The navel orangeworm, Amyelois transitella (Walker), is a polyphagous pest of California nut crops and is responsible for extensive losses in the United States. It directly damages crops by feeding and contaminating nuts with frass and webbing and vectors saprophytic fungi that infect crops. The navel orangeworm is commonly associated with Aspergillus species, including the toxigenic Aspergillus flavus, which causes crop loss by producing carcinogens, including aflatoxin B1. This lepidopteran-fungus association is the most economically serious pest complex in Central Valley orchards, and evidence indicates that this relationship is mutualistic. We assessed preference and performance of navel orangeworm larvae associated with A. flavus in behavioral bioassays in which neonates were allowed to orient within arenas to media with or without fungal tissue, and performance bioassays in which larvae were reared with and without A. flavus on potato dextrose agar (PDA) and a semidefined almond PDA diet to evaluate effects on development and pupal weight. Navel orangeworm larvae were attracted to A. flavus and developed faster in its presence, indicating a nutritional benefit to the caterpillars. Larvae reached pupation ∼33% faster on diet containing A. flavus, and pupal weights were ∼18% higher for males and ∼13% higher for females on this diet. Our findings indicate that A. flavus plays an important role in larval orientation and development on infected hosts. The preference-performance relationship between navel orangeworms and Aspergillus flavus is consistent with a facultative mutualism that has broad implications for pest management efforts and basic understanding of Lepidoptera-plant interactions.

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The navel orangeworm Amyelois transitella (Walker, 1863, Lepidoptera: Pyralidae), a pest of California tree nuts, is associated with the fungus Aspergillus flavus, and previous research suggests these species are facultative mutualists. Because navel orangeworm larvae exhibit improved performance on diets containing this fungus, orientation toward hostplants infected with A. flavus may be adaptive. We conducted behavioral assays to determine if larvae respond to chemical cues produced by almond hull split and fungal infection. In petri dish arenas, larvae showed a preference for 1-octen-3-ol and 2-phenylethanol, volatiles characteristic of damaged plants, as well as methanolic extracts of almond meal with 1-octen-3-ol and the fungal volatile conophthorin. In contrast, larvae displayed aversion to ethyl benzoate, an inhibitor of fungal growth. When we assessed oviposition behavior relative to substrates with and without A. flavus, females laid almost twice as many eggs near inoculated surfaces. Moreover, an average of 63% of eggs laid near inoculated substrates were fertilized, compared with 24% of eggs near uninoculated sites. We also tested the hypothesis that unfertilized eggs are laid on nutrient-poor substrates to provide supplemental nutrition for larvae in an assay comparing larval survivorship in the presence and absence of unfertilized eggs. Neonates given eggs survived 2.5 times longer on an average than unprovisioned neonates (208.8 h vs. 85.2 h), indicating that this species may compensate with cannibalism for oviposition on lower-quality food sources. We conclude that larvae orient to probable host plant and fungal volatiles associated with hull split and document a possible strategy for larvae to establish on low-quality hosts.

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