Bottom-Up and Top-Down Effects of Forest Fragmentation Differ Between Dietary Generalist and Specialist Caterpillars

Abstract

Ecological interactions increasingly occur in the context of anthropogenic landscape alteration, such as landscape fragmentation, which engenders numerous changes to abiotic and biotic processes. Theory and empirical evidence suggest that species that are ecologically specialized or positioned at higher trophic levels are most sensitive to the effects of landscape fragmentation, yet the mechanisms underlying this sensitivity remain hypothetical. Here we present an initial test of the hypothesis that landscape fragmentation affects tri-trophic interactions more severely for dietary specialist than for generalist insect herbivores. We specifically tested a bottom-up hypothesis, that fragmentation reduces hostplant food quality to herbivores, with the most pronounced effects for dietary specialists. We also tested a top-down hypothesis, that fragmentation reduces parasitism of caterpillars, with the most pronounced effects on dietary specialists. We studied interactions among trees, caterpillars, and parasitoids in forest fragments (3-1013 ha) in Connecticut, U.S.A. in 2017 and 2018. To address the bottom-up hypothesis, we measured the growth performance of multiple dietary specialist and generalist caterpillar species fed leaves from red maple and witch hazel trees sampled from large or small forest patches. We assessed the top-down hypothesis by quantifying mortality from insect parasitoids of many of the same caterpillar species on these tree species sampled from a range of forest patch sizes. Fragmentation did not reduce herbivore growth performance for either dietary specialist or generalist caterpillars even though it accelerated desiccation rates of leaves of both tree species over the growing season. However, dietary specialization increased herbivore sensitivity to yearly variation in food quality, as the growth efficiency of specialist caterpillars varied between 2017 and 2018, while that of generalist caterpillars did not. As predicted, parasitism rates of dietary specialist caterpillars declined as forest fragment size declined, whereas parasitism of generalists was independent of fragment size. Therefore, interactions involving dietary specialist herbivores were most sensitive to top-down environmental variation. Assuming that dietary specialist caterpillars are primarily attacked by host-specific parasitoids, this Anderson et al. Effects of Forest Fragmentation on Tri-trophic Interactions top-down effect is consistent with the trophic theory of island biogeography, which predicts the sharpest declines of ecologically specialized predators and parasites in small habitat patches.

Multiscale Determinants Drive Parasitization of Drosophilidae by Hymenopteran Parasitoids in Agricultural Landscapes

“…Tscharntke and Brandl [66] reviewed the relationship of parasitoids' traits with landscape structure and reported that the small body size favors dispersal of parasitoids in woody fragmented areas, while in agricultural area parasitoid richness and diversity dramatically decrease. Moreover, habitat fragmentation has also been shown to negatively affect specialized host-parasitoid associations (e.g., [67]). In our study, neither landscape structure nor composition at larger (500 m radius) or small (100 m) spatial scale had a significant effect on the community of parasitoids.…”

Gypsy moth population outbreak and low host-plant quality amplify a trophic cascade from birds to forest trees

“…Additionally, a key difference between A. rubrum and H. virginiana is that they vary in their food quality to caterpillars. The growth efficiency (mass gained per unit plant material consumed) of dietary generalist caterpillars of several species was higher on H. virginiana than on A. rubrum, and the former had higher water content than the latter (Anderson et al, 2019). Similarly, several focal dietary generalist caterpillar species grew to a larger final size on H. virginiana compared to those reared on A. rubrum (Singer et al, 2012).…”

“…Specifically, I test the indirect effect of bird predation on leaf damage from chewing herbivores, mainly caterpillars. I study trophic cascades on Acer rubrum (red maple) and Hamamelis virginiana (witch hazel), two tree species of contrasting food quality for caterpillars (Anderson et al, 2019). Although it is known that birds initiate trophic cascades in non-outbreak conditions (Mooney et al, 2010;Mantyla et al, 2011;Singer et al, 2014), it is unclear how dramatic increases in the densities of a generalist defoliator will impact this trophic cascade strength.…”

“…Further, it is expected that the per capita consumption by gypsy moths will be greater on A. rubrum than on H. virginiana. Because A. rubrum is a host plant of comparatively lower nutritional quality (Anderson et al, 2019), the gypsy moths that have reached voracious final instars during the population outbreak are expected to compensate by consuming more plant material than those feeding on H. virginiana. Thus, predation of a single gypsy moth caterpillar on A. rubrum during its larval development will save more plant material than predation of a single gypsy moth caterpillar on H. virginiana.…”

“…A. rubrum and H. virginiana were chosen as host plants to study the cascading effect of birds because both harbor many leaf-chewing insect herbivores and were abundant throughout all the field sites used (Futuyma & Gould, 1979, Anderson et al, 2019. Additionally, a key difference between A. rubrum and H. virginiana is that they vary in their food quality to caterpillars.…”