Piscine micronucleus assay and the evidence of environmental degradation: the case of catfish from Brazilian tropical estuaries / Bioensaio de micronúcleo em peixes e evidências de degradação ambientai: o caso dos bagres de estuários tropicais brasileiros

Lígia Maria Borges Marques Santana, Fiamma Eugênia Lemos Abreu, Denis M. S. Abessa

Resumo


Assessing micronuclei (MN) rates in fish blood cells is a useful, fast and cheap tool for monitoring environmental quality, which can identify DNA damage in animals as an early warning of pollution irreversible effects. This technique was used to estimate genotoxicity in catfish collected at three estuaries of Ceará coast, Brazil, with different contamination status, in order to relate their respective damage rates with the contamination levels in each environment, under natural seasonality (dry and rainy season). Despite the estuaries degradation, all catfish presented extremely low rates of MN and other nuclear abnormalities (NA), contradicting the expected results. No statistical differences in the frequencies of both DNA damage endpoints were observed between seasons. Although literature confirms the presence of contaminants in these estuaries and the local biota exhibits biochemical impairment, our results indicate adaptive responses; the catfish seem to deal with contamination and do not exhibit chromosome damage. Besides, as all fish caught were juveniles, the low genotoxicity rates would be explained by younger greater efficiency to repair DNA damages, associated with low contaminants exposure due to the shorter lifetime or the low contaminants bioavailability under estuarine dynamics. Further studies are required to understand the genotoxic effects in catfish from Ceará and tropical estuaries.


Palavras-chave


Environmental monitoring, Genotoxicity, Sciades parkeri, Sciades proops, Sciades herzbergii

Texto completo:

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Referências


Abessa, D. M., Albuquerque, H. C., Morais, L. G., Araujo, G. S., Fonseca, T. G., Cruz, A. C., ... & Choueri, R. B. 2018. Pollution status of marine protected areas worldwide and the consequent toxic effects are unknown. Environmental Pollution, 24: 1450-1459. doi: 10.1016/j.envpol.2018.09.129

Ahmed, M. K., Kundu, G. K., Al-Mamun, M. H., Sarkar, S. K., Akter, M. S. & Khan, M. S. 2013. Chromium (VI) induced acute toxicity and genotoxicity in freshwater stinging catfish, Heteropneustes fossilis. Ecotoxicology and environmental safety, 92: 64-70. doi: 10.1016/j.ecoenv.2013.02.008

Al-Sabti, K. & Metcalfe, C. D. 1995. Fish micronuclei for assessing genotoxicity in water. Mutation Research/Genetic Toxicology, 343(2-3): 121-135. doi: 10.1016/0165-1218(95)90078-0

Amado, L. L., Da Rosa, C. E., Leite, A. M., Moraes, L., Pires, W. V., Pinho, G. L. L., ... & Bianchini, A. 2006. Biomarkers in croakers Micropogonias furnieri (Teleostei: Sciaenidae) from polluted and non-polluted areas from the Patos Lagoon estuary (Southern Brazil): Evidences of genotoxic and immunological effects. Marine Pollution Bulletin, 52(2): 199-206. doi: 10.1016/j.marpolbul.2005.11.006

Andrade, V. M., Da Silva, J., Da Silva, F. R., Heuser, V. D., Dias, J. F., Yoneama, M. L. & De Freitas, T. R. 2004. Fish as bioindicators to assess the effects of pollution in two southern Brazilian rivers using the Comet assay and micronucleus test. Environmental and molecular mutagenesis, 44(5): 459-468. doi: 10.1002/em.20070

Angeli, J. L. F., Trevizani, T. H., Ribeiro, A., Machado, E. C., Figueira, R. C. L., Markert, B., Fraenzle, S. & Wuenschmann, S. 2013. Arsenic and other trace elements in two catfish species from Paranaguá Estuarine Complex, Paraná, Brazil. Environmental Monitoring and Assessment, 185(10): 8333-8342. doi: 10.1007/s10661-013-3176-5

AnvariFar, H., Amirkolaie, A. K., Jalali, A. M., Miandare, H. K., Sayed, A. E. D. H., Üçüncü, S.I., Ouraji, H., Ceci, M. & Romano, N. 2018. Environmental pollution and toxic substances: Cellular apoptosis as a key parameter in a sensible model like fish. Aquatic Toxicology, 204: 144–159. doi: 10.1016/j.aquatox.2018.09.010

Arslan, Ö. Ç., Boyacioğlu, M., Parlak, H., Katalay, S. & Karaaslan, M. A. 2015. Assessment of micronuclei induction in peripheral blood and gill cells of some fish species from Aliağa Bay Turkey. Marine pollution bulletin, 94(1-2): 48-54. doi: 10.1016/j.marpolbul.2015.03.018

Ateeq, B., Ali, M. N. & Ahmad, W. 2002. Induction of micronuclei and erythrocyte alterations in the catfish Clarias batrachus by 2, 4-dichlorophenoxyacetic acid and butachlor. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 518(2): 135-144. doi: 10.1016/S1383-5718(02)00075-X

Authman, M. M., Ibrahim, S. A., El-Kasheif, M. A. & Gaber, H. S. 2013. Heavy metals pollution and their effects on gills and liver of the Nile catfish (Clarias gariepinus) inhabiting El-Rahawy Drain, Egypt. Global Veterinaria, 10(2): 103-115.

Ayllon, 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/Genetic Toxicology and Environmental Mutagenesis, 467(2): 177-186. doi: 10.1016/S1383-5718(00)00033-4

Azevedo, J. D. S., Braga, E. D. 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. doi: 10.1590/S1679-87592012000300005

Bayen, S. 2012. Occurrence, bioavailability and toxic effects of trace metals and organic contaminants in mangrove ecosystems: a review. Environment international, 48: 84-101. doi: 10.1016/j.envint.2012.07.008

Betancur, R., Marceniuk, A. P., Giarrizzo, T. & Fredou, F. L. 2015. Sciades parkeri. The IUCN Red List of Threatened Species 2015: e.T155018A722547. doi: 10.2305/IUCN.UK.2015-2.RLTS.T155018A722547.en

Bombail, V., Aw, D., Gordon, E. & Batty, J. 2001. Application of the comet and micronucleus assays to butterfish (Pholis gunnellus) erythrocytes from the Firth of Forth, Scotland. Chemosphere, 44(3): 383-392. doi: 10.1016/S0045-6535(00)00300-3

Brunetti, R., Majone, F., Gola, I. & Beltrame, C. 1988. The micronucleus test: examples of application to marine ecology. Marine Ecology Progress Series, 44(65): 8. doi: 10.3354/meps044065

Burton, G. A. & Johnston, E. L. (2010). Assessing contaminated sediments in the context of multiple stressors. Environmental Toxicology and Chemistry, 29(12): 2625-2643. doi: 10.1002/etc.332

Cajaraville, M. P., Bebianno, M. J., Blasco, J., Porte, C., Sarasquete, C. & Viarengo, A. 2000. The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Science of the Total Environment, 247(2-3): 295-311. doi: 10.1016/S0048-9697(99)00499-4

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. doi: 10.1139/f90-237

Cavalcante, R. M., Lima, D. M., Correia, L. M., Nascimento, R. F., Silveira, E. R., Freire, G. S. & Viana, R. B. 2008. Técnicas de extrações e procedimentos de clean-up para a determinação de hidrocarbonetos policílicos aromáticos (HPA) em sedimentos da costa do Ceará. Química Nova, 31(6): 1371-1377.

Cavalcante, R. M., Sousa, F. W., Nascimento, R. F., Silveira, E. R. & Freire, G. S. 2009. The impact of urbanization on tropical mangroves (Fortaleza, Brazil): evidence from PAH distribution in sediments. Journal of Environmental Management, 91(2): 328-335. doi: 10.1016/j.jenvman.2009.08.020

Cavalcante, R. M., Rocha, C. A., De Santiago, Í. S., Silva, T. F. A., Cattony, C. M., Silva, M. V. C, Silva, I. B. & Thiers, P. R. 2017. Influence of urbanization on air quality based on the occurrence of particle-associated polycyclic aromatic hydrocarbons in a tropical semiarid area (Fortaleza-CE, Brazil). Air Quality, Atmosphere & Health, 10(4): 437-445. doi: 10.1007/s11869-016-0434-z

Çavaş, T., & Ergene‐Gözükara, S. 2005. Micronucleus test in fish cells: a bioassay for in situ monitoring of genotoxic pollution in the marine environment. Environmental and molecular mutagenesis, 46(1): doi: 10.1002/em.2013064-70.

Chen, G., & White, P. A. 2004. The mutagenic hazards of aquatic sediments: a review. Mutation Research/Reviews in Mutation Research, 567(2-3): 151-225. doi: 10.1016/j.mrrev.2004.08.005

Costa, B. G. B., Soares, T. M., Torres, R. F. & Lacerda, L. D. 2013. Mercury distribution in a mangrove tidal creek affected by intensive shrimp farming. Bulletin of environmental contamination and toxicology, 90(5): 537-541. doi: 10.1007/s00128-012-0957-4

Cuevas, N. & Zorita, I. 2018. Baseline levels of environmental genotoxicity and potential confounding factors using common sole (Solea solea) as sentinel organism. Marine environmental research, 138: 1-8. doi: 10.1016/j.marenvres.2018.03.008

D’Costa, A., Shyama, S. K. & Kumar, M. P. 2017. Bioaccumulation of trace metals and total petroleum and genotoxicity responses in an edible fish population as indicators of marine pollution. Ecotoxicology and environmental safety, 142: 22-28. doi: 10.1016/j.ecoenv.2017.03.049

Dantas, D. V., Barletta, M., Costa, M. F., Barbosa‐Cintra, S. C. T., Possatto, F. E., Ramos, J. A., Lima, A. R. A. & Saint‐Paul, U. 2010. Movement patterns of catfishes (Ariidae) in a tropical semi‐arid estuary. Journal of Fish Biology, 76(10): 2540-2557. doi: 10.1111/j.1095-8649.2010.02646.x

Davanso, M. B., Moreira, L. B., Pimentel, M. F., Costa-Lotufo, L. V. & Abessa, D. M. S. 2013. Biomarkers in mangrove root crab Goniopsis cruentata for evaluating quality of tropical estuaries. Marine Environmental Research, 91: 80-88. doi: 10.1016/j.marenvres.2013.02.006

Duaví, W. C., Gama, A. F., Morais, P. C., de Oliveira, A. H., Nascimento, R. F. D. & Cavalcante, R. M. 2015. Contamination of aquatic environments by" Urban Pesticides”: The case of Cocó and Ceará rivers, Fortaleza-Ceará, Brazil. Química Nova, 38(5): 622-630. doi: 10.5935/0100-4042.20150055

Ergene, S., Çavaş, T., Çelik, A., Köleli, N., Kaya, F. & Karahan, A. 2007. Monitoring of nuclear abnormalities in peripheral erythrocytes of three fish species from the Goksu Delta (Turkey): genotoxic damage in relation to water pollution. Ecotoxicology, 16(4): 385-391. doi: 10.1007/s10646-007-0142-4

Eschmeyer, W. N., Fricke, R. & Van der Laan, R. 2013. Catalog of fishes: genera, species, references, accessible at http://researcharchive.calacademy.org/research/ichthyology/ catalog/fishcatmain.asp. 2013 (Accessed March 2013).

Farag, M. R. & Alagawany, M. 2018. Erythrocytes as a biological model for screening of xenobiotics toxicity. Chemico-biological interactions, 279: 73-83. doi: 10.1016/j.cbi.2017.11.007

Farias, M. F., Rocha-Barreira, C. A., Carvalho, F. C. T., Silva, C. M., Reis, E. M. F., Costa, R. A. & Vieira, R. H. S. F. 2010. Condições microbiológicas de Tagelus plebeius (Lightfoot, 1786) (Mollusca: Bivalvia: Solecurtidae) e da água no estuário do rio Ceará, em Fortaleza, CE. Boletim do Instituto de Pesca, 36(2): 135-142.

Fatima, M., Usmani, N., Firdaus, F., Zafeer, M. F., Ahmad, S., Akhtar, K., Dawar Husain, S. M., Ahmad, M. H., Anis, E. & Hossain, M. M. 2015. In vivo induction of antioxidant response and oxidative stress associated with genotoxicity and histopathological alteration in two commercial fish species due to heavy metals exposure in northern India (Kali) river. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 176: 17-30. doi: 10.1016/j.cbpc.2015.07.004

Fent, K. 2004. Ecotoxicological effects at contaminated sites. Toxicology, 205(3): 223-240. doi: 10.1016/j.tox.2004.06.060

Fiuza, A. B. J. Q., de Oliveira LeHugeur, L. G. & Queiroz, B. J. 2010. Environmental analysis of the conservation status of the lower Pacoti River, Ceará State. Arquivos de Ciências do Mar, 43(1): 18-29.

Gama, A. F., OLIVEIRA, A. D. & Cavalcante, R. M. 2013. Inventário de agrotóxicos e risco de contaminação química dos recursos hídricos no semiárido cearense. Química Nova, 36(3): 462-467.

Gama, A. F., Cavalcante, R. M., Duaví, W. C., Silva, V. P. A. & Nascimento, R. F. 2017. Occurrence, distribution, and fate of pesticides in an intensive farming region in the Brazilian semi-arid tropics (Jaguaribe River, Ceará). Journal of soils and sediments, 17(4): 1160-1169. doi 10.1007/s11368-016-1597-9

Ge, T., Han, J., Qi, Y., Gu, X., Ma, L., Zhang, C., Naeem, S. & Huang, D. 2017. The toxic effects of chlorophenols and associated mechanisms in fish. Aquatic toxicology, 184: 78-93. doi: 10.1016/j.aquatox.2017.01.005

Ghisi, N. C., Oliveira, E. C., Mota, T. F. M., Vanzetto, G. V., Roque, A. A., Godinho, J. P., Bettim, F.L., Assis, H.C.S. & Prioli, A. J. 2016. Integrated biomarker response in catfish Hypostomus ancistroides by multivariate analysis in the Pirapó River, southern Brazil. Chemosphere, 161: 69-79. doi: 10.1016/j.chemosphere.2016.06.113

Gurgel, H. D. C. B., Alburqueque, C. Q., Souza, D. S. L. & Barbieri, G. 2000. Aspectos da biologia pesqueira em fêmeas de Cathorops spixii do estuário do rio Potengi, Natal/RN, com ênfase nos índices biométricos. Acta Scientiarum, 22(2): 503-505. ISSN 1415-6814

Gusso-Choueri, P. K., Choueri, R. B., Santos, G. S., de Araújo, G. S., Cruz, A. C. F., Stremel, T., Campos, S.X., Cestari, M.M., Ribeiro, C.A.O. & Abessa, D. M. S. 2016. Assessing genotoxic effects in fish from a marine protected area influenced by former mining activities and other stressors. Marine pollution bulletin, 104(1-2): 229-239. doi: 10.1016/j.marpolbul.2016.01.025

Harabawy, A. S. & Ibrahim, A. T. A. 2014. Sublethal toxicity of carbofuran pesticide on the African catfish Clarias gariepinus (Burchell, 1822): hematological, biochemical and cytogenetic response. Ecotoxicology and Environmental Safety, 103: 61-67. doi: 10.1016/j.ecoenv.2013.09.022

Hayashi, M., Ueda, T., Uyeno, K., Wada, K., Kinae, N., Saotome, K., Tanaka, N., Takai, A., Sasaki, Y.F., Asano, N., Sofuni, T. & Ojima, Y. 1998. Development of genotoxicity assay systems that use aquatic organisms. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 399(2): 125-133. doi: 10.1016/S0027-5107(97)00251-0

Hussain, B., Sultana, T., Sultana, S., Masoud, M. S., Ahmed, Z. & Mahboob, S. 2018. Fish eco-genotoxicology: Comet and micronucleus assay in fish erythrocytes as in situ biomarker of freshwater pollution. Saudi journal of biological sciences, 25(2): 393-398. doi: 10.1016/j.sjbs.2017.11.048

Ishikawa, M. M., Pádua, S. D., Satake, F., de Pietro, P. S., & Hisano, H. 2010. Procedimentos básicos para colheita de sangue em peixes. Circular Técnica 17, Embrapa, Dourados, MS, pp 1-8

Katsumiti, A., Domingos, F. V., Azevedo, M., Da Silva, M. D., Damian, R. C., Almeida, M. I. M., Assis, H. C. S., Cestari, M. M., Randi, M. A. F., Ribeiro, C. A. O. & Freire, C. A. 2009. An assessment of acute biomarker responses in the demersal catfish Cathorops spixii after the Vicuña Oil Spill in a harbour estuarine area in Southern Brazil. Environmental monitoring and assessment, 152(1-4): 209. doi: 10.1007/s10661-008-0309-3

Kirschbaum, A. A., Seriani, R., Pereira, C. D., Assunção, A., Abessa, D. M., Rotundo, M. M. & Ranzani-Paiva, M. J. 2009. Cytogenotoxicity biomarkers in fat snook Centropomus parallelus from Cananéia and São Vicente estuaries, SP, Brazil. Genetics and Molecular Biology, 32(1): 151-154. doi: 10.1590/S1415-47572009005000007

Kubitza, F. 1997. Transporte de peixes vivos. Panorama da Aqüicultura, 7(43): 20-26.

Lacerda, L. D., Santos, J. A. & Lopes, D. V. 2009. Fate of copper in intensive shrimp farms: bioaccumulation and deposition in pond sediments. Brazilian Journal of Biology, 69(3): 851-858. doi: 10.1590/S1519-69842009000400012

Lima, M. F., Fernandes, G. M., Oliveira, A. H., Morais, P. C., Marques, E. V., Santos, F. R., Nascimento, R. F., Swartout, R. F., Nelson, R. K., Reddy, C. M. & Cavalcante, R. M. 2019. Emerging and traditional organic markers: Baseline study showing the influence of untraditional anthropogenic activities on coastal zones with multiple activities (Ceará coast, Northeast Brazil). Marine pollution bulletin, 139: 256-262. doi: 10.1016/j.marpolbul.2018.12.006

Lotze, H. K., Lenihan, H. S., Bourque, B. J., Bradbury, R. H., Cooke, R. G., Kay, M. C., Kidwell, S. M., Kirby, M. X., Peterson, C. H., & Jackson, J. B. C. 2006. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science, 312(5781): 1806-1809.

Marceniuk, A. P. 2005. Chave para identificação das espécies de bagres marinhos (Siluriformes, Ariidae) da costa brasileira. Boletim do Instituto de Pesca, 31(2): 89-101.

Marins, R. V., Lacerda, L. D., Mounier, S., Paraquetti, H. H. M. & Marques, W. S. 2002. Caracterização hidroquímica, distribuição e especiação de mercúrio nos estuários dos rios Ceará e Pacoti, região metropolitana de Fortaleza, Ceará, Brasil. Geochimica Brasiliensis, 16(1): 37-48. doi: 10.21715/gb.v16i1.497

Mekkawy, I. A., Mahmoud, U. M. & Sayed, A. E. D. H. 2011. Effects of 4-nonylphenol on blood cells of the African catfish Clarias gariepinus (Burchell, 1822). Tissue and cell, 43(4): 223-229. doi:10.1016/j.tice.2011.03.006

Minissi, S., Ciccotti, E. & Rizzoni, M. 1996. Micronucleus test in erythrocytes of Barbus plebejus (Teleostei, Pisces) from two natural environments: a bioassay for the in situ detection of mutagens in freshwater. Mutation Research/Genetic Toxicology, 367(4): 245-251. doi: 10.1016/S0165-1218(96)90084-1

Monserrat, J. M., Martínez, P. E., Geracitano, L. A., Amado, L. L., Martins, C. M. G., Pinho, G. L. L., Chaves, I. S., Ferreira-Cravo, M., Ventura-Lima, J. & Bianchini, A. 2007. Pollution biomarkers in estuarine animals: critical review and new perspectives. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 146(1-2): 221-234. doi: 10.1016/j.cbpc.2006.08.012

Nilin, J., Castro, C. D., Pimentel, M. P., Franklin Júnior, W., Matos, R. F. G., Lotufo, T. M. C. & Costa-Lotufo, L. V. 2007. Water toxicity assessment of the Ceará river estuary (Brazil). Journal of the Brazilian Society of Ecotoxicology, 2(2): 107-113.

Nilin, J., Moreira, L. B., Aguiar, J. E., Marins, R., de Souza Abessa, D. M., Lotufo, T. M. C. & Costa-Lotufo, L. V. 2013. Sediment quality assessment in a tropical estuary: the case of Ceará River, Northeastern Brazil. Marine Environmental Research, 91: 89-96. doi: 10.1016/j.marenvres.2013.02.009

Nwani, C. D., Nnaji, M. C., Oluah, S. N., Echi, P. C., Nwamba, H. O., Ikwuagwu, O. E. & Ajima, M. N. O. 2014. Mutagenic and physiological responses in the juveniles of African catfish, Clarias gariepinus (Burchell 1822) following short term exposure to praziquantel. Tissue and Cell, 46(4): 264-273. doi: 10.1016/j.tice.2014.05.011

Oliveira, A. H., Cavalcante, R. M., Duaví, W. C., Fernandes, G. M., Nascimento, R. F., Queiroz, M. E., Mendonça, K. V. 2016. The legacy of organochlorine pesticide usage in a tropical semi-arid region (Jaguaribe River, Ceará, Brazil): Implications of the influence of sediment parameters on occurrence, distribution and fate. Science of the Total Environment, 542:254-263. doi: 10.1016/j.scitotenv.2015.10.058

Okechukwu, E. O., Auta, J. & Balogun, J. K. 2007. Effects of acute nominal doses of chlorpyrifos-ethyl on some haematological indices of African catfish Clarias gariepinus-Teugels. Journal of Fisheries Internacional, 2: 190-194.

Osman, A. G., Abd El Reheem, A. E. B. M., Moustafa, M. A., Mahmoud, U. M., Abuel-Fadl, K. Y. & Kloas, W. 2011. In situ evaluation of the genotoxic potential of the river Nile: I. Micronucleus and nuclear lesion tests of erythrocytes of Oreochromis niloticus niloticus (Linnaeus, 1758) and Clarias gariepinus (Burchell, 1822). Toxicological & Environmental Chemistry, 93(5): 1002-1017. doi: 10.1080/02772248.2011.564496

Pérez-Coyotl, I., Martínez-Vieyra, C., Galar-Martínez, M., Gómez-Oliván, L. M., García-Medina, S., Islas-Flores, H., Borja, R.P., Gasca-Pérez, E., Novoa-Luna, K. A. & Dublán-García, O. 2017. DNA damage and cytotoxicity induced on common carp by pollutants in water from an urban reservoir. Madín Reservoir, a case study. Chemosphere, 185: 789-797. doi: 10.1016/j.chemosphere.2017.07.072

Pimentel, M. F., Damasceno, É. P., Jimenez, P. C., Araújo, P. F. R., Bezerra, M. F., de Morais, P. C. V., Cavalcante, R. M., Loureiro, S. & Costa-Lotufo, L. V. 2016. Endocrine disruption in Sphoeroides testudineus tissues and sediments highlights contamination in a northeastern Brazilian estuary. Environmental Monitoring and Assessment, 188(5): 298. doi:10.1007/s10661-016-5300-9

Pinto, A. C., Marques, L. H. B. S., Santos, F. L. B. 2020. Utilização de bioensaio na avaliação ecotoxicológica de lagos urbanos (Paulo Afonso/BA) com Poecilia reticulata (Peters, 1859) (Chordata: Teleostei). Brazilian Journal of Animal and Environmental Research, 2(4): 1473-1493. doi:

Prestes, R. M., Vincenci, K. L. 2019. Bioindicadores como avaliação de impacto ambiental / Bioindicators as environmental impact assessment. Brazilian Journal of Animal and Environmental Research, 3(3): 1297-1313.

Queiroz, L., Rossi, S., Meireles, J. & Coelho, C. 2013. Shrimp aquaculture in the federal state of Ceará, 1970–2012: trends after mangrove forest privatization in Brazil. Ocean & Coastal Management, 73: 54-62. doi: 10.1016/j.ocecoaman.2012.11.009

Rodriguez-Cea, A., Ayllon, F. & Garcia-Vazquez, E. 2003. Micronucleus test in freshwater fish species: an evaluation of its sensitivity for application in field surveys. Ecotoxicology and environmental safety, 56(3): 442-448. doi: 10.1016/S0147-6513(03)00073-3

Rosenfeld, G. 1947. Corante pancrômico para hematologia e citologia clínica. Nova combinação dos componentes do May-Grünwald e do Giemsa num só corante. Memórias do Instituto Butantan, 20: 329-34.

Rybakovas, A., Baršienė, J. & Lang, T. 2009. Environmental genotoxicity and cytotoxicity in the offshore zones of the Baltic and the North Seas. Marine Environmental Research, 68(5): 246-256. doi: 10.1016/j.marenvres.2009.06.014

Salvagni, J., Ternus, R. Z. & Fuentefria, A. M. 2011. Assessment of the genotoxic impact of pesticides on farming communities in the countryside of Santa Catarina State, Brazil. Genetics and molecular biology, 34(1): 122-126.

Santana, L. M. B. M. 2014. Avaliação de risco ecotoxicológico de três estuários do litoral do Ceará, nordeste do Brasil. PhD Thesis, Federal University of Ceará, Fortaleza, Brazil, 160 p.

Santana, L. M., Costa, L. V. & Abessa, D. M. 2015. A contaminação antrópica e seus efeitos em três estuários do litoral do ceará, nordeste do Brasil-revisão. Arquivos de Ciências do Mar, 48(2): 93-115.

Schmidt, W. 1975. The micronucleus test. Mutation Research, 31: 9-15. doi: 10.1016/0165-1161(75)90058-8

Schlegel, R. & MacGregor, J. T. 1982. The persistence of micronuclei in peripheral blood erythrocytes: detection of chronic chromosome breakage in mice. Mutation Research Letters, 104(6): 367-369. doi: 10.1016/0165-7992(82)90171-3

Segura-Berttolini, E. C. & Mendoza-Carranza, M. 2013. Importance of male gafftopsail catfish, Bagre marinus (Pisces: Ariidae), in the reproductive process. Ciencias Marinas, 39(1): 29-39. doi: 10.7773/cm.v39i1.2136

Seriani, R., Tavares Ranzani-Paiva, M. J., Silva-Souza, Â. T. & Napoleão, S. R. 2011. Hematology, micronuclei and nuclear abnormalities in fishes from São Francisco river, Minas Gerais state, Brazil. Acta Scientiarum. Biological Sciences, 33(1). doi: 10.4025/actascibiolsci.v33i1.7117

Seriani, R., Abessa, D. M. S., Pereira, C. D. S., Kirschbaum, A. A., Abujamara, L. D., Buruaem, L. M., Félix, C., Turatti, G. C. R., Prado, L. R. G. B., Sousa, E. C. P. M. & Ranzani-Paiva, M. J. T. 2013. Blood parameters of estuarine and marine fish as non-destructive pollution biomarkers. Pp. 182-204. In: Almeida, E. A. & Ribeiro, C. A. O. (Eds.). Pollution and Fish Health in Tropical Ecosystems. CRC Press. Boca Raton, FL, USA.

Siu, W. H., Mak, E., Cao, J., De Luca‐Abbott, S. B., Richardson, B. J. & Lam, P. K. 2004. Micronucleus induction in gill cells of green‐lipped mussels (Perna viridis) exposed to mixtures of polycyclic aromatic hydrocarbons and chlorinated pesticides. Environmental toxicology and chemistry, 23(5): 1317-1325. doi: 10.1897/03-225

Udroiu, I. 2006. The micronucleus test in piscine erythrocytes. Aquatic Toxicology, 79(2): 201-204. doi: 10.1016/j.aquatox.2006.06.013

Vaisman, A. G., Marins, R. V. & Lacerda, L. D. 2005. Characterization of the mangrove oyster, Crassostrea rhizophorae, as a biomonitor for mercury in tropical estuarine systems, northeast Brazil. Bulletin of environmental contamination and toxicology, 74(3): 582-588. doi: 10.1007/s00128-005-0623-1

Van der Oost, R., Beyer, J. & Vermeulen, N. P. 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology, 13(2): 57-149. doi: 10.1016/S0048-9697(99)00499-4




DOI: https://doi.org/10.34188/bjaerv3n4-048

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