# The distribution, phenology, host range and pathogen prevalence of Ixodes ricinus in France: a systematic map and narrative review

Grégoire Perez, Laure Bournez, Nathalie Boulanger, Johanna Fite, Barbara

Livoreil, Karen D Mccoy, Elsa Quillery, Magalie René-Martellet, Sarah I Bonnet

► To cite this version:

Grégoire Perez, Laure Bournez, Nathalie Boulanger, Johanna Fite, Barbara Livoreil, et al. The distribution, phenology, host range and pathogen prevalence of Ixodes ricinus in France: a systematic map and narrative review. Peer Community Journal, 2023, 3, pp.e81. 10.24072/pcjournal.291. hal-04203797v2

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RESEARCH ARTICLE

Published
2023-09-08

**Cite as**
Grégoire Perez, Laure Bournez, Nathalie Boulanger, Johanna Fite, Barbara Livoreil, Karen D. McCoy, Elsa Quillery, Magalie René-Martellet and Sarah I. Bonnet (2023) *The distribution, phenology, host range and pathogen prevalence of Ixodes ricinus in France: a systematic map and narrative review*, Peer Community Journal, 3: e81.

**Correspondence**
gregoire.perez@cirad.fr

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# The distribution, phenology, host range and pathogen prevalence of *Ixodes ricinus* in France: a systematic map and narrative review

Grégoire Perez<sup>1,2,3</sup>, Laure Bournez<sup>1,4</sup>, Nathalie Boulanger<sup>5,6</sup>, Johanna Fite<sup>1,7</sup>, Barbara Livoreil<sup>1,8</sup>, Karen D. McCoy<sup>1,9</sup>, Elsa Quillery<sup>1,7</sup>, Magalie René-Martellet<sup>1,10,11</sup>, and Sarah I. Bonnet<sup>1,12</sup>

Volume 3 (2023), article e81

https://doi.org/10.24072/pcjournal.291

## Abstract

The tick *Ixodes ricinus* is the most important vector species of infectious diseases in European France. Understanding its distribution, phenology, and host species use, along with the distribution and prevalence of associated pathogens at a national scale is essential for developing prevention strategies. The aim of this paper is to provide a systematic map and narrative review of the existing knowledge on the eco-epidemiology of *I. ricinus* in France. Using literature published up to 2020, the present paper provides a distribution map for the species and a summary of environmental factors explaining observed geographical differences in phenology and temporal differences in abundance. The diversity of vertebrate host species used by this tick, along with their degree of infestation when available, are presented and discussed with respect to their potential contribution to the population dynamics of *I. ricinus* and the circulation of tick-borne zoonotic pathogens. Prevalence data of detected pathogens are summarised in different maps. Results from 187 identified references show that the species is present in most departments, but scarce under Mediterranean climates and in coastal habitats. Its phenology is generally bimodal with climate-associated variations. Abundance seems positively influenced by forest cover and host abundance. Rodents and ruminants are the most studied species groups, but the diversity of sampling protocols (e.g., location, season, exhaustivity of inspection) precluded direct comparisons between groups. Data on pathogens are patchy, with most studies conducted near research laboratories. Among pathogens, *Borrelia burgdorferi* sensu lato is the most examined and seems most prevalent in north-eastern and central France. The review highlights the gaps in our knowledge of tick-host-pathogen interactions, their ecologies and their distributions, and demonstrates the need to address these gaps in order to optimize tick and tick-borne diseases prevention and control.

<footnote n="1">¹UMR 0956 BIPAR, Ecole nationale vétérinaire d'Alfort - ANSES - INRAE, 94701 Maisons-Alfort, France,</footnote>

<footnote n="2">²UMR 5558 LBBE, université Claude Bernard Lyon 1 - VetAgro Sup - CNRS, 69622 Villeurbanne, France,</footnote>

<footnote n="3">³Laboratoire Cogitamus, Université de Paris 6, 75005 Paris, France</footnote>

<footnote n="4">⁴Laboratoire de la rage et de la faune sauvage de Nancy, ANSES, 54220 Malzéville, France, ⁵UR 7290 Virulence bactérienne précoce, FMTS, Université de Strasbourg, 67000 Strasbourg, France, ⁶Centre National de Référence Borrelia, Centre Hospitalier Universitaire, 67000 Strasbourg, France, ⁷Direction de l'Évaluation des Risques, ANSES, 94701 Maisons-Alfort, France, ⁸Evidence synthesis consultant, Collaboration for Environmental Evidence France, 83340 Le Luc en Provence, France,</footnote>

<footnote n="9">⁹University of Montpellier-CNRS-IRD, UMR MIVEGEC, 34294 Montpellier, France, ¹⁰UMR EPIA, Université de Lyon - INRAE - VetAgro Sup, 69280 Marcy l'Etoile, France, ¹¹UMR EPIA, Université Clermont Auvergne - INRAE - VetAgro Sup, 63122 Saint-Genès-Champanelle, France, ¹²Unité Écologie et Émergence des Pathogènes Transmis par les Arthropodes, Institut Pasteur, Université Paris Cité, CNRS UMR 2000, INRAE USC 1510, Paris, France</footnote>
Introduction

Among the forty-one tick species known to be present in European (metropolitan) France (i.e., excluding the ultra-marine French territories, France hereafter), the hard tick *Ixodes ricinus* is the most frequently involved in human tick bites (Gilot & Marjolet, 1982; Pérez-Eid, 2007). This tick transmits several pathogens responsible for human and animal diseases (e.g. Lyme borreliosis, tick-borne encephalitis, piroplasmosis, anaplasmosis) (Heyman et al., 2010). Both the biology and ecology of this European tick species have been recently reviewed by Gray et al. (2021), and are known to vary greatly among regions. Data collected at national levels can provide insight into the factors responsible for at least some of this variation, but are rarely available to the scientific community because of a mix of published and unpublished work and its production in different languages. Here, we synthesize the available data on *I. ricinus* and its associated pathogens in France up to 2020.

Some aspects concerning the life cycle of *I. ricinus* are well-known. For example, like most hard ticks (Ixodidae), each life stage of *I. ricinus* (larva, nymph and adult) takes only a single blood meal, except adult males which do not need to feed, but may take a limited amount of blood. After each blood meal, *I. ricinus* drops off to the ground to moult into the next stage or, in the case of adult females, to lay eggs and die. Feeding on a host can last three to six days for larvae, four to seven days for nymphs and seven to ten days for adult females. Other aspects of the life cycle are more geographically variable. Indeed, the *I. ricinus* life cycle can take anywhere from two to four years to complete, depending on environmental conditions and the length of diapause periods (Gray et al., 2021). The questing activity of this tick is regulated by photoperiod and is constrained to temperatures between 5 and 30°C and to a minimum relative humidity of 80% (Gray et al., 2021). Nevertheless, despite these generalities, local adaptation of *I. ricinus* populations is known to occur (Gray et al., 2021; Tomkins et al., 2014). The life cycle of *I. ricinus* is triphasic, that is, each stage feeds on a different individual host. It is a generalist (or telotrope) tick in terms of its host range. The composition and abundance of the local vertebrate host population directly influences tick infestation dynamics, relative abundance and dispersal capacities. In turn, this local vertebrate community will affect the transmission dynamics of tick-borne pathogens and their relative prevalence in questing ticks (Hofmeester et al., 2016). Host choice varies according to tick life stage and can be at least partly explained by the height at which *I. ricinus* ticks quest on the vegetation, which itself depends on their relative resistance to desiccation (lowest in larvae and highest in adults), the type of vegetation, and the microclimatic conditions (Mejlon & Jaensen, 1997; Randolph & Storey, 1999). For example, due to the presence of larval ticks within the leaf litter (where egg laying takes place), small mammals (wood mice, voles and shrews) are often considered as the primary hosts of larvae, followed by passerine birds living in closed habitats (e.g., forest or hedgerows) and feeding on the ground (e.g., blackbirds, thrushes, tits, robin) (Hofmeester et al., 2016). Nymphs are frequently found on birds, lizards, and medium to large mammals, while adult females, which often quest higher on the vegetation, are generally observed only on medium to large mammals (Hofmeester et al., 2016; Mendoza-Roldana & Colella, 2019). Indeed, the distribution and abundance of wild ungulates are considered key factors determining the probability of tick exposure (Takumi et al., 2019). Birds can contribute to the dissemination of ticks in the landscape at short, medium and large scales (Vollmer et al., 2011; Marsot et al., 2012; Hofmeester et al., 2016). The high variation in the population density of small mammals, itself influenced by tree seed production (masting), is also thought to be an important driver of tick population dynamics at local scales (Perez et al., 2016; Bregnard et al. 2020). Because of their differential susceptibility to environmental conditions and to variation in ontological processes, the different tick life stages also differ in their seasonal activity periods, with larvae generally appearing later in the season than nymphs and adults (Wongnak et al., 2022). Identifying the main hosts and the timing of tick activity according to the life stage are essential elements for understanding the transmission dynamics of tick-borne pathogens and thus for implementing local prevention measures (Randoph et al., 1999).

France covers 552,000 km² in Europe, extending through about 9° of latitude and including a large panel of climatic zones (semi-continental, Mediterranean, oceanic and mountainous zones) and a rich diversity of habitats therein. Climates and environments suitable for the development of *I. ricinus* cover a large part of the territory, thus explaining the broad distribution and major importance of this tick species for both human and veterinary health (Wongnak et al., 2022). Consequently, several studies have been conducted on *I. ricinus* and its associated pathogens in France, but in a piecemeal way, focusing for example on a particular tick-borne disease (e.g. Lyme borreliosis, babesiosis), a particular host group (e.g. cattle, small mammals), or a particular geographic area. The present work represents the first attempt to synthesize available data on *I. ricinus* and
the pathogens it transmits in France. On the basis of a systematic literature search, we synthesize knowledge on:

1) Host infestation by *I. ricinus*, to detect potential differences in host use within France and among areas in Europe.

2) The spatio-temporal distribution of *I. ricinus* in France, to identify possible geographic trends in tick abundance, variation in activity patterns and the influence of environmental factors.

3) Tick-borne pathogens detected in *I. ricinus*, to better assess their spatial distribution and variation in exposure risk.

Finally, by highlighting knowledge gaps in the ecology of *I. ricinus* and acarological risk in France, we aim to orient future research and preventive measures in this country, and to provide a comparable basis for studies in other regions of *I. ricinus*' distribution.

## Materials and methods

### Research approach

To retrieve a comprehensive set of available literature on the ecology of *I. ricinus* in France and the pathogens it transmits, we chose a “Population, Context, Comparators and Outcome” (PCCO) approach (Livoreil et al., 2017). This approach aims (1) to determine the words to use in the literature search and (2) to structure the criteria for including or excluding a reference. Studied populations, contexts, comparators and outcome variables are presented in Table 1.

<table><caption>**Table 1** - Components elements of the literature search.</caption><thead><tr><td>Component</td><td>Elements</td></tr></thead><tbody><tr><td>Population</td><td>Any <i>I. ricinus</i> populations at larval, nymphal or adult stage</td></tr><tr><td>Context</td><td>European France, i.e. excluding overseas French territories</td></tr><tr><td>Comparators</td><td>No comparator were excluded. Comparators include, for instance: temporal comparisons, i.e. intra-annual, weather-related and daily; spatial comparisons according to climate (biome), land cover and land use (landscape context and management, habitats, vegetation types, anthropic activities, management); host density and diversity (wildlife management, ex-closure or enclosure, population fluctuation); potential treatments (e.g. acaricide treatments, vaccinations)</td></tr><tr><td>Outcome variables</td><td>Presence/absence; abundance; density; hosts parasitic burden (presence, prevalence or mean infestation); distribution and dispersal (displacements at different scales, gene flows); behaviour (e.g. questing activity, host preference); search for tick-borne pathogens (presence and/or prevalence)</td></tr></tbody></table>

The target “populations” were *I. ricinus* at all life stages: larvae, nymph and adult. The “context” corresponded to European France as the target area (French territories outside the European continent were excluded because they are outside the distributional range of *I. ricinus*) and included the environmental factors of interest identified from both short-term punctual studies and long-term monitoring and from micro-habitat to bio-regional scales. The “comparator” corresponds to the kinds of comparisons that could be made with the references. All types of comparators were eligible for the review a priori. Expected comparators were spatio-temporal comparisons, including inter-annual (i.e., dynamics), intra-annual (i.e., seasonal variation in questing tick density), and daily comparisons (i.e., abundance according to the hour of the day). Spatial comparisons occurred at multiple scales: micro-habitats, habitats, landscapes and the biogeographic scale. It also included comparisons between vegetation management types, levels of anthropic pressure and/or types of anthropic activities, vertebrate host densities and physical, chemical or biological treatments of the environment or the host. The “outcome” variables of interest were those providing information on the ecology of *I. ricinus*: relative abundance in space and time, survival, activity, host use and infestation intensity by life stage, distribution and dispersal. The assessment of tick-borne pathogens in ticks was also considered as an outcome variable.

### Search strategy

#### Keywords and search lines

The literature search was conducted on titles, abstracts and keywords in English, but references in both English and French were considered. The search line included the name of the species of interest, “*Ixodes ricinus*” and all the outcome variables identified in Table 1. The keyword “France” was not included in the search line because the sampling country is not always mentioned in the title or abstract. The keywords
"pathogen" and "infectious agents" were not included to avoid references focused only on cellular or molecular aspects of tick-borne pathogens in *I. ricinus*, assuming that the detection of pathogens would have been expressed as presence or prevalence. The final search line was:

"Ixodes ricinus" AND (abundance OR activity OR [behaviour OR behavior] OR burden OR density OR dispersal OR distribution OR dynamics OR infestation OR presence OR prevalence OR questing).

This search line was adapted to correspond to the different database constraints (see exact search lines in SI 1).

## Databases

The search was conducted between November 14th and December 16th 2019 in the following databases: CAB Direct, JSTOR, Pascal & Francis, PubMed, ScienceDirect, Scopus, WorldCat (see **SI 1** for further details). To access French publications and grey literature, a complementary search was conducted over the same period using "Ixodes ricinus" as the unique keyword in the following databases: Agricola, Open Access Thesis and Dissertations, Thèses vétérinaires - i.e. Doctor in Veterinary Medicine (DVM) dissertation theses - (French only), and theses.fr - i.e. PhD theses - (French only). The efficiency of the search strategy was tested using a previously established test-list of 110 references known to be relevant for at least one of the established criterion references (see **SI 2**). To reach a more exhaustive corpus, additional references identified opportunistically and published until 2020 were also considered and submitted to the same eligibility screening (see below).

## Eligibility screening

We retained peer-reviewed research articles and reviews (not including conference proceedings), book sections, veterinary or university theses published at any time prior to December 16th, 2019. Only references in French or English were considered. Screening was conducted by one of the authors (GP), first on titles, then on abstracts, and finally on the full text when available. Finally, studies were included in this systematic review when they met all of the following criteria (see detailed criteria in table SI 3):

- at the title and abstract stage:

**Population:** The reference title must mention *I. ricinus* or ticks or any word suggesting that *I. ricinus* was studied in the paper (e.g., ectoparasites, tick, vector-borne disease). In the latter case, references were retained for subsequent examination (at full text stage).

**Context:** Studies must be performed at least in part in France. If the country of study was not mentioned, the reference was retained for subsequent examination (at full text stage).

**Comparator:** No type of comparator was excluded.

**Outcome:** Studies must be focused directly on the ecology of *I. ricinus*. For example, those that focused on cellular or molecular aspects of *I. ricinus* biology or on tick-borne pathogens alone, were excluded. If there was a doubt, the reference was retained for subsequent examination of the full text.

- at full text stage:

**Population:** Only articles concerning *I. ricinus* were retained, i.e., with at least one mention of the species.

**Context:** All references including at least one sample from France, Corsica island or other French islands of the Mediterranean Sea, Bay of Biscay, Celtic Sea, English Channel, and North Sea were retained.

**Comparator:** No type of comparator was excluded.

**Outcomes:** The same criteria used for the title and abstract stage were applied.

## Systematic map and narrative synthesis

### Database for the systematic map

A dataset was created, composed of 17 bibliographic fields and 41 descriptive fields. The 41 descriptive fields were filled mainly on the basis of "Materials and methods" and "Results" sections, annexes and supplementary materials of the retained references. These fields described the study type (2 fields), the sampling strategy in time (4 fields) and space (10 fields), the sampling methods (17 fields), the pathogens studied (4 fields) and the explanatory variables (2 fields). A field was added to justify the potential exclusion of the reference, and another field for comments. The dataset, with a detailed fields description, is available in Perez (2023; https://doi.org/10.18167/DVN1/ACTNOI).

### Narrative synthesis

The narrative synthesis presented the type of collected data, the spatial and temporal scales studied, as well as the abiotic and biotic variables associated with the presence (/absence), abundance and activity of
*I. ricinus*. The vertebrate hosts studied and their mean infestation rates by different *I. ricinus* life stages were retrieved from the literature. These data were discussed with respect to existing knowledge on the host species use in Europe. Tick-borne pathogen prevalence per tick life stage was summarised, along with associated detection methods, and distribution maps were established. The collected data on pathogen detection were then discussed taking into account the vector competence of *I. ricinus* and the potential reservoir role of the different vertebrate hosts.

# Results and discussion

## Reference search results and bibliographic description

### Reference search and screening

The systematic search retrieved 19,654 references, as presented in the PRISMA flow chart (Figure 1). This included 3,091 references from CAB Direct, 858 from JSTOR, 662 from Pascal & Francis, 2,102 from PubMed, 2,731 from ScienceDirect, 2,473 from Scopus, and 6,174 from WorldCat databases. The complementary search for grey literature in other databases allowed us to identify 1,316 references from Agricola, 150 references from Open Access Thesis and Dissertations, 40 French DVM dissertation theses, and 57 French PhD theses. Only five of the 110 established references from the test-list were not found during our systematic literature search (i.e., 95.4% of references were found). Additionally, 15 references found opportunistically, including five between 2019 and 2020, were considered and fulfilled the inclusion criteria.

<figure><img src="image_3.png" /><figcaption>**Figure 1** - PRISMA-style scheme reporting the literature search and selection strategy arriving to the final 187 references including the 149 peer-reviewed articles used for data compilation.</figcaption></figure>

After having discarded 11,298 duplicates (57.4%), 8,370 references underwent title and abstract screening and 198 underwent full-text screening for eligibility (Figure 1). The most common reasons for exclusion at the title and abstract stage were that sampling was not conducted in France or studies focused on cellular or molecular aspects of *I. ricinus* biology. The most common reasons for exclusion at the full text stage were that studies focused on tick-borne pathogen without reference to the vector (laboratory studies or interactions with the vertebrate host only) (7 cases), or were laboratory-based studies of *I. ricinus* vector competence. In the end, 187 references fulfilled the inclusion criteria (SI 5).

### Description of eligible references

Most of the 187 references were peer-reviewed journal articles and included primary research articles (n = 137, 73.3%) and reviews (n = 12, 6.4%), whereas other documents were DVM and Doctor of Pharmacy (PharmD) dissertations (n = 22, 11.8%), PhD theses (n = 15, 8.0%), or book sections (n = 1, 0.5%). Two-thirds of the journal articles were in English (n = 97, 65.1%), while others were in French (n = 52, 34.9%). The oldest reference recorded was published in 1965. References were scarce until the 1990's, slowed-down again in the 2000's and then increased again from 2010 onwards (SI 6). The 12 selected reviews provided only a broad
overview of ticks and tick-borne diseases or, conversely, a synthesis on some precise aspect of *I. ricinus* ecology and tick-borne diseases in France; none contained a systematic map providing a summary of existing data for the species.

Of the peer-reviewed articles, most were based on field data followed by laboratory analyses (e.g., searching for pathogens) (n = 130, 87.2%), but some used field-collected ticks to conduct further laboratory experiments (e.g., assessing the effect of a variable on tick activity) (n = 3, 2.2%) or laboratory methodological evaluation (n = 4, 8.1%). Field studies were mainly exploratory (i.e., considering at least one explanatory variable; n = 68, 45.6%) and case/occurrence reports (i.e., only descriptive; n = 60, 40.3%), but two of them (1.5%) were methodological evaluations of sampling techniques. Among studies followed by experiments, one (0.7%) was conducted to assess the reservoir competence of Siberian chipmunks, *Tamia sibiricus barberi*, for *Borrelia* spp., and two (1.3%) combined field data and laboratory experiments to study tick adaptation to climate. Among laboratory methodological evaluations, three (2.2%) were associated with the development of laboratory methods for pathogen detection, and one (0.7%) was involved in the development of a method to study tick population genetics based on field-sampled ticks.

## Descriptive synthesis of the ecology of *Ixodes ricinus* in France

### Distribution of *Ixodes ricinus*

Over the past fifty years, several studies were conducted to assess the distribution of *I. ricinus* in different regions of France. The presence of *I. ricinus* was reported when ticks were questing on vegetation using the dragging or flagging method (n = 98), attached on a host (n = 59), or both (n = 25). The sampling locations at the department level could be identified in 127 articles. Thus, we used this spatial scale (NUTS-3) to depict the known distribution of the tick species. A distribution map by department was produced from the retrieved data (Figure 2 and SI 7). Sampling effort varied greatly across the territory, with most studies concentrated on the departments of Ille-et-Vilaine (n = 23, Brittany, western), Bas-Rhin (n = 18, Alsace, north-eastern), Essonne (n = 16, Paris region), Loire-Atlantique (n = 15, Pays-de-la-Loire, western), Haut-Rhin (n = 15, Alsace, north-eastern), Puy-de-Dôme (n = 13, Auvergne, central), and Sarthe (n = 12, Pays-de-la-Loire, western). Studies covered 90 out of 96 European French departments. Among these 90 departments, the presence of *I. ricinus* was confirmed in 87 (97.7%).

An inventory in the Rhône Valley (south-eastern France) of a 330×80 km area, from Mediterranean sea and northward, recorded the presence of *I. ricinus* in the northern part of the study area, but not the southernmost part (Gilot et al., 1989). In south-western France, in a study that aimed at detecting the presence of *I. ricinus* on 100 sites over 15 different vegetation types covering 23 departments, the species was never detected in sites with Mediterranean vegetation (Doche et al., 1993; Gilot et al., 1995). However, in Corsica, Grech-Angelini et al. (2016) reported the species feeding on cattle in areas above 600 m above sea level (a.s.l.) and recently Sevestre et al. (2021) reported the species on hosts and questing in south-eastern France (Alpes-Maritimes) between 450 m and up to 1300 m a.s.l.. Thus, *I. ricinus* ticks seem to be present in some Mediterranean departments, but only under specific environmental conditions and above a certain altitude (Stachurski & Vial, 2018; Sevestre et al., 2021).

Climate conditions above a certain altitude also limit *I. ricinus*. For instance, Gilot et al. (1989) in the Rhône Valley recorded the species from 200 to 1,150 m a.s.l., but the species was more recently collected at the top of the Pic de Bazès, in the eastern part of the French Pyrenees, at 1,800 m a.s.l. (Akl et al., 2019). These data support other observations in Europe that have shown that its presence is increasingly detected at higher altitudes, beyond the previously established 1,500 m (Gern et al., 2008; Danielova et al., 2006; Gilbert, 2010; Martello et al., 2014; Garcia-Vozmediano et al., 2020).

The species was also considered to be scarce on the Atlantic coast because of coastal environmental conditions, like wind and spray which can be highly desiccative (Degeilh et al., 1994). This tick is nonetheless present on Belle-Île-en-Mer island (Bonnet et al., 2007), indicating that the species can be present on islands, but at low abundance. Indeed, ten years after the first study, Michelet et al. (2016) did not collect any *I. ricinus* ticks on this same island.

At the landscape level, the presence of the species is associated with wooded areas, either deciduous or deciduous/coniferous mixed forests, small woods, copses and hedgerows in agricultural matrix, and can be found in adjacent grassland and wet meadows. The species is rare in other open habitats, like crops and grasslands, but can be found in public parks depending on their level of forestation (Gilot et al., 1975a; Doche et al., 1993; Degeilh et al., 1994; Gilot et al., 1994b; Doby & Degeilh, 1996; Pichot et al., 1997; Mémeteau et al., 1998; Boyard et al., 2007; Boyard et al., 2011; Agoulon et al., 2012; Perez et al., 2016; Vourc'h et al., 2016; Ehrmann et al., 2017; Goldstein et al., 2018; Mathews-Martin et al., 2020). Landscapes with a moderately
fragmented forest, which provides forest-grassland or forest-agriculture ecotones and harbouring high host densities can favour high nymph abundance (Perez et al., 2016; Wongnak et al., 2022).

<figure><img src="image_4.png" /><figcaption>**Figure 2** - Distribution map of *Ixodes ricinus* in European France by departments according to the final 187 references, and whether ticks were questing or attached on host. Refer to SI 7 for the name of the departments.</figcaption></figure>

Temporal variation in the density of questing *Ixodes ricinus*

Of the 98 articles that sampled questing ticks, 42 analysed temporal variation in tick density, either per sampling area (e.g., nymphs/10m²; n = 31) or per sampling time (e.g., nymphs per hour; n = 11). Both the number of collections and sampling intervals varied strongly among these studies (from a single sample to monthly sampling over several years and from one sample per year to several samples on the same day). Studies have mostly focused on nymphs, with few reports on annual or seasonal activity patterns of larvae. As *I. ricinus* is susceptible to desiccation, weather conditions, and particularly temperature and humidity, were most frequently examined. Here, we report variables that have been linked to variation in *I. ricinus* activity, without assessing potential bias.

Temperature is an important factor affecting tick activity. In France, *I. ricinus* activity seems optimal at about 16°C with a very sharp drop below 5°C (Aubert, 1975; Tomkins et al., 2014; Cat et al., 2017). Nonetheless, it should be noticed that despite negative temperatures the days before collection (as low as - 7°C), attached feeding-ticks are reported on large mammals, possibly activated by the animal's warmth while resting (Doby et al., 1994). Conversely, temperatures above 30°C inhibit tick activity, even if residual activity can persist (Cat et al., 2017). More generally, it is the cumulative temperature over several days that affects the activity of *I. ricinus* (Perret et al., 2000; Tagliapietra et al., 2011). For instance, in north-eastern France, adult tick feeding activity – estimated by individuals found feeding on foxes – was triggered by a 10-day mean maximum temperature above 9°C prior to the fox hunt, while a mean minimum 10-day temperature below 1°C inhibited it (Aubert, 1975). It is nonetheless important to note that threshold temperatures for tick activity could vary among climates if tick populations undergo local adaptation, with ticks remaining active at lower temperatures in colder climatic regions for example (Tomkins et al., 2014; Gilbert et al., 2014).

Combined with temperature, humidity is also an important limiting factor for the survival and activity of *I. ricinus* ticks. It is generally considered that ticks need a relative humidity greater than 70-80% to maintain water balance (Gray et al., 2016). Therefore, ticks regularly interrupt host-seeking activity and move down to moist litter to rehydrate. Saturation deficit, which integrates both relative humidity and temperature, is considered as a better predictor of tick activity than temperature or humidity alone (Perret et al., 2000; Hauser et al., 2018). In France, it was reported that the activity of *I. ricinus* nymphs could be partially predicted by the mean 7-day minimal relative humidity, and marginally by precipitation in the four weeks prior to sampling, two determinants of the water available in the environment (Paul et al., 2016; Cat et al., 2017).

Photoperiod can also drive questing activity of *I. ricinus* as it influences the beginning of developmental diapause and the end of behavioural diapause (Gray et al., 2016). Briefly, decreasing daylight induces a developmental diapause in eggs and fed larvae and nymphs, delaying development for at least three months,
and results in a behavioural diapause of tick activity (Perret et al., 2003). Conversely, increasing daylight triggers tick activity for nymphs and adults. Darkness is favourable for the horizontal displacement of ticks, likely because it is generally associated with a reduction in desiccation risk (Perret et al., 2003).

As daylight, temperature and humidity change daily, tick activity is subject to daily variation. Recent results from eastern France (near the city of Lyon, Rhône) suggest that *I. ricinus* nymphal activity in spring decreases during the day (between 7 am and 4 pm) with increasing temperatures and decreasing humidity (Kraemer, 2018). Another study, carried out in south-western France (Haute-Garonne), suggested that ticks were more active during the afternoon (3-6 pm) in winter, at the end of the day in spring and summer, and remained active at night in summer, as long as temperature and humidity are favourable (Coiffait, 2019). These results are concordant with other studies in Europe showing increasing activity after sunrise in cold months, decreasing activity and shift in activity toward the night in hot months (Mejlon, 1997; Zöldi et al., 2013; Edwards & Campbell, 2021). Nocturnal activity in summer could explain an increase in tick infestation of nocturnal and crepuscular host species like red foxes (Aubert, 1975).

It was hypothesized that daily tick activity is adapted to host activity to increase encounter rate. For instance, Matuschka et al. (1990) observed in laboratory conditions that larvae feeding on different host species detached at different periods of the day, but whether this is an effect of host activity (e.g., grooming, exploratory movements) or a behavioural adaptation remains unknown. Recently, in south-western France, Coiffait (2019) compared the daily activity of adult ticks with the daily activity of roe deer, *Capreolus capreolus*, which have a crepuscular activity, but found no relationship. However, these preliminary results need to be confirmed insofar as roe deer behaviour itself can be modified in anthropic landscapes (Bonnot et al., 2013). More data are thus needed on the influence of local host community on tick activity of all stages.

Given these dependencies, tick activity may vary strongly over a year and under different climates, resulting in seasonal and geographical variation in exposure risk for humans and their domestic animals. In France, the general phenology of *I. ricinus* seems to be the same as in other parts of Europe under the same climates (Kurtenbach et al., 2006). In temperate oceanic and temperate semi-continental climates, the activity peak of larvae is generally reached in late spring or summer, depending on meteorological conditions (L'Hostis et al., 1995; Agoulon et al., 2019; Bournez et al., 2020). However, data on larval activity are scarce and differences in phenology should be confirmed. Moreover, vegetation height can bias larval sampling, which typically quest low in the vegetation (Dobson et al., 2011). Larvae are scarce or absent in winter, suggesting that even if a female tick feeds and lays in late autumn or early winter, hatching occurs only in spring (L'Hostis et al., 1995). Under climates with mild temperatures throughout the year, as in the temperate oceanic climate of western France, nymphs can be found throughout the year since the required minimum favourable abiotic conditions are met (Agoulon et al., 2019). Under these climates, the peak in nymphal activity occurs between March and June (Cat et al., 2017; Degeilh, 1996; Agoulon et al., 2019). This peak can be delayed in years with mild springs and shortened by high local host densities that rapidly remove ticks from the questing population (Randolph & Steele, 1985; Vassallo et al., 2000). Under semi-continental climates, the peak of nymphal activity is observed in May-June (Pérez-Eid, 1989; Ferquel et al., 2006; Beytout et al., 2007; Goldstein et al., 2018; Bournez et al., 2020a) with no (or very few) questing nymphs found during the cold season. A weaker peak of activity was sometimes observed in September-October (L'Hostis et al., 1995; Degeilh et al., 1996; Cat et al., 2017; Lejal et al., 2019b); this second peak could result from the emergence of larvae fed in spring rather than to the revived activity of nymphs which survived the summer (Randolph & Steele, 1985; Bregnard et al., 2021). Under mountainous climates, a unique peak of activity is observed in summer (Jouda et al., 2004). As adults are less susceptible to desiccation than immature stages (Perret et al., 2004), their activity tends to be more widespread through the year (Pérez-Eid, 1989), but still follows the same general pattern as nymphs (Aubert, 1975; Degeilh et al., 1996; L'Hostis et al., 1996a; L'Hostis et al., 1996b; Marchant et al., 2017; Goldstein et al., 2018; Agoulon et al., 2019). Under Mediterranean climates, like in Corsica, the peak in adult activity is in autumn, while data on larval and nymphal activity are lacking (Grech-Angelini et al., 2016).

To study the trends in population dynamics of *I. ricinus*, long-term data are needed to dampen year-to-year variation. Paul et al. (2016) sampled questing ticks every spring between 2008 and 2014 in a suburban forest in the Paris region (Essonne). This study reported that main climatic variables explaining inter-annual variation in the density of questing ticks were the number of days below zero degrees within a year and minimal temperatures 8-9 months prior to tick collection. Thus, low winter temperatures, but also large temperature variation in winter and extreme climatic events could have a negative effect on tick survival, explaining part of the annual variation in tick density (Herrmann & Gern, 2013; Paul et al., 2016; Hauser et al., 2018). However, in Paul et al. (2016), inter-annual fluctuations in questing nymph density were considered to be more closely linked to fluctuations in vertebrate host densities and vegetation cover than to meteorological data per se. Similar inferences were made in longitudinal studies performed in Switzerland and Germany
(Brugger et al., 2018; Hauser et al., 2018; Bregnard et al., 2020). Perez et al. (2016) also reported that nymphal
density was associated with both the presence of larvae and the abundance of small mammals the previous
year. Larval density was itself associated with the proportion of woodlands in the surrounding landscape, a
privileged habitat for roe deer, which are the main hosts of adult females (Perez et al., 2016; Morellet et al.,
2011).

Despite some studies documenting a northward and altitudinal expansion of *I. ricinus* in Europe, probably linked to climate changes, few sampling campaigns have been conducted over a sufficiently long time period to test an effect of climate change on tick abundance at more local scales (Lindgren et al., 2000; Léger et al., 2013; Medlock et al., 2013). To our knowledge, the longest *I. ricinus* yearly population survey, conducted in the eastern part of the species range (Tula region, western Russia) between 1977 and 2011, showed a general increase in adult abundance since 1990 in relation to an increase in degree days (cumulated daily temperature) during the August-October period. This increase was also associated with changes in forest coverage and fragmentation observed in the region following socio-economic changes (Korotkov et al., 2015). Thus, while weather conditions have an influence on annual tick population densities, hosts and landscape changes seem to have an influence as well. These factors are nonetheless difficult to disentangle since they generally interact.

Host use

Out of 59 articles reporting tick sampled on hosts, only 33 (55.9%) presented sufficient details to be informative on host-associated infestation rates. The potential vertebrate host species of *I. ricinus* studied in France and the degree of parasitism by each life stage is presented in SI 8. Overall, 55 species were examined for the presence of *I. ricinus* ticks. These species included 29 mammalian species (4 Carnivora, 8 Cetartiodactyla, 4 Eulipotyphla, 1 Lagomorpha, 1 Perissodactyla and 11 Rodentia) reported in 34 articles, and 26 avian species (24 Passiformes and 2 Piciformes) reported in 4 articles. No data on Squamata (i.e., lizards and snakes) were found. More detailed data on parasitism (i.e., infesting life stages and/or prevalence/intensity of infestation) were available in 26 articles for mammalian hosts, but in only two studies for avian hosts. In the first avian study, 21 different avian species were included (Marsot et al., 2012), while in the second one, only the Eurasian blackbird, *Turdus merula*, was considered (Grégoire et al., 2002).

Data from different studies preclude direct comparisons of host infestation levels because biogeographic
zones and sampling season usually differ from one study to another. For instance, wild ungulates are typically
studied in winter, during the hunting season, when ticks are less active (Doby et al., 1994), whereas birds are
captured in spring, when ticks are highly active (Marsot et al., 2012), and small mammals are trapped from
spring to autumn (L'Hostis et al., 1996b; Perez et al., 2016). In addition, it is not possible to compare levels of
host infestation when comparing areas where *I. ricinus* is very frequent, like in the northern part of France
(Pérez-Eid, 1990; Doby et al., 1994; L'Hostis et al., 1996b) to areas where this species is very rare, like in
Corsica (Grech-Angelini et al., 2016). Finally, the modalities (e.g., time of inspection, body part inspected) of
tick collection on hosts also varies from one study to another. For instance, wild boars, *Sus scrofa*, were
inspected only five minutes in the field (Doby et al., 1994), while red foxes *Vulpes vulpes* were meticulously
inspected in laboratory (Aubert et al., 1975). These limits highlight the need to standardize studies, controlling
for spatial and temporal factors, and employing comparable on-host sampling strategies. For instance, two
countrywide standardised studies based on tick collections on red squirrels, *Sciurus vulgaris*, confirmed that
*I. ricinus* is rare under Mediterranean climates compared to Atlantic, semi-continental and mountainous
climates (Romeo et al., 2013; Pisanu et al., 2014).

The proportion of each *I. ricinus* life stage present on a given host species at a given time, can nonetheless
provide some indication on their role as blood source and can enable us to formulate testable hypotheses for
future work. On small rodents (except for Eurasian red squirrels and Siberian chipmunks), larvae were
predominant whereas nymphs were rare (Anderson et al., 1986; Doby et al., 1992; L'Hostis et al., 1996b;
Richter et al., 2004; Vourc'h et al., 2007; Boyard et al., 2008; Marsot et al., 2013; Romeo et al., 2013; Pisanu et
al., 2014; Le Coeur et al., 2015; Perez et al., 2017; Pérez-Eid, 1990; Bournez et al., 2020a). Among rodents,
adult ticks were observed only on black rats, *Rattus rattus*, from Corsica (Cicculli et al., 2019). We can note that
this observation questions the role of black rats in transporting ticks in peri-urban and urban areas.

Larvae and nymphs were frequent on passerine birds, with sometimes more nymphs than larvae (Grégoire et al., 2002; Marsot et al., 2012). In eastern France, Grégoire et al. (2002) found that blackbirds were significantly more infested in rural habitats (74%) compared to urban habitats (2%). This suggests a scarcity of ticks in urban areas compared to rural woodlands, but also a possible role of these hosts in disseminating ticks in urban and peri-urban green spaces. A similar pattern was observed when comparing tick densities in a reference forest plot and peri-urban and urban parks in the City of Lyon (eastern France); ticks were more abundant in the forest plot than in the peri-urban and in urban parks (Mathews-Martin et al., 2020).
Females, nymphs and larvae were all observed on wild ungulates, sometimes with more adults than nymphs (e.g., roe deer, red deer, *Cervus elaphus*, and Pyrenean chamois, *Rupicapra pyrenaica*) (Davoust et al., 2012; Doby et al., 1994; Gilot et al., 1994a). Domestic ungulates can also host numerous female ticks with up to 73 per individual on cattle (L'Hostis et al., 1996a). However, there is no strong evidence that domestic ungulates contribute to an increase of *I. ricinus* populations. For instance, Ruiz-Fons et al. (2012) found a positive relationship of horse abundance with questing larvae, but not nymph, abundance, and Sprong et al. (2019) found a weak negative relationship of cattle abundance with questing adult abundance, while Steigedal et al. (2013) found a negative relationship of sheep presence with nymph and adult abundance. However, in neither case the authors quantified ticks on cattle, horse or sheep, although they may had removed a significant part of the questing ticks (Randolph & Steele, 1985). Furthermore, Ruiz-Fons et al. (2012) and Sprong et al. (2019) found a positive relationship of cattle abundance with *Anaplasma phagocytophilum* prevalence, a pathogen for which cattle are reservoir hosts, suggesting that they had fed a significant part of the tick population.

Few studies were performed and report *I. ricinus* ticks from wild carnivores in France and all were on foxes (Aubert et al., 1975; Doby et al., 1991). Given their low density compared to other host species, their contribution in feeding ticks is likely low (Hofmeester et al., 2016). The presence of wild Carnivores might even have a negative effect on tick populations due to the predation pressure and behavioural modifications they exert on larvae hosts such as small mammals (Hofmeester et al., 2017). More studies are needed to evaluate the importance of wild Carnivores in the population dynamics and maintenance of *I. ricinus* populations.

Studies on domestic Carnivores have focused mainly on infested dogs and cats and frequently fail to report sampling effort, precluding an estimate of infestation level (Panas et al., 1976; Pichot et al., 1997; Gilot et al., 1989; Ulmer et al., 1999; Geurden et al., 2018; Grech-Angelini et al., 2016). However, cats and dogs can be highly infested, with up to 26 and 64 *I. ricinus* ticks, respectively (Geurden et al., 2018). Infestation levels of domestic Carnivores are also influenced by environmental conditions. For instance, Martinod et al. (1985) showed that dog infestation by *I. ricinus* varied greatly between two areas in a 40 km² zone in eastern France (southern Jura mountains) in relation to land use (5.3 and 0.032 *I. ricinus* adult ticks per dogs on 249 dogs from areas with pastures and residential neighbourhoods and 190 dogs from mountainous and plain areas). Like domestic ungulates, the contribution of domestic Carnivores to the population dynamics of *I. ricinus* is unclear. Indeed, domestic vertebrates may act as ecological traps for ticks because of their breeding conditions (housing, antiparasitic treatments).

Despite limited data, observations on host use in France are in general agreement with what is known for the host range of *I. ricinus* across its range (Hofmeester et al., 2016). However, more data is required to better understand the relative contribution of these different host types and to evaluate the contribution of understudied groups (Eulipotyphla, Lagomorpha, Perissodactyla and Squamata) in France and elsewhere.

## Tick-borne pathogens in *Ixodes ricinus* ticks of France

Different tick-borne pathogens, that have been examined in *I. ricinus* ticks in France, are briefly presented below (see McCoy & Boulanger, 2016 for more detail). We summarised existing data from across studies and present these data in detail in the Supplementary Information (SI 9-17). Not enough data exist to establish prevalence maps for most pathogens (with the exception of *Borrelia burgdorferi* s.l.), but presence/absence information is illustrated (Figures 3-10).

### The genus *Anaplasma*

Bacteria of the genus *Anaplasma* are obligate Gram-negative alphaproteobacteria. They are intracellular pathogens transmitted by ticks and responsible for anaplasmoses in vertebrates. Among this genus, *A. phagocytophilum* is the most prevalent species in northern Europe and infects monocytes and granulocytes of ruminants, small mammals, horses, canids, birds and humans (Keesing et al., 2012). Several genetic variants circulate in Europe with some host and vector specificities. Jahfari et al. (2014) identified four genetic variants called “ecotypes” associated with different host groups in Europe. According to these authors, ecotype I is associated with ungulates, dogs, hedgehogs and humans; ecotype II is associated mainly with roe deer; ecotype III is associated with rodents; and ecotype IV is associated with birds, results confirmed by other studies (Jahfari et al., 2014; Stigum et al., 2019; Grassi et al., 2021). These ecotypes also differ by their vectors. Ecotypes I and II are mainly transmitted by *I. ricinus*; ecotype III seems mainly transmitted by *I. trianguliceps*; vectors of ecotype IV are still uncertain, but are suspected to be among the hard ticks that specifically exploit birds; and an ecotype IV-like was associated with *I. ventalloi*, a tick species mostly feeding on European rabbits, *Oryctolagus cuniculus*, and present in France (Gilot et al., 1985; Santos et al., 2018; Jaarsma et al., 2019).
Transmission of some genetic variants by ticks of the genus *Dermacentor* is suspected, but has not been demonstrated (Baldridge et al., 2009). Other tick species might be vector of other specific genetic variants. Anaplasmoses can be of significant medical and economic importance when infecting humans and livestock. It may cause severe disease marked by anemia and leukopenia, fever, headache, and myalgia (Rymaszewska & Grenda, 2008; Stuen et al., 2013; Dugat et al., 2015). Few human cases are diagnosed in France, and occur mainly in the eastern part of the country (Koebel et al., 2012).

DNA of *A. phagocytophilum* bacterium has been detected by PCR methods in questing *I. ricinus* from almost all regions of France and prevalence in ticks shows some geographic disparities (Figure 3; SI 9 and references associated therein), which may be explained, in part, by wild and domestic ungulate densities (Chastagner et al., 2017). Prevalence varied from 0.4% to 5.3% in questing nymphs and from 0.5% to 7.0% in questing adults.

Only five studies have attempted to detect DNA of other *Anaplasma* species in questing *I. ricinus* ticks in France (Bonnet et al., 2013; Michelet et al., 2014; Lejal et al., 2019a; Lejal et al., 2019b; Grech-Angelini et al., 2020a). These other *Anaplasma* species infecting animals are *A. centrale*, *A. marginale* and *A. ovis*, infecting erythrocytes of ruminants, *A. (Ehrlichia) bovis*, infecting monocytes and granulocytes of ruminants, and *A. (E.) platys* infecting mainly platelets of dogs (Rymaszewska & Grenda, 2008). However, *I. ricinus* is not considered to be the vector of these pathogens. Among these other species, *A. marginale* was detected in only one study in *I. ricinus* ticks feeding on cattle and red deer in Corsica with a prevalence of 1.7% (Grech-Angelini et al., 2020a). The presence of these other *Anaplasma* species in *I. ricinus* ticks in France is thus currently anecdotal (*A. marginale*) (see SI 9 for further details).

<figure><img src="image_5.png" /><figcaption>**Figure 3** - Presence maps of *Anaplasma marginale* and *A. phagocytophilum* in questing and attached nymphal and adult *Ixodes ricinus* ticks in European France by department. Detected presence by PCR methods and respective sampling effort per department in number of tested ticks (nymphs and adults) for *A. marginale* (a) and *A. phagocytophilum* (b).</figcaption></figure>

## The genus Bartonella

The *Bartonella* genus is composed of facultative intracellular bacteria transmitted by arthropods such as fleas, lice, haematophagous Diptera, and Acari including ticks, and occurs worldwide (Billeter et al., 2008). Known reservoirs are cats, canids and rodents (Chomel et al., 2004). The main pathogenic species for humans are *B. bacilliformis*, *B. henselae* and *B. quintana* (Angelakis & Raoult, 2014), but only *B. henselae* is of known concern in France. It is responsible for cat-scratch disease which is usually characterized by mild symptoms (aches, malaise), but can sometimes lead to more severe symptoms like endocarditis or meningoencephalitis. Although *B. henselae* is mainly transmitted among the cat reservoirs via fleas (*Ctenocephalides felis felis*) (Chomel et al., 1996), *I. ricinus* is an experimentally confirmed vector and other tick species and haematophagous Diptera are suspected vectors (Billeter et al., 2008; Cotté et al., 2008; Grech-Angelini et al., 2020a; Wechtaisong, 2020). The species *B. birtlessi* that infect rodents is also transmitted by *I. ricinus*, but is likely not pathogenic for humans (Reis et al., 2011b).

In France, Bartonella spp. have been found from different departments, but with limited sampling effort (Figure 4a; SI 10). The bacterium *B. henselae* was the most frequently detected Bartonella species in *I. ricinus*, varying from 0% to 38% (Figure 4b; SI 10). DNA of this bacterium was found in questing nymphs and adults sampled in north-eastern France (Ardennes and Bas-Rhin) (Dietrich et al., 2010; Michelet et al., 2014; Moutailler et al., 2016b), and in feeding adult ticks in Corsica (Grech-Angelini et al., 2020a). In the Paris
region (Essonne), DNA of *B. birtlesii* was detected in questing *I. ricinus* nymphs (Reis et al., 2011b). Other *Bartonella* spp. have been detected in other parts of France, but without an identification to species (Halos et al., 2005; Cotté et al., 2010; Davoust et al., 2012; Bonnet et al., 2013; Paul et al., 2016; Bonnet et al., 2017; Nebbak et al., 2019).

<figure><img src="image_6.png" /><figcaption>**Figure 4** - Presence maps of *Bartonella* spp. and *B. henselae* only in questing and attached nymphal and adult *Ixodes ricinus* ticks in European France by department. Detected presence by PCR methods and respective sampling effort per department in number of tested ticks (nymphs and adults) for *Bartonella* spp. (a) and *B. henselae* (b).</figcaption></figure>

*The Borrelia burgdorferi sensu lato (s.l.) complex*

Some bacterial species of the *B. burgdorferi* s.l. complex are responsible for Lyme borreliosis, the most important vector-borne disease for humans in the northern hemisphere (Borchers et al., 2015) and the most frequent in France. In 2020, the French national surveillance programme estimated a mean incidence of 90 cases/100,000 inhabitants, varying between 11 and 667 cases/100,000 inhabitants depending on the region (https://www.sentiweb.fr). In Europe, several genospecies (genetically-discriminated species) of the complex circulate in different reservoir hosts and can be associated with different pathogenicity (Steinbrink et al., 2022). Small mammal-associated genospecies include *B. afzelii*, *B. (garinii) bavariensis* (formerly *B. garinii* OspA serotype 4, but not differentied from *B. (garnirii) garinii* in all studies; Hördt et al., 2020), *B. bissettii*, and *B. spielmanii*, whereas *B. (garinii) garinii*, *B. turdi*, and *B. valaisiana* are considered to be bird-associated. *B. burgdorferi* sensu stricto (s.s.) is harboured by both small mammals and birds, whereas *B. lusitaniae* is mostly associated with lizards. There is no known reservoir host for *B. finlandensis* (Wolcott et al., 2021). The species most frequently involved in human cases of Lyme borreliosis in Europe are *B. afzelii* and *B. garinii* (Stanek & Reiter, 2011), causing cutaneous and neurological forms of the disease respectively (Strle et al., 2006). Both *B. burgdorferi* s.s. and *B. (garinii) bavariensis* are less frequent in Europe, but are also disease-causing; *B. burgdorferi* s.s. is associated with neurological and arthritic forms of Lyme borreliosis, whereas *B. (garinii) bavariensis* only manifests neurological forms (Wilske et al., 1996; Margos et al., 2013). Other circulating genospecies like *B. spielmanii*, *B. bissettii*, *B. lusitaniae* and *B. valaisiana* rarely cause human borreliosis (Steinbrink et al., 2022). The genospecies *B. finlandensis* and *B. turdi* are only rarely detected in *I. ricinus* ticks and their pathogenicity for humans is unknown (Steinbrink et al., 2022). The role of *I. ricinus* as a vector has been experimentally demonstrated for *B. afzelii*, *B. garinii* and *B. burgdorferi* s.s. (Eisen, 2020).

DNA from different *B. burgdorferi* s.l. genospecies, except *B. (garinii) bavariensis*, *B. bissettii* and *B. finlandensis*, has been detected in questing *I. ricinus* ticks collected in France (SI 11). Although studies on *B. burgdorferi* s.l. have focused on a few French departments, the highest prevalence to date is found in the north-eastern, eastern and central parts of France, where prevalence ranges from 2 to 26% in nymphs (Figure 5a and 5b; SI 11 and references therein). The prevalence of the different genospecies in questing nymphs can be compared between regions from which a sufficient number of ticks were tested. In the north-eastern quarter of France, *B. afzelii* was the most frequently detected genospecies (35-50% of positive ticks) and the only one in Corsica (Figure 5c). The prevalence of *B. burgdorferi* s.s. was generally found to be low across France. However, in one study in northern France, it was the predominant species (32% of positive ticks); the authors suspect that the high prevalence of this genospecies might result from the introduction of the Siberian chipmunk in the sampled forest, which is a competent reservoir with a higher tick burden than local rodent species (Figure 5d) (Pisanu et al., 2010; Marsot et al., 2011; Jacquot et al., 2014; Bonnet et al.,
2015; Jacquot et al., 2016). This genospecies was also the most predominant in southern France (32%) where the overall *B. burgdorferi* s.l. prevalence was low. In north-western France, *B. garinii* was the genospecies most frequently detected (26%), but at low prevalence compared to those observed in the north-eastern quarter of France, again because of an overall low *B. burgdorferi* s.l. prevalence (Figure 5e). The prevalence of *B. valaisiana* varied between 0 and 21% of positive ticks, but did not follow any clear pattern in prevalence (Figure 5f).

<figure><img src="image_7.png" /><figcaption>**Figure 5** - Prevalence maps of *Borrelia burgdorferi* sensu lato and *B. afzelii*, *B. burgdorferi* sensu stricto, *B. garinii*, and *B. valaisiana* in questing and attached nymphal and adult *Ixodes ricinus* ticks in European France by department. Prevalence, corresponding to the minimum detected prevalence by PCR methods, and sampling effort by department, in number of tested ticks, for *B. burghdorferi* s.l. in nymphs (a) and in adults (b), and in nymph and adult ticks together for the genospecies *B. afzelii* (c), *B. burgdorferi* s.s. (d), *B. garinii* (e) and *B. valaisiana* (f).</figcaption></figure>

The higher *B. burgdorferi* s.l. prevalence observed in north-eastern, eastern and central regions can be explained by their high proportion of forested landscapes that support higher wild vertebrate densities, in particular wild ungulates (that are good amplifiers of ticks), and wild rodents and birds (reservoirs of the bacteria), compared to northern and western regions with more open landscapes and less forested areas. Given the strong host specificity of genospecies, regional disparities in prevalence in questing nymphs suggests
that tick host use differs between regions with different climates, landscapes and host communities. For instance, the proportion of *Borrelia* species harboured by avian species (e.g., *B. garinii*) seems higher in western regions and those harboured by small mammal species (e.g., *B. afzelii*) seem higher in north-eastern regions. Nonetheless, when considering genospecies prevalence, these results are mostly in accordance with the E-W geographical gradients in *B. burgdorferi* s.l. prevalence observed across Europe (Strnad et al., 2017).

The *B. burgdorferi* s.l. prevalence was also found to vary from site to site and from year to year within regions (Boulanger et al., 2018). For instance, in a four-year follow-up on four sites in Alsace region, Boulanger et al. (2018) reported prevalence varying from 0.7% to 13.6% between sites in the same year, and from 7.7% to 26.7% between years for the same site. Studies at landscape and local scales suggest that pathogen prevalence is positively associated with wooded habitat ecotypes (Halos et al., 2010; Perez et al., 2020), but negatively to habitat diversity (Ehrman et al., 2018). This may be explained by differences in the proportion of each host group used by larvae, which might also vary temporally because of high fluctuations in small mammal population sizes (Perez et al., 2017).

### Borrelia miyamotoi bacterium

The bacterium *B. miyamotoi* is currently the only known species among *Borrelia* relapsing fever (RF) bacteria to be transmitted by a hard tick in Europe; soft ticks and lice are the vectors of the other species of this group (Platonov et al., 2011; Wagemakers et al., 2015). Suspected reservoir hosts are rodents, but these bacteria can also infect some bird species (e.g., wild turkeys, *Meleagris gallopavo*, common blackbirds) and large mammals (roe deer, wild boars) (Wagemakers et al., 2015). In humans, *B. miyamotoi* is responsible for acute febrile illness and meningoencephalitis (Wagemakers et al., 2015) and the number of human cases reported is continuously increasing in Europe (Henningsson et al., 2019; Tobudic et al., 2020). It has been detected in *Ixodes* ticks, including *I. ricinus*, from different regions of the Northern Hemisphere, and, in contrast with other *Borrelia* spp., trans-ovarial transmission in ticks is thought to occur (Wagemakers et al., 2015; van Duijvendijk et al., 2016).

DNA of *B. miyamotoi* was formally detected by PCR methods for the first time in north-eastern France (Ardennes), both in samples from bank voles (four positive rodents out of 72 tested – 5.5%) and from questing adult female *I. ricinus* ticks (eight positive out of 267 tested – 3.0%) (Cosson et al., 2014; Moutailler et al., 2016b). The presence of this bacterium was subsequently detected by PCR methods in the Paris region, in north-eastern France (Alsace, Champagne-Ardenne), and in Corsica island, with observed prevalence varying between 0.75 and 4.2% in questing nymphs and between 0 and 21.7% in adults (SI 12) (Vayssier-Taussat et al., 2013; Paul et al., 2016; Boulanger et al., 2018; Lejal et al., 2019a; Lejal et al., 2019b; Nebbak et al., 2019; Boyer et al., 2020). Other RF *Borrelia* sp. have been detected in north-eastern France (Alsace region) that could be *B. miyamotoi*, but the species was not identified (Richter et al., 2003).

### Coxiella burnetii bacterium

The *Coxiella burnetii* bacterium is a worldwide pathogen responsible for Q fever (Baca & Paretsky, 1983). Potential reservoir host species include ticks, mammals (more than a hundred species recorded) and birds (at least twenty species recorded) (González-Barrio & Ruiz-Fons, 2018; Ioannou et al., 2009). However, domestic ruminants are the most frequent reservoir host leading to human transmission (Eldin et al., 2017). The disease causes fever, myalgia, nausea, diarrhea, endocarditis and hepatitis or meningoencephalitis in humans. In ruminants, it is responsible for reproductive disorders and abortions (Agerholm, 2013; González-Barrio & Ruiz-Fons, 2018; Eldin et al., 2017). DNA of this bacterium has been found in more than 40 hard tick species and in 14 soft tick species (Eldin et al., 2017), but vector competence has only been experimentally confirmed for few species (*D. andersoni*, *Haemaphysalis humerosa*, *H. aegyptium*, *H. asiaticum*, *I. holocyclus*, *Ornithodoros hermsi*, and *O. moubata*) (Duron et al., 2015). The competence of *I. ricinus* has not been tested, and tick bites are likely not the main transmission route of the bacteria (see in Duron et al., 2015). Indeed, infections can be acquired directly by aerosols from infected vertebrate feces and urine (Eldin et al., 2017) or via the milk of infected female mammals (Pexara et al., 2018; Eldin et al., 2016). The bacterium is also excreted in tick feces, which probably contribute to its dissemination in the environment and to infection via aerosol transmission (Körner et al., 2020).

In France, few studies have searched for *C. burnetii* in questing *I. ricinus* (Figure 6; SI 13). For this bacteria, sequencing is essential to avoid confusion with *Coxiella*-like symbionts (Jourdain et al., 2015). Bonnet et al. (2013) detected DNA of this bacterium in adult ticks from four out of five departments sampled (8 of 44 tested ticks, 18.2%). However, none of 998 questing nymphs, and 60 questing adult ticks from the Paris region (Essonne) were found positive (Lejal et al., 2019a; Lejal et al., 2019b), nor the 62 adults and 3,850 questing
nymphs collected in Alsace (Vayssier-Taussat et al., 2013). The 115 *I. ricinus* ticks collected directly on diverse wild and domestic animals in Corsica were all also negative for *C. burnetii* DNA (Grech-Angelini et al., 2020a).

<figure><img src="image_8.png" /><figcaption>**Figure 6** - Presence map of *Coxiella burnetii* in questing and attached nymph and adult *Ixodes ricinus* ticks in European France by department. Detected presence by PCR methods and respective sampling effort per department in number of tested ticks (nymphs and adults) for *C. burnetii*. * DNA of an unidentified *Coxiella* sp. was detected.</figcaption></figure>

### The genus Ehrlichia

Species of the *Ehrlichia* genus are obligate intracellular bacteria that infect mammalian blood cells. Several *Ehrlichia* species are transmitted by ticks and can cause infections in humans and domestic animals (Rar & Golovljova, 2011). The known pathogenic species for humans *E. chaffeensis*, *E. ewingii*, *E. minasensis* and *E. ruminantium*, and their known reservoir hosts are cervids, canids and cervids, cattle and cervids, and ruminants, respectively. Only *E. canis*, *E. chaffeensis*, *E. minasensis* are known to be present in Europe (Rar & Golovljova, 2011; Cicculli et al., 2019). Symptoms in humans are fever, headache, myalgia, and nausea, with only the more severe disease leading to death.

The role of *I. ricinus* as vector of these bacteria is still uncertain and requires explicit evaluation. Studies were conducted to search for *Ehrlichia* DNA in questing *I. ricinus* ticks sampled in France, but with mixed results. No positive ticks were found in intensive studies of questing ticks carried out in north-eastern France (Ardennes) (Moutailler et al., 2016b), in the Paris region (Essonne) (Lejal et al., 2019a; Lejal et al., 2019b), and in two sites in north-eastern France (Alsace) (Michelet et al., 2014). Similarly, no positive *I. ricinus* adults were collected from hosts in Corsica (Grech-Angelini et al., 2020a). DNA of the *Ehrlichia* genus was however detected in north-eastern France (Alsace region) in questing *I. ricinus* nymphs and adults, but the species was not identified (Ferquel et al., 2006). Another study in Alsace also found *E. canis* DNA in questing *I. ricinus* nymphs, but the prevalence could not be estimated (Vayssier-Taussat et al., 2013). Strains of *Ehrlichia* bacteria were also detected in western France (Brittany region); one was closely related to a strain from northern Italy, one was very similar to the *Ehrlichia* sp. HI-2000 strain of the *E. canis* group, and the last to a strain identified in Japan (*Ehrlichia* sp. Yamaguchi) and closely related to *E. muris*, which infects rodents (Marumoto et al., 2007). These results suggest a low prevalence of these bacteria in questing *I. ricinus* ticks in France.

### Neoehrlichia mikurensis bacterium

*Neoehrlichia mikurensis* is an obligatory intracellular bacterium. It was first detected in *I. ricinus* in the Netherlands and *I. ovatus* in Japan, which are – with *I. persulcatus* – likely the main vectors, and in rodents (brown rats, *R. norvegicus*) in China, the reservoir hosts (Schouls et al., 1999; Pan et al., 2003; Kawahara et al., 2004). The bacterium was also found in dog blood (Rar & Golovljova, 2011). The first human cases of infection by *N. mikurensis* were described in Germany and Sweden in 2007 (von Loewenich et al., 2010; Welinder-Olsson et al., 2010). More recently, the first human cases in France were described (Boyer et al., 2021). This bacterium causes a systemic inflammatory syndrome in persons with hematological or immunological deficiencies, accompanied by fever, diarrhea and other potential complications (Silaghi et al., 2015; Portillo et al., 2018; Wass et al., 2019).

In France, DNA of the bacterium was detected in five out of 276 bank voles from north-eastern France (Ardennes) (Vayssier-Taussat et al., 2012). Questing ticks from the same areas were subsequently tested for infection and 4 out of 267 *I. ricinus* adult females were positive (Moutailler et al., 2016b). Other studies in
north-eastern France (Alsace) have reported the presence of the bacterium: 1.7% of questing adult *I. ricinus* (Richter & Matuschka, 2012), 1.6% (0.9%-2.5%) of questing nymphs and between 3.2%-6.4% of questing adults of the region (Vayssier-Taussat et al., 2013), and 0.2% (0.02%-0.6%) and 1.3% (0.7%-2.2%) of questing nymphs in Murbach and Wasselone respectively (Michelet et al., 2014). In contrast, no DNA of *N. mikurensis* was found in questing nymphs and adults from the Paris region (Essonne) (Lejal et al., 2019a; Lejal et al., 2019b), nor in Corsica from nine tick species collected from hosts, including 115 *I. ricinus* (Grech-Angelini et al., 2020a). It seems that in France *N. mikurensis* is well present in the north-eastern part (Figure 7). Given the limited number of studies to date, additional work will now be required to complete our knowledge of its overall geographical distribution in the country.

<figure><img src="image_9.png" /><figcaption>**Figure 7** - Presence map of *Neoehrlichia mikurensis* in questing and attached nymph and adult *Ixodes ricinus* ticks in European France by department. Detected presence by PCR methods and respective sampling effort per department in number of tested ticks (nymphs and adults) for *N. mikurensis*.</figcaption></figure>

*Francisella tularensis* and *F. philomiragia* bacteria

*Francisella tularensis* is a facultative intracellular bacterium, present in North-America, Asia and Europe, and detected in several mammal species, mainly lagomorphs and rodents, which are highly susceptible to the bacterium (Larson et al., 2020). It is responsible for tularaemia, a disease characterised in humans by endocarditis, fever, ulcer, pneumonia, septicaemia, myalgia and headache depending on subspecies, site and mode of infection (Hestvik et al., 2014; Gaci et al., 2017). It is suspected to be transmitted by biting insects such as bedbugs, deer flies and ticks and via contact with infected mammals or contaminated water or soil (Genchi et al., 2015; Telford & Goethert, 2020).

<figure><img src="image_10.png" /><figcaption>**Figure 8** - Presence map *Francisella tularensis* in questing and attached nymph and adult *Ixodes ricinus* ticks in European France by department. Detected presence by PCR methods and respective sampling effort per department in number of tested ticks (nymphs and adults) for *F. tularensis*. *
Detection of unidentified *Fransicella* sp..</figcaption></figure>
The bacterium *F. philomiragia* causes pneumonia, fever and septicaemia in humans (Mailman & Schmidt, 2005). Infections with this bacterium are however rare and involve mainly immunodeficient persons or those exposed to contaminated water in their lungs such as after a near drowning experience (Mailman & Schmidt, 2005; Kreitmann et al., 2015). Not much is known about the ecology of this bacterium, but it was found in other tick species and possible ecological similarities with the related *F. tularensis* are suspected (Bonnet et al., 2013).

In France, studies on the presence of *F. tularensis* and *F. philomiragia* in questing *I. ricinus* ticks are rare (Figure 8; SI 14). For this bacteria too, sequencing or specific PCR are necessary to discriminate between *Francisella*-like symbionts and *F. tularensis* (Michelet et al., 2013). DNA of *F. tularensis* was detected in questing ticks sampled in Paris region (Essonne) in two studies, while that of *F. philomiragia* was not (Reis et al., 2011a; Paul et al., 2016). The low prevalence (0-4.3%) in questing adult *I. ricinus* ticks in France is similar to results found in other European countries, and suggests that *I. ricinus* might be only a vector of *F. tularensis* (Reye et al., 2013; Sormunen et al., 2021; Egyed et al., 2012; Kirczuk et al., 2021).

## The genus Rickettsia

The genus *Rickettsia* includes more than thirty intracellular bacterial species. The pathogenic species are separated into two groups: the “typhus” group (TG), with two insect-transmitted species (*R. typhi* transmitted by fleas and *R. prowazekii* transmitted by lice) and the “spotted fever” group (SFG), with most species transmitted by hard ticks (except for *R. felis* transmitted by fleas and *R. akari* by mites). Many other *Rickettsiae* are endosymbionts involved in various metabolic functions in their hosts (Abdad et al., 2018; Bonnet & Pollet, 2021). For the pathogenic *Rickettsiae*, several vertebrate species could play the role of reservoir. Species of the SFG are more or less pathogenic in humans and responsible for rickettsioses, characterised by an eschar at the bite site and/or fever and headache, and sometimes with complications like cutaneous necrosis, pneumonia, endothelial damages and organ failure (Abdad et al., 2018).

<figure><img src="image_11.png" /><figcaption>**Figure 9** - Presence maps of *Rickettsia felis*, and *R. helvetica*, and *R. monacensis* in questing and attached nymph and adult *Ixodes ricinus* ticks in European France by department. Detected presence by PCR methods and respective sampling effort per department in number of tested ticks (nymphs and adults) for *R. felis* (a), *R. helvetica* (b), and *R. monacensis* (c).</figcaption></figure>
In France, the *Rickettsia* species detected in questing *I. ricinus* ticks, when identified at the species level, are *R. felis*, *R. helvetica* and *R. monacensis* (SI 15). Data are too scarce to allow valid comparison of the prevalence between geographical regions (Figure 9d). DNA of *R. helvetica* was found in most regions examined, suggesting a distribution throughout France (Figure 9b) (Parola et al., 1998b; Davoust et al., 2012; Michelet et al., 2014; Moutailler et al., 2016b; Bonnet et al., 2017). When detected, observed prevalence was estimated between 1.1 and 14.3% in nymphs and between 1.6 and 25.0% in adults (Cotté et al., 2010; Michelet et al., 2014; Nebbak et al., 2019; Lejal et al., 2019a). DNA of *R. felis* was detected in questing ticks from the Paris region (Essonne) and from north-eastern (Alsace region) France (Figure 8a) (Vayssier-Taussat et al., 2013; Lejal et al., 2019a; Lejal et al., 2019), whereas *R. monacensis* DNA was found in southern France (Hautes-Pyrénées; Figure 8c) (Akl et al., 2019). Tests to detect DNA of *Rickettsia* SFG were carried out on a large number of questing adult and nymphal ticks in northern-eastern France, but none were found positive (Michelet et al., 2014).

## The genus Babesia

*Babesia* sensu stricto belongs to a species-rich genus of unicellular eukaryotes of the Apicomplexa phylum. They are intra-erythrocyte parasites of vertebrates transmitted principally by ticks and generally characterised by transovarian transmission (Walter & Weber, 1981; Schnittger et al., 2012; Vannier & Krause, 2012; Jalovecka et al., 2019). *Babesia* species are responsible for babesiosis, worldwide tick-borne diseases that affect many mammalian species (mainly cattle, sheep, goat, equidae and canids) including humans as accidental hosts (Chauvin et al., 2009). The disease is characterized by hyperthermia, anaemia and haemoglobinuria and can led to death, particularly in immunosuppressed and splenectomised patients (Hildebrandt et al., 2021). Although tick bites are the main mode of transmission, infections can also occur by blood transfusion (Siński et al., 2011; Fang & McCullough, 2016). Transmission between dogs has been reported by dog bites for *B. gibsoni* and vertical transmission in dogs is suspected for *B. canis* and *B. vulpes* (formerly *Theileria annae* or “*B. microti*-like”; Baneth et al., 2019) (Solano-Gallego et al., 2016). *Babesia* species responsible for human infection in Europe are mainly *B. divergens* and *B. venatorum*, and exceptionally *B. microti* (Hildebrandt et al., 2021). Both *B. divergens*, for which the main reservoir host is cattle, and *B. venatorum* (formerly known as sp. EU1), for which the main reservoir hosts are cervids, are transmitted by *I. ricinus* (see review by Bonnet & Nadal, 2021). *Babesia microti*, which infects rodents and shrews, is transmitted by other *Ixodes* species, specific of small mammals such as *I. trianguliceps*. The role of *I. ricinus* in its transmission remains unclear (Walter & Weber, 1981; Gray et al., 2002; Bown et al., 2008).

Several studies have tested for the presence of zoonotic *Babesia* species in questing *I. ricinus* ticks from France (Figure 10a; SI 16). DNA of *B. divergens* was detected in questing *I. ricinus* ticks from north-eastern (Ardennes), the Paris region (Essonne), central (Saône-et-Loire) and western (Ille-et-Vilaine) France (Figure 10c) (Bonnet et al., 2013; Moutailler et al., 2016b; Paul et al., 2016; Jouglin et al., 2017). DNA of *B. venatorum* was detected in ticks from the Paris region (Essonne), and the north-eastern (Alsace region), southern (Haute-Garonne), and south-western (Haute-Garonne and Hautes-Pyrénées) regions of the country (Figure 10d) (Reis et al., 2011a; Michelet et al., 2014; Paul et al., 2016; Akl et al., 2019; Lejal et al., 2019a; Lejal et al., 2019b; Lebert et al., 2020). Differences in the distribution of the *Babesia* species could be explained by differences in the abundance and prevalence of infection of reservoir hosts in each studied area: *B. venatorum* was more often found in forested landscapes, whereas *B. divergens* occurs in more fragmented landscape with a high proportion of land cover dedicated to cattle breeding.

DNA of other *Babesia* species of medical and veterinary interest has also been examined in questing *I. ricinus*: *B. capreoli* that infects cervids (Young et al., 2019); *B. bovis*, *B. bigemina*, *B. major*, *B. occultans* and *B. ovata* which infect mainly cattle; *B. crassa*, *B. motasi* and *B. ovis* which infect mainly goats and sheep; *B. caballi* which infects equines; *B. canis*, *B. gibsoni*, *B. vogeli* and *B. vulpes* which mainly infect canids (Schnittger et al., 2012; Baneth et al., 2015; Solano-Gallego et al., 2016); and *B. microti* (which actually belongs to a separate phylogenetic clade; Schnittger et al., 2012). Among these, only *B. capreoli* was confirmed to be transmitted by *I. ricinus* ticks and its DNA was detected in questing ticks of this species sampled in western France (Ille-et-Vilaine) and in the Paris region (Essonne) (Figure 10b) (Jouglin et al., 2017; Lejal et al., 2019b).

## The genus Theileria

Although closely related, parasites from the *Theileria* genus differ from those of *Babesia* by a pre-erythrocyte stage in lymphocytes in the vertebrate host, and by the absence of transovarian transmission in the tick vector (Mans et al., 2015). These parasites infect mainly ruminants in countries from the southern
Hemisphere, where they are responsible for important economic loss (Mans et al., 2015), and horses (*Theileria equi*) worldwide (Nadal et al., 2021). Parasites belonging to this genus are not known to infect humans.

In several studies, *I. ricinus* ticks sampled in France were examined for the presence of DNA from several *Theileria* species that are known to occur in Europe and around the Mediterranean basin (SI 16); none was detected. However, strains closely related to *T. parva* and *T. taurotragi* were found by high-throughput sequencing methods in questing *I. ricinus* nymphs sampled in north-eastern France (Alsace region), but no prevalence estimates were calculated (Bonnet et al., 2014). Interestingly, *T. equi* DNA was detected in adult *I. ricinus* that were questing or attached to piroplasm-free vertebrate hosts in Spain, Italy and the Netherlands (Butler et al., 2016; Garcia-Sanmartín et al., 2008; Iori et al., 2010). These results highlight the need to study the vector competence of *I. ricinus* for *T. equi* and other *Theileria* species present in Europe to evaluate its potential contribution in the transmission of the pathogen to horses.

<figure><img src="image_12.png" /><figcaption>**Figure 10** - Presence maps of all *Babesia* spp., *B. capreoli*, *B. divergens* and *B. venatorum* in questing and attached nymph and adult *Ixodes ricinus* ticks in European France by department. Detected presence maps and respective sampling effort per department in number of tested ticks (nymphs and adults) for *Babesia* spp. (a), *B. capreoli* (b), *B. divergens* (c) and *B. venatorum* (d).</figcaption></figure>

### Tick-borne encephalitis virus

Tick-borne encephalitis (TBE) was described for the first time in 1931 in Austria and the virus (TBEV) was isolated in 1937 in Russia (see review by Kaiser, 2008, and Zlobin et al., 2017). This virus belongs to the *Flavivirus* genus of the Flaviviridae family (simple stranded RNA virus). Three main virus sub-types have been identified: the “European” sub-type, the “Far-Eastern” subtype, and the “Siberian” sub-type. However, two other subtypes have been recently described: the “Balkanian” and the “Himalayan” sub-types (Ruzek et al., 2019). The main reservoir hosts are small mammals, among which *Apodemus* spp. mice seem to be particularly infectious for ticks (Labuda et al., 1993c; Labuda et al., 1996; Labuda et al., 1997; Knap et al., 2012). The virus causes meningitis and meningoencephalitis in humans, which can lead to neurological sequelae, such as paralysis, and death. The Far-Eastern subtype results in the most severe forms of the disease, with death in up to 2% of patients (Ruzek et al., 2019). TBEV is mainly transmitted by *I. ricinus* and *I. persulcatus* ticks in Europe (Mansfield et al., 2009). Human infections can occur not only by tick bites, but also by consumption of unpasteurised milk or dairy products from infected animals (Süss, 2011). Transovarian transmission in ticks is weak (Danielova et al., 2002; Labuda et al., 1993a), but co-feeding transmission, where an infected tick infects
non-infected ticks feeding nearby on the host, is of greater epidemiological importance (Labuda et al., 1993c; Labuda et al., 1997). Indeed, it was established that co-feeding transmission is of paramount importance in maintaining the virus in tick populations and thus its circulation in vertebrate hosts (Randolph et al., 1996).

Only the "European" sub-type, considered as the least virulent, is present in western Europe (Bestehorn et al., 2018). In France, TBEV prevalence in questing *I. ricinus* ticks seems low (<0.1% in larvae and <1% in nymphs and adults) and is probably localised in micro-foci (Chatelain & Ardouin, 1978; Pérez-Eid et al., 1992; Bournez et al., 2020a). Too few studies have been conducted to conclude on the distribution of TBEV and its spatio-temporal variation in questing ticks in France, but it is likely present throughout the north-eastern part of the country, with well-identified endemic foci in the Alsace region (Figure 11; SI 17) (Pérez-Eidet al., 1992; Hansmann et al., 2006; Rigaud et al., 2016; Bournez et al., 2020a). Serological results from wild ungulates suggest that the virus is also likely circulating in northern, north-eastern and eastern France, and that a closely related virus is present in the Pyrenees (Bournez et al., 2020b). Human TBE cases have been reported in western and central France (Rhône-Alpes and in Auvergne regions) during the last decade (Velay et al., 2018; Botelho-Nevers et al., 2019). In 2020, 43 TBE cases occurred in eastern France (Ain) following the consumption of goat cheese made with contaminated raw milk and thus identified a new focus (Beaufils et al., 2021; Gonzalez et al., 2022). The distribution of the virus seems to be changing in Europe, probably because of global changes that affect larvae and nymph co-occurrence on hosts and thus the probability of co-feeding transmission. However, this trend might be biased by a better detection of human cases and other socio-economic changes (Randoph et al., 2000; Randolph & Rogers, 2000). Since 2021, TBE has been listed as a reportable disease in France, a measure that should improve our knowledge on human exposure.

<figure><img src="image_13.png" /><figcaption>**Figure 11** - Presence map of tick-borne encephalitis virus (TBEV) in questing and attached nymphal and adult *Ixodes ricinus* ticks in European France by department. Detected presence of TBEV by RT-PCR methods and sampling effort per department in number of tested ticks (nymphs and adults).</figcaption></figure>

## Other viruses

The Eyach virus is a *Coltivirus* that could be responsible for neurological damage, as seropositivity was associated with neuropathies in areas of the former Czechoslovakia (Malkova et al., 1980; Charrel et al., 2004). The virus was first isolated in Germany in 1972 from *I. ricinus* ticks and then again in western France in 1981 (Mayenne) from *I. ricinus* and *I. ventalloi* ticks collected from a European rabbit (Rehse-Küpper et al., 1976; Chastel et al., 1984). However, the vector competence of *I. ricinus* for this virus has not been formally demonstrated and the role of the European rabbit as reservoir remains unclear (Chastel, 1998; Charrel et al., 2004). More recently, viral RNA was detected in questing *I. ricinus* ticks in north-eastern France; in the Alsace region in 2010 and in the Ardennes department in 2012 (Moutailler et al., 2016a).

## Conclusions

This systematic map and narrative review assembled results of studies published in European France between 1965 and 2020 at various spatial scales (country-wide to site-specific) and exploring the influence of different variables (meteorological, biogeographic zones, landscape features, host density, local vegetation, soil characteristics) on the density of questing *I. ricinus*. It also provided summary information on the prevalence and distribution of several tick-borne pathogens detected in *I. ricinus* ticks in the country.
The first studies on the distribution of ixodid tick species in France started in the 60's (Lamontellerie, 1965; Panas et al., 1976). Gilot and colleagues then started to examine the association of *I. ricinus* with different vegetation types and its related phenology (Gilot et al., 1975a; Gilot et al., 1975b). After that, more standardised studies on the distribution and phenology of the species were performed (e.g., Gilot et al., 1989; Gilot et al., 1994). More recent work has focused on identifying landscape, vegetation and microclimatic factors associated with the abundance and phenology of the species using standardised methods and new technologies (e.g., via Geographic Information Systems). The advent of PCR technologies also enabled researchers to examine the presence of associated pathogens. These different studies have thus made it possible to accumulate a certain amount of knowledge about *I. ricinus* in France, but no synthesis of these data was available. This study aimed to fill this void and to highlight remaining knowledge gaps on the distribution, phenology, and host range of *I. ricinus* and on the prevalence of its associated pathogens in certain regions of France.

For example, larval phenology is still poorly described overall, and larval-nymphal phenology and host use under Mediterranean climates remain to be investigated. More longitudinal studies on *I. ricinus* phenology that include multiple environmental parameters are also necessary to better define factors essential for the development of the species and to predict acarological risk, particularly in a context of climate change. Very few such studies have been conducted in France so far (Paul et al., 2016; Wongnak et al., 2022).

Studies on tick host use has focused mainly on Rodentia (mice and voles) and wild Cetartiodactyla (e.g., roe deer), whereas the role of domestic Cetartiodactyla (cattle, sheep, and goats), Perissodactyla (horses and donkey), Carnivora (e.g. cats, dogs, foxes), Aves (birds), Eulipotyphla (shrews and hedghogs), Lagomorpha (e.g., rabbits and hares), and Squamata (e.g. lizards and snakes) remain poorly quantified. It should also be noted that the few studies that exist are rarely comparable (different location, season and/or protocol), preventing direct comparisons of tick burdens between species or between different climates or environments for a same species. A standardisation of protocols is thus called for.

Studies of tick-borne pathogens have focused mainly on *B. burgdorferi* s.l. In addition, due to logistical constraints, these studies have often concentrated around locations of the investigating research units and, more distant or isolated regions have therefore received less attention, leading to a lack of data to inform and prevent tick-borne disease in some local populations (Septfons et al., 2018). This highlights the need to scale studies according to expected outcomes, to ensure for instance that the targeted area lies within the expected domain of the desired model. That said, the data available on *B. burgdorferi* s.l. were sufficient to compare prevalence and the occurrence of different genospecies in questing ticks among regions. The observed gradients mirror observations at the European scale: an increasing prevalence along a SW-NE gradient with an increasing proportion of prevalence of *B. afzelii* (Strnad et al., 2017). These prevalence gradients are likely driven by biogeographic gradients in Europe and the evolutionary history of *Borrelia* genospecies (Margos et al., 2011). The distribution and the spatial variation in prevalence of other tick-borne pathogens are still poorly known and deserve further study. Due to the veterinary importance of babesiosis, the fact that several species can infect humans, the numerous side effects of babesicidal drugs, and the absence of a vaccine against most of the species that occur in France (only a vaccine against *B. canis* exists, to our knowledge: Pirodog, Boehringer Ingelheim Animal Health, France), it is particularly important to intensify research and monitoring of these parasites. Likewise, recent distributional changes in TBEV exposure should be more closely tracked to anticipate prevention. For example, understanding the potential role of birds as dispersers of infected ticks for the geographic expansion of the virus would be extremely informative (Wilhelmsson et al., 2020).

Detection methods of infectious agents in ticks have rapidly improved over the last decades, particularly with the development of high throughput sequencing methods and more sensitive PCR techniques (i.e., quantitative PCR, microfluidic PCR, digital PCR). That said, it is important to remember that the detection of pathogen DNA in an arthropod does not imply that the arthropod is a vector of this organism, it only indicates that a blood meal was taken on an infected host. The formal demonstration of vector competence requires experimental study (Khal et al., 2002; Bonnet & Nadal, 2021). Although the vector competence of *I. ricinus* has been experimentally demonstrated for many important infectious agents, its role in the transmission of other agents such as *C. burnetii*, *F. tularensis*, *F. philomiragia*, and *Rickettsia* spp. still requires experimental validation. Reciprocally, other species can be the vectors of some pathogens transmitted by *I. ricinus* and their role in the zoonotic cycle requires explicit consideration. For instance, few tick species have been experimentally assessed for vector competence for *B. burgdorferi* s.l. (Eisen, 2020), although these bacteria have been frequently detected in *I. acuminatus* (Doby et al., 1990; Szekeres et al., 2015), *I. arboricola* (Spitalska et al., 2011; Heylen et al., 2013), *I. frontalis* (Heylen et al., 2013; Heylen et al., 2017a; Heylen et al., 2017b; Palomar et al., 2017), *I. hexagonus* (Gern et al., 1991; Geurden et al., 2018) and *I. trianguliceps* (Doby et al., 1990; Nefedova et al., 2005). Knowledge on vector diversity and the relative roles of different vector
species is essential for understanding the distribution and observed variation in pathogen prevalence and to establish pertinent prevention measures. The role of other co-infecting tick microorganisms, symbiotic or commensal, in the ecology, physiology and vector competence of *I. ricinus* also needs to be investigated (Bonnet & Pollet, 2021; Lejal et al., 2021). Such studies could uncover new ways of controlling ticks and the pathogens they transmit.

To conclude, more studies are needed to better assess the distribution of *I. ricinus* and its associated pathogens in France, particularly in the context of current global changes that could see a shift in the distribution of native species, the emergence of tropical species in Europe and changes in tick phenology and transmission dynamics. Efforts focused on a better understanding of tick-borne pathogen ecology is also necessary to better evaluate acarological risk. Indeed, human cases of Lyme borreliosis have increased over the last two decades for diverse reasons (e.g., awareness of clinicians, increasing outdoor recreational activities, modifications of the tick ecosystems, etc.) and new tick-borne diseases have emerged like relapsing fever associated with *B. miyamotoi* or *N. mikurensis* (Figoni et al., 2019). Current participative science projects like CITIQUE (https://www.citique.fr/), based on voluntary declarations of tick-bites and tick collection, may fulfil some of these gaps in the future. For example, data collected under these programs should help complete the distribution map of *I. ricinus* and its associated pathogens and should provide information on high human exposure periods (Eisen & Eisen, 2021). More generally, an integrated research programme that links data and knowledge from diverse sources would help to develop more efficient strategies to control tick populations and reduce tick-borne disease risk.

## Acknowledgments

The author thanks Gilles Bourgoin, Sébastien Grech-Angelini, Sara Moutailler, Frank Boué, Mathilde Gondard, Guy Joncour, Lorraine Michelet, Gérald Umhang, Muriel Vayssier-Taussat, Olivier Plantard, Alber Agoulon, Thomas Pollet, Karine Chalvet-Montfray, Émilie Lejal, Maud Marsot, Frédéric Stachurski and Laurence Vial for sharing their raw data on the presence of *I. ricinus* (Figure 2). Prepint version 1 of this article has been peer-reviewed and recommended by PCI Infections: https://doi.org/10.24072/pci.infections.100076 (Santos 2023)

## Funding

This work is issued from a scientific report commanded by of the Direction Générale de la Santé (Ministry of Health) to ANSES (French Agency for Food, Environmental and Occupational Health & Safety) who delegated through a research and development agreement to the École nationale vétérinaire d'Alfort (national veterinary School of Alfort) and allocated funds to hire GP for a 13 months postdoc contract (the complete report in French is available at: https://hal-anses.archives-ouvertes.fr/anses-03263410).

## Conflict of interest disclosure

The authors declare that they comply with the PCI rule of having no financial conflicts of interest in relation to the content of the article. KDM is a recommender at PCIInfections.

## Data, code and supplementary material

All encoded and compiled data and supplementary material are available in Perez (2023): https://doi.org/10.18167/DVN1/ACTNOI.

## Authors' contributions

GP and SB designed the study. GP conducted the literature search, screened the references, developed the bibliographic database and compiled all the data, wrote the first draft of the manuscript and produced all figures and tables. BL gave valuable methodological recommendations. LB, NB, KDM, JF, BL, EQ, MRM and SB discussed data interpretation and presentation and edited the manuscript, figures and tables.
References

Abdad MY, Abdallah RA, Fournier P-E, Stenos J, Vasoo S (2018) A concise review of the epidemiology and diagnostics of Rickettsioses: *Rickettsia* and *Orientia* spp. *Journal of Clinical Microbiology*, **56**, e01728-17 (10 p). https://doi.org/10.1128/jcm.01728-17

Agerholm JS (2013) *Coxiella burnetii* associated reproductive disorders in domestic animals-a critical review. *Acta Veterinaria Scandinavica*, **55**, 13 (11 p). https://doi.org/10.1186/1751-0147-55-13

Agoulon A, Hoch T, Heylen D, Chalvet-monfray K, Plantard O (2019) Unravelling the phenology of *Ixodes frontalis*, a common but understudied tick species in Europe. *Ticks and Tick-borne Diseases*, **10**, 505–512. https://doi.org/10.1016/j.ttbdis.2018.12.009

Agoulon A, Malandrin L, Lepigeon F, Vénisse M, Bonnet S, Becker CAMM, Hoch T, Bastian S, Plantard O, Beaudeau F (2012) A vegetation index qualifying pasture edges is related to *Ixodes ricinus* density and to *Babesia divergens* seroprevalence in dairy cattle herds. *Veterinary Parasitology*, **185**, 101–109. https://doi.org/10.1016/j.vetpar.2011.10.022

Akl T, Bourgoin G, Souq M-L, Appolinaire J, Poirel M-T, Gibert P, Abi Rizk G, Garel M, Zenner L (2019) Detection of tick-borne pathogens in questing *Ixodes ricinus* in the French Pyrenees and first identification of *Rickettsia monacensis* in France. *Parasite*, **26**, 9 p. https://doi.org/10.1051/parasite/2019019

Al-Abri SS, Al Abaidani I, Fazlalipour M, Mostafavi E, Leblebicioglu H, Pshenichnaya N, Memish ZA, Hewson R, Petersen E, Mala P, Minh T, Nguyen N, Rahman M, Formenty P, Jeffries R (2017) Current status of Crimean-Congo haemorrhagic fever in the World Health Organization Eastern Mediterranean Region: issues, challenges, and future directions. *International Journal of Infectious Diseases*, **58**, 82–89. https://doi.org/10.1016/j.ijid.2017.02.018

Anderson J, Doby J, Coutarmanac'h A, Hyde F, Johnson R (1986) Différences antigéniques entre des souches de *Borrelia burgdorferi* isolées d'Ixodes ricinus en Bretagne. *Médecine et maladies infectieuses*, **16**, 171–175. https://doi.org/10.1016/S0399-077X(86)80221-9

Angelakis E, Raoult D (2014) Pathogenicity and treatment of *Bartonella* infections. *International Journal of Antimicrobial Agents*, **44**, 16–25. https://doi.org/10.1016/j.ijantimicag.2014.04.006

Aubert MF. (1975) Contribution a l'étude du parasitisme du renard (Vulpes vulpes L.) par les Ixodidae (Acarina) dans le Nord-Est de la France interprétation de la dynamique saisonnière des parasites en relation avec la biologie de l'hôte. *Acarologia*, **53**, 383-415. https://doi.org/10.1051/acarologia/20142144

Baca G, Paretsky D (1983) Q fever and *Coxiella burnetii*: A model for host-parasite interactions. *Microbiological Reviews*, **47**, 127–149. https://doi.org/10.1128/mr.47.2.127-149.1983

Baldrige GD, Scoles GA, Burkhardt NY, Schloeder B, Kurtti TJ, Munderloh UG (2009) Transovarial transmission of *Francisella*-like endosymbionts and *Anaplasma phagocytophilum* variants in *Dermacentor albipictus* (Acari: Ixodidae). *Journal of medical entomology*, **46**, 625–632. https://doi.org/10.1603/033.046.0330

Baneth G, Cardoso L, Simões PB, Schnittger L (2019) Establishment of *Babesia vulpes* n. sp. (Apicomplexa: Babesiidae), a piroplasmid species pathogenic for domestic dogs. *Parasites & Vectors*, **12**, 129. https://doi.org/10.1186/s13071-019-3385-z

Baneth G, Florin-Christensen M, Cardoso L, Schnittger L (2015) Reclassification of *Theileria annae* as *Babesia vulpes* sp. nov. *Parasites and Vectors*, **8**, 207 (7 p). https://doi.org/10.1186/s13071-015-0830-5

Beaufils F, Benet T, Canu N, Leparc-Goffart I, Decouchon C (2021) Épidémie de méningo-encéphalite à tiques alimentaire en France, 2020. *Infectious Diseases Now*, **51**, S27. https://doi.org/10.1016/j.idnow.2021.06.059

Bestehorn M, Weigold S, Kern WV, Chitimia-dobler L, Mackenstedt U, Dobler G, Id JPB (2018) Phylogenetics of tick-borne encephalitis virus in endemic foci in the upper Rhine region in France and Germany. *PLoS ONE*, **13**, e0204790. https://doi.org/10.1371/journal.pone.0204790

Beytout J, George JC, Malaval J, Garnier M, Beytout M, Baranton G, Ferquel E, Postic D (2007) Lyme borreliosis incidence in two French departments: Correlation with infection of *Ixodes ricinus* ticks by *Borrelia burgdorferi* sensu lato. *Vector-Borne and Zoonotic Diseases*, **7**, 507–517. https://doi.org/10.1089/vbz.2006.0633
Billeter SA, Levy MG, Chomel BB, Breitschwerdt EB (2008) Vector transmission of *Bartonella* species with emphasis on the potential for tick transmission. *Medical and Veterinary Entomology*, **22**, 1-15.
https://doi.org/10.1111/j.1365-2915.2008.00713.x

Bonnet S, Choumet V, Masseglia S, Cote M, Ferquel E, Lilin T, Marsot M, Chapuis JL, Vourc'h G (2015) Infection of Siberian chipmunks (*Tamias sibiricus barberi*) with *Borrelia* sp. reveals a low reservoir competence under experimental conditions. *Ticks and Tick-borne Diseases*, **6**, 393-400.
https://doi.org/10.1016/j.ttbdis.2015.03.008

Bonnet S, De La Fuente J, Nicollet P, Liu X, Madani N, Blanchard B, Maingourd C, Alongi A, Torina A, Fernández De Mera IG, Vicente J, George J-C, Vayssier-Taussat M, Joncour G (2013) Prevalence of tick-borne pathogens in adult *Dermacentor* spp. ticks from nine collection sites in France. *Vector-Borne and Zoonotic Diseases*, **13**, 226-236. https://doi.org/10.1089/vbz.2011.0933

Bonnet S, Jouglin M, Malandrin L, Becker C, Agoulon A, L'Hostis M, Chauvin A (2007) Transstadial and transovarial persistence of *Babesia divergens* DNA in *Ixodes ricinus* ticks fed on infected blood in a new skin-feeding technique. *Parasitology*, **134**, 197-207.
https://doi.org/10.1017/S0031182006001545

Bonnet S, Liu XY (2012) Laboratory artificial infection of hard ticks: a tool for the analysis of tick-borne pathogen transmission. *Acarologia*, **52**, 453-464. https://doi.org/10.1051/acarologia/20122068

Bonnet S, Michelet L, Moutailler S, Cheval J, Hébert C, Vayssier-Taussat M, Eloit M (2014) Identification of parasitic communities within European ticks using next-generation sequencing. *PLoS Neglected Tropical Diseases*, **8**, e2753 (6 p). https://doi.org/10.1371/journal.pntd.0002753

Bonnet SI, Nadal C (2021) Experimental infection of ticks: An essential tool for the analysis of *Babesia*. *Pathogens*, **10**, e1403 (1-14). https://doi.org/10.3390/pathogens10111403

Bonnet SI, Paul REL, Bischoff E, Cote M, Le Naour E (2017) First identification of *Rickettsia helvetica* in questing ticks from a French Northern Brittany forest. *PLoS Neglected Tropical Diseases*, **11**, e0005416 (10 p). https://doi.org/10.1371/journal.pntd.0005416

Bonnet SI, Pollet T (2021) Update on the intricate tango between tick microbiomes and tick-borne pathogens. *Parasite Immunology*, **43**, e12813. https://doi.org/10.1111/pim.12813

Bonnot N, Morellet N, Verheyden H, Cargnelutti B, Lourtet B, Klein F, Hewison AJM (2013) Habitat use under predation risk: hunting, roads and human dwellings influence the spatial behaviour of roe deer. *European Journal of Wildlife Research*, **59**, 185-193. https://doi.org/10.1007/s10344-012-0665-8

Borchers AT, Keen CL, Huntley AC, Gershwin ME (2015) Lyme disease: A rigorous review of diagnostic criteria and treatment. *Journal of Autoimmunity*, **57**, 82-115.
https://doi.org/10.1016/j.jaut.2014.09.004

Botelho-Nevers E, Gagneux-Brunon A, Velay A, Guerbois-Galla M, Grard G, Bretagne C, Mailles A, Verhoeven PO, Pozzetto B, Gonzalo S, Fafi-Kremer S, Leparc-Goffart I, Pillet S (2019) Tick-borne encephalitis in Auvergne-Rhône-Alpes Region, France, 2017-2018. *Emerging Infectious Diseases*, **25**, 1944-1948. https://doi.org/10.3201%2Feid2510.181923

Boulanger N, Zilliox L, Goldstein V, Boyer P, Napolitano D, Jaulhac B (2018) Surveillance du vecteur de la borréliose de Lyme, *Ixodes ricinus*, en Alsace de 2013 à 2016. *Bull Epidemiol Hebdo*, **19-20**, 400-405.

Bournez L, Umhang G, Faure E, Boucher J-M, Bou F, Jourdain E, Sarasa M, Llorente F, Jim MA, Moutailler S, Lacour SA, Lecollinet S, Beck C (2020) Exposure of wild ungulates to the Usutu and tick-borne encephalitis viruses in France in 2009 – 2014: Evidence of Undetected Flavivirus circulation a decade ago. *Viruses*, **12**, 10 (16 p). https://doi.org/10.3390/v12010010

Bournez L, Umhang G, Moinet M, Boucher J, Demerson J, Caillot C, Legras L, Devillers E (2020) Disappearance of TBEV circulation among rodents in a natural focus in Alsace, Eastern France. *Pathogens*, **9**, e930 (1-13). https://doi.org/10.3390/pathogens9110930

Bournez L, Umhang G, Moinet M, Richomme C, Demerson J, Caillot C, Devillers E, Boucher J (2020) Tick-borne encephalitis virus: seasonal and annual variation of epidemiological parameters related to nymph-to-larva transmission and exposure of small mammals. *Pathogens*, **9**, e518 (1-19).
https://doi.org/10.3390/pathogens9070518

Bown KJ, Lambin X, Telford GR, Ogden NH, Telfer S, Woldehiwet Z, Birtles RJ (2008) Relative importance of *Ixodes ricinus* and *Ixodes trianguliceps* as vectors for *Anaplasma phagocytophilum* and *Babesia microti* in field vole (*Microtus agrestis*) populations. *Applied and Environmental Microbiology*, **74**, 7118-7125. https://doi.org/10.1128/AEM.00625-08
Boyard C, Barnouin J, Bord S, Gasqui P, Vourc'h G (2011) Reproducibility of local environmental factors for the abundance of questing *Ixodes ricinus* nymphs on pastures. *Ticks and Tick-borne Diseases*, **2**, 104-110. https://doi.org/10.1016/j.ttbdis.2011.02.001

Boyard C, Barnouin J, Gasqui P, Vourc'h G (2007) Local environmental factors characterizing *Ixodes ricinus* nymph abundance in grazed permanent pastures for cattle. *Parasitology*, **134**, 987-994.
https://doi.org/10.1017/S0031182007002351

Boyard C, Vourc'h G, Barnouin J (2008) The relationships between *Ixodes ricinus* and small mammal species at the woodland-pasture interface. *Experimental and Applied Acarology*, **44**, 61-76.
https://doi.org/10.1007/s10493-008-9132-3

Boyer PH, Boulanger N, Nebbak A, Collin E, Jaulhac B, Almeras L (2017) Assessment of MALDI-TOF MS biotyping for *Borrelia burgdorferi* sl detection in *Ixodes ricinus*. *PLoS ONE*, **12**, e0185430 (16 p).
https://doi.org/10.1371/journal.pone.0185430

Boyer PH, Koetsveld J, Zilliox L, Sprong H, Talagrand-Reboul É, Hansmann Y, De Martino SJ, Boulanger N, Hovius JW, Jaulhac B (2020) Assessment of *Borrelia miyamotoi* in febrile patients and ticks in Alsace, an endemic area for Lyme borreliosis in France. *Parasites and Vectors*, **13**, 1-7.
https://doi.org/10.1186/s13071-020-04071-9

Bregnard C, Rais O, Herrmann C, Kahl O, Brugger K, Voordouw MJ (2021) Beech tree masting explains the inter-annual variation in the fall and spring peaks of *Ixodes ricinus* ticks with different time lags. *Parsites and Vectors*, **14**, 1-26. https://doi.org/10.1186/s13071-021-05076-8

Bregnard C, Rais O, Voordouw MJ (2020) Climate and tree seed production predict the abundance of the European Lyme disease vector over a 15-year period. *Parasites & Vectors*, **13**, (12 p).
https://doi.org/10.1186/s13071-020-04291-z

Brugger K, Walter M, Chitimia-Dobler L, Dobler G, Rubel F (2018) Forecasting next season's *Ixodes ricinus* nymphal density: the example of southern Germany 2018. *Experimental & Applied Acarology*, **75**, 281-288. https://doi.org/10.1007/s10493-018-0267-6

Butler CM, Sloet Van Oldruitenborgh-Oosterbaan MM, E Stout TA, Jongejan F, Werners AH, Houwers DJ (2016) Classification of ticks collected from horses in the Netherlands in 2008-2009 and identification of the (zoonotic) agents they contain. *Pferdeheilkunde*, **32**, 329-334.
https://doi.org/10.21836/PEM20160405

Cat J, Beugnet F, Hoch T, Jongejan F, Prangé A, Chalvet-Monfray K (2017) Influence of the spatial heterogeneity in tick abundance in the modeling of the seasonal activity of *Ixodes ricinus* nymphs in Western Europe. *Experimental and Applied Acarology*, **71**, 115-130. https://doi.org/10.1007/s10493-016-0099-1

Charrel RN, Attoui H, Butenko AM, Clegg JC, Deubel V, Frolova TV, Gould EA, Gritsun TS, Heinz FX, Labuda M, Lashkevich V a., Loktev V, Lundkvist A, Lvov DV, Mandl CW, Niedrig M, Papa A, Petrov VS, Plyusnin A, Randolph S, Süss J, Zlobin VI, de Lamballerie X (2004) Tick-borne virus diseases of human interest in Europe. *Clinical Microbiology and Infection*, **10**, 1040-1055. https://doi.org/10.1111/j.1469-0691.2004.01022.x

Chastagner A, Pion A, Verheyden H, Lourtet B, Cargnelutti B, Picot D, Poux V, Bard É, Plantard O, McCoy KD, Leblond A, Vourc'h G, Bailly X (2017) Host specificity, pathogen exposure, and superinfections impact the distribution of *Anaplasma phagocytophilum* genotypes in ticks, roe deer, and livestock in a fragmented agricultural landscape. *Infection, Genetics and Evolution*, **55**, 31-44.
https://doi.org/10.1016/j.meegid.2017.08.010

Chastel C (1998) Erve and Eyach: two viruses isolated in France, neuropathogenic for man and widely distributed in Western Europe. *Bulletin de l'Académie Nationale de Médecine*, **182**, 801-810.

Chastel C, Main AJ, Couatarmanac'h A, Le Lay G, Knudson DL, Quillien MC, Beaucournu JC (1984) Isolation of Eyach virus (Reoviridae, Colorado tick fever group) from *Ixodes ricinus* and *I. ventalloi* ticks in France. *Archives of Virology*, **82**, 161-171. https://doi.org/10.1007/BF01311160

Chatelain J, Ardoin P (1978) Some demographic data from *Ixodes ricinus* Linné: vector of a virus strain of central european encephalitis in Alsace. *Revue d'Épidémiologie et de Sante Publique*, **26**, 211-223.

Chauvin A, Moreau E, Bonnet S, Plantard O, Malandrin L (2009) *Babesia* and its hosts: Adaptation to long-lasting interactions as a way to achieve efficient transmission. *Veterinary Research*, **40**.
https://doi.org/10.1051/vetres/2009020
Chomel BB, Boulouis HJ, Breitschwerdt EB (2004) Cat scratch disease and other zoonotic Bartonella infections. Veterinary Medicine Today, **224**, 1270-1279.
https://doi.org/10.2460/javma.2004.224.1270

Chomel BB, Kasten RW, Floyd-Hawkins K, Chi B, Yamamoto K, Roberts-Wilson J, Gurfield AN, Abbott RC, Pedersen NC, Koehler JE (1996) Experimental transmission of Bartonella henselae by the cat flea. *Journal of Clinical Microbiology*, **34**, 1952-1956. https://doi.org/10.1128/jcm.34.8.1952-1956.1996

Cicculli V, Capai L, Quilichini Y, Masse S, Fernandez-Alvarez A, Minodier L, Bompard P, Charrel R, Falchi A (2019) Molecular investigation of tick-borne pathogens in ixodid ticks infesting domestic animals (cattle and sheep) and small rodents (black rats) of Corsica, France. *Ticks and Tick-borne Diseases*, **10**, 606-613. https://doi.org/10.1016/j.ttbdis.2019.02.007

Coiffait C (2019) Rhythm of the activity of the tick *Ixodes ricinus*: a synchronisation with roe deer's activity? PhD Thesis Thesis. Université Toulouse 3 Paul Sabatier.

Cosson JF, Michelet L, Chotte J, Le Naour E, Cote M, Devillers E, Poulle ML, Huet D, Galan M, Geller J, Moutailler S, Vayssier-Taussat M (2014) Genetic characterization of the human relapsing fever spirochete *Borrelia miyamotoi* in vectors and animal reservoirs of Lyme disease spirochetes in France. *Parasites and Vectors*, **7**, 233 (5 p). https://doi.org/10.1186/1756-3305-7-233

Cotté V, Bonnet S, Cote M, Vayssier-Taussat M (2010) Prevalence of five pathogenic agents in questing *Ixodes ricinus* ticks from western France. *Vector-Borne and Zoonotic Diseases*, **10**, 723-730.
https://doi.org/10.1089/vbz.2009.0066

Cotté V, Bonnet S, Le Rhun D, Le Naour E, Chauvin A, Boulouis HJ, Lecuelle B, Lilin T, Vayssier-Taussat M (2008) Transmission of *Bartonella henselae* by *Ixodes ricinus*. *Emerging Infectious Diseases*, **14**, 1074-1080. https://doi.org/10.3201/eid1407.071110

Danielová V, Holubová J, Pej M, Daniel M (2002) Potential significance of transovarial transmission in the circulation of tick-borne encephalitis virus. *Folia parasitologica*, **49**, 323-325.
https://doi.org/10.14411/fp.2002.060

Danielová V, Rudenko N, Daniel M, Holubová J, Materna J, Golovchenko M, Schwarzová L (2006) Extension of *Ixodes ricinus* ticks and agents of tick-borne diseases to mountain areas in the Czech Republic. *International Journal of Medical Microbiology*, **296**, 48-53.
https://doi.org/10.1016/j.ijmm.2006.02.007

Davoust B, Socolovschi C, Revelli P, Gibert P, Marié JL, Raoult D, Parola P (2012) Detection of *Rickettsia helvetica* in *Ixodes ricinus* ticks collected from Pyrenean chamois in France. *Ticks and Tick-borne Diseases*, **3**, 387-388. https://doi.org/10.1016/j.ttbdis.2012.10.009

Degeilh B (2007) Scientific basis for prevention. *Medecine et Maladies Infectieuses*, **37**, 360-367.
https://doi.org/10.1016/j.medmal.2006.01.031

Degeilh P, Guiguen C, Gilot B, Doche B, Pichot J, Beaucournu J-C (1994) Distribution of *Ixodes ricinus* (Linne, 1758) (Acarina: Ixodidae) in the forest regions of the Massif Armoricain. *Acarologia*, **35**, 327-334.

Degeilh B, Pichot J, Gilot B, Allen S, Doche B, Guiguen C (1996) Dynamics of human primary-infestation with Lyme borreliosis (Erythema Chronicum Migrans) and dynamics of vector tick populations (*Ixodes ricinus* Linnaeus, 1758): attempt at correlation. *Acarologia*, **37**, 7-17.

Dietrich F, Schmidgen T, Maggi RG, Richter D, Matuschka FR, Vonthein R, Breitschwerdt EB, Kempf VAJ (2010) Prevalence of *Bartonella henselae* and *Borrelia burgdorferi* sensu lato DNA in *Ixodes ricinus* ticks in Europe. *Applied and Environmental Microbiology*, **76**, 1395-1398.
https://doi.org/10.1128/AEM.02788-09

Dobson ADM, Taylor JL, Randolph SE (2011) Tick (*Ixodes ricinus*) abundance and seasonality at recreational sites in the UK: hazards in relation to fine-scale habitat types revealed by complementary sampling methods. *Ticks and Tick-borne Diseases*, **2**, 67-74.
https://doi.org/10.1016/j.ttbdis.2011.03.002

Doby J-M, Bigaignon G, Aubert M, Imbert G (1991) Ectoparasites of the fox and Lyme borreliosis. Research on *Borrelia burgdorferi* in ixodid ticks and fleas (Siphonaptera). *Bulletin de la Societe Francaise de Parasitologie*, **9**, 279-288.

Doby JM, Bigaignon G, Degeilh B (1992) Compared potential importance of field-mouse (*Apodemus sylvaticus*) and bank vole (*Clethrionomys glareolus*) in Lyme borreliosis epidemiology in forest in the
western part of France, through relations between rodents and *Ixodes ricinus* tick. *Bulletin de la Société Française de Parasitologie*, **10**, 271-293.

Doby JM, Bigaignon G, Degeilh B, Guiguen C (1994) Ectoparasites of large wild mammals (deer and wild boars) and Lyme borreliosis. Search for *Borrelia burgdorferi* in more than 1400 ticks, lice, Pupipara Diptera and fleas. *Revue de Médecine Vétérinaire*, **145**, 743-748.

Doby JM, Bigaignon G, Godfroid E, Bollen A, Murga-Gutierrez N (1993) Frequency of *Borrelia burgdorferi*, agent of Lyme Borreliosis, in nymphs of *Ixodes ricinus* (Acari: Ixodidae) caught in some forests in the central part of France. *Bulletin de la Societe Francaise de Parasitologie*, **11**, 163-168.

Doby JM, Bigaignon G, Launay H, Costil C, Lorvellec O (1990) Presence of *Borrelia burgdorferi*, agent of tick spirochaetosis, in *Ixodes (Exopalpiger) trianguliceps* Birula, 1895 and *Ixodes (Ixodes) acuminatus* Neumann, 1901 (Acari: Ixodidae) and in *Ctenophthalmus baeticus arvernus* Jordan, 1931 and *Megabothris turbidus* (Rothschild, 1909) (Insecta: Siphonaptera), ectoparasites of small mammals in forests in western France. *Bulletin de la Société Française de Parasitologie*, **8**, 311-322.

Doby JM, Degeilh B (1996) Lyme borreliosis and urban and periurban public parks. *Bulletin de la Société des sciences naturelles de l'Ouest de la France* (1983), **18**, 34-40.

Doche B, Gilot B, Degeilh B, Pichot J, Guiguen C (1993) Utilisation de l'indicateur végétal pour la cartographie d'une tique exophile à l'échelle de la France : exemple d'Ixodes ricinus (Linné, 1758), vecteur de la Borréliose de Lyme. *Annales de Parasitologie Humaine et Comparée*, **68**, 188-195.
https://doi.org/10.1051/parasite/1993684188

Dugat T, Lagrée A, Maillard R, Boulouis H-J, Haddad N (2015) Opening the black box of *Anaplasma phagocytophilum* diversity: current situation and future perspectives. *Frontiers in Cellular and Infection Microbiology*, **5**, 1-18. https://doi.org/10.3389/fcimb.2015.00061

van Duijvendijk G, Coipan C, Wagemakers A, Fonville M, Ersöz J, Oei A, Földvári G, Hovius J, Takken W, Sprong H (2016) Larvae of *Ixodes ricinus* transmit *Borrelia afzelii* and *B. miyamotoi* to vertebrate hosts. *Parasites and Vectors*, **9**, 1-7. https://doi.org/10.1186/s13071-016-1389-5

Duron O, Binetruy F, Noël V, Cremaschi J, McCoy KD, Arnathau C, Plantard O, Goolsby J, Pérez de León AA, Heylen DJA, Van Oosten AR, Gottlieb Y, Baneth G, Guglielmone AA, Estrada-Peña A, Opara MN, Zenner L, Vavre F, Chevillon C (2017) Evolutionary changes in symbiont community structure in ticks. *Molecular Ecology*, **26**, 2905-2921. https://doi.org/10.1111/mec.14094

Duron O, Sidi-Boumedine K, Rousset E, Moutailler S, Jourdain E (2015) The importance of ticks in Q Fever transmission: What has (and has not) been demonstrated? *Trends in Parasitology*, **31**, 536-552.
https://doi.org/10.1016/j.pt.2015.06.014

Edwards CD, Campbell H (2022) Sampling implications of variation in daily activity of the sheep tick, *Ixodes ricinus* at a coastal grassland site in the U.K. *Medical and Veterinary Entomology*, **36**, 127-132.
https://doi.org/10.1111/mve.12543

Egyed L, Élő P, Sréter-Lancz Z, Széll Z, Balogh Z, Sréter T (2012) Seasonal activity and tick-borne pathogen infection rates of *Ixodes ricinus* ticks in Hungary. *ticks and Tick-Borne Diseases*, **3**, 90-94.
https://doi.org/10.1016/j.ttbdis.2012.01.002

Ehrmann S, Liira J, Gärtner S, Hansen K, Brunet J, Cousins SAOO, Deconchat M, Decocq G, de Frenne P, de Smedt P, Diekmann M, Gallet-Moron E, Kolb A, Lenoir J, Lindgren J, Naaf T, Paal T, Valdés A, Verheyen K, Wulf M, Scherer-Lorenzen M (2017) Environmental drivers of *Ixodes ricinus* abundance in forest fragments of rural European landscapes. *BMC Ecology*, **17**, 1-14. https://doi.org/10.1186/s12898-017-0141-0

Ehrmann S, Ruyts SC, Scherer-Lorenzen M, Bauhus J, Brunet J, Cousins SAO, Deconchat M, Decocq G, De Frenne P, De Smedt P, Diekmann M, Gallet-Moron E, Gartner S, Hansen K, Kolb A, Lenoir J, Lindgren J, Naaf T, Paal T, Panning M, Prinz M, Valdes A, Verheyen K, Wulf M, Liira J (2018) Habitat properties are key drivers of *Borrelia burgdorferi* (s.l.) prevalence in *Ixodes ricinus* populations of deciduous forest fragments. *Parasites and Vectors*, **11**, 23. https://doi.org/10.1186/s13071-017-2590-x

Eisen L (2020) Vector competence studies with hard ticks and *Borrelia burgdorferi* sensu lato spirochetes: A review. *Ticks and Tick-borne Diseases*, **11**, 101359. https://doi.org/10.1016/j.ttbdis.2019.101359

Eisen L, Eisen RJ (2021) Benefits and drawbacks of citizen science to complement traditional data gathering approaches for medically important hard ticks (Acari: Ixodidae) in the United States. *Journal of Medical Entomology*, **58**, 1-9. https://doi.org/10.1093/jme/tjaa165
Eldin C, Mélenotte C, Mediannikov O, Ghigo E, Million M, Edouard S, Mege J, Maurin M (2017) From Q fever to *Coxiella burnetii* infection: A paradigm change. *Clinical Microbiology Reviews*, **30**, 115–190.
https://doi.org/10.1128/cmr.00045-16

Fang DC, Mccullough J (2016) Transfusion-transmitted *Babesia microti*. *Transfusion Medicine Reviews*, **30**, 132–138.
https://doi.org/10.1016/j.tmrv.2016.04.002

Ferquel E, Garnier M, Marie J, Bernède-Bauduin C, Baranton G, Pérez-Eid C, Postic D (2006) Prevalence of *Borrelia burgdorferi* sensu lato and Anaplasmataceae members in *Ixodes ricinus* ticks in Alsace, a focus of Lyme borreliosis endemicity in France. *Applied and Environmental Microbiology*, **72**, 3074–3078.
https://doi.org/10.1128/AEM.72.4.3074-3078.2006

Figoni J, Chirouze C, Hansmann Y, Lemogne C, Hentgen V, Saunier A, Bouiller K, Gehanno JF, Rabaud C, Perrot S, Caumes E, Eldin C, de Broucker T, Jaulhac B, Roblot F, Toubiana J, Sellal F, Vuillemet F, Sordet C, Fantin B, Lina G, Gocko X, Dieudonné M, Picone O, Bodaghi B, Gangneux JP, Degeilh B, Partouche H, Lenormand C, Sotto A, Raffetin A, Monsuez JJ, Michel C, Boulanger N, Cathebras P, Tattevin P, societies E by scientific (2019) Lyme borreliosis and other tick-borne diseases. Guidelines from the French Scientific Societies (I): prevention, epidemiology, diagnosis. *Medecine et Maladies Infectieuses*, **49**, 318–334.
https://doi.org/10.1016/j.medmal.2019.04.381

Gaci R, Alauzet C, Selton-suty C, Lozniewski A, Pulcini C, May T, Goehringer F (2017) *Francisella tularensis* endocarditis: two case reports and a literature review. *Infectious Diseases*, **49**, 128-131.
https://doi.org/10.1080/23744235.2016.1222546

García-Sanmartín J, Barandika JF, Juste RA, García-Pérez AL, Hurtado A (2008) Distribution and molecular detection of *Theileria* and *Babesia* in questing ticks from northern Spain. *Medical and Veterinary Entomology*, **22**, 318–325.
https://doi.org/10.1111/j.1365-2915.2008.00748.x

Garcia-Vozmediano A, Krawczyk AI, Sprong H, Rossi L, Ramassa E, Tomassone L (2020) Ticks climb the mountains: ixodid tick infestation and infection by tick-borne pathogens in the Western Alps. *Ticks and Tick-borne Diseases*, **11**, 101489.
https://doi.org/10.1016/j.ttbdis.2020.101489

Genchi M, Prati P, Vicari N, Manfredini A, Sacchi L, Clementi E, Bandi C, Epis S, Fabbi M (2015) *Francisella tularensis*: No evidence for transovarial transmission in the tularemia tick vectors *Dermacentor reticulatus* and *Ixodes ricinus*. *PLoS ONE*, **10**, e0133593 (13 p).
https://doi.org/10.1371/journal.pone.0133593

George JC, Chastel C (2002) Maladies vectorielles à tiques et modifications de l'écosystème en Lorraine. *Bulletin de la Société de Pathologie Exotique*, **95**, 95–99.

Gern L, Morán Cadenas F, Burri C (2008) Influence of some climatic factors on *Ixodes ricinus* ticks studied along altitudinal gradients in two geographic regions in Switzerland. *International Journal of Medical Microbiology*, **298**, 55–59.
https://doi.org/10.1016/j.ijmm.2008.01.005

Gern L, Toutoungi LN, Hu CM, Aeschlimann A (1991) *Ixodes (Pholeoixodes) hexagonus*, an efficient vector of *Borrelia burgdorferi* in the laboratory. *Medical and Veterinary Entomology*, **5**, 431–435.
https://doi.org/10.1111/j.1365-2915.1991.tb00571.x

Geurden T, Becskei C, Six RH, Maeder S, Latrofa MS, Otranto D, Farkas R (2018) Detection of tick-borne pathogens in ticks from dogs and cats in different European countries. *Ticks and Tick-borne Diseases*, **9**, 1431–1436.
https://doi.org/10.1016/j.ttbdis.2018.06.013

Gilbert L (2010) Altitudinal patterns of tick and host abundance: a potential role for climate change in regulating tick-borne diseases? *Oecologia*, **162**, 217–225.
https://doi.org/10.1007/s00442-009-1430-x

Gilbert L, Aungier J, Tomkins JL (2014) Climate of origin affects tick (*Ixodes ricinus*) host-seeking behavior in response to temperature: Implications for resilience to climate change? *Ecology and Evolution*, **4**, 1186–1198.
https://doi.org/10.1002/ece3.1014

Gilot B, Bonnefille M, Degeilh B, Beaucournu J-CC, Pichot J, Guiguen C (1994) The development of *Ixodes ricinus* (Linné, 1758) in French forests: The roe-deer, *Capreolus capreolus* (L., 1758) used as a biological marker. *Parasite*, **1**, 81–85.
https://doi.org/10.1051/parasite/1994011081

Gilot B, Doche B, B, Degeilh B, Guigen C, Pichot J (1995) Bases acarologiques pour l'étude épidémiologique de la borreliose de Lyme: les populations d' *Ixodes ricinus* Linné, 1758 du sud-ouest français. *Acarologia*, **36**, 117–132.

Gilot B, Guiguen C, Degeilh B, Doche B, Pichot J, Beaucournu JC (1994) Phytoecological mapping of *Ixodes ricinus* as an approach to the distribution of Lyme borreliosis in France. In: *Lyme Borreliosis*, pp. 105–112. New York: Plenum, 1984.
https://doi.org/10.1007/978-1-4615-2415-1_17
Gilot B, Marjolet M (1982) Contribution to the study of human parasitism by ticks (Ixodidae and Argasidae), particularly in south-eastern France. *Medecine et Maladies Infectieuses, **12*, 340-351.
https://doi.org/10.1016/S0399-077X(82)80014-0

Gilot B, Pautou G (1982) The evolution of populations of ticks (Ixodidae and Argasidae) in relation to the artificial alteration of the environment in the French Alps. Epidemiologic effects. *Acta Tropica, **39*, 337-354.

Gilot B, Pautou G, Moncada E (1975) Analysis of vegetation applied to the detection of populations of free-living ticks in south-eastern France: *Ixodes ricinus* (Linne 1758) (Acarina, Ixodoidea) as an example. *Acta Tropica, **32*, 340-347.

Gilot B, Pautou G, Moncada E, Ain G (1975) Ecological study of *Ixodes ricinus* (Linné, 1758) (Acarina, Ixodoides) in southeastern France. *Acta tropica, **32*, 232-258.

Gilot B, Perez-Eid C (1998) Bioecology of ticks causing the most important pathology in France. *Médecine et Maladies Infectieuses, **28*, 325-334. https://doi.org/10.1016/s0399-077x(98)70217-3

Gilot B, Pichot J, Doche B (1989) The ticks of the Massif Central (France). 1. - The Ixodides (Acari, Ixodoidea) infesting domestic carnivores and ungulates in the eastern border of the Massif. *Acarologia, **30*, 191-207.

Gilot B, Rogers P, Lachet B (1985) Biological and ecological data on the ticks of lagomorphs (and especially those of the wild rabbit, *Oryctolagus cuniculus* L.) in the French Alps and their surrounding countryside. *Acarologia, **26*, 335-354.

Goldstein V, Boulanger N, Schwartz D, George J-C, Ertlen D, Zilliox L, Schaeffer M, Jaulhac B (2018) Factors responsible for *Ixodes ricinus* nymph abundance: Are soil features indicators of tick abundance in a French region where Lyme borreliosis is endemic? *Ticks and Tick-borne Diseases, **9*, 938-944.
https://doi.org/10.1016/j.ttbdis.2018.03.013

Gonzalez G, Bournez L, Moraes RA, Marine D, Galon C, Vorimore F, Cochin M, Nougairède A, Hennechart-Collette C, Perelle S, Leparc-Goffart I, Durand GA, Grard G, Bénet T, Danjou N, Blanchin M, Lacour SA, Boué F, Chenut G, Mainguet C, Simon C, Brémont L, Zientara S, Moutailler S, Martin-Latil S, Dheilly NM, Beck C, Lecollinet S (2022) A One-Health approach to investigating an outbreak of alimentary tick-borne encephalitis in a non-endemic area in France (Ain, Eastern France): a longitudinal serological study in livestock, detection in ticks, and the first tick-borne encephalitis virus isolation and molecular characterisation. *Frontiers in Microbiology, **13*, 863725.
https://doi.org/10.3389/fmicb.2022.863725

González-Barrio D, Ruiz-fons F (2019) *Coxiella burnetii* in wild mammals: A systematic review. *Transboundary and Emerging Diseases, **66*, 662-671. https://doi.org/10.1111/tbed.13085

Grassi L, Franzo G, Martini M, Mondin A, Cassini R, Pasotto D, Vidorin E, Menandro ML, Drigo M (2021) Ecotyping of *Anaplasma phagocytophilum* from wild ungulates and ticks shows circulation of zoonotic strains in northeastern Italy. *Animals, **11*, 310. https://doi.org/10.3390/ani11020310

Gray JS, Kahl O, Lane RS, Levin ML, Tsao JI (2016) Diapause in ticks of the medically important *Ixodes ricinus* species complex. *Ticks and Tick-borne Diseases, **7*, 992-1003.
https://doi.org/10.1016/j.ttbdis.2016.05.006

Gray J, Kahl O, Zintl A (2021) What do we still need to know about *Ixodes ricinus*? *Ticks and Tick-borne Diseases, **12*, 101682. https://doi.org/10.1016/j.ttbdis.2021.101682

Gray J, Von Stedingk LV, Gürtelschmid M, Granström M (2002) Transmission studies of *Babesia microti* in *Ixodes ricinus* ticks and gerbils. *Journal of Clinical Microbiology, **40*, 1259-1263.
https://doi.org/10.1128/JCM.40.4.1259

Grech-Angelini S, Stachurski F, Lancelot R, Boissier J, Allienne J-F, Marco S, Maestrini O, Uilenberg G (2016) Ticks (Acari: Ixodidae) infesting cattle and some other domestic and wild hosts on the French Mediterranean island of Corsica. *Parasites and Vectors, **9*, 582. https://doi.org/10.1186/s13071-016-1876-8

Grech-Angelini S, Stachurski F, Vayssier-Taussat M, Devillers E, Casabianca F, Lancelot R, Uilenberg G, Moutailler S (2020) Tick-borne pathogens in ticks (Acari: Ixodidae) collected from various domestic and wild hosts in Corsica (France), a Mediterranean island environment. *Transboundary and Emerging Diseases, **67*, 745-757. https://doi.org/10.1111/tbed.13393
Grégoire A, Faivre B, Heeb P, Cezilly F (2002) A comparison of infestation patterns by *Ixodes* ticks in urban and rural populations of the Common Blackbird *Turdus merula*. *Ibis*, **144**, 640–645.
https://doi.org/10.1046/j.1474-919X.2002.00102.x

Halos L, Bord S, Cotté V, Gasqui P, Abrial D, Barnouin J, Boulouis H-J, Vayssier-Taussat M, Vourc'h G (2010) Ecological factors characterizing the prevalence of bacterial tick-borne pathogens in *Ixodes ricinus* ticks in pastures and woodlands. *Applied and Environmental Microbiology*, **76**, 4413–4420.
https://doi.org/10.1128/AEM.00610-10

Halos L, Jamal T, Maillard R, Beugnet F, Le Menach A, Boulouis H-J, Vayssier-Taussat M (2005) Evidence of *Bartonella* sp. in questing adult and nymphal *Ixodes ricinus* ticks from France and co-infection with *Borrelia burgdorferi* sensu lato and *Babesia* sp. *Veterinary Research*, **36**, 79–87.
https://doi.org/10.1051/vetres:2004052

Hansmann Y, Gut JP, Remy V, Martinot M, Witz Allard M, Christmann D (2006) Tick-borne encephalitis in eastern France. *Scandinavian Journal of Infectious Diseases*, **38**, 520–526.
https://doi.org/10.1080/00365540600585073

Hauser G, Rais O, Morán Cadenas F, Gonseth Y, Bouzelboudjen M, Gern L (2018) Influence of climatic factors on *Ixodes ricinus* nymph abundance and phenology over a long-term monthly observation in Switzerland (2000-2014). *Parasites and Vectors*, **11**, 289. https://doi.org/10.1186/s13071-018-2876-7

Henningsson AJ, Asgeirsson H, Hammas B, Karlsson E, Parke Å, Hoornstra D, Wilhelmsson P, Hovius JW (2019) Two cases of *Borrelia miyamotoi* meningitis, Sweden, 2018. *Emerging Infectious Diseases*, **25**, 2017–2020. https://doi.org/10.3201/eid2510.190416

Herrmann C, Gern L (2013) Survival of *Ixodes ricinus* (Acari: Ixodidae) nymphs under cold conditions is negatively influenced by frequent temperature variations. *Ticks and Tick-borne Diseases*, **4**, 445–451.
https://doi.org/10.1016/j.ttbidis.2013.05.002

Hestvik G, Smith LA, Fox NJ, Uhlhorn H, Artois M, Hannant D, Hutchings MR, Mattsson, R., Yon L, Gavier-Widen D (2014) The status of tularemia in Europe in a one-health context: a review. *Epidemiology & Infection*, **143**, 2137–2160. https://doi.org/10.1017/S0950268814002398

Heylen D, Fonville M, Docters-van Leeuwen A, Stroo A, Duisterwinkel M, Van Wieren S, Diuk-Wasser M, de Bruin A, Sprong H (2017) Pathogen communities of songbird-derived ticks in Europe's low countries. *Parasites and Vectors*, **10**, 497. https://doi.org/10.1186/s13071-017-2423-y

Heylen D, Krawczyk A, Lopes de Carvalho I, Núncio MS, Sprong H, Norte AC (2017) Bridging of cryptic *Borrelia* cycles in European songbirds. *Environmental Microbiology*, **19**, 1857–1867.
https://doi.org/10.1111/1462-2920.13685

Heylen D, Tijsse E, Fonville M, Matthysen E, Sprong H (2013) Transmission dynamics of *Borrelia burgdorferi* s.l. in a bird tick community. *Environmental Microbiology*, **15**, 663–673.
https://doi.org/10.1111/1462-2920.12059

Heyman P, Cochez C, Hofhuis A, van der Giessen J, Sprong H, Porter SR, Losson B, Saegerman C, Donoso-Mantke O, Niedrig M, Papa A (2010) A clear and present danger: tick-borne diseases in Europe. *Expert review of anti-infective therapy*, **8**, 33–50. https://doi.org/10.1586/eri.09.118

Hildebrandt A, Zintl A, Montero E, Hunfeld K, Gray J (2021) Human Babesiosis in Europe. *Pathogens*, **20**, e1165 (1-31). https://doi.org/10.3390/pathogens10091165

Hofmeester TR, Coipan EC, van Wieren SE, Prins HHT, Takken W, Sprong H (2016) Few vertebrate species dominate the *Borrelia burgdorferi* s.l. life cycle. *Environmental Research Letters*, **11**, 043001.
https://doi.org/10.1088/1748-9326/11/4/043001

Hofmeester TR, Jansen PA, Wijnen HJ, Coipan EC, Fonville M, Prins HHT, Sprong H, Van Wieren SE (2017) Cascading effects of predator activity on tick-borne disease risk. *Proceedings of the Royal Society B: Biological Sciences*, **284**, 20170453, 8p. https://doi.org/10.1098/rspb.2017.0453

Ioannou I, Chochlakis D, Kasinis N, Anayiotos P, Lyssandrou A, Papadopoulos B, Tselentis Y, Psaroulaki A (2009) Carriage of *Rickettsia* spp., *Coxiella burnetii* and *Anaplasma* spp. by endemic and migratory wild birds and their ectoparasites in Cyprus. *Clinical Microbiology and Infection*, **15**, 158–160.
https://doi.org/10.1111/j.1469-0691.2008.02207.x

Iori A, Gabrielli S, Calderini P, Moretti A, Pietrobelli M, Tampieri MP, Galuppi R, Cancrini G (2010) Tick reservoirs for piroplasms in central and northern Italy. *Veterinary Parasitology*, **170**, 291–296.
https://doi.org/10.1016/j.vetpar.2010.02.027
Jaarsma RI, Sprong H, Takumi K, Kazirova M, Silaghi C, Mysterud A, Rudolf I, Beck R, Földvári G, Tomassone L, Groenevelt M, Everts RR, Rijks JM, Ecke F, Hörnfeldt B, Modrý D, Majerová K, Votýpka J, Estrada-Peña A (2019) *Anaplasma phagocytophilum* evolves in geographical and biotic niches of vertebrates and ticks. *Parasites & Vectors*, **12**, 328. https://doi.org/10.1186/s13071-019-3583-8

Jacquot M, Abrial D, Gasqui P, Bord S, Marsot M, Masseglia S, Pion A, Poux V, Zilliox L, Chapuis J, Vourc G, Bailly X (2016) Multiple independent transmission cycles of a tick-borne pathogen within a local host community. *Scientific Reports*, **6**, 1–12. https://doi.org/10.1038/srep31273

Jacquot M, Gonnet M, Ferquel E, Abrial D, Claude A, Gasqui P, Choumet V, Charras-Garrido M, Garnier M, Faure B, Sertour N, Dorr N, De Goër J, Vourc'H G, Bailly X (2014) Comparative population genomics of the *Borrelia burgdorferi* species complex reveals high degree of genetic isolation among species and underscores benefits and constraints to studying intra-specific epidemiological processes. *PLoS ONE*, **9**. https://doi.org/10.1371/journal.pone.0094384

Jahfari S, Coipan EC, Fonville M, Docters van Leeuwen A, Hengeveld P, Heylen D, Heyman P, van Maanen C, Butler CM, Földvári G, Szekeres S, van Duijvendijk G, Tack W, Rijks JM, van der Giessen J, Takken W, van Wieren SE, Takumi K, Sprong H (2014) Circulation of four *Anaplasma phagocytophilum* ecotypes in Europe. *Parasites and Vectors*. **7**, 365. https://doi.org/10.1186/1756-3305-7-365

Jalovecka M, Sojka D, Ascencio M, Schnittger L (2019) *Babesia* life cycle–when phylogeny meets biology. *Trends in Parasitology*, **35**, 356–368. https://doi.org/10.1016/j.pt.2019.01.007

Jouda F, Perret J-L, Gern L (2004) *Ixodes ricinus* density, and distribution and prevalence of *Borrelia burgdorferi* sensu lato infection along an altitudinal gradient. *Journal of Medical Entomology*, **41**, 162–169. https://doi.org/10.1603/0022-2585-41.2.162

Jouglin M, Perez G, Butet A, Malandrin L, Bastian S (2017) Low prevalence of zoonotic *Babesia* in small mammals and *Ixodes ricinus* in Brittany, France. *Veterinary Parasitology*, **238**, 58–60. https://doi.org/10.1016/j.vetpar.2017.03.020

Jourdain E, Duron O, Barry S, González-Acuña D, Sidi-Boumedine K (2015) Molecular methods routinely used to detect *Coxiella burnetii* in ticks cross-react with *Coxiella*-like bacteria. *Infection Ecology & Epidemiology*, **5**, 29230. https://doi.org/10.3402/iee.v5.29230

Kahl O, Gern L, Eisen L, Lane RS (2002) Ecological research on *Borrelia burgdorferi* sensu lato: terminology and some methodological pitfalls. *Lyme borreliosis: biology, epidemiology and control*, 29–46. https://doi.org/10.1079/9780851996325.0029

Kaiser R (2008) Tick-borne encephalitis. *Infectious Disease Clinics of North America*, **22**, 561–575. https://doi.org/10.1016/j.idc.2008.03.013

Kawahara M, Rikihisa Y, Isogai E, Takahashi M, Misumi H, Suto C, Shibata S, Zhang C, Masayoshi T (2004) Ultrastructure and phylogenetic analysis of ‘Candidatus Neoehrlichia mikurensis’ in the family Anaplasmataceae, isolated from wild rats and found in *Ixodes ovatus* ticks. *International Journal of Systematic and Evolutionary Microbiology*, **54**, 1837–1843. https://doi.org/10.1099/ijs.0.63260-0

Keesing F, Hersh MH, Tibbetts M, Mchenry DJ, Duerr S, Brunner J, Killilea M, Logiudice K, Schmidt KA, Ostfeld RS (2012) Reservoir competence of vertebrate hosts for *Anaplasma phagocytophilum*. *Emerging Infectious Diseases*, **18**, 10–13. https://doi.org/10.3201/eid1812.120919

Kilpatrick AM, Randolph SE (2012) Drivers, dynamics, and control of emerging vector-borne zoonotic diseases. *The Lancet*, **380**, 1946–1955. https://doi.org/10.1016/S0140-6736(12)61151-9

Knap N, Korva M, Dolinsek V, Sekirnik M, Trilar T, Avsic-Zupanc T (2012) Patterns of tick-borne encephalitis virus infection in rodents in Slovenia. *Vector-borne and Zoonotic Diseases*, **12**, 236–242. https://doi.org/10.1089/vbz.2011.0728

Koebel C, Kern A, Edouard S, Hoang AT, Celestin N, Hansmann Y, Jaulhac B, Brouqui P, de Martino SJ, De Martino SJ (2012) Human granulocytic anaplasmosis in eastern France: Clinical presentation and laboratory diagnosis. *Diagnostic Microbiology and Infectious Disease*, **72**, 214–218. https://doi.org/10.1016/j.diagmicrobio.2011.12.005

Körner S, Makert GR, Scholz KM, Henning K, Pfeffer M, Starke A, Nijhof AM, Ulbert S (2020) Uptake and fecal excretion of *Coxiella burnetii* by *Ixodes ricinus* and *Dermacentor marginatus* ticks. *Parasites & Vectors*, **13**, 75 (11 p). https://doi.org/10.1186/s13071-020-3956-z

Korotkov Yu, Kozlova T, Kozlovskaya L (2015) Observations on changes in abundance of questing *Ixodes ricinus*, castor bean tick, over a 35-year period in the eastern part of its range (Russia, Tula region). *Medical and Veterinary Entomology*, **29**, 129–136. https://doi.org/10.1111/mve.12101
Kraemer D (2018) Variation intra-journalière de l'activité des tiques *Ixodes ricinus* en fonction des données météorologiques. PhD Thesis Thesis. VetAgro Sup.

Kreitmann L, Terriou L, Launay D, Caspar Y, Courcol R, Maurin M, Lemaître N (2015) Disseminated infection caused by *Francisella philomiragia*, France, 2014. *Emerging Infectious Diseases*, **21**, 2014–2015. https://doi.org/10.3201%2Feid2112.150615

Kurtenbach K, Hanincová K, Tsao JI, Margos G, Fish D, Ogden NH (2006) Fundamental processes in the evolutionary ecology of Lyme borreliosis. *Nature reviews Microbiology*, **4**, 660–669.
https://doi.org/10.1038/nrmicro1475

Labuda M, Austyn JM, Zuffova E, Kozuch O, Fuchsberger N, Lysy J, Nuttall PA (1996) Importance of localized skin infection in tick-borne encephalitis virus transmission. *Virology*, **219**, 357–366.
https://doi.org/10.1006/viro.1996.0261

Labuda M, Danielova V, Jones LD, Nuttall PA (1993) Amplification of tick-borne encephalitis virus infection during co-feeding of ticks. *Medical and Veterinary Entomology*, **7**, 339–342.
https://doi.org/10.1111/j.1365-2915.1993.tb00702.x

Labuda M, Kozuch O, Zuffova E, Eleckova E, Hails RS, Nuttall PA (1997) Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts. *Virology*, **235**, 138–143.
https://doi.org/10.1006/viro.1997.8622

Labuda M, Nuttall PA, Kozuch O, Eleckova E, Williams T, Zuffova E, Sabo A, Kožuch O, Elečková E, Williams T, Žuffová E, Sabo A, Kozuch O, Elecková E, Zuffová E, Sabó A (1993) Non-viraemic transmission of tick-borne encephalitis virus: a mechanism for arbovirus survival in nature. *Experientia*, **49**, 802–805.
https://doi.org/10.1007/BF01923553

Lamontellerie M (1965) Les tiques du Sud-Ouest de la France. *Annales de Parasitologie*, **40**, 87–100.
https://doi.org/10.1051/parasite/1965401087

Larson MA, Sayood K, Bartling AM, Meyer JR, Starr C, Baldwin J, Dempsey MP (2020) Differentiation of *Francisella tularensis* subspecies and subtypes. *Journal of Clinical Microbiology*, **58**, e01495-19.
https://doi.org/10.1128/jcm.01495-19

Le Coeur C, Robert A, Pisanu B, Chapuis J-L (2015) Seasonal variation in infestations by ixodids on Siberian chipmunks: effects of host age, sex, and birth season. *Parasitology Research*, **114**, 2069–2078.
https://doi.org/10.1007/s00436-015-4391-5

Lebert I, Agoulon A, Bastian S, Butet A, Cargnelutti B, Cèbe N, Chastagner A, Léger E, Lourtet B, Masseglia S, McCoy KD, Merlet J, Noël V, Perez G, Picot D, Pion A, Poux V, Rames J-L, Rantier Y, Verheyden H, Vourc'h G, Plantard O (2020) Distribution of ticks and tick-borne pathogenic agents and associated local environmental conditions, small mammal hosts and livestock in two French agricultural sites: the OSCAR database. *Biodiversity Data Journal*, **8**, e50123 (1-34). https://doi.org/10.3897/BDJ.8.e50123

Léger E, Vourc'h G, Vial L, Chevillon C, McCoy KD (2013) Changing distributions of ticks: causes and consequences. *Experimental and Applied Acarology*, **15**, 219–244. https://doi.org/10.1007/s10493-012-9615-0

Lejal E, Chiquet J, Aubert J, Robin S, Rue O, Midoux C, Mariadassou M, Bailly X, Cougoul A, Gasqui P, Cosson JF, Pollet T (2021) Temporal patterns in *Ixodes ricinus* microbial communities: an insight into tick-borne microbe interactions. *Microbiome*, **9**, 1–21. https://doi.org/10.1186/s40168-021-01051-8

Lejal E, Marsot M, Chalvet-Monfray K, Cosson J-F, Moutailler S, Vayssier-Taussat M, Pollet T (2019) A three-years assessment of Ixodes ricinus-borne pathogens in a French peri-urban forest. *Parasites and Vectors*, **12**, 551 (14 p). https://doi.org/10.1186/s13071-019-3799-7

Lejal E, Moutailler S, Šimo L, Vayssier-Taussat M, Pollet T (2019) Tick-borne pathogen detection in midgut and salivary glands of adult *Ixodes ricinus*. *Parasites and Vectors*, **12**, 152 (8 p).
https://doi.org/10.1186/s13071-019-3418-7

L'Hostis M, Bureaud A, Gorenflot A (1996) Female *Ixodes ricinus* (Acari, Ixodidae) in cattle of western France: infestation level and seasonality. *Veterinary Research*, **27**, 589–597.

L'Hostis M, Dumon H, Dorchies B, Boisdron F, Gorenflot A (1995) Seasonal incidence and ecology of the tick *Ixodes ricinus* (Acari: Ixodidae) on grazing pastures in Western France. *Experimental and Applied Acarology*, **19**, 211–220. https://doi.org/10.1007/bf00130824

L'Hostis M, Dumon H, Fusade A, Lazareff S, Gorenflot A (1996) Seasonal incidence of *Ixodes ricinus* ticks (Acari: Ixodidae) on rodents in western France. *Experimental and Applied Acarology*, **20**, 359–368.
https://doi.org/10.1007/BF00130548
L'Hostis M, Seegers H (2002) Tick-borne parasitic diseases in cattle: Current knowledge and prospective risk analysis related to the ongoing evolution in French cattle farming systems. *Veterinary Research*, **33**, 599-611. https://doi.org/10.1051/vetres:2002041

Lindgren E, Tälleklint L, Polfeldt T (2000) Impact of climatic change on the northern latitude limit and population density of the disease-transmitting European tick *Ixodes ricinus*. *Environmental health perspectives*, **108**, 119-23. https://doi.org/10.1289/ehp.00108119

Livoreil B, Glanville J, Haddaway NR, Bayliss H, Bethel A, Lachapelle FFD, Robalino S, Savilaakso S, Zhou W, Petrokofsky G (2017) Systematic searching for environmental evidence using multiple tools and sources. *Environmental Evidence*, **6**, 1-14. https://doi.org/10.1186/s13750-017-0099-6

von Loewenich FD, Geißdo W, Disque C, Matten J, Schett G, Sakka SG, Bogdan C (2010) Detection of "Candidatus Neoehrlichia mikurensis" in two patients with severe febrile illnesses: Evidence for a European sequence variant. *Journal of Clinical Microbiology*, **48**, 2630-2635. https://doi.org/10.1128/JCM.00588-10

Mailman TL, Schmidt M. (2005) *Francisella philomiragia* adenitis and pulmonary nodules in a child with chronic granulomatous disease. *Canadian Journal of Infectious Diseases and Medical Microbiolology*, **16**, 245-248. https://doi.org/10.1155/2005/486417

Málková D, Holubova J, Kolman J, Marhoul Z, Hanzal F, Kulková H, Markvart K, Simková L (1980) Antibodies against some arboviruses in persons with various neuropathies. *Acta virologica*, **24**, 298.

Mans BJ, Pienaar R, Latif AA (2015) A review of *Theileria* diagnostics and epidemiology. *International Journal for Parasitology: Parasites and Wildlife*, **4**, 104-118. https://doi.org/10.1016/j.ijppaw.2014.12.006

Mansfield KL, Johnson N, Phipps LP, Stephenson JR, Fooks AR, Solomon T (2009) Tick-borne encephalitis virus – a review of an emerging zoonosis. *Journal of general virology*, **90**, 1781-1794. https://doi.org/10.1099/vir.0.011437-0

Marchant A, Le Coupanec A, Joly C, Perthame E, Sertour N, Garnier M, Godard V, Ferquel E, Choumet V (2017) Infection of *Ixodes ricinus* by *Borrelia burgdorferi* sensu lato in peri-urban forests of France. *PLoS ONE*, **12**, e0183543. https://doi.org/10.1371/journal.pone.0183543

Margos G, Vollmer SA, Ogden NH, Fish D (2011) Population genetics, taxonomy, phylogeny and evolution of *Borrelia burgdorferi* sensu lato. *Infection, Genetics and Evolution*, **11**, 1545-1563. https://doi.org/10.1016/j.meegid.2011.07.022

Margos G, Wilske B, Sing A, Hizo-Teufel C, Cao WC, Chu C, Scholz H, Straubinger RK, Fingerle V (2013) *Borrelia bavariensis* sp. nov. is widely distributed in Europe and Asia. *International Journal of Systematic and Evolutionary Microbiology*, **63**, 4284-4288. https://doi.org/10.1099/ijs.0.052001-0

Marsot M, Chapuis JL, Gasqui P, Dozières A, Masséglia S, Pisanu B, Ferquel E, Vourc'h G (2013) Introduced Siberian chipmunks (*Tamias sibiricus barberi*) contribute more to Lyme borreliosis risk than native reservoir rodents. *PLoS ONE*, **8**, e1-8. https://doi.org/10.1371/journal.pone.0055377

Marsot M, Henry P-Y, Vourc'h G, Gasqui P, Ferquel E, Laignel J, Grysan M, Chapuis J-L (2012) Which forest bird species are the main hosts of the tick, *Ixodes ricinus*, the vector of *Borrelia burgdorferi* sensu lato, during the breeding season? *International Journal for Parasitology*, **42**, 781-788. https://doi.org/10.1016/j.ijpara.2012.05.010

Marsot M, Sigaud M, Chapuis JL, Ferquel E, Cornet M, Vourc'h G (2011) Introduced Siberian chipmunks (*Tamias sibiricus barberi*) harbor more-diverse *Borrelia burgdorferi* sensu lato genospecies than native bank voles (*Myodes glareolus*). *Applied and Environmental Microbiology*, **77**, 5716-5721. https://doi.org/10.1128/AEM.01846-10

Martello E, Mannelli A, Ragagli C, Ambrogi C, Selmi M, Ceballos LA, Tomassone L (2014) Range expansion of *Ixodes ricinus* to higher altitude, and co-infestation of small rodents with *Dermacentor marginatus* in the Northern Apennines, Italy. *Ticks and Tick-borne Diseases*, **5**, 970-974. https://doi.org/10.1016/j.ttbidis.2014.07.021

Martinod S, Brossard M, Moreau Y (1985) Immunity of dogs against *Babesia canis*, its vector tick *Dermacentor reticulatus*, and *Ixodes ricinus* in endemic area. *The Journal of parasitology*, **71**, 269-273. https://doi.org/10.2307/3282004

Marumoto K, Joncour G, Lamanda P, Inokuma H, Brouqui Ph (2007) Detection of *Anaplasma phagocytophilum* and *Ehrlichia* sp. HF strains in *Ixodes ricinus* ticks in Brittany, France. *Clinical Microbiology and Infection*, **13**, 338-341. https://doi.org/10.1111/j.1469-0691.2006.01630.x
Mathews-Martin L, Namèche M, Vourc G, Gasser S, Lebert I, Poux V, Barry S, Bord S, Jachacz J, Chalvet-Monfray K, Bourdoiseau G, Pamies S, Sepúlveda D, Chambon-Rouvier S, René-Martellet M (2020) Questing tick abundance in urban and peri-urban parks in the French city of Lyon. *Parasites & Vectors*, **13**, 576. https://doi.org/10.1186/s13071-020-04451-1

Matuschka FR, Richter D, Fischer P, Spielman A (1990) Time of repletion of subadult *Ixodes ricinus* ticks feeding on diverse hosts. *Parasitology Research*, **76**, 540–544. https://doi.org/10.1007/BF00931062

McCoy KD, Boulanger N, others (2016) *Tiques et maladies à tiques: biologie, écologie évolutive, épidémiologie*. IRD Éditions, Marseille.

Medlock JM, Hansford KM, Bormane A, Derdakova M, Estrada-Peña A, George JC, Golovljova I, Jaenson TGT, Jensen JK, Jensen PM, Kazimirova M, Oteo JA, Papa A, Pfister K, Plantard O, Randolph SE, Rizzoli A, Santos-Silva MM, Sprong H, Vial L, Hendrickx G, Zeller H, Van Bortel W (2013) Driving forces for changes in geographical distribution of *Ixodes ricinus* ticks in Europe. *Parasites and Vectors*, **6**. https://doi.org/10.1186/1756-3305-6-1

Mejlon HA (1997) Diel activity of *Ixodes ricinus* Acari:ixodidae at two locations near Stockholm, Sweden. *Experimental & applied acarology*, **21**, 247–255. https://doi.org/10.1023/a:1018446921644

Mejlon HA, Jaenson TGT (1997) Questing behaviour of *Ixodes ricinus* ticks (Acari: Ixodidae). *Experimental and Applied Acarology*, **21**, 747–754. https://doi.org/10.1023/A:1018421105231

Mémeteau S, Seegers H, Jolivet F, L'Hostis M (1998) Assessment of the risk of infestation of pastures by *Ixodes ricinus* due to their phyto-ecological characteristics. *Veterinary Research*, **29**, 487–496. https://doi.org/10.1016/S0928-4249(98)80008-4

Mendoza-Roldan JA, Colella V, Lia RP, Nguyen VL, Barros-Battesti DM, Iatta R, Dantas-Torres F, Otranto D (2019) *Borrelia burgdorferi* (sensu lato) in ectoparasites and reptiles in southern Italy. *Parasites and Vectors*, **12**. https://doi.org/10.1186/s13071-019-3286-1

Michelet L, Bonnet S, Madani N, Moutailler S (2013) Discriminating *Francisella tularensis* and *Francisella*-like endosymbionts in *Dermacentor reticulatus* ticks: Evaluation of current molecular techniques. *Veterinary Microbiology*, **163**, 399–403. https://doi.org/10.1016/j.vetmic.2013.01.014

Michelet L, Delannoy S, Devillers E, Gérald Umhang, Aspan A, Juremalm M, Chirico J, van der Wal FJ, Sprong H, Boye Pihl TP, Klitgaard K, Bødker R, Fach P, Moutailler S (2014) High-throughput screening of tick-borne pathogens in Europe. *Frontiers in Cellular and Infection Microbiology*, **4**, 1–13. https://doi.org/10.3389/fcimb.2014.00103

Michelet L, Joncour G, Devillers E, Torina A, Vayssier-Taussat M, Bonnet SI, Moutailler S (2016) Tick species, tick-borne pathogens and symbionts in an insular environment off the coast of Western France. *Ticks and Tick-borne Diseases*, **7**, 1109–1115. https://doi.org/10.1016/j.ttbdis.2016.08.014

Morellet N, Moorter BV, Cargnelutti B, van Moorter B, Cargnelutti B, Angibault JM, Lourtet B, Merlet J, Ladet S, Hewison AJM (2011) Landscape composition influences roe deer habitat selection at both home range and landscape scales. *Landscape Ecology*, **26**, 999–1010. https://doi.org/10.1007/s10980-011-9624-0

Moutailler S, Popovici I, Devillers E, Vayssier-Taussat M, Eloit M (2016) Diversity of viruses in *Ixodes ricinus*, and characterization of a neurotropic strain of Eyach virus. *New Microbes and New Infections*, **11**, 71–81. https://doi.org/10.1016/j.nmni.2016.02.012

Moutailler S, Valiente Moro C, Vaumourin E, Michelet L, Tran FH, Devillers E, Cosson JF, Gasqui P, Van VT, Mavingui P, Vourc'h G, Vayssier-Taussat M (2016) Co-infection of ticks: the rule rather than the exception. *PLoS Neglected Tropical Diseases*, **10**, e0004539 (17 p). https://doi.org/10.1371/journal.pntd.0004539

Mysterud A, Easterday WR, Stigum VM, Aas AB, Meisingset EL, Viljugrein H (2016) Contrasting emergence of Lyme disease across ecosystems. *Nature Communications*, **7**, 11. https://doi.org/10.1038/ncomms11882

Nadal C, Bonnet SI, Marsot M (2021) Eco-epidemiology of equine piroplasmosis and its associated tick vectors in Europe: A systematic literature review and a meta-analysis of prevalence. *Transboundary and Emerging Diseases*, 1–25. https://doi.org/10.1111/tbed.14261

Nebbak A, Dahmana H, Almeras L, Raoult D, Boulanger N, Jaulhac B, Mediannikov O, Parola P (2019) Co-infection of bacteria and protozoan parasites in *Ixodes ricinus* nymphs collected in the Alsace region, France. *Ticks and Tick-borne Diseases*, **10**, 101241. https://doi.org/10.1016/j.ttbdis.2019.06.001
Nefedova V, Korenberg EI, Gorelova NB (2005) Genetic characteristics of human pathogenic *Borrelia* isolated from *Ixodes trianguliceps* Bir. and *Ixodes pavlovskyi* Pom. *Meditsinskaia parazitologiia i parazitarnye bolezni*, **2**, 9–12.

Palomar AM, Portillo A, Santibáñez P, Mazuelas D, Roncero L, Gutiérrez Ó, Oteo JA (2017) Presence of *Borrelia turdi* and *Borrelia valaisiana* (Spirochaetales: Spirochaetaceae) in ticks removed from birds in the North of Spain, 2009–2011. *Journal of Medical Entomology*, **54**, 243–246.
https://doi.org/10.1093/jme/tjw158

Pan H, Liu S, Ma Y, Tong S, Sun Y (2003) *Ehrlichia*-like organism gene found in small mammals in the suburban district of Guangzhou of China. *Annals of the New York Academy of Sciences*, **990**, 107–111.
https://doi.org/10.1111/j.1749-6632.2003.tb07346.x

Panas E, Leger N, Kretz JL, Dumesnil C (1976) Ixodidae of the Champagne-Ardennes region. Preliminary study. *Acarologia*, **18**, 51–55.

Parola P, Beati L, Cambon M, Brouqui P, Raoult D (1998) Ehrlichial DNA amplified from *Ixodes ricinus* (Acari: Ixodidae) in France. *Journal of Medical Entomology*, **35**, 180–183.
https://doi.org/10.1093/jmedent/35.2.180

Parola P, Beati L, Cambon M, Raoult D (1998) First isolation of *Rickettsia helvetica* from *Ixodes ricinus* ticks in France. *European Journal of Clinical Microbiology and Infectious Diseases*, **17**, 95–100.
https://doi.org/10.1007/s100960050024

Paul REL, Cote M, Le Naour E, Bonnet SI (2016) Environmental factors influencing tick densities over seven years in a French suburban forest. *Parasites and Vectors*, **9**, 1–10.
https://doi.org/10.1186/s13071-016-1591-5

Perez G (2023) The distribution, phenology, host range and pathogen prevalence of *Ixodes ricinus* in France: a systematic map and narrative review. IRAD Dataverse, V1.
https://doi.org/10.18167/DVN1/ACTN01

Perez G, Bastian S, Agoulon A, Bouju A, Durand A, Faille F, Lebert I, Rantier Y, Plantard O, Butet A (2016) Effect of landscape features on the relationship between *Ixodes ricinus* ticks and their small mammal hosts. *Parasites and Vectors*, **9**, 1–18. https://doi.org/10.1186/s13071-016-1296-9

Perez G, Bastian S, Chastagner A, Agoulon A, Rantier Y, Vourc'h G, Plantard O, Butet A (2020) Relationships between landscape structure and the prevalence of two tick-borne infectious agents, *Anaplasma phagocytophilum* and *Borrelia burgdorferi* sensu lato, in small mammal communities. *Landscape Ecology*, **35**. https://doi.org/10.1007/s10980-019-00957-x

Pérez-Eid C (1989) Dynamique saisonnière des nymphes et adultes d' *Ixodes ricinus* en phase libre sur la végétation, dans le foyer alsacien d'encéphalite à tiques. *Acarologia*, **30**, 355-360.

Pérez-Eid C (1990) Les relations tiques-petits mammifères dans le foyer alsacien d'encéphalite à tiques. *Acarologia*, **31**, 131-141.

Pérez-Eid C (2007) *Les tiques : Identification, biologie, importance médicale et vétérinaire*. Paris.

Pérez-Eid C, Hannoun C, Rodhain F (1992) The Alsatian tick-borne encephalitis focus: presence of the virus among ticks and small mammals. *European journal of Epidemiology*, **8**, 178–186.
https://doi.org/10.1007/bf00144797

Perret J-L, Guerin PM, Diehl PA, Vlimant M, Gern L (2003) Darkness induces mobility, and saturation deficit limits questing duration, in the tick *Ixodes ricinus*. *The Journal of Experimental Biology*, **206**, 1809–1815. https://doi.org/10.1242/jeb.00345

Perret JL, Guigoz E, Rais O, Gern L (2000) Influence of saturation deficit and temperature on *Ixodes ricinus* tick questing activity in a Lyme borreliosis-endemic area (Switzerland). *Parasitology research*, **86**, 554–557. https://doi.org/10.1007/s004360000209

Perret J-L, Rais O, Gern L (2004) Influence of climate on the proportion of *Ixodes ricinus* nymphs and adults questing in a tick population. *Journal of medical entomology*, **41**, 361–365.
https://doi.org/10.1603/0022-2585-41.3.361

Pexara A, Solomakos N, Govaris A (2018) Q fever and prevalence of *Coxiella burnetii* in milk. *Trends in Food Science & Technology*, **71**, 65–72. https://doi.org/10.1016/j.tifs.2017.11.004

Pichon B, Mousson L, Figureau C, Rodhain F, Pérez-Eid C (1999) Density of deer in relation to the prevalence of *Borrelia burgdorferi* s.l. in *Ixodes ricinus* nymphs in Rambouillet forest, France. *Experimental & applied acarology*, **23**, 267–75. https://doi.org/10.1023/a:1006023115617
Pichot J, Gilot B, Almire N, Polette K, Degeilh B (1997) *Ixodes* populations (*Ixodes ricinus* Linné, 1758; *Ixodes hexagonus* Leach, 1815) in the city of Lyon (France) and its outskirts: Preliminary results. *Parasite, 4*, 167-171. https://doi.org/10.1051/parasite/1997042167

Pisanu B, Chapuis JL, Dozières A, Basset F, Poux V, Vourc'h G (2014) High prevalence of *Borrelia burgdorferi* s.l. in the European red squirrel *Sciurus vulgaris* in France. *Ticks and Tick-borne Diseases, 5*, 1-6. https://doi.org/10.1016/j.ttbdis.2013.07.007

Pisanu B, Marsot M, Marmet J, Chapuis J-L, Réale D, Vourc'h G (2010) Introduced Siberian chipmunks are more heavily infested by ixodid ticks than are native bank voles in a suburban forest in France. *International Journal for Parasitology, 40*, 1277-1283. https://doi.org/10.1016/j.ijpara.2010.03.012

Platonov AE, Karan LS, Kolyasnikova NM, Makhneva NA, Toporkova MG, Maleev VV, Fish D, Krause PJ (2011) Humans infected with relapsing fever spirochete *Borrelia miyamotoi*, Russia. *Emerging Infectious Diseases, 17*, 1816-1823. https://doi.org/10.3201/eid1710.101474

Portillo A, Santibáñez P, Palomar AM, Santibáñez S, Oteo JA (2018) "Candidatus Neoehrlichia mikurensis" in Europe. *New Microbes and New Infections, 22*, 30-36. https://doi.org/10.1016/j.nmni.2017.12.011

Quessada T, Martial-Convert F, Arnaud S, Leudet De La Vallee H, Gilot B, Pichot J (2003) Prevalence of *Borrelia burgdorferi* species and identification of *Borrelia valaisiana* in questing *Ixodes ricinus* in the Lyon region of France as determined by polymerase chain reaction-restriction fragment length polymorphism. *European Journal of Clinical Microbiology and Infectious Diseases, 22*, 165-173. https://doi.org/10.1007/s10096-002-0866-2

Randolph SE, Gem L, Nuttall PA (1996) Co-feeding ticks: epidemiological significance for tick-borne pathogen transmission. *Parasitology Today, 12*, 472-479. https://doi.org/10.1016/s0169-4758(96)10072-7

Randolph SE, Green RM, Peacey MF, Rogers DJ (2000) Seasonal synchrony: the key to tick-borne encephalitis foci identified by satellite data. *Parasitology, 121*, 15-23. https://doi.org/10.1017/s0031182099006083

Randolph SE, Miklisová D, Lysy J, Rogers DJ, Labuda M (1999) Incidence from coincidence: patterns of tick infestations on rodents facilitate transmission of tick-borne encephalitis virus. *Parasitology, 118*, 177-186. https://doi.org/10.1017/S0031182098003643

Randolph SE, Rogers DJ (2000) Fragile transmission cycles of tick-borne encephalitis virus may be disrupted by predicted climate change. *Proceedings of the Royal Society of London: Biological Sciences, 267*, 1741-1744. https://doi.org/10.1098/rspb.2000.1204

Randolph, S. E., & Steele GM (1985) An experimental evaluation of conventional control measures against the sheep tick, *Ixodes ricinus* (L.) (Acari: Ixodidae). II. The dynamics of the tick-host interaction. *Bulletin of Entomological Research, 75*, 501-518. https://doi.org/10.1017/S0007485300014590

Randolph SE, Storey K (1999) Impact of microclimate on immature tick-rodent host interactions (Acari: Ixodidae): implications for parasite transmission. *Journal of Medical Entomology, 36*, 741-748. https://doi.org/10.1093/jmedent/36.6.741

Rar V, Golovljova I (2011) *Anaplasma, Ehrlichia*, and "Candidatus Neoehrlichia" bacteria: Pathogenicity, biodiversity, and molecular genetic characteristics, a review. *Infection, Genetics and Evolution, 11*, 1842-1861. https://doi.org/10.1016/j.meegid.2011.09.019

Reis C, Cote M, Le Rhun D, Lecuelle B, Levin ML, Vayssier-Taussat M, Bonnet SI (2011) Vector competence of the tick *Ixodes ricinus* for transmission of *Bartonella birtlesii*. *PLoS Neglected Tropical Diseases, 5*, 1-6. https://doi.org/10.1371/journal.pntd.0001186

Reis C, Cote M, Paul REL, Bonnet S (2011) Questing ticks in suburban forest are infected by at least six tick-borne pathogens. *Vector-borne and Zoonotic Diseases, 11*, 907-916. https://doi.org/10.1089/vbz.2010.0103

Reye AL, Stegniy V, Mishaeva NP, Velhin S, Hübschen JM, Ignatyev G, Muller CP (2013) Prevalence of tick-borne pathogens in *Ixodes ricinus* and *Dermacentor reticulatus* ticks from different geographical locations in Belarus. *PLoS one, 8*, e54476. https://doi.org/10.1371/journal.pone.0054476

Richardson M, Khouja C, Sutcliffe K (2019) Interventions to prevent Lyme disease in humans: a systematic review. *Preventive Medicine Reports journal, 13*, 16-22. https://doi.org/10.1016/j.pmedr.2018.11.004

Richter D, Matuschka FR (2012) "Candidatus Neoehrlichia mikurensis", *Anaplasma phagocytophilum*, and Lyme disease spirochetes in questing European vector ticks and in feeding ticks removed from people. *Journal of Clinical Microbiology, 50*, 943-947. https://doi.org/10.1128/JCM.05802-11
Richter D, Schlee DB, Allgöwer R, Matuschka FR (2004) Relationships of a novel Lyme disease spirochete, *Borrelia spielmani* sp. nov., with its hosts in Central Europe. *Applied and Environmental Microbiology*, **70**, 6414–6419. https://doi.org/10.1128/AEM.70.11.6414-6419.2004

Richter D, Schlee DB, Matuschka FR (2003) Relapsing fever-like spirochetes infecting European vector tick of Lyme disease agent. *Emerging Infectious Diseases*, **9**, 697–701. https://doi.org/10.3201/eid0906.020459

Rigaud E, Jaulhac B, Garcia-Bonnet N, Hunfeld K-PP, Féménia F, Huet D, Goulvestre C, Vaillant V, Deffontaines G, Abadia-Benoist G (2016) Seroprevalence of seven pathogens transmitted by the *Ixodes ricinus* tick in forestry workers in France. *Clinical Microbiology and Infection*, **22**, 735.e1-735.e9. https://doi.org/10.1016/j.cmi.2016.05.014

Romeo C, Pisanu B, Ferrari N, Basset F, Tillon L, Wauters LA, Martinoli A, Saino N, Chapuis J-L (2013) Macroparasite community of the Eurasian red squirrel (*Sciurus vulgaris*): poor species richness and diversity. *Parasitology Research*, **112**, 3527–3536. https://doi.org/10.1007/s00436-013-3535-8

Ruiz-Fons F, Fernández-de-Mera IG, Acevedo P, Gortázar C, de la Fuente J (2012) Factors driving the abundance of *Ixodes ricinus* ticks and the prevalence of zoonotic *I. ricinus*-borne pathogens in natural foci. *Applied and Environmental Microbiology*, **78**, 2669–2676. https://doi.org/10.1128/AEM.06564-11

Ruzek D, Županc TA, Borde J, Chrdle A, Eyer L, Karganova G, Kholodilov I, Knap N, Kozlovskaya L, Matveev A, Miller AD, Osolodkin DI, Överby AK, Tikunova N, Tkachev S, Zajkowska J (2019) Tick-borne encephalitis in Europe and Russia: Review of pathogenesis, clinical features, therapy, and vaccines. *Antiviral Research*, **164**, 23–51. https://doi.org/10.1016/j.antiviral.2019.01.014

Rymaszewska A, Grenda S (2008) Bacteria of the genus *Anaplasma*— characteristics of *Anaplasma* and their vectors: a review. *Veterinarni Medicina*, **53**, 573–584. https://doi.org/10.17221/1861-vetmed

Santos AS, de Bruin A, Veloso AR, Marques C, Pereira da Fonseca I, de Sousa R, Sprong H, Santos-Silva MM (2018) Detection of Anaplasma phagocytophilum, Candidatus Neoehrlichia sp., Coxiella burnetii and Rickettsia spp. in questing ticks from a recreational park, Portugal. *Ticks and Tick-borne Diseases*, **9**, 1555–1564. https://doi.org/10.1016/j.ttbdis.2018.07.010

Santos AS (2023) An extensive review of *Ixodes ricinus* in European France. Peer Community Infections, 100076. https://doi.org/10.24072/pci.infections.100076

Schnittger L, Rodriguez AE, Florin-christensen M, Morrison DA (2012) *Babesia*: a world emerging. *Infection, Genetics and Evolution*, **12**, 1788–1809. https://doi.org/10.1016/j.meegid.2012.07.004

Schouls LM, van de Pol I, Rijpkema SGT, Schot CS (1999) Detection and identification of *Ehrlichia*, *Borrelia burgdorferi* sensu lato, and *Bartonella* species in dutch *Ixodes ricinus* ticks. *Journal of Clinical Microbiology*, **37**, 2215–2222. https://doi.org/10.1128/JCM.37.7.2215-2222.1999

Septfons A, Couturier E, Thomas G, Turbelin C, Blanchon T, de Valk H (2018) Borréliose de Lyme : estimation de l'incidence hospitalière en France de 2005 à 2016. *Bulletin Epidemiologie Hebdomadaire*, 389-395.

Sevestre J, Diarra AZ, Oumarou HA, Durant J, Delaunay P, Parola P (2021) Detection of emerging tick-borne disease agents in the Alpes-Maritimes region, southeastern France. *Ticks and Tick-borne Diseases*, **12**, 101800. https://doi.org/10.1016/j.ttbdis.2021.101800

Silaghi C, Beck R, Oteo JA, Pfeffer M, Sprong H (2015) Neoehrlichiosis: an emerging tick-borne zoonosis caused by *Candidatus* Neoehrlichia mikurensis. *Experimental and Applied Acarology*, **68**, 279–297. https://doi.org/10.1007/s10493-015-9935-y

Siński E, Welc-Faleciak R, Poglód R (2011) *Babesia* spp. infections transmitted through blood transfusion. *Wiadomości Parazytologiczne*, **57**, 77–81.

Solano-Gallego L, Sainz Á, Roura X, Estrada-Peña A, Miró G (2016) A review of canine babesiosis: the European perspective. *Parasites & Vectors*, **9**, 336 (18 p). https://doi.org/10.1186/s13071-016-1596-0

Sormunen JJ, Pakanen V, Elo R (2021) Absence of *Francisella tularensis* in Finnish *Ixodes ricinus* and *Ixodes persulcatus* ticks. *Ticks and Tick-borne Diseases*, **12**, 12–15. https://doi.org/10.1016/j.ttbdis.2021.101809

Spitalska E, Literak I, Kocianova E, Taragel'ova V (2011) The importance of *Ixodes arboricola* in transmission of *Rickettsia* spp., *Anaplasma phagocytophilum*, and *Borrelia burgdorferi* sensu lato in the Czech Republic, Central Europe. *Vector-borne and Zoonotic Diseases*, **11**, 1235–1241. https://doi.org/10.1089/vbz.2010.0210
Sprong H, Moonen S, van Wieren SE, Hofmeester TR (2019) Effects of cattle grazing on *Ixodes ricinus*-borne disease risk in forest areas of the Netherlands. *Ticks and Tick-borne Diseases*, **11**, 101355.
https://doi.org/10.1016/j.ttbdis.2019.101355

Stachurski F, Vial L (2018) Installation de la tique *Hyalomma marginatum*, vectrice du virus de la fièvre hémorragique de Crimée-Congo, en France continentale. *Bulletin Epidémiologique Santé animale - Alimentation*, **84**, 1-5. https://publications.cirad.fr/en/une_notice.php?dk=589517

Stanek G, Reiter M (2011) The expanding Lyme Borrelia complex—clinical significance of genomic species? *Clinical Microbiology and Infection*, **17**, 487-493. https://doi.org/10.1111/j.1469-0691.2011.03492.x

Steigedal HH, Loe LE, Grøva L, Mysterud A (2013) The effect of sheep (*Ovis aries*) presence on the abundance of ticks (*Ixodes ricinus*). *Acta Agriculturae Scandinavica, Section A - Animal Science*, **63**, 111-120. https://doi.org/10.1080/09064702.2013.823236

Steinbrink A, Brugger K, Margos G, Kraiczy P, Klimpel S (2022) The evolving story of *Borrelia burgdorferi* sensu lato transmission in Europe. *Parasitology Research*, **121**, 781-803.
https://doi.org/10.1007/s00436-022-07445-3

Stigum VM, Jaarsma RI, Sprong H, Rolandsen CM, Mysterud A (2019) Infection prevalence and ecotypes of *Anaplasma phagocytophilum* in moose *Alces alces*, red deer *Cervus elaphus*, roe deer *Capreolus capreolus* and *Ixodes ricinus* ticks from Norway. *Parasites and Vectors*, **12**, 1.
https://doi.org/10.1186/s13071-018-3256-z

Strle F, Ružić-Sabljić E, Cimperman J, Lotrič-Furlan S, Maraspin V (2006) Comparison of findings for patients with *Borrelia garinii* and *Borrelia afzelii* isolated from cerebrospinal fluid. *Clinical Infectious Diseases*, **43**, 704–710. https://doi.org/10.1086/506936

Strnad M, Hönig V, Ružek D, Grubhoffer L, Ryan R (2017) Europe-wide meta-analysis of *Borrelia burgdorferi* sensu lato prevalence in questing *Ixodes ricinus* ticks. *Applied and Environmental Microbiology*, **83**, 1–16. https://doi.org/10.1128/AEM.00609-17

Süss J (2011) Tick-borne encephalitis 2010: Epidemiology, risk areas, and virus strains in Europe and Asia. An overview. *Ticks and Tick-borne Diseases*, **2**, 2–15. https://doi.org/10.1016/j.ttbdis.2010.10.007

Szekeres S, Coipan EC, Rigó K, Majoros G, Jahfari S, Sprong H, Földvári G (2015) Eco-epidemiology of *Borrelia miyamotoi* and Lyme borreliosis spirochetes in a popular hunting and recreational forest area in Hungary. *Parasites and Vectors*, **8**, 309 (8 p). https://doi.org/10.1186/s13071-015-0922-2

Tagliapietra V, Rosà R, Arnoldi D, Cagnacci F, Capelli G, Montarsi F, Hauffe HC, Rizzoli A (2011) Saturation deficit and deer density affect questing activity and local abundance of *Ixodes ricinus* (Acari, Ixodidae) in Italy. *Veterinary Parasitology*, **183**, 114-24. https://doi.org/10.1016/j.vetpar.2011.07.022

Takumi K, Sprong H, Hofmeester TR (2019) Impact of vertebrate communities on *Ixodes ricinus*-borne disease risk in forest areas. *Parasites and Vectors*, **12**, 434. https://doi.org/10.1186/s13071-019-3700-8

Telford III SR, Goethert HK (2020) Ecology of *Francisella tularensis*. *Annual Review of Entomology*, **65**, 351-372. https://doi.org/10.1146/annurev-ento-011019-025134.Ecology

Tobudic S, Burgmann H, Stanek G, Winkler S, Schötta A-M, Obermüller M, Markowicz M, Lagler H (2020) Human *Borrelia miyamotoi* infection, Austria. *Emerging Infectious Diseases*, **26**, 2201-2204.
https://doi.org/10.3201/eid2609.191501

Tomkins JL, Aungier J, Hazel W, Gilbert L (2014) Towards an evolutionary understanding of questing behaviour in the tick *Ixodes ricinus*. *PLoS ONE*, **9**, e110028.
https://doi.org/10.1371/journal.pone.0110028

Ulmer P, Ferté H, Mercier A, Richard S (1999) Lyme Borreliosis: epidemiological survey carried out in a kennel in north-eastern France. *Revue Française des Laboratoires*, **1999**, 49-56.
https://doi.org/10.1016/S0338-9898(99)80375-8

Vannier E, Krause PJ (2012) Human Babesiosis. *The New England Journal of Medicine*, **366**, 22–26.
https://doi.org/10.1056/NEJMra1202018

Vassallo M, Paul REL, Pérez-Eid C (2000) Temporal distribution of the annual nymphal stock of *Ixodes ricinus* ticks. *Experimental & Applied Acarology*, **24**, 941-949.
https://doi.org/10.1023/a:1010669003887
Vayssier-Taussat M, Moutailler S, Michelet L, Devillers E, Bonnet S, Eloit M, Cheval J, He C, Hébert C, Eloit M (2013) Next generation sequencing uncovers unexpected bacterial pathogens in ticks in Western Europe. *PLoS ONE*, **8**, e81439 (7 p). https://doi.org/10.1371/journal.pone.0081439

Vayssier-Taussat M, le Rhun D, Buffet J-P, Maaoui N, Galan M, Guivier E, Charbonnel N, Cosson J-F (2012) *Candidatus* Neoehrlichia mikurensis in bank voles, France. *Emerging Infectious Diseases*, **18**, 2063–2065. https://doi.org/10.3201/eid1812.120846

Velay A, Solis M, Kack-Kack W, Gantner P, Maquart M, Martinot M, Augereau O, Briel DD, Kieffer P, Lohmann C, Poveda JD, Cart-Tanneur E, Argemi X, Leparc-Goffart I, de Martino S, Jaulhac B, Raguet S, Wendling M-J, Hansmann Y, Fafi-Kremer S (2018) A new hot spot for tick-borne encephalitis (TBE): a marked increase of TBE cases in France in 2016. *Ticks and Tick-borne Diseases*, **9**, 120–125. https://doi.org/10.1016/j.ttbdis.2017.09.015

Vollmer SA, Bormane A, Dinnis RE, Seelig F, Dobson ADM, Aanensen DM, James MC, Donaghy M, Randolph SE, Feil EJ, Kurtenbach K, Margos G (2011) Host migration impacts on the phylogeography of Lyme Borreliosis spirochaete species in Europe. *Environmental Microbiology*, **13**, 184–192. https://doi.org/10.1111/j.1462-2920.2010.02319.x

Vourc'h G, Abrial D, Bord S, Jacquot M, Masseglia S, Poux V, Pisanu B, Bailly X, Chapuis J-L (2016) Mapping human risk of infection with *Borrelia burgdorferi* sensu lato, the agent of Lyme borreliosis, in a periurban forest in France. *Ticks and tick-borne diseases*, **7**, 644–652. https://doi.org/10.1016/j.ttbdis.2016.02.008

Vourc'h G, Marmet J, Chassagne M, Bord S, Chapuis J-L (2007) *Borrelia burgdorferi* sensu lato in Siberian chipmunks (*Tamias sibiricus*) introduced in suburban forests in France. *Vector-borne and Zoonotic Diseases*, **7**, 637–641. https://doi.org/10.1089/vbz.2007.0111

Wagemakers A, Staarink PJ, Sprong H, Hovius JWR (2015) *Borrelia miyamotoi*: a widespread tick-borne relapsing fever spirochete. *Trends in Parasitology*, **31**, 260–269. https://doi.org/10.1016/j.pt.2015.03.008

Walter G, Weber G (1981) A study on the transmission (transstadial, transovarial) of *Babesia microti*, strain "Hannover I", in its tick vector, *Ixodes ricinus* (author's transl). *Tropenmedizin und Parasitologie*, **32**, 228–230.

Wass L, Grankvist A, Bell-sakyi L, Bergström M, Ulfhammer E (2019) Cultivation of the causative agent of human neoehrlichiosis from clinical isolates identifies vascular endothelium as a target of infection. *Emerging Microbes & Infections*, **8**, 413–425. https://doi.org/10.1080/22221751.2019.1584017

Wechtaisong W, Bonnet SI, Lien Y-Y, Chuang S-T, Tsai Y-L (2020) Transmission of *Bartonella henselae* within *Rhipicephalus sanguineus*: Data on the potential vector role of the tick. *PLoS Neglected Tropical Diseases*, **14**, e0008664 (1-14). https://doi.org/10.1371/journal.pntd.0008664

Welinder-Olsson C, Kjellin E, Vaht K, Jacobsson S, Wennerås C (2010) First case of human "*Candidatus* Neoehrlichia mikurensis" infection in a febrile patient with chronic lymphocytic leukemia. *Journal of Clinical Microbiology*, **48**, 1956–1959. https://doi.org/10.1128/JCM.02423-09

White A, Gaff H (2018) Review: application of tick control technologies for blacklegged, lone star, and American dog ticks. *Journal of Integrated Pest Management*, **9**, 12 (10 p). https://doi.org/10.1093/jipm/pmy006

Wilhelmsson P, Jaenson TGT, Olsen B, Waldenström J, Lindgren PE (2020) Migratory birds as disseminators of ticks and the tick-borne pathogens *Borrelia* bacteria and tick-borne encephalitis (TBE) virus: a seasonal study at Ottenby Bird Observatory in South-eastern Sweden. *Parasites & Vectors*, **13**, 607. https://doi.org/10.1186/s13071-020-04493-5

Wilske B, Busch U, Eiffert H, Fingerle V, Pfister HW, Rössler D, Preac-Mursic V (1996) Diversity of OspA and OspC among cerebrospinal fluid isolates of *Borrelia burgdorferi* sensu lato from patients with neuroborreliosis in Germany. *Medical Microbiology and Immunology*, **184**, 195–201. https://doi.org/10.1007/BF02456135

Wolcott KA, Margos G, Fingerle V, Becker NS (2021) Host association of *Borrelia burgdorferi* sensu lato: A review. *Ticks and Tick-borne Diseases*, **12**, e101766. https://doi.org/10.1016/j.ttbdis.2021.101766

Wongnak P, Bord S, Jacquot M, Agoulon A, Beugnet F, Bournez L, Cèbe N, Chevalier A, Cosson JF, Dambrine N, Hoch T, Huard F, Korboulewsky N, Lebert I, Madouasse A, Mårell A, Poux V, René-Martellet M, Vayssier-Taussat M, Verheyden H, Vourc'h G, Chalvet-Monfray K (2022) Meteorological and climatic variables predict the phenology of *Ixodes ricinus* nymph activity in France,
accounting for habitat heterogeneity. *Scientific Reports*, **12**, 1–16. https://doi.org/10.1038/s41598-022-11479-z

Young KM, Corrin T, Wilhelm B, Uhland C, Greig J, Mascarenhas M, Waddell LA (2019) Zoonotic *Babesia*: A scoping review of the global evidence. *PLoS ONE*, **14**, e0226781 (31 p). https://doi.org/10.1371/journal.pone.0226781

Zlobin VI, Pogodina VV, Kahl O (2017) A brief history of the discovery of tick-borne encephalitis virus in the late 1930s (based on reminiscences of members of the expeditions, their colleagues, and relatives). *Ticks and Tick-borne Diseases*, **8**, 813–820. https://doi.org/10.1016/j.ttbdis.2017.05.001

Zöldi V, Reicziegel J, Egyed L (2013) Monitoring the diel activity of *Ixodes ricinus* ticks in Hungary over three seasons. *Experimental and Applied Acarology*, **61**, 509–517. https://doi.org/10.1007/s10493-013-9708-4