Can the glyphosate herbicide cause behavioral changes in worker bees?

Authors

DOI:

https://doi.org/10.33448/rsd-v12i6.42439

Keywords:

Pesticides; Behavior; Apis.

Abstract

The objective of this study was to observe possible behavioral alterations of Africanized bees (Apis mellifera Linnaeus, 1758) after exposure to glyphosate herbicide. For this, two exposure methods were used (ingestion and spraying) and concentrations of 0 (Control Group), 0.01 and 1 mL.L-1 during 24 hours of exposure. In the ingestion method, the bees were fed with honey added to the solutions, while in the contact test, the bees were sprayed with the herbicide concentrations. Contact interactions (antennation and trofalaxis), mobility (ability to take off) and lethargy (difficulty taking off and poor flight) were analyzed, in addition to individual mortality. In general, in both types of exposure (ingestion and spraying), at the lowest concentration tested (0.01 mL.L-1) higher frequency of contact and lower mobility of bees were observed. While bees exposed to 1 mL.L-1 of glyphosate showed less contact and greater mobility and lethargy, in addition to a higher bee mortality rate. It was confirmed that higher concentrations of the herbicide can affect the social interactions of bees; however, the spraying method was the one that led to the highest mortality. Thus, we conclude that exposure to glyphosate causes effects on social interactions in individuals of A. mellifera.

Author Biographies

Letícia Gonçalves Ribeiro, Universidade Federal de São Carlos



Kátila Maria Ferreira, Universidade Federal de São Carlos



References

Abraham, J., Benhotons, G. S., krampah, I., Tagba, J., Amissah, C. & Abraham, J. D. (2018). Commercially formulated glyphosate can kill non-target pollinator bees under laboratory conditions. Entomologia Experimentalis et Applicata, 166(8): 695–702. https://doi.org/10.1111/eea.12694

AGROFIT (2020). Sistema de Agrotóxicos Fitossanitários. Consulta de Ingrediente Ativo 2020. http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons.

Amarante Junior, O. P., Santos, T. C. R., Brito, N. M. & Ribeiro, M. L. (2002). Glifosato: propriedades, toxicidade, usos e legislação. Química Nova, 25(4): 589–593. https://doi.org/10.1590/S0100-40422002000400014

Bacon, M.-H., Vandelac, L., Gagnon, M.-A., & Parent, L. (2023). Poisoning regulation, research, health, and the environment: The Glyphosate-based herbicides case in Canada. Toxics, 11(2): 121. https://doi.org/10.3390/toxics11020121

Balbuena, M. S., Tison, L., Hahn, M.-L., Greggers, U., Menzel, R., & Farina, W. M. (2015). Effects of sublethal doses of glyphosate on honeybee navigation. Journal of Experimental Biology, 218(17): 2799–2805. https://doi.org/10.1242/jeb.117291

Berg, C.J., King, H. P., Delenstarr, G., Kumar, R., Rubio, F., & Glaze, T. (2018). Glyphosate residue concentrations in honey attributed through geospatial analysis to proximity of large-scale agriculture and transfer off-site by bees. PLOS ONE, 13(7): e0198876. https://doi.org/10.1371/journal.pone.0198876

Claudianos, C., Ranson, H., Johnson, R. M., Biswas, S., Schuler, M. A., Berenbaum, M. R., Feyereisen, R., & Oakeshott, J. G. (2006). A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Molecular Biology, 15(5): 615–636. https://doi.org/10.1111/j.1365-2583.2006.00672.x

Costa, L. G. de L., Barchuk, A. R. & Teixeira, I. R. do V. (2020). Effects of the Neonicotinoid Imidacloprid on the feeding behavior of Melipona quadrifasciata anthidioides Lep. Revista Agrogeoambiental, 12(1). http://dx.doi.org/10.18406/2316-1817v12n120201411

De Jong, D. (1996). Africanized honey bees in Brazil, forty years of adaptation and success. Bee World, 77(2): 67–70. https://doi.org/10.1080/0005772x.1996.11099289

Domingos, H. G. T. & Gonçalves, L. S. (2014). Termorregulação de abelhas com ênfase em Apis mellifera. Acta Veterinaria Brasilica, 8(3): 151–154. https://doi.org/10.21708/avb.2014.8.3.3491

Engel, P.; Martinson, V. G. & Moran, N. A. (2012). Functional diversity within the simple gut microbiota of the honey bee. Proceedings of the National Academy of Sciences, 109(27): 11002-11007.

Faita, M. R., Oliveira, E. M., Alves-Júnior, V. V., Orth, A. I. & Nodari, R. O. (2018). Changes in hypopharyngeal glands of nurse bees (Apis mellifera) induced by pollen-containing sublethal doses of the herbicide Roundup®. Chemosphere, 211: 566–572. https://doi.org/10.1016/j.chemosphere.2018.07.189

Farina, W. M., Balbuena, M. S., Herbert, L.T., Goñalons, C. M. & Vázquez, D. E. (2019). Effects of the herbicide glyphosate on honey bee sensory and cognitive abilities: Individual impairments with implications for the hive. Insects, 10(10): 354. https://doi.org/10.3390/insects10100354

Fent, K., Haltiner, T., Kunz, P. & Christen, V. (2020). Insecticides cause transcriptional alterations of endocrine related genes in the brain of honey bee foragers. Chemosphere, 260: 127542.

Freitas, B. M. & Pinheiro, J. N. (2010). Efeitos sub-letais dos pesticidas agrícolas e seus impactos no manejo de polinizadores dos agroecossistemas brasileiros. Oecologia Australis, 14(1): 282–298. https://doi.org/10.4257/oeco.2010.1401.17

Frings, H. & Frings, M. (1949). The loci of contact chemoreceptors in insects: a review with new evidence. The American Midland Naturalist. 41(3): 602- 658.

Galli, A. J. B. & Montezuma, M. C. (2005). Glifosato: Alguns aspectos da utilização do herbicida glifosato na agricultura. Santo André: ACADCOM Gráfica e Editora.

Groh, C., Tautz, J. & Rossler, W. (2004). Synaptic organization in the adult honey bee brain is influenced by brood-temperature control during pupal development. Proceedings of the National Academy of Sciences, 101(12): 4268–4273. https://doi.org/10.1073/pnas.0400773101

Helmer, S. H., Kerbaol, A., Aras, P., Jumarie, C. & Boily, M. (2014). Effects of realistic doses of atrazine, metolachlor, and glyphosate on lipid peroxidation and diet-derived antioxidants in caged honey bees (Apis mellifera). Environmental Science and Pollution Research, 22(11): 8010–8021. https://doi.org/10.1007/s11356-014-2879-7

Herbert, L. T., Vázquez, D. E., Arenas, A. & Farina, W. M. (2014). Effects of field-realistic doses of glyphosate on honeybee appetitive behavior. The Journal of Experimental Biology, 217(19): 3457–3464. https://doi.org/10.1242/jeb.109520

Imperatriz-Fonseca, V. L. & Joly, C. A. (2017). Capítulo 1 - Avaliação polinizadores, polinização e produção de alimentos da Plataforma Intergovernamental de Biodiversidade e Serviços de Ecossistemas (IPBES). In: Centro de Gestão e Estudos Estratégicos (CGEE), Org. Importância dos polinizadores na produção de alimentos e na segurança alimentar global. Brasília, DF: Centro de Gestão e Estudos Estratégicos, 17–38.

Jacob, C. R. O., Zanardi, O. Z., Malaquias, J. B., Silva, C. A. S., & Yamamoto, P. T. (2019) The impact of four widely used neonicotinoid insecticides on Tetragonisca angustula (Latreille) (Hymenoptera: Apidae). Chemosphere, 224: 65–70. https://doi.org/10.1016/j.chemosphere.2019.02.105

Jay, S. C. (1986) Spatial management of honeybees on crops. Annual Review of Entomology, 31: 49–65. https://doi.org/10.1146/annurev.en.31.010186.000405

Kasiotis, K. M., Anagnostopoulos, C., Anastasiadou, P. & Machera, K. (2014). Pesticide residues in honeybees, honey and bee pollen by LC–MS/MS screening: Reported death incidents in honeybees. Science of the Total Environment, 485-486: 633–642. https://doi.org/10.1016/j.scitotenv.2014.03.042

Kwong, W. K. & Moran, N. A. (2016). Gut microbial communities of social bees. Nature Reviews Microbiology, 14(6): 374-384.

Mello, M. H. S. H., Silva, E. A. & Natal, D. (2003). Abelhas africanizadas em área metropolitana do Brasil: abrigos e influências climáticas. Revista de Saúde Pública, 37(2): 237–241. https://doi.org/10.1590/s0034-89102003000200012

Michener, C. D. (1969). Comparative social behavior of bees. Annual Review of Entomology, 14(1): 299–342. https://doi.org/10.1146/annurev.en.14.010169.001503

Miranda, J. E., Navickiene, H. M. D., Nogueira-Couto, R. H., Bortoli, S. A., Kato, M. J., Bolzani, V. S. & Furlan, M. (2003). Susceptibility of Apis mellifera (Hymenoptera: Apidae) to pellitorine, an amide isolated from Piper tuberculatum (Piperaceae). Apidologie, 34(4): 409–415. https://doi.org/10.1051/apido:2003036

Moreira, D. D. O., Viana-Bailez, A. M., Ferreira, F. F., Erthal Junior, M., Carrera, F. & Samuels, R. I. (2007). Trofalaxia oral entre operárias de Acromyrmex subterraneus subterraneus Forel 1893 (Formicidae: Attini) em mini-formigueiros, XVIII Simpósio de Mirmecologia Biológico, 69(2), 300-402.

Oliveira, G. (2019). Desempenho produtivo, reprodutivo e resposta fisiológica de abelhas africanizadas que receberam suplementação alimentar. [Dissertação de Mestrado]. Universidade Federal de Goiás, Goiânia-GO.

Oliveira, M. L. & Cunha, J. A. (2005). Abelhas africanizadas Apis mellifera scutellata Lepeletier, 1836 (Hymenoptera: Apidae: Apinae) exploram recursos na Floresta Amazônica? Acta Amazonica, 35(3): 389-394. https://doi.org/10.1590/s004459672005000300013

Rodrigues, S. P., Da Silva, J. C. I., De Oliveira, T. C., Da Silva, L. I. & Menezes, N. C. (2021) O papel da microbiota bacteriana intestinal de abelhas eussociais: uma revisão de literatura. Research, Society and Development, 10(14): e30101421623-e30101421623

Rubio, F., Guo, E. & Kamp, L. (2014). Survey of glyphosate residues in honey, corn and soy products. Journal of Environmental & Analytical Toxicology, 5(1). https://doi.org/10.4172/2161-0525.1000249

Scheffer, J. da L. (2022). Efeito de dose letal e subletal do herbicida glifosato no transcriptoma de abelhas Apis mellifera africanizadas na fase de campeiras. [Dissertação de Mestrado]. Universidade Estadual Paulista "Júlio de Mesquita Filho", Faculdade de Medicina Veterinária e Zootecnia.

Silva, P. H. O. S., Corrêa, F. R., da Silva, N. F., Cavalcante, W. S. da S., Ribeiro, D. F & Rodrigues, E. (2023). Eficiência de herbicidas pré-emergentes no manejo de plantas daninhas na cultura da soja. Brazilian Journal of Science, 2(4): 21-31. https://doi.org/10.14295/bjs.v2i4.267

Singh, S., Kumar, V., Gill, J. P. K., Datta, S., Singh, S., Dhaka, V., Kapoor, D., Wani, A. B., Dhanjal, D. S., Kumar, M., Harikumar, S. L. & Singh. J. (2020). Herbicide Glyphosate: Toxicity and Microbial Degradation. Intenartional Journal Environmental Research Public Health, 17(7519). https://www.mdpi.com/1660-4601/17/20/7519

Sousa, J. R. L., Amarante Junior, O. P., Brito, N. M. & Franco, T. C. R. S. (2013). Ação de pesticidas sobre abelhas: Avaliação do risco de contaminação de méis. Acta Tecnológica, 8(1): 28–36.

Stanley, D. A & Raine, N. E. (2016). Chronic exposure to a Neonicotinoid pesticide alters the interactions between bumblebees and wild plants. Functional Ecology, 30: 1132–1139. https://doi.org/10.1111/1365-2435.12644

Suárez, M. E. & Thorne, B. L. (2000). Rate, amount, and distribution pattern of alimentary fluid transfer via trofallaxis in three species of termites (Isoptera: Rhinotermitidae, Termopsidae). Annals of the Entomological Society of América, 93(1): 145-155.

Thompson, H. M., Levine, S. L., Doering, J., Norman, S., Manson, P., Sutton, P. & Von Mérey, G. (2014). Evaluating exposure and potential effects on honeybee brood (Apis mellifera) development using glyphosate as an example. Integrated Environmental Assessment and Management, 10(3): 463–470. https://doi.org/10.1002/ieam.1529

Weatherspark.com, [n.d.] [viewed 5 November 2021]. Clima, condições meteorológicas e temperatura média por mês de Buri (Brasil) - Weather Spark [online]. Minneapolis. Available from: https://pt.weatherspark.com/y/30060/Clima-caracter%C3%ADstico-em-Buri-Brasil-durante-o-ano

Wolff, L. F., Pereira, F. M., Lopes, M. T. R., Camargo, R. C. R. & Vieira Neto, J. M. (2006). Povoamento das colméias (Embrapa Meio-Norte - Documentos 146). Teresina: Embrapa Meio-Norte.

Zgurzynski, M. I. & Lushington, G. H. (2019). Glyphosate impact on Apis mellifera navigation: A combined behavioral and cheminformatics study. EC Pharmacology and Toxicology, 7(8): 806–824.

Published

04/07/2023

How to Cite

ANTUNES, B. C. .; RIBEIRO, L. G. .; ROQUE, A. M. .; FERREIRA, K. M. .; WINKALER, E. U. .; LHANO, M. G. . Can the glyphosate herbicide cause behavioral changes in worker bees?. Research, Society and Development, [S. l.], v. 12, n. 6, p. e29412642439, 2023. DOI: 10.33448/rsd-v12i6.42439. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/42439. Acesso em: 16 nov. 2024.

Issue

Section

Agrarian and Biological Sciences