Evaluation of the use of bioaccumulation and biological effects tools in caged mussels, within the European Water Framework Directive

References

• EC, Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for community action in the field of water policy. Official Journal of the European Union. 2000;L327, 1–72.
   Google Scholar
• EC, Directive 2008/105/EC of the European Parliament and of the Council of 16 December 2008, establishing environmental quality standards in the field of water policy, amending and subsequently repealing Council Directives 82/176/EEC, 83/513/EEC, 84/156/EEC, 84/491/EEC, 86/280/EEC and amending Directive 2000/60/EC of the European Parliament and of the Council. Official Journal of the European Union. 2008;L348, 84–97.
   Google Scholar
• EC, Directive 2013/39/EU of the European Parliament and of the council of 12 August 2013 amending Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy. Official Journal of the European Union. 2013;L226, 1–17.
   Google Scholar
• Ferreira JG, Vale C, Soares CV, Salas F, Stacey PE, Bricker SB, Silva MC, Marques JC. Monitoring of coastal and transitional waters under the E.U. Water Framework Directive. Environ Monit Assess. 2007;135:195–216. doi: 10.1007/s10661-007-9643-0
   PubMed Web of Science ®Google Scholar
• Borja A, Tueros I, Belzunce MJ, Galparsoro I, Garmendia JM, Revilla M, Solaun O, Valencia V. Investigative monitoring within the European Water Framework Directive: a coastal blast furnace slag disposal, as an example. J Environ Monitor. 2008;10:453–462. doi: 10.1039/b801269e
   PubMed Web of Science ®Google Scholar
• Sanchez W, Porcher JM. Fish biomarkers for environmental monitoring within the Water Framework Directive of the European Union. Trends Anal Chem. 2009;28:150–158. doi: 10.1016/j.trac.2008.10.012
   Web of Science ®Google Scholar
• Borja A, Franco J, Valencia V, Bald J, Muxika I, Belzunce MJ, Solaun O. Implementation of the European Water Framework Directive from the Basque Country (northern Spain): a methodological approach. Mar Pollut Bull. 2004;48:209–218. doi: 10.1016/j.marpolbul.2003.12.001
   PubMed Web of Science ®Google Scholar
• Borja A, Galparsoro I, Solaun O, Muxika I, Tello EM, Uriarte A, Valencia V. The European Water Framework Directive and the DPSIR, a methodological approach to assess the risk of failing to achieve good ecological status. Estuar Coast Shelf S. 2006;66:84–96. doi: 10.1016/j.ecss.2005.07.021
   Web of Science ®Google Scholar
• Tueros I, Borja A, Larreta J, Rodríguez JG, Valencia V, Millán E. Integrating long-term water and sediment pollution data, in assessing chemical status within the European Water Framework Directive. Mar Pollut Bull. 2009;58:1389–1400. doi: 10.1016/j.marpolbul.2009.04.014
   PubMed Web of Science ®Google Scholar
• Uriarte A, Borja A. Assessing fish quality status in transitional waters, within the European Water Framework Directive: setting boundary classes and responding to anthropogenic pressures. Estuar Coast Shelf S. 2009;82:214–224. doi: 10.1016/j.ecss.2009.01.008
   Web of Science ®Google Scholar
• Borja A, Muxika I, Rodríguez JG. Paradigmatic responses of marine benthic communities to different anthropogenic pressures, using M-AMBI, within the European Water Framework Directive. Mar Ecol. 2009;30:214–227. doi: 10.1111/j.1439-0485.2008.00272.x
   Web of Science ®Google Scholar
• Montero N, Belzunce-Segarra MJ, del Campo A, Garmendia JM, Ferrer L, Larreta J, González M, Maidana MA, Espino M. Integrative environmental assessment of the impact of Pasaia harbour activities on the Oiartzun estuary (southeastern Bay of Biscay). J Mar Syst. 2013;109–110:S252–S260. doi: 10.1016/j.jmarsys.2011.06.002
   Google Scholar
• van Strien AJ, van Duuren L, Foppen RPB, Soldaat LL. A typology of indicators of biodiversity change as a tool to make better indicators. Ecol Indic. 2009;9:1041–1048. doi: 10.1016/j.ecolind.2008.12.001
   Web of Science ®Google Scholar
• Melwani AR, Gregorio D, Jin Y, Stephenson M, Ichikawa G, Siegel E, Crane D, Lauenstein G, Davis JA. Mussel watch update: long-term trends in selected contaminants from coastal California, 1977–2010. Mar Pollut Bull. 2014;81:291–302. doi: 10.1016/j.marpolbul.2013.04.025
   PubMed Web of Science ®Google Scholar
• Cajaraville MP, Bebianno MJ, Blasco J, Porte C, Sarasquete C, Viarengo A. The use of biomarkers to assess the impact of pollution in coastal environments of the Iberian Peninsula: a practical approach. Sci Total Environ. 2000;247:201–212. doi: 10.1016/S0048-9697(99)00491-X
   PubMed Web of Science ®Google Scholar
• Scarpato A, Romanelli G, Galgani F, Andral B, Amici M, Giordano P, Caixach J, Calvo M, Campillo JA, Benedicto J, Cento A, Benbrahim S, Sammari C, Deudero S, Boulahdid M, Giovanardi F. Western Mediterranean coastal waters – Monitoring PCBs and pesticides accumulation in Mytilus galloprovincialis by active mussel watching: the Mytilos project. J Environ Monit. 2010;12:924–935. doi: 10.1039/b920455e
   PubMed Web of Science ®Google Scholar
• Hagger JA, Jones MB, Lowe D, Leonard DRP, Owen R, Galloway TS. Application of biomarkers for improving risk assessments of chemicals under the Water Framework Directive: a case study. Mar Pollut Bull. 2008;56:1111–1118. doi: 10.1016/j.marpolbul.2008.03.040
   PubMed Web of Science ®Google Scholar
• Martínez-Haro M, Beiras R, Bellas J, Capela R, Coelho JP, Lopes I, Moreira-Santos M, Reis-Henriques AM, Ribeiro R, Santos MM, Marques JC. A review on the ecological quality status assessment in aquatic systems using community based indicators and ecotoxicological tools: what might be the added value of their combination? Ecol Indic. 2015;48:8–16. doi: 10.1016/j.ecolind.2014.07.024
   Web of Science ®Google Scholar
• van der Oost R, Beyer J, Vermeulen NPE. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Phar. 2003;13:57–149. doi: 10.1016/S1382-6689(02)00126-6
   PubMed Web of Science ®Google Scholar
• Cajaraville MP, Marigómez JA, Angulo E. Comparative effects of the water accomodated fraction of three oils on mussels-1. Survival, growth and gonad development. Comp Biochem Phys A. 1992;102:103–112.
   PubMed Web of Science ®Google Scholar
• Viarengo A, Canesi L, Pertica M, Mancinelli G, Accomando R, Smaal AC, Orunesu M. Stress on stress response: a simple monitoring tool in the assessment of general stress syndrome in mussels. Mar Environ Res. 1995;39:245–248. doi: 10.1016/0141-1136(94)00075-Z
   Web of Science ®Google Scholar
• Pampanin DM, Volpato E, Marangon I, Nasci C. Physiological measurements from native and transplanted mussel (Mytilus galloprovincialis) in the canals of Venice. Survival in air and condition index. Comp Biochem Phys A. 2005;140:41–52. doi: 10.1016/j.cbpb.2004.10.016
   PubMed Web of Science ®Google Scholar
• Kim Y, Ashton-Alcox A, Powell EN. Histological techniques for marine bivalve molluscs: update NOAA technical memorandum. National Centers for Coastal and Ocean Science. 2006;27:76.
   Google Scholar
• Bignell JO, Dodge MJ, Feist SW, Lyons B, Martin PD, Taylor NGH, Stone D, Travalent L, Stentiford GD. Mussel histopathology: effects of season, disease and species. Aquat Biol. 2008;2:1–15. doi: 10.3354/ab00031
   Web of Science ®Google Scholar
• Baršiene J, Lazutka J, Syvokiene J, Dedonyte V, Rybakovas A, Bjørnstad A, Andersen OK. Analysis of micronuclei in blue mussels and fish from the Baltic and North Seas. Environ Toxicol. 2004;19:365–371. doi: 10.1002/tox.20031
   PubMed Web of Science ®Google Scholar
• Sundt RC, Pampanin DM, Grung M, Baršiene J, Ruus A. PAH body burden and biomarker responses in mussel (Mytilus edulis) exposed to produced water from a North Sea oil field: laboratory and field assessments. Mar Pollut Bull. 2011;62:1489–1505. doi: 10.1016/j.marpolbul.2011.04.009
   Web of Science ®Google Scholar
• Shaw JP, Large AT, Donkin P, Evans SV, Staff FJ, Livingstone DR, Chipman JK, Peters LD. Seasonal variation in cytochrome P450 immunopositive protein levels, lipid peroxidation and genetic toxicity in digestive gland of the mussel Mytilus edulis. Aquat Toxicol. 2004;67:325–336. doi: 10.1016/j.aquatox.2004.01.013
   PubMed Web of Science ®Google Scholar
• Giarratano E, Gil MN, Malanga G. Biomarkers of environmental stress in gills of ribbed mussel Aulacomya atra atra (Nuevo Gulf, Northern Patagonia). Ecotox Environ Safe. 2014;107:111–119. doi: 10.1016/j.ecoenv.2014.05.003
   PubMed Web of Science ®Google Scholar
• Gagné F, Blaise C, Pellerin J, Pelletier E, Douville M, Gauthier-Clerc S, Viglino L. Sex alteration in soft-shell clams (Mya arenaria) in an intertidal zone of the Saint Lawrence River (Quebec, Canada). Comp Biochem Phys A. 2003;134:189–198. doi: 10.1016/S1096-4959(02)00250-6
   PubMed Web of Science ®Google Scholar
• Ortiz-Zarragoitia M, Cajaraville MP. Biomarkers of exposure and reproduction-related effects in mussels exposed to endocrine disruptors. Arch Environ Con Tox. 2006;50:361–369. doi: 10.1007/s00244-005-1082-8
   PubMed Web of Science ®Google Scholar
• Borja A, Chust G, del Campo A, González M, Hernández C. Setting the maximum ecological potential of benthic communities, to assess ecological status, in heavily morphologically-modified estuarine water bodies. Mar Pollut Bull. 2013;71:199–208. doi: 10.1016/j.marpolbul.2013.03.014
   PubMed Web of Science ®Google Scholar
• Solaun O, Rodríguez JG, Borja A, Franco J, Larreta J, Valencia V. Background metal levels determination in bivalves – quality assessment of the European Water Framework Directive. Chem Ecol. 2013;29:11–27. doi: 10.1080/02757540.2012.704912
   Web of Science ®Google Scholar
• Bradford MM. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of the protein-dye binding. Anal Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3
   PubMed Web of Science ®Google Scholar
• Franco J, Borja A, Solaun O, Pérez V. Heavy metals in molluscs from the Basque Coast (Northern Spain): results from an 11-year monitoring programme. Mar Pollut Bull. 2002;44:973–976. doi: 10.1016/S0025-326X(02)00122-4
   PubMed Web of Science ®Google Scholar
• Besada V, Andrade JM, Schulze F, González JJ. Monitoring of heavy metals in wild mussels (Mytilus galloprovincialis) from the Spanish North-Atlantic coast. Cont Shelf Res. 2011;31:457–465. doi: 10.1016/j.csr.2010.04.011
   Web of Science ®Google Scholar
• Turja R, Soirinsuo A, Budzinski H, Devier MH, Lehtonen KK. Biomarker responses and accumulation of hazardous substances in mussels (Mytilus trossulus) transplanted along a pollution gradient close to an oil terminal in the Gulf of Finland (Baltic Sea). Comp Biochem Phys A. 2013;157:80–92.
   PubMed Web of Science ®Google Scholar
• Ruiz Y, Suarez P, Alonso A, Longo E, Villaverde A, San Juan F. Environmental quality of mussel farms in the Vigo estuary: pollution by PAHs, origin and effects on reproduction. Environ Pollut. 2011;159:250–265. doi: 10.1016/j.envpol.2010.08.031
   PubMed Web of Science ®Google Scholar
• Cáceres-Martínez J, Figueras A. Long-term survey on wild and cultured mussels (Mytilus galloprovincialis Lmk) reproductive cycles in the Ria de Vigo (NW Spain). Aquaculture. 1998;162:141–156. doi: 10.1016/S0044-8486(98)00210-5
   Web of Science ®Google Scholar
• Garmendia L, Soto M, Cajaraville MP, Marigómez I. Seasonality in cell and tissue-level biomarkers in Mytilus galloprovincialis: relevance for long-term pollution monitoring. Aquat Biol. 2010;9:203–219. doi: 10.3354/ab00245
   Web of Science ®Google Scholar
• Suárez-Alonso P, Álvarez González C, Molist García P, San Juan Serrano F. Gonadal atresia during the gametogenic cycle of Mytilus galloprovincialis Lamarck, 1819 cultured in the estuary of Vigo (northwestern of the Iberian Peninsula). Bol. Inst. Esp. Oceanog. 2007;23:3–10. Spanish
   Google Scholar
• Hellou J, Law RJ. Stress on stress response of wild mussels, Mytilus edulis and Mytilus trossulus, as an indicator of ecosystem health. Environ Pollut. 2003;126:407–416. doi: 10.1016/S0269-7491(03)00231-8
   PubMed Web of Science ®Google Scholar
• Giannapas M, Karnis L, Dailianis S. Generation of free radicals in haemocytes of mussels after exposure to low molecular weight PAH components: Immune activation, oxidative and genotoxic effects. Comp Biochem Phys A. 2012;155:182–189.
   PubMed Web of Science ®Google Scholar
• Auffret M. Histopathological changes related to chemical contamination in Mytilus edulis from field and experimental conditions. Mar Ecol-Prog Ser. 1988;46:101–107. doi: 10.3354/meps046101
   Web of Science ®Google Scholar
• Da Ros L, Nasci C, Marigómez I, Soto M. Biomarkers and trace metals in the digestive gland of indigenous and transplanted mussels, Mytilus galloprovincialis, in Venice Lagoon, Italy. Mar Environ Res. 2000;50:417–423. doi: 10.1016/S0141-1136(00)00038-6
   PubMed Web of Science ®Google Scholar
• Zorita I, Ortiz-Zarragoitia M, Soto M, Cajaraville MP. Biomarkers in mussels from a copper site gradient (Visnes, Norway): an integrated biochemical, histochemical and histological study. Aquat Toxicol. 2006;78:109–116. doi: 10.1016/j.aquatox.2006.02.032
   PubMed Web of Science ®Google Scholar
• Kim Y, Powell EN, Wade TL, Presley BJ. Relationship of parasites and pathologies to contaminant body burden in sentinel bivalves: NOAA Status and Trends ‘Mussel Watch’ Program. Mar Environ Res. 2008;65:101–127. doi: 10.1016/j.marenvres.2007.09.003
   PubMed Web of Science ®Google Scholar
• Suárez MP, Álvarez C, Molist P, San Juan F. Particular aspects of gonadal cycle and seasonal distribution of gametogenic stages of Mytilus galloprovincialis cultured in the estuary of Vigo. J Shellfish Res. 2005;24:531–540. doi: 10.2983/0730-8000(2005)24[531:PAOGCA]2.0.CO;2
   Web of Science ®Google Scholar
• Bocchetti R, Fattorini D, Pisanelli B, Macchia S, Oliviero L, Pilato F, Pellegrini D, Regoli F. Contaminant accumulation and biomarker responses in caged mussels, Mytilus galloprovincialis, to evaluate bioavailability and toxicological effects of remobilized chemicals during dredging and disposal operations in harbour areas. Aquat Toxicol. 2008;89:257–266. doi: 10.1016/j.aquatox.2008.07.011
   PubMed Web of Science ®Google Scholar
• Bolognesi C, Rabboni R, Roggieri P. Genotoxicity biomarkers in M. galloprovincialis as indicators of marine pollutants. Comp Biochem Phys A. 1996;113:319–323.
   Web of Science ®Google Scholar
• Vlahogianni TH, Valavanidis A. Heavy-metal effects on lipid peroxidation and antioxidant defence enzymes in mussels Mytilus galloprovincialis. Chem Ecol. 2007;23:361–371. doi: 10.1080/02757540701653285
   Web of Science ®Google Scholar
• Grintzalis K, Georgiou CD, Dailianis S. Total thiol redox status as a potent biomarker of PAH-mediated effects on mussels. Mar Environ Res. 2012;81:26–34. doi: 10.1016/j.marenvres.2012.08.004
   PubMed Web of Science ®Google Scholar
• Matthiessen P. Historical perspective on endocrine disruption in wild life. Pure Appl Chem. 2003;75:2197–2206.
   Web of Science ®Google Scholar
• Aarab N, Lemaire-Gony S, Unruh E, Hansen PD, Larsen BK, Andersen OK, Narbonne JF. Preliminary study of responses in mussel (Mytilus edulis) exposed to bisphenol A, diallyl phthalate and tetrabromodiphenyl ether. Aquat Toxicol. 2006;78:86–92. doi: 10.1016/j.aquatox.2006.02.021
   Web of Science ®Google Scholar