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.
Using the hoary squash bee ( Peponapis pruinosa ) as a model, we provide the first probabilistic risk assessment of exposure to systemic insecticides in soil for ground-nesting bees. To assess risk in acute and chronic exposure scenarios in Cucurbita and field crops, concentrations of clothianidin, thiamethoxam and imidacloprid (neonicotinoids) and chlorantraniliprole (anthranilic diamide) in cropped soil were plotted to produce an environmental exposure distribution for each insecticide. The probability of exceedance of several exposure endpoints (LC 50 s) was compared to an acceptable risk threshold (5%). In Cucurbita crops, under acute exposure, risk to hoary squash bees was below 5% for honey bee LC 50 s for all residues evaluated but exceeded 5% for clothianidin and imidacloprid using a solitary bee LC 50 . For Cucurbita crops in the chronic exposure scenario, exposure risks for clothianidin and imidacloprid exceeded 5% for all endpoints, and exposure risk for chlorantraniliprole was below 5% for all endpoints. In field crops, risk to ground-nesting bees was high from clothianidin in all exposure scenarios and high for thiamethoxam and imidacloprid under chronic exposure scenarios. Risk assessments for ground-nesting bees should include exposure impacts from pesticides in soil and could use the hoary squash bee as an ecotoxicology model.
This is an open access article under the terms of the Creat ive Commo ns Attri bution-NonCo mmercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
The increasing demand for insect-pollinated crops highlights the need for crop pollination paradigms that include all available pollinators. In North America, Cucurbita crops (pumpkin, squash) depend on both wild (solitary and Bombus spp.: Hymenoptera: Apidae) and managed honey bees (Apis mellifera L. 1758: Hymenoptera: Apidae) for pollination. Temporal and spatial differences in abundance may determine which bee taxa are the most important pollinators of Cucurbita crops. We surveyed bees visiting Cucurbita crop flowers on 19 farms over four years (2015–2018) during the crop flowering period (July 1–August 30 from 06:00–12:00). All the farms surveyed had hoary squash bees (Eucera pruinosa (Say, 1867), and most also had some combination of honey bees, bumble bees (Bombus spp.), or other wild bees present on their Cucurbita crop flowers. All four bee taxa were present on about two-thirds of farms. Spatially and temporally, wild bees were more abundant on Cucurbita crop flowers than managed honey bees. Hoary squash bees were the most abundant wild bees, maintaining their abundance relative to other wild bee taxa year-over-year. Male hoary squash bees were both more frequently and consistently seen visiting crop flowers than females in all years. Peak activity of hoary squash bees and bumble bees coincided with the daily crop pollination window, whereas peak activity of honey bees and other wild bees occurred after that window. In addition to elucidating the ecological interactions among wild and managed pollinators on Cucurbita crops, our work provides a novel practical way to evaluate pollinator abundance using a crop-centered benchmark framework.
Considering the critical importance of insect pollination to food security and documented declines in wild bee populations, it is imperative to develop effective conservation and management strategies that promote the health of wild bee communities associated with agroecosystems. Identifying wild bee visitors of crops, including crop-flower visitors and species that nest within cropping areas, may prove critical to this endeavor as optimal conservation strategies may differ among bee species and/or guilds, regions, and cropping systems. Although lists of bee species that are associated with North American crops are scattered throughout the literature, there is a need for a comprehensive compilation of those species by crop, region, and nesting guild. Here, we searched the literature to compile a list of wild bee species associated with 33 major crops in North America and assessed the overlap in bee species communities among crops and regions. Of the 739 crop-associated bee species retrieved, 405 species (54.8%) were ground nesters, and 438 species (59.3%) were identified as crop-flower visitors of at least one crop. Because of their nesting and foraging behavior, we argue that these species are more likely to be exposed to agricultural pesticide residues than bee species that do not nest in the ground or feed directly on crop flowers. We further compiled lists of wild bees that have been found to be associated with all of the four most surveyed perennial fruit crops (apple, blueberry, cranberry, strawberry) and all of the three most surveyed cucurbit crops (cucumber, Cucurbita, watermelon) in eastern North America. These lists of bee species can be used to focus attention on species needing better protection strategies within agroecosystems, especially for these two important North American crop groups and can also inform the development of multi-species pesticide risk assessment schemes.
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