Fungicides and bees: a review of exposure and risk.

Fungicides account for more than 35% of the global pesticide market and their use is predicted to increase in the future. While fungicides are commonly applied during bloom when bees are likely foraging on crops, whether real-world exposure to these chemicals - alone or in combination with other stressors - constitutes a threat to the health of bees is still the subject of great uncertainty. The first step in estimating the risks of exposure to fungicides for bees is to understand how and to what extent bees are exposed to these active ingredients. Here we review the current knowledge that exists about exposure to fungicides that bees experience in the field, and link quantitative data on exposure to acute and chronic risk of lethal endpoints for honey bees (Apis mellifera). From the 702 publications we screened, 76 studies contained quantitative data on residue detections in honey bee matrices, and a further 47 provided qualitative information about exposure for a range of bee taxa through various routes. We compiled data for 90 fungicides and metabolites that have been detected in honey, beebread, pollen, beeswax, and the bodies of honey bees. The risks posed to honey bees by fungicide residues was estimated through the EPA Risk Quotient (RQ) approach. Based on residue concentrations detected in honey and pollen/beebread, none of the reported fungicides exceeded the levels of concern (LOC) set by regulatory agencies for acute risk, while 3 and 12 fungicides exceeded the European Food Safety Authority (EFSA) chronic LOC for honey bees and wild bees, respectively. When considering exposure to all bees, fungicides of most concern include many broad-spectrum systemic fungicides, as well as the widely used broad-spectrum contact fungicide chlorothalonil. In addition to providing a detailed overview of the frequency and extent of fungicide residue detections in the bee environment, we identified important research gaps and suggest future directions to move towards a more comprehensive understanding and mitigation of the risks of exposure to fungicides for bees, including synergistic risks of co-exposure to fungicides and other pesticides or pathogens.

Population decline in a ground-nesting solitary squash bee (Eucera pruinosa) following exposure to a neonicotinoid insecticide treated crop (Cucurbita pepo).

Insect pollinators are threatened by multiple environmental stressors, including pesticide exposure. Despite being important pollinators, solitary ground-nesting bees are inadequately represented by pesticide risk assessments reliant almost exclusively on honeybee ecotoxicology. Here we evaluate the effects of realistic exposure via squash crops treated with systemic insecticides (Admire-imidacloprid soil application, FarMore FI400-thiamethoxam seed-coating, or Coragen-chlorantraniliprole foliar spray) for a ground-nesting bee species (Hoary squash bee, Eucera pruinosa) in a 3-year semi-field experiment. Hoary squash bees provide essential pollination services to pumpkin and squash crops and commonly nest within cropping areas increasing their risk of pesticide exposure from soil, nectar, and pollen. When exposed to a crop treated at planting with soil-applied imidacloprid, these bees initiated 85% fewer nests, left 5.3 times more pollen unharvested, and produced 89% fewer offspring than untreated controls. No measurable impacts on bees from exposure to squash treated with thiamethoxam as a seed-coating or foliage sprayed with chlorantraniliprole were found. Our results demonstrate important sublethal effects of field-realistic exposure to a soil-applied neonicotinoid (imidacloprid) on bee behaviour and reproductive success. Soil must be considered a potential route of pesticide exposure in risk assessments, and restrictions on soil-applied insecticides may be justified, to mitigate impacts on ground-nesting solitary bee populations and the crop pollination services they provide.

Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees.

Recent concern over global pollinator declines has led to considerable research on the effects of pesticides on bees. Although pesticides are typically not encountered at lethal levels in the field, there is growing evidence indicating that exposure to field-realistic levels can have sublethal effects on bees, affecting their foraging behaviour, homing ability and reproductive success. Bees are essential for the pollination of a wide variety of crops and the majority of wild flowering plants, but until now research on pesticide effects has been limited to direct effects on bees themselves and not on the pollination services they provide. Here we show the first evidence to our knowledge that pesticide exposure can reduce the pollination services bumblebees deliver to apples, a crop of global economic importance. Bumblebee colonies exposed to a neonicotinoid pesticide provided lower visitation rates to apple trees and collected pollen less often. Most importantly, these pesticide-exposed colonies produced apples containing fewer seeds, demonstrating a reduced delivery of pollination services. Our results also indicate that reduced pollination service delivery is not due to pesticide-induced changes in individual bee behaviour, but most likely due to effects at the colony level. These findings show that pesticide exposure can impair the ability of bees to provide pollination services, with important implications for both the sustained delivery of stable crop yields and the functioning of natural ecosystems.

Combined pesticide exposure severely affects individual- and colony-level traits in bees.

Reported widespread declines of wild and managed insect pollinators have serious consequences for global ecosystem services and agricultural production. Bees contribute approximately 80% of insect pollination, so it is important to understand and mitigate the causes of current declines in bee populations . Recent studies have implicated the role of pesticides in these declines, as exposure to these chemicals has been associated with changes in bee behaviour and reductions in colony queen production. However, the key link between changes in individual behaviour and the consequent impact at the colony level has not been shown. Social bee colonies depend on the collective performance of many individual workers. Thus, although field-level pesticide concentrations can have subtle or sublethal effects at the individual level, it is not known whether bee societies can buffer such effects or whether it results in a severe cumulative effect at the colony level. Furthermore, widespread agricultural intensification means that bees are exposed to numerous pesticides when foraging, yet the possible combinatorial effects of pesticide exposure have rarely been investigated. Here we show that chronic exposure of bumblebees to two pesticides (neonicotinoid and pyrethroid) at concentrations that could approximate field-level exposure impairs natural foraging behaviour and increases worker mortality leading to significant reductions in brood development and colony success. We found that worker foraging performance, particularly pollen collecting efficiency, was significantly reduced with observed knock-on effects for forager recruitment, worker losses and overall worker productivity. Moreover, we provide evidence that combinatorial exposure to pesticides increases the propensity of colonies to fail.

Pollen foraging: learning a complex motor skill by bumblebees (Bombus terrestris).

To investigate how bumblebees (Bombus terrestris) learn the complex motor skills involved in pollen foraging, we observed naïve workers foraging on arrays of nectarless poppy flowers (Papaver rhoeas) in a greenhouse. Foraging skills were quantified by measuring the pollen load collected during each foraging bout and relating this to the number of flowers visited and bout duration on two consecutive days. The pollen standing crop (PSC) in each flower decreased drastically from 0530 to 0900 hours. Therefore, we related foraging performance to the changing levels of pollen available (per flower) and found that collection rate increased over the course of four consecutive foraging bouts (comprising between 277 and 354 individual flower visits), suggesting that learning to forage for pollen represents a substantial time investment for individual foragers. The pollen collection rate and size of pollen loads collected at the start of day 2 were markedly lower than at the end of day 1, suggesting that components of pollen foraging behaviour could be subject to imperfect overnight retention. Our results suggest that learning the necessary motor skills to collect pollen effectively from morphologically simple flowers takes three times as many visits as learning how to handle the most morphologically complex flowers to extract nectar, potentially explaining why bees are more specialised in their choice of pollen flowers.