Effects of stress exposure in captivity on physiology and infection in avian hosts: no evidence of increased Borrelia burgdorferi s.l. infectivity to vector ticks.

Exposure to environmental stressors, an increasingly recurring event in natural communities due to anthropogenic-induced environmental change, profoundly impacts disease emergence and spread. One mechanism through which this occurs is through stress-induced immunosuppression increasing disease susceptibility, prevalence, intensity and reactivation in hosts. We experimentally evaluated how exposure to stressors affected both the physiology of avian hosts and the prevalence of the zoonotic bacteria Borrelia burgdorferi sensu lato (s.l.), in two model species-the blackbird Turdus merula and the robin Erithacus rubecula captured in the wild, using xenodiagnoses and analysis of skin biopsies and blood. Although exposure to stressors in captivity induced physiological stress in birds (increased the number of circulating heterophils), there was no evidence of increased infectivity to xenodiagnostic ticks. However, Borrelia detection in the blood for both experimental groups of blackbirds was higher by the end of the captivity period. The infectivity and efficiency of transmission were higher for blackbirds than robins. When comparing different methodologies to determine infection status, xenodiagnosis was a more sensitive method than skin biopsies and blood samples, which could be attributed to mild levels of infection in these avian hosts and/or dynamics and timing of Borrelia infection relapses and redistribution in tissues.

Patterns of tick infestation and their Borrelia burgdorferi s.l. infection in wild birds in Portugal.

Wild birds may act as reservoirs for zoonotic pathogens and may be mechanical carriers of pathogen infected vector ticks through long distances during migration. The aim of this study was to assess tick infestation patterns in birds in Portugal and the prevalence of tick infection by Borrelia burgdorferi s.l. using PCR techniques. Seven tick species were collected from birds including Haemaphysalis punctata, Hyalomma spp., Ixodes acuminatus, Ixodes arboricola, Ixodes frontalis, Ixodes ricinus and Ixodes ventalloi. We found that I. frontalis and Hyalomma spp. were the most common ticks infesting birds of several species and that they were widespread in Portugal. Turdus merula was the bird species that presented the highest diversity of infesting ticks and had one of the highest infestation intensities. B. burgdorferi s.l. was detected in 7.3% (37/505) of Ixodidae ticks derived from birds. The most common genospecies was Borrelia turdi (6.9%), detected in ticks collected from Parus major, T. merula and Turdus philomelos, but Borrelia valaisiana (0.2%) and one Borrelia sp. (0.2%) similar to Borrelia bissettii (96% of similarity of the flaB gene in Blastn) were also detected. This study contributed to a better knowledge of the Ixodidae tick fauna parasitizing birds in Western Europe and to the assessment of the prevalence of B. burgdorferi s.l. associated with birds and their ticks.

Do ticks and Borrelia burgdorferi s.l. constitute a burden to birds?

Ticks consume resources from their hosts shaping their life-history traits and are vectors of many zoonotic pathogens. Several studies have focused on the health effects of blood-sucking ectoparasites on avian hosts, but there is limited information on the effects of ticks on adult and sub-adult birds, which may actively avoid ticks and are likely to present low infestation intensities. We evaluated the effects of the presence of feeding ticks and intensity of infestation on health variables of avian hosts. We also evaluated whether these variables were affected by tick infection by Borrelia burgdorferi sensu lato (s.l.) and by the presence of Borrelia infection on the birds' skin. Presence of parasite association among ticks, haemosporidea and Borrelia within the bird-host was also tested. We found that infestation by ticks significantly increased heterophyl/lymphocyte ratio in Turdus merula suggesting increased stress. This was especially evident at high infestation intensities when a significant decrease in body mass and body condition (body mass corrected for size) was also observed. Erithacus rubecula infested with more than 10 larvae tended to have lower haematocrit and blood haemoglobin. Plasma globulin concentration in T. merula tended to be affected by the presence of attached ticks and their infection with Borrelia, but this depended on the age of the bird. No association was detected among ticks, haemosporidea and Borrelia infection. We showed that ticks have detrimental effects on their avian hosts even under natural infestation conditions and that confirmed Borrelia reservoir hosts may also present symptoms of infection, though these may be subtle.

Birds as reservoirs for Borrelia burgdorferi s.l. in Western Europe: circulation of B. turdi and other genospecies in bird-tick cycles in Portugal.

Birds are important in the ecology of Borrelia burgdorferi sensu lato (s.l.) because they are important hosts for vector tick immature stages and are known reservoirs for some Borrelia genospecies. The aim of our study was to assess the role of common passerine bird species as reservoirs for B. burgdorferi s.l. in Western Europe. We surveyed birds in enzootic areas in Portugal, where no information is available for birds as reservoirs for this aetiologic agent and where B. lusitaniae, for which few reservoirs have been identified, is the dominant genospecies. Twenty-three birds (2.9%), including Turdus merula, T. philomelos, Parus major and Fringilla coelebs harboured infected ticks, but only Turdus sp. harboured infected tick larvae. In one study area, although B. lusitaniae was dominant in questing Ixodes ricinus, no ticks feeding on birds were infected with this genospecies, and B. valaisiana was the dominant genospecies in I. ricinus larvae feeding on birds. In the other area ticks collected from birds were mainly I. frontalis which were infected with B. turdi. Two skin biopsies (4.2%) from two T. merula were positive, one for B. valaisiana and the other for B. turdi. This is the first report for B. turdi in Western Europe.

Diversity and seasonal patterns of ticks parasitizing wild birds in western Portugal.

The diversity and abundance of questing ticks and ticks parasitizing birds was assessed during 1 year in two recreational forests in western Portugal, a suburban forest and an enclosed game area. The aim of this study was to assess the distribution and seasonality of tick species and to understand the role of bird species as hosts for ticks. Ixodes ricinus was the most abundant questing tick collected in the enclosed game area, whereas in the suburban forest, only three ticks were collected by blanket dragging. Tick species parasitizing birds included I. ricinus, I. frontalis, I. arboricola, I. acuminatus, Haemaphysalis punctata, Hyalomma marginatum and H. lusitanicum. This is the first record of I. arboricola in Portugal. Tick prevalence and intensity of infestation differed between study areas and was higher in birds from the game area where a large population of deer and wild boar may support tick populations. Ground and shrub dwelling bird species such as Turdus merula, Erithacus rubecula and Sylvia melanocephala were the most heavily parasitized by ticks, but the importance of different bird species as hosts of larvae and nymphs of I. ricinus and I. frontalis differed. Therefore, different bird species may contribute differently for tick population maintenance.