Costs of Inducible Defense: Protein Limitation, Growth, and Detoxification in Parsnip Webworms

Abstract

Although xanthotoxin, a linear furanocoumarin, is toxic to a wide variety of lepidopterans, the parsnip webworm, Depressaria pastinacella (Lepidoptera: Oecophoridae), is restricted to feeding on only two genera of Apiaceae, both of which contain large quantities of this toxin. The cost of cytochrome P450—mediated detoxification of xanthotoxin by this oligophagous species was examined in two artificial diet experiments. In the first experiment, growth rates, silkspinning rates, and detoxification capacity of larvae were measured after they had consumed diets ranging in protein content from 0 to 100% of the amount required for maximum growth. As protein became progressively more limited, growth rates declined progressively while silkspinning rates and detoxification capacity remained unchanged; only when dietary protein was completely absent did silkspinning rates and xanthotoxin metabolism rates decline. These findings suggest that xanthotoxin detoxification capacity is maintained at the expense of growth. In the second experiment, growth rates, silkspinning rates, and xanthotoxin metabolism were measured in larvae that consumed diets with or without xanthotoxin in the presence or absence of protein. As in the previous experiment, the absence of protein led to significant reductions in growth, silkspinning, and detoxification. The presence of xanthotoxin in the diet resulted in an increase in the rates of xanthotoxin metabolism and silkspinning but did not have any effect on growth rates. Inasmuch as there were no interactions between protein and xanthotoxin treatments, induction of xanthotoxin metabolism by xanthotoxin was not affected by protein limitation. The fact that xanthotoxin metabolism is induced almost threefold in the absence of dietary protein, conditions that result in reduction of growth rates by almost 80%, is also consistent with the greater importance of detoxification capacity relative to growth over the short term. Due to its highly oligophagous habits, the parsnip webworm is unlikely to encounter host plants tissue entirely lacking furanocoumarins; circumstances under which the inability to respond to the presence of xanthotoxin in the diet by increasing rates of its metabolism may never exist. Thus, maintaining high and inducible levels of cytochrome P450—mediated xanthotoxin metabolism may be regarded as one of the costs associated with the highly specialized diet of D. pastinacella.

Dietary mixing in three generalist herbivores: nutrient complementation or toxin dilution?

“…A similar result, reduced growth and ECD with no e ects on consumption and digestibility, was obtained by Lincoln et al (1982) when they incorporated plant resins into arti®cial diets of a given protein composition and fed them to caterpillars of Euphydryas chalcedona (Lepidoptera, Nymphalidae). Berenbaum and Zangerl (1994) also found good evidence for the hypothesis that detoxi®cation of the furanocoumarin xanthotoxin imposes a metabolic load on the parsnip webworm, Depressaria pastinacella (Lepidoptera, Oecophoridae). However, Neal (1987) was unable to ®nd metabolic costs of mixed-function oxidase induction, which is a metabolic system responsible for most detoxi®cation processes.…”

Energetic costs of detoxification systems in herbivores feeding on chemically defended host plants: a correlational study in the grain aphid,Sitobion avenae

“…Appel and Martin (Appel and Martin, 1992) found that Manduca sexta (Lepidoptera) changed neither metabolic rate nor growth variables when it was fed on artificial diets with different concentrations of nicotine. Finally, Berenbaum and Zangerl demonstrated that xanthotoxin induced the expression of detoxification systems in Depressaria pastinacella (Lepidoptera) but did not affect its growth parameters (Berenbaum and Zangerl, 1994). On the other hand, Cresswell et al reported that an artificial diet containing nicotine produced an increase in metabolic rate and a reduction of net growth efficiency in larvae of Spodoptera eridania (Lepidoptera) (Cresswell et al, 1992).…”

Energetic costs of pyrene metabolism in isolated hepatocytes of rainbow trout, Oncorhynchus mykiss

“…Specifically, dietary nicotine (0.5%), a substrate of the polysubstrate monooxygenase detoxification system, was found to have significant negative effects on the weight of food ingested, weight gained, relative growth rate and conversion efficiency of digested food by S. eridania larvae on a nutrient-rich artificial diet. Furthermore, in Berenbaum et al (1994), it was shown that the detoxification of the plant allelochemical xanthotoxin was maintained, at the expense of growth, in the parsnip webworm (Depressaria pastinacella) fed nutrient deficient diets.…”