Soil community composition drives aboveground plant-herbivore-parasitoid interactions

Soil organisms can influence higher trophic level aboveground organisms, but only very few studies have considered such effects. We manipulated soil community composition of model grassland ecosystems by introducing nematode communities, microorganisms, neither or both groups. Above ground, aphids (Rhopalosiphum padi) and parasitoids (Aphidius colemani) were introduced, and we measured individual performance and population dynamics of plants, aphids and parasitoids. In microcosms with nematode inoculations either with or without microorganism inoculation, aphids offspring production was significantly reduced by 31%. Aphid populations on both host plants Agrostis capillaris and Anthoxanthum odoratum were lowest in microcosms with combined nematode and microorganism inoculations. Opposite results were found for parasitoids. While the number of emerged parasitoids did not differ between treatments, parasitoid mortality and the proportion of males were significantly lower in microcosms with nematode and microorganism inoculations. Parasitized aphids were significantly larger in microcosms with nematodes inoculated. Plant biomass did not differ, but in the preferred host plant A. odoratum, foliar phenolic content was reduced in the presence of nematodes, and also the concentration of amino acids in the phloem. This study shows that the composition of the soil community matters for aboveground multitrophic interactions.