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Brachiopod tentacles: Ultrastructure and functional significance of the connective tissue and myoepithelial cells in Terebratalia

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Summary

The fine structure of the tentacles of the articulate brachiopod Terebratalia transversa has been studied by light and electron microscopy. The epidermis consists of a simple epithelium that is ciliated in frontal and paired latero-frontal or latero-abfrontal longitudinal tracts. Bundles of unsheathed nerve fibers extend longitudinally between the bases of the frontal epidermal cells and appear to end on the connective tissue cylinder; no myoneural junctions were found. The acellular connective tissue cylinder in each tentacle is composed of orthogonal arrays of collagen fibrils embedded in an amorphous matrix. Baffles of parallel crimped collagen fibrils traverse the connective tissue cylinder in regions where it buckles during flexion of the tentacle.

The tentacular peritoneum consists of four cell types: 1) common peritoneal cells that line the lateral walls of the coelomic canal, 2) striated and 3) smooth myoepithelial cells that extend along the frontal and abfrontal sides of the coelomic canal, and 4) squamous smooth myoepithelial cells that comprise the tentacular blood channel.

Experimental manipulations of a tentacle indicate that its movements are effected by the interaction of the tentacular contractile apparatus and the resilience of the supportive connective tissue cylinder. The frontal contractile bundle is composed of a central group of striated fibers and two lateral groups of smooth fibers which function to flex the tentacle and to hold it down, respectively. The small abfrontal group of smooth myoepithelial cells effects the re-extension of the tentacle, in conjunction with the passive resiliency of the connective tissue cylinder and the concomitant relaxation of the frontal contractile bundle.

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References

  • Atkins, D.: A new species and genus of Kraussinidae (Brachiopoda) with a note on feeding. Proc. Zool. Soc. London 131, 559–581 (1958)

    Google Scholar 

  • Atkins, D.: The early growth stages and adult structure of the lophophore of Macandrevia cranium (Müller) (Brachiopoda, Dallinidae). J. Mar. Biol. Assoc. U.K. 38, 335–350 (1959a)

    Google Scholar 

  • Atkins, D.: The growth stages of the lophophore and loop of the brachiopod Terebratalia transversa (Sowerby). J. Morph. 105, 401–426 (1959b)

    Google Scholar 

  • Atkins, D., Rudwick, M.J.S.: The lophophore and ciliary feeding mechanisms of the brachiopod Crania anomala (Müller). J. Mar. Biol. Assoc. U.K. 42, 469–480 (1962)

    Google Scholar 

  • Beauchamp, P. de: Classe des Brachiopodes. In: Traité de Zoologie, Tome V, fasc. II (P.-P. Grassé, ed.), pp. 1380–1499. Paris: Masson 1960

    Google Scholar 

  • Bemmelen, J.F. van: Untersuchungen über den anatomischen und histologischen Bau der Brachiopoda Testicardina. Jena. Z. Naturw. 16, 88–161 (1883)

    Google Scholar 

  • Blochmann, F.: Untersuchungen über den Bau der Brachiopoden. I. Die Anatomie von Crania anomala O.F. Müller, pp. 1–65. Jena: Gustav Fischer 1892

    Google Scholar 

  • Blochmann, F.: Untersuchungen über den Bau der Brachiopoden. II. Die Anatomie von Discinisca lamellosa (Broderip) und Lingula anatina (Brugière), pp. 69–124. Jena: Gustav Fischer, 1900

    Google Scholar 

  • Bullock, T.H. Horridge, G.A.: Structure and function in the nervous systems of invertebrates, Vol. I, pp. 50. San Francisco and London: W.H. Freeman and Co. 1965

    Google Scholar 

  • Cavey, M.J., Cloney, R.A.: Fine structure and differentiation of ascidian muscle. I. Differentiated caudal musculature of Distaplia occidentalis tadpoles. J. Morph. 138, 349–374 (1972)

    Google Scholar 

  • Chuang, S.H.: The ciliary feeding mechanisms of Lingula unguis (L.) (Brachiopoda). Proc. Zool. Soc. London 127, 167–189 (1956)

    Google Scholar 

  • Dall, W.H.: Annotated list of the recent Brachiopoda in the collection of the United States National Museum, with descriptions of thirty-three new forms. Proc. U.S. Nat. Museum 57, 261–377 (1921)

    Google Scholar 

  • Dawydoff, C., Grasse, P.-P.: Classe des Phoronidiens. In: Traité de Zoologie, Tome V, fasc. I (P.-P. Grassé, ed.), pp. 1008–1053. Paris: Masson, 1959

    Google Scholar 

  • Dilly, P.N.: The structure of the tentacles of Rhabdopleura compacta (Hemichordata) with special reference to neurociliary control. Z. Zellforsch. 129, 20–39 (1972)

    Google Scholar 

  • Fawcett, D.W., McNutt, N.S.: The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J. Cell Biol. 42, 1–45 (1969)

    Google Scholar 

  • Florey, E., Cahill, M.A.: Ultrastructure of sea urchin tube feet. Evidence for connective tissue involvement in motor control. Cell Tiss. Res. 177, 195–214 (1977)

    Google Scholar 

  • Gordon, D.P.: Microarchitecture and function of the lophophore in the bryozoan Cryptosula pallasiana. Marine Biol. 27, 147–163 (1974)

    Google Scholar 

  • Gosline, J.M.: Connective tissue mechanics of Metridium senile. II. Visco-elastic properties and macromolecular model. J. exp. Biol. 55, 775–795 (1971)

    Google Scholar 

  • Gupta, B.L., Little, C.: Studies on Pogonophora. II. Ultrastructure of the tentacular crown of Siphonobrachia. J. Mar. Biol. Ass. U.K. 49, 717–741 (1969)

    Google Scholar 

  • Hancock, A.: On the organisation of the brachiopoda. Phil. Trans. 148, 791–869 (1859)

    Google Scholar 

  • Helmcke, von J-G.: Brachiopoda. In: Kükenthal's Handbuch der Zoologie, V. 3, II Teil 5, pp. 139–262. Berlin-Leipzig: Walter de Gruyter and Co. 1937

    Google Scholar 

  • Heyer, C.B., Kater, S.B.: Neuromuscular systems in molluscs. Amer. Zool. 13, 249–270 (1973)

    Google Scholar 

  • Huxley, T.H.: Contributions to the Anatomy of the Brachiopoda. Proc. roy. Soc. London 7 (1854)

  • Hyman, L.H.: The lophophorate coelomates-Phylum Brachiopoda. In: The invertebrates, Vol. 5, Chap. 21, pp. 516–609. New York: McGraw-Hill. 1959

    Google Scholar 

  • Johnson, E.A., Sommer, J.R.: A strand of cardiac muscle. Its ultrastructure and the electrophysiological implications of its geometry. J. Cell Biol. 33, 103–129 (1967)

    Google Scholar 

  • Levine, R.J.C., Elfvin, M., Dewey, M.M., Walcott, B.: Paramyosin in invertebrate muscles. II. Content in relation to structure and function. J. Cell Biol. 71, 273–279 (1976)

    Google Scholar 

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

    Google Scholar 

  • Lutaud, G.: L'innervation du lophophore chez le Bryozoaire chilostome Electra pilosa (L.) Z. Zellforsch. 140, 217–234 (1973)

    Google Scholar 

  • Mattox, N.T.: Observations on the brachiopod communities near Santa Catalina Island. Essays Nat. Sci. in honor of Captain Allan Hancock, pp. 73–86. Univ. Southern Calif. Press 1955

  • McCammon, H.M., Reynolds, W.A.: Experimental evidence for direct nutrient assimilation by the lophophore of articulate brachiopods. Mar. Biol. 34, 41–51 (1976)

    Google Scholar 

  • Nielsen, C., Rostgaard, J.: Structure and function of an entoproct tentacle with a discussion of ciliary feeding types. Ophelia 15, 115–140 (1976)

    Google Scholar 

  • Oliphant, L.W., Cloney, R.A.: The ascidian myocardium: Sarcoplasmic reticulum and excitationcontraction coupling. Z. Zellforsch 129, 395–412 (1972)

    Google Scholar 

  • Orton, J.: On ciliary mechanisms in brachiopods and some polychaetes, with a comparison of the ciliary mechanisms on the gills of molluscs, Protochordata, Brachiopods, and cryptocephalous polychaetes, and an account of the endostyle of Crepidula and its allies. J. Mar. Biol. Ass. U.K. 10, 283–311 (1914)

    Google Scholar 

  • Person, P., Philpott, D.E.: The nature and significance of invertebrate cartilages. Biol. Rev. 44, 1–16 (1969)

    Google Scholar 

  • Prosser, C.L.: Comparative physiology of non-striated muscles. In: Invertebrate Nervous Systems. Their significance for Mammalian Neurophysiology (C.A.G. Wiersma, ed.), pp. 133–149. Chicago and London: The University of Chicago Press 1967

    Google Scholar 

  • Reynolds, E.S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–211 (1963)

    Google Scholar 

  • Reynolds, W.A., McCammon, H.M.: Aspects of the functional morphology of the lophophore in articulate brachiopods. Amer. Zool. 17, 121–132 (1977)

    Google Scholar 

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

    Google Scholar 

  • Rudwick, M.J.S.: Living and Fossil Brachiopods. London: Hutchinson and Co. 1970

    Google Scholar 

  • Schiaffino, S., Margreth, A.: Coordinated development of the sarcoplasmic reticulum and T-system during postnatal differentiation of rat skeletal muscle. J. Cell Biol. 41, 855–875 (1969)

    Google Scholar 

  • Silén, L.: On the nervous system of Phoronis. Ark. Zool. 6, 1–40 (1954)

    Google Scholar 

  • Storch, V., Welsch, U.: Elektronenmikroskopische und enzymhistochemische Untersuchungen über Lophophor und Tentakeln von Lingula unguis (L.)(Brachiopoda). Zool. Jb. Anat. 96, 225–237 (1976)

    Google Scholar 

  • Thomson, J.A.: Brachiopod morphology and genera (Recent and Teriary). N.Z. Bd. Sci. Art, Manual 7, 338p. (1927)

    Google Scholar 

  • Williams, A., Rowell, A.J.: Brachiopod anatomy. In: Treatise on invertebrate paleontology: part H: Brachiopoda (R.C. Moore, ed.), pp. H6-H57. The University of Kansas Press and the Geol. Soc. America 1965

    Google Scholar 

  • Winkelman, L.: Comparative studies of paramyosins. Comp. Biochem. Physiol. 55B, 391–397 (1976)

    Google Scholar 

  • Wood, R.L., Luft, J.H.: The influence of buffer systems on fixation with osmium tetroxide. J. Ultrastruct. Res. 12, 22–45 (1965)

    Google Scholar 

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The authors wish to express their appreciation to Professor Robert L. Fernald for his advice and encouragement throughout the course of this study. Some of the work was conducted at the Friday Harbor Laboratories of the University of Washington. The authors are indebted to the Director, Professor A.O.D. Willows, for use of the facilities. Part of this study was supported by NIH Developmental Biology Training Grant No. 5-T01-HD00266 and NSF grant BMS 7507689

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Reed, C.G., Cloney, R.A. Brachiopod tentacles: Ultrastructure and functional significance of the connective tissue and myoepithelial cells in Terebratalia . Cell Tissue Res. 185, 17–42 (1977). https://doi.org/10.1007/BF00226666

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