The effects of leaf quality on herbivore performance and attack from natural enemies

A diverse array of sublethal plant secondary compounds are commonly found i n the foliage of temperate deciduous trees. These traits are thought to def end a plant in two principal ways, either directly by reducing insect ovipo sition, feeding, reducing insect oviposition, feeding, or biomass gain, or indirectly, through digestive inhibition. Such inhibition is hypothesized t o slow the rate of herbivore development, thereby increasing their suscepti bility to natural enemies (the slow-growth-high-mortality hypothesis). To c larify the defensive role of these compounds, field experiments were conduc ted to examine the relationships among oak leaf quality, herbivore family, and three herbivore performance measures: survivorship, development time, a nd pupal mass, for a bivoltine leaf-tying caterpillar, Psilocorsis quercice lla (Lepidoptera: Oecophoridae). Two experiments, one for each generation o f the insect, were conducted to examine the effects of intraspecific variat ion in leaf chemistry of its host, white oak trees (Quercus alba). In each experiment, full-sib neonate larvae were placed in experimental leaf ties o n high- versus low-quality trees and allowed to feed for 2 weeks under fiel d conditions. To determine the effect of the third trophic level, a portion of each family in each leaf-quality treatment was bagged to prevent attack from natural enemies. This treatment also allowed us to test a prediction of the slow-growth-high-mortality hypothesis, i.e., that development time, as measured for full sibs in the bagged treatment, should be positively cor related with mortality of their full sibs exposed to natural enemies. Low l eaf quality significantly reduced survivorship of the caterpillars in the f irst generation but not the second. The third trophic level decreased survi vorship in both generations. Larval development time was not affected by le af quality in either generation, but varied significantly among insect fami lies in both generations. In turn, larvae from slower-developing families d id not suffer increased predation and parasitism, as predicted by the slow- growth-high mortality hypothesis. In contrast to develop ment time, pupal m ass showed a greater response to intraspecific variation in leaf quality, a lthough the effect was only significant in generation 1. Concentrations of both total phenolics and hydrolyzable tannins in Q. alba foliage appear to be important negative predictors of pupal mass in P. quercicella. In marked contrast to development time, no main family effect was found for pupal ma ss in either experiment; however, significant familyxenvironment interactio ns were found for the effects of the bagging treatment (generation 1) and t he leaf-quality treatment (generation 2). Overall, the first trophic level had a greater influence on pupal mass (a fecundity correlate), while larval development time was determined more by the insect's family (genotype+mate rnal environment). The third trophic level was a consistently strong source of mortality in both experiments, but as a whole did not respond to famili al differences in development time. Thus, from the perspective of P. querci cella, plant quality appears to serve as a defense more through its direct effect on herbivore survivorship and fecundity than through an indirect eff ect on predation via changes in development time.