Field evidence for a proximate role of food shortage in the regulation of hibernation and daily torpor: a review

Abstract

Hibernation and daily torpor (heterothermy) have long been assumed to be adaptive responses to seasonal energy shortage. Laboratory studies have demonstrated that food shortage alone can trigger the use of heterothermy. However, their potential to predict heterothermic responses in the wild is limited, and few field studies demonstrate the dependence of heterothermy on food availability under natural conditions. Thus, the view of heterothermy as an energy saving strategy to compensate for food shortage largely remains an untested hypothesis. In this paper, we review published evidence on the proximate role of food availability in heterothermy regulation by endotherms, and emphasize alternative hypotheses that remain to be tested. Most studies have relied on correlative evidence. Manipulations of food availability, that demonstrate the proximate role of food availability, have been conducted in only five free-ranging heterotherms. Several other metabolic constraints covary with food availability and can confound its effect. Shortage in water availability, the nutritional composition of food, or subsequent conversion of food in fat storage all could be actual proximate drivers of heterothermy regulation, rather than food shortage. Social interactions, competition for food and predation also likely modulate the relative strength of food shortage between individuals. The ecological relevance of the dependence of heterothermy on food availability remains to be assessed in field experiments that account for the confounding effects of covarying environmental and internal factors.

When to initiate torpor use? Food availability times the transition to winter phenotype in a tropical heterotherm

“…In the wild, food supplementation during periods of natural food shortage is the most direct experimental approach to test for the dependence of heterothermy on energy availability (Humphries et al 2003b;Vuarin and Henry 2014). The aim of the present study was to provide the first test of a direct dependence of the launching of torpor use on seasonal food availability under natural conditions.…”

“…To date, it remains controversial whether heterothermy is mainly expressed in anticipation of upcoming seasonal unfavourable conditions, and triggered by fixed seasonal cues, or mainly a flexible thermal strategy that fine-tunes energy expenditure according to short-term fluctuations in energy availability (Vuarin and Henry 2014;Williams et al 2014). Photoperiod is an ubiquitous, proximal environmental cue for seasonal acclimation (Helm et al 2013).…”

“…As heterothermy is generally expressed during harsh climatic conditions and/or lean periods (Körtner and Geiser 2000;Heldmaier et al 2004;Vuarin and Henry 2014), it has commonly been regarded as an adaptive strategy to cope with energy shortage (Humphries et al 2003a;Munro et al 2005;Landry-Cuerrier et al 2008;see Geiser 2013;Vuarin and Henry 2014, for other functions). But heterothermy comes with costs, such as oxidative stress, reduced immunocompetence or cognitive impairments (Humphries et al 2003a;Angilletta et al 2010).…”

Modelling mammalian energetics: the heterothermy problem

“…For hibernating species the extent of torpor use can also be dependent on body condition or quantity of available food stores [102,130]. For example, in southern African hedgehogs (Atelerix frontalis) and mouse lemurs, only heavy individuals will undergo hibernation during the winter period, whereas individuals with a lower body mass will only use shorter bouts of torpor [98,131,132].…”

“…Studies on the T b patterns and thermoregulation of freeranging animals have illustrated the effects, and sometimes confounding influences, of a number of factors including predation risk [150], presence of conspecifics [145], food availability [130,161], competition [162] and extreme events [50,51,153,163] on T b . Yet, robust predictions of responses to climate change require an in-depth understanding of how animals exist in the wild [4,8].…”