Neonicotinoids in excretion product of phloem-feeding insects kill beneficial insects

Abstract

Pest control in agriculture is mainly based on the application of insecticides, which may impact nontarget beneficial organisms leading to undesirable ecological effects. Neonicotinoids are among the most widely used insecticides. However, they have important negative side effects, especially for pollinators and other beneficial insects feeding on nectar. Here, we identify a more accessible exposure route: Neonicotinoids reach and kill beneficial insects that feed on the most abundant carbohydrate source for insects in agroecosystems, honeydew. Honeydew is the excretion product of phloem-feeding hemipteran insects such as aphids, mealybugs, whiteflies, and psyllids. We allowed parasitic wasps and pollinating hoverflies to feed on honeydew from hemipterans feeding on trees treated with thiamethoxam or imidacloprid, the most commonly used neonicotinoids. LC-MS/MS analyses demonstrated that both neonicotinoids were present in honeydew. Honeydew with thiamethoxam was highly toxic to both species of beneficial insects, and honeydew with imidacloprid was moderately toxic to hoverflies. Collectively, our data provide strong evidence for honeydew as a route of insecticide exposure that may cause acute or chronic deleterious effects on nontarget organisms. This route should be considered in future environmental risk assessments of neonicotinoid applications.

Keywords: biological control agents; environmental risk assessment; honeydew; pollinators; thiamethoxam.

Fig. 1.

Mortality of beneficial insects fed on honeydew contaminated with neonicotinoid insecticides. Mortality (mean ± SE) of (A) the pollinating hoverfly S. rueppellii and (B) the parasitic wasp A. pseudococci fed on honeydew of P. citri feeding on water-treated trees or on honeydew of P. citri feeding on soil- (Left) or foliar-treated trees (Right) with the neonicotinoid insecticides imidacloprid or thiamethoxam. Mortality was assessed after feeding on honeydew during 72 h. Columns sharing the same letter are not significantly different from each other (Bonferroni test, P < 0.05).

Fig. 2.

Survival of beneficial insects fed on honeydew contaminated with neonicotinoid insecticides. Survival curves estimated by Kaplan–Meier of (A) the pollinating hoverfly S. rueppellii, and (B), the parasitic wasp A. pseudococci fed on honeydew of P. citri feeding on water-treated trees or on honeydew of P. citri feeding on soil- (Left) or foliar-treated trees (Right) with the neonicotinoid insecticides imidacloprid or thiamethoxam.

Fig. 3.

Honeydew contaminated by neonicotinoid insecticides. Percentage (mean ± SE) of soil-treated trees (Left) or foliar-treated trees (Right) with P. citri honeydew contaminated by neonicotinoids. Neonicotinoids were detected using LC-MS/MS. Columns with different letters are significantly different from each other (Fisher´s exact test, P < 0.05; number of trees per treatment = 6 to 7).