Abstract
BackgroundTicks are obligate haematophagous ectoparasites of vertebrates and frequently parasitize avian species that can carry them across continents during their long-distance migrations. Ticks may have detrimental effects on the health state of their avian hosts, which can be either directly caused by blood-draining or mediated by microbial pathogens transmitted during the blood meal. Indeed, ticks host complex microbial communities, including bacterial pathogens and symbionts. Midichloria bacteria (Rickettsiales) are widespread tick endosymbionts that can be transmitted to vertebrate hosts during the tick bite, inducing an antibody response. Their actual role as infectious/pathogenic agents is, however, unclear.MethodsWe screened for Midichloria DNA African ticks and blood samples collected from trans-Saharan migratory songbirds at their arrival in Europe during spring migration.ResultsTick infestation rate was 5.7%, with most ticks belonging to the Hyalomma marginatum species complex. Over 90% of Hyalomma ticks harboured DNA of Midichloria bacteria belonging to the monophylum associated with ticks. Midichloria DNA was detected in 43% of blood samples of avian hosts. Tick-infested adult birds were significantly more likely to test positive to the presence of Midichloria DNA than non-infested adults and second-year individuals, suggesting a long-term persistence of these bacteria within avian hosts. Tick parasitism was associated with a significantly delayed timing of spring migration of avian hosts but had no significant effects on body condition, whereas blood Midichloria DNA presence negatively affected fat deposits of tick-infested avian hosts.ConclusionsOur results show that ticks effectively transfer Midichloria bacteria to avian hosts, supporting the hypothesis that they are infectious to vertebrates. Bird infection likely enhances the horizontal spread of these bacteria across haematophagous ectoparasite populations. Moreover, we showed that Midichloria and tick parasitism have detrimental non-independent effects on avian host health during migration, highlighting the complexity of interactions involving ticks, their vertebrate hosts, and tick-borne bacteria.
Highlights
Ticks are obligate haematophagous ectoparasites of vertebrates and frequently parasitize avian species that can carry them across continents during their long-distance migrations
Tick parasitism in trans-Saharan migratory birds We found that 5.7% of the 1772 screened individuals belonging to the three target species was tick-infested (Table 1)
Molecular screening for Midichloria DNA in ticks and blood samples Due to the very small sample of Ixodes and Haemaphysalis ticks, we focused on Hyalomma ticks only
Summary
Ticks are obligate haematophagous ectoparasites of vertebrates and frequently parasitize avian species that can carry them across continents during their long-distance migrations. Midichloria bacteria (Rickettsiales) are widespread tick endosymbionts that can be transmitted to vertebrate hosts during the tick bite, inducing an antibody response Their actual role as infectious/pathogenic agents is, unclear. Birds are frequent intermediate or definitive hosts of many tick species [4], and they appear to play a key role for the spread of ticks and tick-borne agents of veterinary and medical relevance over broad geographical areas [5, 6] During their migratory movements, birds may disperse ticks attached to their bodies (and tickassociated microbial communities) across continents and along migration routes [5, 7]. Some studies reported increased stress levels, anaemia due to blood loss, hypoproteinaemia, mass loss and low body condition in tick-infested birds compared to noninfested ones [10, 11, 13,14,15,16], sometimes leading to increased mortality of heavily infested individuals [10], while others failed to detect significant negative effects of natural levels of tick infestation on health parameters [12, 17, 18]
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