Ultrastructural aspects of nervous-system and statocyst morphogenesis during embryonic development of Convoluta psammophila (Turbellaria, Acoela)

  • Enrico A. Ferrero
  • Celina Bedini
Conference paper
Part of the Developments in Hydrobiology 69 book series (DIHY, volume 69)

Abstract

The notion that statocysts originated from an infolding of ectoderm lined by ciliated sensory cells has been challenged with evidence of ‘capsule’-limited, non-ciliary statocysts in several independent phyla. Statocysts in turbellarians primitively lack cilia and are embedded within or closely adjoined to the cerebral ganglion; they are likely to be derived from nervous tissue. We investigated the development of the simple statocyst in an acoel turbellarian, a statocyst consisting of three cells. Observations of serial TEM sections of embryos at different stages of development support the hypothesis of an inner (nonepithelial) origin of the statocyst. First, a three-cell complex is delimited by a basal lamina; it then undergoes cavitation by swelling, autophagy, and fluid secretion. The statocyst becomes discernible within the precursor ganglion cells while they still contain yolk inclusions. The two outer (parietal) cells, enclosed together by a 10-nm-thick basal lamina, arrange themselves in an ovoid of about 10µm diameter and surround the inner statolith-forming cell. The statolith is formed later within vacuoles of the statolith-forming cell.

Key words

Turbellaria Acoela development morphogenesis statocyst nervous system 
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References

  1. Apelt, G., 1969. Fortpfianzungsbiologie, Entwicklungszyklen und vergleichende Fruehentwicklung acoeler Turbellarien. Mar. Biol. 4: 267–325.Google Scholar
  2. Aronova, M., 1974. Electron microscopic observation on the aboral organ of Ctenophora. I. The gravity receptor. Z. mikrosk.-anat. Forsch., Leipzig 88: 401–412.Google Scholar
  3. Ax, P., 1985. The position of the Gnathostomulida and Platyhelminthes in the phylogenetic system of the Bilateria. In S. Conway Morris, J. D. George, R. Gibson & H. M. Platt (eds), The origins and relationships of lower invertebrates. Clarendon Press, Oxford: 168–180.Google Scholar
  4. Bedini, C. & A. Lanfranchi, 1991. The central and peripheral nervous system of Acoela (Plathelminthes). An electron microscopical study. Acta zool. (Stockh.) 72: 101–106.Google Scholar
  5. Bedini, C., A. Lanfranchi & R. Nobili, 1973. The ultrastructure of the Muller body in Remanella (Ciliata Holotrica Loxodidae). Monit. zool. ital. (N.S.) 7: 87–95.Google Scholar
  6. Beklemishev, W. N., 1969. Principles of comparative anatomy of invertebrates. Oliver & Boyd, Edinburgh, 490 + 529 pp.Google Scholar
  7. Boaden, P. J. S., 1975. Anaerobiosis, meiofauna and early metazoan evolution. Zool. Scripta 4: 21–40.Google Scholar
  8. Boyer, B. C., 1971. Regulative development in a spiralian embryo as shown by cell deletion experiments on the acoel, Childia. J. exp. Zool. 176: 97–106.Google Scholar
  9. Bresslau, E., 1909. Die Entwicklungen der Acoelen. Verhandl. Dtsch. Zool. Gesell. 19: 314–324.Google Scholar
  10. Brüggemann, J. & U. Ehlers, 1981. Ultrastruktur der Statocyste von Ototyphlonemertes pallida (Keferstein, 1862) (Nemertini). Zoomorphology 97: 75–87.Google Scholar
  11. Campbell, R. D., 1972. Statocyst lacking cilia in the coelenterate Corymorpha palma. Nature 238: 49–51.Google Scholar
  12. Dilly, P. N., 1962. Studies on the receptors in the cerebral vesicle ofthe ascidian tadpole.I. The otolith. Q. J. microsc. Sci. 103: 393–398.Google Scholar
  13. Eakin, R. M. & A. Kuda, 1971. Ultrastructure of sensory receptors in ascidian tadpoles. Z. Zellforsch. mikrosk. Anat. 112: 287–312.Google Scholar
  14. Ehlers, U., 1985a. Phylogenetic relationships within the Platyhelminthes. In S. Conway Morris, J. D. George, R. Gibson & H. M. Platt (eds), The origins and relationships of lower invertebrates. Clarendon Press, Oxford: 143–158.Google Scholar
  15. Ehlers, U., 1985b. Das Phylogenetische System der Plathelminthes. Gustav Fischer Verlag, Stuttgart, 317 pp.Google Scholar
  16. Ehlers, U., 1985c. Organisation der Statocyste von Retronectes (Catenulida, Plathelminthes). Microfauna Marina 2: 7–22.Google Scholar
  17. Ehlers, U., 1991. Comparative morphology of statocysts in the Plathelminthes and the Xenoturbellida. Hydrobiology 227/Dev. Hydrobiol 69: 263–271.Google Scholar
  18. Ehlers, U. & B. Sopott-Ehlers, 1990. Organization of statocysts in the Otoplanidae (Plathelminthes): an ultrastructural analysis with implications for the phylogeny of the Proseriata. Zoomorphology 109: 309–310.Google Scholar
  19. Ferrero, E., 1970. Alcuni dati sull’ultrastruttura della statocisti in Convoluta psammophila Bekl. (Turbellaria, Acoela). Boll. Zool. 37: 492–493.Google Scholar
  20. Ferrero, E., 1973. A fine structural analysis of the statocyst in Turbellaria Acoela. Zool. Scr. 2: 5–16.Google Scholar
  21. Ferrero E. A., C. Bedini & A. Lanfranchi, 1985. An ultrastructural account of otoplanid Turbellaria neuroanatomy. II. The statocyst design: evolutionary and functional implications. Acta zool. (Stockh.) 66: 75–87Google Scholar
  22. Fraenkel, G., 1929. Ueber die Geotaxis von Convoluta roscoffensis. Z. vergl. Physiol. 10: 237–247.Google Scholar
  23. Gardiner, E. G., 1895. Early development of Polychoerus caudatus Mark. J. Morph. 11: 155–176.Google Scholar
  24. George’vitch, J., 1899. Etude sur Ie developpement de la Convoluta roscoffensis Graff. Arch. Zool. exp., Ser. 3, 7: 343–361.Google Scholar
  25. Giesa, S., 1966. Die Embryonalentwicklung von Monocelis fusca Oersted (Turbellaria, Proseriata). Z. Morph. Oekol. Tiere 57: 137–230.Google Scholar
  26. Hadzi, J., 1953. An attempt to reconstruct the system of animal classification. Syst. Zool. 2: 145–154.Google Scholar
  27. Horridge, G. A., 1969. Statocysts of medusae and evolution of stereocilia. Tissue Cell 1: 341–353.Google Scholar
  28. Ivanov, A. V., 1988. On the early evolution of the Bilateria. Fortschr. Zool. 36: 349–352.Google Scholar
  29. Ivanov, V. P., Yu. V. Mamkaev & R. A. Pevzner, 1972. Electron microscopic study on the statocyst in the acoelan turbellarian Convoluta convoluta. Zh. Evol. Biokhim. Fiziol. 8: 189–193.Google Scholar
  30. Katz, M. J., 1983. Comparative anatomy of the tunic ate tadpole, Ciona intestinalis. Biol. Bull. 164: 1–27.Google Scholar
  31. Merker, G. & M. Vaupel von Harnack, 1967. Zur Feinstruktur des ‘Gehirns’ und der Sinnesorgane von Protodrilus rubropharyngaeus J aegersten (Archiannelida). Z. Zellforsch. mikrosk. Anat. 81: 221–239.Google Scholar
  32. Pereyaslawzew, S., 1885. Sur le developpement des Turbellariés. Zool. Anz. 8: 269–271.Google Scholar
  33. Reisinger, E., 1924. Die Gattung Rhynchoscolex. Z. Morph. Oekol. Tiere 1: 1–37.Google Scholar
  34. Rieger, R., W. Sterrer, W. Salvenmoser & G. Rieger, 1990. Preliminary data on statocyst ultrastucture in the rhabdocoel genus Lurus (Turbellaria). Abstract of poster presented at The Sixth International Symposium on the Biology of the Turbellaria, Hirosaki University, Hirosaki, Japan, 7–12 August, 1990.Google Scholar
  35. Singla, C. L., 1972. Sense organs of hydromedusae. Ph. D. Thesis, University of Victoria, Victoria B.C., Canada 134 pp.Google Scholar
  36. von Buddenbrock, W., 1952. Sinnesphysiologie. In Vergleichende Physiologie, Bd. 1, Birkhauser Verlag, Basel 425 pp.Google Scholar

Copyright information

© Kluwer Academic Publishers 1991

Authors and Affiliations

  • Enrico A. Ferrero
    • 1
  • Celina Bedini
    • 2
  1. 1.Dipartimento di BiologiaUniversità di TriesteTriesteItaly
  2. 2.Dipartimento di Scienze del Comportamento Animale e dell’UomoUniversità di PisaPisaItaly

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