Nutrition interacts with parasitism to influence growth and physiology of the insectManduca sextaL.

Abstract

SUMMARY 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.

Host nutrition determines blood nutrient composition and mediates parasite developmental success:Manduca sextaL. parasitized byCotesia congregata(Say)

“…The relationships between blood protein nitrogen and trehalose levels in normal and parasitized M. sexta larvae on the various diets are strikingly similar to the nutrient intake arrays demonstrating the relationships between protein and carbohydrate consumption (Thompson et al, 2005). Alterations of nutrient intake as a result of parasitism, therefore, may be an adaptive strategy by C. congregata, where resultant blood metabolite levels are closest to optimal for supporting parasite growth and development on specific diets.…”

“…Insect culture Stock colonies of Manduca sexta L. were reared on a semidefined wheat germ-based artificial diet as previously outlined (Thompson et al, 2005). Larvae used in the experiments were reared on the rearing diet until completion of the third stadium.…”

“…Previously, we reported the effects of dietary nutrient ratio and parasitism on equilibrium blood concentrations (mg·ml -1 ) of protein, total free amino acids and trehalose in normal and parasitized M. sexta larvae (Thompson et al, 2005). Here, we use those data to estimate the total quantities or levels of these metabolites in the blood of normal and parasitized larvae based on their final mass and water content, assuming 50% extracellular water (Chapman, 1998).…”

“…For normal THE JOURNAL OF EXPERIMENTAL BIOLOGY unparasitized larvae, total blood trehalose decreased as the dietary level of sucrose decreased, with the exception of the 0.125C:1.875S diet. This diet was previously judged 'pathological' (Raubenheimer and Simpson, 1999) based on earlier findings that normal host larvae fail to adjust consumption in response to the poor nutrient balance of this diet (Thompson et al, 2005). In contrast, with parasitized larvae total blood trehalose increased as dietary level of sucrose decreased reaching a maximum on the 1.0C:1.0S diet, thereafter decreasing with further decreases in dietary carbohydrate.…”

“…Recent studies establish that dietary nutrient balance influences growth and development of Manduca sexta over the last two larval stadia (Thompson et al, 2005). Feeding and nutrient intake differ markedly between normal and parasitized larvae and depend on the ratio of digestible protein and carbohydrate.…”