Survival and flight capacity of Apis mellifera L. (Hymenoptera: Apidae) after exposure to insecticide residues on melon leaves

Authors

DOI:

https://doi.org/10.5433/1679-0359.2025v46n3p757

Keywords:

Mortality, Pollinators, Toxicity, Selective insecticide.

Abstract

The bee Apis mellifera is crucial in pollinating melon (Cucumis melo L.) and producing its fruit. Proper use of insecticides and understanding their toxicity to pollinators is necessary to protect bees in the field. This study aimed to evaluate the residual toxicity of insecticides from the anthranilic diamide and spinosyn on A. mellifera. The experiment was conducted under laboratory conditions, evaluating two commercial doses of the anthranilic diamides Chlorantraniliprole, Cyantraniliprole, and Chlorantraniliprole + Abamectin, and the spinosyns Spinetoram and Spinosad when applied to melon leaves. After exposure to insecticide residues, survival for up to 72 hours and flight capacity of bee were assessed. Spinosad, Spinetoram, and Chlorantraniliprole + Abamectin, regardless of the dose, were toxic to bees, causing mortality rates above 85%. Chlorantraniliprole and Cyantraniliprole were less harmful, resulting in lower mortality rates. Anthranilic diamide insecticides did not affect the flight capacity of A. mellifera. Residues from insecticides tested in field doses on melon crops harm the survival of pollinating bees. However, the insecticides Chlorantraniliprole and Cyantraniliprole are viable for use in management strategies that prevent bees from being exposed to highly toxic products.

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Author Biographies

Carlos Henrique Peixoto de Barros, Universidade Federal de Campina Grande

Bachelor in Agronomy, Universidade Federal de Campina Grande, UFCG, Pombal, PB, Brazil.

Ewerton Marinho da Costa, Universidade Federal de Campina Grande

Ph.D. in Agronomy, Crop Science, Associate Professor, UFCG, Pombal, PB, Brazil.

Anderson Bruno Anacleto de Andrade, Universidade Federal de Campina Grande

Ph.D. in Plant Protection, Researcher in the Graduate Program in Tropical Horticulture, PPGHT, UFCG, Pombal, PB, Brazil.

Tiago Augusto Lima Cardoso, Universidade Federal de Campina Grande

Ph.D. in Biological Sciences, Laboratory Technician, UnUFCG, Pombal, PB, Brazil.

Elton Lúcio Araújo, Universidade Federal Rural do Semi-Árido

Ph.D. in Agricultural Entomology, Associate Professor, Universidade Federal Rural do Semi Árido, UFERSA, Mossoró, Brazil.

Brenda Carla Rosendo Martins, Universidade Federal de Campina Grande

Master Student in the Graduate Program in Tropical Horticulture, PPGHT, UFCG, Pombal, PB, Brazil.

Luiz Antônio Freire Alencar Silva, Universidade Federal de Campina Grande

Student in Undergraduate Agronomy, UFCG, Pombal, PB, Brazil.

Emanoely Karoliny Santos da Silva, Universidade Federal de Campina Grande

Master Student in the Graduate Program in Tropical Horticulture, PPGHT, UFCG, Pombal, PB, Brazil.

References

Abbott, W. S. (1925). A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18(1), 265-267. doi: 10.1093/jee/18.2.265a

Akça, R., & Saruhan, I. (2022). The effects of some insecticides on honeybees (Apis mellifera). Israel Journal of Ecology and Evolution, 69(1-2), 37-43. doi: 10.1163/22244662-bja10043

Araújo, R. D. S., Lopes, M. P., Viana, T. A., Bastos, D. S. S., Machado-Neves, M., Botina, L. L., & Martins, G. F. (2023). Bioinsecticide spinosad poses multiple harmful effects on foragers of Apis mellifera. Environmental Science and Pollution Research, 30(25), 66923-66935. doi: 10.1007/s11356-023-27143-6

Carmo, D. G., Marsaro, A. L., Jr., Costa, T. L., Farias, E. de S., Ribeiro, A. V., & Picanço, M. C. (2017). Toxicidade de inseticidas comerciais, por ação de contato, para Apis mellifera. Insetos e Entomologia, 145-148.

Carvalho, S. M., Carvalho, G. A., Carvalho, C. F., Carvalho, J. S. S., & Baptista, A. P. M. (2009). Toxicidade de acaricidas/inseticidas empregados na citricultura para a abelha africanizada Apis mellifera L., 1758 (Hymenoptera: Apidae). Arquivos do Instituto Biológico, 76(4), 597-606. doi: 10.1590/1808-1657v76p5972009

Costa, E. M., Araujo, E. L., Maia, A. V. P., Silva, F. E. L., Bezerra, C. E. S., & Silva, J. G. (2014). Toxicity of insecticides used in the Brazilian melon crop to the honey bee Apis mellifera under laboratory conditions. Apidologie, 45(1), 34-44. doi: 10.1007/s13592-013-0226-5

Costa, E. M., Augusto, L. P., Silva, E. K. S. da, Rocha, V. H. M., Cardoso, T. A. L., Araujo, E. L., & Almeida, F. A. (2024). Honey bee survival and flight capacity after exposure to sulfoxaflor residues. Sociobiology, 71(4), e10729-e10729. doi: 10.13102/sociobiology.v71i4.10729

Edwards, C. R., Gerber, C. K., & Hunt, G. J. (2003). A laboratory study to evaluate the toxicity of the Mediterranean fruit fly, Ceratitis capitata, bait, Success 0.02 CB, to the honey bee, Apis mellifera. Apidologie, 34(2), 171-180. doi: 10.1051/apido:2003005

Farooqi, M. A., & Arshad, M. (2016). Toxicity of three commonly used nicotinoids and spinosad to Apis mellifera L. (Hymenoptera: Apidae) using surface residual bioassays. Pakistan Journal of Zoology, 48(6), 1983-1987.

Fent, K., & Christen, V. (2017). Exposure of honeybees (Apis mellifera) to different classes of insecticides exhibit distinct molecular effect patterns at concentrations that mimic environmental contamination. Environmental Pollution, 226, 48-59. doi: 10.1016/j.envpol.2017.04.003

Fernandes, N. S., Luz, L. R., Alves, E. G., Fº., Aragão, F. A. S. D., Zocolo, G. J., & Freitas, B. M. (2023). Differences in the chemical composition of melon (Cucumis melo L.) nectar explain flower gender preference by its pollinator, Apis mellifera. Journal of the Brazilian Chemical Society, 34(7), 976-986. doi: 10.21577/0103-5053.20230010

Godfray, H. C. J., Blacquière, T., Field, F. M., Hails, R. S., Petrokofsky, G., Potts, S. G., Raine, N. E., Vandergen, A. J., & Mclean, A. R. (2014). A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Published by the Royal Society B, 281(1786), 20140558. doi: 10.1098/rspb.2014.0558

Gomes, I. N., Vieira, K. I. C., Gontijo, L. M., & Resende, H. C. (2020). Honeybee survival and flight capacity are compromised by insecticides used for controlling melon pests in Brazil. Ecotoxicology, 29, 97-107. doi: 10.1007/s10646-019-02145-8

Heard, M. S., Baas, J., Dorne, J. L., Lahive, E., Robinson, A. G., Rortais, A., Spurgeon, D. J., Svendsen, C., & Hesketh, H. (2017). Comparative toxicity of pesticides and environmental contaminantsin bees: are honey bees a useful proxy for wild bee species? Science of the Total Environment, 578(1), 357-365. doi: 10.1016/j.scitotenv.2016.10.180

Hung, K. L. J., Kingston, J. M., Albrecht, M., Holway, D. A., & Kohn, J. R. (2018). The worldwide importance of honey bees as pollinators in natural habitats. Proceedings of the Royal Society B: Biological Sciences, 285(1870), 20172140. doi: 10.1098/rspb.2017.2140

Hünicken, P. L., Morales, C. L., Villalobos, A. E. de, & Garibaldi, L. A. (2022). Evaluation of interactions between honeybees and alternative managed pollinators: a meta-analysis of their effect on crop productivity. Agriculture, Ecosystems & Environment, 340, 108156. doi: 10.1016/j.agee.2022.108156

Ibrahim, E. D. S., Abd Alla, A. E., El-Masarawy, M. S., Salem, R. A., Hassan, N. N., & Moustafa, M. A. (2023). Sulfoxaflor influences the biochemical and histological changes on honeybees (Apis mellifera L.). Ecotoxicology, 32(5), 674-681. doi: 10.1007/s10646-023-02677-0

Kaabeche, M., Charreton, M., Kadala, A., Mutterer, J., Charnet, P., & Collet, C. (2024). Cardiotoxicity of the diamide insecticide chlorantraniliprole in the intact heart and in isolated cardiomyocytes from the honey bee. Scientific Reports, 14(1), 14938. doi: 10.1038/s41598-024-65007-2

Kadala, A., Charreton, M., Charnet, P., & Collet, C. (2019). Honey bees long-lasting locomotor deficits after exposure to the diamide chlorantraniliprole are accompanied by brain and muscular calcium channels alterations. Scientific Reports, 9(1), 2153. doi: 10.1038/s41598-019-39193-3

Kim, J., Chon, K., Kim, B. S., Oh, J. A., Yoon, C. Y., & Park, H. H. (2022). Assessment of acute and chronic toxicity of cyantraniliprole and sulfoxaflor on honey bee (Apis mellifera) larvae. Pest Management Science, 78(12), 5402-5412. doi: 10.1002/ps.7162

Leonhardt, S. D., Gallai, N., Garibaldi, L. A., Kuhlmann, M., & Klein, A. M. (2013). Economicgain, stability of pollination and bee diversity decrease from southern to northern Europe. Basic and Applied Ecology, 14(6), 461-471. doi: 10.1016/j.baae.2013.06.003

Lopes, M. P., Fernandes, K. M., Tomé, H. V. V., Gonçalves, W. G., Miranda, F. R., Serrão, J. E., & Martins, G. F. (2018). Spinosadâ€mediated effects on the walking ability, midgut, and Malpighian tubules of Africanized honey bee workers. Pest Management Science, 74(6), 1311-1318. doi: 10.1002/ps.4815

Martelli, F., Ravenscroft, T. A., Hutchison, W., & Batterham, P. (2023). Tissueâ€specific transcriptome analyses in Drosophila provide novel insights into the mode of action of the insecticide spinosad and the function of its target, nAChRα6. Pest Management Science, 79(10), 3913-3925. doi: 10.1002/ps.7585

Messellem, I., Aguib, S., Abed, R., & Abderrezak, S. (2024). Comparative study of pollination efficiency and yield components of melon crops by three bee species in algeria. Journal of the Kansas Entomological Society, 97(1), 1-12. doi: 10.2317/0022-8567-97.1.1

Naccari, V., Trevisi, G., Naccari, C., Ferrara, G., Bava, R., & Palma, E. (2024). Poisoning due to Spinosad in honey bees: toxicological report. Journal of Apicultural Research, 63, 1-8. doi: 10.1080/00218839.2024.2425913

Pham-Delègue, M. H., Decourtye, A., Kaiser, L., & Devillers, J. (2002). Behavioural methods to assess the effects of pesticides on honey bees. Apidologie, 33(5), 425-432. doi: 10.1051/apido:2002033

Pinheiro, J. N., & Freitas, B. M. (2010). Efeitos letais dos pesticidas agrícolas sobre polinizadores eperspectivas de manejo para os agroecossistemas brasileiros. Oecologia Australis, 14(1), 266-281.

Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O., & Kunin, W. E. (2010). Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution, 25(6), 345-353. doi: 10.1016/j.tree.2010.01.007

R Core Team (2022). R: uma linguagem e ambiente para computação estatística. R Foundation for Statistical Computing.

Ratnakar, V., Koteswara, R. S. R., Sridevi, D., & Vidyasagar, B. (2017). Sublethal lethal exposure of certain newer insecticides molecules to honeybee, Apis mellifera Linnaeus. Indian Journal of Pure & Applied Biosciences, 5(4), 641-646. doi: 10.18782/2320-7051.5234

Ribeiro, M. D. F., Silva, E. M. S. D., Lima, I. D. O., & Kiill, L. H. P. (2015). Honey bees (Apis mellifera) visiting flowers of yellow melon (Cucumis melo) using different number of hives. Ciência Rural, 45(10), 1768-1773. doi: 10.1590/0103-8478cr20140974

Rosa, J. M., Arioli, C. J., Nunes-Silva, P., & Garcia, F. R. M. (2019). Disappearance of pollinating bees in natural and agricultural systems: is there an explanation?. Revista de Ciências Agroveterinárias, 18(1), 154-162. doi: 10.5965/223811711812019154

Salgado, V. L. (1998). Studies on the mode of action of spinosad: insect symptoms and physiological correlates. Pesticide Biochemistry and Physiology, 60(2), 91-102. doi: 10.1006/pest.1998.2332

Shannon, B., Walker, E., & Johnson, R. M. (2023). Toxicity of spray adjuvants and tank mix combinations used in almond orchards to adult honey bees (Apis mellifera). Journal of Economic Entomology, 116(5), 1467-1480. doi: 10.1093/jee/toad161

Shi, T., Jiang, X., Cao, H., & Yu, L. (2023). Exposure to sublethal concentrations of thiacloprid insecticide modulated the expression of microRNAs in honeybees (Apis mellifera L.). Ecotoxicology and Environmental Safety, 264, 115499. doi: 10.1016/j.ecoenv.2023.115499

Silva, I. P., Oliveira, F. A. S., Pedroza, H. P., Gadelha, I. C. N., Melo, M. M., & Soto-Blanco, B. (2015). Pesticide exposure of honeybees (Apis mellifera) pollinating melon crops. Apidologie, 46(6), 703-715. doi: 10.1007/s13592-015-0360-3

Sousa, R. M., Aguiar, O. S., Andrade, A. B. A., Medeiros, A. C., & Maracajá, P. B. (2013). Densidade de colméias com abelhas africanizadas (Apis mellifera L.) para polinização da cultura do melão (Cucumis melo L.) no estado do Ceará-Brasil. ACTA Apicola Brasilica, 1(1), 9-12. doi: 10.18378/aab.v1i1.3586

Souza, A. A., Silva, E. K. S., Costa, E. M., Cardoso, T. A. L., Costa, J. A. D. M. A., Silva, D. M. T., & Oliveira Gondim, A. R. (2024). Survival and flight capacity of Apis mellifera after contact with residues of spiromesifen on melon leaves. Sociobiology, 71(4), e10753-e10753. doi: 10.13102/sociobiology.v71i4.10753

Therneau, T., Lumley, T. (2020). Survival: Survival analysis, including penalised likelihood. R package version. http://CRAN.Rproject.org/package=survival

Tschoeke, P. H., Oliveira, E. E., Dalcin, M. S., Silveira-Tschoeke, M. C. A., Sarmento, R. A., & Santos, G. R. (2019). Botanical and synthetic pesticides alter the flower visitation rates of pollinator bees in Neotropical melon fields. Environmental Pollution, 251, 591-599. doi: 10.1016/j.envpol.2019.04.133

Walker, E. K., Brock, G. N., Arvidson, R. S., & Johnson, R. M. (2022). Acute toxicity of fungicide insecticide adjuvant combinations applied to almonds during bloom on adult honey bees. Environmental Toxicology and Chemistry, 41(4), 1042-1053. doi: 10.1002/etc.5297

Williams, J. R., Swale, D. R., & Anderson, T. D. (2020). Comparative effects of technicalâ€grade and formulated chlorantraniliprole to the survivorship and locomotor activity of the honey bee, Apis mellifera (L.). Pest Management Science, 76(8), 2582-2588. doi: 10.1002/ps.5832

Wu, W. Y., Liao, L. H., Lin, C. H., Johnson, R. M., & Berenbaum, M. R. (2023). Effects of pesticide-adjuvant combinations used in almond orchards on olfactory responses to social signals in honey bees (Apis mellifera). Scientific Reports, 13(1), 15577. doi: 10.1038/s41598-023-41818-7

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Published

2025-05-08

How to Cite

Barros, C. H. P. de, Costa, E. M. da, Andrade, A. B. A. de, Cardoso, T. A. L., Araújo, E. L., Martins, B. C. R., … Silva, E. K. S. da. (2025). Survival and flight capacity of Apis mellifera L. (Hymenoptera: Apidae) after exposure to insecticide residues on melon leaves. Semina: Ciências Agrárias, 46(3), 757–770. https://doi.org/10.5433/1679-0359.2025v46n3p757

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