Abstract
Damage of crop plants in Greece by aphids results in serious economic losses for growers. In Greece, aphids are mainly controlled by chemical insecticides such as neonicotinoids and pyrethroids. In the present study, the response of Myzus persicae (Sulzer) and Aphis fabae Scopoli (Hemiptera: Aphididae) parthenogenetic lineages to imidacloprid and deltamethrin was examined. We evaluated toxicity of imidacloprid and deltamethrin on the fourth instar larvae of Coccinella septempunctata L. and Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae). Most of the A. fabae lineages showed low resistance factors (RRs) to both insecticides. However, 40% and 100% of M. persicae lineages showed moderate Resistance Ratios RRs values (> 10) for imidacloprid and deltamethrin, respectively. The Hazard quotient (HQ) values indicated that imidacloprid and deltamethrin may adversely affect C. septempunctata and H. variegata. We suggest that, the use of these insecticides should be carefully applied within Integrated Pest Management (IPM) programs.
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References
Afza, R., Riaz, M. A., & Afzal, M. (2020). Sublethal Effect of Six Insecticides on Predatory Activity and Survival of Coccinella Septempunctata (Coleoptera: Coccinellidae) Following Contact with Contaminated Prey and Residues. Gesunde Pflanzen, 72, 77–86.
Barratt, B. I. P., Moran, V. C., Bigler, F., & van Lenteren, J. C. (2018). The status of biological control and recommendations for improving uptake for the future. BioControl, 63, 155–167.
Bass, C., Denholm, I., Williamson, M. S., & Nauen, R. (2015). The global status of insect resistance to neonicotinoid insecticides. Pesticide Biochemistry and Physiology, 121, 78–87.
Blackman, R. L. (1971). Variation in the photoperiodic response within natural populations of Myzus persicae (Sulz). Bulletin of Entomological Research, 60, 533–546.
Blackman, R. L., & Eastop, V. F. (2000). Aphids on the World’s Crops, An Identification and Information Guide (2nd ed.). Wiley.
Bozsik, A. (2006). Susceptibility of adult Coccinella septempunctata (Coleoptera: Coccinellidae) to insecticides with different modes of action. Pest Management Science, 62, 651–654.
Brown, R. A. (1989). Pesticides and non-target terrestrial invertebrates: An industrial approach. In P. E. Jepson (Ed.), Pesticides and Non-target Terrestrial Invertebrates (pp. 19–42). Wimborne.
Bueno, A. D. F., Carvalho, G. A., Santos, A. C. D., Sosa-Gómez, D. R., & Silva, D. M. D. (2017). Pesticide selectivity to natural enemies: Challenges and constraints for research and field recommendation. Ciência Rural, 47, 1–10.
Candolfi, M., Barrett, K., Campbell, P., Forster, R., Grandy, N., Huet, M., Lewis, G., Oomen, P., Schmuck, R., Vogt, H. (2001). Guidance Document on Regulatory Testing and Risk Assessment Procedures for Plant Protection Products with Non-target Arthropods, from the ESCORT 2 Workshop SETAC. Pensacola.
Colares, F., Michaud, J. P., Bain, C. L., & Torres, J. B. (2017). Relative Toxicity of Two Aphicides to Hippodamia convergens (Coleoptera: Coccinellidae): Implications for Integrated Management of Sugarcane Aphid, Melanaphis sacchari (Hemiptera: Aphididae). Journal of Economic Entomology, 110, 52–58.
Dai, C., Ricupero, M., Puglisi, R., Lu, Y., Desneux, N., Biondi, A., & Zappalà, A. (2020). Can contamination by major systemic insecticides affect the voracity of the harlequin ladybird? Chemosphere, 256, 126986.
Desneux, N., Denoyelle, R., & Kaiser, L. (2006). A multi-step bioassay to assess the effect of the deltamethrin on the parasitic wasp. Aphidius Ervi. Chemosphere, 65, 1697–1706.
Desneux, N., Decourtye, A., & Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52, 81–106.
Fogel, M. N., Schneider, M. I., Desneux, N., González, B., & Ronco, A. E. (2013). Impact of the neonicotinoid acetamiprid on immature stages of the predator Eriopis connexa (Coleoptera: Coccinellidae). Ecotoxicology, 22, 1063–1071.
Foster, S. P., Denholm, I., & Thompson, R. (2003). Variation in response to neonicotinoid insecticides in peach-potato aphids, Myzus persicae (Hemiptera: Aphididae). Pest Management Science, 59, 166–173.
Foster, S. P., Devine, G., & Devonshire, A. L. (2007). Insecticide resistance. In H. F. van Emden & R. Harrington (Eds.), Aphids as crop pests (pp. 261–285). CABI.
Godoy, M. S., Carvalho, G. A., Carvalho, B. F., & Lasmar, O. (2010). Seletividade fisiológica de inseticidas em duas espécies de crisopídeos. Pesquisa Agropecuária Brasileira, 45, 1253–1258.
He, F., Sun, S., Tan, H., Sun, X., Shang, D., Yao, C., Qin, C., Ji, S., Li, X., Zhang, J., & Jiang, X. (2019). Compatibility of chlorantraniliprole with the generalist predator Coccinella septempunctata L. (Coleoptera: Coccinellidae) based toxicity, life-cycle development and population parameters in laboratory microcosms. Chemosphere, 225, 182–190.
He, Y., Zhao, J., Zheng, Y., Desneux, N., & Wu, K. (2012). Lethal effect of imidacloprid on the coccinellid predator Serangium japonicum and sublethal effects on predator voracity and on functional response to the whitefly Bemisia tabaci. Ecotoxicology, 21, 1291–1300.
Hodek, I., & Honek, A. (1996). Ecology of Coccinellidae. Kluwer Academic Publishers.
IRAC (Insecticide Resistance Action Committee). (2011). Prevention and Management of Insecticide Resistance in Vectors of Public Health Importance. 2nd ed. URL http://www.irac-online.org/content/uploads/2009/09/VM-Layout-v2.6_LR.pdf [accessed 8 Feb 2019].
Jiang, J., Ma, D., Zhang, Z., Yu, C., Liu, F., & Mu, W. (2018a). Favorable compatibility of nitenpyram with the aphid predator, Coccinella septempunctata L. (Coleoptera: Coccinellidae). Environmental Science and Pollution Research, 25, 27393–27401.
Jiang, J., Zhang, Z., Yu, X., Ma, D., Yu, C., Liu, F., & Mu, W. (2018b). Influence of lethal and sublethal exposure to clothianidin on the seven-spotted lady beetle, Coccinella septempunctata L. (Coleoptera: Coccinellidae). Ecotoxicology and Environmental Safety, 161, 208–213.
Karagounis, C., Kourdoumbalos, A. K., Margaritopoulos, J. T., Nanos, G. D., & Tsitsipis, J. A. (2006). Organic farming compatible insecticides against the aphid Myzus persicae (Sulzer) in peach orchards. Journal of Applied Entomology, 130, 150–154.
Kontodimas, D. C., & Stathas, G. J. (2005). Phenology, fecundity and life table parameters of the predator Hippodamia variegata reared on Dysaphis crataegi. BioControl, 50, 223–233.
Kramer, T., & Nauen, R. (2011). Monitoring of spirodiclofen susceptibility in field populations of European red mites, Panonychus ulmi (Koch) (Acari: Tetranychidae), and the cross-resistance pattern of a laboratory-selected strain. Pest Management Science, 67, 1285–1293.
Margaritopoulos, J., Kati, A., Voudouris, C., Skouras, P., & Tsitsipis, J. (2020). Long-term studies on the evolution of resistance of Myzus persicae (Hemiptera: Aphididae) to insecticides in Greece. Bulletin of Entomological Research, 111, 1–16. https://doi.org/10.1017/S0007485320000334
Santos, K. F. A., Zanuzo Zanardi, O., de Morais, M. R., Jacob, C. R. O., de Oliveira, M. B., & Yamamoto, P. T. (2017). The impact of six insecticides commonly used in control of agricultural pests on the generalist predator Hippodamia convergens (Coleoptera: Coccinellidae). Chemosphere, 186, 218–226.
Skouras, P. J., Brokaki, M., Stathas, G. J., Demopoulos, V., Louloudakis, G., & Margaritopoulos, J. T. (2019a). Lethal and sub-lethal effects of imidacloprid on the aphidophagous coccinellid Hippodamia variegata. Chemosphere, 229, 392–400.
Skouras, P. J., Margaritopoulos, J. T., Zarpas, K. D., & Tsitsipis, J. A. (2015). Development, growth, feeding and reproduction of Ceratomegilla undecimnotata, Hippodamia variegata and Coccinella septempunctata fed on the tobacco aphid, Myzus persicae nicotianae. Phytoparasitica, 43, 159–169.
Skouras, P. J., & Stathas, G. J. (2015). Development, growth and body weight of Hippodamia variegata fed Aphis fabae in the laboratory. Bulletin of Insectology, 68, 193–198.
Skouras, P. J., Stathas, G. J., Voudouris, C. C., Darras, A. I., Tsitsipis, J. A., & Margaritopoulos, J. T. (2017). Effect of synthetic insecticides on the larvae of Coccinella septempunctata from Greek populations. Phytoparasitica, 45, 165–173.
Skouras, P. J., Stathas, G. J., Demopoulos, V., Louloudakis, G., & Margaritopoulos, J. T. (2019b). The effect of five insecticides on the predators Coccinella septempunctata and Hippodamia variegata. Phytoparasitica, 47, 197–205.
Torres, J. B., & Bueno, A. D. F. (2018). Conservation biological control using selective insecticides – A valuable tool for IPM. Biological Control, 126, 53–64.
Vontas, J., Hernández-Crespo, P., Margaritopoulos, J. T., Ortego, F., Feng, H., Mathiopoulos, K. D., & Hsu, J. (2011). Insecticide resistance in Tephritid flies. Pesticide Biochemistry and Physiology, 100, 199–205.
Wilkinson, C. F. (2013). Uptake of insecticides. In C. F. Wilkinson (Ed.), Insecticide biochemistry and physiology (2nd ed., pp. 281–312). Springer.
Xiao, D., Zhao, J., Guo, X., Chen, H., Qu, M., Zhai, W., Desneux, N., Biondi, A., Zhang, F., & Wang, S. (2016). Sublethal effects of imidacloprid on the predatory seven-spot ladybird beetle Coccinella septempunctata. Ecotoxicology, 25, 1782–1793.
Yao, F., Zheng, Y., Zhao, J., Desneux, N., He, Y., & Weng, Q. (2015). Lethal and sublethal effects of thiamethoxam on the whitefly predator Serangium japonicum (Coleoptera: Coccinellidae) through different exposure routes. Chemosphere, 128, 49–55.
Acknowledgements
We thank Spiro Gianakouli for assistance with the laboratory bioassays.
Funding
This research is implemented through IKY scholarships programme and co-financed by the European Union (European Social Fund—ESF) and Greek national funds through the action entitled ʻʻReinforcement of Postdoctoral Researchers”, in the framework of the Operational Programme” Human Resources Development Program, Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF) 2014 – 2020.
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Skouras, P.J., Demopoulos, V., Mprokaki, M. et al. Relative toxicity of two insecticides to Coccinella septempunctata and Hippodamia variegata (Coleoptera: Coccinellidae): Implications for Integrated Management of the aphids, Myzus persicae and Aphis fabae (Hemiptera: Aphididae). Phytoparasitica 50, 141–150 (2022). https://doi.org/10.1007/s12600-021-00935-7
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DOI: https://doi.org/10.1007/s12600-021-00935-7