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Metal loads and biomarker suite responses in a tropical carnivorous fish indicative of anthropogenic impacts in a Southeastern Brazilian lagoon

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Abstract

Tropical coastal lagoons are highly productive environments exhibiting high biodiversity. However, the use of these ecosystems by local communities is of concern, since this generally leads to environmental degradation. The Imboassica coastal lagoon, located in Macaé city, in Northern Rio de Janeiro, is an important ecosystem in the state, however, already displaying signs of anthropogenic impacts. Carnivorous fish Hoplias malabaricus specimens were sampled from this impacted site, as well as from a reference area. Fish from Imboassica Lagoon presented lower condition factor, lower cholinesterase activity, and higher percentage of erythrocyte micronuclei when compared to fish from the reference site. Metals in fish from Imboassica Lagoon were always higher than Encantada Lagoon, with some seasonal differences, where some metals were higher in the rainy season compared to the dry season in muscle tissue, with the exception of Cu, Fe, Sr, and Zn; and in the liver, except for Ba, Cd, Cr, Ni, and Sr. Cr and Mn in the edible muscle portion of the fish were higher than the limits established by Brazilian and International legislations as permissible for human consumption, thus leading to concerns regarding public health risks for the local population that use fish as their main protein source.

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References

  • Alkan, N., Alkan, A., Gedik, K., & Fisher, A. (2016). Assessment of metal concentrations in commercially important fish species in Black Sea. Toxicology and Industrial Health, 32, 447–456.

    Article  CAS  Google Scholar 

  • Al-Sabti, K., & Metcalfe, C. D. (1995). Fish micronuclei for assessing genotoxicity in water. Mutation Research/Genetic Toxicology, 343, 121–135.

    Article  CAS  Google Scholar 

  • Amiard, J. C., et al. (2006). Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquatic Toxicology, 76, 160–202.

    Article  CAS  Google Scholar 

  • Bastos, W. R., et al. (1998). Establishment and analytical quality control of laboratories for Hg determination in biological and geological samples in the Amazon, Brazil. Ciência e Cultura, 50, 255–260.

    CAS  Google Scholar 

  • Bowles, D. (1999). An overview of the concentrations and effects of metals in cetacean species. Journal of Cetacean Research and Management, 1, 125–148.

    Google Scholar 

  • Calabrese, E. J. (2008). Hormesis: why it is important to toxicology and toxicologists. Environmental Toxicology and Chemistry, 27, 1451–1474.

    Article  CAS  Google Scholar 

  • Calmano, W., et al. (1994). Mobilization and scavenging of heavy metals following resuspension of anoxic sediments from the Elbe river. In C. N. Alpers & D. W. Blowes (Eds.), Environmental geochemistry of Sulfie oxidation (pp. 298–321). Washington, DC: American Chemical Society.

    Google Scholar 

  • Camara, E. M., Caramaschi, É. P., & Petry, A. C. (2011). Fator de condição: bases conceituais, aplicações e perspectivas de uso em pesquisas ecológicas com peixes. Oecologia Australis, 15, 249–274.

    Article  Google Scholar 

  • Campbell, P. G. C., Kraemer, L. D., Giguère, A., Hare, L., & Hontela, A. (2008). Subcellular distribution of cadmium and nickel in chronically exposed wild fish: inferences regarding metal detoxification strategies and implications for setting water quality guidelines for dissolved metals. Human and Ecological Risk Assessment, 14, 290–316.

    Article  CAS  Google Scholar 

  • CONAMA, (2005). RESOLUÇÃO No 357, DE 17 DE MARÇO DE 2005. Publicada no DOU n° 053, de 18/03/2005, págs. 58-63.

  • Eastwood, S., & Couture, P. (2002). Seasonal variations in condition and liver metal concentrations of yellow perch (Perca flavescens) from a metal-contaminated environment. Aquatic Toxicology, 58, 43–56.

    Article  CAS  Google Scholar 

  • Ellman, G. L., Courtney, K. D., Andres Jr., V., & Featherstone, R. M. (1961). A new and rapid colorimetric determination of acetylcholinesterase activity. Biochemical Pharmacology, 7, 88–95.

    Article  CAS  Google Scholar 

  • El-Moselhy, K. M., et al. (2014). Bioaccumulation of heavy metals in some tissues of fish in the Red Sea, Egypt. Egyptian Journal of Basic and Applied Sciences, 1, 97–105.

    Article  Google Scholar 

  • Filipak Neto, F., Zanata, S. M., Silva de Assis, H. C., Bussolaro, D., Ferraro, M. V. M., Randi, M. A. F., Alves Costa, J. R. M., Cestari, M. M., Roche, H., & Oliveira Ribeiro, C. A. (2007). Use of hepatocytes from Hoplias malabaricus to characterize the toxicity of a complex mixture of lipophilic halogenated compounds. Toxicology In Vitro, 21, 706–715.

    Article  CAS  Google Scholar 

  • Frasco, M. F., Colletier, J. P., Weik, M., Carvalho, F., Guilhermino, L., Stojan, J., & Fournier, D. (2007). Mechanisms of cholinesterase inhibition by inorganic mercury. FEBS Journal, 274, 1849–1861.

    Article  CAS  Google Scholar 

  • Fulton, T. W., (1902). The rate of growth of fishes. 20th annual report of the fishery Board of Scotland. 3, 326-446.

  • Fulton, M. H., & Key, P. B. (2001). Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environmental Toxicology and Chemistry, 20, 37–45.

    Article  CAS  Google Scholar 

  • Funk, A. E., et al. (1987). Displacement of zinc and copper from copper-induced metallothionein by cadmium and by mercury: in vivo and ex vivo studies. Comparative Biochemistry and Physiology: Part C, 86, 1–6.

    Article  CAS  Google Scholar 

  • Gorur, F. K., et al. (2012). Radioactivity and heavy metal concentrations of some commercial fish species consumed in the Black Sea region of Turkey. Chemosphere, 87, 356–361.

    Article  CAS  Google Scholar 

  • Hauser-Davis, R. A., Lavandier, R. C., Bastos, F. F., Oliveira, T. F., Ribeiro, C. A. O., Ziolli, R. L., & de Campos, R. C. (2012). Alterations in morphometric and organosomatic indices and histopathological analyses indicative of environmental contamination in mullet, Mugil liza, from southeastern Brazil. Bulletin of Environmental Contamination and Toxicology, 89, 1154–1160.

    Article  CAS  Google Scholar 

  • Hauser-Davis, R. A., Bordon, I. C. A. C., Oliveira, T. F., & Ziolli, R. L. (2016). Metal bioaccumulation in edible target tissues of mullet (Mugil liza) from a tropical bay in southeastern Brazil. Journal of Trace Elements in Medicine and Biology, 36, 38–43.

    Article  CAS  Google Scholar 

  • Heidary, S., et al. (2012). Bioaccumulation of heavy metals Cu, Zn, and Hg in muscles and liver of the stellate sturgeon (Acipenser stellatus) in the Caspian Sea and their correlation with growth parameters Iranian Journal of Fisheries. Sciences, 11, 325–337.

    Google Scholar 

  • Hennemann, M. C., & Petrucio, M. M. (2011). Spatial and temporal dynamic of trophic relevant parameters in a subtropical coastal lagoon in Brazil. Environmental Monitoring and Assessment, 181, 347–361.

    Article  Google Scholar 

  • Henriques-de-Oliveira, C., Baptista, D. F., & Nessimian, J. L. (2007). Sewage input effects on the macroinvertebrate community associated to Typha domingensis Pers in a coastal lagoon in southeastern Brazil. Brazilian Journal of Biology, 67, 73–80.

    Article  CAS  Google Scholar 

  • Javed, M., Ahmad, I., Ahmad, A., Usmani, N., & Ahmad, M. (2016). Studies on the alterations in haematological indices, micronuclei induction and pathological marker enzyme activities in Channa punctatus (spotted snakehead) perciformes, channidae exposed to thermal power plant effluent. Springerplus, 5, 761.

    Article  CAS  Google Scholar 

  • Kalnejais, L. H., et al. (2007). Role of sediment resuspension in the remobilization of particulate-phase metals from coastal sediments. Environmental Science and Technology, 41, 2822–2288.

    Article  CAS  Google Scholar 

  • Kasimoglu, C. (2014). The effect of fish size, age and condition factor on the contents of seven essential elements in Anguilla anguilla from Tersakan Stream Mugla (Turkey). Journal of Pollution Effects and Control, 2, 1–6.

    Article  Google Scholar 

  • Kim, J., & Kang, J. (2016). Oxidative stress, neurotoxicity, and metallothionein (MT) gene expression in juvenile rock fish Sebastes schlegelli under the different levels of dietary chromium (Cr6+) exposure. Ecotoxicology and Environmental Safety, 125, 78–84.

    Article  CAS  Google Scholar 

  • Kozlowsky-Suzuki, B., & Bozelli, R. L. (2002). Experimental evidence of the effect of nutrient enrichment on the zooplankton in a Brazilian coastal lagoon. Brazilian Journal of Biology, 62, 835–846.

    Article  CAS  Google Scholar 

  • Laflamme, J. S., et al. (2000). Interrenal metallothionein and cortisol secretion in relation to cd, cu, and Zn exposure in yellow perch, Perca flavescens, from Abitibi lakes. Canadian Journal of Fisheries and Aquatic Sciences, 57, 1692–1700.

    Article  CAS  Google Scholar 

  • Lemos, C. T., et al. (2001). Evaluation of basal micronucleus frequency and hexavalent chromium effects in fish erythrocytes. Environmental Toxicology and Chemistry, 20, 1320–1324.

    Article  Google Scholar 

  • Lemos, C. T., et al. (2008). Biomonitoring of genotoxicity using micronuclei assay in native population of Astyanax jacuhiensis (Characiformes: Characidae) at sites under petrochemical influence. Science of the Total Environment, 406, 337–343.

    Article  CAS  Google Scholar 

  • Li, L., Chen, H., Bi, R., & Xie, L. (2015). Bioaccumulation, subcellular distribution, and acute effects of chromium in japanese medaka (Oryzias latipes). Environmental Toxicology and Chemistry, 34, 2611–2617.

    Article  CAS  Google Scholar 

  • Lionetto, M. G., et al., (2013). Acetylcholinesterase as a biomarker in environmental and occupational medicine: new insights and future perspectives. Biomed Research International. 321213 pp. 8.

  • Luzhna, L., et al. (2013). Micronuclei in genotoxicity assessment: from genetics to epigenetics and beyond. Frontiers in Genetis, 4, 131.

    CAS  Google Scholar 

  • Nunes, B. (2011). The use of cholinesterases in ecotoxicology. In D. M. Whitacre (Ed.), Reviews of environmental contamination and toxicology (pp. 29–59). New York: Springer New York.

    Google Scholar 

  • Obe, G., Pfeiffer, P., Savage, J. R. K., Johannes, C., Goedecke, W., Jeppesen, P., Natarajan, A. T., Martínez-López, W., Folle, G. A., & Drets, M. E. (2002). Chromosomal aberrations: formation, identification and distribution. Mutation Research, 504, 17–36.

    Article  CAS  Google Scholar 

  • Oliveira, M. M., Silva Filho, M. V., Cunha Bastos, V. L. F., Fernandes, F. C., & Cunha Bastos, J. (2007). Brain acetylcholinesterase as a marine pesticide biomarker using Brazilian fishes. Marine Enviroemental Research, 63, 303–312.

    Article  CAS  Google Scholar 

  • Páez-Osuna, F., Frías-Espericueta, M. G., & Osuna-López, J. I. (1995). Trace metal concentrations in relation to season and gonadal maturation in the oyster Crassostrea iridescens. Marine Environmental Research, 40, 19–31.

    Article  Google Scholar 

  • Panosso, R. F., et al. (1998). Morfometria das lagoas Imboassica, Cabiúnas, Comprida e Carapebus: implicações para o seu funcionamento e manejo. In: F. A. Esteves, (Ed.), Ecologia das lagoas costeiras do Parque Nacional da Restinga de Jurubatiba e do município de Macaé (RJ), Macaé: Núcleo de Pesquisas Ecológicas de Macaé (NUPEM)/Universidade Federal do Rio de Janeiro pp. 464.

  • Potter, V. R. (1955). Tissue homogenates. Methods in Enzymology, 5, 10–15.

    Article  Google Scholar 

  • Rajotte, J., et al., (2003). Indicators of chronic metal stress in wild yellow perch from metal-contaminated environments. In: Conference presentations, mining and environment, 28th annual meeting.

  • Richetti, S. K., Rosemberg, D. B., Ventura-Lima, J., Monserrat, J. M., Bogo, M. R., & Bonan, C. D. (2011). Acetylcholinesterase activity and antioxidant capacity of zebrafish brain is altered by heavy metal exposure. Neurotoxicology, 32, 116–122.

    Article  CAS  Google Scholar 

  • Sanchez-Galan, S., Linde, A. R., Ayllon, F., & Garcia-Vazquez, E. (2001). Induction of micronuclei in eel (Anguilla anguilla L.) by heavy metals. Ecotoxicology and Environmental Safety, 49, 139–143.

    Article  CAS  Google Scholar 

  • Santos, R. F. B., & Ferreira, M. I. P. (2014). Impactos negativos, positivos e propostas mitigadoras em bacias hidrográficas: estudo de caso da BH da Lagoa Imboassica (Macaé-RJ). Boletim do Observatório Ambiental Alberto Ribeiro Lamego, 8, 77–99.

    Article  Google Scholar 

  • Saulnier, I., & Mucci, A. (2000). Trace metal remobilization following the resuspension of estuarine sediments: Saguenay Fjord, Canada. Applied Geochemistry, 15, 203–222.

    Article  Google Scholar 

  • Sinaie, M., Bastami, K. D., Ghorbanpour, M., Najafzadeh, H., Shekari, M., & Haghparast, S. (2010). Metallothionein biosynthesis as a detoxification mechanism in mercury exposure in fish, spotted scat (Scatophagus argus). Fish Physiology and Biochemistry, 36, 1235–1242.

    Article  CAS  Google Scholar 

  • Sipaúba-Tavares, L. H., Guariglia, C. S. T., & Braga, F. M. S. (2007). Effects of rainfall on water quality in six sequentially disposed fishponds with continuous water flow. Brazilian Journal of Biology, 67, 643–649.

    Article  Google Scholar 

  • Skoog, D. A., et al., (1992). Fundamentals of analytical chemistry. Brooks Cole. Fundamentals of analytical chemistry. Fort Worth, Tex Saunders College Pub. 6th ed.

  • Squadrone, S., Prearo, M., Brizio, P., Gavinelli, S., Pellegrino, M., Scanzio, T., Guarise, S., Benedetto, A., & Abete, M. C. (2013). Heavy metals distribution in muscle, liver, kidney and gill of European catfish (Silurus glanis) from Italian rivers. Chemosphere, 90, 358–365.

    Article  CAS  Google Scholar 

  • Udroiu, I. (2006). The micronucleus test in piscine erythrocytes. Aquatic Toxicology, 79, 201–204.

    Article  CAS  Google Scholar 

  • van der Oost, R., Beyer, J., & Vermeulen, N. P. E. (2003). Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environmental Toxicology and Pharmacology, 13, 57–149.

    Article  Google Scholar 

  • Van Dyk, J. S., & Pletschke, B. (2011). Review on the use of enzymes for the detection of organochlorine, organophosphate and carbamate pesticides in the environment. Chemosphere, 82, 291–307.

    Article  CAS  Google Scholar 

  • Vicari, M. R., Pazza, R., Artoni, R. F., Margarido, V. P., & Bertollo, L. A. C. (2006). Cytogenetics and biogeography: considerations about the natural origin of Hoplias malabaricus (Characiformes, Erythrinidae) on the Iguaçu river. Brazilian Archives of Biology and Technology, 49, 297–303.

    Article  Google Scholar 

  • Yadav, K. K., & Trivedi, S. P. (2009). Sublethal exposure of heavy metals induces micronuclei in fish, Channa punctata. Chemosphere, 77, 1495–1500.

    Article  CAS  Google Scholar 

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Coimbra, R.S.C., Mascarenhas, M.S., Saraiva, V.B. et al. Metal loads and biomarker suite responses in a tropical carnivorous fish indicative of anthropogenic impacts in a Southeastern Brazilian lagoon. Environ Monit Assess 190, 564 (2018). https://doi.org/10.1007/s10661-018-6910-1

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