The novel pesticide flupyradifurone (Sivanto) affects honeybee motor abilities
Honeybees and other pollinators are threatened by changing landscapes and pesticides resulting from intensified agriculture. In 2018 the European Union prohibited the outdoor use of three neonicotinoid insecticides due to concerns about pollinators. A new pesticide by the name of “Sivanto” was recently released by Bayer AG. Its active ingredient flupyradifurone binds to the nicotinic acetylcholine receptor (AchR) in the honeybee brain, similar to neonicotinoids. Nevertheless, flupyradifurone is assumed to be harmless for honeybees and can even be applied on flowering crops. So far, only little has been known about sublethal effects of flupyradifurone on honeybees. Intact motor functions are decisive for numerous behaviors including foraging and dancing. We therefore selected a motor assay to investigate in how far sublethal doses of this pesticide affect behavior in young summer and long-lived winter honeybees. Our results demonstrate that flupyradifurone (830 µmol/l) can evoke motor disabilities and disturb normal motor behavior after a single oral administration (1.2 µg/bee). These effects are stronger in long-lived winter bees than in young summer bees. After offering an equal amount of pesticide (1.0–1.75 µg) continuously over 24 h with food the observed effects are slighter. For comparisons we repeated our experiments with the neonicotinoid imidacloprid. Intriguingly, the alterations in behavior induced by this pesticide (4 ng/bee) were different and longer-lasting compared to flupyradifurone, even though both substances bind to nicotinic acetylcholine receptors.
KeywordsHoneybee Motor ability Acetylcholine receptor Insecticide Flupyradifurone Imidacloprid
We thank our departmental beekeeper Dirk Ahrens for beekeeping. We thank Laura Degirmenci for help with the manuscript.
We thank the Heinrich Stockmeyer Stiftung, Bad Rothenfelde, for financial support to HH.
HH gained data. Both authors wrote the main manuscript text and HH prepared all of the figures. Both authors reviewed the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Bicker G (1999) Histochemistry of classical neurotransmitters in antennal lobes and mushroom bodies of the honeybee. Microsc Res Tech 45:174–183. https://doi.org/10.1002/(SICI)1097-0029(19990501)45:3<174:AID-JEMT5>3.3.CO;2-L CrossRefGoogle Scholar
- Butler CG (1945) The influence of various physical and biological factors of the environment on honeybee activity. An examination of the relationship between activity and nectar concentration and abundance. J Experiment Biol 21:5–12Google Scholar
- Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440 CrossRefGoogle Scholar
- EFSA (2015) Conclusion on the peer review of the pesticide risk assessment of the active substance flupyradifurone. EFS2 13:4020. https://doi.org/10.2903/j.efsa.2015.4020
- European Commission (2018a) Commission ImplementingRegulation (EU) 2018/783 of 29 May 2018 amending Implementing Regulation (EU) No 540/2011 as regards the conditions of approval of the active substance imidacloprid. Off J Eur Union 132:31–34. Accessed 21 Aug 2018Google Scholar
- European Commission (2018b) Commission ImplementingRegulation (EU) 2018/784 of 29 May 2018 amending Implementing Regulation (EU) No 540/2011 as regards the conditions of approval of the active substance clothianidin:L 132/35-39. Accessed 21 Aug 2018Google Scholar
- European Commission (2018c) Commission ImplementingRegulation (EU) 2018/785 of 29 May 2018 amending Implementing Regulation (EU) No 540/2011 as regards the conditions of approval of the active substance thiamethoxam. Off J Eur Union 132:40–44. Accessed 21 Aug 2018Google Scholar
- Glaberman S, White K (2014) Environmental fate and ecological risk assessment for foliar, soil drench, and seed treatment uses of the new insecticide flupyradifurone (BYI02960). U.S. Environmental Protection Agency Office of Pesticide Programs, Environmental Fate and Effects Division EFED, Environmental Risk Branch IV 187Google Scholar
- Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H, Stenmans W, Müller A, Sumser H, Hörren T, Goulson D, Kroon Hde (2017) 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 CrossRefGoogle Scholar
- Lee D, O’Dowd DK (1999) Fast excitatory synaptic transmission mediated by nicotinic acetylcholine receptors in Drosophila neurons. J Neurosci 19:5311–5321. https://doi.org/10.1523/JNEUROSCI.19-13-05311.1999 CrossRefGoogle Scholar
- Nation JL (2008) Insect physiology and biochemistry, 2nd edn. CRC Press, HobokenGoogle Scholar
- Smirle MJ (1993) The influence of colony population and brood rearing intensity on the activity of detoxifying enzymes in worker honey bees. Physiol Entomol 18:420–424. https://doi.org/10.1111/j.1365-3032.1993.tb00616.x CrossRefGoogle Scholar
- Suchail S, Guez D, Belzunces LP (2001) Discrepancy between acute and chronic toxicity induces by imidacloprid and its metabolites in Apis mellifera. Environ Toxicol Chem 20:2482. https://doi.org/10.1897/1551-5028(2001)020<2482:DBAACT>2.0.CO;2 CrossRefGoogle Scholar
- Winston ML (1987) Biology of the honey bee, New edn. Harvard University Press, CambridgeGoogle Scholar