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Ultrastructure of spermiogenesis and the spermatozoon in the genus Joyeuxiella Fuhrmann, 1935 (Cestoda, Cyclophyllidea, Dipylidiidae): comparative analysis of J. echinorhynchoides (Sonsino, 1889) and J. pasqualei (Diamare, 1893)

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Abstract

This paper describes the ultrastructure of spermiogenesis and the mature spermatozoon of two Dipylidiidae cestodes, Joyeuxiella echinorhynchoides and J. pasqualei. In both species, spermiogenesis follows the type III described by Bâ and Marchand for the cyclophyllideans. Nevertheless, it is interesting to note the presence of striated roots associated with the centrioles. The spermatozoon presents the same ultrastructural features in J. echinorhynchoides and J. pasqualei. The apical cone in the anterior extremity of the sperm is more than 2.0 μm long in both J. echinorhynchoides and J. pasqualei. Both species present a single crest-like body, 150 nm thick in J. echinorhynchoides and 75 nm thick in J. pasqualei. The cortical microtubules are spiralled at an angle of 40–45° to the spermatozoon axis in both Joyeuxiella species. A periaxonemal sheath and glycogen granules are also described in the mature sperm. We also describe, for the first time, the disposition of glycogen granules in two opposed and spiralled cords in cestodes and the formation of the periaxonemal sheath in the final stage of spermiogenesis.

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References

  • Azzouz-Draoui N (1985) Étude ultrastructurale comparée de la spermiogenèse et du spermatozoïde de quatre Cestodes Diphyllidea. Thesis, University of Tunis, Tunis

  • Azzouz-Draoui N, Mokhtar-Maamouri F (1986/88) Ultrastructure comparée de la spermiogenèse et du spermatozoïde de Echinobothrium affine Diesing, 1863 et E. harfordi MacVicar, 1976 (Cestoda, Diphyllidea). Bull Soc Sci Nat Tunisie 18:9–20

    Google Scholar 

  • Bâ A, Bâ CT, Marchand B (2000) Ultrastructure of spermiogenesis and the spermatozoon of Sudarikovina taterae (Cestoda, Cyclophyllidea, Anoplocephalidae) intestinal parasite of Tatera gambiana (Rodentia, Gerbillidae). J Submicrosc Cytol Pathol 32:137–144

    PubMed  Google Scholar 

  • Bâ A, Bâ CT, Marchand B (2002) Ultrastructural study of the spermatozoon of Echinocotyle dolosa (Cestoda, Cyclophyllidea, Hymenolepididae). Acta Parasitol 47:131–136

    Google Scholar 

  • Bâ CT, Marchand B (1992a) Ultrastructural particularities of the spermatozoon of Stilesia globipunctata (Cestoda) parasite of the small intestine of sheep and goats in Senegal. J Submicrosc Cytol Pathol 24:29–34

    Google Scholar 

  • Bâ CT, Marchand B (1992b) Reinvestigation of the ultrastructure and the spermatozoon of Hymenolepis nana (Cestoda, Cyclophyllidea), parasite of the small intestine of Rattus rattus. Mol Reprod Dev 33:39–45

    PubMed  Google Scholar 

  • Bâ CT, Marchand B (1994a) Comparative ultrastructure of the spermatozoa of Inermicapsifer guineensis and I. madagascariensis (Cestoda, Anoplocephalidae, Inermicapsiferinae) intestinal parasites of rodents in Senegal. Can J Zool 72:1633–1638

    Google Scholar 

  • Bâ CT, Marchand B (1994b) Ultrastructure of spermiogenesis and the spermatozoon of Mathevotaenia herpestis (Cestoda), intestinal parasite of Atelerix albiventrix in Sénégal. Acta Zool (Stockh) 75:167–175

    Google Scholar 

  • Bâ CT, Marchand B (1994c) Similitude ultrastructurale des spermatozoïdes de quelques Cyclophyllidea. Parasite 1:51–55

    PubMed  Google Scholar 

  • Bâ CT, Marchand B (1994d) Ultrastructure of spermiogenesis and the spermatozoon of Raillietina (Raillietina) tunetensis (Cyclophyllidea, Davaineidae) intestinal parasite of turtle doves in Senegal. Int J Parasitol 24:237–248

    Google Scholar 

  • Bâ CT, Marchand B (1994e) Ultrastructure of spermiogenesis and the spermatozoon of Aporina delafondi (Cyclophyllidea, Anoplocephalidae) intestinal parasite of turtle doves in Senegal. Int J Parasitol 24:225–235

    Google Scholar 

  • Bâ CT, Marchand B (1995) Spermiogenesis, spermatozoa and phyletic affinities in the Cestoda. In: Jamieson BGM, Ausió J, Justine JL (eds) Advances in spermatozoal phylogeny and taxonomy. Mem Mus Natl Hist Nat 166:87–95

    Google Scholar 

  • Bâ CT, Marchand B (1998) Ultrastructure of spermiogenesis and the spermatozoon of Vampirolepis microstoma (Cestoda, Hymenolepididae), intestinal parasite of Rattus rattus. Microsc Res Tech 42:218–225

    PubMed  Google Scholar 

  • Bâ CT, Marchand B, Mattei X (1991) Demonstration of the orientation of the Cestodes spermatozoon illustrated by the ultrastructural study of spermiogenesis of a Cyclophyllidea: Thysaniezia ovilla, Rivolta, 1874. J Submicrosc Cytol Pathol 23:606–612

    Google Scholar 

  • Barrett NJ, Smyth JD (1983) Observations on the structure and ultrastructure of sperm development in Echinococcus multilocularis, both in vitro and in vivo. Parasitology 87:li

    Google Scholar 

  • Brunanska M, Nebesarova J, Scholz T, Fagerholm H-P (2001) Spermiogenesis in the pseudophyllid cestode Eubothrium crassum (Bloch, 1779). Parasitol Res 87:579–588

    CAS  PubMed  Google Scholar 

  • Chomicz L, Swiderski Z (1992) Spermiogenesis and ultrastructure of the ultrastructure of the cestode Dicranotaenia coronula (Dujardin, 1845) (Cyclophyllidea, Hymenolepidae). Proceedings of the 5th Asia-Pacific Electron Microscopy Conference, Beijing, 324–325

  • Euzet L, Swiderski Z, Mokhtar-Maamouri F (1981) Ultrastructure comparée du spermatozoïde des Cestodes. Relations avec la phylogénèse. Ann Parasitol Hum Comp 56:247–259

    CAS  PubMed  Google Scholar 

  • Featherston DW (1971) Taenia hydatigena. III. Light and electron microscope study of spermatogenesis. Z Parasitenkd 37:148–168

    CAS  PubMed  Google Scholar 

  • Hidalgo C, Miquel J, Torres J, Marchand B (2000) Ultrastructural study of spermiogenesis and the spermatozoon in Catenotaenia pusilla, an intestinal parasite of Mus musculus. J Helminthol 74:73–81

    CAS  PubMed  Google Scholar 

  • Jones A (1983) A revision of the cestode genus Joyeuxiella Fuhrmann, 1935 (Dilepididae: Dipylidiinae). Syst Parasitol 5:203–213

    Google Scholar 

  • Justine J-L (1991) Phylogeny of parasitic Platyhelminthes: a critical study of synapomorphies proposed on the basis of the ultrastructure of spermiogenesis and spermatozoa. Can J Zool 69:1421–1440

    Google Scholar 

  • Justine J-L (1998) Spermatozoa as phylogenetic characters for the Eucestoda. J Parasitol 84:385–408

    CAS  PubMed  Google Scholar 

  • Justine J-L (2001) Spermatozoa as phylogenetic characters for the Platyhelminthes. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor and Francis, London, pp 231–238

  • Kelsoe GH, Ubelaker JE, Allison VF (1977) The fine structure of spermiogenesis in Hymenolepis diminuta (Cestoda) with a description of the mature spermatozoon. Z Parasitenkd 54:175–187

    Google Scholar 

  • Khalil LF, Jones A, Bray RA (1994) Keys to the cestode parasites of vertebrates. CAB International, Cambridge

  • Mahendrasingam S, Fairweather I, Halton DW (1989) Spermatogenesis and the fine structure of the mature spermatozoon in the free proglottis of Trilocularia acanthiaevulgaris (Cestoda, Tetraphyllidea). Parasitol Res 75:287–298

    CAS  PubMed  Google Scholar 

  • Mariaux J (1998) A molecular phylogeny of the Eucestoda. J Parasitol 84:114–124

    CAS  PubMed  Google Scholar 

  • Matevosyan EM (1953) Re-organisation of the classification of dilepidid cestodes. Papers on helminthology presented to Academician K.I. Skryabin on his 75th birthday. Izdatel'stvo Akademii Nauk SSSR, Moscow, pp 392–397

  • Matevosyan EM (1963) Principles of cestodology, vol. III. Dilepidoidea, tapeworms of domestic and wild animals. Academiya Nauk SSSR, Moscow

  • Miquel J, Marchand B (1997) Ultrastructure of the spermatozoon of Dipylidium caninum (Cestoda, Cyclophyllidea, Dilepididae), an intestinal parasite of Canis familiaris. Parasitol Res 83:349–355

    CAS  PubMed  Google Scholar 

  • Miquel J, Marchand B (1998) Ultrastructure of spermiogenesis and the spermatozoon of Anoplocephaloides dentata (Cestoda, Cyclophyllidea, Anoplocephalidae), an intestinal parasite of Arvicolidae rodents. J Parasitol 84:1128–1136

    CAS  PubMed  Google Scholar 

  • Miquel J, Bâ CT, Marchand B (1997) Ultrastructure of the spermatozoon of Skrjabinotaenia lobata (Cyclophyllidea, Catenotaeniidae), intestinal parasite of Apodemus sylvaticus (Rodentia, Muridae). J Submicrosc Cytol Pathol 29:521–526

    Google Scholar 

  • Miquel J, Bâ CT, Marchand B (1998) Ultrastructure of spermiogenesis of Dipylidium caninum (Cestoda, Cyclophyllidea, Dipylidiidae), an intestinal parasite of Canis familiaris. Int J Parasitol 28:1453–1458

    Google Scholar 

  • Miquel J, Feliu C, Marchand B (1999) Ultrastructure of spermiogenesis and the spermatozoon of Mesocestoides litteratus (Cestoda, Mesocestoididae). Int J Parasitol 29:499–510

    CAS  PubMed  Google Scholar 

  • Mokhtar-Maamouri F (1979) Étude en microscopie électronique de la spermiogenèse et du spermatozoïde de Phyllobothrium gracile Weld, 1855 (Cestoda, Tetraphyllidea, Phyllobothriidae). Z Parasitenkd 59:245–258

    Google Scholar 

  • Mokhtar-Maamouri F (1982) Étude ultrastructurale de la spermiogenèse de Acanthobothrium filicolle var. filicolle Zschokke, 1888 (Cestoda: Tetraphyllidea, Onchobothriidae). Ann Parasitol Hum Comp 57:429–442

    CAS  PubMed  Google Scholar 

  • Mokhtar-Maamouri F, Azzouz-Draoui N (1984) Spermiogenèse et ultrastructure du spermatozoïde de deux Cestodes Diphyllidea. 4ème Ecole Franco-Africaine Biol Mol, Djerba, Tunisie, pp 467–469

  • Mokhtar-Maamouri F, Azzouz-Draoui N (1990) Spermiogenèse et ultrastructure du spermatozoïde de Nematotaenia chantalae Dollfus, 1957 (Cestoda, Cyclophyllidea, Nematotaeniidae). Ann Parasitol Hum Comp 65:221–228

    Google Scholar 

  • Mokhtar-Maamouri F, Swiderski Z (1975) Étude en microscopie électronique de la spermatogénèse de deux Cestodes Acanthobothrium filicolle benedenii Loennberg, 1889 et Onchobothrium uncinatum (Rud.,1819) (Tetraphyllidea, Onchobothriidae). Z Parasitenkd 47:269–281

    PubMed  Google Scholar 

  • Ndiaye PI, Miquel J, Marchand B (2003) Ultrastructure of spermiogenesis and spermatozoa of Taenia parva Baer, 1926 (Cestoda, Cyclophyllidea, Taeniidae), a parasite of the common genet (Genetta genetta). Parasitol Res 89:34–43

    Article  PubMed  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    CAS  Google Scholar 

  • Schmidt GD (1986) Handbook of tapeworm identification. CRC Press, Boca Raton, Florida

  • Sène A, Bâ CT, Marchand B (1997) Ultrastructure of spermiogenesis and the spermatozoon of Nomimoscolex sp. (Cestoda, Proteocephalidea) intestinal parasite of Clarotes laticeps (Fish, Teleost) in Senegal. J Submicrosc Cytol Pathol 29:1–6

    CAS  PubMed  Google Scholar 

  • Sène A, Bâ CT, Marchand B (1999) Ultrastructure of spermiogenesis of Phyllobothrium lactuca (Cestoda, Tetraphyllidea, Phyllobothriidae). Folia Parasitol 6:191–198

    Google Scholar 

  • Shi DZ, Liu DS, Wang SK, Craig PS (1994) The ultrastructure of Echinococcus multilocularis. Chin J Parasit Dis Control 7:40–41

    Google Scholar 

  • Stoitsova SR, Georgiev BB, Dacheva RB (1995) Ultrastructure of spermiogenesis and the mature spermatozoon of Tetrabothrius erostris Loennberg, 1896 (Cestoda, Tetrabothriidae). Int J Parasitol 25:1427–1436

    Google Scholar 

  • Swiderski Z (1984) Spermatogenesis in the davaineid cestode Inermicapsifer madagascariensis, a parasite of man and rodents: SEM observations. Proceedings of the 23th Annual Conference of the Electron Microscopy Society of South Africa, Stellenbosch, pp 29–130

  • Swiderski Z (1985) Spermiogenesis in the proteocephalid cestode Proteocephalus longicollis. Proceedings of the 24th Annual Conference of the Electron Microscopy Society of South Africa, Pietermaritzburg, pp 181–182

  • Swiderski Z (1994) Spermiogenesis in the Trypanorhinchid Cestode Lacistorhynchus tenuis. Proceedings of the 13th International Congress of Electron Microscopy, Paris, pp 691–692

  • Swiderski Z, Mackiewicz JS (2002) Ultrastructure of spermatogenesis and spermatozoa of the caryophyllidean cestode Glaridacris catostomi Cooper, 1920. Acta Parasitol 47:83–104

    Google Scholar 

  • Swiderski Z, Mokhtar-Maamouri F (1980) Étude de la spermatogénèse de Bothriocephalus clavibothrium Ariola, 1899 (Cestoda: Pseudophyllidea). Arch Inst Pasteur Tunis 57:323–347

    CAS  PubMed  Google Scholar 

  • Swiderski ZP, Tkach VV (1996) Ultrastructure of the spermatozoon of the cestode Monorcholepis dujardini (Cyclophyllidea, Hymenolepididae). Proceedings of the 6th Asia-Pacific Electron Microscopy Conference, Hong Kong, pp 507–508

  • Swiderski Z, Salamatin RV, Tkach VV (2000) Electron microscopial study of spermatozoa of the cestode Dilepis undula (Cyclophyllidea, Dilepididae). Vest Zool 34:3–7

    Google Scholar 

  • Tian X, Yuan L, Li Y, Huo X, Han X, Xu M, Lu M, Dai J, Dong L (1998) Ultrastructural observation on spermatocytogenesis in taeniid cestode. Chin J Parasitol Parasit Dis 16:209–212

    CAS  Google Scholar 

  • Wardle RA, McLeod JA, Radinovsky S (1974) Advances in the zoology of tapeworms, 1950–1970. University of Minnesota Press, Minneapolis

  • Yamaguti S (1959) Systema Helminthum, vol II. The cestodes of vertebrates. Interscience, New York

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Acknowledgements

This study was partially supported by the Spanish projects BOS2000-0570-CO2-01, 2001-SGR-00088 and HF2002-0063. We are grateful to "Serveis Cientificotècnics" of the University of Barcelona for their support in the preparation of materials. Papa Ibnou Ndiaye received a grant from the "Agencia Española de Cooperación Internacional" of the "Ministerio de Asuntos Exteriores" of Spain, and Dr. Sylvia Agostini received a grant from the "Collectivité Territorial de Corse".

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Authors and Affiliations

  1. Laboratori de Parasitologia, Facultat de Farmàcia, Universitat de Barcelona, Av. Joan XXIII s/n, 08028 , Barcelona, Spain

    Papa Ibnou Ndiaye, Sylvia Agostini & Jordi Miquel

  2. Laboratoire Parasites et Écosystèmes Méditerranéens, Faculté des Sciences et Techniques, Université de Corse, 20250, Corte, France

    Sylvia Agostini & Bernard Marchand

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  1. Papa Ibnou Ndiaye
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  2. Sylvia Agostini
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  3. Jordi Miquel
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Correspondence to Jordi Miquel.

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Ndiaye, P.I., Agostini, S., Miquel, J. et al. Ultrastructure of spermiogenesis and the spermatozoon in the genus Joyeuxiella Fuhrmann, 1935 (Cestoda, Cyclophyllidea, Dipylidiidae): comparative analysis of J. echinorhynchoides (Sonsino, 1889) and J. pasqualei (Diamare, 1893). Parasitol Res 91, 175–186 (2003). https://doi.org/10.1007/s00436-003-0936-0

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