The significance of metabolic load in the evolution of host specificity in a lepidopteran larva (Manduca sexta).

Abstract

Allelochemicals have been proposed to divert energy from growth to detoxification and provide a selective advantage for herbivores which restrict their detoxification activity to a small number of defensive compounds. Similarly, other food processing costs have been proposed to lower the growth of herbivores on foods of low water content or low protein quality. I investigated the effects of xanthotoxin, canavanine, precocene II, nicotine, and water on the growth and energy metabolism of third instar M. sexta (Lepidoptera: Sphingidae). Two estimates of energy expenditure were examined, rates of respiration and the amount of assimilated food allocated to respiration. I found no evidence that any of the four toxins decreased the growth of M. sexta by imposition of high metabolic costs of detoxification. In no case were rates of respiration higher for larvae on toxin diets. Similarly, in no case were the amounts of food respired higher for larvae on toxin diets independent of increases in instar duration. Both respiration rates and the amount of food respired were higher for larvae on low-water diets. However, water budgets indicate that growth on the low-water diet was not limited by energy but by the availability of water to hydrate new tissue, which in turn mandated a greater metabolic expenditure for water conservation, nitrogen excretion, and maintenance of a longer instar. Thus, the poor nutritive quality of low-water food is primarily a consequence of nutrient limitation and not increased metabolic costs of food processing. I conclude that (1) allelochemicals defend plants against adapted and non-adapted lepidopteran herbivores by their toxic action and by limiting consumption, not by elevating metabolic rates; (2) detoxification carries a very low metabolic cost to lepidopteran herbivores; (3) processing of low-water diets does carry with it an elevated metabolic cost but this metabolic load is not responsible for the reductions in growth; (4) lepidopteran herbivores are not likely to be energy-limited; and (5) the concept of metabolic load is not a useful one in understanding either the effects of plant allelochemicals on insect growth or the evolution of dietary specialization of larval Lepidoptera.