Skip to main content
Log in

Spermiogenesis and ultrastructure of the spermatozoon of Wardula capitellata (Digenea, Mesometridae), an intestinal parasite of the sparid teleost Sarpa salpa in Senegal

  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

The spermiogenesis process in Wardula capitellata begins with the formation of a differentiation zone containing two centrioles associated with striated rootlets and an intercentriolar body. Each centriole develops into a free flagellum orthogonal to a median cytoplasmic process. Later these flagella rotate and become parallel to the median cytoplasmic process, which already exhibits two electron-dense areas and spinelike bodies before its proximodistal fusion with the flagella. The final stage of the spermiogenesis is characterized by the constriction of the ring of arched membranes, giving rise to the young spermatozoon, which detaches from the residual cytoplasm. The mature spermatozoon of W. capitellata presents most of the classical characters reported in digenean spermatozoa such as two axonemes of different lengths of the 9 + “1” trepaxonematan pattern, nucleus, mitochondrion, two bundles of parallel cortical microtubules and granules of glycogen. However, some peculiarities such as two lateral expansions accompanied by external ornamentation of the plasma membrane and spinelike bodies characterize the mature sperm. Moreover, a new spermatological character is described for the first time, the so-called cytoplasmic ornamented buttons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agostini S., Miquel J., Ndiaye P.I., Marchand B. 2005. Dicrocoelium hospes Looss, 1907 (Digenea, Dicrocoeliidae): spermiogenesis, mature spermatozoon and ultrastructural comparative study. Parasitology Research, 96, 38–48. DOI: 10.1007/s00 436-005-1318-6.

    Article  PubMed  Google Scholar 

  • Ashour A.A., Garo K., Gamil I.S. 2007. Spermiogenesis in two paramphistomes from Nile fish in Egypt: an ultrastructural study. Journal of Helminthology, 81, 219–226:. DOI 10.1017/S0022149X07409816.

    Article  PubMed  CAS  Google Scholar 

  • Bakhoum A.J.S., Ba C.T., 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). Revista Ibero-Latinoamericana de Parasitología, 1, 32–45.

    Google Scholar 

  • Bakhoum A.J.S., Torres J., Shimalov V.V., Bâ C.T., Miquel J. 2011a. Spermiogenesis and spermatozoon ultrastructure of Diplodiscus subclavatus (Pallas, 1760) (Paramphistomoidea, Diplodiscidae), an intestinal fluke of the pool frog Rana lessonae. Parasitology International, 60, 64–74. DOI: 10.1016/j.parint.2010.10.006.

    Article  PubMed  CAS  Google Scholar 

  • Bakhoum A.J.S., Ba C.T., Shimalov V.V., Torres J., Miquel J. 2011b. Spermatological characters of the digenean Rubenstrema exasperatum (Rudolphi, 1819) (Plagiorchioidea, Omphalometridae). Parasitology Research, 108, 1283–1293. DOI: 10.1007/s00436-010-2178-2.

    Article  PubMed  Google Scholar 

  • Brooks D.R., O’Grady R.T., Glen D.R. 1985. Phylogenetic analysis of the Digenea (Platyhelminthes, Cercomeria) with comments on their adaptative radiation. Canadian Journal of Zoology, 63, 411–443.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Burton P.R. 1972. Fine structure of the reproductive system of a frog lung-fluke. III. The 376 spermatozoon and its differentiation. Journal of Parasitology, 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). Parasitology Research, 79, 204–212. DOI: 10.1007/BF00931894.

    Article  PubMed  CAS  Google Scholar 

  • Cribb T.H., Bray R.A., Littlewood D.T.J., Pichelin S., Herniou E.A. 2001. The Digenea. In: (Eds. D.J.T. Littlewood and R.A. Bray) Interrelationships of the Platyhelminthes. Taylor and Francis, London, 168–185.

    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. Par asitology Research, 101, 843–852. DOI: 10.1007/s00436-007-0550-7.

    Google Scholar 

  • Gracenea M., Ferrer J.R., González-Moreno O., Trullols M. 1997. Ultrastructural study of spermatogenesis and spermatozoon in Postorchigenes gymnesicus (Trematoda, Lecithodendriidae). Journal of Morphology, 234, 223–232. DOI: 10.1002/(SICI)1097-4687(199712)234:3<223::AID-JMOR2>3.0.CO;2-A.

    Article  Google Scholar 

  • Holliman R.B. 1961. Larval trematodes from the Apalachee Bay area, Florida, with checklist of known marine cercariae arranged in a key to their superfamilies. Tulane Studies in Zoology, 9, 2–72.

    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  CAS  Google Scholar 

  • Jones A., Blair D. 2005. Superfamily Microscaphidioidea Looss, 1900. In: (Eds. A. Jones, R.A. Bray and D.I. Gibson) Keys to the Trematoda. CABI Publishing and The Natural History Museum, Wallingford, 189–219.

    Google Scholar 

  • Jousson O., Bartoli P. 1999. The life-cycle of three species of the Mesometridae (Digenea) with comments on the taxonomic status of this family. Systematic Parasitology, 44, 217–228. DOI: 10.1023/A:1006203806109.

    Article  PubMed  CAS  Google Scholar 

  • Justine J.-L. 1995. Spermatozoal ultrastructure and phylogeny of the parasitic Platyhelminthes. 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, 55–86.

  • Justine J.-L. 1998. Spermatozoa as phylogenetic characters for the Eucestoda. Journal of Parasitology, 84, 385–408. DOI: 10.2307/3284502.

    Article  PubMed  CAS  Google Scholar 

  • 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, 231–238.

    Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • La Rue G. 1957. The classication of digenetic Trematoda: a review and new system. Experimental Parasitology, 6, 306–349. DOI: 10.1016/0014-4894(57)90025-5.

    Article  Google Scholar 

  • Levron C., Miquel J., Oros M., Scholz T. 2010. Spermatozoa of tapeworms (Platyhelminthes, Eucestoda): advances in ultrastructural and phylogenetic studies. Biological Reviews, 85, 523–543. DOI: 10.1111/j.1469-185X.2009.00114.x.

    PubMed  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 Parasitologica, 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). Parasitology Research, 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 Parasitologica, 49, 190–200.

    Google Scholar 

  • Liu Y., Pan Y. 1990. Electron microscope studies of Metorchis (sic) orientalis. III. The spermatozoa and spermatogenesis. Journal of Shanghai Agriculture College, 8, 57–62.

    Google Scholar 

  • Miquel J., Feliu C., Marchand B. 1999. Ultrastructure of spermiogenesis and the spermatozoon of Mesocestoides litteratus (Cestoda, Mesocestoididae). International Journal for Parasitology, 29, 499–510. DOI: 10.1016/S0020-7519(98)00202-1.

    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). Journal of Parasitology, 92, 441–453. DOI: 10.1645/GE-743R.1.

    Article  PubMed  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). Parasitology Research, 86, 301–310. DOI: 10.1007/s004360050047.

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Ndiaye P.I., Miquel J., Ba C.T., 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. Journal of Parasitology, 90, 30–40. DOI: 10.1645/GE-3171.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Olson P.D., Cribb T.H., Tkach V.V., Bray R.A., Littlewood D.T.J. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755. DOI: 10.1016/S0020-7519(03)00049-3.

    Article  PubMed  CAS  Google Scholar 

  • Quilichini Y., Foata J., Justine J.-L., Bray R.A., Marchand B. 2010a. Ultrastructural study of the spermatozoon of Heterolebes maculosus (Digenea, Opistholebetidae), a parasite of the porcupinefish Diondon hystrix (Pisces, Teleostei). Parasitology International, 59, 427–434. DOI: 10.1016/j.parint.2010.06.002.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Quilichini Y., Foata J., Marchand B. 2007c. Ultrastructural study of the spermatozoon of Nicolla testiobliquum (Digenea, Opecoelidae) parasite of brown trout Salmo trutta (Pisces, Teleostei). Parasitology Research, 101, 1295–1301. DOI: 10. 1007/s00436-007-0636-2.

    Article  PubMed  Google Scholar 

  • Quilichini Y., Foata J., Marchand B. 2007d. Ultrastructural study of the spermatozoon of Pronoprymna ventricosa (Digenea, Baccigerinae), parasite of the twaite shad Alosa fallax Lacepede (Pisces, Teleostei). Parasitology Research, 101, 1125–1130. DOI: 10.1007/s00436-007-0599-3.

    Article  PubMed  Google Scholar 

  • Quilichini Y., Foata J., Orsini A., Marchand B. 2007a. Spermiogenesis and spermatozoon ultrastructure of Nicolla wisniewskii (Digenea: Opecoelidae), an intestinal parasite of brown trout Salmo trutta (Pisces: Teleostei). Journal of Parasitology, 93, 469–478. DOI: 10.1645/GE-1085R.1.

    Article  PubMed  Google Scholar 

  • Quilichini Y., Foata J., Orsini A., Marchand B. 2007b. Ultrastructural study of spermiogenesis and the spermatozoon of Crepidostomum metoecus (Digenea: Allocreadiidae), a parasite of Salmo trutta (Pisces: Teleostei). Journal of Parasitology, 93, 458–468. DOI: 10.1645/GE-1045R.1.

    Article  PubMed  Google Scholar 

  • Rees F.G. 1979. The ultrastructure of the spermatozoon and spermiogenesis in Cryptocotyle lingua (Digenea: Heterophyidae). International Journal for Parasitology, 9, 405–419. DOI: 10.1016/0020-7519(79)90044-4.

    Article  Google Scholar 

  • Reynolds E.S. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology, 17, 208–212.

    Article  PubMed  CAS  Google Scholar 

  • Seck M.T., Marchand B., Ba C.T. 2007. Ultrastructure of spermiogenesis and the spermatozoon of Paramphistomum microbothrium (Fischoeder 1901; Digenea, Paramphistomidae), a parasite of Bos taurus in Senegal. Parasitology Research, 101, 259–268. DOI: 10.1007/s00436-007-0503-1.

    Article  PubMed  Google Scholar 

  • Seck M.T., Marchand B., Ba C.T. 2008a. Spermiogenesis and sperm ultrastructure of Cotylophoron cotylophorum (Trematoda, Digenea, Paramphistomidae), a parasite of Bos taurus in Senegal. Parasitology Research, 103, 157–166. DOI: 10.1007/s00436-008-0944-1.

    Article  PubMed  Google Scholar 

  • Seck M.T., Marchand B., Ba C.T. 2008b. Spermiogenesis and sperm ultrastructure of Carmyerius endopapillatus (Digenea, Gastrothylacidae), a parasite of Bos taurus in Senegal. Acta Parasitologica, 53, 9–18. DOI: 10.2478/s11686-008-0006-y.

    Article  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). Parasitology Research, 104, 801–807. DOI: 10.1007/s00436-008-1259-y.

    Article  PubMed  CAS  Google Scholar 

  • Thiéry J.P. 1967. Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. Journal of Microscopy, 6, 987–1018.

    Google Scholar 

  • Ždárská Z., Soboleva T.N., Štěrba J., Valkounová J. 1991. Ultrastructure of the male reproductive system of the trematode Brachylaimus aequans. Folia Parasitologica, 38, 33–37.

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jordi Miquel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bakhoum, A.J.S., Ndiaye, P.I., Sène, A. et al. Spermiogenesis and ultrastructure of the spermatozoon of Wardula capitellata (Digenea, Mesometridae), an intestinal parasite of the sparid teleost Sarpa salpa in Senegal. Acta Parasit. 57, 34–45 (2012). https://doi.org/10.2478/s11686-012-0008-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11686-012-0008-7

Keywords

Navigation