Adverse Effects of Commonly Used Acaricides on the Reproductive Physiology of Drone Honeybees (Apis mellifera L.)

Year 2025, Volume: 6 Issue: 4, 246 - 252, 30.12.2025

Yaşar Erdoğan

https://doi.org/10.56430/japro.1790717

Abstract

This study evaluated the adverse effects of three widely used commercial acaricides (amitraz, flumethrin, and formic acid) on the reproductive physiology and quality parameters of drones (Apis mellifera caucasica), commonly used for the control of the destructive pest, Varroa destructor. The experiment was conducted on 20 colonies at the Bayburt University Beekeeping Application and Research Station during the spring-summer of 2025. The acaricides were applied to different experimental groups shortly before the drone cells were capped. Key reproductive quality parameters including body weight, sexual maturity rate, sperm viability, sperm concentration, and semen volume were assessed. The results showed that all three acaricide applications had statistically significant negative effects (p<0.05) on all measured reproductive parameters. Notably, the amitraz and formic acid treatments caused the most significant decreases in sperm viability and sperm concentration. Furthermore, compared to the control group, significant reductions were observed in both sexual maturity rates and drone body weights. The amitraz treatment group, in particular, exhibited the lowest sperm concentration (0.90±0.04×106/μL), a finding that aligns with the most substantial decrease in body weight (52.24 mg lower than the control). These findings clearly demonstrate that the common acaricidal compounds used against Varroa mites pose potential physiological and reproductive risks to drone. This highlights a critical concern for sustainable beekeeping, especially in queen bee rearing programs, and underscores the need for careful consideration of treatment methods and timing.

Keywords

Acaricide toxicity , Amitraz , Formic acid , Honey bee , Sperm viability , Varroa destructor

Ethical Statement

This study does not require ethical committee approval.

References

• Abdelkader, F. B. (2019). Impact of pesticides on honeybee (Apis mellifera L.) drones. Uludag Bee Journal, 19(2), 188-194. https://doi.org/10.31467/uluaricilik.626929
• Abdelkader, F. B., Çakmak, İ., Çakmak, S. S., Nur, Z., İncebıyık, E., Aktar, A., & Erdost, H. (2021). Toxicity assessment of chronic exposure to common insecticides and bee medications on colony development and drones sperm parameters. Ecotoxicology, 30, 806-817. https://doi.org/10.1007/s10646-021-02416-3
• Abrol, D. P. (2011). Honeybee and crop pollination. In D. P. Abrol (Ed.), Pollination biology: Biodiversity Conservation and Agricultural Production (pp. 85-110). Springer. https://doi.org/10.1007/978-94-007-1942-2_5
• Almecija, G., Poirot, B., Cochard, P., & Suppo, C. (2020). Inventory of Varroa destructor susceptibility to amitraz and tau-fluvalinate in France. Experimental Applied Acarology, 82, 1-16. https://doi.org/10.1007/s10493-020-00535-w
• Al-Waili, N., Salom, K., Al-Ghamdi, A., & Ansari, M. J. (2012). Antibiotic, pesticide, and microbial contaminants of honey: human health hazards. The Scientific World Journal, 2012(1), 930849. https://doi.org/10.1100/2012/930849
• Anderson, D. L., & Trueman, J. W. H. (2000). Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental Applied Acarology, 24, 165-189. https://doi.org/10.1023/A:1006456720416
• Aufauvre, J., Biron, D. G., Vidau, C., Fontbonne, R., Roudel, M., Diogon, M., Viguès, B., Belzunces, L. P., Delbac, F., & Blot, N. (2012). Parasite-insecticide interactions: A case study of Nosema ceranae and fipronil synergy on honeybee. Scientific Reports, 2, 326. https://doi.org/10.1038/srep00326
• Bevk, D., Kralj, J., & Čokl, A. (2012). Coumaphos affects food transfer between workers of honeybee Apis mellifera. Apidologie, 43, 465-470. https://doi.org/10.1007/s13592-011-0113-x
• Bieńkowska, M., Panasiuk, B., Węgrzynowicz, P., & Gerula, D. (2011). The effect of different thermal conditions on drone semen quality and number of spermatozoa entering the spermatheca of queen bee. Journal of Apicultural Science, 55(2), 161-168.
• Brandorf, A., Shestakova, A., Larkina, E., & Lapynina, E. (2023). Effect of acaricide treatment on body weight and reproductive characteristics of drones of the Prioksky breed type of Central Russian honeybees (Apis mellifera Linnaeus, 1758). Sel’skokhozyaistvennaya Biologiya, 58(2), 345-354. https://doi.org/10.15389/agrobiology.2023.2.345eng
• Burley, L. M. (2007). The effects of miticides on the reproductive physiology of honey bee (Apis mellifera L.) queens and drones (Doctoral dissertation, Virginia Tech).
• Burley, L. M., Fell, R. D., & Saacke, R. G. (2008). Survival of honey bee (Hymenoptera: Apidae) spermatozoa incubated at room temperature from drones exposed to miticides. Journal of Economic Entomology, 101(4), 1081-1087. https://doi.org/10.1093/jee/101.4.1081
• Chaimanee, V., Evans, J. D., Chen, Y., Jackson, C., & Pettis, J. S. (2016). Sperm viability and gene expression in honey bee queens (Apis mellifera) following exposure to the neonicotinoid insecticide imidacloprid and the organophosphate acaricide coumaphos. Journal of İnsect Physiology, 89, 1-8. https://doi.org/10.1016/j.jinsphys.2016.03.004
• Ciereszko, A., Wilde, J., Dietrich, G. J., Siuda, M., Bąk, B., Judycka, S., & Karol, H. (2017). Sperm parameters of honeybee drones exposed to imidacloprid. Apidologie, 48, 211-222. https://doi.org/10.1007/s13592-016-0466-2
• Clermont, A., Eickermann, M., Kraus, F., Georges, C., Hoffmann, L., & Beyer, M. (2014). A survey on some factors potentially affecting losses of managed honey bee colonies in Luxembourg over the winters 2010/2011 and 2011/2012. Journal of Apicultural Research, 53(1), 43-56. https://doi.org/10.3896/IBRA.1.53.1.04
• Cobey, S. (1983). Drone rearing for instrumental insemination. III.[Honeybees]. American Bee Journal, 123, 284-289.
• Duncan, D. B. (1955). Multiple range and multiple F tests. Biometrics, 11(1), 1-42. https://doi.org/10.2307/3001478
• Evans, J. D., & Schwarz, R. S. (2011). Bees brought to their knees: Microbes affecting honey bee health. Trends in Microbiology, 19(12), 614-620.
• Fell, R., & Tignor, K. (2001). Miticide effects on the reproductive physiology of queens and drones. American Bee Journal, 141(12), 888-889.
• Glenny, W., Cavigli, I., Daughenbaugh, K. F., Radford, R., Kegley, S. E., & Flenniken, M. L. (2017). Honey bee (Apis mellifera) colony health and pathogen composition in migratory beekeeping operations involved in California almond pollination. PLoS One, 12(8), e0182814. https://doi.org/10.1371/journal.pone.0182814
• Guzman, L. D., Rinderer, T. E., Lancaster, V. A., Delatte, G. T., & Stelzer, A. (1999). Varroa in the mating yard: III. The effects of formic acid gel formulation on drone production. American Bee Journal, 139(4), 304-307.
• Harbo, J. (1985). Instrumental insemination of queen bees-1985. 1. American Bee Journal, 125(3), 197-202.
• Ilyasov, R., Lim, S., Lee, M. L., Kwon, H. W., & Nikolenko, A. (2021). Effect of miticides amitraz and fluvalinate on reproduction and productivity of honey bee Apis mellifera. Uludag Bee Journal, 21(1), 21-30. https://doi.org/10.31467/uluaricilik.883775
• Johnson, R. M., Dahlgren, L., Siegfried, B. D., & Ellis, M. D. (2013). Effect of in-hive miticides on drone honey bee survival and sperm viability. Journal of Apicultural Research, 52(2), 88-95. https://doi.org/10.3896/IBRA.1.52.2.18
• Kaftanoglu, O., & Peng, Y.-S. (1984). Preservation of honeybee spermatozoa in liquid nitrogen. Journal of Apicultural Research, 23(3), 157-163. https://doi.org/10.1080/00218839.1984.11100625
• Kairo, G., Poquet, Y., Haji, H., Tchamitchian, S., Cousin, M., Bonnet, M., Pelissier, M., Kretzschmar, A., Belzunces, L. P., & Brunet, J. L. (2017). Assessment of the toxic effect of pesticides on honey bee drone fertility using laboratory and semifield approaches: A case study of fipronil. Environmental Toxicology Chemistry, 36(9), 2345-2351. https://doi.org/10.1002/etc.3773
• Messan, K., Messan, M. R., Chen, J., DeGrandi-Hoffman, G., & Kang, Y. (2021). Population dynamics of Varroa mite and honeybee: Effects of parasitism with age structure and seasonality. Ecological Modelling, 440, 109359. https://doi.org/10.1016/j.ecolmodel.2020.109359
• Metz, B. N., & Tarpy, D. R. (2019). Reproductive senescence in drones of the honey bee (Apis mellifera). Insects, 10(1), 11. https://doi.org/10.3390/insects10010011
• Rangel, J., & Fisher, A. (2019). Factors affecting the reproductive health of honey bee (Apis mellifera) drones—A review. Apidologie, 50, 759-778. https://doi.org/10.1007/s13592-019-00684-x
• Rhodes, J. W., Harden, S., Spooner-Hart, R., Anderson, D. L., & Wheen, G. (2011). Effects of age, season and genetics on semen and sperm production in Apis mellifera drones. Apidologie, 42, 29-38. https://doi.org/10.1051/apido/2010026
• Rinderer, T. E., Guzman, L. D., Lancaster, V. A., Delatte, G. T., & Stelzer, J. A. (1999). Varroa in the mating yard: I. The effects of Varroa jacobsoni and Apistan® on drone honey bees. American Bee Journal, 139(2), 134-139.
• Rosenkranz, P., Aumeier, P., & Ziegelmann, B. (2010). Biology and control of Varroa destructor. Journal of Invertebrate Pathology, 103(Supplement), S96-S119. https://doi.org/10.1016/j.jip.2009.07.016
• Sammataro, D. (2011). Global status of honey bee mites. In D. Sammataro & J. A. Yoder (Eds.), Honey bee colony health (pp. 37-54). CRC Press. https://doi.org/10.1201/b11318
• Shoukry, R. S., Khattaby, A., El-Sheakh, A., Abo-Ghalia, A., & Elbanna, S. M. (2013). Effect of some materials for controlling varroa mite on the honeybee drones (Apis mellifera L.). Egyptian Journal of Agricultural Research, 91(3), 825-834. https://doi.org/10.21608/ejar.2013.165098
• Smodiš Škerl, M. I., Kmecl, V., & Gregorc, A. (2010). Exposure to pesticides at sublethal level and their distribution within a honey bee (Apis mellifera) colony. Bulletin of Environmental Contamination Toxicology, 85, 125-128. https://doi.org/10.1007/s00128-010-0069-y
• Soroker, V., Hetzroni, A., Yakobson, B., David, D., David, A., Voet, H., Slabezki, Y., Efrat, H., Levski, S., Kamer, Y., Klinberg, E., Zioni, N., Inbar, S., & Kamer, Y. (2011). Evaluation of colony losses in Israel in relation to the incidence of pathogens and pests. Apidologie, 42, 192-199. https://doi.org/10.1051/apido/2010047
• Tihelka, E. (2018). Effects of synthetic and organic acaricides on honey bee health: A review. Slovenian Veterinary Research, 55(2), 119-40. https://doi.org/10.26873/SVR-422-2017
• Wakonigg, G., Eveleigh, L., Arnold, G., & Crailsheim, K. (2000). Cuticular hydrocarbon profiles reveal age-related changes in honey bee drones (Apis mellifera carnica). Journal of Apicultural Research, 39(3-4), 137-141. https://doi.org/10.1080/00218839.2000.11101033