Short and hyperthermic torpor responses in the Malagasy bat Macronycteris commersoni reveal a broader hypometabolic scope in heterotherms

Abstract

The energy budgets of animal species are closely linked to their ecology, and balancing energy expenditure with energy acquisition is key for survival. Changes in animals' environments can be challenging, particularly for bats, which are small endotherms with large uninsulated flight membranes. Heterothermy is a powerful response used to cope with changing environmental conditions. Recent research has revealed that many tropical and subtropical species are heterothermic and display torpor with patterns unlike those of "classical" heterotherms from temperate and arctic regions. However, only a handful of studies investigating torpor in bats in their natural environment exist. Therefore, we investigated whether the Malagasy bat Macronycteris commersoni enters torpor in the driest and least predictable region in Madagascar. We examined the energy balance and thermal biology of M. commersoni in the field by relating metabolic rate (MR) and skin temperature (T) measurements to local environmental characteristics in the dry and rainy seasons. Macronycteris commersoni entered torpor and showed extreme variability in torpor patterns, including surprisingly short torpor bouts, lasting on average 20 min, interrupted by MR peaks. Torpid MR was remarkably low (0.13 ml O h g), even when T exceeded that of normothermia (41 °C). Macronycteris commersoni is thus physiologically capable of (1) entering torpor at high ambient temperature and T and (2) rapidly alternating between torpid and normothermic MR resulting in very short bouts. This suggests that the scope of hypometabolism amongst heterothermic animals is broader than previously assumed and underlines the importance of further investigation into the torpor continuum.

Variable Climates Lead to Varying Phenotypes: “Weird” Mammalian Torpor and Lessons From Non-Holarctic Species

“…Another, only recently studied, example is the Malagasy bat, Macronycteris commersoni. This species roosts in hot caves (≥32 • C year-round) and displays a whole spectrum of different torpor responses during summer and winter (Reher et al, 2018). In summer, individuals may remain euthermic or enter torpor bouts lasting up to 6 days (sometimes coinciding with cyclones), while in winter their responses range from short torpor bouts, over prolonged torpor to hibernation with single bouts lasting up to 16 days; the triggers for the duration of torpor use remain unknown (Reher et al, unpublished data).…”

“…It enables species to respond to the context of specific environmental parameters and their own body condition. For example, in the lemur Microcebus griseorufus and the bat Macronycteris commersoni all of these responses have been observed in different individuals in the same population at the same site (Kobbe and Dausmann, 2009;Kobbe et al, 2011;Reher et al, 2018). Similarly, western rock elephant shrews, E. rupestris, are highly heterothermic in South Africa, whereas the closely-related cape rock elephant shrews, E. edwardii, at the same site remain mostly homeothermic, although the species is capable of short to prolonged bouts of torpor (McKechnie and Mzilikazi, 2011;Boyles et al, 2012).…”

Phylogeography and population genetics of the endemic Malagasy bat,Macronycteris commersonis.s. (Chiroptera: Hipposideridae)

“…On the other hand, there is evidence from the northwest, specifically the region of Anjohibe, that local M . commersoni populations remain inactive in caves during times of resource shortage (AR Rakotoarivelo, 2010, unpublished data), which may explain the genetic uniqueness of clade C. Reher et al (2018) reported similar torpor behavior in the Tsimanampetsotsa National Park in south-western Madagascar.…”

Thermal physiology and activity in relation to reproductive status and sex in a free-ranging semelparous marsupial

“…Our study provides further evidence that daily torpor has alternative benefits other than just short-term energy savings for energetically stressed individuals (Nowack et al ., 2017; Reher et al ., 2018; Besler and Broders, 2019). Torpor may be employed by many heterothermic endotherms before and early during reproduction to enhance reproductive success by facilitating additional fat storage to be accessed later during pregnancy and lactation (Willis et al ., 2006; Morrow and Nicol, 2009; Stawski, 2010; Dzal and Brigham, 2013; Klug and Barclay, 2013; McAllan and Geiser, 2014).…”