Investigations of the tick burden on passeriform, water-associated and predatory birds reveal new tick-host associations and habitat-related factors of tick infestation
Language English Country England, Great Britain Media electronic
Document type Journal Article
Grant support
TKI 1500107
HUN-REN
PubMed
38500221
PubMed Central
PMC10949810
DOI
10.1186/s13071-024-06229-1
PII: 10.1186/s13071-024-06229-1
Knihovny.cz E-resources
- Keywords
- Accipitriformes, Ixodidae, Passeriformes, Pelecaniformes,
- MeSH
- Ecosystem MeSH
- Geese MeSH
- Tick Infestations * epidemiology veterinary MeSH
- Ixodidae * MeSH
- Ixodes * MeSH
- Larva MeSH
- Nymph MeSH
- Passeriformes * MeSH
- Songbirds * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
BACKGROUND: Previous studies on the tick infestation of birds in the Carpathian Basin focused on songbirds (Passeriformes). Thus, the primary aim of the present work was to extend the scope of previous studies, i.e. to include aquatic (water-associated) bird species in a similar context, especially considering that these birds are usually long-distance migrants. METHODS: Between March 2021 and August 2023, 11,919 birds representing 126 species were checked for the presence of ticks. From 352 birds belonging to 40 species, 905 ixodid ticks were collected. Tick species were identified morphologically and/or molecularly. RESULTS: Ticks from avian hosts belonged to seven species: Ixodes ricinus (n = 448), I. frontalis (n = 31), I. festai (n = 2), I. arboricola (n = 36), I. lividus (n = 4), Haemaphysalis concinna (n = 382) and Dermacentor reticulatus (n = 2). Nymphs of I. ricinus occurred with a single activity peak around March-May, whereas its larvae typically infested birds in May, June or July. By contrast, H. concinna usually had its activity maximum during the summer (nymphs in June-July, larvae later in July-August). Interestingly, two ornithophilic species, I. frontalis and I. arboricola, were most active around winter months (between October and April). A significantly lower ratio of aquatic birds was found tick-infested than songbirds. Several new tick-host associations were revealed, including I. ricinus from Greylag Goose (Anser anser) and D. reticulatus from Great Egret (Ardea alba) and Sedge Warbler (Acrocephalus schoenobaenus). Ticks were collected for the first time in Europe from two species of predatory birds as well as from Little Bittern (Ixobrychus minutus). Bird species typically inhabiting reedbeds were most frequently infested with H. concinna, and most ticks localized at their throat, as opposed to forest-dwelling avian hosts, on which I. ricinus predominated and ticks were more evenly distributed. CONCLUSIONS: In the evaluated region, aquatic birds appear to be less important in tick dispersal than songbirds. However, newly revealed tick-host associations in this category attest to their hitherto neglected contribution. The results suggest that the habitat type will have significant impact not only on the species composition but also on the feeding location of ticks on birds.
BirdLife Hungary Budapest Hungary
Department of Ecology Charles University Prague Czechia
Department of Parasitology and Zoology University of Veterinary Medicine Budapest Hungary
HUN REN PE Evolutionary Ecology Research Group University of Pannonia Pf 1158 8210 Veszprém Hungary
Institute of Vertebrate Biology Czech Academy of Sciences Brno Czechia
Plant Protection Institute HUN REN Centre for Agricultural Research Budapest Hungary
See more in PubMed
Madison-Antenucci S, Kramer LD, Gebhardt LL, Kauffman E. Emerging tick-borne diseases. Clin Microbiol Rev. 2020;33:e00083–e118. doi: 10.1128/CMR.00083-18. PubMed DOI PMC
de la Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE. Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci. 2008;13:6938–6946. doi: 10.2741/3200. PubMed DOI
de la Fuente J, Estrada-Peña A, Cabezas-Cruz A, Brey R. Flying ticks: anciently evolved associations that constitute a risk of infectious disease spread. Parasit Vectors. 2015;8:538. doi: 10.1186/s13071-015-1154-1. PubMed DOI PMC
Hansford KM, Gillingham EL, Vaux AGC, Cull B, McGinley L, Catton M, Wheeler BW, Tschirren B, Medlock JM. Impact of green space connectivity on urban tick presence, density and Borrelia infected ticks in different habitats and seasons in three cities in southern England. Ticks Tick Borne Dis. 2023;14:102103. doi: 10.1016/j.ttbdis.2022.102103. PubMed DOI
Hornok S, Cutajar B, Takács N, Galea N, Attard D, Coleiro C, Galea R, Keve G, Sándor AD, Kontschán J. On the way between Africa and Europe: molecular taxonomy of ticks collected from birds in Malta. Ticks Tick Borne Dis. 2022;13:102001. doi: 10.1016/j.ttbdis.2022.102001. PubMed DOI
Janisch M. Kullancsgazda madarak különféle betegségek közvetítői [Birds as tick hosts spreading various diseases] Aquila. 1960;67:191–194.
Hornok S, Flaisz B, Takács N, Kontschán J, Csörgő T, Csipak Á, Jaksa BR, Kováts D. Bird ticks in Hungary reflect western, southern, eastern flyway connections and two genetic lineages of Ixodes frontalis and Haemaphysalis concinna. Parasit Vectors. 2016;9:101. doi: 10.1186/s13071-016-1365-0. PubMed DOI PMC
Hornok S, Csörgő T, de la Fuente J, Gyuranecz M, Privigyei C, Meli ML, Kreizinger Z, Gönczi E, Fernández de Mera IG, Hofmann-Lehmann R. Synanthropic birds associated with high prevalence of tick-borne rickettsiae and with the first detection of Rickettsia aeschlimannii in Hungary. Vector Borne Zoonotic Dis. 2013;13:77–83. doi: 10.1089/vbz.2012.1032. PubMed DOI
Hornok S, Kováts D, Csörgő T, Meli ML, Gönczi E, Hadnagy Z, Takács N, Farkas R, Hofmann-Lehmann R. Birds as potential reservoirs of tick-borne pathogens: first evidence of bacteraemia with Rickettsia helvetica. Parasit Vectors. 2014;7:128. doi: 10.1186/1756-3305-7-128. PubMed DOI PMC
Keve G, Csörgő T, Benke A, Huber A, Mórocz A, Németh Á, Kalocsa B, Tamás EA, Gyurácz J, Kiss O, Kováts D, Sándor AD, Karcza Z, Hornok S. Ornithological and molecular evidence of a reproducing Hyalomma rufipes population under continental climate in Europe. Front Vet Sci. 2023;10:1147186. doi: 10.3389/fvets.2023.1147186. PubMed DOI PMC
Hornok S, Kováts D, Horváth G, Kontschán J, Farkas R. Checklist of the hard tick (Acari: Ixodidae) fauna of Hungary with emphasis on host-associations and the emergence of Rhipicephalus sanguineus. Exp Appl Acarol. 2020;80:311–328. doi: 10.1007/s10493-019-00461-6. PubMed DOI
Keve G, Sándor AD, Hornok S. Hard ticks (Acari: Ixodidae) associated with birds in Europe: review of literature data. Front Vet Sci. 2022;9:928756. doi: 10.3389/fvets.2022.928756. PubMed DOI PMC
Ernek E, Kozuch O, Hudec K, Urbán S. Occurrence of tick-borne encephalitis virus neutralizing antibody in aquatic birds in Central Europe. Acta Virol. 1967;11:562. PubMed
Michel F, Ziegler U, Fast C, Eiden M, Klaus C, Dobler G, Stiasny K, Groschup MH. Role of ducks in the transmission cycle of tick-borne encephalitis virus? Transbound Emerg Dis. 2021;68:499–508. doi: 10.1111/tbed.13704. PubMed DOI
Jaenson TGT, Wilhelmsson P. First records of tick-borne pathogens in populations of the taiga tick Ixodes persulcatus in Sweden. Parasit Vectors. 2019;12:559. doi: 10.1186/s13071-019-3813-0. PubMed DOI PMC
Seils G, Maskow I. Beitrag zu einer durch Zecken (Ixodes ricinus) hervorgerufenen Erkrankung bei Gösseln [Gosling disease caused by ticks (Ixodes ricinus)] Monatsh Veterinarmed. 1970;25:268–270. PubMed
Estrada-Peña A, Mihalca AD, Petney TN. Ticks of Europe and North Africa: a guide to species identification. Berlin: Springer International Publishing; 2017. p. 404.
Hornok S. Allochronic seasonal peak activities of Dermacentor and Haemaphysalis spp. under continental climate in Hungary. Vet Parasitol. 2009;163:366–369. doi: 10.1016/j.vetpar.2009.03.048. PubMed DOI
Ciebiera O, Jerzak L, Nowak-Chmura M, Bochenski M. Ticks (Acari: Ixodida) on birds (Aves) migrating through the Polish Baltic coast. Exp Appl Acarol. 2019;77:241–251. doi: 10.1007/s10493-019-00341-z. PubMed DOI
Zając Z, Kulisz J, Kunc-Kozioł R, Woźniak A, Filipiuk M, Rudolf R, Bartosik K, Cabezas-Cruz A. Tick infestation in migratory birds of the Vistula River Valley, Poland. Int J Environ Res Public Health. 2022;19:13781. doi: 10.3390/ijerph192113781. PubMed DOI PMC
Stanko M, Derdáková M, Špitalská E, Kazimírová M. Ticks and their epidemiological role in Slovakia: from the past till present. Biologia (Bratisl) 2022;77:1575–1610. doi: 10.1007/s11756-021-00845-3. PubMed DOI PMC
Nosek J. The ecology, bionomics, and behaviour of Haemaphysalis (Aboimisalis) punctata tick in Central Europe. Z Parasitenk. 1971;37:198–210. doi: 10.1007/BF00259499. PubMed DOI
Keve G, Csörgő T, Kováts D, Hornok S. Long term evaluation of factors influencing the association of ixodid ticks with birds in Central Europe. Hungary Sci Rep. 2024;14:4958. doi: 10.1038/s41598-024-55021-9. PubMed DOI PMC
Hillyard PD. Ticks of North-West Europe. Field studies council 1996, Shrewsbury
Janisch M. A hazai kullancsfauna feltérképezése [Geographical distribution of tick species in Hungary] Állattani Közl. 1959;47:103–110.
Babos S. Kullancsok—Ixodidea [Ticks—Ixodidea] Fauna Hungariae. 1965;18:1–38.
Heylen D, De Coninck E, Jansen F, Madder M. Differential diagnosis of three common Ixodes spp. ticks infesting songbirds of Western Europe: Ixodes arboricola, I. frontalis and I. ricinus. Ticks Tick Borne Dis. 2014;5:693–700. doi: 10.1016/j.ttbdis.2014.05.006. PubMed DOI
Uchikawa K, Sato A. The occurrence of Argas japonicus and Ixodes lividus in Nagano prefecture, Japan (Ixodoidea: Argasidae; Ixodidae) J Med Entomol. 1969;6:95–97. doi: 10.1093/jmedent/6.1.95. PubMed DOI
Ulmanen I, Saikku P, Vikberg P, Sorjonen J. Ixodes lividus (Acari) in sand martin colonies in Fennoscandia. Oikos. 1977;1:20–26. doi: 10.2307/3543318. DOI
Thompson GB, Arthur DR. VI—Records of ticks collected from birds in the British Isles−2. Ann Mag Nat Hist. 1955;8:57–60. doi: 10.1080/00222935508651824. DOI
Whittaker DJ, Reichard DG, Drouilly M, Battle K, Ziegenfus C. Avian olfactory displays: a hypothesis for the function of bill-wiping in a social context. Behav Ecol Sociobiol. 2014;69:159–167. doi: 10.1007/s00265-014-1829-1. DOI