Hallmann, C. A. et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12, e0185809 (2017).
Google Scholar
Sánchez-Bayo, F. & Wyckhuys, K. A. G. Worldwide decline of the entomofauna: a review of its drivers. Biol. Conserv. 232, 8–27 (2019).
Google Scholar
Wagner, D. L. Insect declines in the Anthropocene. Annu. Rev. Entomol. 65, 457–480 (2020).
Google Scholar
Michener, C. D. The Bees of the World. (The Johns Hopkins University Press, 2007).
Biesmeijer, J. C. et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science (80-. ). 313, 351–354 (2006).
Nieto, A. et al. European Red List of Bees. IUCN Global Species Programm (Publication Office of the European Union, 2014). https://doi.org/10.2779/77003.
Zattara, E. E. & Aizen, M. A. Worldwide occurrence records suggest a global decline in bee species richness. One Earth 4, 114–123 (2021).
Google Scholar
Ollerton, J., Winfree, R. & Tarrant, S. How many flowering plants are pollinated by animals?. Oikos 120, 321–326 (2011).
Google Scholar
Klein, A. M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 274, 303–313 (2007).
Google Scholar
Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science (80-. ). 347, 1255957 (2015).
Kremen, C., Williams, N. M. & Thorp, R. W. Crop pollination from native bees at risk from agricultural intensification. Proc. Natl. Acad. Sci. U. S. A. 99, 16812–16816 (2002).
Google Scholar
Mullin, C. A. et al. High levels of miticides and agrochemicals in north American apiaries: implications for honey bee health. PLoS ONE 5, e9754 (2010).
Google Scholar
Tosi, S., Costa, C., Vesco, U., Quaglia, G. & Guido, G. A 3-year survey of Italian honey bee-collected pollen reveals widespread contamination by agricultural pesticides. Sci. Total Environ. 615, 208–218 (2018).
Google Scholar
Cedergreen, N. Quantifying synergy: A systematic review of mixture toxicity studies within environmental toxicology. PLoS ONE 9, e96580 (2014).
Google Scholar
Thompson, H. M., Fryday, S. L., Harkin, S. & Milner, S. Potential impacts of synergism in honeybees (Apis mellifera) of exposure to neonicotinoids and sprayed fungicides in crops. Apidologie 45, 545–553 (2014).
Google Scholar
Carnesecchi, E. et al. Investigating combined toxicity of binary mixtures in bees: Meta-analysis of laboratory tests, modelling, mechanistic basis and implications for risk assessment. Environ. Int. 133, 105256 (2019).
Google Scholar
Sgolastra, F. et al. Bees and pesticide regulation: Lessons from the neonicotinoid experience. Biol. Conserv. 241, 108356 (2020).
Google Scholar
Arena, M. & Sgolastra, F. A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23, 324–334 (2014).
Google Scholar
Uhl, P., Awanbor, O., Schulz, R. S. & Brühl, C. A. Osmia bicornis is rarely an adequate regulatory surrogate species. Comparing its acute sensitivity towards multiple insecticides with regulatory Apis mellifera endpoints . bioRxiv 366237 (2018). https://doi.org/10.1101/366237.
Heard, M. S. et al. Comparative toxicity of pesticides and environmental contaminants in bees: Are honey bees a useful proxy for wild bee species?. Sci. Total Environ. 578, 357–365 (2017).
Google Scholar
Biddinger, D. J. et al. Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS One 8, e72587 (2013).
Robinson, A. et al. Comparing bee species responses to chemical mixtures: Common response patterns?. PLoS ONE 12, e0176289 (2017).
Google Scholar
FAO. Fluxapyroxad (256). 659–926 (2015). Available at: http://www.fao.org/fileadmin/templates/agphome/documents/Pests_Pesticides/JMPR/Evaluation12/Fluxapyroxad.pdf.
Bénit, P. et al. Evolutionarily conserved susceptibility of the mitochondrial respiratory chain to SDHI pesticides and its consequence on the impact of SDHIs on human cultured cells. PLoS ONE 14, e0224132 (2019).
Google Scholar
EFSA. Conclusion on the peer review of the pesticide risk assessment of the active substance fluxapyroxad (BAS 700 F). EFSA J. 10, 2522 (2012).
Sierotzki, H. & Scalliet, G. A review of current knowledge of resistance aspects for the next-generation succinate dehydrogenase inhibitor fungicides. Phytopathology 103, 880–887 (2013).
Google Scholar
Zhu, Y. et al. Discovery and characterization of sulfoxaflor, a novel insecticide targeting sap-feeding pests. J. Agric. Food Chem. 59, 2950–2957 (2011).
Google Scholar
Sparks, T. C. et al. Sulfoxaflor and the sulfoximine insecticides: Chemistry, mode of action and basis for efficacy on resistant insects. Pestic. Biochem. Physiol. 107, 1–7 (2013).
Google Scholar
Brown, M. J. F. et al. A horizon scan of future threats and opportunities for pollinators and pollination. PeerJ 4, e2249 (2016).
Google Scholar
Siviter, H., Brown, M. J. F. & Leadbeater, E. Sulfoxaflor exposure reduces bumblebee reproductive success. Nature 561, 109–112 (2018).
Google Scholar
Siviter, H., Horner, J., Brown, M. J. F. & Leadbeater, E. Sulfoxaflor exposure reduces egg laying in bumblebees Bombus terrestris. J. Appl. Ecol. 57, 160–169 (2019).
Google Scholar
Siviter, H. et al. No evidence for negative impacts of acute sulfoxaflor exposure on bee olfactory conditioning or working memory. PeerJ 7, e7208 (2019).
Google Scholar
Cheng, Y. et al. A semi-field study to evaluate effects of sulfoxaflor on honey bee (Apis mellifera). Bull. Insectol. 71, 225–233 (2018).
Zhu, Y. C., Yao, J., Adamczyk, J. & Luttrell, R. Synergistic toxicity and physiological impact of imidacloprid alone and binary mixtures with seven representative pesticides on honey bee (Apis mellifera). PLoS ONE 12, e0176837 (2017).
Google Scholar
Zhu, Y. C., Yao, J., Adamczyk, J. & Luttrell, R. Feeding toxicity and impact of imidacloprid formulation and mixtures with six representative pesticides at residue concentrations on honey bee physiology (Apis mellifera). PLoS ONE 12, e0178421 (2017).
Google Scholar
Thompson, H. M., Wilkins, S., Harkin, S., Milner, S. & Walters, K. F. A. Neonicotinoids and bumblebees (Bombus terrestris): effects on nectar consumption in individual workers. Pest Manag. Sci. 71, 946–950 (2015).
Google Scholar
Cresswell, J. E. et al. Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology 115, 365–371 (2012).
Google Scholar
Azpiazu, C. et al. Chronic oral exposure to field-realistic pesticide combinations via pollen and nectar: effects on feeding and thermal performance in a solitary bee. Sci. Rep. 9, 13770 (2019).
Google Scholar
Berenbaum, M. R. & Johnson, R. M. Xenobiotic detoxification pathways in honey bees. Curr. Opin. Insect Sci. 10, 51–58 (2015).
Google Scholar
Therneau, T. M. Package ‘ survival ’. (2020).
Demidenko, E. & Miller, T. W. Statistical determination of synergy based on Bliss definition of drugs independence. PLoS ONE 14, 1–22 (2019).
Google Scholar
Casida, J. E. Neonicotinoids and other insect nicotinic receptor competitive modulators: progress and prospects. Annu. Rev. Entomol. 63, 125–144 (2018).
Google Scholar
Matsuda, K., Ihara, M. & Sattelle, D. B. Neonicotinoid insecticides: molecular targets, resistance, and toxicity. Annu. Rev. Pharmacol. Toxicol. 60, 241–255 (2020).
Google Scholar
Sanchez-Bayo, F. & Goka, K. Pesticide residues and bees-a risk assessment. PLoS ONE 9, e94482 (2014).
Google Scholar
Sgolastra, F. et al. Synergistic mortality between a neonicotinoid insecticide and an ergosterol-biosynthesis-inhibiting fungicide in three bee species. Pest Manag. Sci. 73, 1236–1243 (2017).
Google Scholar
Lewis, K. A., Tzilivakis, J., Warner, D. J. & Green, A. An international database for pesticide risk assessments and management. Hum. Ecol. Risk Assess. An Int. J. 22, 1050–1064 (2016).
Lambert, O. et al. Widespread occurrence of chemical residues in beehive matrices from apiaries located in different landscapes of western France. PLoS ONE 8, e67007 (2013).
Google Scholar
Iwasa, T., Motoyama, N., Ambrose, J. T. & Roe, R. M. Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee. Apis mellifera. Crop Prot. 23, 371–378 (2004).
Google Scholar
Sgolastra, F. et al. Combined exposure to sublethal concentrations of an insecticide and a fungicide affect feeding, ovary development and longevity in a solitary bee. Proc. R. Soc. B Biol. Sci. 285, 20180887 (2018).
Google Scholar
Tosi, S. & Nieh, J. C. Lethal and sublethal synergistic effects of a new systemic pesticide, flupyradifurone (Sivantow), on honeybees. Proc. R. Soc. B Biol. Sci. 286, 20190433 (2019).
Google Scholar
Johnson, R. M., Dahlgren, L., Siegfried, B. D. & Ellis, M. D. Acaricide, Fungicide and Drug Interactions in Honey Bees (Apis mellifera). PLoS ONE 8, e54092 (2013).
Google Scholar
Tsvetkov, N. et al. Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science (80-. ). 356, 1395–1397 (2017).
Uhl, P., Awanbor, O., Schulz, R. S. & Brühl, C. A. Osmia bicornis is rarely an adequate regulatory surrogate species. Comparing its acute sensitivity towards multiple insecticides with regulatory Apis mellifera endpoints. PLoS One 14, e0201081 (2019).
Beadle, K. et al. Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis. 1–19 (2019).
Hayward, A. et al. The leafcutter bee, Megachile rotundata, is more sensitive to N-cyanoamidine neonicotinoid and butenolide insecticides than other managed bees. Nat. Ecol. Evol. 3, 1521–1524 (2019).
Google Scholar
EPA. Ecological Risk Assessment for the Registration Review of Sulfoxaflor. United States Environ. Prot. Agency (2019).
EFSA. Peer review of the pesticide risk assessment for the active substance sulfoxaflor in light of confirmatory data submitted. EFSA J. 17, e05633 (2019).
Mundy-Heisz, K. A., Prosser, R. S. & Raine, N. E. Acute oral toxicity and risks of exposure to the neonicotinoid thiamethoxam, and other classes of systemic insecticide, for the Common Eastern Bumblebee (Bombus impatiens). bioRxiv (2020). https://doi.org/10.1101/2020.01.27.921510.
EFSA. European Food Safety Authority. Guidance on the risk assessment of plant protection products on bees (Apis mellifera , Bombus spp. and solitary bees). EFSA J. 11, 3295 (2013).
Sgolastra, F. et al. Pesticide exposure assessment paradigm for solitary bees. Environ. Entomol. 48, 22–35 (2019).
Google Scholar
Gradish, A. E. et al. Comparison of pesticide exposure in honey bees (Hymenoptera: Apidae) and bumble bees (Hymenoptera: Apidae): implications for risk assessments. Environ. Entomol. 48, 12–21 (2019).
Google Scholar
Chan, D. S. W., Prosser, R. S., Rodríguez-Gil, J. L. & Raine, N. E. Assessment of risk to hoary squash bees (Peponapis pruinosa) and other ground-nesting bees from systemic insecticides in agricultural soil. Sci. Rep. 9, 1–13 (2019).
Boyle, N. K. & Pitts-Singer, T. L. Assessing blue orchard bee (Osmia lignaria) propagation and pollination services in the presence of honey bees (Apis mellifera) in Utah tart cherries. PeerJ 7, e7639 (2019).
Google Scholar
Franklin, E. L. & Raine, N. E. Moving beyond honeybee-centric pesticide risk assessments to protect all pollinators. Nat. Ecol. Evol. 3, 1373–1375 (2019).
Google Scholar
OECD. Test No. 213: Honeybees, Acute Oral Toxicity Test. (OECD Guidelines for the Testing of Chemicals, Section 2, 1998). https://doi.org/10.1787/9789264070165-en.
OECD. Test No. 247: Bumblebee, Acute Oral Toxicity Test. (OECD Guidelines for the Testing of Chemicals, Section 2, 2017). https://doi.org/10.1787/9789264284128-en.
Medrzycki, P. et al. Standard methods for toxicology research in Apis mellifera. J. Apic. Res. 52, 1–60 (2013).
Google Scholar
Brandt, A. et al. Immunosuppression response to the neonicotinoid insecticide thiacloprid in females and males of the red mason bee Osmia bicornis L. Sci. Rep. 10, 4670 (2020).
Google Scholar
Ladurner, E., Bosch, J., Maini, S. & Kemp, W. P. A method to feed individual bees (Hymenoptera: Apiformes) known amounts of pesticides. Apidologie 34, 597–602 (2003).
Google Scholar
Kassambara, A., Kosinski, M., Biecek, P. & Fabian, S. Package ‘survminer’. The Comprehensive R Archive Network (2020).
Oller, R. & Langohr, K. FHtest : An R Package for the Comparison of Survival Curves with Censored Data . J. Stat. Softw. 81, (2017).
Robertson, J. L., Russell, R. M., Preisler, H. K. & Savin, N. E. Bioassays with Arthropods. (CRC Press, 2007).
Jonker, M. J., Svendsen, C., Bedaux, J. J. M., Bongers, M. & Kammenga, J. E. Significance testing of synergistic/antagonistic, dose level-dependent, or dose ratio-dependent effects in mixture dose-response analysis. Environ. Toxicol. Chem. 24, 2701–2713 (2005).
Google Scholar
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