Ultrastructural characteristics of the reproductive organs of adult male helminth Heterakis dispar (Nematoda: Heterakidae)
Keywords:
Heterakis dispar; adult male nematode; reproductive organs; ultrastructure; transmission electron microscope
Abstract
Nematodes belonging to the Heterakidae family are similar in appearance and their identification causes certain difficulties. For this reason, there is a need to define new taxonomic characteristics. On the other hand, despite the fact that the nematode Heterakis dispar Schrank, 1790, included in the same family, has a wide distribution area, there is little information about the ultrastructure of the parasite. Research on the ultrastructure of the reproductive system of this helminth hase not been conducted. Parasitic worms collected from the caeca of birds were identified, following which, based on the accepted methods of electron microscopy, blocks were prepared, cut, stained, pictures and electrograms were prepared and described. In the present study, the ultrastructural characteristics of the reproductive organs (testis, seminal vesicle, vas deferens and ejaculatory duct) of the adult nematode H. dispar, a specific parasite of domestic waterfowl, were studied with the help of light and electron microscopic methods. The obtained results were compared with the structure of other studied species (H. gallinarum Gmelin, 1790 and H. spumosa Schneider, 1866) of the Heterakidae family. Firstly, it was revealed that the reproductive organs of the male nematode H. dispar are located in the pseudocoelomic cavity, which is considered a taxonomic sign of this family. As in other species of the family, the testis, seminal vesicle, and wall of the vas deferens of the male nematode H. dispar consist of a basement membrane and an epithelial layer. In addition to the basement membrane, muscular and epithelial layers, the wall of the ejaculatory duct is also composed of glandular cells in the front part of the duct. It was revealed that, in the lumen of the tubular reproductive organs of the adult male nematode H. dispar, germ-cells turn into spermatogonia in the germinal zone and spermatocytes in the growth zone of the testis, spermatids in the seminal vesicle, incomplete formed spermatozoa in the vas deferens, and fully formed spermatozoa in the ejaculatory duct of the parasite. The spicules of the parasite nematode, which are the secondary sexual organs consist of a thick cuticle on the outside, and hypodermal origin cells and processes of nerve cells (dendrites and axons) on the inside. Two processes are found on the spicules, which is not observed in other nematodes of the same family.References
Afanasiev-Grigoriev, A. G., & Yushin, V. V. (2009). Electron microscopic study of spermiogenesis in the free-living marine nematode Leptosomatides marinae Platonova, 1976 (Enoplida: Leptosomatidae). Russian Journal of Marine Biology, 35(20), 156–163.
Agayeva, N. J., Rzayev, F. H., Gasimov, E. K., Mamedov, C. A., Ahmadov, I. S., Sadigova, N. A., Khusro, A., Al-Dhabi, N. A., & Arasu, M. V. (2020). Exposure of rainbow trout (Oncorhynchus mykiss) to magnetite (Fe3O4) nanoparticles in simplified food chain: Study on ultra-structural characterization. Saudi Journal of Biological Sciences, 27(2), 3258–3266.
Baker, A. (1973). Studies of Heterakis gallinarum (Gmelin, 1970) Freeborn, 1923 a nematode parasite of domestic fowls. Transactions of the Royal Canadian Institute, 21, 31–86.
Baran, M. (2011). Nematodes reproductive system. Parasitology, 7, 163.
Basyoni, M. M. A., & Rizk, E. M. A. (2016). Nematodes ultrastructure: Complex systems and processes. Journal of Parasitic Diseases, 40(4), 1130–1140.
Bird, F. A., & Bird, J. (1991). The structure of Nematodes. 2nd edition. Academic Press, San Diego.
Bobrek, K., Hildebrand, J., Urbanowicz, J., & Aweł, A. (2019). Molecular identification and phylogenetic analysis of Heterakis dispar isolated from Geese. Acta Parasitologica, 64, 753–760.
Bogoyavlensky, Y. K., Bogolepova, I. I., & Onushko, N. V. (1982). Mikrostruktura tkaney paraziticheskikh nematod [Microstructure of tissues of parasitic nematodes]. Nauka, Moscow (in Russian).
Bogoyavlensky, Y. K., Onushko, N. V., & Andreeva, A. M. (1978). Mikromorfologichekaya organizatsiya polovoy sistemy samtsov nematod [Micromorphological organization of the genital system of male nematodes]. Proceedings of Helminthological Laboratory of the Academy of Sciences, 28, 193–199.
Borah, N., Phukan, S. C., Islam, S., Tamuli, S., Tamuli, S. M., & Rajbongshi, P. (2018). Prevalence of helminth parasites of domestic ducks in Upper Assam (India). International Journal of Chemical Studies, 6(4), 131–134.
Croll, N. A., & Wright, K. A. (1976). Observations on the movements and structure of the bursa of Nippostrongylus brasiliensis and Nematospiroides dubius. Canadian Journal of Zoology, 54, 1466–1480.
D’Amico, F. (2005). A polychromatic staining method for epoxy embedded tissue: A new combination of methylene blue and basic fuchsine for light microscopy. Biotechnic and Histochemestry, 80(5–6), 207–210.
Dubinina, M. N. (1971). Parazitologicheskoe issledovaniye ptits. Metody parazitologicheskikh issledovanij [Parasitological study of birds. Methods of parasitological research]. Leningrad, Nauka (in Russian).
Elshahawy, I., El-Siefy, M., Fawy, S., & Mohammed, E. (2021). Epidemiological studies on nematode parasites of domestic geese (Anser anser f. domesticus) and first molecular identification and phylogenetic analysis of Heterakis dispar (Schrank, 1790) in Egypt. Acta Parasitologica, 66, 1297–1306.
Geo, J. F., Hou, M. R., Wang, W. F., Geo, Z. Y., Zhang, X. G., Lu, Y. X., & Shi, T. R. (2019). The complete mitochondrial genome of Heterakis dispar (Ascaridida: Heterakidae). Mitochondrial DNA, part B, 4(1), 1630–1631.
Hulinska, D. (1968). The development of the male Enterobius vermicularis and the morphological of its sexual organ. Folia Parasitologica, 15(1), 15–28.
Kuo, J. (2014). Electron microscopy: Methods and protocols. Humana Press, Totowa.
Lee, D. L. (1973). Evidence for a sensory function for the copulatory spicules of nematodes. Journal of Zoology, 169, 281–285.
Mehlhorn, H., & Harder, A. (1997). Effects of the synergistic action of febantel and pyrantel on the nematode Heterakis spumosa: A light and transmission electron microscopy study. Parasitology Research, 83, 419–434.
Nasirov, A. M., Bunyatova, K. I., Kaziyeva, N. S., & Rzayev, F. H. (2008). Mikromorfologiya tkaney nematody Ganguleterakis dispar (Schrank, 1790) [Micromorphology of tissues of the nematode Ganguleterakis dispar (Schrank, 1790)]. In: Galaktionov, K. V., & Dobrovolskij, A. A. (Eds.). Parasitology in the XXI century – problems, methods, solutions. Lemma, Saint Petersburg, 208–210 (in Russian).
Rammah, A., & Hirschmann, H. (1987). Morphological comparison and taxonomic utility of copulatory structures of selected nematode species. Journal of Nematology, 19(3), 314–323.
Rukambile, E. J., Chengula, A., Swai, E. S., & Jongejan, F. (2020). Poultry ecto-, endo- and haemoparasites in Tanzania: A review. Austin Journal of Veterinary Science and Animal Husbandry, 7(1), 1066.
Ryzhikov, K. M. (1967). Opredelitel’ gel’mintov domashnikh vodoplavayushchikh ptits [Keys to helminths of domestic waterfowl]. Nauka, Moscow (in Russian).
Rzayev, F. H. (2010). To studying of morphology of nematode Ganguleterakis dispar (Schrank, 1790). News of Azerbaijan National Academy of Science, 65(1–2), 141–146.
Rzayev, F. H. (2021) Cestodes (Plathelminthes: Cestoda) of domestic waterfowl. Advances in Biology and Earth Sciences, 6(2), 133–141.
Rzayev, F. H. (2023a). Helminths of domestic waterfowl of Azerbaijan and influence on them of plants with anthelmintic properties. Zangazurda, Baku.
Rzayev, F. H. (2023b). Ultrastructural features of the digestive system of the helminth Heterakis dispar Schrank, 1790 (Nematoda: Heterakidae). Egyptian Journal of Veterinary Sciences, 54(3), 503–514.
Rzayev, F. H., Nasirov, A. M., & Gasimov, E. K. (2021). A systematic review of tapeworms (Plathelminthes, Cestoda) of domestic ducks (Anas platyrhynchos dom.). Regulatory Mechanisms in Biosystems, 12(2), 353–361.
Slos, D., Yushin, V. V., Claeys, M., Ivanova, E. S., Kosaka, H., & Bert, W. (2020). Structure, development, and evolutive patterns of spermatozoa in rhabditid nematodes (Nematoda: Rhabditida). Journal of Morphology, 281(11), 1411–1435.
Wright, K. A. (1978). Structure and function of the male copulatory apparatus of the nematodes Capillaria hepatica and Trichuris muris. Canadian Journal of Zoology, 56, 651–662.
Yevstafieva, V., Yeresko, V., Melnychuk, V., & Bakhur, T. (2020). Prevalence and co-infection of Baruscapillaria genus (Nematoda, Capillariidae) in domestic geese in Ukraine. Folia Veterinaria, 64(1), 32–38.
Yevstafieva, V., Kanivets, N., Melnichuk, V., & Kravchenko, S. (2022). Monitoring shlunkovo-kishkovykh parazitoziv vodoplanoj ptytsi u sviti [Monitoring of gastrointestinal parasitoses of waterfowl in the world]. Bulletin of Poltava State Agrarian Academy, 3, 117–123 (in Ukrainian).
Yushin, V. V., Afanasiev-Grigoriev, A. G., & Malakhov, V. V. (2014). The male gonad of the marine nematode Enoplus: No single distal tip cell but multiple uniform epithelial cells. Invertebrate Zoology, 11(2), 361–372.
Yushin, V. V., Claeys, M., Leunissen, J. L. M., & Zograf, J. K. (2021). Electron microscopy techniques. In: Perry, R. N., Hunt, D. J., & Subbotin, S. A. (Eds.). Techniques for work with plant and soil nematodes. Boston, CABI. Pp. 152–176.
Yushin, V. V., & Malakhov, V. V. (2014). The origin of nematode sperm: Progenesis at the cellular level. Russian Journal of Marine Biology, 40(2), 71–81.
Yushin, V. V., & Ryss, A. Y. (2011). Sperm development and structure in Bursaphelenchus mucronatus (Nematoda: Aphelenchoidea: Aphelenchoididae). Nematology, 13(4), 395–407.
Zhang, S., Bu, Y., Huang, G., Wen, Q., & Zhang, L. (2012). A checklist of parasitic nematodes (Nematoda) from birds (Aves) in China. Zootaxa, 3446, 1–31.
Agayeva, N. J., Rzayev, F. H., Gasimov, E. K., Mamedov, C. A., Ahmadov, I. S., Sadigova, N. A., Khusro, A., Al-Dhabi, N. A., & Arasu, M. V. (2020). Exposure of rainbow trout (Oncorhynchus mykiss) to magnetite (Fe3O4) nanoparticles in simplified food chain: Study on ultra-structural characterization. Saudi Journal of Biological Sciences, 27(2), 3258–3266.
Baker, A. (1973). Studies of Heterakis gallinarum (Gmelin, 1970) Freeborn, 1923 a nematode parasite of domestic fowls. Transactions of the Royal Canadian Institute, 21, 31–86.
Baran, M. (2011). Nematodes reproductive system. Parasitology, 7, 163.
Basyoni, M. M. A., & Rizk, E. M. A. (2016). Nematodes ultrastructure: Complex systems and processes. Journal of Parasitic Diseases, 40(4), 1130–1140.
Bird, F. A., & Bird, J. (1991). The structure of Nematodes. 2nd edition. Academic Press, San Diego.
Bobrek, K., Hildebrand, J., Urbanowicz, J., & Aweł, A. (2019). Molecular identification and phylogenetic analysis of Heterakis dispar isolated from Geese. Acta Parasitologica, 64, 753–760.
Bogoyavlensky, Y. K., Bogolepova, I. I., & Onushko, N. V. (1982). Mikrostruktura tkaney paraziticheskikh nematod [Microstructure of tissues of parasitic nematodes]. Nauka, Moscow (in Russian).
Bogoyavlensky, Y. K., Onushko, N. V., & Andreeva, A. M. (1978). Mikromorfologichekaya organizatsiya polovoy sistemy samtsov nematod [Micromorphological organization of the genital system of male nematodes]. Proceedings of Helminthological Laboratory of the Academy of Sciences, 28, 193–199.
Borah, N., Phukan, S. C., Islam, S., Tamuli, S., Tamuli, S. M., & Rajbongshi, P. (2018). Prevalence of helminth parasites of domestic ducks in Upper Assam (India). International Journal of Chemical Studies, 6(4), 131–134.
Croll, N. A., & Wright, K. A. (1976). Observations on the movements and structure of the bursa of Nippostrongylus brasiliensis and Nematospiroides dubius. Canadian Journal of Zoology, 54, 1466–1480.
D’Amico, F. (2005). A polychromatic staining method for epoxy embedded tissue: A new combination of methylene blue and basic fuchsine for light microscopy. Biotechnic and Histochemestry, 80(5–6), 207–210.
Dubinina, M. N. (1971). Parazitologicheskoe issledovaniye ptits. Metody parazitologicheskikh issledovanij [Parasitological study of birds. Methods of parasitological research]. Leningrad, Nauka (in Russian).
Elshahawy, I., El-Siefy, M., Fawy, S., & Mohammed, E. (2021). Epidemiological studies on nematode parasites of domestic geese (Anser anser f. domesticus) and first molecular identification and phylogenetic analysis of Heterakis dispar (Schrank, 1790) in Egypt. Acta Parasitologica, 66, 1297–1306.
Geo, J. F., Hou, M. R., Wang, W. F., Geo, Z. Y., Zhang, X. G., Lu, Y. X., & Shi, T. R. (2019). The complete mitochondrial genome of Heterakis dispar (Ascaridida: Heterakidae). Mitochondrial DNA, part B, 4(1), 1630–1631.
Hulinska, D. (1968). The development of the male Enterobius vermicularis and the morphological of its sexual organ. Folia Parasitologica, 15(1), 15–28.
Kuo, J. (2014). Electron microscopy: Methods and protocols. Humana Press, Totowa.
Lee, D. L. (1973). Evidence for a sensory function for the copulatory spicules of nematodes. Journal of Zoology, 169, 281–285.
Mehlhorn, H., & Harder, A. (1997). Effects of the synergistic action of febantel and pyrantel on the nematode Heterakis spumosa: A light and transmission electron microscopy study. Parasitology Research, 83, 419–434.
Nasirov, A. M., Bunyatova, K. I., Kaziyeva, N. S., & Rzayev, F. H. (2008). Mikromorfologiya tkaney nematody Ganguleterakis dispar (Schrank, 1790) [Micromorphology of tissues of the nematode Ganguleterakis dispar (Schrank, 1790)]. In: Galaktionov, K. V., & Dobrovolskij, A. A. (Eds.). Parasitology in the XXI century – problems, methods, solutions. Lemma, Saint Petersburg, 208–210 (in Russian).
Rammah, A., & Hirschmann, H. (1987). Morphological comparison and taxonomic utility of copulatory structures of selected nematode species. Journal of Nematology, 19(3), 314–323.
Rukambile, E. J., Chengula, A., Swai, E. S., & Jongejan, F. (2020). Poultry ecto-, endo- and haemoparasites in Tanzania: A review. Austin Journal of Veterinary Science and Animal Husbandry, 7(1), 1066.
Ryzhikov, K. M. (1967). Opredelitel’ gel’mintov domashnikh vodoplavayushchikh ptits [Keys to helminths of domestic waterfowl]. Nauka, Moscow (in Russian).
Rzayev, F. H. (2010). To studying of morphology of nematode Ganguleterakis dispar (Schrank, 1790). News of Azerbaijan National Academy of Science, 65(1–2), 141–146.
Rzayev, F. H. (2021) Cestodes (Plathelminthes: Cestoda) of domestic waterfowl. Advances in Biology and Earth Sciences, 6(2), 133–141.
Rzayev, F. H. (2023a). Helminths of domestic waterfowl of Azerbaijan and influence on them of plants with anthelmintic properties. Zangazurda, Baku.
Rzayev, F. H. (2023b). Ultrastructural features of the digestive system of the helminth Heterakis dispar Schrank, 1790 (Nematoda: Heterakidae). Egyptian Journal of Veterinary Sciences, 54(3), 503–514.
Rzayev, F. H., Nasirov, A. M., & Gasimov, E. K. (2021). A systematic review of tapeworms (Plathelminthes, Cestoda) of domestic ducks (Anas platyrhynchos dom.). Regulatory Mechanisms in Biosystems, 12(2), 353–361.
Slos, D., Yushin, V. V., Claeys, M., Ivanova, E. S., Kosaka, H., & Bert, W. (2020). Structure, development, and evolutive patterns of spermatozoa in rhabditid nematodes (Nematoda: Rhabditida). Journal of Morphology, 281(11), 1411–1435.
Wright, K. A. (1978). Structure and function of the male copulatory apparatus of the nematodes Capillaria hepatica and Trichuris muris. Canadian Journal of Zoology, 56, 651–662.
Yevstafieva, V., Yeresko, V., Melnychuk, V., & Bakhur, T. (2020). Prevalence and co-infection of Baruscapillaria genus (Nematoda, Capillariidae) in domestic geese in Ukraine. Folia Veterinaria, 64(1), 32–38.
Yevstafieva, V., Kanivets, N., Melnichuk, V., & Kravchenko, S. (2022). Monitoring shlunkovo-kishkovykh parazitoziv vodoplanoj ptytsi u sviti [Monitoring of gastrointestinal parasitoses of waterfowl in the world]. Bulletin of Poltava State Agrarian Academy, 3, 117–123 (in Ukrainian).
Yushin, V. V., Afanasiev-Grigoriev, A. G., & Malakhov, V. V. (2014). The male gonad of the marine nematode Enoplus: No single distal tip cell but multiple uniform epithelial cells. Invertebrate Zoology, 11(2), 361–372.
Yushin, V. V., Claeys, M., Leunissen, J. L. M., & Zograf, J. K. (2021). Electron microscopy techniques. In: Perry, R. N., Hunt, D. J., & Subbotin, S. A. (Eds.). Techniques for work with plant and soil nematodes. Boston, CABI. Pp. 152–176.
Yushin, V. V., & Malakhov, V. V. (2014). The origin of nematode sperm: Progenesis at the cellular level. Russian Journal of Marine Biology, 40(2), 71–81.
Yushin, V. V., & Ryss, A. Y. (2011). Sperm development and structure in Bursaphelenchus mucronatus (Nematoda: Aphelenchoidea: Aphelenchoididae). Nematology, 13(4), 395–407.
Zhang, S., Bu, Y., Huang, G., Wen, Q., & Zhang, L. (2012). A checklist of parasitic nematodes (Nematoda) from birds (Aves) in China. Zootaxa, 3446, 1–31.
Published
2023-05-22
Issue
Section
Articles
This work is licensed under a Creative Commons Attribution 4.0 International License.
