Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies

Herbivore-damaged plants emit volatile organic compounds that attract natural enemies of the herbivores. This form of indirect plant defence occurs aboveground as well as belowground, but it remains unclear how simultaneous feeding by different herbivores attacking leaves and roots may affect the production of the respective defence signals. We employed a setup that combines trapping of volatile organic signals and simultaneous measurements of the attractiveness of these signals to above and belowground natural enemies. Young maize plants were infested with either the foliar herbivore <i>Spodoptera littoralis</i>, the root herbivore <i>Diabrotica virgifera virgifera</i>, or with both these important pest insects. The parasitic wasp <i>Cotesia marginiventris</i> and the entomopathogenic nematode <i>Heterorhabditis megidis</i> were strongly attracted if their respective host was feeding on a plant, but this attraction was significantly reduced if both herbivores were on a plant. The emission of the principal root attractant was indeed reduced due to double infestation, but this was not evident for the leaf volatiles. The parasitoid showed an ability to learn the differences in odour emissions and increased its response to the odour of a doubly infested plant after experiencing this odour during an encounter with hosts. This first study to measure effects of belowground herbivory on aboveground tritrophic signalling and vice-versa reemphasizes the important role of plants in bridging interactions between spatially distinct components of the ecosystem.