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The Species Composition of the Definitive Hosts of the Trematode Bilharziella polonica (Schistosomatidae) of Southern Karelia (Northwestern Russia)

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Abstract

A helminth fauna study of 398 waterfowl specimens belonging to 43 species living in southern Karelia wetlands (northwestern Russia) was conducted. This is the first time when data on the species composition and the infection of birds that are definitive hosts of Bilharziella polonica Schistosomatidae have been obtained. Bilharziella polonica has been recorded only in seven bird species, namely in the mallard, the Eurasia-n teal, the common goldeneye, the tufted duck, the northern shoveler, and the red-necked grebe; the infestation of the latter is noted in northwestern Russia for the first time. Of the bird species examined, this study describes the role of trematoda-infected birds in maintaining the focus of cercariosis, also known as “swimmer’s itch,” a disease pathogenic for humans. The data presented in our study indicates that the tremat-ode development cycle occurs successfully in the environment of Karelia.

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REFERENCES

  1. Akramova, F., Shakarbaev, U., Yorkulov, Z., Arepbaev, I., Mirzaeva, A., and Azimov, D., Life cycle of Bilharziella polonica (Trematoda, Schistosomatidae) parasite of semi-aquatic birds in Uzbekistan, Biosyst. Diversity, 2022, vol. 30, no. 2, pp. 137–142. https://doi.org/10.15421/012213

    Article  Google Scholar 

  2. Bayssade-Dufour, C., Jouet, D., Rudolfová, J., Horák, P., and Ferté, H., Seasonal morphological variations in bird schistosomes, Parasite, 2006, vol. 13, pp. 205–214.

    Article  CAS  PubMed  Google Scholar 

  3. Beer, S.A. and Voronin, M.V., Tserkariozy v urbanizirovannykh ekosistemakh (Cercarioses in Urbanized Ecosystems), Moscow: Nauka, 2007.

  4. Beer, S.A., Kolosovskii, B.S., Solonets, T.M., German, S.M., Dorozhenkova, T.E., Chistenko, G.N., Veden’kov, A.L., and Shalapenko, E.S., Metodicheskie rekomendatsii po diagnostike, mediko-ekologicheskoi ekspertize i profilaktike tserkariozov (Methodological Recommendations for Diagnosis, Medical-Ecological Examination, and Prevention of Cercarioses), MZ Respubliki Belarus’, Minsk, 1995.

  5. Bianki, V.V. and Dobrynina, I.N., Migratsii ptits Vostochnoi Evropy i Severnoi Azii. Plastinchatoklyuvye. Rechnye utki (Bird Migrations of Eastern Europe and Northern Asia. Lamellaridae. River Ducks), Moscow: Nauka, 1997.

  6. Bush, A.O., Lafferty, K.D., Lotz, J.M., and Shostak, A.W., Parasitology meets ecology on its own terms: Margolis et al. revisited, J. Parasitol., 1997, vol. 83, no. 4, pp. 575–583.

    Article  CAS  PubMed  Google Scholar 

  7. Bykhovskaya-Pavlovskaya, I.E., Trematody ptits SSSR: ekologo-geograficheskii obzor (Trematodes of Birds of the USSR: Ecological and Geographical Review), Moscow: Akad. Nauk SSSR, 1962.

  8. Chrisanfova, G.G., Lopatkin, A.A., Shestak, A.G., Mishchenkov, V.A., Zhukova, T.V., Akimova, L.N., and Semyenova, S.K., Polymorphism of the cox1 mtDNA gene from cercarial isolates of the avian schistosome Bilharziella polonica (Trematoda: Schistosomatidae) from Belarussian lakes, Russ. J. Genet., 2011, vol. 47, no. 5, pp. 684–690.

    Article  Google Scholar 

  9. Dorozhenkova, T.E., Okolotovich, S.I., and Kolosovskii, B.S., Cercarioses as a medical and biological problem of Lake Naroch, in Materialy nauchno-prakticheskoi konferentsii “Aktual’nye problemy gigieny i epidemiologii” (Proc. Sci. and Pract. Conf. “Current Problems of Hygiene and Epidemiology”), Minsk, 2006, pp. 267–272.

  10. Dubinina, M.N., Parazitologicheskoe issledovanie ptits (Parasitological Study of Birds), Leningrad: Nauka. Leningr. Otd., 1971.

  11. Ekimova, E.N., Trematodes of waterfowl and semi-aquatic birds of the Eastern European tundra, Tr. Komi Nauchn. Tsentra Ural. Otd. Akad. Nauk SSSR, 1989, no. 100, pp. 111–115.

  12. Faltýnková, A., Niewiadomska, K., Santos, M.J., and Valtonen, T.E., Furcocercous cercariae (trematoda) from freshwater snails in central Finland, Acta Parasitol., 2007, vol. 52, no. 4, pp. 310–317. https://doi.org/10.2478/s11686-007-0050-z

    Article  Google Scholar 

  13. Harkema, R., Study of Alaskan Schistosomes, Arct. Aeromed. Lab., Ladd Air Force Base, Alaska, Proj. 22-1401-005, 1953, pp. 1–26.

  14. Harkema, R., Further Study of Alaskan Schistosomes, Arct. Aeromed. Lab., Ladd AFB, Alaska, Rpt. no. 3, 1955, pp. 1–15.

  15. Harkema, R., Further Study of Alaskan Schistosomes, Arct. Aeromed. Lab., Ladd Air Force Base, Alaskan Air Command, 1960, pp. 1–23.

  16. Horák, P. and Kolářová, L., Survival of bird schistosomes in mammalian lungs, Int. J. Parasitol., 2000, vol. 30, no. 1, pp. 65–68.

    Article  PubMed  Google Scholar 

  17. Horák, P., Mikeš, L., Lichtenbergová, L., Skála, V., Soldánová, M., and Brant, S.V., Avian schistosomes and outbreaks of cercarial dermatitis, Clin. Microbiol. Rev., 2015, vol. 28, pp. 165–190. https://doi.org/10.1128/CMR.00043-14

    Article  PubMed  PubMed Central  Google Scholar 

  18. Jouet, D., Ferte, H., Hologne, C., Kaltenbach, M.L., and Depaquit, J., Avian schistosomes in French aquatic birds: a molecular approach, J. Helminthol., 2009, vol. 83, pp. 181–189. https://doi.org/10.1017/S0022149X09311712

    Article  CAS  PubMed  Google Scholar 

  19. Khalil, L.F., Family Schistosomatidae Stiles & Hassall, 1898, in Keys to the Trematoda, Gibson, D.I., Jones, A., and Bray, R.A., Eds., Wallingford: CAB International and the Natural History Museum, 2002, vol. 1, pp. 419–432.

    Google Scholar 

  20. Kheidorova, E.E., Species composition of the definitive hosts of trematodes of the family Schistosomatidae (Trichobilharzia sp., Bilharziella polonica) on Lake Naroch, Uch. Zap. Uchrezhd. Obraz. “Vitebskaya Ordena “Znak Pocheta” Gos. Akad. Vet. Med.,” Vitebsk, 2011, vol. 47, no. 2, part 1, pp. 106–109.

  21. Kheidorova, E.E., Patterns of population interactions between waterfowl and avian schistosomes as a factor of cercarial danger in water bodies, Extended Abstract of Cand. Sci. (Biol.) Dissertation, Minsk, 2012.

  22. Kolárová, L., Schistosomes causing cercarial dermatitis: a mini-review of current trends in systematics and of host specificity and pathogenicity, Folia Parasitol., 2007, vol. 54, pp. 81–87.

    Article  Google Scholar 

  23. Kolárová, L., Skirnisson, K., and Horak, P., Schistosome cercariae as the causative agent of swimmers itch in Iceland, J. Helminthol., 1999, vol. 73, pp. 215–220.

    Article  PubMed  Google Scholar 

  24. Kouřilová, P., Hogg, K.G., Kolářová, L., and Mountford, A.P., Cercarial dermatitis caused by bird schistosomes comprises both immediate and late phase cutaneous hypersensitivity reaction, J. Immunol., 2004, vol. 172, pp. 3766–3774.

    Article  PubMed  Google Scholar 

  25. Lashaki, E.K., Teshnizi, S.H., Gholami, S., Fakhar, M., Brant, S.V., and Dodangeh, S., Global prevalence status of avian schistosomes: a systematic review with meta-analysis, Parasite Epidemiol. Control, 2020, vol. 9, p. e00142. https://doi.org/10.1016/j.parepi.2020.e00142

    Article  PubMed  PubMed Central  Google Scholar 

  26. Lebedeva, D.I., Yakovleva, G.A., and Artem’ev, A.V., Parasites of the common tern (Sterna hirundo) and polar tern (Sterna paradisaea) (Charadriiformes, Laridae) in Karelia, Zool. Zh., 2019, vol. 98, no. 9, pp. 1019–1024. https://doi.org/10.1134/S2075111720010129

    Article  Google Scholar 

  27. Lorenti, E., Brant, S.V., Gilardoni, C., Diaz, Ju.I., and Cremonte, F., Two new genera and species of avian schistosomes from Argentina with proposed recommendations and discussion of the polyphyletic genus Gigantobilharzia (Trematoda, Schistosomatidae), Parasitology, 2022, pp. 1–59. https://doi.org/10.1017/S0031182022000130

  28. Nekrasov, A.V., Sanzhieva, S.D., and Egorov, V.G., Helminth fauna of waterfowl of Lake Baikal, in Biologicheskie resursy Zabaikal’ya i ikh okhrana (Biological Resources of Transbaikalia and Their Protection), Ulan-Ude: Buryat. Fil. Sib. Otd. Akad. Nauk SSSR, 1982, pp. 69–81.

  29. Noskov, G.A., Rymkevich, T.A., and Gaginskaya, A.R., Migratsii ptits Severo-Zapada Rossii. Nevorob’inye (Migrations of Birds in North-West Russia. Non-Passerines), St. Petersburg: ANO LA Professional, 2016.

  30. Opredelitel’ trematod ryboyadnykh ptits Palearktiki (brakhilaimidy, klinostomidy, tsiklotselidy, fastsiolidy, notokotilidy, plagiorkhidy, shistosomatidy) (Identification Guide to Trematodes of Fish-Eating Birds of the Palaearctic (Brachylaimids, Clinostomids, Cyclocelids, Fasciolids, Notocotylids, Plagiorchids, and Schistosomatids)), Moscow: Nauka, 1985.

  31. Oshmarin, P.G., On the fauna of helminths of commercial animals of Buryatia, in Paraziticheskie chervi domashnikh i dikikh zhivotnykh (Parasitic Worms of Domestic and Wild Animals), Vladivostok: Dal’nevost. Fil. Sib. Otd. Akad. Nauk SSSR, 1965, pp. 209–212.

  32. Pirilä, V. and Wikgren, B.J., Cases of swimmers itch in Finland, Acta Dermato-Venerol., 1957, vol. 37, pp. 140–148.

    Google Scholar 

  33. Reiczigel, J., Marozzi, M., Fábián, I., and Rózsa, L., Biostatistics for parasitologists—a primer to quantitative parasitology, Trends Parasitol., 2019, vol. 35, pp. 277–281. https://doi.org/10.1016/j.pt.2019.01.003

    Article  PubMed  Google Scholar 

  34. Rezvyi, S.P., Savinich, I.B., Noskov, G.A., Gaginskaya, A.R., Kovalev, V.A., Buzun, V.A., Afanas’eva, G.A., Rymkevich, T.A., Smirnov, O.P., Smirnov, E.N., and Shutenko, E.V., Atlas of bird migrations based on ringing data in the Leningrad oblast, Tr. St. Petersb. O-va Estestvoispyt., 1995, vol. 85, no. 4.

  35. Rudolfova, J., Sitko, J., and Horak, P., Nasal schistosomes in wildfowl in the Czech Republic, Parasitol. Res., 2002, vol. 88, pp. 1093–1095.

    Article  PubMed  Google Scholar 

  36. Rudolfová, J., Littlewood, D.T.J., Sitko, J., and Horak, P., Bird schistosomes of wildfowl in the Czech Republic and Poland, Folia Parasitol., 2007, vol. 54, pp. 88–93.

    Article  Google Scholar 

  37. Semenova, S.K., Khrisanfova, G.G., Filippova, E.K., Beer, S.A., Voronin, M.V., and Ryskov, A.P., Individual and population variability of schistosomatid cercariae of the Trichobilharzia ocellata group (Trematoda, Schistosomatidae) detected using polymerase chain reaction, Genetika, 2005, vol. 41, no. 1, pp. 17–22.

    CAS  PubMed  Google Scholar 

  38. Sitko, J., Faltýnková, A., and Scholz, T., Checklist of the Trematodes (Digenea) of Birds of the Czech and Slovak Republics, Praha: Academia, 2006, vol. 1.

  39. Skryabin, K.I., Trematody zhivotnykh i cheloveka. Osnovy trematodologii (Trematodes of Animals and Humans. Fundamentals of Trematodology), Moscow: Akad. Nauk SSSR, 1951, vol. 5.

  40. Skryabina, V.I., On the helminth fauna of the European teal, Tr. Barguzin. Zapov., Irkutsk, 1962a, vl. 4, pp. 221–225.

  41. Skryabina, V.I., On the helminth fauna of mallards and domestic ducks in Eastern Siberia, in Opyt bor’by s zabolevaniyami sel’skokhozyaistvennykh zhivotnykh Irkutskoi oblasti (Experience in Combating Diseases of Farm Animals in the Irkutsk Oblast), Irkutsk, 1962b, pp. 68–69.

    Google Scholar 

  42. Smogorzhevskaya, L.A., Gel’minty vodoplavayushchikh i bolotnykh ptits fauny Ukrainy (Helminths of Waterfowl and Wading Birds of the Fauna of Ukraine), Kiev: Naukova Dumka, 1976.

  43. Syrota, Ya.Yu., Greben, O.B., Poluda, A.M., Maleha, O.M., Lisitsyna, O.I., and Kornyushin, V.V., Helminths of the mallard, Anas platyrhynchos (Aves, Anatidae), in Ukraine: analysis of the diversity in mixed forest zone and the Black Sea region, Vestn. Zool., 2018, vol. 52, no. 4, pp. 267–278. https://doi.org/10.2478/vzoo-2018-0028

    Article  Google Scholar 

  44. Tkacheva, N., Study of the development of cercariae of Bilharziella polonica (Trematoda: Schistosomatidae), in Materialy XXI Mezhvuzovskoi studencheskoi nauchnoi konferentsii “Student-issledovatel’- uchitel’” (Proc. XXI Interuniversity Student Sci. Conf. “Student–Researcher–Teacher”), St. Petersburg: RGPU im. A.I. Gertsena, 2020, pp. 182–190.

  45. Tupitsyn, I.I. and Timoshenko, T.M., Shorebirds of the Selenga River delta (diversity, abundance, and helminths), in Sokhranenie biologicheskogo raznoobraziya v Baikal’skom regione: problemy, podkhody, praktika (Conservation of Biological Diversity in the Baikal Region: Problems, Approaches, and Practice), Ulan-Ude: Buryat. Nauchn. Tsentr Sib. Otd. Ross. Akad. Nauk, 1996, vol. 2, pp. 32–34.

  46. Vinogradova, A.A. and Skvortsov, V.V., Helminthofauna of ducks of the North-West of Russia and Estonia, Parazitologiya, 2022, vol. 56, no. 2, pp. 108–125. https://doi.org/10.31857/S0031184722020028

    Article  Google Scholar 

  47. Voronin, M.V. and Beer, S.A., Features of the morphology of schistosomatid cercariae of the Trichobilharzia cf ocellata group from populations of Moscow and St. Petersburg, Parazitologiya, 2002, vol. 36, no. 1, pp. 60–70.

    CAS  Google Scholar 

  48. WoRMS Editorial Board. World Register of Marine Species, 2023. https://www.marinespecies.org. https://doi.org/10.14284/170

  49. Yakovleva, G.A. and Lebedeva, D.I., The role of duck birds in the dispersal of the trematode Bilharziella polonica (Kowalewski, 1895) Looss, 1899 in Karelia, in Tezisy 19-i mezhdunarodnoi Pushchinskoi shkoly-konferentsii molodykh uchenykh “Biologiya – nauka XXI veka” (Proc. 19th International Pushchino School-Conference of Young Scientists “Biology—The Science of the 21st Century”), Pushchino: Institut fiziologii rastenii RAN, 2015, p. 454.

  50. Yakovleva, G.A., Lebedeva, D.I., and Ieshko, E.P., Ecological and faunal features of the species composition of trematodes of waterbirds in Karelia, Tr. Karel. Nauchn. Tsentra Ross. Akad. Nauk, 2013, no. 2, pp. 108–110. https://doi.org/10.17076/eco119i

  51. Yakovleva, G.A., Lebedeva, D.I., and Ieshko, E.P., Trematodes of waterbirds of Karelia (based on materials of the 319th Union Helminthological Expedition of 1958–1962), Tr. Karel. Nauchn. Tsentra Ross. Akad. Nauk, 2015, no. 2, pp. 95–110. https://doi.org/10.17076/eco119i

  52. Yurlova, N.I., Helminths of wild duck birds in the south of Western Siberia, Cand. Sci. (Biol.) Dissertation, Novosibirsk, 1979.

  53. Yushkov, V.F., Trematodes of birds of the family Anatidae of the European North-East of Russia, Tr. Komi Nauchn. Tsentra Ural. Otd. Ross. Akad. Nauk, 1996, no. 148, pp. 128–139.

  54. Zimin, V.B. and Ivanter, E.V., Ptitsy (Birds), Petrozavodsk: Petrozav. Gos. Univ., 2002.

    Google Scholar 

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ACKNOWLEDGMENTS

The author is grateful to Doctor of Biological Sciences E.P. Ieshko for valuable comments and suggestions during the preparation of the article manuscript as well as to Doctor of Biological Sciences A.V. Artemyev for the assistance in determining the species and age of the birds, and is also grateful to the reviewer for useful comments with regard to the manuscript.

Funding

This work was supported by the state order of Russian Ministry of Education and Science 122032100130-3 (FMEN-2022-0005).

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  1. Institute of Biology, Karelian Research Center, Russian Academy of Sciences, 185910, Petrozavodsk, Russia

    G. A. Yakovleva

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Author contributed to the study conception and design. Material preparation, data collection and analysis were performed by Galina Yakovleva. Galina Yakovleva performed autopsies on birds, collected worms, made slides, and identified parasite species.

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Correspondence to G. A. Yakovleva.

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The author of this work declares that she has no conflicts of interest.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

All the host birds were obtained dead and therefore no ethics permit was required by Russian law. The research on birds was authorized by the Ministry of the Environment of the Karelian Republic; part of the birds were hunted by licensed hunters under licenses 00006-2013, 00007-2014, and 00009-2015 by the Republic of Karelia, Russian Federation.

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Yakovleva, G.A. The Species Composition of the Definitive Hosts of the Trematode Bilharziella polonica (Schistosomatidae) of Southern Karelia (Northwestern Russia). Biol Bull Russ Acad Sci 51, 667–674 (2024). https://doi.org/10.1134/S1062359023603415

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