Evidence for a facultative mutualism between the navel orangeworm (Amyelois transitella) and Aspergillus flavus

The navel orangeworm (Amyelois transitella) is a major pest of Californian orchard crops, including figs, pomegranates, and most tree nuts. It causes mechanical damage to the fruits and contaminates them with frass and webbing. Moreover, both larvae and adults are associated with the fungal pathogen Aspergillus flavus, a highly toxigenic mold that produces aflatoxin B1 among other compounds and renders crops unsaleable. We present several lines of evidence that these two species make up an economically important pest mutualism. When raised together on almond agar diet, both species experience developmental benefits. The navel orangeworm completes development 33% faster when A. flavus is present in the diet, while the fungus grows 43% faster in the presence of A. transitella. In addition, when incorporated into a semi-defined artificial diet, bergapten and xanthotoxin (furanocoumarins that occur in two of its host plants) reduce the growth rate of A. transitella, but only when the fungus is absent. Through larval behavioral choice assays, we also found that volatiles produced by fungal infection of almonds are attractive to first instar caterpillars. Extracts of A. flavus itself produced no such response, but larvae significantly preferred agar medium containing A. flavus over uninoculated agar in two-choice bioassays. Additionally, these larvae are more attracted to A. flavus growing on agar containing almond meal rather than unaugmented PDA. In light of these multiple lines of evidence, we suggest that Aspergillus flavus and Amyelois transitella are mutualists, a relationship that may influence the design and implementation of pest management strategies.