Above‐ and below‐ground organisms can interact by altering the quality of shared host plants. Arbuscular mycorrhizal fungi (AMF) influence plant nutrient uptake, including nitrogen (N) acquisition. Under low N and phosphorus conditions, AMF delivery of N from organic sources not immediately available to the plant can have large impacts on plant N status, a limiting nutrient in the aphid diet. This study investigated the effect of AMF colonisation upon aphid number and determined the consequences of AMF directly accessing an organic nutrient patch that the plant cannot. We hypothesised that AMF colonisation of plants will increase plant and aphid N status, plant performance and aphid number, but only when the AMF had direct access to the added organic patch. Barley plants hosting the grain aphid Sitobion avenae were colonised by the AMF, Funneliformis mosseae, or no AMF. A two‐compartment microcosm was used to separate the plant roots from a 15N‐labelled organic patch in a second compartment. AMF‐colonised plants, but without access to the second compartment, were used to examine the effect of AMF colonisation on aphid number. In a separate treatment, and to determine whether AMF access to a plant inaccessible N source modified the effect of AMF colonisation on aphid number, AMF hyphae were permitted access to the second compartment containing an organic patch. As a control for AMF accessing a larger substrate volume, AMF were allowed access to a second compartment without an organic patch. When the AMF accessed the organic patch, more N from the patch was delivered to the plant resulting in a higher grain N concentration although plant growth was depressed. More N from the patch was also delivered to the aphids, but the N status of the aphid remained unchanged. Regardless of the level of access to the organic patch, AMF colonisation did not affect aphid number. Our data show that by accessing N sources not readily available to plants, AMF can indirectly deliver N to above‐ground organisms, a finding which has major implications for N‐transfer between higher trophic levels. A plain language summary is available for this article.

Arbuscular mycorrhizal fungi (AMF) form symbioses with the roots of most plant species, including cereals. AMF can increase the uptake of nutrients including nitrogen (N) and phosphorus (P), and of silicon (Si) as well as increase host resistance to various stresses. Plants can simultaneously interact with above-ground insect herbivores such as aphids, which can alter the proportion of plant roots colonized by AMF. However, it is unknown if aphids impact the structure of AMF communities colonizing plants or the extent of the extraradical mycelium produced in the soil, both of which can influence the defensive and nutritional benefit a plant derives from the symbiosis. This study investigated the effect of aphids on the plant-AMF interaction in a conventionally managed agricultural system. As plants also interact with other soil fungi, the non-AMF fungal community was also investigated. We hypothesized that aphids would depress plant growth, and reduce intraradical AMF colonization, soil fungal hyphal density and the diversity of AM and non-AM fungal communities. To test the effects of aphids, field plots of barley enclosed with insect proof cages were inoculated with Sitobion avenae or remained uninoculated. AMF specific and total fungal amplicon sequencing assessed root fungal communities 46 days after aphid addition. Aphids did not impact above-ground plant biomass, but did increase the grain N:P ratio. Whilst aphid presence had no impact on AMF intraradical colonization, soil fungal hyphal length density, or AMF community characteristics, there was a trend for the aphid treatment to increase vesicle numbers and the relative abundance of the AMF family Gigasporaceae. Contrary to expectations, the aphid treatment also increased the evenness of the total fungal community. This suggests that aphids can influence soil communities in conventional arable systems, a result that could have implications for multitrophic feedback loops between crop pests and soil organisms across the above-below-ground interface.