Root herbivore identity matters in plant-mediated interactions between root and shoot herbivores

Abstract

Summary Plants are simultaneously attacked by a multitude of herbivores that affect plant responses and plant-mediated interactions in a variety of ways. So far, studies on indirect interactions between below- and aboveground herbivores have almost exclusively focused on interactions between only one root and one shoot herbivore species at the same time. Since these studies show a variety of outcomes, we test the hypothesis that root herbivore identity matters in below-/aboveground interactions. We studied the combined effects root-feeding nematodes ( Pratylenchus penetrans ) and wireworms ( Agriotes lineatus larvae) on Plantago lanceolata and on the performance of aboveground phloem-feeding aphids ( Myzus persicae ) and chewing caterpillars ( Chrysodeixis chalcites larvae). Since root herbivores may also affect resource availability and the microbial community in the rhizosphere, we examined resource utilization by soil microorganisms using BIOLOG EcoPlates™. Wireworms decreased root biomass by 13%, but led to compensatory shoot growth. Nematodes and the aboveground herbivores did not affect the biomass of Plantago lanceolata . Feeding by C. chalcites larvae enhanced the concentration of aucubin in leaves, which might explain the high mortality of the caterpillars. Aphids and the belowground herbivores did not change iridoid glycoside levels in the leaves. However, the number of aphid offspring was reduced by 44% when nematodes had been added to the soil, whereas wireworms had no effect. We observed higher utilization of BIOLOG carbon sources by the soil microorganisms only in the presence of Pratylenchus penetrans . Our results suggest that the outcome of below–aboveground interactions highly depends on herbivore identity.