Abstract
The neuro-muscular system (NMS) in cercariae of the family Schistosomatidae from Belarus was studied with immunocytochemical methods and confocal scanning laser microscopy. The specimens of Bilharziella polonica were compared with Trichobilharzia szidati and Trichobilharzia franki. The patterns of F-actin in the musculature, 5-HT-immunoreactive (IR), FMRFamide-IR neuronal elements and α-tubulin-IR in sensory receptors and nerves were investigated. No indications of structural differences in the musculature, the 5-HT-IR, FMRF-IR neuronal elements and the general distribution of sensory receptors were noticed between cercariae of Trichobilharzia spp. The number of 5-HT-IR neurons in the cercarial bodies is 16. In cercaria B. polonica, the tail musculature is weaker than in Trichobilharzia spp. A detailed schematic picture of the NMS in the tail of Trichobilharzia spp. cercaria is given. The function of NMS elements in the tail is discussed.
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Bogéa T (2004) Functional and phylogenetic components in cercarial nervous systems. Folia Parasitol 51:311–319
Bogéa T, Caira JN (2001) Ultrastructure and chaetotaxy of sensory receptors in the cercariae of a species of Crepidostomum Braun, 1900 and Bunodera Railliet, 1896 (Digenea: Allocreadiidae). J Parasitol 87:273–286
Brachs S, Haas W (2008) Swimming behaviour of Schistosoma mansoni cercariae: responses to irradiance changes and skin attractants. Parasitol Res 102:685–690
Bulantova J, Chanova M, Houzvickova L, Horak P (2011) Trichobilharzia regenti (Digenea: Schistosomatidae): changes of body wall musculature during the development from miracidium to adult worm. Micron 42:47–54
Cassone J, Bayssade-Dufour C, Albaret JL, Jourdane J (1978) Chaetotaxic variations of the cercaria Schistosoma mansoni from a human strain during successive transmissions through mice. Ann Parasitol Hum Comp 53:387–391
Cebrià F (2008) Organization of the nervous system in the model planarian Schmidtea mediterramea: an immunocytochemical study. Neurosci Res 61:375–384
Coons AH, Leduc EH, Connolly JM (1955) Studies of antibody production. I. A method for the histochemical demonstration of specific antibody and its application to a study of the hyperimmune rabbit. J Exp Med 102:49–60
Cousin CE, Dorsey CH (1991) Nervous system of Schistosoma mansoni cercaria: organization and fine structure. Parasitol Res 77:132–141
Dvorak J, Vanacova S, Hampl V, Flegr J, Horak P (2002) Comparison of European Trichobilharzia species based on ITS1 and ITS2 sequences. Parasitology 124:307–313
Galaktionov KV, Dobrovolskij AA (2003) Biology and evolution of trematodes. An essay on the biology, morphology, life cycles, transmission, and evolution of digenetic trematodes. Kluwer Academic Publ, London, p 620
Gustafsson MKS, Halton DW, Kreshchenko ND, Movsessian SO, Raikova OI, Reuter M, Terenina NB (2002) Neuropeptides in flatworms. Peptides 23:2053–2061
Haas W (1992) Physiological analysis of cercarial behavior. J Parasitol 78:243–255
Haas W (1994) Physiological analyses of host-finding behavior in trematode cercariae: adaptations for transmission success. Parasitology 109:15–29
Haas W, Haberlein S (2009) Penetration of cercariae into the living human skin: Schistosoma mansoni vs. Trichobilharzia szidati. Parasitol Res 105:1061–1066
Halton DW, Gustafsson MKS (1996) Functional morphology of the platyhelminth nervous system. Parasitology 113:S47–S72
Halton DW, Maule AG (2004) Flatworm nerve-muscle: structural and functional analysis. Can J Zool 82:316–333
Horák P, Mikes L, Rudolfová J, Kolárová L (2008) Penetration of Trichobilharzia cercariae into mammals: dangerous or negligible event? Parasite 15:299–303
Jouet D, Skirnisson K, Kolarova L, Ferte H (2010) Molecular diversity of Trichobilharzia franki in two intermediate hosts (Radix auricularia and Radix peregra): a complex of species. Inf Genet Evol 10:1218–1227
Khalifa R (1972) Studies on Schistosomatidae Looss, 1899 (Trematoda) of aquatic birds of Poland. I. On the life cycle of Bilharziella polonica Kowalewski, 1895, with a discussion of the subfamily Bilharziellinae Price, 1929. Acta Parasitologica 20:343–365
Kock S, Böckeler W (1998) Observations on cercarial chaetotaxy as a means for the identification of European species of Trichobilharzia Skrjabin & Zakharow, 1920 (Digenea: Schistosomatidae). Syst Parasitol 43:159–166
Korsunenko AV, Chrisanfova GG, Ryskov AP, Movsessian SO, Vasilyev VA, Semyenova SK (2010) Detection of European Trichobilharzia schistosomes (T. franki, T. szidati, and T. regenti) based on novel genome sequences. J Parasitol 96:802–806
Nuttman CJ (1974) The fine structure and organization of the tail musculature of the cercaria of Schistosoma mansoni. Parasitology 68:147–154
Orido Y (1989) Histochemical evidence of the catecholamine-associated nervous system in certain schistosome cercariae. Parasitol Res 76:146–149
Podhorsky M, Huzova Z, Libor Mikeš L, Horak P (2009) Cercarial dimensions and surface structures as a tool for species determination of Trichobilharzia spp. Acta Parasitologica 54:28–36
Reger JF (1976) Studies on the fine structure of cercarial tail muscle of Schistosoma sp. (Trematoda). J Ultrastruct Res 57:77–86
Rudolfova J, Littlewood DT, Sitko J, Horák P (2007) Bird schistosomes of wildfowl in the Czech Republic and Poland. Folia Parasitol 54:88–93
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
Skuce PJ, Johnston CF, Fairweather I, Halton DW, Shaw C, Buchanan K (1990) Immunoreactivity to pancreatic polypeptide family in the nervous system of the adult blood fluke Schistosoma mansoni. Cell Tissue Res 261:573–581
Solis-Soto JM, De Jong Brink M (1994) Immunocytochemical study on biologically active neurosubstances in daughter sporocysts and cercariae of Trichobilharzia ocellata and Schistosoma mansoni. Parasitology 108:301–311
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
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 Opistorchis felineus (Digenea). Acta Parasitologica 55:123–132
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
Wahlberg MH (1998) The distribution of F-actin during the development of Diphyllobothrium dendriticum. Cell Tissue Res 291:561–570
Acknowledgements
The authors thank the staff and the students of the Biological Station of Belarus State University for the friendly atmosphere and help. The study was supported by RFBR grants 09-04-01611a and 09-04-00243-a, grant SSch-2107.2008.4, Molecular and cell biology program RAS, FCP SC P-1043, 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 and Mr. Jari Korhonen for the technical assistance and the reviewer for fruitful criticism of the manuscript.
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Tolstenkov, O.O., Akimova, L.N., Chrisanfova, G.G. et al. The neuro-muscular system in fresh-water furcocercaria from Belarus. I Schistosomatidae. Parasitol Res 110, 185–193 (2012). https://doi.org/10.1007/s00436-011-2468-3
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DOI: https://doi.org/10.1007/s00436-011-2468-3