Skip to main content
SpringerLink
Log in

Bioaccumulation of Lead, Calcium and Strontium and their Relationships in the Octopus Octopus vulgaris

  • Published:
Water, Air, and Soil Pollution Aims and scope Submit manuscript

Abstract

Octopuses (Octopus vulgaris) landed from commercial fishing were sampled and the concentrations of lead, calcium and strontium, in digestive gland, branchial heart, gills, mantle and arms, were determined using PIXE (particle-induced X-ray emission). Lead was detected in all tissues, although not in samples from all animals analysed. Female octopuses accumulated more lead in digestive gland than did males. The digestive gland index, an indicator of nutritional status, showed a negative correlation with lead concentration in both sexes. There were positive correlations between the concentration of lead and those of calcium and strontium in digestive gland and a negative correlation between lead and calcium in branchial heart tissue. Concentrations of calcium in arms were lower in autumn and spring than in winter and summer. Lead content increased with increasing body weight and mantle length so we can conclude that lead continues to accumulate during the animal’s life. Concentrations of lead in two samples were higher than the maximum legally permitted concentration of lead in food.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amiard, J.: 1988, ‘Les mecanimes de transfer des elements metaliques dans la chaine alimentaires aboutissant à lħuitre et à la moule, mollusques filtreurs, formes chimiques de stokage, consequences ecotoxicologiques’, Oceanus 14, 283–287.

    CAS  Google Scholar 

  • Armstrong, C. and Palti, Y.: 1991, ‘Potassium channel block by internal calcium and strontium’, J. Gen. Physiol. 97, 627–638.

    Article  CAS  PubMed  Google Scholar 

  • Baker, P. and Singh, R.: 1982, ‘Metabolism and transport of strontium in giant axons of Loligo’, J. Physiol. London 330, 373–392.

    CAS  PubMed  Google Scholar 

  • Barreiros, M., Pinheiro, T., Araújo, M., Costa, M., Palha, M. and Silva, R.: 2001, ‘Quality assurance of X-ray spectrometry for chemical analysis’, Spectrochim. Acta B 56, 2095–2106.

    Article  Google Scholar 

  • Barton, J., Conrad, M., Harrison, L. and Nuby, S.: 1978, ‘Effects of calcium on the absorption and retention of lead’, J. Lab. Clin. Med. 91, 366–376.

    CAS  PubMed  Google Scholar 

  • Becker, P.: 2000, ‘Concentration of chlorinated hydrocarbons and heavy metals in Alaska Arctic marine mammals’, Mar. Pollut. Bull. 40, 819–829.

    CAS  Google Scholar 

  • Biemann, M. and Piatkowski, U.: 2001, ‘Amounts and composition of trace elements in the statoliths of loliginid squids: Reflection of environmental conditions?’, International Council for the Exploration of the Sea CM 2001/K:05.

  • Blanchier, B. and Boucaud-Camou, E.: 1980, ‘Contenu lipidique de la glande digestive de Sepia officinalis à maturité sexuelle’, Haliotis 10, 1–20.

    Google Scholar 

  • Buffle, J.: 1994, ‘The ecological role of aquatic organic and inorganic components, deduced from their nature, circulation and interactions’, in Environmental Chemistry Inorganic Pollutants – a Course on Risk Assessment of Metals Compounds and Other Inorganics, European Environmental Research Organization, pp. 23–26.

  • Bustamante, P., Caurant, F., Fowler, S. W. and Miramand, P.: 1998, ‘Cephalopods as a vector for the transfer of cadmium to top marine predators in the north-east Atlantic Ocean’, Sci. Total Environ. 220, 71–80.

    CAS  PubMed  Google Scholar 

  • Costa, M., Barreiros, M., Carvalho, M. and Queralt, I.: 1999, ‘Multi-element characterization of estuarine sediments and waters’, X-Ray Spectrom. 28, 410–413.

    CAS  Google Scholar 

  • Domouhtsidou, G. and Dimitriadis, V.: 2000, ‘Ultrastrutural localization of heavy metals (Hg, Ag, Pb, and Cu) in gills and digestive gland of mussels, Mytilus galloprovinciallis (L.)’, Arch. Environ. Contam. Toxicol. 38, 472–478.

    CAS  PubMed  Google Scholar 

  • Dosi, A.: 2000, ‘Heavy metals in blubber and skin of Mediterranean monk seal, Monachus monachus from Greek waters’, PhD Thesis, University of Bangor, 85 pp.

  • Duc, M., Kaminsky, P. and Klein, M.: 1994, ‘Intoxication par plomb et ses sels’, Encycl. Méd. Chir. Paris. Toxicologie-Pathologie professionelle, 16-007, 10 pp.

  • Falandysz, J.: 1988, ‘Trace metals in squid Illex argentinus’, Z. Lebensm. Unters. For. 187, 359–361.

    CAS  Google Scholar 

  • Fullmer, C.: 1992, ‘Intestinal interactions of lead and calcium’, Neurotoxicology 13, 799–807.

    CAS  PubMed  Google Scholar 

  • Galdies, Ch. and Axiak, V.: 1992, ‘The fate of lead in a benthic bivalve (Venus verrucosa)’, MAP Tech. Rep. Ser. 69, 135–141.

    Google Scholar 

  • Goodman-Lowe, G., Carpenter, J., Atkinson, S. and Ako, H.: 1999, ‘Nutrient, fatty acid, amino acid and mineral analysis of natural prey of the Hawaiian monk seal, Monachus schauinslandi’, Comput. Biochem. Phys. A 123, 137–146.

    CAS  Google Scholar 

  • Gončalves, J.: 1993, ‘Octopus vulgaris Cuvier, 1797 (polvo comum): Sinopse da biologia e exploračão’, Provas de Aptidão Pedagógica e Científica, Universidade dos Ačores, 447 pp.

  • González, A., Guerra, A., Pascual, S. and Briand, P.: 1998, ‘Vulcanoptus hydrothermalis gen. Et sp. Nov. (Mollusca, Cephalopoda): An octopod from a deep–sea hydrothermal vent site’, Cah. Biol. Mar. 39, 169–184.

    Google Scholar 

  • Guerra, A.: 1975, ‘Determinación de las diferentes fases del desarrollo sexual de Octopus vulgaris Lamarck, mediante un índice de madurez’, Invest. Pesq. 39, 397–416.

    Google Scholar 

  • Hanlon, R., Bidwell, J. and Tait, R.: 1989, ‘Strontium is required for statolith development and thus normal swimming behaviour of hatchling cephalopods’, J. Exp. Biol. 141, 187–195.

    CAS  PubMed  Google Scholar 

  • Ichihashi, H., Kohno, H., Kannan, K., Tsumura, A. and Yamasaki, S.: 2001a, ‘Multielemental analysis of purpleback flying squid using high resolution inductively coupled plasma-mass spectrometry (HR ICP-MS)’, Environ. Sci. Technol. 35, 3103–3108.

    CAS  Google Scholar 

  • Ichihashi, H., Nakamura, Y., Kannan, K., Tsumura, A. and Yamasaki, S.: 2001b, ‘Multi-elemental concentration in tissues of Japanese common squid (Todarodes pacificus)’, Arch. Environ. Contam. Toxicol. 41, 483–490.

    CAS  Google Scholar 

  • Iriato, P., Santovito, G., Cassini, A., Piccinni, E. and Albergoni, V.: 2003, ‘Metal accumulation and binding protein induction in Mytilus galloprovincialis, Scapharca inaequivalvis, and Tapes philippinarum from the Lagoon of Venice’, Arch. Environ. Contam. Toxicol. 44, 476–484.

    PubMed  Google Scholar 

  • Kerper, L. and Hinkle, P.: 1997, ‘Cellular uptake of lead is activated by depletion of intracellular calcium stores’, J. Biol. Chem. 272, 8346–8352.

    CAS  PubMed  Google Scholar 

  • Law, R., Fileman, C., Hopkins, A., Baker, R., Harwood, J., Jackson, D., Kennedy, S., Martin, A. and Morris, R.: 1991, ‘Concentrations of trace metals in the livers of marine mammals (seals, porpoises and dolphins) from waters around the British Isles’, Mar. Pollut. Bull. 22, 183–191.

    CAS  Google Scholar 

  • MAFF 1998, ‘Concentrations of metals and other elements in marine fish and shellfish’, Food Surveill. Informat. Sheet 151, 1–13.

    Google Scholar 

  • Mangold, K. and Bidder, A.: 1989, ‘Láppareil digestif et la digestion’, in K. Mangold (ed.), P.P. Grassé (Series ed.), Céphalopodes, Tome V, Traité de Zoologie Anatomie, Systématique, Biologie, Masson, Paris, pp. 321–373.

  • Mangold, K., Bidder, A. and Portmann, A.: 1989, ‘Structures cutanées’, in K. Mangold (ed.), P.P. Grassé (Series ed.), Céphalopodes. Tome V. Traité de Zoologie Anatomie, Systématique, Biologie, Masson, Paris, pp. 121–162.

  • Marigomez, I., Angulo, E. and Moya, J.: 1986, ‘Copper treatment of the digestive gland of the slug, Arion ater L. 1. Bioassay conduction and histochemical analysis’, Biol. Environ. Contam. Toxicol. 36, 600–607.

    CAS  Google Scholar 

  • Miramand, P. and 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’, Mar. Biol. 114, 407–414.

    CAS  Google Scholar 

  • NAS: 1991, Seafood Safety, National Academy of Science, Washington, 452 pp.

    Google Scholar 

  • NAS: 1993, Measuring Lead Exposure in Infants, Children, and Other Sensitive Populations, National Academy of Science, Washington, 356 pp.

    Google Scholar 

  • NAS: 2000, Mineral Tolerance of Domestic Animals, National Academy Press, 3rd edn., Washington, 577 pp.

    Google Scholar 

  • Pounds, J.: 1984, ‘Effect of lead intoxication on calcium homeostasis and calcium-mediated cell function: A review’, Neurotoxicology 5, 295–331.

    CAS  PubMed  Google Scholar 

  • Quetglas, A., Alemany, F., Carbonell, A., Merella, P. and Sánchez, P.: 1998, ‘Biology and fishery of Octopus vulgaris Cuvier, 1797, caught by trawlers in Mallorca (Balearic Sea, Western Mediterranean)’, Fish. Res. 36, 237–249.

    Google Scholar 

  • Regoli, F.: 1998, ‘Trace metals and antioxidant enzymes in gills and digestive gland of the Mediterranean mussel Mytilus gallopronvincialis’, Arch. Environ. Contam. Toxicol. 34, 48–63.

    CAS  PubMed  Google Scholar 

  • Regoli, F. and Orlando, E.: 1993, ‘Mytilus gallopronvicialis as a bioindicator of lead pollution: Biological variables and cellular responses’, Sci. Total Environ., Supplement 1993, 1283–1293.

    Google Scholar 

  • Reico, A., Marigomez, J., Angula, E. and Moya, J.: 1988, ‘Zinc treatment of the digestive gland of the slug Arion ater (L.) 1. Cellular distribuition of zinc and calcium’, Biol. Environ. Contam. Toxicol. 41, 858–864.

    Google Scholar 

  • Reis, M. and Alves, L.: 1992, ‘DATTPIXE, a computer package for TTPIXE data analysis’, Nucl. Instrum. Meth. B 68, 300–304.

    Google Scholar 

  • Rius, R., Govoni, S. and Trabucchi, M.: 1986, ‘Regional modification of brain calcium antagonist binding after in vivo chronic lead exposure’, Toxicology 40, 191–197.

    CAS  PubMed  Google Scholar 

  • Ruelas-Inzunza, J., Soto, L. A. and Paez-Osuna, F.: 2003. ‘Heavy-metal accumulation in the hydrothermal vent clam Vesicomya gigas from Guaymas basin, Gulf of California’, Deep-Sea Res. Pt 1 50, 757–761.

    CAS  Google Scholar 

  • Santos, M., Pierce, G., Boyle, P., Reid, R., Ross, H., Patterson, I., Kinze, C., Tougaard, S., Lick, R., Piatkowski, U. and Hernández-García, V.: 1999, ‘Stomach contents of sperm whales Physeter macrocephalus stranded in the North Sea 1990–1996’, Mar. Ecol. Prog. Ser. 183, 281–294.

    Google Scholar 

  • Santos, M., Clarke, M. and Pierce, G.: 2001a, ‘Assessing the importance of cephalopods in diets of marine mammals and other top predators: Problems and solutions’, Fish. Res. 52, 121–139.

    Google Scholar 

  • Santos, M., Pierce, G., Reid, R., Patterson, I., Ross, H. and Mente, E.: 2001b, ‘Stomach contents of bottlenose dolphins (Tursiops truncatus) in Scottish waters’, J. Mar. Biol. Assoc. U.K. 81, 873–878.

    Google Scholar 

  • Santos, M., Pierce, G., Smeenk, C., Addink, M., Kinze, C., Tougaard, S. and Herman, J.: 2001c, ‘Stomach contents of northern bottlenose whales Hyperoodon ampullatus stranded in the North Sea’, J. Mar. Biol. Assoc. U.K. 81, 143–150.

    Google Scholar 

  • Seixas, S.: 1995, ‘Efeitos da Acumulačão de chumbo em pós-larvas de amêijoa boa (Ruditapes decussatus L.)’ Tese de Mestrado em Estudos Marinhos e Costeiros, Universidade do Algarve, 88 pp.

  • Seixas, S., Bustamante, P. and Pierce, G. J.: in press a, ‘Accumulation of mercury in the tissues of the common octopus Octopus vulgaris (L.) in two localities on the Portuguese coast’, Sci. Total Environ. (in press).

  • Seixas, S., Bustamante, P. and Pierce, G.J.: in press b, ‘Interannual patterns of variation in concentrations of trace elements in arms of Octopus vulgaris’ Chemosphere (in press).

  • Seixas, S., Pinheiro, T. and Sousa Reis, C.: 2002, ‘Lead in octopus (Octopus vulgaris) in Portugal: A preliminary study’, Biol. Mar. Sci. 71, 1091–1093.

    Google Scholar 

  • Silva, L., Sobrino, I. and Ramos, F.: 2002, ‘Reproductive biology of the common octopus, Octopus vulgaris Cuvier, 1797 (Cephalopoda: Octopodidae) in the Gulf of Cádiz (SW Spain)’, Biol. Mar. Sci. 71, 837–850.

    Google Scholar 

  • Sukhanov, B., Korolev, A., Marninchuk, A. and Merzliakova, N.: 1990, ‘Experimental study of the protective role of calcium in lead poisoning’, Gigiena i Sanitariya 12, 47–49.

    Google Scholar 

  • Sydeman, W. and Jarman, W.: 1998, ‘Trace metals in seabirds, Steller sea lion, and forage fish and zooplankton from Central California’, Mar. Pollut. Bull. 36, 828–832.

    CAS  Google Scholar 

  • Van Espen, P., Janssens, K. and Swentens, I.: 1986, AXIL X-ray Analysis Software-Users Manual, Camberra Packard, Benelux.

    Google Scholar 

  • Wells, M. and Smith, P.: 1987, ‘The performance of the octopus circulatory system: A triumph of engineering over design’, Experientia 43, 487–499.

    Google Scholar 

  • WHO: 1995, ‘Inorganic Lead’ Enviromental Health Criteria 165. World Health Organisation, Geneva, 206 pp.

    Google Scholar 

  • WHO: 2000, ‘Lead’ WHO Food Additives Series 44. World Health Organization, Geneva, 39 pp.

    Google Scholar 

  • Yatsu, A., Mochioka, N., Morishita, K. and Toh, H.: 1998, ‘Strontium/calcium ratios in statoliths of the neon flying squid, Ommastrephes bartrami (Cephalopoda), in North Pacific Ocean’, Mar. Biol. 131, 275–282.

    CAS  Google Scholar 

  • Zumholz, K., Piatkowski, U. and Hansteen, T.: 2004, ‘Trace element distributions in cuttlefish (Sepia officinalis) statoliths in response to a manipulated environment’, International Council for the Exploration of the Sea CM 2004 CC:38.

Download references

Author information

Authors and Affiliations

  1. Universidade Aberta, Rua Escola Politecnica, 147, 1269-001, Lisboa, Portugal

    Sónia Seixas & Graham Pierce

Authors
  1. Sónia Seixas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Graham Pierce
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sónia Seixas.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Seixas, S., Pierce, G. Bioaccumulation of Lead, Calcium and Strontium and their Relationships in the Octopus Octopus vulgaris. Water Air Soil Pollut 163, 137–152 (2005). https://doi.org/10.1007/s11270-005-0007-5

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11270-005-0007-5

Keywords

Search

Navigation