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Interspecific and geographical variations of trace metal concentrations in cephalopods from Tunisian waters

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Abstract

The concentrations of six metals (Ag, Cd, Cu, Hg, Pb, and Zn) were investigated and compared in three tissues (arms, digestive gland, and mantle) of three cephalopod species from the Tunisian waters: the common octopus (Octopus vulgaris), the common cuttlefish (Sepia officinalis), and the European squid (Loligo vulgaris). Whatever the species or the sites, the digestive gland displayed the highest concentrations of Ag, Cd, Cu, Pb, and Zn, highlighting its major role in their bioaccumulation and detoxification. This is also true for Hg but only for the digestive gland of O. vulgaris. Muscle from the arms and the mantle contained thus relatively low trace metal concentrations except for Hg in L. vulgaris and S. officinalis. Geographic comparison of metal concentrations in Tunisian cephalopods from three locations indicates that higher concentrations of Ag, Pb, and Hg were observed in cephalopods from northern and eastern coasts, whereas the highest Cd levels were detected in the southeastern, reflecting different conditions of exposure. Comparing the trace element concentrations between species, Ag, Cd, Cu, Hg, and Zn concentrations were the highest in the digestive gland of octopuses. This may be related to the differences in ecological features and swimming behavior among different cephalopod species. Effects of length and sex on metal levels were also considered, indicating a limited influence of sex on metal concentration.

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References

  • Ayas, D., & Ozogul, Y. (2011). The effects of season and sex in the metal levels of mature common cuttlefish (Sepia officinalis) in Mersin Bay, Northeastern Mediterranean. Journal of Food Science, 76, 121–124.

    Article  Google Scholar 

  • Banni, M., Jebali, J., Daubeze, M., Clerandau, C., Guerbej, H., Narbonne, J. F., et al. (2005). Monitoring pollution in Tunisian coasts: Application of a classification scale based on biochemical markers. Biomarkers, 10, 105–116.

    Article  CAS  Google Scholar 

  • Banni, M., Dondero, F., Jebali, J., Guerbej, H., Boussetta, H., & Viarengo, A. (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.

    Article  CAS  Google Scholar 

  • Barghigiani, C., D'Ulivo, A., Zamboni, R., & Lampugnani, L. (1993). Interaction between selenium and cadmium in Eledone cirrhosa of the northern Tyrrhenian Sea. Marine Pollution Bulletin, 26, 212–216.

    Article  CAS  Google Scholar 

  • Barghigiani, C., Ristori, T., Biagi, F., & De Ranieri, S. (2000). Size related mercury accumulations in edible marine species from an area of the Northern Tyrrhenian Sea. Water, Air, and Soil Pollution, 124, 169–176.

    Article  CAS  Google Scholar 

  • Bloom, N. S. (1992). On the chemical form of mercury in edible fish and marine invertebrate tissue. Canadian Journal of Fisheries and Aquatic Sciences, 49, 1010–1017.

    Article  CAS  Google Scholar 

  • Boujelben, B. (1998). Dosage de métaux lourds (Plomb, Cadmium, Cuivre, Zinc) dans les poissons péchés dans la région de Sfax. Doctorat en médecine vétérinaire. Faculté de médecine vétérinaire de Sidi Thabet. 79pp.

  • Boyle, P. R. (1990). Cephalopod biology in the fisheries context. Fisheries Research, 8, 303–321.

    Article  Google Scholar 

  • Boyle, P., & Rodhouse, P. (2005). Cephalopods: Ecology and fisheries. Oxford: Blackwell Publishing.

  • Bustamante, P., Caurant, F., Fowler, S. W., & Miramand, P. (1998a). Cephalopods as a vector for the transfer of cadmium to top marine predators in the north-east Atlantic Ocean. Science of The Total Environment, 220, 71–80.

    Article  CAS  Google Scholar 

  • Bustamante, P., Cherel, Y., Caurant, F., & Miramand, P. (1998b). Cadmium, copper and zinc in octopuses from Kerguelen Islands, Southern Indian Ocean. Polar Biology, 19, 264–271.

    Article  Google Scholar 

  • Bustamante, P., Cosson, R. P., Gallien, I., Caurant, F., & Miramand, P. (2002a). Cadmium detoxification processes in the digestive gland of cephalopods in relation to accumulated cadmium concentrations. Marine Environmental Research, 53, 227–241.

    Article  CAS  Google Scholar 

  • Bustamante, P., Teyssié, J. L., Fowler, S. W., Cotret, O., Danis, B., Miramand, P., et al. (2002b). Biokinetics of zinc and cadmium accumulation and depuration at different stages in the life cycle of the cuttlefish Sepia officinalis. Marine Ecology-Progress Series, 231, 167–177.

    Article  CAS  Google Scholar 

  • Bustamante, P., Lahaye, V., Durnez, C., Churlaud, C., & Caurant, F. (2006a). Total and organic Hg concentrations in cephalopods from the North Eastern Atlantic waters: Influence of geographical origin and feeding ecology. Science of The Total Environment, 368, 585–596.

    Article  CAS  Google Scholar 

  • Bustamante, P., Bertrand, M., Boucaud-Camou, E., & Miramand, P. (2006b). Subcellular distribution of Ag, Cd, Co, Cu, Fe, Mn, Pb, and Zn in the digestive gland of the common cuttlefish Sepia officinalis. Journal of Shellfish Research, 25, 987–993.

    Google Scholar 

  • Bustamante, P., Gonzalez, A., Rocha, F., Miramand, P., & Guerra, A. (2008). Metal and metalloid concentrations in the giant squid Architeuthis dux from Iberian waters. Marine Environmental Research, 66, 278–287.

    Article  CAS  Google Scholar 

  • Canli, M., Kalay, M., & Ay, Ö. (2001). Metal (Cd, Pb, Cu, Zn, Fe, Cr, Ni) concentrations in tissues of a fish Sardina pilchardus and a prawn Peaenus japonicus from three stations on the Mediterranean Sea. Bulletin of Environmental Contamination and Toxicology, 67, 75–82.

    CAS  Google Scholar 

  • CGP. (1996). Annuaire des statistiques des pêches en Tunisie. Tunisie: Ministère de l’agriculture.

    Google Scholar 

  • Chouvelon, T., Spitz, J., Cherel, Y., Caurant, F., Sirmel, R., Mendez-Fernandez, P., et al. (2011) Inter-specific and ontogenic differences in δ13C and δ15N values and Hg and Cd concentrations in cephalopods. Marine Ecology-Progress Series, 433, 107–120.

    Article  CAS  Google Scholar 

  • Cossa, D., Thibaud, Y., Roméo, M., Gnassia-Barelli, M. (1990). Le mercure en milieu marin. Biogéochimie et écotoxicologie. Rapport scientifiques et techniques de l'IFREMER, Brest.

  • R Development Core Team (2010). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, www.R-project.org.

  • Dorneles, P. R., Lailson-Brito, J., dos Santos, R. A., Silva da Costa, P. A., Malm, O., Azevedo, A. F., et al. (2007). Cephalopods and cetaceans as indicators of offshore bioavailability of cadmium off Central South Brazil Bight. Environmental Pollution, 148, 352–359.

    Article  CAS  Google Scholar 

  • El Ati-Hellal, M., Hedhili, A., Hellal, F., Boujlel, K., Dachraoui, M., Bousnina, M., et al. (2005). Lead and cadmium concentrations in seawater and algae of the Tunisian coast (Vol. 82). Tunis, TUNISIE: Institut Pasteur de Tunis.

    Google Scholar 

  • FAO (2007). Fisheries and Aquaculture Information and Statistics Service, Fisheries commodities production and trade 1976–2005. Food and Agriculture Organization of the United Nations, FISHSTAT Plus-Universal software for fishery statistical time series [online or CD-ROM]. Available at: http://www.fao.org/fi/statist/FISOFT/FISHPLUS.asp.

  • Hamza-Chaffai, A., Cosson, R. P., 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. Comparative Biochemistry and Physiology. Part C, Pharmacology, Toxicology and Endocrinology, 111, 329–341.

    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. Archives of Environmental Contamination and Toxicology, 33, 53–62.

    Article  CAS  Google Scholar 

  • Hamza-Chaffai, A., Pellerin, J., & Amiard, J. C. (2003). Health assessment of a marine bivalve Ruditapes decussatus from the Gulf of Gabès (Tunisia). Environment International, 28, 609–617.

    Article  CAS  Google Scholar 

  • Jackson, G., Wotherspoon, S., & Jackson, C. (2007). Temporal life history plasticity of the Southern Ocean squid Todarodes filippovae from waters off Tasmania, Australia. Marine Biology, 150, 575–584.

    Article  Google Scholar 

  • Jebali, J., Banni, M., de Almeida, E. A., & Boussetta, H. (2007). Oxidative DNA damage levels and catalase activity in the clam Ruditapes decussatus as pollution biomarkers of Tunisian marine environment. Environmental Monitoring Assessment, 124, 195–200.

    Article  CAS  Google Scholar 

  • Joiris, C. R., Holsbeek, L., & Moatmeri, N. L. (1999). Total and methylmercury in sardines Sardinella aurita and Sardina pilchardus from Tunisia. Marine Pollution Bulletin, 38, 188–192.

    Article  CAS  Google Scholar 

  • Jozet-Alves, C., Modéran, J., & Dickel, L. (2008). Sex differences in spatial cognition in an invertebrate: The cuttlefish. Proceedings of the Royal Society B: Biological Sciences, 275, 2049–2054.

    Article  Google Scholar 

  • Kojadinovic, J., Jackson, C. H., Cherel, Y., Jackson, G. D., & Bustamante, P. (2011). Multi-elemental concentrations in the tissues of the oceanic squid Todarodes filippovae from Tasmania and the southern Indian Ocean. Ecotoxicology and Environmental Safety, 74, 1238–1249.

    Article  CAS  Google Scholar 

  • Lacoue-Labarthe, T., Warnau, M., Oberhänsli, F., Teyssié, J.-L., Jeffree, R., & Bustamante, P. (2008). First experiments on the maternal transfer of metals in the cuttlefish Sepia officinalis. Marine Pollution Bulletin, 57, 826–831.

    Article  CAS  Google Scholar 

  • Lacoue-Labarthe, T., Martin, S., Oberhansli, F., Teyssie, J. L., Markich, S., Ross, J., et al. (2009a). Effects of increased pCO(2) and temperature on trace element (Ag, Cd and Zn) bioaccumulation in the eggs of the common cuttlefish, Sepia officinalis. Biogeosciences, 6, 2561–2573.

    Article  CAS  Google Scholar 

  • Lacoue-Labarthe, T., Warnau, M., Oberhänsli, F., Teyssié, J.-L., & Bustamante, P. (2009b). Bioaccumulation of inorganic Hg by the juvenile cuttlefish Sepia officinalis exposed to 203Hg radiolabelled seawater and food. Aquatic Biology, 6, 91–98.

    Article  Google Scholar 

  • Lourenço, H. M., Anacleto, P., Afonso, C., Ferraria, V., Martins, M. F., Carvalho, M. L., et al. (2009). Elemental composition of cephalopods from Portuguese continental waters. Food Chemistry, 113, 1146–1153.

    Article  Google Scholar 

  • Manso, M., Carvalho, M. L., & Nunes, M. L. (2007). Characterization of essential and toxic elements in cephalopod tissues by EDXRF and AAS. X-Ray Spectrometry, 36, 413–418.

    Article  CAS  Google Scholar 

  • Martin, J. H., & Flegal, A. R. (1975). High copper concentrations in squid livers in association with elevated levels of silver, cadmium, and zinc. Marine Biology, 30, 51–55.

    Article  CAS  Google Scholar 

  • McQuaid, C. D. (1994). Feeding behaviour and selection of bivalve prey by Octopus vulgaris Cuvier. Journal of Experimental Marine Biology and Ecology, 177, 187–202.

    Article  Google Scholar 

  • Metian, M., Warnau, M., Chouvelon, T., Pedraza, F., Rodriguez y Baena, A. M., Bustamante P. (2013) Trace element bioaccumulation in reef fish from New Caledonia: Influence of trophic groups and risk assessment for consumers. Marine Environmental Research, 87–88C: 26–36.

  • Miramand, P., & Bentley, D. (1992). Concentration and distribution of heavy metals in tissues of two cephalopods, Eledone cirrhosa and Sepia officinalis, from the French coast of the English Channel. Marine Biology, 114, 407–414.

    Article  CAS  Google Scholar 

  • Miramand, P., & Guary, J. C. (1980). High concentrations of some heavy metals in tissues of the Mediterranean octopus. Bulletin of Environmental Contamination and Toxicology, 24, 783–788.

    Article  CAS  Google Scholar 

  • Miramand, P., Bustamante, P., Bentley, D., & Kouéta, N. (2006). Variation of heavy metal concentrations (Ag, Cd, Co, Cu, Fe, Pb, V, and Zn) during the life cycle of the common cuttlefish Sepia officinalis. Science of The Total Environment, 361, 132–143.

    Article  CAS  Google Scholar 

  • Monteiro, L. R., Porteiro, F. M., & Gonçalves, J. M. (1992). Inter- and intra-specific variation of mercury levels in muscle of cephalopods from the Azores. Arquipélago, 10, 13–22.

    Google Scholar 

  • Napoleão, P., Pinheiro, T., & Sousa Reis, C. (2005). Elemental characterization of tissues of Octopus vulgaris along the Portuguese coast. Science of The Total Environment, 345, 41–49.

    Article  Google Scholar 

  • Nessim, R. B., & Riad, R. G. (2003). Bioaccumulation of heavy metals in Octopus vulgaris from coastal waters of Alexandria (Eastern Mediterranean) (19th ed., p. 7). Abingdon, UK: Taylor & Francis.

    Google Scholar 

  • Pereira, P., Raimundo, J., Vale, C., & Kadar, E. (2009). Metal concentrations in digestive gland and mantle of Sepia officinalis from two coastal lagoons of Portugal. Science of The Total Environment, 407, 1080–1088.

    Article  CAS  Google Scholar 

  • Piatkowski, U., Pierce, G. J., & Morais da Cunha, M. (2001). Impact of cephalopods in the food chain and their interaction with the environment and fisheries: An overview. Fisheries Research, 52, 5–10.

    Article  Google Scholar 

  • Pierce, G. J., Boyle, P. R., Hastie, L. C., & Santos, M. B. (1994). Diets of squid Loligo forbesi and Loligo vulgaris in the northeast Atlantic. Fisheries Research, 21, 149–163.

    Article  Google Scholar 

  • Pierce, G. J., Stowasser, G., Hastie, L. C., & Bustamante, P. (2008). Geographic, seasonal and ontogenetic variation in cadmium and mercury concentrations in squid (Cephalopoda: Teuthoidea) from UK waters. Ecotoxicology and Environmental Safety, 70, 422–432.

    Article  CAS  Google Scholar 

  • Raimundo, J., Caetano, M., & Vale, C. (2004). Geographical variation and partition of metals in tissues of Octopus vulgaris along the Portuguese coast. Science of The Total Environment, 325, 71–81.

    Article  CAS  Google Scholar 

  • Raimundo, J., Pereira, P., Vale, C., & Caetano, M. (2005). Fe, Zn, Cu and Cd concentrations in the digestive gland and muscle tissues of Octopus vulgaris and Sepia officinalis from two coastal areas in Portugal. Ciencias Marinas, 31, 243–251.

    CAS  Google Scholar 

  • Raimundo, J., Costa, P. M., Vale, C., Costa, M. H., & Moura, I. (2010). Metallothioneins and trace elements in digestive gland, gills, kidney and gonads of Octopus vulgaris. Comparative Biochemistry and Physiology. C, 152, 139–146.

    CAS  Google Scholar 

  • Renzoni, A., Bacci, E., Falciai, L. (1973). Mercury concentration in the water, sediments and fauna of an area of the Tyrrhenian coast. Revue Internationale Océanographie. Méditerannée 31–32.

  • Rossi, A., Pellegrini, D., Belcari, P., & Barghigiani, C. (1993). Mercury in Eledone cirrhosa from the Northern Tyrrhenian Sea: Contents and relations with life cycle. Marine Pollution Bulletin, 26, 683–686.

    Article  CAS  Google Scholar 

  • Seixas, S., Bustamante, P., & Pierce, G. (2005). Accumulation of mercury in the tissues of the common octopus Octopus vulgaris (L.) in two localities on the Portuguese coast. Science of The Total Environment, 340, 113–122.

    Article  CAS  Google Scholar 

  • Smaoui-Damak, W., Hamza-Chaffai, A., Berthet, B., & Amiard, J. C. (2003). Preliminary study of the clam Ruditapes decussatus exposed in situ to metal contamination and originating from the Gulf of Gabès, Tunisia. Bulletin Environmental Contamination Toxicology, 71, 961–970.

    Article  CAS  Google Scholar 

  • Stoepler, M., Berhnard, M., Backhaus, F., & Schulte, E. (1979). Comparative studies on trace metal levels in marine biota: I. Mercury in marine organisms from Western Italian coast, the Strait of Gibraltar and the North Sea. Science of the Total Environment, 13, 209–223.

    Article  Google Scholar 

  • Storelli, M. M., & Marcotrigiano, G. O. (1999). Cadmium and total mercury in some cephalopods from the South Adriatic Sea (Italy). Food Additives and Contaminants, 16, 261–265.

    Article  CAS  Google Scholar 

  • Villanueva, R., Koueta, N., Riba, J., & Boucaud-Camou, E. (2002). Growth and proteolytic activity of Octopus vulgaris paralarvae with different food rations during first feeding, using Artemia nauplii and compound diets. Aquaculture, 205, 269–286.

    Article  CAS  Google Scholar 

  • Zuur, A. F., Ieno, E. N., & Smith, G. M. (2007). Analysing ecological data. New York: Springer.

    Google Scholar 

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Acknowledgments

MR benefits from a PhD fellowship provided by the Tunisian Ministry of Higher Education and Scientific Research. MM is Nippon Foundation Senior Nereus Fellow at the Stockholm Resilience Centre. We are grateful to C. Churlaud for her help in the Hg analyses. This study has been financially supported by the laboratory LIENSs and the CPER (Contrat de Projet Etat Région).

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Authors and Affiliations

  1. Faculty of Sciences of Tunis, University Campus, Tunis, 2092, Tunisia

    Moncef Rjeibi

  2. Littoral Environnement et Sociétés (LIENSs), UMRi 7266 CNRS-Université de La Rochelle, 2 rue Olympe de Gouges, 17000, La Rochelle, France

    Marc Metian, Thierry Guyot & Paco Bustamante

  3. Unité de recherche d’Ecophysiologie et de Procédés Agroalimentaires UR11-ES44, Institut Supérieur de Biotechnologie de Sidi Thabet (ISBST), Université La Manouba, BiotechPole Sidi Thabet, Sidi Thabet, CP 2020, Tunisia

    Moncef Rjeibi, Tarek Hajji & Rafika Ben Chaouacha-Chékir

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  1. Moncef Rjeibi
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Rjeibi, M., Metian, M., Hajji, T. et al. Interspecific and geographical variations of trace metal concentrations in cephalopods from Tunisian waters. Environ Monit Assess 186, 3767–3783 (2014). https://doi.org/10.1007/s10661-014-3656-2

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