Structural flexibility of the small intestine and liver of garter snakes in response to feeding and fasting

Abstract

Garter snakes Thamnophis sirtalis parietalis feed frequently but also tolerate extended periods of fasting when food is unavailable. We studied the dynamics, reversibility and repeatability of size changes of the small intestine and liver using ultrasonography. We employed light and transmission electron microscopy and flow cytometry to study the tissue mechanism that drives this flexibility. We compared garter snakes that fed every other day, snakes that fed once a week and fasting snakes. In all feeding trials, the size of the small intestine and the liver increased rapidly after feeding. Constantly feeding snakes maintained an elevated level of organ size, while snakes that were fed only once a week showed a marked up- and downregulation of organ size. Histology revealed the mucosal epithelium to be a transitional epithelium that can change cell configuration considerably to accommodate organ size changes. Upregulation of small intestine and liver size was always associated with the incorporation of lipid droplets into enterocytes and hepatocytes. Cell proliferation was not involved in upregulation of organ size. In contrast, cell proliferation increased during downregulation of organ size, indicating that cells worn out during digestion were replaced. The dynamics of flexibility and the functional features of the tissue were the same as described for the Burmese python Python molurus bivittatus. We suggest that garter snakes employ the same energetically cheap mechanism of organ size regulation as pythons, which allows for rapid, repeated and reversible size changes with no cell proliferation involved. Comparative evidence suggests that the transitional mucosal epithelium is an ancestral character of snakes and that feeding ecology is not directly related to the cytological features of the mucosal epithelium.