Environmental Science and Pollution Research

, Volume 21, Issue 18, pp 10638–10651 | Cite as

Mercury accumulation and tissue-specific antioxidant efficiency in the wild European sea bass (Dicentrarchus labrax) with emphasis on seasonality

  • C. L. Mieiro
  • M. Dolbeth
  • T. A. Marques
  • A. C. Duarte
  • M. E. Pereira
  • M. Pacheco
Research Article


The main goal of this study was to assess both mercury (Hg) accumulation and organs’ specific oxidative stress responses of gills, liver and kidney of Dicentrarchus labrax with emphasis on seasonality. Fish were collected in cold and warm periods in three stations: reference, moderated and highly contaminated sites. Our results showed that seasonal factors slightly influenced Hg accumulation between year periods (cold and warm) and strongly affected organs’ response basal levels. In contrast, seasonality seemed not to influence oxidative stress responses, since similar response patterns were obtained for both year periods, and moderate degree of antioxidant responses was obtained. Moreover, the oxidative stress profile may be attributed to Hg contamination degree, which showed organ-specific response and accumulation patterns. Hence, gills showed to be able to adapt to Hg contamination, and in opposition, kidney and liver demonstrated some vulnerability to Hg toxicity. The critical Hg concentrations indicated specific threshold limits for each organ. Overall, seasonality should be taken into account in monitoring programmes, helping to characterize the individuals’ reference values of response and thus to discriminate between the effects induced by natural causes or by contamination.


Seasonality Mercury Oxidative stress Benchmark Wild fish 



This work was supported by European Funds through COMPETE and by National Funds through the Portuguese Science Foundation (FCT) within project PEst-C/MAR/LA0017/2013 and through a post-doctoral grant to C.L. Mieiro (SFRH/BPD/79445/2011) along with CESAM, University of Aveiro.

Supplementary material

11356_2014_3053_MOESM1_ESM.docx (110 kb)
ESM 1 (DOCX 109 kb)


  1. Athar M, Iqbal M (1998) Ferric nitrilotriacetate promotes N-diethylnitrosamine-induced renal tumorigenesis in the rat: implications for the involvement of oxidative stress. Carcinogenesis 19:1133–1139CrossRefGoogle Scholar
  2. Baker MA, Cerniglia GJ, Zaman A (1990) Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples. Anal Biochem 190:360–365CrossRefGoogle Scholar
  3. Beckvar N, Dillon TM, Read LB (2005) Approaches for linking whole-body fish tissue residues of mercury or DDT to biological effects thresholds. Environ Toxicol Chem 24:2094–2105CrossRefGoogle Scholar
  4. Beyer J, Sandvikb M, Hylland K, Fjeld E, Egaas E, Aas E, Skfueb JU, Gokssyr A (1996) Contaminant accumulation and biomarker responses in flounder (Platichthys jlesus L.) and Atlantic cod (Gadus morhua L.) exposed by caging to polluted sediments in Sarrfjorden, Norway. Aquat Toxicol 36:75–98CrossRefGoogle Scholar
  5. Bird RP, Draper AH (1984) Comparative studies on different methods of malondialdehyde determination. Methods Enzymol 90:105–110Google Scholar
  6. Black D, Love M (1986) The sequential mobilisation and restoration of energy reserves in tissues of Atlantic cod during starvation and refeeding. J Comp Physiol B 156:469–479CrossRefGoogle Scholar
  7. Bodin N, Burgeota T, Stanisièreb JY, Bocquené G, Menarda D, Minierc C, Boutetd I, Amate A, Cherelf Y, Budzinskig H (2004) Seasonal variations of a battery of biomarkers and physiological indices for the mussel Mytilus galloprovincialis transplanted into the northwest Mediterranean Sea. Comp Biochem Physiol C 138:411–427Google Scholar
  8. Carlberg I, Mannervik B (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250:5475–5480Google Scholar
  9. Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) Handbook of methods in oxygen radical research. CRC, Boca Raton, pp 283–284Google Scholar
  10. Coelho JP, Pereira ME, Duarte A, Pardal MA (2005) Macroalgae response to a mercury contamination gradient in a temperate coastal lagoon (Ria de Aveiro, Portugal). Estuar Coast Shelf Sci 65:492–500CrossRefGoogle Scholar
  11. Coelho JP, Nunes M, Dolbeth M, Pereira ME, Duarte AC, Pardal MA (2008) The role of two sediment-dwelling invertebrates on the mercury transfer from sediments to the estuarine trophic web. Estuar Coast Shelf Sci 78:505–512CrossRefGoogle Scholar
  12. Costley CT, Mossop KF, Dean JR, Garden LM, Marshall J, Carroll J (2000) Determination of mercury in environmental and biological samples using pyrolysis atomic absorption spectrometry with gold amalgamation. Anal Chim Acta 405:179–183CrossRefGoogle Scholar
  13. Depew DC, Basu N, Burgess NM, Campbell LM, Devlin EW, Drevnick E, Hammerschmidt CR, Murphy CM, Sandheinrich MB, Wiener JG (2012) Toxicity of dietary methylmercury to fish: Derivation of ecologically meaningful threshold concentrations. Environ Toxicol Chem 31:1536–1547Google Scholar
  14. Dillon T, Beckvar N, Kern J (2010) Residue-based mercury dose-response in fish: an analysis using lethality-equivalent test endpoints. Environ Toxicol Chem 29:2559–2565CrossRefGoogle Scholar
  15. Dolbeth M, Martinho F, Viegas I, Cabral H, Pardal MA (2008) Estuarine production of resident and nursery fish species: conditioning by drought events? Estuar Coast Shelf Sci 78:51–60CrossRefGoogle Scholar
  16. Drevnick P, Roberts A, Otter R, Hammerschmidt C, Klaper R, Oris J (2008) Mercury toxicity in livers of northern pike (Esox lucius) from Isle Royale. USA Comp Biochem Physiol C 147(3):331–338Google Scholar
  17. El-Shehawi AM, Ali FK, Seehy MA (2007) Estimation of water pollution by genetic biomarkers in tilapia and catfish species shows species-site interaction. Afr J Biotechnol 6:840–846Google Scholar
  18. Filho WD, Giuvili C, Boveris A (1993) Antioxidant defenses in marine fish. I. Teleosts. Comp Biochem Physiol 106C:409–414Google Scholar
  19. Filho DW, Tribess T, Gaspári C, Cláudio FD, Torres MA, Magalhães ARM (2001a) Seasonal changes in antioxidant defenses of the digestive gland of the brown mussel (Perna perna). Aquaculture 203:149–158CrossRefGoogle Scholar
  20. Filho WD, Torres MA, Tribess TB, Pedrosa RC, Soares CHL (2001b) Influence of season and pollution on the antioxidant defenses of the cichlid fish acará (Geophagus brasiliensis). Braz J Med Biol Res 34:719–726Google Scholar
  21. Giri U, Iqbal M, Athar M (1996) Porphyrin-mediated photosensitization has a weak tumor promoting effect in mouse skin: possible role of in situ generated reactive oxygen species. Carcinogenesis 17:2023–2028CrossRefGoogle Scholar
  22. Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751–766Google Scholar
  23. Guilherme S, Válega M, Pereira M, Santos M, Pacheco M (2008) Antioxidant and biotransformation responses in Liza aurata under environmental mercury exposure—relationship with mercury accumulation and implications for public health. Mar Pollut Bull 56:845–859CrossRefGoogle Scholar
  24. Habig WH, Pabst MJ, Jokoby WB (1974) Glutathione-S-transferase. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
  25. Kane AS, Salierno JD, Brewer SK (2005) Fish models in behavioral toxicology: automated techniques, updates and perspectives. In: Ostrander GK (ed) Methods in aquatic toxicology (Chapter 32), Volume 2. Lewis Publishers, Boca Raton, pp 559–590Google Scholar
  26. Leiniö S, Lehtonen KK (2005). Seasonal variability in biomarkers in the bivalves Mytilus edulis and Macoma balthica from the northern Baltic Sea. Comp Biochem Physiol C 140:408–421Google Scholar
  27. Manduzio H, Monsinjon T, Galap C, Leboulenger F, Rocher B (2004) Seasonal variations in antioxidant defences in blue mussels Mytilus edulis collected from a polluted area: major contributions in gills of an inducible isoform of Cu/Zn-superoxide dismutase and of glutathione S-transferase. Aquat Toxicol 70:83–93CrossRefGoogle Scholar
  28. Maria VL, Ahmad I, Oliveira M, Serafim A, Bebianno MJ, Pacheco M, Santos MA (2009) Wild juvenile Dicentrarchus labrax L. liver antioxidant and damage responses at Aveiro Lagoon, Portugal. Ecotox Environ Safe 72:1861–1870Google Scholar
  29. Martinho F, Viegas I, Dolbeth M, Leitão R, Cabral HN, Pardal MA (2008) Assessing estuarine environmental quality using fish-based indices: performance evaluation under climatic instability. Mar Pollut Bull 56:1834–1843CrossRefGoogle Scholar
  30. Mieiro CL, Ahmad I, Pereira ME, Duarte AC, Pacheco M (2010) Antioxidant system breakdown in brain of feral golden grey mullet (Liza aurata) as an effect of mercury exposure. Ecotoxicology 19:1034–1045Google Scholar
  31. Mieiro CL, Pereira ME, Duarte AC, Pacheco M (2011a) Brain as a critical target of mercury in environmentally exposed fish (Dicentrarchus labrax)—bioaccumulation and oxidative stress profiles. Aquat Toxicol 103:233–240CrossRefGoogle Scholar
  32. Mieiro CL, Duarte AC, Pereira ME, Pacheco M (2011b) Mercury accumulation patterns and biochemical endpoints in wild fish (Liza aurata): a multi-organ approach. Ecotoxicol Environ Saf 74:2225–2232CrossRefGoogle Scholar
  33. Mieiro CL, Pacheco M, Pereira ME, Duarte AC (2011c) Mercury organotropism in feral European sea bass (Dicentrarchus labrax). Arch Environ Contam Toxicol 61:135–143CrossRefGoogle Scholar
  34. Mieiro CL, Coelho JP, Pacheco M, Duarte AC, Pereira ME (2012a) Trace elements in two marine fish species during estuarine residency: non-essential versus essential. Mar Pollut Bull 64:2844–2848CrossRefGoogle Scholar
  35. Mieiro CL, Coelho JP, Pacheco M, Duarte AC, Pereira ME (2012b) Evaluation of species-specific dissimilarities in two marine fish species: mercury accumulation as a function of metal levels in consumed prey. Arch Environ Contam Toxicol 63:125–136CrossRefGoogle Scholar
  36. Mohandas J, Marshall JJ, Duggins GG, Horvath JS, Tiller D (1984) Differential distribution of glutathione and glutathione related enzymes in rabbit kidney. Possible implications in analgesic neuropathy. Cancer Res 44:5086–5091Google Scholar
  37. Monterroso P, Pato P, Pereira M, Millward G, Vale C, Duarte A (2007) Metal-contaminated sediments in a semi-closed basin: implications for recovery. Estuar Coast Shelf Sci 71:148–158CrossRefGoogle Scholar
  38. Mucci A, Lucotte M, Montgomery S, Plourde Y, Pichet P, Tra HV (1995) Mercury remobilization from flooded soils in a hydro-electric reservoir of northern Quebec, La Grande-2: results of a soil resuspension experiment. Can J Fish Aquat Sci 52:2507–2517CrossRefGoogle Scholar
  39. Ohkawa H (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358CrossRefGoogle Scholar
  40. Oliveira M, Pacheco M, Santos M (2008) Organ specific antioxidant responses in golden grey mullet (Liza aurata) following a short-term exposure to phenanthrene. Sci Total Environ 396:70–78CrossRefGoogle Scholar
  41. Oliveira M, Maria VL, Ahmad I, Serafim A, Bebianno MJ, Pacheco M, Santos MA (2009) Contamination assessment of a coastal lagoon (Ria de Aveiro, Portugal) using defence and damage biochemical indicators in gill of Liza aurata—an integrated biomarker approach. Environ Pollut 157:959–967CrossRefGoogle Scholar
  42. Pacheco M, Santos MA, Teles M, Oliveira M, Rebelo JE, Pombo L (2005) Biotransformation and genotoxic biomarkers in mullet species (Liza sp.) from a contaminated coastal lagoon (Ria de Aveiro, Portugal). Environ Monit Assess 107:133–153CrossRefGoogle Scholar
  43. Pavlović SZ, Belić D, Blagojević DP, Radojičić RM, Žikić RV, Saičić ZS, Lajšić GG, Spasić MB (2004) Seasonal variations of cytosolic antioxidant enzyme activities in liver and white muscle of thinlip gray mullet (Liza ramada Risso) from the Adriatic Sea. Cryoletters 25:273–285Google Scholar
  44. Pavlović SZ, Borković-Mitić SS, Radovanović TB, Perendija BR, Despotović GSV, Gavrić JP, Saicić ZS (2009) Activity of oxidative stress biomarkers in the white muscle of red mullet (Mullus barbatus L.) from the Adriatic sea. Arch Biol Sci 61(4):693–701CrossRefGoogle Scholar
  45. Pavlović SZ, Borković-Miti S, Gavrilovi B, Despotovi SG, Gavri JP, Saii ZS (2013) Seasonal changes of oxidative stress biomarkers in white muscle of longfin gurnard (Chelidonychthys obscurus) from the Adriatic Sea. Water Res Manag 3(2):19–25Google Scholar
  46. Pereira ME, Duarte A, Millward GE, Abreu SN, Vale C (1998) An estimation of industrial mercury stored in sediments of a confined area of the Lagoon of Aveiro (Portugal). Water Sci Technol 37:125–130CrossRefGoogle Scholar
  47. Pereira ME, Lillebø AI, Pato P, Válega M, Coelho JP, Lopes CB, Rodrigues S, Cachada A, Otero M, Pardal MA, Duarte AC (2009) Mercury pollution in Ria de Aveiro (Portugal): a review of the system assessment. Environ Monit Assess 155:39–49CrossRefGoogle Scholar
  48. Pereira P, de Pablo H, Pacheco M, Vale C (2010) The relevance of temporal and organ specific factors on metals accumulation and biochemical effects in feral fish (Liza aurata) under a moderate contamination scenario. Ecotoxicol Environ Saf 73:805–816CrossRefGoogle Scholar
  49. Pinheiro JC, Bates DM (2001) Mixed models in S and S-Plus, 2de print. Springer, New YorkGoogle Scholar
  50. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1-107Google Scholar
  51. R Development Core Team (2005) R: A language and environment for statistical computing, reference index version 2.x.x. R Foundation for Statistical Computing. Vienna, AustriaGoogle Scholar
  52. Ramalhosa E, Pato P, Monterroso P, Pereira E, Vale C, Duarte AC (2006) Accumulation versus remobilization of mercury in sediments of a contaminated lagoon. Mar Pollut Bull 52(3):353–356CrossRefGoogle Scholar
  53. RIVM (2001) RIVM report 711701 020 ecotoxicological serious risk concentrations for soil, sediment and (ground) water: updated proposals for first series of compounds. E. M. J. Verbruggen, R. Posthumus, A. P. van Wezel April 2001Google Scholar
  54. Sandheinrich MB, Bhavsar SP, Bodaly RA, Drevnick PE, Paul EA (2011) Ecological risk of methylmercury to piscivorous fish of the Great Lakes region. Ecotoxicology 20:1577–1587CrossRefGoogle Scholar
  55. Tietze F (1969) Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione. Anal Biochem 27:502–522CrossRefGoogle Scholar
  56. Válega M, Abreu S, Pato P, Rocha L, Gomes AR, Pereira ME, Duarte AC (2006) Determination of organic mercury in biota, plants and contaminated sediments using a thermal atomic absorption spectrometry technique. Water Air Soil Pollut 174:223–234CrossRefGoogle Scholar
  57. Wiener JG, Spry DJ (1996) Toxicological significance of mercury in freshwater fish. In: Beyer WN, Heinz GH, Redmon-Norwood AW (eds) Environmental contaminants in wildlife: interpreting tissue concentrations. CRC, Boca Raton, p 512Google Scholar
  58. Witters HE (1998) Chemical speciation dynamics and toxicity assessment in aquatic ecosystems. Ecotoxicol Environ Saf 41:90–95CrossRefGoogle Scholar
  59. Zhang L, Campbell LM, Johnson TB (2012) Seasonal variation in mercury and food web biomagnification in Lake Ontario, Canada. Environ Pollut 161(C):178–184Google Scholar
  60. Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • C. L. Mieiro
    • 1
  • M. Dolbeth
    • 2
    • 3
  • T. A. Marques
    • 4
  • A. C. Duarte
    • 1
  • M. E. Pereira
    • 1
  • M. Pacheco
    • 2
  1. 1.CESAM and Department of ChemistryUniversity of AveiroAveiroPortugal
  2. 2.CESAM and Department of BiologyUniversity of AveiroAveiroPortugal
  3. 3.CFE, Department of Life SciencesUniversity of CoimbraCoimbraPortugal
  4. 4.Centre for Research into Ecological and Environmental ModellingUniversity of St AndrewsSt AndrewsScotland

Personalised recommendations