Skip to main content
SpringerLink
Log in

Ultrastructural features of the spermatozoon and its differentiation in Brandesia turgida (Brandes, 1888) (Digenea, Microphalloidea, Pleurogenidae)

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Spermatological characters of the digenean Brandesia turgida (Brandes, 1888), an intestinal parasite of the frog Pelophylax ridibundus (Pallas, 1771), have been investigated by means of transmission electron microscopy for the first time. The process of the spermatozoon formation begins with the appearance of the differentiation zone bordered by cortical microtubules and containing two centrioles associated with striated rootlets and with an intercentriolar body. The intercentriolar body is made up of seven distinct electron-dense plates, two less electron-dense, and four electron-lucent zones. The orthogonal development of the two flagella is followed by a flagellar rotation and their proximodistal fusion with the median cytoplasmic process. This process is accompanied by an extension of both the mitochondrion and nucleus into the median cytoplasmic process. The mature spermatozoon of B. turgida contains two parallel axonemes of unequal lengths with the 9 + “1” trepaxonematan pattern, mitochondrion, nucleus, parallel cortical microtubules, four electron-dense attachment zones, an external ornamentation of the plasma membrane, and electron-dense glycogen granules. The anterior extremity of the male gamete contains one complete centriole, a small component of the central element of the second centriole, and peripheral cortical microtubules (up to 45). The posterior extremity of the mature spematozoon exhibits tubular elements of the disorganized axoneme. The present study provides the first data on spermiogenesis within the family Pleurogenidae. Variations of the spermatozoa ultrastructural characters within Digenea, in particular, between different families of the superfamily Microphalloidea, are discussed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agostini S, Miquel J, Ndiaye PI, Marchand B (2005) Dicrocoelium hospes Looss, 1907 (Digenea, Dicrocoeliidae): spermiogenesis, mature spermatozoon and ultrastructural comparative study. Parasitol Res 96:38–48

    Article  PubMed  Google Scholar 

  • Bakhoum AJS, Bâ CT, 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). Rev Ibero-latinoam Parasitol 1:32–45

    Google Scholar 

  • Bakhoum AJS, Bâ CT, Shimalov VV, Torres J, Miquel J (2011a) Spermatological characters of the digenean Rubenstrema exasperatum (Rudolphi, 1819) (Plagiorchioidea, Omphalometridae). Parasitol Res 108:1283–1293

    Article  PubMed  Google Scholar 

  • Bakhoum AJS, Torres J, Shimalov VV, Bâ CT, 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

    Article  CAS  PubMed  Google Scholar 

  • Bakhoum AJS, Feliu C, Bâ CT, Miquel J (2012) Spermiogenesis and spermatozoon of the liver fluke Mediogonimus jourdanei (Microphalloidea: Prosthogonimidae), a parasite of the bank vole Myodes glareolus (Rodentia: Cricetidae). Folia Parasitol 59:32–42

    Article  PubMed  Google Scholar 

  • Bakhoum AJS, Ribas A, Eira C, Bâ CT, Miquel J (2013) Brachycoelium salamandrae (Frölich, 1789) (Digenea: Brachycoeliidae): ultrastructural study of spermiogenesis and the mature spermatozoon. Zool Anz 252:149–156

    Article  Google Scholar 

  • Bray RA (2008) Superfamily Microphalloidea Ward, 1901. In: Bray RA, Jones A, Gibson DI (eds) Keys to the Trematoda, vol 3. CABI, Wallingford, pp 447–450

    Google Scholar 

  • Bruňanská M (2010) Recent insights into spermatozoa development and ultrastructure in the Eucestoda. In: Lejeune T, Delvaux P (eds) Human spermatozoa: Maturation, capacitation and abnormalities. Nova Science, New York, pp 327–354

    Google Scholar 

  • Bruňanská M, Poddubnaya LG, Xylander WER (2013) A reinvestigation of spermiogenesis in Amphilina foliacea (Platyhelminthes: Amphilinidea). Folia Parasitol 60:43–50

    Article  PubMed  Google Scholar 

  • Burton PR (1972) Fine structure of the reproductive system of a frog lung-fluke: III. The spermatozoon and its differentiation. J Parasitol 58:68–83

    Article  CAS  PubMed  Google Scholar 

  • Castilho F, Barandela T (1990) Ultrastructural study on the spermiogenesis and spermatozoon of the metacercariae of Microphallus primas (Digenea), a parasite of Carcinus maenas. Mol Reprod Dev 25:140–146

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ehlers U (1985) Phylogenetic relationship within the Platyhelminthes. In: Conway Morris S, George JD, Gibson R, Platt HM (eds) The origin and relationships of lower invertebrates. Oxford University Press, Oxford, pp 143–158

    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. Parasitol Res 101:843–852

    Article  PubMed  Google Scholar 

  • Gracenea M, Ferrer JR, González-Moreno O, Trullols M (1997) Ultrastructural study of spermatogenesis and spermatozoon in Postorchigenes gymnesicus (Trematoda, Lecithodendriidae). J Morphol 234:223–232

    Article  Google Scholar 

  • Hendow HT, James BL (1988) Ultrastructure of spermatozoon and spermatogenesis in Maritrema linguilla (Digenea: Microphallidae). Int J Parasitol 18:53–63

    Article  CAS  PubMed  Google Scholar 

  • Hoberg EP, Mariaux J, Brooks DR (2001) Phylogeny among the orders of the Eucestoda (Cercomeromorphae): integrating morphology, molecules and total evidence. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp 112–126

    Google Scholar 

  • Justine JL (1995) Spermatozoal ultrastructure and phylogeny of the parasitic Platyhelminthes. Mém Mus Natl Hist Nat 166:55–86

    Google Scholar 

  • Justine JL (1998) Spermatozoa as phylogenetic characters for the Eucestoda. J Parasitol 84:385–408

    Article  CAS  PubMed  Google Scholar 

  • Justine JL (2001) Spermatozoa as phylogenetic characters for the Platyhelminthes. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp 231–238

    Google Scholar 

  • Justine JL (2003) Ultrastructure des spermatozoïdes et phylogénie des Neodermata. In: Combes C, Jourdane J (eds) Taxonomie, Écologie et Évolution des Métazoaires Parasites. PUP, Perpignan, pp 359–380

    Google Scholar 

  • Justine JL, Mattei X (1984) Atypical spermiogenesis in a parasitic flatworm, Didymozoon (Trematoda: Digenea: Didymozoidae). J Ultrastruct Res 87:106–111

    Article  Google Scholar 

  • Kacem H, Bakhoum AJS, Torres J, Neifar L, Miquel J (2010) Spermiogenesis and ultrastructure of the spermatozoon of Neoapocreadium chabaudi Kohn & Fernandes, 1982 (Digenea, Apocreadiidae), a parasite of Ballistes capriscus (Pisces, Teleostei). Parasitol Int 59:358–366

    Article  CAS  PubMed  Google Scholar 

  • 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. CR Biol 335:637–644

    Article  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 Parasitol 48:255–264

    Google Scholar 

  • Levron C, Ternengo S, Marchand B (2004a) Spermiogenesis and sperm ultrastructure of Diphterostomum brusinae (Digenea, Zoogonidae), a parasite of Diplodus annularis (Pisces, Teleostei). Parasitol Res 94:147–154

    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 Parasitol 49:190–200

    Google Scholar 

  • Levron C, Ternengo S, Marchand B (2004c) 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Lotz JM, Font WF (2008) Family Pleurogenidae Looss 1899. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol. 3. CABI Publishing, Wallingford, pp 563–575

    Google Scholar 

  • Miquel J, Nourrisson C, Marchand B (2000) Ultrastructure of spermiogenesis and the spermatozoon of Opecoeloides furcatus (Trematoda, Digenea, Opecoelidae), a parasite of Mullusbarbatus (Pisces, Teleostei). Parasitol Res 86:301–310

    Article  CAS  PubMed  Google Scholar 

  • Miquel J, Fournier-Chambrillon C, Fournier P, Torres J (2006) Spermiogenesis and spermatozoon of the cranial digenean Troglotrema acutum (Leuckart, 1842). J Parasitol 92:441–453

    Article  PubMed  Google Scholar 

  • Miquel J, Vilavella D, Świderski Z, Shimalov VV, Torres J (2013) Spermatological characteristics of Pleurogenidae (Digenea) inferred from the ultrastructural study of Pleurogenes claviger, Pleurogenoides medians and Prosotocus confusus. Parasite 20:28

    Article  PubMed Central  PubMed  Google Scholar 

  • Ndiaye PI, 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 Parasitol 48:182–194

    Google Scholar 

  • Ndiaye PI, Quilichini Y, Sène A, Tkach VV, Bâ CT, 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

    Article  PubMed  Google Scholar 

  • Ndiaye PI, Quilichini Y, Tkach VV, Greiman SE, Bâ CT, Marchand B (2013) Ultrastructure of the spermatozoon of the digenean Plagiorchis elegans (Rudolphi, 1802) (Plagiorchioidea, Plagiorchiidae). J Morphol 274:965–972

    Article  CAS  PubMed  Google Scholar 

  • Pamplona-Basilio MC, Baptista-Farias MFD, Kohn A (2001) Spermatogenesis and spermiogenesis in Didymocystis wedli Ariola, 1902 (Didymozoidae, Digenea). Mem Inst Oswaldo Cruz 96:1153–1159

    Article  CAS  PubMed  Google Scholar 

  • Poddubnaya LG, Bruňanská M, Brázová T, Zhokhov AE, Gibson DI (2013) Ultrastructural characteristics of the vitellarium of Brandesia turgida (Brandes, 1888) (Digenea: Pleurogenidae) and an examination of the potential usefulness of such vitelline traits in digenean systematics. Helminthologia 50:119–126

    Article  Google Scholar 

  • Quilichini Y, Foata J, Marchand B (2007a) 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

    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). J Parasitol 93:458–468

    Article  PubMed  Google Scholar 

  • Quilichini Y, Foata J, Orsini A, Marchand B (2007c) Spermiogenesis and spermatozoon ultrastructure of Nicolla wisniewskii (Digenea: Opecoelidae), an intestinal parasite of brown trout Salmo trutta (Pisces: Teleostei). J Parasitol 93:469–478

    Article  PubMed  Google Scholar 

  • Quilichini Y, Foata J, Justine JL, Bray RA, Marchand B (2010) Ultrastructural study of the spermatozoon of Heterolebes maculosus (Digenea, Opistholebetidae), a parasite of the porcupinefish Diodon hystrix (Pisces, Teleostei). Parasitol Int 59:427–434

    Article  CAS  PubMed  Google Scholar 

  • Quilichini Y, Foata J, Justine JL, Bray RA, Marchand B (2011) Spermatozoon ultrastructure of Gyliauchen sp. (Digenea: Gyliauchenidae), an intestinal parasite of Siganus fuscescens (Pisces: Teleostei). Biol Bull 221:197–205

    CAS  PubMed  Google Scholar 

  • Robinson RD, Halton DW (1982) Fine structural observations on spermatogenesis in Corrigia vitta (Trematoda: Dicrocoeliidae). Z Parasitenkd 68:53–72

    Article  Google Scholar 

  • Rohde K (1988) Phylogenetic relationship of free-living and parasitic Platyhelminthes on the basis of ultrastructural evidence. In: Ax P, Ehlers U (eds) Free-living and symbiotic Platyhelminthes. Gustav Fischer Verlag, Stuttgart, pp 353–357

    Google Scholar 

  • Sharma PN, Rai N (1995) Ultrastructural study on spermatogenesis in Ganeo trigrinum, an intestinal trematode of Ranatigrina. J Helminthol 69:77–84

    Article  Google Scholar 

  • Świderski Z, Poddubnaya LG, Zhokhov AE, Miquel J, Gibson DI (2013) An ultrastructural study of the egg wall surrounding the miracidium of the digenean Brandesia turgida (Brandes, 1888) (Plagiorchiida: Pleurogenidae), with the description of a unique cocoon-like envelope. Zool Anz 253:114–118

    Article  Google Scholar 

  • Tkach VV, Littlewood TDJ, Olson PD, Kinsella M, Świderski Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst Parasitol 56:1–15

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The authors are grateful to the staff of the Centre of Electron Microscopy, I.D. Papanin Institute for the Biology of Inland Waters, Russian Academy of Sciences, Borok, Russia, for technical assistance. The work was realized within the framework of a project of the Parasitological Research and Training Centre of the SAS (Code ITMS: 26110230045) based on the support of the Operational Programme “Education” funded from the European Regional Development Fund. The present study was supported by the Russian Foundation for Fundamental Research (Project no. 12-04-00149-a to LP) and the Grant Agency of the Slovak Republic VEGA (Project no. 2/0047/11 to MB).

Author information

Authors and Affiliations

  1. Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, 040 01, Košice, Slovak Republic

    Magdaléna Bruňanská & Timea Brázová

  2. I.D. Papanin Institute for Biology of Inland Waters, Russian Academy of Sciences, 152742, Borok, Yaroslavl Province, Russia

    Alexander E. Zhokhov & Larisa G. Poddubnaya

Authors
  1. Magdaléna Bruňanská
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Timea Brázová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexander E. Zhokhov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Larisa G. Poddubnaya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Magdaléna Bruňanská.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bruňanská, M., Brázová, T., Zhokhov, A.E. et al. Ultrastructural features of the spermatozoon and its differentiation in Brandesia turgida (Brandes, 1888) (Digenea, Microphalloidea, Pleurogenidae). Parasitol Res 113, 2483–2491 (2014). https://doi.org/10.1007/s00436-014-3897-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-3897-6

Keywords

Search

Navigation