Direct and indirect effects of light environment generate ecological trade-offs in herbivore performance and parasitism

A variety of ecological factors influence host use by parasitoids, including both abiotic and biotic factors. Light environment is one important abiotic parameter that differs among habitats and influences a suite of plant nutritional and resistance traits that in turn affect herbivore performance. However, the extent to which these bottom-up effects "cascade up" to affect higher trophic levels and the relative importance of direct and indirect effects of sunlight on tritrophic interactions are unclear. The objective of this study was to test how light environment (light gap vs. shaded forest understory) and leaf type (sun vs. shade leaves) affect the performance and incidence of parasitism of two species of moth larvae, Euclea delphinii and Acharia stimulea (Limacodidae). We manipulated the leaf phenotype of potted white oak saplings by growing them in either full sun or full shade throughout leaf expansion to produce sun and shade leaves, respectively. These saplings were then placed in light gap and adjacent shaded understory habitats in the forest in a full-factorial design, and stocked with sentinel larvae that were exposed to parasitism ("exposed" experiments). We reared additional larvae in sleeve cages (protected from parasitism) to isolate light environment and leaf phenotype treatment effects on larval performance in the absence of enemies ("bagged" experiments). In the exposed experiments, light environment strongly affected the likelihood of parasitism, while leaf phenotype did not. Euclea delphinii larvae were up to 6.6 times more likely to be parasitized in light gaps than in shaded understory habitats. This pattern was consistent for both tachinid fly and wasp parasitoids across two separate experiments. However, the larval performance of both species in the bagged experiments was maximized in the shade-habitat/sun-leaf treatment, a habitat/leaf-type combination that occurs infrequently in nature. Taken together, our results suggest that the direct effects of light environment on the incidence of parasitism supersede any indirect effects resulting from altered leaf quality and reveal inherent ecological trade-offs for herbivores confronted with choosing between sunny (high leaf quality, harsh environment, high parasitism) and shaded (reduced leaf quality less harsh environment, reduced parasitism) habitats.