Advertisement

Spermatological characteristics of Siphoderina aloysiae (Digenea, Cryptogonimidae), an intestinal parasite of Sciaena umbra (Teleostei, Sciaenidae)

  • Hichem KacemEmail author
  • Jordi Miquel
Original Paper
  • 4 Downloads

Abstract

The ultrastructural organisation of the spermatozoon of Siphoderina aloysiae (Digenea, Cryptogonimidae) is described based upon examination by transmission electron microscopy. Live digeneans were collected from the digestive tract of the Brown meagre Sciaena umbra (Teleostei: Sciaenidae), caught off the Gulf of Gabès in La Chebba (Tunisia). The male gamete of S. aloysiae is a filiform cell, tapered at both extremities, and exhibits typical characteristics of digenean sperm such as two axonemes showing the 9 + ‘1’ trepaxonematan pattern with different lengths. The first axoneme is disorganised and disappears near the anterior nuclear extremity. However, the second axoneme reaches the posterior extremity of the spermatozoon. The latter also contains a nucleus, 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 extremity of the spermatozoon and appear after the disappearance of the electron-dense material. In addition, the male gamete of S. aloysiae has two mitochondria. The first mitochondrion is associated with the external ornamentation of the plasma membrane and spine-like bodies. The second is more posteriorly located at the nuclear region after the disappearance of the first axoneme. The present study provides new data on the mature male gamete of S. aloysiae that may be useful for the understanding of digenean relationships and phylogenetic studies.

Keywords

Siphoderina aloysiae Cryptogonimidae Digenea Ultrastructure Spermatozoon 

Notes

Acknowledgements

The authors wish to thank the staff of the “Centres Científics i Tecnològics” of the University of Barcelona (CCTiUB) for their assistance in the preparation of samples.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. 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. Parasitol Res 109:1099–1106.  https://doi.org/10.1007/s00436-011-2352-1 CrossRefGoogle Scholar
  2. Bakhoum AJS, Bâ CT, 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). Rev Ibero-latinoam Parasitol 68:37–45Google Scholar
  3. Bakhoum AJS, Sène A, Ndiaye PI, Bâ CT, Miquel J (2012) Spermiogenesis and the spermatozoon ultrastructure of Robphildollfusium fractum (Digenea: Gyliauchenidae), an intestinal parasite of Sarpa salpa (Pisces: Teleostei). C R Biol 335:435–444.  https://doi.org/10.1016/j.crvi.2012.06.003 CrossRefGoogle Scholar
  4. Bakhoum AJS, Miquel J, Ndiaye PI, Justine J-L, Falchi A, Bâ CT, Marchand B, Quilichini Y (2017) Advances in spermatological characters in the Digenea: review and proposal of spermatozoa models and their phylogenetic importance. Adv Parasitol 98:111–165.  https://doi.org/10.1016/bs.apar.2017.04.001 CrossRefGoogle Scholar
  5. Burton PR (1972) Fine structure of the reproductive system of a frog lung-fluke. III. The spermatozoon and its differentiation. J Parasitol 58:68–83CrossRefGoogle Scholar
  6. Cribb TH (1986) The life cycle and morphology of Stemmatostoma pearsoni, gen. et sp. nov., with notes on the morphology of Telogaster opisthorchis Macfarlane (Digenea: Cryptogonimidae). Aust J Zool 34:279–304CrossRefGoogle Scholar
  7. Ehlers U (1984) Phylogenetisches system der plathelminthes. Verh Naturwiss Ver Hambg (NF) 27:291–294Google Scholar
  8. 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.  https://doi.org/10.1016/j.tice.2011.10.001 CrossRefGoogle Scholar
  9. Jamieson BGM, Daddow LM (1982) The ultrastructure of the spermatozoon of Neochasmus sp. (Cryptogonimidae, Digenea, Trematoda) and its phylogenetic significance. Int J Parasitol 12:547–559.  https://doi.org/10.1016/0020-7519(82)90051-0 CrossRefGoogle Scholar
  10. Jamieson BGM, Justine J-L (2017) Spermatozoa, spermatogenesis and fertilization in Schistosoma. In: Jamieson BGM (ed) Schistosoma: biology, pathology and control. CRC Press, Florida, pp 300–318Google Scholar
  11. Jeong K-H, Rim H-J (1984) A study on the fine structure of Clonorchis sinensis, a liver fluke. V. The mature spermatozoa. Korean J Parasitol 22:30–36CrossRefGoogle Scholar
  12. Justine J-L (1991a) Phylogeny of parasitic Platyhelminthes: a critical study of synapomorphies proposed on the basis of the ultrastructure of spermiogenesis and spermatozoa. Can J Zool 69:1421–1440.  https://doi.org/10.1139/z91-203 CrossRefGoogle Scholar
  13. Justine J-L (1991b) Cladistic study in the Monogenea (Platyhelminthes), based upon a parsimony analysis of spermiogenetic and spermatozoal ultrastructural characters. Int J Parasitol 21:821–838.  https://doi.org/10.1016/0020-7519(91)90151-V CrossRefGoogle Scholar
  14. Justine J-L (1998) Spermatozoa as phylogenetic characters for the Eucestoda. J Parasitol 84:385–408.  https://doi.org/10.2307/3284502 CrossRefGoogle Scholar
  15. 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 231–238Google Scholar
  16. Justine J-L, Mattei X (1983) A spermatozoon with two 9 + 0 axonemes in a parasitic flatworm, Didymozoon (Digenea: Didymozoidea). J Submicr Cytol 15:1101–1105Google Scholar
  17. 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.  https://doi.org/10.1051/parasite/1993684185 CrossRefGoogle Scholar
  18. Kacem H, Bakhoum AJS, 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.  https://doi.org/10.1016/j.parint.2010.04.008 CrossRefGoogle Scholar
  19. Kacem H, Bakhoum AJS, 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. C R Biol 335:637–644.  https://doi.org/10.1016/j.crvi.2012.10.002 CrossRefGoogle Scholar
  20. Kacem H, Blasco S, Foronda P, Miquel J (2017) Sperm characters of Timoniella imbutiforme (Digenea, Opisthorchioidea, Cryptogonimidae), a parasite of the European seabass Dicentrarchus labrax. Zool Anz 271:49–56.  https://doi.org/10.1016/j.jcz.2017.11.005 CrossRefGoogle Scholar
  21. 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.  https://doi.org/10.1111/j.1469-185X.2009.00114.x Google Scholar
  22. Liu Y, Pan Y (1990) Electron microscope studies of Metorchis (sic) orientalis. III. The spermatozoa and spermatogenesis. J Shanghai Agric Coll 8:57–62Google Scholar
  23. Martínez-Aquino A, Vidal-Martínez VM, Aguirre-Macedo ML (2017) A molecular phylogenetic appraisal of the acanthostomines Acanthostomum and Timoniella and their position within Cryptogonimidae (Trematoda: Opisthorchioidea). PeerJ 5:e4158.  https://doi.org/10.7717/peerj.4158 CrossRefGoogle Scholar
  24. Miller TL, Cribb TH (2008a) Eight new species of Siphoderina Manter, 1934 (Digenea, Cryptogonimidae) infecting Lutjanidae and Haemulidae (Perciformes) off Australia. Acta Parasitol 53:344–364.  https://doi.org/10.2478/s11686-008-0053-4 CrossRefGoogle Scholar
  25. Miller TL, Cribb TH (2008b) Family Cryptogonimidae Ward, 1917. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CAB International, Wallingford, pp 51–112CrossRefGoogle Scholar
  26. Miller TL, Bray RA, Goiran C, Justine J-L, Cribb TH (2009) Adlardia novaecaledoniae n.g., n.sp. (Digenea: Cryptogonimidae) from the fork-tailed threadfin bream Nemipterus furcosus (Val.) (Perciformes: Nemipteridae) off New Caledonia. Syst Parasitol 73:151–160.  https://doi.org/10.1007/s11230-009-9187-5 CrossRefGoogle Scholar
  27. 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.  https://doi.org/10.1007/s004360050047 CrossRefGoogle Scholar
  28. Miquel J, Świderski Z, Sripa B, Ribas A (2017) Ultrastructural characters of the spermatozoon of the liver fluke Opisthorchis viverrini (Poirier, 1886) (Opisthorchiidae). Parasitol Res 116:2499–2506.  https://doi.org/10.1007/s00436-017-5559-y CrossRefGoogle Scholar
  29. Ndiaye PI, Quilichini Y, Sène A, Bray RA, Bâ CT, Marchand B (2013) Prosorchis palinurichthi Kurochkin. Parukhin & Korotaeva, 1971 (Digenea, Sclerodistomidae): ultrastructure of the mature spermatozoon. Zool Anz 252:404–409.  https://doi.org/10.1016/j.jcz.2012.11.001 CrossRefGoogle Scholar
  30. Ndiaye PI, Quilichini Y, Sène A, Tkach VV, Bâ CT, Marchand B (2014) Ultrastructural characters of the spermatozoa in digeneans of the genus Lecithochirium Lühe, 1901 (Digenea, Hemiuridae), parasites of fishes: comparative study of L. microstomum and L. musculus. Parasite 21:49.  https://doi.org/10.1051/parasite/2014050 CrossRefGoogle Scholar
  31. Ndiaye PI, Bakhoum AJS, Sène A, Diagne PM, 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 Zool (Stockh) 96:91–98.  https://doi.org/10.1111/azo.12054 CrossRefGoogle Scholar
  32. Ndiaye PI, Quilichini Y, Marigo AM, Bâ CT, Tkach VV, Marchand B (2017) Ultrastructural characteristics of the mature spermatozoon of the digenean Sclerodistomum italicum (Stossich, 1893) (Hemiuroidea, Sclerodistomidae) intestinal parasite of Hypocanthus amia (Teleostei, Carangidae). Tissue Cell 49:15–21.  https://doi.org/10.1016/j.tice.2016.12.007 CrossRefGoogle Scholar
  33. Pamplona-Basilio MC, Baptista-Farias MFD, Kohn A (2001) Spermatogenesis and spermiogenesis in Didymocystis wedli Ariola, 1902 (Didymozoidae, Digenea). Mem Inst Oswaldo Cruz 96:1153–1159CrossRefGoogle Scholar
  34. 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.  https://doi.org/10.1007/s00436-007-0599-3 CrossRefGoogle Scholar
  35. Quilichini Y, Foata J, Justine J-L, Bray RA, Marchand B (2009) Sperm ultrastructure of the digenean Siphoderina elongata (Platyhelminthes, Cryptogonimidae) intestinal parasite of Nemipterus furcosus (Pisces, Teleostei). Parasitol Res 105:87–95.  https://doi.org/10.1007/s00436-009-1366-4 CrossRefGoogle Scholar
  36. Quilichini Y, Foata J, Justine J-L, Bray RA, Marchand B (2010a) Spermatozoon ultrastructure of Aponurus laguncula (Digenea: Lecithasteridae), a parasite of Aluterus monoceros (Pisces, Teleostei). Parasitol Int 59:22–28.  https://doi.org/10.1016/j.parint.2009.06.007 CrossRefGoogle Scholar
  37. Quilichini Y, Foata J, Justine J-L, Bray RA, 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.  https://doi.org/10.1016/j.parint.2010.06.002 CrossRefGoogle Scholar
  38. Quilichini Y, Foata J, Justine J-L, Bray RA, Marchand B (2011) Spermatozoon ultrastructure of Gyliauchen sp. (Digenea: Gyliauchenidae), an intestinal parasite of Siganus fuscescens (Pisces: Teleostei). Biol Bull 221:197–205CrossRefGoogle Scholar
  39. Rees FG (1979) The ultrastructure of the spermatozoon and spermiogenesis in Cryptocotyle lingua (Digenea: Heterophyidae). Int J Parasitol 9:405–419.  https://doi.org/10.1016/0020-7519(79)90044-4 CrossRefGoogle Scholar
  40. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212CrossRefGoogle Scholar
  41. 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.  https://doi.org/10.1007/s00436-008-1259-y CrossRefGoogle Scholar
  42. Thiéry JP (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc 6:987–1018Google Scholar
  43. WoRMS (2018) Cryptogonimidae Ward, 1917. http://www.marinespecies.org/aphia.php?p=taxdetails&id=108440 on 2018-11-01. Accessed 5 Oct 2018
  44. Zhukova MV, Mordvinov VA, Kiseleva E (2014) Ultrastructure of spermatozoa in the seminal receptacle of the liver fluke Opisthorchis felineus (Rivolta, 1884). Parasitol Res 113:1093–1101.  https://doi.org/10.1007/s00436-013-3746-z CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratoire de Biodiversité et Ecosystèmes Aquatiques, Département des Sciences de la VieFaculté des Sciences de SfaxSfaxTunisia
  2. 2.Secció de Parasitologia, Departament de Biologia, Sanitat i Medi Ambient, Facultat de Farmàcia i Ciències de l’AlimentacióUniversitat de BarcelonaBarcelonaSpain
  3. 3.Institut de Recerca de la Biodiversitat (IRBio)Universitat de BarcelonaBarcelonaSpain

Personalised recommendations