Skip to main content
Log in

Heavy metal accumulation in Diplodus annularis, Liza aurata, and Solea vulgaris relevant to their concentration in water and sediment from the southwestern Mediterranean (coast of Sfax)

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The concentrations of heavy metals (Cd, Cu, Fe, Pb, Ni, and Zn) were measured in the liver, gills, and muscle of Solea vulgaris, Liza aurata, and Diplodus annularis, collected from the south coast of Sfax (Gabes Gulf, southwestern Mediterranean). The concentrations of heavy metals in water exhibited the following decreasing order (expressed in μg l−1): Fe > Ni > Zn > Cu > Pb > Cd whereas the trend is somewhat different in sediments (mg kg−1 D.W.) Fe > Zn > Pb > Ni > Cu > Cd. The levels of heavy metals varied significantly among fish species and tissues. Heavy metal levels were found generally higher in the liver and gills than the muscle in all species. The liver was the target organ for Cd, Cu, Fe, Ni, and Zn accumulation. Nickel and lead, however, exhibited their highest concentrations in the gills. The three studied fishes showed a difference in metals accumulation decreasing in following order S. vulgaris > D. annularis > L. aurata. Solea vulgaris with the highest TFwater, TFsediment, and metal concentrations in tissues would be considered as a potential bio-indicator in the south coast of Sfax for the assessment of environmental pollution status. Comparative studies with Luza zone indicate considerable bioaccumulation of heavy metals (Pb and Zn) in the various tissues of fish samples of the south coast of Sfax.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agah H, Leermakers M, Elskens M et al (2009) Accumulation of trace metals in the muscle and liver tissues of five fish species from the Persian Gulf. Environ Monit Assess 157:499–514. doi:10.1007/s10661-008-0551-8

    Article  CAS  Google Scholar 

  • Al Sayegh Petkovšek S, Mazej Grudnik Z, Pokorny B (2012) Heavy metals and arsenic concentrations in ten fish species from the Šalek lakes (Slovenia): assessment of potential human health risk due to fish consumption. Environ Monit Assess 184:2647–2662. doi:10.1007/s10661-011-2141-4

    Article  Google Scholar 

  • Amiard J, Amiardtriquet 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. doi:10.1016/j.aquatox.2005.08.015

    Article  CAS  Google Scholar 

  • Arain MB, Kazi TG, Jamali MK et al (2008) Total dissolved and bioavailable elements in water and sediment samples and their accumulation in Oreochromis mossambicus of polluted Manchar Lake. Chemosphere 70:1845–1856. doi:10.1016/j.chemosphere.2007.08.005

    Article  CAS  Google Scholar 

  • Ashraf W, Seddigi Z, Abulkibash A, Khalid M (2006) Levels of selected metals in canned fish consumed in Kingdom of Saudi Arabia. Environ Monit Assess 117:271–279. doi:10.1007/s10661-006-0989-5

    Article  CAS  Google Scholar 

  • Banni M, Jebali J, Daubeze M et al (2005) Monitoring pollution in Tunisian coasts: application of a classification scale based on biochemical markers. Biomarkers 10:105–116. doi:10.1080/13547500500107497

    Article  CAS  Google Scholar 

  • Banni M, Dondero F, Jebali J et al (2007) Assessment of heavy metal contamination using real-time PCR analysis of mussel metallothionein mt10 and mt20 expression: a validation along the Tunisian coast. Biomarkers 12:369–383. doi:10.1080/13547500701217061

    Article  CAS  Google Scholar 

  • Barhoumi S, Messaoudi I, Deli T et al (2009) Cadmium bioaccumulation in three benthic fish species, Salaria basilisca, Zosterisessor ophiocephalus and Solea vulgaris collected from the Gulf of Gabes in Tunisia. J Environ Sci 21:980–984. doi:10.1016/S1001-0742(08)62371-2

    Article  CAS  Google Scholar 

  • Ben Rebah F, Abdelmouleh A, Kammoun W, Yezza A (2010) Seasonal variation of lipid content and fatty acid composition of Sardinella aurita from the Tunisian coast. J Mar Biol Assoc U K 90:569. doi:10.1017/S0025315409990658

    Article  CAS  Google Scholar 

  • Ben Salem Z, Capelli N, Laffray X et al (2014) Seasonal variation of heavy metals in water, sediment and roach tissues in a landfill draining system pond (Etueffont, France). Ecol Eng 69:25–37. doi:10.1016/j.ecoleng.2014.03.072

    Article  Google Scholar 

  • Ben Salem Z, Drira Z, Ayadi H (2015) What factors drive the variations of phytoplankton, ciliate and mesozooplankton communities in the polluted southern coast of Sfax, Tunisia? Environ Sci Pollut Res. doi:10.1007/s11356-015-4416-8

    Google Scholar 

  • Bervoets L, Blust R (2003) Metal concentrations in water, sediment and gudgeon (Gobio gobio) from a pollution gradient: relationship with fish condition factor. Environ Pollut 126:9–19. doi:10.1016/S0269-7491(03)00173-8

    Article  CAS  Google Scholar 

  • Brumbaugh WG, Schmitt CJ, May TW (2005) Concentrations of cadmium, lead, and zinc in fish from mining-influenced waters of northeastern Oklahoma: sampling of blood, carcass, and liver for aquatic biomonitoring. Arch Environ Contam Toxicol 49:76–88. doi:10.1007/s00244-004-0172-3

    Article  CAS  Google Scholar 

  • Bryan GW, Langston WJ (1992) Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries: a review. Environ Pollut 76:89–131

    Article  CAS  Google Scholar 

  • Bustamante P, Bocher P, Chérel Y et al (2003) Distribution of trace elements in the tissues of benthic and pelagic fish from the Kerguelen Islands. Sci Total Environ 313:25–39. doi:10.1016/S0048-9697(03)00265-1

    Article  CAS  Google Scholar 

  • Cairo G, Bernuzzi F, Recalcati S (2006) A precious metal: iron, an essential nutrient for all cells. Genes Nutr 1:25–40. doi:10.1007/BF02829934

    Article  CAS  Google Scholar 

  • Castro-González MI, Méndez-Armenta M (2008) Heavy metals: implications associated to fish consumption. Environ Toxicol Pharmacol 26:263–271. doi:10.1016/j.etap.2008.06.001

    Article  Google Scholar 

  • Chaouch H, Hamida-Ben Abdallah O, Ghorbel M, Jarboui O (2013) Reproductive biology of the annular seabream, Diplodus annularis (Linnaeus, 1758), in the Gulf of Gabes (Central Mediterranean). J Appl Ichthyol 29:796–800

    Article  Google Scholar 

  • Chovanec A, Hofer R, Schiemer HG (2003) Trace metals and other contaminants in the environment 6. In: Markert BA, Breure AM, Zechmeister HG (eds) Fish as bioindicators. Oxford UK, pp 1–997

  • Cizdziel J, Hinners T, Cross C, Pollard J (2003) Distribution of mercury in the tissues of five species of freshwater fish from Lake Mead, USA. J Environ Monit 5:802. doi:10.1039/b307641p

    Article  CAS  Google Scholar 

  • Connor MS (1984) Fish/sediment concentration ratios for organic compounds. Environ Sci Technol 18:31–35

    Article  CAS  Google Scholar 

  • D G P A (2004) Annuaires des statistiques des produits de la pêche. Ministère de l’Agriculture, Tunisie. 144

  • Dallinger R (1993) In ecotoxicology of metals in invertebrates, strategies of metal detoxification in terrestrial invertebrates. Lewis Publisher, Boca Raton

    Google Scholar 

  • DeForest DK, Brix KV, Adams WJ (2007) Assessing metal bioaccumulation in aquatic environments: The inverse relationship between bioaccumulation factors, trophic transfer factors and exposure concentration. Aquat Toxicol 84:236–246. doi:10.1016/j.aquatox.2007.02.022

    Article  CAS  Google Scholar 

  • Degirmenci N (2008) Utilization of phosphogypsum as raw and calcined material in manufacturing of building products. Constr Build Mater 22:1857–1862. doi:10.1016/j.conbuildmat.2007.04.024

    Article  Google Scholar 

  • Derbal F, Nouacer S, Kara MH (2007) Composition et variations du régime alimentaire du sparaillon Diplodus annularis (Sparidae) du golfe d’Annaba (Est de l’Algérie). Cybium 31:443–450

  • Dhaneesh KV, Gopi M, Ganeshamurthy R et al (2012) Bio-accumulation of metals on reef associated organisms of Lakshadweep Archipelago. Food Chem 131:985–991. doi:10.1016/j.foodchem.2011.09.097

    Article  CAS  Google Scholar 

  • Doraghi A, Monikh FA, Safahieh A, Savari A (2011) Heavy metals concentration in mullet fish, Liza abu from Petrochemical Waste Receiving Creeks, Musa Estuary (Persian Gulf). J Environ Prot 02:1218–1226. doi:10.4236/jep.2011.29140

    Article  Google Scholar 

  • Dural M, Göksu MZL, Özak AA (2007) Investigation of heavy metal levels in economically important fish species captured from the Tuzla lagoon. Food Chem 102:415–421. doi:10.1016/j.foodchem.2006.03.001

    Article  CAS  Google Scholar 

  • Ebrahimpour M, Pourkhabbaz A, Baramaki R et al (2011) Bioaccumulation of heavy metals in freshwater fish species, Anzali, Iran. Bull Environ Contam Toxicol 87:386–392. doi:10.1007/s00128-011-0376-y

    Article  CAS  Google Scholar 

  • El-mor M, Ahamed AI (2008) Feeding habits of the common sole, Solea vulgaris (Quensel, 1806), from Mediterranean Sea, port said Egypt. Egypt J Aquat Biol Fish 12:5–61

    Google Scholar 

  • El-Moselhy KM, Othman AI, Abd El-Azem H, El-Metwally MEA (2014) Bioaccumulation of heavy metals in some tissues of fish in the Red Sea, Egypt. Egypt J Basic Appl Sci 1:97–105. doi:10.1016/j.ejbas.2014.06.001

    Article  Google Scholar 

  • Ersoya B, Celik M (2009) Essential elements and contaminants in tissues of commercial pelagic fish from the Eastern Mediterranean Sea. J Sci Food Agric 89:1615–1621

    Article  Google Scholar 

  • FAO/WHO (1989) Evaluation of certain food additives and the contaminants mercury, lead and cadmium. WHO Technical Report Series

  • FAO/WHO (2004) Summary of Evaluations Performed by the joint FAO/WHO Expert Committee on Food Additives (JECFA 1956–2003), ILSI Press International Life Sciences Institute 2004

  • Farkas A, Salánki J, Specziár A (2003) Age-and size-specific patterns of heavy metals in the organs of freshwater fish Abramis brama L. populating a low-contaminated site. Water Res 37:959–964

    Article  CAS  Google Scholar 

  • Flemming CA, Trevors JT (1989) Copper toxicity and chemistry in the environment: a review. Water Air Soil Pollut 44:143–158

    Article  CAS  Google Scholar 

  • Forti E, Salovaara S, Cetin Y et al (2011) In vitro evaluation of the toxicity induced by nickel soluble and particulate forms in human airway epithelial cells. Toxicol In Vitro 25:454–461. doi:10.1016/j.tiv.2010.11.013

    Article  CAS  Google Scholar 

  • Gao X, Chen C-TA (2012) Heavy metal pollution status in surface sediments of the coastal Bohai Bay. Water Res 46:1901–1911. doi:10.1016/j.watres.2012.01.007

    Article  CAS  Google Scholar 

  • García-Lestón J, Méndez J, Pásaro E, Laffon B (2010) Genotoxic effects of lead: an updated review. Environ Int 36:623–636. doi:10.1016/j.envint.2010.04.011

    Article  Google Scholar 

  • Gargouri D, Azri C, Serbaji MM et al (2011) Heavy metal concentrations in the surface marine sediments of Sfax Coast, Tunisia. Environ Monit Assess 175:519–530. doi:10.1007/s10661-010-1548-7

    Article  CAS  Google Scholar 

  • Gorell JM, Johnson CC, Rybicki BA et al (1997) Occupational exposures to metals as risk factors for Parkinson’s disease. Neurology 48:650–658

    Article  CAS  Google Scholar 

  • Gu Y-G, Wang Z-H, Lu S-H et al (2012a) Multivariate statistical and GIS-based approach to identify source of anthropogenic impacts on metallic elements in sediments from the mid Guangdong coasts, China. Environ Pollut 163:248–255. doi:10.1016/j.envpol.2011.12.041

    Article  CAS  Google Scholar 

  • Gu Y, Yang Y, Lin Q et al (2012b) Spatial, temporal, and speciation variations of heavy metals in sediments of Nan’ao Island, a representative mariculture base in Guangdong coast, China. J Environ Monit 14:1943–1950

    Article  CAS  Google Scholar 

  • Hamza-Chaffai A, Cosson RP, Amiard-Triquet C, El Abed A (1995) Physico-chemical forms of storage of metals (Cd, Cu and Zn) and metallothionein-like proteins in gills and liver of marine fish from the Tunisian coast: ecotoxicological consequences. Camp Biochem Physiol 111:329–341. doi:10.1016/0742-8413(95)00058-V

    Article  Google Scholar 

  • Hamza-Chaffai A, Amiard-Triquet C, El Abed A (1997) Metallothionein-like protein: is it an efficient biomarker of metal contamination? A case study based on fish from the Tunisian coast. Arch Environ Contam Toxicol 33:53–62. doi:10.1007/s002449900223

    Article  CAS  Google Scholar 

  • Hamza-Chaffai A, Pellerin J, Amiard JC (2003) Health assessment of a marine bivalve Ruditapes decussatus from the Gulf of Gabès (Tunisia). Environ Int 28:609–617

    Article  CAS  Google Scholar 

  • Hernández PP, Moreno V, Olivari FA, Allende ML (2006) Sub-lethal concentrations of waterborne copper are toxic to lateral line neuromasts in zebrafish (Danio rerio). Hear Res 213:1–10. doi:10.1016/j.heares.2005.10.015

    Article  Google Scholar 

  • Ip CCM, Li XD, Zhang G et al (2005) Heavy metal and Pb isotopic compositions of aquatic organisms in the Pearl River Estuary, South China. Environ Pollut 138:494–504. doi:10.1016/j.envpol.2005.04.016

    Article  CAS  Google Scholar 

  • Jayaprakash M, Kumar RS, Giridharan L et al (2015) Bioaccumulation of metals in fish species from water and sediments in macrotidal Ennore creek, Chennai, SE coast of India: a metropolitan city effect. Ecotoxicol Environ Saf 120:243–255. doi:10.1016/j.ecoenv.2015.05.042

    Article  CAS  Google Scholar 

  • Kalfakakou V, Akrida-Demertzi K (2000) Transfer factors of heavy metals in aquatic organisms of different trophic level. Artic Available Adress Httpbusiness Nol Gr ∼ BioallfileHtmlKalfak Htm Last View 0101 2010 1:768–786

  • Karadede H, Oymak SA, Ünlü E (2004) Heavy metals in mullet, Liza abu, and catfish, Silurus triostegus, from the Atatürk Dam Lake (Euphrates), Turkey. Environ Int 30:183–188. doi:10.1016/S0160-4120(03)00169-7

    Article  CAS  Google Scholar 

  • Kargin F (1998) Metal concentrations in tissues of the freshwater fish Capoeta barroisi from the Seyhan River (Turkey). Bull Environ Contam Toxicol 60:822–828

    Article  CAS  Google Scholar 

  • Kessabi K, Kerkeni A, Saïd K, Messaoudi I (2009) Involvement of Cd bioaccumulation in spinal deformities occurrence in natural populations of Mediterranean killifish. Biol Trace Elem Res 128:72–81. doi:10.1007/s12011-008-8255-z

    Article  CAS  Google Scholar 

  • Ketata Khitouni I, Boudhrioua Mihoubi N, Bouain A, Ben Rebah F (2014) Accumulation of Hg, Pb, Cr, and Fe in muscle and head of four fish species: Diplodus annularis, Zosterisessor ophiocephalus, Liza aurata and Caranx rhonchus. J Adv Biol 5:1–559

    Google Scholar 

  • Korkmaz Görür F, Keser R, Akçay N, Dizman S (2012) Radioactivity and heavy metal concentrations of some commercial fish species consumed in the Black Sea Region of Turkey. Chemosphere 87:356–361. doi:10.1016/j.chemosphere.2011.12.022

    Article  Google Scholar 

  • Kucuksezgin F, Gonul LT, Tasel D (2014) Total and inorganic arsenic levels in some marine organisms from Izmir Bay (Eastern Aegean Sea): a risk assessment. Chemosphere 112:311–316. doi:10.1016/j.chemosphere.2014.04.071

    Article  CAS  Google Scholar 

  • Kuryatnyk T, Angulski da Luz C, Ambroise J, Pera J (2008) Valorization of phosphogypsum as hydraulic binder. J Hazard Mater 160:681–687. doi:10.1016/j.jhazmat.2008.03.014

    Article  CAS  Google Scholar 

  • Licata P, Trombetta D, Cristani M et al (2005) Heavy metals in liver and muscle of bluefin tuna (Thunnus thynnus) caught in the straits of Messina (Sicily, Italy). Environ Monit Assess 107:239–248. doi:10.1007/s10661-005-2382-1

    Article  CAS  Google Scholar 

  • MacDonald DD, Ingersoll CG, Berger TA (2000) Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Arch Environ Contam Toxicol 39:20–31. doi:10.1007/s002440010075

    Article  CAS  Google Scholar 

  • March D, Alós J, Grau A, Palmer M (2011) Short-term residence and movement patterns of the annular seabream Diplodus annularis in a temperate marine reserve. Estuar Coast Shelf Sci 92:581–587. doi:10.1016/j.ecss.2011.02.015

    Article  Google Scholar 

  • Messaoudi I, Barhoumi S, Saïd K, Kerken A (2009a) Study on the sensitivity to cadmium of marine fish Salaria basilisca (Pisces: Blennidae). J Environ Sci 21:1620–1624. doi:10.1016/S1001-0742(08)62464-X

    Article  CAS  Google Scholar 

  • Messaoudi I, Deli T, Kessabi K et al (2009b) Association of spinal deformities with heavy metal bioaccumulation in natural populations of grass goby, Zosterisessor ophiocephalus Pallas, 1811 from the Gulf of Gabès (Tunisia). Environ Monit Assess 156:551–560. doi:10.1007/s10661-008-0504-2

    Article  CAS  Google Scholar 

  • Monikh AF, Safahieh A, Savari A et al (2013) The relationship between heavy metal (Cd, Co, Cu, Ni and Pb) levels and the size of benthic, benthopelagic and pelagic fish species, Persian Gulf. Bull Environ Contam Toxicol 90:691–696. doi:10.1007/s00128-013-0986-7

    Article  Google Scholar 

  • Monteiro SM, dos Santos NMS, Calejo M et al (2009) Copper toxicity in gills of the teleost fish, Oreochromis niloticus: effects in apoptosis induction and cell proliferation. Aquat Toxicol 94:219–228. doi:10.1016/j.aquatox.2009.07.008

    Article  CAS  Google Scholar 

  • Moon TW, Walsh PJ, Mommsen TP (1985) Fish hepatocytes: a model metabolic system. Can J Fish Aquat Sci 42:1772–1782

    Article  CAS  Google Scholar 

  • Morillo J, Usero J, Gracia I (2004) Heavy metal distribution in marine sediments from the southwest coast of Spain. Chemosphere 55:431–442. doi:10.1016/j.chemosphere.2003.10.047

    Article  CAS  Google Scholar 

  • Naser HA (2013) Assessment and management of heavy metal pollution in the marine environment of the Arabian Gulf: A review. Mar Pollut Bull 72:6–13. doi:10.1016/j.marpolbul.2013.04.030

    Article  CAS  Google Scholar 

  • Niyogi S, Wood CM (2006) Interaction between dietary calcium supplementation and chronic waterborne zinc exposure in juvenile rainbow trout, Oncorhynchus mykiss. Comp Biochem Physiol Part C: Toxicol Pharmacol 143:94–102. doi:10.1016/j.cbpc.2005.12.007

    CAS  Google Scholar 

  • Nor Hasyimah AK, James Noik V, Teh YY et al. (2011) Assessment of cadmium (Cd) and lead (Pb) levels in commercial marine fish organs between wet markets and supermarkets in Klang Valley, Malaysia

  • Oliveira M, Santos M, Pacheco M (2004) Glutathione protects heavy metal-induced inhibition of hepatic microsomal ethoxyresorufin O-deethylase activity in Dicentrarchus labrax L. Ecotoxicol Environ Saf 58:379–385. doi:10.1016/j.ecoenv.2004.03.003

    Article  CAS  Google Scholar 

  • Oliveira M, Ahmad I, Maria VL et al (2010) Monitoring pollution of coastal lagoon using Liza aurata kidney oxidative stress and genetic endpoints: an integrated biomarker approach. Ecotoxicology 19:643–653. doi:10.1007/s10646-009-0436-9

    Article  CAS  Google Scholar 

  • Omar WA, Saleh YS, Marie M-AS (2014) Integrating multiple fish biomarkers and risk assessment as indicators of metal pollution along the Red Sea coast of Hodeida, Yemen Republic. Ecotoxicol Environ Saf 110:221–231. doi:10.1016/j.ecoenv.2014.09.004

    Article  CAS  Google Scholar 

  • Paez-Osuna F, Ruiz-Fernandez C (1995) Trace metals in the Mexican shrimp Penaeus vannamei from estuarine and marine environments. Environ Pollut 87:243–247

    Article  CAS  Google Scholar 

  • Pita C, Gamito S, Erzini K (2002) Feeding habits of the gilthead seabream (Sparus aurata) from the Ria Formosa (southern Portugal) as compared to the black seabream (Spondyliosoma cantharus) and the annular seabream (Diplodus annularis). J Appl Ichthyol 18:81–86

    Article  Google Scholar 

  • Qadir A, Malik RN (2011) Heavy metals in eight edible fish species from two polluted tributaries (Aik and Palkhu) of the River Chenab, Pakistan. Biol Trace Elem Res 143:1524–1540. doi:10.1007/s12011-011-9011-3

    Article  CAS  Google Scholar 

  • Rabaoui L, Balti R, Zrelli R, Tlig-Zouari S (2013) Assessment of heavy metals pollution in the gulf of Gabes (Tunisia) using four mollusk species. Mediterr Mar Sci. doi:10.12681/mms.504

    Google Scholar 

  • Randall D (1990) Control and co-ordination of gas exchange in water breathers. In: Boutilier DRG (ed) Vertebrate gas exchange, advances in comparative and environmental physiology. Berlin Heidelberg, pp 253–278

  • Rashed MN (2001) Monitoring of environmental heavy metals in fish from Nasser Lake. Environ Int 27:27–33

    Article  CAS  Google Scholar 

  • Roesijudi G (1996) Metallothionein and its role in toxic metal regulation. Comp Biochem Pysiol Part C: Pharmacol, Toxicol Endoctrinol 113:117–123

    Google Scholar 

  • Romeo M, Siau Y, Sidoumou Z, Gnassia-Barelli M (1999) Heavy metal distribution in different fish species from the Mauritania coast. Sci Total Environ 232:169–175

    Article  CAS  Google Scholar 

  • Sapkota A, Sapkota AR, Kucharski M et al (2008) Aquaculture practices and potential human health risks: current knowledge and future priorities. Environ Int 34:1215–1226. doi:10.1016/j.envint.2008.04.009

    Article  Google Scholar 

  • Serbaji MM, Azri C, Medhioub K (2012) Anthropogenic contributions to heavy metal distributions in the surface and sub-surface sediments of the northern coast of Sfax, Tunisia. Int J Environ Res 6:613–626

    CAS  Google Scholar 

  • Sfakianakis DG, Renieri E, Kentouri M, Tsatsakis AM (2015) Effect of heavy metals on fish larvae deformities: a review. Environ Res 137:246–255. doi:10.1016/j.envres.2014.12.014

    Article  CAS  Google Scholar 

  • Sivaperumal P, Sankar T, Viswanathannair P (2007) Heavy metal concentrations in fish, shellfish and fish products from internal markets of India vis-a-vis international standards. Food Chem 102:612–620. doi:10.1016/j.foodchem.2006.05.041

    Article  CAS  Google Scholar 

  • Smaoui-Damak W, Hamza-Chaffai A, Berthet B, Amiard JC (2003) Preliminary study of the clam Ruditapes decussatus exposed in situ to metal contamination and originating from the Gulf of Gabs, Tunisia. Bull Environ Contam Toxicol 71:961–970

    Article  CAS  Google Scholar 

  • Smaoui-Damak W, Berthet B, Hamza-Chaffai A (2009) In situ potential use of metallothionein as a biomarker of cadmium contamination in Ruditapes decussatus. Ecotoxicol Environ Saf 72:1489–1498. doi:10.1016/j.ecoenv.2009.01.005

    Article  CAS  Google Scholar 

  • Stancheva M, Makedonski L, Petrova E (2013) Determination of heavy metals (Pb, Cd, As and Hg) in black sea grey mullet (Mugil cephalus). Bulg J Agric Sci 19:30–34

    Google Scholar 

  • Storelli MM, Barone G, Storelli A, Marcotrigiano GO (2006) Trace metals in tissues of mugilids (Mugil auratus, Mugil capito, and Mugil labrosus) from the Mediterranean Sea. Bull Environ Contam Toxicol 77:43–50. doi:10.1007/s00128-006-1030-y

    Article  CAS  Google Scholar 

  • Tapia J, Vargas-Chacoff L, Bertrán C et al (2012) Heavy metals in the liver and muscle of Micropogonias manni fish from Budi Lake, Araucania Region, Chile: potential risk for humans. Environ Monit Assess 184:3141–3151. doi:10.1007/s10661-011-2178-4

    Article  CAS  Google Scholar 

  • Tekin-Özan S, Kir İ (2008) Seasonal variations of heavy metals in some organs of carp (Cyprinus carpio L., 1758) from Beyşehir Lake (Turkey). Environ Monit Assess 138:201–206. doi:10.1007/s10661-007-9765-4

    Article  Google Scholar 

  • Terra BF, Araújo FG, Calza CF et al (2007) Heavy metal in tissues of three fish species from different trophic levels in a tropical Brazilian river. Water Air Soil Pollut 187:275–284. doi:10.1007/s11270-007-9515-9

    Article  Google Scholar 

  • Triebskorn R, Köhler H-R, Honnen W et al (1997) Induction of heat shock proteins, changes in liver ultrastructure, and alterations of fish behavior: are these biomarkers related and are they useful to reflect the state of pollution in the field? J Aquat Ecosyst Stress Recover 6:57–73

    Article  CAS  Google Scholar 

  • Tuzen M (2009) Toxic and essential trace elemental contents in fish species from the Black Sea, Turkey. Food Chem Toxicol 47:1785–1790. doi:10.1016/j.fct.2009.04.029

    Article  CAS  Google Scholar 

  • Uluozlu OD, Tuzen M, Mendil D, Soylak M (2007) Trace metal content in nine species of fish from the Black and Aegean Seas, Turkey. Food Chem 104:835–840. doi:10.1016/j.foodchem.2007.01.003

    Article  CAS  Google Scholar 

  • USEPA (1999) National recommended water quality criteria—Correction: EPA 822/Z-99-001

  • Usero J, Izquierdo C, Morillo J, Gracia I (2004) Heavy metals in fish (Solea vulgaris, Anguilla anguilla and Liza aurata) from salt marshes on the southern Atlantic coast of Spain. Environ Int 29:949–956. doi:10.1016/S0160-4120(03)00061-8

    Article  CAS  Google Scholar 

  • Valle C, Bayle JT, Ramos AA (2003) Weight–length relationships for selected fish species of the western Mediterranean Sea. J Appl Ichthyol 19:261–262

    Article  Google Scholar 

  • WHO (1989) Heavy metals environmental aspects, environment health criteria. Geneva Switzerland

  • 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. doi:10.1016/j.envpol.2011.06.011

    Article  CAS  Google Scholar 

  • Yilmaz AB (2003) Levels of heavy metals (Fe, Cu, Ni, Cr, Pb, and Zn) in tissue of Mugil cephalus and Trachurus mediterraneus from Iskenderun Bay, Turkey. Environ Res 92:277–281. doi:10.1016/S0013-9351(02)00082-8

    Article  CAS  Google Scholar 

  • Yilmaz F (2009) The comparison of heavy metal concentrations (Cd, Cu, Mn, Pb, and Zn) in tissues of three economically important fish (Anguilla anguilla, Mugil cephalus and Oreochromis niloticus) inhabiting Köycegiz Lake-Mugla (Turkey). Turk J Sci Technol 4:7–15

    Google Scholar 

  • Yılmaz F, Ozdemir N, Demirak A, Tuna AL (2007) Heavy metal levels in two fish species Leuciscus cephalus and Lepomis gibbosus. Food Chem 100:830–835. doi:10.1016/j.foodchem.2005.09.020

    Article  Google Scholar 

  • Zaghden H, Kallel M, Louati A et al (2005) Hydrocarbons in surface sediments from the Sfax coastal zone, (Tunisia) Mediterranean Sea. Mar Pollut Bull 50:1287–1294. doi:10.1016/j.marpolbul.2005.04.045

    Article  CAS  Google Scholar 

  • Zhao S, Feng C, Quan W et al (2012) Role of living environments in the accumulation characteristics of heavy metals in fishes and crabs in the Yangtze River Estuary, China. Mar Pollut Bull 64:1163–1171. doi:10.1016/j.marpolbul.2012.03.023

    Article  CAS  Google Scholar 

  • Zhou F, Guo H, Hao Z (2007) Spatial distribution of heavy metals in Hong Kong’s marine sediments and their human impacts: a GIS-based chemometric approach. Mar Pollut Bull 54:1372–1384. doi:10.1016/j.marpolbul.2007.05.017

    Article  CAS  Google Scholar 

  • Zhuang P, Li Z, McBride MB et al (2013) Health risk assessment for consumption of fish originating from ponds near Dabaoshan mine, South China. Environ Sci Pollut Res 20:5844–5854. doi:10.1007/s11356-013-1606-0

    Article  CAS  Google Scholar 

  • Zubcov E, Zubcov N, Ene A, Biletchi L (2012) Assessment of copper and zinc levels in fish from freshwater ecosystems of Moldova. Environ Sci Pollut Res 19:2238–2247. doi:10.1007/s11356-011-0728-5

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the research unit of Biodiversity and Aquatic Ecosystems UR/11ES72 Research Unit, Department of Life Sciences Research, Sfax Faculty of Sciences, University of Sfax.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zohra Ben Salem.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ben Salem, Z., Ayadi, H. Heavy metal accumulation in Diplodus annularis, Liza aurata, and Solea vulgaris relevant to their concentration in water and sediment from the southwestern Mediterranean (coast of Sfax). Environ Sci Pollut Res 23, 13895–13906 (2016). https://doi.org/10.1007/s11356-016-6531-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-6531-6

Keywords

Navigation