Skip to main content
Log in

The Accumulation of Lead and Mercury from Seawater and Their Depuration by Eggs of the Spotted Dogfish Scyliorhinus canicula (Chondrichthys)

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

Radiotracer experiments using 210Pb and 203Hg demonstrated that eggs of the spotted dogfish Scyliorhinus canicula absorbed lead and inorganic mercury directly from seawater over 21 days of experimental exposure, attaining total egg concentration factors (CFs) relative to water of approximately 400 for Pb and 180 for Hg, predominantly (≥98%) due to their accumulation by the collagenous egg case. The rates of accumulation of both Pb and Hg by the total egg were significantly (P < 0.0001) reduced by its increasing age since parturition, whereas only the rate of depuration of Pb was reduced (P < 0.0001) with increasing age; these effects indicate a declining chemical reactivity of the egg case that may be due to the continued tanning of the case following parturition. The egg case per se, attained average CFs of about 1,500 and 850 for Pb and Hg, respectively. Both Pb and Hg showed declining concentration gradients from the exterior to the interior membranes of the wall of the egg case; CFs for Pb declined from 3,500 to 2,000 and for Hg from 5,000 to 500. Comparison of concentrations in separate membranes also demonstrated significant (P ≤ 0.01) depurations of Hg from the external and internal membranes during the loss experiments. The presence of radiotracers of Pb and Hg in the internal components of the egg at the end of uptake phase, and prior to the opening of the apertures, confirmed the permeability of the egg case wall to them, consistent with their observed gradients in it. The average CFs for all embryos at the end of the uptake experiment were 34 and 44 for Pb and Hg, respectively, but were significantly (P < 0.001) enhanced for Hg by a factor of 6 in the older eggs. The accumulatory and kinetic characteristics of the egg-case may operate to optimize the exposure of embryos to Pb and Hg following episodic contaminant events in coastal habitats.

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

  • Ballard WW, Mellinger J, Lechenault H (1993) A series of normal stages for development of Scyliorhinus canicula, the lesser spotted dogfish (Chondrichthyes: Scyliorhinidae). J Exp Zool 267:318–336

    Article  Google Scholar 

  • Baxter DC, Frech W (1995) Speciation of lead in environmental and biological samples. Pure Appl Chem 67:615–648

    Article  CAS  Google Scholar 

  • Boening DW (2000) Ecological effects, transport, and fate of mercury: A general review. Chemosphere 40:1335–1351

    Article  CAS  Google Scholar 

  • Bone S E, Charette MA, Lamborg CH, Gonneea M E (2007) Has submarine groundwater discharge been overlooked as a source of mercury to coastal Waters. Environ Sci Technol 41:3090–3095

    Article  CAS  Google Scholar 

  • Brown PL, Haworth, A, Sharland SM, Tweed CJ (1991) HARPHRQ: An Extended Version of the Geochemical Code PHREEQE. Nirex Safety Studies Report 188. UK Atomic Energy Authority, Oxford

  • CCME (2003) Canadian Water Quality Guidelines for the Protection of Aquatic Life: Inorganic Mercury and Methylmercury. Canadian Council of Ministers of the Environment, Winnipeg

    Google Scholar 

  • Childs EA, Gaffke JN, Crawford DL (1973) Exposure of dogfish shark feti to mercury. Bull Environ Contam Toxicol 9(5):276–280

    Article  CAS  Google Scholar 

  • Ebinghaus R, Hintelmann H, Wilken RD (1994) Mercury cycling in surface waters and in the atmosphere: Species analysis for the investigation of transformation and transport properties of mercury. Fresenius J Anal Chem 350:21–29

    Article  CAS  Google Scholar 

  • Falck WE, Thomas JB, Read D (1996) CHEMVAL Thermodynamic Database. W.S. Atkins Environment, Surrey, UK

    Google Scholar 

  • GESAMP (2001) Protecting the Oceans from Land-based Activities. Land-based sources and activities affecting the quality and uses of the marine, coastal and associated freshwater environment. Rep Stud GESAMP No 71, 162 pp

  • Hamlett WC, Koob T J (1999) Female reproductive system. In: Hamlett WC (eds) The biology of elasmobranch fish. John Hopkins University Press, Baltimore, ch 15, pp 398–443

  • Hornsey DJ (1978) Permeability coefficients of the egg-case membrane of Scyliorhinus canicula L. Experientia 34:1596–1601

    Article  CAS  Google Scholar 

  • Jeffree RA, Warnau M, Oberhaensli F, Teyssie JL (2006a) Bioaccumulation from seawater of heavy metals and radionuclides by encased embryos of the spotted dogfish Scyliorhinus canicula. Mar Poll Bull 52:1278–1286

    Article  CAS  Google Scholar 

  • Jeffree R, Teyssie JL, Obershansli F (2006b) Distributions of cobalt-60, zinc-65 and selenium-75 in encased embryos of the spotted dogfish (S. canicula): comparison of absorption by maternal transfer and from seawater. Proc 15th Pacific Basin Nuclear Conf, 15–20 Oct. 2006, Sydney, pp 6

  • Jeffree RA, Warnau M, Teyssie JL, Markich SJ (2006c) Comparison of the bioaccumulation from seawater and depuration of heavy metals and radionuclides in the spotted dogfish Scyliorhinus canicula (Chondrichthys) and the turbot Psetta maxima (Actinopterygii: Teleostei). Sci Tot Environ 368:839–852

    Article  CAS  Google Scholar 

  • Jeffree RA, Oberhaensli F, Teyssie JL (2007) Accumulation and transport behaviour of 241americium, 60cobalt and 134cesium by eggs of the spotted dogfish Scyliorhinus canicula. Marine Pollution Bull 54:912–920

    Article  CAS  Google Scholar 

  • Knight DP, Feng D (1992) Formation of the dogfish egg capsule: a coextruded multilayer laminate. J Biomimet 1:151–175

    Google Scholar 

  • Knight DP, Feng D, Stewart M (1996) Structure and function of the selachian egg case. Biol Rev 71:81–111

    Article  Google Scholar 

  • Krishnan G (1959) Histochemical studies on the nature and formation of egg capsules of the shark Chiloscyllium griseum. Biol Bull 117:298–307

    Article  CAS  Google Scholar 

  • Koob TJ, Cox DL (1993) Stabilization and sclerotization of Raja erinacea egg capsule proteins. Environ Biol Fish 38(1–3):151–157

    Article  Google Scholar 

  • Markich SJ, Brown PL (1999) Thermochemical Data (log K) for Environmentally Relevant Elements. ANSTO/E735. Australian Nuclear Science and Technology Organisation, Sydney

    Google Scholar 

  • Mellinger J, Wrisez F, Alluchon-Gerard MJ (1986) Developmental Biology of an Oviparous Shark, Scyliorhinus canicula. Proc. Second Int Conf on Indo-Pacific Fishes, Uyeno T, Arai R, Taniuchi T, Matsuura K (eds.), Tokyo, pp 310–332

  • Millero F (2000) The Physical Chemistry of Natural Waters. Wiley, New York

    Google Scholar 

  • Nieboer E, Richardson DHS (1980) The replacement of the nondescript term ‘heavy metals’ by a biologically and chemically significant classification of metal ions. Environ Poll Series B 1:3–26

    Article  CAS  Google Scholar 

  • Pilson MEQ (1998) An Introduction to the Chemistry of the Sea. Prentice Hall, Upper Saddle River, New Jersey

    Google Scholar 

  • Powell KJ, Brown PL, Byrne RH, Gajda T, Hefter G, Sjöberg S, Wanner H (2004) Chemical speciation of Hg(II) with environmental ligands. Aust J Chem 57:993–1000

    Article  CAS  Google Scholar 

  • Ravichandran M (2004) Interactions between mercury and dissolved organic matter-a review. Chemosphere 55:319–331

    Article  CAS  Google Scholar 

  • Smith EB (2004) Basic Chemical Thermodynamics, 5th Ed. Imperial College Press, London

    Google Scholar 

  • Smith RM, Martell AE (2004) NIST Critically Selected Stability Constants of Metal Complexes Database, Version 8. National Institute of Standards and Technology, Gaithersberg

    Google Scholar 

  • Weis P, Weis JS (1991) The developmental toxicity of metals and metalloids in fish. In: Metal Ecotoxicology: Concepts and Applications. Advances in Trace Metal Research, Lewis, Chelsea, Michigan, pp 145–169

  • Wood L (2002) Sea fishes and invertebrates of the Mediterranean Sea. New Holland, London, p 128

    Google Scholar 

  • Wourms JP, Demski LS (1993) The reproduction and development of sharks, rays and ratfishes: introduction, history, overview and future prospects. Environ Biol Fish 38:7–21

    Article  Google Scholar 

Download references

Acknowledgments

The IAEA is grateful for the support provided to its Marine Environment Laboratories by the Government of the Principality of Monaco. Dr Scott Markich is thanked for the provision of results on chemical speciation modelling. Drs Scott Fowler and Fauzi Mantoura are thanked for their helpful comments on the manuscript. The comments by three anonymous referees improved the text.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. A. Jeffree.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jeffree, R.A., Oberhansli, F. & Teyssie, JL. The Accumulation of Lead and Mercury from Seawater and Their Depuration by Eggs of the Spotted Dogfish Scyliorhinus canicula (Chondrichthys). Arch Environ Contam Toxicol 55, 451–461 (2008). https://doi.org/10.1007/s00244-007-9103-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-007-9103-4

Keywords

Navigation