Toxicity assessment of a comercial Bacillus thuringiensis-based insecticide on Nile tilápia, Oreochromis niloticus

Authors

DOI:

https://doi.org/10.33448/rsd-v10i8.16775

Keywords:

biomarker; nuclear alteration; histophatology; Cytotoxicity; Teleost.

Abstract

Biopesticides are used as an alternative to synthetic chemical pesticides application. Formulations based on Bacillus thuringiensis (Bt) spores are widely used, however, little is known about their effects on aquatic biota. The aim of the study was to evaluate the genotoxic and histopathological effects of a sublethal concentration of a commercial Bt-based biopesticide on Oreochromis niloticus. The fish were divided (n = 10) into a control group (CG) and an exposed group (GBt) at a concentration of 60 mg L-1 of the biopesticide Dipel® WP for 48 hours. After exposure, blood, gill, liver and kidney samples were collected for analysis of toxicity biomarkers. The results demonstrate that an acute exposure to Bt induces the increase of erythrocyte nuclei with segmented morphology. No micronucleus induction was observed. Histopathological analysis showed that within 48 hours of exposure, in GBt, there was a decrease in the frequency of hypertrophied hepatocytes. However, the biopesticide did not compromise tissue morphology in acute toxicity. Pesticides in general are constantly applied and usage regulations are not widely followed, our results suggest that sublethal concentrations can induce effects when exposed acutely. Biopesticides based on Bt in low concentrations appear to be less toxic to fish.

References

Artega, M. E., Mancebo, A., Molier, T., Gómez, D., González, C., Bada, A. M., González, B., Rojas, N. M., & Rodríguez, G. (2014). Dermal toxicity, eye and dermal irritation and skin sensitization evaluation of a new formulation of Bacillus thuringiensis var israelensis SH-14. Regulatory Toxicology and Pharmacology, 68, 147 – 151. 10.1016/j.yrtph.2013.12.003

Ayllón, F., & Garcia-Vazquez, E. (2000). Induction of micronuclei and other nuclear abnormalities in European minnow Phoxinus phoxinus and mollie Poecilia latipinna: An assessment of the fish micronucleus test. Mutation Research, 467, 177 – 186. 10.1016/s1383-5718(00)00033-4

Azevedo, J. S., Braga, E. S., & Ribeiro, C. A. O. (2012). Nuclear abnormalities in erythrocytes and morphometric indexes in the catfish Cathorops spixii (Ariidae) from different sites on the southeastern Brazilian coast. Brazilian Journal of Oceanography, 60(3), 323 – 330. https://www.scielo.br/j/bjoce/a/585HvcPvQhXCCrjM8hPPzpc/?lang=en

Benli, A. Ç. K., & Özkul, A. (2010). Acute toxicity and histopathological effects of sublethal fenitrothion on Nile tilapia, Oreochromis niloticus. Pesticide Biochemistry and Physiology, 97, 32 – 35. 10.1016/j.pestbp.2009.12.001

Bernet, D., Schmidt, H., Meier, W., Burkhardt-Holm, P., & Wahli, R. (1999). Histopathology in fish: proposal for a protocol to assess aquatic pollution. Journal of Fish Diseases, 22, 25 – 34. 10.1046/j.1365-2761.1999.00134.x

Bravo, A., Likitvivatanavong, S., Gill, S. S., & Soberón, M. (2011). Bacillus thuringiensis: A story of a successful bioinsecticide. Insect Biochemistry and Molecular Biology, 41(7), 423 – 431. 10.1016/j.ibmb.2011.02.006

Camargo, M. M. P., & Martinez, C. B. R. (2007). Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream. Neotropical Ichthyology, 5(3), 327 – 336. 10.1590/S1679-62252007000300013

Carrasco, K. R., Tilbury, K. L., & Myers, M. S. (1990). Assessment of the piscine micronucleus test as an in situ biological indicator of chemical contaminant effects. Canadian Journal of Fisheries and Aquatic Sciences, 47(11), 2123 – 2136. 10.1139/f90-237

Cavalcante, D., Martinez, C., & Sofia, S. (2008). Genotoxic effects of Roundup® on the fish Prochilodus lineatus. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 655, 41 – 46. 10.1016/j.mrgentox.2008.06.010

Chaudhary, S., Kanwar, R. K., Sehgal, A., Cahill, D. M., Barrow, C. J., Sehgal, R., & Kanwar, J. R. (2017). Progress on Azadirachta indica based biopesticides in replacing synthetic toxic pesticides. Frontiers in Plant Science, 8, 1 – 13. 10.3389/fpls.2017.00610

Chen, J., Zhu, N., Kong, L., Bei, Y., Zheng, T., Ding, X., & He, Z. (2014). First reported fatal Bacillus thuringiensis infections in Chinese soft-shelled turtles (Trionyx sinensis). Aquaculture, 428-429, 16 – 20. DOI: 10.1159/000479795

Copping, L. G., & Menn, J. J. (2000). Biopesticides: a review of their action, applications and efficacy. Pest Management Science, 56, 651 – 676. 10.1002/1526-4998(200008)56:8<651::AID-PS201>3.0.CO;2-U

Cruz, C., Machado-Neto, J. G., & Menezes, M. L. D. (2004). Toxicidade aguda do inseticida parationmetílico e do biopesticida azadiractina de folhas de neem (Azadirachta indica) para alevino e juvenil de pacu (Piaractus mesopotamicus). Pesticidas: Revista de Ecotoxicologia e Meio Ambiente, 14, 93 – 102. 10.5380/pes.v14i0.3127

Del-Guercio, A. M. F., Christofoletti, C. A., & Fontanetti, C. S. (2017). Evaluation of the domestic wastewater treatment efficiency by micronucleus test on Oreochromis niloticus (Cichlidae). Eng Sanit Ambient, 22(6), 1121-1128. 10.1590/S1413-4152201773709

Devine, G. J., & Furlong, M. J. (2007). Insecticide use: Contexts and ecological consequences. Agriculture and Human Values, 24, 281 – 306. 10.1007/s10460-007-9067-z

Disner, G. R., Rocha, M. V., & Miranda, G. B. (2011). Avaliação da atividade mutagênica do Roundup® em Astyanax altiparanae (Chordata, Actinopterygii). Evidência, Joaçaba. 11(1) 33-42. https://portalperiodicos.unoesc.edu.br/evidencia/article/view/1384

Douville, M., Gagné, F., Masson, L., McKay, J., & Blaise, C. (2005). Tracking the source of Bacillus thuringiensis Cry1Ab endotoxin in the environment. Biochemical Systematics and Ecology, 33, 219 – 232. 10.1016/j.bse.2004.08.001

Fanta, E., Rios, F. S., Romão, S., Vianna, A. C. C., & Freiberger, S. (2003). Histopathology of the fish Corydoras paleatus contaminated with sublethal levels of organophosphorus in water and food. Ecotoxicology and Environmental Safety, 54(2), 119 – 130. 10.1016/s0147-6513(02)00044-1

Freire, I. S., Miranda-Vilela, A. L., Fascineli, M. L., Oliveira-Filho, E. C., Martins, E. S., Monnerat, R. G., & Grisolia, C. K. (2014). Genotoxic evaluation in Oreochromis niloticus (Fish: Characidae) of recombinant spore–crystal complexes Cry1Ia, Cry10Aa and Cry1Ba6 from Bacillus thuringiensis. Ecotoxicology, 23, 267 – 272. 10.1007/s10646-013-1170-x

Glare, T., Caradus, J., Gelernter, W., Jackson, T., Keyhani, N., Köhl, J., Marrone, P., Morin, L., & Stewart, A. (2012). Have biopesticides come of age? Trends in Biotechnology, 30(5), 250 – 258. 10.1016/j.tibtech.2012.01.003

Grisolia, C. K., Oliveira-Filho, E. C., Ramos, F. R., Lopes, M. C., Muniz, D. H. F., & Monnerat, R. G. (2009). Acute toxicity and cytotoxicity of Bacillus thuringiensis and Bacillus sphaericus strains on fish and mouse bone marrow. Ecotoxicology, 18, 22 – 26. DOI 10.1007/s10646-008-0252-7

Hooftman, R. N., & de Raat, W. K. (1982). Induction of nuclear anomalies (micronuclei) in the peripheral blood erythrocytes of the eastern mudminnow Umbra pygmaea by ethyl methanesulphonate. Mutation Research Letters, 104(1-3), 147 – 152. 10.1016/0165-7992(82)90136-1

Kitada, S., Abe, Y., Shimada, H., Kusaka, Y., Matsuo, Y., Katayama, H., Okumura, S., Akao, T., Mizuki, E., Kuge, O., Sasaguri, Y., Ohba, M., & Ito, A. (2006). Cytocidal actions of parasporin-2, an anti-tumor crystal toxin from Bacillus thuringiensis. The Journal of Biological Chemistry, 281(36), 26350 – 26350. 10.1074/jbc.M602589200

Liebel, S., Tomotake, M. E. M., & Ribeiro, C. A. O. (2013). Fish histopathology as biomarker to evaluate water quality. Ecotoxicology and Environmental Contamination, 8(2), 09 – 15. https://doi.org/10.5132/eec.2013.02.002

Lins, J. A. P. N., Kirschnik, P. G., Queiroz, V. S., & Cirio, S. M. (2010). Uso de peixes como biomarcadores para monitoramento ambiental aquático. Revista Acadêmica: Ciências Agrárias e Ambientais, 8(4), 469 – 484. http://dx.doi.org/10.7213/cienciaanimal.v8i4.11018

Mariano, W. S., Azevedo, S. B., Gomes, F. L., Lima, L. B., 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). 10.1590/0001-3765201920180474

Martins, E. S., Aguiar, R. W. S., Martins, N. F., Melatti, V. M., Falcão, R., & Gomes, A. C. M. M., Ribeiro, B. M., & Monnerat, R. G. (2008). Recombinant Cry1Ia protein is highly toxic to cotton boll weevil (Nathonomus grandis Boheman) nad fall armyworm (Spodoptera frugiperda). Journal of Applied Microbiology, 104, 1363 – 1371. 10.1111/j.1365-2672.2007.03665x

Meher, S. M., Bodhankar, S. L., Arunkumar, Dhuley, J. N., Khodape, D. J., & Naik, S. R. (2002). Toxicity studies of microbial insecticide Bacillus thuringiensis var. kenyae in rats, rabbits, and fish. Intenational Journal of Toxicology, 21, 99 – 105. /10.1080/10915810252866079

Moraes, F. D., Venturini, F. P., Rossi, P. A., Avilez, I. M., Souza, N. E. S., & Moraes, G. (2018). Assessment of biomarkers in the neotropical fish Brycon amazonicus exposed to cypermethrin-based insecticide. Ecotoxicology, 27, 188 – 197. https://link.springer.com/article/10.1007/s10646-017-1884-2

Mossa, A-T. H., Mohafrash, S. M. M., & Chandrasekaran, N. (2018). Safety of natural insecticides: toxic effects on experimental animals. BioMed Research International. 10.1155/2018/4308054

Murussi, C. R., Menezes, C. C., Nunes, M. E. M., Araújo, M. C. S., Quadros, V. A., Rosemberg, D. B., & Loro, V. L. (2015). Azadirachtin, a neem-derived biopesticide, impairs behavioral and hematological parameters in carp (Cyprinus carpio). Environmental Toxicology, 31(11), 1381 – 1388. 10.1002/tox.22143

Oliveira, A. R., Castro, T. R., Capalbo, D. M. F., & Delalibera Jr., I. (2007). Toxicological evaluation of genetically modified cotton (Bollgard®) and Dipel® WP on the non-target soil mite Scheloribates praeincisus (Acari: Oribatida). Experimental and Applied Acarology, 41, 191 – 201. 10.1007/s10493-007-9059-0

Oliveira-Filho, E. C. (2008). Avaliação da periculosidade ambiental de bioinseticidas como uma nova perspectiva para a ecotoxicologia no Brasil. Journal of the Brazilian Society of Ecotoxicology, 3(1), 1 – 7. 10.5132/JBSE.2008.01.001

Omoya, F. O., & Akharaiyi, F. C. (2015). Physiological changes in Clarias gariepinus induced with Bacillus species used as biological agent in aquatic environment. Journal of Scientific Research & Reports, 7(2), 117 – 128. 10.9734/JSRR/2015/8711

Pacheco, M., & Santos, M. A. (2002). Biotransformation, genotoxic, and histopathological effects of environmental contaminants in European eel (Anguilla anguilla L.). Ecotoxicology and Environmental Safety, 53(3), 331 – 347. 10.1016/s0147-6513(02)00017-9

Paulino, M. G., Tavares, D., Terezan, A. P., Sakuragui, M. M., Posenti, E., Giani, A., Cestari, M. M., Fernandes, J, B., & Fernandes, M. N (2020). Biotransformations, Antioxidant System Responses, and Histopathological Indexes in the Liver of Fish Exposed to Cyanobacterial Extract. Environmental Toxicology and Chemistry, v.39, n. 5, 1041–1051. 10.1002/etc.4696

Pino-Otín, M. R., Ballestero, D., Navarro, E., González-Coloma, A., Val, J., & Mainar, A. M. (2019). Ecotoxicity of a novel biopesticide from Artemisia absinthium on non-target aquatic organisms. Chemosphere, 216, 131 – 146. 10.1016/j.chemosphere.2018.09.071

Ranzani-Paiva, M. J. T., Lombardi, J. V., Maiorino, F. C., Gonçalves, A., & Dias, D. C. (2014). Hematologia e histopatologia de tilápia-do-nilo exposta a concentrações sub-letais de selenito de sódio (Na2SeO3 Se4+). Boletim do Instituto de Pesca, 40(1), 23 – 33. https://www.pesca.agricultura.sp.gov.br/boletim/index.php/bip/article/view/1017

Sadauskas-Henrique, H., Sakuragui, M. M., Paulino, M. G., & Fernandes, M. N. (2010). Using condition factor and blood variable biomarkers in fish to assess water quality. Environ Monit Assess, 181, 29–42 10.1007/s10661-010-1810-z

Santos, R. F. B., Dias, H. M., & Fujimoto, R. Y. (2012). Acute toxicity and histopathology in ornamental fish amazon bluespotted corydora (Corydoras melanistius) exposed to formalin. Anais da Academia Brasileira de Ciências, 84(4). 10.1590/S0001-37652012000400014

Schweizer, M., Miksch, L., Köhler, H., & Triebskorn, R. (2019). Does Bti (Bacillus thuringiensis var. israelensis) affect Rana temporaria tadpoles? Ecotoxicology and Environmental Safety, 181, 121 – 129. 10.1016/j.ecoenv.2019.05.080

Shaban, N. Z., Helmy, M. H., El-Kersh, M. A. R., & Mahmoud, B. F. (2003). Effects of Bacillus thuringiensis toxin on hepatic lipid peroxidation and free-radical scavengers in rat given alpha-tocopherol or acetylsalicylate. Comparative Biochemistry and Physiology Part C, 135, 405 – 414. 10.1016/s1532-0456(03)00142-x

Sharma, N., & Singhvi, R. (2017). Effects of Chemical Fertilizers and Pesticides on Human Health and Environment: A Review. International Journal of Agriculture, Environment and Biotechnology, 10(6), 675-679. 10.5958/2230-732X.2017.00083.3

Silva, A. G., & Martinez, C. B. R. (2007). Morphological changes in the kidney of a fish living in an urban stream. Environmental Toxicology and Pharmacology, 23, 185 – 192. 10.1016/j.etap.2006.08.009

Silva, J. M., & Santos, J. R. (2007). Toxicologia de agrotóxicos em ambientes aquáticos. Oecologia Brasiliensis, 11(4), 565 – 573.

Udroiu, I. (2006). The micronucleus test in piscine erythrocytes. Aquatic Ecotoxicology, 79, 201 – 204. 10.1016/j.aquatox.2006.06.013

Venter, H. J., & Bohn, T. (2016). Interactions between Bt crops and aquatic ecosystems: a review. Environmental Toxicology and Chemistry, 35(12), 2891 – 2902. 10.1002/etc.3583

Ventura, B. C., Angelis, D. F., & Marin-Morales, M. A. (2008). Mutagenic and genotoxic effects of the Atrazine herbicide in Oreochromis niloticus (Perciformes, Cichlidae) detected by the micronuclei test and the comet assay. Pesticide Biochemistry and Physiology, 90, 42 – 51. 10.1016/j.pestbp.2007.07.009

Vieira, C. E. D., Costa, P. G., Cabrera, L. C., Primel, E. G., Fillmann, G., Bianchini, A., & Martinez, C. B. R. (2017). A comparative approach using biomarkers in feral and caged Neotropical fish: Implications for biomonitoring freshwater ecosystems in agricultural areas. Science of the Total Environment, 586, 598 – 609. 10.1016/j.scitotenv.2017.02.026

Villaverde, J. J., Sevilla-Morán, B., Sandín-España, P., López-Goti, C., & Alonso-Prados, J. L. (2014). Biopesticides in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Management Science, 70, 2 – 5. 10.1002/ps.3663

Wolf, J. C., Baumgartner, W. A., Blazer, V. S., Camus, A. C., Engelhardt, J. A., Fournie, J. W., Frasca Jr., S., Groman, D. B., Kent, M. L., Khoo, L. H., Law, J. M., Lombardini, E. D., Ruehl-Fehlert, C., Segner, H. E., Smith, S. A., Spitsbergen, J. M., Weber, K., & Wolfe, M. J. (2015). Nonlesions, misdiagnoses, missed diagnoses, and other interpretive challenges in fish histopathology studies: a guide for investigators, authors, reviewers, and readers. Toxicologic Pathology, 43(3), 297 – 325. 10. 1177/0192623314540229.

Wolf, J. C., & Wolfe, M. J. (2005). A brief overview of nonneoplastic hepatic toxicity in fish. Toxicologic Pathology, 33(1), 75 – 85. 10.1080/01926230590890187

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04/07/2021

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SIMÃO, A. M. T.; SILVA, D. do C. da .; SOARES, M. A. M.; DIAS, G. V. B. .; FERREIRA, E. R. R.; MORON, S. E.; MARIANO, W. dos S.; PAULINO, M. G. Toxicity assessment of a comercial Bacillus thuringiensis-based insecticide on Nile tilápia, Oreochromis niloticus. Research, Society and Development, [S. l.], v. 10, n. 8, p. e2910816775, 2021. DOI: 10.33448/rsd-v10i8.16775. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/16775. Acesso em: 22 nov. 2024.

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Vol. 10 No. 8

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Agrarian and Biological Sciences

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Copyright (c) 2021 Alexia Marta Turchetto Simão; Ducilene do Carmo da Silva; Marco Aurélio Miranda Soares; Geraldo Vinícius Barbosa Dias; Ericsson Rubens Rodrigues Ferreira; Sandro Estevan Moron; Wagner dos Santos Mariano; Marcelo Gustavo Paulino

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