Feeding rate and the structure of protein digestion and absorption in lepidopteran midguts

The transformation of leaf protein into insect tissue can be distilled grossly into four serial steps: consumption of protein, digestion of protein into small peptides and free amino acids, absorption of these fragments across the gut epithelium, and construction of tissue from the absorbed fragments. We examine these steps in caterpillars, with emphasis on determining which, if any, process is limiting and how digestive events influence-and are influenced by-the rate of consumption. Five competing hypotheses are (1) the steps are matched, (2) consumption is limiting, (3) digestion is limiting, (4) absorption is limiting, and (5) post-absorptive processes are limiting. For conditions appropriate to each of the five hypotheses, we use a chemical reactor model to predict the concentration profiles of protein and protein breakdown products along the midgut. We test the predictions in two ways. First, based on midgut morphology and rates of digesta flow and protein breakdown estimated from in vitro experiments, we calculate the axial concentration profile of protein in the midgut of fifth instar Manduca sexta. This calculation suggests that protein breakdown occurs primarily in the anterior midgut, thus excluding the hypotheses that feeding and digestive processes are matched or that digestion is limiting. In addition, caterpillar feeding responses to reduced concentrations of protein are not consistent with the hypothesis that consumption is limiting. Second, we review published studies that show midgut concentration profiles of protein and breakdown products, one supporting the hypothesis that absorption across the midgut epithelium is limiting and the other suggesting that post-absorptive processes are limiting. Consequently, we interpret compensatory feeding by larval M. sexta as a mechanism for maintaining saturated rates of protein absorption or of tissue construction. Arch. Copyright 1999 Wiley-Liss, Inc.