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Cytocomposition of the vitellarium in Khawia sinensis Hsü, 1935 (Cestoda, Caryophyllidea, Lytocestidae): another caryophyllidean species with lamellar bodies and lipids

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Abstract

The vitellarium of the invasive caryophyllidean tapeworm Khawia sinensis Hsü, 1935 from carp Cyprinus carpio L. was examined by means of transmission electron microscopy and cytochemical staining for glycogen with periodic acid–thiosemicarbazide–silver proteinate (PA-TSC-SP). A vitellarium consists of numerous follicles of irregular size that are interconnected by a net of vitelline ducts. Vitelline follicles are composed of vitelline cells at various stages of development that are interconnected by interstitial tissue. Vitelline follicles are surrounded by a cytoplasmic sheath associated with an intercellular matrix. Extensive development of the granular endoplasmic reticulum and Golgi complexes are both involved in the production of shell globules/shell globule clusters and characterise cytodifferentiation of vitellocytes. Nuclear and nucleolar transformation lead to the formation and storage of intranuclear glycogen, a feature specific for the Caryophyllidea. Newly observed within the mature vitellocytes of Khawia sp. is the presence of lamellar bodies and a few lipid droplets. These cytoplasmic inclusions first occur in the mature cells within the follicles and persist in the vitelline cells within vitelloducts and intrauterine eggs. Two types of lamellar bodies are detected: regular lamellar-structured body and irregular lamellar-structured body. None of the lamellar bodies are membrane bound. Results of the present study indicate that the formation of lamellar bodies may be closely related to the endoplasmic reticulum or shell globule clusters. Some of the shell globule clusters are transformed into lamellar body clusters. Ultrastructural features of vitellocytes in K. sinensis are compared with those of other monopleuroid, polypleuroid, and strobilated cestodes.

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References

  • Arafa SZA (2012a) Ultrastructure of vitellocytes in Electrotaenia malopteruri (Fritsch, 1886) (Cestoda: Proteocephalidae), a parasite of Malapterurus electricus (Siluriformes: Malapteruridae) from Egypt. Life Sci J 9:1410–1414

    Google Scholar 

  • Arafa SZA (2012b) Light and electron microscopic study on vitellogenesis of the caryophyllidean cestode Monobothrioides chalmersius (Woodland, 1924) Hunter, 1930 (Lytocestidae) from the catfish Clarias gariepinus. J Basic Appl Zool 65:125–132

    Article  Google Scholar 

  • Björkman N, Thorsell W (1963) On the fine morphology of the formation of the eggshell globules in vitelline glands of the liver fluke (Fasciola hepatica L.). Exp Cell Res 39:18–28

    Google Scholar 

  • Bruňanská M (1997) Proteocephalus exiguus La Rue 1911 (Cestoda, Proteocephalidae): ultrastructure of the vitelline cells. Helminthologia 34:9–13

    Google Scholar 

  • Bruňanská M (1999) Ultrastructure of primary embryonic envelopes in Proteocephalus longicollis (Cestoda, Proteocephalidea). Helminthologia 36:83–89

    Google Scholar 

  • Bruňanská M, Drobníková P, Mackiewicz JS, Nebesářová J (2013) Reinvestigation of vitellogenesis in Caryophyllaeus laticeps (Pallas, 1781) (Cestoda, Caryophyllidea, Caryophyllaeidae), monozoic tapeworm of Abramis brama (Pisces: Teleostei). Helminthologia 50:73–81

    Article  Google Scholar 

  • Bruňanská M, Drobníková P, Oros M (2009) Vitellogenesis in the cestode Atractolytocestus huronensis Anthony, 1958 (Caryophyllidea: Lytocestidae). Parasitol Res 105:647–654

    Article  PubMed  Google Scholar 

  • Bruňanská M, Drobníková P, Oros M, Poddubnaya LG, Hanzelová V (2010) Caryophyllidea: comparative ultrastructure of the vitellocytes. Proceed ICOPA XII, Melbourne, Australia, p. 833

    Google Scholar 

  • Bruňanská M, Mackiewicz JS, Młocicki D, Świderski Z, Nebesářová J (2012a) Early intrauterine embryonic development in Khawia sinensis Hsü, 1935 (Cestoda, Caryophyllidea, Lytocestidae), an invasive tapeworm of carp (Cyprinus carpio): an ultrastructural study. Parasitol Res 110:1009–1017

    Article  PubMed  Google Scholar 

  • Bruňanská M, Mackiewicz JS, Nebesářová J (2012b) Vitellogenesis in Archigetes sieboldi Leuckart, 1878 (Cestoda, Caryophyllidea, Caryophyllaeidae), an intestinal parasite of carp (Cyprinus carpio L.). Histol Histopathol 27:1611–1620

    PubMed  Google Scholar 

  • Bruňanská M, Poddubnaya LG, Dezfuli BS (2005) Vitellogenesis in two spathebothriidean cestodes. Parasitol Res 96:390–397

    Article  PubMed  Google Scholar 

  • Erasmus DA (1973) A comparative study of the reproductive system of mature, immature and ‘unisexual’ female Schistosoma mansoni. Parasitology 67:165–183

    Article  PubMed  CAS  Google Scholar 

  • Falleni A, Lucchesi P, Gremigni V (2001) The ultrastructure of oocyte and vitellocyte inclusions in a scutariellid (Platyhelminthes, Rhabdocoela, Temnocephalida) with phylogenetic implications. Belg J Zool 131(Suppl):187–189

    Google Scholar 

  • Grant WC, Harkema R, Muse KE (1977) Ultrastructure of Pharyngostomoides procyonis Harkema (1942) (Diplostomatidae). II. The female reproductive system. J Parasitol 63:1019–1030

  • Gremigni V, Falleni A (1991) Ultrastructural features of cocoon-shell globules in the vitelline cells of neoophoran platyhelminths. Hydrobiologia 227:105–111

    Article  Google Scholar 

  • Gremigni V, Falleni A (1998) Characters of the female gonad and the phylogeny of Platyhelminthes. Hydrobiologia 383:235–242

    Article  Google Scholar 

  • Halton DW, Stranock SD, Hardcastle A (1974) Vitelline cell development in monogenean parasites. Z Parasitenkd 45:45–61

    Article  PubMed  CAS  Google Scholar 

  • Hanna REB (1976) Fasciola hepatica: a light and electron autoradiographic study of shell protein and glycogen synthesis by vitelline follicles in tissue slices. Exp Parasitol 39:18–28

    Article  PubMed  CAS  Google Scholar 

  • Irwin SW, Threadgold LT (1970) Electron-microscope studies on Fasciola hepatica VIII. The development of the vitelline cells. Exp Parasitol 28:399–411

    Article  PubMed  CAS  Google Scholar 

  • Korneva JV (2001) Vitellogenesis and capsule formation during embryogenesis in Triaenophorus nodulosus (Cestoda, Pseudophyllidea, Triaenophoridae). Zool Zh 80:1422–1428

    Google Scholar 

  • Korneva JV (2002) Fine structure of reproductive system in Nippotaenia mogurndae (Cestoda, Nippotaeniidea). Zool Zh 81:266–275

    Google Scholar 

  • Korneva JV, Davydov VG (2001) The female reproductive system in the proteocephalidean cestode Gangesia parasiluri (Cestoda, Proteocephalidea, Proteocephalidae). Zool Zh 80:131–144

    Google Scholar 

  • Levron C, Poddubnaya LG, Kuchta R, Freeman M, Scholz T (2007) Vitellogenesis and vitelline system in the pseudophyllidean tapeworm Paraechinophallus japonicus: ultrastructural and cytochemical studies. Folia Parasitol 54:43–50

    PubMed  Google Scholar 

  • Mackiewicz JS (1968) Vitellogenesis and egg-shell formation in Caryophyllaeus laticeps (Pallas) and Caryophyllaeoides fennica (Schneider) (Cestoidea: Caryophyllidea). Z Parasitenkd 30:18–32

    Article  PubMed  CAS  Google Scholar 

  • Młocicki D, Świderski Z, Mackiewicz JS, Ibraheem MH (2010) Ultrastructure of intrauterine eggs: evidence of early ovoviviparity in the caryophyllidean cestode Wenyonia virilis Woodland, 1923. Acta Parasitol 55:349–358

    Article  Google Scholar 

  • Młocicki D, Świderski Z, Mackiewicz JS, Ibraheem MH (2011) Ultrastructural and cytochemical studies of GER-bodies in the intrauterine eggs of Wenyonia virilis Woodland, 1923 (Cestoda, Caryophyllidea). Acta Parasitol 56:40–47

    Article  Google Scholar 

  • Oros M, Hanzelová V, Scholz T (2009) Tapeworm Khawia sinensis: Review of the introduction and subsequent decline of a pathogen of carp, Cyprinus carpio. Vet Parasitol 164:217–222

    Article  PubMed  Google Scholar 

  • Ortner-Schönbach P (1913) Zur Morphologie des Glykogens bei Trematoden und Cestoden. Arch Zellforsch 11:413–449

    Google Scholar 

  • Poddubnaya LG, Bruňanská M, Świderski Z, Gibson DI (2012) Ultrastructure of the vitellarium in the digeneans Phyllodistomum angulatum (Plagiorchiida: Gorgoderidae) and Azygia lucii (Strigeida: Azygiidae). Acta Parasitol 57:235–246

    Article  PubMed  Google Scholar 

  • Poddubnaya LG, Bruňanská M, Świderski Z, Gibson DI (2013) Ultrastructure of the vitellarium of Ancyrocephalus paradoxus (Monogenea: Monopisthocotylea), with comments on the nature of the vitellarium in the Monogenea and related platyhelminth groups. Parasitol Res 112:1169–1177

    Article  PubMed  Google Scholar 

  • Poddubnaya LG, Gibson DI, Świderski Z, Olson PD (2006) Vitellocyte ultrastructure in the cestode Didymobothrium rudolphi (Monticelli, 1890): possible evidence for the recognition of divergent taxa within the Spathebothriidea. Acta Parasitol 51:255–263

    Article  Google Scholar 

  • Scholz T, Brabec J, Kráľová-Hromadová I, Oros M, Bazsalovicsová E, Ermolenko A, Hanzelová V (2011) Revision of Khawia spp. (Cestoda: Caryophyllidea), parasites of cyprinid fish, including a key to their identification and molecular phylogeny. Folia Parasitol 58:197–223

    PubMed  Google Scholar 

  • Świderski Z, Bruňanská M, Poddubnaya LG (2004a) Ultrastructural and cytochemical studies on vitellogenesis in the caryophyllidean cestode Caryophyllaeus laticeps. Proceed IX Eur Multicolloq Parasitol. Valencia, Spain, p. 602

  • Świderski Z, Bruňanská M, Poddubnaya LG, Mackiewicz JS (2004b) Cytochemical and ultrastructural study on vitellogenesis in caryophyllidean cestode Khawia armeniaca (Cholodkovski, 1915). Acta Parasitol 49:16–24

    Google Scholar 

  • Świderski Z, Gibson DI, Marigo AM, Delgado E, Torres J, Miquel J (2011a) Ultrastructure and cytochemistry of vitellogenesis and the vitellocytes of the bothriocephalidean cestode Clestobothrium crassiceps (Rudolphi, 1819), a parasite of the teleost fish Merluccius merluccius (L., 1758) (Gadifores, Merlucciidae). Acta Parasitol 56:392–405

    Article  Google Scholar 

  • Świderski Z, Mackiewicz JS (1976) Electron microscope study of vitellogenesis in Glaridacris catostomi (Cestoidea: Caryophyllidea). Int J Parasitol 6:61–73

    Article  PubMed  Google Scholar 

  • Świderski Z, Mackiewicz JS, Eira C, Miquel J (2011b) Ultrastructural and cytochemical study on vitellogenesis in the diphyllidean cestode Echinobothrium euterpes (Echinobothriidae) and its phylogenetical implications. Acta Parasitol 56:180–190

    Article  Google Scholar 

  • Świderski Z, Miquel J, Marigo AM, Gibson DI (2012) Ultrastructure of vitellogenesis and vitellocytes in the trypanorhynch cestode Aporhynchus menezesi, a parasite of the velvet belly lanternshark Etmopterus spinax. CR Biologies 335:573–584

    Article  Google Scholar 

  • Świderski Z, Miquel J, Młocicki D, Neifar L, Grytner-Zięcina B, Mackiewicz JS (2006a) Ultrastructural and cytochemical studies on vitellogenesis in the trypanorhynch cestode Dolfusiella spinulifera Beveridge, Neifar et Euzet, 2004 (Eutetrarhynchidae). Acta Parasitol 51:182–193

    Article  Google Scholar 

  • Świderski Z, Miquel J, Młocicki D, Neifar L, Grytner-Zięcina B, Mackiewicz JS (2006b) Ultrastructure of the vitellocytes in the cestode Progrillotia pastinacae Dollfus, 1946 (Trypanorhyncha, Progrillotiidae). Acta Parasitol 51:194–199

    Article  Google Scholar 

  • Świderski Z, Młocicki D, Mackiewicz JS, Miquel J, Ibraheem MH, Bruňanská M (2009) Ultrastructure and cytochemistry of vitellogenesis in Wenyonia virilis Woodland, 1923 (Cestoda, Caryophyllidea). Acta Parasitol 54:131–142

    Article  Google Scholar 

  • Świderski Z, Miquel J, Neifar L, Mackiewicz JS (2007) Ultrastructural and cytochemical studies on vitellogenesis in the trypanorhynch cestode Parachristianella trygonis Dollfus, 1946 (Eutetrarhynchidae). Acta Parasitol 52:114–126

    Article  Google Scholar 

  • Świderski Z, Mokhtar F (1974) Étude de la vitellogénèse de Bothriocephalus clavibothrium Ariola, 1899 (Cestoda: Pseudophyllidea). Z Parasitenkd 43:135–149

    Article  PubMed  Google Scholar 

  • Świderski Z, Xylander WER (2000) Vitellocytes and vitellogenesis in cestodes in relation to embryonic development, egg production and life cycle. Int J Parasitol 30:805–817

    Article  PubMed  Google Scholar 

  • Thiéry J-P (1967) Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J Microsc 6:987–1018

    Google Scholar 

  • Xylander WER (1987) Ultrastructural studies on the reproductive system of Gyrocotylidea and Amphilinidea (Cestoda). II. Vitellaria, vitellocyte development and vitelloduct of Gyrocotyle urna. Zoomorphology 107:293–297

    Article  Google Scholar 

  • Xylander WER (1988) Ultrastructural studies on the reproductive system of Gyrocotylidea and Amphilinidea (Cestoda). I. Vitellarium, vitellocyte development and vitelloduct in Amphilina foliacea (Rudolphi, 1819). Parasitol Res 74:63–370

    Article  Google Scholar 

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Acknowledgements

We are grateful to Blanka Škoríková, Institute of Parasitology, BC AS CR, České Budějovice, for her help with collecting parasites. Our appreciation is extended to the staff of the Laboratory of Electron Micrscopy, Institute of Parasitology, BC AS CR, České Budějovice, Czech Republic for excellent technical assistance. This study was supported by the Grant Agency of the Slovak Republic VEGA (project no. 2/0047/11), and the Slovak Research and Development Agency (project no. APVV-0653-11). The work was realised within a frame of Centre of Excellence for Parasitology (Code ITMS: 26220120022) based on the support of the Operational Programme ”Research & Development” funded from the European Regional Development Fund (rate 0.1).

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Authors and Affiliations

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

    Magdaléna Bruňanská

  2. Faculty of Biological Sciences, University of South Bohemia, 370 05, České Budějovice, Czech Republic

    Petra Drobníková

  3. Department of Biological Sciences, University at Albany, State University of New York, Albany, NY, 12222, USA

    John S. Mackiewicz

  4. Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 370 05, České Budějovice, Czech Republic

    Jana Nebesářová

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  1. Magdaléna Bruňanská
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  2. Petra Drobníková
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  4. Jana Nebesářová
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Correspondence to Magdaléna Bruňanská.

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Bruňanská, M., Drobníková, P., Mackiewicz, J.S. et al. Cytocomposition of the vitellarium in Khawia sinensis Hsü, 1935 (Cestoda, Caryophyllidea, Lytocestidae): another caryophyllidean species with lamellar bodies and lipids. Parasitol Res 112, 2703–2711 (2013). https://doi.org/10.1007/s00436-013-3477-1

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