Sending Mixed Messages: A Trophic Cascade Produced by a Belowground Herbivore-Induced Cue

Abstract

Plants defend themselves against herbivores both directly (chemical toxins and physical barriers) and indirectly (attracting natural enemies of their herbivores). Previous work has shown that plant roots of citrus defend against root herbivores by releasing an herbivore-induced plant volatile (HIPV), pregeijerene (1,5-dimethylcyclodeca-1,5,7-triene), that attracts naturally occurring entomopathogenic nematodes (EPNs) to Diaprepes abbreviatus larvae when applied in the field. However, the soil community is complex and contains a diversity of interspecific relationships that modulate food web assemblages. Herein, we tested the hypothesis that other nematode types beyond EPNs, as well as, nematophagous fungi are affected by the same HIPV that attracts EPNs to herbivore-damaged roots. We employed molecular probes designed to detect and quantify nematodes from the Acrobeloides-group (free-living bacterivorous nematodes, FLBNs), some of which compete with EPNs by 'hyperparasitizing' insect cadavers, and five species of nematophagous fungi (NF), which attack and kill EPNs. In two different agricultural systems (citrus and blueberry), we detected diverse species of nematodes and fungi; however, only the behavior of FLBNs was affected in a manner similar to that reported previously for EPNs. Although detected, NF abundance was not statistically affected by the presence of the belowground HIPV. We provide the first evidence showing subterranean HIPVs behave much the same as those aboveground, attracting not only parasitoids, but also hyperparasites and other food web members.