A mesocosm experiment in ecological physiology: adaptive modulation of energy budget in a hibernating marsupial under chronic caloric restriction

Abstract

During the last sixty years, mammalian hibernation (i.e., seasonal torpor) has been interpreted as a physiological adaptation for energy economy. However -and crucially for validating this idea - direct field comparisons of energy expenditure in hibernating and active free-ranging animals are scarce. Using replicated mesocosms and a combination of energy budgeting approaches (i.e., doubly labelled water, rates of CO2 production and food intake), we experimentally manipulated energy availability and quantified net energy costs of hibernation in a marsupial. We hypothesized that, when facing chronic caloric restriction (CCR), a hibernator should maximize torpor use for compensating the energetic deficit, compared to ad libitum fed individuals (=controls). However, intensifying torpor duration at low temperatures could increase other burdens (e.g., cost of rewarming, freezing risk). In order to explore this trade-off, we followed the complete hibernation cycle of the relict marsupial Dromiciops gliroides, and estimated its total energy requirements, and compared this with a control condition. Our results revealed: (1) that energy restricted animals, instead of promoting heat conservation strategies during hibernation (e.g., social clustering and thermoregulation), maximized torpor use and saved just enough energy to cover the deficit, and (2) that hibernation represents a net energy saving of 51% compared with animals that remained active. This work provides compelling evidence of a fine-tuning use of hibernation in response to food availability and presents the first direct estimation of energy savings by hibernation encompassing the total hibernation cycle.