Helmintological Examination of Pica pica (Linnaeus, 1758) (Passeriformes: Corvidae) Specimens Collected from Bursa and Its Surroundings in Türkiye
-
Mohamed Warsame Dirshe
,
Hikmet Sami Yıldırımhan
,
Yeliz Civil
,
Adel Mohammed Redhwan
,
Sinem Yıldırım
,
Ali Adan Hassan
Abstract
Background: The Eurasian magpie, Pica pica (Linnaeus, 1758), is a widely distributed bird species inhabiting both rural and urban environments in Türkiye. Despite its ecological importance, information on its helminth fauna remains limited. We aimed to investigate the helminth fauna of P. pica specimens collected in Bursa Province and to contribute to the knowledge of parasite biodiversity in Türkiye.
Methods: A total of 53 P. pica specimens, brought dead between June 2015 and August 2025 from Bursa Zoo and the Celal Acar Wildlife Rescue and Rehabilitation Center (Karacabey Ova Korusu, Bursa, Türkiye), were examined for helminths using standard parasitological techniques. Recovered helminths were identified morphologically.
Results: Ten helminth species were identified: Brachylaima fuscata (Rudolphi, 1819) Joyeux, Baer & Timon-David, 1932, B. lobatum (Railliet, 1900), Lyperosomum longicauda (Rudolphi, 1809) (Digenea); Raillietina echinobothrida (Megnin, 1881), Passerilepis stylosa (Rudolphi, 1809), Choanotaenia macracantha (Krabbe, 1869) (Cestoda); Dispharynx nasuta (Rudolphi, 1819), Baruscapillaria obsignata (Madsen, 1945) Moravec, 1982, B. resecta (Dujardin, 1845) (Nematoda); and Sphaerirostris picae (Rudolphi, 1819) (Acanthocephala). R. echinobothrida, C. macracantha, B. obsignata, and B. resecta were recorded from P. pica for the first time worldwide. In addition, B. fuscata, B. lobatum, L. longicauda, C. macracantha, P. stylosa, and B. resecta represent new records for the helminth fauna of Türkiye.
Conclusion: This study expands current knowledge of the helminth fauna of P. pica and provides several novel host and geographical records. The findings highlight the importance of continued parasitological investigations of wild birds in Türkiye to improve our understanding of parasite diversity and host–parasite associations.
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4. Georgiev B, Biserkov V, Genov T. In toto staining method for cestodes with iron acetocarmine. Helminthol. 1986; 23:279–81.
5. Anderson RC. Nematode Parasites of Vertebrates: Their Development and Transmission. 2nd ed. Wallingford, UK: CABI Publishing; 2000.
6. Gibson DI, Jones A, Bray RA. Keys to the Trematoda. Vol. 1. London: CAB International; 2002. 521 p.
7. Khalil LF, Jones A, Bray RA. Keys to the Cestode Parasites of Vertebrates. Wallingford, UK: CAB International; 1994. 751 p.
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9. Merdivenci A. Türkiye’nin Marmara Bölgesinde Evcil tavuk, Hindi, Ördek ve Kazlarda Görülen Trematod, Cestod ve Nematodlara Dair Araştırmalar. İstanbul: Kurtulmuş Matbaası; 1967.
10. Yamaguti S. Systema Helminthum. Volume III. The Nematodes of Vertebrates. New York: Interscience Publishers Inc; 1961.
11. Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revised. J Parasitol. 1997; 83(4):575–83.
12. Tolgay N. Saksağanlarda (Pica Pica) Bulunan Cestod Türleri Üzerinde Araştırmalar. Ankara Univ. Vet. Fak. Derg. 1972a, 19(03).
13. Tolgay N. Çeşitli Kanatlılarda Bulduğumuz Helmint Türleri Üzerine Araştırmalar. Türk Vet Hek Der Derg. 1972b; 42(9-10):36–46.
14. Çetindağ M, Bıyıkoğlu G. Occurrence of Dispharynx nasuta (Rudolphi, 1819) and Trichomonas sp. in magpies (Pica pica) in Türkiye. Etlik Vet Mikrob Derg. 1997; 9(1):149–56.
15. Girişgin AO, Demirer AA, Büyükcangaz E, Khider M, Birlik S, İpek V. Postmortem findings on a group of Pica pica (Passeriformes: Corvidae). Ankara Üniv Vet Fak Derg. 2019;66(2):155–61.
16. Yılmaz AB, Azizoğlu E, Adızel Ö. Examination of helminth parasites in the fecal samples of magpies (Pica pica), jackdaws (Coloeus monedula), and rooks (Corvus frugilegus) in the vicinities of Van Province/Türkiye. Commagene J Biol. 2020;4(2):91–5.
17. Girişgin AO, Akyol ÇV, Çimenlikaya N, Saygın B. Bazı Vahşi Kuşlarda Trichinella spp. Larvasının Araştırılması. Harran Üniv Vet Fak Derg. 2021;10(1):73–6.
18. Güven T. Denizli İlindeki Bazı Kuş Türlerinin Helmint Faunası Üzerine Bir Araştırma \ [Master's thesis]. Denizli: Pamukkale University; 2022.
19. Sitko J, Faltýnková A, Scholz T. Checklist of the Trematodes (Digenea) of birds of the Czech and Slovak Republics. Praha: Academia; 2006. 111 p. ISBN 80-200-1428-4.
20. Sitko J, Heneberg P. Avian trematodes of central European corvids are heterogeneous regarding preferences for host species and age. J Helminthol. 2024;98\: e17.
21. Stoimenov K. Contribution to the helminth fauna of the magpie (Pica pica L.) in North-Eastern Bulgaria \ [in Bulgarian]. Izvestiia na Tsentralnata Khelmintologichna Laboratoriia. 1962; 7:161–7.
22. Ryšavý B, Baruš V, Groschaft J. Helminths of birds from Peking (China). Folia Parasitol. 1970; 17:291–2.
23. Heneberg P, Sitko J, Casero M, Rząd I. New molecular data help clarify the taxonomy of Central European avian Dicrocoeliidae Looss, 1899 (Trematoda: Plagiorchiida). Int J Parasitol Parasites Wildl. 2023; 22:276–99.
24. Chernobai VJ. \ [Parasites of Corvidae in the lower Volga area]. In: Markov GS, et al., editors. \ [Parasitic animals in the Volgograd region]. Volgograd: Volgograd State Pedagogical Institute Serafimovicha; 1969. p. 166–97.
25. Todd KS Jr, Worley DE. Helminth parasites of the black-billed magpie, Pica pica hudsonia (Sabine, 1823), from southwestern Montana. J Parasitol. 1967;53(2):364–7.
26. Borgsteede FHM, Okulewicz A, Okulewicz J. A study of the helminth fauna of birds belonging to the Passeriformes in the Netherlands. Acta Parasitol. 2000; 45(1):14–21.
27. Sitko J, Heneberg P. Long-term dynamics of trematode infections in common birds that use farmlands as their feeding habitats. Parasites Vectors. 2021; 14:1–18.
28. Chernobai BF. \ [Parasitic worms of magpies in the Volgograd region]. In: Kobyshev NM, editor. \ [Questions of ecology and parasitology of animals]. Saratov: Saratov University Publishers; 1966. p. 124–43.
29. Skrjabin KI, Udinzew AN. Two new trematodes from the biliary ducts of birds from Armenia. J Parasitol. 1930;16(4):213–9.
30. Koubek P, Vojtek J. Příspěvek k poznání helmintofauny našich havranovitých (Corvidae). Folia Fac Sci Nat Univ Purkynianae Brunensis. 1973; 14:71–101.
31. Halajian A, Eslami A, Mobedi I, et al. Gastrointestinal helminths of magpies (Pica pica), rooks (Corvus frugilegus) and carrion crows (Corvus cornix) in Mazandaran Province, North of Iran. Iran J Parasitol. 2011;6(2):38–44.
32. Gabrion C. Étude expérimentale du développement larvaire d’Anomotaenia constricta (Molin, 1858) Cohn, 1900 chez un Coléoptère Pimelia sulcata Geoffr. Z Parasitenkd. 1975;47(4):249–62. doi:10.1007/bf00389884.
33. Clapham PA. Helminth parasites in some wild birds. Bird Study. 1957; 4(4):193–6.
34. Luft K The helminths of jay (Garrulus glandarius L.) and magpie (Pica pica L.) from Lublin Palatinate. Acta Parasitol. Pol. 1960; 8, 351–356.
35. Ryabov AV, Ponomaryov VA. Invasive diseases of synanthropic corvids. Kostroma State Univ Bull. 2014;20(7):37–41.
36. Kornyushin VV, Salamatin RV, Greben OB, Georgiev BB. Spiniglans sharpiloi sp. n. (Cestoda, Dilepididae), a parasite of the common magpie, Pica pica, in the Palaearctic. Vestn Zool Suppl. 2009; 23:85–93.
37. Kalmykov AP, Strelkov VA. Species diversity of the nematode fauna of the Corvidae Vigors family in the Volga River delta, 1825. Russ J Parasitol. 2018;12(3):11–7.
38. Campbell JW. The gapeworm (Syngamus) in wild birds. J Anim Ecol. 1935; 4(2):208–15.
39. Hibler CP. Onchocercidae (Nematoda: Filarioidea) of the American magpie, Pica pica hudsonia (Sabine) in Northern Colorado \ [PhD thesis]. Fort Collins, CO: Colorado State University; 1963.
40. Millet P, Bain O. Une novelle filaire de la pie, Eufilaria kalifai, n.sp (Lemdaninae) et son développement chez Culicoides nebeculosus. Ann Parasitol Hum Comp. 1984; 59:177–87.
41. Amin OM, Heckmann RA, Halajian A, Eslami A. Redescription of Sphaerirostris picae (Acanthocephala: Centrorhynchidae) from magpie, Pica pica, in northern Iran, with special reference to unusual receptacle structures and notes on histopathology. J Parasitol. 2010; 96(3):561–8.
42. Dezfuli BS, Manera M, Rubini S. Intestinal histopathology due to an acanthocephalan in two corvid species from Northern Italy. J Wildl Dis. 2021;57(1):215–9.
43. Birkhead TR. The Magpies: The Ecology and Behaviour of Black-Billed and Yellow-Billed Magpies. London, UK: T & AD Poyser; 1991.
44. Jerzak L, Rössler M. Ecology and Behaviour of the Eurasian Magpie (Pica pica). Cham, Switzerland: Springer; 2018.
45. Marzluff JM, Angell T. In the Company of Crows and Ravens. New Haven, CT: Yale University Press; 2005.
46. Loye JE, Zuk M. Bird–Parasite Interactions: Ecology, Evolution, and Behaviour. Oxford, UK: Oxford University Press; 1991.
2. Kustr. Turkish Bird Records Committee. Turkish bird species list. [Internet]. Available from: https://www.kustr.org/kuskayitkomitesi/Türkiye-tur-listesi/) [Accessed 2025 Aug 12].
3. Karataş A, Yavuz KE, Yavuz N, et al. Trakus Türkiye'nin Kuşları. İstanbul: Türkiye İş Bankası Kültür Yayınları; 2021. p. 236–40.
4. Georgiev B, Biserkov V, Genov T. In toto staining method for cestodes with iron acetocarmine. Helminthol. 1986; 23:279–81.
5. Anderson RC. Nematode Parasites of Vertebrates: Their Development and Transmission. 2nd ed. Wallingford, UK: CABI Publishing; 2000.
6. Gibson DI, Jones A, Bray RA. Keys to the Trematoda. Vol. 1. London: CAB International; 2002. 521 p.
7. Khalil LF, Jones A, Bray RA. Keys to the Cestode Parasites of Vertebrates. Wallingford, UK: CAB International; 1994. 751 p.
8. Lisitsyna O. Fauna of Ukraine. Vol. 31. Acanthocephala. Kyiv: Scientific and technical enterprise "Scientific Thought" of the National Academy of Sciences of Ukraine; 2019.
9. Merdivenci A. Türkiye’nin Marmara Bölgesinde Evcil tavuk, Hindi, Ördek ve Kazlarda Görülen Trematod, Cestod ve Nematodlara Dair Araştırmalar. İstanbul: Kurtulmuş Matbaası; 1967.
10. Yamaguti S. Systema Helminthum. Volume III. The Nematodes of Vertebrates. New York: Interscience Publishers Inc; 1961.
11. Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revised. J Parasitol. 1997; 83(4):575–83.
12. Tolgay N. Saksağanlarda (Pica Pica) Bulunan Cestod Türleri Üzerinde Araştırmalar. Ankara Univ. Vet. Fak. Derg. 1972a, 19(03).
13. Tolgay N. Çeşitli Kanatlılarda Bulduğumuz Helmint Türleri Üzerine Araştırmalar. Türk Vet Hek Der Derg. 1972b; 42(9-10):36–46.
14. Çetindağ M, Bıyıkoğlu G. Occurrence of Dispharynx nasuta (Rudolphi, 1819) and Trichomonas sp. in magpies (Pica pica) in Türkiye. Etlik Vet Mikrob Derg. 1997; 9(1):149–56.
15. Girişgin AO, Demirer AA, Büyükcangaz E, Khider M, Birlik S, İpek V. Postmortem findings on a group of Pica pica (Passeriformes: Corvidae). Ankara Üniv Vet Fak Derg. 2019;66(2):155–61.
16. Yılmaz AB, Azizoğlu E, Adızel Ö. Examination of helminth parasites in the fecal samples of magpies (Pica pica), jackdaws (Coloeus monedula), and rooks (Corvus frugilegus) in the vicinities of Van Province/Türkiye. Commagene J Biol. 2020;4(2):91–5.
17. Girişgin AO, Akyol ÇV, Çimenlikaya N, Saygın B. Bazı Vahşi Kuşlarda Trichinella spp. Larvasının Araştırılması. Harran Üniv Vet Fak Derg. 2021;10(1):73–6.
18. Güven T. Denizli İlindeki Bazı Kuş Türlerinin Helmint Faunası Üzerine Bir Araştırma \ [Master's thesis]. Denizli: Pamukkale University; 2022.
19. Sitko J, Faltýnková A, Scholz T. Checklist of the Trematodes (Digenea) of birds of the Czech and Slovak Republics. Praha: Academia; 2006. 111 p. ISBN 80-200-1428-4.
20. Sitko J, Heneberg P. Avian trematodes of central European corvids are heterogeneous regarding preferences for host species and age. J Helminthol. 2024;98\: e17.
21. Stoimenov K. Contribution to the helminth fauna of the magpie (Pica pica L.) in North-Eastern Bulgaria \ [in Bulgarian]. Izvestiia na Tsentralnata Khelmintologichna Laboratoriia. 1962; 7:161–7.
22. Ryšavý B, Baruš V, Groschaft J. Helminths of birds from Peking (China). Folia Parasitol. 1970; 17:291–2.
23. Heneberg P, Sitko J, Casero M, Rząd I. New molecular data help clarify the taxonomy of Central European avian Dicrocoeliidae Looss, 1899 (Trematoda: Plagiorchiida). Int J Parasitol Parasites Wildl. 2023; 22:276–99.
24. Chernobai VJ. \ [Parasites of Corvidae in the lower Volga area]. In: Markov GS, et al., editors. \ [Parasitic animals in the Volgograd region]. Volgograd: Volgograd State Pedagogical Institute Serafimovicha; 1969. p. 166–97.
25. Todd KS Jr, Worley DE. Helminth parasites of the black-billed magpie, Pica pica hudsonia (Sabine, 1823), from southwestern Montana. J Parasitol. 1967;53(2):364–7.
26. Borgsteede FHM, Okulewicz A, Okulewicz J. A study of the helminth fauna of birds belonging to the Passeriformes in the Netherlands. Acta Parasitol. 2000; 45(1):14–21.
27. Sitko J, Heneberg P. Long-term dynamics of trematode infections in common birds that use farmlands as their feeding habitats. Parasites Vectors. 2021; 14:1–18.
28. Chernobai BF. \ [Parasitic worms of magpies in the Volgograd region]. In: Kobyshev NM, editor. \ [Questions of ecology and parasitology of animals]. Saratov: Saratov University Publishers; 1966. p. 124–43.
29. Skrjabin KI, Udinzew AN. Two new trematodes from the biliary ducts of birds from Armenia. J Parasitol. 1930;16(4):213–9.
30. Koubek P, Vojtek J. Příspěvek k poznání helmintofauny našich havranovitých (Corvidae). Folia Fac Sci Nat Univ Purkynianae Brunensis. 1973; 14:71–101.
31. Halajian A, Eslami A, Mobedi I, et al. Gastrointestinal helminths of magpies (Pica pica), rooks (Corvus frugilegus) and carrion crows (Corvus cornix) in Mazandaran Province, North of Iran. Iran J Parasitol. 2011;6(2):38–44.
32. Gabrion C. Étude expérimentale du développement larvaire d’Anomotaenia constricta (Molin, 1858) Cohn, 1900 chez un Coléoptère Pimelia sulcata Geoffr. Z Parasitenkd. 1975;47(4):249–62. doi:10.1007/bf00389884.
33. Clapham PA. Helminth parasites in some wild birds. Bird Study. 1957; 4(4):193–6.
34. Luft K The helminths of jay (Garrulus glandarius L.) and magpie (Pica pica L.) from Lublin Palatinate. Acta Parasitol. Pol. 1960; 8, 351–356.
35. Ryabov AV, Ponomaryov VA. Invasive diseases of synanthropic corvids. Kostroma State Univ Bull. 2014;20(7):37–41.
36. Kornyushin VV, Salamatin RV, Greben OB, Georgiev BB. Spiniglans sharpiloi sp. n. (Cestoda, Dilepididae), a parasite of the common magpie, Pica pica, in the Palaearctic. Vestn Zool Suppl. 2009; 23:85–93.
37. Kalmykov AP, Strelkov VA. Species diversity of the nematode fauna of the Corvidae Vigors family in the Volga River delta, 1825. Russ J Parasitol. 2018;12(3):11–7.
38. Campbell JW. The gapeworm (Syngamus) in wild birds. J Anim Ecol. 1935; 4(2):208–15.
39. Hibler CP. Onchocercidae (Nematoda: Filarioidea) of the American magpie, Pica pica hudsonia (Sabine) in Northern Colorado \ [PhD thesis]. Fort Collins, CO: Colorado State University; 1963.
40. Millet P, Bain O. Une novelle filaire de la pie, Eufilaria kalifai, n.sp (Lemdaninae) et son développement chez Culicoides nebeculosus. Ann Parasitol Hum Comp. 1984; 59:177–87.
41. Amin OM, Heckmann RA, Halajian A, Eslami A. Redescription of Sphaerirostris picae (Acanthocephala: Centrorhynchidae) from magpie, Pica pica, in northern Iran, with special reference to unusual receptacle structures and notes on histopathology. J Parasitol. 2010; 96(3):561–8.
42. Dezfuli BS, Manera M, Rubini S. Intestinal histopathology due to an acanthocephalan in two corvid species from Northern Italy. J Wildl Dis. 2021;57(1):215–9.
43. Birkhead TR. The Magpies: The Ecology and Behaviour of Black-Billed and Yellow-Billed Magpies. London, UK: T & AD Poyser; 1991.
44. Jerzak L, Rössler M. Ecology and Behaviour of the Eurasian Magpie (Pica pica). Cham, Switzerland: Springer; 2018.
45. Marzluff JM, Angell T. In the Company of Crows and Ravens. New Haven, CT: Yale University Press; 2005.
46. Loye JE, Zuk M. Bird–Parasite Interactions: Ecology, Evolution, and Behaviour. Oxford, UK: Oxford University Press; 1991.
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| Issue | Vol 21 No 2 (2026) | |
| Section | Original Article(s) | |
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| Pica pica Digenea Cestoda Nematoda Acanthocephala Türkiye. | ||
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How to Cite
1.
Dirshe M, Yıldırımhan H, Civil Y, Redhwan A, Yıldırım S, Hassan A. Helmintological Examination of Pica pica (Linnaeus, 1758) (Passeriformes: Corvidae) Specimens Collected from Bursa and Its Surroundings in Türkiye. Iran J Parasitol. 2026;21(2):205-216.
