Inherited microbial symbionts increase herbivore abundances and alter arthropod diversity on a native grass

Some microbial symbionts of plants are maternally inherited and thus functionally increase genetic and phenotypic variation within plant populations. This variation, coupled with that of the host plant and environment, may alter abundances, diversity, and trophic structure of associated plant and animal communities. Fungal endophytes in the genus Neotyphodium are vertically transmitted, asexual microbial symbionts of grasses that remain asymptomatic and rely upon their hosts for resources and transmission via seeds, often providing benefits to their hosts, including protection against herbivores. Endophyte infections may influence associated arthropod communities in agronomic grasses, but the long‐term effects of endophytes and variation in host genotype and resource availability on arthropod communities in native grass populations are unknown. We conducted a long‐term field experiment with four maternal genotypes of an infected (E+) native grass (Festuca arizonica) from whence the endophyte was experimentally removed (E−) and water availability was controlled, to test the effects of infection, plant genotype, and resources on abundances, biomass, diversity (richness and evenness), and trophic structure of the arthropod community. Generally, E+ grasses harbored more arthropods, including more herbivores, predators, and detritivores, suggesting that the effects of endophytes cascaded upward through trophic levels in terms of abundances, at least in early ontogeny of the host. That E+ plants harbored more herbivorous insects than E− plants suggests that infection does not increase but instead decreases resistance to herbivores, contrary to prevailing concepts of endophytes as defensive mutualists. Infection did not alter overall species richness of the arthropod community or richness of herbivores but reduced natural enemy richness, especially that of parasites, and increased richness of detritivores. Reduced richness and shifts in evenness of natural enemies on E+ plants suggest that endophytes may disproportionately affect diversity at higher trophic levels and may partially explain increases in abundances of herbivorous insects on E+ plants. Biomass of predators, detritivores, and omnivores increased on plants with supplemented water, and arthropod and herbivore biomass varied by plant genotype. Symbiont‐mediated phenotypic variation interacts with variation from plant genotype and environmental factors to alter arthropod abundances and diversity, and these effects shift with ontogeny of the host.