Skip to main content

Advertisement

Log in

Metal and metallothionein concentrations in Paracentrotus lividus from Amvrakikos gulf (Ionian Sea-Greece)

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

Concentrations of Cd, Cu, Cr, Ni, Zn, Fe and metallothioneins (MTs) were measured in the gonads of Paracentrotus lividus from Amvrakikos gulf (Ionian Sea, Greece). Three natural populations were selected; two of them, growing inside the gulf (Agios Thomas and Koronisia), presented higher density and smaller body size than the population living in a coastal area just outside the gulf (Mytikas). Metal and MT levels were not elevated, with the exception of Zn, showing high values related to the reproduction stage of the sea urchins. Significant geographical variations were recorded in the concentrations of Cu, Zn, Cd, Cr and MTs. The highest mean and maximum values of Cu, Zn and MTs were recorded in Agios Thomas while Cd and Cr were higher in Mytikas population. Copper, Zn, Fe and MT concentrations were negatively correlated to the sea urchin body size, while a positive concentration-size relationship was observed for Cd. Although all studied populations grow in a low metal level marine environment, urchins with smaller body size living in a food limited marine environment showed higher gonadosomatic index, metal concentrations and MT levels in their gonads (Agios Thomas and Koronisia) than larger specimens growing in a food unlimited area (Mytikas).

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
Fig. 4

Similar content being viewed by others

References

  • Ahn, I. Y., Ji, J., & Park, H. (2009). Metal accumulation in sea urchins and their kelp diet in an Arctic fjord (Kongsfjorden, Svalbard). Marine Pollution Bulletin, 58, 1571–1577.

    Article  CAS  Google Scholar 

  • Amiard, J. C., Amiard-Triquet, C., Barka, S., Pellerin, J., & Rainbow, P. S. (2006). Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquatic Toxicology, 76, 160–202.

    Article  CAS  Google Scholar 

  • Andral, B., Stanisiere, J. Y., Sauzade, D., Damier, E., Thebault, H., Galgani, F., et al. (2004). Monitoring chemical contamination levels in the Mediterranean based on the use of mussel caging. Marine Pollution Bulletin, 49, 704–712.

    Article  CAS  Google Scholar 

  • Aspholm, O., & Hylland, K. (1998). Metallothionein in green sea urchins (Strongylocentrotus droebachiensis) as a biomarker for metal exposure. Marine Environmental Research, 46, 537–540.

    Article  CAS  Google Scholar 

  • Attig, H., Dagnino, A., Negri, A., Jebali, J., Boussetta, H., Viarengo, A., et al. (2010). Uptake and biochemical responses of mussels Mytilus galloprovincialis exposed to sublethal nickel concentrations. Ecotoxicology and Environmental Safety, 73, 1712–1719.

    Article  CAS  Google Scholar 

  • Azad, A. K., Pearce, C. M., & McKinley, R. S. (2011). Effects of diet and temperature on ingestion, absorption, assimilation, gonad yield, and gonad quality of the purple sea urchin (Strongylocentrotus purpuratus). Aquaculture, 317, 187–196.

    Article  Google Scholar 

  • Barka, S., Pavillon, J. F., & Amiard, J. C. (2001). Influence of different essential and non-essential metals on MTLP levels in the copepod Tigriopus brevicornis. Comparative Biochemistry and Physiology - Part C: Toxicology & Pharmacology, 128, 479–493.

    Article  CAS  Google Scholar 

  • Bayed, A., Quiniou, F., Benrha, A., & Guillou, M. (2005). The Paracentrotus lividus populations from the northern Moroccan Atlantic coast: growth, reproduction and health condition. Journal of the Marine Biological Association of the United Kingdom, 85, 999–1007.

    Article  Google Scholar 

  • Bielmyer, G. K., Jarvis, T. A., Harper, B. T., Butler, B., Rice, L., Ryan, S., et al. (2012). Metal accumulation from dietary exposure in the sea urchin, Strongylocentrotus droebachiensis. Archives of Environmental Contamination and Toxicology, 63, 86–94.

    Article  CAS  Google Scholar 

  • Boyden, C. R. (1977). Effect of size upon metal content of shellfish. Journal of the Marine Biological Association of the United Kingdom, 57, 675–714.

    Article  CAS  Google Scholar 

  • Catsiki, V. A., & Strogyloudi, E. (1999). Survey of metal levels in common fish species from Greek waters. Science of the Total Environment, 237(238), 387–400.

    Article  Google Scholar 

  • Catsiki, V. A., Papathanassiou, E., & Bei, F. (1991). Heavy metal levels in characteristic benthic flora and fauna in the central Aegean Sea. Marine Pollution Bulletin, 22, 566–569.

    Article  CAS  Google Scholar 

  • Chou, C. L., Haya, K., Paon, L. A., & Moffatt, J. D. (2003). Metals in the green sea urchin (Strongylocentrotus droebrachiensis) as an indicator for the near-field effects of chemical wastes from salmon aquaculture sites in New Brunswick, Canada. Bulletin of Environmental Contamination and Toxicology, 70, 948–956.

    Article  CAS  Google Scholar 

  • Gonzalez, H., Pomares, M., Ramirez, M., & Torres, I. (1999). Heavy metals in organisms and sediments from the discharge zone of the submarine sewage outfall of Havana City, Cuba. Marine Pollution Bulletin, 38, 1048–1051.

    Article  CAS  Google Scholar 

  • Guillou, M., Quiniou, F., Huart, B., & Pagano, G. (2000). Comparison of embryonic development and metal contamination in several populations of the sea urchin Sphaerechinus granularis (Lamarck) exposed to anthropogenic pollution. Archives of Environmental Contamination and Toxicology, 39, 337–344.

    Article  CAS  Google Scholar 

  • Hernández, O. D., Gutiérrez, Á. J., González-Weller, D., Lozano, G., Melón, E. G., Rubio, C., et al. (2010). Accumulation of toxic metals (Pb and Cd) in the sea urchin Diadema aff. antillarum Philippi, 1845, in an oceanic island (Tenerife, Canary Islands). Environmental Toxicology, 25, 227–233.

    Article  Google Scholar 

  • Jenkins, K. D., Brown, D. A., Oshida, P. S., & Perkins, E. M. (1982). Cytosolic metal distribution as an indicator of toxicity in sea urchins from the Southern California bight. Marine Pollution Bulletin, 13, 413–421.

    Article  CAS  Google Scholar 

  • Karageorgis, A. P. (2007). Geochemical study of sediments from the Αmvrakikos gulf lagoon complex, Greece. Transitional Waters Bulletin, 3, 3–8.

    Google Scholar 

  • Karageorgis, P. A., Krasakopoulou, E., Pappas, G., Papageorgiou, A., & Taxiarchi, M. (2006). Geochemical characteristics of surface sediments from the lagoons of Amvrakikos Gulf, Ionian Sea. In Proceedings of the 8th Hellenic Symposium in Oceanography and Fisheries (pp. 793–799). Thessaloniki, Greece.

  • Kountoura, K., & Zacharias, I. (2011). Temporal and spatial distribution of hypoxic/seasonal anoxic zone in Amvrakikos gulf, western Greece. Estuarine, Coastal and Shelf Science, 94, 123–128.

    Article  CAS  Google Scholar 

  • McCarron, E., Burnell, G., & Mouzakitis, G. (2009). Growth assessment on three size classes of the purple sea urchin Paracentrotus lividus using continuous and intermittent feeding regimes. Aquaculture, 288, 83–91.

    Article  Google Scholar 

  • Mouneyrac, C., Amiard, J. C., Amiard-Triquet, C., Cottier, A., Rainbow, P. S., & Smith, B. D. (2002). Partitioning of accumulated trace metals in the talitrid amphipod crustacean Orchestia gammarellus: a cautionary tale on the use of metallothionein-like proteins as biomarkers. Aquatic Toxicology, 57, 225–242.

    Article  CAS  Google Scholar 

  • Nedelec, H. (1983). Sur un nouvel indice de réplétion pour les oursins régulier. Rapport Commission International pour l’exploration scientifique de la Mer Mediterranee, 28, 149–151.

  • Ouréns, R., Fernández, L., & Freire, J. (2011). Geographic, population, and seasonal patterns in the reproductive parameters of the sea urchin Paracentrotus lividus. Marine Biology, 158, 793–804.

    Article  Google Scholar 

  • Panayotidis, P., & Florou, H. (1994). Copper, cadmium and iron in marine organisms in a eutrophic estuarine area (Amvrakikos gulf, Ionian Sea, Greece). Toxicological and Environmental Chemistry, 45, 211–219.

    Article  CAS  Google Scholar 

  • Pancucci-Papadopoulou, M. A. (1996). Ecology and distribution of Greek seas echinoderm: study of the dwarfism of the echinoid Paracentrotus lividus (Lamark) as an ecological adaption, PhD Thesis, University of Athens, Greece, 243 pp.

  • Pancucci-Papadopoulou, M. A., & Panayotidis, P. (1994). Impact of eutrophication on sea urchin populations of the Amvrakikos gulf (Ionian Sea, Greece). In G. P Gabrielides (Ed.), Final reports on research projects dealing with eutrophication problems, MAP Technical Reports Series, no. 78 (pp. 75–90). Athens (Greece): UNEP.

  • Poulos, S. E., Kapsimalis, V., Tziavos, C., & Paramana, T. (2008). Origin and distribution of surface sediments and human impacts on recent sedimentary processes. The case of the Amvrakikos Gulf (NE Ionian Sea). Continental Shelf Research, 28, 2736–2745.

    Article  Google Scholar 

  • Ramsar (1975). The Ramsar Convention on Wetlands. www.ramsar.org.

  • Riek, R., Prêcheur, B., Wang, Y., MacKay, E. A., Wider, G., Güntert, P., et al. (1999). NMR structure of the sea urchin (Strongylocentrotus purpuratus) metallothionein MTA. Journal of Molecular Biology, 291, 417–428.

    Article  CAS  Google Scholar 

  • Rizzo, C., Cammarata, M., Di Carlo, M., Pancucci, A., & Parrinello, N. (2009). RAPD profiles distinguish Paracentrotus lividus populations living in a stressing environment (Amvrakikos gulf, Greece). Russian Journal of Genetics, 45, 499–503.

    Article  CAS  Google Scholar 

  • Sadiq, M., Mian, A. A., & Saji, A. P. (1996). Metal bioaccumulation by sea urchin (Echinometra mathaei) from the Saudi coastal areas of Arabian gulf: 2. Cadmium, copper, chromium, barium, calcium, and strontium. Bulletin of Environmental Contamination and Toxicology, 57, 964–971.

    Article  CAS  Google Scholar 

  • Scoullos, M., Dassenakis, M., & Zeri, C. (1996). Trace metal behaviour during summer in a stratified Mediterranean system: the Louros estuary (Greece). Water, Air, & Soil Pollution, 88, 269–295.

    Article  CAS  Google Scholar 

  • Scudiero, R., Capasso, C., De Prisco, P. P., Capasso, A., Filosa, S., & Parisi, E. (1994). Metal-binding proteins in eggs of various sea urchin species. Cell Biology International, 18, 47–53.

    Article  CAS  Google Scholar 

  • Scudiero, R., Capasso, C., Del Vecchio-Blanco, F., Savino, G., Capasso, A., Parente, A., et al. (1995). Isolation and primary structure determination of a metallothionein from Paracentrotus lividus (echinodermata, echinoidea). Comparative Biochemistry and Physiology. Part B, Biochemistry and Molecular Biology, 111, 329–336.

    Article  CAS  Google Scholar 

  • Scudiero, R., Capasso, C., Carginale, V., Riggio, M., Capasso, A., Ciaramella, M., et al. (1997). PCR amplification and cloning of metallothionein complementary DNAs in temperate and Antarctic sea urchin characterized by a large difference in egg metallothionein content. Cellular and Molecular Life Sciences, 53, 472–477.

    Article  CAS  Google Scholar 

  • Sellem, F., & Guillou, M. (2007). Reproductive biology of Paracentrotus lividus (Echinodermata: Echinoidea) in two contrasting habitats of northern Tunisia (southeast Mediterranean). Journal of the Marine Biological Association of the United Kingdom, 87, 763–767.

    Article  Google Scholar 

  • Storelli, M. M., Storelli, A., & Marcotrigiano, G. O. (2001). Heavy metals in the aquatic environment of the Southern Adriatic Sea, Italy: macroalgae, sediments and benthic species. Environment International, 26, 505–509.

    Article  CAS  Google Scholar 

  • Strogyloudi, E., & Catsiki, V. A. (1999). Seasonal variations in mussel metal concentrations from two coastal areas of the Amvrakikos gulf. In Proceedings of the 6th Greek-Cyprus Chemistry Symposium (pp. 300–304). Rhodes, Greece.

  • Strogyloudi, E., Angelidis, M. O., Christides, A., & Papathanassiou, E. (2012). Metal concentrations and metallothionein levels in Mytilus galloprovincialis from Elefsis bay (Saronikos gulf, Greece). Environmental Monitoring and Assessment, 184, 7189–7205.

    Article  CAS  Google Scholar 

  • Tenuzzo, B. A., Zaccarelli, N., & Dini, L. (2012). The reproductive cycle of the commercial sea urchin Paracentrotus lividus (Lamark, 1816) (Echinodermata: Echinoidea) in the Ionian Sea. Italian Journal of Zoology, 79, 200–211.

    Article  Google Scholar 

  • Tsangaris, C., Cotou, E., Papathanassiou, E., & Nicolaidou, A. (2010). Assessment of contaminant impacts in a semi-enclosed estuary (Amvrakikos Gulf, NW Greece): bioenergetics and biochemical biomarkers in mussels. Environmental Monitoring and Assessment, 161, 259–269.

    Article  CAS  Google Scholar 

  • UniProtKB (2013). http://www.uniprot.org/uniprot/. Accessed early June 2013.

  • Unuma, T., Ikeda, K., Yamano, K., Moriyama, A., & Ohta, H. (2007). Zinc-binding property of the major yolk protein in the sea urchin—implications of its role as a zinc transporter for gametogenesis. FEBS Journal, 274, 4985–4998.

    Article  CAS  Google Scholar 

  • Vareli, K., Zarali, E., Zacharioudakis, G. S. A., Vagenas, G., Varelis, V., Pilidis, G., et al. (2012). Microcystin producing cyanobacterial communities in Amvrakikos Gulf (Mediterranean Sea, NW Greece) and toxin accumulation in mussels (Mytilus galloprovincialis). Harmful Algae, 15, 109–118.

    Article  CAS  Google Scholar 

  • Vassilopoulou, V., Papaconstantinou, C., & Caragitsou E. (2002). Life history adaptations of a demersal fish species in a nutrient rich embayment of the Ionian Sea (Greece). US EPA 600/R02/097, 107–119.

  • 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 molluscs. Marine Environmental Research, 44, 69–84.

    Article  CAS  Google Scholar 

  • Warnau, M., Ledent, G., Temara, A., Alva, V., Jangoux, M., & Dubois, P. (1995). Allometry of heavy metal bioconcentration in the echinoid Paracentrotus lividus. Archives of Environmental Contamination and Toxicology, 29, 393–399.

    Article  CAS  Google Scholar 

  • Warnau, M., Teyssié, J. L., & Fowler, S. W. (1997). Cadmium bioconcentration in the echinoid Paracentrotus lividus: influence of the cadmium concentration in seawater. Marine Environmental Research, 43, 303–314.

    Article  CAS  Google Scholar 

  • Warnau, M., Biondo, R., Temara, A., Bouquegneau, J. M., Jangoux, M., & Dubois, P. (1998). Distribution of heavy metals in the echinoid Paracentrotus lividus from the Mediterranean Posidonia oceanica ecosystem: seasonal and geographical variations. Journal of Sea Research, 39, 267–280.

    Article  CAS  Google Scholar 

  • Zenetos, A., Christianidis, S., Pancucci, M.-A., Simboura, N., & Tziavos, C. (1997). Oceanologic study of an open coastal area in the Ionian Sea with emphasis on its benthic fauna and some zoogeographical remarks. Oceanologica Acta, 20(2), 437–451.

    Google Scholar 

  • Zorita, I., Strogyloudi, E., Buxens, A., Mazon, L. I., Papathanassiou, E., Soto, M., et al. (2005). Application of two SH-based methods for metallothionein determination in mussels and intercalibration of the spectrophotometric method: laboratory and field studies in the Mediterranean Sea. Biomarkers, 10, 342–359.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr V.A. Catsiki for providing laboratory facilities for metal analysis. Financial support was provided by the Hellenic Centre for Marine Research (HCMR).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Evangelia Strogyloudi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Strogyloudi, E., Pancucci–Papadopoulou, MA. & Papadopoulos, G.L. Metal and metallothionein concentrations in Paracentrotus lividus from Amvrakikos gulf (Ionian Sea-Greece). Environ Monit Assess 186, 5489–5499 (2014). https://doi.org/10.1007/s10661-014-3798-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-014-3798-2

Keywords

Navigation