Beware of hitchhiking ticks? Clarifying the variable roles of bird families in tick movement along migratory routes

Description

Ticks are blood-feeding parasites which act as major vectors for various pathogenic microorganisms affecting both animal and human health. Hard ticks are known to “hitchhike” on migratory birds as they transit from breeding to overwintering grounds in spring and autumn, potentially leading to exchange and establishment of non-endemic tick species in novel environments. Even though, there is a lack of understanding of which migratory bird families play a role in movement of specific tick genera and what influence migratory season may have. To fill this knowledge gap, we performed a systematic literature review regarding primary data of ticks moving on migratory birds within the African-Western Palearctic flyways. In total, 34 studies were found which showed 123 bird species from 37 families connected to potential movement of 26 tick species representing six genera (Amblyomma, Dermacentor, Haemaphysalis, Hyalomma, Ixodes, Rhipicephalus). Statistical analysis showed bird families which carried above average number of ticks were only found for interactions with Hyalomma and Ixodes ticks with below average estimates found for all tick genera besides Rhipicephalus. Contrary to expectation, no tick genus, which was found in both migratory seasons, was estimated to have increased numbers in one season or the other. In certain cases, tick genera (e.g., Amblyomma) were only found on birds during spring migration. This pattern could highlight that the assemblage of ticks present on a bird at capture does not represent the ticks present at the point of migratory departure, highlighting an understudied importance of stopover sites to potential tick introduction or turnover. Taken together, the results presented here provide guiding information for further analysis into species specific interactions which will allow for the integration of individual level variation into understanding the risk of tick movement with migratory birds and potential for emergent disease. Data included here are the studies and the raw collected data in relation to the above mentioned project.

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For data acquisition, we searched SCOPUS and Web of Science (WoS) utilizing a standardized search term. Both databases were accessed on February 21st 2023 using the search string “Tick AND Bird AND Migration NOT America” for both databases. Processing was done in two rounds. First, all previously published reviews matching the criteria: (1) concerns hard ticks (Acarii:Ixodidae) infesting birds, and (2) research focused on the African-Western Palearctic flyways were taken. In total seven review articles were used and all references (n =363) from these were added to the primary research articles found through the SCOPUS and WoS queries. This lead to a total of 1024 studies which were then screened based on the following criteria: 1) remove duplicated publications, 2) provides primary data of hard ticks (Acarii:Ixodidae) infesting birds, 2) research focuses on African-Western Palearctic flyways, 3) study conducted during active migration period (March-May, August-October), 4) data on individual tick and bird species interactions provided, and 5) includes the number of birds caught per species. After screening, 35 studies met all criteria of which one had to be removed as it was unavailable. The data collected from the 34 studies included in the analyses were: 1) bird species, 2) tick species, 3) number of caught birds, 4) number of ticks infesting a given bird species per tick species and life-stage (if available), 5) migratory direction (Spring, Autumn, Combined) . To account for sampling effort between studies, we calculated a standardized tick value for each combination of tick and bird species present in the dataset. This was calculated as the number of ticks of a given species found on a given bird species divided by the total number of birds belonging to that species caught in the given study. To quantify the impact of bird families in moving specific tick genera, we utilized generalized linear mixed effects models (GLMM). The dataset was first filtered to only include bird species which were found in at least two independent studies (n=1046). Analysis was done in two parts, first a non-intercept GLMM was run including an interaction term for each bird family and tick genera reported to interact with each other from the collected data as a fixed effect. Random effects were included for mean year, number of birds caught, study identifier, country, and bird species. Mean year is defined as the mean of all years present in a study, i.e. if a study ran from 2010-2012 the year coded would be 2011. Prior to running the model, both mean year and number of birds caught were mean centered. The second GLMM retained the same random effect´s structure but instead included an interaction term between migratory direction and tick genus and only included data for which a clear migratory direction (i.e., spring or autumn) was apparent within the filtered dataset (n=809).

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