Acta Parasitologica

, Volume 55, Issue 1, pp 58–65 | Cite as

Spermiogenesis and spermatozoon of the tapeworm Parabothriocephalus gracilis (Bothriocephalidea): Ultrastructural and cytochemical studies

  • Lenka Šípková
  • Céline Levron
  • Mark Freeman
  • Tomáš Scholz


Spermiogenesis and spermatozoon ultrastructure of the tapeworm Parabothriocephalus gracilis were described using transmission electron microscopy (TEM). Spermiogenesis is characterized by the formation of a zone of differentiation with two centrioles associated with striated rootlets, and an intercentriolar body between them. The two flagella undergo a rotation of 90° until they become parallel to the median cytoplasmic extension with which they fuse. Electron-dense material is present in the apical region of the zone of differentiation in the early stages of spermiogenesis. This electron-dense material is characteristic for the orders Bothriocephalidea and Diphyllobothriidea. The mature spermatozoon contains two axonemes of the 9 + ‘1’ trepaxonematan pattern, nucleus, parallel cortical microtubules and electron-dense granules of glycogen. The anterior extremity of the spermatozoon exhibits a single helical electron-dense crested body 130 nm thick. One of the most interesting features is the presence of a ring of cortical microtubules surrounding the axoneme. This character has been reported only for species of the order Bothriocephalidea and may be unique in this cestode group.


Eucestoda Bothriocephalidea Parabothriocephalus gracilis spermiogenesis spermatozoon ultrastructure 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bâ C.T., Bâ A., Marchand B. 2007. Ultrastructure of the spermatozoon of Bothriocephalus claviceps (Cestoda, Pseudophyllidea): a parasite of Anguilla anguilla (Fish, Teleostei). Parasitology Research, 101, 77–83. DOI: 10.1007/s00436-006-0445-z.CrossRefPubMedGoogle Scholar
  2. Bâ C.T., Marchand B. 1995. Spermiogenesis, spermatozoa and phyletic affinities in the Cestoda. In: (Eds. B.G.M. Jamieson, J. Ausió and J.-L. Justine) Advances in spermatozoal phylogeny and taxonomy. Mémoires du Muséum National d’Histoire Naturelle, 166, 87–95.Google Scholar
  3. Bonsdorff C.H. von, Telkkä A. 1965. The spermatozoon flagella inDiphyllobothrium latum (fish tapeworm). Zeitschrift für Zellforschung und Mikroskopische Anatomie, 66, 643–648. DOI: 10.1007/BF00339248.CrossRefGoogle Scholar
  4. Brabec J., Kuchta R., Scholz T. 2006. Paraphyly of the Pseudophyllidea (Platyhelminthes: Cestoda): Circumscription of monophyletic clades based on phylogenetic analysis of ribosomal RNA. International Journal for Parasitology, 36, 1535–1541. DOI: 10.1016/j.ijpara.2006.08.003.CrossRefPubMedGoogle Scholar
  5. Brooks D.R. 1989. The phylogeny of the Cercomeria (Platyhelminthes: Rhabdocoela) and general evolutionary principles. Journal of Parasitology, 75, 606–616.CrossRefPubMedGoogle Scholar
  6. Bruňanská M., Nebesářová J. Spermiogenesis in the pseudophyllidean cestode Eubothrium crassum Bloch, 1779. Parasitology Research, 87, 579–588. DOI: 10.1007/s004360100392.Google Scholar
  7. Bruňanská M., Nebesářová J. Scholz T., Fagerholm H.-P. 2002. Ultrastructure of the spermatozoon of the pseudophyllidean cestode Eubothrium crassum (Bloch, 1779). Parasitology Research, 88, 285–291. DOI: 10.1007/s00436-001-0532-0.CrossRefPubMedGoogle Scholar
  8. Bruňanská M., Poddubnaya L.G. 2006. Spermiogenesis in the caryophyllidean cestode Khawia armeniaca Cholodkovski, 1915. Parasitology Research, 99, 449–454. DOI: 10.1007/s00436-006-0155-6.CrossRefPubMedGoogle Scholar
  9. Bruňanská M., Scholz T., Dezfuli B.S., Poddubnaya L.G. 2006. Spermiogenesis and sperm ultrastructure of Cyathocephalus truncatus (Pallas, 1781) Kessler, 1868 (Cestoda: Spathebothriidea). Journal of Parasitology, 92, 884–892. DOI: 10.1645/GE-718R1.1.CrossRefPubMedGoogle Scholar
  10. Ehlers U. 1984. Phylogenetisches System der Platyhelminthes. Verhandlungen des Naturwissenschaftlichen Vereins in Hamburg (NF), 27, 291–294.Google Scholar
  11. Ehlers U. 1985. Das Phylogenetische System der Platyhelminthes. G. Fischer, Stuttgart, Germany, 317 pp.Google Scholar
  12. Ehlers U. 1986. Comments on a phylogenetic system of the Platyhelminthes. Hydrobiologia, 132, 1–12. DOI: 10.1007/BF00046222.CrossRefGoogle Scholar
  13. Euzet L., Świderski Z., Mokhtar-Maamouri F. 1981. Ultrastructure comparée du spermatozoide des cestodes. Relation avec la phylogénèse. Annales de Parasitologie (Paris), 56, 247–259.Google Scholar
  14. Gamil I.S. 2008. Ultrastructural studies of the spermatogenesis and spermiogenesis of the caryophyllidean cestode Wenyonia virilis (Woodland, 1923). Parasitology Research, 103, 777–785. DOI: 10.1007/s00436-008-1040-2.CrossRefPubMedGoogle Scholar
  15. Justine J.-L. 1986. Ultrastructure of the spermatozoon of the cestode Duthiersia fimbriata Diesing, 1854 (Pseudophyllidea, Diphyllobothriidae). Canadian Journal of Zoology, 64, 1545–1548. DOI: 10.1139/z86-230.CrossRefGoogle Scholar
  16. Justine J.-L. 1998. Spermatozoa as phylogenetic characters for the Eucestoda. Journal of Parasitology, 84, 385–408. DOI: 10.2307/3284502.CrossRefPubMedGoogle Scholar
  17. Justine J.-L. 2001. Spermatozoa as phylogenetic characters for the Platyhelminthes. In: (Eds. D.T.J. Littlewood and R.A. Bray) Interrelationships of the Platyhelminthes. Taylor and Francis, London, New York, 231–238.Google Scholar
  18. Kuchta R., Scholz T., Brabec J., Bray R.A. 2008. Suppression of the tapeworm order Pseudophyllidea (Platyhelminthes: Eucestoda) and proposal of two new orders, Bothriocephalidea and Diphyllobothriidea. International Journal for Parasitology, 38, 49–55. DOI: 10.1016/j.ijpara.2007.08.005.CrossRefPubMedGoogle Scholar
  19. Levron C., Bruňanská M., Kuchta R., Freeman M., Scholz T. 2006b. Spermatozoon ultrastructure of the pseudophyllidean cestode Paraechinophallus japonicus, a parasite of deep-sea fish Psenopsis anomala (Perciformes, Centrolophidae). Parasitology Research, 100, 115–121. DOI: 10.1007/s00436-006-0224-x.CrossRefPubMedGoogle Scholar
  20. Levron C., Bruňanská M., Marchand B. 2005. Spermiogenesis and sperm ultrastructure of the pseudophyllidean cestode Triaenophorus nodulosus (Pallas, 1781). Parasitology Research, 98, 26–33. DOI: 10.1007/s00436-005-0009-7.CrossRefPubMedGoogle Scholar
  21. Levron C., Bruňanská M., Poddubnaya L.G. 2006c. Spermatological characters in Diphyllobothrium latum (Cestoda, Pseudophyllidea). Journal of Morphology, 267, 1110–1119. DOI: 10.1002/jmor.10460.CrossRefPubMedGoogle Scholar
  22. Levron C., Bruňanská M., Poddubnaya L.G. 2006a. Spermatological characters of the pseudophyllidean cestode Bothriocephalus scorpii Müller, 1776. Parasitology International, 55, 113–120. DOI: 10.1016/j.parint.2005.11.055.CrossRefPubMedGoogle Scholar
  23. Levron C., Sitko J., Scholz T. 2009. Spermiogenesis and spermatozoon of the tapeworm Ligula intestinalis (Diphyllobothriidea): Phylogenetic implications. Journal of Parasitology, 95, 1–9. DOI: 10.1645/GE-1646.1.CrossRefPubMedGoogle Scholar
  24. MacKinnon B.M., Burt M.D.B. 1985. Ultrastructure of spermatogenesis and the mature spermatozoon of Haplobothrium globuliforme Cooper, 1914 (Cestoda: Haplobothrioidea). Canadian Journal of Zoology, 63, 1478–1487. DOI: 10.1139/z85-221.CrossRefGoogle Scholar
  25. Miquel J., Eira C., Świderski Z., Conn D.B. 2007b. Mesocestoides lineatus (Goeze, 1782) (Mesocestoididae): new data on sperm ultrastructure. Journal of Parasitology, 93, 545–552. DOI: 10.1645/GE-1008R.1.CrossRefPubMedGoogle Scholar
  26. Miquel J., Świderski Z. 2006. Ultrastructure of the spermatozoon of Dollfusiella spinulifera (Beveridge and Jones, 2000) Beveridge, Neifar and Euzet, 2004 (Trypanorhyncha, Eutetrarhynchidae). Parasitology Research, 99, 37–44. DOI: 10.1007/s00436-005-0094-7.CrossRefPubMedGoogle Scholar
  27. Miquel J., Świderski Z., Mackiewicz J.S., Ibraheem M.H. 2008. Ultrastructure of spermiogenesis in the caryophyllidean cestode Wenyonia virilis Woodland, 1923, with re-assessment of flagellar rotation in Glaridacris catostomi Cooper, 1920. Acta Parasitologica, 53, 19–29. DOI: 10.2478/s11686-008-0013-z.CrossRefGoogle Scholar
  28. Miquel J., Świderski Z., Neifar L., Eira C. 2007a. Ultrastructure of the spermatozoon of Parachristianella trygonis Dollfus, 1946 (Trypanorhyncha: Eutetrarhynchidae). Journal of Parasitology, 93, 1296–1302. DOI: 10.1645/GE-1193.1.CrossRefPubMedGoogle Scholar
  29. Olson P.D. 2008. Hox genes and the parasitic flatworms: New opportunities, challenges and lessons from the free-living. Parasitology International, 57, 8–17. DOI: 10.1016/j.parint.2007.09.007.CrossRefPubMedGoogle Scholar
  30. Świderski Z. 1968. The fine structure of the spermatozoon of sheep tapeworm, Moniezia expansa (Rud., 1810) (Cyclophyllidea, Anoplocephalidae). Zoologica Poloniae, 18, 475–486.Google Scholar
  31. Świderski Z. 1986. Three types of spermiogenesis in cestodes. In: Electron Microscopy — 1986. Proceedings of the XI International Congress of Electron Microscopy, Kyoto, Japan, 2959–2960.Google Scholar
  32. Świderski Z., Mackiewicz J.S. 2002. Ultrastructure of spermatogenesis and spermatozoa of the caryophyllidean cestode Glaridacris catostomi Cooper, 1920. Acta Parasitologica, 47, 83–104.Google Scholar
  33. Świderski Z., Mokhtar-Maamouri F. 1980. Etude de la spermatogénèse de Bothriocephalus clavibothrium Ariola, 1899 (Cestoda: Pseudophyllidea). Archives de l’Institut Pasteur de Tunis, 57, 323–357.PubMedGoogle Scholar
  34. Thiéry J.-P. 1967. Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. Journal of Microscopy, 6, 987–1018.Google Scholar
  35. Waeschenbach A., Webster B.L., Bray R.A., Littlewood D.T.J. 2007. Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Molecular Phylogenetics and Evolution, 45, 311–325. DOI: 10.1016/j.ympev.2007.03.019.CrossRefPubMedGoogle Scholar

Copyright information

© © Versita Warsaw and Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Lenka Šípková
    • 1
    • 2
  • Céline Levron
    • 1
  • Mark Freeman
    • 3
  • Tomáš Scholz
    • 1
  1. 1.Institute of ParasitologyBiology Centre of the Academy of Sciences of the Czech RepublicČeské BudějoviceCzech Republic
  2. 2.Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic
  3. 3.Institute of Biological SciencesUniversity of MalayaKuala LumpurMalaysia

Personalised recommendations