Diversity and abundance of phyllosphere bacteria are linked to insect herbivory

Simultaneous or sequential attack by herbivores and microbes is common in plants. Many seed plants exhibit a defence trade-off against chewing herbivorous insects and leaf-colonizing ('phyllosphere') bacteria, which arises from cross-talk between the phytohormones jasmonic acid (JA, induced by many herbivores) and salicylic acid (SA, induced by many bacteria). This cross-talk may promote reciprocal susceptibility in plants between phyllosphere bacteria and insect herbivores. In a population of native bittercress (Cardamine cordifolia, Brassicaceae), we tested whether simulating prior damage with JA or SA treatment induced resistance or susceptibility (respectively) to chewing herbivores. In parallel, we conducted culture-dependent surveys of phyllosphere bacteria to test the hypothesis that damage by chewing herbivores correlates positively with bacterial abundance in leaves. Finally, we tested whether bacterial infection induced susceptibility to herbivory by a major chewing herbivore of bittercress, Scaptomyza nigrita (Drosophilidae). Overall, our results suggest that reciprocal susceptibility to herbivory and microbial attack occurs in bittercress. We found that JA treatment reduced and SA treatment increased S. nigrita herbivory in bittercress in the field. Bacterial abundance was higher in herbivore-damaged vs. undamaged leaves (especially Pseudomonas syringae). However, Pedobacter spp. and Pseudomonas fluorescens infections were negatively associated with herbivory. Experimental Pseudomonas spp. infections increased S. nigrita herbivory in bittercress. Thus, plant defence signalling trade-offs can have important ecological consequences in nature that may be reflected in a positive correlation between herbivory and phyllosphere bacterial abundance and diversity. Importantly, the strength and direction of this association varies within and among prevalent bacterial groups.