Centro de Protección Vegetal y Biotecnología, Instituto Valenciano de Investigaciones Agrarias (IVIA), Carretera de Moncada-Náquera Km. 4,5, 46113, Moncada, Valencia, Spain.
Laboratory of Entomology, Wageningen University, PO Box 16, 6700AA, Wageningen, The Netherlands.
Biol Rev Camb Philos Soc. 2022 Apr;97(2):664-678. doi: 10.1111/brv.12817. Epub 2021 Nov 21.
Honeydew 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.
甘露蜜是半翅目吸食韧皮部的昆虫（如蚜虫、粉虱、介壳虫和木虱等）富含糖分的排泄物，在一些生态系统中可能是有益昆虫的主要碳水化合物来源。最近的研究表明，水溶性、系统性杀虫剂会污染吸食这些杀虫剂处理过的植物的半翅目昆虫所分泌的甘露蜜。这种受污染的甘露蜜可能对有益昆虫（如传粉昆虫、寄生蜂和以其为食的一般捕食性天敌）有毒。在三种植物、五种系统性杀虫剂和四种半翅目昆虫中已经证明了这种暴露途径；因此，我们预计在某些生态系统中，这种暴露途径将广泛存在。在这篇观点文章中，我们通过探讨以下几个方面来强调这种暴露途径的重要性：（i）甘露蜜可能被杀虫剂污染的潜在途径；（ii）更有可能分泌受污染甘露蜜的半翅目昆虫科；（iii）通过植物可能污染甘露蜜的不同作用模式的系统性杀虫剂。此外，我们分析了欧洲和/或美国的几个模型情景，在这些情景中，受污染的甘露蜜可能对以这种普遍存在的碳水化合物为食的有益生物构成问题。最后，我们解释了当外来入侵的、产甘露蜜的物种被系统性杀虫剂处理时，这种暴露途径为何可能很重要。总的来说，本综述在生态毒理学领域开辟了一个新的研究领域，以了解杀虫剂如何到达非靶标有益昆虫。此外，我们旨在揭示在甘露蜜是昆虫重要碳水化合物来源的生态系统中，昆虫数量减少的潜在未被描述的原因，并倡导在未来的环境风险评估中纳入这种暴露途径。
