Abstract
Impacts to honey bees due to exposure to agricultural pesticides is one of the most serious threats to the beekeeping industry. Our research evaluated toxicity of the formulated insecticides Lufenuron+Emamectin benzoate (Proclaim Fit®) on the European honey bee Apis mellifera L. at field-realistic concentration (worst-case scenario). Newly emerged (≤24-h old) and forager (unknown age) worker bees were treated with the field recommended concentration of Proclaim Fit® using three routes of exposure including residual contact, oral, and spray within the laboratory. We also assessed the effects of Proclaim Fit® on the specific activity of some well-known detoxifying enzymes including α-esterase, β-esterase, and Glutathione S-transferase (GST) in the honey bees. In addition, toxicity of the formulation was tested on 4th instar larvae within the hive. Based on estimated median survival times (MSTs), Proclaim Fit® was highly toxic to the bees, especially when applied as spray. According to our estimated relative median potency (RMP) values, newly emerged bees were 1.72× more susceptible than foragers to Proclaim Fit® applied orally. Enzyme assays revealed the considerable involvement of the enzymes, especially GST and α-esterase, in detoxification of the Proclaim Fit®, but their activities were significantly influenced by route of exposure and age of bee. Notably, Proclaim Fit® was highly toxic to 4th instar honey bee larvae. Our results generally indicate a potent toxicity of Proclaim Fit® toward honey bees. Therefore, its application requires serious consideration and adherence to strict guidelines, especially during the flowering time of crops.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Badawy MEI, Nasr HM, Rabea EI (2015) Toxicity and biochemical changes in the honey bee Apis mellifera exposed to four insecticides under laboratory conditions. Apidologie 46:177–193. https://doi.org/10.1007/s13592-014-0315-0
Berenbaum MR, Johnson RM (2015) Xenobiotic detoxification pathways in honey bees. Curr Opin Insect Sci 10:51–58. https://doi.org/10.1016/j.cois.2015.03.005
Bispo dos Santos SA, Roselino AC, Hrncir M, Bego LR (2009) Pollination of tomatoes by the stingless bee Melipona quadrifasciata and the honey bee Apis mellifera (Hymenoptera, Apidae). Genet Mol Res 8:751–757. https://doi.org/10.4238/vol8-2kerr015
Boncristiani H, Ellis JD, Bustamante T, Graham J, Jack C, Kimmel CB, Mortensen A, Schmehl DR (2021) World honey bee health: the global distribution of western honey bee (Apis mellifera L.) pests and pathogens. Bee World 98:2–6. https://doi.org/10.1080/0005772X.2020.1800330
Dahan-Moss YL, Koekemoer LL (2016) Analysis of esterase enzyme activity in adults of the major malaria vector Anopheles funestus. Parasit Vectors 9:110. https://doi.org/10.1186/s13071-016-1379-7
Dai P, Jack CJ, Mortensen AN, Bustamante TA, Bloomquist JR, Ellis JD (2019) Chronic toxicity of clothianidin, imidacloprid, chlorpyrifos, and dimethoate to Apis mellifera L. larvae reared in vitro. Pest Manag Sci 75:29–36. https://doi.org/10.1002/ps.5124
Desneux N, Decourtye A, Delpuech JM (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
du Rand EE, Smit S, Beukes M, Apostolides Z, Pirk CWW, Nicolson SW (2015) Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine. Sci Rep 5:11779. https://doi.org/10.1038/srep11779
Estabrook RW(2003) A passion for P450s (remembrances of the earlyhistory of research on cytochrome P450). Drug Metab Dispos 31:1461–1473. https://doi.org/10.1124/dmd.31.12.1461
Finney, DJ (1971) Probit analysis. 3th ed. 333 pp. Cambridge University, London. https://doi.org/10.1002/jps.2600600940
Gashout HA, Guzmán-Novoa E (2009) Acute toxicity of essential oils and other natural compounds to the parasitic mite, Varroa destructor, and to larval and adult worker honey bees (Apis mellifera L.). J Apic Res 48:263–269. https://doi.org/10.3896/IBRA.1.48.4.06
Gong Y, Diao Q (2017) Current knowledge of detoxification mechanisms of xenobiotic in honey bees. Ecotoxicol 26:1–12. https://doi.org/10.1007/s10646-016-1742-7
Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Sci 347:1255957. https://doi.org/10.1126/science.1255957
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S- transferase, the first step in mercapturic acid formation. J Biol Chem 249:7130–7139. https://doi.org/10.1016/S0021-9258(19)42083-8
Han W, Wang Y, Gao J, Wang S, Zhao S, Liu J, Zhong Y, Zhao D (2018) Acute toxicity and sublethal effects of myclobutanil on respiration, flight and detoxification enzymes in Apis cerana cerana. Pestic Biochem Physiol 147:133–138. https://doi.org/10.1016/j.pestbp.2017.11.001
Han W, Yang Y, Gao J, Zhao D, Ren C, Wang S, Zhao S, Zhong Y (2019) Chronic toxicity and biochemical response of Apis cerana cerana (Hymenoptera: Apidae) exposed to acetamiprid and propiconazole alone or combined. Ecotoxicol 28:399–411. https://doi.org/10.1007/s10646-019-02030-4
Human H, Brodschneider R, Dietemann V, Dively G, Ellis JD, Forsgren E, Fries I, Hatjina F, Hu FL, Jaffé R, Jensen AB, Köhler A, Magyar JP, Özkýrým A, Pirk CWW, Rose R, Strauss U, Tanner G, Tarpy DR, van der Steen JJM, Vaudo A, Vejsnæs F, Wilde J, Williams GR, Zheng HQ (2013) Miscellaneous standard methods for Apis mellifera research. J Apic Res 52:1–53. https://doi.org/10.3896/IBRA.1.52.4.10
Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–253. https://doi.org/10.1146/annurev.ento.51.110104.151104
Mullin CA, Fine JD, Reynolds RD, Frazier MT (2016) Toxicological risks of agrochemical spray adjuvants: Organosilicone surfactants may not be safe. Front Public Health 4:92. https://doi.org/10.3389/fpubh.2016.00092
Naghizadeh M, Taher MA, Tamaddon AM (2019) Facile synthesis and characterization of magnetic nanocomposite ZnO/CoFe2O4 hetero-structure for rapid photocatalytic degradation of imidacloprid. Heliyon 5:e02870. https://doi.org/10.1016/j.heliyon.2019.e02870
Ricke DF, Lin CH, Johnson RM (2021) Pollen treated with a combination of agrochemicals commonly applied during almond bloom reduces the emergence rate and longevity of honey bee (Hymenoptera: Apidae) queens. J Insect Sci 21:5. https://doi.org/10.1093/jisesa/ieab074
Rinkevich FD, Margotta JW, Pittman JM, Danka RG, Tarver MR, Ottea JA, Healy KB (2015) Genetics, synergists, and age affect insecticide sensitivity of the honey bee, Apis mellifera. PLoS ONE 10:e0139841. https://doi.org/10.1371/journal.pone.0139841
Sanchez-Bayo F, Goulson D, Pennacchio F, Nazzl F, Goka K, Desneux N (2016) Are bee diseases linked to pesticides? A brief review. Environ Int 89-90:7–11. https://doi.org/10.1016/j.envint.2016.01.009
Singla A, Barmota H, Sahoo SK, Kang BK (2021) Influence of neonicotinoids on pollinators: A review. J Apic Res 60:19–32. https://doi.org/10.1080/00218839.2020.1825044
Van Asperen E (1962) A study of housefly esterase by mean of a sensitive colorimetric method. J Insect Physiol 8:401–416. https://doi.org/10.1016/0022-1910(62)90074-4
Xu JH, Strange JP, Welker DL, James RR (2013) Detoxification and stress response genes expressed in a western North American bumble bee, Bombus huntii (Hymenoptera: Apidae). BMC Genom 14:874. https://doi.org/10.1186/1471-2164-14-874
Zhu W, Schmehl DR, Mullin CA, Frazier JL (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
Zhu YC, Caren J, Reddy GVP, Li W, Yao J (2020) Effect of age on insecticide susceptibility and enzymatic activities of three detoxification enzymes and one invertase in honey bee workers (Apis mellifera). Comp Biochem Physiol Part C: Toxicol Pharmacol 238:108844. https://doi.org/10.1016/j.cbpc.2020.108844
Acknowledgements
We gratefully acknowledge anonymous reviewers for their valuable comments and suggestions.
Author contributions
The authors contributed equally to this work.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ghasemi, V., Salehinejad, A., Ghadamyari, M. et al. Toxic evaluation of Proclaim Fit® on adult and larval worker honey bees. Ecotoxicology 31, 1441–1449 (2022). https://doi.org/10.1007/s10646-022-02601-y
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-022-02601-y