Arbuscular mycorrhizal fungi and belowground herbivores interact to determine plant productivity and performance of subsequently feeding conspecifics by changing plant metabolites

Insect herbivores and arbuscular mycorrhizal fungi (AMF) often occur simultaneously on a host plant, altering plant morphological and biochemical traits and thereby not only affecting each other’s performance, but also plant interactions with subsequent above- or belowground herbivores. Here, we investigate the combined effects of AMF and above- and belowground herbivory on plant productivity and performance of subsequent above- and belowground herbivores. We conducted a 3 × 2 full-factorial experiment with three levels of ‘Herbivory (no herbivory, leaf herbivory, and tuber herbivory) and two levels of ‘AMF inoculation’ (no AMF inoculation and AMF inoculation) in the tuber-plant, potato (Solanum tuberosum). We showed that both AMF and tuber herbivory increased tuber biomass and tuber primary metabolites (protein, starch). Tuber herbivory reduced the performance of subsequent conspecifics feeding on leaves potentially via increased leaf levels of phenolics, α-solanine and α-chaconine. By contrast, it increased the performance of subsequent conspecifics feeding on tubers potentially via increased protein, however, only in plants inoculated with AMF. This indicates that the belowground facilitation among conspecific insects was contingent upon the presence of AMF. Leaf herbivory did not affect subsequent above- or belowground insect performance. These feedings improve our understanding of the ecological consequences of antagonists and mutualists interactions mediated by phytochemistry, especially for agroecosystems.