Influence of genetic variation in the fungal endophyte of a grass on an herbivore and its parasitoid

Neotyphodium coenophialum (Glenn, Bacon, Price & Hanlin) (Ascomycota: Clavicipitaceae) is an endophytic fungus that lives symbiotically within grasses and produces alkaloids that can help protect its hosts from some insect pests. We used laboratory-based experiments to investigate whether fungal genotype influences an herbivore and its parasitoid. We tested whether variation in novel isolates, plus a control lacking fungal infection, affected preference by fall armyworm, Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae: Amphipyrini), and growth and survival of Euplectrus comstockii Howard (Hymenoptera: Eulophidae: Euplectrini), a parasitoid of fall armyworm. Caterpillars preferred leaf blades in choice experiments from uninfected tall fescue [Lolium arundinaceum (Schreb.) Darbysh., cultivar Jesup (Poaceae)] and tended to avoid blades from plants containing fungal isolates AR502, AR542, or the most common strain from pastures in Georgia, USA, in tall fescue. However, caterpillars fed as much on leaf blades from plants containing isolate AR502 as from those lacking infection. Parasitoid pupal mass was not influenced by fungal isolate, yet fungal isolate did influence parasitoid survival. Survival was higher than expected for parasitoids reared from hosts fed plants lacking fungal infection, but was lower than expected for those reared from hosts fed plants infected with the common strain or AR542 isolates. In contrast, parasitoids reared from hosts fed plants infected with isolate AR502 did not experience higher mortality than expected by chance. Our results show that N. coenophialum can modify bottom-up trophic cascades through direct effects on herbivores, as well as indirect effects on a natural enemy of the herbivores and that the fungus may influence the tritrophic interaction in ways that counterbalance herbivore protection provided by the symbiont. Our work also shows that these effects are influenced by fungal genotype. As attempts are made to produce forage cultivars with strains of fungal endophyte that lack negative influences on livestock, it will be prudent for investigators to assess the multi-trophic effects of these novel associations within agroecosystems.