Impact of chronic stylet-feeder infestation on folivore-induced signaling and defenses in a conifer

Our understanding of how conifers respond biochemically to multiple simultaneous herbivore attacks is lacking. Eastern hemlock (Tsuga canadensis; 'hemlock') is fed on by hemlock woolly adelgid (Adelges tsugae; 'adelgid') and by later-instar gypsy moth (Lymantria dispar; 'gypsy moth') caterpillars. The adelgid is a stylet-feeding insect that causes a salicylic acid (SA)-linked response in hemlock, and gypsy moth larvae are folivores that presumably cause a jasmonic acid (JA)-linked response. This system presents an opportunity to study how invasive herbivore-herbivore interactions mediated through host biochemical responses. We used a factorial field experiment to challenge chronically adelgid-infested hemlocks with gypsy moth caterpillars. We quantified 17 phytohormones, 26 phenolic and terpene metabolites, and proanthocyanidin, cell wall-bound (CW-bound) phenolic, and lignin contents. Foliage infested with adelgid only accumulated gibberellins and SA; foliage challenged by gypsy moth only accumulated JA phytohormones. Gypsy moth folivory on adelgid-infested foliage reduced the accumulation of JA phytohormones and increased the SA levels. Both herbivores increased CW-bound phenolics and gypsy moth increased lignin content when feeding alone but not when feeding on adelgid-infested foliage. Our study illustrates the importance of understanding the biochemical mechanisms and signaling antagonism underlying tree responses to multiple stresses and of disentangling local and systemic stress signaling in trees.

Automated summary

Our study investigated the biochemical responses of Eastern hemlock trees to herbivore attacks, specifically by hemlock woolly adelgid and later-instar gypsy moth caterpillars. We found that foliage infested with only adelgid accumulated gibberellins and SA, while foliage challenged by only gypsy moth accumulated JA phytohormones. When gypsy moth caterpillars fed on adelgid-infested foliage, they reduced the accumulation of JA phytohormones and increased the SA levels. Both herbivores increased CW-bound phenolics, and gypsy moth also increased lignin content when feeding alone but not when feeding on adelgid-infested foliage. This highlights the importance of understanding tree responses to multiple stresses and signaling antagonism.