Evidence that Treehoppers Induce Susceptibility of Oak Trees to Dietary Generalist Caterpillars

<p>Theory on the evolutionary ecology of plant-herbivore interactions is predominantly based on studies of these interactions in isolation from the rest of the ecological community. Yet in real ecosystems, plants are often attacked by multiple species and guilds of herbivores. This reality influences the predictions of plant defense theory, as plants' inducible resistance traits consist of defense mechanisms that target specific feeding guilds that are attacking them. The induction of anti-herbivore resistance traits is limited by antagonistic crosstalk between two phylogenetically conserved biochemical pathways mediated by the phytohormones salicyclic acid (SA) and jasmonic acid (JA), respectively. The induction of SA-mediated plant resistance by phloem-feeding herbivores has been shown to inhibit JA-mediated inducible resistance against leaf-chewing herbivores, a phenomenon called ‘induced susceptibility’. The existence and broader effects of induced susceptibility in ecological communities are virtually unstudied. To address this gap, we study the possibility that phloem-feeding herbivores induce susceptibility to leaf-chewing herbivores in Connecticut forests. We hypothesize that induced susceptibility will benefit dietary generalist leaf-chewers more than dietary specialist leaf-chewers because the latter are expected to possess specific counteradaptations to plant resistance traits. We test this induced susceptibility hypothesis for white oak (<em>Quercus alba</em>) and its community of insect herbivores because white oak is frequently co-colonized by the phloem-feeding guild, which largely consists of dietary specialist treehoppers (Membracidae), and the leaf-chewing guild, which consists largely of caterpillars (Lepidoptera) that range widely in dietary specialization. We compared community structure and the growth performance of dietary generalist and specialist caterpillars that fed on white oak leaves that were experimentally manipulated by 1) treehopper removal, 2) JA addition, and 3) inactivation of tannin chemical defenses. Dietary generalist caterpillars were more abundant on branches that were also hosting sap-sucking treehoppers, whereas dietary specialist caterpillars were less abundant. Assays of caterpillar growth showed that treehopper colonization of oak branches increased the growth performance of dietary generalist caterpillars, and this growth benefit was removed by JA addition to experimental branches. In contrast, JA addition did not reduce the growth performance of dietary specialist caterpillars. Experimental inactivation of tannin defenses benefited dietary generalist caterpillar growth, but not that of dietary specialists. Evidence from this study suggests that treehoppers induce localized inhibition in leaf tannin production, thereby inducing susceptibility of white oak to dietary generalist caterpillars.</p>