A manipulative field study was carried out to determine whether the foliar endophyte fungus, Phialocephala scopiformis DAOM 229536, decreased the performance of eastern spruce budworm, Choristoneura fumiferana larvae developing on white spruce trees. Overwintered second-instar budworm larvae from a laboratory colony or from a wild population were placed on endophyte positive or negative trees one or two weeks before budburst. The presence of the endophyte in the needles reduced the survival of C. fumiferana from both a wild population and a laboratory colony. Survival for budworm juveniles up to pupation and to adult emergence was 13% and 17% lower, respectively, on endophyte positive trees. The endophyte did not influence the size or sex of survivors and budworm survival was not influenced by any two- or three-way interactions. Budworm survival was higher for wild than for laboratory-reared budworm and for budworm placed on trees a week before budburst. This may be the first field study to demonstrate the efficacy of an endophytic fungus against wild individuals of a major forest insect pest. The efficacy of the endophyte at low larval densities suggests that it could be a useful tactic to limit spruce budworm population growth in the context of an early intervention strategy.

Insect herbivore diet mediates interactions with entomopathogens, yet this is relatively unexplored for microsporidia. Here, we examine a diet‐mediated tri‐trophic interaction between an outbreaking forest defoliator, forest tent caterpillar (FTC) Malacosoma disstria Hübner and Nosema sp. microsporidia. We conducted two experiments where diet quality was manipulated by incorporating lyophilized aspen ( Populus tremuloides Michaux) foliage into an artificial diet, which was compared to a standard artificial diet. Diet quantity varied between fully fed and partially starved conditions, simulating an outbreak scenario. Microsporidia infection occurred naturally or was induced via experimental inoculation. We assessed FTC survival, microsporidia infection and load, and sublethal effects of treatments on FTC traits. Plant secondary metabolite concentrations in aspen‐augmented diets varied between experiments. In Experiment 1, the aspen‐augmented diet contained lyophilized aspen foliage with low concentrations of secondary metabolites, which increased FTC survival and reduced microsporidia infection. Diet quality and infection load also interactively influenced adult wing traits in Experiment 1. In Experiment 2, the aspen‐augmented diet contained lyophilized aspen foliage with higher concentrations of secondary metabolites, which negatively affected FTC. No diet‐mediated interactions with microsporidia were observed in Experiment 2. Diet quality (Experiments 1 and 2), diet quantity (Experiment 2) and microsporidia infection (Experiments 1 and 2) directly influenced FTC survival and/or had sublethal effects on FTC that may have cascading effects on population dynamics and dispersal. We demonstrated that diet quality can mediate interactions between FTC and microsporidia, but these interactions depend on the defensive chemistry of the FTC diet. To our knowledge, this is the first study to report diet‐mediated interactions between an outbreaking forest pest and microsporidia and one of only a few studies to examine this tri‐trophic interaction among Lepidoptera.