AccScience Publishing / EER / Online First / DOI: 10.36922/eer.8078
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REVIEW ARTICLE

Bioaccumulation of trace elements in mussels as sentinels of environmental pollution in the Mediterranean Sea: A review

Daniele Fattorini1,2*
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1 Department of Life and Environmental Sciences (DISVA), Polytechnic University of Marche (UNIVPM), Ancona, Marche, Italy
2 National Inter-University Consortium for Marine Sciences, CoNISMa, Ancona, Marche, Italy
EER, 8078 https://doi.org/10.36922/eer.8078
Submitted: 19 December 2024 | Revised: 6 March 2025 | Accepted: 11 March 2025 | Published: 2 April 2025
© 2025 by the Author(s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
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Abstract

Mussels, as filter feeders, efficiently accumulate various pollutants from the surrounding water, making them valuable bioindicators of marine environmental quality. This review focuses on their application in assessing trace element contamination in the Mediterranean Sea. Trace elements such as arsenic, cadmium, lead, mercury, and zinc are commonly identified in mussels due to their potential toxicity and bioaccumulation. Seasonal variations in trace element concentrations in mussel tissues are influenced by factors such as phytoplankton blooms, gametogenesis, temperature, and salinity. However, anthropogenic activities, including industrial discharges, mining, and urban runoff, can significantly elevate these levels. The Mediterranean Sea is particularly vulnerable to pollution due to its enclosed nature and high human population density. Natural and geological phenomena contribute to the increased bioavailability of certain elements, such as arsenic and mercury, in the Adriatic Sea and the Tyrrhenian Sea. An in-depth understanding of these phenomena is fundamental for interpreting data from scientific studies and environmental monitoring. Regions with historical mining activities, such as the Iberian Peninsula and North Africa, show elevated levels of elements such as lead and zinc. Areas with significant industrial activities, such as the Gulf of Taranto and the Gulf of Trieste (Italy), also exhibit elevated levels of trace elements in mussels. The Eastern Mediterranean, including the Aegean and Marmara Seas, is characterized by widespread pollution from urban and industrial sources, as well as maritime traffic. Mussels from these regions often exhibit high levels of trace elements, particularly in areas near major cities and industrial centers. This review examines literature from the past 25 years concerning the use of mussels as bioindicators in the study of natural and anthropogenic phenomena affecting the bioavailability of trace elements in the Mediterranean Sea, providing an overview of case studies and environmental monitoring commonly carried out in this area.

Keywords
Bioaccumulation
Environmental monitoring
Mediterranean
Mussels
Pollution
Trace elements
Funding
None.
Conflict of interest
Daniele Fattorini is an Editorial Board Member of this journal but was not involved in any way in the editorial and peer-review process conducted for this paper, either directly or indirectly. Separately, the author declares that he has no known competing financial interests or personal relationships that could have influenced the work reported in this paper.
References
  1. Lelieveld J, Berresheim H, Borrmann S, et al. Global air pollution crossroads over the Mediterranean. Science. 2002;298(5594):794-799. doi: 10.1126/science.1075457

 

  1. Danovaro R. Pollution threats in the Mediterranean Sea: An overview. Chem Ecol. 2003;19(1):15-32. doi: 10.1080/0275754031000081467

 

  1. Kanakidou M, Mihalopoulos N, Kindap T, et al. Megacities as hot spots of air pollution in the East Mediterranean. Atmos Environ. 2001;45(6):1223-1235. doi: 10.1016/j.atmosenv.2010.11.048

 

  1. Fattorini D, Notti A, Di Mento R, et al. Seasonal, spatial and inter-annual variations of trace metals in mussels from the Adriatic sea: A regional gradient for arsenic and implications for monitoring the impact of off-shore activities. Chemosphere. 2008;72(10):1524-1533. doi: 10.1016/j.chemosphere.2008.04.071

 

  1. Coll M, Piroddi C, Steenbeek J, et al. The biodiversity of the Mediterranean Sea: Estimates, patterns, and threats. PLoS ONE. 2010;5(8):11842. doi: 10.1371/journal.pone.0011842

 

  1. Burkhard B, Kroll F, Nedkov S, Müller F. Mapping ecosystem service supply, demand and budgets. Ecol Indic. 2012;21:17-29. doi: 10.1016/j.ecolind.2011.06.019

 

  1. Halpern BS, Longo C, Hardy D, et al. An index to assess the health and benefits of the global ocean. Nature. 2012;488(7413):615-620. doi: 10.1038/nature11397

 

  1. Geissen V, Mol H, Klumpp E, et al. Emerging pollutants in the environment: A challenge for water resource management. Int Soil Water Conserv Res. 2015;3(1):57-65. doi: 10.1016/j.iswcr.2015.03.002

 

  1. Piva F, Ciaprini F, Onorati F, et al. Assessing sediment hazard through a weight of evidence approach with bioindicator organisms: A practical model to elaborate data from sediment chemistry, bioavailability, biomarkers and ecotoxicological bioassays. Chemosphere. 2011;83(4):475-485. doi: 10.1016/j.chemosphere.2010.12.064

 

  1. Benedetti M, Ciaprini F, Piva F, et al. A multidisciplinary weight of evidence approach for classifying polluted sediments: Integrating sediment chemistry, bioavailability, biomarkers responses and bioassays. Environ Int. 2012;38(1):17-28. doi: 10.1016/j.envint.2011.08.003

 

  1. Regoli F, Frenzilli G, Bocchetti R, et al. Time-course variations of oxyradical metabolism, DNA integrity and lysosomal stability in mussels, Mytilus galloprovincialis, during a field translocation experiment. Aquat Toxicol. 2004;68(2):167-178. doi: 10.1016/j.aquatox.2004.03.011

 

  1. Avio CG, Gorbi S, Milan M, et al. Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environ Pollut. 2015;198:211-222. doi: 10.1016/j.envpol.2014.12.021

 

  1. Mezzelani M, Fattorini D, Gorbi S, Nigro M, Regoli F. Human pharmaceuticals in marine mussels: Evidence of sneaky environmental hazard along Italian coasts. Mar Environ Res. 2020;162:105137. doi: 10.1016/j.marenvres.2020.105137

 

  1. Regoli F. Trace metals and antioxidant enzymes in gills and digestive gland of the mediterranean mussel Mytilus galloprovincialis. Arch Environ Contam Toxicol. 1998;34(1):48-63. doi: 10.1007/s002449900285

 

  1. Regoli F, Orlando E. Seasonal variation of trace metal concentrations in the digestive gland of the Mediterranean mussel Mytilus galloprovincialis: Comparison between a polluted and a non-polluted site. Arch Environ Contam Toxicol. 1994;27(1):36-43. doi: 10.1007/BF00203885

 

  1. Cossa D, Rondeau JG. Seasonal, geographical and size-induced variability in mercury content of Mytilus edulis in an estuarine environment: a re-assessment of mercury pollution level in the Estuary and Gulf of St. Lawrence. Mar Biol. 1985;88(1):43-9. doi: 10.1007/BF00393042

 

  1. Valette-Silver NJ, Riedel GF, Crecelius EA, Windom H, Smith RG, Dolvin SS. Elevated arsenic concentrations in bivalves from the southeast coasts of the USA. Mar Environ Res. 1999;48(4-5):311-333. doi: 10.1016/S0141-1136(99)00057-4

 

  1. Bodin N, Burgeot T, Stanisière JY, et al. 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. 2004;138(4):411-427. doi: 10.1016/j.cca.2004.04.009

 

  1. Caskie VA, Florou H. Study on the behavior of the heavy metals Cu, Cr, Ni, Zn, Fe, Mn and 137Cs in an estuarine ecosystem using Mytilus galloprovincialis as a bioindicator species: The case of Thermaikos gulf, Greece. J Environ Radioact. 2006;86(1):31-44. doi: 10.1016/j.jenvrad.2005.07.005

 

  1. Sunlu U. Trace metal levels in mussels (Mytilus galloprovincialis L. 1758) from Turkish Aegean sea coast. Environ Monit Assess. 2006;114(1-3):273-286. doi: 10.1007/s10661-006-4780-4

 

  1. Türk Çulha S, Koçbaş F, Gündocdu A, Baki B, Çulha M, Topçuoclu S. The seasonal distribution of heavy metals in Mussel sample from Yalova in the Marmara Sea, 2008-2009. Environ Monit Assess 2011;183(1-4):525-529. doi: 10.1007/s10661-011-1937-6

 

  1. Kristan U, Kanduč T, Osterc A, Šlejkovec Z, Ramšak A, Stibilj V. Assessment of pollution level using Mytilus galloprovincialis as a bioindicator species: The case of the Gulf of Trieste. Mar Pollut Bull. 2014;89(1-2):455-463. doi: 10.1016/j.marpolbul.2014.09.046

 

  1. Bajc Z, Kirbiš A. Trace element concentrations in mussels (Mytilus galloprovincialis) from the gulf of Trieste, Slovenia. J Food Protec. 2019;82(3):429-434. doi: 10.4315/0362-028X.JFP-18-378

 

  1. Azizi G, Layachi M, Akodad M, Baghour M, et al. The Accumulation of Al, As, Li, Mg, Mn, S, Si, Ti, and V in the Mussel Mytilus galloprovincialis from the Moroccan Mediterranean Coastal Areas: Trends pertaining to seasons and levels. Ocean Sci J. 2020;55(3):405-418. doi: 10.1007/s12601-020-0025-7

 

  1. Esposito G, Mudadu AG, Abete MC, et al. Seasonal accumulation of trace elements in native Mediterranean mussels (Mytilus galloprovincialis Lamarck, 1819) collected in the Calich Lagoon (Sardinia, Italy). Environ Sci Pollut Res. 2021;28(20):25770-25781. doi: 10.1007/s11356-021-12380-4

 

  1. Peycheva K, Panayotova V, Stancheva R, et al. Seasonal variations in the trace elements and mineral profiles of the bivalve species, Mytilus galloprovincialis, Chamelea gallina and Donax trunculus, and human health risk assessment. Toxics. 2023;11(4):319. doi: 10.3390/toxics11040319

 

  1. Dogruyol H, Mol S, Ulusoy Ş, Atanasoff A. Evaluation of health risks attributed to toxic trace elements and selenium in farmed Mediterranean Mussels from Türkiye and Bulgaria. Biol Trace Element Res. 2024;202(11):5177-5189. doi: 10.1007/s12011-024-04084-w

 

  1. Žurga P, Dubrović I, Kapetanović D, et al. Performance of mussel Mytilus galloprovincialis under variable environmental conditions and anthropogenic pressure: A survey of two distinct farming sites in the Adriatic Sea. Chemosphere. 2024;364:143156. doi: 10.1016/j.chemosphere.2024.143156

 

  1. Kanduč T, Šlejkovec Z, Falnoga I, et al. Environmental status of the NE Adriatic Sea, Istria, Croatia: insights from mussel Mytilus galloprovincialis condition indices, stable isotopes and metal (loid)s. Marine Poll Bull. 2018;126:525-534. doi: 10.1016/j.marpolbul.2017.09.052

 

  1. Francesconi KA, Gailer J, Edmonds JS, Goessler W, Irgolic KJ. Uptake of arsenic-betaines by the mussel Mytilus edulis. Comp Biochem Physiol C. 1999;122(1):131-137. doi: 10.1016/S0742-8413(98)10095-6

 

  1. Clowes LA, Francesconi KA. Uptake and elimination of arsenobetaine by the mussel Mytilus edulis is related to salinity. Comp Biochem Physiol C. 2004;137(1):35-42. doi: 10.1016/j.cca.2003.11.003

 

  1. Fattorini D, Notti A, Regoli F. Characterization of arsenic content in marine organisms from temperate, tropical, and polar environments. Chem Ecol. 2006;22(5):405-414. doi: 10.1080/02757540600917328

 

  1. Larsen EH, Francesconi KA. Arsenic concentrations correlate with salinity for fish taken from the North sea and Baltic waters. J Mar Biol Ass UK. 2003;83:283-284.

 

  1. Bernhard M. Heavy metals and chlorinated hydrocarbons in the Mediterranean. Ocean Management. 1978;3(3-4):253-313. doi: 10.1016/0302-184X(78)90008-2

 

  1. Barghigiani C, Bargagli R, Siegel BZ, Siegel SM. A comparative study of mercury distribution on the aeolian volcanoes, Vulcano and Stromboli. Water Air Soil Pollut. 1990;53(1-2):179-188. doi: 10.1007/BF00155002

 

  1. Ferrara R. The biogeochemical cycle of mercury in the Mediterranean: Part II: Mercury in the atmosphere, aerosol and in rainwater of a Northern Tyrrhenian area. Environ Technol Lett. 1082;3(1-11):449-456. doi: 10.1080/09593338209384149

 

  1. Ferrara R, Mazzolai B, Edner H, Svanberg S, Wallinder E. Atmospheric mercury sources in the Mt. Amiata area, Italy. Sci Total Environ. 1998;213(1-3):13-23. doi: 10.1016/S0048-9697(98)00067-9

 

  1. Fornasaro S, Morelli G, Costagliola P, Rimondi V, Lattanzi P, Fagotti C. Total mercury mass load from the Paglia-Tiber River System: The contribution to Mediterranean Sea Hg Budget. Toxics. 2022;10(7):395. doi: 10.3390/toxics10070395

 

  1. Morel FMM, Kraepiel AML, Amyot M. The chemical cycle and bioaccumulation of mercury. Annual Rev Ecol Syst. 1998;29:543-566. doi: 10.1146/annurev.ecolsys.29.1.543

 

  1. Dron J, Wafo E, Chaspoul F, et al. Long-term trends (2002- 2016) reveal an increase of mercury levels along with the decline of several metal elements in striped dolphins (Stenella coeruleoalba) stranded in the North-West Mediterranean. Sci Total Environ. 2024;957:177741. doi: 10.1016/j.scitotenv.2024.177741

 

  1. Francesconi KA, Lenanton RCJ, Caputi N, Stewart J. Long-term study of mercury concentrations in fish following cessation of a mercury-containing discharge. Mar Environ Res. 1997;43(1-2):27-40. doi: 10.1016/0141-1136(95)00028-3

 

  1. Sager DR. Long-term variation in mercury concentrations in estuarine organisms with changes in releases into Lavaca Bay, Texas. Mar Pollut Bulletin. 2002;44(8):807-815. doi: 10.1016/s0025-326x(02)00064-4

 

  1. Ausili A, Gabellini M, Cammarata G, et al. Ecotoxicological and human health risk in a petrochemical district of southern Italy. Mar Environ Res. 2008;66(1):215-217. doi: 10.1016/j.marenvres.2008.02.062

 

  1. Bruno DE, D’Amore F, Simone FD, et al. Mercury bioindicators across the Mediterranean basin: Evidence from a dataset on Mytilus galloprovincialis. In: 2021 IEEE International Workshop on Metrology for the Sea: Learning to Measure Sea Health Parameters, MetroSea 2021 - Proceedings; 2021. p. 209-214. doi: 10.1109/MetroSea52177.2021.9611602

 

  1. Kljaković-Gašpić Z, Odžak N, Ujević I, Zvonarić T, Horvat M, Barić A. Biomonitoring of mercury in polluted coastal area using transplanted mussels. Sci Total Environ. 2006;368(1):199-209. doi: 10.1016/j.scitotenv.2005.09.080

 

  1. Kayhan FE. Mercury (Hg) Levels in the Mediterranean Mussel (Mytilus galloprovincialis) on Bosphorus, Istanbul, Turkey. J Biol Sci. 2007;7(2):369-373. doi: 10.3923/jbs.2007.369.373

 

  1. Benzaoui MY, Bentaallah MEA, Ben Naoum BE, Kerfouf A, Boutiba Z. Heavy metals (Hg, Cd, Pb) concentrations in Mytilus galloprovincialis (Lamarck, 1819) in Oran coastal waters (Western Algeria): new evidences. J Appl Environ Biol Sci. 2015;5:1-9.

 

  1. Odžak N, Zvonarić T, Kljaković Gašpić Z, Horvat M, Barić A. Biomonitoring of mercury in the Kastela Bay using transplanted mussels. Sci Total Environ. 2000;261(1-3):61-68. doi: 10.1016/S0048-9697(00)00595-7

 

  1. Clarkson TW, Magos L. The toxicology of mercury and its chemical compounds. Crit Rev Toxicol. 2006;36 (8):609-662. doi: 10.1080/10408440600845619

 

  1. Benedetti M, Romano E, Ausili A, et al. 10-year time course of Hg and organic compounds in Augusta Bay: Bioavailability and biological effects in marine organisms. Front Public Health. 2022;10-968296. doi: 10.3389/fpubh.2022.968296

 

  1. Martinez-Frias J. Mine waste pollutes Mediterranean. Nature. 1997;388:120. doi: 10.1038/40506

 

  1. Mestre NC, Rocha TL, Canals M, et al. Environmental hazard assessment of a marine mine tailings deposit site and potential implications for deep-sea mining. Environ Pollut. 2017;228:169-178. doi: 10.1016/j.envpol.2017.05.027

 

  1. Santos-Echeandía J, Campillo JA, Egea JA, et al. The influence of natural vs anthropogenic factors on trace metal (loid) levels in the Mussel Watch programme: Two decades of monitoring in the Spanish Mediterranean sea. Mar Environ Res. 2021;169:105382. doi: 10.1016/j.marenvres.2021.105382

 

  1. Mehouel F, Fowler SW. Review of the toxic trace elements arsenic, cadmium, lead and mercury in seafood species from Algeria and contiguous waters in the Southwestern Mediterranean Sea. Environ Sci Pollut Res. 2022;29:3288-3301. doi: 10.1007/s11356-021-17130-0

 

  1. Cardellicchio N, Buccolieri A, Di Leo A, Giandomenico S, Spada L. Levels of metals in reared mussels from Taranto Gulf (Ionian Sea, Southern Italy). Food Chem. 2008;107(2):890-896. doi: 10.1016/j.foodchem.2007.09.011

 

  1. Kucuksezgin F, Pazi I, Yucel-Gier G, Akcali B, Galgani F. Monitoring of heavy metal and organic compound levels along the Eastern Aegean coast with transplanted mussels. Chemosphere. 2013;93(8):1511-1518. doi: 10.1016/j.chemosphere.2013.07.058

 

  1. Pazi I, Kucuksezgin F, Gonul LT, Guclusoy H, Akcali B. Metal levels in sediments and caged mussels in one of the industrial zones of the Eastern Aegean Sea. Environ Sci Pollut Res. 2023;30:121161-121174. doi: 10.1007/s11356-023-30802-3

 

  1. Kayhan FE, Gulsoy N, Balkis N, Yuce R. Cadmium (Cd) and Lead (Pb) Levels of Mediterranean Mussel (Mytilus galloprovincialis Lamarck, 1819) From Bosphorus, Istanbul, Turkey. Pakistan J Biol Sci. 2007;10(6):915-919. doi: 10.3923/pjbs.2007.915.919

 

  1. Kozanoglou C, Catsiki VA. Impact of products of a ferronickel smelting plant to the marine benthic life. Chemosphere. 1997;34(12):2673-2682. doi: 10.1016/S0045-6535(97)00093-3

 

  1. Tsangaris C, Papathanasiou E, Cotou E. Assessment of the impact of heavy metal pollution from a ferro-nickel smelting plant using biomarkers. Ecotox Environ Safety. 2007;66(2):232-243. doi: 10.1016/j.ecoenv.2006.03.011

 

  1. Strogyloudi E, Angelidis MO, Christides A, Papathanassiou E. Metal concentrations and metallothionein levels in Mytilus galloprovincialis from Elefsis bay (Saronikos gulf, Greece). Environ Monit Assess. 2012;184:7189-7205. doi: 10.1007/s10661-011-2490-z
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