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Sub-lethal effects of thiamethoxam on Apis mellifera Linnaeus

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Pages 1044-1057 | Received 17 Jul 2021, Accepted 18 Jul 2021, Published online: 26 Dec 2021

References

  • Aizen, M.A. and Harder, L.D., 2009. The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Current biology, 19, 915–918.
  • Aliouane, Y., et al., 2009. Subchronic exposure of honey bees to sublethal doses of pesticides: effects on behaviour. Environmental toxicology and chemistry, 28 (1), 113–122.
  • Ascher, J.S. and Pickering, J., 2021. Discover life: apoidea species guide. Available from: http://www.discoverlife.org [Accessed 15 July 2021].
  • Aupinel, P., et al., 2005. Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. Bulletin of insectology, 58 (2), 107–111.
  • Badiou-Bénéteau, A., et al., 2012. Development of biomarkers of exposure to xenobiotics in the honey bee Apis mellifera: application to the systemic insecticide thiamethoxam. Ecotoxicology and environmental safety, 82, 22–31.
  • Bauer, D.M. and Wing, I.S., 2016. The macroeconomic cost of catastrophic pollinator declines. Ecological economics, 126, 1–13.
  • Beuhne, R., 1910. Bee mortality. Journal of the department of agriculture of Victoria, 7, 149–151.
  • Botias, C., et al., 2016. Contamination of wild plants near neonicotinoid seed-treated crops, and implications for non-target insects. The science of the total environment, 566–567, 269–278.
  • Botias, C., et al., 2015. Neonicotinoid residues in wildflowers, a potential route of chronic exposure for bees. Environmental science and technology, 49 (21), 12731–12740.
  • Bullamore, G.W., 1922. Nosema apis and Acarapis (Tarsonemus) woodi in relation to Isle of Wight disease. Parasitology, 14, 53–62.
  • Carr, E.G., 1918. An unusual disease of honey bees. Journal of economic entomology, 11, 347–351.
  • Catae, A.F., et al., 2014. Cytotoxic effects of thiamethoxam in the midgut and malpighian tubules of Africanized Apis mellifera (Hymenoptera: Apidae). Microscopy research and technique, 77 (4), 274–281.
  • Charreton, M., 2015. A locomotor deficit induced by sublethal doses of pyrethroid and neonicotinoid insecticides in the honey bee Apis mellifera. PLoS One, 10 (12), e0144879.
  • Christen, V., Mittner, F., and Fent, K., 2016. Molecular effects of neonicotinoids in honey bees (Apis mellifera). Environmental science and technology, 50 (7), 4071–4081.
  • Christina, L.M. and Jonathan, G.L., 2016. Neonicotinoid contaminated pollinator strips adjacent to cropland reduce honey bee nutritional status. Scientific reports, 14, 6:29608. doi:10.1038/srep29608.
  • Claudianos, C., et al., 2006. A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect molecular biology, 15, 615–636.
  • Codling, G., et al., 2016. Neonicotinoid insecticides in pollen, honey and adult bees in colonies of the European honey bee (Apis mellifera L.) in Egypt. Ecotoxicology, 27 (2), 122–131.
  • Codling, G., et al., 2016. Concentrations of neonicotinoid insecticides in honey, pollen and honey bees (Apis mellifera L.) in central Saskatchewan, Canada. Chemosphere, 144, 2321–2328.
  • Coulon, M., et al., 2019. Influence of chronic exposure to thiamethoxam and chronic bee paralysis virus on winter honey bees. PLoS One, e0220703. doi:10.1371/journal.pone.0220703
  • Cutler, C.D.S., et al., 2014. A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success. Peer J, 2, e652.
  • Decourtye, A. and Devillers, J., 2010. Ecotoxicity of neonicotinoid insecticides to bees. In: S.H. Thany, ed. Insect nicotinic acetylcholine receptors. New York, NY: Springer, 85–95.
  • Dicks, L., 2013. Bees, lies and evidence-based policy. Nature, 494, 283.
  • Dively, G.P. and Kamel, A., 2012. Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. Journal of agricultural and food chemistry, 60, 4449–4456.
  • El Hassani, A.K., et al., 2008. Effects of sublethal doses of acetamiprid and thiamethoxam on the behavior of the honeybee (Apis mellifera). Archives of environmental contamination and toxicology, 54, 653–661.
  • El-Hady, E.A., El-Sharkawy, H.M., and Sanad, R.E., 2019. Evaluates the possible risk of pollen grains contamination by pesticide residues and their affects on honey bee survival. Journal of productivity and development, 24 (4), 869–883.
  • Evans, J.D., et al., 2006. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect molecular biology, 15 (5), 645–656.
  • FAO. 2021. FAO Specifications and evaluations for agricultural pesticides ‘Thiamethoxam’. Available from: http://www.fao.org/3/ca9665en/ca9665en.pdf/ [Accessed 13 July 2021].
  • Faucon, J.P., et al., 2002. Honey bee winter mortality in France in 1999 and 2000. Bee world, 83, 14–23.
  • Friol, P.S., et al., 2017. Can the exposure of Apis mellifera (Hymenoptera, Apiadae) larvae to a field concentration of thiamethoxam affect newly emerged bees? Chemosphere, 185, 56–66.
  • Gajger, I.T., Sakac, M., and Gregorc, A., 2017. Impact of thiamethoxam on honey bee queen (Apis mellifera carnica) reproductive morphology and physiology. Bulletin of environmental contamination and toxicology, 99 (3), 297–302.
  • Girolami, V., et al., 2011. Fatal powdering of bees in flight with particulates of neonicotinoids seed coating and humidity implication. Journal of applied entomology, 136 (1–2), 17–26.
  • Gregorc, A., et al., 2016. Effects of Nosema ceranae and thiametoxam in Apis mellifera: A comparative study in Africanized and Carniolan honey bees. Chemosphere, 147, 328–336.
  • Gross, M., 2013. EU ban puts spotlight on complex effects of neonicotinoids. Current biology, 23, 462–464.
  • Hardstone, M.C. and Scott, J.G., 2010. Is Apis mellifera more sensitive to insecticides than other insects? Pest management science, 66 (11), 1171–1180.
  • Hashimoto, J.H., Ruvolo-Takasusuki, M.C.C., and Arnaut de Toledo, V.A., 2003. Evaluation of the use of the inhibition esterases activity on Apis mellifera as bioindicators of insecticide thiamethoxam pesticide residue. Sociobiology, 42 (3), 693–699.
  • Henry, M., et al., 2012. A common pesticide decreases foraging success and survival in honey bees. Science, 336 (6079), 348–350.
  • Henry, M., et al., 2015. Reconciling laboratory and field assessments of neonicotinoid toxicity to honey bees. Proceedings of the royal society on biological sciences, 282, 20152110.
  • Hernando, M.D., et al., 2018. Viability of honeybee colonies exposed to sunflowers grown from seeds treated with the neonicotinoids thiamethoxam and clothianidin. Chemosphere, 202, 609–617.
  • Hu, S., et al., 2008. Early steps of angiosperm pollinator coevolution. Proceedings of the national academy of sciences of the United States of America, 105 (1), 240–245.
  • IPBES. 2016. The assessment report of the intergovernmental science policy platform on biodiversity and ecosystem services on pollinators, pollination and food production. In: S.G. Potts, V. L. Imperatriz-Fonseca, and H. T. Ngo, eds. Secretariat of the intergovernmental science-policy platform on biodiversity and ecosystem services. Bonn, 552.
  • Ishaaya, I., et al., 2007. Insecticides with novel modes of action: mechanism, selectivity and cross‐resistance. Entomological research, 37 (3), 148–152.
  • Iwasa, T., et al., 2004. Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop protection, 23, 371–378.
  • Jeschke, P., et al., 2011. Overview of the status and global strategy for neonicotinoids. Journal of agricultural and food chemistry, 59, 2897–2908.
  • Klein, A., et al., 2007. Importance of pollinators in changing landscapes for world crops. Proceedings: biological sciences, 274, 303–313.
  • Krupke, C.H., et al., 2012. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS One, 7, e0029268.
  • Kuwabara, M., 1957. Bildung des bedingten reflexes von Pavlovstypusbei der honigbiene, Apis mellifica. Journal of the faculty of science, Hokkaido university, series VI zoology, 13, 458.
  • Laurino, D., et al., 2011. Toxicity of neonicotinoid insecticides to honey bees: laboratory tests. Bulletin of insectology, 64 (1), 107–113.
  • Lautenbach, S., et al., 2012. Spatial and temporal trends of global pollination benefit. PLoS One, 7 (4), e35954.
  • Marzaro, M., et al., 2011. Lethal aerial powdering of honey bees with neonicotinoids from fragments of maize seed coat. Bulletin of insectology, 64, 119–126.
  • Menail, A. H., et al., 2014., Negative sub-lethal effect of the insecticide thiamethoxam on honey bees. In: P.A. Oomen and J. Pistorius, eds. Hazards of pesticides to bees: 12th international symposium of the ICP-PR bee protection group, 15–17 September 2014, Ghent, Belgium, 151.
  • Mulati, P., et al., 2018. Evaluation of neonicotinoid residues in hive products from selected counties in Kenya. Journal of environmental and analytical toxicology, 8, 577.
  • Nauen, R., et al., 2003. Thiamethoxam is a neonicotinoid precursor converted to clothianidin in insects and plants. Pesticide biochemistry and physiology, 76, 55–69.
  • Nelson, C.M., et al., 2007. The gene vitellogenin has multiple coordinating effects on social organization. PLoS biology, 5, 3.
  • NPIC. 2021. DDT (technical fact sheet). Available from: http://npic.orst.edu/ [Accessed 7 July 2021].
  • Oliveira, R.A., et al., 2013. Side-effects of thiamethoxam on the brain and midgut of the Africanized honeybee Apis mellifera (Hymenopptera: Apidae). Environmental toxicology, 29, 1122–1133.
  • Olivier, S.R., et al., 2017. Planting of neonicotinoid-coated corn raises honey bee mortality and sets back colony development. PeerJ, 5, e3670.
  • Ollerton, J., Winfree, R., and Tarrant, S., 2011. How many flowering plants are pollinated by animals? Oikos, 120, 321–326.
  • Olotu, M.I., and Gujar, G.T., 2016. Many-fold less than the field recommended concentrations of neonicotinoids and malathion affect foraging of honey bee in three important crops in India. Entomon, 41 (1), 47–60.
  • Overmyer, J., et al., 2017. Thiamethoxam honey bee colony feeding study: linking effects at the level of the individual to those at the colony level. Environmental toxicology and chemistry, 9999, 1–13.
  • Papach, A., et al., 2017. Larval exposure to thiamethoxam and American foulbrood: effects on mortality and cognition in the honey bee Apis mellifera. Journal of apicultural research, 56 (4), 475–486.
  • Pelosi, P., et al., 2006. Soluble proteins in insect chemical communication. Cellular and molecular life sciences, 63, 1658–1676.
  • Pervez, M. and Manzoor, F., 2020. Analysis of pesticide residues in pollen and nectar samples from various agricultural areas of Pakistan through high performance liquid chromatography. Sarhad journal of agriculture, 36 (1), 1–9.
  • Pilling, E., et al., 2013. A four-year field program investigating long-term effects of repeated exposure of honey bee colonies to flowering crops treated with thiamethoxam. PLoS One, 8 (10), e0077193.
  • Pohorecka, K., et al., 2013. Effects of exposure of honey bee colonies to neonicotinoid seed–treated maize crops. Journal of apicultural sciences, 57 (2), 199–208.
  • Poquet, Y., et al., 2015. Wings as a new route of exposure to pesticides in the honey bee. Environmental toxicology and chemistry, 34 (9), 1983–1988.
  • Potts, S., et al., 2006. Plant-pollinator biodiversity and pollination services in a complex Mediterranean landscape. Biological conservation, 129, 519–529.
  • Renzi, M.T., et al., 2016. Combined effect of pollen quality and thiamethoxam on hypopharyngeal gland development and protein content in Apis mellifera. Apidologie, 47, 779–788.
  • Rundlof, M., et al., 2015. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature, 521, 77–93.
  • Sanchez-Gracia, A., Vieira, F.G., and Rozas, J., 2009. Molecular evolution of the major chemosensory gene families in insects. Heredity, 103, 208–216.
  • Sandrock, C., et al., 2014. Impact of chronic neonicotinoid exposure on honey bee colony performance and queen supersedure. PLoS One, 9, e0103592.
  • Seehuus, S.C., et al., 2006. Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proceedings of the national academy of sciences of the United States of America, 103, 962–967.
  • Senn, R., et al., 1998., CGA 293’343: a novel broad-spectrum insecticide supporting sustainable agriculture worldwide. Brighton Crop Protection Conference, Pests and Diseases, Vol. 1, Brighton, UK, 27–36.
  • Shi, T.F., et al., 2017. Sublethal effects of the neonicotinoid insecticide thiamethoxam on the transcriptome of the honeybee (Apis mellifera). bioRxiv.
  • Stewart, S.D., et al., 2014. Potential exposure of pollinators to neonicotinoid insecticides from the use of insecticide seed treatments in the mid-southern United States. Environmental science and technology, 48, 9762–9769.
  • Straub, L., et al., 2016. Neonicotinoid insecticides can serve as inadvertent insect contraceptives. Proceedings of the royal society on biological sciences, 283, 20160506. doi: 10.1098/rspb,2016.0506.
  • Svensson, B., 2003. Silent spring in northern Europe? Available from: http://www.beekeeping.com/intoxications/silent_spring.htm/ [Accessed 22 January 2017].
  • Tavares, D.A., et al., 2015. In vitro effects of thiamethoxam on larvae of Africanized honey bee Apis mellifera (Hymenoptera: Apidae). Chemosphere, 135, 370–378.
  • Tesovnik, T., et al., 2020. Exposure of honey bee larvae to thiamethoxam and its interaction with Nosema ceranae infection in adult honey bees. Environmental pollution, 256, 113443. doi: 10.1016/j.envpol.2019.113443
  • Thompson, H., et al., 2016. Thiamethoxam: assessing flight activity of honeybees foraging on treated oilseed rape using radio frequency identification technology. Environmental toxicology and chemistry, 35 (2), 385–393.
  • Tosi, S. and Nieh, J.C., 2017. A common neonicotinoid pesticide, thiamethoxam, alters honey bee activity, motor functions, and movement to light. Scientific reports, 7, 15132. doi: 10.1038/s41598-017-15308-6
  • Tosi, S., Burgio, G., and Nieh, J.C., 2017. A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability. Scientific reports, 7, 1201.
  • Tosi, S., et al., 2016. Effects of a neonicotinoid pesticide on thermoregulation of African honey bees (Apis mellifera scutellata). Journal of insect physiology, 93–94, 56–63.
  • Tsvetkov, N., et al., 2017. Chronic exposure to neonicotinoids reduces honey bee health near corn crops. Science, 356, 1395–1397.
  • Underwood, R. M. and vanEngelsdorp, D., 2020. Colony collapse disorder: have we seen this before? The Pennsylvania State University, Department of Entomology. Available from: https://ento.psu.edu/pollinators/publications/ [Accessed 21 June 2020].
  • Van der Sluijs, J.P., et al., 2013. Neonicotinoids, bee disorders and the sustainability of pollinator services. Current opinion in environmental sustainability, 5, 1–13.
  • Williams, G.R., et al., 2015. Neonicotinoid pesticides severely affect honey bee queens. Scientific reports, 5, 14621. doi: 10.1038/srep14621.
  • Williamson, S.M., Willis, S.J., and Wright, G.A., 2014. Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology, 23 (8), 1409–1418.
  • Wright, G.A., Softley, S., and Earnshaw, H., 2015. Low doses of neonicotinoid pesticides in food rewards impair short-term olfactory memory in foraging-age honey bees. Scientific reports, 5, 15322. doi: 10.1038/srep15322.
  • Xu, T., et al., 2016. Clothianidin in agricultural soils and uptake into corn pollen and canola nectar after multiyear seed treatment applications. Environmental toxicology and chemistry, 35 (2), 311–321.

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