Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-25T08:06:58.090Z Has data issue: false hasContentIssue false
  • English
  • Français

Muscle architecture during the course of development of Diplostomum pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomidae) from cercariae to metacercariae

Published online by Cambridge University Press:  18 May 2015

A. Petrov  and
I. Podvyaznaya
A. Petrov*
Affiliation:
Zoological Institute, Russian Academy of Sciences, Universitetskaya Emb. 1, 199034Saint Petersburg, Russia
I. Podvyaznaya
Affiliation:
Zoological Institute, Russian Academy of Sciences, Universitetskaya Emb. 1, 199034Saint Petersburg, Russia
*
*E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Recent confocal microscopy studies have greatly expanded our knowledge of muscle systems in cercariae and adult digeneans, but the gross anatomy and development of metacercarial musculature remain relatively little known. To further our understanding of metacercarial development, this study used phalloidin staining and confocal microscopy to examine changes in muscle architecture over the course of development from cercariae to infective metacercariae in Diplostomum pseudospathaceum Niewiadomska, 1984. The paper describes muscle development in the body wall, anterior organ (oral sucker), acetabulum, pharynx and midgut and in the musculo-glandular organs that first appear in metacercariae (lappets and holdfast). The muscle architecture of the cercarial tail is also described. The results of the study support previously reported observations that diplostomid musculature undergoes substantial transformation during metacercarial development. The most profound changes, involving extensive remodelling and replacement of cercarial muscles, were seen in the body-wall musculature and in the anterior organ as it developed into the oral sucker. Muscle systems of other cercarial organs showed more gradual changes. The adaptive importance of developmental changes in musculature is discussed.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 3 , May 2016 , pp. 321 - 336
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bahia, D., Avelar, L.G.A., Vigorosi, F., Cioli, D., Oliveira, G.C. & Mortara, R.A. (2006) The distribution of motor proteins in the muscles and flame cells of the Schistosoma mansoni miracidium and primary sporocyst. Parasitology 133, 321–329.CrossRefGoogle ScholarPubMed
Bell, A.S., Gibson, D.I. & Sommerville, C. (1996) Chaetotaxy and armature of Ichthyocotylurus erraticus (Rudolphi, 1809) and I. variegatus (Creplin, 1825) cercariae (Digenea, Strigeidae). Parasitology Research 83, 70–76.Google Scholar
Bulantová, J., Chanová, M., Houžvičková, L. & Horák, P. (2011) Trichobilharzia regenti (Digenea: Schistosomatidae): changes of body wall musculature during the development from miracidium to adult worm. Micron 42, 47–54.CrossRefGoogle ScholarPubMed
Czubaj, A. & Niewiadomska, K. (1997) The muscular system of the cercaria of Diplostomum pseudospathaceum Niew., 1984 (Digenea): a phalloidin–rhodamine fluorescence and TEM study. Acta Parasitologica 42, 199–218.Google Scholar
Erasmus, D.A. (1958) Studies on the morphology, biology and development of a strigeid cercaria (Cercaria ×  Baylis 1930). Parasitology 48, 312–335.Google Scholar
Erasmus, D.A. (1959) The migration of Cercaria ×  Baylis (Strigeida) within the fish intermediate host. Parasitology 49, 173–190.Google Scholar
Erasmus, D.A. (1969) Studies on the host–parasite interface of strigeoid trematodes. VI. Ultrastructural observations on the lappets of Diplostomum phoxini Faust, 1918. Zeitschrift für Parasitenkunde 32, 48–58.Google Scholar
Erasmus, D.A. (1970) The host–parasite interface of strigeoid trematodes. VII. Ultrastructural observations on the adhesive organ of Diplostomum phoxini Faust, 1918. Zeitschrift für Parasitenkunde 33, 211–224.Google ScholarPubMed
Galaktionov, K.V. & Dobrovolskij, A.A. (2003) The biology and evolution of trematodes. 592 pp. Dordrecht, Kluwer.Google Scholar
Ginetsinskaya, T. (1988) Trematodes, their life cycles, biology and evolution. 559 pp. New Delhi, Amerind.Google Scholar
Höglund, J. (1991) Ultrastructural observations and radiometric assay on cercarial penetration and migration of the digenean Diplostomum spathaceum in the rainbow trout Oncorhynchus mykiss . Parasitology Research 77, 283–289.Google Scholar
Krupenko, D.Y. (2010) Muscle system of Microphallus pygmaeus (Trematoda: Microphallidae) metacercariae. Parazitologiia 44, 250–261 (in Russian).Google Scholar
Krupenko, D.Y. (2011) Spatial organisation of the musculature of Himasthla elongata (Trematoda: Echinostomatidae) cercariae. Parazitologiia 45, 449–460 (in Russian).Google Scholar
Krupenko, D.Y. (2014a) Morpho-functional characteristics of the organization of digenean muscle system. Candidate of Sciences Dissertation, Saint-Petersburg State University, Saint-Petersburg (in Russian).Google Scholar
Krupenko, D.Y. (2014b) Muscle system of Diplodiscus subclavatus (Trematoda: Paramphistomida) cercariae, pre-ovigerous, and ovigerous adults. Parasitology Research 113, 941–952.Google Scholar
Kumar, D., McGeown, J.G., Reynoso-Ducoing, O., Ambrosio, J.R. & Fairweather, I. (2003) Observations on the musculature and isolated muscle fibres of the liver fluke, Fasciola hepatica . Parasitology 127, 457–473.Google Scholar
Mair, G.R., Maule, A.G., Shaw, C., Johnston, C.F. & Halton, D.W. (1998) Gross anatomy of the muscle systems of Fasciola hepatica as visualized by phalloidin-fluorescence and confocal microscopy. Parasitology 117, 75–82.Google Scholar
Mair, G.R., Maule, A.G., Day, T.A. & Halton, D.W. (2000) A confocal microscopical study of the musculature of adult Schistosoma mansoni . Parasitology 121, 163–170.Google Scholar
Mair, G.R., Maule, A.G., Fried, B., Day, T.A. & Halton, D.W. (2003) Organization of the musculature of schistosome cercariae. Journal of Parasitology 89, 623–625.Google Scholar
Nasir, P. (1960) Trematode parasites of snails from Edgbaston Pool: the life history of the strigeid Cotylurus brevis Dubois & Rausch, 1950. Parasitology 50, 551–575.Google Scholar
Niewiadomska, K. (1986) Verification of the life-cycles of Diplostomum spathaceum (Rudolphi, 1819) and D. pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomidae). Systematic Parasitology 8, 23–31.Google Scholar
Niewiadomska, K. (1996) The genus Diplostomum – taxonomy, morphology and biology. Acta Parasitologica 41, 55–66.Google Scholar
Niewiadomska, K. & Moczoń, T. (1984) The nervous system of Diplostomum pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomatidae). II. Structure and development of the nervous system in metacercariae. Zeitschrift für Parasitenkunde 70, 537–548.Google Scholar
Niewiadomska, K., Czubaj, A. & Moczon, T. (1996) Cholinergic and aminergic nervous systems in developing cercariae and metacercariae of Diplostomum pseudospathaceum Niewiadomska, 1984 (Digenea). International Journal for Parasitology 26, 161–168.Google Scholar
Öhman, C. (1965) The structure and function of the adhesive organ in strigeid trematodes. Part II. Diplostomum spathaceum Braun, 1893. Parasitology 55, 481–502.Google Scholar
Öhman, C. (1966) The structure and function of the adhesive organ in strigeid trematodes. Part III. Apatemon gracilis minor Yamaguti, 1933. Parasitology 56, 209–226.Google Scholar
Podvyaznaya, I.M. (1999) The fine structure of the tegument of cercariae and developing metacercariae of Diplostomum chromatophorum (Trematoda: Diplostomidae). Parazitologiia 33, 507–519 (in Russian).Google Scholar
Podvyaznaya, I.M. (2013) Ultrastructural changes in the digestive system during the metacercarial development in Diplostomum pseudospathaceum (Trematoda: Digenea: Diplostomidae). Proceedings of the Zoological Institute 317, 101–109 (in Russian).Google Scholar
Podvyaznaya, I.M. & Dobrovolsky, A.A. (2001) On the development of body-wall musculature in Diplostomum chromatophorum (Trematoda: Diplostomidae) metacercariae. Parazitologiia 35, 531–538 (in Russian).Google Scholar
Šebelová, Š., Stewart, M.T., Mousley, A., Fried, B., Marks, N.J. & Halton, D.W. (2004) The musculature and associated innervation of adult and intramolluscan stages of Echinostoma caproni (Trematoda) visualised by confocal microscopy. Parasitology Research 93, 196–206.Google Scholar
Shigin, A.A. (1986) Trematode fauna of the USSR. The genus Diplostomum. Metacercariae. 253 pp. Moscow, Nauka (in Russian).Google Scholar
Stewart, M.T., Marks, N.J. & Halton, D.W. (2003a) Neuroactive substances and associated major muscle systems in Bucephaloides gracilescens (Trematoda: Digenea) metacercaria and adult. Parasitology Research 91, 12–21.Google Scholar
Stewart, M.T., Mousley, A., Koubková, B., Šebelová, Š., Marks, N.J. & Halton, D.W. (2003b) Development in vitro of the neuromusculature of two strigeid trematodes, Apatemon cobitidis proterorhini and Cotylurus erraticus . International Journal for Parasitology 33, 413–424.Google Scholar
Stewart, M.T., Mousley, A., Koubková, B., Šebelová, Š., Marks, N.J. & Halton, D.W. (2003c) Gross anatomy of the muscle systems and associated innervation of Apatemon cobitidis proterorhini metacercaria (Trematoda: Strigeidea), as visualized by confocal microscopy. Parasitology 126, 273–282.Google Scholar
Sweeting, R. (1974) Investigations into natural and experimental infections of freshwater fish by the common eye-fluke Diplostomum spathaceum Rud. Parasitology 69, 291–300.CrossRefGoogle ScholarPubMed
Szidat, L. (1924) Beiträge zur Entwicklungsgeschichte der Holostomiden. II. Zoologischer Anzeiger 61, 249–266.Google Scholar
Szidat, L. (1929) Beiträge zur Kenntnis der Gattung Strigea (Abildg.). Zeitschrift für Parasitenkunde 1, 688–764.Google Scholar
Tolstenkov, O.O., Prokofiev, V.V., Terenina, N.B. & Gustafsson, M.K. (2011) The neuro-muscular system in cercaria with different patterns of locomotion. Parasitology Research 108, 1219–1227.Google Scholar
Tolstenkov, O.O., Akimova, L.N., Chrisanfova, G.G., Terenina, N.B. & Gustafsson, M.K. (2012a) The neuro-muscular system in fresh-water furcocercaria from Belarus. I Schistosomatidae. Parasitology Research 110, 185–193.CrossRefGoogle ScholarPubMed
Tolstenkov, O.O., Akimova, L.N., Terenina, N.B. & Gustafsson, M.K. (2012b) The neuromuscular system in freshwater furcocercaria from Belarus. II Diplostomidae, Strigeidae, and Cyathocotylidae. Parasitology Research 110, 583–592.Google Scholar
Tolstenkov, O.O., Akimova, L.N., Terenina, N.B. & Gustafsson, M.K. (2012c) The neuro-muscular system in continuously swimming cercariae from Belarus. I Xiphidiocercariae. Parasitology Research 111, 1977–1983.Google Scholar
Tolstenkov, O.O., Akimova, L.N., Terenina, N.B. & Gustafsson, M.K. (2012d) The neuromuscular system in continuously swimming cercariae from Belarus. II Echinostomata, Gymnocephala and Amphistomata. Parasitology Research 111, 2301–2309.Google Scholar
Wiśniewski, W.L. (1958) The development cycle of Posthodiplostomum brevicaudatum (v. Nordmann, 1832) Kozicka, 1958. Acta Parasitologica Polonica 6, 251–271.Google Scholar