Nutrition interacts with parasitism to influence growth and physiology of the insect Manduca sexta L

Abstract

The influence and interaction of dietary protein:carbohydrate balance and parasitism by Cotesia congregata on nutrient intake and growth were examined over the last two larval stadia of Manduca sexta. Effects of nutritional status on host blood metabolite concentrations were also determined. Six fat-free chemically defined diets were tested, each having the same total level of casein and sucrose, but with casein to sucrose ratios varying from low protein/high carbohydrate to equal levels of both nutrients through to high protein/no carbohydrate. Nutrient ratio and parasitism each affected nutrient consumption and growth. Feeding responses differed between normal and parasitized larvae, as illustrated by nutrient arrays, two-dimensional plots of protein and carbohydrate consumption on diets having different nutrient ratios. Normal larvae consumed more nutrients and took longer to develop as dietary nutrient ratio was displaced from equal levels of both nutrients. Except on the diet having the same amount of protein and carbohydrate, parasitized larvae consumed less nutrients than normal larvae, although on all diets parasitized larvae took longer to develop. When the contribution of parasite biomass was excluded, parasitized larvae showed lower mass gain than normal larvae on all diets. Total mass gain by normal and parasitized larvae with parasite biomass included, however, was similar on diets having intermediate nutrient ratios. Differences in mass gain between diets relative to nutrient consumption were evident from multi-dimensional representations of mass gain with protein and carbohydrate consumption. Three-dimensional plots and contour maps of normal and parasitized larvae were different. When differences in nutrient consumption between diets were taken into account, protein consumption had a greater effect on growth than carbohydrate consumption and normal larvae generally displayed greater mass gain than parasitized larvae on the same diets. Utilization efficiency, the efficiency of conversion of ingested food to body mass, was, therefore, generally reduced in parasitized insects. Concentrations of blood protein, total free amino acids and trehalose were each influenced by dietary nutrient ratio and parasitism. Concentrations of protein and free amino acids generally increased and trehalose concentration decreased as dietary protein increased and carbohydrate decreased. The opposite was the case as dietary carbohydrate increased and protein decreased. Dietary nutrient ratio, however, affected normal and parasitized larvae differently. Parasitized larvae had higher overall trehalose concentrations while normal larvae had higher protein and total free amino acid concentrations. When differences in nutrient consumption between diets were accounted for, protein consumption had a greater effect on blood protein and free amino acid concentrations than did dietary nutrient ratio or parasitism. Protein consumption, however, did not affect trehalose concentration. Carbohydrate consumption had no effect on the concentration of any of the metabolites after differences in nutrient consumption were taken into account. Effects of nutrient consumption on trehalose concentration, therefore, were due to dietary nutrient ratio and parasitism. The potential relevance of the above findings to the biology of parasitized M. sexta larvae is discussed.