Plant and soil biodiversity can have significant effects on herbivore resistance mediated by plant metabolites. Here, we disentangled the independent effects of plant diversity and soil legacy on constitutive and herbivore-induced plant metabolomes of three plant species in two complementary microcosm experiments. First, we grew plants in sterile soil with three different plant diversity levels. Second, single plant species were grown on soil with different plant diversity-induced soil legacies. We infested a subset of all plants with Spodoptera exigua larvae, a generalist leaf-chewing herbivore, and assessed foliar and root metabolomes. Neither plant diversity nor soil legacy had significant effects on overall foliar, root, or herbivore-induced metabolome composition. Herbivore-induced metabolomes, however, differed from those of control plants. We also detected 139 significantly regulated metabolites by comparing plants grown in monocultures with conspecifics growing in plant or soil legacy mixtures. Moreover, plant-plant and plant-soil interactions regulated 141 metabolites in herbivore-induced plants. Taken together, plant diversity and soil legacy independently alter the concentration and induction of plant metabolites, thus affecting the plant's defensive capability. This is a first step towards disentangling plant and soil biodiversity effects on herbivore resistance, thereby improving our understanding of the mechanisms that govern ecosystem functioning.

Plant monocultures growing for extended periods face severe losses of productivity. This phenomenon, known as ‘yield decline’, is often caused by the accumulation of above- and belowground plant antagonists. The effectiveness of plant defences against antagonists might help explaining differences in yield decline among species. Using a trait-based approach, we studied the role of 20 physical and chemical defence traits of leaves and fine roots on yield decline of 18-year old monocultures of 27 grassland species. We hypothesized that yield decline is lower for species with high defences, that root defences are better predictors of yield decline than leaf defences, and that in roots, physical defences better predict yield decline than chemical defences, while the reverse is true for leaves. We additionally hypothesized that species increasing the expression of defence traits after long-term monoculture growth would suffer less yield decline. We summarized leaf and fine root defence traits using principal component analysis and analysed the relationship between defence traits mean as a measure of defence strenght and defence traits temporal changes of the most informative components and monoculture yield decline. The only significant predictors of yield decline were the mean and temporal changes of the component related to specific root length and root diameter (e.g. the so called collaboration gradient of the root economics space). The principal component analysis of the remaining traits showed strong trade-offs between defences suggesting that different plant species deploy a variety of strategies to defend themselves. This diversity of strategies could preclude the detection of a generalized correlation between the strength and temporal changes of defence gradients and yield decline. Our results show that yield decline is strongly linked to belowground processes particularly to root traits. Further studies are needed to understand the mechanism driving the effect of the collaboration gradient on yield decline.