Ornithological and molecular evidence of a reproducing Hyalomma rufipes population under continental climate in Europe

Abstract

Reports on adult Hyalomma ticks in certain regions of the Carpathian Basin date back to the 19th century. 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. From 38 passeriform bird species 956 ixodid ticks were collected at seven locations in Hungary. Tick species were identified as Ixodes ricinus (n = 598), Ixodes frontalis (n = 18), Ixodes lividus (n = 6), Haemaphysalis concinna (n = 321), and D. reticulatus (n = 1). All 12 Hyalomma sp. ticks (11 engorged nymphs and 1 unengorged larva) were identified as H. rufipes based on three mitochondrial markers. This species was only found in the Transdanubian region and along its southeastern border. The Common Blackbird and the European Robin were the two main hosts of I. ricinus and I. frontalis, whereas H. concinna was almost exclusively collected form long-distance migrants. The predominant hosts of H. rufipes were reed-associated bird species, the Sedge Warbler and the Bearded Reedling, both in their nesting period. This study provides ornithological explanation for the regional, century-long presence of adult Hyalomma ticks under continental climate in the Transdanubian Region of the Carpathian Basin. More importantly, the autochthonous occurrence of a H. rufipes population was revealed for the first time in Europe, based on the following observations: (1) the bird species infested with H. rufipes are 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) all H. rufipes found in the relevant location were identical in their haplotypes based on three maternally inherited mitochondrial markers, probably reflecting founder effect. This study also demonstrated regional and temporal differences in tick species carried by birds.

Keywords: Central Europe; Haemaphysalis; Hungary; Hyalomma; Ixodes; bird migration.

Figure 1

Map of Hungary showing ringing stations and the ratio of tick species collected in (A) the first semiannual period (March to July) and (B) the second semiannual period (August to November). In the former (A) the location of the first Hyalomma nymph reported from a bird in Hungary in 1955 is marked with a red dot, and the place where adult Hyalomma rufipes ticks were found on cattle is indicated with a red star.

Figure 2

Illustration of the possible consequences of bird-borne transportation of Hyalomma rufipes into countries north of the Mediterranean Basin, including Hungary. Green arrows indicate molting. (A) Nymphs transported by birds may die after drop-off, or (B) molt to adult which cannot overwinter, or (C) if they overwinter as adults, females will not produce eggs in the absence of previous mating, or (D) if nymphs carried by birds detach and molt to male and another (carried independently) to female and these meet and mate on cattle, females will be able to lay eggs after drop-off. First generation larvae and nymphs developing from these eggs probably will have a similar state of engorgement but molting to adults they will find host and will mate at different time. Therefore, existence of a second generation may involve the simultaneous presence of larvae and nymphs of different cohorts on local birds, as shown in this study.