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Acta Parasitologica

, Volume 62, Issue 3, pp 520–528 | Cite as

Ultrastructure of the spermatozoon of Macvicaria obovata (Digenea: Opecoelidae), a parasite of Sparus aurata (Pisces: Teleostei) from the Gulf of Gabès, Mediterranean Sea

  • Hichem KacemEmail author
  • Yann Quilichini
  • Lassad Neifar
  • Jordi Torres
  • Jordi Miquel
Article

Abstract

The ultrastructural organization of the spermatozoon of the digenean Macvicaria obovata (Opecoelidae) is described by transmission electron microscopy. Alive digeneans were collected from the digestive tract of Sparus aurata (Teleostei, Sparidae), caught from the Gulf of Gabès in Chebba, Tunisia (Eastern Mediterranean Sea). The male gamete of M. obovata is a filiform cell, tapered at both extremities and exhibits typical characters such as two axonemes of different lengths showing the 9+‘1’ trepaxonematan pattern, a nucleus, mitochondria, two bundles of parallel cortical microtubules, external ornamentation of the plasma membrane, spine-like bodies and granules of glycogen. Cortical microtubules are absent in the anterior spermatozoon extremity and appear after the disappearance of the electron-dense material. The first mitochondrion is of moniliform type and it is associated with the external ornamentation of the plasma membrane and spine-like bodies. The second mitochondrion is more posteriorly located, reaching the nuclear region. The present study provides new data on the mature male gamete of M. obovata that may be useful for the understanding of digenean relationships and phylogenetic studies.

Keywords

Macvicaria obovata Opecoelidae Digenea ultrastructure spermatozoon 

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References

  1. 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/s00436-005-1318-6CrossRefGoogle Scholar
  2. 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/S0022149X07409816CrossRefGoogle Scholar
  3. Bâ CT., Ndiaye PI., Dione A., Quilichini Y., Marchand B. 2011. Ultrastructure of the spermatozoon of Holorchis micracanthum (Digenea: Lepocreadiidae), an intestinal parasite of Plectorhinchus mediterraneus (Pisces, Teleostei) in Senegal. Parasitology Research, 109, 1099–1106. DOI: 10.1007/s00436-011-2352-1CrossRefGoogle Scholar
  4. Bakhoum A.J.S. 2012. Contribution à la connaissance de l’ultrastructure de la spermiogenèse et du spermatozoïde des Digènes. PhD Thesis, University of Barcelona, pp. 303. (In Spanish)Google Scholar
  5. Bakhoum A.J.S., Bâ C.T., Fournier-Chambrillon C., Torres J., Fournier P., Miquel J. 2009. Spermatozoon ultrastructure of Euryhelmis squamula (Rudolphi, 1819) (Digenea, Opisthorchiodea, Heterophyidae), an intestinal parasite of Mustela vison (Carnivora, Mustelidae). Revista Ibero-latinoamericana de Parasitología, 1, 37–45Google Scholar
  6. Bakhoum A.J.S., Sène A., Ndiaye P.I., Bâ C.T., Miquel J. 2012. Spermiogenesis and the spermatozoon ultrastructure of Robphildollfusium fractum (Digenea: Gyliauchenidae), an intestinal parasite of Sarpa salpa (Pisces: Teleostei). Comptes Rendus Biologies, 335, 435–444. DOI: 10.1016/j.crvi.2012.06.003CrossRefGoogle Scholar
  7. Bakhoum A.J.S., Ribas A., Eira C., Bâ C.T., Miquel J. 2013. Brachycoelium salamandrae (Frölich, 1789) (Digenea: Brachycoeliidae): ultrastructural study of spermiogenesis and the mature spermatozoon. Zoologischer Anzeiger, 252, 149–156. DOI: 10.1016/j.jcz.2012.05.003CrossRefGoogle Scholar
  8. Bakhoum A.J.S, Quilichini Y., Justine J.L., Bâ C.T., Marchand B. 2015a. Neomultitestis aspidogastriformis Bray and Cribb, 2003 (Digenea, Lepocreadiidae): mature spermatozoon and sperm morphologies in the Lepocreadioidea. Cell Biology International, 39, 799–807. DOI: 10.1002/cbin.10449CrossRefGoogle Scholar
  9. Bakhoum A.J.S., Quilichini Y., Justine J.L., Bray R.A., Bâ C.T., Marchand B. 2015b. Ultrastructural study of sperm cells in Acanthocolpidae: the case of Stephanostomum murielae and Stephanostomoides tenuis (Digenea). PeerJ, 3, e744. DOI: 10.7717/peerj.744CrossRefGoogle Scholar
  10. Bakhoum A.J.S., Kacem H., Neifar L., Miquel J. 2017. The Opecoelidae sperm model and its contribution to phylogeny: Spermatozoon ultrastructural particularities of Allopodocotyle pedicellata (Plagioporinae, Digenea, Platyhelminthes). Zoologischer Anzeiger, 266, 28–34. DOI: 10.1016/j.jcz.2016.10.006CrossRefGoogle Scholar
  11. Bray R.A., Cribb T.H., Littlewood D.T.J., Waeschenbach A. 2016. The molecular phylogeny of the digenean family Opecoelidae Ozaki, 1925 and the value of morphological characters, with the erection of a new subfamily. Folia Parasitologica, 63, 013. DOI 10.14411/fp.2016.013Google Scholar
  12. Cribb T.H. 2005. Family Opecoelidae Ozaki 1925. In: Jones, A., Bray, R.A., Gibson, D.I. (Eds), Keys to the Trematoda, vol. 2. CAB International and the Natural History Museum, London, pp. 443–531CrossRefGoogle Scholar
  13. Diagne P.M., Bâ C.T., Ndiaye P.I., Bray R.A., Marchand B., Quilichini Y. 2016. Sperm ultrastructure of Podocotyloides magnatestis (Digenea, Opecoeloidea, Opecoelidae) a parasite of Parapristipoma octolineatum (Pisces, Teleostei). Zoologischer Anzeiger, 264, 56–63. DOI: 10.1016/j.jcz.2016.06.004CrossRefGoogle Scholar
  14. Ehlers U. 1984. Phylogenetisches System der Platyhelminthes. Verhandlungen des Naturwissenschaftlichen Vereins in Hamburg, 27, 291–294. (In German)Google Scholar
  15. Foata J, Quilichini Y, Greani S, Marchand B. 2012. Sperm ultrastructure of the Digenean Aphallus tubarium (Rudolphi, 1819) Poche, 1926 (Platyhelminthes, Cryptogonimidae) intestinal parasite of Dentex dentex (Pisces, Teleostei). Tissue & Cell, 44, 15–21. DOI: 10.1016/j.tice.2011.10.001CrossRefGoogle Scholar
  16. Justine J.-L. 1991. Phylogeny of parasitic Platyhelminthes: a critical study of synapomorphies proposed on the basis of the ultrastructure of spermiogenesis and spermatozoa. Canadian Journal of Zoology, 69, 1421–1440. DOI: 10.1139/z91-203CrossRefGoogle Scholar
  17. Justine J.-L. 1995. Spermatozoal ultrastructure and phylogeny of the parasitic Platyhelminthes. Mémoires du Muséum National d’Histoire Naturelle Paris 166, 55–86Google Scholar
  18. Justine J.-L. 1998. Spermatozoa as phylogenetic characters for the Eucestoda. Journal of Parasitology, 84, 385–408. DOI: 10.2307/3284502CrossRefGoogle Scholar
  19. Justine J.-L. 2001. Spermatozoa as phylogenetic characters for the Platyhelminthes. In: Littlewood D.T.J. and Bray R.A. (Eds), Interrelationships of the Platyhelminthes. Taylor and Francis, London: 231–238Google Scholar
  20. Justine J.-L., Mattei X. 1983. A spermatozoon with two 9+0 axonemes in a parasitic flatworm, Didymozoon (Digenea: Didymozoidae). Journal of Submicroscopic Cytology and Pathology, 15, 1101–1105Google Scholar
  21. Justine J.-L., Jamieson B.G.M., Southgate V.R. 1993. Homogeneity of sperm structure in six species of Schistosomes (Digenea, Platyhelminthes). Annales de Parasitologie Humaine et Comparée, 68, 185–187CrossRefGoogle Scholar
  22. Kacem H., Bakhoum A.J.S., Neifar L., Miquel J. 2010. Spermiogenesis and spermatozoon ultrastructure of the digenean Neoapocreadium chabaudi (Apocreadiidae), a parasite of Balistes capriscus (Pisces, Teleostei). Parasitology International, 59, 358–366. DOI: 10.1016/j.parint.2010.04.008CrossRefGoogle Scholar
  23. Kacem H., Bakhoum A.J.S., Eira C., Neifar L., Miquel J. 2012. Ultrastructural characters of the spermatozoon of the digenean Hypocreadium caputvadum Kacem et al. 2011 (Lepocreadioidea: Lepocreadiidae), an intestinal parasite of Balistes capriscus in Tunisia. Comptes Rendus Biologies, 335, 637–644. DOI: 10.1016/j.crvi.2012.10.002CrossRefGoogle Scholar
  24. Kacem H., Ndiaye P.I., Neifar L., Torres J., Miquel J. 2015. Ultrastructure of the spermatozoon of the digenean Tergestia acanthocephala (Stossich, 1887) (Gymnophalloidea: Fellodistomidae): An intestinal parasite of Belone belone gracilis (Pisces: Teleostei). Tissue & Cell, 47, 235–241. DOI: 10.1016/j.tice.2015.01.008CrossRefGoogle Scholar
  25. 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, 255–264Google Scholar
  26. Levron C., Ternengo S., Marchand B. 2004. Spermiogenesis and sperm ultrastructure of Poracanthium furcatum (Digenea, Opecoelidae), a parasite of Mullus surmuletus (Pisces, Teleostei). Acta Parasitologica, 49, 190–200Google Scholar
  27. 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.xPubMedGoogle Scholar
  28. 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/s004360050047CrossRefGoogle Scholar
  29. Miquel J., Vilavella D., Świderski Z., Shimalov V.V., Torres J. 2013. Spermatological characteristics of Pleurogenidae (Digenea) inferred from the ultrastructural study of Pleurogenes claviger, Pleurogenoides medians and Prosotocus confusus. Parasite, 20, 1–28. DOI: 10.1051/parasite/2013028CrossRefGoogle Scholar
  30. Ndiaye P.I., Miquel J., Bâ 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, 259–271Google Scholar
  31. Ndiaye P.I., Bakhoum A.J.S., Sène A., Diagne P.M., Miquel J. 2015. The ultrastructural characters of the spermatozoon of Opechona bacillaris (Molin, 1859) (Digenea, Lepocreadiidae) a parasite of Scomber colias Gmelin, 1789 (Scombridae) off the coast of Dakar (Senegal). Acta Zoologica (Stockholm), 96, 91–98. DOI: 10.1111/azo.12054CrossRefGoogle Scholar
  32. 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). Parasitology Research, 101, 1295–1301. DOI: 10.1007/s00436-007-0636-2CrossRefGoogle Scholar
  33. Quilichini Y., Foata J., Orsini A., Marchand B. 2007b. 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.1CrossRefGoogle Scholar
  34. Quilichini Y., Foata J., Justine J.-L., Bray R.A., Marchand B. 2010. Ultrastructural study of the spermatozoon of Heterolebes maculosus (Digenea, Opistholebetidae), a parasite of the porcupinefish Diodon hystrix (Pisces, Teleostei). Parasitology International, 59, 427–434. DOI: 10.1016/j.parint.2010.06.002CrossRefGoogle Scholar
  35. Quilichini Y, Foata J, Justine J-L, Bray RA, Marchand B. 2011b. Sperm ultrastructure of Helicometra epinepheli (Platyhelminthes, Digenea, Opecoelidae), parasite of Epinephelus fasciatus (Pisces, Teleostei). Histology and Histopathology, 26, 1019–1028PubMedGoogle Scholar
  36. Quilichini Y., Foata J., Justine J.-L., Bray R.A., Marchand B. 2011a. Spermatozoon ultrastructure of Gyliauchen sp. (Digenea: Gyliauchenidae), an intestinal parasite of Siganus fuscescens (Pisces: Teleostei). Biological Bulletin, 221, 197–205CrossRefGoogle Scholar
  37. Reynolds E.S. 1963. The use of lead citrate at high pH as an electronopaque stain in electron microscopy. Journal of Cell Biology, 17, 208–212CrossRefGoogle Scholar
  38. 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-yCrossRefGoogle Scholar
  39. Thiéry J.P. 1967. Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. Journal de Microscopie, 6, 987–1018Google Scholar
  40. Zhukova M.V., Mordvinov V.A., Kiseleva E. 2014. Ultrastructure of spermatozoa in the seminal receptacle of the liver fluke Opisthorchis felineus (Rivolta, 1884). Parasitology Research, 113, 1093–101. DOI: 10.1007/s00436-013-3746-zCrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2017

Authors and Affiliations

  • Hichem Kacem
    • 1
    Email author
  • Yann Quilichini
    • 2
  • Lassad Neifar
    • 1
  • Jordi Torres
    • 3
    • 4
  • Jordi Miquel
    • 3
    • 4
  1. 1.Laboratoire de Biodiversité et Ecosystèmes Aquatiques, Département des Sciences de la VieFaculté des Sciences de SfaxSfaxTunisia
  2. 2.CNRS UMR 6134University of Corsica, Laboratory “Parasites and Mediterranean Ecosystems”Corte, CorsicaFrance
  3. 3.Secció de Parasitologia, Departament de Biologia, Sanitat i Medi Ambient, Facultat de Farmàcia i Ciències l’AlimentacióUniversitat de BarcelonaBarcelonaSpain
  4. 4.Institut de Recerca de la Biodiversitat, Facultat de BiologiaUniversitat de BarcelonaBarcelonaSpain

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