Avoidance test with earthworms (Eisenia andrei) in natural soil treated with a Bacillus thuringiensis-based biopesticide to soil quality evaluation
DOI:
https://doi.org/10.33448/rsd-v9i8.5774Keywords:
Behavior test; toxicity; Biosensor; Oligochaetes; Terrestrial ecotoxicology.Abstract
Tests using earthworms is an important preliminary screening tool in soil ecotoxicology studies. The aim was to evaluate the natural soil quality containing Bacillus thuringiensis (Bt) as an agent in a biopesticide using Eisenia andrei as bioindicator. The filter contact test was based on OECD 207 guideline and avoidance test based on ISO 17512-1, with modifications. After exposure by contact, no mortality was observed, however, excess mucus released lethargic movements and decreased touch reflexes were observed from 100 mg L-1. These results raise the question of whether sublethal effects are relevant when about the physiological effects that would harm organism and their important functions in the ecosystem. In the avoidance test, there was no response to Bt soil, suggesting that the biopesticide does not alter the soil quality or present high toxicity to E. andrei. The use of Bt biopesticides indicates to few negative effects to annelids, what suggests, at least, a viable alternative in relation to the high toxicity of chemical insecticides frequently used in agriculture.
References
Amado, T. J. C., Conceição, P. C., Bayer, C., & Eltz, F. L. F. (2007). Qualidade do solo avaliada pelo “soil quality kit test” em dois experimentos de longa duração no Rio Grande do Sul. Revista Brasileira de Ciência do Solo, 31, 109-121. DOI: 10.1590/S0100-06832007000100012
Andreatta, L. F. O. K. M. (2013). Avaliação de toxicidade de três substâncias de referência ao microcrustáceo Daphnia magna. Monografia de conclusão de curso. Universidade Federal Tecnológica do Paraná, Curitiba, Brasil.
Babić, S., Barišić, J., Bielen, A., Bošnjak, I., Klobučar, R. S., Ujević, I., & Strunjak-Perović et al. (2016). Multilevel ecotoxicity assessment of environmentally relevant bisphenol A concentrations using the soil invertebrate Eisenia fetida. Journal Hazardous Materials, 15(318), 477-486. Doi: 10.1016/j.jhazmat.2016.07.017
Berg, G. L. (1984). Farm chemicals handbook. Willoughby, OH. 1st ed., Ohio USA: Meister Publishing Company; 1984.
Candello, F. P. (2014). Comportamento de fuga de minhocas na presença do antimicrobiano sulfadiazina em solo. Dissertação de mestrado. Programa de Pós-Graduação em Engenharia Civil. Universidade Estadual de Campinas, Campinas, Brasil.
Cantelli, K. B. (2011). Toxicidade aguda de carbofurano e carbendazim a minhocas em solo natural. Dissertação de mestrado. Programa de Pós-Graduação em Ciência do Solo. Universidade Federal do Paraná, Curitiba, Brasil.
Chen, Y., Yang, Y., Zhu, H., Romeis, J., Li, Y., Peng, Y., & Chen, X. (2018). Safety of Bacillus thuringiensis Cry1C protein for Daphnia magna based on different functional traits. Ecotoxicology and Environmental Safety, 147, 631-636. DOI: 10.1016/j.ecoenv.2017.08.065
Chini, P. (2014). Uso de minhocas da espécie Eisenia fetida, como bioindicadores em solos contaminados com agrotóxicos. Monografia de conclusão de curso. Universidade do Sul de Santa Catarina, Palhoça, SC.
Edwards, C. A., & Bohlen, P. J. (1996). Biology and ecology of earthworms. 3rd ed., London: Chapman & Hall.
Galzer, E. C. W., & Azevedo Filho, W. S. (2016). Utilização do Bacillus thuringiensis no controle biológico de pragas. Revista Interdisciplinar de Ciência Aplicada -USC, 01, 13-16.
Gao, Y. J., Zhu, H. J., Chen, Y., Li, Y. H., Peng, Y. F., & Chen, X. P. (2018). Safety assessment of Bacillus thuringiensis insecticidal proteins Cry1C and Cry2A with a zebrafish embryotoxicity test. Journal of Agricultural and Food Chemistry, 66(17), 4336-4344. DOI: 10.1021/acs.jafc.8b01070
Garcia, M., Römbke, J., Brito, M. T., & Scheffczyk, A. (2008). Effects of three pesticides on the avoidance behavior of earthworms in laboratory tests performed under temperate and tropical conditions. Environmental Pollution, 153(2), 450-456. DOI:10.1016/j.envpol.2007.08.007
García-Santos, G., & Keller-Forrer, K. (2011). Avoidance behaviour of Eisenia fetida to carbofuran, chlorpyrifos, mancozeb and metamidophos in natural soils from the highlands of Colombia. Chemosphere, 84(5), 651-656. DOI: 10.1016/j.chemosphere.2011.03.036
ISO - International Organization for Standardization. (2008). ISO 17512-1 – Soil quality: Avoidance test for determining the quality of soils and effects of chemicals on behavior – Part 1: Test with earthworms (Eisenia fetida and Eisenia andrei), ISO guideline: Geneva, Switzerland.
Klauck, C. R. (2018). Tratamento de efluente petroquímico: avaliação da toxicidade. Tese de doutorado. Programa de Pós-Graduação em Qualidade Ambiental. Universidade Feevale, Novo Hamburgo, Brasil.
Kuebutornye, F. K. A., Abarike, E. D., & Yishan, L. (2019). A review on the application of Bacillus as probiotics in aquaculture. Fish & Shellfish Immunology, 87, 820-828. DOI:10.1016/j.fsi.2019.02.010
Lima, N. C. (2010). Avaliação do impacto da contaminação do solo de áreas agrícolas de Bom Repouso (MG) por meio de ensaios ecotoxicológicos. Dissertação de mestrado. Programa de Pós-Graduação em Ciências da Engenharia Ambiental. Universidade de São Paulo, São Carlos, Brasil.
Lukkari, T., Aatsinki, M., Väisänen, A., & Haimi, J. (2005). Toxicity of copper and zinc assessed with three different earthworm tests. Applied Soil Ecology, 30(2), 133-146. DOI: 10.1016/j.apsoil.2005.02.001
Malajovich, M. A. (2012). Biotecnologia 2011. 3rd ed. Rio de Janeiro: Biblioteca Max Feffer do Instituto de Tecnologia ORT.
Mariano, W. S., Azevedo, S. B., Gomes, F. L., Lima, L. B. D., Moron, S. E., & Tavares-Dias, M. (2019). Physiological parameters of Piaractus mesopotamicus (Osteichthyes: Characidae) exposed to a biopesticide based on Bacillus thuringiensis. Anais da Academia Brasileira de Ciências, 91(2), e20180474. DOI: 10.1590/0001-3765201920180474
Niemeyer, J. C., Carniel, L. S. C., Pech, T. M., Crescencio, L. P., & Klauberg-Filho, O. (2018). Boric acid as a reference substance in avoidance behaviour tests with Porcellio dilatatus (Crustacea: Isopoda). Ecotoxicology and Environmental Safety, 161, 392-396. DOI: 10.1016/j.ecoenv.2018.05.058
Niva, C. C., & Brown, G. G. (2019). Ecotoxicologia terrestre: métodos e aplicações dos ensaios com oligoquetas. 1st ed. Brasília: Embrapa.
Nunes, M. E., & Espíndola, E.L. (2012). Sensitivity of Eisenia andrei (Annelida, Oligochaeta) to a commercial formulation of abamectin in avoidance tests with artificial substrate and natural soil under tropical conditions. Ecotoxicology, 21(4), 1063-1071. DOI: 10.1007/s10646-012-0859-6.
OECD - Organisation for Economic Co-operation and Development. (1984). Guideline N° 207 - Earthworm, Acute Toxicity Tests, Organization for Economic Co-operation and Development. (OECD): Paris, France.
Oliveira, V. B. M., Bianchi, M. O., & Espíndola, E. L. G. (2018). Hazard assessment of the pesticides KRAFT 36 EC and SCORE in a tropical natural soil using an ecotoxicological test battery. Environmental Toxicology and Chemistry,37(11), 2919–2924. DOI: 10.1002/etc.4056.
Pereira, P. C. G., Soares, L. O. S., Júnior, S. F. S., Saggioro, E. M., & Correia, F. V. (2019). Sub-lethal effects of the pesticide imazalil on the earthworm Eisenia andrei: reproduction, cytotoxicity, and oxidative stress. Environmental Science and Pollution Research International [published online ahead of print, 2019 May 22]. DOI: 10.1007/s11356-019-05440-3
Pino-Otín, M. R., Val, J., Ballestero, D., Navarro, E., Sánchez, E., González-Coloma, A., & Mainar, A. M. (2019). Ecotoxicity of a new biopesticide produced by Lavandula luisieri on non-target soil organisms from different trophic levels. Science of the Total Environment, 671, 83-93. DOI: 10.1016/j.scitotenv.2019.03.293
Roe, R. M., Kallapur, V. L., Dauterman, W. C., & Edens, F.W. (1991). Vertebrate toxicology of the solubilized parasporal crystalline proteins of Bacillus thuringiensis subsp. Israelensis. In: Hodgson, E.; Roe, R. M. & Motoyama, N. (Eds.) Pesticides and the Future: Toxicological Studies of Risks and Benefits. (pp.384) 1st ed. United States: North Carolina State University Press.
Römbke, J., Waichman, A. V., & Garcia, M. V. B. (2008). Risk assessment of pesticides for soils of the Central Amazon, Brazil: comparing outcomes with temperate and tropical data. Integrated Environmental Assessment and Management, 4(1), 94-104. DOI: 10.1897/ieam_2007-052.1.
Silva, M. (2009). Pesticide effects on earthworms: A tropical perspective. Enschede: Ipskamp Drukkers BV.
Sisinno, C. L. S., Bulus, M. R. M., Rizzo, A. C., & Moreira, J. C. (2006). Ensaio de comportamento com minhocas (Eisenia fetida) para avaliação de áreas contaminadas: resultados preliminares para contaminação por hidrocarbonetos. Journal of the Brazilian Society of Ecotoxicology, 1(2), 137-140. DOI: 10.5132/jbse.2006.02.009
Sousa, A. P. A. de, & Andréa, M. M. (2011). Earthworm (Eisenia andrei) avoidance of soils treated with cypermethrin. Sensors, 11(12), 11056-11063. DOI: 10.3390/s111211056
Vampré, T. M., Fuccillo, R., & Andréa, M. M. (2001). Oligocheta Eisenia andrei como bioindicador de contaminação de solo por hexaclorobenzeno. Revista Brasileira de Ciência do Solo, 34(1), 59-66. DOI: 10.1590/S0100-06832010000100006.
Hund-Rinke, K., & Wiechering, H. (2001). Earthworm avoidance test for soil assessments. Journal of Soils and Sediments, 1, 15–20. DOI: 10.1007/BF02986464
Venter, H. J., & Bøhn, T. (2016). Interactions between Bt crops and aquatic ecosystems: A review. Environmental Toxicology and Chemistry, 35, 2891–2902. DOI: 10.1002/etc.3583
Zhao, Z.; Li, Y., Xiao, Y., Ali, A., Dhiloo, K. H., Chen, W., & Wy, K. (2016). Distribution and metabolism of Bt-Cry1Ac toxin in tissues and organs of the cotton Bollworm, Helicoverpa armígera. Toxins, 8(7):pii212. DOI: 10.3390/toxins8070212
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