild and captive E. wahlbergi do not support the prediction that nocturnal mammals inhabiting subtropical latitudes have only modest capacities for resting metabolic heat production compared with species inhabiting cold, north-temperate climates. Among the bat species for which estimates of M sum do exist, T. brasiliensis, C. perspicillata, S. lilium and A. lituratus are all known to use torpor (Audet and Thomas, 1997;Hirshfeld and O'Farrell, 1976;Studier and Wilson, 1970), whereas torpor has not been documented in E. wahlbergi or any other pteropodid with M b >50 g (Stawski et al, 2014). Thus, there is no clear link between the use of torpor and high M sum in Chiroptera (Fig.…”

Modelling mammalian energetics: the heterothermy problem

“…But factors other than energy expenditure, such as low water availability (see above) or the reproductive status of an individual can also influence torpor use. While some species abandon torpor use during pregnancy and lactation [63,138,139], others will continue to use torpor to save energy during inclement conditions and even to delay parturition until a more favourable time [107,140,141]. When attempting to model how a species will respond to changes in climate, it is important to have an understanding of how often, and for how long, they will be able to employ torpor.…”