Root‐feeding larvae increase their performance by inducing leaf volatiles that attract above‐ground conspecific adults

Abstract

Abstract Herbivore‐induced changes in plant volatile emissions mediate above–below‐ground interactions by determining host plant colonization of different herbivores. By changing shoot‐emitted volatiles, below‐ground herbivores may use the plant to extend their capacity to interact with above‐ground con‐ and heterospecifics. We investigated the attractiveness of Triadica sebifera plants infested by larvae of a specialist beetle or root‐knot nematodes to above‐ground herbivores. We then determined the contribution of leaf volatiles to the observed recruitment patterns using olfactometer experiments. We also identified volatiles through gas chromatography–mass spectrometry (GC–MS) and electroantennography, and conducted field experiments to confirm their effects. Leaf volatiles induced by the root‐feeding larvae attracted above‐ground conspecific adults in laboratory and field experiments, but repelled a heterospecific specialist weevil, whereas induction by root‐knot nematodes had no effects on either. Greater leaf consumption by conspecific adults increased root nutrients, decreased root defences and facilitated root feeding larval performance. Thus, larvae and adults appear to manipulate their host plant, which increases aggregation above‐ground and feeding below‐ground. Synthesis. The resulting colonization dynamics may shape the composition of plant rhizosphere and phyllosphere herbivore communities by enhancing conspecific establishment and reducing colonization by other herbivores. By modifying above‐ground volatiles and above‐ground herbivore behaviour, root feeders could mediate plant and leaf herbivore interactions and benefit via plant responses to above‐ground feeding.