A contribution to avian ectoparasite fauna of Turkey: the reports of feather mites and tick on the Great tit (Parus major L.)

Abstract

Birds have a symbiotic relationship with many ectoparasite groups such as chewing lice (Mallophaga: Amblycera, Ischnocera), fleas (Siphonaptera), keds (Diptera: Hippoboscidae), mites (Acari: Sarcoptiformes, Trombidiformes) and ticks (Acari: Ixodidae, Argasidae). In fact, this relationship is mainly based on parasitism, but feather mites are mostly classified as commensal ectosymbionts, compared to other parasitic insects and arachnids. This study reports tick and feather mite species detected on a dead specimen of the Great Tit (Parus major L.) that was brought to the Department of Parasitology, Faculty of Veterinary Medicine, Ondokuz Mayıs University, Samsun, Turkey. As a result of the parasitological examination, the tick samples were identified as Ixodes frontalis (Panzer) and feather mites were identified as Analges mucronatus (Buchholz) and Proctophyllodes stylifer (Buchholz). With this study, A. mucronatus and P. stylifer have been reported for the first time from Turkey, and the feather mite fauna of Turkey has reached 42 identified species.

Keywords

• Analges mucronatus
• Ixodes frontalis
• Proctophyllodes stylifer

References

1. Aksin, N. 2007. Freyana anatina (Koch, 1844) feather mites (Acarina, Freyanoidea) recorded for the first time on wild ducks (Subfamily, Anatinae) in Turkey. Türkiye Parazitoloji Dergisi, 31 (4): 302-305.
2. Aksin, N. 2010. Chewing lice and feather mites on wild partridges. The Indian Veterinary Journal, 87: 940-941.
3. Aksin, N. 2011. Feather mites (Acari: Astigmata) on wild quail (Coturnix coturnix). Indian Veterinary Journal, 88 (4): 69.
4. Atyeo, W.T. and Braasch, N.L. 1966. The feather mite genus Proctophyllodes (Sarcoptiformes: Proctopbyllodidae). Bulletin of the University of Nebraska State Museum, 5: 1-354.
5. Bakırcı, S. and Güleğen, E. 2005. Bir güvercinde tüy akarı (Falculifer rostratus, Buchholz, 1869) olgusu. 14. Ulusal Parazitoloji Kongresi, 25-27 Eylül 2005, İzmir, Turkey, 217. [In Turkish]
6. Beaman, M. and Madge, S. 2010. The handbook of bird identification: for Europe and the western Palearctic. A&C Black Publishers, p.715, London, U.K, 868 pp.
7. Behnke, J.M., McGregor, P.K., Shepherd, M., Wiles, R., Barnard, C., Gilbert, F.S. and Hurst, J.L. 1995. Identity, prevalence and intensity of infestation with wing feather mites on birds (Passeriformes) from the Setubal Peninsula of Portugal. Experimental and Applied Acarology, 19 (8): 443-458. doi: 10.1007/BF00048263
8. Blanco, G., Tella, J.L., Potti, J. and Baz, A. 2001. Feather mites on birds: costs of parasitism or conditional outcomes?. Journal of Avian Biology, 32 (3): 271-274. doi: 10.1111/j.0908-8857.2001.320310.x.

9. Bursali, A., Keskin, A. and Tekin, S. 2012. A review of the ticks (Acari: Ixodida) of Turkey: species diversity, hosts and geographical distribution. Experimental and Applied Acarology, 57 (1): 91-104. doi: 10.1007/s10493-012-9530-4
10. Brinkerhoff, R.J., Dang, L., Streby, H.M. and Gimpel, M. 2019. Life history characteristics of birds influence patterns of tick parasitism. Infection Ecology and Epidemiology, 9 (1): 1547096. doi: 10.1080/20008686.2018.1547096
11. Clifford, C.M. and Anastos, G. 1960. The use of chaetotaxy in the identification of larval ticks (Acarina: Ixodidae). The Journal of Parasitology, 46 (5): 567-578.
12. Dabert. J. and Mironov, S.V. 1999. Origin and evolution of feather mites (Astigmata). Experimental and Applied Acarology, 23: 437-454. doi: 10.1023/A:1006180705101
13. Dabert, M., Solarczyk, P., Badek, A. and Dabert, J. 2004. Taxonomic status of the oligoxenous feather mite species: are we dealing with species in statu nascendi? Phytophaga, 14: 425-431.
14. Dabert, J., Mironov, S.V. and Janiga, M. 2018. Two new species of the feather mite genus Analges Nitzsch, 1818 (Analgoidea: Analgidae) from accentors (Passeriformes: Prunellidae)-morphological descriptions with DNA barcode data. Systematic and Applied Acarology, 23 (12): 2288-2303. doi: 10.11158/saa.23.12.2
15. Dik, B. and Kandir, E.H. 2021. Ectoparasites in Some Wild Birds (Aves) in Turkey. Progress in Nutrition, 23, e2021261. doi: 10.23751/pn.v23iS2.11919
16. Eren, G., Açıcı, M., Özkoç, Ö.Ü. and Gürler, A.T. 2021. First record of Pelargodacna heteromorpha Perez & Atyeo, 1992 (Pterolichidae, Xoloptopidinae) on a black stork (Ciconia nigra) from Turkey. Eduvet International Veterinary Science Congress, 25-27 June 2021, Turkey, 292-293.
17. Esch, G.W., Gibbons, J.W. and Bourque, J.E. 1975. An analysis of the relationship between stress and parasitism. The American Midland Naturalist, 93: 339-353.
18. Evans, G.O. 1992. Principles of Acarology. CAB International, Wallingford, United Kingdom, 563 pp.
19. Gaud, J. and Atyeo W.T. 1978. Nouvelles superfamilles pour les Acariens astigmates parasites d'oiseaux. Acarologia, 19: 678-685. [In French]
20. Gaud, J. and Atyeo, W.T. 1996. Feather mites of the world (Acarina, Astigmata): The supraspecific taxa (Part I). Annales du Musée Royal de l’Afrique Centrale, Sciences Zoologiques, Belgium.
21. Gürler, A.T., Mironov, S.V. and Erciyes-Yavuz, K. 2013. Avian feather mites (Acari: Astigmata) of Samsun, Turkey. Acarologia, 53 (1): 17-23. doi: 10.1051/acarologia/20132078
22. Hasle, G. 2013. Transport of ixodid ticks and tick-borne pathogens by migratory birds. Frontiers in Cellular and Infection Microbiology, 3 (48): 1-6. doi: 10.3389/fcimb.2013.00048
23. Karatepe, B. and Karatepe, M. 2015. Arthropodların toplanması ve muhafaza yöntemleri, In: Arthropodoloji. Karaer, K.Z. and Dumanlı, N. (Ed.). Medisan Yayın Serisi, Ankara, Turkey, 81: 309-319. [In Turkish]
24. Keskin, A., Koprulu, T.K., Bursali, A., Ozsemir, A.C., Yavuz, K.E. and Tekin, S. 2014. First record of Ixodes arboricola (Ixodida: Ixodidae) from Turkey with presence of Candidatus Rickettsia vini (Rickettsiales: Rickettsiaceae). Journal of Medical Entomology, 51 (4): 864-867. doi:10.1603/ME13169
25. Keskin, A. and Erciyas-Yavuz, K. 2016. A preliminary investigation on ticks (Acari: Ixodidae) infesting birds in Kızılırmak Delta, Turkey. Journal of Medical Entomology, 53 (1): 217-220. doi: 10.1093/jme/tjv149
26. Keskin, A., Bulut, Y.E., Keskin, A. and Bursalı, A. 2017. Tick attachment sites in humans living in the Tokat province of Turkey. Türk Hijyen ve Deneysel Biyoloji Dergisi, 74 (2): 121-128. doi: 10.5505/TurkHijyen.2017.24993
27. Keskin, A. and Erciyas-Yavuz, K. 2019. Ticks (Acari: Ixodidae) parasitizing passerine birds in Turkey with new records and new tick–host associations. Journal of Medical Entomology, 56 (1): 156-161. doi: 10.1093/jme/tjy151
28. Klimov P.B, Mironov, S.V. and OConnor, B.M. 2017. Convergent and unidirectional evolution of extremely long aedeagi in the largest feather mite genus, Proctophyllodes (Acari: Proctophyllodidae): evidence from comparative molecular and morphological phylogenetics. Molecular Phylogenetics and Evolution, 114: 212-224. doi: 10.1016/j.ympev.2017.06.008
29. Kurtpınar, H. 1954. Türkiye Keneleri (Ixodoidea): Morfoloji, biyoloji, konakçı yayılışları ve medikal önemleri. Güven Matbaası, Ankara, Turkey, 102 pp. [In Turkish]
30. Krantz, G.W. and Walter, D.E. 2009. A manual of acarology. 3rd edition. Texas Tech University Press, Lubbock, USA, 807 pp.
31. Leblebicioglu, H., Eroglu, C., Erciyas-Yavuz, K., Hokelek, M., Acici, M. and Yilmaz, H. (2014). Role of migratory birds in spreading Crimean-Congo hemorrhagic fever, Turkey. Emerging Infectious Diseases, 20 (8): 1331-1334. doi: 10.3201/eid2008.131547
32. Merdivenci, A. 1970. Türkiye parazitleri ve parazitolojik yayınları. İstanbul Üniversitesi, Cerrahpaşa Tıp Fakültesi Yayınları, Kutulmuş Matbaası, İstanbul, Turkey, 324 pp. [In Turkish]
33. Mironov, S.V. 1985. Feather mites of the genera Analges and Pteronyssoides from the European part of the USSR (Sarcoptiformes, Analgoidea). Parazitologicheskii Sbornik, 33: 159-208. [In Russian]
34. Mironov, S.V. 1987. Morphological adaptations of feather mites to different types of plumage and skin of birds. Parazitologicheskii Sbornik, 34: 114-132. [In Russian]
35. Mironov, S.V. 1996. Feather mites of the passerines in the North-West of Russia. Parazitologiya, 30 (6): 521-539. [In Russian]
36. Mironov, S.V. 1999. Feather mites: general morphological adaptations, phylogeny and coevolutionary relationships with birds. Ekologija (Vilnius, Lithuania), 2: 57-66.
37. Mironov, S.V. 2012. New species of the feather mite genus Proctophyllodes Robin, 1877 (Acari: Analgoidea: Proctophyllodidae) from European passerines (Aves: Passeriformes), with an updated checklist of the genus. Acarina, 20 (2): 130-158.
38. Mironov, S.V. 2019. A new species of the feather mite genus Analges Nitzsch, 1818 (Acariformes: Analgidae) from the streaked spiderhunter Arachnothera magna (Passeriformes: Nectariniidae), with a renewed diagnosis and world checklist to the genus. Acarina, 27 (1): 19-43. doi: 10.21684/0132-8077-2019-27-1-19-43
39. Monks, D., Fisher, M. and Forbes, N.A. 2006. Ixodes frontalis and avian tick‐related syndrome in the United Kingdom. Journal of Small Animal Practice, 47 (8): 451-455. doi: 10.1111/j.1748-5827.2006.00031.x
40. OConnor, B.M. 1982. Evolutionary ecology of astigmatid mites. Annual Review of Entomology, 27: 385-409. Oğuz, B., Değer, S., Özdal, N., Biçek, K., Kılınç, Ö.O. and Aslan, L. 2015. The first case of Rhipicephalus turanicus from red hawk (Buteo rufinus) in Van. Van Veterinary Journal, 26 (1): 39-41.
41. Per, E. and Aktaş, M. 2018. The monitoring of feather mites (Acari, Astigmata) of the Warbler (Aves: Sylviidae) species in the Kızılırmak delta, Samsun, Turkey. Turkish Journal of Zoology, 42 (4): 394-401. doi: 10.3906/zoo-1711-12
42. Peterson, P.C. 1975. An analysis of host-parasite associations among feather mites (Acari: Analgoidea). Miscellaneous Publications of the Entomological Society of America, 9: 237-242.
43. Pfäffle, M.P., Madder, M., Santos-Silva, M.M. and Petney, T.N. 2017. Ixodes frontalis (Panzer, 1798), In: Ticks of Europe and North Africa: A Guide to Species Identification. Estrada-Peña, A., Mihalca, A.D., and Petney, T.N. (Eds). Springer, Cham, Switzerland, 91-96.
44. Proctor, H.C. 2003. Feather mites (Acari: Astigmata): ecology, behavior and evolution. Annual Review of Entomology, 48: 185-209. doi: 10.1146/annurev.ento.48.091801.112725