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

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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.

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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/s00436-005-1318-6

    Article  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  CAS  Google Scholar 

  • 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/s00436-011-2352-1

    Article  Google Scholar 

  • 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 

  • 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, 37–45

    Google Scholar 

  • 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.2012.06.003

    Article  Google Scholar 

  • 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.2012.05.003

    Article  Google Scholar 

  • 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.10449

    Article  Google Scholar 

  • 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.744

    Article  Google Scholar 

  • 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.2016.10.006

    Article  Google Scholar 

  • 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.2016.013

  • 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. 443–531

    Article  Google Scholar 

  • 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.2016.06.004

    Article  Google Scholar 

  • Ehlers U. 1984. Phylogenetisches System der Platyhelminthes. Verhandlungen des Naturwissenschaftlichen Vereins in Hamburg, 27, 291–294. (In German)

    Google Scholar 

  • 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.2011.10.001

    Article  CAS  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. Canadian Journal of Zoology, 69, 1421–1440. DOI: 10.1139/z91-203

    Article  Google Scholar 

  • Justine J.-L. 1995. Spermatozoal ultrastructure and phylogeny of the parasitic Platyhelminthes. Mémoires du Muséum National d’Histoire Naturelle Paris 166, 55–86

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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: 231–238

    Google Scholar 

  • 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, 1101–1105

    Google Scholar 

  • 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, 185–187

    Article  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 Balistes capriscus (Pisces, Teleostei). Parasitology International, 59, 358–366. DOI: 10.1016/j.parint.2010.04.008

    Article  CAS  Google Scholar 

  • 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.2012.10.002

    Article  Google Scholar 

  • 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.2015.01.008

    Article  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 Parasitologica, 48, 255–264

    Google Scholar 

  • 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, 190–200

    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 

  • 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  CAS  Google Scholar 

  • 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/2013028

    Article  Google Scholar 

  • 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, 259–271

    Google Scholar 

  • 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.12054

    Article  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). Parasitology Research, 101, 1295–1301. DOI: 10.1007/s00436-007-0636-2

    Article  Google Scholar 

  • 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.1

    Article  Google Scholar 

  • 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.2010.06.002

    Article  CAS  Google Scholar 

  • 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, 1019–1028

    CAS  PubMed  Google Scholar 

  • 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, 197–205

    Article  CAS  Google Scholar 

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

    Article  CAS  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  CAS  Google Scholar 

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

    Google Scholar 

  • 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-z

    Article  Google Scholar 

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Kacem, H., Quilichini, Y., Neifar, L. et al. Ultrastructure of the spermatozoon of Macvicaria obovata (Digenea: Opecoelidae), a parasite of Sparus aurata (Pisces: Teleostei) from the Gulf of Gabès, Mediterranean Sea. Acta Parasit. 62, 520–528 (2017). https://doi.org/10.1515/ap-2017-0062

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