Biomarkers responses in fish (Atherinella brasiliensis) of paranaguá bay, southern Brazil, for assessment of pollutant effects

Ribeiro, Ciro Alberto de Oliveira; Katsumiti, Alberto; França, Patrícia; Maschio, Jocieli; Zandoná, Eliandra; Cestari, Marta Margarete; Vicari, Thainá; Roche, Hélène; Assis, Helena Cristina Silva de; Filipak Neto, Francisco

Abstracts

Paranaguá bay is a complex estuary located in southern Brazil containing three protected areas listed by UNESCO. Historically, the estuary has been affected by urban, industrial, agricultural and harbor activities, and occasional accidents. Specifically, the explosion of the Chilean ship Vicuña in December 2004 spilled methanol and crude and fuel oils which affected both protected and non-protected areas. The present study sought to investigate the pollution threat to aquatic organisms in order to evaluate the potential effects of pollutants. One hundred and twenty adult fish Atherinella brasiliensis were collected from different sites within Paranaguá estuary, including the harbor and open ocean, during summer, autumn and winter of 2005. Among the biomarkers, the somatic index, chemical analysis of bile, biochemical, genetic and morphological parameters were considered. Chemical analysis of bile showed a continuous bioavailability of polycyclic aromatic hydrocarbons (PAHs) according to proximity to the harbor site. The histopathological findings have demonstrated aconsiderable incidence of severe pathologies in the liver and gills, corroborated by biochemical disturbances and genetic damage. These findings indicate that more studies are necessary to evaluate both water quality and fish health so as to permit a better analysis of the impact of pollution in Paranaguá estuary.

Biomonitoring; Biomarkers; Aterinella brasiliensis; Paranaguá bay

A Baia de Paranaguá é um complexo estuarino localizado no sul do Brasil constituído de três áreas de proteção ambiental listadas pela UNESCO. Historicamente, o estuário tem sido afetado por atividade urbana, industrial, agricultura e portuária, e eventualmente por acidentes. Particularmente a explosão do navio Chileno Vicuña em dezembro de 2004 derramou metanol, óleo cru e combustível atingindo áreas protegidas e não protegidas. O presente estudo tem por objetivo investigar a poluição em organismos aquáticos. Cento e vinte indivíduos adultos do peixe Atherinella brasiliensis foram coletados em quatro diferentes pontos de coleta no estuário de Paranaguá, partindo do porto até o oceano aberto nos períodos de verão, inverno e primavera de 2005. Os índices somáticos, parâmetros químicos, enzimáticos, genéticos e morfológicos foram considerados. As análises histopatológicas demonstraram expressiva incidência de patologia no fígado e nas brânquias algumas vezes corroboradas pelas alterações bioquímicas. Danos genéticos e anormalidades genéticas também foram observados. As análises químicas na bile mostraram uma contínua biodisponibilidade de hidrocarbonetos policíclicos aromáticos para os organismos aquáticos. Os dados obtidos indicam que a qualidade da água e a saúde dos peixes encontram-se bastante comprometidos no estuário de Paranaguá.

Biomonitoramento; Biomarcadores; Aterinella brasiliensis; Baia de Paranaguá

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AKAISHI, F. M.; ST-JEAN, S. D.; BISHAY, F.; CLARKE, J.; RABITTO, I.S.; OLIVEIRA RIBEIRO, C.A. Immunological responses, histopathological finding and disease resistance of blue mussel (Mytilus edulis) exposed to treated and untreated municipal wastewater. Aquat. Toxicol v. 82, p. 1-14, 2007.
ALBERTO, A.; CAMARGO, A. D. M.; VERANI, J. R.; COSTA, O. F. T.; FERNANDES, M. N. Heath variables and gill morphology in the tropical fish Astyanax fasciatus from a sewage contaminated river. Ecotox. Environ. Saf., v. 61, p. 247-255, 2005.
AL-SABTI, K.; METCALFE, C. D. Fish micronuclei for assessing genotoxicity in water. Mutat. Res, v. 343, p. 121-135, 1995.
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BURKE, M. D.; MAYER, R. T. Ethoxyresorufin: direct fluorimetric assay of a microssomal O-dealkylation which is preferentially inducible by 3-methylcholantrene. Drug Metabol. Dispos, v. 2, p. 583-588, 1974.
CARRASCO, K. R.; TILBURY, K. L.; MYERS, M .S. Assessment of the piscine micronucleus test as in situ biological indicator of chemical contaminant effects. Can. J. Fish Aquat. Sci, v. 47, p. 2123-2136, 1990.
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COLLINS, A.; DUSINSKÁ, M.; FRANKLIN, M.; PETROVSKÁ, H.; DUTHIE, S.; FILLION, L.; PANAYIOTIDIS, M.; RASLOVÁ, K.; VAUGHAN, N. Comet assay in human biomonitoring studies: reliability, validation, and applications. Environ. Mol. Mutagen, v. 30, n. 2, p. 139-146, 1997.
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Publication Dates

Publication in this collection
17 Apr 2013
Date of issue
Mar 2013

History

Received
14 Apr 2011
Accepted
17 Jan 2013
Reviewed
29 Nov 2012

This work is licensed under a Creative Commons Attribution 4.0 International License.

[1] AAS, E.; KLUGSOYR, J. PAH metabolites in bile and EROD activity in North Sea Fish. Mar. Environ Res, v. 46, n.1-5, p. 229-232, 1998.

[2] AAS, E.; BEYER, I.; GOKSOYR, A. Fixed wavelength fluorescence (FF) of bile as a monitoring tool for polyaromatic hydrocarbon exposure in fish: an evaluation of compound specificity, inner filter effect and signal interpretation. Biomarkers, v. 5, p. 9-23, 2000.

[3] AEBI, H. Catalase in vitro. Meth. Enzymol, v. 105, p. 121-126, 1984.

[4] AKAISHI, F.M.; SILVA DE ASSIS, H. C.; JAKOBI, S. S. G.; EIRAS-STOFELLA, D. R.; ST-JEAN, S. D.; COURTENAY, S. C.; LIMA, E. F.; WAGENER, A. L. R.; SCOFIELD, A. L.; OLIVEIRA RIBEIRO, C. A. Morphological and neurotoxicological findings in tropical freshwater fish (Astyanax sp.) after waterborne and acute exposure to water soluble fraction (wsf) of crude oil. Arch. Environ. Con. Tox., v. 46, p. 244-253, 2004.

[5] AKAISHI, F. M.; ST-JEAN, S. D.; BISHAY, F.; CLARKE, J.; RABITTO, I.S.; OLIVEIRA RIBEIRO, C.A. Immunological responses, histopathological finding and disease resistance of blue mussel (Mytilus edulis) exposed to treated and untreated municipal wastewater. Aquat. Toxicol v. 82, p. 1-14, 2007.

[6] ALBERTO, A.; CAMARGO, A. D. M.; VERANI, J. R.; COSTA, O. F. T.; FERNANDES, M. N. Heath variables and gill morphology in the tropical fish Astyanax fasciatus from a sewage contaminated river. Ecotox. Environ. Saf., v. 61, p. 247-255, 2005.

[7] AL-SABTI, K.; METCALFE, C. D. Fish micronuclei for assessing genotoxicity in water. Mutat. Res, v. 343, p. 121-135, 1995.

[8] ALVES COSTA, J. R. M.; MELA, M.; SILVA DE ASSIS, H. C.; PELLETIER, E.; RANDI, M. A. F.; OLIVEIRA RIBEIRO, C. A. Enzymatic inhibition and morphological changes in Hoplias malabaricus from dietary exposure to lead (II) or methylmercury. Ecotox. Environ. Saf., v. 67, p. 82-88, 2007.

[9] ANDRIGHETTI-FRÖHNER, C. R.; KRATZ, J. M.; ANTONIO, R. V.; CRECZYNSKI-PASA, T. B.; BARARDI, C. R. M.; SIMÕES, C. M. O. In vitro testing for genotoxicity of violacein assessed by Comet and Micronucleus assays. Mutat. Res., v.603, p. 97-103, 2006.

[10] BRADFORD, M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Ann. Bioch, v. 72, p. 248-254, 1976.

[11] BURKE, M. D.; MAYER, R. T. Ethoxyresorufin: direct fluorimetric assay of a microssomal O-dealkylation which is preferentially inducible by 3-methylcholantrene. Drug Metabol. Dispos, v. 2, p. 583-588, 1974.

[12] CARRASCO, K. R.; TILBURY, K. L.; MYERS, M .S. Assessment of the piscine micronucleus test as in situ biological indicator of chemical contaminant effects. Can. J. Fish Aquat. Sci, v. 47, p. 2123-2136, 1990.

[13] CARRELL, C. J.; CARRELL, T. G.; CARRELL, H. L.; PROUT, K.; GLUSKE, J.P. Benzo[a]pyrene and its analogues: structural studies of molecular strain. Carcinogenesis, v. 18, n. 2, p. 415-422, 1997.

[14] COLLINS, A.; DUSINSKÁ, M.; FRANKLIN, M.; PETROVSKÁ, H.; DUTHIE, S.; FILLION, L.; PANAYIOTIDIS, M.; RASLOVÁ, K.; VAUGHAN, N. Comet assay in human biomonitoring studies: reliability, validation, and applications. Environ. Mol. Mutagen, v. 30, n. 2, p. 139-146, 1997.

[15] DAMÁSIO, J. B.; BARATA, C.; MUNNÉ, A.; GINEBREDA, A.; GUASCH, H.; SABATER, S.; CAIXACH, J.; PORTE, C. Comparing the response of biochemical indicators (biomarkers) and biological indices to diagnose the ecological impact of an oil spillage in a Mediterranean river (NE Catalunya, Spain). Chemosphere, v. 66, n. 7, p. 1206-1216, 2007.

[16] ELLMANN, G. L.; COURTNEY, K. O.; ANDRRES, V.; FEATHERSTONE, R. M. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol, v. 7, p. 88-95, 1961.

[17] 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. Use of hepatocytes from Hoplias malabaricusto characterize the toxicity of a complex mixture of lipophilic halogenated compounds. Toxicol. In Vitro, v. 21, p. 706-715, 2007.

[18] HELCOM. Manual formarine monitoring in the COMBINE Programme of HELCOM, http://sea.helcom.fi/Monas/Combine-Manual2/CombineHome.htm, 2006.

[19] HOQUE, M. T.; YUSOFF, F. M. Law A.; SYED, M. A. Effect of hydrogen sulphide on liver-somatic index and Fulton's condition factor in Mystus nemurus J. Fish Biol, v. 52, p. 23-30, 1998.

[20] ICES. Report of the Advisory Committee on the Marine Environment ICES Cooperative Research Report, 2001. v. 248, p. 203.

[21] KATSUMITI, A.; VALDEZ DOMINGOS, F.X.; AZEVEDO, M.; DA SILVA, M. D.; DAMIAN, R. C.; ALMEIDA, M. I. M.; SILVA DE ASSIS, H. C.; CESTARI, M.M.; RANDI, M. A. F.; OLIVEIRA RIBEIRO, C. A.; FREIRE, C. A. 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. Environ Monit. Assess, v. 152, p. 209-222, 2009.

[22] KEEN, J. H.; HABIG, W.; JAKOBY, W. B. Mecanism for several activities of the glutatione S-transferase, J. Biol Chem, v. 251, p.6183-6188, 1976.

[23] LYONS, B. P.; STENTIFORD, G. D.; BIGNELL, J.; GOODSIR, F.; SIVYER, D. B.; DEVLIN, M. J.; LOWE, D.; BEESLEY, A.; PASCOE, C. K.; MOORE, M. N.; GARNACHO, E. Biological effects monitoring survey of Cardigan bay using flatfish histopathology, Cellular biomarkers and Sediment bioassays: findings of the prince madog prize. Mar. Environ. Res, v. 62, p. 342-346, 2006.

[24] MARIGÓMEZ, I.; SOTO, M.; CANCIO, I.; ORBEA, A.; GARMENDIA, L.; CAJARAVILLE, M. P. Cell and tissue biomarkers in mussel, and histopathology in hake and anchovy from Bay of Biscay after the Prestige oil spill (Monitoring Campaign 2003). Mar. Pollut. Bull, v. 53, p.287-304, 2006.

[25] MARTY, G. D.; HOFFMANN, A.; OKIHIRO, M. S.; HEPLER, K.; HANES, D. Retrospective analyses: bile hydrocarbons and histopathology of demersal rockfish in Prince William sound, Alaska, after the Exxon Valdez oil spill. Mar. Environ. Res, v. 56, p. 569-584, 2003.

[26] MELA, M.; RANDI, M. A. F.; VENTURA, D. F.; CARVALHO, C. E. V.; PELLETIER, E.; OLIVEIRA RIBEIRO, C. A. Effects of dietary methylmercury on liver and kidney histology in the neotropical fish Hoplias malabaricus Ecotox. Environ. Saf, v. 68, p. 426-435, 2007.

[27] MIRANDA, A. L.; ROCHE, H.; RANDI, M. A. F.; MENEZES, M. L.; OLIVEIRA RIBEIRO, C. A. Bioaccumulation of chlorinated pesticides and PCBs in the tropical freshwater fish Hoplias malabaricus: Histopathological, physiological, and immunological findings. Environ. Int, v. 34, p. 939-949, 2008.

[28] OLIVEIRA RIBEIRO C. A; SILVA DE ASSIS, H. C. AChE inhibition as a Biomarker for pollutants contamination in tropical aquatic ecossistems. In: MAHIRA PARVEEN; SANTOSH KUMAR.(Org.). Recent trendsin Acetylcholinesterase Amsterdam: IOS Press, 2005a.p .103-124.

[29] OLIVEIRA RIBEIRO, C. A.; VOLLAIRE, Y.; SANCHEZ-CHARDI, A.; ROCHE, H. Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the Eel (Anguilla anguilla) at the Camargue Nature Reserve, France. Aquat. Toxicol, v. 74, p. 53-69, 2005b.

[30] PIKKARAINEN, A. Ethoxyresorufin-O-deethylase (EROD) activity and bile metabolites as contamination indicators in Baltic Sea perch: Determination by HPLC. Chemosphere, v. 65, p. 1888-1897, 2006.

[31] PINKNEY, A. E.; HARSHBARGER, J. C.; MAY, E. B.; MELANCON, M. J. Tumor prevalence and biomarkers of exposure in brown bullheads (Ameiurus nebulosus) from the tidal Potomac River, USA, Watershed. Environ. Toxicol. Chem, v. 20, p. 1196-1205, 2001.

[32] RABITTO, I. S.; BASTOS, W. R.; ALMEIDA, R.; ANJOS, A.; DE HOLANDA, I. B. B.; GALVÃO, R. C. F.; FILIPAK NETO, F.; MENEZES, M.L.; SANTOS, C.A.M.; OLIVEIRA RIBEIRO, C.A. Mercury and DDT exposurerisktofish-eatinghuman populations in Amazon. Environ. Int, v. 37, p. 56-65, 2011.

[33] RAMSDORF, W. A.; FERRARO, M. V. M.; OLIVEIRA RIBEIRO, C. A.; ALVES COSTA, J. R. M.; CESTARI, M. M. Genotoxic evaluation of different doses of inorganic lead (PbII) in Hoplias malabaricus Environ. Monit. Assess, v. 158, n. 1-4, p. 77-85, 2008.

[34] RUDDOCK, P. J.; BIRD, D. J.; MCCALLEY, D. V. Bile metabolites of polycyclic aromatic hydrocarbons in three species of fish from the Severn Estuary. Ecotox. Environ. Saf, v. 39, p. 147-153, 2002.

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