06OCT

News on Acta Limnologica Brasiliensia to our fellow Limnologists

Fellow Limnologist! Click here to access the latest report from the editorial board of Acta Limnologica Brasiliensia.

Acta Limnologica Brasiliensia
https://actalb.org/article/doi/10.1590/S2179-975X7821
Acta Limnologica Brasiliensia
Original Article

Acute toxicity of potentially toxic elements on ciliated protozoa from Lake Maracaibo (Venezuela)

Toxicidade aguda de elementos potencialmente tóxicos em protozoários ciliados do Lago de Maracaibo (Venezuela)

Julio César Marín-Leal; Neil José Rincón-Miquilena; Laugeny Chiquinquirá Díaz-Borrego; María Carolina Pire-Sierra

Downloads: 0
Views: 130

Abstract

Abstract:: Aim: In this article the acute ecotoxicological effects of Cr(III), Cr(VI), Cd(II) and V(V) on ciliated protozoa isolated from Lake Maracaibo were evaluated, by estimating of the LC50 for an exposure time of 1-h and observations every 5 min.

Methods: Isolations and cultures of ciliated protozoa were made from surface water samples to then carry out toxicity essays under static and controlled conditions, identifying cell immobility (death) as the endpoint.

Results: The response of the ciliated protozoa made it possible to unequivocally determine the acute toxicity in presence of potentially toxic elements (PTE), with variable mortalities depending on the gender, the element tested and its concentration. The results obtained with Euplotes sp. indicate that protozoan is a sensitive biomonitor indicated for the biomonitoring of PTE contamination in Lake Maracaibo.

Conclusions: The use of shorter exposure periods offers opportunities to show early toxicity effects on natural populations and to act in a timely manner (early warning systems) in contamination events by PTEs, as well as the development of sensitive and rapid biomonitoring methods for detection of these elements in the environment.

Keywords

Euplotes sp., heavy metal, lethal concentration, short-term exposure, zooplankton

Resumo

Resumo:: Objetivo: Neste artigo, os efeitos ecotoxicológicos agudos de Cr(III), Cr(VI), Cd(II) e V(V) foram avaliados em protozoários ciliados isolados do Lago de Maracaibo, estimando o CL50 para um tempo de 1 h exposição e observações a cada 5 min.

Métodos: Isolamentos e culturas de protozoários ciliados foram feitos a partir de amostras de águas superficiais para então realizar testes de toxicidade em condições estáticas e controladas, identificando a imobilidade celular (morte) como critério de avaliação.

Resultados: A resposta dos protozoários ciliados permitiu determinar inequivocamente a toxicidade aguda na presença de elementos potencialmente tóxicos (EPT), com mortalidades variáveis ​​dependendo do gênero, do elemento testado e da sua concentração. Os resultados obtidos com Euplotes sp. indicam que o protozoário é um biomonitor sensível e indicado para o biomonitoramento de contaminação por EPT no Lago Maracaibo.

Conclusões: O uso de períodos de exposição mais curtos oferece oportunidades de mostrar os efeitos da toxicidade precoce em populações naturais e de atuar em tempo hábil (sistemas de alerta precoce) em eventos de contaminação de EPT, bem como o desenvolvimento de métodos de biomonitoramento sensíveis e rápidos para a detecção desses elementos no meio ambiente.
 

Palavras-chave

Euplotes sp., metal pesado, concentração letal, exposição de curto prazo, zooplâncton

References

Abdel-Gawad, S.S., 2006. Toxicity and bioaccumulation of cadmium in the freshwater bivalve Corbicula fluminalis Müller, 1774. Egypt. J. Aquat. Biol. Fish. 10(4), 33-43. http://dx.doi.org/10.21608/ejabf.2006.1899.

Alayo, M., & Iannacone, J., 2002. Ensayos ecotoxicológicos con petróleo crudo, diésel 2 y diésel 6 con dos subespecies de Brachionus plicatilis Müller 1786 (Rotifera: Monogononta). Gayana, 66(1), 45-58. http://dx.doi.org/10.4067/S0717-65382002000100007.

Ali, H., & Khan, E., 2018. Trophic transfer, bioaccumulation, and biomagnification of non-essential hazardous heavy metals and metalloids in food chains/webs - concepts and implications for wildlife and human health. Hum. Ecol. Risk Assess. 2018, 1353-1376.

Amaro, F., Turkewitz, A.P., Martín-González, A., & Gutiérrez, J.C., 2011. Whole-cell biosensors for detection of heavy metal ions in environmental samples based on metallothionein promoters from Tetrahymena thermophila. Microb. Biotechnol. 4(4), 513-522. PMid:21366892. http://dx.doi.org/10.1111/j.1751-7915.2011.00252.x.

American Public Health Association – APHA, 2017. Standard methods for the examination of water and wastewater (23th ed.). Washington: APHA.

Aslam, S., & Yousafzai, A.M., 2017. Chromium toxicity in fish: a review article. J. Entomol. Zool. Stud. 5(3), 1483-1488.

Ávila, H., Gutiérrez, E., Ledo, H., Araujo, M., & Sánquiz, M., 2010. Heavy metals distribution in superficial sediments of Maracaibo Lake (Venezuela). Rev. Tec. Fac. Ing. Univ. Zulia, 33(2), 122-129.

Blanck, H., & Wängberg, S., 1988. Validity of an ecotoxicological test system: short-term and long-term effects of arsenate on marine periphyton communities in laboratory systems. Can. J. Fish. Aquat. Sci. 45(10), 1807-1815. http://dx.doi.org/10.1139/f88-212.

Borsari, M., 2014. Cadmium: inorganic chemistry. In: Scott, R.A., ed. Encyclopedia of inorganic and bioinorganic chemistry. New York: John Wiley & Sons. p. 56-87.

Bracho, G., Cuador-Gil, J.Q., & Rodríguez-Fernández, R.M., 2016. Calidad del agua y sedimento en el Lago de Maracaibo, estado Zulia. Miner. Geol. 32(1), 1-14.

Cáceres, A., 2012. La Creole Petroleum Corporation en Venezuela: la gran fusión petrolera de los años cuarenta. Debates IESA, 2012(17), 58-61.

Canadian Council of Ministers of the Environment – CCME, 1999. Canadian water quality guidelines for the protection of aquatic life: chromium-hexavalent chromium and trivalent chromium. In: Canadian environmental quality guidelines. Winnipeg: CCME.

Canadian Council of Ministers of the Environment – CCME, 2014. Canadian water quality guidelines for the protection of aquatic life: cadmium. In: Canadian environmental quality guidelines. Winnipeg: CCME.

Castro, F., & Marín, J., 2018. Comparación de la ecotoxicidad por metales pesados sobre bacterias heterótrofas de dos sitios contrastados del Lago de Maracaibo (Venezuela). Rev. Fac. Cienc. Básicas 14, 1-10.

Colina de Vargas, M., & Romero, R., 1992. Mercury determination by cold vapour atomic absorption spectrometry in several biological indicators from Lake Maracaibo, Venezuela. Analyst, 117(3), 645-647. PMid:1580413. http://dx.doi.org/10.1039/an9921700645.

Colina, M., 2001. Determination of nutrients and heavy metal species in samples from Lake Maracaibo [Doctoral dissertation]. Sheffield: Sheffield Hallam University.

Contraloría General de la República – CGR, 2010. Actuación coordinada en el sistema nacional de control fiscal para evaluar los problemas ambientales y el deterioro de las relaciones ecológicas en la cuenca del río más importante de cada entidad federal [online]. Caracas. Retrieved in 2020, May 12, from: http://www.cgr.gob.ve

Corona, J., 2013. Contaminación antropogénica en el Lago de Maracaibo, Venezuela. Biocenosis 27(1-2), 85-93.

Díaz, S., Martín-González, A., & Gutiérrez, J.C., 2006. Evaluation of heavy metal acute toxicity and bioaccumulation in soil ciliated protozoa. Environ. Int. 32(6), 711-717. PMid:16650895. http://dx.doi.org/10.1016/j.envint.2006.03.004.

Díaz-Borrego, L., Dupontt, J., Espina, K., Rincón, N., García, M., & Atencio, L., 2007. Utilización de sustratos orgánicos y resistencia a metales pesados por bacterias asociadas a Lemna spp. Bol. Cent. Invest Biol. 41(1), 27-43.

Dunlop, S., & Chapman, G., 1981. Detoxification of zinc and cadmium by the freshwater protozoan Tetrahymena pyriformis. Environ. Res. 24(2), 264-274. http://dx.doi.org/10.1016/0013-9351(81)90156-0.

El-Serehy, H., Al-Rasheid, K., & Shafik, H., 2012. Microbial loop populations: their abundances and trophodynamics in the Gulf of Aqaba, Red Sea. Turk. J. Fish. Aquat. Sci. 12, 565-573.

Fang, Z., Zhao, M., Zhen, H., Chen, L., Shi, P., & Huang, Z., 2014. Genotoxicity of tri- and hexavalent chromium compounds in vivo and their modes of action on DNA damage in vitro. PLoS One 9(8), e103194. PMid:25111056. http://dx.doi.org/10.1371/journal.pone.0103194.

Faure, V., Pinazo, C., Torréton, J., & Jacquet, S., 2010. Modelling the spatial and temporal variability of the SW lagoon of New Caledonia I: a new biogeochemical model based on microbial loop recycling. Mar. Pollut. Bull. 61(7-12), 465-479. PMid:20667554. http://dx.doi.org/10.1016/j.marpolbul.2010.06.041.

Fernandez-Leborans, G., & Olalla Herrero, Y., 2000. Toxicity and bioaccumulation of lead and cadmium in marine protozoan communities. Ecotoxicol. Environ. Saf. 47(3), 266-276. PMid:11139180. http://dx.doi.org/10.1006/eesa.2000.1944.

Foissner, W., & Berger, H., 1996. A user-friendly guide to the ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology. Freshw. Biol. 35(2), 375-482. http://dx.doi.org/10.1111/j.1365-2427.1996.tb01775.x.

Foissner, W., 1999. Protist diversity: estimates of the near-imponderable. Protist 150(4), 363-368. PMid:10714770. http://dx.doi.org/10.1016/S1434-4610(99)70037-4.

Fried, J., Ludwig, W., Psenner, R., & Schleifer, K.H., 2002. Improvement of ciliate identification: a new protocol for fluorescence in situ hybridization (FISH) in combination with silver stain techniques. Syst. Appl. Microbiol. 25(4), 555-571. PMid:12583717. http://dx.doi.org/10.1078/07232020260517706.

Gadd, G.M., 2010. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156(Pt 3), 609-643. PMid:20019082. http://dx.doi.org/10.1099/mic.0.037143-0.

Girling, A.E., Pascoe, D., Janssen, C.R., Peither, A., Wenzel, A., Schäfer, H., Neumeier, B., Mitchell, G.C., Taylor, E.J., Maund, S.J., Lay, J.P., Jüttner, I., Crossland, N.O., Stephenson, R.R., & Persoone, G., 2000. Development of methods for evaluating toxicity to freshwater ecosystems. Ecotoxicol. Environ. Saf. 45(2), 148-176. PMid:10648133. http://dx.doi.org/10.1006/eesa.1999.1847.

Gomiero, A., Dagnino, A., Nasci, C., & Viarengo, A., 2013. The use of protozoa in ecotoxicology: application of multiple endpoint tests of the ciliate E. crassus for the evaluation of sediment quality in coastal marine ecosystems. Sci. Total Environ. 442, 534-544. PMid:23202299. http://dx.doi.org/10.1016/j.scitotenv.2012.10.023.

Gomiero, A., Sforzini, S., Dagnino, A., Nasci, C., & Viarengo, A., 2012. The use of multiple endpoints to assess cellular responses to environmental contaminants in the interstitial marine ciliate Euplotes crassus. Aquat. Toxicol. 114-115, 206-216. PMid:22459342. http://dx.doi.org/10.1016/j.aquatox.2012.02.030.

Guertin, J., 2005. Toxicity and health effects of chromium (all oxidation states). In: Guertin, J., Avakiam, C.P. & Jacobs, J.A., eds. Chromium (VI) handbook. Boca Raton: CRC Press, 216-234.

Gupta, A.K., & Rajbanshi, V.K., 1988. Acute toxicity of cadmium to Channa punctatus (BLOCH). Acta Hydrochim. Hydrobiol. 16(5), 525-535. http://dx.doi.org/10.1002/aheh.19880160513.

Gustafsson, J.P., 2019. Vanadium geochemistry in the biogeosphere -speciation, solid-solution interactions, and ecotoxicity. J. Appl. Geochem. 102, 1-25. http://dx.doi.org/10.1016/j.apgeochem.2018.12.027.

Hong, Y.J., Liao, W., Yan, Z.F., Bai, Y.C., Feng, C.L., Xu, Z.X., & Xu, D.Y., 2020. Progress in the research of the toxicity effect mechanisms of heavy metals on freshwater organisms and their water quality criteria in China. J. Chem. 2020, 1-12. http://dx.doi.org/10.1155/2020/9010348.

Isibor, P.O., Imoobe, T.O., Dedeke, G.A., Adagunodo, T.A., & Taiwo, O.S., 2020. Health risk indices and zooplankton-based assessment of a tropical rainforest river contaminated with iron, lead, cadmium, and chromium. Sci. Rep. 10(1), 16896. PMid:33037243. http://dx.doi.org/10.1038/s41598-020-72526-1.

Jaishankar, M., Tseten, T., Anbalagan, N., Mathew, B., & Beeregowda, K., 2014. Toxicity, mechanism and health effects of some heavy metals. Interdiscip. Toxicol. 7(2), 60-72. PMid:26109881. http://dx.doi.org/10.2478/intox-2014-0009.

Kamika, I., & Momba, M.N.B., 2013. Synergistic effects of vanadium and nickel on heavy metal-tolerant microbial species in wastewater systems. Desalin. Water Treat. 51(40-42), 7431-7446. http://dx.doi.org/10.1080/19443994.2013.777680.

Kamika, I., & Momba, M.N.B., 2014. Effect of vanadium toxicity at its different oxidation states on selected bacterial and protozoan isolates in wastewater systems. Environ. Technol. 35(13-16), 2075-2085. PMid:24956802. http://dx.doi.org/10.1080/09593330.2014.893023.

Kuhn, R., Pattard, M., Pernak, K., & Winter, A., 1989. Results of the harmful effects of water pollutants to Daphnia magna in the 21 day reproduction test. Water Res. 23(4), 501-510. http://dx.doi.org/10.1016/0043-1354(89)90142-5.

Liu, J., Qu, W., & Kadiiska, M.B., 2009. Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicol. Appl. Pharmacol. 238(3), 209-214. PMid:19236887. http://dx.doi.org/10.1016/j.taap.2009.01.029.

Lynn, D., 2008. The ciliated protozoa (3rd ed.). Bern: Springer Science and Business Media B.V.

Madoni, P., & Romeo, M.G., 2006. Acute toxicity of heavy metals towards freshwater ciliated protists. Environ. Pollut. 141(1), 1-7. PMid:16198032. http://dx.doi.org/10.1016/j.envpol.2005.08.025.

Madoni, P., Davoli, D., & Gorbi, G., 1994. Acute toxicity of lead, chromium and other heavy metals to ciliates from activated sludge plants. Bull. Environ. Contam. Toxicol. 53(3), 420-425. PMid:7919720. http://dx.doi.org/10.1007/BF00197235.

Madoni, P., Davoli, D., Gorbi, G., & Vescovi, L., 1996. Toxic effect of heavy metals on the activated Sludge protozoan community. Water Res. 30(1), 135-141. http://dx.doi.org/10.1016/0043-1354(95)00124-4.

Mannazzu, I., 2001. Vanadium detoxification and resistance in yeast: a mini-review. Ann. Microbiol. 51(1), 1-9.

Marín-Leal, J.C., Carrasquero-Ferrer, S.C., Pire-Sierra, M.C., & Behling de Calmón, E.H., 2017. Dynamic of priority pollutants and wastewater adequacy in the Lake Maracaibo basin (Venezuela). In: Araújo, C.V.M. & Shinn, C., eds. Ecotoxicology in Latin America. New York: Nova Science Publishers, Chapter 29, 457-479.

Martin, T.R., & Holdich, D.M., 1986. The acute lethal toxicity of heavy metals to peracarid crustaceans (with particular reference to fresh-water asellids and gammarids). Water Res. 20(9), 1137-1147. http://dx.doi.org/10.1016/0043-1354(86)90060-6.

Martín-González, A., Díaz, S., Borniquel, S., Gallego, A., & Gutiérrez, J.C., 2006. Cytotoxicity and bioaccumulation of heavy metals by ciliated protozoa isolated from urban wastewater treatment plants. Res. Microbiol. 157(2), 108-118. PMid:16129584. http://dx.doi.org/10.1016/j.resmic.2005.06.005.

Maurya, R., & Pandey, A.K., 2020. Importance of protozoa Tetrahymena in toxicological studies: a review. Sci. Total Environ. 741, 140058. PMid:32599397. http://dx.doi.org/10.1016/j.scitotenv.2020.140058.

Moore, J.W., 1991. Chromium. In: Moore, J.W., ed. Inorganic contaminants of surface water: research and monitoring priorities. New York: Springer-Verlag New York, 83-97. http://dx.doi.org/10.1007/978-1-4612-3004-5_9.

Mortimer, M., Kasemets, K., & Kahru, A., 2010. Toxicity of ZnO and CuO nanoparticles to ciliated protozoa Tetrahymena thermophila. Toxicology 269(2-3), 182-189. PMid:19622384. http://dx.doi.org/10.1016/j.tox.2009.07.007.

Mukherjee, B., Halder, S., Ghosh, M.K., & Manasadeepa, R., 2013. Vanadium ions and proteins, distribution, metabolism, and biological significance. In: Uversky, V.N., ed. Encyclopedia of metalloproteins. Bern: Springer Science, 2306-2316. http://dx.doi.org/10.1007/978-1-4614-1533-6_136.

Nalecz-Jawecki, G., Demkowicz-Dobrzainski, K., & Sawicki, J., 1993. Protozoan Spirostomum ambiguum as a highly sensitive bioindicator for rapid and easy determination of water quality. Sci. Total Environ. 134(Suppl.1993), 1227-1234. http://dx.doi.org/10.1016/S0048-9697(05)80128-7.

Narayanan, N., Priya, M., Haridas, A., & Manilal, V.B., 2007. Isolation and culturing of a most common anaerobic ciliate, Metopus sp. Anaerobe 13(1), 14-20. PMid:17223583. http://dx.doi.org/10.1016/j.anaerobe.2006.10.003.

Nilsson, J., 1981. Effects of copper on phagocytosis in Tetrahymena. Protoplasma 109(3-4), 359-370. http://dx.doi.org/10.1007/BF01287453.

Okamoto, A., Yamamuro, M., & Tatarazako, N., 2015. Acute toxicity of 50 metals to Daphnia magna. J. Appl. Toxicol. 35(7), 824-830. PMid:25382633. http://dx.doi.org/10.1002/jat.3078.

Paiva, T.S., Borges, B.N., & Silva-Neto, I.D., 2013. Phylogenetic study of class Armophorea (Alveolata, Ciliophora) based on 18S-rDNA data. Genet. Mol. Biol. 36(4), 571-585. PMid:24385862. http://dx.doi.org/10.1590/S1415-47572013000400017.

Panda, S.K., & Choudhury, S., 2005. Chromium stress in plants. Braz. J. Plant Physiol. 17(1), 95-102. http://dx.doi.org/10.1590/S1677-04202005000100008.

Parra-Pardi, G., 1979. Estudio integral sobre la contaminación del Lago de Maracaibo y sus afluentes, parte II: evaluación del proceso de eutroficación. Caracas: Ministerio del Ambiente y de los Recursos Naturales Renovables.

Piccinni, E., Irato, P., Coppellotti, O., & Guidolin, L., 1987. Biochemical and ultrastructural data on Tetrahymena pyriformis treated with copper and cadmium. J. Cell Sci. 88(Pt 3), 283-293. PMid:3129439. http://dx.doi.org/10.1242/jcs.88.3.283.

Pickering, Q.H., & Henderson, C., 1966. The acute toxicity of some heavy metals of different species of warmwater fishes. Air Water Pollut. 10(6), 453-463. PMid:5946974.

Plaper, A., Jenko-Brinovec, S., Premzl, A., Kos, J., & Raspor, P., 2002. Genotoxicity of trivalent chromium in bacterial cells. Possible effects on DNA topology. Chem. Res. Toxicol. 15(7), 943-949. PMid:12119005. http://dx.doi.org/10.1021/tx010096q.

Poirier, I., Hammann, P., Kuhn, L., & Bertrand, M., 2013. Strategies developed by the marine bacterium Pseudomonas fluorescens BA3SM1 to resist metals: a proteome analysis. Aquat. Toxicol. 128-129, 215-232. PMid:23314334. http://dx.doi.org/10.1016/j.aquatox.2012.12.006.

Premke, K., & Arndt, H., 2000. Predation on heterotrophic flagellates by protist: food selectivity determined using a live-staining technique. Arch. Hydrobiol. 150(1), 17-28. http://dx.doi.org/10.1127/archiv-hydrobiol/150/2000/17.

Pudpong, S., & Chantangsi, C., 2015. Effects of four heavy metals on cell morphology and survival rate of the ciliate Bresslauides sp. Trop. Nat. Hist. 15(2), 117-125.

Qing-Hua, C., Run-Lin, X., Nora, F.Y.T., Siu G.C. & Paul, K.S.S., 2008. Use of ciliates (Protozoa: Ciliophora) as bioindicator to assess sediment quality of two constructed mangrove sewage treatment belts in Southern China. Mar. Pollut. Bull. 57(6-12), 689-694.

Rico, D., Martín-González, A., Díaz, S., De Lucas, P., & Gutiérrez, J.C., 2009. Heavy metals generate reactive oxygen species in terrestrial and aquatic ciliated protozoa. Comp. Biochem. Physiol. Part C Toxicol Pharmacol. 149(1), 90-96. PMid:18725323. http://dx.doi.org/10.1016/j.cbpc.2008.07.016.

Rodríguez, G., 2000. El sistema de Maracaibo, biología y ambiente. Caracas: Instituto Venezolano de Investigaciones Científicas.

Rojas, J., 2012. Polymesoda solida como bioindicador de metales pesados en el sistema del Lago de Maracaibo [Doctoral dissertation]. Maracaibo: Universidad del Zulia.

Rojas, J., Rincón, J., Marín, J., Ortega, P., Buonocore, R., Colina, M., & Montilla, J., 2015. Toxicidad y bioacumulación de cromo (Cr+6) en la almeja Polymesoda solida del sistema estuarino Lago de Maracaibo. Bol. Cent. Inv. Biol. 49(1), 5-25.

Sanders, C.L., 1986. Toxicological aspect of energy production. New York: MacMillan Publishing Company.

Sauvant, M.P., Pepin, D., Groliere, C.A., & Bohatier, J., 1995. Effects of organic and inorganic substances on the cell proliferation of L-929 fibroblasts and Tetrahymena pyriformis GL protozoa used for toxicological bioassays. Bull. Environ. Contam. Toxicol. 55(2), 171-178. PMid:7579920. http://dx.doi.org/10.1007/BF00203006.

Shi, W., Zhao, X., Han, Y., Che, Z., Chai, X., & Liu, G., 2016. Ocean acidification increases cadmium accumulation in marine bivalves: a potential threat to seafood safety. Sci. Rep. 6(1), 20197. PMid:26795597. http://dx.doi.org/10.1038/srep20197.

Simanov, L., 1987. Toxic effect of copper and cadmium on algae and protozoa. Inst. Land Ecol. Czech. Acad. Sci. 28, 81-82.

Stendahl, D.H., & Sprague, J.B., 1982. Effects of water hardness and pH on vanadium lethality to rainbow trout. Water Res. 16(10), 1479-1488. http://dx.doi.org/10.1016/0043-1354(82)90246-9.

U. S. Environmental Protection Agency – USEPA, 1985. Ambient water quality criteria for chromium - 1984, EPA-440/5-84-031. Washington: USEPA.

Vignati, D.A.L., Dominik, J., Beye, M.L., Pettine, M., & Ferrari, B.J.D., 2010. Chromium (VI) is more toxic than chromium (III) to fresh water algae: a paradigm to revise? Ecotoxicol. Environ. Saf. 73(5), 743-749. PMid:20138363. http://dx.doi.org/10.1016/j.ecoenv.2010.01.011.

Vilas-Boas, J.A., Xavier, M., & Pedroso, R., 2020. Ciliates in ecotoxicological studies: a minireview. Acta Limnol. Bras. 32, e202. http://dx.doi.org/10.1590/s2179-975x6719.

Wang, Y., Fang, J., Leonard, S.S., & Krishna Rao, K.M., 2004. Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic. Biol. Med. 36(11), 1434-1443. PMid:15135180. http://dx.doi.org/10.1016/j.freeradbiomed.2004.03.010.

Wong, M.H., Lau, W.M., Tong, T.Y., Liu, W.K., & Luk, K.C., 1982. Toxic effects of chromic sulphate on the common carp, Cyprinus carpio. Toxicol. Lett. 10(2-3), 225-232. PMid:7080089. http://dx.doi.org/10.1016/0378-4274(82)90079-0.

World Health Organization – WHO, 2009. Inorganic chromium (III) compounds, concise international chemical assessment document 76. Huntingdon: WHO.
 


Submitted date:
12/13/2021

Accepted date:
08/16/2022

Publication date:
09/06/2022

6317a3daa953954ac04009b5 alb Articles
Links & Downloads

Acta Limnol. Bras. (Online)

Share this page
Page Sections