Root herbivores and detritivores shape above‐ground multitrophic assemblage through plant‐mediated effects

Abstract

1. Indirect effects mediated by changes in plant traits are the main mechanism by which above- and below-ground herbivores affect each other and their enemies. Only recently the role of decomposers in the regulation of such plant-based systems has been considered. We hypothesized that: (i) below-ground organisms, both herbivores (negative effect on plants) and detritivores (positive effect on plants), will have a profound effect on the interactions among above-ground arthropods; (ii) floral herbivores will negatively affect other above-ground herbivores associated with the plant; and (iii) not only above- and below-ground herbivores, but also detritivores will affect the production of secondary metabolites, i.e. glucosinolates, in the plants. 2. We manipulated the presence of above-ground herbivores, below-ground herbivores and below-ground detritivores on the Brassicaceae Moricandia moricandioides in the field to disentangle their individual and combined effects on other organism groups. We also investigated their effects on the plant's chemical defence to evaluate potential mechanisms. 3. Our results show that not only above- and below-ground herbivores, but also detritivores affected other herbivores and parasitoids associated with the host plant. Most effects were not additive because their strength changed when other organisms belonging to different functional groups or food web compartments were present. Moreover, below-ground herbivore and detritivore effects on above-ground fauna were related to changes in glucosinolate concentrations and in quantity of resources. 4. This study indicates that multitrophic interactions in plant-based food webs can dramatically change by the action of below-ground organisms. One of the most important and novel results is that detritivores induced changes in plant metabolites, modifying the quality and attractiveness of plants to herbivores and parasitoids under field conditions.