Metabolic and digestive response to food ingestion in a binge-feeding lizard, the Gila monster (Heloderma suspectum)

Abstract

The gastrointestinal tract possesses the capacity to change in form and function in response to fasting and feeding. Such plasticity can be dramatic for species that naturally experience long episodes of fasting between large meals (e.g. sit-and-wait foraging snakes, estivating anurans). By contrast, for active foraging species that feed more frequently on smaller meals, gastrointestinal responses are more modest in magnitude. The Gila monster Heloderma suspectum is an active foraging lizard that feeds infrequently on meals weighing up to one-third of its body mass. Additionally, Gila monsters possess a species-specific salivary peptide, exendin-4, which may be involved in the regulation of metabolic and digestive performance. To investigate the adaptive postprandial response of Gila monsters and the potential regulatory role of exendin-4, we measured metabolic and intestinal responses to feeding in the presence or absence of circulating exendin-4. Following the consumption of rodent or egg meals equivalent to 10% of lizard body mass, metabolic rates peaked at 4.0- to 4.9-fold of standard metabolic rates and remained elevated for 5-6 days. Specific dynamic action of these meals (43-60 kJ) was 13-18% of total meal energy. Feeding triggered significant increases in mucosal mass, enterocyte width and volume, and the upregulation of D-glucose uptake rates and aminopeptidase-N activity. Total intestinal uptake capacity for L-leucine, L-proline and D-glucose were significantly elevated within 1-3 days after feeding. Whereas the absence of circulating exendin-4 had no impact on postprandial metabolism or the postprandial response of intestinal structure and nutrient uptake, it significantly increased intestinal aminopeptidase-N activity. Within the continuum of physiological responses to feeding and fasting, Gila monsters occupy an intermediate position in experiencing moderate, though significant, regulation of intestinal performance with feeding.