A fungal endophyte of an annual weed reduces host competitive ability and confers associational protection to wheat

Abstract Epichloid fungal endophytes (Epichloe spp., Ascomycota: Clavicipitaceae) inhabit aerial tissues of several cool-season grasses, and enhance host growth and defence against herbivores. The presence of these symbionts can also affect interactions between the host and other non-epichloid plants. The role of an epichloid endophyte on interspecific competition has been tested on perennial grasses with contrasting results, but it has been scarcely tested using annual species in agroecosystems. We evaluated the impact of Epichloe-grass symbiosis on the competitive interaction between a non-host cereal crop (Triticum aestivum, wheat) and a host weed (Lolium multiflorum, ryegrass), growing in the presence of invertebrate herbivores (aphids) under no resource limitation. We conducted an outdoor mesocosm experiment with wheat plants growing in monoculture or in mixture with low or high proportion of ryegrass plants. Ryegrass plants presented either low (E-) or high (E+) incidence of Epichloe occultans (i.e. frequency of epichloid endophytic plants). We measured wheat vegetative and reproductive yield and its natural aphid infestation. Although epichloid endophyte incidence did not affect ryegrass biomass, wheat reproductive yield in mixtures (relative to wheat monocultures) was 45% higher when grown with E+ ryegrass plants than E- conspecific plants. Aphids preferred wheat plants grown with E- plants rather than wheat plants grown with E+ plants, but only in mixtures with high proportion of ryegrass. Our results demonstrate that epichloid endophyte incidence can decrease host competitive ability and confers associational protection to the non-endophytic neighbouring plants. Thus, ryegrass-endophyte symbiosis can increase crop yield by positive neighbourhood effects through different mechanisms probably related to the density of the weed. The benefits of this endosymbiont cannot be considered host-exclusive since they can be disseminated to non-endophytic plants. Furthermore, our results suggest that the epichloid endophyte incidence on annual weeds can contribute to agroecosystem sustainability by influencing pest management and increasing crop yield.