Facultative mutualism between navel orangeworm (Amyelois transitella) and Aspergillus flavus and its effects on commercial orchards

The highly toxigenic fungal species Aspergillus flavus is closely associated with the navel orangeworm, Amyelois transitella Walker, which attacks damaged or overripe tree nuts and fruits. Recent work suggests that this association is a facultative mutualism; A. flavus opportunistically infects nuts damaged by navel orangeworm, for example, and may be phoretic on mobile life stages of the insect. We now provide evidence of a nutritional component of this apparent mutualism, in which A. flavus detoxifies phytochemicals in host plants and increases the quality of the caterpillar's diet, while A. transitella provides additional nitrogen-rich substrate (in the form of frass) for A. flavus. Growth rates for A. transitella and A. flavus were measured separately and together on a diet containing almond meal, in the presence and absence of the furanocoumarin xanthotoxin (which occurs in some fruit hosts of A. transitella). In the absence of xanthotoxin, each species grows faster in the presence of the other than they do in isolation. A. transitella reaches adulthood 33% more quickly in the presence of A. flavus, while the fungus covers its medium 43% faster in the presence of A. transitella. In addition, xanthotoxin in the diet reduces the growth rate of A. transitella, but only when the fungus is absent. These data are indicative of an ectosymbiotic mutualism between the fungus and the lepidopteran, an ecological relationship that may be more widespread than hitherto suspected and that has important implications for management of A. transitella in almonds and other economically important host plants.