Skip to main content
Log in

A multi-biomarker approach in cross-transplanted mussels Mytilus galloprovincialis

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The present work integrates the active biomonitoring (ABM) concept in mussels Mytilus galloprovincialis from the South coast of Portugal transplanted during 28 days between two sites with different sources of contamination, and vice versa, in order to assess biological effects in these mussels. For that purpose a multibiomarker approach was used. The suit of biomarkers indicative of metal contamination were metallothioneins (MT) and the enzyme δ-aminolevulinic acid dehydratase (ALAD), for organic contamination mixed function oxidase system (MFO), glutathione-S-transferase (GST) and acetylcholinesterase (AChE), as oxidative stress biomarkers superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx) and lipid peroxidation (LPO). These biomarkers were used to determine an index to evaluate the stress levels in these two sites. Site A is strongly influenced by metallic contamination, with higher Cu, Cr and Pb in M. galloprovinciallis, as well as higher MT levels, antioxidant enzymes activities and LPO concentrations, and lower ALAD activity. In site B organic compounds (PAHs) are prevalent and native mussels show higher activities of the MFO system components and GST. Transplanted mussels had significant alterations in some biomarkers that reflect the type of contaminants present in each site, which demonstrates the primary role of the environment in determining the physiological characteristics of resident mussels. Therefore the application of ABM using a battery of biomarkers turns out to be a useful approach in sites where usually complex mixtures of contaminants occurs. In this study the biomarkers that better differentiate the impact of different contaminants at each site were MT, CYP450, SOD and CAT.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Akcha F, Izuel C, Venier P, Budzinski H, Burgeot T, Narbonne JF (2000) Enzymatic biomarker measurement and study of DNA adduct formation in benzo[a]pyrene-contaminated mussels, Mytilus galloprovincialis. Aquat Toxicol 49:269–287

    Article  CAS  Google Scholar 

  • Babic M, Radic S, Cvjetko P, Roje V, Pevalek-Kozlina B, Pavlica M (2009) Antioxidative response of Lemna minor plants exposed to thallium(I)-acetate. Aquat Bot 91:166–172

    Article  CAS  Google Scholar 

  • Barroso CM, Moreira MH (2002) Spatial and temporal changes of TBT pollution along the Portuguese coast: inefficacy of the EEC directive 89/677. Mar Pollut Bull 44:480–486

    Article  CAS  Google Scholar 

  • Barroso CM, Mendo S, Moreira MH (2004) Organotin contamination in the mussel Mytilus galloprovincialis from Portuguese coastal waters. Mar Pollut Bull 48:1145–1167

    Article  Google Scholar 

  • Bebianno MJ, Langston WJ (1989) Quantification of metallothioneins in marine invertebrates using differential pulse polarography. Port Electrochim Acta 7:511–524

    CAS  Google Scholar 

  • Bebianno MJ, Machado LM (1997) Concentrations of metal and metallothioneins in Mytilus galloprovincialis along the South Coast of Portugal. Mar Pollut Bull 34:666–671

    Article  CAS  Google Scholar 

  • Bebianno MJ, Serafim MA (2003) Variation of metal and metallothionein concentrations in a natural population of Ruditapes decussatus. Arch Environ Contam Toxicol 44:53–66

    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(4):550–558

    Article  CAS  Google Scholar 

  • Berlin A, Schaller K (1974) European standardized method for determination of delta-ALAD activity in blood. Z Klin Chem Klin Biochem 12:389–390

    CAS  Google Scholar 

  • Besada V, Fumega J, Vaamonde A (2002) Temporal trends of Cd, Cu, Hg, Pb and Zn in mussel (Mytilus galloprovincialis) from the Spanish North-Atlantic coast 1991–1999. Sci Total Environ 288:239–253

    Article  CAS  Google Scholar 

  • Bocchetti R, Lamberti CV, Pisanelli B, Razzetti EM, Maggi C, Catalano B, Sesta G, Martuccio G, Gabellini M, Regoli F (2008) Seasonal variations of exposure biomarkers, oxidative stress responses and cell damage in the clams, Tapes philippinarum, and mussels, Mytilus galloprovincialis, from Adriatic Sea. Mar Environ Res 66(1):24–26

    Article  CAS  Google Scholar 

  • Bocquene G, Galgani F (1998) Biological effects of contaminants: cholinesterase inhibition by organophosphate and carbamate compounds. In: Proceedings of the ICES techniques in marine environmental sciences, vol 22, p 12

  • Bodin N, Burgeot T, Stanisière JY, Bocquené G, Menard D, Minier C, Boutet I, Amat A, Cherel Y, Budzinski 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

    CAS  Google Scholar 

  • Bolognesi C, Frenzilli G, Lasagna C, Perrone E, Roggieri P (2004) Genotoxicity biomarkers in Mytilus galloprovincialis: wild versus caged mussels. Mutat Res 552:153–162

    Article  CAS  Google Scholar 

  • Borkovic S, Saponjic JS, Pavlovic SZ, Blagojevic DP, Kovacevic TB, Radojicic RM, Spasic MB, Zikic RV, Saicic ZS (2005) The activity of antioxidant defence enzymes in the mussel Mytilus galloprovincialis from the Adriatic Sea. Comp Biochem Physiol C 141(4):366–374

    Google Scholar 

  • Cajaraville MP, Bebianno MJ, Blasco JC, Porte CS, Viarengo A (2000) The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Sci Total Environ 247:295–311

    Article  CAS  Google Scholar 

  • Chafik A, Cheggour M, Cossa D, Benbrahim S, Sifeddine M (2001) Quality of Moroccan Atlantic coastal waters: water monitoring and mussel watching. Aquat Living Resour 14:239–249

    Article  Google Scholar 

  • Coelho MR, Bebianno MJ, Langston WJ (2002) TBT levels in the Ria Formosa Lagoon. Appl Organomet Chem 16:1–8

    Article  Google Scholar 

  • Company R, Serafim A, Lopes B, Cravo A, Shepherd TJ, Pearson G, Bebianno MJ (2008) Using biochemical and isotope geochemistry to understand the environmental and public health implications of lead pollution in the River Guadiana, Iberia: a freshwater bivalve study. Sci Total Environ 405(1–3):109–119

    CAS  Google Scholar 

  • Company R, Serafim A, Lopes B, Cravo A, Kalman J, Riba I, DelValls TA, Blasco J, Delgado J, Sarmiento AM, Nieto JM, Shepherd TJ, Nowell MJ, Bebianno MJ (2011) Source and impact of lead contamination on δ-aminolevulinic acid dehydratase activity in several marine bivalve species along the Gulf of Cadiz. Aquat Toxicol 101(1):146–154

    Article  CAS  Google Scholar 

  • Cravo A, Lopes B, Serafim A, Company R, Barreira L, Gomes T, Bebianno MJ (2009) A multibiomarker approach in Mytilus galloprovincialis to assess environmental quality. J Environ Monit 11:1673–1686

    Article  CAS  Google Scholar 

  • Da Ros L, Meneghetti F, Nasci C (2002) Field application of lysosomal destabilisation indices in the mussel Mytilus galloprovincialis: biomonitoring and transplantation in the Lagoon of Venice (north-east Italy). Mar Environ Res 54:817–822

    Article  Google Scholar 

  • Dagnino A, Allen JI, Moore MN, Broeg K, Canesi L, Viarengo A (2007) Development of an expert system for the integration of biomarker responses in mussels into an animal health index. Biomarkers 12(2):155–172

    Article  CAS  Google Scholar 

  • Damiens G, Gnassia-Barelli M, Loquès F, Roméo M, Salbert V (2007) Integrated biomarker response index as a useful tool for environmental assessment evaluated using transplanted mussels. Chemosphere 66:574–583

    Article  CAS  Google Scholar 

  • Depledge MH (1994) The rationale basis for the use of biomarkers as ecotoxicological tools. In: Fossi MC, Leonzio C (eds) Nondestructive biomarkers in vertebrates. Lewis, Boca Raton, pp 261–285

    Google Scholar 

  • Diez S, Lacorte S, Viana P, Barcelo D, Bayona JM (2005) Survey of organotin compounds in rivers and coastal environments in Portugal 1999–2000. Environ Pollut 136:525–536

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney KO, Anders V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  Google Scholar 

  • Erdelmeier I, Gerard-Monnier D, Yadan JC, Acudiere J (1998) Reactions of N-methyl-2-phenylindole with malondialdehyde and 4-hydroxyalkenals. Mechanistic aspects of the colorimetric assay of lipid peroxidation. Chem Res Toxicol 11:1184–1194

    Article  CAS  Google Scholar 

  • Fabbri D, Baravelli V, Giannotti K, Donnini F, Fabbri E (2006) Bioaccumulation of cyclopenta[cd]pyrene and benzo[ghi]fluoranthene by mussels transplanted in a coastal lagoon. Chemosphere 64:1083–1092

    Article  CAS  Google Scholar 

  • Fernandes D, Porte C, Bebianno MJ (2007) Chemical residues and biochemical responses in wild and cultured European sea bass (Dicentrarchus labrax L.). Environ Res 103:247–256

    Article  CAS  Google Scholar 

  • Fernández B, Campillo JA, Martínez-Gómez C, Benedicto J (2010) Antioxidant responses in gills of mussel (Mytilus galloprovincialis) as biomarkers of environmental stress along the Spanish Mediterranean coast. Aquat Toxicol 99:186–197

    Article  Google Scholar 

  • Frenzilli G, Bocchetti R, Pagliarecci M, Nigro M, Annarumma F, Scarcelli V, Fattorini D, Regoli F (2004) Time-course evaluation of ROS-mediated toxicity in mussels, Mytilus galloprovincialis, during a field translocation experiment. Mar Environ Res 58:609–613

    Article  CAS  Google Scholar 

  • Gorbi S, Lamberti CV, Notti A, Benedetti M, Fattorini D, Moltedo G, Regoli F (2008) An ecotoxicological protocol with caged mussels, Mytilus galloprovincialis, for monitoring the impact of an offshore platform in the Adriatic Sea. Mar Environ Res 65:34–49

    Article  CAS  Google Scholar 

  • Greenwald RA (1985) Handbook of methods for oxygen radical research. CRC Press, Boca Raton

    Google Scholar 

  • Guilhermino L, Barros P, Silva MC, Soares AMVM (1998) Should the use of cholinesterases as a specific biomarker for organophosphate and carbamate pesticides be questioned? Biomarkers 3:157–163

    Article  CAS  Google Scholar 

  • Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 246:7130–7139

    Google Scholar 

  • Kalman J, Riba I, Blasco J, DelValls TA (2008) Is δ-aminolevulinic acid dehydratase activity in bivalves from south-west Iberian Peninsula a good biomarker of lead exposure? Mar Environ Res 66:38–40

    Article  CAS  Google Scholar 

  • Lawrence RA, Burk RF (1976) Glutathione peroxidase activity in selenium-deficient rat liver. Biochem Biophys Res Commun 71(4):952–958

    Article  CAS  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

    Google Scholar 

  • Livingstone DR (1988) Responses of microsomal NADPH-cytochrome c reductase activity and cytochrome P-450 in digestive glands of Mytilus edulis and Littorina littorea to environmental and experimental exposure to pollutants. Mar Ecol Prog Ser 46:37–43

    Article  CAS  Google Scholar 

  • Livingstone DR (1996) Cytochrome P450 in pollution monitoring. Use of cytochrome P4501A (CYP1A) as a biomarker of organic pollution in aquatic and other organisms. In: Richardson M (ed) Environmental xenobiotics. Taylor and Francis, London, pp 143–160

    Google Scholar 

  • Livingstone DR, Farrar SV (1984) Tissue and subcellular distribution of enzyme activities of mixed-function oxygenase and benzo(a)pyrene metabolism in the common mussel, Mytilus edulis. Sci Total Environ 39:209–235

    Article  CAS  Google Scholar 

  • Locatelli C (2003) Heavy metal determinations in algae, mussels and clams. Their possible employment for assessing the sea water quality criteria. J Phys IV 107:785–788

    CAS  Google Scholar 

  • Lowe DM, Fossato VU, Depledge MH (1995) Contaminant-induced lysosomal membrane damage in blood cells of mussel Mytilus galloprovincialis from the Venice Lagoon: an in vitro study. Mar Ecol Prog Ser 129:189–196

    Article  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Maanan M (2008) Heavy metal concentrations in marine molluscs from the Moroccan coastal region. Environ Pollut 153(1):176–183

    Article  CAS  Google Scholar 

  • Martin M (1992) California mussel watch: monitoring metal and organic toxicants in marine waters. In: Miskiewicz AG (ed) Impacts and bioaccumulation of contaminants in aquatic environments. Proceedings of a bioaccumulation workshop: assessment of the distribution. Water Board and Australian Marine Sciences Association Inc., Sydney, pp 15–37

  • McCord JM, Fridovich I (1969) Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244(22):6049–6055

    CAS  Google Scholar 

  • Monserrat JM, Martínez PE, Geracitano LA, Amado LL, Martins CMG, Lopes G, Pinho L, 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 Toxicol Pharmacol 146(1–2):221–234

    Article  Google Scholar 

  • Narbonne JF, Aarab N, Clérandeau C, Daubèze M, Narbonne J, Champeau O, Garrigues P (2005) Scale of classification based on biochemical markers in mussels: application to pollution monitoring in Mediterranean coasts and temporal trends. Biomarkers 10(1):58–71

    Article  CAS  Google Scholar 

  • Nasci C, Da Ros L, Nesto N, Sperni L, Passarini F, Pavoni B (2000) Biochemical and histochemical responses to environmental contaminants in clam, Tapes philippinarum, transplanted to different polluted areas of Venice Lagoon, Italy. Mar Environ Res 50:425–430

    Article  CAS  Google Scholar 

  • Nasci C, Nesto N, Monteduro RA, Da Ros L (2002) Field application of biochemical markers and a physiological index in the mussel, Mytilus galloprovincialis: transplantation and biomonitoring studies in the Lagoon of Venice (NE Italy). Mar Environ Res 54:811–816

    Article  CAS  Google Scholar 

  • Nigro M, Falleni A, Del Barga I, Scarcelli V, Lucchesi P, Regoli F, Frenzilli G (2006) Cellular biomarkers for monitoring estuarine environments: transplanted versus native mussels. Aquat Toxicol 77:339–347

    Article  CAS  Google Scholar 

  • O’Connor TP (1992) Recent trends in coastal environmental quality: results from the first five years of the NOAA Mussel Watch Project. US National Status and Trends Program, NOAA Coastal Monitoring Branch

  • Orbea A, Montoya J, Saitua E, Cajaraville MP (2000) Antioxidant enzymes and peroxisome proliferation in transplanted mussels as biomarkers of organic pollution. Comp Biochem Physiol A Mol Integr Physiol 126:113

    Article  Google Scholar 

  • Payne JF, Mathieu A, Melvin W, Fancey LL (1996) Acetylcholinesterase, an old biomarker with a new future? Field trials in association with two urban rivers and a paper mill in Newfoundland. Mar Pollut Bull 32:225–231

    Article  CAS  Google Scholar 

  • Pfeifer S, Schiedek D, Dippner J (2005) Effect of temperature and salinity on acetylcholinesterase activity, a common pollution biomarker, in Mytilus sp. from the south-western Baltic Sea. J Exp Mar Biol Ecol 320:93–103

    Article  CAS  Google Scholar 

  • Porte C, Solé M, Albaigés J, Livingstone DR (1991) Responses of mixed-function oxygenase and antioxidase enzyme system of Mytilus sp. to organic pollution. Comp Biochem Physiol C 100:138–186

    Article  Google Scholar 

  • Porte C, Biosca M, Solé M, Albaiges J (2001) The integrated use of chemical analysis, cytochrome P450 and stress proteins in mussels to assess pollution along the Galician coast (NW Spain). Environ Pollut 112:26–268

    Article  Google Scholar 

  • Rank J, Lehtonen KK, Strand J, Laursen M (2007) DNA damage, acetylcholinesterase activity and lysosomal stability in native and transplanted mussels (Mytilus edulis) in areas close to coastal chemical dumping sites in Denmark. Aquat Toxicol 84:50–61

    Article  CAS  Google Scholar 

  • Regoli F (1992) Lysosomal response as a sensitive index in biomonitoring heavy metal pollution. Mar Ecol Prog Ser 84:63–69

    Article  CAS  Google Scholar 

  • Regoli F (2000) Total oxyradical scavenging capacity (TOSC) in polluted and translocated mussels: a predictive biomarker of oxidative stress. Aquat Toxicol 50:351–361

    Article  CAS  Google Scholar 

  • Regoli F, Orlando E (1994) Accumulation and subcellular distribution of metals (Cu, Fe, Mn, Pb and Zn) in the Mediterranean mussels Mytilus galloprovincialis during a field transplant experiment. Mar Pollut Bull 28:592–600

    Article  CAS  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 

  • Riveros A, Zuniga M, Hernandez A, Camano A (2002) Cellular biomarkers in native and transplanted populations of the mussel Perumytilus purpuratus in the intertidal zones of San Jorge Bay, Antofagasta, Chile. Arch Environ Contam Toxicol 42:303–312

    Article  CAS  Google Scholar 

  • Riveros A, Zuniga M, Larrain A (2003) Copper metallothionein-like proteins as exposure biomarker in native and transplanted intertidal populations of the mussel Perumytilus purpuratus from San Jorge Bay, Antofagasta, Chile. Bull Environ Contam Toxicol 70:233–241

    Article  CAS  Google Scholar 

  • Roméo M, Hoarau P, Garrello 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 

  • Serafim MA, Bebianno MJ (2001) Variation of metallothionein and metal concentrations in the digestive gland of the clam Ruditapes decussatus: sex and seasonal effects. Environ Toxicol Chem 20:544–552

    CAS  Google Scholar 

  • Serafim A, Lopes B, Company R, Ferreira AM, Bebianno MJ (2008) Comparative petroleum hydrocarbons levels and biochemical responses in mussels from hydrothermal vents (Bathymodiolus azoricus) and coastal environments (Mytilus galloprovincialis). Mar Pollut Bull 5:529–537

    Article  Google Scholar 

  • Smolders R, Bervoets L, Blust R (2002) Transplanted zebra mussels (Dreissena polymorpha) as active biomonitors in an effluent-dominated river. Environ Toxicol Chem 21:1889–1896

    CAS  Google Scholar 

  • Solé M, Porte C, Albaigés J (1995) Seasonal variations in the mixed-function oxygenase system components and antioxidant enzymes of the mussel Mytilus galloprovincialis. Environ Toxicol Chem 14:157–164

    Google Scholar 

  • ter Braak CJF, Smilauer P (1998) CANOCO reference manual and user’s guide to Canoco for Windows: software for canonical community ordination (version 4). Microcomputer Power, Ithaca

    Google Scholar 

  • Tsangaris C, Kormas K, Strogyloudi E, Hatzianestis I, Neofitou C, Andral B, Galgani F (2010) Multiple biomarkers of pollution effects in caged mussels on the Greek coastline. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 151:369–378

    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 Pharmacol Toxicol Endocrinol 146:281–300

    Article  CAS  Google Scholar 

  • Wepener V, Bervoets L, Mubiana V, Blust R (2008) Metal exposure and biological responses in resident and transplanted blue mussels (Mytilus edulis) from the Scheldt estuary. Mar Pollut Bull 57:624–631

    Article  CAS  Google Scholar 

  • Wu H, Liu J, Zhang R, Zhang J, Guo Y, Ma E (2011) Biochemical effects of acute phoxim administration on antioxidant system and acetylcholinesterase in Oxya chinensis (Thunberg) (Orthoptera: Acrididae). Pest Biochem Physiol 100:23–26

    Article  CAS  Google Scholar 

  • Zhou JL, Fileman TW, Evans S, Donkin P, Llewellyn C, Readman JW, Mantoura RFC, Rowland SJ (1998) Fluoranthene and pyrene in the suspended particulate matter and surface sediments of the Humber estuary, UK. Mar Pollut Bull 36:587–597

    Article  CAS  Google Scholar 

  • Zinkl JG, Lockhart WL, Kenny SA, Ward FJ (1991) The effects of cholinesterase inhibiting insecticides on fish. In: Mineau P (ed) Cholinesterase inhibiting insecticides. Elsevier, Amsterdam, pp 233–254

    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 148:236–250

    Article  CAS  Google Scholar 

Download references

Acknowledgment

This study was financially supported by the FCT project ref: POCTI/CTA/48027/2002.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Angela Serafim or Maria João Bebianno.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Serafim, A., Lopes, B., Company, R. et al. A multi-biomarker approach in cross-transplanted mussels Mytilus galloprovincialis . Ecotoxicology 20, 1959–1974 (2011). https://doi.org/10.1007/s10646-011-0737-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-011-0737-7

Keywords

Navigation