Collembola grazing on arbuscular mycorrhiza fungi modulates nutrient allocation in plants

Arbuscular mycorrhiza (AM) mycelia networks are important for nutrient allocation in many plants, but fungivorous soil invertebrates such as Collembola can modulate the symbiosis by grazing on the extra-radical mycelium (ERM). This study employs a dual biomarker approach with stable isotopes and fatty acids to disentangle trophic interactions of Collembola in a plant-fungal soil system with maize (Zea mays) and the AM fungus Glomus mosseae. To separate ERM and root mediated effects, root (RC) and hyphal compartments (HC) were used, and the latter was spiked with labeled ¹⁵N substrate. The euedaphic Collembola species Protaphorura fimata was introduced as the fungal and root grazer. Generally, the presence of Collembola in RC fostered biomass and phosphorous uptake in roots colonized with AM. Nitrogen transport from HC to RC was not altered, indicating that Collembola did not disrupt the ERM network via grazing. Collembola–fungus interactions fostered AM hyphal proliferation in HC, whereas in RC it induced a change from fungal senescence with build-up of storage reserves, to an active foraging phase. A distinct diet switch by Collembola between HC and RC indicated different ERM palatability meditated by the presence or absence of the host plant. Overall, Collembola grazing increased ERM nutrient sequestration, particularly phosphorus, and in turn plant performance. Collembola modified fungal phenology, favoring fungal colonization over reproductive phases. These trophic interactions were strongly determined by fungal life stage, with the establishment of a functional mycorrhiza as a crucial factor.