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Summary Herbaceous plants harbour species‐rich communities of asymptomatic endophytic fungi. Although some of these endophytes are entomopathogenic, many are not, and remarkably little is known about how the presence of these fungi in plant tissues affects phytophagous insects. Here we show through a meta‐analysis that both entomopathogenic and nonentomopathogenic endophytes have a negative effect on insect herbivores. Growth and performance of polyphagous and sucking insects are reduced by nonentomopathogenic endophytes, but monophages are unaffected, likely because the latter are better adapted to secondary metabolites produced or induced by the fungi. Furthermore, studies using excised leaves report weaker effects than those with intact plants, likely caused by chemical changes being masked by leaf excision. Most surprisingly, endophyte infection of seeds produces the greatest effect on insect herbivores in subsequent mature plants, even though the usual mode of fungal transmission is infection of leaves by airborne spores. We conclude that these ubiquitous hidden fungi may be important bodyguards of plants. However, in order to fully understand their roles in plant protection, we must be aware that minor differences in experimental design can lead to contradictory results.

Fall armyworm (FAW), Spodoptera frugiperda, is a migratory polyphagous pest that causes major damage to economically important cultivated grasses, such as corn. Native to the neotropics in America but recently reported as an invasive pest in Africa and Asia, FAW imposes a serious threat to food security and sustainable crop productivity due to lack of effective management. In this study, the introduction of entomopathogenic fungi as endophytes was explored as an alternative more sustainable management strategy against FAW in corn. The study determined (1) the effect of isolates and inoculation methods on the ability of entomopathogenic fungi to colonize corn plants, and (2) the effect of colonized plants on S. frugiperda survival, development, reproduction, and food preference. Although all tested isolates (twelve of Beauveria bassiana and one each of Metarhizium anisopliae and Metarhizium robertsii) colonized inoculated plants, there was a highly significant interaction between isolates and inoculation methods. Highest plant colonization was obtained by Beauveria bassiana isolate (LPSc 1098) using foliar spray. Endophytic B. bassiana caused significant reductions in larval and pupal survival, length of different developmental stages, total S. frugiperda lifespan, and leaf area consumed by third instar larvae. Plant colonization also significantly reduced female longevity, fecundity, and fertility. This is the first report for the negative effects of endophytic B. bassiana on S. frugiperda growth, reproduction, and food preference. Our results highlight the promising potential of incorporating entomopathogenic fungi as endophytes in integrated pest management practices to protect corn against FAW if their efficacy is also confirmed under field conditions.

1. Fungal endophytes are ubiquitous associates of virtually all plant species. Although many studies have focused on the role of these microorganisms as mediators of plant-herbivore interactions, these studies have usually been conducted using short-term experiments.2. Truly effective defences against herbivores may require normal functioning of the plant, as excised leaves may be less resistant as compared with those still attached to the plant. Yet, most studies investigating possible effects of endophytes in conferring host resistance to herbivores have been conducted with plant parts rather than intact plants.3. Using the root endophytic fungus (Acremonium strictum)-broad bean (Vicia faba)-generalist herbivore (Helicoverpa armigera) model, we conducted experiments to examine whether endophyte effects on herbivory would depend on the experimental setting used in the investigation and whether they would translate into a subsequent generation of the herbivore.4. Acremonium strictum negative effects on the fitness of H . armigera first generation were more evident when the larvae foraged freely on inoculated intact whole plants than when offered leaf discs of inoculated plants. Furthermore, these effects were carried over into H . armigera second generation reared on an artificial diet.5. Acremonium strictum could not be re-isolated from V . faba leaves; hence direct contact between the endophyte and the insect could be excluded. Alternatively, loss of volatiles or inhibitory effects of compounds that were stronger in situ might have caused changes in larval feeding and performance on leaf discs as compared with intact plants, regardless of infection status.6. We suggest that the reduction in fitness parameters of H . armigera across two generations is caused indirectly via an endophyte-triggered reduction in plant quality.

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