Forecasting next season’s <Emphasis Type="Italic">Ixodes ricinus</Emphasis> nymphal density: the example of southern Germany 2018

The castor bean tick, Ixodes ricinus (L.) (Ixodida: Ixodidae), is the principal vector of pathogens causing tick-borne encephalitis or Lyme borreliosis in Europe. It is therefore of general interest to make an estimate of the density of I. ricinus for the whole year at the beginning of the tick season. There are two necessary conditions for making a successful prediction: a long homogeneous time series of observed tick density and a clear biological relationship between environmental predictors and tick density. A 9-year time series covering the period 2009–2017 of nymphal I. ricinus flagged at monthly intervals in southern Germany has been used. With the hypothesis that I. ricinus density is triggered by the fructification of the European beech 2 years before, the mean annual temperature of the previous year, and the current mean winter temperature (December–February), a forecast of the annual nymphal tick density has been made. Therefore, a Poisson regression model was generated resulting in an explained variance of 93.4% and an error of \(\hbox {RMSE} = 21\) ticks per \(100\,\hbox {m}^2\) (annual \(\hbox {MEAN} = 260\) collected ticks/\(100\,\hbox {m}^2\)). An independent verification of the forecast for the year 2017 resulted in 187 predicted versus 180 observed nymphs per \(100\,\hbox {m}^2\). For the year 2018 a relatively high number of 443 questing I. ricinus nymphs per \(100\,\hbox {m}^2\) is forecasted, i.e., a “good” tick year.     

Influence of selected meteorological variables on the questing activity of Ixodes ricinus ticks in Lower Silesia,SW Poland

The relationship between climate data and tick questing activity is crucial for estimation of the spatial and temporal distribution of the risk of ticks and tick‐borne diseases. This study establishes correlations between selected meteorological variables provided by the Weather Research and Forecasting model (WRF) and the questing activity of Ixodes ricinus nymphs and adults on a regional scale across Lower Silesia, Poland. Application of Generalized Linear Mixed Models (GLMM), built separately for adults and nymphs, showed that solar radiation, air temperature, and saturation deficit appeared to be the meteorological variables of prime importance, whereas the wind speed was less important. However, the effect of meteorological parameters was different for adults and nymphs. The adults are also more influenced by forest cover and the percentage of forest type if compared to nymphs. The WRF model providing meteorological variables separately for each location and day of tick sampling can be useful in studies of questing activity of ticks on a regional scale.     

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.     

Activity periods and questing behavior of the seabird tick Ixodes uriae (Acari: Ixodidae) on Gull Island, Newfoundland: the role of puffin chicks

Questing behavior of Ixodes uriae and their associated seasonal, host-feeding patterns are crucial to our understanding of tick life history strategies and the ecology of diseases that they transmit. Consequently, we quantified questing behavior of nymphs and adult female I. uriae ticks at Gull Island, a seabird colony in Newfoundland, Canada, to examine seasonal variation of off-host and on-host tick activity. We sampled a total of 133 adult Atlantic puffins (Fratercula arctica), 152 puffin chicks, and 145 herring gull (Larus argentatus) chicks for ticks during the breeding seasons of 2004 and 2005. Questing ticks were sampled by dragging a white flannel cloth across the grassy breeding areas during the mo of May, June, July, and August. Nymph questing activity reached a peak during mid-July (79 and 110 individuals/hr in 2004 and 2005, respectively). The prevalence of nymphs and adult female ticks on different seabird hosts varied between years and during the seasons. Puffin chicks had the highest prevalence (above 70% in July) of nymphs in both years and this was correlated with questing activity. Female ticks rarely fed on puffin chicks, but were prevalent on adult puffins and gulls, although prevalence and questing of ticks were not correlated in these hosts. These patterns of off-host and on-host tick activity suggests that I. uriae ticks likely use a combination of questing and passive waiting, e.g., in puffin burrows, to detect hosts, depending on the tick stage and the host species.     

Ticks in the ecotone: the impact of agri-environment field margins on the presence and intensity of Ixodes ricinus ticks (Acari: Ixodidae) in farmland in southern England

The present study aimed to assess whether agri-environment field margins provide a habitat for the sheep/deer tick Ixodes ricinus. Field studies were conducted in arable farmland in southern England in both extant and newly constructed field margins. The presence and intensity (i.e. the mean number of nymphs per transect, excluding zeros) of questing nymphs and adult I. ricinus were compared between field margins with three adjacent habitats: woodland, hedgerow and arable land. The presence and intensity of ticks within a field margin was also compared between three ecozones: the ecotone, the margin and the crop. It was found that field margins do support I. ricinus, although the intensity of ticks was associated with field margins with adjacent woodland, with a higher tick intensity along the ecotonal ecozone, compared with the rest of the margin or the crop edge. The presence of a hedge also increased the likelihood of finding questing nymphs in a field margin compared with a margin adjacent to arable land. This effect, however, was less pronounced than in field margins with adjacent woodland. The provision of footpaths within the margin (at least 1–2 m from the ecotone), or on the edge of the crop where paths run next to woodland known to be an important tick habitat, could be promoted to minimize tick exposure. In addition, based on the results of the present study, raising awareness that walking alongside woodlands also constitutes a tick risk could be promoted.     

Comparison of tick-borne microorganism communities in Ixodes spp. of the Ixodes ricinus species complex at distinct geographical regions

Characterizing the tick-borne microorganism communities of Ixodes ricinus (sheep tick) and Ixodes persulcatus (taiga tick) from the I. ricinus species complex in distinct geographical regions of Eastern Europe and European Russia, we demonstrated differences between the two ticks. Taiga ticks were more frequently mono- and co-infected than sheep ticks: 24.4 % (45/184 tested ticks) versus 17.5 % (52/297) and 4.3 % (8/184) versus 3.4 % (10/297), respectively. Ginsberg co-infection index values were significant at the various sites. Diversity of the tick-borne microorganism communities was estimated by the Shannon index, reaching values of 1.71 ± 0.46 and 1.20 ± 0.15 at the sheep-tick and the taiga-tick harbored sites, respectively. Richness of the tick-borne microorganism community in the sheep tick collection sites was about twice the value of the taiga tick collection sites. Future investigations are warranted to further characterize the peculiarities of the tick-borne microorganism communities among the ticks of the Ixodes ricinus complex.     

Climate of origin affects tick (Ixodes ricinus) host-seeking behavior in response to temperature: implications for resilience to climate change?

Climate warming is changing distributions and phenologies of many organisms and may also impact on vectors of disease-causing pathogens. In Europe, the tick Ixodes ricinus is the primary vector of medically important pathogens (e.g., Borrelia burgdorferi sensu lato, the causative agent of Lyme borreliosis). How might climate change affect I. ricinus host-seeking behavior (questing)? We hypothesize that, in order to maximize survival, I. ricinus have adapted their questing in response to temperature in accordance with local climates. We predicted that ticks from cooler climates quest at cooler temperatures than those from warmer climates. This would suggest that I. ricinus can adapt and therefore have the potential to be resilient to climate change. I. ricinus were collected from a cline of climates using a latitudinal gradient (northeast Scotland, North Wales, South England, and central France). Under laboratory conditions, ticks were subjected to temperature increases of 1°C per day, from 6 to 15°C. The proportion of ticks questing was recorded five times per temperature (i.e., per day). The theoretical potential to quest was then estimated for each population over the year for future climate change projections. As predicted, more ticks from cooler climates quested at lower temperatures than did ticks from warmer climates. The proportion of ticks questing was strongly associated with key climate parameters from each location. Our projections, based on temperature alone, suggested that populations could advance their activity season by a month under climate change, which has implications for exposure periods of hosts to tick-borne pathogens. Our findings suggest that I. ricinus have adapted their behavior in response to climate, implying some potential to adapt to climate change. Predictive models of I. ricinus dynamics and disease risk over continental scales would benefit from knowledge of these differences between populations.     

Models of temporal variation in questing activity in individuals of Ixodes recinus (Acari: Ixodidae)

Intensive observations of the questing activity of Ixodes ricinus ticks in the field were made to provide data on the range of durations of periods of continuous questing activity, and of the variation in questing activity between individuals. Continuous periods of questing were observed to extend to a maximum of 28 hours. Substantial variation in questing activity between individuals was observed. Models fitted to the distribution of durations of bouts of questing activity provide insights into the questing ecology of I. ricinus. Results suggest that questing duration may not be solely dependent on the state of hydration of the tick. A function fitted to the frequency distribution of the proportions of active life that individuals spend on questing, provides an empirically-based model that can be used to generate a stochastic expression of variation of questing activity in individuals in a questing population.     

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.     

Preferences of different tick species for human hosts in Turkey

The ticks removed from the patients who applied to the hospitals in Istanbul and neighboring cities, Turkey, with the complaint of tick bite were examined in this study, on account of their species, biological stages, attachment sites on the body, and the age of the affected patients. A total of 16,969 ticks were identified. Encountered species were as follows: 33.6 % Ixodes spp. immature, 25.3 % Hyalomma spp. immature, 24.3 % I. ricinus, 9.5 % Rhipicephalus sanguineus gr., 3.2 % R. bursa, 2.2 % Hyalomma marginatum, 1.96 % Haemaphysalis adults, 1.66 % Hyalomma aegyptium, 0.52 % Dermacentor marginatus, 0.39 % Rhipicephalus spp. nymphs, 0.12 % Dermacentor spp. nymphs, 0.11 % Haemaphysalis spp. nymphs, 0.09 % Hyalomma scupense, and 0.03 % Hyalomma excavatum. The distribution of attachment sites of the species and instars showed significant differences. Furthermore, age data of the patients also revealed that certain tick species were more common within certain age groups.     

Lack of resistance against the tick Ixodes ricinus in two related passerine bird species

Although many wild bird species may act as reservoir hosts for tick-transmitted diseases and/or support long-distance dispersal of infected ticks, to date no research has been done on the extent to which songbirds may acquire resistance to ixodid ticks. Here we investigate whether two passerine species belonging to the family Paridae, the blue tit (Cyanistes caeruleus) and the great tit (Parus major), are able to acquire resistance after repeated infestations with Ixodes ricinus nymphs. As blue tits are less frequently exposed to I. ricinus in the wild than great tits, we expected I. ricinus to be less adapted towards the blue tit’s resistance mechanisms. Over the three infestation sessions we observed consistently high tick attachment rates and yields, high engorgement weights, and short engorgement and moulting durations, indicating that neither of the two songbird species is able to mount effective immune responses against I. ricinus nymphs after repeated infestations. As a consequence of the lack of resistance, birds were unable to prevent the direct harm (acute blood depletion) caused by tick feeding. Birds compensated the erythrocyte loss without reduction in general body condition (body mass corrected for tarsus length). The lack of resistance suggests that I. ricinus has a long co-evolutionary history with both avian hosts, which enables the tick to avoid or suppress the host’s resistance responses.     

Molecular Detection of Murine Herpesvirus 68 in Ticks Feeding on Free-living Reptiles

The MHV-68 (designed as Murid herpesvirus 4 (MuHV 4) strain 68) isolated from two rodents, Myodes glareolus and Apodemus flavicollis, is considered as a natural pathogen of free-living murid rodents. Recently, the detection of MHV antibodies in the blood of animals living in the same biotope as MHV-infected mice has suggested that ticks may have a role in the transmission of this pathogen. Ixodes ricinus is one the most abundant tick species in Europe known to transmit multiple pathogens causing human and animal diseases. In this study, nymphs and larvae feeding on 116 individuals of a temperate lizard species—the green lizard Lacerta viridis captured in the Slovak Karst National Park, were examined for MHV-68. The specific sequence of virion glycoprotein 150 was amplified in DNA individually isolated from I. ricinus ticks using single-copy sensitive nested polymerase chain reaction. MHV-68 was detected in ten of 649 nymphs and in five of 150 larvae, respectively. We found that 9.6% of green lizards fed at least one MHV-68-infected immature tick. Occurrence of MHV-68 within all ticks tested was 1.8%. This study is first to show that immature I. ricinus ticks feeding on free-living lizards in a Central European region could be infected with gammaherpesvirus (MHV-68), naturally infecting free-living murid rodents. Our results provide evidence supporting the hypothesis that ticks may play a mediating role in circulation of MHV-68 in nature.     

Woodland biodiversity management as a tool for reducing human exposure to Ixodes ricinus ticks: A preliminary study in an English woodland

This paper presents preliminary findings towards developing a UK‐specific approach to reducing public exposure to woodland questing Ixodes ricinus tick populations by harnessing existing biodiversity‐enhancing woodland ride (i.e., linear non‐wooded herbaceous habitat either side of track within woodland) management strategies. This preliminary study in an English woodland firstly assesses whether ecological and environmental factors determine presence and density of questing Ixodes ricinus along woodland rides. Secondly, it sets these findings in the context of woodland ride management guidelines in England in order to understand what impact ride management strategies might have on numbers of questing ticks and tick survival. Nymph and adult I. ricinus presence and abundance were modelled in relation to relevant microclimate and ecological parameter variables. Predictor variables for increased questing nymph abundance included ride orientation, mat depth, occurrence of bracken/bramble and animal tracks, ride/path width, and sward height. Ticks thrive in the ecotonal habitat of a woodland ride, therefore we urge woodland managers to consider the impact of their ride management on ticks and human exposure to ticks. Possible recommendations for mitigating questing I. ricinus in line with biodiversity management guidelines rides are discussed in this paper and include seasonal mowing regimes, management of mulch/mat, and bracken/bramble management through use of scalloped ride edges.     

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.     

Abundance and seasonal activity of questing Ixodes ricinus ticks in their natural habitats in southern Germany in 2011

Questing ticks were sampled monthly over a period of 11 months from February, 2011 to December, 2011 at 13 sites in southern Germany using the flagging method. The ticks were identified to species, gender, and stadium. Although both I. ricinus and D. reticulatus were sampled, this study concentrated on I. ricinus, since it was the most abundant tick to be found. Additional weather data (air and soil temperature, relative air humidity, precipitation, sunshine duration) were recorded on each sampling site and the local vegetation described. A total of 14, 394 ticks was collected (7,862 larvae, 5,568 nymphs, 964 adults) and their activity was recorded in order to determine the seasonal activity pattern over different periods of the year. In contrast to the widely accepted pattern of a bimodal seasonal activity in moderate areas with a dominant peak in spring and a minor peak in autumn, a unimodal activity pattern was found for all development stages on six of the 12 sampling sites. Tick abundance was compared to weather variables. Tick host‐seeking activity was found to be significantly dependent on the temperature at ground level, precipitation, and sunshine duration as well as relative air humidity. Adult ticks showed a positive correlation with the duration of sunshine, whereas nymphs were mostly unaffected by this phenomenon.     

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.     

Habitat and occurrence of ixodid ticks in the Liguria region,northwest Italy

Questing ticks were collected during monthly dragging sessions (March–August 2011) in three provinces of the Liguria region, north-western Italy, to evaluate the species occurrence, spatial distribution and relative abundance. A total of 1,464 specimens were collected in 94 dragging sites. Ixodes ricinus was the most abundant species (81.3 % of collected ticks), followed by Haemaphysalis punctata (10.9 %), Dermacentor marginatus (5.5 %), Ixodes frontalis (1.3 %), and Rhipicephalus spp. (0.9 %). Ixodes frontalis is reported for the first time in Liguria. An aggregation of I. ricinus positive sites was observed in inland areas characterized by dense forests dominated by deciduous trees (Castanetum and Fagetum phytoclimatic zones), especially in the west of the region where the differences in the Normalized Difference Vegetation Index (NDVI) were higher between inland and coastal sites. Negative binomial regression for repeated measures was used to model the associations of NDVI and season with counts of host-seeking I. ricinus nymphs. The NDVI was a good predictor of I. ricinus nymphs abundance, and confirmed its utility in discriminating habitat suitability for this vector in north-western coastal Italy, where dry habitat conditions may limit the distribution of this species.     

Association of Borrelia garinii and B. valaisiana with Songbirds in Slovakia

In Europe, 6 of the 11 genospecies of Borrelia burgdorferi sensu lato are prevalent in questing Ixodes ricinus ticks. In most parts of Central Europe, B. afzelii, B. garinii, and B. valaisiana are the most frequent species, whereas B. burgdorferi sensu stricto, B. bissettii, and B. lusitaniae are rare. Previously, it has been shown that B. afzelii is associated with European rodents. Therefore, the aim of this study was to identify reservoir hosts of B. garinii and B. valaisiana in Slovakia. Songbirds were captured in a woodland near Bratislava and investigated for engorged ticks. Questing I. ricinus ticks were collected in the same region. Both tick pools were analyzed for spirochete infections by PCR, followed by DNA-DNA hybridization and, for a subsample, by nucleotide sequencing. Three of the 17 captured songbird species were infested with spirochete-infected ticks. Spirochetes in ticks that had fed on birds were genotyped as B. garinii and B. valaisiana, whereas questing ticks were infected with B. afzelii, B. garinii, and B. valaisiana. Furthermore, identical ospA alleles of B. garinii were found in ticks that had fed on the birds and in questing ticks. The data show that songbirds are reservoir hosts of B. garinii and B. valaisiana but not of B. afzelii. This and previous studies confirm that B. burgdorferi sensu lato is host associated and that this bacterial species complex contains different ecotypes.     

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.