Evidence that the sap-feeding guild induces susceptibility of oak trees to dietary generalist caterpillars

Background/Question/Methods To understand plant-insect interactions at a community level, it necessary to study how population interactions between herbivores in coexisting feeding guilds are mediated through plant traits, such as induced defenses. Based on studies of model plant systems, it appears that phloem-feeders primarily induce the salicylic acid (SA) defensive pathway in plants, which inhibits the jasmonic acid (JA) defensive pathway induced by chewing herbivores. This paradigm of induced susceptibility has not been tested in more complex communities or with respect to dietary specialization of chewing herbivores. Here we test the hypothesis that phloem-feeders induce susceptibility to herbivory by chewing herbivores, especially dietary generalists, in a forest community. We studied the insect herbivore community interacting with white oak (Quercus alba) in Connecticut, USA. White oak hosts both phloem-feeding and chewing herbivores, the latter inducing phenolic compounds, such as hydrolyzable tannins, in leaves. We employed field observations of associations between phloem-feeders and dietary generalist and specialist caterpillars, experiments analyzing leaf phenolics and growth performance of caterpillars on leaves manipulated in the field by phloem-feeder removal and JA application, and growth performance of caterpillars on leaves manipulated by JA application and phenolic inactivation with polyethylene glycol (PEG).

Results/Conclusions Field observations supported the induced susceptibility hypothesis in showing that dietary generalist caterpillars were more abundant and dietary specialist caterpillars less abundant in association with phloem-feeders on white oak. Chemical analysis of leaf phenolics found a reduction in putatively induced phenolic compounds in leaves from branches occupied by phloem-feeders relative to leaves from phloem-feeder-removal and JA-treated branches. Growth of dietary generalist caterpillars increased on leaves from branches occupied by phloem-feeders relative to growth on leaves from phloem-feeder-removal, but JA-application reversed this pattern. In the absence of phloem-feeders, dietary generalist caterpillars grew larger when phenolics were experimentally inactivated with PEG and grew smaller when JA was applied to leaves. Growth of dietary specialist caterpillars was not significantly affected by phloem-feeder removal or inactivation of phenolics with PEG. JA application increased the growth of an oak-specialist caterpillar species, but had no effect on two other specialists. These experimental results are mostly consistent with the induced susceptibility hypothesis in this community, but further experiments are needed. Our findings suggest that the occurrence of the phloem-feeding guild could be an important source of variation in the community structure of the leaf-chewing guild on trees.