Abstract
ABSTRACTHoneydew is the sugar‐rich excretion of phloem‐feeding hemipteran insects such as aphids, mealybugs, whiteflies, and psyllids, and can be a main carbohydrate source for beneficial insects in some ecosystems. Recent research has revealed that water‐soluble, systemic insecticides contaminate honeydew excreted by hemipterans that feed on plants treated with these insecticides. This contaminated honeydew can be toxic to beneficial insects, such as pollinators, parasitic wasps and generalist predators that feed on it. This route of exposure has now been demonstrated in three plant species, for five systemic insecticides and four hemipteran species; therefore, we expect this route to be widely available in some ecosystems. In this perspective paper, we highlight the importance of this route of exposure by exploring: (i) potential pathways through which honeydew might be contaminated with insecticides; (ii) hemipteran families that are more likely to excrete contaminated honeydew; and (iii) systemic insecticides with different modes of action that might contaminate honeydew through the plant. Furthermore, we analyse several model scenarios in Europe and/or the USA where contaminated honeydew could be problematic for beneficial organisms that feed on this ubiquitous carbohydrate source. Finally, we explain why this route of exposure might be important when exotic, invasive, honeydew‐producing species are treated with systemic insecticides. Overall, this review opens a new area of research in the field of ecotoxicology to understand how insecticides can reach non‐target beneficial insects. In addition, we aim to shed light on potential undescribed causes of insect declines in ecosystems where honeydew is an important carbohydrate source for insects, and advocate for this route of exposure to be included in future environmental risk assessments.
Highlights
Honeydew is the sugar-excretion product of hemipterans, such as aphids, coccids, whiteflies, and psyllids, that feed on plants
It was shown that hemipterans feeding on plants treated with systemic insecticides excreted honeydew laden with the active ingredient of the insecticides or its metabolites, and the honeydew was toxic to insects that consumed it (Calvo-Agudo et al, 2019, 2020, 2021; Quesada, Scharf & Sadof, 2020)
Water-soluble systemic insecticides might reach honeydew through three different pathways (Fig. 2). (i) Direct contamination of honeydew: honeydew already present on a plant can be contaminated by the direct spraying of insecticides (Fig. 2). (ii) Through insects that excrete honeydew: insecticides can be directly absorbed into the body of honeydew producers when they are sprayed, and honeydew producers could excrete the insecticide via their honeydew (Fig. 2). (iii) Through plants and honeydew producers: systemic insecticides are translocated to all parts of the plant, and honeydew producers that feed on treated plants can excrete the insecticide via their honeydew (Calvo-Agudo et al, 2019) (Fig. 2)
Summary
Honeydew is the sugar-excretion product of hemipterans, such as aphids, coccids, whiteflies, and psyllids, that feed on plants. Honeydew as route of exposure to water-soluble insecticides has been demonstrated for four species of honeydew producers belonging to four different families of hemipterans, five systemic insecticides with four different modes of action and translocation routes, and three plant species (Calvo-Agudo et al, 2019, 2020, 2021; Quesada et al, 2020). This route of exposure, is likely to be common in agroecosystems where water-soluble and. The crop species were selected because they have high economic importance in the EU and/or the USA, are commonly treated with systemic insecticides, and honeydew can be the main carbohydrate source for beneficial insects in fields of these crops
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