Skip to main content
SpringerLink
Log in

The sublethal effects of ethiprole on the development, defense mechanisms, and immune pathways of honeybees (Apis mellifera L.)

  • Original Paper
  • Published:
Environmental Geochemistry and Health Aims and scope Submit manuscript

Abstract

Ethiprole has been widely used in agriculture, but there have been few studies on the adverse effects of ethiprole on nontarget organisms. This study focused on the mechanism of the sublethal effects of ethiprole on the development, antioxidation mechanisms, detoxification mechanisms and immune-related gene expression of honeybees (Apis mellifera L.). Honeybee larvae were found to be more sensitive than pupae to ethiprole. It was found that ethiprole inhibited the pupation and eclosion of bee larvae in a dose-dependent manner, with ethiprole doses of 1 × 10–3 mg/L decreasing pupation and eclosion rates to 50.00 ± 8.84% and 20.83 ± 10.62%, respectively. The activities of antioxidative enzymes (superoxide dismutase and catalase) and detoxification factors (glutathione and glutathione S-transferase) were also significantly increased in ethiprole-exposed honeybees, indicating that a sublethal dose of ethiprole also induced oxidative stress in honeybees. In the 1 × 10–3 mg/L ethiprole-exposure group, the expression of pathogen recognition-related gene PGRP-4300 was upregulated 11.10 ± 0.45-fold, and that of detoxification-related gene CYP4G11 was upregulated 8.84 ± 0.11-fold, indicating that ethiprole induced an immune reaction in honeybees. To the best our knowledge, this study represents the first demonstration that sublethal concentrations of ethiprole inhibit honeybee development and activate honeybee defense and immune systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Apilux, A., Isarankuranaayudhya, C., Tantimongcolwat, T., & Prachayasittikul, V. (2015). Paper-based acetylcholinesterase inhibition assay combining a wet system for organophosphate and carbamate pesticides detection. Excli Journal, 14, 307–319.

    Google Scholar 

  • Arthur, F. H. (2002). Efficacy of ethiprole applied alone and in combination with conventional insecticides for protection of stored wheat and stored corn. Journal of Economic Entomology, 95(6), 1314–1318.

    CAS  Google Scholar 

  • Badiou, A., Meled, M., & Belzunces, L. P. (2008). Honeybee Apis mellifera acetylcholinesterase–a biomarker to detect deltamethrin exposure. Ecotoxicology and Environmental Safety, 69(2), 246–253.

    CAS  Google Scholar 

  • Badioubeneteau, A., Benneveau, A., Geret, F., Delatte, H., Becker, N., Brunet, J., et al. (2013). Honeybee biomarkers as promising tools to monitor environmental quality. Environment International, 60, 31–41.

    CAS  Google Scholar 

  • Berenbaum, M. R., & Johnson, R. M. (2015). Xenobiotic detoxification pathways in honey bees. Current Opinion in Insect Science, 10, 51–58.

    Google Scholar 

  • Boncristiani, H. F., Underwood, R. M., Schwarz, R. S., Evans, J. D., Pettis, J. S., & Vanengelsdorp, D. (2012). Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera. Journal of Insect Physiology, 58(5), 613–620.

    CAS  Google Scholar 

  • Bovi, T. S., Zaluski, R., & Orsi, R. O. (2018). Toxicity and motor changes in Africanized honey bees (Apis mellifera L.) exposed to fipronil and imidacloprid. Anais da Academia Brasileira de Ciências, 90(1), 239–245.

    CAS  Google Scholar 

  • Caboni, P., Sammelson, R. E., & Casida, J. E. (2003). Phenylpyrazole insecticide photochemistry, metabolism, and GABAergic Action: Ethiprole compared with fipronil. Journal of Agricultural and Food Chemistry, 51(24), 7055–7061.

    CAS  Google Scholar 

  • Christen, V., & Fent, K. (2017). Exposure of honey bees (Apis mellifera) to different classes of insecticides exhibit distinct molecular effect patterns at concentrations that mimic environmental contamination. Environmental Pollution, 226, 48–59.

    CAS  Google Scholar 

  • Cizelj, I., Glavan, G., Božic, J., Oven, I., Mrak, V., & Narat, M. (2016). Prochloraz and coumaphos induce different gene expression patterns in three developmental stages of the Carniolan honey bee (Apis mellifera carnica Pollmann). Pesticide Biochemistry and Physiology, 128, 68–75.

    CAS  Google Scholar 

  • Claudianos, C., Ranson, H., Johnson, R. M., Biswas, S., Schuler, M. A., Berenbaum, M. R., et al. (2006). A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Molecular Biology, 15(5), 615–636.

    CAS  Google Scholar 

  • Cole, L. M., Nicholson, R. A., & Casida, J. E. (1993). Action of phenylpyrazole insecticides at the GABA-Gated chloride channel. Pesticide Biochemistry and Physiology, 46(1), 47–54.

    CAS  Google Scholar 

  • Dai, P., Yan, Z., Ma, S., Yang, Y., Wang, Q., Hou, C., et al. (2018). The herbicide glyphosate negatively affects midgut bacterial communities and survival of honey bee during larvae reared in vitro. Journal of Agricultural and Food Chemistry, 66(29), 7786–7793.

    CAS  Google Scholar 

  • Du Rand, E. E., Smit, S., Beukes, M., Apostolides, Z., Pirk, C. W. W., & Nicolson, S. W. (2015). Detoxification mechanisms of honey bees (Apis mellifera) resulting in tolerance of dietary nicotine. Scientific Reports, 5(1), 11779–11779.

    Google Scholar 

  • Evans, J. D., Aronstein, K. A., Chen, Y., Hetru, C., Imler, J., Jiang, H., et al. (2006). Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology, 15(5), 645–656.

    CAS  Google Scholar 

  • Garrood, W. T., Zimmer, C. T., Gorman, K. J., Nauen, R., Bass, C., & Davies, T. G. (2015). Field-evolved resistance to imidacloprid and ethiprole in populations of brown planthopper Nilaparvata lugens collected from across South and East Asia. Pest Management Science, 72(1), 140–149.

    Google Scholar 

  • Hemingway, J., Hawkes, N. J., Mccarroll, L., & Ranson, H. (2004). The molecular basis of insecticide resistance in mosquitoes. Insect Biochemistry and Molecular Biology, 34(7), 653–665.

    CAS  Google Scholar 

  • Johnson, R. M., Ellis, M. D., Mullin, C. A., & Frazier, M. (2010). Pesticides and honey bee toxicity — USA. Apidologie, 41(3), 312–331.

    CAS  Google Scholar 

  • Kathage, J., Castanera, P., Alonsoprados, J. L., Gomezbarbero, M., & Rodriguezcerezo, E. (2018). The impact of restrictions on neonicotinoid and fipronil insecticides on pest management in maize, oilseed rape and sunflower in eight European Union regions. Pest Management Science, 74(1), 88–99.

    CAS  Google Scholar 

  • Kevan, P. G., Guzman, E., Skinner, A., & Van Englesdrop, D. (2007). Colony collapse disorder in Canada: Do we have a problem? Hive Lights, 20(2), 15–18.

    Google Scholar 

  • Kimura, K., Yoshiyama, M., Saito, K., Nirasawa, K., & Ishizaka, M. (2014). Examination of mass honey bee death at the entrance to hives in a paddy rice production district in Japan: the influence of insecticides sprayed on nearby rice fields. Journal of Apicultural Research, 53(5), 599–606.

    Google Scholar 

  • Klein, A., Steffandewenter, I., & Tscharntke, T. (2003). Fruit set of highland coffee increases with the diversity of pollinating bees. Proceedings of The Royal Society B: Biological Sciences, 270(1518), 955–961.

    Google Scholar 

  • Klein, A., Vaissiere, B. E., Cane, J. H., Steffandewenter, I., Cunningham, S. A., Kremen, C., et al. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of The Royal Society B: Biological Sciences, 274(1608), 303–313.

    Google Scholar 

  • Li-Byarlay, H., Huang, M. H., Simone-Finstrom, M., Strand, M. K., Tarpy, D. R., & Rueppell, O. (2016). Honey bee (Apis mellifera) drones survive oxidative stress due to increased tolerance instead of avoidance or repair of oxidative damage. Experimental Gerontology, 83, 15–21.

    CAS  Google Scholar 

  • Liang-De, T., Hai-Yan, Z., Bu-Li, F., Hai-Yan, Q., Jian-Hui, W., Peng, L., et al. (2018). Insecticide resistance monitoring of the Hainan field populations of Megalurothrips usitatus and their susceptibility to 6 insecticides. Journal of Environmental Entomology, 40(05):1175–1181.

    Google Scholar 

  • Naggar, Y. A., Wiseman, S., Sun, J., Cutler, G. C., Aboulsoud, M. A. M., Naiem, E., et al. (2015). Effects of environmentally-relevant mixtures of four common organophosphorus insecticides on the honey bee (Apis mellifera L.). Journal of Insect Physiology, 82, 85–91.

    Google Scholar 

  • Narahashi, T., Zhao, X., Ikeda, T., Nagata, K., & Yeh, J. (2007). Differential actions of insecticides on target sites: basis for selective toxicity. Human & Experimental Toxicology, 26(4), 361–366.

    CAS  Google Scholar 

  • Niu, X., Qi, S., Wu, L., Zhang, Z., & Shi, M. (2019). Toxicity studies of ethiprole suspension concentrate to newly emerged honey bees (Apis mellifera L.). Asian Journal of Ecotoxicology, 014(003), 203–213.

    Google Scholar 

  • OECD. (2014). Honey bee (Apis mellifera) larval toxicity test, repeated exposure. OECD Draft Guidance Document. http://www.oecd.org/chemicalsafety/testing/Draft_GD_honeybee_larval_tox_repeated_exposure_25_February_2014.pdf.

  • Pesticide Properties DataBase. https://sitem.herts.ac.uk/aeru/ppdb/en/Reports/316.htm.

  • Prisco, G. D., Cavaliere, V., Annoscia, D., Varricchio, P., Caprio, E., Nazzi, F., et al. (2013). Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees. Proceedings of the National Academy of Sciences of the United States of America, 110(46), 18466–18471.

    Google Scholar 

  • Punyawattoe, P., Han, Z., Sriratanasak, W., Arunmit, S., Chaiwong, J., & Bullangpoti, V. (2013). Ethiprole resistance in Nilaparvata lugens (Hemiptera: Delphacidae): Possible mechanisms and cross-resistance. Applied Entomology and Zoology, 48(2), 205–211.

    Google Scholar 

  • Qi, S., Niu, X., Wang, D. H., Wang, C., Zhu, L., Xue, X., et al. (2020). Flumethrin at sublethal concentrations induces stresses in adult honey bees (Apis mellifera L.). Science of The Total Environment, 700, 134500.

    CAS  Google Scholar 

  • Schmehl, D. R., Tomé, H. V., Mortensen, A. N., Martins, G. F., & Ellis, J. D. (2016). Protocol for the in vitro rearing of honey bee (Apis mellifera L.) workers. Journal of Apicultural Research, 55(2), 113–129.

    Google Scholar 

  • Schmitzer, S. (2015) Proposal for a new OECD guideline for the testing of chemical on adult honey bees (Apis mellifera L.) in a 10 day chronic feeding test in the laboratory and results of the recent ring test 2014.

  • Soreq, H., & Seidman, S. (2001). Acetylcholinesterase–new roles for an old actor. Nature Reviews Neuroscience, 2(4), 294–302.

    CAS  Google Scholar 

  • Suchail, S., Guez, D., & Belzunces, L. P. (2001). Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environmental Toxicology & Chemistry, 20(11), 2482–2486.

    CAS  Google Scholar 

  • Tanaka, T., & Inomata, A. (2017). Reproductive and neurobehavioral effects of ethiprole administered to mice in the diet. Birth defects research, 109(19), 1568–1585.

    CAS  Google Scholar 

  • Tanaka, T., Suzuki, T., & Inomata, A. (2018). Reproductive and neurobehavioral effects of maternal exposure to ethiprole in F1-generation mice. Birth defects research, 110(3), 259–275.

    CAS  Google Scholar 

  • Tavares, D. A., Roat, T. C., Carvalho, S. M., Silvazacarin, E. C. M., & Malaspina, O. (2015). In vitro effects of thiamethoxam on larvae of Africanized honey bee Apis mellifera (Hymenoptera: Apidae). Chemosphere, 135, 370–378.

    CAS  Google Scholar 

  • Thamm, M., Balfanz, S., Scheiner, R., Baumann, A., & Blenau, W. (2010). Characterization of the 5-HT1A receptor of the honeybee (Apis mellifera) and involvement of serotonin in phototactic behavior. Cellular and Molecular Life Sciences, 67(14), 2467–2479.

    CAS  Google Scholar 

  • Tingle, C. C. D., Rother, J. A., Dewhurst, C. F., Lauer, S., & King, W. J. (2003). Fipronil: Environmental fate, ecotoxicology, and human health concerns. Reviews of Environmental Contamination and Toxicology, 176, 1–66.

    Google Scholar 

  • Weinstock, G. M., Robinson, G. E., Gibbs, R. A., Worley, K. C., Evans, J. D., Maleszka, R., et al. (2006). Insights into social insects from the genome of the honeybee Apis mellifera. Nature, 443(7114), 931–949.

    CAS  Google Scholar 

  • Zhang, J., Shen, M., Zhu, C., Yu, F., Liu, Z., Ally, N., et al. (2014). 3-Nitropropionic acid induces ovarian oxidative stress and impairs follicle in mouse. PLoS ONE, 9(2), e86589.

    Google Scholar 

Download references

Acknowledgements

We are grateful to the National Natural Science Foundation of China (Grant No. 21707162) and the Agricultural Science and Technology Innovation Program (talent training programs, No. 180818) for providing financial support for this study.

Author information

Authors and Affiliations

  1. Lab of Environmental Geochemistry, College of Ecology and Environment, Inner Mongolia University, Hohhot, 010000, China

    Yueyue Liu & Jiang He

  2. State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing, 100012, China

    Yueyue Liu, Chen Wang & Yingchen Bai

  3. Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, 100093, China

    Suzhen Qi

Authors
  1. Yueyue Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suzhen Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiang He
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yingchen Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Chen Wang or Suzhen Qi.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 112 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y., Wang, C., Qi, S. et al. The sublethal effects of ethiprole on the development, defense mechanisms, and immune pathways of honeybees (Apis mellifera L.). Environ Geochem Health 43, 461–473 (2021). https://doi.org/10.1007/s10653-020-00736-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-020-00736-7

Keywords

Search

Navigation