Histopathological changes in Lithobates catesbeianus tadpoles used as biomarkers of pesticide poisoning

Authors

  • Adriana Sacioto Marcantonio Agência Paulista de Tecnologia dos Agronegócios, Secretaria de Agricultura e Abastecimento – Pindamonhangaba (SP), Brazil. https://orcid.org/0000-0002-2897-577X
  • Fernanda Menezes França Fisheries Institute, Agência Paulista de Tecnologia dos Agronegócios, Secretaria de Agricultura e Abastecimento – São Paulo (SP), Brazil. https://orcid.org/0000-0002-6097-5366
  • Diego Sales Santos Fisheries Institute, Agência Paulista de Tecnologia dos Agronegócios, Secretaria de Agricultura e Abastecimento – São Paulo (SP), Brazil. https://orcid.org/0000-0002-4344-2111
  • Ana Mara Cristina Rebello Pinto Fonseca Martins Biological Institute, Agência Paulista de Tecnologia dos Agronegócios, Secretaria de Agricultura e Abastecimento – São Paulo (SP), Brasil . https://orcid.org/0000-0002-4061-0298
  • Márcio Hipólito Biological Institute, Agência Paulista de Tecnologia dos Agronegócios, Secretaria de Agricultura e Abastecimento – São Paulo (SP), Brasil . https://orcid.org/0000-0002-1932-8829
  • Sérgio Henrique Canello Schalch Agência Paulista de Tecnologia dos Agronegócios, Secretaria de Agricultura e Abastecimento – Pindamonhangaba (SP), Brazil. https://orcid.org/0000-0001-7960-6213
  • Cristina Viriato Institute of Biosciences, Universidade Estadual Paulista “Júlio de Mesquita Filho” – Botucatu (SP), Brazil. https://orcid.org/0000-0002-5208-9639
  • Cláudia Maris Ferreira Fisheries Institute, Agência Paulista de Tecnologia dos Agronegócios, Secretaria de Agricultura e Abastecimento – São Paulo (SP), Brazil. https://orcid.org/0000-0001-9549-4178

DOI:

https://doi.org/10.20950/1678-2305/bip.2022.48.e711

Keywords:

Amphibian, Biomarker, Ecotoxicology, Lithobates catesbeianus

Abstract

The use of biological indicators has increased in recent years with the aim of investigating environmental pollution in aquatic environments that are vulnerable to the constant use of pesticides. Some biomarkers can help assess the health status, indicating physical, metabolic, and behavioral changes under acute and sublethal poisoning. The mixture of the active ingredients cyproconazole and picoxystrobin is a widely used fungicide for the control of pests in cotton, rice, coffee, sugarcane, corn, soybean, and wheat. The objective of this study was to verify the occurrence of possible histopathological lesions in the liver and kidneys of bullfrog tadpoles (Lithobates catesbeianus) caused by a fungicide commercial formula composed of picoxystrobin and cyproconazole. The animals were subjected to different concentrations of the fungicide to determine the median lethal concentration (LC50-96h = 0.05 mg L-1), that is, the lethal dose for 50% of the animals in 96 h. After determining the value of LC50-96h, the animals were subjected to three sublethal concentrations (LC50-96h/2, LC50-96h/10, and LC50-96h/100). Through histological biomarkers, it was verified that this fungicide changed the morphology of the animals' kidney and liver tissues in a chronic way, impairing the functioning of organs that are essential for their survival and metamorphosis, which can result in an imbalance in the biodiversity of aquatic ecosystems.

References

Agência Nacional de Vigilância Sanitária (ANVISA). 2019. Alterações das classificações toxicológicas dos produtos formulados agrotóxicos e afins. ANVISA. Available at: https://alimentusconsultoria.com.br/wpcontent/uploads/2019/08/RESOLU%C3%87%C3%83O-RE-N%C2%BA-2.080-DE-31-DE-JULHO-DE-2019-ANVISA.pdf. Accessed on: Dec 12, 2022).

Agius, C. 1981. Preliminary Studies on the Ontogeny of the Melano-Macrophages of Teleost Haemopoietic Tissues and Age-Related Changes. Developmental & Comparative Immunology, 5(4): 597-606. https://doi.org/10.1016/S0145-305X(81)80034-1

Agius, C.; Roberts, R.J. 2003. Melano-macrophage centres and their role in fish pathology. Journal of Fish Biology, 26(9): 499-509. https://doi.org/10.1046/j.1365-2761.2003.00485.x

Amphibia. 2008. Impact of habitat degradation. Available at: https://amphibiaweb.org/declines/habitat.html. Accessed in: Sep, 2022.

ASTM E729-96. (2014). Standard Guide for Conducting Acute Toxicity Tests on Test Materials with Fishes, Macroinvertebrates, and Amphibians. West Conshohocken: ASTM International.

Bach, N.C.; Marino, D.J.G.; Natale, G.S.; Somoza, G.M. 2018. Effects of glyphosate and its commercial formulation, Roundup® Ultramax, on liver histology of tadpoles of the neotropical frog, Leptodactylus latrans (amphibia: Anura). Chemosphere, 202: 289-297. https://doi.org/10.1016/j.chemosphere.2018.03.110

Boncompagni, E.; Fenoglio, C.; Vaccarone, R.; Chiari, P.; Milanesi, G.; Fasola, M.; Barni, S. 2004. Toxicity of chromium and heptachlor epoxide on liver of Rana kl. esculenta: A morphological and histochemical study. Ecology & Ethology, 71(Suppl. 2): 163-167. https://doi.org/10.1080/11250000409356628

Çakici, Ö. 2015. Histopathologic changes in liver and kidney tissues induced bycarbaryl in Bufotes variabilis (Anura: Bufonidae). Experimental and Toxicologic Pathology, 67(3): 237-243. https://doi.org/10.1016/j.etp.2014.12.003

Césarini, J.P. 1996. Melanins and their possible roles through biological Evolution. Advances in Space Research, 18(12): 35-40. https://doi.org/10.1016/0273-1177(96)00025-7

Companhia Ambiental do Estado de São Paulo (CETESB). 2021. Diagnóstico da contaminação de águas superficiais, subterrâneas e sedimentos por agrotóxicos. Available at: https://cetesb.sp.gov.br/wp-content/uploads/2021/10/Diagnostico-da-Contaminacao-de-Aguas-Superficiais-Subterraneas-e-Sedimentos-por-Agrotoxicos_.pdf. Accessed on: Sep 16, 2022.

Costa, C.R.; Olivi, P.; Botta, C.M.; Espindola, E.L. 2008. A toxicidade em ambientes aquáticos: discussão e métodos de avaliação. Química Nova, 31(7): 1820-1830. https://doi.org/10.1590/S0100-40422008000700038

Crawshaw, G.J.; Weinkle, T.K. 2000. Clinical and pathological aspects of the amphibian liver. Journal of Exotic Pet Medicine, 9(3): 165-173. https://doi.org/10.1053/ax.2000.7133

Dufresnes, C. 2019. Amphibians of Europe, North Africa and the Middle East: A Photographic Guide. Bloomsbury Publishing, 224 p.

Fenoglio, C.; Boncompagni, E.; Fasola, M.; Fenoglio, C.; Boncompagni, E.; Fasola, M.; Gandini, C.; Comizzoli, S.; Milanesi, G. 2005. Effects of environmental pollution on the liver parenchymal cells and Kupffer-melanomacrophagic cells of the frog Rana esculenta. Ecotoxicology and Environmental Safety, 60(3): 259-268. https://doi.org/10.1016/j.ecoenv.2004.06.006

Fishelson, L. 2006. Cytomorphological alterations of the thymus, spleen, headkidney, and liver in cardinal fish (Apogonidae, Teleostei) as bioindicators of stress. Journal of Morphology, 267(1): 57-69. https://doi.org/10.1002/jmor.10385

França, F.M.; Brazil de Paiva, T.C.; Marcantonio, A.S.; Teixeira, P.C.; Ferreira, C.M. 2015. Acute toxicity and ecotoxicological risk assessment of rice pesticides to Lithobates catesbeianus tadpoles. Journal of Environmental Science and Health. Part B. Pesticides, Food Contaminants, and Agricultural Wastes, 50(6): 406-410. https://doi.org/10.1080/03601234.2015.1011950

Franco-Belussi, L.; Castrucci, A.M.L.; Oliveira, C. 2013. Responses of melanocytes and melanomacrophages of Eupemphix nattereri (Anura: Leiuperidae) to Nle4, D-Phe7-α-melanocyte stimulating hormone and lipopolysaccharides. Zoology, 116(5): 316-324. https://doi.org/10.1016/j.zool.2013.06.003

Gartner, L.P.; Hiatt, J.L. 1999. Tratado de histologia em cores. Rio de Janeiro: Guanabara Koogan S.A.

Giagnessi, L.; Reigner, N. 2006. Pesticide Use in U.S, Crop Production: 2002 With Comparison to 1992 & 1997, Fungicides and Herbicides. Washington, D.C.: Croplife Foundation.

Gosner, K.L. 1960. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16(3): 183-190.

Grott, S.C.; Israel, N.; Lima, D.; Bitschinski, D.; Abel, G.; Alves, T.C.; Silva, E.B.; Albuquerque, C.A.C.; Mattos, J.J.; Bainy, A.C.D.; Almeida, E.A. 2022. Influence of temperature on growth, development and thyroid metabolism of American bullfrog tadpoles (Lithobates catesbeianus) exposed to the herbicide tebuthiuron. Environmetal Toxicology and Pharmacology, 94: 103910. https://doi.org/10.1016/j.etap.2022.103910

Guyton, A.C.; Hall, J.E. 2002. Tratado de fisiologia médica. 10ª ed. Rio de Janeiro: Guanabara-Koogan.

Hamilton, M.A.; Russo, R.C.; Thurston, R.V. 1977. Trimmed Spearman Karber method for estimating median lethal concentrations in toxicity bioassays. Environmental Science & Technology, 11(7): 714-719. https://doi.org/10.1021/es60130a004

Hipolito, M.; Martins, A.M.C.R.P.F.; Bach, E.E. 2004. Aspectos bioquímicos em fígado de rãs-touro (Rana catesbeiana Shaw, 1802) sadias e doentes. Arquivos do Instituto Biológico, 71(2): 147-153.

Jayawardena, U.A.; Mangunawela, P.; Wickramasinghe, D.D.; Ratnasooriya, W.D.; Udagama, P.V. 2017. Heavy metal–induced toxicity in the Indian green frog: Biochemical and histopathological alterations. Environmental Toxicology and Chemistry, 36(10): 2855-2867. https://doi.org/10.1002/etc.3848

Jha, A.N. 2008. Ecotoxicological applications and significance of the comet assay. Mutagenesis, 23(3): 207-221. https://doi.org/10.1093/mutage/gen014

Kranz, H. 1989. Changes in Splenic Melano-Macrophages Centres of Dab, Limanda limanda During and After Infection with Ulcer Disease. Disease of Aquatic Organisms, 6: 167-173.

Manso, P.P.A.; Brito-Gitirana, L.; Pelajo-Machado, M. 2009. Localization of hematopoietic cells in the bullfrog (Lithobates catesbeianus). Cell and Tissue Research, 337: 301-312. https://doi.org/10.1007/s00441-009-0803-0

Medina, M.F.; Gonzalez, M.E.; Klyver, S.M.R.; Aybar Odstrcil, I.M. 2016. Histopathological and biochemical changes in the liver, kidney, and blood of amphibians intoxicated with cadmium. Turkish Journal of Biology, 40: 229-238. https://doi.org/10.3906/biy-1505-72

Miaud, C.; Dejean, T.; Savard, K.; Millery-Vigues, A.; Valentibi, A.; Gaudin, N.C.G.; Garner, T.W. 2016. Invasive North American bullfrogs transmit lethal fungus Batrachochytrium dendrobatidis. Biological Invasions, 18(8): 2299-2308. https://doi.org/10.1007/s10530-016-1161-y

Mikó, Z.; Ujszegi, J.; Gál, Z.; Hettyey, A. 2017. Standardize or Diversify Experimental Conditions in Ecotoxicology? A Case Study on Herbicide Toxicity to Larvae of Two Anuran Amphibians. Archives of Environmental Contamination Toxicology, 73: 562-569. https://doi.org/10.1007/s00244-017-0427-4

Ministério da Agricultura, Pecuária e Abastecimento (MAPA). 2022. Agrofit: Sistema de Agrotóxicos Fitossanitários. Consulta de Ingrediente Ativo. Brasil: MAPA.

Monteiro, J.A.N.; Cunha, L.A.; Costa, M.H.P.; Reis, H.S.; Aguiara, A.C.S.; Oliveira-Bahia, V.R.L.; Burbano Rocha, C.A.M. 2018. Mutagenic and histopathological effects of hexavalent chromium in tadpoles of Lithobates catesbeianus (Shaw, 1802) (Anura, Ranidae). Ecotoxicology Environmental Safety, 163: 400-407. https://doi.org/10.1016/j.ecoenv.2018.07.083

Nkontcheu, D.B.K.; Tchamadeu, N.N.; Ngealekeleoh, F.; Nchase, S. 2017. Ecotoxicological Effects of Imidacloprid and Lambda-Cyhalothrin (Insecticide) on Tadpoles of the African Common Toad, Amietophrynus Regularis (Reuss, 1833) (Amphibia: Bufonidae). Italian Journal of Science & Engineering, 1(2): 49-53.

Ossana, N.A.; Castañé, P.M.; Salibián, A. 2013. Use of Lithobates catesbeianus tadpoles in a multiple biomarker approach for the assessment of water quality of the Reconquista river (Argentina). Archives of Environmental Contamination and Toxicology, 65(3): 486-497. https://doi.org/10.1007/s00244-013-9920-6

Paetow, L.J.; McLaughlin, J.D.; Cue, R.I.; Pauli, B.D.; Marcogliese, D.J. 2012. Effects of herbicides and the chytrid fungus Batrachochytrium dendrobatidis on the health of post-metamorphic northern leopard frogs (Lithobates pipiens). Ecotoxicology Environmental Safety, 80: 372-380. https://doi.org/10.1016/j.ecoenv.2012.04.006

Passantino, L.; Santamaria, N.; Zupa, R.; Pousis, C.; Garofalo, R.; Cianciotta, A.; Jirillo, E.; Acone, F.; Corriero, A. 2014. Liver melanomacrophage centres as indicators of Atlantic bluefin tuna, Thunnus thynnus L. well‐being. Journal of Fish Diseases, 37(3): 241-250. https://doi.org/10.1111/jfd.12102

Pinto-Vidal, F.A.; Carvalho, C.S.; Abdalla, F.A.; Utsunomiya, H.S.M.; Salla, R.F.; Jone-Costa, M. 2022. Effects of lithium and selenium in the tail muscle of American bullfrog tadpoles (Lithobates catesbeianus) during premetamorphosis Environmental Science and Pollution Research, 29: 1975-1984. https://doi.org/10.1007/s11356-021-15686-5

Pontes, J.R.S.; Lopes, I.; Ribeiro, R.; Araújo, CV.M. 2022. Humane acute testing with tadpoles for risk assessment of chemicals: Avoidance instead of lethality. Chemosphere, 303(Part 3): 135197. https://doi.org/10.1016/j.chemosphere.2022.135197

Santos, L.R.S.; Franco-Belussi, L.; Zieri, R.; Borges, R.E.; Oliveira, C. 2014. Effects of Thermal Stress on Hepatic Melanomacrophages of Eupemphix nattereri (Anura). The Anatomical Record, 297(5): 864-875. https://doi.org/10.1002/ar.22884

United Nations. 2011. Globally harmonized system of classification and labelling of chemicals. New York: United Nations. Available at: https://www.unece.org/fileadmin/DAM/trans/danger/publi/ghs/ghs_rev04/English/ST-SG-AC10-30-Rev4e.pdf. Accessed on: Sep 16, 2022.

Verdade, V.K.; Dixo, M.; Curcio, F.F. 2010. Risks of Extinction of Frogs and Toads as a Result of Environmental Changes. Estudos Avançados, 24(68): 161-172. https://doi.org/10.1590/S0103-40142010000100014

Viriato, C.; França, F.M.; Santos, D.S.; Marcantonio, A.S.; Badaró-Pedroso, C.; Ferreira, C.M. 2021. Evaluation of the potential teratogenic and toxic effect of the herbicide 2,4-D (DMA® 806) in bullfrog embryos and tadpoles (Lithobates catesbeianus). Chemosphere, 266: 129018. https://doi.org/10.1016/j.chemosphere.2020.129018

Zuasti, A.; Jiménez-Cervantes, C.; García-Borrón, J.C.; Ferrer, C. 1998. The melanogenic system of Xenopus laevis. Archives of Histology and Cytology, 61(4): 305-316. https://doi.org/10.1679/aohc.61.305

Downloads

Published

2023-02-09

Issue

Vol. 48 (2022): BOLETIM DO INSTITUTO DE PESCA

Section

Scientific Article

License

Copyright (c) 2023 Boletim do Instituto de Pesca

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Most read articles by the same author(s)

1 2 > >>