IPM-recommended insecticides harm beneficial insects through contaminated honeydew

Calvo-Agudo, Miguel; González‐Cabrera, Joel; Sadutto, Daniele; Picó, Yolanda; Urbaneja, Alberto; Dicke, Marcel; Tena, Alejandro

doi:10.1016/j.envpol.2020.115581

Cited by 15 publications

(13 citation statements)

References 44 publications

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“…Systemic insecticides are applied using at least six techniques: spraying, soil drenching, injection into the plant (mostly for tree crops), as granules, drip irrigation (chemigation) or as seed coatings. When systemic insecticides are applied by spraying (Calvo‐Agudo et al ., 2019 , 2020 ), all three exposure pathways are likely to take place. By contrast, if systemic insecticides are applied to the soil, in the irrigation system, injected into the trunk, as granules or used as seed coatings, only the third pathway can occur (Calvo‐Agudo et al ., 2019 , 2020 , 2021 ).…”

Section: How Can Systemic Insecticides Reach Honeydew?mentioning

confidence: 99%

“…When systemic insecticides are applied by spraying (Calvo‐Agudo et al ., 2019 , 2020 ), all three exposure pathways are likely to take place. By contrast, if systemic insecticides are applied to the soil, in the irrigation system, injected into the trunk, as granules or used as seed coatings, only the third pathway can occur (Calvo‐Agudo et al ., 2019 , 2020 , 2021 ). Within this third pathway, systemic insecticides might reach honeydew under several possible scenarios (Fig.…”

Section: How Can Systemic Insecticides Reach Honeydew?mentioning

confidence: 99%

“…1 ), honeydew is highly accessible and can be abundant in nearly all crops and seasons (Lundgren, 2009 ). Notably, it was recently demonstrated that honeydew can contain insecticides that can negatively influence beneficial insect species (Calvo‐Agudo et al ., 2019 , 2020 , 2021 ). More specifically, it was shown that hemipterans feeding on plants treated with systemic insecticides (i.e.…”

Section: Introductionmentioning

confidence: 99%

“…More specifically, it was shown that hemipterans feeding on plants treated with systemic insecticides (i.e. water‐soluble insecticides that can move within plant vascular tissue) 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 ).…”

Section: Introductionmentioning

confidence: 99%

“…Honeydew as route of exposure to water‐soluble insecticides has now 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, therefore, is likely to be common in agroecosystems where water‐soluble and systemic insecticides are used.…”

Section: Introductionmentioning

confidence: 99%

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Insecticide‐contaminated honeydew: risks for beneficial insects

et al. 2021

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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.

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Section: How Can Systemic Insecticides Reach Honeydew?mentioning

confidence: 99%

Section: How Can Systemic Insecticides Reach Honeydew?mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Insecticide‐contaminated honeydew: risks for beneficial insects

et al. 2021

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Essential oils-based repellents for the management of Myzus persicae and Macrosiphum euphorbiae

et al. 2021

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Chemical cues from honeydew-associated bacteria to enhance parasitism efficacy: from laboratory to field assay

Liu,

Xiao,

Liu

et al. 2023

J Pest Sci

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Honeydew from Hemipteran insects serves as carbohydrate source to beneficial insects but also to various microorganisms. Microbial volatile organic compounds (mVOCs) may play diverse roles in herbivore-microbe-natural enemy interactions. However, the functional significance of mVOCs from aphid honeydew remains largely unclear. In this study, a total of seven cultivable bacteria from Sitobion miscanthi honeydew have been isolated and identified based on 16S rRNA technique, which included Lysinibacillus fusiformis, Erwinia aphidicola, E. tasmaniensis, Acinetobacter bereziniae, Klebsiella quasipneumoniae subsp. Similipneumoniae, Staphylococcus capitis and Bacillus safensis subsp. safensis. One bacterial strain, L. fusiformis MH1, was found to be most attractive to Aphidius gifuensis parasitic wasp in Y-tube olfactometer. Two compounds, namely 1-ethyl-2-methylbenzene and 2-butyl-1-octanol, were emitted from L. fusiformis MH1 and were attractive to A. gifuensis and identified by using coupled gas chromatography-electroantennography and coupled gas chromatography with mass spectrometry. Application of bacterial and mVOCs formulations in crop field resulted in significant aphid abundance decrease associated with higher parasitism rates compared with control. Our results indicated that some microbes in aphid honeydew could manipulate the herbivore-natural enemy interactions and could be developed as a novel alternative for environmentally friendly biological control of aphids.

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IPM-recommended insecticides harm beneficial insects through contaminated honeydew

Cited by 15 publications

References 44 publications

Insecticide‐contaminated honeydew: risks for beneficial insects

Insecticide‐contaminated honeydew: risks for beneficial insects

Essential oils-based repellents for the management of Myzus persicae and Macrosiphum euphorbiae

Chemical cues from honeydew-associated bacteria to enhance parasitism efficacy: from laboratory to field assay

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