Honeydew management to promote biological control.

Honeydew is the excretion of plant-feeding hemipterans and it is one of the most abundant source of carbohydrates for parasitoids and predators in agroecosystems. Being so abundant, honeydew mediates direct and indirect interactions that affect biological control. We describe these interactions and identify honeydew-management strategies to reduce pest pressure. First, the presence of nondamaging honeydew producers in cover crops and hedges increases the efficacy of parasitoids and predators. Second, breaking the mutualism between ants and honeydew-producing pests with alternative sugar sources promotes biological control of these pests. Third, we propose to explore honeydew volatiles to attract biological control agents and repel pests, as well as to induce plant defenses. Finally, we urge reducing the use of systemic pesticides that contaminate honeydew and negatively affect biological control agents that feed on it. Overall, we propose that honeydew management is integrated in pest management programs to contribute to sustainable agriculture.

Insecticide-contaminated honeydew: risks for beneficial insects.

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.

Neonicotinoids from coated seeds toxic for honeydew-feeding biological control agents.

Seed coating ('seed treatment') is the leading delivery method of neonicotinoid insecticides in major crops such as soybean, wheat, cotton and maize. However, this prophylactic use of neonicotinoids is widely discussed from the standpoint of environmental costs. Growing soybean plants from neonicotinoid-coated seeds in field, we demonstrate that soybean aphids (Aphis glycines) survived the treatment, and excreted honeydew containing neonicotinoids. Biochemical analyses demonstrated that honeydew excreted by the soybean aphid contained substantial concentrations of neonicotinoids even one month after sowing of the crop. Consuming this honeydew reduced the longevity of two biological control agents of the soybean aphid, the predatory midge Aphidoletes aphidimyza and the parasitic wasp Aphelinus certus. These results have important environmental and economic implications because honeydew is the main carbohydrate source for many beneficial insects in agricultural landscapes.

IPM-recommended insecticides harm beneficial insects through contaminated honeydew.

The use of some systemic insecticides has been banned in Europe because they are toxic to beneficial insects when these feed on nectar. A recent study shows that systemic insecticides can also kill beneficial insects when they feed on honeydew. Honeydew is the sugar-rich excretion of hemipterans and is the most abundant carbohydrate source for beneficial insects such as pollinators and biological control agents in agroecosystems. Here, we investigated whether the toxicity of contaminated honeydew depends on i) the hemipteran species that excretes the honeydew; ii) the active ingredient, and iii) the beneficial insect that feeds on it. HPLC-MS/MS analyses demonstrated that the systemic insecticides pymetrozine and flonicamid, which are commonly used in Integrated Pest Management programs, were present in honeydew excreted by the mealybug Planococcus citri. However, only pymetrozine was detected in honeydew excreted by the whitefly Aleurothixus floccosus. Toxicological studies demonstrated that honeydew excreted by mealybugs feeding on trees treated either with flonicamid or pymetrozine increased the mortality of the hoverfly Sphaerophoria rueppellii, but did not affect the parasitic wasp Anagyrusvladimiri. Honeydew contaminated with flonicamid was more toxic for the hoverfly than that contaminated with pymetrozine. Collectively, our data demonstrate that systemic insecticides commonly used in IPM programs can contaminate honeydew and kill beneficial insects that feed on it, with their toxicity being dependent on the active ingredient and hemipteran species that excretes the honeydew.

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

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.