Skip to main content
Log in

Phylogenetic relationships of rotifers, as derived from photoreceptor morphology and other ultrastructural analyses

  • Published:
Hydrobiologia Aims and scope Submit manuscript

Summary

The first chapter summarizes the state of the disagreements about the phylogeny of rotifers and lower metazoa in 1963. The only arguments were morphological, and the only problem was the definition of homologies. There are today more diversified approaches of the evolution: electron microscopy, ethology, genetics and ecology.

The second chapter shows, using an example, that phylogeny is very complex. A synthesis is made on the photosensitivities and the photoreceptors of rotifers, with several original ultrastructural descriptions (ocelli of Rhinoglena frontalis and Philodina roseola; cerebral eyes of Brachionus calyciflorus and P. roseola). After a criticism of several theories on the use of photoreceptors in phylogeny, a new polyphyletic theory is proposed and the classical criteria of homology (Remane, 1955) are discussed.

The third chapter considers two major evolutionary features of rotifers: parthenogenetic reproduction, which is correlated with feeding, and special adaptations promoting survivorship in harsh environments (anhydrobiosis in Bdelloïdea, resting eggs production in Monogononta). In addition to classical meiotic recombination, evolutionary mechanisms in the Rotatoria include mutation during parthenogenesis and maternal effects.

The forth chapter describes some constant ultrastructural features in rotifers, and compares them to homologous structures in related groups: skeletal integument, flame-cells, pseudocoel, thick myofilaments and a glia-free nervous system. Since some of these structures (integument and flame-cell) have the same fonctions in all rotifers, their variations are good indicators of phylogeny.

In conclusion (V), not one argument corroborates Remane's hypothesis of the coelomate origin of rotifers. The hypothesis of Josse (1979), founded on embryological works, is corroborated by several ultrastructural features discussed herein, although rotifers have been placed in the phylum Aschelminthes, several aspects of their ultrastructural morphology suggest more relationships to the Acanthocephala and Platyhelminths than to the other classes of Aschelminths. Other ultrastructural observations show that this relationship Rotatoria-Platyhelminths is not direct: they have a common ancestor. The relationship Rotifera-Phytoflagellates is also discussed. Finally it is necessary to carry on other ultrastructural, ethological and genetic work on both rotifers and related groups.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams, E. 1978. Invertebrate Collagens. Marked differences from vertebrate collagens appear in only a few invertebrate groups. Science, 302: 591–598.

    Google Scholar 

  • Amsellem, J. & Clement, P. 1977. Correlation between ultrastructural features and contraction rates in rotiferan muscles. I. Preliminary observations 0n longitudinal retractor muscles in Trichocerca rattus. Cell. Tiss. Res., 181: 81–90.

    Google Scholar 

  • Atwood, H. L. 1972. Crustacean muscle. in: ‘The structure and function of muscle’ 2nd ed., C. H. Bourne ed., Acad. Press, 1: 422–490.

  • Ax, P. 1963. Relationships and phylogeny of the Turbellaria. in: ‘The Lower Metazoa’, E. C. Dougherty ed., Univ. Calif. Press, p. 191–224.

  • Bairati, A. 1972. Collagen: an analysis of phylogenetic aspects. Boll. Zool., 39: 205–248.

    Google Scholar 

  • Beauchamp, P. de 1907. Morphologie et variations de l'appareil rotateur des Rotifères. Arch. Zool. exp. gén., 6: 1–29.

    Google Scholar 

  • Beauchamp, P. de 1909. Recherches sur les Rotifères: les formations tégumentaires et l'appareil digestif. Arch. Zool. exp. gén., 10: 1–410.

    Google Scholar 

  • Beauchamp, P. de 1965. Classe des Rotifères. in ‘Traité de Zoologie, Anatomie, Systématique, Biologie’ P. P. Grasse ed., IV, 3: 1225–1379.

  • Beklemishev, V. N. 1963. On the relationship of the Turbellaria to other groups of the animal kingdom. in: ‘The Lower Metazoa’, E. C. Dougherty ed., Univ. Calif. Press, p. 234–246.

  • Bentfeld, M. E. 1971a. Studies of oogenis in the rotifer Asplanchna. I. Fine structure of the female reproductive system. Z. Zellforsch., 115: 165–183.

    PubMed  Google Scholar 

  • Bentfeld, M. E. 1971b. Studies of oogenis in the rotifer Asplanchna. II. Oocyte growth and development. Z. Zellforsch., 115: 184–195.

    PubMed  Google Scholar 

  • Birky, C. W. & Field, B. 1966. Nuclear number in the rotifer Asplunchna: intraclonal variation and environmental control. Science, 151: 585–587.

    Google Scholar 

  • Brandenburg, J. 1962. Elektronenmikroskopische Untersuchung des Terminalapparatus von Chaetonotus sp. (Gastrotrichen) als ersten Beispiels einer Cyrtocyte bei Askelminthen. Z. Zellforsch., 57: 136–144.

    Google Scholar 

  • Braun, G., Kummel, G. & Mangos, J. A. 1966. Studies on the ultrastructure and function of a primitive excretory organ, the protonephridium on the rotifer Asplanchna priodonta. Pflügers Archiv., 289: 141–154.

    Google Scholar 

  • Brooker, B. E. 1972. The sense organs of trematode miracidia. in: ‘Behavioural aspects of parasite transmission’, Canning, E. U. & Wright, C. A. eds., Acad. Press, London, p. 171–180.

    Google Scholar 

  • Champ, P. 1976. Etude des populations d'un Rotifère épiphyte dans la Loire. Thèse doctorat 3ème cycle, Univ. Paris VI, 80 p.

  • Clark, A. W. 1967. The fine structure of the eye of the leech, Helobdella stagnalis. J. Cell Sci., 2: 314–348.

    Google Scholar 

  • Clément, P. 1967. Ultrastructure du système osmorégulateur d'un Rotifère Notommata copeus. Conclusions physiologiques et phylogénétiques. Thèse doctorat 3ème cycle, Univ. Lyon I, 248, 116 p.

  • Clément, P. 1968. Ultrastructures d'un Rotifère, Notommata copeus. I. La cellule-flamme. Hypothèses physiologiques. Z. Zellforsch., 89: 478–498.

    Article  PubMed  Google Scholar 

  • Clément, P. 1969a. Ultrastructures d'un Rotifère Notommata copeus. II. Le tube protonéphridien. Z. Zellforsch., 94: 103–117.

    Article  PubMed  Google Scholar 

  • Clément, P. 1969b. Premières observations sur l'ultrastructure comparée des téguments de Rotifères. Vie Milieu A, 20: 461–482.

    Google Scholar 

  • Clément, P. 1975. Ultrastructure de l'oeil cérébral d'un Rotifère, Trichocerca rattus. J. Microsc. Biol. cell., 22: 69–86.

    Google Scholar 

  • Clément, P. 1977a. Introduction à la photobiologie des Rotifères dont le cycle reproducteur est contrôlé par la photopériode. Approches ultrastructurale et expérimentale. Thèse doctorat Etat, Univ. Lyon I, 7716, 262 p.

  • Clément, P. 1977b. Ultrastructural research on rotifers. Arch. Hydrobiol. Beih. 8: 270–297.

    Google Scholar 

  • Clément, P. 1977c. Phototaxis in rotifers (action spectra). Arch. Hydrobiol. Beih., 8: 67–70.

    Google Scholar 

  • Clément, P., Amsellem, J., Luciani, A. & Cornillac, A. 1980. Ultrastructure des yeux cérébraux des Rotifères. Colloque ‘La vision chez les Invertébrés’, C.N.R.S. Paris sept. 1979, in press.

  • Clément, P., Amsellem, J., Cornillac, A. & Luciani, A. 1980b. A la recherche (ultrastructurale) des photorécepteurs extraoculaires chez les Rotifères. Ibid., in press.

  • Clément, P., Amsellem, J., Cornillac, A. M., Luciani, A. & Ricci, C. 1980c. idem. I. The buccal velum. In this volume, pp. 127–131.

  • Clément, P., Amsellem, J., Cornillac, A. M., Luciani, A. & Ricci, C. 1980d. An ultrastructural approach to feeding behaviour in Philodina roseola and Brachionus calyciflorus. II. The oesophagus. In this volume, pp. 133–136.

  • Clément, P., Amsellem, J., Cornillac, A. M., Luciani, A. & Ricci, C. 1980e. Idem. III. Cilia and muscles. Conclusions. In this volume, pp. 137–141.

  • Clément, P. & Pourriot, R. 1979. Influence de l'âge des grands-parents sur l'apparition des mâles chez le Rotifère Notommata copeus. Int. J. Invert. Repr. 1: 89–98.

    Google Scholar 

  • Clément, P. & Pourriot, R. 1980. About a transmissible influence through several generations in a clone of the Rotifer Notommata copeus Ehr. In this volume, pp. 27–31.

  • Clément, P., Rougier, C. & Pourriot, R. 1976. Les facteurs exogènes et endogènes qui contrôlent l'apparition des mâles chez les Rotifères. Bull. Soc. Zool. Fr., 101, suppl. 4: 86–95.

    Google Scholar 

  • Eakin, R. M. 1965. Evolution of photoreceptors. Cold Spring Harb. Symp. quant. Biol., 30: 363–370.

    PubMed  Google Scholar 

  • Eakin, R. M. 1968. Evolution of photoreceptors. In: ‘Evolutionary biology’, Dobzhansky, T., Hecht, M. K. & Steere, W. C. eds, New York, p. 194–242.

  • Eakin, R. M. 1972. Structure of invertebrate photoreceptors. In: ‘Handbook of sensory physiology’, Springer-Verlag, 7: 625–684.

  • Eakin, R. M. & Brandenburger, J. L. 1974. Ultrastructural features of a Gordian Worm (Nematomorpha). J. Ultrastr. Res., 46: 351–374.

    Google Scholar 

  • Eakin, R. M. & Westfall, J. A. 1965. Ultrastructure of the eye of the rotifer Asplanchna brightwelli. J. Ultrastr. Res. 12: 46–62.

    Google Scholar 

  • Fauré-Fremiet, E. 1961. Cils vibratiles et flagelles. Biol. Rev., 36: 464–536.

    PubMed  Google Scholar 

  • Fauré-Fremiet, E. & Rouiller, C. 1957. Le flagelle interne d'une Chrysomonadale: Chromulina psammobia. C. R. Acad. Sci. Fr., 244: 2655–2657.

    Google Scholar 

  • Fournier, A. 1980. Les photorécepteurs des Plathelminthes parasites. Colloque ‘La vision chez les invertébrés’, C.N.R.S., Paris sept. 1979, in press.

    Google Scholar 

  • Fournier, A. & Combes, F. 1978. Structure of photoreceptors of Polystoma integerrimum (Platyhelminths, Monogena). Zoomorphologie, 91: 147–155.

    Google Scholar 

  • Franc, J. M. 1972. Activités des rosettes ciliées et leurs supports ultrastructuraux chez les Cténaires. Z. Zellforsch, 130: 527–544.

    Article  PubMed  Google Scholar 

  • Franc, S., Franc, J. M. & Garrone, R. 1976. Fine structure and cellular origin of collagenous matrices in primitive animals: Porifera, Cnidaria and Ctenophora. Front. Matrix. Biol., 3: 143–156.

    Google Scholar 

  • Garrone, R. 1975. Nature, génèse et fonctions des formations conjonctives chez les Spongiaires. Thèse Doctorat Etat. Univ. Lyon I, Fr., 302 p.

  • Gilbert, J. J. 1967. Asplanchna and postero-lateral spine production in Brachionus calyciflorus. Arch. Hydrobiol. 64: 1–62.

    Google Scholar 

  • Gilbert, J. J. 1977a. Selective cannibalism in the rotifer Asplanchna sieboldi. Arch. Hydrobiol. Beih. 8: 267–269.

    Google Scholar 

  • Gilbert, J. J. 1977b. Mictic-female production in monogonont rotifers. Arch. Hydrobiol. Beih. 8: 142–155.

    Google Scholar 

  • Gilbert, J. J. & Starkweather, P. L. 1977. Feeding in the rotifer Brachionus calyciflorus. I. Regulatory mechanisms. Oecologia, 28: 125–131.

    Google Scholar 

  • Hadzi, J. 1944. Turbelarÿska Teorija Knidarijev. (Turbellarien-Theorie der Knidarier). Slov. Akad. Znan. Um., Ljubljana (in Slovenian with German summary).

  • Hadzi, J. 1953. An attempt to reconstruct the system of animal classification. Syst. Zool., 2: 145–154.

    Google Scholar 

  • Hand, C. 1959. On the origin and phylogeny of the coelenterates. Syst. Zool., 8: 191–202.

    Google Scholar 

  • Hand, C. 1963. The Early Worm: a Planula. in: ‘The Lower Metazoa’, E. C. Dougherty ed; Univ. Calif. Press, p. 33–39.

  • Hanson, E. D. 1958. On the origin of the Eumetazoa. Syst. Zool. 7: 16–47.

    Google Scholar 

  • Hanson, E. D. 1963. Homologies and the ciliate origin of the Eumetazoa. in ‘The lower Metazoa’, E. C. Dougherty ed., Univ. Calif. Press, p. 7–22.

  • Hendelberg, M., Morling, G. & Pejler, B. 1979. The ultrastructure of the lorica of the rotifer Keratella serrulata (Ehrbg). Zoon, 7: 49–54.

    Google Scholar 

  • Hernandez-Nicaise, M. L. & Amsellem, J. 1980. A giant multinucleated smooth muscle cell: the muscle fiber of Beroe (Ctenophora). J. Cell Sci., in press.

  • Hertel, H. 1979. Phototactic reations of Aslanchna priodonta to monochromatic light. Z. Naturforsch., 34: 1–2.

    Google Scholar 

  • Horridge, G. A. 1968. Interneurons. Their origin, action, specificity, growth and plasticity. W. H. Freeman and al. ed., London and San Francisco, p. 1–83.

    Google Scholar 

  • Huxley, 1853. cited by Hyman, 1951.

  • Hyman, L. H. 1951. Class Rotifers. in: ‘The Invertebrates’, Mc. Graw-Hill Book Company Inc., 3, p. 59–151.

  • Jägersten, G. 1955. On the early phylogeny of the Metazoa. Zool. Bidr. Uppsala, 30: 321–354.

    Google Scholar 

  • Jägersten, G. 1959. Further remarks on the early phylogeny of the Metazoa. Zool. Bidr. Uppsala, 33: 79–108.

    Google Scholar 

  • Jennings, H. S. 1901. On the significance of spiral swimming of organisms. Amer. Nat., 35: 369–378.

    Article  Google Scholar 

  • Joffe, B. I. 1979. (The comparative embryological analysis of the development of Nemathelminthes). (in russian)., Proc. Zool. Inst. Akad. Sci. URSS, 84: 39–62.

    Google Scholar 

  • King, C. E. 1977. Genetics of reproduction, variation and adaptation in rotifers. Arch. Hydrobiol. Beih., 8: 187–201.

    Google Scholar 

  • Koehler, J. K. 1965. A fine study of the rotifer integument. J. Ultrastr. Res., 12: 113–134.

    Google Scholar 

  • Koehler, J. K. 1966. Some comparative fine structure relationships of the rotifer integument. J. Exp. Zool., 162: 231–243.

    Google Scholar 

  • Koopowitz, H. & Chien, P. 1974. Ultrastructure of the nerve plexus in flatworms. I. Peripheral organization. Cell Tissue Res., 155: 337–351.

    Article  PubMed  Google Scholar 

  • Koste, W. 1978. Rotatoria. Borntraeger, Berlin, 2 vols., 673 pp. 234 Pls.

  • Kryvi, H. 1973. Ultrastructural studies of the sucker cells in Hemiurus communis (Trematoda). Norm. J. Zool., 21: 273–280.

    Google Scholar 

  • Kümmel, G. & Brandenburg, J. 1961. Die Reusengeisselzellen (Cyrtocyten). Z. Naturforsch., 16b: 692–697.

    Google Scholar 

  • Lansing, A. I. 1947. A transmissible, cumulative, and reversible factor in aging. J. Gerontology, 2: 228–239.

    Google Scholar 

  • Lansing, A. I. 1954. A non-genic factor in the longevity of rotifers. Ann. N.Y. Acad. Sci., 57: 455–464.

    PubMed  Google Scholar 

  • Lanzavecchia, G., Valvassori, R., Eguileor, M. de, & Lanzavecchia, P. 1979. Three dimensional reconstruction of the contractile system of the Nematophore muscle fiber. J. Ultrastr. Res., 66: 201–223.

    Google Scholar 

  • Lender, Th. 1976. Rôle de la neurosécrétion au cours de la régénération et de la scissiparité des Planaires d'eau douce. in: ‘Ac-tualités sur les hormones d'Invertérés’, Colloques internationaux du C.N.R.S., 251: 39–48.

    Google Scholar 

  • Lentz, T. L. 1968. Primitive nervous systems. Yale Univ. Press, New Haven and London. 141 p.

    Google Scholar 

  • Lyons, K. M. 1972. Sense organs of monogeneans. in: ‘Behavioural aspects of parasite transmission’, Canning, E. U. & Wright, C. A. eds., London: Acad. Press, p. 181–199.

    Google Scholar 

  • McKanna, J. A. 1968. Fine structure of the protonephridial system in Planaria. I. Flame cells. Zellforsch., 92: 509–523.

    Article  Google Scholar 

  • Marcus, E. 1958. On the evolution of the animal phyla. Quart. Rev. Biol. 33: 24–58.

    Article  Google Scholar 

  • Mattern, C. F. T. & Daniel, W. A. 1966. The flame-cell of rotifer. Electron microscope observations of supporting rootlets structures. J. Cell Biol., 29: 547–551.

    Article  PubMed  Google Scholar 

  • Mayr, E. 1974. Populations, espèces et évolution. Herman ed., Paris, 496 p.

  • Menzel, R. & Roth, F. 1972. Spektrale Phototaxis von Plankton-rotatorien. Experientia, 28: 356–357.

    Google Scholar 

  • Morita, M. & Best, J. B. 1966. Electron microscopic studies of planaria. III. Some observations on the fine structure of planarian nervous tissue. J. Exp. Zool., 161: 391–411.

    PubMed  Google Scholar 

  • Nachtwey, R. 1925. Untersuchungen über die Keimbahn Organogenese und Anatomie von Asplanchna priodonta Gosse. Z. wiss. Zool., 126: 239–492.

    Google Scholar 

  • Nørevang, A. 1974. Photoreceptors of the phaosome (hirudinean) type in a pogonophore. Zool. Anz., 193: 297–304.

    Google Scholar 

  • Pikkarainen, J. & Kulonen, E. 1969. Collagen. Some generalizations 0n comparative chemistry. Nature, Lond., 223: 839–841.

    Google Scholar 

  • Pontin, R. M. 1964. A comparative account of the protonephridia of Asplanchna (Rotifera) with special reference to the flame bulbs. Proc. Zool. Soc. Lond., 143: 511–525.

    Google Scholar 

  • Pontin, R. M. 1966. The osmoregulatory function of the vibratile flames and the contractile vesicle of Asplanchna (Rotifera). Comp. Biochem. Physiol., 17: 1111–1126.

    Article  Google Scholar 

  • Pourriot, R. 1963. Influence du rythme nycthéméral sur le cycle sexuel de quelques Rotifères. C.R. Acad. Sci., 256: 5216–5219.

    Google Scholar 

  • Pourriot, R. 1965. Recherches sur l'écologie des Rotifères. Thèse Doct. d'état, Vie Milieu, Suppl. 21, 224 p.

  • Pourriot, R. 1974. Relations prédateur-proie chez les Rotifères. Influence du prédateur (Asplanchna brightwelli) sur la morphologie de la proie (Brachionus bidentata) Ann. Hydrobiol., 5: 43–55.

    Google Scholar 

  • Pourriot, R. 1977. Food and feeding habits of Rotifera. Arch. Hydrobiol. Beih., 8: 243–260.

    Google Scholar 

  • Pourriot, R. & Clément, P. 1973. Photopériodisme et cycle hétérogonique chez Notommata copeus (Rotifère Monogononte). II. Influence de la qualité de la lumière. Spectres d'action. Arch. Zool. exp. gén., 114: 277–300.

    Google Scholar 

  • Pourriot, R., Clément, P. & Luciani, A. 1980. Influence de la photopériode sur un Rotifère. Hypothèses sur les mécanismes. in: ‘Colloque sur la vision chez les invertébrés’, C.N.R.S., Paris Sept. 79, in press.

    Google Scholar 

  • Pourriot, R. & Rougier, C. 1976. Influence de l'âge des parents sur la production de femelles mictiques chez Brachionus calyciflorus Pallas et B. rubens Ehr. (Rotifères). C.R. Acad. Sci. Paris, 283: 1497–1500.

    Google Scholar 

  • Pourriot, R., Rougier, C. & Benest, D. 1980. Hatching of Brachionus rubens O. F. Muller resting eggs (Rotifers). In this volume, pp. 51–54.

  • Preissler, K. 1977. Horizontal distribution and ‘avoidance of shore’ by rotifers. Arch. Hydrobiol. Beih., 8: 43–46.

    Google Scholar 

  • Pringle, J. W. S. 1972. Arthropod muscles. in: ‘The structure and function of muscle’, 2nd ed., G. H. Bourne ed., Acad. Press, I: 491–542.

  • Reger, J. F. 1976. Studies on the fine structure of cercarial tail muscle of Schistosoma sp. (Trematoda). J. Ultrastr. Res. 57: 77–86.

    Google Scholar 

  • Remane, A. 1929–1933. Rotatoria. in: Dr. H. G. Bronn's Klassen und Ordnungen des Tier-Reichs’, IV (Vermes), 2 (Aschelminthes), I (Rotatorien, Gastrotrichen und Kinorhynchen), 3: 1–448.

  • Remane, A. 1955 Morphologie als Homologienforschung. Verh. dtsch. Zool. Ges., Tübingen (1954). Also in: Zool. Anz., Suppl. 18: 159–183.

    Google Scholar 

  • Remane, A. 1958. Zur Verwandtschaft und Ableitung der niederen Metazoen. Zool. Anz., Suppl. 21: 179–195.

    Google Scholar 

  • Remane, A. 1960. Die Beziehungen Zwischen Phylogenie und Ontogenie. Zool. Anz., 164: 306–337.

    Google Scholar 

  • Remane, A. 1963. The systematic position and phylogeny of the pseudocoelomates. in: ‘The lower Metazoa’, E. C. Dougherty ed., Unif. Calif Press, p. 247–255.

  • Remane, A., Storch, V. & Welsch, V. 1972. Kurzes Lehrbuch der Zoologie. I–X, Stuttgart, G. Fischer ed., p. 1–493.

    Google Scholar 

  • Remane, A., Storch, V. & Welsch, U. 1976. Systematische Zoologie. Stuttgart. p. 1–678.

  • Röhlich, P., Aros, B. & Viragh, S. 1970. Fine structure of photoreceptor cells in the earthworm Lumbricus terrestris. Z. Zellforsch., 104: 345–357.

    PubMed  Google Scholar 

  • Ruttner-Kolisko, A. 1963. The interrelationships of the Rotatoria. in: ‘The Lower Metazoa’, E. C. Dougherty ed., Univ. Calif. Press, p. 263–272.

  • Ruttner-Kolisko, A. 1972. Plankton Rotifers. Biology and Taxonomy. Binnengewässer, 26: 99–234.

    Google Scholar 

  • Salvini-Plawen, L. V. & Mayr, E. 1977. On the evolution of photoreceptors and eyes. Evolutionary Biol., 10: 207–263.

    Google Scholar 

  • Saunders, D. S. 1976. Insect Clocks. Pergamon Press. 280 p.

  • Schaller, H. C. 1976. Action of a neurohormone from Hydra. in: ‘Actualités sur les hormones d'invertébrés’, Colloques Internat. C.N.R.S., 251: 33–38.

    Google Scholar 

  • Schramm, U. 1978a. On the excretory system of the rotifer Habrotrocha rosa Donner. Cell tiss. Res., 189: 515–524.

    Google Scholar 

  • Schramm, U. 1978b. Studies on the ultrastucture of the integument of the Rotifer Habrotrocha rosa Donner (Aschelminthes). Cell tiss. Res., 189: 167–177.

    Google Scholar 

  • Short, R. B. & Gagne, H. T. 1975. Fine structure of a possible photoreceptor in cercariae of Schistosoma mansoni. J. Parsitol., 61: 69–74.

    Google Scholar 

  • Starkweather, P. L. 1980. Aspects of the feeding behavior and trophic ecology of suspensionfeeding rotifers. In this volume, pp. 63–72.

  • Steinböck, O. 1952. Keimblätterlehre und Gastraea-Theorie. Pyramide, 2: 13–15; 26–31.

    Google Scholar 

  • Steinböck, O. 1958. Zur Phylogenie der Gastrotrichen. Zool. Anz., Suppl. 21: 128–169; Schlusswort zur Diskussion RemaneSteinbock. Ibid p. 196–218.

    Google Scholar 

  • Steinböck, O. 1963. Origin and affinities of the Lower Metazoa: the ‘aceloid’ ancestry of the Eumetazoa. In: ‘The Lower Metazoa’, Dougherty, E. C. ed., Univ. Calif. Press, p. 40–54.

  • Storch, V. & Welsch, U. 1969. Über den Aufbau des Rotatorienintegumentes. Z. Zellforsch., 95: 405–414.

    PubMed  Google Scholar 

  • Swiderski, Z., Euzet, L. & Schonenberger, N. 1975. Ultrastructures du système néphridien des Cestodes Cyclophyllides. Cellule, 71: 7–18.

    Google Scholar 

  • Teuchert, G. 1973. Die Feinstruktur des Protonephridialsystems von Turbanella cornuta Remane, einem marinen Gastrotisch der Ordnung Macrodasyoidea. Z. Zellforsch., 136: 277–289.

    Article  PubMed  Google Scholar 

  • Vanfleteren, J. R. & Coomans, A. 1975. Photoreceptor evolution and phylogeny. Z. Zool. Syst. Evolut. -forsch, 14: 157–169.

    Google Scholar 

  • Viaud, G. 1940–1943 Recherches expérimentales sur le phototropisme des Rotiferes: Bull. Biol. Fr. Belg., 74: 249–308 (1940); 77: 68–93 (1943); 77: 224–242 (1943).

    Google Scholar 

  • Villeneuve-Amsellem, J. & Clement, P. 1971. Le neuropile du cerveau de Rotifère:observations ultrastructurales préliminaires. J. Microscopie Fr., 11: 108.

    Google Scholar 

  • Wallace, R. 1980. Ecology of sessile rotifers. In this volume, pp. 181–193.

  • Ward, S., Thomson, N., White, J. G. & Brenner, S. 1975. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J. Comp. Neurology, 160: 313–337.

    Google Scholar 

  • Ware, R. W., Clark, D., Crossland, K. & Russell, R. L. 1975. The nerve ring of the nematode Caenorhabditis elegans: sensory input and motor output. J. Comp. Neurology, 162: 71–110.

    Google Scholar 

  • Warner, F. D. 1969. The fine structure of the protonephridia in the Rotifer Asplanchna. J. Ultrastructure Res., 29: 499–524.

    Google Scholar 

  • Wergin, W. P. & Endo, B. Y. 1976. Ultrastructure of a neurosensory organ in a root-knot nematode. J. Ultrastructure Res., 56: 258–276.

    Google Scholar 

  • Wilson, E. O. 1979. L'humaine nature. Essai de sociobiologie. ed. Stock, Paris, 318 p. Wilson, R. A. 1970. Fine structure of the nervous system and specialized nerve endings in the miracidium of Fasciola hepatica. Parasitol., p. 399–410.

  • Wolken, J. J. 1971. Invertebrate photoreceptors: a comparative analysis. Acad. Press. ed., New York, London.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Clément, P. Phylogenetic relationships of rotifers, as derived from photoreceptor morphology and other ultrastructural analyses. Hydrobiologia 73, 93–117 (1980). https://doi.org/10.1007/BF00019432

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00019432

Keywords

Navigation