Spatial disaggregation of tick occurrence and ecology at a local scale as a preliminary step for spatial surveillance of tick-borne diseases: general framework and health implications in Belgium
© Obsomer et al.; licensee BioMed Central Ltd. 2013
Received: 25 May 2013
Accepted: 16 June 2013
Published: 22 June 2013
The incidence of tick-borne diseases is increasing in Europe. Sub national information on tick distribution, ecology and vector status is often lacking. However, precise location of infection risk can lead to better targeted prevention measures, surveillance and control.
In this context, the current paper compiled geolocated tick occurrences in Belgium, a country where tick-borne disease has received little attention, in order to highlight the potential value of spatial approaches and draw some recommendations for future research priorities.
Mapping of 89,289 ticks over 654 sites revealed that ticks such as Ixodes ricinus and Ixodes hexagonus are largely present while Dermacentor reticulatus has a patchy distribution. Suspected hot spots of tick diversity might favor pathogen exchanges and suspected hot spots of I. ricinus abundance might increase human-vector contact locally. This underlines the necessity to map pathogens and ticks in detail. While I. ricinus is the main vector, I. hexagonus is a vector and reservoir of Borrelia burgdorferi s.l., which is active the whole year and is also found in urban settings. This and other nidiculous species bite humans less frequently, but seem to harbour pathogens. Their role in maintaining a pathogenic cycle within the wildlife merits investigation as they might facilitate transmission to humans if co-occurring with I. ricinus. Many micro-organisms are found abroad in tick species present in Belgium. Most have not been recorded locally but have not been searched for. Some are transmitted directly at the time of the bite, suggesting promotion of tick avoidance additionally to tick removal.
This countrywide approach to tick-borne diseases has helped delineate recommendations for future research priorities necessary to design public health policies aimed at spatially integrating the major components of the ecological cycle of tick-borne diseases. A systematic survey of tick species and associated pathogens is called for in Europe, as well as better characterisation of species interaction in the ecology of tick-borne diseases, those being all tick species, pathogens, hosts and other species which might play a role in tick-borne diseases complex ecosystems.
KeywordsTick Vector Spatial distribution Ecology Vector-borne diseases
The incidence of tick-borne diseases is increasing in Europe  and follows an increase in the number of tick bites  attributed to two factors: abundance of questing ticks and human exposure to ticks . Measures targeting human exposure by promoting timely removal of ticks failed to stop the rise in Lyme borreliosis incidence in the Netherlands. On the other hand, this rise was related to an increase in Ixodes ricinus abundance . Knowing the local variations in the distribution of the species interacting in tick-borne diseases systems, including ticks, pathogens and species influencing the presence and abundance of ticks and pathogens, could provide new opportunities to estimate potential infection risks locally, identify local hot spots and develop targeted prevention, surveillance and control.
Necessary information is lacking at national and sub national levels in many countries. The first missing information concerns the presence and distribution of tick species. Efforts to characterise tick distribution on a European scale [4–6] are limited by the information available at sub national level and only target major vectors such as I. ricinus. Other tick species less willingly biting humans sometimes harbour high pathogen prevalence’s and might contribute locally to the pathogens’ cycles . The role of all tick species present should be investigated jointly per pathogen and their distribution clarified. The second missing information concerns the spatial distribution of hosts, predators and species influencing tick populations and pathogens’ prevalence in ticks. The presence and abundance of tick species varies locally according to many factors, including host availability . Pathogen prevalence in ticks also varies locally according to availability of reservoirs, dead-end hosts and vectors . The third set of missing information concerns pathogens associated to ticks, their presence, reservoirs, vectors and distribution. Pathogens found using classical PCR methods are those searched for, while others might be present but undetected. Because micro-organisms are increasingly found in ticks, a more systematic approach is needed. The list of micro-organisms found locally or abroad in local tick species could be narrowed by clarifying pathogenicity, vector capacity and presence of reservoirs to provide a list of potential pathogens to investigate locally. This would clarify the spectrum of pathogens potentially transmitted locally through a tick bite.
In this paper, occurrence records and information on tick species relevant for public health have been compiled for a country where tick-borne diseases received little attention. In Belgium, the limited quality of current information is obvious because of proximity to the Netherlands, a country that stands out for efficient investigations of tick-borne diseases. In the Netherlands, tick bites are subject to spatial monitoring . Lyme borreliosis is monitored by physician surveys targeting Erythema migrans, the most common symptom . In Belgium, only Lyme borreliosis is regularly diagnosed. In 2009, official numbers of cases varied from 500 to 1500  or 9000 cases  according to the source. In the Netherlands, 22000 cases were recorded for that same year . I. ricinus is believed to occur in Southeast Belgium but records occur elsewhere. Detailed distribution can approximate local exposure to ticks. This is of direct public health interest because according to European guidelines for Lyme borreliosis, an individual presenting an Erythema migrans is considered a confirmed case if potentially exposed to areas favourable for vector ticks . Laboratory confirmation and remembering a tick bite are not necessary to confirm this diagnosis.
This study aims to show how an integrated spatial approach on tick species in a given country can provide the preliminary information needed for adapted national public health policies by providing: 1) a list of tick species present and their detailed distribution, 2) the micro-organisms they could harbour, 3) ecological traits influencing vector status, 4) implications for public health and suggestions for future research priorities.
Three sources of tick locations were considered: new tick collections, literature collections and “grey datasets”. Quality levels are proposed for each record to document for example accuracy of tick location according to type of host/vegetation (lower if captured on moving animals such as dog or deer). Information on localisation, collection, vegetation or host, pathogen load, and original data source were compiled in an excel database (Additional file 1). A systematic literature search was made based on ISI web of knowledge using the keywords “tick AND ecology” from 1989 to 2001 and “tick” from 2002 to 2011. Additional articles resulted from a specific search on presence and pathogenicity of microorganisms found in ticks. The database and additional literature articles form the basis for this paper and are examined for the following items: geographical distribution, species behaviour, ecology, presence of micro-organisms. Consequences for public health and prevention are highlighted. For some sites additional details were provided by authors, however, the methodology is already described in published articles and summarised in the Additional file 1. This includes (1) Collection BAYER, 579 sites , (2) Collection RLVBD, 51 sites , (3) Collection UGENT FOREST, 33 sites [15, 16], (4) Collection ARSIA, 17 sites , (5) Collection UCLIREC, 5 sites , and (6) Collection UA1, 16 sites [7, 19–22]. Collection GREY DATA includes tick field observations from the website of NATAGORA and NATUURPUNT (http://www.observations.be, http://www.waarnemingen.be) by registered users involved with nature related activities from 1980 until February 2012. Methodologies for original tick collections are described in detail below:
In the framework of the convention 5284a funded by IRSIA (Institut pour l′encouragement de la recherche dans l′industrie et l′agriculture), the center of acarology (UCL) led two collection campaigns in the Campine, the plateau brabançon and the Condroz. The regions were selected based on local Lyme borreliosis cases and favourable tick habitat. The first campaign in 1989 targeted 30 sites and the second campaign prospected 234 sites from May to October 1990 including 79 days of prospection. Ticks were collected from the environment by flagging. Each collection lasted 2 hours and UTM coordinates were checked on maps (100 m).
From 2007 to 2009, ticks from wild cervids (Cervus elaphus and Capreolus capreolus) found dead, hunted or killed for sanitary reasons were collected by the Wild Screen Network disease monitoring activities in Southern Belgium . Ticks were preserved in 70% ethanol at room temperature, and morphologically identified up to stage and species level (by L. Lempereur and A. Nahayo). Sex and repletion were recorded. Dermacentor reticulatus was also collected on wild cervids from 2010 to 2012. As D. reticulatus and D. marginatus may show overlapping phenotypes , a PCR was used for confirmation, targeting the Dermacentor second Internal Transcribed Spacer 2 (ITS2) with the following primers: ITS_forward (5′-GTG-CGT-CCG-TCG-ACT-CGT-TTT-GA-3′) and ITS_reverse (5′-ACG-GCG-GAC-TAC-GAC-GGA-ATG-C-3′) . The DNA purification was carried out using the NucleoSpin tissue kit for tissue protocol (Macherey-Nagel GmbH, Germany). Samples were frozen in liquid nitrogen and homogenized on a Tissue Lyser® (Qiagen, GmbH, Germany). PCR conditions were as follow: each reaction was carried out in 50 μL volume containing 4 μl of the DNA preparation, 5 μl of each 2 mM dNTP, 2 μl of each 10 μM oligonucleotide primer, 2 U of TaqDNA polymerase (New England Bio labs) with 5 μl of the 10x PCR supplied buffer and completed to 50 μl with sterile water. PCR was achieved with an initial denaturation cycle at 95°C for 5 min, followed by 35 cycles (94°C, 45 s), annealing (53°C, 45 s), extension (72°C, 70 s) and a final extension step at 72°C for 10 min. All ITS2 PCR products were sequenced using a modified Sanger method with the Big Dye terminator kit version 3.1 and resolved with a 3730 ABI capillary sequencer (Applied Bio systems). Sequencing reaction was performed with the same primers as for the PCR and sequences aligned by BLAST search.
Ticks were collected by flagging for several years (site 1, 60, 172).
Additional tick locations registered in museum collections were provided by the IRSNB (Institut Royal des Sciences Naturelles de Belgique).
While investigating anaplasmosis in 11 farms in Flanders, in 2011, the Dierengezonheidzorg (DGZ – Animal Health Care Flanders, Belgium) recorded I. ricinus ticks on several animals from those 11 farms.
Ticks were captured by flagging in 1999 in 3 sites in Belgium (sites 228, 242, 353).
D. reticulatus was found on a human around Namur and a trypanosome discovered in the intestine of I. ricinus in the context of other research .
Collection UGENT VETE
The clinic of poultry diseases of Ghent University performs diagnosis required by individuals. In this framework they recorded a tick infestation on a pigeon from Argas species, probably Argas reflexus in July 2012 near Berlaar (site 303) in the province of Antwerp.
Results and discussion
Tick species found in Belgium per collection
Number of species
Number of ticks
Number of records
Ixodes ricinus (1801/395)
Ixodes hexagonus (634/164)
Dermacentor reticulatus (18/5)
Rhipicephalus sanguineus (6/5)
Ixodes ricinus (868/271)
Dermacentor reticulatus (297/10)
Collection GREY DATA
Ixodes lividus (5/1)
Ixodes ricinus (43150/175)
Ixodes lividus (7/2)
Ixodes hexagonus (792/33)
Rhipicephalus sanguineus (97/13)
Argas reflexus (17/7)
Argas vespertilionis (9/3)
Hyalomma aegyptium (26/4)
Ixodes acuminatus (1/1)
Ixodes arboricola (190/3)
Ixodes canisuga (2/1)
Ixodes frontalis (7/4)
Ixodes trianguliceps (9/8)
Ixodes vespertilionis (29/11)
Ixodes ricinus (5819/192)
Ixodes hexagonus (1/1)
Rhipicephalus sanguineus (1/1)
Ixodes ricinus (2232/87)
Dermacentor reticulatus (159/11)
Ixodes ricinus (4000/8)
Dermacentor reticulatus (66/66)
Ixodes frontalis (2/2)
Ixodes ricinus (22435/45)
Ixodes ricinus (2670/5)
Ixodes hexagonus (1/1)
Ixodes arboricola (2790/12)
Ixodes lividus (18/2)
Ixodes ricinus (600/17)
Ixodes ricinus (6/4)
Ixodes hexagonus (4/2)
Dermacentor reticulatus (2/1)
Argas vespertilionis (5/1)
Dermacentor reticulatus (2/1)
Ixodes canisuga (1/1)
Ixodes frontalis (1/1)
Ixodes trianguliceps (1/1)
Ixodes vespertilionis (18/4)
Ixodes ricinus (11/11)
Ixodes ricinus (167/3)
Ixodes ricinus (1/1)
Dermacentor reticulatus (1/1)
Argas reflexus (1/1)
Tick species in Belgium
Tick species of Belgium
Records in BE (Ticks)
Year for last record
Established in the wild
Established in houses and recurrently imported on host
Not established but recurrently imported on host
Potentially present but never found in Belgium
Tick hosts and ecology in Belgium (details in Additional file 2 )
Canis lupus familiaris, Felis silvestris catus, Erinaceus europaeus, Bos taurus, Homo sapiens, Capreolus capreolus, Carduelis chloris, Cervus elaphus, Parus major, Cyanistes caeruleus, Anthus pratensis, Anthus trivialis, Apodemus sylvaticus, Clethrionomys glareolus, Erithacus rubecula, Hippolais icterina, Sturnus vulgaris, Talpea europaea, Turdus ericetorum, Phylloscopus erolius, Turdus pilaris, Turdus merula, Phylloscopus inornatus, Turdus iliacus, Sitta europea, Ficedula hypoleuca, Fringilla coelebs, Lacerta vivipara, Bubo bubo
Plant species: Fagus sylvatica, Carpinus betulus(hornbeam), Betula pendula (birch), Quercus robur (oak), Quercus petraea (oak), Castanea sativa, Anemone nemorosa, Convallaria majalis, Prunus padus, Pteridium aquilinum, Athyrium filix-femina, Calamagrostis epigejos, Calluna vulgaris, Cytisus scoparius, Dryopteris filix-mas, Sorbus aucuparia, Cytisus scoparius, Holcus lanatus, Holcus mollis, Juncus effusus, Molinia caerulea, Persicaria hydropiper, Urtica dioica, Acer pseudoplatanus, Convallaria majalis, Maianthemum bifolium, Carpinus sp.., Corylus avellana, Cerasus sp, Sambucus nigra,Crataegus monogyna, Vaccinium myrtillus / Pinus, Hedera helix, Rubus fructicosus, Quercus robur & Carpinus sp., Molinia caerulea
Soils: loam or silt with limestone, clay and limestone or schists, leaf litter, schist in Famenne, limestone from Givet, sandstone, poor acid sandy soils, siliceous rock, nettles, impermeable clay soils
Habitat: grazed pasture, forest ecotone, mixed acidophilous to acidophilous oak stands, birch stand with eagle fern, grassy path, garden, urban parcs, forest, dense thicket of beech, forest secondary pine poor acid sandy soils
Capreolus capreolus, Cervus elaphus, Homo sapiens, Canis lupus familiaris
Plant species: grasses, hawthorn, blackthorn (Prunus spinosa), brambles blackberry (Rubus fruticosus), birch (Betula pendula), mixture of grasses, hornbeam (Carpinus betulus), woodland (mainly Picea abies), ferns (Pteridium aquilinum), jennets (Genista scorpius), oak (Quercus robur)
Habitat: Fallow land, marshland, pasture used for grazing, woodland open
Felis silvestris catus, Canis lupus familiaris, Ericaneus europeus, Cervus elaphus, mustela putorius
Rabbit burrow, in herbis, in grassy nest, in house, burrow of Meles meles, endolithe nest of Coloeus monedula, pasture with edges or forest, impermeable clay soils, cave, burrow of fox
Polecat: Mustela putorius
Rodents, Rattus rattus, Rattus norvegicus, Apodemus sylvaticus, Clethrionomys glareolus
Burrow of rodents
Rodents: Apodemus sylvaticus
Birds: Parus major, Turdus merula, Sylvia atricapilla, Cyanistes caeruleus, Sturnus vulgaris, Parus montanus, Turdus viscivoru
It is sometimes found in understorey vegetation, experimental nest box
Birds: Parus major, Cyanistes caeruleus, Sitta europea, Corvus monedula
Occurs in particular in bird nests inside cavities (like tree-holes for example), nest, Delichon urbica nest, experimental nest box
Birds: Riparia riparia
Riparia riparia (nest)
Canis lupus familiaris
flat, house, dovecot
Bats: Pipistrellus pipistrellus, Eptesicus serotinus, rhinocephalus hipposideros
Bats: Rhinolophus hipposideros, Rhinolophus ferrumequinum, Barbastelle, Myotis myotis
Cave wall and on stalagmites
Tortoise: Testudo graeca, Testudo mauritanica
Seasonality of tick observations (number of ticks) in Belgium
Co-occurrence of tick species in some sites raises the question of potential interactions with species recorded together on the same hosts , or their eggs found in the same shelter [43, 44]. Sites with high diversity of tick species might be hot spots of potential micro-organism exchanges. Indeed, although ticks specific, for example, to birds rarely bite humans, they might maintain a cycle of pathogens in their host populations. Those might be picked up by the generalist species I. ricinus, and passed onto humans [7, 45]. The possibility that co-occurring exotic and local species might facilitate establishment of exotic micro-organisms should be investigated.
Microorganisms associated to tick species
In addition to potential paralysis caused by the saliva of some female ticks, which seems very rare in Europe , the main impact of ticks on human health is through transmission of pathogens. Ticks acquire microorganisms through an infected meal or transovarial transmission. Micro-organisms recorded in ticks might come from a recent blood meal and presence in a tick does not mean that this tick species is a competent vector. For Ixodidae ticks feeding once per stage, the microorganisms need to survive molting and be transmitted to the next host while argasidae nymphs and adults bite repeatedly. Then, to be a pathogenic for humans, they must cause symptoms in humans. A list of 300 recorded micro-organism/tick associations is presented in Additional file 3. Some sources have a low reliability but this exhaustive list is a basis for systematic investigations and reliability of vector status and pathogenicity are compiled to propose priorities for investigations. Associations are recorded mostly outside Belgium as this was little investigated in the country. Notably, while mycoplasmas are increasingly related to ticks in the USA , and their prevalence is increasing throughout Europe [48, 49], there are no investigations of Mycoplasma in Belgian tick species in the literature.
Tick/micro-organism associations for which pathogenic status and vector status for human should be investigated as a priority: pathogens and suspected pathogens/tick species associations found abroad or in Belgium referenced in the literature for tick species found in Belgium
Coxiella, Franciscella Anaplasma
burgdorferi sensu stricto * , afzelii * , garinii *, lusitaniae valaisiana * , spielmanii *, sp bavariensis *, miyamotoi*,
venatorum * , divergens * , microti *
F. tularensis* A. phagocytophilum *
CCHF*, TBEV*, Louping Ill*
bovis, bigemina, rodhaini
prowazekii*, conorii * , slovaca*, monacensis*, felis*, massiliae*, typhi*, sp.
C. burnetii *
WNV*, Eyack*, Erve* Tettnang*, Tribec*, KEMV*
Bartonella henselae*, Serratia marcescens*, Staphylococcus aureus*, Candidatus Neoehrlichia mikurensis*, Toxoplasma gondii*, Pasteurella pneumotropica*, Chromobacterium violaceum*, Pseudomonas aeruginosa*, Diplorickettsia massilinsis
afzelii * , garinii * , turdi-like burgdorferi sensu lato,
Candidatus Neoehrlichia mikurensis*
burgdorferi sensu lato
C. burnetii* F. tularensis*
burgdorferi sensu lato
burgdorferi sensu stricto *, valaisiana *, spielmanii *, garinii *, afzelii *, lusitaniae , bavariensis*
conorii*, helvetica , sp.
A. phagocytophilum *
garinii * , valaisiana * afzelii * , burgdorferi sensu lato, spielmanii *
burgdorferi sensu stricto*, garinii*
burgdorferi sensu lato
Yersinia pestis (Plague) *
burgdorferi sensu lato, afzelii*, garinii*
C. burnetii*, F. tularensis* A. phagocytophilum*
Louping-ill*, TBEV*, CCHF*
burgdorferi sensu lato
slovaka*, canada*, conorii*, sp, helvetica*, raoultii*
F. tularensis* Francisella-like A. phagocytophilum *
burgdorferi sensu lato
Candidatus rickettsia kulagini, massiliae *, canis, felis*, rickettsi*, rhipicephali,
C. burnetii*, A. phagocytophilum*
Ehrlichia canis, Ehrlichia ewingii Hepatozoon canis, Salmonella bacteria, Batonella vinsonii, Rangelia vitalii, Dipetalonema dracunculoides, Mycoplasma haemocanis, Leishmania infantum
WNV*, TBEV*, NYMV, QRFV
burgdorferi sensu lato, borrelia sp
rabies*, IK (KTR),SOK
Wolbachia persica, Treponoma vespertilionis
Ecological traits influencing the potential vector role of tick species
The major vector I. ricinus – a generalist species
Secondary vectors I. hexagonus and D. reticulatus
I. hexagonus is a confirmed vector of B. burgdorferi s.l. with 28% prevalence recorded . It is a nidiculous species found in burrows and occasionally in caves . This reduces human vector contact but several characteristics must be highlighted: 1) human infestations were frequent during the war when people sheltered in underground sites during air raids  and I. hexagonus is considered a common parasite of man in Germany and the United Kingdom , 2) the species has a wide range of hosts such as hedgehogs, mustelids, foxes, polecat, badger, roe deer , as well as dogs and cats which can increase the spread of ticks and import ticks in gardens close to humans, 3) I. hexagonus is found in urban gardens , 4) most hedgehogs are infested  and the presence of ticks in their surface nests is a potential threat when gardening , 5) This species brings pathogens to people normally not at risk for tick bites (just gardening) and can remain undetected for a longer time, 6) it is active throughout the year , 7) because of B. burgdorferi s.l. transovarial transmission , this species could maintain a silent high rate of infection creating long term foci of high infection in the wildlife in areas where it acts as reservoir, 8) finally, Lyme borreliosis could be picked up by I. ricinus sharing the same host. In Belgium, I. hexagonus is widespread on cats and dogs  and has been observed on many mammals (Table 3), on humans , in nests, burrows, caves (sites 594, 617), house (site 200) and on grass (sites 492, 670). Populations might fluctuate between years . The species in Belgium carries all the pathogenic species of Borrelia burgdorferi s.l., A. phagocytophilum as well as the suspected pathogen R. helvetica.
D. reticulatus might be restricted to limited areas and not actively questing in the warm months when people are entering risky areas. D. reticulatus is reported on wild boar, cervids, dogs, horses and cats in the French Ardennes , wolves or rarely birds [27, 32, 43]. It can bite humans . Adults are captured by flagging but immatures are nidiculous. This species seems to be expanding its distribution in Europe. In Belgium, the tick has probably been present for some time with one specimen recorded on vegetation in 1950 (site 553), on a dog (site 567) and a human in the eighties (site 376). Established populations have only recently been monitored. Between 2007 and 2009, 16 out of 2297 ticks taken from 161 wild cervids  (WILDSCREEN collection) were D. reticulatus. From 2010 until March 2012, 150 additional D. reticulatus were discovered on 3 cervids in 6 sites including one confirmed by flagging (site 797). Confirmation of the species at a molecular level was carried out when sequences of the 646 bp of a part of the ITS2 gene were successfully obtained for 16 D. reticulatus. These 6 sites are in the Southeast but this tick is found on vegetation in the North (60, 130, 172, 535)  and on hosts in other locations .
Ticks parasite of birds
Birds probably carry ticks to most geographical locations but this does not mean that ticks will survive in these locations. The presence of all pathogenic species of B. burgdorferi s.l. in I. frontalis and I. arboricola in Belgium suggests a potential role in the Borrelia life cycle . Up to 50% of I. frontalis and also I. lividus were infected with B. burgdorferi s.l. in other countries. While seldom reported as biting humans, they might maintain the pathogen cycle in wildlife. I. frontalis (previously I. pari) is associated with a broad range of songbirds, including thrushes (Turdidae), the Great tit and the collared dove [7, 28, 43], with up to 30 specimens per bird . I. frontalis is occasionally collected by flagging  and evidence suggests that it might be more often present in under-storey vegetation than in nests . In Belgium it has been found on birds in 11 sites. I. arboricola is found mainly in Europe but was recorded in Egypt on birds coming back to Europe . It is a nidicolous tick infesting birds and bats . The Great tit might be the dominant host but heavy infestations occur on the Common starling and Peregrine falcon . In Belgium it was recorded in 10 places including 3 sites with 70 specimens (sites 233, 252, 337) where the species was actively surveyed. Specimens were found on birds (Table 3) and in nests of the House martin. I. lividus is found on the Sand martin and in their nests . Experimental records showed that these ticks were collected on the Great tit  and it was found repeatedly in nests of the House martin in Japan .
Ticks parasite of rodents and small mammals
Small mammals and particularly rodents are reservoirs of many diseases, but few studies have targeted ticks on rodents in Belgium. Next to I. ricinus and I. hexagonus, ticks present on rodents and small mammals include I. canisuga, I. trianguliceps and I. acuminatus. These species are carriers of some pathogens (Table 5) including B. burgdorferi s.l.[76–78] with 30% prevalence for I. canisuga in Spain . I. canisuga is part of a group of species difficult to discriminate morphologically (including I. hexagonus, I. arboricola and I. lividus) . I. canisuga is widely distributed and found on half of the foxes in Northern France  but also on polecats, weasels, badgers, Eurasian owls, dogs and cats [79, 80] with up to 200 specimens reported on one dog . In Great Britain, 11% of the ticks found on dogs were I. canisuga but none were reported in a Belgian survey . This nidiculous species is found in nests, burrows or rarely in caves  with fed females climbing upwards in crevices above ground . In Belgium, only two specimens were found, on a polecat (site 132) and a nest (site 207). I. trianguliceps is found almost exclusively on micromammals including shrews and rodents, exceptionally on moles, birds or goats and very rarely on humans [27, 55]. The tick is nidiculous but may wait for hosts on the soil surface . It is commonly found in wet biotopes including moorlands, meadows, or pine, deciduous and birch forests . In France, immature are found with immature of D. reticulatus, I. acuminatus, and I. ricinus on the same rodents [84, 85]. In Belgium, I. trianguliceps is probably frequent and found on rodents in 8 sites. I. acuminatus parasitizes small mammals, birds and sometimes humans and is mostly found in nests and burrows . Only one specimen was found in Belgium on a wood mouse (site 630).
Other tick species sharing habitats with humans
Three tick species are not frequent but bite humans and can establish populations inside houses, making them a potential threat. Rhipicephalus sanguineus is a tropical tick imported on dogs or rarely with hares, cattles, horses, or plants . The tick cannot survive outside but multiplies inside houses and dog kennels . Ticks hunt for hosts by moving actively , can drink free water and survive for years inside. This was shown to cause house infestations in 12 cities in the Netherlands, in Switzerland  and 334 foci in Berlin . Tick populations can build up in some years from one engorged female to thousands of ticks and eggs [87, 89, 90]. Eggs are hidden in cracks and crevices and ticks crawl around. Mean temperature probably limits its northward distribution . This species is rarely found on humans , but seems to more willingly bite humans occasionally, representing at times up to 7% of ticks biting men . Up to 22 ticks on one man were reported in France . Some studies suggest that this highlights a change of behaviour related to temperature increase [94, 95] but this needs to be further investigated. R. sanguineus is a vector of highly pathogenic Rickettsiae conorii with confirmed transovarial passage . Prevalence in nymphs infesting houses can reach up to 40% , against usually 1%  outside. In Belgium, R. sanguineus was found in houses in Antwerp  (site 210), Hoboken (site 199)  and Maldegem (site 71), but also on dogs with a travel history (e.g. sites 338, 426, 536, 684)  and on humans (site 210) .
Argas reflexus is frequent mainly on pigeons but readily bites humans, chickens or horses in buildings in the absence of pigeons [43, 55]. With Argas vespertilionis (see below) this species belongs to the Argasidae family, which differs from Ixodidae in their feeding habits. Ticks take many short meals. Nymphs and adults engorge in less than an hour. Ticks feed on eight to twelve hosts per life cycle and spend most of their life in the hosts’ habitat . Building infestations are undetected for years because of nocturnal host-seeking behaviour, high host specificity and short meals . However, when pigeons are eradicated, A. reflexus appear seeking for alternative hosts . Even if the build-up of a large number of ticks takes years, thousands of ticks were found repeatedly when investigating 188 infested buildings in Germany . Searching for ticks before renovating is now a current recommendation in Germany. Particularities include a long lifetime of up to 9 years without food, low water loss rate, absorption of water vapour at 75% relative humidity and high tolerance of temperature extremes. Movements are restricted to periods of host-seeking, the remaining time being spent resting aggregated in cracks of walls [97–99]. In Belgium ticks were recorded in 7 sites from pigeons, pigeon houses, houses and flats. The bites may cause allergy, anaphylactic shock or loss of consciousness . It is an unconfirmed vector of human pathogens.
Argas vespertilionis parasitizes bats . They stay the whole year in or near caves or other shelters (roofs of houses), the hosts being present or not. Eggs were found together with eggs of I. hexagonus and I. vespertilionis[43, 44]. Ticks bite alternative hosts in the absence of their usual host and readily bite man. People reported being bitten in caves or in their bed when bats are in the attics . Larvae attach for 19 days. Nymphs and adults feed in less than one hour . They take many small meals on many hosts potentially accumulating pathogens. A. vespertilionis causes irritating bites on humans and viable strains of C. burnetii were isolated from ticks which had been dead for a year . While 84% of museum specimens tested positive for B. burgdorferi s.l. in the UK , this might reflect sample contamination. Borrelia sp. organisms related to Borrelia recurrentis, B. duttonii and B. crocidurae were present in numbers in a dying bat in the UK  parasitized by A. vespertilionis. In Belgium, 11 ticks were found on hosts in four locations.
Species of little interest for human health
Ixodes vespertilionis was never recorded biting man. It parasites the Lesser horseshoe and the Great bats. It actively searches for hosts by walking slowly on very long legs in caves. It is restricted to the darkest part of the caves, offering 100% humidity [28, 102]. Decrease of humidity to 61% increases tick activity until they die after a few hours. All stages are mainly found in caves, moving away with the host but coming back for molting and egg laying . Specimens are not on the ground but on walls and roof crevices. In West France low densities are present in most caves. Ticks were found in caves or on bats in 10 sites in East Belgium .
Main findings and suggestions for further research priorities
Suggestions for future research priorities
• The current national list of occurring tick species (not previously available)
• Search for tick species recorded in neighbouring countries country (targeting prefered host species or habitat)
• A first distribution map for Ixodes ricinus based on occurrences which highlights presence of the species in all the provinces
• Build up a distribution model for exophilic species such as Ixodes ricinus and Dermacentor reticulatus based on habitat preferences and distribution of other influencing species
• Current very partial knowledge of distribution for the other tick species
• Build up a distribution model for nidiculous species based on distribution of major host species
• Perform a systematic tick survey across the country
Tick hosts/ reservoirs
• Provide for each tick a list of hosts on which they have been recorded in the country
• For each local vertebrate species check potential host status for each tick species or potential influence on tick population
• Map the distribution of relevant species
Presence of pathogens
• Potential presence of pathogens such as Borrelia burgdoferi s.l. in many tick species
• Check the pathogenicity of each micro-organisms species
• List of microorganisms potentially present locally or aborad in local ticks species
• For pathogenic microorganisms check vector status of associated ticks Identify presence of potential reservoirs for pathogens (tick/ hosts)
• List of tick/ micro-organisms associations
• Investigate pathogen distribution across species to better comprehend
• risk before modelling risk map
• First map of (suspected) pathogens found in ticks
• Search for additional pathogens in ticks of the country
• Make a pathogen distribution map (found in ticks, hosts, reservoirs)
• Use public knowledge from nature defense group, scouts, veterinary, general practitioner to localise and quantify tick bites
Tick-borne diseases risk map
• Some hot spot with highest I. ricinus abundance are highlighted but because of unreliable sampling those should be further investigated
• Investigate presence and prevalence of pathogenic species
• Make a countrywide standardised survey to allow comparing abundance between sites.
• In a given area, what is the probability 1) to get a tick bite, 2) that this tick was infected with pathogens 3) infected by which pathogen(s)
I. ricinus is the main vector of diseases in Belgium because it is present in most vegetated areas, carries many pathogens and is responsible for most tick bites in humans. Its distribution highlights the possibility of becoming infected by the pathogenic agent of Lyme borreliosis in any province. Other species might play a role by maintaining pathogens present in wildlife, or by bringing pathogens closer to people in their houses and gardens. While the number of bites on humans caused by other species is less than by I. ricinus, occurrence of such an event in unexpected areas such as houses or gardens or during the winter season extends the risk to people not considered to be at risk and increases the probability of a tick bite being ignored. Some places seem to pose a greater risk with more abundant tick populations, higher diversity of pathogens or both, but this should be confirmed. Current prevention measures target B. burgdorferi s.l. mainly through deticking. Other pathogens are increasingly investigated and found in domestic animals, wildlife or humans and transmission of some of those can occur at the time of the tick bite without delay (e.g. TBEV). Avoidance behaviour should be promoted such as avoiding areas with ferns , wearing boots and long trousers or repellent, using deticking as the second line measure. Another reason to avoid ticks is that in Belgium only 30% of Lyme patients remember a bite and 35% never develop Erythema migrans. Lyme disease can be difficult to diagnose in the absence of Erythema migrans and particularly if additional symptoms are caused by co-occurring pathogens.
The analysis of the presence of pathogens in ticks might be easier than in human blood as organisms are more easily detected by PCR in ticks than in blood. Systematic surveys using ticks as sentinels could assess the prevalence of the pathogens in wildlife. Geolocation of tick and pathogen records allows integration into a more general databases such as those developed in the framework of The Vbornet  or the TICK MAP initiative  and could help fulfil the empty maps for tick and tick-borne disease occurrence in Belgium [4, 6]. This study based on imperfect sampling data calls for an increased surveillance of ticks and tick-borne species at a detailed spatial scale as well as clarification of local vector status for tick species and pathogens which occur in these species. A systematic survey of ticks and associated pathogens is called for in Europe, as well as better characterisation of species interaction in the ecology of tick-borne diseases.
Association Régionale de Santé et d’Identification Animale
Basic Local Alignment Search Tool
Crimean Congo Hemorrhagic Fever virus
Dierengezonheidzorg Animal Health Care Flanders Belgium
deoxy ribonucleotide triphosphate
Issuk Kul virus
Institut pour l′encouragement de la recherche dans l′industrie et l′agriculture
Institut Royal des Sciences Naturelles de Belgique
second Internal Transcribed Spacer 2
Looping Ill virus
Omsk Hemorragic fever virus
Polymerase Chain Reaction
Reference Laboratory for Vector Borne Disease
Tick-borne Encephalitis virus
University of Antwerp collection
- UGENT FOREST:
Ghent University, Forestry department collection
- UGENT VETE:
Ghent University, Faculty of Veterinary Medicine
Université Catholique de Louvain Clinical and experimental research institute
Network for disease surveillance in wildlife
West Nyle virus.
Many thanks to Adrien Nahayo and other collaborators of the WILDSCREEN network for monitoring of diseases in wildlife and for their time and effort in collecting ticks. The authors would also like to thank Philippe Martin from the Saint-Luc hospital in Bouge Belgium, Thomas Kesteman from the UCL IREC Institute, the staff of the Royal Institute for Natural Sciences of Belgium (IRSNB) including Georges Wauthy and Léon Baert, the staff of GlaxoSmithKline including Yves Lobet and Pierre Voet for providing fresh records or additional details on their published records. The authors are grateful to the nature organisation NATAGORA and NATUURPUNT and particularly Wouter Vanreusel, Marc Herremans, Karin Gielen, Jean-Yves Paquet and Antoine Derouaux for providing details and numerous records of tick location. Thanks to Sophie Vanwambeke, Eva De Clercq, Sen li and Nienke Harteminck for support and raw literature. Thanks to BAYER for accepting to share their records for our research. Many thanks to the Belgian Sciences Policy Office for funding this work through the STEREO II project for Earth Observation (MULTITICK project).
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