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The neuromuscular system in freshwater furcocercaria from Belarus. II Diplostomidae, Strigeidae, and Cyathocotylidae

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Abstract

The neuromuscular system (NMS) in cercariae of Diplostomum pseudospathaceum, Cotylurus szidati, Australapatemon burti, Holostephanus volgensis, and Paracoenogonimus ovatus was studied with immunocytochemical methods and confocal scanning laser microscopy. The patterns of F-actin in the musculature, 5-HT immunoreactive (−IR), FMRF-amide-IR neuronal elements, and α-tubulin-IR in sensory receptors were investigated. The NMS in the five species studied were compared with each other and with three species of Schistosomatidae studied earlier (Bilharziella polonica, Trichobilharzia szidati, and Trichobilharzia franki). No major structural differences in the musculature, the 5-HT-IR or FMRF-IR neuronal elements were noticed between the cercariae. The minor variations observed in the musculature were related to the size and organization of the muscle fibers. The checked pattern formed by the transverse muscle fibers in the tail stems of D. pseudospathaceum, C. szidati, A. burti, H. volgensis, and P. ovatus was not observed in B. polonica, T. szidati, and T. franki. A trend in the differentiation of the longitudinal muscle fibers in the furca from evenly distributed fibers in H. volgensis and P. ovatus to many bundles in D. pseudospathaceum and two well-organized lateral bundles in C. szidati, A. burti, and Trichobilharzia spp. was observed. The transverse muscle fibers in the furca follow the same trend. The number of 5-HT-IR neurons in the cercarial bodies varied between 10 and 16. In cercariae of H. volgensis and P. ovatus, the central nervous system (CNS) was less centralized compared to the CNS in the other species studied, with only two 5-HT-IR marker neurons in each brain ganglion and the other neurons distributed evenly along the main cords. In the tails of H. volgensis and P. ovatus, many transverse 5-HT-IR comissures were found. In the tails of higher strigeidid cercariae, only a few crosslinks were observed. The number and distribution of sensory receptors on the bodies and tails of the cercarial species differed from each other. A trend in the differentiation of the sensory receptors in the tails was discerned. A process of grouping and decrease in number of ciliated receptors in the stem and in the furca from H. volgensis and P. ovatus to Schistosomatid cercariae took place.

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References

  • Bell AS, Gibson DI, Sommerville C (1997) Chaetotaxy and armature of Ichthyocotylurus erraticus (Rudolphi, 1809) and I. variegatus (Creplin, 1825) cercariae (Digenea, Strigeidae). Parasitol Res 83:70–76

    Article  PubMed  CAS  Google Scholar 

  • Combes C (1980) Atlas Mondial des Cercaires. Mem Mus Natl Hist Nat Ser A Zool 115:5–235

    Google Scholar 

  • Czubaj A, Niewiadomska K (1996) Ultrastructure of sensory endings in Diplostomum pseudospathaceum Niewiadomska, 1984 cercariae (Digenea, Diplostomidae). Int J Parasitol 26:1217–1225

    Article  PubMed  CAS  Google Scholar 

  • Faltýnková A, Našincová V, Kablasková L (2007a) Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gastropoda: Pulmonata) in Central Europe: a survey of species and key to their identification. Parasite 14:39–51

    PubMed  Google Scholar 

  • Faltýnková A, Niewiadomska K, Santos MJ, Valtonen ET (2007b) Furcocercous cercariae (Trematoda) from freshwater snails in Central Finland. Acta Parasitol 52:310–317

    Article  Google Scholar 

  • Galaktionov KV, Dobrovolskij AA (2003) Biology and evolution of trematodes. An essay on the biology, morphology, life cycles, transmission, and evolution of digenetic trematodes. Boston, Dordrecht, London, Kluwer Academic Publ. 620p

  • Ginetsinskaya TA, Dobrovolsky AA (1963) A new method for detecting sensilla of larval trematodes and the significance of these structures for systematics. Dok Acad Sci USSR 151:460–463 (in Russian)

    Google Scholar 

  • Ginetsinskaya TA, Kosheva AF (1959) On the life cycle and taxonomy of Paracoenogonimus ovatus Katsurada (Trematoda) and about the identity of metacercariae of that species with Neodiplostomum hughesi Markewitsh. Vestnik Leningrad Univ 9:68–75 (in Russian)

    Google Scholar 

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

    Google Scholar 

  • Halton DW, Gustafsson MKS (1996) Functional morphology of the platyhelminth nervous system. Parasitology 113:S47–S72

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Niewiadomska К (1986) Verification of the life-cycle of Diplostomum spathaceum (Rudolphi, 1819) and D. pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomatidae). Syst Parasitol 8:23–31

  • Niewiadomska K, Moczoń T (1982) The nervous system of Diplostomum pseudospathaceum Niewiadomska, (Digenea, Diplostomatidae). Parasitol Res 68:295–304

    Google Scholar 

  • Niewiadomska K, Czubaj A, Moczoń T (1996) Cholinergic and aminergic nervous systems in developing cercariae and metacercariae of Diplostomum pseudospathaceum Niewiadomska, 1984 (Digenea). Int J Parasitol 26:161–168

    Article  PubMed  CAS  Google Scholar 

  • Reuter M, Gustafsson MKS (1995) The flatworm nervous system: pattern and phylogeny. In: Breidbach O, Kutsch W (eds) The nervous system of invertebrates: an evolutionary and comparative approach. Birkhäuser Verlag, Basel, pp 25–59

    Chapter  Google Scholar 

  • Reuter M, Mäntylä K, Gustafsson MKS (1998) Organization of the orthogon—main and minor nerve cords. Hydrobiologia 383:175–182

    Article  Google Scholar 

  • Richard J (1971) La chetotaxie des cercaires valeur systematique et phyletique. Mem Mus Natl Hist Nat Ser A Zool 67:1–179

    Google Scholar 

  • Santos MJ, Karvonen A, Pedro JC, Faltýnková A, Seppälä O, Valtonen ET (2007) Qualitative and quantitative behavioral traits in a community of furcocercaiae trematodes: tools for species separation? J Parasitol 93:1319–1323

    Article  PubMed  CAS  Google Scholar 

  • Solis-Soto JM, De Jong BM (1995) An immunocytochemistry study comparing the occurrence of neuroactive substances in the nervous system of cercariae and metacercariae of the eye fluke Diplostomum spathaceum. Parasitol Res 81:553–559

    Article  PubMed  CAS  Google Scholar 

  • Terenina NB, Gustafsson MKS (2002) Nitric oxide and its target cells in cercaria of Diplostomum chromatophorum: a histochemical and immunocytochemical study. Parasitol Res 89:199–206

    PubMed  Google Scholar 

  • Terenina NB, Tolstenkov OO, Fagerholm H-P, Serbina EA, Vodjanitskaja 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. Tissue Cell 38:151–157

    Article  PubMed  CAS  Google Scholar 

  • Tolstenkov OO, Terenina NB, Serbina EA, Gustafsson MKS (2010) The spatial relationship between the musculature and the 5-HT and FMRFamide immunoreactivities in cercaria, metacercaria and adult Opisthorchis felineus (Digenea). Acta Parasitol 55:123–132

    Article  Google Scholar 

  • Tolstenkov OO, Prokofiev VV, Terenina NB, Gustafsson MKS (2011a) 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 (2011b) The neuro-muscular system in fresh-water furcocercaria from Belarus. I Schistosomatidae. Parasitol Res (in press)

  • Vojtkova L (1966) Zur kenntnis des entwicklungszyklus von Holostephanus volgensis (Sudarikov, 1962) n. comb. (Trematoda: Digenea: Cyathocotylidae). Acta Ceskoslov Spolec Zool 30:275–286

    Google Scholar 

  • Zazornova OP (1991) A new species of trematodes, Cotylurus szidati n. sp. (family Strigeidae), and comments on the taxonomy of the genus Cotylurus. Morphology, taxonomy and ecology of helminthes of humans and animals. Proc Helminthol Lab RAS 38:32–43, In Russian

    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 grant 09-04-00243-a, grant of the President of Russian Federation MК-1093.2011.4, The Research Institute of the Foundation of the Åbo Akademi University, the Rector of Åbo Akademi University and the Academy of Finland. The authors want to thank Mr. Esa Nummelin for the technical assistance.

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Correspondence to Oleg O. Tolstenkov.

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Tolstenkov, O.O., Akimova, L.N., Terenina, N.B. et al. The neuromuscular system in freshwater furcocercaria from Belarus. II Diplostomidae, Strigeidae, and Cyathocotylidae. Parasitol Res 110, 583–592 (2012). https://doi.org/10.1007/s00436-011-2526-x

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