Honeydew as a newly described route of insecticide exposure to beneficial insects

A plethora of beneficial insects need carbohydrates to meet their requirements for daily physical activities and metabolic processes. In agricultural lands, beneficial insects find carbohydrates mainly in nectar and honeydew. Nectar is often scarce in most agroecosystems because it is limited to the brief flowering period of the crop (if present). This sugar can also be available in the spontaneously flowering plants that appear along crop borders, ditches and roadsides, but these plants are often removed to avoid competition with the crop. Instead, honeydew, the excretion product of many hemipteran insects such as aphids, whiteflies, coccids, mealybugs or psyllids, is highly abundant and accessible in agricultural lands throughout the year. For this reason, many beneficial insects rely on honeydew as a main carbohydrate source of their diet, especially when nectar is scarce.The use of systemic insecticides had been considered an excellent option for integrated pest management programs because once applied, they move systemically to all plant tissues, harming herbivores that feed on the plant. Yet, the fact that the insecticides move to all plant tissues, means that they also reach plant-derived food sources such as nectar or pollen. Many insects that feed on these food sources are therefore exposed to several systemic insecticides. The aim of this PhD thesis was to explore whether honeydew, like nectar, is a route of insecticide exposure for beneficial insects. This route of exposure could be more impactful than the route of nectar because honeydew is ubiquitous in agroecosystems.First, I present the newly described route of insecticide exposure to beneficial insects: honeydew excreted by hemipterans feeding on trees treated with some systemic insecticides contains insecticide residues that affect insects feeding on it. This route of exposure was demonstrated for: 1) two different crop species: citrus and soybean plants; 2) three hemipteran species: the citrus mealybug Planococcus citri, the woolly whitefly Aleurothrixus floccosus and the soybean aphid Aphis glycines; 3) four active ingredients: the neonicotinoids thiamethoxam and imidacloprid, and the IPM-recommended insecticides flonicamid and pymetrozine; 4) three modes of application: foliar, soil drenching, and seed coatings; 5) five beneficial insects: the hoverfly Sphaerophoria rueppellii, the parasitic wasps Anagyrus vladimiri, Aphelinus glycinis and Aphelinus certus, and the predatory midge Aphidoletes aphidimyza. Overall, these results demonstrate that honeydew is a route of exposure to systemic insecticides for beneficial insects.Second, I studied whether beneficial insects discriminate between food sources uncontaminated and contaminated with neonicotinoids. It has been shown that some pollinator species prefer food with neonicotinoids after feeding on this contaminated source, but this had never been tested for honeydew. Hoverflies did not discriminate between honeydew contaminated with insecticides or uncontaminated honeydew. Instead, parasitic wasps did discriminate between uncontaminated honeydew or honeydew with thiamethoxam, and preferred the contaminated food source. These results may have important consequences because in previous studies, I collected uncontaminated honeydew and honeydew contaminated with systemic insecticides in samples from the same plant and day.Finally, in a perspective paper I present an overview of the importance of honeydew as a route of insecticide exposure to beneficial insects by exploring: 1) the potential pathways through which honeydew might be contaminated with insecticides; 2) the hemipteran families that are more likely to excrete contaminated honeydew due to their different feeding behaviour. 3) the systemic insecticides that are more likely to contaminate honeydew due to the physiochemical properties; and 4) several model crops where contaminated honeydew can be highly accessible for beneficial organisms and commonly contaminated with systemic insecticides.In conclusion, this thesis describes a new, highly common route, in which beneficial insects can be harmed by insecticides. This route of exposure is widely variable and complex, and further studies are needed to include honeydew in future environmental risk assessments.&nbsp