Abstract
Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian-mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (∼35°) than daily heterotherms (∼25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30-fold longer, and mean torpor bout duration >25-fold longer in hibernators. Mean minimum body temperature differed by ∼13°C, and the mean minimum torpor metabolic rate was ∼35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.
Highlights
Birds and mammals spend a large proportion of their energy expenditure on maintaining high euthermic1 body temperatures (Tb)
Other traits that point to functional differences are the minimum metabolic rate (MR) during torpor (TMRmin), which in in animals categorized as hibernators appears to be much lower, as well as the minimum body temperature (Tb min) that is defended during torpor, which seems higher in species regarded as daily heterotherms, the variation among species in Tb min is large
Given that classifying species as daily heterotherms was confirmed by bimodal variable distributions (Fig. 3) as well as cluster analyses, and could be based largely on variables beyond TBDmax, such as TMRmin and Tb min alone (Fig. 4), we refer to these groups as “daily heterotherms” and “hibernators”, and maintain our preliminary classification of species
Summary
Birds and mammals spend a large proportion of their energy expenditure on maintaining high euthermic body temperatures (Tb). The only ‘logical solution’ (Schmidt-Nielsen, 1979) for animals that cannot escape harsh environmental conditions by migration is to suspend the maintenance of high body temperatures (Tb) and employ a mode of living that saves energy This is the strategy used by many birds and mammals that employ hypometabolism, i.e., periods of profoundly reduced metabolic rate (MR) and Tb, which typically occur on a seasonal basis (Lyman et al, 1982). Other traits that point to functional differences are the minimum metabolic rate (MR) during torpor (TMRmin), which in in animals categorized as hibernators appears to be much lower, as well as the minimum body temperature (Tb min) that is defended during torpor, which seems higher in species regarded as daily heterotherms, the variation among species in Tb min is large It appears that body mass differs between the two categories with species conventionally viewed as hibernators being significantly bigger than species classified as daily heterotherms (Geiser & Ruf, 1995)
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