The effects of contact exposure to azole fungicides on insect metamorphosis

Abstract External stressors often cause delayed post-exposure effects by affecting the larvae that survive until but not beyond metamorphosis. Despite that, little information is available regarding the effects of anthropogenic external stressors, such as the fungicides, on insect metamorphosis success and timing. We tested the effects of four azole fungicides that are widely used in agriculture (epoxiconazole, flusilazole, thiophanate-methyl, and thiabendazole). We applied the fungicides topically on prepupae of the abundant polyphagous predator of aphids, the crabronid wasp Pemphredon fabricii (M. Muller, 1911) (Hymenoptera: Crabronidae). We recorded the number of prepupae that molted successfully into pupae and adults, the mortality and the time to metamorphosis. We found the pupation to be delayed in prepupae collected from field margins compared to other sampling sites. This delay in pupation was further strengthened by the contact application of any of the four tested azole fungicides. The metamorphosis into adults was prolonged by flusilazole and thiabendazole but only in individuals that were collected from wetlands at field margins. Only flusilazole increased premature mortality during pupation. Because the shared metabolic degradation pathways of azoles, neonicotinoids, and acaricides used in beehives, further research should examine the possible synergistic effects of these compounds on farmland aculeates, including commercially exploited species.