Ultrastructure of cephalopod chromatophore organs

  • Richard A. Cloney
  • Ernst Florey
Article

Summary

The chromatophore organs of Loligo opalescens are composed of five different types of cells: the chromatophore proper; radial muscle fibers; neuronal processes (axons); glial cells; and chromatophoral sheath cells.

The surface of a retracted chromatophore is extensively folded, but upon contraction of the radial muscle fibers it becomes flattened and the folds of the surface disappear. The cell membrane cannot be responsible for the elasticity of the chromatophore as claimed by earlier investigators.

The pigment granules are confined within a filamentous compartment (cytoelastic sacculus) throughout the cycle of expansion and retraction. The sacculus decreases in thickness during expansion and increases in thickness during retraction and does not become folded. The elastic properties of the chromatophore are attributed to the cytoelastic sacculus.

Primary infoldings of the chromatophore surface are anchored to the sacculus at points called focal haptosomes. The periphery of the sacculus attaches to the plasmalemma of the equatorial part of the chromatophore, opposite the area of attachment of the radial muscle fibers (myochromatophoral junction) by a zonular haptosome.

The regular, obliquely striated muscle fibers that expand the chromatophore are associated with axons and glial cell processes. Adjacent muscle fibers may be electrically coupled through close junctions. The entire chromatophore and the muscle fibers are surrounded by sheath cells.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Albini, G.: Sui movimenti dei cromatofori nei cefalopodi. Rend. Acad. Sci. fis. e mat. 24, 121–124 (1885).Google Scholar
  2. Behnke, O., and A. Forer: Evidence for four classes of microtubules in individual cells. J. Cell Sci. 2, 169–192 (1967).Google Scholar
  3. Blanchard, R.: A propos des chromatophores des Céphalopodes. C. R. Acad. Sci. (Paris) 113, 565–566 (1891).Google Scholar
  4. Boll, F.: Beiträge zur vergleichenden Histologie des Molluskentypus. Arch. mikr. Anat. 5 (Suppl.), 1–111 (1869).Google Scholar
  5. Bozler, E.: Über die Tätigkeit der einzelnen glatten Muskelfaser bei der Kontraktion. II. Mitt. Die Chromatophorenmuskeln der Cephalopoden. Z. vergl. Physiol. 7, 379–406 (1928).Google Scholar
  6. —: Weitere Untersuchungen zur Frage des Tonussubstrates. Z. vergl. Physiol. 8, 371–390 (1929).Google Scholar
  7. —: Über die Tätigkeit der einzelnen glatten Muskelfaser bei der Kontraktion. III. Mitt. Registrierung der Kontraktionen der Chromatophorenmuskelzellen von Cephalopoden. Z. vergl. Physiol. 13, 762–772 (1931).Google Scholar
  8. Brücke, E. V.: Vergleichende Bemerkungen über Farben und Farbwechsel bei Cephalopoden und bei den Chamaeleonen. S.-B. Akad. Wiss. Wien 8, 196–230 (1851).Google Scholar
  9. Bulger, R. E.: The shape of rat kidney tubular cells. Amer. J. Anat. 116, 237–256 (1965).Google Scholar
  10. Cate, J. Ten: Contribution à la question de l'innervation des chromatophores chez Octopus vulgaris. Arch. neerl. Physiol. 12, 568–599 (1928).Google Scholar
  11. Chiaje, S. delle: Memorie sulla storia e notomia degli animali senza vertebre del Regno di Napoli. 6, Mem. II (sui cefalopodi) Art. 2 (Cuticola), p. 63 (1829).Google Scholar
  12. Farquhar, M. G., and G. E. Palade: Junctional complexes in various epithelia. J. Cell Biol. 17, 375–412 (1963).Google Scholar
  13. Fawcett, D.: An atlas of fine structure. The cell, its organelles and inclusions. Philadelphia and London: W.B. Saunders Co. 1966.Google Scholar
  14. Florey, E.: Nervous control and spontaneous activity of the chromatophores of a cephalopod, Loligo opalescens. Comp. Biochem. Physiol. 18, 305–324 (1966).Google Scholar
  15. Fuchs, R.F.: Der Farbenwechsel und die chromatische Hautfunktion der Tiere. In: H. Winterstein, Handbuch der vergleichenden Physiologie, Bd. 3, S. 1189–1656 (1914).Google Scholar
  16. Girod, P.: Recherches sur la peau des céphalopodes. Arch. zool. exp. gen., II. ser. 1, 225–266 (1883).Google Scholar
  17. Graziadei, P.: The ultrastructure of motor nerve endings in the muscle of cephalopods. J. Ultrastruct. Res. 15, 1–13 (1966).Google Scholar
  18. Hanson, J., and J. Lowy: Structure and function of the contractile apparatus in the muscles of invertebrate animals. In: G. H. Bourne (ed.), Structure and function of muscle (1). New York: Academic Press 1960.Google Scholar
  19. Hofmann, F. B.: Histologische Untersuchungen über die Innervation der glatten und der ihr verwandten Muskulatur der Wirbeltiere und Mollusken. Arch. mikr. Anat. 70, 361–413 (1907a).Google Scholar
  20. —: Gibt es in der Muskulatur der Mollusken periphere, kontinuierlich leitende Nervennetze bei Abwesenheit von Ganglienzellen? I. Untersuchungen an Cephalopoden. Pflügers Arch. ges. Physiol. 118, 375–412 (1907b).Google Scholar
  21. —: Über einen peripheren Tonus der Cephalopoden-Chromatophoren und über ihre Beeinflussung durch Gifte. Pflügers Arch. ges. Physiol. 118, 413–451 (1907c).Google Scholar
  22. —: Chemische Reizung und Lähmung markloser Nerven und glatter Muskeln wirbelloser Tiere. Untersuchungen an den Chromatophoren der Kephalopoden. Pflügers Arch. ges. Physiol. 132, 82–130 (1910a).Google Scholar
  23. —: Gibt es in der Muskulatur der Mollusken periphere, kontinuierlich leitende Nervennetze bei Abwesenheit von Ganglienzellen? II. Weitere Untersuchungen an den Chromatophoren der Kephalopoden. Innervation der Mantellappen von Aplysia. Pflügers Arch. ges. Physiol. 132, 43–81 (1910b).Google Scholar
  24. Kelly, D. E.: Fine strucutre of desmosomes, hemidesmosomes and an adepidermal globular layer in developing newt epidermis. J. Cell Biol. 28, 51–72 (1966).Google Scholar
  25. -, and J. H. Luft: Fine structure, development and classification of desmosomes and related attachment mechanisms. Sixth Internat. Congr. for Electron Microscopy, Kyoto, p. 401–402 (1966).Google Scholar
  26. Kinosita, H., K. Ueda, K. Takahashi, and A. Murakami: Contraction of squid chromatophore muscle. J. Fac. Sci. Univ. Tokyo, sec. IV, 10 (3), 409–419 (1965).Google Scholar
  27. Klemensiewicz, R.: Beiträge zur Kenntnis des Farbwechsels der Cephalopoden. S.-B. Akad. Wiss. Wien, math.-nat. Kl. (3) 78, 7–50 (1879).Google Scholar
  28. Kriebel, M. E., and E. Florey: Electrical and mechanical responses of obliquely striated muscle fibers of squid to ACh, 5-hydroxy-tryptamine and nerve stimulation. Fed. Proc. 27 (2), 236 (1968).Google Scholar
  29. Leblond, C. P., H. Puchtler, and Y. Clermont: Structures corresponding to terminal bars and terminal web in many types of cells. Nature (Lond.) 186, 784–788 (1960).Google Scholar
  30. Ledbetter, M. C., and K. R. Porter: A “microtubule” in plant cell fine structure. J. Cell Biol. 19, 239–250 (1963).Google Scholar
  31. Luft, J. H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414 (1961).Google Scholar
  32. Millman, B. M.: Mechanism of contraction in molluscan muscle. Amer. Zoologist 7, 583–591 (1967).Google Scholar
  33. Millonig, G.: A modified procedure for lead staining of thin sections. J. biophys. biochem. Cytol. 11, 736–739 (1961).Google Scholar
  34. Nicol, J. A. C.: Special effectors: Luminous organs, chromatophores, pigments, and poison glands. In: K. N. Wilbur and C. M. Yonge (eds.), Physiology of mollusca (1), p. 473. New York: Academic Press 1964.Google Scholar
  35. Parker, G.H.: Animal colour changes and their neurohumours. Cambridge: University Press 1948.Google Scholar
  36. Phisalix, C.: Recherches physiologiques sur les chromatophores des céphalopodes. Arch. Physiol. norm. path. 4, 209–224 (1892).Google Scholar
  37. Rabl, H.: Über Bau und Entwicklung der Chromatophoren der Cephalopoden, nebst allgemeinen Bemerkungen über die Haut dieser Thiere. S.-B. Akad. Wiss. Wien, math.-nat. Kl. 109, 341–404 (1900).Google Scholar
  38. Rhodin, J. A. G.: Anatomy of kidney tubules. Int. Rev. Cytol. 7, 485–534 (1958).Google Scholar
  39. Richardson, K. C., L. Jarett, and E.H. Finke: Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960).Google Scholar
  40. Solger, B.: Zur Kenntnis der Chromatophoren der Cephalopoden und ihrer Adnexa. Arch. mikr. Anat. 53, 1–19 (1899).Google Scholar
  41. Steinach, E.: Studien über die Hautfärbung und über den Farbenwechsel der Cephalopoden. Pflügers Arch. ges. Physiol. 87, 1–37 (1901).Google Scholar
  42. Trelstad, R. L., E. D. Hay, and J. P. Revel: Cell contact during early morphogenesis in the chick embryo. Develop. Biol. 16, 78–106 (1967).Google Scholar
  43. Uexküll, J. V.: Physiologische Untersuchungen an Eledone moschata. I. Anhang. Die Chromatophoren. Z. Biol. 28, 550–566 (1892).Google Scholar
  44. Weiss, P., and W. Ferris: The basement lamella of amphibian skin. Its reconstruction after wounding. J. biophys. biochem. Cytol., Suppl. 2, 275–282 (1956).Google Scholar
  45. Wood, R. L.: Intercellular attachment in the epithelium of Hydra as revealed by electron microscopy. J. biophys. biochem. Cytol 6, 343–352 (1959).Google Scholar

Copyright information

© Springer-Verlag 1968

Authors and Affiliations

  • Richard A. Cloney
    • 1
  • Ernst Florey
    • 1
  1. 1.Department of ZoologyUniversity of WashingtonSeattle

Personalised recommendations