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Chemical and biomarker responses for site-specific quality assessment of the Lake Maggiore (Northern Italy)

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Abstract

Since the 1990s, the Lake Maggiore (Northern Italy) has been recognized as an aquatic environment contaminated by DDTs and other persistent organic pollutants, but to date just few studies were carried out to investigate the effects of pollution to aquatic organisms. The aim of this study was the application of a stepwise approach based on chemical data, a suite of biomarkers and the integration of their responses into a biomarker response index (BRI) to evaluate the site-specific quality assessment in different sampling stations of Lake Maggiore, one of the largest European lakes. We used as biological model the freshwater bivalve Zebra mussel (Dreissena polymorpha). Several hundred bivalve specimens were sampled on May 2011 from eight sampling sites located along the lake shoreline. We measured levels of DDTs, PCBs, HCHs, HCB, and PAHs accumulated in D. polymorpha soft tissues by GC/MSn, while the activities of catalase, superoxide dismutase, glutathione peroxidase, and glutathione S-transferase, as well as the lipid peroxidation and protein carbonyl content were evaluated in homogenates from native bivalves as oxidative stress indices. Moreover, DNA damage was investigated by the alkaline precipitation assay. Significant imbalances of enzymatic activity were found in mussels from most of the sampling sites, as well as notable increases of damage to macromolecules. Health status of mussels from Baveno was greatly affected by lake pollution, probably due to high levels of DDTs measured in this site, while a wide variability in biomarker responses was found in all the other stations. The application of a BRI allowed distinguishing impacts of pollution to bivalves, confirming mussels from Baveno as the most threatened and revealing that also the health status of bivalves from Suna, Brissago, Pallanza, and Laveno is affected. These evidences suggest the usefulness of a specific index to integrate all the biomarker endpoints in order to provide a correct environmental risk assessment.

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References

  • Almeida JR, Oliveira C, Gravato C, Guilhermino L (2010) Linking behavioural alterations with biomarkers responses in the European seabass Dicentrarchus labrax L. exposed to the organophosphate pesticide fenitrothion. Ecotoxicology 19:1369–1381

    Article  CAS  Google Scholar 

  • Binelli A, Bacchetta R, Vailati G, Galassi S, Provini A (2001) DDT contamination in Lake Maggiore (N. Italy) and effects on zebra mussel spawning. Chemosphere 45:409–415

    Article  CAS  Google Scholar 

  • Binelli A, Ricciardi F, Provini A (2004) Present status of POP contamination in Lake Maggiore (Italy). Chemosphere 57:27–34

    Google Scholar 

  • Binelli A, Ricciardi F, Riva C, Provini A (2006) New evidences for old biomarkers: effects of several xenobiotics on EROD and AChE activities in Zebra mussel (Dreissena polymorpha). Chemosphere 62:510–519

    Article  CAS  Google Scholar 

  • Binelli A, Sarkar SK, Chatterjee M, Riva C, Parolini M, Bhattacharya B, Bhattacharya AK, Satpathy KK (2008a) Congener profiles of polychlorinated biphenyls in core sediments of Sunderban mangrove wetland (N.E. India) and their ecotoxicological significance. Environ Monit Assess 153:221–234

    Article  Google Scholar 

  • Binelli A, Sarkar SK, Chatterjee M, Riva C, Parolini M, Bhattacharya B, Bhattacharya AK, Satpathy KK (2008b) A comparison of sediment quality guidelines for toxicity assessment in the Sunderban wetlands (Bay of Bengal, India). Chemosphere 73:1129–1137

    Article  CAS  Google Scholar 

  • Binelli A, Guzzella L, Roscioli C (2008c) Levels and congener profiles of polybrominated diphenyl ethers (PBDEs) in Zebra mussels (D. polymorpha) from Lake Maggiore (Italy). Environ Pollut 153:610–617

    Article  CAS  Google Scholar 

  • Binelli A, Cogni D, Parolini M, Riva C, Provini A (2009) In vivo experiments for the evaluation of genotoxic and cytotoxic effects of triclosan in zebra mussel hemocytes. Aquat Toxicol 91:238–244

    Google Scholar 

  • Box A, Sureda A, Galgani F, Pons A, Deudero S (2007) Assessment of environmental pollution at Balearic Islands applying oxidative stress biomarkers in the mussel Mytilus galloprovincialis. Comp Biochem Physiol C 146:531–539

    CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Brooks S, Harman C, Zaldibar B, Izagirre U, Glette T, Marigómez I (2011) Integrated biomarker assessment of the effects exerted by treated produced water from an onshore natural gas processing plant in the North Sea on the mussel Mytilus edulis. Mar Pollut Bull 62:327–339

    Article  CAS  Google Scholar 

  • Camusso M, Balestrini R, Binelli A (2001) Use of zebra mussel (Dreissena polymorpha) to assess trace metal contamination in the largest Italian subalpine lakes. Chemosphere 44:263–270

    Article  CAS  Google Scholar 

  • Carballeira A (2003) Considerations in the design of a monitoring program of the biological effects of the Prestige oil spill. Cienc Mar 29:123–139

    CAS  Google Scholar 

  • Ceschi M, De Rossa M, Jaggli M (1996) Contaminanti organici, inorganici e radionuclidi nell_ittiofauna dei laghi Ceresio e Verbano (bacini svizzeri). Travaux de chimie alimentaire et d’ hygiène 87:189–211

    CAS  Google Scholar 

  • Cheung CCC, Zheng GJ, Lam PKS, Richardson BJ (2002) Relationships between tissue concentrations of chlorinated hydrocarbons (polychlorinated biphenyls and chlorinated pesticides) and antioxidative responses of marine mussels, Perna viridis. Mar Pollut Bull 45:181–191

    Article  CAS  Google Scholar 

  • CIPAIS (1999) Ricerche sulla distribuzione e gli effetti del DDT nell’ecosistema Lago Maggiore. Rapporto finale sui risultati delle indagini. Ed. Commissione internazionale per la protezione acque italo-svizzere: 81 pp

  • CIPAIS (2002) Monitoraggio della presenza del DDT e di altri contaminanti nell’ecosistema Lago Maggiore. Rapporto annuale aprile 2001–marzo 2002. Ed. Commissione Internazionale per la protezione delle acque italo-svizzere: 89 pp

  • CIPAIS (2003) Monitoraggio della presenza del DDT e di altri contaminanti nell’ecosistema Lago Maggiore. Rapporto annuale aprile 2002–marzo 2003. Ed. Commissione Internazionale per la protezione delle acque italo-svizzere: 68 pp

  • CIPAIS (2004) Monitoraggio della presenza del DDT e di altri contaminanti nell’ecosistema Lago Maggiore. Rapporto annuale aprile 2003–marzo 2004. Ed. Commissione Internazionale per la protezione delle acque italo-svizzere: 68 pp

  • CIPAIS (2005) Monitoraggio della presenza del DDT e di altri contaminanti nell’ecosistema Lago Maggiore. Rapporto annuale aprile 2004–marzo 2005. Ed. Commissione Internazionale per la protezione delle acque italo-svizzere: 76 pp

  • CIPAIS (2006) Monitoraggio della presenza del DDT e di altri contaminanti nell’ecosistema Lago Maggiore. Rapporto annuale aprile 2005–marzo 2006. Ed. Commissione Internazionale per la protezione delle acque italo-svizzere: 76 pp

  • CIPAIS (2007) Monitoraggio della presenza del DDT e di altri contaminanti nell’ecosistema Lago Maggiore. Campagna 2006-2007. Rapporto finale 2001-2007. Ed. Commissione Internazionale per la protezione delle acque italo-svizzere: 102 pp

  • CIPAIS (2008) Indagini su DDT e sostanze pericolose nell’ecosistema del Lago Maggiore. Programma 2008–2012. Rapporto annuale 2008. Ed. Commissione Internazionale per la protezione delle acque italo-svizzere: 85 pp

  • CIPAIS (2009) Indagini su DDT e sostanze pericolose nell’ecosistema del Lago Maggiore. Programma 2008–2012. Rapporto annuale 2009. Ed. Commissione Internazionale per la protezione delle acque italo-svizzere: 108 pp

  • CIPAIS (2010) Indagini su DDT e sostanze pericolose nell’ecosistema del Lago Maggiore. Programma 2008–2012. Rapporto annuale 2010. Ed. Commissione Internazionale per la protezione delle acque italo-svizzere: 129 pp

  • CIPAIS (2011) Indagini su DDT e sostanze pericolose nell’ecosistema del Lago Maggiore. Programma 2008–2012. Rapporto annuale 2011. Ed. Commissione Internazionale per la protezione delle acque italo-svizzere: 108 pp

  • Cortinovis S, Galassi S, Melon G, Saino N, Porte C, Bettinetti R (2008) Organochlorine contamination in the Great Crested Grebe (Podiceps cristatus): effects on eggshell thickness and egg steroid levels. Chemosphere 73:320–325

    Article  CAS  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 12:155–172

    Article  CAS  Google Scholar 

  • Dondero F, Dagnino A, Jonsson H, Caprì F, Gastaldi L, Viarengo A (2006) Assessing the occurrence of a stress syndrome in mussel (Mytilus edulis) using a combined biomarker/gene expression approach. Aquat Toxicol 78:13–24

    Article  Google Scholar 

  • Elia AC, Galarini R, Dorra AJM, Taticchi MI (2007) Heavy metal contamination and antioxidant response of a freshwater bryozoan (Lophopus crystallinus Pall., Phylactolaemata). Ecotoxicol Environ Saf 66:188–194

    Google Scholar 

  • El-Shenawy NS, Mohammadden A, Al-Fahmie ZH (2012) Using the enzymatic and non-enzymatic antioxidant defense system of the land snail Eobania vermiculata as biomarkers of terrestrial heavy metal pollution. Ecotox Environ Safe 84:347–354

    Article  CAS  Google Scholar 

  • Faria M, Huertas D, Soto DX, Grimalt JO, Catalan J, Riva MC, Barata C (2010) Contaminant accumulation and multi-biomarker responses in field collected zebra mussels (Dreissena polymorpha) and crayfish (Procambarus clarkii), to evaluate toxicological effects of industrial hazardous dumps in the Ebro river (NE Spain). Chemosphere 78:232–240

    Article  CAS  Google Scholar 

  • Hagger JA, Galloway TS, Oehlmann J, Jobling S, Depledge MH (2006) Is there a causal association between genotoxicity and the imposex effect? Environ Health Perspect 114:20–26

    Article  Google Scholar 

  • Hagger JA, Jones MB, Lowe D, Leonard DRP, Owen R, Galloway T (2008) Application of biomarkers for improving risk assessments of chemicals under the Water Framework Directive: a case study. Mar Pollut Bull 56:1111–1118

    Article  CAS  Google Scholar 

  • Hagger JA, Lowe D, Dissanayake A, Jones MB, Galloway TS (2010) The influence of seasonality on biomarker responses in Mytilus edulis. Ecotoxicology 19:953–962

    Article  CAS  Google Scholar 

  • 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 

  • Mecocci P, Fano G, Fulle S, MacGarvey U, Shinobu L, Polidori MC, Cherubini A, Vecchiet J, Senin U, Beal MF (1998) Age-dependent increases in oxidative damage to DNA, lipids, and proteins in human skeletal muscle. Free Radical Bio Med 26:303–308

    Article  Google Scholar 

  • Monserrat JM, Martinez 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 

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

    Article  CAS  Google Scholar 

  • Olive P (1988) DNA precipitation assay: a rapid and simple method for detecting DNA damage in mammalian cells. Environ Mol Mutagen 11:487–495

    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 (Riade 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 

  • Orbea A, Ortiz-Zarragoitia M, Solé M, Porte C, Cajaraville MP (2002) Antioxidant enzymes and peroxisome proliferation in relation to contaminant body burdens of PAHs and PCBs in bivalve molluscs, crabs and fish from the Urdaibai and Plentzia estuaries (Bay of Biscay). Aquat Toxicol 58:75–98

    Article  CAS  Google Scholar 

  • Parolini M, Binelli A (2011) Cyto-genotoxic effects induced by three brominated diphenyl ether congeners on the freshwater mussel Dreissena polymorpha. Ecotoxicol Environ Saf 76:1586–1594

    Article  Google Scholar 

  • Parolini M, Binelli A (2012) Sub-lethal effects induced by a mixture of three non-steroidal anti-inflammatory drugs (NSAIDs) on the freshwater bivalve Dreissena polymorpha. Ecotoxicology 21:379–392

    Article  CAS  Google Scholar 

  • Parolini M, Binelli A, Cogni D, Provini A (2010) Multi-biomarker approach for the evaluation of the cyto-genotoxicity of paracetamol on Zebra mussel (Dreissena polymorpha). Chemosphere 79:489–498

    Article  CAS  Google Scholar 

  • Parolini M, Binelli A, Provini A (2011a) Assessment of the potential cyto-genotoxicity of the nonsteroidal anti-inflammatory drug (NSAID) diclofenac on the zebra mussel (Dreissena polymorpha). Water Air Soil Pollut 217:589–601

    Article  CAS  Google Scholar 

  • Parolini M, Binelli A, Provini A (2011b) Chronic effects induced by ibuprofen on the freshwater bivalve Dreissena polymorpha. Ecotox Environ Safe 74:1586–1594

    Google Scholar 

  • Parolini M, Pedriali A, Riva C, Binelli A (2013) Sub-lethal effects caused by the cocaine metabolite benzoylecgonine to the freshwater mussel Dreissena polymorpha. Sci Total Environ 444:43–50

    Google Scholar 

  • Pereira CDS, Martin-Dıaz ML, Zanette J, Cesar A, Choueri RB, de SouzaAbessa DM, Catharino MGM, Vasconcellos MBA, Bainy ACD, Moreira de Sousa ECP, Del Valls TA (2011) Integrated biomarker responses as environmental status descriptors of a coastal zone (Sao Paulo, Brazil). Ecotox Environ Safe 74:1257–1264

    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, 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 

  • Ricciardi F, Binelli A, Provini A (2006) Use of two biomarkers (CYP450 and acetylcholinesterase) in zebra mussel for the biomonitoring of Lake Maggiore (Northern Italy). Ecotox Environ Safe 63:406–412

    Article  CAS  Google Scholar 

  • Richardson BJ, Mak E, De Luca-Abbott SB, Martin M, McClellan K, Lam PKS (2008) Antioxidant responses to polycyclic aromatic hydrocarbons and organochlorine pesticides in green-lipped mussels (Perna viridis): do mussels integrate biomarker responses? Mar Pollut Bull 57:503–514

    Article  CAS  Google Scholar 

  • Riva C, Binelli A, Provini A (2008) Evaluation of several priority pollutants in zebra mussels (Dreissena polymorpha) in the largest Italian subalpine lakes. Environ Pollut 151:652–662

    Article  CAS  Google Scholar 

  • Riva C, Binelli A, Parolini M, Provini A (2010) The case of pollution of Lake Maggiore: a 12-year study with the bioindicator mussel Dreissena polymorpha. Water Air Soil Pollut 210:75–86

    Article  CAS  Google Scholar 

  • Sarkar SK, Binelli A, Riva C, Parolini M, Chatterjee M, Bhattacharya AK (2008) Monitoring of organochlorine pesticide residues in sediment cores of Sunderban mangrove wetland, Northeaster part of the Bay of Bengal, India. Arch Environ Contam Toxicol 55(3):58–71

    Article  Google Scholar 

  • Solé M (2000) Assessment of the results of chemical analyses combined with the biological effects of organic pollution on mussels. Trends Anal Chem 19:1–9

    Article  Google Scholar 

  • Tabachnic BG, Fidell LS (1996) Using multivariate statistics. Harper Collins, New York

    Google Scholar 

  • Vidal-Liñán L, Bellas J, Campillo JA, Beiras R (2011) Integrated use of antioxidant enzymes in mussels, Mytilus galloprovincialis, for monitoring pollution in highly productive coastal areas of Galicia (NW Spain). Chemosphere 78:265–272

    Article  Google Scholar 

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Correspondence to Marco Parolini.

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Parolini, M., Pedriali, A. & Binelli, A. Chemical and biomarker responses for site-specific quality assessment of the Lake Maggiore (Northern Italy). Environ Sci Pollut Res 20, 5545–5557 (2013). https://doi.org/10.1007/s11356-013-1556-6

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