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Biochemical biomarker responses to pollution in selected sentinel organisms across the Eastern Mediterranean and the Black Sea

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An Erratum to this article was published on 29 September 2016

Abstract

Pollution effects were assessed by means of biochemical biomarkers (catalase, glutathione S-transferase and acetylcholinesterase activities, and metallothioneins content) in five species at selected coastal sites across the Eastern Mediterranean and the Black Sea. The mussel Mytilus galloprovincialis, a well-established sentinel species, was investigated in the Adriatic Sea, Aegean Sea, and Black Sea. The mussel Brachidontes pharaonis and the striped red mullet Mullus surmuletus were used in the Levantine Sea where M. galloprovincialis is not present. The white seabream Diplodus sargus sargus and the gastropod Rapana venosa were additionally sampled in the Adriatic and the Black Sea, respectively. Mussels showed catalase, glutathione S-transferase, and acetylcholinesterase responses to pollution in most geographical areas while the response of metallothioneins was restricted to a few sites. R. venosa showed marked responses of catalase and metallothioneins whereas both fish species did not generally exhibit variations in biomarker values among sites. The approach based on the reference deviation concept using the “Integrated Biological Responses version 2” index was useful for the interpretation of overall biomarker responses.

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References

  • Amiard J-C, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202

    Article  CAS  Google Scholar 

  • ARSO (2012) Common database on monitoring of water quality data. Environmental Agency of the Republic Slovenia http://kazalci.arso.gov.si/?data=indicator&ind_id=69

  • ARSO (2013) Common database on monitoring of water quality data. Environmental Agency of the Republic Slovenia http://kazalci.arso.gov.si/?data=indicator&ind_id=69

  • ARSO (2015) Common database on monitoring of water quality data. Environmental Agency of the Republic Slovenia http://kazalci.arso.gov.si/?data=indicator&ind_id=69

  • Bajt O (2012) Aliphatic and polycyclic aromatic hydrocarbons in sediments of the Slovenian coastal area (Gulf of Trieste, northern Adriatic). Environ Monit Assess 184:7439–7452

    Article  CAS  Google Scholar 

  • Bebianno MJ, Lopes B, Guerra L, Hoarau P, Ferreira AM (2007) Glutathione S-transferases and cytochrome P450 activities in Mytilus galloprovincialis from the South coast of Portugal: effect of abiotic factors. Environ Int 33:550–558

    Article  CAS  Google Scholar 

  • Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316–1322

    Article  CAS  Google Scholar 

  • Bellas J, Albentosa M, Vidal-Liñán L, Besada V, Franco MA, Fumega J, González-Quijano A, Viñas L, Beiras R (2014) Combined use of chemical, biochemical and physiological variables in mussels for the assessment of marine pollution along the N-NW Spanish coast. Mar Environ Res 96:105–117

    Article  CAS  Google Scholar 

  • Benali I, Boutiba Z, Merabet A, Chèvre N (2015) Integrated use of biomarkers and condition indices in mussels (Mytilus galloprovincialis) for monitoring pollution and development of biomarker index to assess the potential toxic of coastal sites. Mar Pollut Bull doi:10.1016/j.marpolbul.2015.03.041

  • Benedetti M, Giuliani ME, Regoli F (2015) Oxidative metabolism of chemical pollutants in marine organisms: molecular and biochemical biomarkers in environmental toxicology. Ann NY Acad Sci 1340:8–19

    Article  CAS  Google Scholar 

  • Bocquené G, Galgani F, Burgeot T, Le Dean L, Truquet P (1993) Acetylcholinesterase levels in marine organisms along French coasts. Mar Pollut Bull 26:101–106

    Article  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 772:248–264

    Article  Google Scholar 

  • Broeg K, Lehtonen KK (2006) Indices for the assessment of environmental pollution of the Baltic Sea coasts: integrated assessment of a multi-biomarker approach. Mar Pollut Bull 53:508–522

    Article  CAS  Google Scholar 

  • BSC (2008). State of the Environment of the Black Sea (2001–2006/7). Edited by Temel Oguz. Publications of the Commission on the Protection of the Black Sea Against Pollution (BSC) 2008-3, Istanbul, Turkey, 448 pp

  • Cappello T, Maisano M, D’Agata A, Natalotto A, Mauceri A, Fasulo S (2013) Effects of environmental pollution in caged mussels (Mytilus galloprovincialis). Mar Environ Res 91:52–60

    Article  CAS  Google Scholar 

  • Coatu V, Oros A, Tiganuş D (2013) Contamination indicators in Report on the state of the marine and coastal environment in 2012. Cercet Mar 43:46–75, ISSN 0250–3069

    Google Scholar 

  • Cohen G, Kim M, Ogwu V (1996) A modified catalase assay suitable for a plate reader and for the analysis of brain cell cultures. J Neurosci Methods 67:53–56

    Article  CAS  Google Scholar 

  • Corsi I, Mariottini M, Menchi V, Sensini C, Balocchi C, Focardi S (2002) Monitoring a marine coastal area: use of Mytilus galloprovincialis and Mullus barbatus as bioindicators. Mar Ecol 23(Supplement 1):138–153

    Article  Google Scholar 

  • Database of the State Oceanographic Institute http://esimo.oceanography.ru/esp2/index/index/esp_id/10/section_id/8/menu_id/4426

  • Davenport J, Chen X (1987) A comparison of methods for the assessment of condition in the mussel (Mytilus edulis L.). J Molluscan Stud 53:293–297

    Article  Google Scholar 

  • Davies IM, Vethaak AD (2012) Integrated marine environmental monitoring of chemicals and their effects. ICES Coop Res Rep No 315, 277 pp

  • Dell’Anno A, Mei ML, Pusceddu A, Danovaro R (2002) Assessing the trophic state and eutrophication of coastal marine systems: a new approach based on the biochemical composition of sediment organic matter. Mar Pollut Bull 44:611–622

    Article  Google Scholar 

  • DFMR (2012) Initial assessment of the marine environment of Cyprus—part I—characteristics. Implementation of article 8 of the marine strategy framework-directive (2008/56/EC). Department of Fisheries and Marine Research, Republic of Cyprus, pp 38

  • Ellman G, Courtney KD, Jr Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  Google Scholar 

  • Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20:37–45

    Article  CAS  Google Scholar 

  • Gagné F, Burgeot T, Hellou J, St-Jean S, Farcy É, Blaise C (2008) Spatial variations in biomarkers of Mytilus edulis mussels at four polluted regions spanning the Northern Hemisphere. Environ Res 107:201–217

    Article  Google Scholar 

  • Galloway TS, Brown RJ, Browne MA, Dissanayake A, Lowe D, Jones MB, Depledge HM (2004) Ecosystem management bioindicators: the ECOMAN project—a multibiomarker approach to ecosystem management. Mar Environ Res 58:233–237

    Article  CAS  Google Scholar 

  • Giltrap M, Ronan J, Hardenberg S, Parkes G, McHugh B, McGovern E, Wilson JG (2013) Assessment of biomarkers in Mytilus edulis to determine good environmental status for implementation of MSFD in Ireland. Mar Pollut Bull 71:240–249

    Article  CAS  Google Scholar 

  • Gudimov AV (2008) Marine Mussels of the Karadag (Black Sea): population decay, ecology, and physiological adaptations. Dokl Biol Sci 422:330–332

    Article  CAS  Google Scholar 

  • Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405

    Article  CAS  Google Scholar 

  • Hagger JA, Jones MB, Leonard DRP, Owen R, Galloway TS (2006) Biomarkers and integrated environmental risk assessment: are there more questions than answers? Integr Environ Assess Manage 2:312–329

    Article  CAS  Google Scholar 

  • Hagger JA, Galloway TS, Langston W, Jones MB (2009) Application of biomarkers to assess the condition of European Marine Sites. Environ Pollut 157:2003–2010

    Article  CAS  Google Scholar 

  • HCMR (2003) In: Zeri C (ed) Record and assessment of the state of the marine environment in marina Zeas. Final report. Hellenic Center for Marine Research, Anavyssos, p 19

    Google Scholar 

  • Holmstrup M, Bindesbøl A-M, Janneke Oostingh G, Dusch A, Scheil V, Köhler HR, Loureiro S, Soares AMVM, Ferreira ALG, Kienle C, Gerhardt A, Laskowski R, Kramarz PE, Bayley M, Svendsen C, Spurgeon DJ (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408:3746–3762

    Article  CAS  Google Scholar 

  • Hyne RV, Maher WA (2003) Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotox Environ Saf 54:366–374

    Article  CAS  Google Scholar 

  • IAEA-MEL (1999) Standard operating procedures for trace metals determination

  • IAEA-MEL/Marine Environmental Studies Laboratory (1995) Training manual on the measurement of organochlorine and petroleum hydrocarbons in environmental samples

  • Ianni C, Ruggieri N, Frache R (2003) Distribution and speciation of heavy metals in Apulian coastal sediments. Toxicol Environ Chem 85:169–182

    Article  CAS  Google Scholar 

  • Jebali J, Sabbagh M, Banni M, Kamel N, Ben-Khedher S, M’hamdi N, Boussetta H (2013) Multiple biomarkers of pollution effects in Solea solea fish on the Tunisia coastline. Environ Sci Pollut Res 20:3812–3821

    Article  CAS  Google Scholar 

  • Kaberi H, Zeri C (2004) Heavy metal distribution in the inner Saronikos Gulf: an area affected by the Athens WWTP outfall—Greece, 9th FECS Conference—Behaviour of Chemicals in the Environment, Abstracts, p.430.

  • Kehrer JP (2000) The Haber–Weiss reaction and mechanisms of toxicity. Toxicology 149(1):43–50

    Article  CAS  Google Scholar 

  • Kopecka J, Lehtonen KK, Baršienė J, Broeg K, Vuorinen PJ, Gercken J, Pempkowiak J (2006) Measurements of biomarker levels in flounder (Platichthys flesus) and blue mussel (Mytilus trossulus) from the Gulf of Gdan’sk (southern Baltic). Mar Pollut Bull 53:406–421

    Article  CAS  Google Scholar 

  • Laboratory Network of the Environmental Quality monitoring of the Hellenic Seas, 2006. Environmental Quality Monitoring Program of the Hellenic Seas, Final Technical Report, Scoullos M. (ed) Athens

  • Lazar L, Boicenco L, Coatu V, Oros A, Tiganus D, Mihailov ME (2013) Nutrient levels and eutrophication of the Romanian Black Sea Waters (2006–2011)—assessment related to the marine strategy framework directive implementation. Cercet Mar 43:148–162, ISSN 0250–3069

    Google Scholar 

  • Lehtonen KK, Schiedek D, Köhler A, Lang T, Vuorinen PJ, Förlin L, Barŝiené J, Pempkowiak J, Gercken J (2006) The BEEP project in the Baltic Sea: overview of results and outline for a regional biological effects monitoring strategy. Mar Pollut Bull 53:523–5377

    Article  CAS  Google Scholar 

  • Liang LN, He B, Jiang GB, Chen DY, Yao ZW (2004) Evaluation of mollusks as biomonitors to investigate heavy metal contaminations along the Chinese Bohai Sea. Sci Total Environ 324:105–113

    Article  CAS  Google Scholar 

  • Lionetto MG, Caricato R, Giordano ME, Pascariello MF, Marinosc L, Schettino T (2003) Integrated use of biomarkers (acetylcholinesterase and antioxidant enzymes activities) in Mytilus galloprovincialis and Mullus barbatus in an Italian coastal marine area. Mar Pollut Bull 46:324–330

    Article  CAS  Google Scholar 

  • Lionetto MG, Caricato R, Calisi A. Giordano M.E, Schettino T (2013). Acetylcholinesterase as a biomarker in environmental and occupational medicine: new insights and future perspectives. BioMed Res Int 2013: art. no. 321213

  • Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666

    Article  CAS  Google Scholar 

  • Long ER, Macdonald DD, Smith SL, Calder FD (1995) Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environ Manag 19:81–97

    Article  Google Scholar 

  • Lucas A, Beninger G (1985) The use of physiological condition indices in marine bivalve aquaculture. Aquaculture 187:67–85

    Google Scholar 

  • Lyons BP, Thain JE, Stentiford GD, Hylland K, Davies IM, Vethaak AD (2010) Using biological effects tools to define Good Environmental Status under the European Union Marine Strategy Framework Directive. Mar Pollut Bull 60:1647–1651

    Article  CAS  Google Scholar 

  • Marigómez I, Zorita I, Izagirre U, Ortiz-Zarragoitia M, Navarro P, Etxebarria N, Orbea A, Soto M, Cajaraville MP (2013) Combined use of native and caged mussels to assess biological effects of pollution through the integrative biomarker approach. Aquat Toxicol 136–137:32–48

    Article  Google Scholar 

  • McFarland VA, Inouye LS, Lutz C, Jarvis AS, Clarke JU, McCant DD (1999) Biomarkers of oxidative stress and genotoxicity in livers off field-collected brown bullhead, Ameiurus nebulosus. Arch Enviro Contam Toxicol 37:236–241

    Article  CAS  Google Scholar 

  • Meneghetti F, Moschino V, Da Ros L (2004) Gametogenic cycle and variations in oocyte size of Tapes philippinarum from the Lagoon of Venice. Aquaculture 240:473–488

    Article  Google Scholar 

  • Monserrat JM, Martínez PE, Geracitano LA, Amado LL, Martins MC, Pinho CL, Chaves IS, Ferreira-Cravo M, Ventura-Lima J, Bianchini A (2007) Pollution biomarkers in estuarine animals: critical review and new perspectives. Comp Biochem Physiol C 146:221–234

    Google Scholar 

  • Moore M, Depledge M, Readman JW, Leonard DRP (2004) An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutat Res 552:247–268

    Article  CAS  Google Scholar 

  • Moschino V, Delaney E, Meneghetti F, Ros L (2011) Biomonitoring approach with mussel Mytilus galloprovincialis (Lmk) and clam Ruditapes philippinarum (Adams and Reeve, 1850) in the Lagoon of Venice. Environ Monit Assess 177:649–663

    Article  CAS  Google Scholar 

  • Moschino V, Delaney E, Da Ros L (2012) Assessing the significance of Ruditapes philippinarum as a sentinel for sediment pollution: bioaccumulation and biomarker responses. Environ Pollut 171:52–60

    Article  CAS  Google Scholar 

  • Mozetič P, Solidoro C, Cossarini G, Socal G, Precali R, Francé J, Bianchi F, De Vittor C, Smodlaka N, Fonda Umani S (2010) Recent trends towards oligotrophication of the Northern Adriatic: evidence from chlorophyll a time series. Estuar Coast 33:362–375

    Article  Google Scholar 

  • Nash RD, Valencia AH, Geffen AJ (2006) The origin of Fulton’s condition factor—setting the record straight. Fisheries 31(5):236–238

    Google Scholar 

  • Oliva M, Vicente JJ, Gravato C, Guilhermino L, Galindo-Riaño MD (2012) Oxidative stress biomarkers in Senegal sole, Solea senegalensis, to assess the impact of heavy metal pollution in a Huelva estuary (SW Spain): seasonal and spatial variation. Ecotox Environ Saf 75:151–162

    Article  CAS  Google Scholar 

  • Olivares-Rubio HF, Martínez-Torres ML, Domínguez-López ML, García-Latorre E, Vega-López A (2013) Pro-oxidant and antioxidant responses in the liver and kidney of wild Goodea gracilis and their relation with halomethanes bioactivation. Fish Physiol Biochem 39:1603–1617

    Article  CAS  Google Scholar 

  • Pampanin DM, Camus L, Gomiero A, Marangon I, Volpato E, Nasci C (2005a) Susceptibility to oxidative stress of mussels (Mytilus galloprovincialis) in the Venice Lagoon (Italy). Mar Pollut Bull 50:1548–1557

    Article  CAS  Google Scholar 

  • Pampanin DM, Volpato E, Marangon I, Nasci C (2005b) Physiological measurements from native and transplanted mussel (Mytilus galloprovincialis) in the canals of Venice. Survival in air and condition index. Comp Biochem Physiol A 140:41–52

    Article  Google Scholar 

  • Pavlidou A, Kontoyiannis H, Zarokanelos N, Hatzianestis I, Assimakopoulou G, Psyllidou-Giouranovits R (2014) Seasonal and spatial nutrient dynamics in Saronikos Gulf: the impact of sewage effluents from Athens sewage treatment plant. In: A.A. Ansari and S.S. Gill (Eds.) Eutrophication: causes, consequences and control Vol. 2, Springer, 598p.

  • Pereira P, Carvalho S, Pereira F, de Pablo H, Gaspar MB, Pacheco M, Vale C (2012) Environmental quality assessment combining sediment metal levels, biomarkers and macrobenthic communities: application to the Óbidos coastal lagoon (Portugal). Environ Monit Assess 184:7141–7151

    Article  CAS  Google Scholar 

  • Ramšak A, Ščančar J, Horvat M (2012) Evaluation of metallothioneins in blue mussels (Mytilus galloprovincialis) as a biomarker of mercury and cadmium exposure in the Slovenian waters (Gulf of Trieste): a long-term field study. Acta Adriat 53:71–86

    Google Scholar 

  • Rätz H-J, Lloret J (2003) Variation in fish condition between Atlantic cod (Gadus morhua) stocks, the effect on their productivity and management implications. Fish Res 60:369–380

    Article  Google Scholar 

  • Regoli F, Winston GW, Gorbi S, Frenzilli G, Nigro M, Corsi I, Focardi S (2003) Integrating enzymatic responses to organic chemical exposure with total oxyradical absorbing capacity and DNA damage in the European eel Anguilla anguilla. Environ Toxicol Chem 22:56–65

    Article  Google Scholar 

  • Regoli F, Frenzilli G, Bocchetti R, Annarumma F, Scarcelli V, Fattorini D, Nigro M (2004) Time-course variations of oxyradical metabolism, DNA integrity and lysosomal stability in mussels, Mytilus galloprovincialis, during a field translocation experiment. Aquat Toxicol 68:167–178

    Article  CAS  Google Scholar 

  • Richardson N, Gordon AK, Muller WJ, Whitfield AK (2011) A weight-of-evidence approach to determine estuarine fish health using indicators from multiple levels of biological organization. Aquat Conserv 21:423–432

    Article  Google Scholar 

  • Roméo M, Hoarau P, Garello G, Gnassia-Barelli M, Girard JP (2003) Mussel transplantation and biomarkers as useful tools for assessing water quality in the NW Mediterranean. Environ Pollut 122:369–378

    Article  Google Scholar 

  • Sanchez W, Porcher J-M (2009) Fish biomarkers for environmental monitoring within the Water Framework Directive of the European Union. Trac Trend Anal Chem 28:150–158

    Article  CAS  Google Scholar 

  • Sanchez W, Burgeot T, Porcher JM (2013) A novel “Integrated Biomarker Response” calculation based on reference deviation concept. Environ Sci Pollut Res 20:2721–2725

    Article  CAS  Google Scholar 

  • Ščančar J, Zuliani T, Turk T, Milačič R (2007) Organotin compounds and selected metals in the marine environment of Northern Adriatic Sea. Environ Monit Assess 127:271–282

    Article  Google Scholar 

  • Seabra Pereira CD, Abessa DM, Choueri RB, Almagro-Pastor V, Cesa A, Maranho LA, Martín-Díaz ML, Torres RJ, Gusso-Choueri PK, Almeida JE, Cortez FS, Mozeto AA, Silbiger HL, Sousa EC, Del Valls TA, Bainy AC (2014) Ecological relevance of sentinels’ biomarker responses: a multi-level approach. Mar Environ Res 96:118–126

    Article  CAS  Google Scholar 

  • Sfriso A, Facca C (2013) Annual growth and environmental relationships of the invasive species Sargassum muticum and Undaria pinnatifida in the lagoon of Venice. Estuar Coast Shelf 129:162–172

    Article  Google Scholar 

  • Sklivagou E, Varnavas SP, Hatzianestis I, Kanias G (2008) Assessment of aliphatic and polycyclic aromatic hydrocarbons and trace elements in coastal sediments of the Saronikos Gulf, Greece (Eastern Mediterranean). Mar Georesour Geotechnol 26:372–393

    Article  CAS  Google Scholar 

  • Stathopoulou E, Dassenakis M, Skoullos M (2001) Levels of mercury concentration in sediments of the Saronikos Gulf. Proceedings 7th International Conference on Environmental Science and Technology, 3–6 September, Syros, Greece, p 854–860.

  • Thain JE, Vethaak AD, Hylland K (2008) Contaminants in marine ecosystems: developing an integrated indicator framework using biological-effect techniques. ICES J Mar Sci 65:1508–1514

    Article  Google Scholar 

  • Tsangaris C, Hatzianestis I, Catsiki VA, Kormas KA, Strogyloudi E, Neofitou C, Andral B, Galgani F (2011a) Active biomonitoring in Greek coastal waters: application of the integrated biomarker response index in relation to contaminant levels in caged mussels. Sci Total Environ 412(413):359–365

    Article  Google Scholar 

  • Tsangaris C, Vergolyas M, Fountoulaki E, Nizheradze K (2011b) Oxidative stress and genotoxicity biomarker responses in grey mullet (Mugil cephalus) from a polluted environment in Saronikos Gulf, Greece. Ach Environ Con Tox 61:482–490

    Article  CAS  Google Scholar 

  • Tsapakis M, Dakanali E, Stephanou EG, Karakassis I (2010) PAHs and n-alkanes in Mediterranean coastal marine sediments: aquaculture as a significant point source. J Environ Monit 12:958–963

    Article  CAS  Google Scholar 

  • Turja R, Höher N, Snoeijs P, Baršienė J, Butrimavičienė L, Kuznetsova T, Kholodkevich SV, Devier M-H, Budzinski H, Lehtonen KK (2014) A multibiomarker approach to the assessment of pollution impacts in two Baltic Sea coastal areas in Sweden using caged mussels (Mytilus trossulus). Sci Total Environ 473–474:398–409

    Article  Google Scholar 

  • UNEP (1984) Determination of total Cd, Zn, Pb and Cu in selected marine organisms by atomic absorption spectrophotometry. Reference Methods for Marine Pollution Studies, No 11, Rev 1;1984

  • Usero J, Gonzalez-Regalado E, Gracia I (1996) Trace metals in the bivalve mollusk Chamelea gallina from the Atlantic coast of Southern Spain. Mar Pollut Bull 32:305–310

    Article  CAS  Google Scholar 

  • Viarengo A, Ponzano E, Dondero F, Fabbri R (1997) A simple spectrophotometric method for metallothionein evaluation in marine organisms: application to Mediterranean and Antarctic molluscs. Mar Environ Res 44:69–84

    Article  CAS  Google Scholar 

  • Viarengo A, Lowe D, Bolognesi C, Fabbri E, Koehler A (2007) The use of biomarkers in biomonitoring: a 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comp Biochem Physiol C 146:281–300

    CAS  Google Scholar 

  • Zorita I, Apraiz I, Ortiz-Zarragoitia M, Orbea A, Cancio I, Soto M, Marigómez I, Cajaraville MP (2007) Assessment of biological effects of environmental pollution along the NW Mediterranean Sea using mussels as sentinel organisms. Environ Pollut 148(1):236–250

    Article  CAS  Google Scholar 

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Acknowledgments

This study was funded by the PERSEUS (Policy-oriented marine Environmental Research for the Southern EUropean Seas) FP7-OCEAN-2011-287600 Project. The authors greatly appreciate the contribution of E. Papathanassiou in the implementation of this study. We also thank D. Kaparou and L. Bordbar for assistance with biomarker analyses and N. Kouerinis for assistance in chemical analyses.

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Correspondence to Tsangaris Catherine.

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Responsible editor: Cinta Porte

An erratum to this article can be found at http://dx.doi.org/10.1007/s11356-016-7740-8.

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Catherine, T., Vanessa, M., Evangelia, S. et al. Biochemical biomarker responses to pollution in selected sentinel organisms across the Eastern Mediterranean and the Black Sea. Environ Sci Pollut Res 23, 1789–1804 (2016). https://doi.org/10.1007/s11356-015-5410-x

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