Ornithological and molecular evidence of a reproducingHyalomma rufipespopulation under continental climate in Europe

Abstract

AbstractBackgroundReports on adultHyalommaticks in certain regions of the Carpathian Basin date back to the 19thcentury. These ticks were thought to emerge from nymphs dropping from birds, then molting to adults. Although the role of migratory birds in carrying ticks of this genus is known from all parts of Europe, in most countries no contemporaneous multiregional surveillance of bird-associated ticks was reported which could allow the recognition of hotspots in this context.MethodsIxodid ticks were collected from birds at seven ringing stations in Hungary, including both the spring and autumn migration period in 2022.IxodesandHaemaphysalisspecies were identified morphologically, whereasHyalommaspecies molecularly.ResultsFrom 38 passeriform bird species 957 ixodid ticks were collected. The majority of developmental stages were nymphs (n=588), but 353 larvae and 16 females were also present. On most birds (n=381) only a single tick was found and the maximum number of ticks removed from the same bird was 30. Tick species were identified asIxodes ricinus(n=598),Ixodes frontalis(n=18),Ixodes lividus(n=6),Haemaphysalis concinna(n=322), andD. reticulatus(n=1). All twelveHyalommasp. ticks (11 engorged nymphs and an unengorged larva) were identified asHyalomma rufipesbased on three mitochondrial markers. This species was only found in the Transdanubian region and along its southeastern border. The Common Blackbird (Turdus merula) and the European Robin (Erithacus rubecula) were the two main hosts ofI. ricinusandI. frontalis, whereasH. concinnawas almost exclusively collected form long-distance migrants. The predominant hosts ofH. rufipeswere reed-associated bird species, the Sedge Warbler (Acrocephalus schoenobaenus) and the Bearded Reedling (Panurus biarmicus), both harboring these ticks at the end of June (i.e., the nesting period) in southwestern Hungary.ConclusionsThis study provides ornithological explanation for the regional, century-long presence of adultHyalommaticks under continental climate in the Transdanubian Region of the Carpathian Basin. More importantly, the autochthonous occurrence of aH. rufipespopulation was revealed for the first time in Europe, based on the following observations: (1) the bird species infested withH. rufipesare not known to migrate during their nesting period; (2) one larva was not yet engorged; (3) the larva and the nymphs must have belonged to different local generations; and (4) allH. rufipesfound in the relevant location were identical in their haplotypes based on three maternally inherited mitochondrial markers, probably reflecting founder effect. This study also demonstrated that the species of ticks carried by birds were significantly different between collection sites even within a geographically short distance (200 km). Therefore, within a country multiregional monitoring is inevitable to assess the overall epidemiological significance of migratory birds in importing exotic ticks, and also in maintaining newly established tick species.