Trace elements and oxidative stress in the Ark shell Arca noae from a Mediterranean coastal lagoon (Bizerte lagoon, Tunisia): are there health risks associated with their consumption?
Arca noae; Southern Mediterranean Sea; Trace elements; Contamination; Redox status; Human health
Abstract :
[en] The current study examined the concentrations of ten trace elements (TE) (nickel, chromium, cadmium, iron, zinc, manganese, aluminum, copper, selenium and lead) in the edible tissue of the Ark shell Arca noae (L. 1758) from a Mediterranean coastal lagoon, the Bizerte lagoon during 2013–2014. The analysis of several redox status biomarkers, metallothioneins (MTs), malondialdehyde (MDA), glutathione peroxidase (GPx), reduced glutathione (GSH) and acetylcholinesterase (AChE), was monitored as a response to TE bioaccumulation and environmental parameters variability. Significant differences (p < 0.05) were observed between mean seasonal TE concentrations in A. noae soft tissue. The highest TE concentrations in A. noae soft tissues were recorded during summer, which coincided with the increase of body dry weight (BDW) and the gonad index (GI). During this season, biomarker responses were enhanced, revealing significant increases of MTs, MDA and GSH levels as well as GPx activity in A. noae tissues, while a decrease of AChE activity was observed. The levels of TE analyzed in A. noae and several parameters used to assess the potential human risk (estimated weekly intake, target hazard quotient and target hazard risk) were lower than the permissible limits for safe seafood consumption. Consequently, this shellfish can be considered safe for human consumption. This preliminary study presents prospects for the valorization of this seafood product in Tunisia’s food sector. It also gives basal information for future environmental assessment studies in which A. noae could be used as early warning tools in the field of biomonitoring programs and confirms the usefulness of biomarkers to monitor the health status of aquatic organisms.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Richir, Jonathan ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (COU)
Bejaoui, Safa
Boussoufa, Dhouha
Marengo, Michel ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
El Cafsi, M'hamed
Gobert, Sylvie ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Language :
English
Title :
Trace elements and oxidative stress in the Ark shell Arca noae from a Mediterranean coastal lagoon (Bizerte lagoon, Tunisia): are there health risks associated with their consumption?
Adamo P, Arienzo M, Imperato M, Naimo D, Nardi G, Stanziones D (2005) Distribution and partition of heavy metals in surface and sub-surface sediments of Naples city port. Chemosphere 61:800–809
Ali M, Abdel-Satar A (2005) Studies of some heavy metals in water, sediment, fish and fish diets in some fish farms in El-Fayoum province. Egypt J Aquat Res 31:261–273
Ali Z, Malik RN, Qadir A (2013) Heavy metals distribution and risk assessment in soils affected by tannery effluents. Chem Ecol 29:676–692. 10.1080/02757540.2013.810728
Amiard JC, Pineau A, Boiteau HL, Metayer C, Amiard-Triquet C (1987) Application de la spectrométrie d'absorption atomique Zeeman aux dosages de huit éléments traces (Ag, Cd, Cr, Cu, Mn, Ni, Pb et Se) dans des matrices biologiques solides. Water Res 21:693–697. 10.1016/0043-1354(87)90081-9
Amiard JC, Berthet B (1996) Fluctuations of cadmium, copper, lead and zinc concentrations in field populations of the Pacific oyster Crassostrea gigas in the bay of Bourgneuf (France). Ann Inst Oceanogr 72:195–207
Aminot A, Chaussepied C (1983) Manuel des Analyses Chimiques en Milieu Marin. Centre National d’Exploitation des Océans, Brest
Barhoumi B, Le Menach K, Clérandeau C, Ameur WB, Budzinski H, Driss MR, Cachot J (2014) Assessment of pollution in the Bizerte lagoon (Tunisia) by the combined use of chemical and biochemical markers in mussels, Mytilus galloprovincialis. Mar Pollut Bull 84:379–390. 10.1016/j.marpolbul.2014.05.002
Barhoumi B (2014) Biosurveillance de la pollution de la lagune de Bizerte (Tunisie) par l'analyse comparée des niveaux de contamination et de l'écotoxicité des sédiments et du biote. Université de Bordeaux, Thèse de doctorat, 245p
Basraoui Y, Zegmout M, Eladdouli J, Demnati S, Chahlaoui A (2010) Contribution à l'étude de la pollution de la zone côtière Saidia/Moulouya (Maroc Nord Oriental). Afrique Sci 6:64–74 http://www.afriquescience.info/document.php?id=2044
Béjaoui B, Harzallah A, Moussa M, Chapelle A (2008) Modèle couplé dynamique-écologie pour la lagune de Bizerte. BullInst Nat Sci Tech Mer Salammbô 35:31–148
Béjaoui B, Solidoro C, Harzallah A, Chevalier C, Chapelle A, Zaaboub N, Aleya L (2017) 3D modeling of phytoplankton seasonal variation and nutrient budget in a southern Mediterranean lagoon. Mar Pollut Bull 114:962–976. 10.1016/j.marpolbul.2016.11.001
Bejaoui S, Boussoufa D, Tir M, Haouas-Gharsallah I, Boudawara T, Ghram A, El Cafsi M, Soudani N (2017) DNA damage and oxidative stress in digestive gland of Venerupis decussata collected from two contrasting habitats in the southern Tunisian coast: biochemical and histopathological studies. Cah Biol Mar 58:123–135. 10.21411/CBM.A.133C71C1
Bejaoui S, Telahigue K, Chetoui I, Rabeh I, Fouzai C, Trabelsi W, Houas-Gharsallah I, El Cafsi M, Soudani N (2018) Integrated effect of metal accumulation, oxidative stress responses and DNA damage in Venerupis decussata gills collected from two coast Tunisian lagoons. J Chem Environm biol Eng 2:44–51. 10.11648/j.jcebe.20180202.12
Ben Garali A, Ouakad M, Gueddari M (2009) Bilans hydrologiques de la lagune de Bizerte nord-est de la Tunisie. J Water Sci 22:525–534. 10.7202/038329ar
Blust R, Ginneken LV, Decleir W (1994) Effect of temperature on the uptake of copper by the brine shrimp, Artemia fransiscana. Aquat Toxicol 30:343–356. 10.1016/0166-445X(94)00049-2
Bordin G, McCourt J, Rodriguez A (1992) Trace metals in the marine bivalve Macoma balthica in the Westerschelde estuary, the Netherland. Part 1: analysis of total copper, cadmium, zinc and iron- locational and seasonal variations. Sci Total Environ 127:225–280. 10.1016/0048-9697(92)90507-O
Bocchetti R, Regoli F (2006) Seasonal variability of oxidative biomarkers, lysosomal parameters, metallothioneins and peroxisomal enzymes in the Mediterranean mussel Mytilus galloprovincialis from Adriatic Sea. Chemosphere 65:913–921. 10.1016/j.chemosphere.2006.03.049
Bocquené G, Roig A, Fournier D (1997) Cholinesterases from the common oyster (Crassostrea gigas) evidence for the presence of a soluble acetylcholmesterase insensitive to organophosphate and carbamate inhibitors. FEBS Lett 407:261–266
Bouki E, Dimitriadis VK, Kaloyianni M, Dailianis S (2013) Antioxidant and pro-oxidant challenge of tannic acid in mussel hemocytes exposed to cadmium. Mar Environ Res 85:13–20. 10.1016/j.marenvres.2012.12.005
Boussoufa D, Ghazali N, Masmoudi W, El Cafsi M (2014) Biomonitoring of trace metal pollution using the mollusc bivalve Donax Trunculus and the surface sediment from the Mediterranean coast of northern Tunisia. Int J Engin Sci Res Tech 3:355–375
Brik B, Aydi A, Riahi C, Sdiri A, Regaya K (2018) Contamination levels and vertical distribution of trace metals with application of geochemical indices in the sediment cores of the Bizerte Lagoon-Ichkeul lake complex in northeastern Tunisia. Arab J Geosci 11:23–15. 10.1007/s12517-017-3382-5
Byrne RH, Kump LR, Cantrell KJ (1988) The influence of temperature and pH on trace metal speciation in seawater. Mar Chem 25:168–181. 10.1016/0304-4203(88)90062-X
Carregosa V, Velez C, Soares AM, Figueira E, Freitas R (2014) Physiological and biochemical responses of three Veneridae clams exposed to salinity changes. Comp Biochem Physiol B Biochem Mol Biol 178:1–9. 10.1016/j.cbpb.2014.08.001
Chamannejadian A, Sayyad G, Moezzi A, Jahangiri A (2013) Evaluation of estimated daily intake (EDI) of cadmium and lead for rice (Oryza sativa L.) in calcareous soils. Iran J environ health Sci Eng 10:1. 10.1186/1735-2746-10-28
Chandurvelan R, Marsden I, Glover C, Gaw S (2015) Assessment of a mussel as a metal bioindicator of coastal contamination: relationships between metal bioaccumulation and multiple biomarker responses. Sci Total Environ 511:663–675. 10.1016/j.scitotenv.2014.12.064
Cheggour M, Chafik A, Texier H, Bouhallaoui A, Gharbi N, Boumezzough A, Elattar J (1999) Bioaccumulation de quelques éléments métalliques chez l’huître Crassostrea gigas en élevage dans la lagune de Oualidia (Maroc): Rôle des facteurs écologiques et biologiques. Haliotis 28:31–44
Chen CW, Kao CM, Chen CF, Dong CD (2007) Distribution and accumulation of heavy metals in the sediments of Kaohsiung Harbor, Taiwan. Chemosphere 66:1431–1440
Chien LC, Hung TC, Choang KY, Yeh CY, Meng PJ, Shieh MJ, Han BC (2002) Daily intake of TBT, Cu, Zn, Cd and As for fishermen in Taiwan. Sci Total Environ 285:177–185
Chiffoleau JF, Claisse D, Cossa D, Ficht A, Gonzalez JL, Guyot T, Michel P, Miramand P, Oger C, Petit F (2001) La contamination métallique. Ifremer, Editions, 39p
Copat C, Arena G, Fiore M, Ledda C, Fallico R, Sciacca S, Ferrante M (2013) Heavy metals concentrations in fish and shellfish from eastern Mediterranean Sea: consumption advisories. Food Chem Toxicol 53:33–37. 10.1016/j.fct.2012.11.038
Cravo A, Pereira C, Gomes T, Cardoso C, Serafim A, Almeida C, Rocha T, Lopes B, Company R, Medeiros A, Norberto R, Pereira R, Araújo O, Bebianno MJ (2012) A multibiomarker approach in the clam Ruditapes decussatus to assess the impact of pollution in the Ria Formosa lagoon, south coast of Portugal. Mar Environ Res 75:23–34. 10.1016/j.marenvres.2011.09.012
Cuculic VV, Cukrov N, Kwokal Z, Mlakar M (2010) Trace metals in bivalves’ soft tissue from Mljet National Park Aquatorium, Croatia. Rapp 39 Congr Comm Int Explor Sci Mediterr 39:237
Currie L (1999) Nomenclature in evaluation of analytical methods including detection and quantification capabilities (IUPAC recommendations 1995). Anal Chim Acta 391:105–126
D’Adamo R, Di Stasio M, Fabbrochini A (2008) Migratory crustaceans as biomonitors of metal pollution in their nursery areas.The Lesina lagoon (SE Italy) as a case study. Eviron Monit Assess 143:15–24. 10.1007/s10661-007-9944-3
De Clercq N (2016) Seasonal variations in biochemical composition and metallothionein contents of digestive gland of Noah’s ark shell (Arca noae Linnaeus, 1758) from the Adriatic Sea., diplomski rad, preddiplomski, faculty education, health and social work, master degree, University of Ghent, 77p
Dellali M, Gnassia Barelli M, Romeo M, Aissa P, (2001) The use of acetylcholinesterase activity in Ruditapes decussatus and Mytilus galloprovincialis in the biomonitoring of Bizerta lagoon. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 130 (2): 227-235
Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol l86:421–431
EC (2006) Regulation (EC) No. 1881/2006 of the European Parliament and the Council of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Official Journal of the European Communities L364/5-22
Edokpayi JN, Odiyo JO, Popoola OE, Msagati TAM (2016) Assessment of trace metals contamination of surface water and sediment: a case study of Mvudi River, South Africa. Sustainability8:1-13.10.3390/su8020135
Ellman GL, Courtney KD, Anders V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. 10.1016/0006-2952(61)90145-9
Elumalai M, Antunes C, Guilhermino L (2002) Single metals and their mixtures on selected enzymes of Carcinus maenas. Water Air Soil Pollut 141:273–280. 10.1023/A:1021352212089
Erk M, Ivanković D, Župan I, Čulin J, Draguna Z, Puljas S, Peharda M (2018) Changes in the tissue concentrations of trace elements during the reproductive cycle of Noah's ark shells (Arca noae Linnaeus, 1758). Mar Pollut Bull 133:357–366. 10.1016/j.marpolbul.2018.05.054
FAO (1983) Compilation of legal limits for hazardous substances in fish and fishery products. FAO fishery circular no 464:5–100
FAO/WHO (2011) Evaluation of Certain Food Additives and Contaminants: Seventy-third [73rd] Report of the Joint FA
Flohe L, Günzler WA (1984) Assay of glutathione peroxidase. Methods Enzymol 105:115–121
Frías-Espericueta MG, Osuna-López JI, Sandoval-Salazar G, López-López G (1999) Distribution of trace metals in different tissues in the rock oyster Crassostrea iridescens: seasonal variation. Bull Environ Contam Toxicol 63:73–79
Geffard A, Amiard JC, Amiard-Triquet C (2002) Use of metallothionein in gills from oysters (Crassostrea gigas) as a biomarker: seasonal and intersite fluctuations. Biomarkers 7:123–137. 10.1080/13547500110091292
George RG, Martin D, Nair SM, Chandramohanakumar N (2013) Biomonitoring of trace metal pollution using the bivalve molluscs, Villorita cyprinoides, from the Cochin backwaters. Environ Monit Assess 185:10317–10331. 10.1007/s10661-013-3334-9
Ghribi F, Bello G, Zupa R, Passantino L, Santamaria N, El Cafsi M, Corriero A (2017) Reproductive and tissue plasticity in Arca noae (Bivalvia: Arcidae). European Zool J84:473–478. 10.1080/24750263.2017.1368725
Ghribi F, Boussoufa D, Aouini F, Bejaoui S, Chetoui I, Rabeh I, El Cafsi M (2018) Seasonal variation of biochemical composition of Noah's ark shells (Arca noae L. 1758) in a Tunisian coastal lagoon in relation to its reproductive cycle and environmental conditions. Aquatic. Living. Res. 31: 14. https://doi.org/10.1051/alr/2018002
Gofas S (2008) Arca noae. In: Mollusca Base 2016. Accessed through: world register of marine species at http://www.marinespecies.org/aphia.php?p=taxdetails&id=138788 [accessed on 10.8.2016]
Goldberg ED (1975) The mussel watch - a first step in a global marine monitoring. Mar Pollut Bull 6:111–114
Gourlay C (2004) Biodisponibilité des hydrocarbures aromatiques polycycliques dans les écosystèmes aquatiques: influence de la matière organique naturelle et anthropique. PhD Thesis. Ecole Nationale du Génie Rural, des Eaux et des Forêts
Grinzaid EL, Zil’bershtein KI, Nadezhina LS, Yufa BY (1977) Terms and methods of estimating detection limits in various analytical methods. J Analytic Chem USSR 32:1678–1684
Hrs-Brenko M, Legac M (1996) A review of bivalve species in the eastern Adriatic Sea: II. Pteriomorphia (Arcidae and Noetidae). Nat Croat 5:221–247
Ibrahim ATHA, Omar HM (2013) Seasonal variation of heavy metals accumulation in muscles of the African catfish Clarias gariepinus and in River Nile water and sediments at Assiut governorate, Egypt. J Biol Earth Sci 3:B236–B248
Idardare Z, Moukrim A, Chiffoleau JF, Ait Alla A (2011) Trace metals in the clam Donax trunculus L. from the Bouadisse sandy beach, discharge zone of a plant sewage outfall in Agadir Bay (Morocco). Bayed A. (ed.). Sandy beaches and coastal zone management – Proceedings of the Fifth International Symposium on Sandy Beaches, 19th-23rd October 2009, Rabat, Morocco Travaux de l'Institut Scientifique, Rabat, série générale, N°6, 51-58
IUPAC, Inczédy J, Lengyel T, Ure AM, Gelencsér A, Hulanicki A (1998) Compendium of analytical nomenclature, 3rd edn. Blackwell, Oxford
Ivankovic D, Erk M, Zupan I, Culin J, Dragun Z, Bacic N, Cindric AM (2016) Trace metals in Noah’s ark shells (Arca noae Linnaeus, 1758): impact of tourist season and human health risk. Arch Environ Contam Toxicol 71:394–404. 10.1007/s00244-016-0298-0
Joksimović D, Castelli A, Perošević A, Djurović D, Stanković S (2018) Determination of trace metals in Mytilus galloprovincialis along the Boka Kotorska Bay. Montenegrin coast J Trace Elements Med Biol 50:601–608
Jović M, Stanković S (2014) Human exposure to trace metals and possible public health risks via consumption of mussels Mytilus galloprovincialis from the Adriatic coastal area. Food Chem Toxicol 70:241–251. 10.1016/j.fct.2014.05.012
Kamel N, Burgeot T, Banni M, Chalghaf M, Devin S, Minier C, Boussetta H (2014) Effects of increasing temperatures on biomarker responses and accumulation of hazardous substances in rope mussels (Mytilus galloprovincialis) from Bizerte lagoon. Environ Sci Pollut Res 21:6108–6123. 10.1007/s11356-014-2540-5
Kefi FJ, Mleiki A, Maâtoug-Béjaoui J, Trigui-El Menif N (2015) Seasonal variations of trace metal concentrations in the soft tissue of Lithophaga Lithophaga collected from the Bizerte Bay (northern Tunisia, Mediterranean Sea). J Aquac Res Dev 7:432. 10.4172/2155-9546.1000432
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. 10.1016/j.cca.2005.04.005
Lodish H, Berk A, Zipursky SL et al. (2000) Molecular Cell Biology.4th edition. New York: W. H. freeman
Lowry OH, Rosebrough NJ, Farr AL, Randal RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Mahmoud N, Dellali M, El Bour M, Aissa P, Mahmoudi E (2010) The use of Fulvia fragilis (Mollusca: Cardiidae) in the biomonitoring of Bizerta lagoon: a mutimarkers approach. Ecol Indic 10:696–702. 10.1016/j.ecolind.2009.11.010
Marengo M, Durieux EDH, Ternengo S, Lejeune P, Degrange E, Pasqualini V, Gobert S (2018) Comparison of elemental composition in two wild and cultured marine fish and potential risks to human health. Ecotoxicol Environ Saf 30(158):204–212. 10.1016/j.ecoenv.2018.04.034
Marie V, Baudrimont M, Boudou A (2006) Cadmium and zinc bioaccumulation and metallothionein response in two freshwater bivalves (Corbicula fluminea and Dreissena polymorpha) transplanted along a polymetallic gradient. Chemosphere 65:609–617
Milun V, Lušić J, Despalatović M (2016) Polychlorinated biphenyls, organochlorine pesticides and trace metals in cultured and harvested bivalves from the eastern Adriatic coast (Croatia). Chemosphere 153:18–27. 10.1016/j.chemosphere.2016.03.039
Mubiana VK, Qadah D, Meys J, Blust R (2005) Temporal and spatial trends in heavy metal concentrations in the marine mussel Mytilus edulis from the Western Scheldt estuary (the Netherlands). Hydrobiologia 540:169–180 10.1007/s10750-004-7134-7
Nadal M, Ferre-Huguet N, Marti-Cid R, Schuhmacher M, Domingo JL (2008) Exposure to metals through the consumption of fish and seafood by the population living near the Ebro River in Catalonia, Spain: health risks. Hum Ecol Risk Assess 14:780–795. 10.1080/10807030802235235
Nieto R, Garcia-Barrera T, Gomez-Ariza JL, Lopez Barea J (2010) Environmental monitoring of Domingo Rubio stream (Huelva estuary, SW Spain) by combining conventional biomarkers and proteomic analysis in Carcinus maenas. Environ Pollut 158:401–408. 10.1016/j.envpol.2009.09.005
ODEQ (2007) Guidance for assessing bioaccumulative Chemicals of Concern in sediment. Oregon Department of Environmental Quality. Environmental cleanup program: 07-LQ-023A
Olesik J, Jones D (2006) Strategies to develop methods using ion-molecule reactions in a quadrupole reaction cell to overcome spectral overlaps in inductively coupled plasma mass spectrometry. J Anal Atomic Spectro 21:141–159
Orbea A, Ortiz-Zarragoitia M, Sole 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
Ozretic B, Krajnovic-Ozretic M, Santin J, Medjugorac B, Kras M (1990) As, Cd, Pb and Hg in benthic animals from the Kvarner-Rijeka Bay region, Yugoslavia. Mar Pollut Bull 21:595–597. 10.1016/0025-326X(90)90610-K
Pelletier E (2006) Seasonal variations of physiological parameters in the blue mussel Mytilus spp. from farm sites of eastern Quebec. Aquaculture 261:729–751. 10.1016/j.aquaculture.2006.08.017
Perić L, Ribarić L, Nerlović V (2013) Cholinesterase activity in the tissues of bivalves Noah’s ark shell (Arca noae) and warty venus (Venus verrucosa): characterisation and in vitro sensitivity to organophosphorous pesticide trichlorfon. Comp Biochem Physiol B 165:243–249. 10.1016/j.cbpb.2013.05.002
Petrović S, Ozretić B, Krajnović-Ozretić M, Bobinac D (2001) Lysosomal membrane stability and metallothioneins in digestive gland of mussels (Mytilus galloprovincialis) as biomarkers in a field study. Mar Pollut Bull 42:1373–1378
Phillips DJH (1976) The common mussel Mytilus edulis as an indicator of pollution by zinc, cadmium, lead and copper: effects of environmental variables on uptake of metals. Mar Biol 38:59–69. 10.1007/BF00391486
Phuong TTM (2014) Bioaccumulation of heavy metals in Nha Trang bay, Khanh Hoa, Viet Nam. Earth Sciences. Université Nice Sophia Antipolis, PhD Thesis, NNT: 2014NICE4058. tel01080132
Pinta M (1980) Spectrométrie d’absorption atomique, application à l’analyse chimique. 2ième édition, Paris
Prato E, Biandolino F, Parlapiano I, Giandomenico S, Denti G, Calo M, Spada L, DiLeo A (2019) Proximate, fatty acids and metals in edible marine bivalves from Italian market: beneficial and risk for consumers health. Sci Total Environ 648:153–163
Poutiers JM (1987) Bivalves. In: Fischer W, Bauchot ML, Schneider M, editors. Fiches FAO d’identification des espèces pour les besoins de la pêche. (Révision 1). Méditerranée et Mer noire. Rome: food and agriculture Organization of the United Nations, FAO, 369-512p
Prevodnik A, Gardeström J, Lilja K, Elfwing T, McDonagh B, Petrović N, Tedengren M, Sheehan D, Bollner T (2007) Oxidative stress in response to xenobiotics in the blue mussel Mytilus edulis L.: evidence for variation along a natural salinity gradient of the Baltic Sea. Aquat Toxicol 82:63–71. 10.1016/j.aquatox.2007.01.006
Puljas S, Peharda M, Župan I, Bukša F (2015) Maximum recorded life span of Arca noae Linnaeus, 1758 in the marine protected area Telaščica, Adriatic Sea. Cah Biol Mar 56:163–168
Raspor B, Dragun Z, Erk M, Ivanković D, Pavii J (2004) Is the digestive gland of Mytilus galloprovincialis a tissue of choice for estimating cadmium exposure by means of metallothioneins? Sci Total Environ 333:99–108. 10.1016/j.scitotenv.2004.05.008
Richir J, Gobert S (2014) The effect of size, weight, body compartment, sex and reproductive status on the bioaccumulation of 19 trace elements in rope-grown Mytilus galloprovincialis. Ecol Indic 36:33–47. 10.1016/j.ecolind.2013.06.021
Rinbio (2001) Evaluation de la qualité des eaux basée sur l’utilisation de stations artificielles de moules en Méditerranée: résultats de la campagne 2000. Ifremer et Ministère de l’Ecologie et du Développement Durable. 94p
Rouane Hacene O, Boutiba Z, Belhaouaria B, Guibbolini-sabatier M, Francour P, Risso-de Faverney C (2015) Seasonal assessment of biological indices, bioaccumulation and bioavailability of heavy metals in mussels Mytilus galloprovincialis from Algerian west coast, applied to environmental monitoring. Oceanologia 57:362–374. 10.1016/j.oceano.2015.07.004
Roesijadi G (1994) Metallothionein induction as a measure of response to metal exposure in aquatic animals. Environ Health Perspect 102:91–95
Saha N, Mollah MZI, Alam MF, Rahman MS (2016) Seasonal investigation of heavy metals in marine fishes captured from the Bay of Bengal and the implications for human health risk assessment. Food Control 70:110–118. 10.1016/j.foodcont.2016.05.040
Spencer KL, MacLeod CL, Tuckett A, Johnson SM (2006) Source and distribution of trace metals in the Medway and Swale estuaries, Kent. Mar Pollut Bull 52:226–231. 10.1016/j.marpolbul.2005.10.019
Staines-Urías F, Douglas RG, Gorsline DS (2009) Oceanographic variability in the southern Gulf of California over the past 400 years: evidence from faunal and isotopic records from planktic foraminifera. Palaeoecol 284:337–354. 10.1016/j.palaeo.2009.10.016
Strizak Z, Ivankovic D, Profrock D, Helmholz H, Cindric AM, Erk M, Prange A (2014) Characterization of the cytosolic distribution of priority pollutant metals and metalloids in the digestive gland cytosol of marine mussels: seasonal and spatial variability. Sci Total Environ 470-471:159–170. 10.1016/j.scitotenv.2013.09.051
Storelli MM, Marcotrigiano GO (2001) Total mercury levels in muscle tissue of swordfish (Xiphias gladius) and bluefin tuna (Thunnus thynnus) from the Mediterranean Sea (Italy). J Food Prot 64:1058–1061
Storelli MM (2008) Potential human health risks from metals (Hg, Cd, and Pb) and polychlorinated biphenyls (PCBs) via seafood consumption: estimation of target hazard quotients (THQs) and toxic equivalents (TEQs). Food Chem Toxicol 46:2782–2788. 10.1016/j.fct.2008.05.011
Trabelsi S, Driss MR (2005) Polycyclic aromatic hydrocarbons in superficial coastal sediments from Bizerte lagoon, Tunisia. Mar Pollut Bull 50:344–359
Türkmen A, Türkmen M, Tepe Y, Çekiç M (2010) Metals in tissues of fish from Yelkoma lagoon, northeastern Mediterranean. Environ Monit Assess 168:223–230. 10.1007/s10661-009-1106-3
USEPA (2010) Risk-based concentration table. Region 3. Philadelphia, PA
USFDA (2001) United States Food and Drug Administration, fish and fisheries products hazards and controls guidance. Appendix 5—FDA and EPA safety levels in regulations and guidance, 3rd edn
Uluturhan E, Darılmaz E, Kontas A, Bilgin M, Alyuruk H, Altay O, Sevgi S (2019) Seasonal variations of multi-biomarker responses to metals and pesticides pollution in M. galloprovincialis and T. decussatus from Homa lagoon, eastern Aegean Sea. Mar Pollut Bull 141:176–186
Verlecar XN, Jena KB, Chainy GBN (2007) Biochemical markers of oxidative stress in Perna viridis exposed to mercury and temperature. Chem Biol Interact 167:219–226. 10.1016/j.cbi.2007.01.018
Viarengo A, Ponzano E, Dondero F, Fabbri R (1997) A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic mollusks. Mar Environ Res 44:69–84. 10.1016/S0141-1136(96)00103-1
Vieira C, Morais S, Ramos S, Delerue-Matos C, Oliveira M (2011) Mercury, cadmium, lead and arsenic levels in three pelagic fish species from the Atlantic Ocean: intra-and inter-specific variability and human health risks for consumption. Food Chem Toxicol 49:923–932. 10.1016/j.fct.2010.12.016
Viegas CN, Nunes S, Fernández R, Neves R (2009) Streams contribution on bathing water quality after rainfall events in Costa do Estoril- a tool to implement an alert system for bathing water. J Coast Res 56:1691–1695
Waeles M, Riso RD, Le Corre P (2007) Distribution and seasonal changes of lead in an estuarine system affected by agricultural practices: the Penze estuary, NW France. Estuar Coast Shelf S 74:570–578
Wang WX (2009) Metals and organic contaminants in bivalve molluscs. Shellfish safety and quality. Woodhead publishing series in food science, technology and Nutrition Pages 228-247
Wang Z, Ma X, Lin Z, Na G, Yao Z (2009) Congener specific distributions of polybrominated diphenyl ethers (PBDEs) in sediment and mussel (Mytilus edulis) of the Bo Sea, China. Chemosphere 74:896–901. 10.1016/j.chemosphere.2008.10.064
Warwick R (2005) Taxonomic distincness as an indicator of stress in the marine macrobenthos. Indicators of stress in the marine benthos, IOC workshop report No 195:10–11p
Yamaguchi S, Miura C, Kikuchi K, Celino FT, Agusa T, Tanabe S, Miura T (2009) Zinc is an essential trace element for spermatogenesis. Proc Natl Acad Sci U S A 106:10859–10864. 10.1073/pnas.0900602106
Yi Y, Yang Z, Zhang S (2011) Ecological risk assessment of heavy metals in sediment and human health risk assessment of heavy metals in fishes in the middle and lower reaches of the Yangtze River basin. Environ Pollut 159:2575–2585. 10.1016/j.envpol.2011.06.011
Yusa V, Suelves T, Ruiz-Atienza L, Cervera ML, Benedito V, Pastor A (2008) Monitoring program on cadmium, lead and mercury in fish and seafood from Valencia, Spain: levels and estimated weekly intake. Food Addit Contam Part B Surveill 1:22–31. 10.1080/19393210802236935
Zaaboub N, Alves Martins MV, Dhib A, Béjaoui B, Galgani F, El Bour M, Aleya L (2015) Accumulation of trace metals in sediments in a Mediterranean lagoon: usefulness of metal sediment fractionation and elutriate toxicity assessment. Environ Pollut 207:226–237. 10.1016/j.envpol.2015.09.033
Župan I, Peharda M, Ezgeta-Balić D, Šarić T (2012) Noah’s ark shell (Arca noae Linnaeus, 1758) - what do we need to know for starting up its aquaculture? Croat J Fish 70:71–81
