Life cycle of Bilharziella polonica (Trematoda, Schistosomatidae) parasite of semi-aquatic birds in Uzbekistan
Keywords:
eggs; miracidia; sporocysts; cercariae; molluscs; intermediate hosts; definitive hosts
Abstract
Schistosomatidae are an actively studied ecological group of trematodes. Their ability to cause various parasitic diseases in animals and humans makes them an interesting object of study for a number of research centres worldwide. One of the commonest species in this group is Bilharziella polonica (Kowalewsky, 1895), whose mature stages have been recorded in aquatic and semi-aquatic birds in Uzbekistan. Our research team established that the following birds were infected with mature trematodes B. polonica: Anas platyrhynchos (23%), A. crecca (18%), Podiceps ruficollis (11%), Ardea cinerea (14%) and one individual of Oxyura leucocephala. The highest infection rate was shown by the mallard A. platyrhynchos (23%) and common teal A. crecca (18%). The infection intensity ranged between 2 and 27 individuals. Research into various types of water bodies in Karakalpakstan identified 10 mollusc species – Lymnaeidae (4 species), Planorbidae (4 species) and Physidae (2 species). Cercariae morphologically similar to larvae of B. polonica were found in two species, Planorbis planorbis and P. tangitarensis. 6 chicks of domestic ducks were experimentally infected with those cercariae to track the life cycle of B. polonica in the organism of a definitive host. Helmintholological dissections showed that every duck was infected with B. polonica, which became mature 23–27 days after the infection. Eggs of B. polonica were recorded in the excrement of one of the birds 33–35 days after the infection. Based on field and experimental research, we identify the mollusc P. tangitarensis as a new intermediate host for B. polonica in Uzbekistan.References
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Akimova, L. N. (2014). Analiz uchastiya vodnykh bryukhonogikh mollyuskov v tsirkulyatsii digeney (Trematoda: Digenea) na territorii Belorusi [Analysis of the participation of aquatic gastropods in the circulation of digeneans (Trematoda: Digenea) on the territory of Belarus]. In: Proceedings of the Center for Parasitology of the Institute of Ecology and Evolution A. N. Severtsev. Moscow. Vol. 48. Pp. 10–12 (in Russian).
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Aristanov, E. (1968). Furkotserkarii iz presnovodnykh mollyuskov del’ty Amudaryi [Furcocercariae from freshwater molluscs of the Amudarya delta]. Bulletin of Leningrad University, 9(2), 79–88 (in Russian).
Azimov, D. A. (1975). Shistosomatidy zhivotnykh i cheloveka [Schistosomatids of animals and humans]. Tashkent, Fan (in Russian).
Bayssade-Dufour, C., Jouet, D., Rudolfova, J., Horák, P., & Ferté, H. (2006). Seasonal morphological variations in bird schistosomes. Parasite, 13, 205–214.
Butenko, Y. V. (1967). Zarazhennost molliuskov vodoyemov Yuzhnogo Kazakhstana lichinkami trematod [Infection of mollusks in reservoirs of Southern Kazakhstan with trematode larvae]. In: Collection of scientific work Institute of Zoology of the Academy of Sciences of the Kazakh USSR “Helminths and helminthiases of animals in Kazakhstan”. Alma-Ata. Pp. 22–52 (in Russian).
Bykhovskaya-Pavlovskaya, I. E., & Ryzhikov, K. M. (1958). Shistozomatidy gusinykh ptits Yakutii [Schistosomatids of geese of Yakutia]. Parasitological Collection Zoological Institute of the Academy of Sciences, 18, 283–294 (in Russian).
Chauhan, A. S., Srivastava, C. B., & Chauhan, B. S. (1974). Studies on the trematoda fauna of India, 6. Digenea: Schistosomatidae. A monographic aid to the identification of Indian schistosomes. Journal of the Zoological Society of India, 25, 83–127.
Chrisanfova, G. G., Heidorova, E. E., Shestak, A. G., Lopatkin, A. A., Bychkova, E. I., & Semenova, S. K. (2010). Geneticheskaya izmenchivost ptichikh shistosom Bilharziella polonica (Trematod: Schistosomatidae) ozera Naroch [Genetic variability of bird schistosomes Bilharziella polonica (Trematode: Schistosomatidae) from Lake Naroch. In: Theoretical and practical problems of parasitology. Moscow. Pp. 398–402 (in Russian).
Chrisanfova, G. G., Lopatkin, A. A., Mishchenkov, V. A., Kheidorova, E. E., Dorozhenkova, T. E., Zhukova, T. V., Ryskov, A. P., & Semyenova, S. K. (2009). Genetic variability of bird schistosomes (class Trematoda, family Schistosomatidae) of Naroch Lake: Identification of a new species in the Trichobilharzia ocellata group. Doklady Biochemistry and Biophysics, 428, 268–272 (in Russian).
Dubinina, M. N. (1971). Parazitologicheskoye issledovaniye ptits [Parasitological study of birds]. Nauka, Leningrad (in Russian).
Farley, J. A. (1971). Review of the family Schistosomatidae: Excluding the genus Schistosoma from mammals. Journal of Helminthology, 45, 289–320.
Fillimonova, L. V. (1985). Trematody fauny SSSR. Notokotilidy [Trematodes of the fauna of the USSR. Notocotylides]. Nauka, Moscow (in Russian).
Ginetsinskaya, T. A. (1968). Trematody, ikh zhiznennyye tsikly, biologiya i evolyutsiya [Trematodes, their life cycles, biology and evolution]. Nauka, Leningrad (in Russian).
Ginetsinskaya, T. A., & Dobrovolsky, A. A. (1963). Novyy metod obnaruzheniya sensill lichinok trematod i znacheniye etikh obrazovaniy dlya sistematiki [A new method for detecting sensilla of trematode larvae and the significance of these formations for taxonomy]. Doklady Academy of Sciences of the USSR, 151(2), 460–463 (in Russian).
Horák, P., & Kolárová, L. (2000). Survival of bird schistosomes in mammalian lungs. International Journal for Parasitology, 30, 65–68.
Jadin, V. I. (1952). Mollyuski presnykh i solonovatykh vod SSSR. Opredeliteli po faune SSSR [Shellfish fresh and brackish waters of the USSR. Keys to the fauna of the USSR]. Academy of Sciences of the USSR, Moscow, Leningrad (in Russian).
Kahlil, L. F. (2002). Family Schistosomatidae Stiles and Hassal, 1898. In: Gibson, A., Jones, A., & Bray, R. A. Keys to the Trematoda. Vol. I. CAB Publishing, London. Pp. 419–432.
Khalifa, R. (1972). Studies on Schistosomatidae Looss, 1899 (Trematoda) of aquatic bird of Poland. I. On the cycle of Bilharziella polonica Kowalesski, 1895, with a discussion of the subfamily Bilharziellinae Price, 1929. Acta Parasitologica Polonica, 20, 343–365.
Kolárová, L., Gottwaldová, V., Cechová, D., & Sevcová, M. (1989). The occurence of cercarial dermatitis in Central Bohemia. Zentrablatt und Hygiene, 189, 1–13.
Kotelnikov, G. A. (1976). Diagnostika gel’mintozov zhivotnykh [Diagnosis of helminthiases in animals]. Kolos, Moscow (in Russian).
Kowalewski, L. (1895). Bilharziella polonica sp. nov. (Studya helmintologiczne 3). Rozprawy Wydzialu Matematyczno-Przyrodniczego Polskiej Akademii Umiejetnosci, Krakow, 31, 41–70.
Kreysberg-Mukhina, Y. A., Kashkarov, D. Y., Lanovenko, Y. N., Shernazarov, E. S., & Peregonsev, Y. A. (2005). Ptitsy vodoyemov Uzbekistana i Tsentral’no-Aziaskogo regiona. Polevoy opredelitel’ vodno-bolotnykh ptits [Birds of water bodies of Uzbekistan and the Central Asian region. Field guide to wetland birds]. Nauka, Tashkent, Alma-Aty (in Russian).
Litvienko, N. T. (1963). Opyty po vyyasneniyu promezhutochnykh khozyayev vozbuditelya bil’khartsiyelleza domashnikh utok [Experiments to identify the intermediate hosts of the causative agent of bilharziellosis in the domestic duck]. Proceedings of Kharkov Zooveterinary Institut, 25, 71–74 (in Russian).
Palm, V. (1965). Ein Beitrag zur Helminthenfauna des Blesshuhns (Fulica atra L.) aus dem Raum von Postdam. Acta Parasitologica Polonica, 13, 425–444.
Shakarbaev, U., Akramova, F., & Azimov, D. (2020). The taxonomic survey of the fauna of cercariae (Platyhelminthes, Trematoda) in the mollusks of Uzbekistan. Zoodiversity, 54(6), 505–522.
Skrjabin, K. I. (1928). Metody polnykh gel’mintologicheskikh vskrytiy pozvonochnykh, vklyuchaya i cheloveka [Methods of complete helminthological dissections of vertebrates, including humans]. Publishing House of Moscow State University, Moscow (in Russian).
Skrjabin, K. I. (1951). Trematody zhivotnykh i cheloveka. Osnovy trematodologii [Trematodes of animals and humans. Fundamentals of trematodology]. Academy of Sciences of the USSR, Moscow (in Russian).
Sulgostowska, T. (1972). Trematodes of the mute swan Cygnus olor from central and northern regions of Poland. Acta Parasitologica Polonica, 20, 473–481.
Szidat, L. (1929). Die Parasiten des Hausgeflügels. 3 Bilharziella polonica Kow. ein im Blut Schmarotzender Trematode unserer Enten, seine Entwicklung und Ubertragung. Archiv für Geflügelkude, 3, 78–87.
Szidat, L. (1930). Uber Hautinfektionen bei Bluttrematoden insbesondere bei Bilharziella polonica Kow. Archiv für Dermatologie und Syphilis, 160, 304–308.
Vergun, G. I. (1856). K faune lichinok trematod nekotorykh molliuskov v rayone srednego technija r Donec [On the fauna of the trematod larvae of small molluscs in the area of the Middle Donec]. Problemy Parazitologii, 2, 30–32 (in Slovak).
Wiśniewski, L. W. (1958). Characterization of the parasitofauna of aneutrophic lake (Parasitofauna of the biocoenosis of Druzno Lake, part 1). Acta Parasitologica, 6, 1–64.
Yamaguti, S. (1971). Synopsis of digenetic trematodes of vertebrates. Keigaku, Tokyo.
Zbikowska, E. (2002). Is there a potential danger of “swimmer’s itch” in Poland? Parasitology Research, 89, 59–62.
Zbikowska, E. (2004). Infection of snails with bird schistosomes and the threat of swimmer’s itch in selected Polish lakes. Parasitology Research, 92, 30–35.
Zbikowska, E., & Nowak, A. (2009). One hundred years of research on the natural infection of freshwater snails by trematode larvae in Europe. Parasitology Research, 105(2), 301–311.
Ždárská, Z. (1963). Larvální stadia motolic z vodních plžů na území ČSSR (Larval trematodes of fresh-water snails in Czechoslovakia) [Larval stages of water snails in the Czechoslovak Republic (Larval trematodes of fresh-water snails in Czechoslovakia)]. Československá Parasitologie, 10, 207–262 (in Czech).
Zdun, W. (1959). Cercariae from Coretus corneus (L.) in the environments of Warszawa. Acta Parasitologica, 7, 95–115.
Akimova, L. N. (2014). Analiz uchastiya vodnykh bryukhonogikh mollyuskov v tsirkulyatsii digeney (Trematoda: Digenea) na territorii Belorusi [Analysis of the participation of aquatic gastropods in the circulation of digeneans (Trematoda: Digenea) on the territory of Belarus]. In: Proceedings of the Center for Parasitology of the Institute of Ecology and Evolution A. N. Severtsev. Moscow. Vol. 48. Pp. 10–12 (in Russian).
Akramova, F. D. (2011). Trematody bil’gartsiyellidy, ikh proiskhozhdeniya i evolyutsiya [Bilharzia trematodes, their origin and evolution]. Institute of Zoology of Academy of Sciences of the Republic of Uzbekistan, Tashkent (in Russian).
Aristanov, E. (1968). Furkotserkarii iz presnovodnykh mollyuskov del’ty Amudaryi [Furcocercariae from freshwater molluscs of the Amudarya delta]. Bulletin of Leningrad University, 9(2), 79–88 (in Russian).
Azimov, D. A. (1975). Shistosomatidy zhivotnykh i cheloveka [Schistosomatids of animals and humans]. Tashkent, Fan (in Russian).
Bayssade-Dufour, C., Jouet, D., Rudolfova, J., Horák, P., & Ferté, H. (2006). Seasonal morphological variations in bird schistosomes. Parasite, 13, 205–214.
Butenko, Y. V. (1967). Zarazhennost molliuskov vodoyemov Yuzhnogo Kazakhstana lichinkami trematod [Infection of mollusks in reservoirs of Southern Kazakhstan with trematode larvae]. In: Collection of scientific work Institute of Zoology of the Academy of Sciences of the Kazakh USSR “Helminths and helminthiases of animals in Kazakhstan”. Alma-Ata. Pp. 22–52 (in Russian).
Bykhovskaya-Pavlovskaya, I. E., & Ryzhikov, K. M. (1958). Shistozomatidy gusinykh ptits Yakutii [Schistosomatids of geese of Yakutia]. Parasitological Collection Zoological Institute of the Academy of Sciences, 18, 283–294 (in Russian).
Chauhan, A. S., Srivastava, C. B., & Chauhan, B. S. (1974). Studies on the trematoda fauna of India, 6. Digenea: Schistosomatidae. A monographic aid to the identification of Indian schistosomes. Journal of the Zoological Society of India, 25, 83–127.
Chrisanfova, G. G., Heidorova, E. E., Shestak, A. G., Lopatkin, A. A., Bychkova, E. I., & Semenova, S. K. (2010). Geneticheskaya izmenchivost ptichikh shistosom Bilharziella polonica (Trematod: Schistosomatidae) ozera Naroch [Genetic variability of bird schistosomes Bilharziella polonica (Trematode: Schistosomatidae) from Lake Naroch. In: Theoretical and practical problems of parasitology. Moscow. Pp. 398–402 (in Russian).
Chrisanfova, G. G., Lopatkin, A. A., Mishchenkov, V. A., Kheidorova, E. E., Dorozhenkova, T. E., Zhukova, T. V., Ryskov, A. P., & Semyenova, S. K. (2009). Genetic variability of bird schistosomes (class Trematoda, family Schistosomatidae) of Naroch Lake: Identification of a new species in the Trichobilharzia ocellata group. Doklady Biochemistry and Biophysics, 428, 268–272 (in Russian).
Dubinina, M. N. (1971). Parazitologicheskoye issledovaniye ptits [Parasitological study of birds]. Nauka, Leningrad (in Russian).
Farley, J. A. (1971). Review of the family Schistosomatidae: Excluding the genus Schistosoma from mammals. Journal of Helminthology, 45, 289–320.
Fillimonova, L. V. (1985). Trematody fauny SSSR. Notokotilidy [Trematodes of the fauna of the USSR. Notocotylides]. Nauka, Moscow (in Russian).
Ginetsinskaya, T. A. (1968). Trematody, ikh zhiznennyye tsikly, biologiya i evolyutsiya [Trematodes, their life cycles, biology and evolution]. Nauka, Leningrad (in Russian).
Ginetsinskaya, T. A., & Dobrovolsky, A. A. (1963). Novyy metod obnaruzheniya sensill lichinok trematod i znacheniye etikh obrazovaniy dlya sistematiki [A new method for detecting sensilla of trematode larvae and the significance of these formations for taxonomy]. Doklady Academy of Sciences of the USSR, 151(2), 460–463 (in Russian).
Horák, P., & Kolárová, L. (2000). Survival of bird schistosomes in mammalian lungs. International Journal for Parasitology, 30, 65–68.
Jadin, V. I. (1952). Mollyuski presnykh i solonovatykh vod SSSR. Opredeliteli po faune SSSR [Shellfish fresh and brackish waters of the USSR. Keys to the fauna of the USSR]. Academy of Sciences of the USSR, Moscow, Leningrad (in Russian).
Kahlil, L. F. (2002). Family Schistosomatidae Stiles and Hassal, 1898. In: Gibson, A., Jones, A., & Bray, R. A. Keys to the Trematoda. Vol. I. CAB Publishing, London. Pp. 419–432.
Khalifa, R. (1972). Studies on Schistosomatidae Looss, 1899 (Trematoda) of aquatic bird of Poland. I. On the cycle of Bilharziella polonica Kowalesski, 1895, with a discussion of the subfamily Bilharziellinae Price, 1929. Acta Parasitologica Polonica, 20, 343–365.
Kolárová, L., Gottwaldová, V., Cechová, D., & Sevcová, M. (1989). The occurence of cercarial dermatitis in Central Bohemia. Zentrablatt und Hygiene, 189, 1–13.
Kotelnikov, G. A. (1976). Diagnostika gel’mintozov zhivotnykh [Diagnosis of helminthiases in animals]. Kolos, Moscow (in Russian).
Kowalewski, L. (1895). Bilharziella polonica sp. nov. (Studya helmintologiczne 3). Rozprawy Wydzialu Matematyczno-Przyrodniczego Polskiej Akademii Umiejetnosci, Krakow, 31, 41–70.
Kreysberg-Mukhina, Y. A., Kashkarov, D. Y., Lanovenko, Y. N., Shernazarov, E. S., & Peregonsev, Y. A. (2005). Ptitsy vodoyemov Uzbekistana i Tsentral’no-Aziaskogo regiona. Polevoy opredelitel’ vodno-bolotnykh ptits [Birds of water bodies of Uzbekistan and the Central Asian region. Field guide to wetland birds]. Nauka, Tashkent, Alma-Aty (in Russian).
Litvienko, N. T. (1963). Opyty po vyyasneniyu promezhutochnykh khozyayev vozbuditelya bil’khartsiyelleza domashnikh utok [Experiments to identify the intermediate hosts of the causative agent of bilharziellosis in the domestic duck]. Proceedings of Kharkov Zooveterinary Institut, 25, 71–74 (in Russian).
Palm, V. (1965). Ein Beitrag zur Helminthenfauna des Blesshuhns (Fulica atra L.) aus dem Raum von Postdam. Acta Parasitologica Polonica, 13, 425–444.
Shakarbaev, U., Akramova, F., & Azimov, D. (2020). The taxonomic survey of the fauna of cercariae (Platyhelminthes, Trematoda) in the mollusks of Uzbekistan. Zoodiversity, 54(6), 505–522.
Skrjabin, K. I. (1928). Metody polnykh gel’mintologicheskikh vskrytiy pozvonochnykh, vklyuchaya i cheloveka [Methods of complete helminthological dissections of vertebrates, including humans]. Publishing House of Moscow State University, Moscow (in Russian).
Skrjabin, K. I. (1951). Trematody zhivotnykh i cheloveka. Osnovy trematodologii [Trematodes of animals and humans. Fundamentals of trematodology]. Academy of Sciences of the USSR, Moscow (in Russian).
Sulgostowska, T. (1972). Trematodes of the mute swan Cygnus olor from central and northern regions of Poland. Acta Parasitologica Polonica, 20, 473–481.
Szidat, L. (1929). Die Parasiten des Hausgeflügels. 3 Bilharziella polonica Kow. ein im Blut Schmarotzender Trematode unserer Enten, seine Entwicklung und Ubertragung. Archiv für Geflügelkude, 3, 78–87.
Szidat, L. (1930). Uber Hautinfektionen bei Bluttrematoden insbesondere bei Bilharziella polonica Kow. Archiv für Dermatologie und Syphilis, 160, 304–308.
Vergun, G. I. (1856). K faune lichinok trematod nekotorykh molliuskov v rayone srednego technija r Donec [On the fauna of the trematod larvae of small molluscs in the area of the Middle Donec]. Problemy Parazitologii, 2, 30–32 (in Slovak).
Wiśniewski, L. W. (1958). Characterization of the parasitofauna of aneutrophic lake (Parasitofauna of the biocoenosis of Druzno Lake, part 1). Acta Parasitologica, 6, 1–64.
Yamaguti, S. (1971). Synopsis of digenetic trematodes of vertebrates. Keigaku, Tokyo.
Zbikowska, E. (2002). Is there a potential danger of “swimmer’s itch” in Poland? Parasitology Research, 89, 59–62.
Zbikowska, E. (2004). Infection of snails with bird schistosomes and the threat of swimmer’s itch in selected Polish lakes. Parasitology Research, 92, 30–35.
Zbikowska, E., & Nowak, A. (2009). One hundred years of research on the natural infection of freshwater snails by trematode larvae in Europe. Parasitology Research, 105(2), 301–311.
Ždárská, Z. (1963). Larvální stadia motolic z vodních plžů na území ČSSR (Larval trematodes of fresh-water snails in Czechoslovakia) [Larval stages of water snails in the Czechoslovak Republic (Larval trematodes of fresh-water snails in Czechoslovakia)]. Československá Parasitologie, 10, 207–262 (in Czech).
Zdun, W. (1959). Cercariae from Coretus corneus (L.) in the environments of Warszawa. Acta Parasitologica, 7, 95–115.
