Folia Parasitologica, vol. 59 (2012), issue 3

Folia Parasitologica 59[3] 173-178 (2012) | 10.14411/fp.2012.024

Ultrastructure of the spermatozoon of the digenean Lecithocladium excisum (Rudolphi, 1819) (Hemiuroidea: Hemiuridae), a parasite of marine teleosts in Senegal

Papa Ibnou Ndiaye1, Papa Mbagnick Diagne1, Aminata Sène1, Abdoulaye J.S. Bakhoum2,3, Jordi Miquel2,3
1 Laboratory of Evolutionary Biology, Ecology and Management of Ecosystems, Faculty of Sciences and Techniques, Cheikh Anta Diop University of Dakar, BP 5055, Dakar, Senegal
2 Laboratori de Parasitologia, Departament de Microbiologia i Parasitologia Sanitàries, Facultat de Farmàcia, Universitat de Barcelona, Av. Joan XXIII, s/n, 08028 Barcelona, Spain
3 Institut de Recerca de la Biodiversitat, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal, 645, 08028 Barcelona, Spain

The present study describes the ultrastructure of the mature spermatozoon of Lecithocladium excisum (Rudolphi, 1819) (Digenea: Hemiuroidea: Hemiuridae) from the stomach of the marine teleost Scomber japonicus Houttuyn (Scombridae) captured in the Atlantic Ocean, off Dakar (Senegal). The ultrastructural organization of the spermatozoon of L. excisum follows the general model described in most digeneans. It presents two axonemes of the 9+'1' pattern of the Trepaxonemata, nucleus, mitochondrion and parallel cortical microtubules, among other characters. However, some particularities of the spermatozoon of L. excisum are (i) the presence of a membranous ornamentation not associated with cortical microtubules in its anterior extremity, (ii) the presence of a very reduced number of cortical microtubules located only in the ventral side of the spermatozoon and (iii) the absence of several structures described in most digeneans such as spine-like bodies and cytoplasmic expansions.

Keywords: Lecithocladium excisum, Hemiuridae, Digenea, spermatozoon, ultrastructure, Scomber japonicus, Scombridae, fish, Senegal

Received: June 14, 2012; Accepted: July 13, 2012; Published: September 21, 2012


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. Parasitol. Res. 96: 38-48 Go to original source... Go to PubMed...
  2. Ba C.T., Marchand B. 1995: Spermiogenesis, spermatozoa and phyletic affinities in the Cestoda. Mem. Mus. Natl. Hist. Nat. 166: 87-95
  3. Bakhoum A.J.S., Ba C.T., Shimalov V.V., Torres J., Miquel J. 2011a: Spermatological characters of the digenean Rubenstrema exasperatum (Rudolphi, 1819) (Plagirochioidea, Omphalometridae). Parasitol. Res. 108: 1283-1293 Go to original source... Go to PubMed...
  4. Bakhoum A.J.S., Ndiaye P.I., Ba C.T., Miquel J.: Spermatological characteristics of Elstia stossichianum (Digenea, Mesometridae) from the intestine of the cow bream (Sarpa salpa) off Dakar, Senegal. J. Helminthol. (In press.)
  5. Bakhoum A.J.S., Ndiaye P.I., Sene A., Ba C.T., Miquel J. 2012: Spermiogenesis and ultrastructure of the spermatozoon of Wardula capitellata (Digenea, Mesometridae), an intestinal parasite of the sparid teleost Sarpa salpa in Senegal. Acta Parasitol. 57: 34-45 Go to original source... Go to PubMed...
  6. Bakhoum A.J.S., Torres J., Shimalov V.V., Ba C.T., Miquel J. 2011b: Spermiogenesis and spermatozoon ultrastructure of Diplodiscus subclavatus (Pallas, 1760) (Paramphistomoidea, Diplodiscidae), an intestinal fluke of the pool frog Rana lessonae (Amphibia, Anura). Parasitol. Int. 60: 64-74 Go to original source... Go to PubMed...
  7. Baptista-Farias M.F.D., Kohn A., Cohen S.C. 2001: Ultrastructure of spermatogenesis and sperm development in Saccocoelioides godoyi Kohn & Froes, 1986 (Digenea, Haploporidae). Mem. Inst. Oswaldo Cruz 96: 61-70 Go to original source... Go to PubMed...
  8. Burton P.R. 1972: Fine structure of the reproductive system of a frog lung-fluke. III. The spermatozoon and its differentiation. J. Parasitol. 58: 68-83 Go to original source... Go to PubMed...
  9. 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 Go to original source... Go to PubMed...
  10. Daddow L.Y.M., Jamieson B.G.M. 1983: An ultrastructural study of spermiogenesis in Neochasmus sp. (Cryptogonimidae: Digenea: Trematoda). Aust. J. Zool. 31: 1-14 Go to original source...
  11. Ehlers U. 1984: Phylogenetisches System der Plathelminthes. Verh. Naturwiss. Ver. Hamburg (NF) 27: 291-294
  12. 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 Go to original source... Go to PubMed...
  13. Gibson D.I. 2002a: Family Hemiuridae Looss, 1899. In: D.I. Gibson, A. Jones and R.A. Bray (Eds.), Keys to the Trematoda. Vol. 1. CABI Publishing, Wallingford and The Natural History Museum, London, UK, pp. 305-340
  14. Gibson D.I. 2002b: Superfamily Hemiuroidea Looss, 1899. In: D.I. Gibson, A. Jones and R.A. Bray (Eds.), Keys to the Trematoda. Vol. 1. CABI Publishing, Wallingford and The Natural History Museum, London, UK, pp. 299-304
  15. Hoberg E.P., Mariaux J., Brooks D.R. 2001: Phylogeny among orders of the Eucestoda (Cercomeromorphae): integrating morphology, molecules and total evidence. In: D.T.J. Littlewood and R.A. Bray (Eds.), Interrelationships of the Platyhelminthes. Taylor and Francis, London, UK, pp. 112-126
  16. Hoberg E.P., Mariaux J., Justine J.-L., Brooks D.R., Weekes P.J. 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 Go to original source... Go to PubMed...
  17. 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 Go to original source... Go to PubMed...
  18. Jamieson B.G.M., Daddow L.M. 1982: The ultrastructure of the spermatozoon of Neochasmus sp. (Cryptogonimidae, Digenea, Trematoda) and its phylogenetic significance. Int. J. Parasitol. 12: 547-559 Go to original source...
  19. Justine J.-L. 1995: Spermatozoal ultrastructure and phylogeny of the parasitic Platyhelminthes. Mem. Mus. Natl. Hist. Nat. 166: 55-86
  20. Justine J.-L. 1998: Spermatozoa as phylogenetic characters for the Eucestoda . J. Parasitol. 84: 385-408 Go to original source... Go to PubMed...
  21. Justine J.-L. 2001: Spermatozoa as phylogenetic characters for the Platyhelminthes. In: D.T.J. Littlewood and R.A. Bray (Eds.), Interrelationships of the Platyhelminthes. Taylor and Francis, London, UK, pp. 231-238
  22. Justine J.-L., Mattei X. 1982a: Etude ultrastructurale de la spermiogenese et du spermatozoide d'un Plathelminthe: Gonapodasmius (Trematoda: Didymozoidae). J. Ultrastruct. Res. 79: 350-365 Go to original source... Go to PubMed...
  23. Justine J.-L., Mattei X. 1982b: Reinvestigation de l'ultrastructure du spermatozoide d'Haematoloechus (Trematoda: Haematoloechidae). J. Ultrastruct. Res. 81: 322-332 Go to original source... Go to PubMed...
  24. Justine J.-L., Mattei X. 1983: A spermatozoon with two 9 + 0 axonemes in a parasitic flatworm, Didymozoon (Digenea: Didymozoidae). J. Submicrosc. Cytol. 15: 1101-1105.
  25. Justine J.-L., Mattei X. 1984: Ultrastructural observations on the spermatozoon, ovocyte and fertilization process in Gonapodasmius, a gonochoristic trematode (Trematoda: Digenea: Didymozoidae). Acta Zool. (Stockh.) 65: 171-177 Go to original source...
  26. 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). Parasitol. Int. 59: 358- 366 Go to original source... Go to PubMed...
  27. 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 Go to original source...
  28. 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 Go to original source... Go to PubMed...
  29. 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 Go to original source...
  30. 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 Go to original source... Go to PubMed...
  31. 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 Go to original source... Go to PubMed...
  32. 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 Parasitol. 47: 259-271
  33. Ndiaye P.I., Miquel J., Feliu C., Marchand B. 2003: Ultrastructure of spermiogenesis and spermatozoa of Notocotylus neyrai Gonzalez Castro, 1945 (Digenea, Notocotylidae), intestinal parasite of Microtus agrestis (Rodentia: Arvicolidae) in Spain. Invert. Reprod. Dev. 43: 105-115 Go to original source...
  34. Ndiaye P.I., Quilichini Y., Sene A., Ba C.T., Marchand B. 2011: Ultrastructure of the spermatozoon of the digenean Cricocephalus albus (Kuhl & van Hasselt 1822) Looss, 1899 (Platyhelminthes, Pronocephaloidea, Pronocephalidae) parasite of the "hawksbill sea turtle" Eretmochelis imbricata (Linnaeus, 1766) in Senegal. Zool. Anz. 250: 215-222 Go to original source...
  35. Ndiaye P.I., Quilichini Y., Sene A., Tkach V.V., Ba C.T., Marchand B. 2012: Ultrastructural study of the spermatozoon of the digenean Enodiotrema reductum Looss, 1901 (Platyhelminthes, Plagiorchioidea, Plagiorchiidae) parasite of the green turtle Chelonia mydas (Linnaeus, 1758) in Senegal. Parasitol. Res. 111: 859-864 Go to original source... Go to PubMed...
  36. Olson P.D., Littlewood D.T.J., Bray R.A., Mariaux J. 2001: Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Mol. Phylogenet. Evol. 19: 443-467 Go to original source... Go to PubMed...
  37. Pamplona-Basilio M.C., Baptista-Farias M.F.D., Kohn A. 2001: Spermatogenesis and spermiogenesis in Didymocystis wedli Ariola, 1902 (Didymozoidae, Digenea). Mem. Inst. Oswaldo Cruz 96: 1153-1159 Go to original source... Go to PubMed...
  38. Quilichini Y., Foata J., Justine J.-L., Bray R.A., Marchand B. 2010a: Spermatozoon ultrastructure of Aponurus laguncula (Digenea: Lecithasteridae), a parasite of Aluterus monoceros (Pisces, Teleostei). Parasitol. Int. 59: 22-28 Go to original source... Go to PubMed...
  39. Quilichini Y., Foata J., Justine J.-L., Bray R.A., Marchand B. 2010b: Ultrastructural study of the spermatozoon of Heterolebes maculosus (Digenea, Opistholebetidae), a parasite of the porcupinefish Diodon hystrix (Pisces, Teleostei). Parasitol. Int. 59: 427-434 Go to original source... Go to PubMed...
  40. Quilichini Y., Foata J., Justine J.-L., Bray R.A., Marchand B. 2011: Spermatozoon ultrastructure of Gyliauchen sp. (Digenea: Gyliauchenidae), an intestinal parasite of Siganus fuscescens (Pisces: Teleostei). Biol. Bull. 221: 197-205 Go to PubMed...
  41. Quilichini Y., Foata J., Marchand B. 2007: 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 Go to original source... Go to PubMed...
  42. Reynolds E.S. 1963: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17: 208-212 Go to original source... Go to PubMed...
  43. Robinson R.D., Halton D.W. 1982: Fine structural observations on spermatogenesis in Corrigia vitta (Trematoda: Dicrocoeliidae). Z. Parasitenkd. 68: 53-72 Go to original source...
  44. Seck M.T., Marchand B., Ba C.T. 2008: Spermiogenesis and sperm ultrastructure of Cotylophoron cotylophorum (Trematoda, Digenea, Paramphistomidae), a parasite of Bos taurus in Senegal. Parasitol. Res. 103: 157-166 Go to original source... Go to PubMed...
  45. Swiderski Z. 1986: Three types of spermiogenesis in cestodes. Proc. 11th Int. Cong. Electron Microsc., Kyoto, pp. 2959-2960
  46. Tang J., Wang W., Wang G. 1998: Studies on ultrastructure of spermatogenesis and sperm in Pseudorhipidocotyle elpichthys. Acta Hydrobiol. Sin. 22: 168-173
  47. Thiery J.P. 1967: Mise en evidence des polysaccharides sur coupes fines en microscopie electronique. J. Microsc. 6: 987-1018