Seasonal Changes and Phenotypic Flexibility in the Digestive System of the Hibernating Marsupial Dromiciops gliroides

Abstract

During hibernation, reduced metabolic activity enables to withstand periods of limited resources and harsh weather. Therefore, animals exhibit reduced activity and decreased feeding, which involves energy savings. Thus, a reduction in both physiological and morphological digestive capacities is expected due to the prolonged metabolic depression of hibernation, which involves phenotypic flexibility of the digestive system at several levels. We studied Dromiciops gliroides a heterothermic marsupial endemic of the temperate rainforests of southern South America, by comparing the morphology and physiology of the small intestine between summer (active) and winter (hibernation) seasons. We collected individuals near Valdivia (Chile) in winter (n = 10) and summer (n = 7) using Tomahawk traps, for extracting small intestines, which were then processed for routine histology and biochemistry analysis. We measured disaccharidase activities (sucrase and maltase) as indicators of carbohydrate digestive capacity and N-aminopeptidase activity as an indicator of protein digestion. Our result showed a 32%–44% reduction in disaccharidase activity and 60% reduction in protease activity in torpid animals. Additionally, aminopeptidase-N activity decreased along the proximal-to-distal intestinal axis. In contrast, small intestine weight and villi length remained unchanged between seasons. These findings suggest that gut remodeling occurs in response to seasonal energetic demands, with greater biochemical changes than morphological ones, possibly reflecting the high energetic costs associated with intestinal shrinking and regrowth after hibernation. We conclude that hibernation triggers gut remodeling and phenotypic flexibility in the digestive systems of D. gliroides, representing a crucial mechanism for coping with seasonal environmental conditions.