Acta Parasitologica

, Volume 57, Issue 2, pp 131–148 | Cite as

Advanced stages of embryonic development and cotylocidial morphogenesis in the intrauterine eggs of Aspidogaster limacoides Diesing, 1835 (Aspidogastrea), with comments on their phylogenetic implications

  • Zdzisław Świderski
  • Larisa G. Poddubnaya
  • David I. Gibson
  • Daniel Młocicki
Original Paper

Abstract

Ultrastructural aspects of the advanced embryonic development and cotylocidial morphogenesis of the aspidogastrean Aspidogaster limacoides are described. The posterior or distal regions of the uterus are filled with eggs containing larvae at advanced stages of morphogenesis and fully-formed cotylocidia. Various stages and organs of this larva are described in detail, including the aspects of the developing and fully-differentiated cotylocidium, the body wall (tegument and musculature), glandular regions and the protonephridial excretory system. Blastomere multiplication by means of mitotic divisions takes place simultaneously with the degeneration or apoptosis of some micromeres; this frequently observed characteristic is compared and discussed in relation to corresponding reports for other neodermatans. During the advanced stages of the embryonic development of A. limacoides, the vitelline syncytium disappears and the size of the embryo increases rapidly. Evident polarization of the differentiating larva was observed; towards one pole of the egg, cytodifferentiation of the mouth, surrounded by the oral sucker and cephalic glands, takes place, whereas, towards the opposite pole, differentiation of the posterior sucker (incipient ventral disc) occurs. The oral and posterior suckers are formed from numerous embryonic cells which have differentiated into myocytes. The central part of the oral sucker undergoes invagination and forms the future pharynx and intestine. Fully-developed cotylocidia of A. limacoides have a neodermatan type of tegument, flame cells and two types of glandular structures. These results suggest a sister relationship between the Aspidogastrea and the Digenea, although the systematic position of aspidogastreans in relation to other platyhelminth taxa remains somewhat equivocal.

Keywords

Aspidogastrea Aspidogastridae Aspidogaster limacoides embryogenesis cotylocidial morphogenesis cotylocidium intrauterine eggs ultrastructure 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aubert H. 1855. Ueber der Wassergafassystem die Geschlchtsverhaltnisse, die Eibildung und die Entwicklung des Aspidogaster conchicola mit Berucksichtingung und Vergleichung anderre Trematoden. Zeitschrift für Wissenschaftliche Zoologie, 7, 349–376.Google Scholar
  2. Brinkmann A., Jr. 1957. Fish trematodes from Norwegian waters. IIa. The Norwegian species of the orders Aspidogastrea and Digenea (Gasterostomata). Arbok for Universitetet i Bergen. Naturvitenskapelig Rekke, 4, 1–29.Google Scholar
  3. Brooks D.R., Bandoni S.M., MacDonald C.A., O’Grady R.T. 1989. Aspects of the phylogeny of the Trematoda Rudolphi, 1808 (Platyhelminthes, Cercomeria). Canadian Journal of Zoology, 67, 2609–2624. DOI: 10.1139/z89-370.CrossRefGoogle Scholar
  4. Bruňanská M., Mackiewicz J.S., Młocicki D., Świderski Z., Nebesářová J. 2012. Early intrauterine embryonic development in Khawia sinensis Hsü, 1935 (Cestoda, Caryophyllidea, Lytocestidae), an invasive tapeworm of carp (Cyprinus carpio): an ultrastructural study. Parasitology Research, 110, 1009–1017. DOI: 10.1007/s00436-011-2590-2.PubMedCrossRefGoogle Scholar
  5. Burmeister H. 1856. Zoonomische Briefe: Allgemeine Darstellung der thierischen Organisation. II. Leipzig: O. Wigand.Google Scholar
  6. Chauhan B.S. 1954. Studies on trematode fauna of India. Part II. Subclass Aspidogastrea. Records of the Indian Museum, 51, 209–30.Google Scholar
  7. Chen M.X., Gao Q., Nie P. 2007. Phylogenetic systematic inference in the Aspidogastrea (Platyhelminthes, Trematoda) based on the 18S rRNA sequence. Acta Hydrobiologica Sinica, 31, 817–821 (In Chinese and English).Google Scholar
  8. Cousin C.E., Dorsey C.H. 1991. Nervous system of Schistosoma mansoni cercaria: organization and fine structure. Parasitology Research, 77, 132–141. DOI: 10.1007/BF00935427.PubMedCrossRefGoogle Scholar
  9. Cribb T.H., Bray R.A., Littlewood D.T.J., Pichelin S.P., Herniou E.A. 2001. The Digenea. In: (Eds. D.T.J. Littlewood and R.A. Bray) Interrelationships of the Platyhelminthes. London, New York: Taylor and Francis, pp. 168–185.Google Scholar
  10. Dollfus R.Ph. 1958. Cours d’helminthologie. I. Trematodes. Sousclasse Aspidogastrea. Annales de Parasitologie Humaine et Comparée, 33, 305–395.PubMedGoogle Scholar
  11. Eklu-Natey D.T. 1986. Contribution à l’étude ultrastructurale de la gametogenèse, du développement embryonnaire et du miracidium chez Schistosoma haematobium. PhD Thesis, University of Geneva, 169 pp.Google Scholar
  12. Eklu-Natey D.T., Świderski Z., Huggel H., Striebel H. 1982a. Schistosoma haematobium: egg-shell formation. Proceedings of the 11th International Congress on Electron Microscopy, August 17–24, 1982, Hamburg, Germany, 2, 605–606.Google Scholar
  13. Eklu-Natey D.T., Świderski Z., Moczoń T., Striebel H.P., Huggel H. 1982b. Ultrastructure and histochemistry of egg-shell formation in Schistosoma haematobium. Molecular and Biochemical Parasitology, 1982 Supplement, p. 708.Google Scholar
  14. Faust E.C. 1932. The excretory system as a method of classification of digenetic trematodes. Quarterly Review of Biology, 7, 458–468.CrossRefGoogle Scholar
  15. Faust E.C., Tang C.C. 1936. Notes on a new aspidogastrid species, with a consideration of the phylogeny of the group. Parasitology, 28, 487–507. DOI: 10.1017/S0031182000022678.CrossRefGoogle Scholar
  16. Fairweather I., Threadgold L.T. 1981. Hymenolepis nana: the functional structure of the “penetration gland” and nerve cells within the oncosphere. Parasitology, 82, 445–458. DOI: 10.1017/S003118200006697X.PubMedCrossRefGoogle Scholar
  17. Fried B., Haseeb M.A. 1991. Platyhelminthes: Aspidogastrea, Monogenea, and Digenea. In: (Eds. F.W. Harrison and B.J. Bogitsh) Microscopic anatomy of invertebrates. Vol. 3. Platyhelminthes and Nemertinea. New York, Wiley-Liss Inc., pp. 141–209.Google Scholar
  18. Furhmann O. 1928. Trematoda. In: (Eds. W. Kükenthal and I. Krumbach) Handbuch der Zoologie. Berlin, Vol. 2, pp. 1–140.Google Scholar
  19. Gibson D.I. 1987. Questions in digenean systematics and evolution. Parasitology, 95, 429–460. DOI: 10.1017/S0031182000057851.PubMedCrossRefGoogle Scholar
  20. Gibson D.I. 2002. Class Trematoda Rudolphi, 1808. In: (Eds. D.I. Gibson, A. Jones and R.A. Bray) Keys to the Trematoda. Vol. 1. Wallingford, CABI Publishing and the Natural History Museum, pp. 1–3.Google Scholar
  21. Gibson D.I, Chinabut S. 1984. Rohdella siamensis gen. nov., sp. nov. (Aspidogastridae: Rohdellinae subfam. nov.) from freshwater fishes in Thailand, with a reorganization of the classification of the Aspidogastrea. Parasitology, 88, 383–393. DOI: 10.1017/S0031182000054652.CrossRefGoogle Scholar
  22. Halton D.W., Gustaffson M.K.S. 1996. Functional morphology of the platyhelminth nervous system. Parasitology, 113(Supplement), pp. 47–72. DOI: 10.1017/S0031182000077891.CrossRefGoogle Scholar
  23. Littlewood D.T.J. 2006. The evolution of parasitism in flatworms. In: (Eds. A.G. Maule and N.J. Marks) Parasitic flatworms. Molecular biology, immunology and physiology. Wallingford, CABI Publishing, pp. 1–36.Google Scholar
  24. Littlewood D.T.J., Rohde K., Clough K.A. 1999a. The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biological Journal of the Linnean Society, 66, 75–114. DOI: 10.1006/bijl.1998.0276.CrossRefGoogle Scholar
  25. Littlewood D.T.J., Rohde K., Bray R.A., Herniou E.A. 1999b. Phylogeny of the Platyhelminthes and the evolution of parasitism. Biological Journal of the Linnean Society, 68, 257–287. DOI: 10.1006/bijl.1999.0341.CrossRefGoogle Scholar
  26. Lockyer A.E., Olson P.D., Littlewood D.T.J. 2003. Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biological Journal of the Linnean Society, 78, 155–171. DOI: 10.1046/j.1095-8312.2003.00141.x.CrossRefGoogle Scholar
  27. Młocicki D., Świderski Z., Eira C., Miquel J. 2005. An ultrastructural study of embryonic envelope formation in the anoplocephalid cestode Mosgovoyia ctenoides (Railliet, 1890) Beveridge, 1978. Parasitology Research, 95, 243–251. DOI: 10.1007/s00436-004-1276-4.PubMedCrossRefGoogle Scholar
  28. Młocicki D., Świderski Z., Miquel J., Eira C., Conn D.B. 2006. Cellular organization of the oncosphere of Mosgovoyia ctenoides (Cestoda: Anoplocephalidae). Journal of Parasitology, 92, 953–961. DOI: 10.1645/GE-790R1.1.PubMedCrossRefGoogle Scholar
  29. Młocicki D., Świderski Z., Brunanská M., Conn D.B. 2010a. Functional ultrastructure of the hexacanth larvae in the bothriocephalidean cestode Eubothrium salvelini (Schrank, 1790) — phylogenetic implications. Parasitology International, 59, 539–548. DOI: 10.1016/j.parint.2010.07.001.PubMedCrossRefGoogle Scholar
  30. Młocicki D., Świderski Z., Mackiewicz J.S., Ibraheem M.H. 2010b. Ultrastructure of intrauterine eggs: evidence of early ovoviviparity in the caryophyllidean cestode Wenyonia virilis Woodland, 1923. Acta Parasitologica, 55, 349–358. DOI: 10.2478/s11686-010-0044-0.CrossRefGoogle Scholar
  31. Młocicki D., Świderski Z., Conn D.B. 2010c. Ultrastructure of the early embryonic development of Corallobothrium fimbriatum (Cestoda: Proteocephalidea). Journal of Parasitology, 96, 839–846. DOI: 10.1645/GE-2438.1.PubMedCrossRefGoogle Scholar
  32. Monticelli F.S. 1892. Cotylogaster michaelis n. g., n. sp. e revisione degli Aspidobothridae. Festschrift zum Siebenzigsten Geburtstages Rudolf Leuckart’s. Leipzig: Wilhelm Engelmann, pp. 168–214.Google Scholar
  33. Olson P.D., Cribb T.H., Tkach V.V., Bray R.A., Littlewood D.T.J. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology, 33, 733–755. DOI:10.1016/S0020-7519(03)000 49-3.PubMedCrossRefGoogle Scholar
  34. Osborn H.L. 1903. On the habits and structure of Cotylaspis insignis Leidy, from Lake Chautauqua, New York. Journal of Morphology, 18, 1–44. DOI: 10.1002/jmor.1050180102.CrossRefGoogle Scholar
  35. Pan S.C.-T. 1980. The fine structure of the miracidium of Schistosoma mansoni. Journal of Invertebrate Pathology, 36, 307–372. DOI: 10.1016/0022-2011(2880)2990040-3.PubMedCrossRefGoogle Scholar
  36. Poddubnaya L.G., Levron C., Gibson D.I. 2011. Ultrastructural characteristic of the uterine epithelium of aspidogastrean and digenean trematodes. Acta Parasitologica, 56, 131–139. DOI: 10.2478/s11686-011-0016-z.CrossRefGoogle Scholar
  37. Poddubnaya L.G., Xylander W.E.R., Gibson D.I. 2012. Ultrastructural characteristics of the protonephridial terminal organ and associated ducts of adult specimens of the Aspidogastrea, Digenea and Monogenea, with comments on the relationships between these groups. Systematic Parasitology (in press).Google Scholar
  38. Rai S.L. 1964. Morphology and life history of Aspidogaster indicum Dayal, 1943 (Trematoda: Aspidogastridae). Indian Journal of Helminthology, 16, 100–141.Google Scholar
  39. Rohde K. 1972. The Aspidogastrea, especially Multicotyle purvisi Dawes, 1941. Advances in Parasitology, 10, 77–151. DOI: 10.1016/S0065-308X(08)60173-6.CrossRefGoogle Scholar
  40. Rohde K. 1973. Structure and development of Lobatostoma manteri sp. nov. (Trematoda: Aspidogastrea) from the Great Barrier Reef, Australia. Parasitology, 66, 63–83. DOI: 10.1017/S0031182000044450.PubMedCrossRefGoogle Scholar
  41. Rohde K. 1986. Ultrastructural studies of Austramphilina elongata Johnston, 1931 (Cestoda, Amphilinidea). Zoomorphology, 106, 91–102. DOI: 10.1007/BF00312111.CrossRefGoogle Scholar
  42. Rohde K. 1987. The formation of glandular secretion in the larval Austramphilina elongata (Amphilinidea). International Journal for Parasitology, 17, 821–828. DOI: 10.1016/0020-7519(87)90064-6.CrossRefGoogle Scholar
  43. Rohde K. 1994. The minor groups of parasitic Platyhelminthes. Advances in Parasitology, 33, 145–234. DOI: 10.1016/S0065-308X(08)60413-3.PubMedCrossRefGoogle Scholar
  44. Rohde K. 2001. The Aspidogastrea: an archaic group of Platyhelminthes. In: (Eds. D.T.J. Littlewood and R.A. Bray) Interrelationships of the Platyhelminthes. London, NewYork, Taylor and Francis, pp. 159–167.Google Scholar
  45. Rohde K. 2002. Subclass Aspidogastrea Faust & Tang, 1936. In: (D.I. Gibson, A. Jones and R.A. Bray) Keys to the Trematoda. Vol. 1. Wallingford, CABI Publishing and the Natural History Museum, pp. 5–14.Google Scholar
  46. Rybicka K. 1961. Cell reduction in the embryonic development of the cestode Diorchis ransomi Schultz, 1940. Nature, 192, 771–772. DOI: 10.1038/192771a0.CrossRefGoogle Scholar
  47. Rybicka K. 1966. Embryogenesis in cestodes. Advances in Parasitology, 4, 107–186. DOI: 10.1016/S0065-308X(08)604 49-2.PubMedCrossRefGoogle Scholar
  48. Schell S.C. 1973. Rugogaster hydrolagi gen. et sp. n. (Trematoda: Aspidobothria: Rugogastridae fam. n.) from the ratfish Hydrolagus colliei (Lay and Bennett, 1839). Journal of Parasitology, 59, 803–805. DOI: 10.2307/3278410.CrossRefGoogle Scholar
  49. Stirewalt M.A. 1973. Schistosoma mansoni: histological localization of gelatinase in the preacetabular glands of cercariae. Experimental Parasitology, 34, 382–392. DOI: 10.1016/0014-4894(73)90098-2.PubMedCrossRefGoogle Scholar
  50. Stirewalt M.A. 1974. Schistosoma mansoni: cercaria to schistosomule. Advances in Parasitology, 12, 115–182. DOI: 10.1016?S0065-308X(08)60388-7.PubMedCrossRefGoogle Scholar
  51. Stunkard H.W. 1946. Interrelationships and taxonomy of the digenetic trematodes. Biological Reviews, 21, 148–158. DOI: 10.1111/j.1469-185X.1946.tb00321.x.PubMedCrossRefGoogle Scholar
  52. Stunkard H.W. 1970. Trematode parasites of insular and relict vertebrates. Journal of Parasitology, 56, 334–335. DOI: 10.2307/3277544.Google Scholar
  53. Świderski Z. 1968. An electron microscopic evidence of the degeneration of some micromeres during embryonic development of the cestode Catenotaenia pusilla (Goeze, 1782) (Cyclophyllidea, Catenotaeniidae). Zoologica Poloniae, 18, 469–474.Google Scholar
  54. Świderski Z. 1972. La structure fine de l’oncosphere du cestode Catenotaenia pusilla (Goeze, 1782) (Cyclophyllidea, Catenotaeniidae). La Cellule, 69, 207–237.Google Scholar
  55. Świderski 1981. Reproductive and developmental biology of the cestodes. In: (Eds. W.H. Clark, Jr. and T.S. Adams) Advances in Invertebrate Reproduction. Elsevier/North Holland, New York, Amsterdam, Oxford, pp. 365–366.Google Scholar
  56. Świderski Z. 1984. Embryonic development of Schistosoma mansoni. South African Journal of Science, 80, 434.Google Scholar
  57. Świderski Z. 1985. Embryonic development of Schistosoma mansoni and S. haematobium: egg envelope formation. South African Journal of Science, 81, 43–45.Google Scholar
  58. Świderski Z. 1994a. Origin, differentiation and ultrastructure of egg envelopes surrounding the miracidia of Schistosoma mansoni. Acta Parasitologica, 39, 64–72.Google Scholar
  59. Świderski Z. 1994b. Origin, differentiation and ultrastructure of egg envelopes surrounding the coracidia of Bothriocephalus clavibothrium. Acta Parasitologica, 39, 73–81.Google Scholar
  60. Świderski Z. 1994c. Homology and analogy in of egg envelopes surrounding the coracidia of Bothriocephalus clavibothrium and miracidia of Schistosoma mansoni. Acta Parasitologica, 39, 123–130.Google Scholar
  61. Świderski Z. 1994d. Echinococcus multilocularis: ultrastructure of the oncospheral nerve cells. In: (Eds. B. Jouffrey and C. Colleix) Electron Microscopy — 1994: ICEM 13. Paris. Proceedings of the 13th International Congress on Electron Microscopy, Paris, 17–22 July, 1994, 3B, 1425–1426.Google Scholar
  62. Świderski Z. 1997. Ultrastructure of the oncospheral nerve cells in Echinococcus granulosus and E. multilocularis. In: Archivos Internacionales de la Hidatidosis. Vol. 32. 18th International Congress of Hydatidology, Lisboa, Portugal, pp. 126–128.Google Scholar
  63. Świderski Z., Mackiewicz J.S. 2004. Ultrastructural studies on the cellular organisation of the coracidium of the cestode Bothriocephalus clavibothrium Ariola, 1899 (Pseudophyllidea, Bothriocephalidae). Acta Parasitologica, 49, 116–139.Google Scholar
  64. Świderski Z., Tkach V.V. 2002. Ultrastructure of embryonic development of Inermicapsifer madagascariensis (Cestoda, Anoplocephalidae) with emphasis on the cellular organisation of the infective eggs. Acta Parasitologica, 47, 105–120.Google Scholar
  65. Świderski Z., Poddubnaya L.G., Gibson D.I., Levron C., Młocicki D. 2011. Egg formation and the early embryonic development of Aspidogaster limacoides Diesing, 1835 (Aspidogastrea: Aspidogastridae), with comments on their phylogenetic significance. Parasitology International, 60, 371–380. DOI: 10.1016/j.parint.2011.06.006.PubMedCrossRefGoogle Scholar
  66. Tang Z., Tang C. 1980. Life histories of two species of aspidogastrids and the phylogeny of the group. Acta Hydrobiologica Sinica, 7, 153–169 + 5 plates (In Chinese and English).Google Scholar
  67. Timofeeva T.A. 1975. On the evolution and phylogeny of the aspidogastrids. Parazitologiya, 9, 105–111 (In Russian).Google Scholar
  68. Timofeeva T.A. 2005. Ecological approach to the problem of monophyly of Neodermata (Platyhelminthes). Parazitologiya, 39, 89–102 (In Russian).Google Scholar
  69. Voeltzkow A. 1888a. Aspidogaster conchicola. Arbeiten aus dem Zoologisch-Zootomischen Institut in Würzburg, 8, 249–288.Google Scholar
  70. Voeltzkow A. 1888b. Aspidogaster limacoides. Arbeiten aus dem Zoologisch-Zootomischen Institut in Würzburg, 8, 290–292.Google Scholar
  71. Williams C.O. 1942. Observations on the life history and taxonomic relationships of the trematode Aspidogaster conchicola. Journal of Parasitology, 28, 467–475. DOI: 10.2307/3272907.CrossRefGoogle Scholar
  72. Wilson R.A. 1969. The fine structure of the protonephridial system in the miracidium of Fasciola hepatica. Journal of Parasitology, 55, 124–133. DOI: 10.1017/S003118200008241X.PubMedCrossRefGoogle Scholar
  73. Wilson R.A., Webster L.A. 1974. Protonephridia. Biological Reviews, 49, 127–160. DOI: 10.1111/j.1469-185X.1974.tb01572.x.PubMedCrossRefGoogle Scholar
  74. Xylander W.E.R. 1986. Zur Biologie und Ultrastruktur der Gyrocotylida und Amphilinida sowie ihre Stellung in phylogenetischen System der Platyhelminthes. PhD Thesis, Universitat zu Göttingen.Google Scholar
  75. Xylander W.E.R. 1987. Ultrastructure of the lycophora larvae of Gyrocotyle urna (Cestoda, Gyrocotylidea). III. The protonephridial system. Zoomorphology, 107, 88–95. DOI: 10.1007/ BF00312118. (Accepted March 12, 2012)CrossRefGoogle Scholar
  76. Xylander W.E.R. 1990. Ultrastructure of the lycophora larva of Gyrocotyle urna (Cestoda, Gyrocotylidea). IV. The glandular system. Zoomorphology, 109, 319–328. DOI: 10.1007/BF00803572.Google Scholar
  77. Xylander W.E.R. 2001. Gyrocotylidea, Amphilinidea and the early evolution of Cestoda. In: (Eds. D.T.J. Littlewood and R.A. Bray) Interrelationships of the Platyhelminthes. London, New York, Taylor and Francis, pp. 103–111.Google Scholar
  78. Zamparo D., Brooks D.R. 2003. Phylogenetic systematic assessment of the Aspidobothrea (Platyhelminthes, Neodermata, Trematoda). Zoologica Scripta, 32, 83–93. DOI: 10.1046/j.1463-6409.2003.00088.x.CrossRefGoogle Scholar

Copyright information

© Versita Warsaw and Springer-Verlag Wien 2012

Authors and Affiliations

  • Zdzisław Świderski
    • 1
    • 2
  • Larisa G. Poddubnaya
    • 3
  • David I. Gibson
    • 4
  • Daniel Młocicki
    • 1
    • 2
  1. 1.W. Stefański Institute of ParasitologyPolish Academy of SciencesWarsawPoland
  2. 2.Department of General Biology and ParasitologyMedical University of WarsawWarsawPoland
  3. 3.Institute of Biology of Inland WatersRussian Academy of SciencesBorok, Yaroslavl ProvinceRussia
  4. 4.Department of ZoologyNatural History MuseumLondonUK

Personalised recommendations