Growing evidence for declines in bee populations has caused great concern because of the valuable ecosystem services they provide. Neonicotinoid insecticides have been implicated in these declines because they occur at trace levels in the nectar and pollen of crop plants. We exposed colonies of the bumble bee Bombus terrestris in the laboratory to field-realistic levels of the neonicotinoid imidacloprid, then allowed them to develop naturally under field conditions. Treated colonies had a significantly reduced growth rate and suffered an 85% reduction in production of new queens compared with control colonies. Given the scale of use of neonicotinoids, we suggest that they may be having a considerable negative impact on wild bumble bee populations across the developed world.

https://science.sciencemag.org/content/sci/336/6079/351.full.pdf

Neonicotinoid Pesticide Reduces Bumble Bee Colony Growth and Queen Production

Systemic insecticides are applied to plants using a wide variety of methods, ranging from foliar sprays to seed treatments and soil drenches. Neonicotinoids and fipronil are among the most widely used pesticides in the world. Their popularity is largely due to their high toxicity to invertebrates, the ease and flexibility with which they can be applied, their long persistence, and their systemic nature, which ensures that they spread to all parts of the target crop. However, these properties also increase the probability of environmental contamination and exposure of nontarget organisms. Environmental contamination occurs via a number of routes including dust generated during drilling of dressed seeds, contamination and accumulation in arable soils and soil water, runoff into waterways, and uptake of pesticides by nontarget plants via their roots or dust deposition on leaves. Persistence in soils, waterways, and nontarget plants is variable but can be prolonged; for example, the half-lives of neonicotinoids in soils can exceed 1,000 days, so they can accumulate when used repeatedly. Similarly, they can persist in woody plants for periods exceeding 1 year. Breakdown results in toxic metabolites, though concentrations of these in the environment are rarely measured. Overall, there is strong evidence that soils, waterways, and plants in agricultural environments and neighboring areas are contaminated with variable levels of neonicotinoids or fipronil mixtures and their metabolites (soil, parts per billion (ppb)-parts per million (ppm) range; water, parts per trillion (ppt)-ppb range; and plants, ppb-ppm range). This provides multiple routes for chronic (and acute in some cases) exposure of nontarget animals. For example, pollinators are exposed through direct contact with dust during drilling; consumption of pollen, nectar, or guttation drops from seed-treated crops, water, and consumption of contaminated pollen and nectar from wild flowers and trees growing near-treated crops. Studies of food stores in honeybee colonies from across the globe demonstrate that colonies are routinely and chronically exposed to neonicotinoids, fipronil, and their metabolites (generally in the 1–100 ppb range), mixed with other pesticides some of which are known to act synergistically with neonicotinoids. Other nontarget organisms, particularly those inhabiting soils, aquatic habitats, or herbivorous insects feeding on noncrop plants in farmland, will also inevitably receive exposure, although data are generally lacking for these groups. We summarize the current state of knowledge regarding the environmental fate of these compounds by outlining what is known about the chemical properties of these compounds, and placing these properties in the context of modern agricultural practices.

/pdf/environmental-fate-and-exposure-neonicotinoids-and-fipronil-ln5a08bl9m.pdf

Environmental fate and exposure; neonicotinoids and fipronil

Neonicotinoid insecticides are successfully applied to control pests in a variety of agricultural crops; however, they may not only affect pest insects but also non-target organisms such as pollinators. This review summarizes, for the first time, 15 years of research on the hazards of neonicotinoids to bees including honey bees, bumble bees and solitary bees. The focus of the paper is on three different key aspects determining the risks of neonicotinoid field concentrations for bee populations: (1) the environmental neonicotinoid residue levels in plants, bees and bee products in relation to pesticide application, (2) the reported side-effects with special attention for sublethal effects, and (3) the usefulness for the evaluation of neonicotinoids of an already existing risk assessment scheme for systemic compounds. Although environmental residue levels of neonicotinoids were found to be lower than acute/chronic toxicity levels, there is still a lack of reliable data as most analyses were conducted near the detection limit and for only few crops. Many laboratory studies described lethal and sublethal effects of neonicotinoids on the foraging behavior, and learning and memory abilities of bees, while no effects were observed in field studies at field-realistic dosages. The proposed risk assessment scheme for systemic compounds was shown to be applicable to assess the risk for side-effects of neonicotinoids as it considers the effect on different life stages and different levels of biological organization (organism versus colony). Future research studies should be conducted with field-realistic concentrations, relevant exposure and evaluation durations. Molecular markers may be used to improve risk assessment by a better understanding of the mode of action (interaction with receptors) of neonicotinoids in bees leading to the identification of environmentally safer compounds.

/pdf/neonicotinoids-in-bees-a-review-on-concentrations-side-2xp7dar74f.pdf

Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment

We assessed the state of knowledge regarding the effects of large-scale pollution with neonicotinoid insecticides and fipronil on non-target invertebrate species of terrestrial, freshwater and marine environments. A large section of the assessment is dedicated to the state of knowledge on sublethal effects on honeybees (Apis mellifera) because this important pollinator is the most studied non-target invertebrate species. Lepidoptera (butterflies and moths), Lumbricidae (earthworms), Apoidae sensu lato (bumblebees, solitary bees) and the section “other invertebrates” review available studies on the other terrestrial species. The sections on freshwater and marine species are rather short as little is known so far about the impact of neonicotinoid insecticides and fipronil on the diverse invertebrate fauna of these widely exposed habitats. For terrestrial and aquatic invertebrate species, the known effects of neonicotinoid pesticides and fipronil are described ranging from organismal toxicology and behavioural effects to population-level effects. For earthworms, freshwater and marine species, the relation of findings to regulatory risk assessment is described. Neonicotinoid insecticides exhibit very high toxicity to a wide range of invertebrates, particularly insects, and field-realistic exposure is likely to result in both lethal and a broad range of important sublethal impacts. There is a major knowledge gap regarding impacts on the grand majority of invertebrates, many of which perform essential roles enabling healthy ecosystem functioning. The data on the few non-target species on which field tests have been performed are limited by major flaws in the outdated test protocols. Despite large knowledge gaps and uncertainties, enough knowledge exists to conclude that existing levels of pollution with neonicotinoids and fipronil resulting from presently authorized uses frequently exceed the lowest observed adverse effect concentrations and are thus likely to have large-scale and wide ranging negative biological and ecological impacts on a wide range of non-target invertebrates in terrestrial, aquatic, marine and benthic habitats.

/pdf/effects-of-neonicotinoids-and-fipronil-on-non-target-4tz7hct25w.pdf

Effects of neonicotinoids and fipronil on non-target invertebrates

Bees are essential pollinators of many plants in natural ecosystems and agricultural crops alike. In recent years the decline and disappearance of bee species in the wild and the collapse of honey bee colonies have concerned ecologists and apiculturalists, who search for causes and solutions to this problem. Whilst biological factors such as viral diseases, mite and parasite infections are undoubtedly involved, it is also evident that pesticides applied to agricultural crops have a negative impact on bees. Most risk assessments have focused on direct acute exposure of bees to agrochemicals from spray drift. However, the large number of pesticide residues found in pollen and honey demand a thorough evaluation of all residual compounds so as to identify those of highest risk to bees. Using data from recent residue surveys and toxicity of pesticides to honey and bumble bees, a comprehensive evaluation of risks under current exposure conditions is presented here. Standard risk assessments are complemented with new approaches that take into account time-cumulative effects over time, especially with dietary exposures. Whilst overall risks appear to be low, our analysis indicates that residues of pyrethroid and neonicotinoid insecticides pose the highest risk by contact exposure of bees with contaminated pollen. However, the synergism of ergosterol inhibiting fungicides with those two classes of insecticides results in much higher risks in spite of the low prevalence of their combined residues. Risks by ingestion of contaminated pollen and honey are of some concern for systemic insecticides, particularly imidacloprid and thiamethoxam, chlorpyrifos and the mixtures of cyhalothrin and ergosterol inhibiting fungicides. More attention should be paid to specific residue mixtures that may result in synergistic toxicity to bees.

/pdf/pesticide-residues-and-bees-a-risk-assessment-1ta4vp6g13.pdf

Pesticide Residues and Bees – A Risk Assessment

In a greenhouse metabolism study, sunflowers were seed-treated with radiolabelled imidacloprid in a 700 g kg-1 WS formulation (Gaucho WS 70) at 0.7 mg AI per seed, and the nature of the resulting residues in nectar and pollen was determined. Only the parent compound and no metabolites were detected in nectar and pollen of these seed-treated sunflower plants (limit of detection < 0.001 mg kg-1). In standard LD50 laboratory tests, imidacloprid showed high oral toxicity to honeybees (Apis mellifera), with LD50 values between 3.7 and 40.9 ng per bee, corresponding to a lethal food concentration between 0.14 and 1.57 mg kg-1. The residue level of imidacloprid in nectar and pollen of seed-treated sunflower plants in the field was negligible. Under field-growing conditions no residues were detected (limit of detection: 0.0015 mg kg-1) in either nectar or pollen. There were also no detectable residues in nectar and pollen of sunflowers planted as a succeeding crop in soils which previously had been cropped with imidacloprid seed-treated plants. Chronic feeding experiments with sunflower honey fortified with 0.002, 0.005, 0.010 and 0.020 mg kg-1 imidacloprid were conducted to assess potential long-term adverse effects on honeybee colonies. Testing end-points in this 39-day feeding study were mortality, feeding activity, wax/comb production, breeding performance and colony vitality. Even at the highest test concentration, imidacloprid showed no adverse effects on the development of the exposed bee colonies. This no-adverse-effect concentration of 0.020 mg kg-1 compares with a field residue level of less than 0.0015 mg kg-1 (= limit of detection in the field residue studies) which clearly shows that a sunflower seed dressing with imidacloprid poses no risk to honeybees. This conclusion is confirmed by observations made in more than 10 field studies and several tunnel tests.

Risk posed to honeybees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers

A new method is described for the analytical determination of imidacloprid residues by LC MS/MS. This method allows the concurrent determination of the parent compound imidacloprid and two toxicologically relevant plant metabolites of this systemic insecticide. The method was successfully applied to examine field residue levels of these contaminants in rape and sunflower crop plants which had been seed-treated with imidacloprid. The analyzed samples included pollen, flowers, leaves, nectar, honey, wax and bees. Residues of imidacloprid and its metabolites 5-hydroxy-imidacloprid and olefin-imidacloprid are extracted with methanol/water. The extracts are subjected to liquid-liquid partition on a column filled with diatomaceous earth and subsequent solid phase extraction on a silica gel column. Quantification is performed by reversed phase HPLC with electrospray MS/MS-detection. External bracketing standards in matrix are used to compensate possible matrix effects in the ion source. The overall recoveries for imidacloprid, 5-hydroxy-imidacloprid and olefin-imidacloprid from plant matrices were between 91 and 97% with a relative standard deviation between 6.0 and 8.5%. The detector linearity and the repeatability of the method proved to be very precise. The limits of quantification were 0.005 and 0.01 mg/kg for imidacloprid and 5-hydroxy-imidacloprid, and for the olefin-metabolite, respectively. Field residue studies were conducted on seed-treated rape and sunflower crops. Small bee colonies were caged on flowering sunflower and rape plots and served as collecting devices for nectar and pollen. Flower petals, leaves, honey bees and the collected pollen and nectar samples were analysed by the new HPLC-MS/MS method. The analytical results showed no quantifiable residues in any sample material. Accordingly, honey bees will exposed to only negligible residue levels of imidacloprid when foraging on flowering seed-treated crop plants.

Analytical determination of imidacloprid and relevant metabolite residues by LC MS/MS

contribution to session V

 Honey bee poisoning incidents and monitoring schemes 

In spring of 2008, a bee incident occurred in the Upper Rhine Valley (Germany) during drilling of corn: bees were exposed to dust from abraded particles of the seed-coating containing the insecticide clothianidin. An inspection of drilled seed batches for resistance to abrasion and a geographical correlation analysis between specified seed batches and reported bee damages revealed that the incident was caused by improperly dressed batches of corn seeds with excessive abrasion of seed treatment particles which were subsequently emitted via the outlet air stream of the pneumatic drilling machines. Concerns raised by local beekeepers regarding effects on bees from foraging in seed-treated corn fields during bloom could be dispelled by a large-scale survey of clothianidin residues in pollen from the treated crop and an accompanying monitoring of bee hives exposed to flowering corn fields. In order to ensure the bee safety of seed-dressing products, technical improvements of seed treatment quality and drilling technology were developed resulting in a minimization of formation and emission of dust from abraded seed treatment particles. The efficacy of these improvements was proven in field trials.

Keywords: seed treatment, drilling machines, corn, clothianidin, dust, honey bees

/pdf/an-effective-risk-management-approach-to-prevent-bee-damage-cwhye4eyki.pdf

An effective risk management approach to prevent bee damage due to the emission of abraded seed treatment particles during sowing of seeds treated with bee toxic insecticides

Clothianidin is a commonly used systemic insecticide in seed treatments. Residues of clothianidin can occur in nectar and pollen as a result of within-plant-translocation. Foraging bees can collect contaminated nectar or pollen. Concerns have been brought forward that exposure to pesticide residues might affect colonies especially if they are weakened by varroosis. However, there are few scientific studies investigating such multiple-stressor scenarios in the context of the entire colony. To close this gapa field trial with 24 colonies was set up. The study design comprised four groups of six colonies each fed with uncontaminated sugar syrup ('C0'), or syrup spiked with 10 μg L−1 clothianidin ('C10'), 50 μg L−1 clothianidin ('C50') or 200 μg L−1 clothianidin ('C200'). C10 represented a residue concentration that may exceptionally occur and therefore a worst-case scenario, the higher dietary concentrations exceed and do not reflect fieldrealistic levels. A substantial load of 8 mites of Varroa destructor per ten gram bees in autumn was adjusted. The colonies were followed up for 328 days. The amount of brood and the strength of each colony were regularly assessed. Colony health, bee mortality, overwintering success, hive weights, and levels of in-hive residues were determined. Varroosis turned out to be the significant key factor for the endpoint colony strength. Clothianidin did not have a statistically significant impact on C0, C10 and C50 colonies. No statistical evidence was found for an interaction between varroosis andexposure to clothianidin.

/pdf/a-long-term-field-study-on-the-effects-of-dietary-exposure-32hvcbt0t4.pdf

A long-term field study on the effects of dietary exposure of clothianidin to varroosis-weakened honey bee colonies

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Risk posed to honeybees (Apis mellifera L, Hymenoptera) by an imidacloprid seed dressing of sunflowers

Analytical determination of imidacloprid and relevant metabolite residues by LC MS/MS

An effective risk management approach to prevent bee damage due to the emission of abraded seed treatment particles during sowing of seeds treated with bee toxic insecticides

A long-term field study on the effects of dietary exposure of clothianidin to varroosis-weakened honey bee colonies