A Mesocosm Experiment in Ecological Physiology: The Modulation of Energy Budget in a Hibernating Marsupial under Chronic Caloric Restriction

During the past 60 years, mammalian hibernation (i.e., seasonal torpor) has been interpreted as a physiological adaptation for energy economy. However, direct field comparisons of energy expenditure and torpor use in hibernating and active free-ranging animals are scarce. Here, we followed the complete hibernation cycle of a fat-storing hibernator, the marsupial Dromiciops gliroides, in its natural habitat. Using replicated mesocosms, we experimentally manipulated energy availability and measured torpor use, hibernacula use, and social clustering throughout the entire hibernation season. Also, we measured energy flow using daily food intake, daily energy expenditure (DEE), and basal metabolic rate (BMR) in winter. We hypothesized that when facing chronic caloric restriction (CCR), a hibernator should maximize torpor frequency to compensate for the energetic deficit, compared with individuals fed ad lib. (controls). However, being torpid at low temperatures could increase other burdens (e.g., cost of rewarming, freezing risks). Our results revealed that CCR animals, compared with control animals, did not promote heat conservation strategies (i.e., clustering and hibernacula use). Instead, they gradually increased torpor frequency and reduced DEE and, as a consequence, recovered weight at the end of the season. Also, CCR animals consumed food at a rate of 50.8 kJ d(-1), whereas control animals consumed food at a rate of 98.4 kJ d(-1). Similarly, the DEE of CCR animals in winter was 47.3 & PLUSMN;5.64 kJ d(-1), which was significantly lower than control animals (DEE=88.0 & PLUSMN;5.84 kJ d(-1)). However, BMR and lean mass of CCR and control animals did not vary significantly, suggesting that animals maintained full metabolic capacities. This study shows that the use of torpor can be modulated depending on energy supply, thus optimizing energy budgeting. This plasticity in the use of heterothermy as an energy-saving strategy would explain the occurrence of this marsupial in a broad latitudinal and altitudinal range. Overall, this study suggests that hibernation is a powerful strategy to modulate energy expenditure in mammals from temperate regions.