Environmental Science and Pollution Research

, Volume 23, Issue 2, pp 1789–1804 | Cite as

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

  • Tsangaris CatherineEmail author
  • Moschino Vanessa
  • Strogyloudi Evangelia
  • Coatu Valentina
  • Ramšak Andreja
  • Abu Alhaija Rana
  • Carvalho Susana
  • Felline Serena
  • Kosyan Alisa
  • Lazarou Yiota
  • Hatzianestis Ioannis
  • Oros Andra
  • Tiganus Daniela
Research Article


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.


Pollution effects Biomarkers Acetylcholinesterase Catalase Glutathione S-transferase Metallothioneins Eastern Mediterranean Sea Black Sea 



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.


  1. 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 76:160–202CrossRefGoogle Scholar
  2. ARSO (2012) Common database on monitoring of water quality data. Environmental Agency of the Republic Slovenia
  3. ARSO (2013) Common database on monitoring of water quality data. Environmental Agency of the Republic Slovenia
  4. ARSO (2015) Common database on monitoring of water quality data. Environmental Agency of the Republic Slovenia
  5. Bajt O (2012) Aliphatic and polycyclic aromatic hydrocarbons in sediments of the Slovenian coastal area (Gulf of Trieste, northern Adriatic). Environ Monit Assess 184:7439–7452CrossRefGoogle Scholar
  6. 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 33:550–558CrossRefGoogle Scholar
  7. Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316–1322CrossRefGoogle Scholar
  8. 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 96:105–117CrossRefGoogle Scholar
  9. 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
  10. 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 1340:8–19CrossRefGoogle Scholar
  11. Bocquené G, Galgani F, Burgeot T, Le Dean L, Truquet P (1993) Acetylcholinesterase levels in marine organisms along French coasts. Mar Pollut Bull 26:101–106CrossRefGoogle Scholar
  12. 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 772:248–264CrossRefGoogle Scholar
  13. 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 53:508–522CrossRefGoogle Scholar
  14. 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 ppGoogle Scholar
  15. 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 91:52–60CrossRefGoogle Scholar
  16. 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
  17. 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 67:53–56CrossRefGoogle Scholar
  18. 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):138–153CrossRefGoogle Scholar
  19. Davenport J, Chen X (1987) A comparison of methods for the assessment of condition in the mussel (Mytilus edulis L.). J Molluscan Stud 53:293–297CrossRefGoogle Scholar
  20. Davies IM, Vethaak AD (2012) Integrated marine environmental monitoring of chemicals and their effects. ICES Coop Res Rep No 315, 277 ppGoogle Scholar
  21. 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 44:611–622CrossRefGoogle Scholar
  22. 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 38Google Scholar
  23. Ellman G, Courtney KD, Jr Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95CrossRefGoogle Scholar
  24. Fulton MH, Key PB (2001) Acetylcholinesterase inhibition in estuarine fish and invertebrates as an indicator of organophosphorus insecticide exposure and effects. Environ Toxicol Chem 20:37–45CrossRefGoogle Scholar
  25. 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 107:201–217CrossRefGoogle Scholar
  26. 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 58:233–237CrossRefGoogle Scholar
  27. 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 71:240–249CrossRefGoogle Scholar
  28. Gudimov AV (2008) Marine Mussels of the Karadag (Black Sea): population decay, ecology, and physiological adaptations. Dokl Biol Sci 422:330–332CrossRefGoogle Scholar
  29. Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405CrossRefGoogle Scholar
  30. 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 2:312–329CrossRefGoogle Scholar
  31. Hagger JA, Galloway TS, Langston W, Jones MB (2009) Application of biomarkers to assess the condition of European Marine Sites. Environ Pollut 157:2003–2010CrossRefGoogle Scholar
  32. 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 19Google Scholar
  33. 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 408:3746–3762CrossRefGoogle Scholar
  34. Hyne RV, Maher WA (2003) Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotox Environ Saf 54:366–374CrossRefGoogle Scholar
  35. IAEA-MEL (1999) Standard operating procedures for trace metals determinationGoogle Scholar
  36. IAEA-MEL/Marine Environmental Studies Laboratory (1995) Training manual on the measurement of organochlorine and petroleum hydrocarbons in environmental samplesGoogle Scholar
  37. Ianni C, Ruggieri N, Frache R (2003) Distribution and speciation of heavy metals in Apulian coastal sediments. Toxicol Environ Chem 85:169–182CrossRefGoogle Scholar
  38. 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 20:3812–3821CrossRefGoogle Scholar
  39. 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.Google Scholar
  40. Kehrer JP (2000) The Haber–Weiss reaction and mechanisms of toxicity. Toxicology 149(1):43–50CrossRefGoogle Scholar
  41. 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 53:406–421CrossRefGoogle Scholar
  42. 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) AthensGoogle Scholar
  43. 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
  44. 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 53:523–5377CrossRefGoogle Scholar
  45. 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 324:105–113CrossRefGoogle Scholar
  46. 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 46:324–330CrossRefGoogle Scholar
  47. 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. 321213Google Scholar
  48. Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666CrossRefGoogle Scholar
  49. 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 19:81–97CrossRefGoogle Scholar
  50. Lucas A, Beninger G (1985) The use of physiological condition indices in marine bivalve aquaculture. Aquaculture 187:67–85Google Scholar
  51. 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 60:1647–1651CrossRefGoogle Scholar
  52. 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 136–137:32–48CrossRefGoogle Scholar
  53. 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 37:236–241CrossRefGoogle Scholar
  54. Meneghetti F, Moschino V, Da Ros L (2004) Gametogenic cycle and variations in oocyte size of Tapes philippinarum from the Lagoon of Venice. Aquaculture 240:473–488CrossRefGoogle Scholar
  55. 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 146:221–234Google Scholar
  56. Moore M, Depledge M, Readman JW, Leonard DRP (2004) An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutat Res 552:247–268CrossRefGoogle Scholar
  57. 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 177:649–663CrossRefGoogle Scholar
  58. 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 171:52–60CrossRefGoogle Scholar
  59. 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 33:362–375CrossRefGoogle Scholar
  60. Nash RD, Valencia AH, Geffen AJ (2006) The origin of Fulton’s condition factor—setting the record straight. Fisheries 31(5):236–238Google Scholar
  61. 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 75:151–162CrossRefGoogle Scholar
  62. 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 39:1603–1617CrossRefGoogle Scholar
  63. 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 50:1548–1557CrossRefGoogle Scholar
  64. 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 140:41–52CrossRefGoogle Scholar
  65. 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.Google Scholar
  66. 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 184:7141–7151CrossRefGoogle Scholar
  67. 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 53:71–86Google Scholar
  68. 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 60:369–380CrossRefGoogle Scholar
  69. 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 22:56–65CrossRefGoogle Scholar
  70. 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 68:167–178CrossRefGoogle Scholar
  71. 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 21:423–432CrossRefGoogle Scholar
  72. 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 122:369–378CrossRefGoogle Scholar
  73. Sanchez W, Porcher J-M (2009) Fish biomarkers for environmental monitoring within the Water Framework Directive of the European Union. Trac Trend Anal Chem 28:150–158CrossRefGoogle Scholar
  74. Sanchez W, Burgeot T, Porcher JM (2013) A novel “Integrated Biomarker Response” calculation based on reference deviation concept. Environ Sci Pollut Res 20:2721–2725CrossRefGoogle Scholar
  75. 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 127:271–282CrossRefGoogle Scholar
  76. 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 96:118–126CrossRefGoogle Scholar
  77. 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 129:162–172CrossRefGoogle Scholar
  78. 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 26:372–393CrossRefGoogle Scholar
  79. 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.Google Scholar
  80. Thain JE, Vethaak AD, Hylland K (2008) Contaminants in marine ecosystems: developing an integrated indicator framework using biological-effect techniques. ICES J Mar Sci 65:1508–1514CrossRefGoogle Scholar
  81. 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):359–365CrossRefGoogle Scholar
  82. 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 61:482–490CrossRefGoogle Scholar
  83. 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 12:958–963CrossRefGoogle Scholar
  84. 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 473–474:398–409CrossRefGoogle Scholar
  85. 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;1984Google Scholar
  86. 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 32:305–310CrossRefGoogle Scholar
  87. 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 44:69–84CrossRefGoogle Scholar
  88. 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 146:281–300Google Scholar
  89. 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):236–250CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Tsangaris Catherine
    • 1
    Email author
  • Moschino Vanessa
    • 2
  • Strogyloudi Evangelia
    • 1
  • Coatu Valentina
    • 3
  • Ramšak Andreja
    • 4
  • Abu Alhaija Rana
    • 5
  • Carvalho Susana
    • 6
  • Felline Serena
    • 7
  • Kosyan Alisa
    • 8
  • Lazarou Yiota
    • 9
  • Hatzianestis Ioannis
    • 1
  • Oros Andra
    • 3
  • Tiganus Daniela
    • 3
  1. 1.Institute of Oceanography, Hellenic Center for Marine ResearchAnavyssosGreece
  2. 2.Institute of Marine Sciences—ISMAR-CNRVeneziaItaly
  3. 3.National Institute for Marine Research and Development “Grigore Antipa”Constanta 3Romania
  4. 4.National Institute of BiologyPiranSlovenia
  5. 5.Energy, Environment and Water Research Center (EEWRC), The Cyprus InstituteNicosiaCyprus
  6. 6.KAUST—King Abdullah University of Science and Technology, Red Sea Research CenterThuwalSaudi Arabia
  7. 7.Laboratory of Zoology and Marine Biology, Department of Biological and Environmental Science and TechnologiesUniversity of SalentoLecceItaly
  8. 8.Laboratory of Ecology and Morphology of Marine Invertebrates, A. N. Severtsov Institute of Ecology and EvolutionRussian Academy of SciencesMoscowRussia
  9. 9.Oceanography CentreUniversity of CyprusNicosiaCyprus

Personalised recommendations