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Changes in Glutathione S-Transferase Activity and Parental Care Patterns in a Catfish (Pisces, Ariidae) as a Biomarker of Anthropogenic Impact in a Brazilian Harbor

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Abstract

Catfish have been used as a model system for studying biochemical mechanisms of biotransformation. The main goal of this study was to identify alterations in hepatic glutathione S-transferase (GST) activity and changes in the parental care pattern of a mouth-brooding catfish, Sciades herzbergii, as a biomarker of anthropogenic impact in a port area on the northeastern coast of Brazil. The fish were sampled from a natural reserve (A1 = reference site) and from an industrialized port area (A2 = impacted site). Two analyses were carried out: hepatic GST activity and mouth-brooding behavior of males. Catfish collected from the A1 site displayed all stages of gonadal maturation, and some of the adult males were mouth brooding 12–30 embryos. Not all gonadal maturation stages of the catfish were represented at the A2 site, and no mouth-brooding males were observed. GST activity in the liver of S. herzbergii was significantly higher in fish from the impacted site compared with fish from the reference site. Values for the enzymatic activity increased progressively in fish sampled from the reserve area as they became more reproductively mature (immature ≤ maturing ≤ mature ≤ spent). However, the greatest values for GST activity (2.84 ± 0.31 μmol min−1 mg protein−1) among fish sampled from the impacted area were found in (immature) juveniles. These data suggest that changes in hepatic GST activity and mouth-brooding behavior of S. herzbergii can be used as biomarkers of anthropogenic impact.

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References

  • Abollino O, Aceto M, Saccchero G, Sarzanini C, Mentasti E (1995) Determination of copper, cadmium, iron, manganese, nickel and zinc in Antarctic sea water. Comparison of electrochemical and spectroscopic procedures. Analyt Chim Acta 305:200–206

    Article  CAS  Google Scholar 

  • Adams SM (1990) Biological indicators of stress in fish. Am Fish Soc Symp 8:190–195

    Google Scholar 

  • Antaq (2015) Agência Nacional de Transportes Aquaviários. Principais portos do Brasil. http://www.antaq.gov.br. Accessed 20 Jan 2015

  • Azevedo MCC (1999) Variação espacial e temporal de bagres marinhos (Siluriformes, Ariidae) na Baía de Sepetiba, Rio de Janeiro. Rev Bras Biol 59:443–454

    Article  Google Scholar 

  • Barbieri GM (1992) Biologia de Astyanax scabripinnis paranae (Characiformes, Characidade) do ribeirão do Fazzari. São Carlos. Estado de São Paulo. II. Aspectos quantitativos da reprodução. Rev Bras Biol 52:589–596

    Google Scholar 

  • Bila DM, Dezotti M (2007) Desreguladores endócrinos no meio ambiente: efeitos e consequências. Quím Nova 30:651–656

    Article  CAS  Google Scholar 

  • Canli M, Atli G (2003) The relationships between heavy metal (Cd, Cr, Cu, Fe, Pb, Zn) levels and the size of six Mediterranean fish species. Environ Pollut 121:129–136

    Article  CAS  Google Scholar 

  • Cantanhêde G, Castro ACL, Gubiani EA (2007) Biologia reprodutiva de Hexanematichthys proops (Siluriformes, Ariidae) no litoral ocidental maranhense. Iheringia, Sér Zool 97:498–504

    Article  Google Scholar 

  • Carvalho-Neta RNF, Abreu-Silva AL (2010) Sciades herzbergii oxidative stress biomarkers: an in situ study of estuarine ecosystem (São Marcos Bay, Maranhão, Brazil). Braz J Oceanogr 58:11–17

    Article  Google Scholar 

  • Carvalho-Neta RNF, Abreu-Silva AL (2013) Glutathione S-Transferase as biomarker in Sciades herzbergii (Siluriformes: Ariidae) for environmental monitoring: the case study of São Marcos Bay, Maranhão, Brazil. Braz Lat Am J Aquat Res 41:217–225

    Google Scholar 

  • Carvalho-Neta RNF, Castro ACL (2008) Diversidade das assembléias de peixes estuarinos da Ilha dos Caranguejos, Maranhão. Arq Ciên Mar 41:48–57

    Google Scholar 

  • Carvalho-Neta RNF, Torres ARJ, Abreu-Silva AL (2012) Biomarkers in catfish Sciades herzbergii (Teleostei: Ariidae) from polluted and non-polluted areas (São Marcos’ Bay, Northeastern Brazil). Appl Biochem Biotechnol 166:1314–1327

    Article  CAS  Google Scholar 

  • Carvalho-Neta RNF, Torres ARJ, Silva D, Cortez CM (2014) A simple mathematical model based on biomarkers in stress-resistant catfish species, Sciades herzbergii (Pisces, ariidae), in São Marcos Bay, Brazil. Appl Biochem Biotechnol 174:2380–2391

    Article  CAS  Google Scholar 

  • Conama (2005) Resolucão número 357. Diário Oficial da República Federativa do Brasil. http://www.mma.gov.br/port/conama/res/ res05/res35705.pdf. Accessed 21 Aug 2013

  • Conama (2011) Resolução número 430. Diário Oficial da República Federativa do Brasil. http://www.mma.gov.br/port/conama/ legiabre.cfm?codlegi = 646. Accessed 18 March 2015

  • Das B, Khan YSA, Das P, Shaheen SM (2002) Organochlorine pesticide residues in catfish, Tachysurus thalassinus (Ruppell, 1835), from the south patches of the bay of bengal. Environ Pollut 120:255–259

    Article  CAS  Google Scholar 

  • Dietrich GJ, Dietrich M, Kowalski RK, Dobosz S, Karol H, Demianowicz W, Glogowski J (2010) Exposure of rainbow trout milt to mercury and cadmium alters sperm motility parameters and reproductive success. Aquat Toxicol 97:277–284

    Article  CAS  Google Scholar 

  • EMAP (2015) Empresa Maranhense de Administração Portuária. http//www.emap.ma.gov.br. Accessed 21 Aug 2015

  • Fávaro LF, Frehse FDA, Oliveira RND, Schwarz R (2005) Reproduction of the Madamango sea catfish, Cathorops spixii (Agassiz) (Siluriformes, Ariidae), of the Pinheiros Bay, estuarine coastal area of Paraná, Brazil. Rev Bras Zool 22:1022–1029

    Article  Google Scholar 

  • Fossi MC, Casini S, Marsili L, Mori G, Néri G, Romeo T, Ausili A (2004) Evaluation of the Mediterranean population of swordfish (Xiphias gladius). Mar Environ Res 48:425–429

    Article  Google Scholar 

  • Gagnon MM, Rawson CA (2016) Integrating multiple biomarkers of fish health: a case study of fish health in ports. Arch Environ Contam Toxicol 70:192–203

    Article  CAS  Google Scholar 

  • Galkus A, Joksas K, Stakeniene R, Lagunaviciene L (2010) Heavy metal contamination in harbor bottom sediments. Pol J Environ Stud 21:1583–1594

    Google Scholar 

  • Garcia DAZ, Casimiro ACR, Orsi ML (2012) Introduction of the armored catfish, Pterygoplichthys ambrosettii (Holmberg, 1893) in a large effluent of the Upper Parana River basin. J Appl Ichthyol 28:138–139

    Article  Google Scholar 

  • Gomes ID, Araújo EG, Azevedo MCC, Pessanha ALM (1999) Biologia reprodutiva dos bagres marinhos Genidens genidens (Valencianes) e Cathorops spixii (Agassiz) (Siluriformes, Ariidae) na Baía de Sepetiba, Rio de Janeiro, Brasil. Rev Bras Zool 16:171–180

    Article  Google Scholar 

  • Habig WH, Pabst MJ, Jacoby WB (1974) Glutathione-S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139

    CAS  Google Scholar 

  • Hammerschidt CR, Sandheinrich MB, Wiener JG, Rada RG (2002) Effects or dietary MeHg on reproduction of fathead minnows. Environ Sci Technol 36:877–883

    Article  Google Scholar 

  • Harzer B, Stipp MC, Herrerias T (2015) Avaliação da função hepática de peixes Rhamdia quelen expostos aos desreguladores endócrinos estriol e estrona. Revinter 8:82–85

    Google Scholar 

  • Hilbig CC, Bombardelli RA, Sanches EA (2008) Efeito do chumbo sobre a fertilizacão artificial e incubação de ovos de jundiá cinza (Rhamdia quelen). Acta Sci Anim Sci 30:217–224

    CAS  Google Scholar 

  • IBGE (2015) Instituto Brasileiro de Geografia e Estatística. http://www.ibge.gov.br/estadosat/perfil.php?sigla=ma#. Accessed 24 Sept 2015

  • Kasper D, Botaro D, Palermo EFA, Malm O (2007) Mercúrio em peixes-fontes e contaminação. Oecol Bras 11:228–239

    Article  Google Scholar 

  • Kehrig HA, Malm O, Palermo EF, Seixas TG, Baêta AP, Moreira I (2011) Bioconcentração e biomagnificação de metilmercúrio na baía de Guanabara. Quim Nova 34:377–384

    Article  CAS  Google Scholar 

  • Kime DE (1995) The effects of pollution on reproduction in fish. Rev Fish Biol 5:52–96

    Article  Google Scholar 

  • Kime DE (2000) A strategy for assessing the effects of xenobiotics on fish reproduction. Kluwer Academy Publishers, New York

    Google Scholar 

  • Lacaze JC (2000) Poluição dos mares. Porto editora, São Paulo

    Google Scholar 

  • Latif MA, Bodaly RA, Johnston TA, Fudge RJP (2001) Effects of environmental and maternally derived methylmercury on the embryonic and larval stages of walley (Stizostedion vitrem). Environ Pollut 111:139–148

    Article  CAS  Google Scholar 

  • Leblond V, Hontela A (1999) Effects of in vitro exposures to cadmium, mercury, zinc, and 1-(2-Chlorophenyl)-1-(4-chlorophenyl)-2,2-dichlroethane on steroidogenesis by disposed interrenal cells of rainbow trout (Oncorhynchus mykiss). Toxicol Appl Pharm 157:16–22

    Article  CAS  Google Scholar 

  • Lepland A, Andersen TJ, Lepland A, Arp HPH, Alve E, Breedvly G, Rindby A (2012) Sedimentation and chronology of heavy metal pollution in Oslo Harbor, Norway. Mar Pollut Bull 60:1512–1522

    Article  Google Scholar 

  • Lins JAPN, Kirschnik PG, Queiroz VS, Cirio SM (2010) Uso de peixes como biomarcadores para monitoramento ambiental aquático. Rev Acad Agrár Ambient 8:469–484

    Google Scholar 

  • Manzetti S, van der Spoel ER, van der Spoel D (2014) Chemical properties, environmental fate, and degradation of seven classes of pollutants. Chem Res Toxicol 27:713–737

    Article  CAS  Google Scholar 

  • Marimuthu K, Cheen AC, Muralikrishnan S, Kumar D (2010) Effect of different feeding frequency on the growth and survival of African catfish (Clarias gariepinus) fingerlings. Adv Environ Biol 4:187–193

    CAS  Google Scholar 

  • Martín-Díaz ML, Blasco J, Sales D, DelValls TA (2008) Field validation of a battery of biomarkers to assess sediment quality in Spanish ports. Environ Pollut 151:631–640

    Article  Google Scholar 

  • Martins-Juras IAG (1989) Ictiofauna estuarina da ilha do Maranhão (MA -BRASIL). Tese (Doutorado), Instituto Oceanográfico, USP, São Paulo

  • Oliveira MA, Novelli R (2005) Idade e crescimento do bagre Genidens genidens na Baía da Lagoa do Açu, norte do Estado do Rio de Janeiro. Trop Oceanogr 33:57–66

    Google Scholar 

  • Oruc EO, Sevgiler Y, Uner N (2004) Tissue-specific oxidative stress responses in fish exposed to 2,4-D and azinphosmethyl. Comp Biochem Physiol 137:43–51

    Article  Google Scholar 

  • Penha JMF, Mateus LAF, Barbieri G (2004) Age and growth of the porthole shovelnose catfish (Hemisorubim platyrhynchos) in the Pantanal. Braz J Biol 64:833–840

    Article  CAS  Google Scholar 

  • Pinheiro-Sousa DB, Almeida ZS, Carvalho-Net RNF (2013) Integrated analysis of two biomarkers in Sciades herzbergii (Ariidae, Siluriformes), to assess the environmental impact at São Marcos’ Bay, Maranhão, Brazil/Análisis integrado de dos biomarcadores en Sciades herzbergii (Ariidae, Siluriformes) para evaluar el impacto ambiental en la Bahía de San Marcos, Maranhão, Brasil. Lat Am J Aquat Res 41:305–312

    Google Scholar 

  • Powers DA (1989) Fish as model systems. Science 246:352–358

    Article  CAS  Google Scholar 

  • Rand GM, Petrocelli SR (1985) Fundamentals of aquatic toxicology: methods and applications. Hemisphere Publish, Washington

    Google Scholar 

  • Reis EG (1986) Reproduction and feeding habits of the marine catfish Netuma barba (Siluriformes, Ariidae) in the estuary of Lagoa dos Patos, Brazil. Atlântica 8:35–55

    Google Scholar 

  • Romagosa E (2010) Reproductive status in females of the Brazilian catfish, Pseudoplatystoma fasciatum reared in cages. J Appl Ichthyol 26:806–811

    Article  Google Scholar 

  • Roy S, Bhattacharya S (2006) Arsenic-induced histopathology and synthesis of stress proteins in liver and kidney of Channa punctatus. Ecotox Environ Safe 65:218–229

    Article  CAS  Google Scholar 

  • Sousa JKC (2009) Avaliação de impactos ambientais causados por metais traço em água, sedimento e material biológico na Baia de São Marcos, São Luís—Maranhão. Dissertation, Universidade Federal da Paraíba, João Pessoa, Brasil

  • Triebskorn R, Köhler HR, Honnen W, Schramm M, Adams SM, Müller EF (1997) Induction of heat shock proteins, changes in liver ultrastructure, and alterations of fish behavior: are these biomarkers related and are they useful to reflect the state of pollution in the field? J Aquat Ecosyst Stress Recovery 6:57–73

    Article  CAS  Google Scholar 

  • Van der Oost R, Beyer J, Vermeulen NP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149

    Article  Google Scholar 

  • Vazzoler AEM (1996) Biologia e reproducão de peixes teleósteos: teoria e prática. Eduem Press, Maringá

    Google Scholar 

  • WHO (1990) Enviromental Health Criteria (EHC 101). Methylmercury. WHO, Geneva

    Google Scholar 

  • Wierner JG, Spry DJ (1996) Toxicological significance of mercury in fresh water fish. In: Beyer B (ed) Environmental contaminants. Lewis Publishers, Boca Raton, pp 297–339

    Google Scholar 

  • Wierner JG, Krabbenhoft DP, Heinz GH, Scheuhammer AM (2003) Ecotoxicology of mercury. In: Hoffman DJ, Burton BAGA (eds) Handbook of ecotoxicology. CRC Press, Boca Raton, pp 1311–1312

    Google Scholar 

  • Winkaler EU, das Graças Silva A, Galindo HC, dos Reis Martinez CB (2008) Biomarcadores histológicos e fisiológicos para o monitoramento da saúde de peixes de ribeirões de Londrina, Estado do Paraná. Acta Sci Biol Sci 23:507–514

    Google Scholar 

  • Winston GW, Di Giulio RT (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19:137–161

    Article  CAS  Google Scholar 

  • Witt G, Lang SC, Ullmann D, Schaffrath G, Schulz-Bull D, Mayer P (2013) Passive equilibrium sampler for in situ measurements of freely dissolved concentrations of hydrophobic organic chemicals in sediments. Environ Sci Technol 47:7830–7839

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank the staff of the Laboratory of Biomarkers in Aquatic Organisms (Biomarcadores em Organismos Aquáticos: LABOAq) at the Universidade Estadual do Maranhão (UEMA), Brazil, and the Maranhão State Research Foundation (Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão: FAPEMA) for financial support.

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Authors and Affiliations

  1. Department of Chemistry and Biology, State University of Maranhão (UEMA), Campus Paulo VI, Caixa Postal 9, São Luís, Maranhão, 65000-000, Brazil

    Raimunda Nonata Fortes Carvalho Neta, Débora Martins Silva Santos, Lígia Tchaicka & Zafira da Silva de Almeida

  2. Laboratory of Biomarkers in Aquatic Organisms (LABOAq), State University of Maranhão (UEMA), Campus Paulo VI, São Luís, Maranhão, 65000-000, Brazil

    Raimunda Nonata Fortes Carvalho Neta & Gleyciane Lobato Barbosa

  3. Master Program of Aquatic Resources and Fisheries (PPGRAP), State University of Maranhão (UEMA), Campus Paulo VI, São Luís, Maranhão, 65000-000, Brazil

    Raimunda Nonata Fortes Carvalho Neta, Hetty Salvino Torres, Débora Batista Pinheiro Sousa, Jonatas da Silva Castro, Débora Martins Silva Santos, Lígia Tchaicka, Zafira da Silva de Almeida, Erivania Gomes Teixeira & Audalio Rebelo Torres Jr

  4. Master Programa in Oceanography, Federal University of Maranhão (UFMA), Campus Dom Delgado, São Luís, Maranhão, Brazil

    Raimunda Nonata Fortes Carvalho Neta & Audalio Rebelo Torres Jr

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  1. Raimunda Nonata Fortes Carvalho Neta
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  2. Gleyciane Lobato Barbosa
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Correspondence to Raimunda Nonata Fortes Carvalho Neta.

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Fortes Carvalho Neta, R.N., Barbosa, G.L., Torres, H.S. et al. Changes in Glutathione S-Transferase Activity and Parental Care Patterns in a Catfish (Pisces, Ariidae) as a Biomarker of Anthropogenic Impact in a Brazilian Harbor. Arch Environ Contam Toxicol 72, 132–141 (2017). https://doi.org/10.1007/s00244-016-0326-0

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