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Sperm ultrastructure of the gall bladder fluke Anisocoelium capitellatum (Digenea: Cryptogonimidae), a parasite of Uranoscopus scaber (Pisces: Uranoscopidae)

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Abstract

Ultrastructure of mature spermatozoon of Anisocoelium capitellatum is described with transmission electron microscopy. The description gave evidence of some characteristics of this digenean. The male gamete presents features allowing the distinction between A. capitellatum and other digenetic trematodes. It is characterized by original anterior and posterior extremities. The peripheral doublets appear prior to the central cores in the anterior extremity of axoneme. In the distal part of the spermatozoon, these ultrastructural features are also the first elements disappearing in the axoneme 1 and the last remaining in the axoneme 2. Another important peculiarity of the spermatozoon is the presence of three mitochondria.

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References

  • Agostini S, Miquel J, Ndiaye P, Marchand B (2005) Dicrocoelium hospes Looss, 1907 (Digenea, Dicrocoeliidae): spermiogenesis, mature spermatozoon and ultrastructural comparative study. Parasitol Res 96:38–48

    Article  PubMed  Google Scholar 

  • Ashour AA, Garo K, Gamil IS (2007) Spermiogenesis in two paramphistomes from Nile fish in Egypt: an ultrastructural study. J Helminthol 81:219–226

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Baptista-Farias MFD, Kohn A, Cohen SC (2001) Ultrastructure of spermatogenesis and sperm development in Saccocoelioides godoyi Kohn & Froes, 1986 (Digenea, Haploporidae). Mem Inst Oswaldo Cruz 96:61–70

    Article  PubMed  CAS  Google Scholar 

  • Burton PR (1972) Fine structure of the reproductive system of a frog lung fluke. III. The spermatozoon and its differentiation. J Parasitol 58:68–83

    Article  PubMed  CAS  Google Scholar 

  • Cifrian B, Garcia-Corrales P, Martinez-Alos S (1993) Ultrastructural study of the spermatogenesis and mature spermatozoa of Dicrocoelium dendriticum (Plathelminthes, Digenea). Parasitol Res 79:204–212

    Article  PubMed  CAS  Google Scholar 

  • Cribb TH, Bray RA, Olson PD, Littlewood DTJ (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Adv Parasitol 54:197–254

    Article  PubMed  Google Scholar 

  • Daddow LYM, Jamieson BGM (1983) An ultrastructural study of spermiogenesis in Neochasmus sp. (Cryptogonimidae: Digenea: Trematoda). Aust J Zool 31:1–14

    Article  Google Scholar 

  • Ehlers U (1986) Comments on a phylogenetic system of Platyhelminthes. Hydrobiologia 132:1–12

    Article  Google Scholar 

  • Erwin BE, Halton DW (1983) Fine structural observations on spermatogenesis in a progenetic trematode, Bucephaloides gracilescens. Int J Parasitol 13:413–426

    Article  Google Scholar 

  • Foata J, Quilichini Y, Marchand B (2007) Spermiogenesis and sperm ultrastructure of Deropristis inflata Molin, 1859 (Digenea, Deropristidae), a parasite of Anguilla anguilla. Parasitol Res 101:843–852

    Article  PubMed  Google Scholar 

  • Gracenea M, Ferrer J, Gonzalez-Moreno O (2000) The spermatogenesis and the spermatozoon in Brachylaima sp. (Digenea): ultrastructural study. Acta Parasitol 45:169

    Google Scholar 

  • Iomini C, Justine JL (1997) Spermiogenesis and spermatozoon of Echinostoma caproni (Platyhelminthes, Digenea): transmission and scanning electron microscopy, and tubulin immunocytochemistry. Tissue Cell 29:107–118

    Article  PubMed  CAS  Google Scholar 

  • Jamieson BGM, Daddow LM (1982) The ultrastructure of the spermatozoon of Neochasmus sp. (Cryptogonimidae, Digenea, Trematoda) and its phylogenetic significance. Int J Parasitol 12:547–559

    Article  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(6):1421–1440

    Article  Google Scholar 

  • Justine J-L (1995) Spermatozoal ultrastructure and phylogeny in the parasitic Platyhelminthes. Mem Mus Natl Hist Nat 166:55–86

    Google Scholar 

  • Justine J-L (1999) Spermatozoa of Platyhelminthes: comparative ultrastructure, tubulin immunocytochemistry and nuclear labeling. In: Gagnon C (ed) The male gamete: from basic science to clinical applications. Cache River, Vienna, Illinois, pp 351–362

    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 

  • Justine J-L, Mattei X (1981) Etude ultrastructurale du flagelle spermatique des schistosomes (Trematoda: Digenea). J Ultrastruct Res 76:89–95

    Article  PubMed  CAS  Google Scholar 

  • Justine J-L, Mattei X (1982a) Réinvestigation de l’ultrastructure du spermatozoïde d’Haematoloechus (Trematoda: Haematoloechidae). J Ultrastruct Res 81:322–332

    Article  PubMed  CAS  Google Scholar 

  • Justine J-L, Mattei X (1982b) Etude ultrastructurale de la spermiogenèse et du spermatozoïde d’un plathelminthe: Gonapodasmius (Trematoda: Didymozoidae). J Ultrastruct Res 79:350–365

    Article  PubMed  CAS  Google Scholar 

  • Justine J-L, Mattei X (1983) A spermatozoon with two 9 + 0 axonemes in a parasitic flatworm, Didymozoon (Digenea: Didymozoidea). J Submicr Cytol 15:1101–1105

    Google Scholar 

  • Justine J-L, Mattei X (1984a) Atypical spermiogenesis in a parasitic flatworm, Didymozoon (Trematoda: Digenea: Didymozoidea). J Ultrastruct Res 87:106–111

    Article  Google Scholar 

  • Justine J-L, Mattei X (1984b) Ultrastructural observations on the spermatozoon, oocyte and fertilization process in Gonapodasmius, a gonochoristic trematode (Trematoda: Digenea: Didymozoidae). Acta Zool 65:171–177

    Article  Google Scholar 

  • Levron C, Ternengo S, Marchand B (2003) Ultrastructure of spermiogenesis and the spermatozoon of Helicometra fasciata (Digenea, Opecoelidae), a parasite of Labrus merula (Pisces, Teleostei). Acta Parasitol 48:255–264

    Google Scholar 

  • Levron C, Ternengo S, Marchand B (2004a) Ultrastructure of spermiogenesis and the spermatozoon of Monorchis parvus (Digenea, Monorchiidae), a parasite of Diplodus annularis (Pisces, Teleostei). Parasitol Res 93:102–110

    Article  PubMed  Google Scholar 

  • Levron C, Ternengo S, Marchand B (2004b) Spermiogenesis and sperm ultrastructure of Diphterostomum brusinae (Digenea, Zoogonidae), a parasite of Diplodus annularis (Pisces, Teleostei). Parasitol Res 94:147–154

    PubMed  Google Scholar 

  • Levron C, Ternengo S, Marchand B (2004c) Spermiogenesis and sperm ultrastructure of Poracanthium furcatum (Digenea, Opecoelidae), a parasite of Mullus surmuletus (Pisces, Teleostei). Acta Parasitol 49:190–200

    Google Scholar 

  • Littlewood DTJ, Cribb TH, Olson PD, Bray RA (2001) Platyhelminth phylogenetics—a key to understanding parasitism. Belgian J Zool 131:35–46

    Google Scholar 

  • Miquel J, Nourrisson C, Marchand B (2000) Ultrastructure of spermiogenesis and the spermatozoon of Opecoeloides furcatus (Trematoda, Digenea, Opecoelidae), a parasite of Mullus barbatus (Pisces, Teleostei). Parasitol Res 86:301–310

    Article  PubMed  CAS  Google Scholar 

  • Miquel J, Fournier-Chambrillon C, Fournier P, Torres J (2006) Spermiogenesis and spermatozoon ultrastructure of the cranial digenean Troglotrema acutum (Leuckart, 1842). J Parasitol 92:439–453

    Article  Google Scholar 

  • Ndiaye PN, Miquel J, Ba CT, Feliu C, Marchand B (2002) Spermiogenesis and sperm ultrastructure of Scaphiostomum palaearcticum Mas-Coma, Esteban et Valero, 1986 (Trematoda, Digenea, Brachylaimidae). Acta Parasitol 47:259–271

    Google Scholar 

  • Ndiaye PI, Miquel J, Feliu C, Marchand B (2003a) Ultrastructure of spermiogenesis and spermatozoa of Notocotylus neyrai Gonzalez Castro, 1945 (Digenea, Notocotylidae), intestinal parasite of Microtus agrestis (Rodentia: Arvicolidae) in Spain. Invertebr Repr Dev 43:105–115

    Google Scholar 

  • Ndiaye PI, Miquel J, Fons R, Marchand B (2003b) Spermiogenesis and sperm ultrastructure of the liver fluke Fasciola hepatica L., 1758 (Digenea, Fasciolidae): transmission and scanning electron microscopy, and tubulin immunocytochemistry. Acta Parasitol 48:182–194

    Google Scholar 

  • Ndiaye PI, Miquel J, Ba CT, Marchand B (2004) Ultrastructure of spermiogenesis and the spermatozoon of the liver fluke Fasciola gigantica Cobbold, 1856 (Digenea, Fasciolidae), a parasite of cattle in Sénégal. J Parasitol 90:30–40

    Article  PubMed  Google Scholar 

  • Pamplona-Basilio MC, Baptista-Farias MFD, Kohn A (2001) Spermatogenesis and spermiogenesis in Didymocystis wedli Ariola, 1902 (Didymozoidae, Digenea). Mem Inst Oswaldo Cruz 96:1153–1159

    PubMed  CAS  Google Scholar 

  • Quilichini Y, Foata J, Marchand B (2007a) Ultrastructural study of the spermatozoon of Nicolla testiobliquum (Digenea, Opecoelidae) parasite of brown trout Salmo trutta (Pisces, Teleostei). Parasitol Res 101:1295–1301

    Article  PubMed  Google Scholar 

  • Quilichini Y, Foata J, Marchand B (2007b) Ultrastructural study of the spermatozoon of Pronoprymna ventricosa (Digenea, Baccigerinae), parasite of the twaite shad Alosa fallax Lacepede (Pisces, Teleostei). Parasitol Res 101:1125–1130

    Article  PubMed  Google Scholar 

  • Quilichini Y, Foata J, Orsini A, Marchand B (2007c) Ultrastructural study of spermiogenesis and the spermatozoon of Crepidostomum metoecus (Digenea: Allocreadiidae), a parasite of Salmo trutta (Pisces: Teleostei). J Parasitol 93:458–468

    Article  PubMed  Google Scholar 

  • Quilichini Y, Foata J, Orsini A, Marchand B (2007d) Spermiogenesis and spermatozoon ultrastructure of Nicolla wisniewskii (Digenea: Opecoelidae), an intestinal parasite of brown trout Salmo trutta (Pisces: Teleostei). J Parasitol 93:469–478

    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 RD, Halton DW (1982) Fine structural observations on spermatogenesis in Corriga vitta (Trematoda: Dicrocoelidae). Z Parasitenkd 68:53–72

    Article  Google Scholar 

  • Seck MT, Marchand B, Bâ CT (2007) Ultrastructure of spermiogenesis and the spermatozoon of Paramphistomum microbothrium [Fischoeder 1901] (Digenea: Paramphistomidae), a parasite of Bos taurus in Senegal. Parasitol Res 101:653–662

    Article  PubMed  Google Scholar 

  • Seck MT, Marchand B, Bâ CT (2008a) Spermiogenesis and sperm ultrastructure of Cotylophoron cotylophorum (Trematoda, Digenea, Paramphistomidae), a parasite of Bos taurus in Senegal. Parasitol Res 103:157–166

    Article  PubMed  Google Scholar 

  • Seck MT, Marchand B, Bâ CT (2008b) Spermiogenesis and sperm ultrastructure of Carmyerius endopapillatus (Digenea, Gastrothylacidae), a parasite of Bos taurus in Senegal. Acta Parasitol 53:9–18

    Article  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  PubMed  CAS  Google Scholar 

  • Stitt AW, Fairweather I (1990) Spermatogenesis and the fine structure of the mature spermatozoon of the liver fluke, Fasciola hepatica (Trematoda: Digenea). Parasitology 101:395–407

    Article  PubMed  Google Scholar 

  • Tang J, Wang W, Wang G (1998) Studies on ultrastructures of spermatogenesis and sperm in Pseudorhipidocotyle elpichthys. Acta Hydrobiol Sinica 22:168–174

    Google Scholar 

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Authors and Affiliations

  1. University of Corsica, CNRS UMR6134, “Parasites and Mediterranean Ecosystems” Laboratory, BP 52, 20250, Corte, France

    S. Ternengo, Y. Quilichini & B. Marchand

  2. Institute of Aquaculture, Hellenic Centre for Marine Research, Former American Base of Gournes, P.O. Box 2214, Gournes, Heraklion, 71003, Crete, Greece

    S. Ternengo & P. Katharios

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  1. S. Ternengo
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  2. Y. Quilichini
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  3. P. Katharios
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  4. B. Marchand
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Correspondence to S. Ternengo.

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Ternengo, S., Quilichini, Y., Katharios, P. et al. Sperm ultrastructure of the gall bladder fluke Anisocoelium capitellatum (Digenea: Cryptogonimidae), a parasite of Uranoscopus scaber (Pisces: Uranoscopidae). Parasitol Res 104, 801–807 (2009). https://doi.org/10.1007/s00436-008-1259-y

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  • DOI: https://doi.org/10.1007/s00436-008-1259-y

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