GitHub

Introduction
Reviews on pollinators and neonicotinoid insecticides
Highly cited
Decline of insect pollinators
Exposure of insect pollinators to neonicotinoids
Pesticide levels in pollen and nectar
Dosage effects
Gene expression
nAChRs
Pesticides
Larval exposure
Routes of exposure
Economic value
Methylation
Testing practices

Introduction

Literature on the impacts of various groups of pesticides on insect pollinators. General trends in population declines

Reviews on pollinators and neonicotinoid insecticides

Bass, C., Field, L.M., 2018. Neonicotinoids. Current Biology 28, R772–R773. https://doi.org/10.1016/j.cub.2018.05.061
Berenbaum, M.R., Johnson, R.M., 2015. Xenobiotic detoxification pathways in honey bees. Current Opinion in Insect Science 10, 51–58. https://doi.org/10.1016/j.cois.2015.03.005
Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., Schaffers, A.P., Potts, S.G., Kleukers, R., Thomas, C.D., Settele, J., Kunin, W.E., 2006. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354. https://doi.org/10.1126/science.1127863
Blacquière, T., Smagghe, G., van Gestel, C.A.M., Mommaerts, V., 2012. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21, 973–992. https://doi.org/10.1007/s10646-012-0863-x
Brown, M.J.F., Dicks, L.V., Paxton, R.J., Baldock, K.C.R., Barron, A.B., Chauzat, M.-P., Freitas, B.M., Goulson, D., Jepsen, S., Kremen, C., Li, J., Neumann, P., Pattemore, D.E., Potts, S.G., Schweiger, O., Seymour, C.L., Stout, J.C., 2016. A horizon scan of future threats and opportunities for pollinators and pollination. PeerJ 4, e2249. https://doi.org/10.7717/peerj.2249
Cameron, S.A., Sadd, B.M., 2020. Global trends in bumble bee health. Annual Review of Entomology 65, null. https://doi.org/10.1146/annurev-ento-011118-111847
Casida, J.E., 2018. Neonicotinoids and other insect nicotinic receptor competitive modulators: progress and prospects. Annual Review of Entomology 63, 125–144. https://doi.org/10.1146/annurev-ento-020117-043042
Carreck, N.L., 2017. A beekeeper’s perspective on the neonicotinoid ban. Pest Management Science 73, 1295–1298. https://doi.org/10.1002/ps.4489
Cressey, D., 2017. The bitter battle over the world’s most popular insecticides. Nature 551, 156–158. https://doi.org/10.1038/551156a
Cressey, D., 2015. Bee studies stir up pesticide debate. Nature 520, 416–416. https://doi.org/10.1038/520416a
Cressey, D., 2013. Europe debates risk to bees. Nature 496, 408–408. https://doi.org/10.1038/496408a
Cullen, M.G., Thompson, L.J., Carolan, J.C., Stout, J.C., Stanley, D.A., 2019. Fungicides, herbicides and bees: a systematic review of existing research and methods. PLOS ONE 14, e0225743. https://doi.org/10.1371/journal.pone.0225743
Dani, J.A., Bertrand, D., 2007. Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annual Review of Pharmacology and Toxicology 47, 699–729. https://doi.org/10.1146/annurev.pharmtox.47.120505.105214
Desneux, N., Decourtye, A., Delpuech, J.-M., 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology 52, 81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440
Dicks, L.V., Viana, B., Bommarco, R., Brosi, B., Arizmendi, M. del C., Cunningham, S.A., Galetto, L., Hill, R., Lopes, A.V., Pires, C., Taki, H., Potts, S.G., 2016. Ten policies for pollinators. Science 354, 975–976. https://doi.org/10.1126/science.aai9226
Dupuis, J., Louis, T., Gauthier, M., Raymond, V., 2012. Insights from honeybee (Apis mellifera) and fly (Drosophila melanogaster) nicotinic acetylcholine receptors: From genes to behavioral functions. Neuroscience & Biobehavioral Reviews 36, 1553–1564. https://doi.org/10.1016/j.neubiorev.2012.04.003
Eisenstein, M., 2015. Pesticides: seeking answers amid a toxic debate. Nature 521, S52–S55. https://doi.org/10.1038/521S52a
Feyereisen, R., 2012. Insect CYP genes and P450 enzymes. Insect Molecular Biology and Biochemistry 236–316. https://doi.org/10.1016/B978-0-12-384747-8.10008-X
Feyereisen, R., 2015. Insect P450 inhibitors and insecticides: challenges and opportunities. Pest Management Science 71, 793–800. https://doi.org/10.1002/ps.3895
Feyereisen, R., 2018. Bee P450s take the sting out of cyanoamidine neonicotinoids. Current Biology 28, R560–R562. https://doi.org/10.1016/j.cub.2018.03.013
ffrench-Constant, R.H., Daborn, P.J., Goff, G.L., 2004. The genetics and genomics of insecticide resistance. Trends in Genetics 20, 163–170. https://doi.org/10.1016/j.tig.2004.01.003
Godfray, H.C.J., Blacquière, T., Field, L.M., Hails, R.S., Petrokofsky, G., Potts Simon G., Raine Nigel E., Vanbergen Adam J., McLean Angela R., 2014. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proceedings of the Royal Society B: Biological Sciences 281, 20140558. https://doi.org/10.1098/rspb.2014.0558
Godfray, H.C.J., Blacquière, T., Field, L.M., Hails, R.S., Potts, S.G., Raine, N.E., Vanbergen, A.J., McLean, A.R., 2015. A restatement of recent advances in the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proceedings of the Royal Society B: Biological Sciences 282, 20151821. https://doi.org/10.1098/rspb.2015.1821
Goulson, D., Lye, G.C., Darvill, B., 2008. Decline and conservation of bumble bees. Annual Review of Entomology 53, 191–208. https://doi.org/10.1146/annurev.ento.53.103106.093454
Goulson, D., 2013. An overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology 50, 977–987. https://doi.org/10.1111/1365-2664.12111
Goulson, D., Nicholls, E., Botias, C., Rotheray, E.L., 2015. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957–1255957. https://doi.org/10.1126/science.1255957
Goulson, D., 2019. The insect apocalypse, and why it matters. Current Biology 29, R967–R971. https://doi.org/10.1016/j.cub.2019.06.069
Gradish, A.E., van der Steen, J., Scott-Dupree, C.D., Cabrera, A.R., Cutler, G.C., Goulson, D., Klein, O., Lehmann, D.M., Lückmann, J., O’Neill, B., Raine, N.E., Sharma, B., Thompson, H., 2019. Comparison of pesticide exposure in honey bees (Hymenoptera: Apidae) and bumblebees (Hymenoptera: Apidae): Implications for risk assessments. Environmental Entomology 48, 12–21. https://doi.org/10.1093/ee/nvy168
Grozinger, C.M., Robinson, G.E., 2015. The power and promise of applying genomics to honey bee health. Current Opinion in Insect Science 10, 124–132. https://doi.org/10.1016/j.cois.2015.03.007
Grozinger, C.M., Zayed, A., 2020. Improving bee health through genomics. Nature Reviews Genetics 1–15. https://doi.org/10.1038/s41576-020-0216-1
Grünewald, B., Siefert, P., 2019. Acetylcholine and its receptors in honeybees: involvement in development and impairments by neonicotinoids. Insects 10, 420. https://doi.org/10.3390/insects10120420
Gonzalez-Varo, J.P., Biesmeijer, J.C., Bommarco, R., Potts, S.G., Schweiger, O., Smith, H.G., Steffan-Dewenter, I., Szentgyörgyi, H., Woyciechowski, M., Vilà, M., 2013. Combined effects of global change pressures on animal-mediated pollination. Trends in Ecology & Evolution 28, 524–530. https://doi.org/10.1016/j.tree.2013.05.008
Gross, M., 2018. Bee worries beyond neonicotinoids. Current Biology 28, R1121–R1123. https://doi.org/10.1016/j.cub.2018.09.045
Gross, M., 2014. Systemic pesticide concerns extend beyond the bees. Current Biology 24, R717–R720. https://doi.org/10.1016/j.cub.2014.07.071
Hawkins, N.J., Bass, C., Dixon, A., Neve, P., 2019. The evolutionary origins of pesticide resistance. Biological Reviews 94, 135–155. https://doi.org/10.1111/BRV.12440
Ihara, M., Matsuda, K., 2018. Neonicotinoids: Molecular mechanisms of action, insights into resistance and impact on pollinators. Current Opinion in Insect Science 30, 86–92. https://doi.org/10.1016/J.COIS.2018.09.009
Jeschke, P., Nauen, R., 2008. Neonicotinoids - from zero to hero in insecticide chemistry. Pest Management Science 64, 1084–1098. https://doi.org/10.1002/ps.1631
Jeschke, P., Nauen, R., Schindler, M., Elbert, A., 2011. Overview of the status and global strategy for neonicotinoids. Journal of Agricultural and Food Chemistry 59, 2897–2908. https://doi.org/10.1021/jf101303g
Johnson, R.M., 2015. Honey bee toxicology. Annual Review of Entomology 60, 415–434. https://doi.org/10.1146/annurev-ento-011613-162005
Kulhanek, K., Steinhauer, N., Rennich, K., Caron, D.M., Sagili, R.R., Pettis, J.S., Ellis, J.D., Wilson, M.E., Wilkes, J.T., Tarpy, D.R., Rose, R., Lee, K., Rangel, J., vanEngelsdorp, D., 2017. A national survey of managed honey bee 2015–2016 annual colony losses in the USA. Journal of Apicultural Research 56, 328–340. https://doi.org/10.1080/00218839.2017.1344496
Grozinger, C.M., Flenniken, M.L., 2019. Bee viruses: ecology, pathogenicity, and impacts. Annual Review of Entomology 64, 205–226. https://doi.org/10.1146/annurev-ento-011118-111942
López-Uribe, M.M., Ricigliano, V.A., Simone-Finstrom, M., 2020. Defining pollinator health: assessing bee ecological, genetic, and physiological factors at the individual, colony, and population levels. Annual Review of Animal Biosciences 8, null. https://doi.org/10.1146/annurev-animal-020518-115045
Human, H., Brodschneider, R., Dietemann, V., Dively, G., Ellis, J.D., Forsgren, E., et al. 2013. Miscellaneous standard methods for Apis mellifera research. Journal of Apicultural Research 52, 1–53. https://doi.org/10.3896/IBRA.1.52.4.10
Lundin, O., Rundlöf, M., Smith, H.G., Fries, I., Bommarco, R., 2015. Neonicotinoid insecticides and their impacts on bees: A systematic review of research approaches and identification of knowledge gaps. PLOS ONE 10, e0136928. https://doi.org/10.1371/journal.pone.0136928
Matsuda, K., Buckingham, S.D., Kleier, D., Rauh, J.J., Grauso, M., Sattelle, D.B., 2001. Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends in Pharmacological Sciences 22, 573–580. https://doi.org/10.1016/S0165-6147(00)01820-4
Matsuda, K., Kanaoka, S., Akamatsu, M., Sattelle, D.B., 2009. Diverse actions and target-site selectivity of neonicotinoids: structural insights. Mol Pharmacol 76, 1–10. https://doi.org/10.1124/mol.109.055186
Matsuda, K., Ihara, M., Sattelle, D.B., 2020. Neonicotinoid insecticides: molecular targets, resistance, and toxicity. Annual Review of Pharmacology and Toxicology 60, 241–255. https://doi.org/10.1146/annurev-pharmtox-010818-021747
A. M. Milner, I. L. Boyd. 2017. Toward pesticidovigilance. https://doi.org/10.1126/science.aan2683
Moreira-Hernández, J.I., Muchhala, N., 2019. Importance of pollinator-mediated interspecific pollen transfer for angiosperm evolution. Annual Review of Ecology, Evolution, and Systematics 50, null. https://doi.org/10.1146/annurev-ecolsys-110218-024804
Ollerton, J., 2017. Pollinator diversity: Distribution, ecological function, and conservation. Annual Review of Ecology, Evolution, and Systematics 48, 353–376. https://doi.org/10.1146/annurev-ecolsys-110316-022919
Potts, S.G., Biesmeijer, J.C., Kremen, C., Neumann, P., Schweiger, O., Kunin, W.E., 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology & Evolution 25, 345–353. https://doi.org/10.1016/j.tree.2010.01.007
Potts, S.G., Imperatriz-Fonseca, V., Ngo, H.T., Aizen, M.A., Biesmeijer, J.C., Breeze, T.D., Dicks, L.V., Garibaldi, L.A., Hill, R., Settele, J., Vanbergen, A.J., 2016. Safeguarding pollinators and their values to human well-being. Nature 540, 220–229. https://doi.org/10.1038/nature20588
Rader, R., Cunningham, S.A., Howlett, B.G., Inouye, D.W., 2020. Non-bee insects as visitors and pollinators of crops: biology, ecology and management. Annual Review of Entomology 65, null. https://doi.org/10.1146/annurev-ento-011019-025055
Ratnieks, F.L.W., Balfour, N.J., Carreck, N.L., 2018. Review: Have suitable experimental designs been used to determine the effects of neonicotinoid insecticides on bee colony performance in the field? Journal of Apicultural Research 57, 586–592. https://doi.org/10.1080/00218839.2018.1484055
Sheets, L.P., Li, A.A., Minnema, D.J., Collier, R.H., Creek, M.R., Peffer, R.C., 2016. A critical review of neonicotinoid insecticides for developmental neurotoxicity. Crit Rev Toxicol 46, 153–190. https://doi.org/10.3109/10408444.2015.1090948
Stoner, K.A., 2016. Current pesticide risk assessment protocols do not adequately address differences between honey bees (Apis mellifera) and bumblebees (Bombus spp.). Frontiers in Environmental Science 4. https://doi.org/10.3389/fenvs.2016.00079
Straub, L., Strobl, V., Neumann, P., 2020. The need for an evolutionary approach to ecotoxicology. Nature Ecology & Evolution 1–1. https://doi.org/10.1038/s41559-020-1194-6
Tomizawa, M., Casida, J.E., 2003. Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annual Review of Entomology 48, 339–364. https://doi.org/10.1146/annurev.ento.48.091801.112731
Topping, C.J., Aldrich, A., Berny, P., 2020. Overhaul environmental risk assessment for pesticides. Science 367, 360–363. https://doi.org/10.1126/science.aay1144
van der Sluijs, J.P., Simon-Delso, N., Goulson, D., Maxim, L., Bonmatin, J.-M., Belzunces, L.P., 2013. Neonicotinoids, bee disorders and the sustainability of pollinator services. Current Opinion in Environmental Sustainability 5, 293–305. https://doi.org/10.1016/j.cosust.2013.05.007
Van Leeuwen, T., Dermauw, W., 2016. The molecular evolution of xenobiotic metabolism and resistance in chelicerate mites. Annual Review of Entomology 61, 475–498. https://doi.org/10.1146/annurev-ento-010715-023907
Wang, X., Anadón, A., Wu, Q., Qiao, F., Ares, I., Martínez-Larrañaga, M.-R., Yuan, Z., Martínez, M.-A., 2018. Mechanism of neonicotinoid toxicity: impact on oxidative stress and metabolism. Annual Review of Pharmacology and Toxicology 58, 471–507. https://doi.org/10.1146/annurev-pharmtox-010617-052429
Wood, T.J., Goulson, D., 2017. The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environmental Science and Pollution Research 24, 17285–17325. https://doi.org/10.1007/s11356-017-9240-x
Wright, G.A., Nicolson, S.W., Shafir, S., 2018. Nutritional physiology and ecology of honey bees. Annual Review of Entomology 63, 327–344. https://doi.org/10.1146/annurev-ento-020117-043423

Highly cited

Baron, G.L., Jansen, V.A.A., Brown, M.J.F., Raine, N.E., 2017. Pesticide reduces bumblebee colony initiation and increases probability of population extinction. Nature Ecology & Evolution 1, 1308–1316. https://doi.org/10.1038/s41559-017-0260-1
Biesmeijer, J.C., Roberts, S.P.M., Reemer, M., Ohlemüller, R., Edwards, M., Peeters, T., Schaffers, A.P., Potts, S.G., Kleukers, R., Thomas, C.D., Settele, J., Kunin, W.E., 2006. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313, 351–354. https://doi.org/10.1126/science.1127863
Bonmatin, J.-M., Giorio, C., Girolami, V., Goulson, D., Kreutzweiser, D.P., Krupke, C., Liess, M., Long, E., Marzaro, M., Mitchell, E.A.D., Noome, D.A., Simon-Delso, N., Tapparo, A., 2015. Environmental fate and exposure; neonicotinoids and fipronil. Environ Sci Pollut Res 22, 35–67. https://doi.org/10.1007/s11356-014-3332-7
Bryden, J., Gill, R.J., Mitton, R.A.A., Raine, N.E., Jansen, V.A.A., 2013. Chronic sublethal stress causes bee colony failure. Ecology Letters 16, 1463–1469. https://doi.org/10.1111/ele.12188
Cresswell, J.E., 2011. A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20, 149–157. https://doi.org/10.1007/s10646-010-0566-0
Di Prisco, G., Cavaliere, V., Annoscia, D., Varricchio, P., Caprio, E., Nazzi, F., Gargiulo, G., Pennacchio, F., 2013. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proceedings of the National Academy of Sciences 110, 18466–71. https://doi.org/10.1073/pnas.1314923110
Dively, G.P., Embrey, M.S., Kamel, A., Hawthorne, D.J., Pettis, J.S., 2015. Assessment of chronic sublethal effects of imidacloprid on honey bee colony health. PLOS ONE 10, e0118748. https://doi.org/10.1371/journal.pone.0118748
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Garibaldi, L.A., Steffan-Dewenter, I., Winfree, R., Aizen, M.A., Bommarco, R., et al., 2013. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608–1611. https://doi.org/10.1126/science.1230200
Gill, R.J., Ramos-Rodriguez, O., Raine, N.E., 2012. Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491, 105–108. https://doi.org/10.1038/nature11585
Godfray, H.C.J., Blacquière, T., Field, L.M., Hails, R.S., Petrokofsky, G., Potts Simon G., Raine Nigel E., Vanbergen Adam J., McLean Angela R., 2014. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proceedings of the Royal Society B: Biological Sciences 281, 20140558. https://doi.org/10.1098/rspb.2014.0558
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Hardstone, M.C., Scott, J.G., 2010. Is Apis mellifera more sensitive to insecticides than other insects? Pest Management Science 66, 1171–1180. https://doi.org/10.1002/ps.2001
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Jones, A., Harrington, P., Turnbull, G., 2014. Neonicotinoid concentrations in arable soils after seed treatment applications in preceding years. Pest Management Science 70, 1780–1784. https://doi.org/10.1002/ps.3836
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Mitchell, E.A.D., Mulhauser, B., Mulot, M., Mutabazi, A., Glauser, G., Aebi, A., 2017. A worldwide survey of neonicotinoids in honey. Science 358, 109–111. https://doi.org/10.1126/science.aan3684
Mommaerts, V., Reynders, S., Boulet, J., Besard, L., Sterk, G., Smagghe, G., 2009. Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology 19, 207. https://doi.org/10.1007/s10646-009-0406-2
Ollerton, J., Erenler, H., Edwards, M., Crockett, R., 2014. Extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science 346, 1360–1362. https://doi.org/10.1126/science.1257259
Osterman, J., Wintermantel, D., Locke, B., Jonsson, O., Semberg, E., Onorati, P., Forsgren, E., Rosenkranz, P., Rahbek-Pedersen, T., Bommarco, R., Smith, H.G., Rundlöf, M., de Miranda, J.R., 2019. Clothianidin seed-treatment has no detectable negative impact on honeybee colonies and their pathogens. Nature Communications 10, 692. https://doi.org/10.1038/s41467-019-08523-4
Palmer, M.J., Moffat, C., Saranzewa, N., Harvey, J., Wright, G.A., Connolly, C.N., 2013. Cholinergic pesticides cause mushroom body neuronal inactivation in honeybees. Nature Communications 4, 1634. https://doi.org/10.1038/ncomms2648
Potts, S.G., Imperatriz-Fonseca, V., Ngo, H.T., Aizen, M.A., Biesmeijer, J.C., Breeze, T.D., Dicks, L.V., Garibaldi, L.A., Hill, R., Settele, J., Vanbergen, A.J., 2016. Safeguarding pollinators and their values to human well-being. Nature 540, 220–229. https://doi.org/10.1038/nature20588
Powney, G.D., Carvell, C., Edwards, M., Morris, R.K.A., Roy, H.E., Woodcock, B.A., Isaac, N.J.B., 2019. Widespread losses of pollinating insects in Britain. Nature Communications 10, 1018. https://doi.org/10.1038/s41467-019-08974-9
Raine, N.E., 2018. Pesticide affects social behavior of bees. Science 362, 643–644. https://doi.org/10.1126/science.aav5273
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Pesticide levels in pollen and nectar

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Dosage effects

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Gene expression

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Manjon, C., Troczka, B.J., Zaworra, M., Beadle, K., Randall, E., Hertlein, G., Singh, K.S., Zimmer, C.T., Homem, R.A., Lueke, B., Reid, R., Kor, L., Kohler, M., Benting, J., Williamson, M.S., Davies, T.G.E., Field, L.M., Bass, C., Nauen, R., 2018. Unravelling the molecular determinants of bee sensitivity to neonicotinoid insecticides. Current Biology 28, 1137-1143.e5. https://doi.org/10.1016/j.cub.2018.02.045
Mao, W., Schuler, M.A., Berenbaum, M.R., 2011. CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proceedings of the National Academy of Sciences 108, 12657–62. https://doi.org/10.1073/pnas.1109535108
Mao, W., Schuler, M.A., Berenbaum, M.R., 2017. Disruption of quercetin metabolism by fungicide affects energy production in honey bees (Apis mellifera). Proceedings of the National Academy of Sciences 114, 2538–2543. https://doi.org/10.1073/pnas.1614864114
Morfin, N., Goodwin, P.H., Guzman-Novoa, E., 2020. Interaction of field realistic doses of clothianidin and Varroa destructor parasitism on adult honey bee (Apis mellifera L.) health and neural gene expression, and antagonistic effects on differentially expressed genes. PLOS ONE 15, e0229030. https://doi.org/10.1371/journal.pone.0229030
Osterman, J., Wintermantel, D., Locke, B., Jonsson, O., Semberg, E., Onorati, P., Forsgren, E., Rosenkranz, P., Rahbek-Pedersen, T., Bommarco, R., Smith, H.G., Rundlöf, M., de Miranda, J.R., 2019. Clothianidin seed-treatment has no detectable negative impact on honeybee colonies and their pathogens. Nature Communications 10, 692. https://doi.org/10.1038/s41467-019-08523-4
Perry, T., Somers, J., Yang, Y.T., Batterham, P., 2015. Expression of insect α6-like nicotinic acetylcholine receptors in Drosophila melanogaster highlights a high level of conservation of the receptor:spinosyn interaction. Insect Biochemistry and Molecular Biology 64, 106–115. https://doi.org/10.1016/j.ibmb.2015.01.017
Pu, J., Sun, H., Wang, J., Wu, M., Wang, K., Denholm, I., Han, Z., 2016. Multiple cis-acting elements involved in up-regulation of a cytochrome P450 gene conferring resistance to deltamethrin in smal brown planthopper, Laodelphax striatellus (Fallén). Insect Biochemistry and Molecular Biology 78, 20–28. https://doi.org/10.1016/j.ibmb.2016.08.008
Puinean, A.M., Foster, S.P., Oliphant, L., Denholm, I., Field, L.M., Millar, N.S., Williamson, M.S., Bass, C., 2010. Amplification of a cytochrome P450 gene is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. PLOS Genetics 6, e1000999. https://doi.org/10.1371/journal.pgen.1000999
Pyakurel, P., Shin, M., Venton, B.J., 2018. Nicotinic acetylcholine receptor (nAChR) mediated dopamine release in larval Drosophila melanogaster. Neurochemistry International 114, 33–41. https://doi.org/10.1016/j.neuint.2017.12.012
Schmehl, D.R., Teal, P.E.A., Frazier, J.L., Grozinger, C.M., 2014. Genomic analysis of the interaction between pesticide exposure and nutrition in honey bees (Apis mellifera). Journal of Insect Physiology 71, 177–190. https://doi.org/10.1016/j.jinsphys.2014.10.002
Somers, J., Luong, H.N.B., Batterham, P., Perry, T., 2018. Deletion of the nicotinic acetylcholine receptor subunit gene Dα1 confers insecticide resistance, but at what cost? Fly 12, 46–54. https://doi.org/10.1080/19336934.2017.1396399
Taillebois, E., Beloula, A., Quinchard, S., Jaubert-Possamai, S., Daguin, A., Servent, D., Tagu, D., Thany, S.H., Tricoire-Leignel, H., 2014. Neonicotinoid binding, toxicity and expression of nicotinic acetylcholine receptor subunits in the aphid Acyrthosiphon pisum. PLOS ONE 9, e96669. https://doi.org/10.1371/journal.pone.0096669
Tan, J., Galligan, J.J., Hollingworth, R.M., 2007. Agonist actions of neonicotinoids on nicotinic acetylcholine receptors expressed by cockroach neurons. NeuroToxicology 28, 829–842. https://doi.org/10.1016/j.neuro.2007.04.002
Tesovnik, T., Cizelj, I., Zorc, M., Čitar, M., Božič, J., Glavan, G., Narat, M., 2017. Immune related gene expression in worker honey bee (Apis mellifera carnica) pupae exposed to neonicotinoid thiamethoxam and Varroa mites (Varroa destructor). PLOS ONE 12, e0187079. https://doi.org/10.1371/journal.pone.0187079
Thany, S.H., Crozatier, M., Raymond-Delpech, V., Gauthier, M., Lenaers, G., 2005. Apisα2, Apisα7-1 and Apisα7-2: three new neuronal nicotinic acetylcholine receptor α-subunits in the honeybee brain. Gene 344, 125–132. https://doi.org/10.1016/j.gene.2004.09.010
Tsvetkov, N., MacPhail, V. J., Colla, S. R., & Zayed, A. (2021). Conservation genomics reveals pesticide and pathogen exposure in the declining bumble bee Bombus terricola. Molecular Ecology, 00, 1– 11. https://doi.org/10.1111/mec.16049
Wan, Y., Yuan, G., He, B., Xu, B., Xie, W., Wang, S., Zhang, Y., Wu, Q., Zhou, X., 2018. Foccα6, a truncated nAChR subunit, positively correlates with spinosad resistance in the western flower thrips, Frankliniella occidentalis (Pergande). Insect Biochemistry and Molecular Biology 99, 1–10. https://doi.org/10.1016/J.IBMB.2018.05.002
Wang, H., Smagghe, G., Meeus, I., 2017. The role of a single gene encoding the Single von Willebrand factor C-domain protein (SVC) in bumblebee immunity extends beyond antiviral defense. Insect Biochemistry and Molecular Biology 91, 10–20. https://doi.org/10.1016/j.ibmb.2017.10.002
Wang, K., Fan, R.-L., Ji, W.-N., Zhang, W.-W., Chen, X.-M., Wang, S., Yin, L., Gao, F.-C., Chen, G.-H., Ji, T., 2018. Transcriptome analysis of newly emerged honeybees exposure to sublethal carbendazim during larval stage. Frontiers in Genetics 9, 426. https://doi.org/10.3389/fgene.2018.00426
Wu, M.-C., Chang, Y.-W., Lu, K.-H., Yang, E.-C., 2017. Gene expression changes in honey bees induced by sublethal imidacloprid exposure during the larval stage. Insect Biochemistry and Molecular Biology 88, 12–20. https://doi.org/10.1016/j.ibmb.2017.06.016
Zimmer, C.T., Garrood, W.T., Singh, K.S., Randall, E., Lueke, B., Gutbrod, O., Matthiesen, S., Kohler, M., Nauen, R., Davies, T.G.E., Bass, C., 2018. Neofunctionalization of duplicated P450 genes drives the evolution of insecticide resistance in the brown planthopper. Current Biology 28, 268-274.e5. https://doi.org/10.1016/j.cub.2017.11.060
Zhang, Y., Liu, Y., Bao, H., Sun, H., Liu, Z., 2017. Alternative splicing in nicotinic acetylcholine receptor subunits from Locusta migratoria and its influence on acetylcholine potencies. Neuroscience Letters 638, 151–155. https://doi.org/10.1016/j.neulet.2016.12.041
Xu, G., Wu, S.-F., Teng, Z.-W., Yao, H.-W., Fang, Q., Huang, J., Ye, G.-Y., 2017. Molecular characterization and expression profiles of nicotinic acetylcholine receptors in the rice striped stem borer, Chilo suppressalis (Lepidoptera: Crambidae). Insect Science 24, 371–384. https://doi.org/10.1111/1744-7917.12324

nAChRs

Bass, C., Puinean, A.M., Andrews, M., Cutler, P., Daniels, M., Elias, J., Paul, V.L., Crossthwaite, A.J., Denholm, I., Field, L.M., Foster, S.P., Lind, R., Williamson, M.S., Slater, R., 2011. Mutation of a nicotinic acetylcholine receptor β subunit is associated with resistance to neonicotinoid insecticides in the aphid Myzus persicae. BMC Neuroscience 12, 51. https://doi.org/10.1186/1471-2202-12-51
Beckingham, C., Phillips, J., Gill, M., Crossthwaite, A.J., 2013. Investigating nicotinic acetylcholine receptor expression in neonicotinoid resistant Myzus persicae FRC. Pesticide Biochemistry and Physiology 107, 293–298. https://doi.org/10.1016/j.pestbp.2013.08.005
Casida, J.E., 2018. Neonicotinoids and other insect nicotinic receptor competitive modulators: progress and prospects. Annual Review of Entomology 63, 125–144. https://doi.org/10.1146/annurev-ento-020117-043042
Casida, J.E., Durkin, K.A., 2013. Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annual Review of Entomology 58, 99–117. https://doi.org/10.1146/annurev-ento-120811-153645
Crespin, L., Legros, C., List, O., Tricoire-Leignel, H., Mattei, C., 2016. Injection of insect membrane in Xenopus oocyte: an original method for the pharmacological characterization of neonicotinoid insecticides. Journal of Pharmacological and Toxicological Methods 77, 10–16. https://doi.org/10.1016/j.vascn.2015.09.004
Dederer, H., Werr, M., Ilg, T., 2011. Differential sensitivity of Ctenocephalides felis and Drosophila melanogaster nicotinic acetylcholine receptor α1 and α2 subunits in recombinant hybrid receptors to nicotinoids and neonicotinoid insecticides. Insect Biochemistry and Molecular Biology 41, 51–61. https://doi.org/10.1016/j.ibmb.2010.09.012
Dupuis, J.P., Gauthier, M., Raymond-Delpech, V., 2011. Expression patterns of nicotinic subunits α2, α7, α8, and β1 affect the kinetics and pharmacology of ACh-induced currents in adult bee olfactory neuropiles. Journal of Neurophysiology 106, 1604–1613. https://doi.org/10.1152/jn.00126.2011
Dupuis, J., Louis, T., Gauthier, M., Raymond, V., 2012. Insights from honeybee (Apis mellifera) and fly (Drosophila melanogaster) nicotinic acetylcholine receptors: from genes to behavioral functions. Neuroscience & Biobehavioral Reviews 36, 1553–1564. https://doi.org/10.1016/j.neubiorev.2012.04.003
Jones, A.K., Raymond-Delpech, V., Thany, S.H., Gauthier, M., Sattelle, D.B., 2006. The nicotinic acetylcholine receptor gene family of the honey bee, Apis mellifera. Genome Research 16, 1422–30. https://doi.org/10.1101/gr.4549206
ffrench-Constant, R.H., Williamson, M.S., Davies, T.G.E., Bass, C., 2016. Ion channels as insecticide targets. Journal of Neurogenetics 30, 163–177. https://doi.org/10.1080/01677063.2016.1229781
Honda, H., Tomizawa, M., Casida, J.E., 2006. Insect nicotinic acetylcholine receptors: neonicotinoid binding site specificity is usually but not always conserved with varied substituents and species. J. Agric. Food Chem. 54, 3365–3371. https://doi.org/10.1021/jf0601517
Ihara, M., Shimomura, M., Ishida, C., Nishiwaki, H., Akamatsu, M., Sattelle, D.B., Matsuda, K., 2007. A hypothesis to account for the selective and diverse actions of neonicotinoid insecticides at their molecular targets, nicotinic acetylcholine receptors: catch and release in hydrogen bond networks. Invert Neurosci 7, 47–51. https://doi.org/10.1007/s10158-006-0043-x
Ihara, M., Sattelle, D.B., Matsuda, K., 2015. Probing new components (loop G and the α–α interface) of neonicotinoid binding sites on nicotinic acetylcholine receptors. Pesticide Biochemistry and Physiology, Insecticide and Acaricide Modes of Action and their Role in Resistance and its Management 121, 47–52. https://doi.org/10.1016/j.pestbp.2015.02.011
Ihara, M., Hikida, M., Matsushita, H., Yamanaka, K., Kishimoto, Y., Kubo, K., Watanabe, S., Sakamoto, M., Matsui, K., Yamaguchi, A., Okuhara, D., Furutani, S., Sattelle, D.B., Matsuda, K., 2018. Loops D, E and G in the Drosophila Dα1 subunit contribute to high neonicotinoid sensitivity of Dα1-chicken β2 nicotinic acetylcholine receptor. British Journal of Pharmacology 175, 1999–2012. https://doi.org/10.1111/bph.13914
Kayser, H., Lee, C., Decock, A., Baur, M., Haettenschwiler, J., Maienfisch, P., 2004. Comparative analysis of neonicotinoid binding to insect membranes: I. A structure–activity study of the mode of [3H]imidacloprid displacement in Myzus persicae and Aphis craccivora. Pest Management Science 60, 945–958. https://doi.org/10.1002/ps.919
Kayser, H., Lehmann, K., Gomes, M., Schleicher, W., Dotzauer, K., Moron, M., Maienfisch, P., 2016. Binding of imidacloprid, thiamethoxam and N-desmethylthiamethoxam to nicotinic receptors of Myzus persicae: pharmacological profiling using neonicotinoids, natural agonists and antagonists. Pest Management Science 72, 2166–2175. https://doi.org/10.1002/ps.4249
LaLone, C.A., Villeneuve, D.L., Wu-Smart, J., Milsk, R.Y., Sappington, K., Garber, K.V., Housenger, J., Ankley, G.T., 2017. Weight of evidence evaluation of a network of adverse outcome pathways linking activation of the nicotinic acetylcholine receptor in honey bees to colony death. Sci Total Environ 584–585, 751–775. https://doi.org/10.1016/j.scitotenv.2017.01.113
Lansdell, S.J., Collins, T., Goodchild, J., Millar, N.S., 2012. The Drosophila nicotinic acetylcholine receptor subunits Dα5 and Dα7 form functional homomeric and heteromeric ion channels. BMC Neuroscience 13, 73. https://doi.org/10.1186/1471-2202-13-73
Liu, Z., Williamson, M.S., Lansdell, S.J., Denholm, I., Han, Z., Millar, N.S., 2005. A nicotinic acetylcholine receptor mutation conferring target-site resistance to imidacloprid in Nilaparvata lugens (brown planthopper). PNAS 102, 8420–8425. https://doi.org/10.1073/pnas.0502901102
Longhurst, C., Babcock, J.M., Denholm, I., Gorman, K., Thomas, J.D., Sparks, T.C., 2013. Cross-resistance relationships of the sulfoximine insecticide sulfoxaflor with neonicotinoids and other insecticides in the whiteflies Bemisia tabaci and Trialeurodes vaporariorum. Pest Management Science 69, 809–813. https://doi.org/10.1002/ps.3439
Matsuda, K., Buckingham, S.D., Kleier, D., Rauh, J.J., Grauso, M., Sattelle, D.B., 2001. Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends in Pharmacological Sciences 22, 573–580. https://doi.org/10.1016/S0165-6147(00)01820-4
Matsuda, K., Shimomura, M., Ihara, M., Akamatsu, M., Sattelle, D.B., 2005. Neonicotinoids show selective and diverse actions on their nicotinic receptor targets: electrophysiology, molecular biology, and receptor modeling studies. Bioscience, Biotechnology, and Biochemistry 69, 1442–1452. https://doi.org/10.1271/bbb.69.1442
Matsuda, K., Kanaoka, S., Akamatsu, M., Sattelle, D.B., 2009. Diverse actions and target-site selectivity of neonicotinoids: structural insights. Mol Pharmacol 76, 1–10. https://doi.org/10.1124/mol.109.055186
Meng, X., Zhang, Y., Guo, B., Sun, H., Liu, C., Liu, Z., 2015. Identification of key amino acid differences contributing to neonicotinoid sensitivity between two nAChR α subunits from Pardosa pseudoannulata. Neuroscience Letters 584, 123–128. https://doi.org/10.1016/j.neulet.2014.10.013
Millar, N.S., Denholm, I., 2007. Nicotinic acetylcholine receptors: targets for commercially important insecticides. Invert Neurosci 7, 53–66. https://doi.org/10.1007/s10158-006-0040-0
Perry, T., Somers, J., Yang, Y.T., Batterham, P., 2015. Expression of insect α6-like nicotinic acetylcholine receptors in Drosophila melanogaster highlights a high level of conservation of the receptor:spinosyn interaction. Insect Biochemistry and Molecular Biology 64, 106–115. https://doi.org/10.1016/j.ibmb.2015.01.017
Pyakurel, P., Shin, M., Venton, B.J., 2018. Nicotinic acetylcholine receptor (nAChR) mediated dopamine release in larval Drosophila melanogaster. Neurochemistry International 114, 33–41. https://doi.org/10.1016/j.neuint.2017.12.012
Qu, Y., Chen, J., Li, C., Wang, Q., Guo, W., Han, Z., Jiang, W., 2016. The subunit gene Ldα1 of nicotinic acetylcholine receptors plays important roles in the toxicity of imidacloprid and thiamethoxam against Leptinotarsa decemlineata. Pesticide Biochemistry and Physiology 127, 51–58. https://doi.org/10.1016/j.pestbp.2015.09.006
Rinkevich, F.D., Bourgeois, L., 2020. In silico identification and assessment of insecticide target sites in the genome of the small hive beetle, Aethina tumida. BMC Genomics 21, 154. https://doi.org/10.1186/s12864-020-6551-y
Selvam, B., Graton, J., Laurent, A.D., Alamiddine, Z., Mathé-Allainmat, M., Lebreton, J., Coqueret, O., Olivier, C., Thany, S.H., Le Questel, J.-Y., 2015. Imidacloprid and thiacloprid neonicotinoids bind more favourably to cockroach than to honeybee α6 nicotinic acetylcholine receptor: Insights from computational studies. Journal of Molecular Graphics and Modelling 55, 1–12. https://doi.org/10.1016/j.jmgm.2014.10.018
Shao, X., Xia, S., Durkin, K.A., Casida, J.E., 2013. Insect nicotinic receptor interactions in vivo with neonicotinoid, organophosphorus, and methylcarbamate insecticides and a synergist. PNAS 110, 17273–17277. https://doi.org/10.1073/pnas.1316369110
Shimomura, M., Yokota, M., Ihara, M., Akamatsu, M., Sattelle, D.B., Matsuda, K., 2006. Role in the selectivity of neonicotinoids of insect-specific basic residues in loop D of the nicotinic acetylcholine receptor agonist binding site. Mol Pharmacol 70, 1255–1263. https://doi.org/10.1124/mol.106.026815
Shimomura, M., Okuda, H., Matsuda, K., Komai, K., Akamatsu, M., Sattelle, D.B., 2002. Effects of mutations of a glutamine residue in loop D of the α7 nicotinic acetylcholine receptor on agonist profiles for neonicotinoid insecticides and related ligands. British Journal of Pharmacology 137, 162–169. https://doi.org/10.1038/sj.bjp.0704848
Mesquita, R. da S., Kyrylchuk, A., Grafova, I., Kliukovskyi, D., Bezdudnyy, A., Rozhenko, A., Tadei, W.P., Leskelä, M., Grafov, A., 2020. Synthesis, molecular docking studies, and larvicidal activity evaluation of new fluorinated neonicotinoids against Anopheles darlingi larvae. PLOS ONE 15, e0227811. https://doi.org/10.1371/journal.pone.0227811
Taillebois, E., Beloula, A., Quinchard, S., Jaubert-Possamai, S., Daguin, A., Servent, D., Tagu, D., Thany, S.H., Tricoire-Leignel, H., 2014. Neonicotinoid binding, toxicity and expression of nicotinic acetylcholine receptor subunits in the aphid Acyrthosiphon pisum. PLOS ONE 9, e96669. https://doi.org/10.1371/journal.pone.0096669
Taillebois, E., Cartereau, A., Jones, A.K., Thany, S.H., 2018. Neonicotinoid insecticides mode of action on insect nicotinic acetylcholine receptors using binding studies. Pesticide Biochemistry and Physiology 151, 59–66. https://doi.org/10.1016/J.PESTBP.2018.04.007
Tan, J., Galligan, J.J., Hollingworth, R.M., 2007. Agonist actions of neonicotinoids on nicotinic acetylcholine receptors expressed by cockroach neurons. NeuroToxicology 28, 829–842. https://doi.org/10.1016/j.neuro.2007.04.002
Thany, S.H., Lenaers, G., Crozatier, M., Armengaud, C., Gauthier, M., 2003. Identification and localization of the nicotinic acetylcholine receptor alpha3 mRNA in the brain of the honeybee, Apis mellifera. Insect Molecular Biology 12, 255–262. https://doi.org/10.1046/j.1365-2583.2003.00409.x
Thany, S.H., Crozatier, M., Raymond-Delpech, V., Gauthier, M., Lenaers, G., 2005. Apisα2, Apisα7-1 and Apisα7-2: three new neuronal nicotinic acetylcholine receptor α-subunits in the honeybee brain. Gene 344, 125–132. https://doi.org/10.1016/J.GENE.2004.09.010
Thany, S.H., Lenaers, G., Raymond-Delpech, V., Sattelle, D.B., Lapied, B., 2007. Exploring the pharmacological properties of insect nicotinic acetylcholine receptors. Trends in Pharmacological Sciences 28, 14–22. https://doi.org/10.1016/J.TIPS.2006.11.006
Tomizawa, M., Casida, J.E., 2003. Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annual Review of Entomology 48, 339–364. https://doi.org/10.1146/annurev.ento.48.091801.112731
Tomizawa, M., Casida, J.E., 2005. Neonicotinoid insecticide toxicology: mechanisms of selective action. Annual Review of Pharmacology and Toxicology 45, 247–268. https://doi.org/10.1146/annurev.pharmtox.45.120403.095930
Tomizawa, M., Millar, N.S., Casida, J.E., 2005. Pharmacological profiles of recombinant and native insect nicotinic acetylcholine receptors. Insect Biochemistry and Molecular Biology 35, 1347–1355. https://doi.org/10.1016/j.ibmb.2005.08.006
Tomizawa, M., Casida, J.E., 2009. Molecular recognition of neonicotinoid insecticides: the determinants of life or death. Acc. Chem. Res. 42, 260–269. https://doi.org/10.1021/ar800131p
Tomizawa, M., Maltby, D., Talley, T.T., Durkin, K.A., Medzihradszky, K.F., Burlingame, A.L., Taylor, P., Casida, J.E., 2008. Atypical nicotinic agonist bound conformations conferring subtype selectivity. PNAS 105, 1728–1732. https://doi.org/10.1073/pnas.0711724105
Weill, M., Berthomieu, A., Berticat, C., Lutfalla, G., Nègre, V., Pasteur, N., Philips, A., Leonetti, J.-P., Fort, P., Raymond, M., 2004. Insecticide resistance: a silent base prediction. Current Biology 14, R552–R553. https://doi.org/10.1016/j.cub.2004.07.008
Wellmann, H., Gomes, M., Lee, C., Kayser, H., 2004. Comparative analysis of neonicotinoid binding to insect membranes: II. An unusual high affinity site for [3H]thiamethoxam in Myzus persicae and Aphis craccivora. Pest Management Science 60, 959–970. https://doi.org/10.1002/ps.920
Xu, G., Wu, S.-F., Teng, Z.-W., Yao, H.-W., Fang, Q., Huang, J., Ye, G.-Y., 2017. Molecular characterization and expression profiles of nicotinic acetylcholine receptors in the rice striped stem borer, Chilo suppressalis (Lepidoptera: Crambidae). Insect Science 24, 371–384. https://doi.org/10.1111/1744-7917.12324
Yao, X., Song, F., Chen, F., Zhang, Y., Gu, J., Liu, S., Liu, Z., 2008. Amino acids within loops D, E and F of insect nicotinic acetylcholine receptor β subunits influence neonicotinoid selectivity. Insect Biochemistry and Molecular Biology 38, 834–840. https://doi.org/10.1016/j.ibmb.2008.05.009
Zhang, Y., Liu, S., Gu, J., Song, F., Yao, X., Liu, Z., 2008. Imidacloprid acts as an antagonist on insect nicotinic acetylcholine receptor containing the Y151M mutation. Neuroscience Letters 446, 97–100. https://doi.org/10.1016/j.neulet.2008.09.039

Pesticides

Bass, C., Field, L.M., 2018. Neonicotinoids. Current Biology 28, R772–R773. https://doi.org/10.1016/j.cub.2018.05.061
Bonmatin, J.-M., Giorio, C., Girolami, V., Goulson, D., Kreutzweiser, D.P., Krupke, C., Liess, M., Long, E., Marzaro, M., Mitchell, E.A.D., Noome, D.A., Simon-Delso, N., Tapparo, A., 2015. Environmental fate and exposure; neonicotinoids and fipronil. Environ Sci Pollut Res 22, 35–67. https://doi.org/10.1007/s11356-014-3332-7
Crossthwaite, A.J., Bigot, A., Camblin, P., Goodchild, J., Lind, R.J., Slater, R., Maienfisch, P., 2017. The invertebrate pharmacology of insecticides acting at nicotinic acetylcholine receptors. Journal of Pesticide Science 42, 67–83. https://doi.org/10.1584/jpestics.D17-019
Cutler, P., Slater, R., Edmunds, A.J., Maienfisch, P., Hall, R.G., Earley, F.G., Pitterna, T., Pal, S., Paul, V.-L., Goodchild, J., Blacker, M., Hagmann, L., Crossthwaite, A.J., 2013. Investigating the mode of action of sulfoxaflor: a fourth-generation neonicotinoid. Pest Management Science 69, 607–619. https://doi.org/10.1002/ps.3413
Jeschke, P., Nauen, R., 2008. Neonicotinoids - from zero to hero in insecticide chemistry. Pest Management Science 64, 1084–1098. https://doi.org/10.1002/ps.1631
Jeschke, P., Nauen, R., Schindler, M., Elbert, A., 2011. Overview of the status and global strategy for neonicotinoids. Journal of Agricultural and Food Chemistry 59, 2897–2908. https://doi.org/10.1021/jf101303g
Jeschke, P., Nauen, R., Beck, M.E., 2013. Nicotinic acetylcholine receptor agonists: a milestone for modern crop protection. Angewandte Chemie International Edition 52, 9464–9485. https://doi.org/10.1002/anie.201302550
Jeschke, P., Nauen, R., Gutbrod, O., Beck, M.E., Matthiesen, S., Haas, M., Velten, R., 2015. Flupyradifurone (Sivanto™) and its novel butenolide pharmacophore: structural considerations. Pesticide Biochemistry and Physiology 121, 31–38. https://doi.org/10.1016/j.pestbp.2014.10.011
Liu, Z., Williamson, M.S., Lansdell, S.J., Han, Z., Denholm, I., Millar, N.S., 2006. A nicotinic acetylcholine receptor mutation (Y151S) causes reduced agonist potency to a range of neonicotinoid insecticides. Journal of Neurochemistry 99, 1273–1281. https://doi.org/10.1111/j.1471-4159.2006.04167.x
Matsuda, K., Buckingham, S.D., Kleier, D., Rauh, J.J., Grauso, M., Sattelle, D.B., 2001. Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends in Pharmacological Sciences 22, 573–580. https://doi.org/10.1016/S0165-6147(00)01820-4
Nauen, R., Jeschke, P., Velten, R., Beck, M.E., Ebbinghaus‐Kintscher, U., Thielert, W., Wölfel, K., Haas, M., Kunz, K., Raupach, G., 2015. Flupyradifurone: a brief profile of a new butenolide insecticide. Pest Management Science 71, 850–862. https://doi.org/10.1002/ps.3932
Simon-Delso, N., Amaral-Rogers, V., Belzunces, L.P., Bonmatin, J.M., Chagnon, M., Downs, C., Furlan, L., Gibbons, D.W., Giorio, C., Girolami, V., Goulson, D., Kreutzweiser, D.P., Krupke, C.H., Liess, M., Long, E., McField, M., Mineau, P., Mitchell, E.A.D., Morrissey, C.A., Noome, D.A., Pisa, L., Settele, J., Stark, J.D., Tapparo, A., Van Dyck, H., Van Praagh, J., Van der Sluijs, J.P., Whitehorn, P.R., Wiemers, M., 2015. Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ Sci Pollut Res 22, 5–34. https://doi.org/10.1007/s11356-014-3470-y
Somers, J., Nguyen, J., Lumb, C., Batterham, P., Perry, T., 2015. In vivo functional analysis of the Drosophila melanogaster nicotinic acetylcholine receptor Dα6 using the insecticide spinosad. Insect Biochemistry and Molecular Biology 64, 116–127. https://doi.org/10.1016/j.ibmb.2015.01.018
Somers, J., Luong, H.N.B., Batterham, P., Perry, T., 2018. Deletion of the nicotinic acetylcholine receptor subunit gene Dα1 confers insecticide resistance, but at what cost? Fly 12, 46–54. https://doi.org/10.1080/19336934.2017.1396399
Sparks, T.C., Watson, G.B., Loso, M.R., Geng, C., Babcock, J.M., Thomas, J.D., 2013. Sulfoxaflor and the sulfoximine insecticides: chemistry, mode of action and basis for efficacy on resistant insects. Pesticide Biochemistry and Physiology 107, 1–7. https://doi.org/10.1016/j.pestbp.2013.05.014
Thany, S.H., 2010. Neonicotinoid insecticides, in: Thany, S.H. (Ed.), Insect Nicotinic Acetylcholine Receptors, Advances in Experimental Medicine and Biology. Springer, New York, NY, pp. 75–83. https://doi.org/10.1007/978-1-4419-6445-8_7
Wang, X., Anadón, A., Wu, Q., Qiao, F., Ares, I., Martínez-Larrañaga, M.-R., Yuan, Z., Martínez, M.-A., 2018. Mechanism of neonicotinoid toxicity: impact on oxidative stress and metabolism. Annual Review of Pharmacology and Toxicology 58, 471–507. https://doi.org/10.1146/annurev-pharmtox-010617-052429
Watson, G.B., Olson, M.B., Beavers, K.W., Loso, M.R., Sparks, T.C., 2017. Characterization of a nicotinic acetylcholine receptor binding site for sulfoxaflor, a new sulfoximine insecticide for the control of sap-feeding insect pests. Pesticide Biochemistry and Physiology 143, 90–94. https://doi.org/10.1016/j.pestbp.2017.09.003
Watson, G.B., Loso, M.R., Babcock, J.M., Hasler, J.M., Letherer, T.J., Young, C.D., Zhu, Y., Casida, J.E., Sparks, T.C., 2011. Novel nicotinic action of the sulfoximine insecticide sulfoxaflor. Insect Biochemistry and Molecular Biology, Special Issue: Toxicology and Resistance 41, 432–439. https://doi.org/10.1016/j.ibmb.2011.01.009
Zhu, Y., Loso, M.R., Watson, Gerald.B., Sparks, T.C., Rogers, R.B., Huang, J.X., Gerwick, B.C., Babcock, J.M., Kelley, D., Hegde, V.B., Nugent, B.M., Renga, J.M., Denholm, I., Gorman, K., DeBoer, G.J., Hasler, J., Meade, T., Thomas, J.D., 2011. Discovery and characterization of sulfoxaflor, a novel insecticide targeting sap-feeding pests. J. Agric. Food Chem. 59, 2950–2957. https://doi.org/10.1021/jf102765x

Larval exposure

Azpiazu, C., Bosch, J., Viñuela, E., Medrzycki, P., Teper, D., Sgolastra, F., 2019. Chronic oral exposure to field-realistic pesticide combinations via pollen and nectar: effects on feeding and thermal performance in a solitary bee. Scientific Reports 9, 1–11. https://doi.org/10.1038/s41598-019-50255-4
Christesen, D., Yang, Y.T., Somers, J., Robin, C., Sztal, T., Batterham, P., Perry, T., 2017. Transcriptome analysis of Drosophila melanogaster third instar larval ring glands points to novel functions and uncovers a cytochrome P450 required for development. G3: Genes, Genomes, Genetics 7, 467–479. https://doi.org/10.1534/g3.116.037333
Dai, P., Jack, C.J., Mortensen, A.N., Bustamante, T.A., Bloomquist, J.R., Ellis, J.D., 2019. Chronic toxicity of clothianidin, imidacloprid, chlorpyrifos, and dimethoate to Apis mellifera L. larvae reared in vitro. Pest Management Science 75, 29–36. https://doi.org/10.1002/ps.5124
Derecka, K., Blythe, M.J., Malla, S., Genereux, D.P., Guffanti, A., Pavan, P., Moles, A., Snart, C., Ryder, T., Ortori, C.A., Barrett, D.A., Schuster, E., Stöger, R., 2013. Transient exposure to low levels of insecticide affects metabolic networks of honey bee larvae. PLOS ONE 8, e68191. https://doi.org/10.1371/journal.pone.0068191
Friol, P.S., Catae, A.F., Tavares, D.A., Malaspina, O., Roat, T.C., 2017. Can the exposure of Apis mellifera (Hymenoptera, Apiadae) larvae to a field concentration of thiamethoxam affect newly emerged bees? Chemosphere 185, 56–66. https://doi.org/10.1016/j.chemosphere.2017.06.113
Glavinic, U., Tesovnik, T., Stevanovic, J., Zorc, M., Cizelj, I., Stanimirovic, Z., Narat, M., 2019. Response of adult honey bees treated in larval stage with prochloraz to infection with Nosema ceranae. PeerJ 7, e6325. https://doi.org/10.7717/peerj.6325
Human, H., Archer, C.R., du Rand, E.E., Pirk, C.W.W., Nicolson, S.W., 2014. Resistance of developing honeybee larvae during chronic exposure to dietary nicotine. Journal of Insect Physiology 69, 74–79. https://doi.org/10.1016/j.jinsphys.2014.03.012
Mogren, C.L., Danka, R.G., Healy, K.B., 2019. Larval pollen stress increases adult susceptibility to clothianidin in honey bees. Insects 10, 21. https://doi.org/10.3390/insects10010021
Nicholls, E., Fowler, R., Niven, J.E., Gilbert, J.D., Goulson, D., 2017. Larval exposure to field-realistic concentrations of clothianidin has no effect on development rate, over-winter survival or adult metabolic rate in a solitary bee, Osmia bicornis. PeerJ 5, e3417. https://doi.org/10.7717/peerj.3417
Papach, A., Fortini, D., Grateau, S., Aupinel, P., Richard, F.-J., 2017. Larval exposure to thiamethoxam and American foulbrood: effects on mortality and cognition in the honey bee Apis mellifera. Journal of Apicultural Research 56, 475–486. https://doi.org/10.1080/00218839.2017.1332541
Mesquita, R. da S., Kyrylchuk, A., Grafova, I., Kliukovskyi, D., Bezdudnyy, A., Rozhenko, A., Tadei, W.P., Leskelä, M., Grafov, A., 2020. Synthesis, molecular docking studies, and larvicidal activity evaluation of new fluorinated neonicotinoids against Anopheles darlingi larvae. PLOS ONE 15, e0227811. https://doi.org/10.1371/journal.pone.0227811
Tadei, R., Domingues, C.E.C., Malaquias, J.B., Camilo, E.V., Malaspina, O., Silva-Zacarin, E.C.M., 2019. Late effect of larval co-exposure to the insecticide clothianidin and fungicide pyraclostrobin in Africanized Apis mellifera. Scientific Reports 9, 3277. https://doi.org/10.1038/s41598-019-39383-z
Tavares, D.A., Dussaubat, C., Kretzschmar, A., Carvalho, S.M., Silva-Zacarin, E.C.M., Malaspina, O., Bérail, G., Brunet, J.-L., Belzunces, L.P., 2017. Exposure of larvae to thiamethoxam affects the survival and physiology of the honey bee at post-embryonic stages. Environmental Pollution 229, 386–393. https://doi.org/10.1016/j.envpol.2017.05.092
Tavares, D.A., Roat, T.C., Carvalho, S.M., Silva-Zacarin, E.C.M., Malaspina, O., 2015. In vitro effects of thiamethoxam on larvae of Africanized honey bee Apis mellifera (Hymenoptera: Apidae). Chemosphere 135, 370–378. https://doi.org/10.1016/j.chemosphere.2015.04.090
Tavares, D.A., Roat, T.C., Silva-Zacarin, E.C.M., Nocelli, R.C.F., Malaspina, O., 2019. Exposure to thiamethoxam during the larval phase affects synapsin levels in the brain of the honey bee. Ecotoxicology and Environmental Safety 169, 523–528. https://doi.org/10.1016/j.ecoenv.2018.11.048
Vázquez, D.E., Ilina, N., Pagano, E.A., Zavala, J.A., Farina, W.M., 2018. Glyphosate affects the larval development of honey bees depending on the susceptibility of colonies. PLOS ONE 13, e0205074. https://doi.org/10.1371/journal.pone.0205074
Wade, A., Lin, C.-H., Kurkul, C., Regan, E., Johnson, R., Wade, A., Lin, C.-H., Kurkul, C., Regan, E.R., Johnson, R.M., 2019. Combined toxicity of insecticides and fungicides applied to California almond orchards to honey bee larvae and adults. Insects 10, 20. https://doi.org/10.3390/insects10010020
Wang, K., Fan, R.-L., Ji, W.-N., Zhang, W.-W., Chen, X.-M., Wang, S., Yin, L., Gao, F.-C., Chen, G.-H., Ji, T., 2018. Transcriptome analysis of newly emerged honeybees exposure to sublethal carbendazim during larval stage. Frontiers in Genetics 9, 426. https://doi.org/10.3389/fgene.2018.00426
Whitehorn, P.R., Norville, G., Gilburn, A., Goulson, D., 2018. Larval exposure to the neonicotinoid imidacloprid impacts adult size in the farmland butterfly Pieris brassicae. PeerJ 6, e4772. https://doi.org/10.7717/peerj.4772
Wu, J.Y., Anelli, C.M., Sheppard, W.S., 2011. Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLOS ONE 6, e14720. https://doi.org/10.1371/journal.pone.0014720
Wu, M.-C., Chang, Y.-W., Lu, K.-H., Yang, E.-C., 2017. Gene expression changes in honey bees induced by sublethal imidacloprid exposure during the larval stage. Insect Biochemistry and Molecular Biology 88, 12–20. https://doi.org/10.1016/j.ibmb.2017.06.016
Zhu, W., Schmehl, D.R., Mullin, C.A., Frazier, J.L., 2014. Four common pesticides, their mixtures and a formulation solvent in the hive environment have high oral toxicity to honey bee larvae. PLOS ONE 9, e77547. https://doi.org/10.1371/journal.pone.0077547
Smith Dylan B., Arce Andres N., Ramos Rodrigues Ana, Bischoff Philipp H., Burris Daisy, Ahmed Farah and Gill Richard J. 2020. Insecticide exposure during brood or early-adult development reduces brain growth and impairs adult learning in bumblebeesProc. R. Soc. B.28720192442 http://doi.org/10.1098/rspb.2019.2442
Claus et al. 2021. Larval oral exposure to thiacloprid: Dose-response toxicity testing in solitary bees, Osmia spp. (Hymenoptera: Megachilidae) Author links open overlay panel: https://doi.org/10.1016/j.ecoenv.2021.112143

Routes of exposure

Bonmatin, J.-M., Giorio, C., Girolami, V., Goulson, D., Kreutzweiser, D.P., Krupke, C., Liess, M., Long, E., Marzaro, M., Mitchell, E.A.D., Noome, D.A., Simon-Delso, N., Tapparo, A., 2015. Environmental fate and exposure; neonicotinoids and fipronil. Environmental Science and Pollution Research 22, 35–67. https://doi.org/10.1007/s11356-014-3332-7
Hladik, M.L., Vandever, M., Smalling, K.L., 2016. Exposure of native bees foraging in an agricultural landscape to current-use pesticides. Science of The Total Environment 542, 469–477. https://doi.org/10.1016/j.scitotenv.2015.10.077
Kopit, A.M., Pitts-Singer, T.L., 2018. Routes of pesticide exposure in solitary, cavity-nesting bees. Environmental Entomology 47, 499–510. https://doi.org/10.1093/ee/nvy034
Krupke, C.H., Hunt, G.J., Eitzer, B.D., Andino, G., Given, K., 2012. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLOS ONE 7, e29268. https://doi.org/10.1371/journal.pone.0029268
Radolinski, J., Wu, J., Xia, K., Hession, W.C., Stewart, R.D., 2019. Plants mediate precipitation-driven transport of a neonicotinoid pesticide. Chemosphere 222, 445–452. https://doi.org/10.1016/j.chemosphere.2019.01.150
Siviter, H., Bailes, E.J., Martin, C.D. et al. Agrochemicals interact synergistically to increase bee mortality. Nature (2021). https://doi.org/10.1038/s41586-021-03787-7

Economic value

Bauer, D.M., Sue Wing, I., 2016. The macroeconomic cost of catastrophic pollinator declines. Ecological Economics 126, 1–13. https://doi.org/10.1016/j.ecolecon.2016.01.011
Breeze, T.D., Gallai, N., Garibaldi, L.A., Li, X.S., 2016. Economic measures of pollination services: Shortcomings and future directions. Trends in Ecology & Evolution 31, 927–939. https://doi.org/10.1016/j.tree.2016.09.002
Carreck, N., Williams, I., 1998. The economic value of bees in the UK. Bee World 79, 115–123. https://doi.org/10.1080/0005772X.1998.11099393
Gallai, N., Salles, J.-M., Settele, J., Vaissière, B.E., 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68, 810–821. https://doi.org/10.1016/j.ecolecon.2008.06.014
Garratt, M.P.D., Breeze, T.D., Jenner, N., Polce, C., Biesmeijer, J.C., Potts, S.G., 2014a. Avoiding a bad apple: Insect pollination enhances fruit quality and economic value. Agriculture, Ecosystems & Environment 184, 34–40. https://doi.org/10.1016/j.agee.2013.10.032
Garratt, M.P.D., Coston, D.J., Truslove, C.L., Lappage, M.G., Polce, C., Dean, R., Biesmeijer, J.C., Potts, S.G., 2014b. The identity of crop pollinators helps target conservation for improved ecosystem services. Biological Conservation 169, 128–135. https://doi.org/10.1016/j.biocon.2013.11.001
Hanley, N., Breeze, T.D., Ellis, C., Goulson, D., 2015. Measuring the economic value of pollination services: Principles, evidence and knowledge gaps. Ecosystem Services 14, 124–132. https://doi.org/10.1016/j.ecoser.2014.09.013
Leonhardt, S.D., Gallai, N., Garibaldi, L.A., Kuhlmann, M., Klein, A.-M., 2013. Economic gain, stability of pollination and bee diversity decrease from southern to northern Europe. Basic and Applied Ecology 14, 461–471. https://doi.org/10.1016/j.baae.2013.06.003
Melathopoulos, A.P., Cutler, G.C., Tyedmers, P., 2015. Where is the value in valuing pollination ecosystem services to agriculture? Ecological Economics 109, 59–70. https://doi.org/10.1016/j.ecolecon.2014.11.007
Tscharntke, T., Clough, Y., Wanger, T.C., Jackson, L., Motzke, I., Perfecto, I., Vandermeer, J., Whitbread, A., 2012. Global food security, biodiversity conservation and the future of agricultural intensification. Biological Conservation 151, 53–59. https://doi.org/10.1016/j.biocon.2012.01.068
Vanbergen, A.J., Heard, M.S., Breeze, T.D., Potts, S.G., Hanley, N., 2014. Status and value of pollinators and pollination services (No. PH0514), Department for Environment, Food and Rural Affairs (Defra).
Winfree, R., Gross, B.J., Kremen, C., 2011. Valuing pollination services to agriculture. Ecological Economics 71, 80–88. https://doi.org/10.1016/j.ecolecon.2011.08.001

Methylation

Brevik K., Lindström L., McKay S., Chen Y., 2018. Transgenerational effects of insecticides — implications for rapid pest evolution in agroecosystems. Current Opinion in Insect Science 26, 34-40. https://doi.org/10.1016/j.cois.2017.12.007
Brevik K., Bueno E. M., McKay S., Schoville S. D., Chen Y., 2020. Insecticide exposure affects intergenerational patterns of DNA methylation in the Colorado potato beetle, Leptinotarsa decemlineata. Evolutionary Applications. https://doi.org/10.1111/eva.13153
Hollie Marshall, Alun R C Jones, Zoë N Lonsdale, Eamonn B Mallon, Bumblebee Workers Show Differences in Allele-Specific DNA Methylation and Allele-Specific Expression, Genome Biology and Evolution, Volume 12, Issue 8, August 2020, Pages 1471–1481, https://doi.org/10.1093/gbe/evaa132 METHODS
Navin Elango, Brendan G. Hunt, Michael A. D. Goodisman, Soojin V. Yi, 2009. DNA methylation is widespread and associated with differential gene expression in castes of the honeybee, Apis mellifera. Proceedings of the National Academy of Sciences, 106 (27) 11206-11211; DOI: 10.1073/pnas.0900301106
Robert A. Drewell, Eliot C. Bush, Emily J. Remnant, Garrett T. Wong, Suzannah M. Beeler, Jessica L. Stringham, Julianne Lim, Benjamin P. Oldroyd. 2014. The dynamic DNA methylation cycle from egg to sperm in the honey bee Apis mellifera Development 141:2702-2711; doi: 10.1242/dev.110163
Amarasinghe Harindra E., Clayton Crisenthiya I. and Mallon Eamonn B. 2014. Methylation and worker reproduction in the bumble-bee (Bombus terrestris) Proc. R. Soc. B.28120132502 http://doi.org/10.1098/rspb.2013.2502 METHODS BUMBEBEE
"Epigenetics in an ecotoxicological context" https://doi.org/10.1016/j.mrgentox.2013.08.008

Testing

Vijver et al. 2017. Postregistration monitoring of pesticides is urgently required to protect ecosystems. https://doi.org/10.1002/etc.3721
Francisco Sánchez-Bayo and Henk A. Tennekes. 2014. Environmental Risk Assessment of Agrochemicals — A Critical Appraisal of Current Approaches. https://doi.org/10.5772/60739
Schäfer R. B. et al. 2019. Future pesticide risk assessment: narrowing the gap between intention and reality. https://doi.org/10.1186/s12302-019-0203-3
Francisco Sánchez-Bayo and Henk A. Tennekes. 2017. Assessment of ecological risks of agrochemicals requires a new framework. https://doi.org/10.4066/2529-8046.100025
Robinson C. et al. 2020. Achieving a High Level of Protection from Pesticides in Europe: Problems with the Current Risk Assessment Procedure and Solutions https://doi.org/10.1017/err.2020.18
Klimisch H. J. et al. 1997. A systematic approach for evaluating the quality of experimental toxicological and ecotoxicological data. https://doi.org/10.1006/rtph.1996.1076
- A. M. Milner, I. L. Boyd. 2017. Toward pesticidovigilance. https://doi.org/10.1126/science.aan2683

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Table of contents

Introduction

Reviews on pollinators and neonicotinoid insecticides

Highly cited

Declines of insect pollinators

Exposure of insect pollinators to neonicotinoids

Pesticide levels in pollen and nectar

Dosage effects

Gene expression

nAChRs

Pesticides

Larval exposure

Routes of exposure

Economic value

Methylation

Testing

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Table of contents

Introduction

Reviews on pollinators and neonicotinoid insecticides

Highly cited

Declines of insect pollinators

Exposure of insect pollinators to neonicotinoids

Pesticide levels in pollen and nectar

Dosage effects

Gene expression

nAChRs

Pesticides

Larval exposure

Routes of exposure

Economic value

Methylation

Testing

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