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.
Similar content being viewed by others
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
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
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
Beliaeff B, Burgeot T (2002) Integrated biomarker response: a useful tool for ecological risk assessment. Environ Toxicol Chem 21:1316–1322
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Gudimov AV (2008) Marine Mussels of the Karadag (Black Sea): population decay, ecology, and physiological adaptations. Dokl Biol Sci 422:330–332
Habig WH, Jakoby WB (1981) Assays for differentiation of glutathione S-transferases. Methods Enzymol 77:398–405
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
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
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
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
Hyne RV, Maher WA (2003) Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotox Environ Saf 54:366–374
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
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
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
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
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
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
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
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
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
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
Lucas A, Beninger G (1985) The use of physiological condition indices in marine bivalve aquaculture. Aquaculture 187:67–85
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
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
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
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
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
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
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
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
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
Nash RD, Valencia AH, Geffen AJ (2006) The origin of Fulton’s condition factor—setting the record straight. Fisheries 31(5):236–238
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Cinta Porte
An erratum to this article can be found at http://dx.doi.org/10.1007/s11356-016-7740-8.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-5410-x