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Spermiogenesis and spermatozoon ultrastructure of the paruterinid cestode Notopentorchis sp. (Cyclophyllidea)

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Abstract

Ultrastructural characters of the spermiogenesis and mature spermatozoon of Notopentorchis sp. (Cestoda, Cyclophyllidea, Paruterinidae), a parasite from Apus affinis (Aves, Apodiformes, Apodidae) from Gabon, are described by means of transmission electron microscopy. Cytochemical analysis for detection of glycogen was applied. Vestigial striated roots associated with the two centrioles are present in the zone of differentiation. The spermiogenesis is characterized by an external growth of free flagellum followed by a proximodistal fusion of the latter with cytoplasmic protrusion, thus, corresponding to the cestode spermiogenesis of the type III pattern described by Bâ and Marchand (Mem. Mus. Natl. Hist. Nat. 166:87–95, 1995). In the final stage of spermiogenesis, a single crested body appears at the base of the forming spermatozoon. The mature spermatozoon of Notopentorchis sp. is filiform and tapering at both extremities. It consists of five regions differing in their ultrastructural characteristics. The anterior extremity of the mature spermatozoon is characterized by the presence of an apical cone and a single crested body. The cytoplasm contains one axoneme of 9 + “1” type of the trepaxonematan Platyhelminthes, a periaxonemal sheath, a layer of twisted cortical microtubules, transverse intracytoplasmic walls, and granules of glycogen. The nucleus is coiled in spiral around the axoneme. The posterior extremity of the spermatozoon is characterized by the presence of electron-dense material. This structural organization corresponds to the morphology of cestode spermatozoon of type VII as defined by Levron et al. (Biol Rev 85: 523-543, 2010). The comparison of the results with those of the two previous studies on paruterinids suggests that several characters of the spermiogenesis and the mature spermatozoon are invariable, i.e. the type III spermiogenesis and the presence of vestigial striated roots, a single crested body, a periaxonemal sheath, and intracytoplasmic walls. The main differences of the sperm cells among members of this family are the lack of dense granules (as in Triaenorhina rectangula) and the presence of electron-dense material in the posterior extremity of the spermatozoon (as in Notopentorchis sp.).

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References

  • Bâ A, Bâ CT, Quilichini Y, Dieng T, Marchand B (2011) Ultrastructure of the spermatozoon of Taeniarhynchus saginatus (syn. Taenia saginata) (Goeze, 1782) Weinland, 1858 (Cestoda, Taeniidae) an intestinal parasite of human. Parasitol Res 108:831–836

    Article  PubMed  Google Scholar 

  • Bâ CT, Marchand B (1994a) 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

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

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

    Article  Google Scholar 

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

  • Bâ CT, Marchand B (1995) Spermiogenesis, spermatozoa and phyletic affinities in the Cestoda. Mém Mus Natn Hist Nat 166:87–95

    Google Scholar 

  • Bâ CT, Bâ A, Marchand B (2005a) Ultrastructure of the spermatozoon of Raillietina (Raillietina) baeri (Cyclophyllidea, Davaineidae) an intestinal parasite of the multimammate rat, Mastomys huberti (Rodentia, Muridae). Parasitol Res 97:173–178

    Article  PubMed  Google Scholar 

  • Bâ CT, Bâ A, Marchand B (2005b) Ultrastructure of the spermatozoon of Paroniella reynoldsae (Cyclophyllidea, Davaineidae) an intestinal parasite of Corvus albus (Aves, Corvidae). Acta Parasitol 50:208–214

    Google Scholar 

  • Eira C, Miquel J, Vingada J, Torres J (2006) Spermiogenesis and spermatozoon of the cestode Mosgovoyia ctenoides (Cyclophyllidea: Anoplocephalidae), an intestinal parasite of Oryctolagus cuniculus (Lagomorpha, Leporidae). J Parasitol 92:708–718

    Article  PubMed  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Georgiev BB, Bray RA (1991) Notopentorchis cyathiformis (Froelich, 1791) comb. n. and N. iduncula (Spassky, 1946) (Cestoda: Paruterinidae) from Palaearctic swifts (Aves: Apodiformes), with a review of the genus Notopentorchis Burt, 1938. Syst Parasitol 20:121–133

    Article  Google Scholar 

  • Georgiev BB, Kornyushin VV (1994) Family Paruterinidae Fuhrmann, 1907 (sensu lato). In: Khalil LF, Jones A, Bray RA (eds) Keys to the cestode parasites of vertebrates. CAB International, Wallingford, UK, pp 559–584

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hoberg EP, Mariaux J, Justine J-L, Brooks DR, Weekes PJ (1997) Phylogeny of the Eucestoda (Cercomeromorphae) based on comparative morphology: historical perspectives and a new working hypothesis. J Parasitol 83:1128–1147

    Article  PubMed  CAS  Google Scholar 

  • Hoberg EP, Jones A, Bray RA (1999) Phylogenetic analysis among the families of the Cyclophyllidea (Eucestoda) based on comparative morphology, with new hypotheses for co-evolution in vertebrates. Syst Parasitol 42:51–73

    Article  PubMed  CAS  Google Scholar 

  • Hoberg EP, Mariaux J, Brooks DR (2001) Phylogeny among the orders of the Eucestoda (Cercomeromorphae): integrating morphology, molecules and total evidence. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor and Francis, London, pp 112–126

    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

    Article  Google Scholar 

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

    Article  PubMed  CAS  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

    Google Scholar 

  • Kornyushin VV (1989) [Fauna of Ukraine. Volume 33. Monogenea and Cestoda. Part 3. Davaineoidea. Biuterinoidea. Paruterinoidea] Kiev, Naukova Dumka, pp 252 (In Russian)

  • Levron C, Miquel J, Oros M, Scholz T (2010) Spermatozoa of tapeworms (Platyhelminthes, Eucestoda): advances in ultrastructural and phylogenetic studies. Biol Rev 85:523–543

    PubMed  Google Scholar 

  • Li H-Y, Brennan JP, Halton DW (2003) Spermatogenesis, spermiogenesis and spermatozoon in the cestode (Moniezia expansa) (Cyclophyllidea, Anoplocephalidae). Acta Zool Sin 49:370–379

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Marigo AM, Bâ C, Miquel J (2011) Spermiogenesis and spermatozoon ultrastructure of the dilepidid cestode Molluscotaenia crassiscolex (von Linstow, 1890), an intestinal parasite of the common shrew Sorex aureus. Acta Zool (Stockh) 92:116–125

    Article  Google Scholar 

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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Miquel J, Hidalgo C, Feliu C, Marchand B (2000) Sperm ultrastructure of Taenia mustelae (Cestoda, Taeniidae), an intestinal parasite of the weasel, Mustela nivalis (Carnivora). Invertebr Reprod Dev 38:43–51

    Article  Google Scholar 

  • Miquel J, Świderski Z, Młocicki D, Eira C, Marchand B (2005a) Ultrastructure of spermatogenesis of the anoplocephalid cestode Gallegoides arfaai (Mobedi et Ghadirian, 1977) Tenora et Mas-Coma, 1978. Acta Parasitol 50:132–144

    Google Scholar 

  • Miquel J, Świderski Z, Marchand B (2005b) Spermatological characters in the Dipylidiidae Stiles, 1896 (Cestoda, Cyclophyllidea). Acta Parasitol 50:65–73

    Google Scholar 

  • Miquel J, Eira C, Świderski Z, Conn DB (2007) Mesocestoides lineatus (Goeze, 1782) (Mesocestoididae): new data on sperm ultrastructure. J Parasitol 93:545–552

    Article  PubMed  Google Scholar 

  • Miquel J, Foronda P, Torres J, Świderski Z, Feliu C (2009a) Ultrastructural study of the spermatozoon of Taenia taeniaeformis (Batsch, 1786) (Cestoda, Cyclophyllidea, Taeniidae), an intestinal parasite of Felis catus from La Palma (Canary Islands, Spain). Parasitol Res 104:1477–1483

    Article  PubMed  Google Scholar 

  • Miquel J, Świderski Z, Foronda P, Torres J, Feliu C (2009b) Ultrastructure of spermatogenesis of Taenia taeniaeformis (Batsch, 1786) (Cestoda, Cyclophyllidea, Taeniidae) and comparison of spermatological characters in the family Taeniidae Ludwig, 1886. Acta Parasitol 54:230–243

    Article  Google Scholar 

  • Miquel J, Torres J, Foronda P, Feliu C (2010) Spermiogenesis and spermatozoon ultrastructure of the davaineid cestode Raillietina micracantha (Fuhrmann, 1909). Acta Zool (Stockh) 91:212–221

    Article  Google Scholar 

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

    Google Scholar 

  • Ndiaye PI, Miquel J, Marchand B (2003a) 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 

  • Ndiaye PI, Agostini S, Miquel J, Marchand B (2003b) 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

    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

    Article  PubMed  CAS  Google Scholar 

  • Robinson JM, Bogitsh BJ (1978) A morphological and cytochemical study of sperm development in Hymenolepis diminuta. Z Parasitenkd 56:81–92

    Article  Google Scholar 

  • Thiéry JP (1967) Mise en evidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc 6:987–1018

    Google Scholar 

  • Waeschenbach A, Webster BL, Bray RA, Littlewood DTJ (2007) Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Mol Phylogenet Evol 45:311–325

    Article  PubMed  CAS  Google Scholar 

  • Willms K, Caro JA, Robert L (2003) Ultrastructure of spermatogonia and spermatocyte lobules in Taenia solium strobilae (Cestoda, Cyclophyllidea, Taeniidae) from golden hamsters. Parasitol Res 90:479–488

    Article  PubMed  Google Scholar 

  • Willms K, Robert L, Jimenez JA, Everhart M, Kuhn RE (2004) Ultrastructure of spermiogenesis and the spermatozoon in Taenia crassiceps strobilae WFU strain (Cestoda, Cyclophyllidea, Taeniidae) from golden hamsters. Parasitol Res 93:262–267

    Article  PubMed  Google Scholar 

  • Yoneva A, Georgieva K, Mizinska Y, Georgiev BB, Stoitsova SR (2006) Ultrastructure of spermiogenesis and mature spermatozoon of Skrjabinoporus merops (Cyclophyllidea, Metadilepididae). Acta Parasitol 51:200–208

    Article  Google Scholar 

  • Yoneva A, Georgieva K, Nikolov PN, Mizinska Y, Georgiev BB, Stoitsova SR (2009) Ultrastructure of spermiogenesis and mature spermatozoon of Triaenorhina rectangula (Cestoda: Cyclophyllidea: Paruterinidae). Folia Parasitol 56:275–283

    PubMed  Google Scholar 

  • Yoneva A, Georgieva K, Mizinska Y, Nikolov PN, Georgiev BB, Stoitsova SR (2010) Ultrastructure of spermiogenesis and mature spermatozoon of Anonchotaenia globata (von Linstow, 1879) (Cestoda, Cyclophyllidea, Paruterinidae). Acta Zool (Stockh) 91:184–192

    Article  Google Scholar 

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Acknowledgments

We are grateful to Professor Jean Paul Gonzalez (Director General) and the staff of the CIRMF, Republic of Gabon, for their support and assistance during the field trip in November–December 2009. The field studies were supported by the National Science Foundation (USA), PBI grants DEB 0818696 and DEB 0818823.We thank the staff of the Laboratory of Electron Microscopy, Institute of Parasitology, České Budĕjovice, Czech Republic, for their technical assistance. Special thanks are due to Petra Masařová for the invaluable help in the preparation of samples. This study was supported by the Czech science Foundation (project No. P505/12/G112), and partly supported by the National Science Fund, Ministry of Education and Science of the Republic of Bulgaria, Grant DO/02-271/18.12.08.

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Authors and Affiliations

  1. Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Street, 1113, Sofia, Bulgaria

    Aneta Yoneva, Pavel N. Nikolov, Yana Mizinska & Boyko B. Georgiev

  2. Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05, České Budějovice, Czech Republic

    Céline Levron

  3. Natural History Museum of Geneva, CP 6434, 1211 Geneva 6, Switzerland

    Jean Mariaux

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  1. Aneta Yoneva
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  2. Céline Levron
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  3. Pavel N. Nikolov
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  4. Yana Mizinska
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  5. Jean Mariaux
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  6. Boyko B. Georgiev
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Correspondence to Aneta Yoneva.

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Yoneva, A., Levron, C., Nikolov, P.N. et al. Spermiogenesis and spermatozoon ultrastructure of the paruterinid cestode Notopentorchis sp. (Cyclophyllidea). Parasitol Res 111, 135–142 (2012). https://doi.org/10.1007/s00436-011-2809-2

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