Russian Journal of Marine Biology

, Volume 35, Issue 5, pp 388–404 | Cite as

Microscopic anatomy and ultrastructure of the nervous system of Phoronopsis harmeri Pixell, 1912 (Lophophorata: Phoronida)

  • E. N. Temereva
  • V. V. Malakhov


The microscopic anatomy and ultrastructure of the nervous system of Phoronopsis harmeri was investigated using histological techniques and electron microscopy. The collar nerve ring is basically formed by circular nerve fibers originating from sensitive cells of tentacles. The dorsal nerve plexus principally consists of large motor neurons. It is shown for the first time that the sensitive collar nerve ring immediately passes into the motor dorsal nerve plexus. The basic components of the nervous system have similar cytoarchitectonics and a layered structure. The first layer is formed by numerous nerve fibers surrounded by the processes of glia-like cells. The bodies of glia-like cells constitute the second layer. The third layer consists of neuron bodies overarched by the bodies of epidermal cells. The giant nervous fiber is accompanied by more than one hundred nerve fibers of a common structure and, thus, marks the true longitudinal nerve. The phoronids possess one or two longitudinal nerves. It is supposed that the plexus nature of the nervous system in phoronids may be related to their phylogenesis. A comparison of the nervous system organization and body plans among the Lophophorata suggests that the nervous system of phoronids cannot be considered as a reductive variant of the brachiopod nervous system. At the same time, the structure of the nervous system of bryozoans can be derived from that of phoronids.

Key words

Phoronida Lophophorata nervous system plexus 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Beklemishev, V.N., Principles of Comparative Anatomy of Invertebrates, vol. 1: Promorphology, Moscow: Nauka, 1964.Google Scholar
  2. 2.
    Kovalevskii, A.O., Anatomy and Developmental History of Phoronis, Zap. SPb. Akademii Nauk, 1867, vol. 2, pp. 1–35.Google Scholar
  3. 3.
    Lagutenko, Yu.P., Cell Organization of Afferent Link in Epithelial Nerve Plexus of Metasoma in Phoronids (Tentaculata, Phoronidea), Zhurn. Evol. Biokhim. Fiziol., 1996, vol. 32, no. 4, pp. 440–447.Google Scholar
  4. 4.
    Lagutenko, Yu.P., System of Motor Neurons in Epithelial Nerve Layer (Plexus) of Phoronids (Tentaculata, Phoronidea), Zhurn. Evol. Biokhim. Fiziol., 1997, vol. 33, no. 2, pp. 218–227.Google Scholar
  5. 5.
    Lagutenko, Yu.P., Interneural System in Epithelial Nerve Plexus of Phoronids (Tentaculata, Phoronidea) and the Problem of the Origin of Associative Links in Lower Bilateria, Zhurn. Evol. Biokhim. Fiziol., 1998, vol. 33, no. 1, pp. 64–75.Google Scholar
  6. 6.
    Lagutenko, Yu.P., Early Forms of the Evolution of Basiepidermic Nerve Plexus of Bilateria as a Putative Evidence of Primary diversity of Its Initial Structure, Zhurn. Evol. Biokhim. Fiziol., 2002, vol. 38, no. 3, pp. 354–363.Google Scholar
  7. 7.
    Malakhov, V.V., Structure of Larva in the Inarticulate brachiopod Cnismatocentrum sakhalinensis parvum, Tr. ZIN AN SSSR, 1983, vol. 109, pp. 147–155.Google Scholar
  8. 8.
    Malakhov, V.V. and Galkin, S.V., Vestimentifery—Beskishechnye Bespozvonochnye Morskikh Glubin (Vestimentiferans—Gut-Less Invertebrates of Marine Deep Depths), Moscow: KMK Ltd., 1998.Google Scholar
  9. 9.
    Mamkaev, Yu.V., On Foronids of Far-Eastern Seas, Issled. Dal'nevost. Morei SSSR, 1962, vol. 8, pp. 219–237.Google Scholar
  10. 10.
    Temereva, E.N., Malakhov, V.V., and Yushin, V.V., Histology and Ultrastructure of Skin-Muscular Sac in the Phoronid Phoronopsis harmeri, Biol. Morya, 2001, vol. 27, no. 3, pp. 192–201.Google Scholar
  11. 11.
    Blochmann, F., Untersuchungen über den Bau der Brachiopoden. I: Die Anatomie von Crania anomala (Müller), Jena: Gustav Fischer, 1892, pp. 1–65.Google Scholar
  12. 12.
    Blochmann, F., Untersuchungen über den Bau der Brachiopoden. II: Die Anatomie von Discinisca lamellose (Broderip) und Lingula anatine (Brugiere), Jena: Gustav Fischer, 1900, pp. 69–124.Google Scholar
  13. 13.
    Bullock, H. and Horridge, G.A., Structure and Function in the Nervous System of Invertebrates, San Francisco; London: W.H. Freeman, 1965, vol. 1.Google Scholar
  14. 14.
    Cohen, B.L., Monophyly of Brachiopods and Phoronids: Reconciliation of Molecular Evidence with Linnean Classification (the Subphylum Phoroniformea nov.), Proc. Roy. Soc. London, ser. B, 2000, vol. 267, no. 1440, pp. 225–231.CrossRefGoogle Scholar
  15. 15.
    Cohen, B.L., Gawthrop, A., and Cavalier-Smith, T., Molecular Phylogeny of Brachiopods and Phoronids Based on Nuclear-Encoded Small Subunit Ribosomal RNA Gene Sequences, Phil. Trans. Roy. Soc. London., ser. B, 1998, vol. 353, no. 1378, pp. 2039–2061.CrossRefGoogle Scholar
  16. 16.
    Cohen, B. and Weydmann, A., Molecular Evidence that Phoronids are a Subtaxon of Brachiopods (Brachiopoda: Phoronata) and that Genetic Divergence of Metazoan Phyla Began Long Before the Early Cambrian, Org. Diver. Evol., 2005, vol. 5, pp. 253–273.CrossRefGoogle Scholar
  17. 17.
    Cori, C.J., Phoronidea, Bronn's Kl. Ordn. Tierreichs, 1939, vol. 4, no. 4, pp. 1–183.Google Scholar
  18. 18.
    Emig, C.C., British and Other Phoronids, Synopses of the British Fauna, 1979, vol. 13, pp. 1–57.Google Scholar
  19. 19.
    Fernández, I., Pardos, F., Benito, J., and Roldan, C., Ultrastructural Observation on the Phoronid Nervous System, J. Morph., 1996, vol. 230, pp. 265–281.CrossRefGoogle Scholar
  20. 20.
    Gardiner, S.L. and Jones, M.L., Vestimentifera, Microscopic Anatomy of Invertebrates, vol. 12: Onychophora, Chilopoda, and lesser Protostomata, New York: Willey-Liss, 1993, pp. 371–460.Google Scholar
  21. 21.
    Halanych, K.M., Bacheller, J.D., Aguinaldo, A.M., et al., Evidence from 18S Ribosomal DNA that the Lophophorates are Protostome Animals, Science, 1995, vol. 267, pp., 1641–1643.CrossRefPubMedGoogle Scholar
  22. 22.
    Hay-Schmidt, A., The Nervous System of the Actinotroch Larva of Phoronis muelleri (Phoronida), Zoomorphology, 1989, vol. 108, pp. 333–351.CrossRefGoogle Scholar
  23. 23.
    Hay-Schmidt, A., Distribution of Catecholamine-Containing, Serotonin-Like and Neuropeptide FMRFamide-Like Immunoreactive Neurons and Processes in the Nervous System of the Actinotroch Larva of Phoronis muelleri (Phoronida), Cell Tissue Res., 1990a, vol. 259, pp. 105–118.CrossRefGoogle Scholar
  24. 24.
    Hay-Schmidt, A., Catecholamine-Containing, Serotonin-Like and FMRFamide-Like Immunoreactive Neurons and Processes in the Nervous System of the Early Actinotroch Larva of Phoronis vancouverensis (Phoronida): Distribution and Development, Can. J. Zool., 1990b, vol. 68, no. 7, pp., 1525–1536.CrossRefGoogle Scholar
  25. 25.
    Herrmann, K., Larvalentwicklung und Metamorphose von Phoronis psammophila (Phoronida, Tentaculata), Helgol. Wiss. Meeresuntersuch., 1979, vol. 32, pp. 550–581.CrossRefGoogle Scholar
  26. 26.
    Hiller, S., The So-Called “Colonial Nervous System” in Bryozoa, Nature, 1939, vol. 143, pp., 1069–1070.CrossRefGoogle Scholar
  27. 27.
    Kupelwieser, H., Untersuchungen über den feineren Bau und die Metamorphose der Cyphonautes, Zoologica, 1906, vol. 19, no. 47, pp. 1–50.Google Scholar
  28. 28.
    Lacalli, T.C., Structure and Organization of the Nervous System in the Actinotroch Larva of Phoronis vancouverensis, Phil. Trans. Roy. Soc. London, 1990, vol. 327, pp. 655–685.CrossRefGoogle Scholar
  29. 29.
    Marcus, Er., Beobachtungen und Versuche an lebenden Meeresbryozoen, Zool. Jahrb. Abt. Syst. Ökol. Geogr. Tiere, 1926, vol. 52, pp. 1–102.Google Scholar
  30. 30.
    Masterman, A.T., On the Diplochorda, Quart. J. Microsc. Sci., 1898, vol. 40, pp. 281–366.Google Scholar
  31. 31.
    Mukai, H., Teracado, K., and Reed, C.G., Bryozoa, Microscopic Anatomy of Invertebrates, vol. 13: Lophophorata, Entoprocta, and Cycliophora, New York: Willey-Liss, 1997, pp. 45–206.Google Scholar
  32. 32.
    Nicaise, G., The Gliointerstitial System of Mollusca, Int. Rev. Cytol., 1973, vol. 34, pp., 2530–332.CrossRefGoogle Scholar
  33. 33.
    Nielsen, C., The Development of the Brachiopod Crania (Neocrania) anomala (O. F. Mueller) and Its Phylogenetic Significance, Acta Zool. (Stockholm), 1991, vol. 72, pp. 7–28.Google Scholar
  34. 34.
    Pardos, F., Roldan, C., Benito, J., and Emig, C.C., Fine Structure of the Tentacles of Phoronis australis, Acta Zool., 1991, vol. 72, no. 2, pp. 81–90.Google Scholar
  35. 35.
    Raikova, O.I., Neuroanatomy of Basal Bilaterians (Xenoturbellida, Nemertodermatida, Acoela) and Its Phylogenetic Implications, Academic Diss., Department of Biology, Akademi Univ. Finland, 2004, pp. 1–68.Google Scholar
  36. 36.
    Raikova, O.I., Reuter, M., and Justine, J.-L., Contribution to the Phylogeny and Systematics of the Acoelomorpha, Interrelation of Plathelminthes, London: Taylor and Francis, 2001, pp. 13–23.Google Scholar
  37. 37.
    Raikova, O.I., Reuter, M., Kotikova, E.A., and Gustafsson, M.K.S., A Commissural Brain! The Pattern of 5-HT Immunoreactivity in Acoela (Plathelminthes), Zoomorphology, 1998, vol. 118, pp. 69–77.CrossRefGoogle Scholar
  38. 38.
    Remane, A., Die Entstehung der Metamerie der Wirbellosen: Verh. Deutsch. Zool. Ges. Mainz (1949), Zool. Anz. Suppl., 1949, vol. 42, pp. 16–23.Google Scholar
  39. 39.
    Rieger, R.M., Fine Structure of the Body Wall, the Nervous System, and the Digestive System of the Lobatocerebridae Rieger (Annelida) and Remarks to the Organization of the Gliointerstitial Systems in Annelida, J. Morphol., 1981, vol. 167, pp. 139–165.CrossRefGoogle Scholar
  40. 40.
    Ruppert, E., Barnes, R., and Fox, R., Invertebrate Zoology: A Functional Evolutionary Approach, 7-th Ed., Cengage Learning, 2003.Google Scholar
  41. 41.
    Santagata, S., Structure and Metamorphic Remodeling of the Larval Nervous System and Musculature of Phoronis pallid (Phoronida), Evol. Dev., 2002, vol. 4, pp. 28–42.CrossRefPubMedGoogle Scholar
  42. 42.
    Santagata, S., Evolutionary and Structural Diversification of the Larval Nervous System among Marine Bryozoans, Biol. Bull., 2008, vol. 215, pp. 3–23.PubMedCrossRefGoogle Scholar
  43. 43.
    Santagata, S. and Zimmer, R.L., Comparison of the Neuromuscular System among Actinotroch Larvae: Systematic and Evolutionary Implication, Evol. Dev., 2002, vol. 4, pp. 43–54.CrossRefPubMedGoogle Scholar
  44. 44.
    Selys-Longchamps, M., Phoronis, Fauna und Flora des Golfes von Neapel, Monogr. no. 30, 1907.Google Scholar
  45. 45.
    Siewing, R., Morphologische Untersuchungen zum Archicoelomatenproblem. The Body Segmentation in Phoronis muelleri de Selys-Longchamps (Phoronidea). Ontogenese-Larve-Metamorphose-Adultus, Zool. Jahrb. Abt. Anat., 1974, vol. 92, no. 2, pp. 275–318.Google Scholar
  46. 46.
    Silen, L., On the Nervous System of Phoronis, Ark. Zool., Nye. Ser., 1954, vol. 6, pp. 1–40.Google Scholar
  47. 47.
    Stricker, S.A., Ultrastructure of the Apical Organ in a Cyphonates Larva, Bryozoa: Present and Past, Bellingham, WA: Western Washington University, 1987, pp. 261–268.Google Scholar
  48. 48.
    Stricker, S.A., Metamorphosis of the Marine Bryozoan Membranipora membranacea: An Ultrastructural Study of Rapid Morphogenetic Movements, J. Morphol., 1988, vol. 196, pp. 53–72.CrossRefGoogle Scholar
  49. 49.
    Turbeville, J.M. and Ruppert, E.E., Comparative Ultrastructure and the Evolution of Nemertines, Amer. Zool., 1985, vol. 25, pp. 53–71.Google Scholar

Copyright information

© Pleiades Publishing, Ltd. 2009

Authors and Affiliations

  1. 1.Moscow State UniversityMoscowRussia

Personalised recommendations