Skip to main content
Log in

Morphological framework for attachment and locomotion in several Digenea of the families Microphallidae and Heterophyidae

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

Abstract

Digenea usually use ventral sucker for sustainable attachment within intestine of their definitive vertebrate host. However, if the ventral sucker is absent or poorly developed, the means of attachment are unclear. We investigated attachment and locomotion in such digeneans: three species of the family Microphallidae (Microphallus piriformes, M. pygmaeus, and Levinseniella brachysoma) and two species of the family Heterophyidae (Cryptocotyle concava and C. lingua). Their tegumental spines and musculature were described with use of fluorescent actin staining, confocal microscopy, and scanning electron microscopy. Locomotion of living worms was observed and recorded. Wide serrated tegumental spines probably play the main role in attachment. Their firm contact with the host mucosa may be provided by the action of the ventral concavity—when the entire body or its part acts as a sucker. Dorsoventral muscle bundles act like radial musculature of the sucker generating negative pressure in the ventral concavity. The solid layer of longitudinal muscle fibers on the ventral body surface provides support for the bottom of the ventral concavity. In all microphallids, a U-shaped arrangement of body wall musculature (mostly originating from longitudinal fibers) outlines posterior part of the ventral concavity ridge. In all the studied species, tegumental spines, body wall musculature, and dorsoventral muscle bundles are better developed in the forebody which moves more actively than the hindbody.

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

Access this article

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Notes

  1. The microphallid metacercariae of the “pygmaeus” group have all fully formed marita organs; the growth in the definitive host is minor (Galaktionov 1983).

  2. This characterizes ventrally concaved body (MacKinnon 1982; Boyce et al. 2012); terms describing the regionalization of body surfaces (ventral concavity ridge, slope etc.) are taken from Krupenko and Gonchar (2017).

References

  • Alda P, Bonel N, Hechinger RF, Martorelli SR (2013) Maritrema orensense and Maritrema bonaerense (Digenea: Microphallidae): descriptions, life cycles, and comparative morphometric analyses. J Parasitol 99(2):218–228. https://doi.org/10.1645/GE-3238.1

    Article  PubMed  Google Scholar 

  • Belopolskaya MM (1963) Family Microphallidae Travassos, 1920. In: Skrjabin KI (ed) Trematodes of animals and human, vol 21. Izdatelstvo Akademii Nauk SSSR, Moscow, pp 259–502 (in Russian)

    Google Scholar 

  • Bennett CE (1975) Scanning electron microscopy of Fasciola hepatica L. during growth and maturation in the mouse. J Parasitol 61(5):892–898. https://doi.org/10.2307/3279230

    Article  CAS  PubMed  Google Scholar 

  • Boyce K, Hide G, Craig PS, Harris PD, Reynolds C, Pickles A, Rogan MT (2012) Identification of a new species of digenean Notocotylus malhamensis n. sp. (Digenea: Notocotylidae) from the bank vole (Myodes glareolus) and the field vole (Microtus agrestis). Parasitology 139(12):1630–1639. https://doi.org/10.1017/S0031182012000911

    Article  CAS  PubMed  Google Scholar 

  • Cohen C, Reinhardt B, Castellani L, Norton P, Stirewalt M (1982) Schistosome surface spines are “crystals” of actin. J Cell Biol 95(3):987–988

    Article  CAS  Google Scholar 

  • Collins JJ III, King RS, Cogswell A, Williams DL, Newmark PA (2011) An atlas for Schistosoma mansoni organs and life-cycle stages using cell type-specific markers and confocal microscopy. PLoS Negl Trop Dis 5(3):e1009. https://doi.org/10.1371/journal.pntd.0001009

    Article  PubMed  PubMed Central  Google Scholar 

  • Davies C (1979) The forebody glands and surface features of the metacercariae and adults of Microphallus similis. Int J Parasitol 9(6):553–564. https://doi.org/10.1016/0020-7519(79)90012-2

    Article  Google Scholar 

  • Fried B, Kanev I, Reddy A (2009) Studies on collar spines of echinostomatid trematodes. Parasitol Res 105(3):605–608. https://doi.org/10.1007/s00436-009-1519-5

    Article  PubMed  Google Scholar 

  • Galaktionov KV (1983) Microphallids of the pygmaeus group. I. Description of Microphallus pygmaeus (Levinsen, 1881) nec Odhner, 1905 and of M. piriformes (Odhner, 1905) nom. nov. (Trematoda: Microphallidae). Vestnik Leningradskogo Universiteta Biologiya 15(3):20–30 (in Russian)

    Google Scholar 

  • Køie M (1977) Stereoscan studies of cercariae, metacercariae, and adults of Cryptocotyle lingua (Creplin 1825) Fischoeder 1903 (Trematoda: Heterophyidae). J Parasitol 63(5):835–839. https://doi.org/10.2307/3279888

    Article  PubMed  Google Scholar 

  • Krupenko DY, Dobrovolskij AA (2015) Somatic musculature in trematode hermaphroditic generation. BMC Evol Biol 15(1):189. https://doi.org/10.1186/s12862-015-0468-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krupenko D, Gonchar A (2017) Ventral concavity and musculature arrangement in notocotylid maritae (Digenea: Notocotylidae). Parasitol Int 66(5):660–665. https://doi.org/10.1016/j.parint.2017.06.008

    Article  PubMed  Google Scholar 

  • MacKinnon BM (1982) The structure and possible function of the ventral papillae of Notocotylus triserialis Diesing, 1839. Parasitology 84(2):313–332. https://doi.org/10.1017/S0031182000044875

    Article  Google Scholar 

  • Mair GR, Maule AG, Fried B, Day TA, Halton DW (2003) Organization of the musculature of schistosome cercariae. J Parasitol 89(3):623–625. https://doi.org/10.1645/0022-3395(2003)089[0623:OOTMOS]2.0.CO;2

    Article  CAS  Google Scholar 

  • Niewiadomska K (2002) Family Strigeidae Railliet, 1919. In: Gibson DI et al (eds) Keys to the Trematoda, vol. 1. CAB International and Natural History Museum, London, pp 231–241

    Chapter  Google Scholar 

  • Overstreet RM, Curran SS (2002) Superfamily Bucephaloidea Poche, 1907. In: Gibson DI et al (eds) Keys to the Trematoda, vol. 1. CAB International and Natural History Museum, London, pp 67–110

    Chapter  Google Scholar 

  • Pearson J (2008) Family Heterophyidae Leiper, 1909. In: Bray RA et al (eds) Keys to the Trematoda, vol. 3. CAB International and Natural History Museum, London, pp 113–141

    Chapter  Google Scholar 

  • Pina S, Russell-Pinto F, Rodrigues P (2011) Morphological and molecular study of Microphallus primas (Digenea: Microphallidae) metacercaria, infecting the shore crab Carcinus maenas from northern Portugal. Folia Parasitol 58(1):48–54

    Article  Google Scholar 

  • Rankin JS (1939) Studies on the trematode family Microphallidae Travassos, 1921. I. The genus Levinseniella Stiles and Hassall, 1901, and description of a new genus, Cornucopula. Trans Am Microsc Soc 58(4):431–447. https://doi.org/10.2307/3222784

    Article  Google Scholar 

  • Rees FG (1978) The ultrastructure, development and mode of operation of the ventrogenital complex of Cryptocotyle lingua (Creplin) (Digenea: Heterophyidae). Proc R Soc Lond B Biol Sci 200(1140):245–267. https://doi.org/10.1098/rspb.1978.0019

    Article  Google Scholar 

  • Saville DH, Galaktionov KV, Irwin SWB, Malkova II (1997) Morphological comparison and identification of metacercariae in the ‘pygmaeus’ group of microphallids, parasites of seabirds in western palaearctic regions. J Helminthol 71(2):167–174. https://doi.org/10.1017/S0022149X00015856

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. George Slyusarev and Georgii Kremnev for help with the sampling and to Anna Gonchar and Natalia Lentsman for the revision of the manuscript. This research was carried out using the resources of Educational and Research Station “Belomorskaia” (Marine Biological Station) of Saint Petersburg State University. The confocal microscopy studies were carried out using the equipment of the research resource center “Molecular and Cell Technologies” of Saint Petersburg State University.

Funding

The reported study was funded by Russian Foundation for Basic Research, according to the research project no. 16-34-60156 mol_а_dk, and Saint Petersburg State University project nos. 1.42.1099.2016 and 1.42.739.2017.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Darya Krupenko.

Ethics declarations

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Handling Editor: Julia Walochnik

Electronic supplementary material

Online Resource 1

Locomotion of Cryptocotyle concava marita. Speed *3. (MP4 7486 kb)

Online Resource 2

Locomotion of Microphallus pygmaeus marita. Speed *3. (MP4 5328 kb)

Online Resource 3

Locomotion of Levinseniella brachysoma marita. Speed *3. (MP4 1802 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Krupenko, D., Dobrovolskij, A.A. Morphological framework for attachment and locomotion in several Digenea of the families Microphallidae and Heterophyidae. Parasitol Res 117, 3799–3807 (2018). https://doi.org/10.1007/s00436-018-6085-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-018-6085-2

Keywords

Navigation