Atmospheric nitrogen deposition and anthropogenic land use linked to changing fungal endophyte prevalence in cool-season grasses

Background and AimsAnthropogenic global change is altering the environmental stressors facing plants and their microbial symbionts. Changes in drought and temperature have received wide attention, but how other pervasive human impacts - land conversion for agricultural development and urbanization, and changes in nutrient conditions and pollutants - impact plant- microbe symbioses is relatively unknown. Here, we investigated how these anthropogenic global change drivers influence historic changes in the prevalence of widespread symbionts of grasses, Epichloe fungal endophytes. MethodsWe examined 8,739 seeds from 1,951 herbarium specimens collected between 1895 and 2019 for the presence of seed-transmitted Epichloe fungal endophytes in three grass host species (Agrostis hyemalis, Agrostis perennans, and Elymus virginicus). We hypothesized that the symbiosis provides fitness benefits under anthropogenic stresses (i.e. increased nitrogen deposition and land use change) that should translate to increased prevalence of the interaction among specimens exposed to those stresses. Key ResultsAnthropogenic stresses had contrasting effects on endophyte prevalence. Notably, among Agrostis host species, high nitrogen deposition was associated with high endophyte prevalence and with increasing trends in prevalence through time. We also found that highly urbanized landscapes were associated with reduced prevalence and negative temporal trends in endophyte prevalence across species. We also identified a weak positive relationship between agricultural land cover and average endophyte prevalence for Elymus virginicus, though temporal trends in prevalence did not differ between high and low levels of agricultural land cover. ConclusionsAnthropogenic stressors influenced endophyte prevalence in diverse ways. While we found increasing prevalence in the face of nitrogen deposition, a sign of the potential resilience of the symbiosis, urban land cover was associated with declining endophyte prevalence, a sign that anthropogenic activity may contribute to a breakdown of the symbiosis.