Skip to main content

Transport of cadmium and other metals in the blood of the bivalve mollusc Mercenaria mercenaria

Abstract

The distribution of metals (Ba, Cr, Cu, Fe, Mn, Ni and Zn) in the blood plasma and the circulating hemocytes was determined for a eulamellibranch bivalve, the quahog Mercenaria mercenaria (L.), collected from a relatively clean site at Falmouth, Massachusetts, USA. Whole blood volume was an exponential function of quahog length (Y=5.71×10-5 X3.0678; Y=ml of whole blood; X=mm length). Of this volume, 1.2±0.3% (\((\bar X \pm {\rm{SD)}}\)) was attributable to blood cells. Total metal content (μg metal, or μg metal normalized per g of whole blood) was much higher in blood plasma than in hemocytes. In quahogs exposed in the laboratory to 100 ppb 109Cd, 93.0% of the total accumulated blood Cd was in the plasma rather than in the circulating hemocytes (7.0%), irrespective of the length of exposure (1 h to 31 d). Less than 5% of the plasma Cd was either Cd2+, small inorganic Cd complexes or bound to organic molecules with a molecular weight smaller than 1 000. Cadmium was primarily bound to high molecular weight protein(s) (>60 000 daltons) within the plasma. This plasma protein-Cd complex has a low affinity constant (approximately 104 M -1), indicating non-specific Cd binding, although the capacity for Cd-binding in the plasma is great (as high as 200 μg Cd per ml of plasma). Blood plasma may be far more important in metal transport than has previously been realized.

This is a preview of subscription content, access via your institution.

Literature cited

  1. Ballan-Dufrancais, C., A.-Y. Jeantel, C. Feghali and S. Halpern: Physiological features of heavy metal storage in bivalve digestive cells and amoebocytes: EPMA and factor analysis of correspondences. Biol. Cell 53, 283–292 (1985)

    Google Scholar 

  2. Carmichael, N. G., K. S. Squibb, D. W. Engel and B. A. Fowler: Metals in the molluscan kidney: uptake and subcellular distribution of 109Cd, 54Mn and 65Zn by the clam Mercenaria mercenaria. Comp. Biochem. Physiol. 65A, 203–206 (1980)

    Google Scholar 

  3. Faguet, G. B.: Number of receptor sites from Scatchard and Klotz graphs: complementary approaches. J. Cell. Biochem. 31, 243–250 (1986)

    Google Scholar 

  4. Feng, S. Y.: Heart rate and leucocyte circulation in Crassostrea virginica (Gmelin). Biol. Bull. mar. biol. Lab., Woods Hole 128, 198–210 (1965)

    Google Scholar 

  5. Foley, D. A. and T. C. Cheng: Morphology, hematologic parameters, and behavior of hemolymph cells of the quahog clam, Mercenaria mercenaria. Biol. Bull. mar. biol. Lab., Woods Hole 146, 343–356 (1974)

    Google Scholar 

  6. George, S. G. and J. M. Frazier: Some aspects of the relationship between tolerance to heavy metal pollution and metabolism of Cd, Cu and Zn in oysters. Thalassia jugosl. 18, 203–219 (1982)

    Google Scholar 

  7. George, S. G. and B. J. S. Pirie: Metabolism of zinc in the mussel, Mytilus edulis (L.): a combined ultrastructural and biochemical study. J. mar. biol. Ass. U.K. 60, 575–590 (1980)

    Google Scholar 

  8. George, S. G., B. J. S. Pirie, A. R. Cheyne, T. L. Coombs and P. T. Grant: Detoxication of metals by marine bivalves: an ultrastructural study of the compartmentation of copper and zinc in the oyster Ostrea edulis. Mar. Biol. 45, 147–156 (1978)

    Google Scholar 

  9. George, S. G., B. J. S. Pirie and J. M. Frazier: Effects of cadmium exposure on metal-containing amoebocytes of the oyster Ostrea edulis. Mar. Biol. 76, 63–66 (1983)

    Google Scholar 

  10. Guthans, S. L. and W. T. Morgan: The interaction of zinc, nickel and cadmium with serum albumen and histidine-rich glycoprotein assessed by equilibrium dialysis and immunoadsorbent chromatography. Arch. Biochem. Biophys. 218, 320–328 (1982)

    Google Scholar 

  11. Hartree, E. F.: Determination of protein. A modification of the Lowry method that gives a linear photometric response. Anal. Biochem. 48, 422–427 (1972)

    Google Scholar 

  12. Lowry, O. H., N. J. Rosebrough, A. L. Farr and R. J. Randall: Protein measurement with the Folin-Phenol reagent. J. Biol. Chem. 193, 265–275 (1951)

    Google Scholar 

  13. Lytton, D. G., A. R. Eastgate and N. J. Ashbolt: Digital mapping of metal-bearing amoebocytes in tissue sections of the Pacific oyster by scanning microphotometry. J. Microsc. 138, 1–14 (1985)

    Google Scholar 

  14. Mart, L., H. Rützel, P. Klahre, L. Sipos, U. Platzek, P. Valenta and H. W. Nürnberg: Comparative studies on the distribution of heavy metals in the oceans and coastal waters. Sci. total Envir. 26, 1–17 (1982)

    Google Scholar 

  15. Marsh, M. E. and R. L. Sass: Calcium-binding phosphoprotein particles in the extrapallial fluid and innermost shell lamella of clams. J. exp. Zool. 226, 193–203 (1983)

    Google Scholar 

  16. Marsh, M. E. and R. L. Sass: Distribution and characterization of mineral-binding phosphoprotein particles in bivalvia. J. exp. Zool. 234, 237–242 (1985)

    Google Scholar 

  17. Martin, A. W., F. M. Harrison, M. J. Huston and D. M. Stewart: The blood volumes of some representative molluscs. J. exp. Biol. 35, 260–279 (1958)

    Google Scholar 

  18. Martoja, R. and J.-L. Martin: Detoxification of cadmium by the oyster Crassostrea gigas (Mollusc, Bivalve). Characterization of a cadmium-binding protein in the zinc and copper-containing amoebocytes. C. R. Acad. Sci. Paris 300, 549–554 (1985)

    Google Scholar 

  19. Miramand, P. and P. Germain: Seawater uptake, sediment transfer and histo-autoradiographic study of plutonium (239Pu) and americium (241Am) in the edible cockle Cerastoderma edule. Mar. Ecol. Prog. Ser. 22, 59–68 (1985)

    Google Scholar 

  20. Nieboer, E. and D. H. S. Richardson: The replacement of the nondescript term ‘heavy metals’ by a biologically and chemically significant classification of metal ions. Environ. Pollut. Bull. 3–26 (1980)

  21. Pirie, B. J. S., S. G. George, D. G. Lytton and J. D. Thompson: Metal-containing blood cells of oysters: ultrastructure, histochemistry and X-ray microanalysis. J. mar. biol. Ass. UK 64, 115–123 (1984)

    Google Scholar 

  22. Potts, W. T. W.: The rate of urine production of Anodonta cygnea. J. exp. Biol. 31, 614–617 (1954)

    Google Scholar 

  23. Prosser, C. L. and S. J. F. Weinstein: Comparison of blood volume in animals with open and with closed circulatory systems. Physiol. Zool. 23, 113–124 (1950)

    Google Scholar 

  24. Robinson, W. E., M. P. Morse, B. A. Penney, J. P. Kakareka and E. U. Meyhöfer: The eulamellibranch Mercenaria mercenaria (L.): a review and current data on metals accumulation and the internal transport of cadmium. In: Marine pollution and physiology: recent advances, pp 83–106. Ed. by F. J. Vernberg, F. P. Thurberg, A. Calabrese and W. B. Vernberg. Columbia, SC: University of South Carolina Press 1985

    Google Scholar 

  25. Robinson, W. E. and D. K. Ryan: Metal interactions within the kidney, gill, and digestive gland of the hard clam, Mercenaria mercenaria, following laboratory exposure to cadmium. Arch. envir. Contam. Toxicol. 15, 23–30 (1986)

    Google Scholar 

  26. Rudell, C. L. and D. W. Rains: The relationship between zinc, copper and the basophils of two crassostreid oysters, Crassostrea gigas and Crassostrea virginica. Comp. Biochem. Physiol. 51A, 565–591 (1975)

    Google Scholar 

  27. Thompson, R. J.: Blood chemistry, biochemical composition, and the annual reproductive cycle in the giant scallop, Placopecten magellanicus, from southeast Newfoundland. J. Fish. Res. Bd Can. 34, 2104–2116 (1977)

    Google Scholar 

  28. Thompson, R. J., C. J. Bayne, M. N. Moore and T. H. Carefoot: Haemolymph volume, changes in the biochemical composition of the blood and cytological responses of the digestive cells in Mytilus californianus Conrad, induced by nutritional, thermal and exposure stress. J. comp. Physiol. 127B, 287–298 (1978)

    Google Scholar 

  29. Thomson, J. D., B. J. S. Pirie and S. G. George: Cellular metal distribution in the Pacific oyster, Crassostrea gigas (Thun.) determined by quantitative X-ray microprobe analysis. J. exp. mar. Biol. Ecol. 85, 37–45 (1985)

    Google Scholar 

  30. Walsh, P. J., D. G. McDonald and C. E. Booth: Acid-base balance in the sea mussel, Mytilus edulis. II. Effects of hypoxia and airexposure on intracellular acid-base status. Mar. Biol. Lett. 5, 359–369 (1984)

    Google Scholar 

  31. Zatta, P.: Zinc transport in the haemolymph of Carcinus maenas (Crustacea: Decapoda). J. mar. biol. Ass. UK 64, 801–807 (1984)

    Google Scholar 

Download references

Author information

Affiliations

Authors

Additional information

Communicated by J. P. Grassle, Woods Hole

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Robinson, W.E., Ryan, D.K. Transport of cadmium and other metals in the blood of the bivalve mollusc Mercenaria mercenaria . Mar. Biol. 97, 101–109 (1988). https://doi.org/10.1007/BF00391250

Download citation

Keywords

  • Cadmium
  • Bivalve
  • Blood Volume
  • Blood Plasma
  • Total Metal