Fertilization in the cestode Echinococcus multilocularis (Cyclophyllidea, Taeniidae)
-
Zdzisław Świderski
,
Jordi Miquel
Abstract
Fertilization in the taeniid cestode Echinococcus multilocularis with uniflagellate spermatozoa was examined by means of transmission electron microscopy (TEM). Fertilization in this species occurs in the oviduct lumen or in the fertilization canal proximal to the ootype, where the formation of the embryonic capsule precludes sperm contact with the oocytes. Cortical granules are not present in the cytoplasm of the oocytes of this species, however, several large bodies containing granular material where frequently observed. Spermatozoa coil spirally around the oocytes and syngamy occurs by lateral fusion of oocyte and sperm plasma membranes. In the ootype, one vitellocyte associates with fertilized oocyte, forming a membranous capsule which encloses both cell types. In this stage, the spirally coiled sperm body adheres partly to the external oocyte surface, and partially enters into the perinuclear cytoplasm. The electron-dense sperm nucleus becomes progressively electron-lucent within the oocyte cytoplasm after penetration. Simultaneously with chromatin decondensation, the elongated sperm pronucleus changes shape, forming a spherical male pronucleus, which attains the size of the female pronucleus. Cleavage begins immediately after pronuclear fusion.
References
Brooks D.R. 1989. A summary of the database pertaining to the phylogeny of the major groups of parasitic platyhelminths, with a revised classification. Canadian Journal of Zoology, 67, 714-720. DOI: 10.1139/z89-10310.1139/z89-103Search in Google Scholar
Burton P.R. 1960. Gametogenesis and fertilization in the frog lung fluke, Haematoloechus medioplexus Stafford (Trematoda: Plagiorchiidae). Journal of Morphology, 107, 93-122. DOI: 10.1002/jmor.105107010710.1002/jmor.1051070107Search in Google Scholar
Burton P.R. 1967. Fine structure of the reproductive system of a frog lung fluke. II. Penetration of the ovum by a spermatozoan. Journal of Parasitology, 53, 994-99910.2307/3276825Search in Google Scholar
Coil W.H. 1991. Platyhelminthes: Cestoidea. In: Microscopic anatomy of invertebrates. Platyhelminthes and Nemertinea. Vol. 3 (Ed. F.W. Harrison). Wiley-Liss, Inc., New York, 211-283Search in Google Scholar
Conn D.B. 1988. Are vitelline cell globules a mechanism for polyspermy prevention in cyclophyllidean cestodes? Transactions of the American Microscopical Society, 107, 106Search in Google Scholar
Conn D.B. 2000. Atlas of invertebrate reproduction and development. Wiley-Liss, Inc., New York Search in Google Scholar
Ehlers U. 1985. Phylogenetic relationships within the Platyhelminthes. In: The origins and relationships of lower invertebrates (Eds. S. Conway Morris, J.D. George, R. Gibson and H.M. Platt). Oxford University Press, Oxford, 143-158Search in Google Scholar
Fried B., Haseeb M.A. 1991. Platyhelminthes: Aspidogastrea, Monogenea and Digenea. In: Microscopic anatomy of invertebrates. Platyhelminthes and Nemertinea. Vol. 3 (Ed. F.W. Harrison). Wiley-Liss, Inc., New York, 141-209Search in Google Scholar
Justine J.-L., Mattei X. 1984. Ultrastructural observations on the spermatozoon, oocyte and fertilization process in Gonapodasmius, a gonochoristic trematode (Trematoda: Digenea: Didymozoidae). Acta Zoologica (Stockholm), 65, 171-177. DOI: 10.1111/j.1463-6395.1984.tb00822.x 10.1111/j.1463-6395.1984.tb00822.xSearch in Google Scholar
Justine J.-L., Mattei X. 1986. Ultrastructural observations on fertilization in Dionchus remorae (Platyhelminthes, Monogenea, Dionchidae). Acta Zoologica (Stockholm), 67, 97-101. DOI: 10.1111/j.1463-6395.1986.tb00853.x 10.1111/j.1463-6395.1986.tb00853.xSearch in Google Scholar
Kearn G., Whittington I. 2015. Sperm transfer in monogenean (platyhelminth) parasites. Acta Parasitologica, 60, 567-600. DOI: 10.1515/ap-2015-008210.1515/ap-2015-0082Search in Google Scholar
Mokhtar-Maamouri F. 1980. Particularites des processus de la fécondation chez Acanthobothrium filicolle Zschokke, 1888 (Cestoda: Tetraphyllidea, Onchobothriidae). Archives de l’Institut Pasteur Tunis, 57, 191-20510.1051/parasite/1982575429Search in Google Scholar
Młocicki D., Świderski Z., Conn D.B. 2010. Ultrastructure of the early embryonic stages of Corallobothrium fimbriatum (Cestoda: Proteocephalidea). Journal of Parasitology, 96, 839-846. DOI: 10.1645/GE-2438.110.1645/GE-2438.1Search in Google Scholar
Orido Y. 1988. Fertilization and oogenesis of the lung fluke, Paragonimus ohirai (Trematoda: Troglotrematidae). International Journal for Parasitology, 18, 973-980. DOI: 10.1016/0020-7519(88)90180-410.1016/0020-7519(88)90180-4Search in Google Scholar
Reynolds E.S. 1963. The use of lead citrate at high pH as an electronopaque stain in electron microscopy. Journal of Cell Biology, 17, 208-21210.1083/jcb.17.1.208Search in Google Scholar PubMed PubMed Central
Rieger R., Tyler S., Smith J.P.S., Rieger G. 1991. Platyhelminthes: Turbellaria. In: Microscopic anatomy of invertebrates. Platyhelminthes and Nemertinea. Vol. 3 (Ed. F.W. Harrison). Wiley-Liss, Inc., New York, 7-140Search in Google Scholar
Świderski Z., 1968. Electron microscopy of embryonic envelope formation by the cestode Catenotaenia pusilla. Experimental Parasitology, 23, 104-11310.1016/0014-4894(68)90048-9Search in Google Scholar
Świderski Z. 1976. Fertilization in the cestode Hymenolepis diminuta (Cyclophyllidea, Hymenolepididae). Proceedings of the 6th European Congress of Electron Microscopy, Jerusalem, 2, 311-312Search in Google Scholar
Świderski Z. 1981. Reproductive and developmental biology of the cestodes. In: Advances in invertebrate reproduction, W. H. Clark, Jr., and T.S. Adams (eds.). Elsevier, Amsterdam, The Netherlands, pp. 365-366Search in Google Scholar
Świderski Z., Conn D.B. 1999. Ultrastructural aspect of fertilization in Proteocephalus longicollis, Inermicapsifer madagascariensis, and Mesocestoides lineatus (Platyhelminthes, Cestoda). Acta Parasitologica, 44, 19-30Search in Google Scholar
Świderski Z., Xylander W.E.R. 1998. Types of vitellocytes and vitellogenesis in the cestoda in relation to different types of embryonic development, ovoviviparity and life cycles. Wiadomości Parazytologiczne, 44, 604Search in Google Scholar
Świderski Z., Xylander W.E.R. 2000. Vitellocytes and vitellogenesis in cestodes in relation to embryonic development egg production and life cycles. International Journal for Parasitology, 30, 805-817 10.1016/S0020-7519(00)00066-7Search in Google Scholar
Świderski Z., Conn D.B., Miquel J., Młocicki D. 2004. Fertilization in the cestode Gallegoides arfaai (Mobedi et Ghadirian, 1977) Tenora et Mas-Coma, 1978 (Cyclophyllidea, Anoplocephalidae). Acta Parasitologica, 49, 108-115Search in Google Scholar
Świderski Z., Huggel H., Schonenberger N. 1970. The role of the vitelline cell in the capsule formation during embryogenesis in Hymenolepis diminuta (Cestoda). In: Proceedings of the 7th International Congress of Electron Microscopy, J. Andre (ed.). Societe Francaise de Microscopie Electronique, Grenoble, France, pp. 669-670Search in Google Scholar
Taeleb A.A., Ghobashy M.A. 2014. Fine structural observations on oocyte development, oogenesis and fertilization process of Cotugnia polycantha Diamar, 1893 (Cestoda: Davaineidae) infecting doves (Streptopelia senegalensis). African Journal of Biotechnology, 13, 3204-3216. DOI: 10.5897/AJB2014.1380110.5897/AJB2014.13801Search in Google Scholar
Tappenden T., Kearn G.C., Evans-Gowing R. 1993. Fertilization and the functional anatomy of the germarium in the monogenean Entobdella soleae. International Journal for Parasitology, 23, 901-911. DOI: 10.1016/0020-7519(93)90056-510.1016/0020-7519(93)90056-5Search in Google Scholar
Xylander W.E.R. 1989. Ultrastructural studies on the reproductive system of Gyrocotylidea and Amphilinidea (Cestoda): Spermatogenesis, spermatozoa, testes and vas deferens of Gyrocotyle. International Journal for Parasitology, 19, 897-905. DOI: 10.1016/0020-7519(89)90117-3 10.1016/0020-7519(89)90117-3Search in Google Scholar
© 2016
Articles in the same Issue
- Toxocarosis of the organ of sight – the complex pathological and diagnostic problem
- Trichomonas vaginalis: An Updated Overview Towards Diagnostic Improvement
- New species and records of mites of the superfamily Sarcoptoidea (Acariformes: Psoroptidia) from mammals in Brazil
- The morphology of free-living stages and immature parasites of Rhabdias paraensis (Nematoda: Rhabdiasidae), a parasite of Rhinella marina (Anura: Bufonidae) in Brazil
- Effects of altered water quality and trace elements on the infection variables of Paradiplozoon ichthyoxanthon (Monogenea: Diplozoidae) from two sites in the Vaal River system, South Africa
- Herd-level seroprevalence of Neospora caninum infection in dairy cattle in central and northeastern Poland
- Ultrastructure of Ascaridia galli (Schrank, 1788) (Nematoda: Ascaridida) from the endangered green peafowl Pavo muticus Linnaeus (Galliformes: Phasianidae)
- Prevalence and risk factors associated to Eimeria spp. infection in unweaned alpacas (Vicugna pacos) from Southern Peru
- Description of a new species of Chabaudus Inglis and Ogden, 1965 (Nematoda: Seuratoidea) from the frog Euphlyctis cyanophlyctis from Dehrandun, Uttarakhand, India
- Fertilization in the cestode Echinococcus multilocularis (Cyclophyllidea, Taeniidae)
- Expression analysis of viscerotropic leishmaniasis gene in Leishmania species by real-time RT-PCR
- Fourier transform infrared spectroscopy as a tool for identification of crude microbial extracts with anti-malarial potential
- A 43 kDa recombinant plasmepsin elicits immune response in mice against Plasmodium berghei malaria
- Effects of Echinostoma caproni miracidia dose on the amino acid contents of Biomphalaria glabrata as determined by high-performance thin-layer chromatography
- In search of a potential diagnostic tool for molecular characterization of lymphatic filariasis
- Seasonal pattern in parasite infracommunities of Hoplerythrinus unitaeniatus and Hoplias malabaricus (Actinopterygii: Erythrinidae) from the Brazilian Amazon
- The first detection of the tick-borne encephalitis virus (TBEV) RNA in Dermacentor reticulatus ticks collected from the lowland European bison (Bison bonasus bonasus L.)
- Assessing the influence of geographic distance in parasite communities of an exotic lizard
- Diagnostic value of semi-purified antigens of hydatid cyst fluid in human cystic echinococcosis
- Occurrence and morphogenetic characteristics of Gyrodactylus (Monogenea: Gyrodactylidae) from a rainbow trout farm (Lake Ladoga, Russia)
- Dactylogyrids (Monogenea) parasitic on cichlids from northern Brazil, with description of two new species of Sciadicleithrum and new host and geographical records
- Molecular detection and prevalence of feline hemotropic mycoplasmas in Istanbul, Turkey
- First report of Cystoisospora belli parasitemia in a patient with acquired immunodeficiency syndrome
- Cystic echinococcosis in Southern Israel
- Larval cestodes infecting the deep-water fish, Cataetyx laticeps (Pisces: Bythitidae) from Madeira Archipelago, Atlantic Ocean
- Toxocara canis glycans influence antigen recognition by mouse IgG1 and IgM antibodies
- Phylogenetic relationships among Linguatula serrata isolates from Iran based on 18S rRNA and mitochondrial cox1 gene sequences
- The transstadial persistence of tick-borne encephalitis virus in Dermacentor reticulatus ticks in natural conditions
Articles in the same Issue
- Toxocarosis of the organ of sight – the complex pathological and diagnostic problem
- Trichomonas vaginalis: An Updated Overview Towards Diagnostic Improvement
- New species and records of mites of the superfamily Sarcoptoidea (Acariformes: Psoroptidia) from mammals in Brazil
- The morphology of free-living stages and immature parasites of Rhabdias paraensis (Nematoda: Rhabdiasidae), a parasite of Rhinella marina (Anura: Bufonidae) in Brazil
- Effects of altered water quality and trace elements on the infection variables of Paradiplozoon ichthyoxanthon (Monogenea: Diplozoidae) from two sites in the Vaal River system, South Africa
- Herd-level seroprevalence of Neospora caninum infection in dairy cattle in central and northeastern Poland
- Ultrastructure of Ascaridia galli (Schrank, 1788) (Nematoda: Ascaridida) from the endangered green peafowl Pavo muticus Linnaeus (Galliformes: Phasianidae)
- Prevalence and risk factors associated to Eimeria spp. infection in unweaned alpacas (Vicugna pacos) from Southern Peru
- Description of a new species of Chabaudus Inglis and Ogden, 1965 (Nematoda: Seuratoidea) from the frog Euphlyctis cyanophlyctis from Dehrandun, Uttarakhand, India
- Fertilization in the cestode Echinococcus multilocularis (Cyclophyllidea, Taeniidae)
- Expression analysis of viscerotropic leishmaniasis gene in Leishmania species by real-time RT-PCR
- Fourier transform infrared spectroscopy as a tool for identification of crude microbial extracts with anti-malarial potential
- A 43 kDa recombinant plasmepsin elicits immune response in mice against Plasmodium berghei malaria
- Effects of Echinostoma caproni miracidia dose on the amino acid contents of Biomphalaria glabrata as determined by high-performance thin-layer chromatography
- In search of a potential diagnostic tool for molecular characterization of lymphatic filariasis
- Seasonal pattern in parasite infracommunities of Hoplerythrinus unitaeniatus and Hoplias malabaricus (Actinopterygii: Erythrinidae) from the Brazilian Amazon
- The first detection of the tick-borne encephalitis virus (TBEV) RNA in Dermacentor reticulatus ticks collected from the lowland European bison (Bison bonasus bonasus L.)
- Assessing the influence of geographic distance in parasite communities of an exotic lizard
- Diagnostic value of semi-purified antigens of hydatid cyst fluid in human cystic echinococcosis
- Occurrence and morphogenetic characteristics of Gyrodactylus (Monogenea: Gyrodactylidae) from a rainbow trout farm (Lake Ladoga, Russia)
- Dactylogyrids (Monogenea) parasitic on cichlids from northern Brazil, with description of two new species of Sciadicleithrum and new host and geographical records
- Molecular detection and prevalence of feline hemotropic mycoplasmas in Istanbul, Turkey
- First report of Cystoisospora belli parasitemia in a patient with acquired immunodeficiency syndrome
- Cystic echinococcosis in Southern Israel
- Larval cestodes infecting the deep-water fish, Cataetyx laticeps (Pisces: Bythitidae) from Madeira Archipelago, Atlantic Ocean
- Toxocara canis glycans influence antigen recognition by mouse IgG1 and IgM antibodies
- Phylogenetic relationships among Linguatula serrata isolates from Iran based on 18S rRNA and mitochondrial cox1 gene sequences
- The transstadial persistence of tick-borne encephalitis virus in Dermacentor reticulatus ticks in natural conditions
