Scientia Marina, Vol 80, No 1 (2016)

High metal contents in the fan mussel Pinna nobilis in the Balearic Archipelago (western Mediterranean Sea) and a review of concentrations in marine bivalves (Pinnidae)


https://doi.org/10.3989/scimar.04255.24B

Maite Vázquez-Luis
Instituto Español de Oceanografía (IEO), Centro Oceanográfico de Baleares, Spain

Mercè Morató
Instituto Español de Oceanografía (IEO), Centro Oceanográfico de Baleares, Spain

Juan Antonio Campillo
Instituto Español de Oceanografía (IEO), Centro Oceanográfico de Murcia, Spain

Carlos Guitart
Instituto Español de Oceanografía (IEO), Centro Oceanográfico de Murcia, Spain

Salud Deudero
Instituto Español de Oceanografía (IEO), Centro Oceanográfico de Baleares, Spain

Abstract


Concentrations of metals (Cd, Cu, Hg, Pb and Zn) in the marine bivalve Pinna nobilis at several coastal locations of Majorca and the Cabrera Islands (Mediterranean Sea) were investigated. The elevated concentrations of metals found in the soft tissues of P. nobilis indicate high bioaccumulation factors. All concentrations and the calculated metal pollution index showed significant differences between sites, with particularly high concentrations in the Cabrera Archipelago, a marine protected area (MPA). The datasets were evaluated with the limited information published in the literature for Pinnidae species worldwide. In benthic P. nobilis, concentrations of Cd, Cu and Zn are more than 30 times higher and Hg and Pb concentrations are 4 and 7 times higher, respectively, than concentrations in other bivalve species, such as Mytilus galloprovincialis (Mytilidae). These observations from species inhabiting nearby ecological habitats of the coastal environment (Pinnidae vs. Mytilidae) are also discussed in the context of current marine monitoring strategies and assessments.

Keywords


trace metal; bivalve; mollusc; bioaccumulation; Pinnidae, Mytilidae

Full Text:


PDF HTML XML

References


Alomar C., Vázquez-Luis M., Magraner K., et al. 2015. Evaluating stable isotopic signals in bivalve Pinna nobilis under different human pressures. J. Exp. Mar. Biol. Ecol. 467: 77-86. http://dx.doi.org/10.1016/j.jembe.2015.03.006

Amiard J.C., Amiard-Triquet C., Barka S., et al. 2006. Metallothioneins in aquatic invertebrates: Their role in metal detoxification and their use as biomarkers. Aquat. Toxicol. 76: 160-202. http://dx.doi.org/10.1016/j.aquatox.2005.08.015 PMid:16289342

Andral B., Stanisiere J.Y., Sauzade D., et al. 2004. Monitoring chemical contamination levels in the Mediterranean based on the use of mussel caging. Mar. Poll. Bull. 49: 704-712. http://dx.doi.org/10.1016/j.marpolbul.2004.05.008 PMid:15530513

Benedicto J., Andral B., Martinez-Gomez C., et al. 2011. A large scale survey of trace metal levels in coastal waters of the Western Mediterranean basin using caged mussels (Mytilus galloprovincialis). J. Env. Mon. 13: 1495-1505. http://dx.doi.org/10.1039/c0em00725k PMid:21384032

Besada V., Sericano J.L., Schultze F. 2014. An assessment of two decades of trace metals monitoring in wild mussels from the Northwest Atlantic and Cantabrian coastal areas of Spain, 1991- 2011. Env. Int. 71: 1-12. http://dx.doi.org/10.1016/j.envint.2014.05.024 PMid:24946271

Boening D.W. 1999. An evaluation of bivalves as biomonitors of heavy metals pollution in marine waters. Env. Mon. Assess. 55: 459-470. http://dx.doi.org/10.1023/A:1005995217901

Cabanellas-Reboredo M., Blanco A., Deudero S., et al. 2010. Effects of the invasive macroalga Lophocladia lallemandii on the diet and trophism of Pinna nobilis (Mollusca: Bivalvia) and its guests Pontonia pinnophylax and Nepinnotheres pinnotheres (Crustacea: Decapoda). Sci. Mar. 74(1): 102-110. http://dx.doi.org/10.3989/scimar.2010.74n1101

Catsiki V.A., Katsilieri C. 1992. Presence of chromium in P. nobilis collected from a polluted area. Fres. Envir. Bull. 1: 644-649.

Catsiki V.A. Katsilieri C., Gialamas V. 1994. Chromium distribution in benthic species from a gulf receiving tannery wastes (Gulf of Geras-Lesbos island, Greece). National Centre for Marine Research. A. Kosmas. Hellinikon. Athens 166 04. Greece. Sci. Total Env. 145: 173-185. http://dx.doi.org/10.1016/0048-9697(94)90308-5

Clark R.B. 2001. Marine Pollution. Fifth Ed. Oxford University Press, New York.

Corbin T., Wade S. 2004. Heavy metal concentrations in razorfish (Pinna bicolor) and sediments across northern Spencer Gulf. Environment Protection Authority Adelaide, South Australia.

Daby D. 2006. Coastal Pollution and Potential Biomonitors of Metals in Mauritius. Water, Air Soil Poll. 174(1-4): 63-91. http://dx.doi.org/10.1007/s11270-005-9035-4

Davenport J., Ezgeta-Balic D., Peharda M., et al. 2011. Size-differential feeding in Pinna nobilis L. (Mollusca: Bivalvia): exploitation of detritus, phytoplankton and zooplankton. Estuar. Coast. Shelf Sci. 92: 246-254. http://dx.doi.org/10.1016/j.ecss.2010.12.033

de Mora S., Fowler S.W., Wyse E., et al. 2004. Distribution of heavy metals in marine bivalves, fish and coastal sediments in the Gulf and Gulf of Oman. Mar. Poll. Bull. 49 (5-6): 410-424. http://dx.doi.org/10.1016/j.marpolbul.2004.02.029 PMid:15325209

Deudero S., Box A., March D., et al. 2007. Temporal trends of metals in benthic invertebrate species from the Balearic Islands, Western Mediterranean. Mar. Poll. Bull. 54: 1523-1558. http://dx.doi.org/10.1016/j.marpolbul.2007.05.012 PMid:17618653

Deudero S., Box A., Tejada S., et al. 2009. Stable isotopes and metal contamination in caged marine mussel Mytilus galloprovincialis. Mar. Poll. Bull. 58: 1025-1031. http://dx.doi.org/10.1016/j.marpolbul.2009.02.011 PMid:19303611

Du Y., Lian F., Zhu L. 2011. Biosorption of divalent Pb, Cd, and Zn on aragonite and calcite mollusk shells. Env. Poll. 159: 1763-1768. http://dx.doi.org/10.1016/j.envpol.2011.04.017 PMid:21550150

EU Habitats Directive. 2007. Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Annex IV: animal and plant species of community interest in need of strict protection. http://ec.europa.eu/environment/nature/legislation/ habitatsdirective/index_en.htm

EU MSFD. 2008. Council Directive 2008/56/EC establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive).

FAO. 1992. The state of world fisheries and aquaculture. Food and Agriculture Organization of the United Nations, Electronic publishing policy and support branch. FAO Fisheries and Aquaculture Department 69, 185.

García-Hernández J., García-Rico L., Jara-Marini M.E., et al. 2005. Concentrations of heavy metals in sediment and organisms during a harmful algal Bloom (HAB) at Kun Kaak Bay. Sonora. Mexico. Mar. Poll. Bull. 50: 733-739. http://dx.doi.org/10.1016/j.marpolbul.2005.02.027 PMid:15993140

García-March J.R. 2003. Contribution to the knowledge of the status os Pinna nobilis (L.) 1758 in Spanish coasts. Mem. Inst. Oceanogr. Paul Ricard 9: 29-41.

Goldberg E.D. 1975. The mussel watch – A first step in global marine monitoring. Mar. Poll. Bull. 6: 111. http://dx.doi.org/10.1016/0025-326X(75)90271-4

Goldberg E.D., Bertine K.K. 2000. Beyond Mussel Match – New directions for monitoring marine pollution. Sci. Total Env. 247: 165-174. http://dx.doi.org/10.1016/S0048-9697(99)00488-X

Jebali J., Chouba L., Banni M., et al. 2014. Comparative study of the bioaccumulation and elimination of trace metals (Cd, Pb, Zn, Mn and Fe) in the digestive gland, gills and muscle of bivalve Pinna nobilis during a field transplant experiment. J. Trace El. Med. Biol. 28(2): 212-217. http://dx.doi.org/10.1016/j.jtemb.2013.12.001 PMid:24439521

Jung H.-S., Yun S.-T., Choi B.-Y., et al. 2010. Geochemical studies on the contamination and dispersion of trace metals in intertidal sediments around a military air weapons shooting range. J. Soil. Sedim. 10: 1142-1158. http://dx.doi.org/10.1007/s11368-010-0248-9

Kennedy H., Richardson C.A., Duarte C.M., et al. 2001. Diet and association of Pontonia pinnophylax occurring in Pinna nobilis: insights from stable isotope analysis. J. Mar. Biol. Assoc. U.K. 81(1): 177-178. http://dx.doi.org/10.1017/S0025315401003575

Khristoforova N.K., Kavun V.Ya., Latypov Yu.Ya., et al. 2007. Heavy metals in mass species of bivalves in Ha Long Bay (South China sea, Vietnam). Oceanology 47(5): 685-690. http://dx.doi.org/10.1134/S0001437007050116

Lafabrie C., Pergent-Martini C., Pergent C. 2008. Metal contamination of Posidonia oceanica meadows along the Corsican coastline (Mediterranean). Env. Poll. 151(1): 262-268. http://dx.doi.org/10.1016/j.envpol.2007.01.047 PMid:17428593

Lemer S., Buge B., Bemis A., et al. 2014. First molecular phylogeny of the circumtropical bivalve family Pinnidae (Mollusca, Bivalvia): Evidence for high levels of cryptic species diversity. Mol. Phylog. Evol. 75: 11-23. http://dx.doi.org/10.1016/j.ympev.2014.02.008 PMid:24569016

Maher W.A. 1985. Trace metal concentrations in marine organisms from St. Vicent Gulf, South Australia. Water Air Soil Poll. 29 (1): 77-84. http://dx.doi.org/10.1007/BF00149330

Mathew S., Paterson J., Gauleja B., et al. 1996. Manganese and "Pinnaglobin" in Pinna nobilis. Comp. Biochem. Physiol. 113B (3): 525-532. http://dx.doi.org/10.1016/0305-0491(95)02077-2

Najdek M., Bla?ina M., Ezgeta-Bali? D., et al. 2013. Diets of fan shells (Pinna nobilis) of different sizes: fatty acid profiling of digestive gland and adductor muscle. Mar. Biol. 160(4): 921-930. http://dx.doi.org/10.1007/s00227-012-2144-x

Neira P., Cobelo-García A., Besada V., et al. 2015. Evidence of increased anthropogenic emissions of platinum: Time-series analysis of mussels (1991-2011) of an urban beach. Sci. Total Environ. 514: 366-370. http://dx.doi.org/10.1016/j.scitotenv.2015.02.016 PMid:25679817

O'Connor T.P., Beliaeff B. 1995. Recent trends in coastal environmental quality: results from the Mussel Watch Project. Silver Spring M.N. Ed.

O'Connor T.P., Launstein G.G. 2006. Trends in chemical concentrations in mussels and oysters collected along the US coast: update to 2003. Mar. Env. Res. 62: 261-285. http://dx.doi.org/10.1016/j.marenvres.2006.04.067 PMid:16777213

Pavicic J., Smodis B., Skreblin M., et al. 1994. Embryo-larval tolerance of Mytilus galloprovincialis, exposed to elevated seawater metal concentrations. II. Stage-specific fluctuations in sensitivity toward Zn and Cd and their bioaccumulation into veliger larvae. Comp. Biochem. Physiol. C 109(1): 37-46.

Rabaoui L., Balti R., El Zrelli R., et al. 2014. Assessment of heavy metal pollution in the gulf of Gabes (Tunisia) using four mollusc species. Medit. Mar. Sci. 15(1): 45-58.

Reid R.G.B., Brand D.G. 1989. Giant kidneys and metal-sequestering nephroliths in the bivalve Pinna bicolor, with comparative notes on Atrina vexillum (Pinnidae). J. Exp. Mar. Biol. Ecol. 126: 95-117. http://dx.doi.org/10.1016/0022-0981(89)90083-X

Ross K., Cooper N., Bidwell J.R., et al. 2002. Genetic diversity and metal tolerance of two marine species: a comparison between populations from contaminated and reference sites. Mar. Pollut. Bull. 44: 671-679. http://dx.doi.org/10.1016/S0025-326X(01)00333-2

Santos-Echeandia, J., Laglera, L.M., Prego, R., et al. 2008. Copper speciation in continental inputs to the Vigo Ria: Sewage discharges versus river fluxes. Mar. Poll. Bull. 56(2): 308-317. http://dx.doi.org/10.1016/j.marpolbul.2007.10.021

Schultz P.W., Huber M. 2013. Revision of the worldwide Recent Pinnidae and some remarks on fossil European Pinnidae. Acta Conch. 13: 1-164.

Serafim A, Bebianno M.J. 2009. Metallothionein role in the kinetic model of copper accumulation and elimination in the clam Ruditapes decussatus. Environ. Res. 109: 390-399. http://dx.doi.org/10.1016/j.envres.2009.03.001 PMid:19345346

Soazig L., Marc L. 2003. Potential use of the levels of the mRNA of a specific metallothionein isoform (MT-20) in mussel (Mytilus edulis) as a biomarker of cadmium contamination. Mar. Poll. Bull. 46: 1450-1455. http://dx.doi.org/10.1016/S0025-326X(03)00283-2

Solis-Weiss V., Aleffi F., Bettoso N., et al. 2004. Effects of industrial and urban pollution on the benthic macrofauna in the Bay of Muggia (industrial port of Trieste, Italy). Sci. Total Env. 328: 247-263. http://dx.doi.org/10.1016/j.scitotenv.2004.01.027 PMid:15207588

SPA/BD Protocol. 1995. Annex II of SPA and Biodiversity Protocol. Barcelona Convention Protocol concerning Specially Protected Areas and Biological Diversity in the Mediterranean. http://rac-spa.org/sites/default/files/annex/annex_2_en_2013. pdf

Stuhlbacher A., Bradley M.C., Naylor C., et al. 1992. Induction of cadmium tolerance in two clones of Daphnia magna Straus. Comp. Biochem. Physiol. C 101(3): 571-577. http://dx.doi.org/10.1016/0742-8413(92)90088-O

Sureda A., Box A., Tejada S., et al. 2011. Biochemical responses of Mytilus galloprovincialis as biomarkers of acute environmental pollution caused by the Don Pedro oil spill (Ibiza Island, Spain). Aquat. Toxic. 101: 540-549. http://dx.doi.org/10.1016/j.aquatox.2010.12.011 PMid:21276480

Sureda A., Tejada S., Box A., et al. 2013. Polycyclic aromatic hydrocarbon levels and measures of oxidative stress in the Mediterranean endemic bivalve Pinna nobilis exposed to the Don Pedro oil spill. Mar. Poll. Bull. 71(1-2): 69-73. http://dx.doi.org/10.1016/j.marpolbul.2013.03.033 PMid:23623655

Trigos S., García-March J.R., Vicente N., et al. 2014. Utilization of muddy detritus as organic matter source by the fan mussel Pinna nobilis. Medit. Mar. Sci. 15(3): 667-674.

Usero J., Morillo J., Gracia I. 2005. Heavy metal concentrations in molluscs from the Atlantic coast of southern Spain. Chemosphere 59: 1175-1181. http://dx.doi.org/10.1016/j.chemosphere.2004.11.089 PMid:15833492

Van der Oost R., Beyer J., Vermeulen N.P.E. 2003. Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Env. Toxic. Pharmac. 13: 57-149. http://dx.doi.org/10.1016/S1382-6689(02)00126-6

Vázquez-Luis M., March D., Álvarez E., et al. 2014. Spatial distribution modelling of the endangered bivalve Pinna nobilis in a Marine Protected Area. Medit. Mar. Sci. 15(3): 626-634.

Wei B., Yang L. 2010. A review of heavy metal contaminations in urban soils, urban road dusts and agricultural soils from China. Microch. J. 94(2): 99-170. http://dx.doi.org/10.1016/j.microc.2009.09.014

World Health Organization (WHO). 1989. Heavy metals environmental aspects. Environment Health Criteria, Nº 85. Geneva, Switzerland.

WoRMS, World Register of Marine Species. 2014. Available from http://www.marinespecies.org at VLIZ. Accessed 2014-10-20

Zavodnik D., Hrs-Brenko M., Legac M. 1991. Synopsis on the fan shell Pinna nobilis L. in the eastern Adriatic Sea. In: Boudouresque C.F., Avon M., Gravez V., (eds) Les Espèces Marines à Protéger en Méditerranée. Gis Posidonie publ. Marseille pp. 169-178.

zu Ermgassen P.S.E., Spalding M.D., Grizzle R.E., et al. 2013. Quantifying the Loss of a Marine Ecosystem Service: Filtration by the Eastern Oyster in US Estuaries. Estuar. Coast. 36: 36-43. http://dx.doi.org/10.1007/s12237-012-9559-y




Copyright (c) 2016 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.


Contact us scimar@icm.csic.es

Technical support soporte.tecnico.revistas@csic.es