Mutagenic biomarkers in erythrocytes of free-ranging and captive Kinosternon scorpioides from the Brazilian Amazon

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DOI:

https://doi.org/10.1590/1809-6891v26e-81855E

Abstract

This study aimed to investigate the occurrence of micronuclei (MN) and erythrocyte nuclear abnormalities (ENAs) in natural and captive Kinosternon scorpioides populations and compare their frequencies with the environment type, sex, and seasonal period in an environmental protection area in the state of Maranhão, Amazon. Blood was collected from 112 specimens from regions with direct anthropogenic influence and indirect and control areas to produce blood smears for subsequent cytological analysis under an optical microscope. We found MN (N=91) and ENAs such as binucleated nuclei (N=14), notched (N=81), lobulated (N=35), segmented (N=16), and displaced (N=253) in animals in situ. No abnormalities were recorded in the erythrocytes of the captive specimens. The mean (±standard deviation) MN (1.13±0.47) differed from those of the other chelonians from the natural environment, and the displaced and binucleated nuclei manifested themselves at higher (51.6%) and lower (2.8%) frequencies, respectively. Lobulated nuclei frequency was significantly different between the areas (p<0.05); segmented nuclei (p<0.05) and displaced (p<0.05) had higher frequencies during the dry and rainy periods. Sex did not affect these abnormalities. No significant MN were found; however, erythrocytes with lobulated, segmented, and displaced nuclei were documented in animals from different environments and seasonal periods. Our study provides pioneering data on MN and nuclear anomalies in the erythrocytes of K. scorpioides and confirms the significant differences and relationships between them. The occurrence of abnormalities in wild animals demonstrates the need to maintain protected areas and the continuity of conservation actions aimed at Amazonian turtles. This contributes to reducing the impact on conservation units that employ the sustainable use of biodiversity in Brazil.

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References

Cabrera MR, Colantonio SE. 1997. Taxonomic revision of the South American subspecies of the turtle Kinosternon scorpioides. Journal Herpetology. 1997; 31:507-513. Available from: https://doi.org/10.2307/1565602

Medeiros AM, Rodrigues CAL, Pereira EP, Cunha FAG, Ferreira DIS, Chaves EP, Chaves LPFA, Lima BC, Pereira LA, Sousa AL. Reproductive biology and habitat characterization of the Scorpion Mud Turtle Kinosternon scorpioides (Linnaeus, 1776) in the Amazon-Cerrado ecotone region, northeastern Brasil. Brazilian Journal of Biology. 2024; 84(e285306):1-13. Available from: https://doi.org/10.1590/1519-6984.285306

Júnior GS, Balestra RAM, Luz VLF. Breve histórico da conservação dos quelônios amazônicos no Brasil. In: Balestra RAM. Manejo conservacionista e monitoramento populacional de quelônios amazônicos. Brasília: Ibama, p. 11-14, 2016.Available from: https://www.ibama.gov.br/sophia/cnia/livros/PANqueloniosamazonicos.pdf

Pereira LA, Sousa AL, Cutrim MVJ, Moreira EG. Características ecológicas do habitat de Kinosternon Scorpioides scorpioides Linnaeus, 1766 (Reptila, Chelonia, Kinosternidae) no município de São Bento – Baixada Maranhense (Maranhão, Brasil). Boletim do Laboratório de Hidrobiologia. 2007; 20:9-14. Available from: https://cajapio.ufma.br/index.php/blabohidro/article/view/2026

Valente D, Costa AIC, Carvalho LVB, Dos Santos MVC, Castro VS, Rodrigues DRF, De Falco A. Utilização de biomarcadores de genotoxidade e expressão gênica na avaliação de trabalhadores de postos de combustíveis expostos a vapores de gasolina. Revista Brasileira de Saúde Ocupacional. 2017; 42(suplemento 1):1-21. Available from: https://doi.org/10.1590/2317-6369000124415

Matson CW, Palatnikov G, Izlamzadeh A, Mc Donald TJ, Autenrieth RL, Donnelly KC, Bickham JW. 2005. Chromosomal damage in two Species of aquatic turtles (Emys orbicularis and Mauremys caspica) inhabiting contaminated sites in Azerbaijan. Ecotoxicology. 2005; 14, 1-13. Available from: https://doi.org/10.1007/s10646-005-0001-0

Ryan PB, Burke TA, Hubal EAC, Cura JJ, McKone TE. Using Biomarkers to Inform Cumulative Risk Assessment. Environmental Health Perspectives. 2007; 115, 833-840. Available from: https://pmc.ncbi.nlm.nih.gov/articles/PMC1867975/

Ramsdorf WA, Vicari T, Almeida MIM, Artoni RF, Cestari MM. 2012. Handlingof Astyanax sp, for biomonitoring in Cangüiri Farm within a fountainhead (Iraí River Environment Preservation Area) through the use of genetic biomarkers. Environmental Monitoring and Assessment. 2012; 184, 5841-5849. Available from: https://doi.org/10.1007/s10661-012-2752-4

Flores M, Yamaguchi MU. Teste do micronúcleo: uma triagem para avaliação genotóxica. Revista Saúde e Pesquisa. 2008; 1(3):337-340. Available from: https://periodicos.unicesumar.edu.br/index.php/saudpesq/article/view/907

Obiakor M, Okonkwo JC, Nnabude P, Ezeonyejiaku CD. Eco-ecotoxicology: micronucleus assay in fish erythrocytes as in situ aquatic pollution. Journal of Animal Science Advances. 2012; 2:123-133. Available from: https://api.semanticscholar.org/CorpusID:33690814

Moll D, Moll EO. The ecology, exploitation and conservation of river turtles. New York: Oxford University Press, 2004; 393p. Available from: https://doi.org/10.1093/oso/9780195102291.001.0001

Ministério do Meio Ambiente (MMA), Lista Ramsar – Sítios Ramsar no Brasil. 2000. Available from: https://rsis.ramsar.org/ris/1020

Brasil. Decreto nº. 5.758, de 13 de abril de 2006, que institui o Plano Nacional Estratégico de Áreas Protegidas, Brasília: Diário Oficial. Available from: https://www.planalto.gov.br/ccivil_03/_Ato2004-2006/2006/Decreto/D5758.htm

Martinhão DGS, Lobato E. 2004. Cerrado – Correção do Solo e Adubação. Brasília, DF: Embrapa Informação Tecnológica, 2004, 416p. Available from: https://www.embrapa.br/busca-de-publicacoes/-/publicacao/555355/cerrado-correcao-do-solo-e-adubacao

Grisolia CK, Rivero CLG, Starling FLRM, Silva ICR, Barbosa AC, Dorea JG. Profile of micronucleus frequencies and DNA damage in different species of fish in a eutrophic tropical lake. Genetics and Molecular Biology. 2009; 32:138– 143. Available from: https://doi.org/10.1590/S1415-47572009005000009

Fonseca LA. Biomarcadores de estresse e carcinogênese: um estudo em Chelonia mydas. Vitoria: Universidade Federal do Espírito Santo, 2014. Tese de Doutorado em Ciências Biológicas. Available from: https://repositorio.ufes.br/server/api/core/bitstreams/d92f0833-e498-4015-8182-207d119b1be2/content

Brasil. Resolução CONAMA nº. 357, de 17 de março de 2005. Publicada no Diário Oficial nº. 53 em 18 de março de 2005. Available from: https://www.siam.mg.gov.br/sla/download.pdf?idNorma=2747

Brasil. Resolução CONAMA nº. 430, de 13 de maio de 2011. Publicada no Diário Oficial nº. 92 em 16 de maio de 2011. Available from: https://conama.mma.gov.br/?option=com_sisconama&view=processo&id=1835

Prezotti LC, Guarçoni AM. 2013. Guia de interpretação de análise de solo e foliar. Vitória: Incaper, 2013, 104 p. Available from: https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/1042994/1/Doc206.pdf

Zapata LM, Bock BC, Orozco LY, Palacio JA. Application of the micronucleus test and comet assay in Trachemys callirostris erythrocytes as a model for in situ genotoxic monitoring. Ecotoxicology Environmental Safety. 2016; 127:108–116. Available from: https://doi.org/10.1016/j.ecoenv.2016.01.016

Latorre MA, López González EC, Siroski PA, Poletta GL. Basal frequency of micronuclei and hematological parameters in the Side-necked Turtle, Phrynops hilarii (Duméril & Bibron, 1835). Acta Herpetologica. 2015; 10-1:31-37. Available from: https://doi.org/10.13128/Acta_Herpetol-14988

Frossard A, Vieira LV, Carneiro MTWD, Gomes LC, Chippari-Gomes AR. 2020. Accumulation of trace metals in eggs and hatchlings of Chelonia mydas. Journal of Trace Elements in Medicine and Biology. 2020; 62:126654. Available from: https://doi.org/10.1016/j.jtemb.2020.126654

Silva CC, Klein RD, Barcarolli IF, Niachini A. Metal contamination as a possible etiology of fibro papillomatosis in juvenile female green sea turtles Chelonia mydas from the Southern Atlantic Ocean. Aquatic Toxicology. 2016; 170:42–51. Available from: https://doi.org/10.1016/j.aquatox.2015.11.007

Herrera, V. H. Q., Baena, J. P. 2017. Genotoxic Biomarkers in Erythrocytes of Lepidochelys olivácea (Cheloniidae) from Colombia. Acta Biológica Colombiana 22(3), 322-330. Available from: https://doi.org/10.15446/abc.v22n3.58688

Casini S, Caliani I, Giannetti M, Marsili L, Maltese S, Coppola D, Biachi N, Campani T, Ancora S, Caruso C, Furii G, Parga M, D’Agostino A, Fossi MC. First ecotoxicological assessment of Caretta caretta (Linnaeus, 1758) in the Mediterranean Sea using an integrated nondestructive protocol. Science of The Total Environment. 2018; 631–632, 1221-1233. Available from: https://doi.org/10.1016/j.scitotenv.2018.03.111

Udroiu I. The micronucleus test in piscine erythrocytes. Aquatic Toxicology. 2006; 79:201-20. Available from: https://doi.org/10.1016/j.aquatox.2006.06.013

Carvalho-Neta RNF, Pinheiro-Sousa DB, De Macedo Sobrinho IC, Yarbrough Horton E, Almeida ZS, Tchaicka L, Sousa AL. Genotoxic and hematological parameters in Colossoma macropomum (Pisces, Serrasalmidae) as biomarkers for envinromental impact assessment in a protected área in northeastern Brasil. Environmental Science and Pollution Research International. 2015; 4(1):1. Available from: https://doi.org/10.1007/s11356-015-4748-4

Poletta GL, Larriera A, Kleinsorge E, Mudry MD. Caiman latirostris (broad-snoutedcaiman) as asentin el organism for genotoxic monitoring: Basal values determination of micronucleus and comet assay. Mutation Research. 2008; 650:202–209. Available from: https://doi.org/10.1016/j.mrgentox.2007.12.001

Zúñiga-González G, Torres-Bugarıín O, Zamora-Perez A, Gómez-Meda BC, Ramos Ibarra ML, Martínez-González S, González-Rodrıguez A, Luna Aguirre J, Ramos-Mora A, Ontiveros-Lira D, Gallegos-Arreola MP. Differences in the number of micronucle ated erythrocytes among young and adult animals including humans: Spontaneous micronuclei in 43 species. Mutation Research. 2001; 494:161–167. Available from: https://doi.org/10.1016/s1383-5718(01)00180-2

Cafofo-Silva EG, Delariva RL, Affonso IP. Distribuição espaço temporal de Scinax fuscovarius (Lutz, 1925) (Anura, Hylidae) em Maringá – PR, Brasil. Revista em Agronegócios e Meio Ambiente. 2009; 2, 431-445. Available from: https://periodicos.unicesumar.edu.br/index.php/rama/article/view/1142

Moron SE, Lima LBD, Vieira LPL, Morais PB, Andrade RLT. Monitoramento e caracterização da qualidade da água do rio Javaés. In: Pinheiro RT. 2019. Biodiversidade na região da ilha do Bananal, Tocantins: EDUFT, 2019, 150p.

Gabiatti S. Avaliação da genotoxidade do rio Caçador, Seara – SC através da formação de micronúcleos em Astyanax sp, para análise da presença de contaminantes. In: Oliveira RJ. Águas e florestas: desafios para conservação e utilização. Guarujá: Cientifica Digital, 2021, 400p. Available from: https://doi.org/10.37885/210504527

Castanõ GV, Cabagna MZ, Prieto Y, Manzano AS. Analysis of genotoxicity in erithrocytes of turtles (Phrynops hilarii) from anthropized and natural sites of entre ríos, Argentina. Journal of Basic & Appllied Genetics. 2020; 31:15-22. Available from: http://dx.doi.org/10.35407/bag.2020.31.01.02

Borges ÂO, Erickson J, Silva LA, Fantin C, Domingos-Moreira FXV. Mercury bioaccumulation, genotoxic and biochemical biomarkers revel the health status of yellow-spotted Amazon River turtles (Podocnemis unifilis) in na environmental protection área in the Amazon. Acta Amazonica. 2022; 52:254-263. Available from: https://doi.org/10.1590/1809-4392202201230

Gonçalves VF. Anomalias nucleares eritrocitárias como ferramentas de biomonitoramento por aves no Cerrado. Uberlândia: Universidade Federal de Uberlândia, 2022. Tese de Doutorado em Ecologia e Conservação de Recursos Naturais, Universidade Federal de Uberlândia, Brasil, 84p. Available from: https://repositorio.ufu.br/handle/123456789/35157

Souza JM, Montalvão AR, Silva AR, Rodrigues ASL, Malafaia CA. Pioneering study on cytotoxicity in Australian parakeets (Melopsittacus undulates) exposed to tannery efluente. Chemosphere. 2017; 175:521– 533. Available from: https://doi.org/10.1016/j.chemosphere.2017.02.087

Araújo APC, Lima VS, Vieira JEAV, Mesak C, Malafaia G. First report on the mutagenicity and cytotoxicity of Zno nanoparticles in reptiles. Chemosphere. 2019; 235:556-564. Available from: https://doi.org/10.1016/j.chemosphere.2019.06.164

Carrasco KR, Tilbury KL, Myers MS. Assessment of the Piscine Micronucleus Test as an in situ biological indicator of Chemical Contaminant Effects. Canadian Journal of Fisheries and Aquatic Sciences. 1990; 47:2123–2136. Available from: https://doi.org/10.1139/f90-237

Quero AAM, Ferré D, Zarco A, Cuervo PF, Gorla NBM. Erythrocyte micronucleus cytome assay of 17 wild bird species from the central Monte desert, Argentina. Environmental Science and Pollution Research. 2016; 23:25224–25231. Available from: https://doi.org/10.1007/s11356-016-7638-5

Jindal R, Verma S. In vivo genotoxicity and cytotoxicity assessment of cadmium chloride in peripheral erythrocytes of Labeo rohita (Buchanan-Hamilton, 1822). Ecotoxicology and Environmental Safety. 2015; 118:1–10. Available from: https://doi.org/10.1016/j.ecoenv.2015.04.005

Çavas T, Ergene-Gözükara S. Teste de micronúcleo em células de peixes: um bioensaio para monitoramento in situ da poluição genotóxica no ambiente marinho. Environmental and Molecular Mutagenesis. 2005; 46:64-70. Available from: https://doi.org/10.1002/em.20130

Moro GV, Torati LS, Luiz DB, Matos FT. 2013. Monitoramento e manejo da qualidade da água em pisciculturas. [recurso eletrônico]. In: Rodrigues APO, Lima AF, Alvez AL, Rosa DK, Torati LS, Santos VRV (Editores técnicos). Piscicultura de água doce: multiplicando conhecimentos. Brasília: Embrapa, 2013, 440p. Available from: https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/1083545/1/cap.5.pdf

Gomes JNS. Qualidade da água do rio Pericumã e sua relação com ocupação urbana em Pinheiro – Ma. Belém: Universidade Federal do Pará, 2017. Dissertação de Mestrado em Recursos Hídricos, Universidade Federal do Pará, Brasil, 108p. Available from: https://repositorio.ufpa.br/jspui/handle/2011/10757

Lima MC, Giacomelli MB, Stupp V, Roberge FD, Barrera PB. Especiação de cobre e chumbo em sedimento do rio Tubarão (SC) pelo método Tessier. Química Nova. 2001; 24(6):734 – 742. Available from: https://doi.org/10.1590/S0100-40422001000600005

Jesus HC, Costa EA, Mendonça ASF, Zandonade E. Distribuição de metais pesados em sedimentos do sistema estuarino da Ilha de Vitória – ES. Química Nova. 2004; 27(3):378 – 386. Available from: https://doi.org/10.1590/S0100-40422004000300004

Essington ME. 2004. Soil and Water Chemistry: An integrative approach. Soil and Water Chemistry: An integrative approach. 2004; CRC Press:534. Available from: https://slunik.slu.se/kursfiler/MV0218/20103.1920/Essington_1st_edition.pdf

Lushchak VI. Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology. 2011: 101(1:13 – 30. Available from: https://doi.org/10.1016/j.aquatox.2010.10.006

Santos ES, Zanello S. 2016. Análises físico-químicas das águas e de solos do rio canguri. Available from: http://www.diaadiaeducacao.pr.gov.br/portals/pde/arquivos/1701-8.pdf

Souza NLN, Carneiro MTWD, Pimentel EF, Frossard A, Freire JB, Endringer DC, Ferreira Júnior PD. 2018. Trace elements influence the hatching success and emergence of Caretta caretta and Chelonia mydas. Journal of Trace Elements in Medicine and Biology. 2018; 5. Available from: https://doi.org/10.1016/j.jtemb.2018.06.007

Published

2025-07-28

How to Cite

RODRIGUES, Carlos Alailson Licar; MEDEIROS, Almerinda Macieira; PEREIRA, Elizângela Pinheiro; NOLETO, Katherine Saldanha; NETA, Raimunda Nonata Fortes Carvalho; MOREY, Germán Augusto Murrieta; SOUSA, Alana Lislea de. Mutagenic biomarkers in erythrocytes of free-ranging and captive Kinosternon scorpioides from the Brazilian Amazon. Brazilian Animal Science/ Ciência Animal Brasileira, Goiânia, v. 26, 2025. DOI: 10.1590/1809-6891v26e-81855E. Disponível em: https://revistas.ufg.br/vet/article/view/81855. Acesso em: 21 jan. 2026.

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VETERINARY MEDICINE

Data statement

  • The research data is available on demand, condition justified in the manuscript