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Hard ticks (Acari: Ixodidae) associated with birds in Europe: Review of literature data

Hard ticks (Acari: Ixodidae) are considered the most important transmitters of pathogens in the temperate zone that covers most of Europe. In the era of climate change tick-borne diseases are predicted to undergo geographical range expansion toward the north through regions that are connected to southern areas of the continent by bird migration. This alone would justify the importance of synthesized knowledge on the association of tick species with avian hosts, yet birds also represent the most taxonomically and ecologically diverse part of urban vertebrate fauna. Birds frequently occur in gardens and near animal keeping facilities, thus playing a significant role in the dispersal of ticks and tick-borne pathogens in synanthropic environments. The primary aim of this review is to provide a comprehensive reference source (baseline data) for future studies, particularly in the context of discovering new tick-host associations after comparison with already published data. The records on the ixodid tick infestations of birds were assessed from nearly 200 papers published since 1952. In this period, 37 hard tick species were reported from 16 orders of avian hosts in Europe. Here we compile a list of these tick species, followed by the English and Latin name of all reported infested bird species, as well as the tick developmental stage and country of origin whenever this information was available. These data allowed a first-hand analysis of general trends regarding how and at which developmental stage of ticks tend to infest avian hosts. Five tick species that were frequently reported from birds and show a broad geographical distribution in the Western Palearctic (Ixodes arboricola, I. frontalis, I. ricinus, Haemaphysalis concinna and Hyalomma marginatum) were also selected for statistical comparisons. Differences were demonstrated between these tick species regarding their association with bird species that typically feed from the ground and those that rarely occur at the soil level. The ecology of these five bird-infesting tick species is also illustrated here according to avian orders, taking into account the ecology (habitat type) and activity (circadian rhythm and feeding level) of most bird species that represent a certain order.

Hard ticks (Acari: Ixodidae) are considered the most important transmitters of pathogens in the temperate zone that covers most of Europe. In the era of climate change tick-borne diseases are predicted to undergo geographical range expansion toward the north through regions that are connected to southern areas of the continent by bird migration. This alone would justify the importance of synthesized knowledge on the association of tick species with avian hosts, yet birds also represent the most taxonomically and ecologically diverse part of urban vertebrate fauna. Birds frequently occur in gardens and near animal keeping facilities, thus playing a significant role in the dispersal of ticks and tick-borne pathogens in synanthropic environments. The primary aim of this review is to provide a comprehensive reference source (baseline data) for future studies, particularly in the context of discovering new tick-host associations after comparison with already published data. The records on the ixodid tick infestations of birds were assessed from nearly papers published since . In this period, hard tick species were reported from orders of avian hosts in Europe. Here we compile a list of these tick species, followed by the English and Latin name of all reported infested bird species, as well as the tick developmental stage and country of origin whenever this information was available. These data allowed a first-hand analysis of general trends regarding how and at which developmental stage of ticks tend to infest avian hosts. Five tick species that were frequently reported from birds and show a broad geographical distribution in the Western Palearctic (Ixodes arboricola, I. frontalis, I. ricinus, Haemaphysalis concinna and Hyalomma marginatum) were also selected for statistical comparisons. Di erences were demonstrated between these tick species regarding their association with bird species that typically feed from the ground and those that rarely occur at the soil level. The ecology of these five bird-infesting tick species is also illustrated here according to avian orders, taking into account the ecology (habitat type) and activity (circadian rhythm and feeding level) of most bird species that represent a certain order.

Background
Hard ticks (Acari: Ixodidae) are considered the most important vectors (transmitters) of pathogens under the temperate zone (1) including most of Europe. In the era of climate change (global warming), vector-borne diseases in general, and tick-borne disease in particular are predicted to undergo dramatic changes in geographical distribution (2, 3) mostly implying range expansion of tick species toward more northern latitudes. In such scenarios birds may play the most important role in tick dispersal over both short and long distances due to their migratory habits (4). Passeriform birds can carry significant numbers of ticks [in a large scale study this was up to 20 ticks per bird: (5)]. These ticks are mostly larvae and nymphs of generalist (non-ornithophilic) tick species. These ticks may remain on their avian host for a period raging from a few days (in case of larvae of three-host tick species exemplified by Ixodes ricinus) to even 5 weeks or longer [in case of two-host ticks species, e.g., Hyalomma rufipes: (6)]. While most studies focus on tick species carried by birds during their spring migration from the southern wintering grounds toward the north in Europe, tick "transportation" by birds may equally be important in western, eastern, and north-to-southern directions (5).
If thermophilic ticks carried by birds from south to north detach after engorgement, and find themselves in a suitable (warm enough) environment, they can molt to the next developmental stage. These ticks may then survive through mild winters, potentially establishing new, northern populations (7). This may contribute to the increased risks and evident changes of tick-borne pathogen transmission due to climate warming and tick dispersal by migratory birds, even in northern Europe (8).
On the other hand, several bird-specialist (ornithophilic) Ixodes species occur in the Western Palearctic, most of which associate with sea birds in Western Europe (e.g., I. uriae, I. caledonicus, I. rothschildi). These ticks occur in and near avian nests, or are frequently endophilic and live in tree holes or burrows inhabited by nesting birds, particularly in the subgenus Pholeoixodes (e.g., I. arboricola, I. lividus) (9). Since the avian hosts of tick species are expected to be less affected by climate change in terms of their geographical distribution, ornithophilic ticks will likely undergo less significant changes in their geographical occurrence than generalist tick species carried by birds. In addition, ornithophilic ticks seldom infest humans or domestic mammals [e.g., I. frontalis: (10)] and thus may have a less important epidemiological role from a veterinary-medical point of view.
This review focuses on hard ticks reported from birds in Northern, Western, Central, and Southern Europe, in the hope that the checklist will provide useful baseline information for future scientific research in the topics of ticks and tick-borne pathogens. Nearly 700 scientific papers published since 1952 were checked for this review. Soft ticks (Acari: Argasidae) were not included in this review, because in the majority of cases these are reported from the environment and thus data on their association with avian host species are not representative.

Methods
The primary corpus of publications used in this review was collated with database search using the following keywords: "ticks" OR "Ixodidae" OR "Ixodes" OR "Hyalomma" OR "Haemaphysalis" AND "birds" AND "Europe, " followed by a search with names of bird-specialist tick species (I. arboricola, I. caledonicus, I. eldaricus, I. festai, I. frontalis, I. lividus, I. rothschildi, I. unicavatus and I. uriae). The following databases were used: Web of Science, Zoological Record, and Google Scholar. These records were imported into an Excel file, followed by screening the publications and references cited within. After exclusion of duplicates, we extracted each individual bird hosttick record from these references, noting the location (country), host and parasite species and developmental stage of ticks.
Within Prostriata and Metastriata, tick species names are arranged alphabetically and are used sensu Guglielmone et al. (10). Ixodes redikorzevi is considered as a synonym of I. acuminatus. Data were only included in the checklist if the tick collected from a bird was reported as identified to the species level. E.g., in Norway a rare finding was mentioned, the occurrence of a Dermacentor sp. on a willow warbler (Phylloscopus trochilus) (11), but this was excluded from the main text.
Bird species as hosts of a certain tick species are listed alphabetically according to their international English name (https://bou.org.uk/british-list/bird-names/). When higher avian taxa are mentioned, these follow the phylogenetic order based on Kuhl et al. (12), starting with Passeriformes. Genus names are not abbreviated in the headings, owing to the high number and mixed usage of host and tick Latin names, also taking into account that scientists from a broad range of biology-related fields may use this checklist. Whenever a bird species was mentioned by its binominal name in an article, this was used for identification, even if the English name was also written in the text. English and Latin host species names are followed by tick developmental stages if this information was available (L: larva, N: nymph, M: male, F: female, A: adult [where there was no information about the sex of the adult tick)]. The abbreviation "NA" is used to indicate that no data were available about the sex and developmental stage of ticks collected from birds. If a tick species was reported from bird(s) in a country without mentioning avian host species, an exclamation mark (!) follows the country name in the list.
If tick species infesting a certain bird species are mentioned in a reference but only some of the data inform about the tick developmental stage, only these were incorporated into the text. It is also noteworthy that in some reports blood meal analysis allowed the identification of previous tick hosts. In addition, data on ticks reported from bird nests are included and marked in the text as "in nest": these ticks probably also originate from or can associate with birds. The geographical area covered by this review is in the Western Palearctic, excluding North Africa, the Middle East, Belarus and Russia but including Ukraine. Cyprus however, is also considered. Not just because it is partially European territory, but due to the fact that the island has a high epidemiological significance concerning the aim of this manuscript. Regarding geographical names, old references often refer to Czechoslovakia, which no longer exists. In cases when it was unambiguous whether the samples came from the Czech Republic or Slovakia, the country is mentioned as such. To maintain the user friendliness of this checklist the broader Palearctic distribution, general ecology, and vector role of tick species are not mentioned. This is because this information is available in other sources [e.g., (9)].

Ixodes acuminatus
Overview: Ixodes acuminatus is distributed in temperate and Mediterranean Europe (8). Accordingly, this tick species is occasionally found on birds in South-European countries. Based on literature data it is mainly a parasite of passeriform birds (from this order 15 species have been shown as hosts) but has also been found twice on galliform birds.

Ixodes arboricola
Overview: Ixodes arboricola is widespread throughout Europe. As its English name suggests, the Tree-hole tick is primarily a parasite of hole-nesting birds (8). Literature data usually support this theory, as I. arboricola was mostly found on passeriform (35 species), strigiform (5 species), piciform (1 species), and columbiform (1 species

Ixodes berlesei
Overview: According to literature data, I. berlesei was reported from birds in France. Unfortunately, the source article (18) is not accurate about the host species, but we do know that they belong to the Columbiformes order.

Ixodes caledonicus
Overview: Ixodes caledonicus is an ornithophilic tick species (10). It is primarily a parasite of the northern European bird fauna. Despite the limited data available, the host range appears to be broad: it has been reported from 6 passeriform, 3 falconiform, 1 caprimulgiform, and one procellariiform bird species. Passeriformes

Ixodes canisuga
Overview: Ixodes canisuga is primarily a parasite of mammals (8) and it is relatively rare on birds. So far, it has been found on 5 passeriform and on 2 strigiform hosts. Passeriformes

Ixodes eldaricus
Overview: Ixodes eldaricus is a rare, poorly known tick species. The only available data about this parasite feeding

Ixodes festai
Overview: Ixodes festai is a poorly known species that was reported from 5 passeriform birds, mostly in Central European countries. Passeriformes

Ixodes frontalis
Overview: Ixodes frontalis has a pan-European distribution. However, it appears to be more frequent in warmer regions. It is an ornithophilic tick species that rarely feeds on other, exceptional hosts (10). As such, it is commonly found on birds, mostly on Passeriformes, but the host range appears to be broad. Passeriformes

Ixodes hexagonus
Overview: Ixodes hexagonus is a common parasite of European foxes and hedgehogs (8). In the United Kingdom, this tick was reported from 5 passeriform, 1 galliform, 1 falconiform, 1 columbiform and, 1 strigiform birds. Whereas, in Spain it was reported from 1 galliform bird. This tick species was also found on a bird in Germany but no information is available on the host species.

Ixodes lividus
Overview: Ixodes lividus has a pan-European distribution, and it is the host-specific parasite of the sand martin (Riparia riparia). In Poland, it has been found on a Barn swallow (Hirundo rustica) as well. Passeriformes

Ixodes persulcatus
Overview: Ixodes persulcatus is widely distributed in the Northern European region (Russia, Scandinavia, and the Baltic region) (8). According to literature data however, it should be considered as a rare parasite of birds in Europe. It was reported only from 2 passeriform bird species. Passeriformes

Ixodes rothschildi
Overview: Ixodes rothschildi has so far been reported from birds only in the United Kingdom and France. This tick species is a parasite of seabirds, collected from 4 charadriiform, 1 suliform, and 1 procellariform species. Charadriiformes

Ixodes unicavatus
Overview: Ixodes unicavatus is distributed in the coastal area of the UK, Sweden and France. The hosts are birds that usually nest on rocky cliffs. Six of such bird species have been described as hosts of this parasite. Charadriiformes

Ixodes uriae
Overview: Ixodes uriae is a common parasite of North European seabirds, as it was reported from 8 charadriiform, 1 anseriform, 3 suliform, and 1 procellariform bird species. According to the data it was also recorded from 2 passeriform bird species. Charadriiformes

Ixodes ventalloi
Overview: Ixodes ventalloi, commonly known as the rabbit tick as it mostly feeds on the European rabbit (Oryctolagus cuniculus), is a rare finding on birds (8). This tick species has been recorded from 11 bird species. Four species belong to the order Strigiformes, which are often in contact with small mammals. Strigiformes

Amblyomma lepidum
Overview: While the immature stages of Amlyomma lepidum are relatively common bird parasites in Africa (10)

Amblyomma marmoreum
Overview: Amblyomma marmoreum is an African tick species, where it was reported from several bird species (10). In Europe, it has been found on a Tree pipit in Italy.

Amblyomma nuttalli
Overview: Amlyomma nuttali is distributed in the Afrotropical region, where they may infest several bird species (10). So far, we have only one report in Europe, where it was found on a Thrush nightingale (Passeriformes). Passeriformes

Dermacentor marginatus
Overview: Dermacentor marginatus is a common parasite throughout Europe, but not in Scandinavia (8). Despite this fact, it is rare to find these ticks on birds. D. marginatus has been reported from 1 passeriform and 1 galliform bird species, as well as from the nest of a passeriform bird.

Haemaphysalis concinna
Overview: Haemaphysalis concinna has a pan-European distribution. Interestingly, H. concinna seems to be extremely common on birds in Hungary, compared to other European countries. This parasite was reported from 36 different bird species so far. Thirty-three of these belong to the order Passeriformes. Passeriformes

Haemaphyalis erinacei
Overview: Haemaphysalis erinacei (as its name suggests) is mainly a parasite of hedgehogs and small mammals (8). Finding this tick on birds is a rare event. So far, it has been reported from the South-Eastern European region, where H. erinacei was found on on 4 different bird species. Interestingly, these 4 birds belonged to 4 different orders. Caprimulgiformes

Haemaphyalis parva
Overview: Haemaphysalis parva is a rare tick species on European birds. In Romania, it was found on 2 passeriforms, and on 1 galliform bird.

Haemaphysalis punctata
Overview: Haemaphysalis punctata has a pan-European distribution, and its immature stages are fairly common parasites on birds, especially on Passeriformes. Passeriformes

Haemaphyalis sulcata
Overview: Haemaphysalis sulcata is a relatively rare parasite on birds. According to literature data, it has been recorded from 5 passeriform bird species so far. Passeriformes

Hyalomma aegyptium
Hosts: Overview: Although Hyalomma aegyptium is a common tick in the Mediterranean region, it is primarily a parasite of tortoises and humans (8). Therefore, finding these ticks on European birds is an uncommon event. The only European report of this tick feeding on birds so far is from Greece, where this parasite has been reported from 2 passeriform species. Passeriformes

Hyalomma lusitanicum
Overview: Hyalomma lusitanicum is a common parasite of mammals in Spain and Portugal (8,10). Despite this fact, finding this tick species on bird is occasional. So far, it has been recorded from 2 galliform, 1 passeriform, 1 strigiform, 1 struthioniform and 1 columbiform birds from the Iberian Peninsula. Passeriformes

Hyalomma rufipes
Overview: Hyalomma rufipes is a two-host tick species (8). It is a widely distributed, common bird parasite in the Mediterranean region. It isc occasionally reported on migrating birds from Northern European countries as well. Similarly to H. marginatum [in the past, H rufipes was considered as a subspecies of H. marginatum

Hyalomma truncatum
Overview: There is very limited information about Hyalomma truncatum as a bird parasite. According to the data, it has been found on a passeriform bird in Italy.

Rhipicephalus annulatus
Overview: Despite the fact that Rhipicephalus annulatus is distributed in Southern-Europe (8) it is amazingly rare for this parasite to feed on birds. So far, only one such case was documented in Portugal. Galliformes

Rhipicephalus pusillus
Overview: Rhipicephalus pusillus is found in the Palaearctic region, mainly in Mediterranean climatic areas where birds are considered to be exceptional hosts (8). So far, this was recorded only once.

Rhipicephalus sanguineus
Overview: Rhipicephalus sanguineus s.l. is the most common tick species found on dogs in urban areas around the world (8). However, finding them on birds is rare. So far, it has been recorded from a total of 6 bird species, belonging to 4 different orders. Struthioniformes

Rhipicephalus turanicus
Overview: The taxonomic status of Rhipicephalus turanicus is still under discussion (8). According to literature data, this tick species has been found on three bird species (all birds of prey) in Portugal and in Bulgaria. However, the Portuguese findings (85) were referred to in a later article by the same author (60)

Conclusions
In this review data on the ixodid tick infestation of birds were collected from nearly 200 papers published since 1952. In this period, 37 hard tick species (17 from Prostriata and 20 from Metastriata) were reported from 16 orders of avian hosts in Europe. These include endophilic tick species that are ornithophilic (I. arboricola, I. caledonicus) or those that prefer mammalian hosts, such as rodents (I. acuminatus), The primary aim of this checklist is to provide a comprehensive reference source (baseline data) for future studies, particularly in the context of discovering new tickhost associations after comparison with already published data. Nevertheless, these data also allow a first-hand analysis of general trends regarding how and which developmental stage of ticks tend to infest avian hosts in general. Therefore, five tick species that were frequently reported from birds and show a broad geographical distribution on this continent were selected for statistical comparison (I. arboricola, I. frontalis, I. ricinus, H. concinna and H. marginatum) (Supplementary Figure 1; Supplementary Table 1).
Considering developmental stages, larvae and nymphs predominate on birds in the case of I. ricinus, H. concinna, and H. marginatum (n = 1,667 vs. 37 adults). This is not the case for ornithophilic tick species (I. arboricola and I. frontalis) from which adult ticks were collected significantly more frequently (n = 301 vs. 115 adults) (P < 0.0001). Interestingly, males of generalist tick species occurred significantly more frequently on birds (n = 7 vs. 30 females) than males of ornithophilic tick species (n = 5 vs. 110 females) (P = 0.009).
Based on data that did not specify the tick developmental stage, the tick species I. arboricola was significantly (P < 0.0001) more frequently collected from bird species that typically feed above the ground (n = 134) than from those feeding at the ground level (n = 60). This was not the case for I. ricinus  Table 1). This general tendency on a continental level is in contrast to what was reported from the southern part of Central Europe where H. concinna is mostly associated with bird species typically feeding above the ground level (65,127). The chances for finding H. marginatum on bird species characterized by either ground-feeding or arboreal feeding were more equilibrated (82 vs. 84). This is in line with its active host seeking (hunting) strategy (8).
In addition, considering data from references that included the number of tick developmental stages collected from various bird species, comparison of tick infestations according to five habitat categories of avian hosts (Supplementary Table 1) did not reveal statistically significant associations (data not shown). However, by assigning bird species into two groups (i.e., typically feeding from the ground vs. rarely occurring at the soil level: Supplementary Table 1), the following differences were found: Larvae, nymphs and females of I. arboricola significantly more frequently occur on bird species feeding above the ground (P < 0.0001-0.045), than corresponding stages of I. frontalis, I. ricinus and H. concinna. Females of I. ricinus are more likely to infest ground-feeding than arboreal bird species (18 vs. 4) compared to nymphs of this species (507 vs. 336) (P = 0.046). Interestingly, females of H. marginatum significantly more frequently associate with bird species feeding above the ground level than with those collecting food on the soil surface (4 vs. 1) compared to those of I. ricinus (4 vs. 18) (P = 0.017) and I. frontalis (27 vs. 61) (P = 0.041).
The ecology of bird-infesting tick species (8) is also illustrated here according to avian orders (Supplementary Figure 1), taking into account the ecology (habitat type) and activity (circadian rhythm and feeding level) of most bird species that belong to a certain order (203) (though this has limitations due to difficulties in assigning general traits at this taxonomic level). In this context, I. arboricola was only reported from species of avian orders whose members typically use forested habitats and (with the exception of Columbiformes) typically feed above the ground (Supplementary Figure 1). This tick species was also reported from a high number of nocturnal bird species (Strigiformes), although (as an endophilic tick, with preference for tree holes) it is known to detach from diurnal passerine hosts during the night (50). Except for two bird species from two orders (Falconiformes, Coraciiformes), I. frontalis was always reported from avian orders whose members typically (also) feed from the ground level, in both open and forested habitats (Supplementary Figure 1). This is in line with previous data on I. frontalis from Central Europe (65). By contrast, I. ricinus was reported from 13 out of 16 avian orders, including several examples with preference for forest or open habitats, and which typically feed at the ground level or higher (Supplementary Figure 1). Similarly, the majority of avian hosts that were reported to be infested with H. concinna represent orders that share both open habitatand forest-dwelling bird species, as well as ground level and arboreal feeders (Supplementary Figure 1). Last but not least, H. marginatum was almost exclusively reported from bird species that belong to orders including a significant number of forest dweller bird species and was also collected from a high number of bird species from orders with nocturnal activity (both Caprimulgiformes and Strigiformes: Supplementary Figure 1). This is in agreement with the reported evening activity and occurrence of this tick species in forested habitats (204).

Data availability statement
The original contributions presented in the study are included in the article/Supplementary material, further inquiries can be directed to the corresponding author/s.

Ethics statement
Ethical review and approval was not required for the animal study because the study is based on a bibliographic review, no physical animals were handled.

Author contributions
GK: conceptualization, study design, data curation, and manuscript writing. AS: study design, statistical analyses, ornithological data, and collection of literature data. SH: conceptualization, study design, editing, statistical analyses, and manuscript writing. All authors contributed to the article and approved the submitted version.

Funding
This study was funded by Project no. TKP2020-NKA-01 implemented with the support provided from the National Research, Development and Innovation Fund of Hungary, financed under the Tématerületi Kiválósági Program 2020 (2020-4.1.1-TKP2020) funding scheme. SH and AS were supported by OTKA K-132794 of the National Research, Development and Innovation Office. The Project is supported by the European Union and cofinanced by the European Social Fund (grant agreement no. EFOP-3.6.3-VEKOP-16-2017-00005, project title: Strengthening the scientific replacement by supporting the academic workshops and programs of students, developing a mentoring process).