Bees are subject to numerous pressures in the modern world. The abundance and diversity of flowers has declined, bees are chronically exposed to cocktails of agrochemicals, and they are simultaneously exposed to novel parasites accidentally spread by humans. Climate change is likely to exacerbate these problems in the future. Stressors do not act in isolation; for example pesticide exposure can impair both detoxification mechanisms and immune responses, rendering bees more susceptible to parasites. It seems certain that chronic exposure to multiple, interacting stressors is driving honey bee colony losses and declines of wild pollinators, but such interactions are not addressed by current regulatory procedures and studying these interactions experimentally poses a major challenge. In the meantime, taking steps to reduce stress on bees would seem prudent; incorporating flower-rich habitat into farmland, reducing pesticide use through adopting more sustainable farming methods, and enforcing effective quarantine measures on bee movements are all practical measures that should be adopted. Effective monitoring of wild pollinator populations is urgently needed to inform management strategies into the future.

https://science.sciencemag.org/content/sci/early/2015/02/25/science.1255957.full.pdf

Bee declines driven by combined stress from parasites, pesticides, and lack of flowers

Summary 1. Neonicotinoids are now the most widely used insecticides in the world. They act systemically, travelling through plant tissues and protecting all parts of the crop, and are widely applied as seed dressings. As neurotoxins with high toxicity to most arthropods, they provide effective pest control and have numerous uses in arable farming and horticulture. 2. However, the prophylactic use of broad-spectrum pesticides goes against the long-established principles of integrated pest management (IPM), leading to environmental concerns. 3. It has recently emerged that neonicotinoids can persist and accumulate in soils. They are water soluble and prone to leaching into waterways. Being systemic, they are found in nectar and pollen of treated crops. Reported levels in soils, waterways, field margin plants and floral resources overlap substantially with concentrations that are sufficient to control pests in crops, and commonly exceed the LC50 (the concentration which kills 50% of individuals) for beneficial organisms. Concentrations in nectar and pollen in crops are sufficient to impact substantially on colony reproduction in bumblebees. 4. Although vertebrates are less susceptible than arthropods, consumption of small numbers of dressed seeds offers a route to direct mortality in birds and mammals. 5. Synthesis and applications. Major knowledge gaps remain, but current use of neonicotinoids is likely to be impacting on a broad range of non-target taxa including pollinators and soil and aquatic invertebrates and hence threatens a range of ecosystem services.

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REVIEW: An overview of the environmental risks posed by neonicotinoid insecticides

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

Declines in bumble bee species in the past 60 years are well documented in Europe, where they are driven primarily by habitat loss and declines in floral abundance and diversity resulting from agricultural intensification. Impacts of habitat degradation and fragmentation are likely to be compounded by the social nature of bumble bees and their largely monogamous breeding system, which renders their effective population size low. Hence, populations are susceptible to stochastic extinction events and inbreeding. In North America, catastrophic declines of some bumble bee species since the 1990s are probably attributable to the accidental introduction of a nonnative parasite from Europe, a result of global trade in domesticated bumble bee colonies used for pollination of greenhouse crops. Given the importance of bumble bees as pollinators of crops and wildflowers, steps must be taken to prevent further declines. Suggested measures include tight regulation of commercial bumble bee use and targeted use of environmentally comparable schemes to enhance floristic diversity in agricultural landscapes.

/pdf/decline-and-conservation-of-bumble-bees-1thgzzqlml.pdf

Decline and conservation of bumble bees

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

Bombus terrestris bumblebees are important pollinators of wild flowers, and in modern agriculture they are used to guarantee pollination of vegetables and fruits. In the field it is likely that worker bees are exposed to pesticides during foraging. To date, several tests exist to assess lethal and sublethal side-effects of pesticides on bee survival, growth/development and reproduction. Within the context of ecotoxicology and insect physiology, we report the development of a new bioassay to assess the impact of sublethal concentrations on the bumblebee foraging behavior under laboratory conditions. In brief, the experimental setup of this behavior test consists of two artificial nests connected with a tube of about 20 cm and use of queenless micro-colonies of 5 workers. In one nest the worker bees constructed brood, and in the other food (sugar and pollen) was provided. Before exposure, the worker bees were allowed a training to forage for untreated food; afterwards this was replaced by treated food. Using this setup we investigated the effects of sublethal concentrations of the neonicotinoid insecticide imidacloprid, known to negatively affect the foraging behavior of bees. For comparison within the family of neonicotinoid insecticides, we also tested different concentrations of two other neonicotinoids: thiamethoxam and thiacloprid, in the laboratory with the new bioassay. Finally to evaluate the new bioassay, we also tested sublethal concentrations of imidacloprid in the greenhouse with use of queenright colonies of B. terrestris, and here worker bees needed to forage/fly for food that was placed at a distance of 3 m from their hives. In general, the experiments showed that concentrations that may be considered safe for bumblebees can have a negative influence on their foraging behavior. Therefore it is recommended that behavior tests should be included in risk assessment tests for highly toxic pesticides because impairment of the foraging behavior can result in a decreased pollination, lower reproduction and finally in colony mortality due to a lack of food.

/pdf/risk-assessment-for-side-effects-of-neonicotinoids-against-44qbhm6c6p.pdf

Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior.

This research project examined the potential hazards of a major class of insect growth regulators (IGRs) to survival, reproduction and larval growth in bumblebees Bombus terrestris L. Eight chitin synthesis inhibitors (CSIs) were tested: buprofezin, cyromazine, diflubenzuron, flucycloxuron, flufenoxuron, lufenuron, novaluron and teflubenzuron. These different IGRs, which are important in the control of pest insects in greenhouses, were applied via three different routes of exposure under laboratory conditions: dermal contact, and orally via the drinking of sugar/water and via pollen. The compounds were tested at their respective maximum field recommended concentrations (MFRC) and also in dose-response assays to calculate LC(50) values. In general, none of the CSIs showed acute worker toxicity. However, there was a dramatic reduction in brood production, especially after oral treatment with pollen and sugar/water. Conspicuously, egg fertility was reduced in all treatments with diflubenzuron and teflubenzuron. In addition to egg mortality, the worker bumblebees removed larvae from the treated nest, and in most cases these individuals were dead first-second instars. Under a binocular microscope, such larvae showed an abnormally formed cuticle leading to mechanical weakness and death. In another series of experiments using (14)C-diflubenzuron and (14)C-flufenoxuron, cuticular penetration in workers was studied for a better understanding of the differences in toxicity. With (14)C-diflubenzuron, transovarial transport and accumulation in the deposited eggs supported the strong reproductive effects. Overall, the present results suggest that CSIs should be applied with caution in combination with bumblebees. The compatibility of each compound to be used in combination with B. terrestris is discussed in relation to calculated LC(50) values, routes of uptake and effects.

Hazards and uptake of chitin synthesis inhibitors in bumblebees Bombus terrestris

This study examined the lethal and sublethal effects on the beneficial insect Bombus terrestris by two classes of insect growth regulators (IGRs) that are commercially used in agriculture to control pest insects. Three juvenile hormones analogues (JHAs) (pyriproxyfen, fenoxycarb and kinoprene) and two ecdysone agonists or moulting accelerating compounds (MACs) (tebufenozide and methoxyfenozide) were tested. The bumblebee workers were exposed to the insecticides via three different routes of exposure: dermally by topical contact, and orally via the drinking sugar water or the pollen. In the first series of experiments the IGRs were applied at their respective maximum field recommended concentration (MFRC). These risk hazard tests showed that the tested IGRs caused no acute toxicity on the workers, and any compound had an adverse effect on reproduction (production of males). In addition, larval development was followed in the treated nests compared with the controls. After application of the two MACs and the JHA fenoxycarb no adverse effects were observed on larval development. However, in the nests where the workers were exposed to the JHAs pyriproxyfen and kinoprene higher numbers of dead larvae were scored. These larvae were third and fourth instars, implying a lethal blockage of development before metamorphosis. In a second test, a series of dilutions was made for kinoprene, and these results revealed that only the MFRC caused a toxic effect on the larval development. On the other hand, kinoprene at lower concentrations (0.0650 mg ai/l) had a stimulatory effect on brood production. It was remarkable that ovaries of such treated dominant workers were longer and contained more eggs than in the controls. In a last experiment, the cuticular uptake was determined for a JHA and MAC to evaluate to what extent worker bees accumulate these classes of IGRs. Cuticular uptake ranged from 34 to 83% at 24 h after topical application. Overall, the obtained results indicate that the tested IGRs at their recommended concentration are safe to be used in combination with B. terrestris.

Bumblebees can be used in combination with juvenile hormone analogues and ecdysone agonists.

BACKGROUND: This study was undertaken to identify any potential adverse side effects of the use of seven microbiological control agents (MCAs) on the bumblebee, Bombus terrestris L., in the context of combined use in integrated pest management (IPM).AQ10  (Ampelomycesquisqualis),Binab-T-vector  (Hypocreaparapilulifera +T.atroviride;1/1),Prestop-Mix  (Gliocladium catenulatum J1446), Serenade  (Bacillus subtilis QST713), Trianum-P  (Trichoderma harzianum T22), Botanigard  (Beauveria bassiana GHA )a nd Granupom  (Cydia pomonella granulovirus), comprising five biofungicides and two bioinsecticides, were investigated. Bumblebee workers were exposed under laboratory conditions to each MCA at its maximum field recommended concentration(MFRC) via threedifferentroutes of exposure: dermalcontact and orally via eithertreatedsugar water or pollen. RESULTS:ThetestedMCAs were found to be safefor workers of B.terrestris, with theexception of Botanigard  and Serenade  . Exposure to Botanigard  via contact at its MFRC caused 92% mortality after 11 weeks, while the 1/10 MFRC killed 46% of exposed workers. For Serenade  , topical contact and oral delivery via sugar water resulted in 88 and 100% worker mortality respectively. With lower concentrations (1/2, 1/5 and 1/10 MFRC) the toxicity decreased, but the effect depended on the route of exposure.Inadditionto lethaleffects,nestswerealso evaluatedforsublethaleffects aftertreatmentwiththesevenMCAsat theirrespective MFRCs over 11 weeks. Inthesebioassays, only Botanigard  andSerenade  gave rise to a significant(P < 0.05) decrease in drone production. Sublethal effects on foraging behaviour were also evaluated, and only Botanigard at its MFRC delivered via treated sugar water induced negative effects. CONCLUSION: The results demonstrated that most of the MCAs tested can be considered safe for use in combination with B.terrestris, based on the International Organisation for Biological Control of Noxious Animals and Plants (IOBC) classification. However, some can be harmful, such as the biofungicide Serenade  and the bioinsecticide Botanigard  . Therefore, it is recommendedthatallshouldbetestedbeforeuseincombinationwithpollinators.Inthiscontext,itisalsoadvisablethatthese MCAs should be evaluated in more realistic field situations for the assessment of potentially deleterious effects on foraging behaviour. c � 2009 Society of Chemical Industry

A laboratory evaluation to determine the compatibility of microbiological control agents with the pollinator Bombus terrestris

This study was part of a large-scale monitoring project to assess the possible effects of Elado® (10 g clothianidin & 2 g β-cyfluthrin/kg seed)-dressed oilseed rape seeds on different pollinators in Northern Germany. Firstly, residues of clothianidin and its active metabolites thiazolylnitroguanidine and thiazolylmethylurea were measured in nectar and pollen from Elado®-dressed (test site, T) and undressed (reference site, R) oilseed rape collected by honey bees confined within tunnel tents. Clothianidin and its metabolites could not be detected or quantified in samples from R fields. Clothianidin concentrations in samples from T fields were 1.3 ± 0.9 μg/kg and 1.7 ± 0.9 μg/kg in nectar and pollen, respectively. Secondly, pollen and nectar for residue analyses were sampled from free flying honey bees, bumble bees and mason bees, placed at six study locations each in the R and T sites at the start of oilseed rape flowering. Honey samples were analysed from all honey bee colonies at the end of oilseed rape flowering. Neither clothianidin nor its metabolites were detectable or quantifiable in R site samples. Clothianidin concentrations in samples from the T site were below the limit of quantification (LOQ, 1.0 µg/kg) in most pollen and nectar samples collected by bees and 1.4 ± 0.5 µg/kg in honey taken from honey bee colonies. In summary, the study provides reliable semi-field and field data of clothianidin residues in nectar and pollen collected by different bee species in oilseed rape fields under common agricultural conditions.

/pdf/large-scale-monitoring-of-effects-of-clothianidin-dressed-1tjsps7pcg.pdf

Large-scale monitoring of effects of clothianidin-dressed oilseed rape seeds on pollinating insects in northern Germany: residues of clothianidin in pollen, nectar and honey.

Guido Sterk

Papers

Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior.

Hazards and uptake of chitin synthesis inhibitors in bumblebees Bombus terrestris

Bumblebees can be used in combination with juvenile hormone analogues and ecdysone agonists.

A laboratory evaluation to determine the compatibility of microbiological control agents with the pollinator Bombus terrestris

Large-scale monitoring of effects of clothianidin-dressed oilseed rape seeds on pollinating insects in northern Germany: residues of clothianidin in pollen, nectar and honey.