Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-04T18:51:32.920Z Has data issue: false hasContentIssue false
  • English
  • Français

Functional ultrastructure of eggs and cellular organization of hexacanths of the cyclophyllidean cestode Thysanotaenia congolensis: a phylogenetic implication of obtained results

Published online by Cambridge University Press:  22 December 2015

ZDZISŁAW ŚWIDERSKI ,
JORDI MIQUEL  and
DAVID BRUCE CONN
ZDZISŁAW ŚWIDERSKI*
Affiliation:
W. Stefański Institute of Parasitology, Polish Academy of Sciences, 51/55 Twarda Street, 00-818 Warszawa, Poland
JORDI MIQUEL
Affiliation:
Laboratori de Parasitologia, Departament de Microbiologia i Parasitologia Sanitàries, Facultat de Farmàcia, Universitat de Barcelona, Av. Joan XXIII, sn, 08028 Barcelona, Spain Facultat de Biologia, Institut de Recerca de la Biodiversitat, Universitat de Barcelona, Av. Diagonal, 645, 08028 Barcelona, Spain
DAVID BRUCE CONN
Affiliation:
Department of Biology and One Health Center, Berry College, Mount Berry, GA 30149, USA Department of Invertebrate Zoology, Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA
*
*Corresponding author. W. Stefański. Institute of Parasitology, Polish Academy of Sciences, 51/55 Twarda Street, 00-818 Warszawa, Poland. Tel: (+ 48 22) 697 89 70. Fax: (+ 48 22) 620 62 27. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The functional ultrastructure of eggs and cellular organization of hexacanths from gravid proglottids of Thysanotaenia congolensis, from black rats from Cape Verde, were examined by transmission electron microscopy. Mature eggs with fully formed hexacanths are grouped within parenchymatous capsules of gravid proglottids. Oncospheral envelopes surrounding mature hexacanths are reduced to a very thin membranous embryophore as their protective function is taken over by the parenchymatous capsules originating from the medullary parenchyma of immature proglottids and composed of three layers. Six major cell types are present: a bi-nucleate medullary centre; a six-nucleate U-shaped penetration gland; a second type of penetration gland; two neurosecretory-type nerve cells; about 30 somatic cells; and about 12 germinative cells. Present results on the functional ultrastructure of eggs and cellular organization of hexacanths support the phylogenetic distinction between T. congolensis and cestodes of the subfamily Anoplocephalinae.

Keywords

Thysanotaenia congolensisfunctional ultrastructure of eggscellular organization of hexacanthultrastructural evidences for davaineid characters
Type
Research Article
Information
Parasitology , Volume 143 , Issue 3 , March 2016 , pp. 320 - 333
Check for updates
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

REFERENCES

Baer, J. G. (1956). The taxonomic position of Taenia madagascariensis Davaine, 1870, a tapeworm parasite of man and rodents. Annals of Tropical Medicine and Parasitology 50, 152–156.Google Scholar
Baer, J. G. and Fain, A. (1955). Les Cestodes des Pangolins. Bulletin de la Société Neuchâteloise des Sciences Naturelles 78, 37–52.Google Scholar
Beveridge, I. (1994). Family Anoplocephalidae Cholodkovsky, 1902. In Keys to the Cestode Parasites of Vertebrates (ed. Khalil, L. F., Jones, A., Bray, R. A.), pp. 315–366. CAB International, Wallingford, UK.Google Scholar
Beveridge, I. (2001). The use of life-cycle characters in studies of the evolution of cestodes. In Interrelationships of the Platyhelminthes (ed. Littlewood, D. T. J. and Bray, R. A.), pp. 250–256. Taylor and Francis, London and New York.Google Scholar
Caley, J. (1975). In vitro hatching of the tapeworm Moniezia expansa (Cestoda: Anoplocephalidae) and some properties of the egg membranes. Zeitschrift für Parasitenkunde 45, 335–346.CrossRefGoogle ScholarPubMed
Coil, W. H. (1979). Studies on the embryogenesis of the tapeworm Cittotaenia variabilis (Stiles, 1895) using transmission and scanning electron microscopy. Zeitschrift für Parasitenkunde 59, 151–159.Google Scholar
Collin, W. K. (1969). The cellular organisation of hatched oncospheres of Hymenolepis citelli (Cestoda: Cyclophyllidea). Journal of Parasitology 55, 149–166.Google Scholar
Conn, D. B. (1985 a). Scanning electron microscopy and histochemistry of embryonic envelopes of the porcupine tapeworm, Monoecocestus americanus (Cyclophyllidea: Anoplocephalidae). Canadian Journal of Zoology 63, 1194–1198.Google Scholar
Conn, D. B. (1985 b). Fine structure of the embryonic envelopes of Oochoristica anolis (Cestoda: Linstowiidae). Zeitschrift für Parasitenkunde 71, 639–648.Google Scholar
Conn, D. B. (1988). The role of cellular parenchyma and extracellular matrix in the histogenesis of the paruterine organ of Mesocestoides lineatus (Cestoda: Cyclophyllidea). Journal of Morphology 197, 303–314.Google Scholar
Conn, D. B. (1999). Ultrastructure of the embryonic envelopes and associated maternal structures of Distoichometra bufonis (Platyhelminthes, Cestoidea, Nematotaeniidae). Acta Parasitologica 44, 4–10.Google Scholar
Conn, D. B. and Etges, F. J. (1984). Fine structure and histochemistry of the parenchyma and uterine egg capsules of Oochoristica anolis (Cestoda: Linstowiidae). Zeitschrift für Parasitenkunde 70, 769–779.Google Scholar
Conn, D. B., Etges, F. J. and Sidner, R. A. (1984). Fine structure of the gravid paruterine organ and embryonic envelopes of Mesocestoides lineatus (Cestoda). Journal of Parasitology 70, 68–77.Google Scholar
Conn, D. B. and Świderski, Z. (2008). A standardised terminology of the embryonic envelopes and associated developmental stages of tapeworms (Platyhelminthes: Cestoda). Folia Parasitologica 55, 42–52.Google Scholar
Fairweather, I. and Threadgold, L. T. (1981). Hymenolepis nana: the fine structure of the “penetration gland” and nerve cells within the oncosphere. Parasitology 82, 445–458.Google Scholar
Jabbar, A., Świderski, Z., Młocicki, D., Beveridge, I. and Lightowlers, M. W. (2010 a). The ultrastructure of taeniid cestode oncospheres and localization of host-protective antigens. Parasitology 137, 521–535.Google Scholar
Jabbar, A., Crawford, S., Młocicki, D., Świderski, Z., Conn, D. B., Jones, M. K., Beveridge, I. and Lightowlers, M. W. (2010 b). Ultrastructural reconstruction of Taenia ovis oncospheres from serial sections. International Journal for Parasitology 40, 1419–1431.Google Scholar
Jones, M. K. (1988). Formation of the paruterine capsules and embryonic envelopes in Cylindrotaenia hickmani (Jones, 1985) (Cestoda: Nematotaeniidae). Australian Journal of Zoology 36, 545–563.Google Scholar
Khalil, L. F., Jones, A. and Bray, R. A. (1994). Keys to the Cestode Parasites of Vertebrates. CAB International, Wallingford, UK.CrossRefGoogle Scholar
Korneva, J. V. (1994). Cell compound and ultrastructural organisation of the coracidium of Triaenophorus nodulosus (Cestoda, Pseudophyllidea). Parazitologija 28, 276–282 [in Russian].Google Scholar
Lethbridge, R. C. (1980). The biology of the oncosphere of cyclophyllidean cestodes. Helminthological Abstracts Series A 49, 59–72.Google Scholar
Lethbridge, R. C. and Gijsbers, M. F. (1974). Penetration gland secretion by hexacanths of Hymenolepis diminuta . Parasitology 68, 303–311.Google Scholar
Młocicki, D., Świderski, Z., Eira, C. and 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.Google Scholar
Młocicki, D., Świderski, Z., Miquel, J., Eira, C. and Conn, D. B. (2006). Cellular organization of the oncosphere of Mosgovoyia ctenoides (Cyclophyllidea, Anoplocephalidae). Journal of Parasitology 92, 953–961.Google Scholar
Młocicki, D., Świderski, Z., Bruňanská, M. and Conn, D. B. (2010). Functional ultrastructure of the hexacanth larvae in the bothriocephalidean cestode Eubothrium salvelini (Schrank, 1790) and its phylogenetic implications. Parasitology International 59, 539–548.Google Scholar
Ogren, R. E. (1968 a). Characteristic for two classes of embryonic cells in oncospheres of Hymenolepis diminuta stained for cytoplasmic substances. Transactions of the American Microscopical Society 87, 82–96.Google Scholar
Ogren, R. E. (1968 b). The basic cellular pattern for undifferentiated oncospheres of Hymenolepis diminuta . Transactions of the American Microscopical Society 87, 448–463.Google Scholar
Ogren, R. E. (1971). Criteria for anterior polarity and symmetry in tapeworm hexacanth embryos. Proceedings of the Pennsylvania Academy of Science 45, 40–41.Google Scholar
Reid, W. M. (1948). Penetration glands in cyclophyllidean onchospheres. Transactions of the American Microscopical Society 67, 177–182.Google Scholar
Rybicka, K. (1964). Embryonic development of Moniezia expansa (Rud., 1810) (Cyclophyllidea, Anoplocephalidae). Acta Parasitologica 12, 313–325.Google Scholar
Rybicka, K. (1966). Embryogenesis in cestodes. Advances in Parasitology 4, 107–186.Google Scholar
Rybicka, K. (1967). Embryogenesis in Hymenolepis diminuta. V. Acetylcholinesterase in embryos. Experimental Parasitology 20, 263–266.Google Scholar
Spasskii, A. A. (1951). Anoplocephalate Tapeworms of Domestic and Wild Animals (English Translation). The Academy of Sciences of the USSR, Moscow, Russia.Google Scholar
Świderski, Z. (1972). La structure fine de l'oncosphère du cestode Catenotaenia pusilla (Goeze, 1782) (Cyclophyllidea, Catenotaeniidae). La Cellule 69, 207–237.Google Scholar
Świderski, Z. (1975). Comparative fine structure of cestode embryos. Proceedings of the 2nd European Multicolloquium of Parasitology, Trogir 1, 265–273.Google Scholar
Świderski, Z. (1981). Reproductive and developmental biology of the cestodes. In Advances in Invertebrate Reproduction (ed. Clark, W. H. Jr. and Adams, T. S.), pp. 365–366. Elsevier/North Holland, New York, Amsterdam, Oxford.Google Scholar
Świderski, Z. (1982). Echinococcus granulosus: ultrastructure of the glandular regions of the infective oncosphere. In Electron Microscopy 1982, Proceedings of the 10th International Congress on Electron Microscopy, Hamburg, 3 (ed. Le Poole, J. B. and Zeitler, E.), pp. 511–512. Deutsche Gesellschaft für Elektronenmikroskopie, Hamburg, Germany.Google Scholar
Świderski, Z. (1983). Echinococcus granulosus: hook-muscle system and cellular organisation of infective oncospheres. International Journal for Parasitology 13, 289–299.Google Scholar
Świderski, Z. (1986 a). Ultrastructure of the glandular regions of the infective oncospheres of the cestode Inermicapsifer madagascariensis (Cyclophyllidea, Anoplocephalidae, Inermicapsiferinae). In Electron Microscopy 1986, Proceedings of the 12th International Congress on Electron Microscopy, Kyoto, 3 (ed. Imura, T., Maruse, S. and Suzuki, T.), pp. 3333–3334. Japanese Society for Electron Microscopy, Tokyo, Japan.Google Scholar
Świderski, Z. (1986 b). Ultrastructure of the parenchymatic capsules of the cestode Inermicapsifer madagascariensis (Cyclophyllidea, Anoplocephalidae, Inermicapsiferinae). In Electron Microscopy 1986, Proceedings of the 12th International Congress on Electron Microscopy, Kyoto, 3 (ed. Imura, T., Maruse, S. and Suzuki, T.), pp. 3331–3332. Japanese Society for Electron Microscopy, Tokyo, Japan.Google Scholar
Świderski, Z. (1986 c). SEM study of Inermicapsifer madagascariensis, a tapeworm parasite of man and rodents. In Electron Microscopy 1986, Proceedings of the 12th International Congress on Electron Microscopy, Kyoto, 3 (ed. Imura, T., Maruse, S. and Suzuki, T.), pp. 3329–3330. Japanese Society for Electron Microscopy, Tokyo, Japan.Google Scholar
Świderski, Z. (1994). Echinococcus multilocularis: ultrastructure of the oncospheral nerve cells. In Proceedings of the 13th International Congress on Electron Microscopy, Paris, 3B (ed. Jouffrey, B. and Colleix, C.), pp. 1425–1426. Les Editions de Physique, Paris, France.Google Scholar
Świderski, Z. (1997). Ultrastructure of the oncospheral nerve cells in Echinococcus granulosus and E. multilocularis . In Archivos Internationales de la Hidatidosis, Vol. 32, 18th International Congress of Hydatidology, Lisboa, (ed. Menezes da Silva, A.), pp. 126–128. International Association of Hydatidology, Lisbon, Portugal. Google Scholar
Świderski, Z. and 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
Świderski, Z., Miquel, J., Feliu, C. and Conn, D. B. (2015). Functional ultrastructure of the parenchymatic capsules of the cestode Thysanotaenia congolensis (Cyclophyllidea, Anoplocephalidae, Inermicapsiferinae). Parasitology Research 114, 297–303.Google Scholar
Świderski, Z. and Mokhtar, F. (1974). The fine structure of the coracidia of Bothriocephalus clavibothrium Ariola, 1899 (Cestoda: Pseudophyllidea). In Proceedings of the 3rd International Congress of Parasitology, Munich, 3 (ed. Piekarski, G. and Scholtyseck, E.), pp. 412–413.Google Scholar
Świderski, Z., Ndiaye, P. I., Tkach, V., Miquel, J., Marchand, B., Chomicz, L., Grytner-Ziecina, B. and Sereda, M. J. (2001 a). Ultrastructural study of the embryonic development of the anoplocephalid cestode Anoplocephaloides dentata, an intestinal parasite of Arvicolidae rodents. I. Egg envelope formation. Acta Parasitologica 46, 171–185.Google Scholar
Świderski, Z., Ndiaye, P. I., Tkach, V., Miquel, J., Marchand, B., Chomicz, L., Grytner-Ziecina, B. and Sereda, M. J. (2001 b). Ultrastructural study of the embryonic development of the anoplocephalid cestode Anoplocephaloides dentata, an intestinal parasite of Arvicolidae rodents. II. Differentiation and cellular organisation of the oncosphere. Acta Parasitologica 46, 280–292.Google Scholar
Świderski, Z. and Subilia, L. (1988). Embryonic development of the cestode Oochoristica agamae Baylis, 1919 (Cyclophyllidea: Anoplocephalidae). In Electron Microscopy–1988. Proceedings of the 6th Asia-Pacific Congress & Workshop on Electron MIcroscopy, Bangkok (ed. Mangclaviraj, V.), pp. 699–700. Asia-Pacific Society for Electron Microscopy, Bangkok, Thailand.Google Scholar
Świderski, Z. and Tkach, V. V. (1997 a). Differentiation and ultrastructure of the paruterine organs and paruterine capsules, in the nematotaeniid cestode Nematotaenia dispar (Goeze, 1782) Lühe, 1910, a parasite of amphibians. International Journal for Parasitology 27, 635–644.Google Scholar
Świderski, Z. and Tkach, V. V. (1997 b). Differentiation and ultrastructure of oncospheral and uterine envelopes in the nematotaeniid cestode, Nematotaenia dispar (Goeze, 1782). International Journal for Parasitology 27, 1065–1074.Google Scholar
Świderski, Z. and Tkach, V. V. (1997 c). Ultrastructure of the infective eggs of the hymenolepidid cestode, Ditestolepis tripartita (Zarnowski, 1955), a parasite of shrews. Acta Parasitologica 42, 46–54.Google Scholar
Świderski, Z. and Tkach, V. V. (1997 d). Ultrastructural studies on the cellular organisation of the oncospheres of the nematotaeniid cestode, Nematotaenia dispar (Goeze, 1782). Acta Parasitologica 42, 158–167.Google Scholar
Świderski, Z. and Tkach, V. V. (1999). Electron microscopical studies on the cellular organisation of the oncospheres of the hymenolepidid cestode, Staphylocystoides stefanskii (Zarnowski, 1954). Acta Parasitologica 44, 31–38.Google Scholar
Świderski, Z. and 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
Świderski, Z., Tkach, V. V. and Vaucher, C. (2000). Fine structure of the infective eggs of the dilepidid cestode Hepatocestus hepaticus (Baer, 1932), a parasite of shrews. Acta Parasitologica 45, 71–82.Google Scholar
Thiéry, J. P. (1967). Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. Journal de Microscopie 6, 987–1018.Google Scholar
Tkach, V. V. and Świderski, Z. (1997). Late stages of egg maturation in the cestode Pseudhymenolepis redonica Joyeux et Baer, 1935 (Cyclophyllidea, Hymenolepididae), a parasite of shrews. Acta Parasitologica 42, 97–108.Google Scholar
Voge, M. (1969). Systematics of cestodes - present and future. In Problems in Systematics of Parasites (ed. Schmidt, G. G.), pp. 49–72. University Park Press, Baltimore, USA.Google Scholar
Wikgren, M. C. (1986). The nervous system of early larval stages of the cestode Diphyllobothrium dendriticum . Acta Zoologica (Stockholm) 67, 155–163.Google Scholar