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Spermatological characters of the digenean Rubenstrema exasperatum (Rudolphi, 1819) (Plagiorchioidea, Omphalometridae)

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Abstract

We present the first ultrastructural description of spermiogenesis and of the spermatozoon of Rubenstrema exasperatum (Omphalometridae), an intestinal parasite of Sorex araneus (Soricidae). Spermiogenesis begins with the formation of the differentiation zone delimited at the base by the ring of the arched membranes and bordered by cortical microtubules. This area contains two centrioles associated with striated rootlets and with an intercentriolar body. It also contains the nucleus and numerous mitochondria. The intercentriolar body is made up of seven electron-dense layers. The two centrioles give rise to two free flagella that grow orthogonally to the median cytoplasmic process. Additionally, flagellar rotation is followed by the proximodistal fusion of the flagella with the median cytoplasmic process, while the nucleus and mitochondria migrate along the spermatid. The constriction of the ring of arched membranes gives rise to the young spermatozoon. The mature spermatozoon of R. exasperatum shows several ultrastructural characters found in digenean spermatozoa such as two axonemes, mitochondrion, two bundles of parallel cortical microtubules, nucleus, and granules of glycogen. External ornamentation of the plasma membrane and spinelike bodies are also present in the spermatozoon of this species. In the present study, we produced additional spermatological data concerning a previously unexplored family, and we also compare our data to the existent ultrastructural descriptions within the Digenea in order to assess the use of several characters proposed as phylogenetic tools.

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References

  • Agostini S, Miquel J, Ndiaye PI, Marchand B (2005) Dicrocoelium hospes Looss, 1907 (Digenea, Dicrocoeliidae): spermiogenesis, mature spermatozoon and ultrastructural comparative study. Parasitol Res 96:38–48. doi:10.1007/s00436-005-1318-6

    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. doi:10.1017/S0022149X07409816

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Bakhoum AJS, Bâ CT, Fournier-Chambrillon C, Torres J, Fournier P, Miquel J (2009) Spermatozoon ultrastructure of Euryhelmis squamula (Rudolphi, 1819) (Digenea, Opisthorchioidea, Heterophyidae), an intestinal parasite of Mustela vison (Carnivora, Mustelidae). Rev Ibero Latinoam Parasitol 1:32–45

    Google Scholar 

  • Bakhoum AJS, Torres J, Shimalov VV, Bâ CT, Miquel J (2011) Spermiogenesis and spermatozoon ultrastructure of Diplodiscus subclavatus (Pallas, 1760) (Paramphistomoidea, Diplodiscidae), an intestinal fluke of the pool frog Rana lessonae (Amphibia, Anura). Parasitol Int. doi: 10.1016/jparint.2010.10.006

  • Bruňanská M, Nebesářová J, Scholz T (2003) Spermiogenesis in the proteocephalidean cestode Proteocephalus torulosus (Batsch, 1786). Parasitol Res 90:318–324. doi:10.1007/s00436-003-0858-x

    Article  PubMed  Google Scholar 

  • Bruňanská M, Scholz T, Nebesářová J (2004) Reinvestigation of spermiogenesis in the proteocephalidean cestode Proteocephalus longicollis (Zeder, 1800). J Parasitol 90:23–29

    Article  PubMed  Google Scholar 

  • Bruňanská M, Scholz T, Ibraheem MH (2005) Spermiogenesis in the cestode Corallobothrium solidum Fritsch, 1886 (Proteocephalidea: Corallobothriinae). Acta Zool Stockh 86:55–61. doi:10.1111/j.0001-7272.2005.00186.x

    Article  Google Scholar 

  • Burton PR (1972) Fine structure of the reproductive system of a frog lung-fluke. III The 376 spermatozoon and its differentiation. J Parasitol 58:68–83

    Article  PubMed  CAS  Google Scholar 

  • Castilho F, Barandela T (1990) Ultrastructural study on the spermiogenesis and spermatozoon of the metacercariae of Microphallus primas (Digenea), a parasite of Carcinus maenas. Mol Reprod Dev 25:140–146

    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. doi:10.1007/BF00931894

    Article  PubMed  CAS  Google Scholar 

  • Ehlers U (1984) Phylogenetisches System der Plathelminthes. Verh Natwiss Ver Hambg NF 27:291–294

    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. doi:10.1007/s00436-007-0550-7

    Article  PubMed  Google Scholar 

  • Gracenea M, Ferrer JR, González-Moreno O, Trullols M (1997) Ultrastructural study of spermatogenesis and spermatozoon in Postorchigenes gymnesicus (Trematoda, Lecithodendriidae). J Morphol 234:223–232. doi:10.1002/(SICI)1097-4687(199712)234

    Article  Google Scholar 

  • Hoberg EP, Mariaux J, Justine J-L, Brooks DR, Weekes PJ (1997) Phylogeny of the orders 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, Mariaux J, Brooks DR (2001) Phylogeny among 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 

  • Iomini C, Justine J-L (1997) Spermiogenesis and spermatozoon of Echinostoma caproni (Platyhelminthes, Digenea): transmission and scanning electron microscopy, and tubulin immunocytochemistry. Tissue Cell 29:107–118. doi:10.1016/S0040-8166(97)80077-8

    Article  PubMed  CAS  Google Scholar 

  • Justine J-L (1991) The spermatozoa of the schistosomes and the concept of progenetic spermiogenesis. In: Bacceti B (ed) Comparative spermatology 20 years after. Raven, New York, pp 977–979

    Google Scholar 

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

    Google Scholar 

  • Justine J-L (1998) Spermatozoa as phylogenetic characters 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 

  • Justine J-L (2003) Ultrastructure des spermatozoïdes et phylogénie des Neodermata. In: Combes C, Jourdane J (eds) Taxonomie, écologie et évolution des métazoaires parasites. PUP, Perpignan, pp 359–380

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Justine J-L, Jamieson BGM, Southgate VR (1993) Homogeneity of sperm structure in six species of Schistosomes (Digenea, Platyhelminthes). Ann Parasitol Hum Comp 68:185–187

    Google Scholar 

  • Kacem H, Bakhoum AJS, Neifar L, Miquel J (2010) Spermiogenesis and spermatozoon ultrastructure of the digenean Neoapocreadium chabaudi (Apocreadiidae), a parasite of Ballistes capriscus (Pisces, Teleostei). Parasitol Int 59:358–366. doi:10.1016/j.parint.2010.04.008

    Article  PubMed  CAS  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 Looss, 1902 (Digenea, Monorchiidae), a parasite of Diplodus annularis (Pisces, Teleostei). Parasitol Res 93:102–110. doi:10.1007/s00436-004-1115-7

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • 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. doi:10.1111/j.1469-185X.2009.00114.x

    PubMed  Google Scholar 

  • Liu Y, Pan Y (1990) Electron microscope studies of Metorchis (sic) orientalis. III. The spermatozoa and spermatogenesis. J Shangai Agricult College 8:57–62

    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. doi:10.1016/S0020-7519(98)00202-1

    Article  PubMed  CAS  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. doi:10.1007/s004360050047

    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 92:441–453

    Article  PubMed  Google Scholar 

  • Ndiaye PI, Miquel J, Bâ 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 González Castro, 1945 (Digenea, Notocotylidae), intestinal parasite of Microtus agrestis (Rodentia: Arvicolidae) in Spain. Invertebr Reprod Dev 43:105–115

    Article  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): scanning and transmission electron microscopy, and tubulin immunocytochemistry. Acta Parasitol 48:182–194

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Odening K (1959) Das exkretionssystem von Omphalometra und Brachycoelium (Trematoda, Digenea) und die taxonomie der unterordnung Plagiorchiata. Z Parasitenkd 19:442–457. doi:10.1007/BF00259735

    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. doi:10.1007/s00436-007-0636-2

    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. doi:10.1007/s00436-007-0599-3

    Article  PubMed  Google Scholar 

  • Quilichini Y, Foata J, Orsini A, Marchand B (2007c) 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 

  • Quilichini Y, Foata J, Orsini A, Marchand B (2007d) 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, Justine J-L, Bray RA, Marchand B (2010a) Ultrastructural study of the spermatozoon of Heterolebes maculosus (Digenea, Opistholebetidae), a parasite of the porcupinefish Diondon hystrix (Pisces, Teleostei). Parasitol Int 59:427–434. doi:10.1016/j.parint.2010.06.002

    Article  PubMed  CAS  Google Scholar 

  • Quilichini Y, Foata J, Justine J-L, Bray RA, Marchand B (2010b) Spermatozoon ultrastructure of Aponurus laguncula (Digenea: Lecithasteridae), a parasite of Aluterus monoceros (Pisces, Teleostei). Parasitol Int 59:22–28. doi:10.1016/j.parint.2009.06.007

    Article  PubMed  CAS  Google Scholar 

  • Rees FG (1979) The ultrastructure of the spermatozoon and spermiogenesis in Cryptocotyle lingua (Digenea: Heterophyidae). Int J Parasitol 9:405–419. doi:10.1016/0020-7519(79)90044-4

    Article  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 

  • 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 101:259–268. doi:10.1007/s00436-007-0503-1

    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. doi:10.1007/s00436-008-0944-1

    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. doi:10.2478/s11686-008-0006-y

    Article  Google Scholar 

  • Skrjabin KT (1966) Family omphalometridae odening. Osnovy trematodologii. V. XXII. Nauka, Moskva, pp 89–130

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Tkach VV (2008) Family Omphalometridae Looss, 1899. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda. CABI, Wallingford, pp 391–399

    Google Scholar 

  • Tkach V, Grabda-Kazubska B, Swiderski Z (2001) Systematic position and phylogenetic relationships of the family Omphalometridae (Digenea, Plagiorchiida) inferred from partial lsrDNA sequences. Int J Parasitol 31:81–85. doi:10.1016/S0020-7519(00)00154-5

    Article  PubMed  CAS  Google Scholar 

  • ŽĎárská Z, Soboleva TN, Štĕrba J, Valkounová J (1991) Ultrastructure of the male reproductive system of the trematode Brachylaimus aequans. Folia Parasitol Praha 38:33–37

    PubMed  Google Scholar 

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Acknowledgments

This study was partially supported by a DURSI grant (No. 2009SGR-403). We are grateful to Núria Cortadellas and Almudena García (“Serveis Científics i Tècnics” of the University of Barcelona) for their assistance in the preparation of samples. AJS Bakhoum benefits from MAEC-AECID doctoral grants (No. 2009-10 0000448019 and No. 2010-11 0000538055).

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Authors and Affiliations

  1. Laboratori de Parasitologia, Departament de Microbiologia i Parasitologia Sanitàries, Facultat de Farmàcia, Universitat de Barcelona, Av. Joan XXIII, sn, 08028, Barcelona, Spain

    Abdoulaye J. S. Bakhoum, Jordi Torres & Jordi Miquel

  2. Institut de Recerca de la Biodiversitat, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal, 645, 08028, Barcelona, Spain

    Abdoulaye J. S. Bakhoum, Jordi Torres & Jordi Miquel

  3. Laboratoire de Parasitologie-Helminthologie, Département de Biologie Animale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop de Dakar, Dakar, Senegal

    Cheikh Tidiane Bâ

  4. Brest State University, 224665, Brest, Belarus

    Vladimir V. Shimalov

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  1. Abdoulaye J. S. Bakhoum
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  2. Cheikh Tidiane Bâ
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  3. Vladimir V. Shimalov
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Correspondence to Jordi Miquel.

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Bakhoum, A.J.S., Bâ, C.T., Shimalov, V.V. et al. Spermatological characters of the digenean Rubenstrema exasperatum (Rudolphi, 1819) (Plagiorchioidea, Omphalometridae). Parasitol Res 108, 1283–1293 (2011). https://doi.org/10.1007/s00436-010-2178-2

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