Impact of entomopathogenic nematodes on Africanized honey bees Apis mellifera L. (Hymenoptera: Apidae) workers

Gabriela Libardoni, Raiza Abati, Amanda Roberta Sampaio, Fernanda Caroline Colombo, Rodrigo Mendes Antunes Maciel, Bruna Guide, Fabiana Martins Costa-Maia, Everton Ricardi Lozano, Pedro Manuel Oliveira Janeiro Neves, Michele Potrich


Africanized honey bee populations (Apis mellifera L.) have been decreasing mainly due to the intense use of synthetic insecticides associated with pollution and climate change. To minimize these impacts on the environment and bee populations, the use of biological control agents has been intensified. These products are generally safer for non-target insects, such as bees, which are important pollinating insects. Thus, the objective of this study was to evaluate the impact of entomopathogenic nematodes on the longevity of the Africanized honey bee A. mellifera workers. Seven treatments were used: Heterorhabditis amazonensis, Heterorhabditis bacteriophora, Heterorhabditis indica, Steinernema carpocapsae, Steinernema feltiae, and Steinernema rarum, at a concentration of 40 infective juveniles per cm2 (IJs/cm²), and a control in which autoclaved distilled water was used. Two bioassays were performed: 1) spraying nematodes on the workers and 2) spraying nematodes on glass plates, in which the bees remained for two hours. Each treatment consisted of five replicates with 20 bees each. Bees were kept in cages of PVC (20 × 10 cm) covered with a voile fabric and provided pieces of cotton soaked in water and Candy paste. The cages were kept in a climatized room (27 ± 2 °C temperature, 60 ± 10% relative humidity, and 12 h photophase) and the mortality was evaluated from 12 to 240 hours. In bioassay 1, the three treatments with nematodes of the genus Steinernema reduced the longevity of the workers (103.9, 96.3, and 99.6 h) when compared to treatments with Heterorhabditis (149.7, 126.8, and 134.7 h), of which, only H. amazonensis (149.7 h) did not differ from the control (166.0 h). In bioassay 2, all treatments reduced the longevity of honey bees (155.4 to 93.9 h) in relation to the control (176.1 h). Entomopathogenic nematodes, especially Heterorhabditis, need to be tested using other methodologies and for different durations of exposure and application because in the laboratory, they were less selective to A. mellifera.


Africanized honey bee; Biological control; Steinernema spp; Heterorhabditis spp.

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Aristizábal, L. F., Ortiz, A. L., Quintero, J. C., López-Nuñez, J. C., Toro, H., & Arthurs, S. P. (2015). Effect of Colombian strains of Steinernema colombiense (Rhabditida?: Steinernematidae) and Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) against Eurhizococcus colombianus (Hemiptera: Margarodidae) and Aeneolamia sp . (Hemiptera: Cercopidae). Florida Entomologist, 98(3), 981-983. doi: 10.1653/024.098.0330

Ballantyne, G., Baldock, K. C. R., Rendell, L., & Willmer, P. G. (2017). Pollinator importance networks illustrate the crucial value of bees in a highly speciose plant community. Scientific Reports, 7(1), 1-13. doi: 10.1038/s41598-017-08798-x

Baptista, A. P. M., Carvalho, G. A., Carvalho, S. M., Carvalho, C. F., & Bueno, J. S. S., Fº. (2009). Toxicidade de produtos fitossanitários utilizados em citros para Apis mellifera. Ciência Rural, 39(4), 955-961. doi: 10.1590/S0103-84782009005000049. Recuperado de record.url?eid=2-s2.0-68949107820&partnerID=40&md5=ba13c7d 735d48ae1456d5ee6b7933f27

Blackburn, D., Shapiro-ilan, D. I., & Adams, B. J. (2016). Biological control and nutrition?: Food for thought. Biological Control, 97(1), 1-8. doi: 10.1016/j.biocontrol.2016.03.007

Brighenti, D. M., Carvalho, C. F., Carvalho, G. A., Brighenti, C. R. G., & Carvalho, S. M. (2007). Bioatividade do Bacillus thuringiensis var. kurstaki (Berliner, 1915) para adultos de Apis mellifera Linnaeus, 1758 (Hymenoptera: Apidae). Ciência e Agrotecnologia, 31(2), 279-289. doi: 10.1590/s1413-70542007000200003

Calatayud-Vernich, P., Calatayud, F., Simó, E., Suarez-Varela, M. M., & Picó, Y. (2016). Influence of pesticide use in fruit orchards during blooming on honeybee mortality in 4 experimental apiaries. Science of The Total Environmen, 541(1), 33-41. doi: 10.1016/j.scitotenv.2015.08.131

Carvalho, S. M., Carvalho, G. A., Carvalho, C. F., Bueno, J. S. S., Fº., & 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/s0103-84782009005000049

Colombo, F. C., Maciel, R. M. A., Abati, R., RaulinoDomanski, F., Longhi, S. J., Costa-Maia, F. M., Vismara, E. S., Lozano, E. R. & Potrich, M. (2020) Do Beauveria bassiana and Metarhizium anisopliae affect worker survival and the production of Africanized Apis mellifera queens?, Journal of Apicultural Research, 59(5) 1-10. doi: 10.1080/00218839.2020.1828237

Costa-Maia, F. M., Lino-Lourenço, D. A., & Toledo, V. de A. A. de. (2010). Aspectos econômicos e sustentáveis da polinização por abelhas. In T. N. Martin, A. J. Waclawovsky, F. Kuss, A. S. Mendes, & E. J. Brun (Eds.), Sistemas de produção agropecuária (ciências agrárias, animais e florestais) (pp. 45-67). Dois Vizinhos: Editora UTFPR.

Dutka, A., Mcnulty, A., & Williamson, S. M. (2015). A new threat to bees?? Entomopathogenic nematodes used in biological pest control cause rapid mortality in Bombus terrestris. PeerJ, 3(1), 1-9. doi: 10. 7717/peerj.1413

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

Lewis, E. E., Campbell, J., Gri, C., Kaya, H., & Peters, A. (2006). Behavioral ecology of entomopathogenic nematodes. Biological Control, 38(1), 66-79. doi: 10.1016/j.biocontrol.2005.11.007.

Libardoni, G., Gouvea, A. de, Costa-Maia, F. M., Lozano, E. R., Freitas, P. F. de, Colombo, F. C. Potrich, M. (2018). Effect of different Bacillus thuringiensis strains on the longevity of Africanized honey bee. Semina: Ciências Agrárias, 39(1), 329-337. doi: 10.5433/1679-0359.2018v39n1p329

Molina, J. P., & López, N. J. C. (2001). Producción in vivo de tres entomonematodos con dos sistemas de infección en dos hospedantes. Revista Colombiana de Entomología, 27(1-2), 73-78.

Oliveira, M. O. de. (2015). Declínio populacional das abelhas polinizadoras de culturas agrícolas. Acta Apicola Brasilica, 3(2), 1-6. doi: 10.18378/aab.v3i2.3623

Pires, C. S. S., Pereira, F. de M., Lopes, M. T. do R., Nocelli, R. C. F., Malaspina, O., Pettis, J. S., & Teixeira, É. W. (2016). Enfraquecimento e perda de colônias de abelhas no Brasil?: há casos de CCD?? Pesquisa Agropecuária Brasileira, 51(5), 422-442. doi: 10.1590/S0100-204X2016000500003

Sharma, S., & Aggarwal, N. (2019). Safety assessment of selected biopesticides and botanicals on Trichogramma spp. (Hymenoptera: Trichogrammatidae) in fields. Indian Journal of Experimental Biology, 57(6), 443-449.


Semina: Ciênc. Agrár.
Londrina - PR
E-ISSN 1679-0359
DOI: 10.5433/1679-0359
Este obra está licenciado com uma Licença Creative Commons Atribuição-NãoComercial 4.0 Internacional