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Neonicotinoid Exposure Affects Foraging, Nesting, and Reproductive Success of Ground-Nesting 2 Solitary Bees

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Neonicotinoid Exposure Affects Foraging, Nesting, and Reproductive Success of Ground-Nesting 2 Solitary Bees bioRxiv preprint doi: https://doi.org/10.1101/2020.10.07.330605; this version posted October 8, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Neonicotinoid exposure affects foraging, nesting, and reproductive success of ground-nesting 2 solitary bees 3 D. Susan Willis Chan1, Nigel E. Raine1 4 1School of Environmental Sciences, University of Guelph, Guelph, Ontario, N1G 2W1, Canada 5 Email: [email protected]; [email protected] 6 Despite their indispensable role in food production1,2, insect pollinators are 7 threatened by multiple environmental stressors, including pesticide exposure2-4. Although 8 honeybees are important, most pollinating insect species are wild, solitary, ground-nesting 9 bees1,4-6 that are inadequately represented by honeybee-centric regulatory pesticide risk 10 assessment frameworks7,8. Here, for the first time, we evaluate the effects of realistic 11 exposure to systemic insecticides (imidacloprid, thiamethoxam or chlorantraniliprole) on a 12 ground-nesting bee species in a semi-field experiment. Hoary squash bees (Eucera 13 (Peponapis) pruinosa) provide essential pollination services to North American pumpkin 14 and squash crops9-14 and commonly nest within cropping areas10, placing them at risk of 15 exposure to pesticides in soil8,10, nectar and pollen15,16. Hoary squash bees exposed to an 16 imidacloprid-treated crop initiated 85% fewer nests, left 84% more pollen unharvested, 17 and produced 89% fewer offspring than untreated controls. We found no measurable 18 impact on squash bees from exposure to thiamethoxam- or chlorantraniliprole-treated 19 crops. Our results demonstrate important sublethal effects of field-realistic exposure to a 20 soil-applied neonicotinoid (imidacloprid) on the behaviour and reproductive success of a 21 ground-nesting solitary bee. To prevent potential declines in ground-nesting bee 22 populations and associated impoverishment of crop pollination services, soil must be bioRxiv preprint doi: https://doi.org/10.1101/2020.10.07.330605; this version posted October 8, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 23 considered a possible route of pesticide exposure for bees, and restrictions on soil-applied 24 insecticides may be justified. 25 Main text: 26 Conserving pollinator biodiversity is becoming increasingly important with rising human 27 demand for insect-pollinated crops1,2,17-19. Associated losses of pollination services will be 28 particularly detrimental for growers of crops like pumpkin, squash, and gourds (Cucurbita crops) 29 that are entirely dependent upon pollination by bees to set fruit20,21. 30 Among the most efficient and widely distributed wild pollinator of Cucurbita crops in 31 North America is the solitary hoary squash bee (Eucera (Peponapis) pruinosa (Say, 1837))11- 32 12,21-24. This species exhibits an unusually high degree of dietary specialization, depending 33 entirely upon Cucurbita crops (Cucurbitaceae) for pollen across most of its range22,23,25. Each 34 hoary squash bee female constructs its own nest in the ground26,27, commonly within cropping 35 areas10 where systemic insecticides are often applied as soil drenches or seed treatments8. 36 Historically almost all information on impacts of pesticide exposure for bees has come 37 from honeybees (Apis mellifera Linnaeus, 1758), the model species for insect pollinator pesticide 38 risk assessments4,7,28,29. More recently, exposure to field-realistic levels of systemic 39 neonicotinoid insecticides have been shown to have adverse effects on learning and memory30,31, 40 foraging behaviour32-35, colony establishment36,37, reproductive success38-40, and the delivery of 41 pollination services41,42 in bumblebees (Bombus spp.). 42 Although non-social bees have received less attention, adverse effects from exposure to 43 neonicotinoids on nest establishment40, homing ability43, reproductive output44, developmental 44 delays45, and reduced adult size and longevity45 have been demonstrated for cavity-nesting 45 solitary bees. bioRxiv preprint doi: https://doi.org/10.1101/2020.10.07.330605; this version posted October 8, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 46 While all bees that forage on treated crops may be at risk of exposure to systemic pesticide 47 residues in pollen and nectar28,29, there is an additional risk of exposure to residues in soil for 48 ground-nesting bees4,8. This route of pesticide exposure is currently not considered in regulatory 49 environmental risk assessments for pollinators because honeybees rarely come into direct contact 50 with soil3,4,7,8. Although approximately 70% of solitary bee species nest in the ground4,46 where 51 they spend most of their lives8,46, and many of these are associated with agriculture1,4-6,21,23, no 52 studies have yet evaluated potential impacts of pesticide exposure on this highly significant 53 group of insect pollinators. 54 We are the first to evaluate the potential effects of exposure to a crop treated with one of 55 three different systemic insecticides (neonicotinoids imidacloprid or thiamethoxam or the 56 anthranilic diamide chlorantraniliprole) on nest establishment, foraging behaviour and offspring 57 production for a solitary, ground-nesting bee in a semi-field hoop house study. 58 To assess the impacts on wild squash bees of field realistic systemic insecticide exposure 59 we grew squash plants (Cucurbita pepo) in twelve netted hoop houses. We applied Admire® 60 (imidacloprid) as a soil drench at seeding to three hoop houses; planted FarMoreFI400® 61 (thiamethoxam + fungicides: Cruiser 5FS® + Apron XL®, Maxim 4FS® and Dynasty®) treated 62 seeds in three more hoop houses; applied Coragen® (chlorantraniliprole) as a foliar spray to 63 another three hoop houses, with the remaining three hoop houses left untreated as insecticide 64 controls (Methods; Extended Data; Fig. 1). 65 We introduced mated female hoary squash bees into each hoop house at crop bloom (i.e., 66 8-weeks later: Methods). After mating, hoary squash bee females begin their nesting phase 67 involving three critical overlapping activities: (1) soil excavation and nest establishment; (2) 68 foraging for pollen and nectar to provision nest cells; and (3) laying eggs26,27. bioRxiv preprint doi: https://doi.org/10.1101/2020.10.07.330605; this version posted October 8, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 69 To determine if exposure to squash crops treated with systemic insecticides interfered 70 with nest establishment, we tracked the number of active nests made by foundress (2017) and 71 second generation (2018) females in each hoop house (Methods). Nest establishment was 72 substantially affected by insecticide treatment (F3,14 = 7.33; p = 0.0034; Table S1; Table S2), 73 with significantly fewer nests established in the Admire®-treated hoop houses than in other 74 treatments (mean ± SE: Admire®: 1.50 ± 1.31; Control: 9.83 ± 2.21; Coragen®: 9.83 ± 1.01; 75 FarMoreF1400®: 9.83 ± 2.20; Fig. 1; Table 1). Compared to the untreated control, nest 76 establishment by hoary squash bees exposed to Admire®-treated squash crops was reduced by 77 76% in 2017 (mean ± SE: Admire®: 0.33 ± 0.33; Control: 8.67 ± 2.60), 96% in 2018 (Admire®: 78 2.67 ± 2.67; Control: 11.00 ± 4.04) with an 85% reduction across both years (Admire® vs 79 Control: t13 = -3.83, p = 0.0088; Fig. 1; Table 1; Table S3). We detected no significant 80 differences in the numbers of nests established by females in the control, Coragen®, and 81 FarMoreF1400® treatments (Table 1; Table S3). 82 These results are consistent with studies indicating neonicotinoid-exposure can reduce 83 nesting activity in stem-nesting solitary bees40,44 and delay or reduce the likelihood of nest 84 establishment in bumblebees36,37,47. Our study is the first to report an impact of neonicotinoid- 85 exposure on nesting in any solitary ground-nesting species, arguably the most ecologically 86 important and biodiverse group of bees. The 85% reduction in nest establishment (over 2 years) 87 by squash bee females exposed to imidacloprid under real agricultural conditions incorporates 88 both contact with soil and consumption of contaminated nectar and pollen as potential routes of 89 exposure, whilst previous studies have focused solely on oral exposure36,37,40,44,47. 90 During their nesting phase, hoary squash bees also amass pollen to provision their nest 91 cells. The reproductive success of female solitary bees is limited by the number of nest cells bioRxiv preprint doi: https://doi.org/10.1101/2020.10.07.330605; this version posted October 8, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 92 they can provision44,46, and the amount of pollen harvested affects the subsequent reproductive 93 success of their offspring48-50. 94 To determine if exposure to crops treated with systemic insecticides affected pollen 95 harvesting by female hoary squash bees, we counted the pollen remaining on anthers of squash 96 flowers at the end of the daily foraging period in each hoop house (Methods; Extended Data 97 Table 1). Pollen collection was substantially affected by insecticide treatment (F3,114 = 37.82; p < 98 0.0001; Table S1; Table S2) with 84% more unharvested pollen remaining on anthers in the 99 Admire®-treatment than the control (Admire®: 13662.0 ± 1179.6; Control: 2168.0 ± 461.5; t114 100 = 9.38, p < 0.0001; Fig. 2; Table S3). Although hoary squash bees in the Coragen® treatment 101 also collected significantly less pollen than bees in the control group (Coragen®: 5422.0 ± 102 1075.4; Control: 2168.0 ± 461.5; t114 = -2.65, p = 0.0443; Table 1; Table S3), nest establishment 103 appeared unaffected (Table S2).
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