Fine structure of the respiratory lamellae of teleostean gills

Summary

The blood-water pathway in respiratory lamellae of teleostean gills consists of an epithelial layer one or two cells thick, a basal lamina and a thin layer of cytoplasm which lines the blood lacunae. This layer of cytoplasm is formed by flange-like extensions of the pillar cells. The resulting location of the pillar cell perikarya between the surfaces of the blood lacunae is probably of paramount importance for maintenance of the flattened form of the lamellae.

Collagenous bundles traverse the pillar cells within tubes formed by infolding of the cellular surface. These bundles, which are oriented normal to the flattened aspect of the lamellae, no doubt provide further protection against distension or collapse of the blood spaces. A compartment filled with collagenous tissue is interposed between the basal lamina and the lining layer of the lacunae in some of the species studied.

Regulation of blood flow to the respiratory surfaces is thought to result in part from contraction of the pillar cells. This contractility presumably resides in tracts of filaments which course through the cytoplasm of the pillar cells parallel to the collagenous bundles. Since nervous tissue has not been demonstrated within the gill lamellae it is possible that contraction of the pillar cells is under some form of hormonal control, although existence of local control mechanisms (e.g. self-stimulation of the cells as a result of anoxia) is not excluded.

Within the limited number of species studied, the structure of the blood-water pathway does not appear to be correlated with the characteristics of the normal habitat of a particular species.

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

References

  1. Altschul, R.: Endothelium. Its development, morphology, function, and pathology. New York: Macmillan 1954.

    Google Scholar 

  2. Baker, P. J.: Fine structure and morphogenic movements in the gastrula of the treefrog, Hyla regula. J. biophys. biochem. Cytol. 24, 95–116 (1965).

    Google Scholar 

  3. Bennett, H. S., and J. H. Luft: s-Collidine as a basis for buffering fixatives. J. biophys. biochem. Cytol. 6, 113–114 (1959).

    Google Scholar 

  4. , and J. C. Hampton: Morphological classifications of vertebrate blood capillaries. Amer. J. Physiol. 196, 381–390 (1959).

    Google Scholar 

  5. Bevelander, G.: A comparative study of the branchial epithelium in fishes with special reference to extrarenal excretion. J. Morph. 57, 335–347 (1935).

    Google Scholar 

  6. Clemens, W. A., and G. V. Wilby: Fishes of the Pacific coast of Canada. Canada Fish. Res. Bd., Bull. 68, (second ed.). Ottawa 1961.

  7. Cloney, R. A.: Cytoplasmic movements and cell movements: epidermal cells during ascidian metamorphosis. J. Ultrastruct. Res. 14, 300–328 (1966).

    Google Scholar 

  8. Edds, M. V., and P. R. Sweeny: Chemical and morphological differentiation of the basement lamella. In: Synthesis of molecular and cellular structure (D. Rudnick, ed.), p. 111–138. New York: Ronald Press 1961.

    Google Scholar 

  9. Fawcett, D. W.: Physiologically significant specializations of the cell surface. Circulation 26, 1105–1125 (1962).

    Google Scholar 

  10. Hama, K.: On the existence of filamentous structures in endothelial cells of the amphibian capillary. Anat. Rec. 139, 437–441 (1961).

    Google Scholar 

  11. Hay, E. D., and J.-P. Revel: Autoradiographic studies of the origin of the basement lamella in Ambystoma. Develop. Biol. 7, 152–168 (1963).

    Google Scholar 

  12. Hughes, G. M.: Fish respiratory homeostasis. Symp. Soc. exp. Biol. 18, 81–107 (1964).

    Google Scholar 

  13. : The dimensions of fish gills in relation to their function. J. exp. Biol. 45, 177–195 (1966).

    Google Scholar 

  14. , and A. V. Grimstone: The fine structure of the secondary lamellae of the gills of Gadus pollachius. Quart. J. micr. Sci. 106, 343–353 (1965).

    Google Scholar 

  15. and G. Shelton: Respiratory mechanism and their nervous control in fish. Advanc. comp. Physiol. Biochem. 1, 275–364 (1962).

    Google Scholar 

  16. Kallman, F., and C. Grobstein: Source of collagen at epithelio-mesenchymal interfaces during inductive interaction. Develop. Biol. 11, 169–183 (1965).

    Google Scholar 

  17. Kurtz, S. M., and J. D. Feldman: Experimental studies on the formation of the glomerular basement membrane. J. Ultrastruct. Res. 6, 19–27 (1962).

    Google Scholar 

  18. Leeson, C. R., and T. S. Leeson: Histology. Philadelphia: W. B. Saunders Co. 1966.

    Google Scholar 

  19. Luft, J. H.: The use of acrolein as a fixative for light and electron microscopy. Anat. Rec. 133, 305 (1959).

    Google Scholar 

  20. : Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).

    Google Scholar 

  21. : Fine structure of the vascular wall. In: Evolution of the artherosclerotic plaque (R. J. Jones, ed.), p. 3–14. Chicago: University of Chicago Press 1964.

    Google Scholar 

  22. McBride, J.: Personal communication (1965).

  23. Millonig, G.: Advantages of a phosphate buffer for OsO4 solutions in fixation. J. appl. Physiol. 32, 1637 (1961).

    Google Scholar 

  24. Moe, R. E.: Fine structure of the reticulum and sinuses of lymph nodes. Amer. J. Anat. 112, 311–335 (1963).

    Google Scholar 

  25. Nelson, O. E.: Comparative embryology of the vertebrates. New York: Blakiston Co. 1953.

    Google Scholar 

  26. Newstead, J. D.: Fine structure of respiratory lamellae of teleost gills. Anat. Rec. 153, 393 (1965).

    Google Scholar 

  27. Plehn, M.: Zum feineren Bau der Fischkeime. Zool. Anz. 24, 439–443 (1901).

    Google Scholar 

  28. Revel, J. -P., and E. D. Hay: Fine structure of the developing chick cornea. Anat. Rec. 151, 492–493 (1965).

    Google Scholar 

  29. Reynolds, E. S.: The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963).

    Google Scholar 

  30. Rhodin, J. A. G.: Structure of the gills of the marine fish pollack (Pollachius virens). Anat. Rec. 148, 420 (1964).

    Google Scholar 

  31. - Personal communication (1965).

  32. Richardson, K. C., L. Jarett, and E. H. Finke: Embedding in exposy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960).

    Google Scholar 

  33. Ruud, J. T.: The ice fish. Scientific Amer. 213, 108–114 (1965).

    Google Scholar 

  34. Sabatini, D. D., K. Bensch and R. J. Barrnett: Cytochemistry and electron microscopy. The preservation of cellular ultrastructure and enzymatic activity by aldehyde fixation. J. Cell Biol. 17, 17–58 (1963).

    Google Scholar 

  35. Schulz, H.: Die submikroskopische Morphologie des Kiemenepithels. In: Fourth Int. Conf. Electron Microscopy, Berlin 1958, vol. 2, p. 421–426 (1960).

    Google Scholar 

  36. : Some remarks on the submicroscopic anatomy and pathology of the blood-air pathway in the lung. In: Pulmonary structure and function. A. V. S. de Reuck and M. O'Connor, eds.), p. 205–214. London: Churchill 1962.

    Google Scholar 

  37. Steen, J. B., and A. Kruysse: The respiratory function of teleostean gills. Comp. Biochem. Physiol. 12, 127–142 (1964).

    Google Scholar 

Download references

Author information

Affiliations

Authors

Additional information

This work was performed during the tenure of a post doctoral traineeship under USPHS Grant 5 T 1 GM-136 to the Department of Biological Structure, University of Washington.

Particular thanks are due Dr. John H. Luft of the University of Washington for his advice and criticism while this work was in progress and to Drs. Douglas Kelly, James Koehler and Daniel Szollosi for critical assistance with the manuscipt.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Newstead, J.D. Fine structure of the respiratory lamellae of teleostean gills. Zeitschrift für Zellforschung 79, 396–428 (1967). https://doi.org/10.1007/BF00335484

Download citation

Keywords

  • Local Control
  • Control Mechanism
  • Basal Lamina
  • Nervous Tissue
  • Epithelial Layer