Abstract

The energy metabolism of hibernators has not been characterized for normothermic fasting, and our goal was to quantify oxidative fuel selection of non-hibernating woodchucks Marmota monax during prolonged food deprivation. Indirect calorimetry and nitrogen excretion measurements were used to assess changes in metabolic rate (VO2), fuel selection and composition of nitrogen wastes, as well as seasonal differences. For reference, matching experiments were also performed on rabbits. The results show that woodchucks have a higher metabolic rate in summer (271 micromol O2 kg(-1) min(-1)) than in spring (200 micromol O2 kg(-1) min(-1)) and that fasting-induced metabolic depression is only possible in summer (-25% in 14 days). The metabolic rate of rabbits is high at all times (383 micromol O2 kg(-1) min(-1)), but they show a more rapid depression in response to fasting (-32% in 7 days). Woodchucks have a naturally low reliance on proteins in the fed state (accounting for 8% VO2) in spring; 17% VO2 in summer; vs 28% VO2 in rabbits) and are able to decrease it even further during fasting (spring, 5% VO2); summer, 6% VO2; vs 20% VO2 in rabbits). This study shows that, apart from their notorious capacity for hibernation, woodchucks are particularly well adapted for normothermic fasting. Their ability to cope with prolonged food deprivation is based on a series of integrated responses eliciting deep metabolic depression and a rapid change in fuel selection to spare limited protein reserves. Information presently available on prolonged fasting suggests that such an ability for metabolic depression, possibly down to minimal levels still compatible with normothermic life, may be common among mammals. In contrast, the extreme protein sparing demonstrated in woodchucks is a unique metabolic feature of fasting champions.

Highlights

  • Coping successfully with prolonged periods of fasting depends on two key physiological processes: metabolic depression (Craven, 1951; Markussen and Oritsland, 1986; Merkt and Taylor, 1994) and regulated changes in fuel selection (Cahill, 1970)

  • The prolonged fasting period characterized by phase II shows two important features: (1) the overall energy budget is dominated by lipid oxidation regardless of the organism’s natural history, but (2) the relative importance of proteins varies widely among animals, depending on how often and for how long food deprivation normally occurs in each species

  • The metabolic depression observed during fasting was accompanied by a decrease in body temperature (P

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Summary

Introduction

Coping successfully with prolonged periods of fasting depends on two key physiological processes: metabolic depression (Craven, 1951; Markussen and Oritsland, 1986; Merkt and Taylor, 1994) and regulated changes in fuel selection (Cahill, 1970). Energy metabolism becomes primarily dependent on protein oxidation (phase III), and muscle function starts being compromised, in the heart (Garnett et al, 1969; Van Itallie and Yang, 1984). The prolonged fasting period characterized by phase II shows two important features: (1) the overall energy budget is dominated by lipid oxidation regardless of the organism’s natural history, but (2) the relative importance of proteins varies widely among animals, depending on how often and for how long food deprivation normally occurs in each species. Nitrogenous waste products are subsequently excreted as ammonia, urea, uric acid and creatinine. In mammals, prolonged fasting is typically associated with progressively lower rates of urea excretion, partly compensated by a gradual increase in ammonia production (Nørdoy et al, 1990; Owen et al, 1969, 1998). The composition of nitrogenous end products has never been monitored in a hibernator fasting under normothermic conditions

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