Skip to main content
SpringerLink
Log in

The neuromuscular system in continuously swimming cercariae from Belarus. II Echinostomata, Gymnocephala and Amphistomata

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

Abstract

The neuromuscular system in cercariae of Moliniella anceps, Echinostoma revolutum, Cathaemasia hians, Psilochasmus oxyurus, Sphaeridiotrema globulus, Paramphistomum cervi and Diplodiscus subclavatus was studied with immunocytochemical methods and confocal scanning laser microscopy. The patterns of F-actin in the musculature, 5-HT immunoreactive (IR), FMRFamide-IR neuronal elements and α-tubulin-IR sensory receptors were investigated. The general patterns of musculature, 5-HT- and FMRFamide-IR neuronal elements in the 12 species studied here and in paper I are similar to those observed in other cercariae and reflect the morphology of the groups. The musculature of the tail shows variations which are related to the different strategies of host finding. In the Echinostomatoidea and Paramphistomoidea, the striated musculature of the tail is well developed compared to that in the Xiphidiocercariae. Specialized muscle fibres were found in S. globulus, which are able to change the shape of the tail. Nine of the species studied have seven paired 5-HT-IR neurons in the body, and two species have eight. No correlation between the body size and the number of 5-HT-IR neurons was observed. However, the size of the neurons followed the body size. The number of 5-HT-IR neurons in the brain ganglia increased from the primitive to the advanced forms. The number of FMRFamide-IR transverse commissures in the body correlates with the size of the cercariae. Regardless of the differences in the second intermediate host, the distribution of α-tubulin-IR sensory receptors shows a high degree of conformity in all species except in P. cervi, which encysts on plants.

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

  • Albaret JL, Bayssade-Dufour C, Ngendahayo LD, Postal JM, Picot H (1987) Chaetotaxy of the cercaria of Paramphistomum sp., a parasite of cattle in Vendée. Ann Parasitol Hum Comp 62:271–275

    PubMed  CAS  Google Scholar 

  • Belyakova Y (1978) New data on the life cycle of Sphaeridiotrema globulus Rud., 1819 (Trematoda: Psilostomidae). Life cycles, ecology and morphology of helminths of animals of Kazakhstan. Nauka, Alma-Ata, pp 192–201, in Russian

    Google Scholar 

  • Bihovskaya-Pavlovskaya IE, Kulakova AP (1971) Cercariae of Bithyniidae snails (Bithynia tentaculata and B. leachi) from Kuronian bay. Parasitology 5:222–232 (in Russian)

    Google Scholar 

  • Dawes B (1946) The Trematoda, with special reference to British and European forms. Cambridge University Press, Cambridge, p 644

    Google Scholar 

  • Gibson DI (1996) Trematoda. In: Margolis L, Kabata Z (eds) Guide to the parasites of fishes of Canada. Part IV. Can Spec Publ Fish Aquat Sci 124. NRC Press, Ottawa, p 373

    Google Scholar 

  • Ginetsinskaya TA, Dobrovolsky AA (1964) On the fauna of the larvae of trematodes from freshwater molluscs of the Volga delta. P.2. Ehinostomatid cercariae (family Echinostomatidae). Proc Astrakhan Nat Reserv 9:64–104, in Russian

    Google Scholar 

  • Glöer P (2002) Die Süßwassergastropoden Nord- und Mitteleuropas. Bestimmungschlüssel, Lebesweise, Verbreitung. Die Tierwelt Deutschlands 73:1–237

    Google Scholar 

  • Grabda-Kazubska B, Bayssade-Dufour C, Kiseliene V (1990) Chaetotaxy and excretory system of Echinocercaria choanophila U. Szidat, 1936, a larval of Cathaemasia hians (Rud., 1809) (Trematoda, Cathaemasiidae). Acta Parasitol Polon 35:97–105

    Google Scholar 

  • Haas W (1994) Physiological analyses of host-finding behavior in trematode cercariae: adaptations for transmission success. Parasitology 109:15–29

    Article  Google Scholar 

  • Haas W, Körner M, Hutterer E, Wegner M, Haberl B (1995) Finding and recognition of the snail intermediate hosts by 3 species of echinostome cercariae. Parasitology 110:133–142

    Article  PubMed  Google Scholar 

  • Halton DW, Maule AG (2004) Flatworm nerve-muscle: structural and functional analysis. Can J Zool 82:316–333

    Article  Google Scholar 

  • Herrmann KK, Sorensen RE (2011) Differences in natural infections of two mortality-related trematodes in lesser scaup and American coot. J Parasitol 97:555–558

    Article  PubMed  Google Scholar 

  • Kanev I (1994) Life-cycle, delimitation and redescription of Echinostoma revolutum (Froelich, 1802) (Trematoda: Echinostomatidae). Syst Parasitol 28:125–144

    Article  Google Scholar 

  • Keiser J, Utzinger J (2009) Food-borne trematodiases. Clin Microbiol Rev 22:466–483

    Article  PubMed  Google Scholar 

  • Konstadinova A (1999) Cercarial chaetotaxy of Echinostoma miyagawai Ishii, 1932 (Digenea: Echinostomatidae), with a review of the sensory patterns in the ‘revolutum’ group. Syst Parasitol 44:201–209

    Article  Google Scholar 

  • Körner M, Haas W (1998) Chemo-orientation of echinostome cercariae towards their snail hosts: the stimulating structure of amino acids and other attractants. Int J Parasitol 28:517–525

    Article  PubMed  Google Scholar 

  • Mishra N, Tandon V (1986) Nervous system in Olveria indica, a rumen paramphistome (Digenea) of bovines, as revealed by non-specific esterase staining. J Helminthol 60:193–199

    Article  PubMed  CAS  Google Scholar 

  • Richard J, Klein MJ, Stoeckel ME (1989) Neural and glandular localisation of substance P in Echinostoma caproni (Trematoda-Digenea). Parasitol Res 75:641–648

    Article  PubMed  CAS  Google Scholar 

  • Šebelová Š, Stewart M, Mousley A, Fried B, Marks N, Halton D (2004) The musculature and associated innervation of adult and intramolluscan stages of Echinostoma caproni (Trematoda) visualised by confocal microscopy. Parasitol Res 93:196–206

    Article  PubMed  Google Scholar 

  • Szidat L (1936) Uber die Entwicklungsgeschichte und den ersten Zwischenwirt von Paramphistomum cervi Zeder, 1790, aus dem Magen von Wiederkauern. Z Parasitenkd 9:1–19

    Article  Google Scholar 

  • Szidat L (1957) Life cycle of Psilochasmus oxyurus (Cerplin 1825, Luhe 1910) (Trematoda, Psilostomidae) in Argentina. Z Parasitenkd 18:24–35

    Article  PubMed  CAS  Google Scholar 

  • Terenina NB, Tolstenkov OO, Fagerholm HP, Serbina EA, Vodjanizkaya SN, Gustafsson MKS (2006) The spatial relationship between the musculature and the NADPH-diaphorase activity, 5-HT and FMRFamide immunoreactivities in redia, cercaria and adult Echinoparyphium aconiatum (Digenea). Tissue Cell 38:151–157

    Article  PubMed  CAS  Google Scholar 

  • Tolstenkov OO, Terenina NB, Gustafsson MKS, Serbina EA, Kreshchenko ND, Maklakova LM, Jashina AV (2008) Immunochemical study of cercariae trematodes from different taxonomic groups—a preliminary study. Acta Biol Hung 59:S221–S225

    Article  Google Scholar 

  • Tolstenkov OO, Prokofiev VV, Terenina NB, Gustafsson MKS (2011) The neuro-muscular system in cercaria with different patterns of locomotion. Parasitol Res 108:1219–1227

    Article  PubMed  Google Scholar 

  • Tolstenkov OO, Akimova LN, Chrisanfova GG, Terenina NB, Gustafsson MKS (2012a) The neuro-muscular system in fresh-water furcocercaria from Belarus. I Schistosomatidae. Parasitol Res 110:185–193

    Article  PubMed  Google Scholar 

  • Tolstenkov OO, Akimova LN, Chrisanfova GG, Terenina NB, Gustafsson MKS (2012b) The neuromuscular system in freshwater furcocercaria from Belarus. II Diplostomidae, Strigeidae and Cyathocotylidae. Parasitol Res 110:583–592

    Article  PubMed  Google Scholar 

  • Tolstenkov OO, Akimova LN, Terenina NB, Gustafsson MKS (2012c) The neuromuscular system in continuously swimming cercariae from Belarus. I Xiphidiocercariae. Parasitol Res. doi:10.1007/s00436-012-3044-1

  • Zdárská Z (1992) Transmission electron microscopy of sensory receptors of Echinostoma revolutum (Froelich 1802) cercaria (Digenea: Echinostomatidae). Parasitol Res 78:598–606

    Article  PubMed  Google Scholar 

  • Zdárská Z, Nasincová V, Valkounová J (1989) Ultrastructure of the tail of Echinostoma revolutum cercaria. Folia Parasitol 36(3):239–242

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the staff and students of Biological Station of Belarus State University for the friendly atmosphere and help. The study was supported by RFBR grants 12-04-01051-а, 12-04-01086-а, grant of the President of Russian Federation МК-1093.2011.4, The Research Institute of the Foundation of the Åbo Akademi University and the Academy of Finland. The authors want to thank Mr. Esa Nummelin for technical assistance.

Author information

Authors and Affiliations

  1. Centre of Parasitology of A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky prospect, 33, Moscow, 119071, Russia

    Oleg O. Tolstenkov & Nadezhda B. Terenina

  2. Laboratory of Parasitology, State Scientific and Production Amalgamation, “The Scientific and Practical Center for Bioresources”, 27 Akademicheskaya Street, Minsk, 220072, Republic of Belarus

    Ludmila N. Akimova

  3. Department of Biosciences, Åbo Akademi University, 20520, Åbo, Finland

    Margaretha K. S. Gustafsson

Authors
  1. Oleg O. Tolstenkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ludmila N. Akimova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nadezhda B. Terenina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Margaretha K. S. Gustafsson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Oleg O. Tolstenkov.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tolstenkov, O.O., Akimova, L.N., Terenina, N.B. et al. The neuromuscular system in continuously swimming cercariae from Belarus. II Echinostomata, Gymnocephala and Amphistomata. Parasitol Res 111, 2301–2309 (2012). https://doi.org/10.1007/s00436-012-3084-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-012-3084-6

Keywords

Search

Navigation