Bridging of cryptic Borrelia cycles in European songbirds

Abstract

The principal European vector for Borrelia burgdorferi s.l., the causative agents of Lyme disease, is the host-generalist tick Ixodes ricinus. Almost all terrestrial host-specialist ticks have been supposed not to contribute to the terrestrial Borrelia transmission cycles. Through an experiment with blackbirds, we show successful transmission by the widespread I. frontalis, an abundant bird-specialized tick that infests a broad range of songbirds. In the first phase of the experiment, we obtained Borrelia-infected I. frontalis (infection rate: 19%) and I. ricinus (17%) nymphs by exposing larvae to wild blackbirds that carried several genospecies (Borrelia turdi, B. valaisiana, B. burgdorferi s.s.). In the second phase, pathogen-free blackbirds were exposed to these infected nymphs. Both tick species were able to infect the birds, as indicated by the analysis of xenodiagnostic I. ricinus larvae which provided evidence for both co-feeding and systemic transmission (infection rates: 10%-60%). Ixodes frontalis was shown to transmit B. turdi spirochetes, while I. ricinus transmitted both B. turdi and B. valaisiana. Neither species transmitted B. burgdorferi s.s. European enzootic cycles of Borrelia between songbirds and their ornithophilic ticks do exist, with I. ricinus potentially acting as a bridging vector towards mammals, including man.

Host dispersal shapes the population structure of a tick‐borne bacterial pathogen

“…Ixodes ricinus is a generalist tick and birds are known to be important hosts for its immature stages (Norte et al, ; Santos‐Silva et al, ). The other tick species ( I. frontalis , I. arboricola and I. ventalloi ) and genera ( Haemaphysalis and Hyalomma ) collected from birds in this study have also been previously reported on birds (Diakou et al, ; Norte et al, ; Pérez‐Eid, ) and differ in vector competence for Borrelia (Eisen & Lane, ; Heylen, Krawczyk, et al, ; Heylen, Sprong, et al, ). Some bird species such as hole‐nesting birds ( P. major and F. albicollis ), T. merula and T. philomelos were hosts for different tick species; however, the opportunities for cofeeding transmission of B. burgdorferi s.l.…”

“…Turdus species have been identified as main reservoirs for B. garinii and B. valaisana in Europe (Dubska et al, ; Mannelli et al, ; Michalik et al, ) and Asia (Miyamoto & Masuzawa, ). In addition, T. merula has also been proven as competent reservoir for B. turdi through xenodiagnosis (Heylen, Krawczyk, et al, ; Humair et al, ; Norte, Lopes de Carvalho, et al, ). In an experimental setup in which migratory restlessness was induced, latent B. garinii infections were re‐activated in T. iliacus (Gylfe, Bergstrom, Lunstrom, & Olsen, ).…”

“…In our study it has been detected in I. frontalis and I. ventalloi only, which are host‐ specialised tick species (to birds and rabbits, respectively; Hillyard, ). Ixodes frontalis has been proven to be a competent vector for B. turdi (Heylen, Krawczyk, et al, ) but vector competence of I. ventalloi remains unknown. This Borrelia genospecies may have been overlooked in the past in questing ticks such as I. ricinus probably because of its low prevalence (Heylen, Krawczyk, et al, ).…”

“…Ixodes frontalis has been proven to be a competent vector for B. turdi (Heylen, Krawczyk, et al, ) but vector competence of I. ventalloi remains unknown. This Borrelia genospecies may have been overlooked in the past in questing ticks such as I. ricinus probably because of its low prevalence (Heylen, Krawczyk, et al, ). Because B. turdi prevalence in our study was relatively low, we were unable to evaluate statistically its bird host and vector species' associations.…”

“…Tick species was also included in the models because within the genus Ixodes , different species differ in their vector competence for B. burgdorferi s.l. (Eisen & Lane, ; Heylen, Krawczyk, et al, ; Heylen, Sprong, et al, ). We controlled for the effects of timing of tick collection throughout the year including month of collection as explanatory variable and also by grouping those ticks collected during the birds' breeding season (April–July) and those collected outside the breeding season (August–March), because breeding is one of the most stressful periods in the birds' life cycle and the stress associated with breeding duties may suppress their immune system potentially leading to spirochetaemia.…”