Ticks (Acari: Ixodidae) parasitizing migrating and local breeding birds in Finland

Ticks are globally renowned vectors for numerous zoonoses, and birds have been identified as important hosts for several species of hard ticks (Acari: Ixodidae) and tick-borne pathogens. Many European bird species overwinter in Africa and Western Asia, consequently migrating back to breeding grounds in Europe in the spring. During these spring migrations, birds may transport exotic tick species (and associated pathogens) to areas outside their typical distribution ranges. In Finland, very few studies have been conducted regarding ticks parasitizing migrating or local birds, and existing data are outdated, likely not reflecting the current situation. Consequently, in 2018, we asked volunteer bird ringers to collect ticks from migrating and local birds, to update current knowledge on ticks found parasitizing birds in Finland. In total 430 ticks were collected from 193 birds belonging to 32 species, caught for ringing between 2018 and 2020. Furthermore, four Ixodes uriae were collected from two roosting islets of sea birds in 2016 and 2020. Ticks collected on birds consisted of: Ixodes ricinus (n?=?421), Ixodes arboricola (4), Ixodes lividus (2) and Hyalomma marginatum (3). Ixodes ricinus loads (nymphs and larvae) were highest on thrushes (Passeriformes: Turdidae) and European robins (Erithacus rubecula). The only clearly imported exotic tick species was H. marginatum. This study forms the second report of both I. uriae and I. arboricola from Finland, and possibly the northernmost observation of I. arboricola from Europe. The importation of exotic tick species by migrating birds seems a rare occurrence, as over 97% of all ticks collected from birds arriving in Finland during their spring migrations were I. ricinus, a species native to and abundant in Finland.

     

The Impact of Climate Trends on a Tick Affecting Public Health: A Retrospective Modeling Approach for Hyalomma marginatum (Ixodidae)

The impact of climate trends during the period 1901–2009 on the life cycle of Hyalomma marginatum in Europe was modeled to assess changes in the physiological processes of this threat to public health. Monthly records of temperature and water vapour at a resolution of 0.5° and equations describing the life cycle processes of the tick were used. The climate in the target region affected the rates of the life cycle processes of H. marginatum: development rates increased, mortality rates in molting stages decreased, and the survival rates of questing ticks decreased in wide territories of the Mediterranean basin. The modeling framework indicated the existence of critical areas in the Balkans, central Europe, and the western coast of France, where the physiological processes of the tick improved to extents that are consistent with the persistence of populations if introduced. A spatially explicit risk assessment was performed to detect candidate areas where active surveys should be performed to monitor changes in tick density or persistence after a hypothetical introduction. We detected areas where the critical abiotic (climate) and biotic (host density) factors overlap, including most of the Iberian peninsula, the Mediterranean coast of France, eastern Turkey, and portions of the western Black Sea region. Wild ungulate densities are unavailable for large regions of the territory, a factor that might affect the outcome of the study. The risk of successfully establishing H. marginatum populations at northern latitudes of its current colonization range seems to be still low, even if the climate has improved the performance of the tick in these areas.     

Impact of climate change on risk of incursion of Crimean-Congo haemorrhagic fever virus in livestock in Europe through migratory birds

Aims: To predict the risk of incursion of Crimean‐Congo haemorrhagic fever virus (CCHFV) in livestock in Europe introduced through immature Hyalomma marginatum ticks on migratory birds under current conditions and in the decade 2075–2084 under a climate‐change scenario. Methods and Results: A spatial risk map of Europe comprising 14 282 grid cells (25 × 25 km) was constructed using three data sources: (i) ranges and abundances of four species of bird which migrate from sub‐Saharan Africa to Europe each spring, namely Willow warbler (Phylloscopus trochilus), Northern wheatear (Oenanthe oenanthe), Tree pipit (Anthus trivialis) and Common quail (Coturnix coturnix); (ii) UK Met Office HadRM3 spring temperatures for prediction of moulting success of immature H. marginatum ticks and (iii) livestock densities. On average, the number of grid cells in Europe predicted to have at least one CCHFV incursion in livestock in spring was 1·04 per year for the decade 2005–2014 and 1·03 per year for the decade 2075–2084. In general with the assumed climate‐change scenario, the risk increased in northern Europe but decreased in central and southern Europe, although there is considerable local variation in the trends. Conclusions: The absolute risk of incursion of CCHFV in livestock through ticks introduced by four abundant species of migratory bird (totalling 120 million individual birds) is very low. Climate change has opposing effects, increasing the success of the moult of the nymphal ticks into adults but decreasing the projected abundance of birds by 34% in this model. Significance and Impact of the Study: For Europe, climate change is not predicted to increase the overall risk of incursion of CCHFV in livestock through infected ticks introduced by these four migratory bird species.     

Detection of a questing <Emphasis Type="Italic">Hyalomma marginatum</Emphasis><Emphasis Type="Italic">marginatum</Emphasis> adult female (Acari,Ixodidae) in southern Germany

The first finding of a questing Hyalomma marginatum marginatum female tick in Germany is described. The tick was found in May 2006 on the clothing of a person who had spent the preceding day in rural surroundings in southern Germany. As the infested person had also been visiting Spain where H. m. marginatum is known to occur some weeks prior to finding the tick, it is not clear whether the tick had been imported by him as a female or by another host in a preimaginal stage and succeeded to develop to an adult in Germany. H. m. marginatum is a thermophilic tick species usually occurring in relatively dry and warm regions of southern Europe, northern Africa and some parts of Asia. It is a vector of several disease agents of human relevance including Crimean-Congo hemorrhagic fever virus. Although, by PCR examination, the female was found neither infected with this virus nor with Rickettsia aeschlimannii, another human pathogen which has been found in Spanish Hyalomma ticks, its mere finding should be taken seriously and draw further attention to the increasing problem of the import and spread of putatively tropical vectors of disease to central Europe.     

Hyalomma ticks on northward migrating birds in southern Spain: Implications for the risk of entry of Crimean‐Congo haemorrhagic fever virus to Great Britain

Crimean‐Congo haemorrhagic fever virus (CCHFV) is a zoonotic virus transmitted by Hyalomma ticks, the immature stages of which may be carried by migratory birds. In this study, a total of 12 Hyalomma ticks were recovered from five of 228 migratory birds trapped in Spring, 2012 in southern Spain along the East Atlantic flyway. All collected ticks tested negative for CCHFV. While most birds had zero Hyalomma ticks, two individuals had four and five ticks each and the statistical distribution of Hyalomma tick counts per bird is over‐dispersed compared to the Poisson distribution, demonstrating the need for intensive sampling studies to avoid underestimating the total number of ticks. Rates of tick exchange on migratory birds during their northwards migration will affect the probability that a Hyalomma tick entering Great Britain is positive for CCHFV. Drawing on published data, evidence is presented that the latitude of a European country affects the probability of entry of Hyalomma ticks on wild birds. Further data on Hyalomma infestation rates and tick exchange rates are required along the East Atlantic flyway to further our understanding of the origin of Hyalomma ticks (i.e., Africa or southern Europe) and hence the probability of entry of CCHFV into GB.     

Blood-sucking ticks (Acarina,Ixodoidea) as an essential component of the urban environment

The problem of urban ticks has arisen from the increased rate of urbanization since WWII. Expansion of municipal boundaries encompasses adjacent territories, so that large areas of wilderness together with all their inhabitants get incorporated into city limits. Current strategies of biodiversity conservation include the creation of green corridors and other forms of connectivity between wilderness and urban areas as well as between green patches within cities. All this allows various mammals and birds to migrate from their native habitats into and between various parts of the cities and to establish permanent urban populations. Medium-sized and larger animals provide adult ticks with blood meal, thus creating suitable conditions for the establishment and persistence of tick populations. Independent tick populations can exist in urban forests, parks, private properties, old cemeteries, etc. Over the last decades, the tick populations that originated from those in natural habitats around the cities have become a permanent component of urban fauna. Among such ticks, the castor bean tick Ixodes ricinus is the most important species for European cities, while the deer tick I. scapularis is of great significance for the East Coast of the United States. The taiga tick I. persulcatus is the most important species for the Russian cities and towns within its range. All these and some other ticks aggressively attack humans and their pets inside cities. The tick species especially well adapted to urban life are those which can live and reproduce in buildings. The brown dog tick Rhipicephalus sanguineus (family Ixodidae), the pigeon ticks from the reflexus group of the genus Argas, and Ornithodoros ticks (family Argasidae), which form urban and semi-urban populations, are the main urban tick pests and vectors. House infestation by ticks can lead to human infection with tick-borne pathogens or severe allergic reactions. Some tick hosts, mammals as well as birds, maintain tick-transmitted pathogens and serve as competent reservoir hosts. Urban populations of these animals can participate in the circulation of some pathogens within cities. Thus, the enlargement of urban green areas followed by their population by wild mammals and birds create good opportunities for the establishment of urban populations of tick vectors with the resulting threat to the health of urban dwellers and their pets. At the same time, our understanding of the real scope and complexity of the problem of urban ticks is far from being sufficient. Finding the ways of protecting the environment without increasing the risk to human health in modern cities is a pressing and challenging problem of our time.     

Ticks collected from migratory birds,including a new record of Haemaphysalis formosensis,on Jeju Island,Korea

Migratory birds may disperse parasites across ecological barriers, and recent climate change may alter the pattern of ectoparasite dispersal via changed patterns of bird migration. In order to document the parasitization of migratory birds by Ixodidae ticks on Jeju Island in Korea, we examined 934 migratory birds comprising 75 species for ticks from 2010 to 2012. In total, 313 ticks were collected from 74 migratory birds across 17 avian species and identified based on morphological keys. These ticks represented six species: Haemaphysalis flava, H. formosensis, H. longicornis, H. concinna, Ixodes turdus and I. nipponensis. Of particular note was the presence of H. formosensis, a species not previously reported to have been found in Korea, and H. concinna, which had not been previously reported on Jeju Island. The dominant tick species found were H. flava (226 ticks, 72.2 %) and I. turdus (54 ticks, 17.3 %), and ground-dwelling thrushes such as Pale thrushes (Turdus pallidus; 39 birds, 52.7 %) were the most important hosts. Although H. longicornis is the most abundant and prevalent terrestrial tick on Jeju Island, the species accounted for only 3.8 % of the total ticks collected in this study, suggesting that ticks on migratory birds may differ from the local tick fauna and that exotic ticks may be introduced via migratory birds. Therefore, long-term programs for tick and tick-borne disease surveillance are recommended to understand the role of migratory animals in the introduction of exotic species and associated pathogens and in life cycles of ticks at different stages in this region.     

Agricultural intensification and the collapse of Europe's farmland bird populations

The populations of farmland birds in Europe declined markedly during the last quarter of the 20th century, representing a severe threat to biodiversity. Here, we assess whether declines in the populations and ranges of farmland birds across Europe reflect differences in agricultural intensity, which arise largely through differences in political history. Population and range changes were modelled in terms of a number of indices of agricultural intensity. Population declines and range contractions were significantly greater in countries with more intensive agriculture, and significantly higher in the European Union (EU) than in former communist countries. Cereal yield alone explained over 30% of the variation in population trends. The results suggest that recent trends in agriculture have had deleterious and measurable effects on bird populations on a continental scale. We predict that the introduction of EU agricultural policies into former communist countries hoping to accede to the EU in the near future will result in significant declines in the important bird populations there.     

A bird distribution model for ring recovery data: where do the European robins go?

For the study of migratory connectivity, birds have been individually marked by metal rings for more than 100 years. The resulting ring recovery data have been compiled in numerous bird migration atlases. However, estimation of what proportion of a particular population is migrating to which region is confounded by spatial heterogeneity in ring recovery probability. We present a product multinomial model that enables quantifying the continent‐wide distribution of different bird populations during different seasons based on ring recovery data while accounting for spatial heterogeneity of ring recovery probability. We applied the model to an example data set of the European robin Erithacus rubecula. We assumed that ring recovery probability was equal between different groups of birds and that survival probability was constant. Simulated data indicate that violation of the assumption of constant survival did not affect our estimated bird distribution parameters but biased the estimates for recovery probability. Posterior predictive model checking indicated a good general model fit but also revealed lack of fit for a few groups of birds. This lack of fit may be due to between‐group differences in the spatial distribution on smaller scales within regions. We found that 48% of the Scandinavian robins, but only 31% of the central European robins, wintered in northern Africa. The remaining parts of both populations wintered in southern and central Europe. Therefore, a substantial part of the Scandinavian population appears to leap over individuals from the central European population during migration. The model is applied to summary tables of numbers of ringed and recovered birds. This allows us to handle very large data sets as, for example, those presented in bird migration atlases.     

An Integrative Eco-Epidemiological Analysis of West Nile Virus Transmission

West Nile disease, caused by the West Nile virus (WNV), is a mosquito-borne zoonotic disease affecting humans and horses that involves wild birds as amplifying hosts. The mechanisms of WNV transmission remain unclear in Europe where the occurrence of outbreaks has dramatically increased in recent years. We used a dataset on the competence, distribution, abundance, diversity and dispersal of wild bird hosts and mosquito vectors to test alternative hypotheses concerning the transmission of WNV in Southern France. We modelled the successive processes of introduction, amplification, dispersal and spillover of WNV to incidental hosts based on host–vector contact rates on various land cover types and over four seasons. We evaluated the relative importance of the mechanisms tested using two independent serological datasets of WNV antibodies collected in wild birds and horses. We found that the same transmission processes (seasonal virus introduction by migratory birds, Culex modestus mosquitoes as amplifying vectors, heterogeneity in avian host competence, absence of ‘dilution effect’) best explain the spatial variations in WNV seroprevalence in the two serological datasets. Our results provide new insights on the pathways of WNV introduction, amplification and spillover and the contribution of bird and mosquito species to WNV transmission in Southern France.     

Effects of livestock farming on birds of rural areas in Europe

In the last decades, profound modifications of agricultural practices occurred in Europe, including the introduction of modern livestock farming. These modifications negatively affected the fauna of rural areas, as indicated by the large demographic declines suffered by several populations of birds typical of these habitats. The impact of agricultural practices on bird populations has been widely investigated, while the effect of livestock farming has seldom been assessed. To fill this gap, we carried out a quantitative meta-analysis of the existing scientific literature and evaluated the size of the effects of livestock farming on birds of rural areas in Europe. We only found 26 papers on this topic, from which 72 effect sizes could be estimated. The barn swallow (Hirundo rustica) was the species on which most studies focused. Livestock farming positively influenced presence and distribution of barn swallows in breeding habitats, while it did not significantly affect reproduction of this species. Effects on other bird species typical of rural habitats were non-significant. The positive effect on the insectivorous barn swallow might be mediated by the enhanced insect abundance where livestock is reared. In addition, habitat features typical of rural settings where livestock is reared (e.g. cattle-sheds or large hayfields) positively affected barn swallows independently of actual presence of livestock at a setting. Presence of livestock at rural setting therefore seems beneficial to barn swallows, but not significantly to other bird species typical of rural habitats. The effect of livestock farming on birds of rural habitats has been under-investigated to date.     

Experimental evaluation of birds as disseminators of the cosmopolitan tick Rhipicephalus sanguineus (Acari: Ixodidae)

Rhipicephalus sanguineus is believed to be the most widespread tick species of the world and its dissemination seems to rely on the diffusion of its main host, the dog. Empirical observations indicate that several bird species in urban areas regularly steal dog food. Such circumstances create a chance for R. sanguineus ticks to climb on birds and carry ticks to another site. In this work we evaluated experimentally the likelihood of birds (chicks) to either feed and/or carry R. sanguineus ticks from an infested site to another and to infest a host (rabbit) in the new location. Chicks were not suitable hosts for R. sanguineus ticks. Not a single adult tick engorged on chicks, yield as well as weight of engorged larvae and nymphs were very low and feeding period of these ticks was very long. However, a few larvae and, chiefly, nymphs were delivered to a new location either mechanically or after attachment and engorging total or partially on chicks. A few of these ticks fed successfully on rabbits. Further evidence on the capacity of birds to introduce R. sanguineus into non-infested dog settings should be provided by systematic examination of birds from urban areas, close to tick infested households.     

Agricultural intensification and farmland birds: new insights from a central European country

The relationship between agricultural intensification and a decline in farmland bird populations is well documented in Europe, but the results are mostly based on data from the western part of the continent. In the former socialist eastern and central European countries, political changes around 1990 resulted in a steep decline in the intensity of agriculture. Therefore, one would expect populations of farmland birds to have recovered under these conditions of lower agricultural intensity. We explored population trends of 19 farmland bird species in the Czech Republic between 1982 and 2003 using data from a large‐scale monitoring scheme, and, additionally, we looked for relationships between such population changes and a number of variables describing the temporal development of Czech agriculture. Most farmland species declined during the focal period, and this decline was steepest in farmland specialists (Northern Lapwing Vanellus vanellus, Skylark Alauda arvensis, Linnet Carduelis cannabina and Yellowhammer Emberiza citrinella). Although the intensity of agriculture was lower after than before 1990, the overall decline continued in most farmland bird species, albeit at a slower rate. The correlations between agricultural intensity and farmland bird decline showed opposite patterns to that found in other European studies, because bird populations were highest in years with the most intensive agriculture. We speculate that this pattern could have resulted from the impact of different driving forces causing farmland bird decline in different periods. The high intensity of agriculture could have caused the decline of the originally abundant populations before 1990. After 1990, the decreasing area of arable land could be the most important factor resulting in the continued decline of farmland bird populations. Our results demonstrate that the drivers of farmland bird population changes could differ across Europe, and thus investigations into the effect of farmland management in different parts of the continent are urgently required.     

Blackbirds and Song Thrushes Constitute a Key Reservoir of Borrelia garinii, the Causative Agent of Borreliosis in Central Europe

Blackbirds (Turdus merula) and song thrushes (Turdus philomelos) were found to carry 95% of all spirochete-infected tick larvae among 40 bird species captured in Central Europe. More than 90% of the infections were typed as Borrelia garinii and Borrelia valaisiana. We conclude that thrushes are key players in the maintenance of these spirochete species in this region of Central Europe.     

Dissemination of Spotted Fever Rickettsia Agents in Europe by Migrating Birds

Migratory birds are known to play a role as long-distance vectors for many microorganisms. To investigate whether this is true of rickettsial agents as well, we characterized tick infestation and gathered ticks from 13,260 migratory passerine birds in Sweden. A total of 1127 Ixodes spp. ticks were removed from these birds and the extracted DNA from 957 of them was available for analyses. The DNA was assayed for detection of Rickettsia spp. using real-time PCR, followed by DNA sequencing for species identification. Rickettsia spp. organisms were detected in 108 (11.3%) of the ticks. Rickettsia helvetica, a spotted fever rickettsia associated with human infections, was predominant among the PCR-positive samples. In 9 (0.8%) of the ticks, the partial sequences of 17kDa and ompB genes showed the greatest similarity to Rickettsia monacensis, an etiologic agent of Mediterranean spotted fever-like illness, previously described in southern Europe as well as to the Rickettsia sp.IrITA3 strain. For 15 (1.4%) of the ticks, the 17kDa, ompB, gltA and ompA genes showed the greatest similarity to Rickettsia sp. strain Davousti, Rickettsia japonica and Rickettsia heilongjiangensis, all closely phylogenetically related, the former previously found in Amblyomma tholloni ticks in Africa and previously not detected in Ixodes spp. ticks. The infestation prevalence of ticks infected with rickettsial organisms was four times higher among ground foraging birds than among other bird species, but the two groups were equally competent in transmitting Rickettsia species. The birds did not seem to serve as reservoir hosts for Rickettsia spp., but in one case it seems likely that the bird was rickettsiemic and that the ticks had acquired the bacteria from the blood of the bird. In conclusion, migratory passerine birds host epidemiologically important vector ticks and Rickettsia species and contribute to the geographic distribution of spotted fever rickettsial agents and their diseases.     

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.     

Tick survey and detection of Crimean-Congo hemorrhagic fever virus in tick species from a non-endemic area, South Marmara region, Turkey

Crimean-Congo hemorrhagic fever (CCHF) is an increasing health concern in Turkey since 2002. There were also some recent human cases from the South Marmara region of Turkey; thus, a tick survey was performed, and possible vector tick species for the CCHF virus were determined in the region. A total of 740 adult ticks were collected from infested livestock from five locations: Çanakkale-Biga, Bursa-Orhaneli, Bursa-Keles, Bal?kesir and Bilecik. Total of 11 tick species from the genera Hyalomma, Rhipicephalus, Dermacentor, Ixodes and Haemaphysalis were identified. Rhipicephalus ticks were dominant in the region; the most frequently observed tick species was R. turanicus, (53.1 %), and only 15.4 % of the identified ticks were H. marginatum. The occurrence of H. rufipes infestation in the region fort he first time. A total of 73 pools of adult ticks were tested with both an antigen-detecting ELISA and RT real-time PCR (RT rt PCR). The presence of the CCHF virus was demonstrated in 9 (12.3 %) of the tested tick pools. Although seven of the tick pools were positive for the CCHF virus with both of the methods, one pool was positive only with RT rt PCR and the other pool was only positive with the ELISA. Positive results were obtained from ticks collected from cattle, sheep and goats from two locations, Bursa-Orhaneli and Bilecik. The CCHF virus was detected in R. turanicus (n = 3), R. bursa (n = 2), H. marginatum (n = 2) and D. marginatus (n = 2) ticks. The results of this study confirm the presence of the CCHF virus and present preliminary data on the vector tick species in the southern Marmara region of Turkey.     

Birds as hosts of ixodid ticks (Acarina,Ixodidae)

rophic relations between ixodid ticks of the world fauna parasitizing as adults on birds are analyzed. These ticks include 60 out of 650 species of the family Ixodidae and belong to the genera Ixodes, Haemaphysalis, and Amblyomma. Relations between birds and ticks of the genus Ixodes are most ancient. Colonial marine birds seem to be the first hosts of ixodid ticks in the class of birds. Trophic specialization of ticks is not associated with bird taxa, because in most cases no tick specificity is caused by either phylogenetic features of hosts, or specific environmental conditions.     

Effects of forest fragmentation on European birds: implications of regional differences in species richness

Aim In this paper, we adopted a large‐scale approach to evaluate the effect of regional richness of forest birds on the number of bird species retained by forest fragments in several localities across Europe. Location We studied bird assemblages in fourteen forest archipelagos embedded in agricultural matrices from southern Norway to central Spain. Tree composition varied from oak and beech forests of the northern localities to oak and pine xerophitic woodlands of the southern ones. The number of fragments in each forest archipelago ranged from eighteen to 211. Methods We used the Gleason equation (s = a + z log A; where s and A are, respectively, the species richness and size of forest fragments and z the rate of species loss) to estimate the species richness for 1‐ and 15‐ha fragments in each archipelago. The regional richness of forest birds was estimated by modelling the geographical distribution of species richness in the European atlas of breeding birds. Results The latitudinal distribution of regional richness displayed a convex form, with the highest values being in central Europe. Along this gradient, the number of species retained by fragments and the rate of species loss was positively related to regional richness. In addition, the percentage of the regional pool of species sampled by fragments decreased in the southern localities. Main conclusions Relationships between regional richness of forest birds and richness in fragments seem to explain why fragments in central Europe shelter more species than their southern counterparts. The decreased ability of southern forest fragments to sample the regional richness of forest birds, could be explained as an effect of the low abundance of many species in the Mediterranean, which could depress their ability to prevent extinction in fragments by a rescue effect. Alternatively, high beta diversity in the Mediterranean could produce undersampling by fragments of the regional pool of species. These regional differences in the response of bird assemblages to forest fragmentation are used to discuss the usefulness of large‐scale, biogeographical approaches in the design of conservation guidelines.