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Varying impact of neonicotinoid insecticide and acute bee paralysis virus across castes and colonies of black garden ants, Lasius niger (Hymenoptera: Formicidae)

  • 1.

    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. https://doi.org/10.1371/journal.pone.0185809 (2017).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 2.

    Cardoso, P. et al. Scientists’ warning to humanity on insect extinctions. Biol. Conserv. https://doi.org/10.1016/j.biocon.2020.108426 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 3.

    van Klink, R. et al. Meta-analysis reveals declines in terrestrial but increases in freshwater insect abundances. Science 368, 417–420. https://doi.org/10.1126/science.aax9931 (2020).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 4.

    Costanza, R. et al. The value of the world’s ecosystem services and natural capital. Nature 387, 253. https://doi.org/10.1038/387253a0 (1997).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 5.

    Hill, D. S. The Economic Importance of Insects (Springer, 2012). https://doi.org/10.1007/978-94-011-5348-5.

    Book 

    Google Scholar 

  • 6.

    Gallai, N., Salles, J.-M., Settele, J. & Vaissière, B. E. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 68, 810–821. https://doi.org/10.1016/j.ecolecon.2008.06.014 (2009).

    Article 

    Google Scholar 

  • 7.

    Neumann, P. et al. Ecosystem services, agriculture and neonicotinoids. EASAC Policy Rep. 26, 1–53 (2015).

    CAS 

    Google Scholar 

  • 8.

    Sánchez-Bayo, F. & Wyckhuys, K. A. Worldwide decline of the entomofauna: a review of its drivers. Biol. Cons. 232, 8–27. https://doi.org/10.1016/j.biocon.2019.01.020 (2019).

    Article 

    Google Scholar 

  • 9.

    Seibold, S. et al. Arthropod decline in grasslands and forests is associated with landscape-level drivers. Nature 574, 671–674. https://doi.org/10.1038/s41586-019-1684-3 (2019).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 10.

    Wagner, D. L. Insect declines in the Anthropocene. Annu. Rev. Entomol. 65, 457–480. https://doi.org/10.1146/annurev-ento-011019-025151 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 11.

    Potts, S. G. et al. Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345–353. https://doi.org/10.1016/j.tree.2010.01.007 (2010).

    Article 
    PubMed 

    Google Scholar 

  • 12.

    Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957. https://doi.org/10.1126/science.1255957 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 13.

    Chagnon, M. et al. Risks of large-scale use of systemic insecticides to ecosystem functioning and services. Environ. Sci. Pollut. Res. 22, 119–134. https://doi.org/10.1007/s11356-014-3277-x (2015).

    CAS 
    Article 

    Google Scholar 

  • 14.

    Pisa, L. W. et al. Effects of neonicotinoids and fipronil on non-target invertebrates. Environ. Sci. Pollut. Res. 22, 68–102. https://doi.org/10.1007/s11356-014-3471-x (2015).

    CAS 
    Article 

    Google Scholar 

  • 15.

    Stanley, J. & Preetha, G. Pesticide Toxicity to Non-target Organisms (Springer, 2016). https://doi.org/10.1007/978-94-017-7752-0.

    Book 

    Google Scholar 

  • 16.

    Wood, T. J. & Goulson, D. The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environ. Sci. Pollut. Res. 24, 17285–17325. https://doi.org/10.1007/s11356-017-9240-x (2017).

    CAS 
    Article 

    Google Scholar 

  • 17.

    Humann-Guilleminot, S. et al. A nation-wide survey of neonicotinoid insecticides in agricultural land with implications for agri-environment schemes. J. Appl. Ecol. 56, 1502–1514. https://doi.org/10.1111/1365-2664.13392 (2019).

    CAS 
    Article 

    Google Scholar 

  • 18.

    Goulson, D. Review: an overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol. 50, 977–987. https://doi.org/10.1111/1365-2664.12111 (2013).

    Article 

    Google Scholar 

  • 19.

    Hilton, M. J., Jarvis, T. D. & Ricketts, D. C. The degradation rate of thiamethoxam in European field studies. Pest Manag. Sci. 72, 388–397. https://doi.org/10.1002/ps.4024 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 20.

    Lewis, K. A., Tzilivakis, J., Warner, D. J. & Green, A. An international database for pesticide risk assessments and management. Hum. Ecol. Risk Assess. Int. J. 22, 1050–1064. https://doi.org/10.1080/10807039.2015.1133242 (2016).

    CAS 
    Article 

    Google Scholar 

  • 21.

    Li, Y. et al. Adsorption-desorption and degradation of insecticides clothianidin and thiamethoxam in agricultural soils. Chemosphere 207, 708–714. https://doi.org/10.1016/j.chemosphere.2018.05.139 (2018).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 22.

    Nauen, R., Ebbinghaus-Kintscher, U., Salgado, V. L. & Kaussmann, M. Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pestic. Biochem. Physiol. 76, 55–69. https://doi.org/10.1016/S0048-3575(03)00065-8 (2003).

    CAS 
    Article 

    Google Scholar 

  • 23.

    Straub, L. et al. Neonicotinoid insecticides can serve as inadvertent insect contraceptives. Proc. R. Soc. B 283, 20160506. https://doi.org/10.1098/rspb.2016.0506 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 24.

    Blacquiere, T., Smagghe, G., Van Gestel, C. A. & Mommaerts, V. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21, 973–992. https://doi.org/10.1007/s10646-012-0890-7 (2012).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 25

    Straub, L., Strobl, V. & Neumann, P. The need for an evolutionary approach to ecotoxicology. Nat. Ecol. Evol. https://doi.org/10.1038/s41559-020-1194-6 (2020).

    Article 
    PubMed 

    Google Scholar 

  • 26.

    Wilson, E. O. The Insect Societies (Harvard University Press, 1971).

    Google Scholar 

  • 27.

    Schläppi, D., Kettler, N., Straub, L., Glauser, G. & Neumann, P. Long-term effects of neonicotinoid insecticides on ants. Commun. Biol. 3, 335. https://doi.org/10.1038/s42003-020-1066-2 (2020).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 28.

    Schläppi, D., Stroeymeyt, N. & Neumann, P. Unintentional effects of neonicotinoids on ants (Hymenoptera: Formicidae). Myrmecological News, in press.

  • 29

    Straub, L., Williams, G. R., Pettis, J., Fries, I. & Neumann, P. Superorganism resilience: eusociality and susceptibility of ecosystem service providing insects to stressors. Curr. Opin. Insect Sci. 12, 109–112. https://doi.org/10.1016/j.cois.2015.10.010 (2015).

    Article 

    Google Scholar 

  • 30.

    Cremer, S. Social immunity in insects. Curr. Biol. 29, R458–R463. https://doi.org/10.1016/j.cub.2019.03.035 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 31.

    Straub, L. et al. From antagonism to synergism: extreme differences in stressor interactions in one species. Sci. Rep. 10, 1–8. https://doi.org/10.1038/s41598-020-61371-x (2020).

    CAS 
    Article 

    Google Scholar 

  • 32.

    Crall, J. D. et al. Neonicotinoid exposure disrupts bumblebee nest behavior, social networks, and thermoregulation. Science 362, 683–686. https://doi.org/10.1126/science.aat1598 (2018).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 33

    Hölldobler, B. & Wilson, E. O. The Ants (Springer, 1990). https://doi.org/10.1046/j.1420-9101.1992.5010169.x.

    Book 

    Google Scholar 

  • 34.

    Del Toro, I., Ribbons, R. R. & Pelini, S. L. The little things that run the world revisited: a review of ant-mediated ecosystem services and disservices (Hymenoptera: Formicidae). Myrmecol. News 17, 133–146 (2012).

    Google Scholar 

  • 35.

    Keller, L. & Genoud, M. Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389, 958. https://doi.org/10.1038/40130 (1997).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 36

    Bird, G., Wilson, A. E., Williams, G. R. & Hardy, N. B. Parasites and pesticides act antagonistically on honey bee health. J. Appl. Ecol. https://doi.org/10.1111/1365-2664.13811 (2020).

    Article 

    Google Scholar 

  • 37.

    Siviter, H. et al. Agrochemicals interact synergistically to increase bee mortality. Nature 596, 389–392. https://doi.org/10.1038/s41586-021-03787-7 (2021).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 38.

    Ranjeva, S. et al. Age-specific differences in the dynamics of protective immunity to influenza. Nat. Commun. 10, 1–11. https://doi.org/10.1038/s41467-019-09652-6 (2019).

    CAS 
    Article 

    Google Scholar 

  • 39.

    Dahlgren, L., Johnson, R. M., Siegfried, B. D. & Ellis, M. D. Comparative toxicity of acaricides to honey bee (Hymenoptera: Apidae) workers and queens. J. Econ. Entomol. 105, 1895–1902. https://doi.org/10.1603/EC12175 (2012).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 40

    O’Neal, T. S., Anderson, T. D. & Wu-Smart, J. Y. Interactions between pesticides and pathogen susceptibility in honey bees. Curr. Opin. Insect Sci. 26, 57–62. https://doi.org/10.1016/j.cois.2018.01.006 (2018).

    Article 
    PubMed 

    Google Scholar 

  • 41.

    Feldhaar, H. & Otti, O. Pollutants and their interaction with diseases of social hymenoptera. Insects 11, 153. https://doi.org/10.3390/insects11030153 (2020).

    Article 
    PubMed Central 

    Google Scholar 

  • 42.

    Doublet, V., Labarussias, M., de Miranda, J. R., Moritz, R. F. & Paxton, R. J. Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environ. Microbiol. 17, 969–983. https://doi.org/10.1111/1462-2920.12426 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 43.

    Sánchez-Bayo, F. et al. Are bee diseases linked to pesticides?—a brief review. Environ. Int. 89, 7–11. https://doi.org/10.1016/j.envint.2016.01.009 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 44.

    Annoscia, D. et al. Neonicotinoid Clothianidin reduces honey bee immune response and contributes to Varroa mite proliferation. Nat. Commun. 11, 1–7. https://doi.org/10.1038/s41467-020-19715-8 (2020).

    CAS 
    Article 

    Google Scholar 

  • 45.

    Di Prisco, G. et al. Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proc. Natl. Acad. Sci. 110, 18466–18471. https://doi.org/10.1073/pnas.1314923110 (2013).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 46.

    Coulon, M. et al. Influence of chronic exposure to thiamethoxam and chronic bee paralysis virus on winter honey bees. PLoS ONE 14, e0220703. https://doi.org/10.1371/journal.pone.0220703 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 47.

    Brandt, A. et al. Immunosuppression in honeybee queens by the neonicotinoids thiacloprid and clothianidin. Sci. Rep. 7, 4673. https://doi.org/10.1038/s41598-017-04734-1 (2017).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 48.

    Beaurepaire, A. et al. Diversity and global distribution of viruses of the western honey bee, Apis mellifera. Insects 11, 239. https://doi.org/10.3390/insects11040239 (2020).

    Article 
    PubMed Central 

    Google Scholar 

  • 49.

    Martin, S. J. et al. Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304–1306. https://doi.org/10.1126/science.1220941 (2012).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 50.

    Wilfert, L. et al. Deformed wing virus is a recent global epidemic in honeybees driven by Varroa mites. Science 351, 594–597. https://doi.org/10.1126/science.aac9976 (2016).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 51.

    Neumann, P., Yañez, O., Fries, I. & De Miranda, J. R. Varroa invasion and virus adaptation. Trends Parasitol. 28, 353–354. https://doi.org/10.1016/j.pt.2012.06.004 (2012).

    Article 
    PubMed 

    Google Scholar 

  • 52.

    Woolhouse, M. E., Haydon, D. T. & Antia, R. Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol. Evol. 20, 238–244. https://doi.org/10.1016/j.tree.2005.02.009 (2005).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 53.

    McMahon, D. P. et al. A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. J. Anim. Ecol. 84, 615–624. https://doi.org/10.1111/1365-2656.12345 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 54.

    Levitt, A. L. et al. Cross-species transmission of honey bee viruses in associated arthropods. Virus Res. 176, 232–240. https://doi.org/10.1016/j.virusres.2013.06.013 (2013).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 55.

    Tehel, A., Brown, M. J. & Paxton, R. J. Impact of managed honey bee viruses on wild bees. Curr. Opin. Virol. 19, 16–22. https://doi.org/10.1016/j.coviro.2016.06.006 (2016).

    Article 
    PubMed 

    Google Scholar 

  • 56

    Martin, S. J. & Brettell, L. E. Deformed wing virus in honeybees and other insects. Ann. Rev. Virol. https://doi.org/10.1146/annurev-virology-092818-015700 (2019).

    Article 

    Google Scholar 

  • 57.

    Schläppi, D., Lattrell, P., Yañez, O., Chejanovsky, N. & Neumann, P. Foodborne transmission of deformed wing virus to ants (Myrmica rubra). Insects 10, 394. https://doi.org/10.3390/insects10110394 (2019).

    Article 
    PubMed Central 

    Google Scholar 

  • 58.

    Schläppi, D., Chejanovsky, N., Yañez, O. & Neumann, P. Foodborne Transmission and clinical symptoms of honey bee viruses in ants Lasius spp. Viruses 12, 321. https://doi.org/10.3390/v12030321 (2020).

    Article 
    PubMed Central 

    Google Scholar 

  • 59.

    Seifert, B. Die Ameisen Mittel- und Nordeuropas (Lutra Verlags und Vertriebsgesellschaft, 2007).

    Google Scholar 

  • 60.

    Payne, A. N., Shepherd, T. F. & Rangel, J. The detection of honey bee (Apis mellifera)-associated viruses in ants. Sci. Rep. 10, 2923. https://doi.org/10.1038/s41598-020-59712-x (2020).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 61.

    Kutter, H. & Stumper R. Hermann Appel, ein leidgeadelter Entomologe (1892–1966). in Proceedings of the VI Congress of the International Union for the Study of Social Insects (eds Ernst, E., Frauchiger, L., Hauschteck-Jungen, E., Jungen, H., Leuthold, R., Maurizio, A., Ruppli, E. & Tschumi, P.), 275–279 (Organizing Committee of the VI Congress IUSSI, Bern, 1969).

  • 62.

    Jeschke, P., Nauen, R., Schindler, M. & Elbert, A. Overview of the status and global strategy for neonicotinoids. J. Agric. Food Chem. 59, 2897–2908. https://doi.org/10.1021/jf101303g (2011).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 63.

    Limay-Rios, V. et al. Neonicotinoid insecticide residues in soil dust and associated parent soil in fields with a history of seed treatment use on crops in southwestern Ontario. Environ. Toxicol. Chem. 35, 303–310. https://doi.org/10.1002/etc.3257 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 64.

    Schaafsma, A., Limay-Rios, V., Xue, Y., Smith, J. & Baute, T. Field-scale examination of neonicotinoid insecticide persistence in soil as a result of seed treatment use in commercial maize (corn) fields in southwestern Ontario. Environ. Toxicol. Chem. 35, 295–302. https://doi.org/10.1002/etc.3231 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 65.

    De Miranda, J. R., Cordoni, G. & Budge, G. The acute bee paralysis virus–Kashmir bee virus–Israeli acute paralysis virus complex. J. Invertebr. Pathol. 103, 30–47. https://doi.org/10.1016/j.jip.2009.06.014 (2010).

    CAS 
    Article 

    Google Scholar 

  • 66

    Decourtye, A. & Devillers, J. Ecotoxicity of neonicotinoid insecticides to bees. In Insect Nicotinic Acetylcholine Receptors (ed. Thany, S. H.) 85–95 (Springer, 2010).

    Chapter 

    Google Scholar 

  • 67.

    Diez, L., Lejeune, P. & Detrain, C. Keep the nest clean: survival advantages of corpse removal in ants. Biol. Let. 10, 20140306. https://doi.org/10.1098/rsbl.2014.0306 (2014).

    Article 

    Google Scholar 

  • 68.

    Wang, L., Zeng, L. & Chen, J. Impact of imidacloprid on new queens of imported fire ants, Solenopsis invicta (Hymenoptera: Formicidae). Sci. Rep. 5, 17938. https://doi.org/10.1038/srep17938 (2015).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 69.

    Moya-Laraño, J., Macías-Ordóñez, R., Blanckenhorn, W. U. & Fernández-Montraveta, C. Analysing body condition: mass, volume or density?. J. Anim. Ecol. 77, 1099–1108. https://doi.org/10.1111/j.1365-2656.2008.01433.x (2008).

    Article 
    PubMed 

    Google Scholar 

  • 70

    Knapp, M., Knappová, J. & Miller, T. Measurement of body condition in a common carabid beetle, Poecilus cupreus: a comparison of fresh weight, dry weight, and fat content. J. Insect Sci. https://doi.org/10.1673/031.013.0601 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 71.

    Retschnig, G. et al. Sex-specific differences in pathogen susceptibility in honey bees (Apis mellifera). PLoS ONE 9, e85261. https://doi.org/10.1371/journal.pone.0085261 (2014).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 72.

    Suchail, S., Guez, D. & Belzunces, L. P. Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ. Toxicol. Chem. Int. J. 20, 2482–2486. https://doi.org/10.1002/etc.5620201113 (2001).

    CAS 
    Article 

    Google Scholar 

  • 73.

    Helms, K. R. & Vinson, S. B. Plant resources and colony growth in an invasive ant: the importance of honeydew-producing hemiptera in carbohydrate transfer across trophic levels. Environ. Entomol. 37, 487–493. https://doi.org/10.1093/ee/37.2.487 (2008).

    Article 
    PubMed 

    Google Scholar 

  • 74.

    Dornhaus, A. & Franks, N. R. Colony size affects collective decision-making in the ant Temnothorax albipennis. Insectes Soc. 53, 420–427. https://doi.org/10.1007/s00040-006-0887-4 (2006).

    Article 

    Google Scholar 

  • 75.

    Ruel, C., Cerda, X. & Boulay, R. Behaviour-mediated group size effect constrains reproductive decisions in a social insect. Anim. Behav. 84, 853–860. https://doi.org/10.1016/j.anbehav.2012.07.006 (2012).

    Article 

    Google Scholar 

  • 76.

    Sommer, K. & Hölldobler, B. Colony founding by queen association and determinants of reduction in queen number in the ant Lasius niger. Anim. Behav. 50, 287–294. https://doi.org/10.1006/anbe.1995.0244 (1995).

    Article 

    Google Scholar 

  • 77

    Boomsma, J., Van der Lee, G. & Van der Have, T. On the production ecology of Lasius niger (Hymenoptera: Formicidae) in successive coastal dune valleys. J. Anim. Ecol. https://doi.org/10.2307/4017 (1982).

    Article 

    Google Scholar 

  • 78.

    Zioni, N., Soroker, V. & Chejanovsky, N. Replication of varroa destructor virus 1 (VDV-1) and a varroa destructor virus 1–deformed wing virus recombinant (VDV-1–DWV) in the head of the honey bee. Virology 417, 106–112. https://doi.org/10.1016/j.virol.2011.05.009 (2011).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 79.

    Wood, T. et al. Managed honey bees as a radar for wild bee decline?. Apidologie 51, 1100–1116. https://doi.org/10.1007/s13592-020-00788-9 (2020).

    Article 

    Google Scholar 

  • 80.

    Stroeymeyt, N. et al. Social network plasticity decreases disease transmission in a eusocial insect. Science 362, 941–945. https://doi.org/10.1126/science.aat4793 (2018).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 81.

    Folt, C., Chen, C., Moore, M. & Burnaford, J. Synergism and antagonism among multiple stressors. Limnol. Oceanogr. 44, 864–877. https://doi.org/10.4319/lo.1999.44.3_part_2.0864 (1999).

    ADS 
    Article 

    Google Scholar 

  • 82.

    Gennings, C. et al. A unifying concept for assessing toxicological interactions: changes in slope. Toxicol. Sci. 88, 287–297. https://doi.org/10.1093/toxsci/kfi275 (2005).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 83.

    Jonker, M. J., Svendsen, C., Bedaux, J. J., 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. Int. J. 24, 2701–2713. https://doi.org/10.1897/04-431R.1 (2005).

    CAS 
    Article 

    Google Scholar 

  • 84.

    Brühl, C. A. & Zaller, J. G. Biodiversity decline as a consequence of an inadequate environmental risk assessment of pesticides. Front. Environ. Sci. 7, 177. https://doi.org/10.3389/fenvs.2019.00177 (2019).

    Article 

    Google Scholar 

  • 85.

    Ortega-Calvo, J.-J. et al. From bioavailability science to regulation of organic chemicals. Environ. Sci. Technol. 49, 10255–10264. https://doi.org/10.1021/acs.est.5b02412 (2015).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 86.

    Dauber, J. & Wolters, V. Edge effects on ant community structure and species richness in an agricultural landscape. Biodivers. Conserv. 13, 901–915. https://doi.org/10.1023/B:BIOC.0000014460.65462.2b (2004).

    Article 

    Google Scholar 

  • 87.

    EFSA PPR Panel (EFSA Panel on Plant Protection Products and their Residues). Scientific Opinion addressing the state of the science on risk assessment of plant protection products for non‐target arthropods. EFSA Journal 13, 3996 (2015). https://doi.org/10.2903/j.efsa.2015.3996

  • 88.

    EFSA PPR Panel (EFSA Panel on Plant Protection Products and their Residues). Scientific Opinion addressing the state of the science on risk assessment of plant protection products for in-soil organisms. EFSA Journal 15, 4690. https://doi.org/10.2903/j.efsa.2017.4690 (2017).

  • 89.

    Organization for Economic Cooperation and Development (OECD). OECD Guidelines for the Testing of Chemicals, section 2—Effects on Biotic Systems. (OECD Publishing, 2019).

  • 90.

    Storck, V., Karpouzas, D. G. & Martin-Laurent, F. Towards a better pesticide policy for the European Union. Sci. Total Environ. 575, 1027–1033. https://doi.org/10.1016/j.scitotenv.2016.09.167 (2017).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 91.

    De Miranda, J. R. et al. Standard methods for virus research in Apis mellifera. J. Apic. Res. 52, 1–56. https://doi.org/10.3896/IBRA.1.52.4.22 (2013).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 92.

    Evans, J. D. et al. Standard methods for molecular research in Apis mellifera. J. Apic. Res. 52, 1–54. https://doi.org/10.3896/IBRA.1.52.4.11 (2013).

    CAS 
    Article 

    Google Scholar 

  • 93.

    Lowenthal, M. S., Quittman, E. & Phinney, K. W. Absolute quantification of RNA or DNA using acid hydrolysis and mass spectrometry. Anal. Chem. 91, 14569–14576. https://doi.org/10.1021/acs.analchem.9b03625 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 94.

    Locke, B., Forsgren, E., Fries, I. & De Miranda, J. R. Acaricide treatment affects viral dynamics in Varroa destructor-infested honey bee colonies via both host physiology and mite control. Appl. Environ. Microbiol. 78, 227–235. https://doi.org/10.1128/AEM.06094-11 (2012).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 95.

    R Development Core Team. R: A language and environment for statistical computing. R Version 3.6.3. R Foundation for Statistical Computing (Vienna, 2020). http://cran.r-project.org.

  • 96.

    Therneau, T. A Package for Survival Analysis in S. version 2.38 (2015). http://cran.rproject.org/package=survival

  • 97.

    Kutner, M. H., Nachtsheim, C. J., Neter, J. & Li, W. Applied Linear Statistical Models Vol. 5 (McGraw-Hill Irwin, 2005).

    Google Scholar 

  • 98.

    Wobbrock, J. O., Findlater, L., Gergle, D. & Higgins, J. J. The aligned rank transform for nonparametric factorial analyses using only anova procedures. in Proceedings of the SIGCHI conference on human factors in computing systems (eds. Tan, D., Fitzpatrick, G., Gutwin, C., Begole, B. & Kellogg, W. A.), 143–146, doi:https://doi.org/10.1145/1978942.1978963 (Association for Computing Machinery, New York, United States, 2011)

  • 99.

    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).

    Article 

    Google Scholar 


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