Skip to main content
SpringerLink
Log in

Ultrastructural characteristics of the vaginae of the basal monogenean Chimaericola leptogaster (Leuckart, 1830)

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

Abstract

In the first study of the vaginal ultrastructure of any monogenean, the paired vaginae of Chimaericola leptogaster, a basal polyopisthocotylean from the gills of a holocephalan, are described. Each vagina opens laterally. A unique feature of this relict parasite is a short vagino-intestinal connecting duct, the lining of which is separated by septate junctions from the linings of the vagina and the intestine. After giving rise to this vagino-intestinal duct, each vagina travels in a posterior direction and opens into the vitelline collecting duct. The lining of each vagina close to the vaginal pore resembles the body tegument, the syncytial lining of which measures about 2.5 μm in thickness and has a dense surface layer 0.2 μm in thickness and different apical projections. Proximal to this and before the entrance to the vaginal-intestinal duct, the vaginal lining is characterised by: uniformly distributed electron-dense, lanceolate, spine-like surface structures of about 1.7 μm in length; three kinds of surrounding glands with three kinds of secretory granules (abundant oval or rounded electron-dense granules 0.7–2.5 μm in length, much less numerous spheroidal, vesicular granules 0.3–0.4 μm in diameter, and tightly packed, spheroidal granules 0.8 μm in diameter and containing fine particulate material of low density); and four kinds of sensory receptors (three uniciliate and one aciliate). These features are absent from the rest of the vagina. The likely roles of the vagino-intestinal connection, the different gland cells, sensory structures, and the armament of the distal vaginal regions are discussed. Considering the suggested polyopisthocotylean ancestor for the Neodermata, the relict parasite fauna of holocephalans and the unique vagino-intestinal connection in C. leptogaster, which is also known in turbellarians, an ancient origin for chimaericolids is supported.

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
Figs. 2–6
Figs. 7–16
Figs. 17–25
Figs. 26–33

Similar content being viewed by others

References

  • Andersen K (1975) Ultrastructural studies on Diphyllobothrium ditremum and D. dendriticum (Cestoda, Pseudophyllidea), with emphasis on the scolex tegument and the tegument in the area around the genital atrium. Parasitol Res 46:253–264. doi:10.1007/BF00418519

    CAS  Google Scholar 

  • Beveridge I, Smith K (1985) An ultrastructural study of the cirrus and vagina of Phyllobothrium vagans (Cestoda: Tetraphyllidea). Parasitol Res 71:609–616. doi:10.1007/BF00925594

    Google Scholar 

  • Beverley-Burton M, Chisholm LA, Allison FR (1993) The species of Callorhynchicola Brinkmann (Monogenea: Chimaericolidae) from Callorhinchus spp. (Chimaeriformes: Callorhinchidae): adult morphology and the larval haptor. Syst Parasitol 24:201–215. doi:10.1007/BF00010533

    Article  Google Scholar 

  • Boeger WA, Kritsky DC (1993) Phylogeny and a revised classification of the Monogenoidea Bychowsky, 1937 (Platyhelminthes). Syst Parasitol 26:1–32. doi:10.1007/BF00009644

    Article  Google Scholar 

  • Boeger WA, Kritsky DC (1997) Coevolution of the Monogenoidea (Platyhelminthes) based on a revised hypothesis of parasite phylogeny. Int J Parasitol 27:1495–14511. doi:10.1016/S0020-7519(97)00140-9

    Article  PubMed  CAS  Google Scholar 

  • Boeger WA, Kritsky DC (2001) Phylogenetic relationships of the Monogenoidea. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, UK, pp 92–102

    Google Scholar 

  • Brinkmann A Jr (1952a) Fish trematodes from Norwegian water. The history of fish trematode investigations in Norway and the Norwegian species of the order Monogenea Arbok for Universitetet i Bergen. Naturvitenskapelig rekke 1:1–74

    Google Scholar 

  • Brinkmann A Jr (1952b) Some Chilean monogenetic trematodes. Kungliga Fysiografiska Sällskapets i Lund. Förhandlingar 62:3–26

    Google Scholar 

  • Brinkmann A Jr (1942). On “Öctobothrium” leptogaster F.S. Leuckart. Göteborgs Kungl. Vetenskaps och Vitterhets Samhälles Handlingar, Ser. B 2: 3–29

  • Brooks DR (1989) The phylogeny of the Cercomeria (Platyhelminthes: Rhabdocoela) and general evolutionary principles. J Parasitol 75:606–616

    Article  PubMed  CAS  Google Scholar 

  • Bychowsky BE (1957) Monogenetic trematodes, their systematics and phylogeny. Izdatel’stvo Academiya Nauk SSSR, Moscow, Russia, In Russian

    Google Scholar 

  • El-Naggar MM, Arafa SZ, El-Abbassy SA, Steward MT, Halton DW (2007) Neuromusculature of Macrogyrodactylus congolensis, a monogenean skin parasite of the Nile catfish Clarias gariepinus. Parasitol Res 100:265–279

    Article  PubMed  CAS  Google Scholar 

  • Euzet L, Combes C (2003) Some controversial questions regarding Monogenea. In: Combes C, Jourdane J (eds) Taxonomy, ecology and evolution of metazoan parasites. Vol. 1. Presses Universitaires de Perpignan, Perpignan, France, pp 303–320

    Google Scholar 

  • Gibson DI, Bray RA (1979) The Hemiuroidea: terminology, systematics and evolution. Bull Brit Mus Nat Hist (Zool) 36:35–146

    Google Scholar 

  • Gremigni V (1983) Platyhelminthes—Turbellaria. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates. Vol. 1. Oogenesis, oviposition and oosorption. John Wiley & Sons Ltd, Chichester, UK, pp 67–107

    Google Scholar 

  • Gustafsson MKS, Halton DW, Kreshchenko ND, Movsessian SO, Raikova OI, Reuter M, Terenina NB (2002) Neuropeptides in flatworms. Peptides 23:2053–2061. doi:10.1016/S0196-9781(02)00193-6

    Article  PubMed  CAS  Google Scholar 

  • Halton DW, Hardcastle A (1977) Ultrastructure of the male accessory ducts and prostate gland of Diclidophora merlangi (Monogenoidea). Int J Parasitol 7:393–401. doi:10.1016/0020-7519(77)90065-0

    Article  Google Scholar 

  • Halton DW, Morris GP (1969) Occurrence of cholinesterase and ciliated sensory receptors in a fish gill fluke, Diclidophora merlangi (Trematoda; Monogenea). Parasitol Res 33:21–30. doi:10.1007/BF00259567

    Google Scholar 

  • Halton DW, Brennan GP, Maule AG, Shaw C, Johnston CF, Fairweather I (1991) The ultrastructure and immunogold labelling of pancreatic polypeptide-immunoreactive cells associated with the egg-forming apparatus of a monogenean parasite, Diclidophora merlangi. Parasitology 102:429–436. doi:10.1017/S003118200006404

    Article  PubMed  Google Scholar 

  • Inoue JG, Miya M, Lam K, Tay BH, Danks JA, Bell J, WalkerTI VB (2010) Evolutionary origin and phylogeny of the modern holocephalans (Chondrichthyes: Chimaeriformes): a mitogenomic perspective. Mol Biol Evol 27:2576–2586. doi:10.1093/molbev/msq147

    Article  PubMed  CAS  Google Scholar 

  • Jovelin R, Justine J-L (2001) Phylogenetic relationships within the polyopisthocotylean monogeneans (Platyhelminthes) inferred from partial 28S rDNA sequences. Int J Parasitol 31:393–401. doi:10.1016/S0020-7519(01)00114-X

    Article  PubMed  CAS  Google Scholar 

  • Kearn GC (1986) The eggs of monogeneans. Adv Parasitol 25:175–273. doi:10.1016/S0065-308X(08)60344-9

    Article  PubMed  CAS  Google Scholar 

  • Kearn GC, Evans-Gowing R (1998) Attachment and detachment of the anterior adhesive pads of the monogenean (platyhelminth) parasite Entobdella soleae from the skin of the common sole (Solea solea). Int J Parasitol 28:1583–1593. doi:10.1016/S0020-7519(98)00059-9

    Article  PubMed  CAS  Google Scholar 

  • Kearn GC, Whittington ID, Evans-Gowing R (1995) Use of cement for attachment in Neocalceostomoides brisbanensis, a calceostomatine monogenean from the gill chamber of the blue catfish, Arius graeffei. Int J Parasitol 25:299–306. doi:10.1016/0020-7519(94)00142-B

    Article  PubMed  CAS  Google Scholar 

  • Littlewood DTJ, Rohde K, Clough KA (1999) The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biol J Linn Soc 66:75–114. doi:10.1111/j.1095-8312.1999.tb01918.x

    Article  Google Scholar 

  • Llewellyn J (1965) The evolution of parasitic platyhelminths. In: Taylor A (ed) Evolution of parasites. Third symposium of the British Society for Parasitology. Blackwell, Oxford, UK, pp 47–78

    Google Scholar 

  • Llewellyn J, Simmons JE (1984) The attachment of the monogenean parasite Callorhynchicola multitesticulatus to the gills of its holocephalan host Callorhynchus milii. Int J Parasitol 14:191–196. doi:10.1016/0020-7519(84)90048-1

    Article  Google Scholar 

  • Maule AG, Halton DW, Johnston CF, Shaw C, Fairweather I (1990) A cytochemical study of the serotoninergic, cholinergic and peptidergic components of the reproductive system in the monogenean parasite Diclidophora merlangi. Parasitol Res 76:409–419. doi:10.1007/BF00933549

    Article  PubMed  CAS  Google Scholar 

  • Ogawa K (1997) Copulation and egg production of the monogenean Heterobothrium okamotoi, a gill parasite of cultured tiger puffer (Takifugu rubripes). Fish Pathol 32:219–223. doi:10.3147/jsfp.32.219

    Article  Google Scholar 

  • Pascoe PL (1997) Monogenean parasites of deep-sea fishes from the Rockall Trough (N.E. Atlantic) including a new species. J Mar Biol Ass UK 67:603–622. doi:10.1017/S0025315400027326

    Google Scholar 

  • Perkins EM, Donnellan SC, Bertozzi T, Whittington ID (2010) Closing the mitochondrial circle on paraphyly of the Monogenea (Platyhelminthes) infers evolution in the diet of parasitic flatworms. Int J Parasitol 40:1237–1245. doi:10.1016/j.ijpara.2010.02.0171

    Article  PubMed  CAS  Google Scholar 

  • Poddubnaya LG (2002) Ultrastructure of the reproductive ducts of Diphyllobothrium latum (Cestoda, Pseudophyllidea) males. Zool Zh 81:394–405 (In Russian)

    Google Scholar 

  • Rohde K (1972) Ultrastructure of the nerves and sense receptors of Polystomoides renschi Rohde and P. malayi (Rohde) (Monogenea: Polystomatidae). Parasitol Res 40:307–320. doi:10.1007/BF00328749

    CAS  Google Scholar 

  • Rohde K (1973) Ultrastructure of the caecum of Polystomoides malayi Rohde and P. renschi Rohde (Monogenea: Polystomatidae). Int J Parasitol 3:461–466. doi:10.1016/0020-7519(73)90040-4

    Article  PubMed  CAS  Google Scholar 

  • Rohde K, Ebrahimzadeh A (1969) Das weibliche Geschlechtssystem der Gattung Polystomoides Ward, 1917 (Monogenea). Parasitol Res 33:110–134. doi:10.1007/BF00259512

    CAS  Google Scholar 

  • Rohde K, Watson NA (1995) Ultrastructure of the buccal complex of Polylabroides australis (Monogenea, Polyopisthocotylea, Microcotylidae). Int J Parasitol 3:307–318. doi:10.1016/0020-7519(94)00083-Z

    Article  Google Scholar 

  • Rohde K, Watson NA (1996) Ultrastructure of the buccal complex of Pricea multae (Monogenea: Polyopisthocotylea, Gastrocotylidea). Folia Parasitol 43:117–132

    Google Scholar 

  • Tyler S (1976) Comparative ultrastructure of adhesive systems in the Turbellaria. Zoomorphol 84:1–76. doi:10.1007/BF0256855

    Article  Google Scholar 

  • Whittington ID, Cribb BW (1999) Morphology and ultrastructure of the anterior adhesive areas of the capsalid monogenean parasites Benedenia rohdei from the gills and B. lutjani from the pelvic fins of Lutjanus carponotatus (Pisces: Lutjanidae). Parasitol Res 85:399–408. doi:10.1007/s004360050566

    Article  PubMed  CAS  Google Scholar 

  • Whittington ID, Cribb BW (2001) Adhesive secretions in the Platyhelminthes. Adv Parasitol 48:101–223. doi:10.1016/S0065-308X(01)48006-7

    Article  PubMed  CAS  Google Scholar 

  • Whittington ID, Armstrong WD, Cribb BW (2004) Mechanism of adhesion and detachment at the anterior end of Neoheterocotyle rhinobatidis and Troglocephalus rhinobatidis (Monogenea: Monopisthocotylea: Monocotylidae). Parasitol Res 94:91–95. doi:10.1007/s00436-004-1171-z

    PubMed  CAS  Google Scholar 

  • Wong W-L, Brennan GP, Halton DW, Maule AG, Lim LHS (2008) Secretory products of the haptoral reservoirs and peduncular glands in two species of Bravohollisia (Monogenean: Ancyrocephalidae). Inverteb Biol 127:139–152. doi:10.1111/j.1744-7410.2007.00118.x

    Article  Google Scholar 

Download references

Acknowledgments

Special thanks are due to Prof. Odd Halvorsen, Natural History Museum, Oslo University, Norway for his kind assistance with finding a source of chimaeras. The authors would like to thanks the staff of the RV ‘Johan Ruud’, belonging to Tromsø University, for their invaluable help with the fishing. We are also grateful to the staff of the Centre of Electron Microscopy of the I.D. Papanin Institute of the Biology for Inland Waters, RAS, for technical assistance. The present study was supported by the Russian Foundation for Fundamental Research project no. 12-04-00149a (to LGP).

Author information

Authors and Affiliations

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

    Larisa G. Poddubnaya

  2. Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, University of Tromsø, 9037, Tromsø, Norway

    Willy Hemmingsen

  3. Department of Life Sciences, Natural History Museum, Cromwell Road, London, SW7 5BD, UK

    David I. Gibson

Authors
  1. Larisa G. Poddubnaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Willy Hemmingsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David I. Gibson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Larisa G. Poddubnaya.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Poddubnaya, L.G., Hemmingsen, W. & Gibson, D.I. Ultrastructural characteristics of the vaginae of the basal monogenean Chimaericola leptogaster (Leuckart, 1830). Parasitol Res 112, 4053–4064 (2013). https://doi.org/10.1007/s00436-013-3596-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-013-3596-8

Keywords

Search

Navigation