Skip to main content
Log in

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

Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Athar M, Iqbal M (1998) Ferric nitrilotriacetate promotes N-diethylnitrosamine-induced renal tumorigenesis in the rat: implications for the involvement of oxidative stress. Carcinogenesis 19:1133–1139

    Article  CAS  Google Scholar 

  • 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 190:360–365

    Article  CAS  Google Scholar 

  • 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 24:2094–2105

    Article  CAS  Google Scholar 

  • 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 36:75–98

    Article  CAS  Google Scholar 

  • Bird RP, Draper AH (1984) Comparative studies on different methods of malondialdehyde determination. Methods Enzymol 90:105–110

    Google Scholar 

  • 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 156:469–479

    Article  CAS  Google Scholar 

  • 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 138:411–427

  • Carlberg I, Mannervik B (1975) Purification and characterization of the flavoenzyme glutathione reductase from rat liver. J Biol Chem 250:5475–5480

    CAS  Google Scholar 

  • Claiborne A (1985) Catalase activity. In: Greenwald RA (ed) Handbook of methods in oxygen radical research. CRC, Boca Raton, pp 283–284

    Google Scholar 

  • 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 65:492–500

    Article  CAS  Google Scholar 

  • 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 78:505–512

    Article  CAS  Google Scholar 

  • 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 405:179–183

    Article  CAS  Google Scholar 

  • 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 31:1536–1547

  • Dillon T, Beckvar N, Kern J (2010) Residue-based mercury dose-response in fish: an analysis using lethality-equivalent test endpoints. Environ Toxicol Chem 29:2559–2565

    Article  CAS  Google Scholar 

  • 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 78:51–60

    Article  Google Scholar 

  • 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):331–338

    Google Scholar 

  • 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 6:840–846

    CAS  Google Scholar 

  • Filho WD, Giuvili C, Boveris A (1993) Antioxidant defenses in marine fish. I. Teleosts. Comp Biochem Physiol 106C:409–414

    Google Scholar 

  • 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 203:149–158

    Article  Google Scholar 

  • 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 34:719–726

    Google Scholar 

  • 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 17:2023–2028

    Article  CAS  Google Scholar 

  • Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751–766

    CAS  Google Scholar 

  • 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 56:845–859

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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 559–590

    Google Scholar 

  • 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 140:408–421

  • 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 70:83–93

    Article  CAS  Google Scholar 

  • 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 72:1861–1870

  • 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 56:1834–1843

    Article  CAS  Google Scholar 

  • 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 19:1034–1045

  • 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 103:233–240

    Article  CAS  Google Scholar 

  • 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 74:2225–2232

    Article  CAS  Google Scholar 

  • Mieiro CL, Pacheco M, Pereira ME, Duarte AC (2011c) Mercury organotropism in feral European sea bass (Dicentrarchus labrax). Arch Environ Contam Toxicol 61:135–143

    Article  CAS  Google Scholar 

  • 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 64:2844–2848

    Article  CAS  Google Scholar 

  • 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 63:125–136

    Article  CAS  Google Scholar 

  • 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 44:5086–5091

    CAS  Google Scholar 

  • 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 71:148–158

    Article  Google Scholar 

  • 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 52:2507–2517

    Article  CAS  Google Scholar 

  • Ohkawa H (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  Google Scholar 

  • 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 396:70–78

    Article  CAS  Google Scholar 

  • 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 157:959–967

    Article  CAS  Google Scholar 

  • 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 107:133–153

    Article  CAS  Google Scholar 

  • 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 25:273–285

    Google Scholar 

  • 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):693–701

    Article  Google Scholar 

  • 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):19–25

    Google Scholar 

  • 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 37:125–130

    Article  CAS  Google Scholar 

  • 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 155:39–49

    Article  CAS  Google Scholar 

  • 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 73:805–816

    Article  CAS  Google Scholar 

  • Pinheiro JC, Bates DM (2001) Mixed models in S and S-Plus, 2de print. Springer, New York

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1-107

  • 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, Austria

  • 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):353–356

    Article  CAS  Google Scholar 

  • 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 2001

  • Sandheinrich MB, Bhavsar SP, Bodaly RA, Drevnick PE, Paul EA (2011) Ecological risk of methylmercury to piscivorous fish of the Great Lakes region. Ecotoxicology 20:1577–1587

    Article  CAS  Google Scholar 

  • Tietze F (1969) Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione. Anal Biochem 27:502–522

    Article  CAS  Google Scholar 

  • 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 174:223–234

    Article  Google Scholar 

  • 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 512

    Google Scholar 

  • Witters HE (1998) Chemical speciation dynamics and toxicity assessment in aquatic ecosystems. Ecotoxicol Environ Saf 41:90–95

    Article  CAS  Google Scholar 

  • Zhang L, Campbell LM, Johnson TB (2012) Seasonal variation in mercury and food web biomagnification in Lake Ontario, Canada. Environ Pollut 161(C):178–184

    CAS  Google Scholar 

  • Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. L. Mieiro.

Additional information

Responsible editor: Vera Slaveykova

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 109 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mieiro, C.L., Dolbeth, M., Marques, T.A. et al. Mercury accumulation and tissue-specific antioxidant efficiency in the wild European sea bass (Dicentrarchus labrax) with emphasis on seasonality. Environ Sci Pollut Res 21, 10638–10651 (2014). https://doi.org/10.1007/s11356-014-3053-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3053-y

Keywords

Navigation