Organ sizes and energetics in marmots

The size of organs, particularly those organs involved in the processing of nutrients, in adult animals is not constant but flexibly adjusted to changing energy demands. For instance, organs of the gastrointestinal tract shrink prior to long-distance flights in migratory birds, and are enlarged during lactation in mammals. It has been suggested that the size of organs limits long-term energy turnover in mammals and birds, and that a penalty for maintaining large, energetically costly tissues is an increased basal metabolic rate (BMR). Results of studies addressing this interrelation are equivocal, however, and sometimes failed to identify a link between the size of any particular tissue and metabolic rate. Also, no studies have hitherto come up with detailed budgets of energy gains and losses of such organ changes. We suggest that an ideal animal model in which to address these questions are herbivorous hibernators, such as the Alpine marmot (Marmota marmota). During their seven month hibernation period, marmots do not feed but live on body energy reserves only, and food availability is still limited in spring. We found in a preliminary study that marmots show enormous reductions in the size of alimentary organs over winter. We propose to measure not only organ size, but also BMR (using indirect calorimetry), and daily energy expenditure (by means of the doubly labeled water method) in marmots that are shot routinely within a population control program in their natural alpine habitat in Switzerland. The major goals of this project are threefold: (1) To identify possible relations organ size, BMR, and daily energy expenditure (2) To assess the impact of organ size changes on yearly energy budgets. (3) To investigate mechanisms involved in organ size regulation by analyzing the relation between changes in tissue weight and food intake/composition. The results of this project could significantly contribute to our understanding of the determinants and limits of energy turnover in mammals in general, and the specific seasonal adaptation of energy budgets in hibernators. Furthermore, the questions addressed here have relevance for biomass production (e.g., energy allocation in growing livestock), as well as for clinical applications (hypertrophy of organs, tissue repair) or sports medicine (physiological limits to training regimes).

The size of organs, particularly those organs involved in the processing of nutrients, in adult animals is not constant but flexibly adjusted to changing energy demands. We found that in alpine marmots (Marmota marmota), which are herbivorous animals that do not take up any food during their seven months hibernation season, organs of the gastrointestinal tract shrink to approximately half their size over winter. This is among the largest changes in organ size observed in vertebrates so far. Alimentary organs such as liver and kidneys were also reduced in size by about 30%, but other tissues, such as heart, brain, lungs and skeletal muscle remained unchanged. This points to a differential regulation of organ sizes, and tissues that have important functions during the intermittent phases of warm-ups from the hibernating state, or for activity and foraging immediately after emergence from hibernation are maintained despite their clearly lowered overall use over winter. Reductions of the small intestine, stomach, and other parts of the gastrointestinal tract had strong effects on the energetic costs for maintenance, i.e. basal metabolic rate. By reducing their gastrointestinal tract, marmots lower the basal energy expenditure in spring by approximately 20 %, during a critical time of the year when hibernation must be terminated in order to reproduce timely, but food in the alpine habitat is still scarce. Also, we found that organ size reduction will significantly contribute to energy savings during the hibernation season itself, because in addition to lowering tissue maintenance costs, this strategy also lowers the amount of tissue to be heated (from approximately +3 C to +36 C) during each warm-up from hibernation which in marmots occur every 12 days during winter. Interestingly, the costs of seasonal organ adjustments, which are due to organ re-growth over summer, turn out to be small, and constitute only about 0.5% of the total daily energy expenditure. Thus, our study clearly demonstrates a link between organ size and basal metabolic rate, a relation that has sometimes been disputed based on previous studies with different animal models. The adjustment of tissue sizes apparently is an integral component of seasonal adaptation in hibernators, and probably in many seasonal mammals. We believe that seasonal phenotypic plasticity "inside the body" may have been underestimated in the past and further research in that direction could become relevant for meat production as well as for clinical applications (hypertrophy of organs, tissue repair) or sports medicine.