Herbivore‐induced aspen volatiles temporally regulate two different indirect defences in neighbouring plants

Abstract

Summary1. Many plant species have two inducible indirect defences against herbivores, emission of volatile organic compounds (VOCs) and secretion of extrafloral nectar (EFN). Moreover, herbivore‐induced VOCs can serve as airborne signals in plant–plant communication, inducing and/or priming defences in undamaged neighbouring plants. However, it remains largely unknown, particularly in woody plants, whether herbivore‐induced VOCs induce and/or prime these two indirect defences simultaneously.2. We investigated the VOC‐mediated induction and priming of VOC emission and EFN secretion in the woody plant hybrid aspen (Populus tremula × Populus tremuloides) in the context of plant–plant communication. Hybrid aspen saplings were exposed to VOCs released either from herbivore‐infested or uninfested conspecifics and subsequently challenged by herbivores. VOCs and EFN from exposed plants were collected throughout experiments. Additionally, local and systemic EFN induction was investigated.3. Exposure to VOCs from infested plants directly induced secretion of EFN sugars but not emission of volatile terpenes. Upon subsequent herbivore attack, however, plants previously exposed to herbivore‐induced VOCs released significantly more terpenes than unexposed plants, whereas EFN secretion was not increased, indicating that herbivore‐induced VOCs prime VOC emission but not EFN secretion. This switching in the indirect defence priority from induced EFN secretion to primed VOC emission may reflect the potential fitness disadvantages of VOC emission and EFN secretion on their own. In addition, feeding by Epirrita autumnata larvae reduced EFN sugar production both locally and systemically, which disagrees with previous findings and suggests that EFN secretion varies depending on plant and herbivore species.4. Thereby, our work has parallels and divergences from the most significant previous studies. Nevertheless, it suggests that plants can respond differently to early warning signals and ensuing herbivory and in doing so fine‐tune their different indirect defences timely to achieve optimal use of resources.