Cadmium and lead: genotoxic effects on the broodstock of the fish Prochilodus magdalenae (Characiformes: Prochilodontidae)

Authors

DOI:

https://doi.org/10.15517/ekctvz90

Keywords:

co-exposure, micronuclei, comet assay, biomarkers, sentinel species

Abstract

Introduction: Heavy metals such as cadmium (Cd) and lead (Pb) pose a significant threat to aquatic ecosystems due to their persistence, capacity for bioaccumulation, and genotoxic potential. These contaminants are of particular concern in tropical freshwater systems, where they may impact native species of ecological, economic, and nutritional importance, such as Prochilodus magdalenae, a migratory fish endemic to the Magdalena–Cauca River basin in Colombia. Objective: To evaluate the acute effects of individual and combined exposure to Cd and Pb on behavioral parameters, mortality, and genetic damage in P. magdalenae. Methods: Three individual doses of each metal and five binary combinations were administered via intramuscular injection in adult fish, followed by analysis using genotoxicity biomarkers (micronuclei, nuclear abnormalities, and DNA integrity damage). Results: Evident behavioral changes, increased mortality, and significant genotoxic damage were demonstrated, particularly in treatments involving combined exposures. The highest mortality rate (75 %) occurred in the 0.8 μg Cd/kg + 14 μg Pb/kg treatment. Pb exposure was associated with a greater frequency of micronucleus formation, while Cd exposure induced an increase in nuclear abnormalities, without a clear dose–response trend. The comet assay confirmed primary DNA damage particularly in 0.2 μg Cd/kg + 8.0 μg Pb/kg and 0.8 μg Cd/kg + 14 μg Pb/kg treatments, where effects exceeding those of individual exposures were observed. Nevertheless, non-linear responses were detected in some treatments, possibly due to adaptive cellular responses or apoptosis. A sex-dependent susceptibility was also identified: males exhibited higher mortality rates but lower micronucleus frequencies than females. Conclusions: The toxic potential of Cd and Pb is highlighted, and the suitability of P. magdalenae as a sentinel species for environmental monitoring supported. The study emphasizes the need to consider co-exposure scenarios in ecotoxicological risk assessments, due to their relevance to ecosystem health, human consumption, and food security in regions where this species represents a vital resource.

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References

Abass, N. Y. (2024). The influence of heavy metals on cytotoxicity in Tilapia zillii. Aquaculture International, 32(7), 9079–9098. https://doi.org/10.1007/s10499-024-01604-2 DOI: https://doi.org/10.1007/s10499-024-01604-2

Abdel-Warith, A. A., Younis, E. M., Al Asgah, N. A., & Wahbi, O. M. (2011). Effect of zinc toxicity on liver histology of Nile tilapia, Oreochromis niloticus. Scientific Research and Essays, 6(17), 3760–3769. https://doi.org/10.5897/SRE11.883 DOI: https://doi.org/10.5897/SRE11.883

Ali, Z., Sher, N., Muhammad, I., Nayab, G. E., Alouffi, A., Almutairi, M. M., Khan, I., & Ali, A. (2025). The combined effect of cadmium and copper induces bioaccumulation, and toxicity and disrupts the antioxidant enzymatic activities of goldfish (Carassius auratus). Toxicology Reports, 14, Article 101972. https://doi.org/10.1016/j.toxrep.2025.101972 DOI: https://doi.org/10.1016/j.toxrep.2025.101972

Almeida, J. A., Diniz, Y. S., Marques, S. F. G., Faine, L. A., Ribas, B. O., Burneiko, R. C., & Novelli, E. L. B. (2002). The use of the oxidative stress responses as biomarkers in Nile tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination. Environment International, 27(8), 673–679. https://doi.org/10.1016/S0160-4120(01)00127-1 DOI: https://doi.org/10.1016/S0160-4120(01)00127-1

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

Atli, G., Ariyurek, S. Y., Kanak, E. G., & Canli, M. (2015). Alterations in the serum biomarkers belonging to different metabolic systems of fish (Oreochromis niloticus) after Cd and Pb exposures. Environmental Toxicology and Pharmacology, 40(2), 508–515. https://doi.org/10.1016/j.etap.2015.08.001 DOI: https://doi.org/10.1016/j.etap.2015.08.001

Awad, S. T., Hemeda, S. A., El Nahas, A. F., Abbas, E. M., Abdel-Razek, M. A. S., Ismail, M., Mamoon, A., & Ali, F. S. (2024). Gender-specific responses in gene expression of Nile tilapia (Oreochromis niloticus) to heavy metal pollution in different aquatic habitats. Scientific Reports, 14(1), Article 14671. https://doi.org/10.1038/s41598-024-64300-4 DOI: https://doi.org/10.1038/s41598-024-64300-4

Bault, Z. A., Peterson, S. M., & Freeman, J. L. (2015). Directional and color preference in adult zebrafish: Implications in behavioral and learning assays in neurotoxicology studies. Journal of Applied Toxicology, 35(12), 1502–1510. https://doi.org/10.1002/jat.3169 DOI: https://doi.org/10.1002/jat.3169

Bolognesi, C., Perrone, E., Roggieri, P., Pampanin, D. M., & Sciutto, A. (2006). Assessment of micronuclei induction in peripheral erythrocytes of fish exposed to xenobiotics under controlled conditions. Aquatic Toxicology, 78(1), S93–S98. https://doi.org/10.1016/j.aquatox.2006.02.015 DOI: https://doi.org/10.1016/j.aquatox.2006.02.015

Bonassi, S., El-Zein, R., Bolognesi, C., & Fenech, M. (2011). Micronuclei frequency in peripheral blood lymphocytes and cancer risk: Evidence from human studies. Mutagenesis, 26(1), 93–100. https://doi.org/10.1093/mutage/geq075 DOI: https://doi.org/10.1093/mutage/geq075

Calabrese, E. J., & Baldwin, L. A. (2001). Hormesis: U-shaped dose responses and their centrality in toxicology. Trends in Pharmacological Sciences, 22(6), 285–291. https://doi.org/10.1016/S0165-6147(00)01719-3 DOI: https://doi.org/10.1016/S0165-6147(00)01719-3

Caramello, C. S., & Jorge, L. C. (2022). Evaluación de la mutagenicidad del herbicida glifosato en Prochilodus lineatus a través del test de micronúcleos. Revista Veterinaria, 33(2), 258–265. https://doi.org/10.30972/vet.3326193 DOI: https://doi.org/10.30972/vet.3326193

Chakraborty, S. B. (2021). Non-essential heavy metals as endocrine disruptors: Evaluating impact on reproduction in teleosts. Proceedings of the Zoological Society, 74(4), 417–431. https://doi.org/10.1007/s12595-021-00399-x DOI: https://doi.org/10.1007/s12595-021-00399-x

Chen, X., Wang, J., Xie, Y., Ma, Y., Zhang, J., Wei, H., & Abdou, A. I. E. (2022). Physiological response and oxidative stress of grass carp (Ctenopharyngodon idellus) under single and combined toxicity of polystyrene microplastics and cadmium. Ecotoxicology and Environmental Safety, 245, Article 114080. https://doi.org/10.1016/j.ecoenv.2022.114080 DOI: https://doi.org/10.1016/j.ecoenv.2022.114080

Cherednichenko, O., Magda, I., Nuraliyev, S., Pilyugina, A., & Azizbekova, D. (2024). Cytome analysis (micronuclei and nuclear anomalies) in bioindication of environmental pollution in animals with nuclear erythrocytes. Heliyon, 10(18), Article e37643. https://doi.org/10.1016/j.heliyon.2024.e37643 DOI: https://doi.org/10.1016/j.heliyon.2024.e37643

Chouchene, L., Pellegrini, E., Gueguen, M.-M., Hinfray, N., Brion, F., Piccini, B., Kah, O., Saïd, K., Messaoudi, I., & Pakdel, F. (2016). Inhibitory effect of cadmium on estrogen signaling in zebrafish brain and protection by zinc. Journal of Applied Toxicology, 36(6), 863–871. https://doi.org/10.1002/jat.3285 DOI: https://doi.org/10.1002/jat.3285

Collins, A. R. (2004). The comet assay for DNA damage and repair. Molecular Biotechnology, 26(3), 249–261. https://doi.org/10.1385/MB:26:3:249 DOI: https://doi.org/10.1385/MB:26:3:249

Collins, A. R., Oscoz, A. A., Brunborg, G., Gaivão, I., Giovannelli, L., Kruszewski, M., Smith, C. C., & Stetina, R. (2008). The comet assay: Topical issues. Mutagenesis, 23(3), 143–151. https://doi.org/10.1093/mutage/gem051 DOI: https://doi.org/10.1093/mutage/gem051

Da Rocha, C. A. M., De Lima, P. D. L., Santos, R. A. D., & Burbano, R. M. R. (2009). Evaluation of genotoxic effects of xenobiotics in fishes using comet assay—A review. Reviews in Fisheries Science, 17(2), 170–173. https://doi.org/10.1080/10641260802541791 DOI: https://doi.org/10.1080/10641260802541791

D’Agostini, F., & La Maestra, S. (2021). Micronuclei in fish erythrocytes as genotoxic biomarkers of water pollution: An overview. In Reviews of Environmental Contamination and Toxicology (Vol. 258, pp. 195–240). Springer. https://doi.org/10.1007/398_2021_76 DOI: https://doi.org/10.1007/398_2021_76

Dalzochio, T., Andriguetti, N. B., Simões, L. A. R., Gehlen, G., & Da Silva, L. B. (2019). Genotoxicity biomarkers in fish erythrocytes and water quality parameters. In Pollution of Water Bodies in Latin America (pp. 275–290). Springer. https://doi.org/10.1007/978-3-030-27296-8_15 DOI: https://doi.org/10.1007/978-3-030-27296-8_15

Dhawan, A., Bajpayee, M., & Parmar, D. (2009). Comet assay: A reliable tool for the assessment of DNA damage in different models. Cell Biology and Toxicology, 25(1), 5–32. https://doi.org/10.1007/s10565-008-9072-z DOI: https://doi.org/10.1007/s10565-008-9072-z

Duan, Z., Xing, Y., Feng, Z., Zhang, H., Li, C., Gong, Z., Wang, L., & Sun, H. (2017). Hepatotoxicity of benzotriazole and its effect on the cadmium induced toxicity in zebrafish Danio rerio. Environmental Pollution, 224, 706–713. https://doi.org/10.1016/j.envpol.2017.02.055 DOI: https://doi.org/10.1016/j.envpol.2017.02.055

Fenech, M. (2000). The in vitro micronucleus technique. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 455(1), 81–95. https://doi.org/10.1016/S0027-5107(00)00065-8 DOI: https://doi.org/10.1016/S0027-5107(00)00065-8

Flora, S. J. S., Mittal, M., & Mehta, A. (2008). Heavy metal induced oxidative stress & its possible reversal by chelation therapy. The Indian Journal of Medical Research, 128(4), 501–523.

Frenzilli, G., Nigro, M., & Lyons, B. P. (2009). The Comet assay for the evaluation of genotoxic impact in aquatic environments. Mutation Research, 681(1), 80–92. https://doi.org/10.1016/j.mrrev.2008.03.001 DOI: https://doi.org/10.1016/j.mrrev.2008.03.001

García-Castro, K. L., & Márquez, E. J. (2024). Temporal-scale assessment of population genetics of the freshwater fish Prochilodus magdalenae in an area impacted by construction of a dam. Hydrobiologia, 851(6), 1513–1531. https://doi.org/10.1007/s10750-023-05396-z DOI: https://doi.org/10.1007/s10750-023-05396-z

Gasulla, J., Picco, S. J., Carriquiriborde, P., Dulout, F. N., Ronco, A. E., & de Luca, J. C. (2016). Genotoxic effects induced by Cd+2, Cr+6, Cu+2 in the gill and liver of Odontesthes bonariensis (Piscies, Atherinopsidae). Bulletin of Environmental Contamination and Toxicology, 96(5), 591–595. https://doi.org/10.1007/s00128-016-1774-y DOI: https://doi.org/10.1007/s00128-016-1774-y

Green, A. J., & Planchart, A. (2018). The neurological toxicity of heavy metals: A fish perspective. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 208, 12–19. https://doi.org/10.1016/j.cbpc.2017.11.008 DOI: https://doi.org/10.1016/j.cbpc.2017.11.008

Gu, Y., Xu, D., Liu, J., Chen, Y., Wang, J., Song, Y., Sun, B., & Xia, B. (2023). Bioaccumulation of functionalized polystyrene nanoplastics in sea cucumber Apostichopus japonicus (Selenka, 1867) and their toxic effects on oxidative stress, energy metabolism and mitochondrial pathway. Environmental Pollution, 319, 121015. https://doi.org/10.1016/j.envpol.2023.121015 DOI: https://doi.org/10.1016/j.envpol.2023.121015

Hesser, E. F. (1960). Methods for routine fish hematology. The Progressive Fish-Culturist, 22(4), 164–171. DOI: https://doi.org/10.1577/1548-8659(1960)22[164:MFRFH]2.0.CO;2

Ibrahim, A. T. A., Banaee, M., & Sureda, A. (2021). Genotoxicity, oxidative stress, and biochemical biomarkers of exposure to green synthesized cadmium nanoparticles in Oreochromis niloticus (L.). Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 242, 108942. https://doi.org/10.1016/j.cbpc.2020.108942 DOI: https://doi.org/10.1016/j.cbpc.2020.108942

Jiménez‐Segura, L. F., Palacio, J., & Leite, R. (2010). River flooding and reproduction of migratory fish species in the Magdalena River basin, Colombia. Ecology of Freshwater Fish, 19(2), 178–186. https://doi.org/10.1111/j.1600-0633.2009.00402.x DOI: https://doi.org/10.1111/j.1600-0633.2009.00402.x

Jiménez-Segura, L., Restrepo-Ángel, J. D., & Hernandez-Serna, A. (2022). Drivers for the artisanal fisheries production in the Magdalena River. Frontiers in Environmental Science, 10. https://doi.org/10.3389/fenvs.2022.866575 DOI: https://doi.org/10.3389/fenvs.2022.866575

Lee, J., & Freeman, J. L. (2014). Zebrafish as a model for investigating developmental lead (Pb) neurotoxicity as a risk factor in adult neurodegenerative disease: A mini-review. Neurotoxicology (Park Forest South), 43, 57–64. https://doi.org/10.1016/j.neuro.2014.03.008 DOI: https://doi.org/10.1016/j.neuro.2014.03.008

Lee, R. F., & Steinert, S. (2003). Use of the single cell gel electrophoresis/comet assay for detecting DNA damage in aquatic (marine and freshwater) animals. Mutation Research/Reviews in Mutation Research, 544(1), 43–64. https://doi.org/10.1016/S1383-5742(03)00017-6 DOI: https://doi.org/10.1016/S1383-5742(03)00017-6

Liu, X., Deng, Q., Yang, H., Wang, J., & Wang, M. (2022). Oxidative stress of cadmium and lead at environmentally relevant concentrations on hepatopancreas of Macrobrachium nipponense and their mixture interactivity: Implications for water quality criteria amendment. International Journal of Environmental Research and Public Health, 20(1), Article 360. https://doi.org/10.3390/ijerph20010360 DOI: https://doi.org/10.3390/ijerph20010360

Luzhna, L., Kathiria, P., & Kovalchuk, O. (2013). Micronuclei in genotoxicity assessment: From genetics to epigenetics and beyond. Frontiers in Genetics, 4, Article 131. https://doi.org/10.3389/fgene.2013.00131 DOI: https://doi.org/10.3389/fgene.2013.00131

Mager, E. M. (2011). Lead. In C. M. Wood, A. P. Farrell, & C. J. Brauner (Eds.), Fish Physiology (Vol. 31, pp. 185–236). Academic Press. https://doi.org/10.1016/S1546-5098(11)31026-6 DOI: https://doi.org/10.1016/S1546-5098(11)31026-6

Mancera-Rodríguez, N. J., & Álvarez-León, R. (2006). Estado del conocimiento de las concentraciones de mercurio y otros metales pesados en peces dulceacuícolas de Colombia. Acta Biológica Colombiana, 11(1), 3–23.

Mojica, J. I., Usma Oviedo, J. S., Álvarez León, R., & Lasso, C. A. (2012). Libro rojo de peces dulceacuícolas de Colombia. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt.

Mondal, K., Ghosh, S., & Haque, S. (2018). A review on contamination, bioaccumulation and toxic effect of cadmium, mercury and lead on freshwater fishes. International Journal of Zoology Studies, 3(2), 153–159.

Monteiro, V., Cavalcante, D., Viléla, M. B. F. A., Sofia, S. H., & Martinez, C. B. R. (2011). In vivo and in vitro exposures for the evaluation of the genotoxic effects of lead on the Neotropical freshwater fish Prochilodus lineatus. Aquatic Toxicology, 104(3–4), 291–298. https://doi.org/10.1016/j.aquatox.2011.05.002 DOI: https://doi.org/10.1016/j.aquatox.2011.05.002

Nabi, N., Ahmed, I., & Wani, G. B. (2022). Hematological and serum biochemical reference intervals of rainbow trout, Oncorhynchus mykiss cultured in Himalayan aquaculture: Morphology, morphometrics and quantification of peripheral blood cells. Saudi Journal of Biological Sciences, 29(4), 2942–2957. https://doi.org/10.1016/j.sjbs.2022.01.019 DOI: https://doi.org/10.1016/j.sjbs.2022.01.019

Paduraru, E., Iacob, D., Rarinca, V., Plavan, G., Ureche, D., Jijie, R., & Nicoara, M. (2023). Zebrafish as a potential model for neurodegenerative diseases: A focus on toxic metals implications. International Journal of Molecular Sciences, 24(4), Article 3428. https://doi.org/10.3390/ijms24043428 DOI: https://doi.org/10.3390/ijms24043428

Pájaro-Meza, D. M., & Sánchez-Rincón, P. A. (2016). Evaluación de las concentraciones de metales pesados (Cd y Pb) en especies ícticas comercializadas en la plaza del pescado de la ciudad de Barranquilla y riesgo potencial para la salud humana [Tesis de pregrado, Universidad de la Costa]. Repositorio Institucional CUC. https://repositorio.cuc.edu.co/handle/11323/344

Paschoalini, A. L., Savassi, L. A., Arantes, F. P., Rizzo, E., & Bazzoli, N. (2019). Heavy metals accumulation and endocrine disruption in Prochilodus argenteus from a polluted neotropical river. Ecotoxicology and Environmental Safety, 169, 539–550. https://doi.org/10.1016/j.ecoenv.2018.11.047 DOI: https://doi.org/10.1016/j.ecoenv.2018.11.047

Razzaq, A., Abdullah, S., Naz, H., Abbas, K., Shafique, L., & Liu, Q. (2021). Micronuclei assay: A suitable tool for evaluating the heavy metals induced genotoxicity in fish, Labeo rohita. Pakistan Journal of Zoology, 53(5), 1839–1847. https://doi.org/10.17582/journal.pjz/20190325130338 DOI: https://doi.org/10.17582/journal.pjz/20190325130338

Ruiter, S., Sippel, J., Bouwmeester, M., Lommelaars, T., Beekhof, P., Hodemaekers, H., Bakker, F., Van den Brandhof, E. -J., Pennings, J., & Van der Ven, L. (2016). Programmed effects in neurobehavior and antioxidative physiology in zebrafish embryonically exposed to cadmium: Observations and hypothesized adverse outcome pathway framework. International Journal of Molecular Sciences, 17(11), Article 1830. https://doi.org/10.3390/ijms17111830 DOI: https://doi.org/10.3390/ijms17111830

Sato, M., & Kondoh, M. (2002). Recent studies on metallothionein: Protection against toxicity of heavy metals and oxygen free radicals. The Tohoku Journal of Experimental Medicine, 196(1), 9–22. https://doi.org/10.1620/tjem.196.9 DOI: https://doi.org/10.1620/tjem.196.9

Schaumburg, L. G., Poletta, G. L., Siroski, P. A., & Mudry, M. D. (2012). Baseline values of micronuclei and comet assay in the lizard Tupinambis merianae (Teiidae, Squamata). Ecotoxicology and Environmental Safety, 84, 99–103. https://doi.org/10.1016/j.ecoenv.2012.06.023 DOI: https://doi.org/10.1016/j.ecoenv.2012.06.023

Senut, M.-C., Cingolani, P., Sen, A., Kruger, A., Shaik, A., Hirsch, H., Suhr, S. T., & Ruden, D. (2012). Epigenetics of early-life lead exposure and effects on brain development. Epigenomics, 4(6), 665–674. https://doi.org/10.2217/epi.12.58 DOI: https://doi.org/10.2217/epi.12.58

Singh, N. P., McCoy, M. T., Tice, R. R., & Schneider, E. L. (1988). A simple technique for quantitation of low levels of DNA damage in individual cells. Experimental Cell Research, 175(1), 184–191. https://doi.org/10.1016/0014-4827(88)90265-0 DOI: https://doi.org/10.1016/0014-4827(88)90265-0

Shahjahan, M., Taslima, K., Rahman, M. S., Al-Emran, M., Alam, S. I., & Faggio, C. (2022). Effects of heavy metals on fish physiology-A review. Chemosphere, 300, 134519. https://doi.org/10.1016/j.chemosphere.2022.134519 DOI: https://doi.org/10.1016/j.chemosphere.2022.134519

Sokolova, I. M., & Lannig, G. (2008). Interactive effects of metal pollution and temperature on metabolism in aquatic ectotherms: Implications of global climate change. Climate Research, 37(2–3), 181–201. https://doi.org/10.3354/cr00764 DOI: https://doi.org/10.3354/cr00764

Sonnack, L., Kampe, S., Muth-Köhne, E., Erdinger, L., Henny, N., Hollert, H., Schäfers, C., & Fenske, M. (2015). Effects of metal exposure on motor neuron development, neuromasts and the escape response of zebrafish embryos. Neurotoxicology and Teratology, 50, 33–42. https://doi.org/10.1016/j.ntt.2015.05.006 DOI: https://doi.org/10.1016/j.ntt.2015.05.006

Strunjak-Perovic, I., Lisicic, D., Coz-Rakovac, R., Topic Popovic, N., Jadan, M., Benkovic, V., & Tadic, Z. (2010). Evaluation of micronucleus and erythrocytic nuclear abnormalities in Balkan whip snake Hierophis gemonensis. Ecotoxicology, 19(8), 1460–1465. https://doi.org/10.1007/s10646-010-0531-y DOI: https://doi.org/10.1007/s10646-010-0531-y

Subotić, S., Spasić, S., Višnjić-Jeftić, Ž., Hegediš, A., Krpo-Ćetković, J., Mićković, B., Skorić, S., & Lenhardt, M. (2013). Heavy metal and trace element bioaccumulation in target tissues of four edible fish species from the Danube River (Serbia). Ecotoxicology and Environmental Safety, 98, 196–202. https://doi.org/10.1016/j.ecoenv.2013.08.020 DOI: https://doi.org/10.1016/j.ecoenv.2013.08.020

Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K., Sutton, D. J., & Luch, A. (2012). Heavy metal toxicity and the environment. In A. Luch (Ed.), Molecular, Clinical and Environmental Toxicology (Vol. 3, pp. 133–164). Springer. https://doi.org/10.1007/978-3-7643-8340-4_6 DOI: https://doi.org/10.1007/978-3-7643-8340-4_6

Tomasello, B., Copat, C., Pulvirenti, V., Ferrito, V., Ferrante, M., Renis, M., Sciacca, S., & Tigano, C. (2012). Biochemical and bioaccumulation approaches for investigating marine pollution using Mediterranean rainbow wrasse, Coris julis (Linnaeus, 1798). Ecotoxicology and Environmental Safety, 86, 168–175. https://doi.org/10.1016/j.ecoenv.2012.09.012 DOI: https://doi.org/10.1016/j.ecoenv.2012.09.012

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

Vivas, A. H., Arboleda, M. A., Sánchez, R., Benítez-Campo, N., Bravo, E., Soto, A., Jiménez, G. A., Muñoz, L. A., & Larmat, F. E. (2015). Evaluación de la mutagenicidad causada por metales pesados presentes en agua del río Cauca en la ciudad de Cali, Colombia. Revista Colombiana de Química, 43(2), 18–24. https://doi.org/10.15446/rev.colomb.quim.v43n2.53119 DOI: https://doi.org/10.15446/rev.colomb.quim.v43n2.53119

Wang, J., Zhang, P., Shen, Q., Wang, Q., Liu, D., Li, J., & Wang, L. (2013). The effects of cadmium exposure on the oxidative state and cell death in the gill of freshwater crab Sinopotamon henanense. PLoS ONE, 8(5), Article e64020. https://doi.org/10.1371/journal.pone.0064020 DOI: https://doi.org/10.1371/journal.pone.0064020

Wang, L., & Gallagher, E. P. (2013). Role of Nrf2 antioxidant defense in mitigating cadmium-induced oxidative stress in the olfactory system of zebrafish. Toxicology and Applied Pharmacology, 266(2), 177–186. https://doi.org/10.1016/j.taap.2012.11.010 DOI: https://doi.org/10.1016/j.taap.2012.11.010

Xu, X., Weber, D., Burge, R., & VanAmberg, K. (2016). Neurobehavioral impairments produced by developmental lead exposure persisted for generations in zebrafish (Danio rerio). NeuroToxicology, 52, 176–185. https://doi.org/10.1016/j.neuro.2015.12.009 DOI: https://doi.org/10.1016/j.neuro.2015.12.009

Younis, E., Abdel-Warith, A.-W., Al-Asgah, N., & Ebaid, H. (2015). Histopathological alterations in the liver and intestine of Nile tilapia Oreochromis niloticus exposed to long-term sublethal concentrations of cadmium chloride. Chinese Journal of Oceanology and Limnology, 33(4), 846–852. https://doi.org/10.1007/s00343-015-4082-1 DOI: https://doi.org/10.1007/s00343-015-4082-1

Yu, B., Wang, X., Dong, K. F., Xiao, G., & Ma, D. (2020). Heavy metal concentrations in aquatic organisms (fishes, shrimp and crabs) and health risk assessment in China. Marine Pollution Bulletin, 159, Article 111505. https://doi.org/10.1016/j.marpolbul.2020.111505 DOI: https://doi.org/10.1016/j.marpolbul.2020.111505

Zapata, A. M., Páez Melo, M. I., Méndez Paz, F., Abrahams Chow, N., Artunduaga Trejos, Y. P., & Ordóñez, J. (2018). Estudio exploratorio de evaluación de riesgo en la salud de madres lactantes por consumo de pescado contaminado del río Cauca, en el Valle del Cauca (Colombia). Ambiente y Desarrollo, 22(43), 1–19. https://doi.org/10.11144/Javeriana.ayd22-43.eeer DOI: https://doi.org/10.11144/Javeriana.ayd22-43.eeer

Zapata, L. M., Bock, B. C., Orozco, L. Y., & Palacio, J. A. (2016). Application of the micronucleus test and comet assay in Trachemys callirostris erythrocytes as a model for in situ genotoxic monitoring. Ecotoxicology and Environmental Safety, 127, 108–116. https://doi.org/10.1016/j.ecoenv.2016.01.016 DOI: https://doi.org/10.1016/j.ecoenv.2016.01.016

Zhang, T., Zhou, X.-Y., Ma, X.-F., & Liu, J.-X. (2015). Mechanisms of cadmium-caused eye hypoplasia and hypopigmentation in zebrafish embryos. Aquatic Toxicology, 167, 68–76. https://doi.org/10.1016/j.aquatox.2015.07.021 DOI: https://doi.org/10.1016/j.aquatox.2015.07.021

Zhou, Q., Zhang, J., Fu, J., Shi, J., & Jiang, G. (2008). Biomonitoring: An appealing tool for assessment of metal pollution in the aquatic ecosystem. Analytica Chimica Acta, 606(2), 135–150. https://doi.org/10.1016/j.aca.2007.11.018 DOI: https://doi.org/10.1016/j.aca.2007.11.018

Zhu, B., Wang, Q., Shi, X., Guo, Y., Xu, T., & Zhou, B. (2016). Effect of combined exposure to lead and decabromodiphenyl ether on neurodevelopment of zebrafish larvae. Chemosphere, 144, 1646–1654. https://doi.org/10.1016/j.chemosphere.2015.10.006 DOI: https://doi.org/10.1016/j.chemosphere.2015.10.056

Published

2026-10-09