An experimental test to compare potential and realised specificity in ticks with different ecologies

The majority of studies on ecological specialisation rely on data reflecting realised specificity, without considering species’ potential specificity. Most species of ticks, a large family of hematophagous ectoparasites, have a narrow host range in nature, but it is unclear whether this is due to host-driven adaptations or other processes (such as off-host abiotic environment). We investigated the potential specificity of two tick species with contrasting ecology by infesting three avian host species that occur in the same off-host macrohabitat but are unequally infested by the ticks in nature (i.e. have contrasting realised specificity). The endophilic specialist tick Ixodes arboricola resides inside the hosts’ nest and has high realised host specificity, whereas the exophilic generalist tick I. ricinus encounters hosts in the field and has very low realised specificity. As hosts, we used great tits (frequently infested by both tick species), blackbirds (frequently infested by I. ricinus but never by I. arboricola) and great spotted woodpeckers (no ticks of either species have been reported). If realised specificity is constrained by host-driven adaptations there should be no differences between potential and realised specificity, whereas if realised specificity is constrained by other processes potential specificity and realised specificity should be different. We found that attachment rates and weight during feeding of I. arboricola were lower on blackbirds than on great tits, whereas there were no such differences for I. ricinus. No ticks of either species attached to woodpeckers. These results indicate that realised host specificity of ticks is, at least partially, constrained by host-driven adaptations. This specificity therefore strongly depends on the ticks’ encounter rates with particular host types, which are affected by the ticks’ off-host ecological requirements, behaviour and life-history characteristics.     

Experiments on the transmission of Babesia divergens to cattle by the tick Ixodes ricinus

A modification of the method of rearing Ixodes ricinus gave a successful method of producing and reliably rearing adequate numbers of this tick for experimental work.Experiments on transmission of Babesia divergens by I. ricinus showed that infections could be initiated only in the adult stage of the tick. Whilst all stages of the F₁ generation of an infected female could transmit infection, larvae and nymphs could not acquire it. Infection persisted throughout the F₁ generation and sometimes up to the F₂ larval stage even when the ticks were maintained on hosts not susceptible to B. divergens. Both parasitaemic and premune carrier hosts were infective to ticks. A single infected adult or nymph could transmit infection.     

Population regulation in ticks: the role of acquired resistance in natural and unnatural hosts

Attachment, engorgement and subsequent development of successive infestations of Ixodes trianguliceps larvae and nymphs on natural hosts, Apodemus sylvaticus, and unnatural hosts, laboratory mice, are compared. In laboratory mice, primary infestations above a threshold level of about 10 ticks elicit an immunological response which reduces, in a density-dependent manner, the rate of successful tick engorgement during subsequent infestations. In contrast, in A. sylvaticus successive infestations of larvae result in unchanged or slightly improved survival through to nymphs. The relevance of these results to the concept of host-parasite co-evolution and to tick population regulation is discussed.     

Monitoring the diel activity of Ixodes ricinus ticks in Hungary over three seasons

Ixodes ricinus is the most common tick species in Europe and vector of many diseases of humans. The risk of contracting such a disease is influenced by many factors, but one of the crucial points is questing activity of unfed ticks. In order to supplement the few literature data on patterns of diel activity of this tick species and to examine the correlations between data on diel activity of ticks and their small mammal hosts and some meteorological variables, a survey was performed. Diel activity of questing I. ricinus and small rodents was studied in a known natural tick-borne encephalitis virus focus over 7 months at one sampling day monthly. 1,063 I. ricinus ticks and 25 rodents were sampled. Air temperature and humidity data were also recorded in the 24 study plots at time of sampling. From April to October questing activity of nymphs increased in the 3-h-period after sunrise, comparing to activity of the 3 h before sunrise. Proportion of nymphs sampled 3 h after sunset compared to total sampled nymphs 3 h before and 3 h after sunset showed correlation to activity of rodents. In the period of April–July both nymphs and larvae showed stronger activity from sunrise to sunset, this turned to dominant nighttime activity in August–September, whereas activity changed to equal in day and night in October. Our results indicate that natural light and rodent population have positive effect on questing activity of I. ricinus.     

Tick infestation of small mammals in an English woodland

Tick infestations on small mammals were studied from April to November, 2010, in deciduous woodland in southern England in order to determine whether co‐infestations with tick stages occurred on small mammals, a key requirement for endemic transmission of tick‐borne encephalitis virus (TBEV). A total of 217 small mammals was trapped over 1,760 trap nights. Yellow‐necked mice (Apodemus flavicollis) made up the majority (52.5%) of animals, followed by wood mice (A. sylvaticus) 35.5% and bank voles (Myodes glareolus) 12%. A total of 970 ticks was collected from 169 infested animals; 96% of ticks were Ixodes ricinus and 3% I. trianguliceps. Over 98% of ticks were larval stages. Mean infestation intensities of I. ricinus were significantly higher on A. flavicollis (6.53 ± 0.67) than on A. sylvaticus (4.96 ± 0.92) and M. glareolus (3.25 ± 0.53). Infestations with I. ricinus were significantly higher in August than in any other month. Co‐infestations with I. ricinus nymphs and larvae were observed on six (3.6%) infested individuals, and fifteen small mammals (8.9%) supported I. ricinus – I. trianguliceps co‐infestations. This work contributes further to our understanding of European small mammal hosts that maintain tick populations and their associated pathogens, and indicates that co‐infestation of larvae and nymph ticks does occur in lowland UK. The possible implications for transmission of tick‐borne encephalitis virus between UK ticks and small mammals are discussed.     

Infestation of urban populations of the Northern white‐breasted hedgehog,Erinaceus roumanicus,by Ixodes spp. ticks in Poland

Infestation by the nest‐dwelling Ixodes hexagonus Leach and the exophilic Ixodes ricinus (Linnaeus) (Ixodida: Ixodidae) on the Northern white‐breasted hedgehog, Erinaceus roumanicus (Erinaceomorpha: Erinaceidae), was investigated during a 4‐year study in residential areas of the city of Poznań, west‐central Poland. Of 341 hedgehogs, 303 (88.9%) hosted 10 061 Ixodes spp. ticks encompassing all parasitic life stages (larvae, nymphs, females). Ixodes hexagonus accounted for 73% and I. ricinus for 27% of the collected ticks. Male hedgehogs carried significantly higher tick burdens than females. Analyses of seasonal prevalence and abundance of I. hexagonus revealed relatively stable levels of infestation of all parasitic stages, with a modest summer peak in tick abundance noted only on male hosts. By contrast, I. ricinus females and nymphs peaked in spring and declined steadily thereafter in summer and autumn, whereas the less abundant larvae peaked in summer. This is the first longterm study to evaluate the seasonal dynamics of both tick species on populations of wild hedgehogs inhabiting urban residential areas.     

The role of deer as vehicles to move ticks, Ixodes ricinus, between contrasting habitats

In Europe the most important hosts maintaining Ixodes ricinus tick populations are deer. Therefore, excluding deer by fencing or culling are potential tick management tools. Here we test the hypothesis that deer act as vehicles for moving ticks between two distinct habitats: forest and open heather moorland. We utilised an ideal “natural experiment” whereby forests were either fenced or unfenced to prevent or allow deer to move between habitats. We aimed to test the hypothesis that deer cause a net movement of ticks from high tick density areas, i.e. forests, to low tick density areas, i.e. open moorland. We recorded I. ricinus and host abundance in 10 unfenced and seven fenced forests and their respective surrounding heather moorland. We found that fenced forests had fewer deer and fewer I. ricinus nymphs than unfenced forests. However, we found no evidence that fencing forests reduced I. ricinus abundance on adjacent heather moorland. Thus there was insufficient evidence for our hypothesis that deer cause a net movement of ticks from forest onto adjacent moorland. However, we found that deer abundance generally correlates with I. ricinus abundance. We conclude that fencing can be used as a tool to reduce ticks and disease risk in forests, but that fencing forests is unlikely to reduce ticks or disease risk on adjacent moorland. Instead, reducing deer numbers could be a potential tool to reduce tick abundance with implications for disease mitigation.     

Introduced Siberian chipmunks are more heavily infested by ixodid ticks than are native bank voles in a suburban forest in France

By serving as hosts for native vectors, introduced species can surpass native hosts in their role as major reservoirs of local pathogens. During a 4-year longitudinal study, we investigated factors that affected infestation by ixodid ticks on both introduced Siberian chipmunks Tamias sibiricus barberi and native bank voles Myodes glareolus in a suburban forest (Forêt de Sénart, Ile-de-France). Ticks were counted on adult bank voles and on adult and young chipmunks using regular monthly trapping sessions, and questing ticks were quantified by dragging. At the summer peak of questing Ixodes ricinus availability, the average tick load was 27-69 times greater on adult chipmunks than on adult voles, while average biomass per hectare of chipmunks and voles were similar. In adult chipmunks, individual effects significantly explained 31% and 24% of the total variance of tick larvae and nymph burdens, respectively. Male adult chipmunks harboured significantly more larvae and nymphs than adult females, and than juveniles born in spring and in summer. The higher tick loads, and more specifically the ratio of nymphs over larvae, observed in chipmunks may be caused by a higher predisposition - both in terms of susceptibility and exposure - to questing ticks. Tick burdens were also related to habitat and seasonal variation in age- and sex-related space use by both rodents. Introduced chipmunks may thus have an important role in the dynamics of local vector-borne pathogens compared with native reservoir hosts such as bank voles.     

Being a parasitoid of parasites: host finding in the tick wasp Ixodiphagus hookeri by odours from mammals

The parasitic wasp Ixodiphagus hookeri Howard (Hymenoptera: Encyrtidae) parasitizes larvae and nymphs of a number of tick species worldwide. Ticks themselves are parasitic on vertebrate hosts. To study the specificity and reliability of vertebrate odours used by I. hookeri for host location, we conducted bioassays in a four‐chamber olfactometer. Wasps were arrested by carbon dioxide and by odours from roe deer faeces and odours from hair of roe deer and wild boar. Odours from faeces of cattle, rabbit, and field mouse as well as odours from hair of cattle and field mouse had no effect. Odours from faeces of the host tick species Ixodes ricinus L. (Acari: Ixodidae) were attractive only up to a distance of 1 cm. Thus, I. hookeri reacts to general (carbon dioxide) and specific vertebrate odours from wild boar and deer. Examination of freshly shot specimens demonstrates that deer and wild boars are infested with a sufficient number of tick nymphs to tap the full reproductive potential of an I. hookeri female, which makes cues from these mammal species reliable. These results indicate that I. hookeri locates its hosts using specific and reliable mammal odours and that ticks are parasitized on their vertebrate hosts. The implications of this host‐finding strategy and its benefits for the parasitoid are discussed.     

Relative Importance of Ixodes ricinus and Ixodes trianguliceps as Vectors for Anaplasma phagocytophilum and Babesia microti in Field Vole (Microtus agrestis) Populations

The importance of Ixodes ricinus in the transmission of tick-borne pathogens is well recognized in the United Kingdom and across Europe. However, the role of coexisting Ixodes species, such as the widely distributed species Ixodes trianguliceps, as alternative vectors for these pathogens has received little attention. This study aimed to assess the relative importance of I. ricinus and I. trianguliceps in the transmission of Anaplasma phagocytophilum and Babesia microti among United Kingdom field voles (Microtus agrestis), which serve as reservoir hosts for both pathogens. While all instars of I. trianguliceps feed exclusively on small mammals, I. ricinus adults feed primarily on larger hosts such as deer. The abundance of both tick species and pathogen infection prevalence in field voles were monitored at sites surrounded with fencing that excluded deer and at sites where deer were free to roam. As expected, fencing significantly reduced the larval burden of I. ricinus on field voles and the abundance of questing nymphs, but the larval burden of I. trianguliceps was not significantly affected. The prevalence of A. phagocytophilum and B. microti infections was not significantly affected by the presence of fencing, suggesting that I. trianguliceps is their principal vector. The prevalence of nymphal and adult ticks on field voles was also unaffected, indicating that relatively few non-larval I. ricinus ticks feed upon field voles. This study provides compelling evidence for the importance of I. trianguliceps in maintaining these enzootic tick-borne infections, while highlighting the potential for such infections to escape into alternative hosts via I. ricinus.     

Ixodes ricinus parasitism of birds increases at higher winter temperatures

Increasing winter temperatures are expected to cause seasonal activity of Ixodes ricinus ticks to extend further into the winter. We caught birds during winter months (November to February) at a site in the west of Scotland over a period of 24 years (1993–1994 to 2016–2017) to quantify numbers of attached I. ricinus and to relate these to monthly mean temperature. No adult ticks were found on any of the 21,731 bird captures, but 946 larvae and nymphs were found, with ticks present in all winter months, on 16 different species of bird hosts. All ticks identified to species were I. ricinus. I. ricinus are now active throughout the year in this area providing temperature permits. No I. ricinus were present in seven out of eight months when the mean temperature was below 3.5º C. Numbers of I. ricinus attached to birds increased rapidly with mean monthly temperatures above 7º C. Winter temperatures in Scotland have been above the long‐term average in most years in the last two decades, and this is likely to increase risk of tick‐borne disease.     

Resistance in cattle to Haemaphysalis (Kaiseriana) longicornis

Samples of each instar of the 3-host tick, Haemaphysalis (Kaiseriana) longicornis were collected from grazing Bos taurus cattle to investigate their survival on hosts with previous exposure to the tick and on previously unexposed ‘naive’ hosts. The ticks were allocated to categories based on their size to observe at what stage of development mortality occurred. Analysis of the age structure of the ticks showed that small but variable proportions of larvae, nymphs and females matured on previously exposed hosts and larger proportions on the naive hosts. This suggests that cattle acquire and express different levels of resistance against each instar of the tick. The technique used has potential for estimating levels of resistance of hosts to 3-host ticks under field conditions.     

Entomopathogenic fungi associated with Ixodes ricinus ticks

The objective of this study was to demonstrate the occurrence of entomopathogenic fungi on Ixodes ricinus ticks in relation to the tick stage, engorgement and season. Ticks were collected from the vegetation, from small rodents and from deer. All entomopathogenic fungi found belonged to the Hyphomycetes. Paecilomyces farinosus and Verticillium lecanii were the predominant species. Other species, found only on engorged females were: Beauveria bassiana, B. brongniartii, P. fumosoroseus and V. aranearum. Eight out of 1833 ticks collected from the vegetation and three out of 269 engorged nymphs were infected with fungi. Thirty-three out of 149 engorged females were infected, whereas males and engorged larvae were not infected. Throughout the season, a significantly higher proportion of ticks collected in autumn were infected. Entomopathogenic fungi may have a significant impact on the size of the I. ricinus population, since females were the most frequently infected stage.     

The effect of inflammatory and hypersensitive reactions,in response to the feeding of the tick Amblyomma variegatum,on the progression of experimental dermatophilosis infections

Initial infestations of Amblyomma variegatum larvae and nymphs, on rabbits and sheep respectively, produced inflammatory reactions in the host's skin; repeated infestations resulted in an increase in development of delayed type hypersensitive reactions. Dermatophilus congolensis cocci were applied in titrated doses to hosts at sites of inflammatory or hypersensitive reactions to ticks, and to control hosts with no exposure to ticks. We assessed the resulting infections for three weeks and found no significant difference between the infections on the three groups. We conclude that the local effects of the feeding of immature stages of this tick do not influence the pathogenesis of dermatophilosis.     

Interstadial and Infestation Level-dependent Variation in the Transmission Efficiency of Borrelia Burgdorferi from Mice to Ixodes Ricinus Ticks

The efficiency with which the spirochaete Borrelia burgdorferi sensu stricto was transmitted from laboratory mice to larval and nymphal Ixodes ricinus ticks was assessed, using the polymerase chain reaction. The transmission efficiency to nymphs was significantly greater than to larvae when both fed together on the same host. Increased tick infestation levels of mice were correlated with significantly greater engorgement weights and higher B. burgdorferi transmission coefficients from mice to nymphs. These observations indicate that both the feeding success of ticks and the transmission coefficients from host to tick may be influenced by the tick infestation level of an infected host. The infestation level and the relative numbers of each life stage of the tick are factors which should be considered in the design of transmission experiments.     

The importance of passerine birds as tick hosts and in the transmission of Borrelia burgdorferi,the agent of Lyme disease: a case study from Scotland

Borrelia burgdorferi sensu lato (s.l.) is the causative agent of Lyme borreliosis, the most common tick‐borne zoonosis of humans in Europe and North America. Here, we assessed the relative importance of different passerine bird species as tick hosts and their contribution to the B. burgdorferi s.l. transmission cycle in a rural residential area in Scotland. We caught 1229 birds of 22 species during the tick‐questing season. On average, 29% carried larval ticks (0.8 larvae per individual) and 5% carried nymph ticks (0.06 nymphs per individual). All attached ticks tested were Ixodes ricinus. Using a nested‐PCR, we found that 20% of nymphs tested positive to B. burgdorferi s.l. and all these were of the genospecies Borrelia garinii. We identified two new bird species carrying infected nymphs: Eurasian Siskin Carduelis spinus and European Greenfinch Carduelis chloris. Ground‐foraging species were more important than arboreal species in hosting I. ricinus nymphs and B. burgdorferi s.l. Common Blackbirds Turdus merula were the most common hosts, with Song Thrushes Turdus philomelos, Dunnocks Prunella modularis, European Greenfinches and Chaffinches Fringilla coelebs also hosting high rates of infection.     

Vector competence of the tick Ixodes ricinus for transmission of Bartonella birtlesii

Bartonella spp. are facultative intracellular vector-borne bacteria associated with several emerging diseases in humans and animals all over the world. The potential for involvement of ticks in transmission of Bartonella spp. has been heartily debated for many years. However, most of the data supporting bartonellae transmission by ticks come from molecular and serological epidemiological surveys in humans and animals providing only indirect evidences without a direct proof of tick vector competence for transmission of bartonellae. We used a murine model to assess the vector competence of Ixodes ricinus for Bartonella birtlesii. Larval and nymphal I. ricinus were fed on a B. birtlesii-infected mouse. The nymphs successfully transmitted B. birtlesii to naïve mice as bacteria were recovered from both the mouse blood and liver at seven and 16 days after tick bites. The female adults successfully emitted the bacteria into uninfected blood after three or more days of tick attachment, when fed via membrane feeding system. Histochemical staining showed the presence of bacteria in salivary glands and muscle tissues of partially engorged adult ticks, which had molted from the infected nymphs. These results confirm the vector competence of I. ricinus for B. birtlesii and represent the first in vivo demonstration of a Bartonella sp. transmission by ticks. Consequently, bartonelloses should be now included in the differential diagnosis for patients exposed to tick bites.