The Expanding Threat of Crimean-Congo Haemorrhagic Fever Virus: Role of Migratory Birds and Climate Change as Drivers of Hyalomma spp. Dispersal in Europe

Simple Summary

This review analysed published data on the detection of Hyalomma ticks transported by migratory birds across Europe since 2008. By compiling evidence from multiple studies, we identified key migratory bird species involved in the dispersal of immature Hyalomma ticks, including those infected by Crimean-Congo Haemorrhagic Fever Virus (CCHFV), highlighting the important role of bird migration in the long-distance spread of these vectors. In Europe, CCHFV-positive Hyalomma ticks have been recovered from the Great Reed Warbler, Woodchat Shrike, Western Black-Eared Wheatear, and Whinchat. Additionally, we discuss how climate change is expanding the environmental suitability of European regions for Hyalomma survival and establishment, thereby increasing the potential risk of CCHFV as an emerging threat.

Abstract

Crimean-Congo Haemorrhagic Fever Virus (CCHFV) is an emerging zoonotic pathogen with a high case fatality risk. Its primary vectors, Hyalomma spp. ticks, are expanding their geographic range, raising concerns about the increasing risk of Crimean-Congo Haemorrhagic Fever (CCHF) outbreaks in Europe. Migratory birds contribute considerably to the spread of Hyalomma ticks, transporting immature forms over long distances during spring migrations. Additionally, climate change plays a crucial role in this expansion by creating favorable conditions for Hyalomma spp. survival and dispersal. This review explores the interplay between Hyalomma spp. ecology as vectors of CCHFV, the role of migratory birds and the impact of climate change on the dispersal of CCHFV across Europe. Understanding these dynamics is essential for assessing future risks, improving surveillance strategies, and implementing effective public health interventions.

1. Introduction

Crimean-Congo Haemorrhagic Fever (CCHF), caused by the emerging zoonotic Crimean-Congo Haemorrhagic Fever Virus (CCHFV), is an expanding public health concern, classified as a priority disease by the World Health Organisation (WHO) since the disease is associated with high case fatality risk and the absence of effective vaccines and a specific treatment [1,2,3].

The CCHFV belongs to the genus Orthonairovirus of the family Nairoviridae and order Bunyavirales [1,2]. The emergence of CCHF in new non-endemic regions is mainly due to international animal trade, human travel, transportation of infected ticks by migratory birds and climate change [4]. Historically concentrated in Africa, Asia, and parts of Eastern and Southern Europe [5], CCHFV has been progressively expanding into new areas, raising awareness about potential establishment in previously unaffected regions of Europe [6,7,8,9].

Humans may be exposed to CCHFV either through tick bites or by direct contact with infected animal tissues and fluids [10]. Livestock handlers, slaughterhouse workers, and agricultural and healthcare workers are at higher risk of CCHFV infection [11].

Although infection is usually asymptomatic and may circulate unnoticed in wild and domestic animals, the case fatality risk may range from 5% to 40% in humans, with the possibility of reaching 80% in some nosocomial settings [2,12,13]. The incubation period varies depending on the mode of viral transmission and load, with the possibility of lasting between 1 and 3 days (maximum 9 days), after tick-bite and 5 to 6 days (maximum 13 days) if the infection occurs by contact with infected tissues or blood [14]. Symptoms and clinical signs include, among other, high fever, nausea, vomiting, headache, diarrhoea, myalgia, hypotension, haemorrhage (petechiae, ecchymoses, epistaxis, hematuria, melena) and, ultimately, multiorgan failure [2,12]. As previously mentioned, no vaccine or specific effective antiviral treatment is available [1].

Hyalomma spp. ticks are the primary vectors of CCHFV, and their distribution correlates with the global distribution of CCHF [12]. These ticks parasite domestic animals such as livestock and wild ungulates [10]. Small animals (e.g., hares, hedgehogs, rodents, ground-resident birds) amplify immature ticks, while adult forms prefer larger hosts, including cattle, goats, sheep, horses, and sometimes, humans [10,15,16]. Although evidence for active CCHFV transmission by non-Hyalomma ticks is limited, the virus has also been detected in ticks of the genera Amblyomma, Boophilus, Dermacentor, Haemaphysalis, and Rhipicephalus. However, their role in natural transmission cycles or in maintaining CCHFV foci remains uncertain [17].

Migratory birds are recognised as important contributors to the dispersal of ticks and tick-borne pathogens across regions and continents. During seasonal movements, birds can carry immature ticks, especially larvae and nymphs, over long distances, potentially introducing them into non-endemic areas where environmental conditions allow establishment [18]. Particularly, this phenomenon has been noted for Hyalomma marginatum and H. rufipes [19,20,21].

Bird migration routes are important to consider when studying how ticks and their pathogens spread. For instance, North-East/South-West migrants like thrushes (Turdus spp.), European Robin (Erithacus rubecula), Common Redstart (Phoenicurus phoenicurus), and Dunnock (Prunella modularis), which show high tick infestation, may carry Tick-borne Encephalitis Virus (TBEV) from Central to Southwestern Europe, while species migrating North/South or North-West/South-East, such as Lesser Whitethroat (Sylvia curruca), Common Whitethroat (Sylvia communis), Eurasian Blackcap (Sylvia atricapilla), and White Wagtail (Motacilla alba), could transport infected ticks from Central Europe to Norway and Sweden [22].

Ground-foraging birds are more often parasitised due to their contact with vegetation layers where ticks quest for hosts [18]. The highest diversity of tick species and the highest prevalence of tick infestation in migratory birds have been recorded at stopover sites along their seasonal migration routes. These sites play a key role in this dynamic, providing opportunities for ticks to detach, establish, and potentially initiate new transmission cycles in suitable environments [18].

Birds not only transport ticks but can also act as reservoirs for various pathogens, including Borrelia burgdorferi, Anaplasma phagocytophilum, and Rickettsia spp. [18,23]. Moreover, several studies have also linked migratory birds to the spread of viruses such as influenza A, arboviruses, and even antimicrobial-resistant bacteria [24].

Ground-feeding migratory birds play an essential role in the dispersal and importation of Hyalomma spp. ticks, especially Hyalomma marginatum complex, into Europe during their migration season [13]. This phenomenon facilitates the introduction of Hyalomma spp. into new environments, potentially accelerating the spread of CCHFV in Europe [16]. Moreover, it is expected that climatic factors, such as temperature and precipitation, may be helpful predictors of CCHF once climatic variability influences the distribution of ticks [11,25].

This review investigates the expansion of CCHF in Europe, highlighting the role of Hyalomma spp. as vectors of CCHFV and the contribution of migratory birds to their introduction and dispersal across the continent. It also provides a descriptive inventory of bird species previously reported as hosts of Hyalomma spp. in Europe and explores the role of climate change in the dispersal of Hyalomma ticks in this region.

2. Materials and Methods

This review was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [26], with the search strategy illustrated in the flowchart presented in Figure 1. A comprehensive literature search was conducted from January to March 2025 across the PubMed, Google Scholar, CAB Abstracts, and ScienceDirect databases.

The inclusion of articles was limited to those published in peer-reviewed/academic journals or conference proceedings, written in English or Spanish, and that addressed at least one of the following topics: (1) the occurrence of CCHFV and CCHF in Europe; (2) the life cycle and ecology of Hyalomma ticks as vectors of CCHFV in Europe; (3) the occurrence of Hyalomma spp. and CCHFV-positive Hyalomma ticks in migratory birds in Europe over the last 17 years (studies with data collection starting in 2008); and (4) the impact of climate change on the expansion of Hyalomma spp. in Europe were included. Additionally, studies describing migratory patterns of bird species known to host Hyalomma spp., as identified in the selected literature, were included.

Search keywords included, among other variations, “Crimean-Congo Haemorrhagic Fever Virus” OR “CCHFV” OR “CCHF”; “Crimean-Congo Haemorrhagic Fever Virus” OR “CCHFV” AND “Europe”; “Hyalomma” AND “Europe”; “Migratory birds” AND “CCHFV” AND “Hyalomma”; “Crimean-Congo Haemorrhagic Fever Virus” AND “Hyalomma”; “Climate change” AND “Hyalomma” OR “CCHFV” were considered as search terms. The removal of duplicates across journals and databases was then carried out.

One reviewer screened all titles and abstracts identified in the search. Full texts of potentially relevant articles were then retrieved and assessed by the same reviewer against the inclusion criteria. No automation tools were used in the data collection process, and no study investigators were contacted for additional information or clarification.

Regarding studies reporting Hyalomma spp. infestation in bird species, 20 studies assessing the occurrence of Hyalomma species in migratory birds and the detection of CCHFV-positive ticks on these hosts in Europe were retained after full-text screening. All these studies were published after 2012 and described sampling periods ranging from 2008 to 2022. In this selection, studies were excluded if they were not conducted in Europe, lacked a clear distinction of European findings, or failed to specify the bird species reported to be infested with Hyalomma. The following variables were recorded, when available: study location (country), sampling period (year, season, and months), host species, tick species, number of infested birds and number of collected ticks. When relevant information was missing or unclear, no assumptions were made beyond what was explicitly stated by the authors. Ambiguous or incomplete data (e.g., undefined numbers of infested birds, or unspecified tick counts per species) were classified as “not given” (N/G) in the data extraction table. A summary of these data provided in the Supplementary Materials (Table S1).

The remaining 56 articles were used as the basis for a narrative approach to examine evidence of CCHFV in Europe; to discuss the role of Hyalomma spp. as vectors of CCHFV and their distribution in Europe; to introduce the theme concerning the role of migratory birds in the dispersal of Hyalomma spp. across Europe; to provide an overview of the migratory patterns of bird species reported to be infested by Hyalomma spp. in non-endemic regions and by CCHFV-positive Hyalomma ticks; and to discuss the impact of climate change on the expansion of Hyalomma spp. The selected records per topic are listed in the Supplementary Materials (Table S2).

Complementary data from the European Centre for Disease Prevention and Control (ECDC) were used to discuss reported cases of CCHFV [27], and the distribution of Hyalomma marginatum and Hyalomma lusitanicum in Europe [28]. At the same time, information from the BirdLife Datazone [29] was consulted to explore the ecology of migratory bird species, particularly their breeding seasons and locations, as well as their migratory routes.

3. Evidence of Crimean-Congo Haemorrhagic Fever Virus (CCHFV) in Europe

According to the model developed by Okely et al. [30], CCHFV exhibited high degree of environmental suitability across Southern and Central Europe, namely in Western Mediterranean countries, driven by bioclimatic factors such as temperature, precipitation, and vegetation cover that favour both the survival of vectors and the potential distribution of the virus in these regions [30]. Currently, CCHF is considered endemic in Southwestern Europe [3]. In the European Union (EU)/European Economic Area (EEA), between 2013 and May 2025, human cases have been detected in Bulgaria (n = 41 cases), Spain (n = 18 cases), Greece (n = 1 case), Portugal (n = 1 case), and in the United Kingdom (n = 1 case) [27]. Excluding data from the United Kingdom, the distribution of CCHF cases reported in the EU/EEA between 2013 and May 2025 is represented in Figure 2. From these cases, seven and six deaths were registered in Bulgaria and Spain, respectively [27]. In Portugal, the only reported death since 2013 associated with CCHF occurred in 2024 [31]. Additionally, CCHF is endemic in Turkey, particularly in the Central Anatolian region [12].

The presence of antibodies against CCHFV in animal populations is a good indicator of the virus’s occurrence in a given region [32]. For instance, sheep seroconvert to CCHFV and are considered suitable sentinels for monitoring the virus and its circulation in new non-endemic regions [33]. Additionally, antibodies against CCHFV have been detected in several wild and domestic animals, such as cattle, swine, horses, donkeys, lagomorphs, and rodents [33]. Moreover, to assess the risk of exposure to CCHFV in the Iberian Peninsula, the seroprevalence of CCHFV has been studied in populations of red deer (Cervus elaphus), wild boar (Sus scrofa), and roe deer (Capreolus capreolus) [1,34,35]. However, the role of birds in CCHFV transmission remains poorly understood, and further studies are needed, particularly on the susceptibility of different bird species to CCHFV infection, as well as on the presence of antibodies in avian populations across Europe. Most birds are refractory to CCHFV, showing low antibody rates, as in chickens and ducks [10]. Some species, like Eurasian Magpies (Pica pica), show occasional antibody presence. Ostriches (Struthio camelus) develop antibodies and viremia, with the virus persisting in organs for days [10]. Furthermore, experimental studies have shown that some bird species, such as the Red-Billed Hornbill (Tockus erythrorhynchus) and the Glossy Starling (Lamprotornis spp.) may produce antibodies [36]; others, like the Blue-Helmeted Guinea Fowl (Numida meleagris), may develop low-intensity viremia followed by a transient immune response [37]. Although most birds do not exhibit infection, they can serve as hosts for immature Hyalomma ticks, potentially aiding virus spread via cofeeding or non-viremic transmission, and may play a role in the transboundary movement of CCHFV-infected ticks [10,38].

4. Hyalomma Ticks in Europe

The genus Hyalomma comprises more than 20 species [8]. The natural distribution of Hyalomma species is confined to the continents of Asia, Africa, and Europe [39]. The distribution of Hyalomma spp. has been expanding since the first recorded evidence of Hyalomma marginatum into Europe in the late 20th century [40]. In Europe, several Hyalomma species have been documented, including H. marginatum, H. rufipes, and H. lusitanicum [41,42]. Hyalomma excavatum has been occasionally recorded in countries such as Italy and Greece, typically associated with mesomediterranean biotopes, and may represent sporadic introductions from North Africa [41]. Scattered records of Hyalomma anatolicum s.s. have also been documented in Europe, although these may reflect misidentifications or isolated introductions via bird migration [41]. According to the European Food Safety Authority (EFSA) [43], Hyalomma marginatum is considered the most important potential vector in Europe, a species widespread in Mediterranean regions [43]. Given their documented presence in Europe and potential epidemiological relevance, particular attention is given to H. marginatum, H. rufipes, and H. lusitanicum in the present review.

The majority of Hyalomma spp. have a three-host cycle, with exception of H. marginatum complex, which are diphasic, with the larvae and nymph taking their meals on the same host [40,44]. Hyalomma marginatum sensu lato (s.l.) includes, among other species, Hyalomma marginatum sensu stricto (s.s.) and Hyalomma rufipes [16].

Hyalomma ticks can become infected by CCHFV when feeding on infected host (Figure 3). Immature ticks prefer to feed on rodentia, lagomorpha, and aves, while adults infest large ungulates, with a lower yet notable preference for lagomorpha and suidae [45].

Regarding the mechanism of CCHFV infection of Hyalomma marginatum, initial viral replication occurs in the intestinal epithelium following ingestion, with subsequent dissemination to other tissues. The highest viral loads are typically observed in the reproductive organs and salivary glands [46]. Following replication and dissemination, the virus can be transmitted both vertically and horizontally, including via co-feeding [46]. Co-feeding transmission among Hyalomma ticks occurs when infected ticks introduce the virus into the host’s skin or bloodstream during feeding, enabling non-infected ticks feeding in close proximity on the same host to acquire the virus, thereby increasing the overall probability of transmission [45,47]. Given that small mammals tend to develop prolonged viremia, the feeding preference of Hyalomma spp. for these hosts may result in high tick burdens on key reservoir species, facilitating sustained viral circulation [45].

Hyalomma marginatum s.s. may act as natural reservoir of CCHFV once ticks carry the virus throughout the life stages [46]. Hyalomma marginatum is primarily distributed in Southern Europe, Northern Africa and parts of Asia [48]. In Europe, H. marginatum is endemic in the Mediterranean regions and Balkan countries, where established populations are present, however it is also occasionally found in Central Europe [16]. Besides CCHFV, H. marginatum can transmit diverse tick-borne pathogens, such as spotted fever rickettsiae to humans [16], Anaplasma spp. [49] and Theileria annulata to cattle, and Babesia caballi and Theileria equi to horses [16].

Hyalomma marginatum is commonly found in migratory birds. Jameson et al. [20] reported that up to 21% of birds migrating from Africa to the United Kingdom were infested with H. marginatum nymphs. Consequently, it is predicted that every year a high number of immature ticks are passively transported by migrating birds from Africa and Southern Europe into or over Central Europe [50].

Along with H. marginatum, Hyalomma lusitanicum is endemic in the Iberian Peninsula [51]. Hyalomma lusitanicum is a vector of CCHFV, but it is also suspected to transmit Theileria equi, T. annulata, Babesia pecorum, Anaplasma phagocytophilum, Borrelia burgdorferi, B. lusitaniae, and Coxiella burnetti, although this species remains poorly understood in terms of its vectorial ability for these pathogens [40]. The detection of the genetic material of CCHFV in adult H. lusitanicum ticks collected from red deer in Spain highlights the potential role of this species in the virus circulation among wild ungulates in the region [6].

Based on the ECDC data [28], Figure 4 illustrates the current known distribution of Hyalomma marginatum and Hyalomma lusitanicum in Europe.

Hyalomma rufipes is also one of the vectors of CCHFV [40]. Low temperatures in northern Europe can limit the ability of H. rufipes nymphs, dropped by migratory birds, to moult [52]. However, increasing temperatures in some regions may create more favourable conditions for nymphs to moult in non-endemic areas. Hansford et al. [52] documented, for the first time, likely evidence of successful moulting of H. rufipes in the UK during the summer of 2018. Similarly, in April 2020, Rudolf et al. [53] reported a live adult H. rufipes in the Czech Republic, which may have moulted during the autumn–spring period and overwintered as an adult. These findings raise concerns about the potential establishment of H. rufipes populations in Northern and Central Europe.

5. The Role of Migratory Birds in the Dispersal of Hyalomma spp. in Europe

Migratory birds play a key role in the passive transport of Hyalomma spp. from Africa and Southern Europe to the northern breeding areas, as millions of birds migrate between these continents, breeding in the northern hemisphere during summer and returning to warmer regions of Africa in autumn to the wintering locations, thus contributing to intercontinental dispersal of several pathogens and vectors [10,54,55]. The role of migratory birds in the spread of tick-borne pathogens, including CCHFV, has been studied and highlighted [18,56].

Immature Hyalomma ticks can remain attached to the primary host for up to 26 days, enabling migratory birds to transport ticks over long distances [15,33,56]. The role of migratory birds in the life cycle and dispersal of immature Hyalomma ticks across Europe is depicted in Figure 5.

Viremia does not develop in most birds [56]. Understanding the contribution of migratory birds in the dispersal of pathogens plays a crucial part in assessing the risk of spread and introducing emerging diseases and pathogens [56]. Findings of ticks belonging to Hyalomma spp., including H. marginatum and H. rufipes, collected from migratory birds between 2008 and 2022 are summarised in

Table 1. Species of birds reported to be infested by Hyalomma ticks in Europe (2008–2022).

Bird Species	Species of Collected Ticks	Country	References
Barn Swallow (Hirundo rustica)	Hyalomma spp.	Italy	[57]
	Hyalomma rufipes	Italy, Malta	[56,58]
Black Redstart (Phoenicuros ochruros)	Hyalomma spp.	Italy	[57]
	Hyalomma marginatum	Spain	[23]
	Hyalomma rufipes	Italy	[56,57]
Black-Eared Wheatear (Oenanthe hispanica)	Hyalomma spp.	Italy	[33,56,59]
	Hyalomma rufipes	Italy	[56]
Citril Finch (Carduelis citrinella)	Hyalomma marginatum	Spain	[23]
Collared flycatcher (Ficedula albicollis)	Hyalomma spp.	Italy	[56]
	Hyalomma rufipes	African-Western Palaearctic region, Italy, Malta	[6,56,57,58]
Common Chaffinch (Fringilla coelebs)	Hyalomma marginatum	Spain	[23]
Common Chiffchaff (Phylloscopus collybita)	Hyalomma spp.	Italy	[56]
Common Cuckoo (Cuculus canorus)	Hyalomma spp.	Italy	[33]
Common Hoopoe (Upupa epops)	Hyalomma spp.	Italy	[33,56]
	Hyalomma rufipes	African-Western Palaearctic region, Malta	[6,58]
Common Kestrel (Falco tinnunculus)	Hyalomma marginatum	Spain, Malta	[23,58]
Common Kingfisher (Alcedo atthis)	Hyalomma marginatum	Malta	[58]
Common Linnet (Linaria cannabina)	Hyalomma marginatum	Spain	[23]
Common Nightingale (Luscinia megarhynchos)	Hyalomma spp.	Italy	[33,56,59]
	Hyalomma marginatum s.l.	Czech Republic	[15]
	Hyalomma marginatum	African-Western Palaearctic region, Spain, Italy, Bulgaria	[6,23,56,60]
	Hyalomma rufipes	African-Western Palaearctic region, Italy	[6,56]
Common Redstart (Phoenicurus phoenicurus)	Hyalomma spp.	United Kingdom, Italy, Turkey	[20,33,56,57,59,61]
	Hyalomma marginatum	African-Western Palaearctic region, Greece, Italy	[6,44,56]
	Hyalomma rufipes	African-Western Palaearctic region, Italy, Malta	[6,56,57,58,62]
Common Reed-Warbler (Acrocephalus scirpaceus)	Hyalomma spp.	Italy	[56]
	Hyalomma marginatum s.l.	Czech Republic, Slovakia	[15]
	Hyalomma marginatum	Spain	[23]
	Hyalomma rufipes	African-Western Palaearctic region, Italy, Malta, Netherlands	[6,56,58,63]
Common Whitethroat (Sylvia communis)	Hyalomma spp.	United Kingdom, Italy, Malta, Spain	[20,33,56,57,58,59,64]
	Hyalomma marginatum	African-Western Palaearctic region, Italy, Malta, Bulgaria	[6,56,58,60]
	Hyalomma rufipes	African-Western Palaearctic region, Italy, Malta, Hungary	[6,56,57,58,65]
Dunnock (Prunella modularis)	Hyalomma spp.	Italy	[57]
	Hyalomma marginatum	Italy, France	[56,66]
Eurasian Blackbird (Turdus merula)	Hyalomma spp.	Italy	[59]
	Hyalomma marginatum	Spain	[23]
Eurasian Blackcap (Sylvia atricapilla)	Hyalomma spp.	Italy	[59]
	Hyalomma rufipes	African-Western Palaearctic region, France	[6,66]
Eurasian Blue Tit (Cyanistes caeruleus)	Hyalomma marginatum	Spain	[23]
Eurasian Buzzard (Buteo buteo)	Hyalomma spp.	Italy	[59]
	Hyalomma marginatum	Spain	[23]
Eurasian Golden Oriole (Oriolus oriolus)	Hyalomma spp.	Italy	[33,56]
	Hyalomma marginatum	Spain, Greece, Italy	[23,44,56]
	Hyalomma rufipes	African-Western Palaearctic region, Italy	[6,56]
Eurasian Scops-Owl (Otus scops)	Hyalomma spp.	Italy	[33,56]
	Hyalomma marginatum	Italy	[56]
Eurasian Siskin (Spinus spinus)	Hyalomma marginatum	Greece	[44]
European Goldfinch (Carduelis carduelis)	Hyalomma spp.	Italy	[56]
	Hyalomma marginatum	Italy	[56]
European Greenfinch (Chloris chloris)	Hyalomma marginatum	Spain	[23]
European Honey-Buzzard (Pernis apivorus)	Hyalomma spp.	Italy	[59]
European Nightjar (Caprimulgus europaeus)	Hyalomma spp.	Italy	[56]
	Hyalomma rufipes	African-Western Palaearctic region, Italy	[6,56]
European Opied Flycatcher (Ficedula hypoleuca)	Hyalomma spp.	Italy, Hungary	[33,56,57,59,65]
	Hyalomma marginatum	Spain	[23]
	Hyalomma rufipes	African-Western Palaearctic region, Italy, Malta	[6,56,58]
European Robin (Erithacus rubecula)	Hyalomma spp.	Italy	[56]
	Hyalomma marginatum	African-Western Palaearctic region, Italy, France	[6,56,66]
	Hyalomma rufipes	Italy	[57]
European Turtle-Dove (Streptopelia turtur)	Hyalomma rufipes	African-Western Palaearctic region	[6]
Garden Warbler (Sylvia borin)	Hyalomma spp.	Italy, Netherlands/Belgium	[33,56,67]
	Hyalomma rufipes	African-Western Palaearctic region, Italy	[6,56]
Great Reed-Warbler (Acrocephalus arundinaceus)	Hyalomma spp.	Italy, Turkey	[33,61]
	Hyalomma marginatum s.l.	Czech Republic, Slovakia	[15]
	Hyalomma marginatum	Spain, Greece, Moldova	[23,44,68]
	Hyalomma rufipes	Italy, Malta	[56,58]
Great Tit (Parus major)	Hyalomma spp.	Italy	[56]
	Hyalomma marginatum	Spain	[23]
House Sparrow (Passer domesticus)	Hyalomma marginatum	Spain	[23]
Icterine Warbler (Hippolais icterina)	Hyalomma spp.	Italy	[33,56,57]
	Hyalomma marginatum	Italy	[56]
	Hyalomma rufipes	African-Western Palaearctic region, Italy	[6,56]
Kentish Plover (Charadrius alexandrinus)	Hyalomma marginatum	African-Western Palaearctic region	[6]
Long-Tailed Tit (Aegithalos caudatus)	Hyalomma marginatum	Spain	[23]
Marsh Warbler (Acrocephalus palustris)	Hyalomma marginatum s.l.	Czech Republic	[15]
	Hylomma marginatum	Bulgaria	[60]
Melodious Warbler (Hippolais polyglotta)	Hyalomma spp.	Italy	[59]
Northern Wheatear (Oenanthe oenanthe)	Hyalomma spp.	United Kingdom, Italy	[20,33,56,57]
	Hyalomma marginatum	African-Western Palaearctic region	[6]
	Hyalomma rufipes	African-Western Palaearctic region, Italy	[6,56,57]
Ortolan Bunting (Emberiza hortulana)	Hyalomma marginatum	Spain	[23]
Red-Backed Shrike (Lanius collurio)	Hyalomma spp.	Turkey	[61]
Rock Bunting (Emberiza cia)	Hyalomma marginatum	Spain	[23]
Rock Sparrow (Petronia petronia)	Hyalomma marginatum	Spain	[23]
Rufous-Tailed Rock-Thrush (Monticola saxatilis)	Hyalomma rufipes	African-Western Palaearctic region	[6]
Savi’s Warbler (Locustella luscinioides)	Hyalomma marginatum s.l.	Slovakia	[15]
Sedge Warbler (Acrocephalus schoenobaenus)	Hyalomma spp.	Malta, United Kingdom, Italy, Spain	[6,20,33,56,64]
	Hyalomma marginatum s.l.	Slovakia	[15]
	Hyalomma marginatum	Greece, Malta	[44,58]
	Hyalomma rufipes	African-Western Palaearctic region, Greece, Italy, Malta, Hungary	[6,44,56,58,65]
Song Thrush (Turdus philomelos)	Hyalomma spp.	Italy	[56,57]
	Hyalomma marginatum	Greece, Italy	[44,56]
	Hyalomma rufipes	Italy	[56,57]
Spanish Sparrow (Passer hispaniolensis)	Hyalomma lusitanicum	Malta	[58]
Spotted Flycatcher (Muscicapa striata)	Hyalomma spp.	Italy	[33,56,59]
	Hyalomma marginatum	Italy	[56]
	Hyalomma rufipes	African-Western Palaearctic region, Italy	[6,56,57]
Subalpine Warbler (Curruca cantillans)	Hyalomma spp.	Italy	[33,57]
	Hyalomma rufipes	Italy	[56]
Thrush Nightingale (Luscinia luscinia)	Hyalomma spp.	Turkey	[61]
Tree Pipit (Anthus trivialis)	Hyalomma spp.	African-Western Palaearctic region, Italy	[6,33,56,57,59]
	Hyalomma rufipes	African-Western Palaearctic region, Italy	[6,56]
Western Olivaceous Warbler (Iduna opaca)	Hyalomma spp.	Spain	[64,69]
Western Subalpine Warbler (Curruca iberiae)	Hyalomma rufipes	Malta	[58]
Western yellow wagtail (Motacilla flava)	Hyalomma spp.	Italy	[33,56,59]
	Hyalomma rufipes	African-Western Palaearctic region, Italy, Malta	[6,56,58]
Whinchat (Saxicola rubetra)	Hyalomma spp.	African-Western Palaearctic region, Italy	[6,33,56,57,59]
	Hyalomma rufipes	African-Western Palaearctic region, Italy	[6,56,57,62]
Willow Warbler (Phylloscopus trochilus)	Hyalomma spp.	Italy, Spain	[33,56,57,59,64]
	Hyalomma marginatum	Malta	[58]
	Hyalomma rufipes	Italy, Malta	[56,58]
Wood Warbler (Phylloscopus sibilatrix)	Hyalomma spp.	Italy, Malta	[33,56,57,58,62]
	Hyalomma marginatum	Italy	[56]
	Hyalomma rufipes	African-Western Palaearctic region, Italy, Malta	[6,56,57,58,62]
Woodchat Shrike (Lanius senator)	Hyalomma spp.	Italy	[33,56,59]
	Hyalomma marginatum	African-Western Palaearctic region	[6]
	Hyalomma rufipes	African-Western Palaearctic region, Italy, Malta	[6,56,58,62]
Woodlark (Lullula arborea)	Hyalomma marginatum	Spain	[23]

. In most studies, sampling sites were located in coastal locations, often the first landfall sites for migrating birds [20] or in lowland regions such as marshes and fish ponds densely overgrown with wetland vegetation [15], habitats that provide favourable conditions for migratory birds during stopover and breeding periods. These habitats offer favourable conditions for migratory birds during stopover and breeding periods, thereby increasing the likelihood of tick-host encounters.

5.1. Detection of Hyalomma spp. on Migratory Birds in Non-Endemic European Regions (2008–2022)

Several studies have documented the occurrence of Hyalomma spp. on migratory birds in European regions considered non-endemic (Table 1). Sampling studies on migratory birds conducted prior to 2008 reported the presence of Hyalomma marginatum s.l. in parts of Northern and Central Europe, including Germany [70], Norway [19], and Slovenia [71], among others such as the former Czechoslovakia, Denmark, Finland, Norway, Poland, Sweden, and the United Kingdom [15]. The following section summarises findings from 2008 to 2022, with a particular focus on Northern and Central Europe.

5.1.1. Northern Europe

During the spring migration period (March to May) of 2010 and 2011, Jameson et al. [20] reported the detection of Hyalomma spp. ticks on several migratory bird species in Dorset, England. These included the Sedge Warbler (Acrocephalus schoenobaenus) (n = 1/10; 1 tick), Common Whitethroat (Curruca communis) (n = 2/53; 4 ticks), Northern Wheatear (Oenanthe Oenanthe) (n = 2/51; 8 ticks), and Common Redstart (Phoenicurus phoenicurus) (n = 1/30; 1 tick). The Sedge Warbler is found in diverse types of low, dense vegetation, often near to water or moist depressions, wintering in sub-Saharan Africa. In Western Europe its egg laying mainly begins in late April, while in Central Europe it starts from early May [29]. The Common Whitethroat is a long-distance migrant that overwinters in sub-Saharan Africa, breeding primarily from April to July [29,72]. The Northern Wheatear is a mountain generalist and open grassland species that primarily breeds in Southern Europe, migrating approximately 3500 km to its wintering grounds in sub-Saharan Africa [73]. The Common Redstart is a migratory species that breeds from late-April to mid-July, with earlier breeding in Southern Europe and later May to late-June in northern Finland [29].

In addition to the records from England, between 2012 and 2014, Heylen et al. [67] carried out a study on pathogen communities of songbird-derived ticks in the Netherlands and Belgium, finding one Hyalomma spp. nymph collected from a Garden Warbler (Sylvia borin) (n = 1). Garden Warblers are long-distance migrants that migrate north from non-breeding grounds in sub-Saharan Africa from mid-March to the end of May [74].

Additionally, in 2012, Uiterwijk et al. [63] registered the presence of a Hyalomma rufipes nymph in a Eurasian Reed Warbler (Acrocephalus scirpaceus) (n = 1) in the Netherlands. This species lives in Central Europe from April to October and winters in sub-Saharan Africa in the region inhabited by Hyalomma spp. ticks [70].

5.1.2. Central Europe

Surveillance efforts in Central Europe have also detected Hyalomma spp. on migratory birds. In Czech Republic, during the spring migration in 2008–2012, Capek et al. [15] reported on records of ticks of the H. marginatum complex in Great Reed Warbler (Acrocephalus arundinaceus) (n = 1; 8 ticks), Marsh Warbler (Acrocephalus palustris) (n = 1; 1 tick), Eurasian Reed Warbler (Acrocephalus scirpaceus) (n = 1; 1 tick), and in Common Nightingale (Luscinia megarhynchos) (n = 1 bird; 4 ticks in 2010 and n = 1; 1 tick in 2012). In Slovakia, the same authors [15] also recorded H. marginatum complex ticks in Great Reed Warbler (Acrocephalus arundinaceus) (n = 1; 1 tick); Sedge Warbler (Acrocephalus schoenobaenus) (n = 7; 10 ticks), Reed Warbler (Acrocephalus scirpaceus) (n = 1; 1 tick in 2008 and n = 1; 2 tick in 2009), and in Savi’s Warbler (Locustella luscinioides) (n = 1; 1 tick).

The Great Reed Warbler and the Common Nightingale are migratory birds that winter in sub-Saharan Africa [29,75]. The Marsh Warbler, like other Acrocephalus warblers, is among the most frequent long-distance bird migrants along the eastern route, wintering in south-east Africa and breeding between the second half of May and July [29,76]. The Savi’s Warbler is a long-distance migratory bird that breeds in wetlands across the Palaearctic region, ranging from Portugal to Mongolia and from Estonia in the north to Morocco in the south [77]. Western European populations of Savi’s Warbler are thought to migrate south or southwest in autumn and return in the opposite direction in spring. A migratory divide appears to exist in Central Europe [77].

In Hungary, in 2022, Hyalomma rufipes ticks were collected from Sedge Warbler (Acrocephalus schoenobaenus) (n = 3; 3 ticks), European Pied Flycatcher (Ficedula hypoleuca) (n = 1; 1 tick), Common Whitethroat (Sylvia communis) (n = 1; 1 tick), and, although not considered a migratory bird, a Bearded Reedling (Panurus biarmicus) (n = 2; 6 ticks) [64]. The European Pied Flycatcher inhabits semi-open areas, breeding across a vast area of the Western Palearctic region and wintering in West Africa [78].

5.2. Migratory Bird Species Infested by CCHFV-Positive Ticks

Bird screening and direct captures have provided evidence of an active role of migratory birds in the dispersion of CCHFV-infected ticks in countries where the virus is endemic [56]. Since 2008, some studies have reported the detection of Hyalomma spp. ticks which tested positive for CCHFV on various migratory bird species across Europe (

Table 2. Species of migratory birds reported as being infested by CCHFV-positive Hyalomma spp. ticks since 2008.

Infested Migratory Bird	CCHFV-Positive Tick	Hyalomma Life Stage	Country	Reference
Great Reed Warbler (Acrocephalus arundinaceus)	Hyalomma spp.	Nymph (n = 1)	Turkey	[61]
Woodchat Shrike (Lanius senator)	Hyalomma marginatum	Nymph (n = 3)	Greece	[5]
Western Black-Eared Wheatear (Oenanthe hispanica)	Hyalomma rufipes	Larva (n = 1)	Italy	[56]
Whinchat (Saxicola rubetra)	Hyalomma rufipes	Nymph (n = 1)	Italy	[56]

).

Below is provided a brief overview of the ecology and infestation records for each bird species found carrying CCHFV-positive ticks.

5.2.1. Great Reed Warbler (Acrocephalus arundinaceus)

In Turkey, Leblebicioglu et al. [61] reported a CCHFV-positive Hyalomma spp. nymph collected from a Great Reed Warbler (Acrocephalus arundinaceus) (Table 2). The Great Reed Warbler is a migratory bird, preferring wet habitats, that travels between its European breeding grounds and African wintering quarters [76]. The Great Reed Warbler inhabits reed vegetation habitats with water in Europe and Western Palearctic, preferring canals, ponds, shallow lakes and fish ponds [79].

Individuals of Great Reed Warbler were regarded as carriers of Hyalomma spp. ticks in Turkey (n = 6 ticks in 3 birds) [61] and in Italy (n = 1 tick in a bird) [33]. Moreover, H. marginatum was recovered from a Great Reed Warbler in the Czech Republic as previously mentioned (n = 8 ticks) [15], in Spain (n = 7 ticks) [23], in Greece (n = 1 tick) [44], Moldova (n = 2 ticks) [68], and in Slovakia (n = 1 tick) [15]. More recently, 14 H. rufipes ticks were sampled from two Great Reed Warblers in Malta [58] and in Italy (n = 3 ticks) [56].

5.2.2. Woodchat Shrike (Lanius senator)

Three CCHFV-positive H. marginatum nymphs were already obtained from Woodchat Shrike (Lanius senator) in a Greek study [5] (Table 2). Woodchat Shrike is adapted to open landscapes, widely distributed from the Iberian Peninsula to Western Turkey, and preferring to breed in semi-open, dry grassland habitats with scattered shrubs [80,81]. Non-specified Hyalomma spp. were previously reported in Woodchat Shrikes in three Italian studies (n = 1 tick) [59], (n = 2 ticks) [33], and (n = 12 ticks) [56].

5.2.3. Black-Eared Wheatear (Oenanthe hispanica)

In Italy, in 2018, Mancuso et al. [56] recovered a CCHFV-positive larva of H. rufipes from a Black-Eared Wheatear [56] (Table 2). The Black-Eared Wheatear (Oenanthe hispanica) is a bird species associated with warm areas in the Mediterranean region, where it breeds [82]. The Black-Eared Wheatear has been described as carrier of Hyalomma spp. in Italy. Mancini et al. [59] reported the occurrence of a tick in a bird of this species, similarly to the findings of De Liberato et al. [33]. Meanwhile, Mancuso et al. [56] found four ticks of Hyalomma spp. (the species was not defined) and, more specifically, two ticks of H. rufipes infesting Black-Eared Wheatear.

5.2.4. Whinchat (Saxicola rubetra)

In April 2017, an Italian study [56] found a H. rufipes nymph positive to CCHFV collected from a Whinchat (Saxicola rubetra) (Table 2). The Whinchat breeds from Western Europe into Western Asia, spending the winter in the humid zone of sub-Saharan Africa [83].

The infestation of Hyalomma spp. ticks in these individuals is extensively reported. Hoffman et al. [6] revealed the infestation by 123 H. rufipes ticks. In Italy, 65 and seven H. rufipes ticks were sampled from Whinchats by Battisti et al. [57] and by Mancuso et al. [56], respectively. Mancuso et al. [56] also detected H. rufipes. Non-defined Hyalomma spp. ticks were sampled from Whinchats by Mancuso et al. [56] (n = 214 ticks), by De Liberato et al. [22] (n = 41 ticks in 22 birds), by Mancini et al. [59] (n = 20 ticks), by Battisti et al. [57] (n = 13 ticks), and by Hoffman et al. [6] (n = 8 ticks).

6. Climate Change and Its Effects on the Expansion of Hyalomma spp.

Climate change is considered the main factor behind the observed expansion of Hyalomma marginatum [7]. Factors such as temperature, precipitation, and air currents influence the seasonal migration routes of migratory birds, as well as the time of attachment of ticks to birds and the distance over which the feeding immature ticks are transported [18]. Moreover, climate and weather changes determine the time of birds’ stay in their wintering grounds and the course of seasonal migrations [18], and impact the moulting from nymphs to adults [63].

In several regions of Europe, spring temperatures are generally considered insufficient to support the moulting of Hyalomma spp. nymphs into adults [33]. Nevertheless, recent reports have documented successful moulting events in newly colonized areas, indicating that Hyalomma spp. may adapt to changing climatic conditions or benefiting from localized microclimates [8]. In Southern Europe and Northern Africa, the summer rainfall and evapotranspiration regulate the Hyalomma marginatum populations [84]. In Eastern Europe and the Caucasus, warmer autumns are considered ideal conditions for Hyalomma marginatum and are associated with decreased mortality rates [84].

Areas where the annual sum of daily temperatures (i.e., cumulative temperatures) reaches between 3000–4000 °C and the water vapor deficit is below 15 hPa are favorable for the distribution of Hyalomma marginatum [84,85]. Furthermore, established populations of H. marginatum are found in areas where the cumulative temperatures between September and December reach approximately 800 °C [84,86]. Thus, warm autumns enable engorged nymph populations to moult into adults and taking into account that adults are colder-more resistant in comparison to nymphs, autumn temperatures are connected with lower winter mortality [84].

The timing of first arrival for many migratory bird species is closely linked to average monthly temperatures, with warmer conditions often associated with earlier arrivals. As temperatures rise, suitable breeding and stopover habitats are also expected to shift northward. Conversely, approximately one-eighth of bird species are projected to face a high risk of extinction in the coming decades [87].

There is growing interest in creating maps that delineate areas where the risk of ticks or tick-borne pathogens is likely to occur [88], with several studies modelling the distribution of Hyalomma spp. and the potential expansion of CCHF under climate change scenarios. A retrospective study revealed changes in the life cycle of Hyalomma marginatum along a latitudinal gradient, with more significant changes between 1901–1922 and 1989–2009 [25]. Climate modelling carried out by Estrada-Peña et al. [25] showed that warmer temperatures and lower humidity have increased the tick’s development and survival rates, particularly in regions where the tick has been historically present. Their model results [25] predicted that large regions in the Atlantic domain could experience a 60–80% increase in development rates and over 80% in survival rates during the developmental and questing stages. In turn, Gale et al. [89] projected that, by 2075–2084, the number of European regions meeting the moulting threshold for Hyalomma marginatum nymphs (≥8 °C for 15 consecutive days) will increase relative to 2005–2014, particularly in coastal areas during March and expanding inland by April. Despite this, the frequency of annual CCHFV incursions via immature ticks on migratory birds (e.g., Common Quail, Tree Pipit, Willow Warbler, Northern Wheatear) is expected to remain stable, with reduced risk in Central and Southern Europe but increased risk in the North [89]. More recent projections by Okely et al. [30] suggest a possible northward expansion of Hyalomma rufipes into Germany and the UK. Similarly, Gillingham et al. [84] identified regions in the UK with suitable temperatures for H. marginatum nymphal moulting between 2000–2019, although autumn conditions remain suboptimal for population establishment. The model developed by Fanelli et al. [90] predicts areas at risk of further CCHFV expansion, such as Italy and France, but highlights a still low risk of CCHFV entry and exposure in most Western European countries. Moreover, in comparison with Cuadrado-Matías et al. [34], the predictions carried out by Fanelli et al. [90] show a more expansive distribution of favourable CCHF occurrence conditions in the Iberian Peninsula.

As climate change persists, predictive models incorporating data regarding Hyalomma spp. habitat suitability, host distribution and temperature project a continued expansion of CCHFV into Central and Northern Europe, with a medium risk of CCHFV introduction in France, Italy and Germany [9].

7. Limitations

This review faced several limitations that warrant acknowledgment. Firstly, the studies assessing bird species infested by Hyalomma ticks varied in methodology. Most relied on targeted sampling during migration periods, while a few reported incidental findings. In some cases, tick identification was incomplete or based solely on morphology, and the number of infested birds was not always clearly reported. Moreover, small sample sizes may have limited the detection of CCHFV-positive ticks. These factors highlight the need for more standardized and comprehensive future research. Finally, the availability of peer-reviewed studies specifically focused on the detection of Hyalomma spp. in migratory birds across Europe remains limited. This gap is also present in several countries where Hyalomma spp. are considered endemic. Consequently, identifying consistent trends in the role of migratory birds in the long-distance dispersal of Hyalomma ticks across the continent remains a challenge.

8. Conclusions

This review highlighted the detection of the Hyalomma tick in migratory birds in Europe, including in non-endemic regions, such as Northern and Central Europe. These findings reinforce the role of migratory birds in the geographic expansion of this vector. Additionally, climate change may further favour the survival and establishment of Hyalomma populations in areas that were previously unsuitable, by creating more favourable environmental conditions for their development. Moreover, this review identified four migratory bird species (Great Reed Warbler, Woodchat Shrike, Western Black-Eared Wheatear, and Whinchat) from which CCHFV-positive Hyalomma ticks have been recovered in endemic regions. Such findings provide evidence supporting the role of migratory birds as passive carriers enabling the long-distance dispersal of infected ticks. Based on these observations, enhanced surveillance should be prioritised. Effective monitoring systems should include targeted sampling of migratory birds at key stopover sites, molecular screening of ticks for CCHFV, and longitudinal studies to detect tick moulting and overwintering success. Citizen science initiatives may serve as an effective complementary tool, facilitating early detection of Hyalomma spp. and engaging the public in surveillance efforts. Strengthening collaboration between European countries is essential because current efforts are often isolated and heterogeneous in methodology. A harmonised and integrated surveillance approach, combining ornithological, ecological, veterinary, and public health perspectives, would increase the sensitivity of detection, promote early warning capabilities, and improve preparedness for the possible emergence of CCHFV in new areas.