Skip to main content
SpringerLink
Log in

Ultrastructural study of the egg wall surrounding the developing miracidia of the digenean Prosotocus confusus (Looss, 1894) (Plagiorchiida: Pleurogenidae), with the description of a unique cocoon-like envelope

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

Abstract

Helminth eggs play a critical role in movement of the parasite from definitive to intermediate host. Eggs of the pleurogenid digenean trematode Prosotocus confusus (Looss, 1894), a parasite of naturally infected frogs Pelophylax lessonae (Amphibia: Ranidae) in Europe, are described here for the first time. Particular emphasis is placed on the ultrastructure on the egg wall and on the detailed description of a unique cocoon-like envelope. Each embryonating egg is composed of an early embryo surrounded by a four-layered egg wall: (1) an outer, anucleate layer external to the eggshell, which forms a thick cocoon; (2) the operculate eggshell; (3) not fully formed, a differentiating outer embryonic envelope containing large nuclei of macromeres; and (4) situated below, an undifferentiated layer of the future inner embryonic envelope containing mesomere nuclei. Layers enveloping the egg apparently play an important role in the protection, metabolism, and storage of nutritive reserves for the developing miracidium. The outer anucleate layer, or cocoon, is situated externally to the eggshell and composed of an electron-lucent substance with numerous electron-dense islands attached to its peripheral membrane. A cocoon envelope such as this has never been seen in previous TEM studies of the eggs of parasitic platyhelminths, with the exception of another pleurogenid Brandesia turgida. The origin, formation, functional ultrastructure, and chemical composition of this peculiar layer remain enigmatic, although its function appears to be protective. The thick, electron-dense eggshell resembles that of other trematodes, exhibiting a characteristic fissure zone around the operculum. Numerous lysosome-like structures observed in some eggs may be involved in the autolysis of both the embryonic envelopes (particularly the early degeneration of macromere nuclei of the outer envelope, characteristic for this species) and in the disintegration of several early micromeres. The inner envelope, which forms later from mesomeres, persists longer during embryogenesis.

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.

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

Similar content being viewed by others

References

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

    Google Scholar 

  • Conn DB (1985) Fine structure of the embryonic envelopes of Oochoristica anolis (Cestoda: Linstowiidae). Z Parasitenkd 71:639–648. doi:10.1007/BF00925597

    Article  Google Scholar 

  • Conn DB (1988) Development of the embryonic envelopes of Mesocestoides lineatus (Cestoda: Cyclophyllidea). Int J Invert Reprod Dev 14:119–130. doi:10.1080/01688170.1988.10510372

    Article  Google Scholar 

  • Conn DB, Etges FJ (1983) Inhibition of egg production in an anomalous Plagitura salamandra Holl, 1928 (Trematoda: Plagiorchiidae). J Parasitol 69:784–786

    Article  Google Scholar 

  • Conn DB, Etges FJ (1984) Fine structure and histochemistry of the parenchyma and uterine egg capsules of Oochoristica anolis (Cestoda: Linstowiidae). Z Parasitenkd 70:769–779. doi:10.1007/BF00927130

    Article  CAS  Google Scholar 

  • Conn DB, Świderski Z (2008) A standardised terminology of the embryonic envelopes and associated developmental stages of tapeworms (Platyhelminthes: Cestoda). Folia Parasitol 55:42–52. doi:10.14411/fp.2008.006

  • Conn DB, Świderski Z, Miquel J, Torres J (2014) Unique cocoon-like envelope in the intrauterine eggs of the pleurogenid digenean Prosotocus confusus. Abstracts 13th Int Congr Parasitol (ICOPA-13), Mexico City, Mexico

  • Dubinina MN (1958) Ekological studies on parasitofauna of Rana ridibunda (Pall.) of Volga delta. Parazitol Sb 12:250–300

    Google Scholar 

  • Eklu-Natey DT (1986) Contribution à l’étude ultrastructurale de la gamétogenèse, du développement embryonnaire et du miracidium chez Schistosoma haematobium. PhD Thesis, University of Geneva

  • Eklu-Natey DT, Wüest J, Huggel H (1981) Morphologie du miracidium de Schistosoma japonicum Katsurada, 1904, étudiée au microscope électronique à balayage. Arch Sci Genève 34:401–408

    Google Scholar 

  • Eklu-Natey DT, Świderski Z, Huggel H, Striebel H (1982a) Schistosoma haematobium: egg-shell formation. Proc 11th Int Congr Electr Microsc 2:605–606

    Google Scholar 

  • Eklu-Natey DT, Świderski Z, Moczon T, Striebel HP, Huggel H (1982b) Ultrastructure and histochemistry of egg-shell formation in Schistosoma haematobium. Mol Biochem Parasitol Suppl:708

  • Eklu-Natey DT, Wüest J, Świderski Z, Striebel HP, Huggel H (1985) Comparative scanning electron microscope (SEM) study of miracidia of four human schistome species. Int J Parasitol 15:33–42. doi:10.1016/0020-7519(85)90098-0

    Article  CAS  PubMed  Google Scholar 

  • Ginetsinskaya TA (1968) Trematodes their life cycles biology and evolution. Nauka Leningrad. Translated from Russian to English in 1988 by Amerind, Publ. Co. Pvt. Ltd., New Delhi (in Russian)

  • Higgins-Opitz SB, Evers P (1983) Observations by scanning electron microscopy of miracidial hatching from Schistosoma mansoni ova. J Parasitol 69:432–433

    Article  CAS  PubMed  Google Scholar 

  • Jones MK, Bong SH, Green KM, Holmes P, Duke M, Lukas A, McManus DP (2008) Correlative and dynamic imaging of the hatching biology of Schistosoma japonicum from eggs prepared by high pressure freezing. PLoS Negl Trop Dis 2:e334

    Article  PubMed Central  PubMed  Google Scholar 

  • Khampoosa P, Jones MK, Lovas EM, Srisawangwong T, Laha T, Piratae S, Thammasiri C, Suwannatrai A, Sripanidkulchai B, Eursitthichai V, Tesana S (2011) Light and electron microscopy observations of embryogenesis and egg development in the human liver fluke, Opisthorchis viverrini (Platyhelminthes Digenea). Parasitol Res 110:799–808. doi:10.1007/s00436-011-2557-3

    Article  PubMed  Google Scholar 

  • Køie M, Christensen NØ, Nansen P (1976) Stereoscan studies of eggs, free-swimming and penetrating miracidia and early sporocysts of Fasciola hepatica. Z Parasitenkd 51:79–90. doi:10.1007/BF00380530

    Article  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 and The Natural History Museum, London, pp 563–575

    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. doi:10.2478/s11686-011-0011-4

    Article  Google Scholar 

  • Pan SC (1985) The fine structure of the miracidium of Schistosoma mansoni. J Invert Pathol 36:307–372

    Article  Google Scholar 

  • Pavlyuk RS (1972) The biology of the metacercariae of the trematode Prosotocus confusus Looss, 1894. Poblemy Parazit 2:100–101

    Google Scholar 

  • Pearson JC (1972) A phylogeny of life cycle patterns of the Digenea. Adv Parasitol 10:153–189

    Article  CAS  PubMed  Google Scholar 

  • Sey O (1992) Helminth parasites of amphibians of the Lake Balaton area. Misc Zool Hung 7:5–8

    Google Scholar 

  • Shevchenko NN, Vergun GI (1961) Life-cycle of Prosotocus confusus Looss, 1894 Looss, 1899 of amphibians. Helminthologia 3:294–298

    Google Scholar 

  • Shimalov VV (2002) The helminth fauna of amphibians of open channels in meliorated regions of the Belorussian Polesie. Parazitologiya 36:304–309

    CAS  Google Scholar 

  • Sinitzin DF (1905) Materials on natural history of trematodes. Digeneans of fishes and frogs of. Warsaw suburbs, Warsaw

    Google Scholar 

  • Smyth JD, Halton DW (1983) The physiology of Trematodes, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Świderski Z (1984) Embryonic development of Schistosoma mansoni. South Afr J Sci 80:434

    Google Scholar 

  • Świderski Z (1985) Embryonic development of Schistosoma mansoni and S. haematobium: egg envelope formation. South Afr J Sci 81:43–44

    Google Scholar 

  • Świderski Z (1994a) Origin, differentiation and ultrastructure of egg envelopes surrounding the miracidia of Schistosoma mansoni. Acta Parasitol 39:64–72

    Google Scholar 

  • Świderski Z (1994b) Origin, differentiation and ultrastructure of egg envelopes surrounding the coracidia of Bothriocephalus clavibothrium. Acta Parasitol 39:73–81

    Google Scholar 

  • Świderski Z (1994c) Homology and analogy of egg envelopes surrounding the coracidia of Bothriocephalus clavibothrium and miracidia of Schistosoma mansoni. Acta Parasitol 39:123–130

    Google Scholar 

  • Świderski Z (1986) Schistosoma mattheei: egg-shell degeneration in the liver of Praomys (Mastomys) natalensis during chronic infection. In: Imura T, Maruse S, Suzuki T (eds), Proc 11th Int Congr Electron Microsc, pp 3567–3568

  • Świderski Z (1988) Ultrastructure of schistosome eggs. Proc 4th Asia Pacific Conf Workshop Electr Microsc:555–556

  • Świderski Z (2008) Biodiversity of parasite eggs: their importance for disease dissemination and diagnostics. In: Commemorative Volume of Proceedings Published on the Occasion of the International Conference Dedicated to the 130th Anniversary of the Birthday of Academician K.I. Skrjabin, pp 453–459

  • Świderski Z, Moser P, Eklu-Natey DT (1980) The fine structure of protective envelopes of the egg of Schistosoma mansoni. In: Brederoo P, De Priester W (eds), Electron Microscopy, vol. 2. Leiden, pp 218–219

  • Świderski Z, Conn DB (2014) Comparative ultrastructure of the intrauterine eggs of four European trematodes. In: Oros M, Vasilková Z (eds) V4 Parasitological Meeting: Parasites in the Heart of Europe. Slovak Society for Parasitology at SAS, Kosice, pp 27–28

    Google Scholar 

  • Świderski Z, Bakhoum AJS, Młocicki D, Miquel J (2010) Ultrastructural studies on egg envelopes surrounding the miracidia of Mediogonimus jourdanei Mas-Coma et Rocamora 1978 (Digenea, Microphalloidea, Prosthogonimidae). Acta Parasitol 55:245–253. doi:10.2478/s11686-010-0031-5

    Article  Google Scholar 

  • Świderski Z, Miquel J, Montoliu I, Feliu C, Gibson DI (2013a) Ultrastructure of the intrauterine eggs of the microphallid trematode Maritrema feliui: evidence of early embryonic development. Parasitol Res 112:3325–3333. doi:10.1007/s00436-013-3512-2

    Article  PubMed  Google Scholar 

  • Świderski Z, Poddubnaya LG, Zhokhov AE, Miquel J, Gibson DI (2013b) 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. doi:10.1016/j.jcz.2013.09.001

    Article  Google Scholar 

  • Świderski Z, Poddubnaya LG, Zhokhov AE, Miquel J, Conn DB (2014) Ultrastructural evidence for completion of the entire miracidial maturation in intrauterine eggs of the digenean Brandesia turgida (Brandes, 1888) (Plagiorchiida: Pleurogenidae). Parasitol Res 113:1103–1111. doi:10.1007/s00436-013-3747-y

    Article  PubMed Central  PubMed  Google Scholar 

  • Tkach VV, Littlewood DTJ, Olson PD, Kinsella JM, Świderski Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst Parasitol 56:1–15. doi:10.1023/A:1025546001611

    Article  PubMed  Google Scholar 

  • Wiśniewski W (1958) Characterization of the parasitic fauna of an eutrophic lake. Acta Parasitol Pol 4:1–64

    Google Scholar 

  • Yamaguti S (1975) A synoptical review of the life histories of the digenetic trematodes of vertebrates. Keigaku Publishing, Tokyo

Download references

Acknowledgments

The authors are grateful to Almudena García from the “Centres Científics i Tecnològics” of the University of Barcelona (CCiTUB) for her assistance in the preparation of samples.

Author information

Authors and Affiliations

  1. W. Stefański Institute of Parasitology, Polish Academy of Sciences, 51/55 Twarda Street, 00-818, Warsaw, Poland

    Zdzisław Świderski

  2. Laboratori de Parasitologia, Departament de Microbiologia i Parasitologia Sanitàries, Facultat de Farmàcia, Universitat de Barcelona, Av. Joan XXIII, sn, 08028, Barcelona, Spain

    Jordi Miquel & Jordi Torres

  3. Institut de Recerca de la Biodiversitat, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal, 645, 08028, Barcelona, Spain

    Jordi Miquel & Jordi Torres

  4. Department of Biology and One Health Center, Berry College, Mount Berry, GA, 30149, USA

    David Bruce Conn

  5. Department of Invertebrate Zoology, Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA, 02138, USA

    David Bruce Conn

Authors
  1. Zdzisław Świderski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jordi Miquel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jordi Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David Bruce Conn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zdzisław Świderski.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Świderski, Z., Miquel, J., Torres, J. et al. Ultrastructural study of the egg wall surrounding the developing miracidia of the digenean Prosotocus confusus (Looss, 1894) (Plagiorchiida: Pleurogenidae), with the description of a unique cocoon-like envelope. Parasitol Res 114, 185–191 (2015). https://doi.org/10.1007/s00436-014-4177-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-4177-1

Keywords

Search

Navigation