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Two invasive herbivores on a shared host: patterns and consequences of phytohormone induction

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Abstract

Herbivore-induced changes in host quality mediate indirect interactions between herbivores. The nature of these indirect interactions can vary depending on the identity of herbivores involved, species-specific induction of defense-signaling pathways, and sequence of attack. However, our understanding of the role of these signaling pathways in the success of multiple exotic herbivores is less known. Eastern hemlock (Tsuga canadensis) is attacked by two invasive herbivores [elongate hemlock scale (EHS; Fiorinia externa) and hemlock woolly adelgid (HWA; Adelges tsugae)] throughout much of its range, but prior attack by EHS is known to deter HWA. The potential role of phytohormones in this interaction is poorly understood. We measured endogenous levels of phytohormones in eastern hemlock in response to attack by these invasive herbivores. We also used exogenous application of methyl jasmonate (MJ) and acibenzolar-S-methyl (ASM), a salicylic acid (SA) pathway elicitor, to test the hypothesis that defense-signaling phytohormones typically induced by herbivores could deter HWA. Resistance to adelgid attack was assessed using a behavioral assay. Adelgid feeding significantly elevated both abscisic acid (ABA) and SA in local tissues, while EHS feeding had no detectable effect on either phytohormone. HWA progrediens and sistens crawlers preferred to settle on ASM-treated foliage. In contrast, HWA crawlers actively avoided settlement on MJ-treated foliage. We suggest that induction of ABA- and SA-signaling pathways, in concert with defense-signaling interference, may aid HWA invasion success, and that defense-signaling interference, induced by exotic competitors, may mediate resistance of native hosts.

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Acknowledgements

We are especially grateful to K. Boroczky, A. Agrawal, and the Chemical Ecology Core Facility at Cornell University for assistance with analyses of phytohormones. We also thank P. Candelas and K. Pieper for laboratory and field assistance, and C. Blubaugh, C. Rigsby, R. Schweiger, and two anonymous reviewers for helpful comments on an earlier draft of this manuscript. This project was funded by the National Science Foundation, grants NSF-DEB 1256826 to CMO and NSF-DEB 1256769 to ELP and CST. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation.

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Contributions

RNS, CST, ELP, and CMO conceived and designed the experiments, RNS and ZW performed the experiments, and RNS analyzed data and wrote the first draft of the manuscript. All authors contributed to revisions.

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Correspondence to Robert N. Schaeffer.

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Communicated by Evan H. DeLucia.

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Schaeffer, R.N., Wang, Z., Thornber, C.S. et al. Two invasive herbivores on a shared host: patterns and consequences of phytohormone induction. Oecologia 186, 973–982 (2018). https://doi.org/10.1007/s00442-018-4063-0

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  • DOI: https://doi.org/10.1007/s00442-018-4063-0

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