Transmission of Lyme disease spirochetes (Borrelia burgdorferi)

The field and laboratory evidence incriminating nymphalIxodes dammini as the main vectors ofBorrelia burgdorferi is substantial. Furthermore, other members of theIxodes (Ixodes) ricinus complex, includingI. ricinus, I. persulcatus, I. pacificus, andI. scapularis, are competent vectors of the Lyme disease spirochete. Although ticks in other genera are also naturally infected withB. burgdorferi, experimental evidence suggests thatAmblyomma andDermacentor ticks are inefficient vectors of these spirochetes. Current research on the kinetics ofB. burgdorferi growth within ticks demonstrates that Lyme disease spirochetes are dramatically influenced by physiological events during the tick's life-cycle.     

Molecular analysis of <Emphasis Type="Italic">Ixodes granulatus</Emphasis>, a possible vector tick for <Emphasis Type="Italic">Borrelia burgdorferi</Emphasis> sensu lato in Taiwan

The genetic identity of Ixodes granulatus ticks was determined for the first time in Taiwan. The phylogenetic relationships were analyzed by comparing the sequences of mitochondrial 16S ribosomal DNA gene obtained from 19 strains of ticks representing seven species of Ixodes and two outgroup species (Rhipicephalus sanguineus and Haemaphysalis inermis). Four major clades could be easily distinguished by neighbour-joining analysis and were congruent by maximum-parsimony method. All these I. granulatus ticks of Taiwan were genetically affiliated to a monophyletic group with highly homogeneous sequences (92.2–99.3% similarity), and can be discriminated from other Ixodes species and other genera of ticks with a sequence divergence ranging from 11.7 to 30.8%. Moreover, intraspecific analysis revealed that two distinct lineages are evident between the same species of I. granulatus ticks collected from Taiwan and Malaysia. Our results demonstrate that all these I. granulatus ticks of Taiwan represent a unique lineage distinct from the common vector ticks (I. ricinus complex) for Borrelia burgdorferi spirochetes.     

Species identification of <Emphasis Type="Italic">Ixodes granulatus</Emphasis> (Acari: Ixodidae) based on internal transcribed spacer 2 (ITS2) sequences

To investigate the genetic specificity of Ixodes granulatus ticks collected from Taiwan, the genetic identities and phylogenetic relationships were analyzed by comparing the sequences of the internal transcribed spacer 2 (ITS2) region obtained from 27 strains of ticks representing twelve species of Ixodes. Five major clades can be easily distinguished by neighbour-joining analysis and were congruent by maximum-parsimony method. All these I. granulatus ticks collected from Taiwan and Japan were genetically affiliated to a monophyletic group with highly homogeneous sequences (95.8–99.5% similarity), and can be discriminated from other species and subgenera of Ixodes ticks with a sequence divergence ranging from 13.6% to 62.9%. Moreover, interspecific analysis revealed that four distinct lineages are evident between Ixodes ticks, and all these I. granulatus ticks collected from Taiwan and Japan belong to the same lineage. Our results provide the first investigation on the genetic specificity of I. granulatus ticks, and demonstrate that all these I. granulatus ticks represent a unique lineage distinct from other species and subgenera of Ixodes ticks. The feasibility of ITS2-based genetic analysis for species-specific identification of I. granulatus ticks around East Asia was highly anticipated.     

Isolation of a cultivable spirochete fromIxodes ricinus ticks of Switzerland

We have isolated in BSK medium a spirochete ofIxodes ricinus ticks. The ticks were collected from an area of Switzerland where erythema chronicum migrans, a tick-borne, penicillin-ameliorated inflammatory disorder, is endemic. TheI. ricinus spirochete was very similar in its morphology, polyacrylamide-gel-electrophoresis profile, and antigenic determinants to a spirochete that was previously isolated fromIxodes dammini ticks of the United States.     

Comparison of flagging,walking, trapping,and collecting from hosts as sampling methods for northern deer ticks,Ixodes dammini,and lone-star ticks,Amblyomma americanum (Acari: Ixodidae)

Ticks were sampled by flagging, collecting from the investigator's clothing (walking samples), trapping with dry-ice bait, and collecting from mammal hosts on Fire Island, NY, U.S.A. The habitat distribution of adult deer ticks,Ixodes dammini, was the same in simultaneous collections from the investigator's clothing and from muslin flags. Walking and flagging samples can both be biased by differences between investigators, so the same person should do comparative samples whenever possible. Walking samples probably give a more accurate estimate than flagging samples of the human risk of encountering ticks. However, ticks (such as immatureI. dammini) that seek hosts in leaf litter and ground-level vegetation are poorly sampled by walking collections. These ticks can be sampled by flagging at ground level.Dry-ice-baited tick-traps caught far more lone-star ticks,Amblyomma americanum, than deer ticks, even in areas where deer ticks predominated in flagging samples. In comparisons of tick mobility in the lab, nymphalA. americanum were more mobile than nymphalI. dammini in 84% of the trials. Therefore, the trapping bias may result from increased trap encounter due to more rapid movement byA. americanum, although greater attraction to carbon dioxide may also play a role. Tick traps are useful for intraspecific between-habitat comparisons.Early in their seasonal activity period, larvalI. dammini were better represented in collections from mouse hosts than in flagging samples. Apparently, sampling from favored hosts can detect ticks at low population levels, but often cannot be used to get accurate estimates of pathogen prevalence in questing ticks.     

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.     

Water vapour uptake from subsaturated atmospheres by engorged immature ixodid ticks

Contrary to current opinion, fully engorged and detached larvae and nymphs of some ixodid ticks consistently take up substantial amounts of atmospheric water vapour and thereby display their regulative capacity for maintaining water balance in subsaturated air. Net uptake of vapour generally begins some days after detachment and the capability persists until shortly after initiation of apolysis, a period which in diapausing specimens may extend up to several months. This was shown forIxodes ricinus, Haemaphysalis punctata, and the North AmericanI. dammini. Apparently, some other engorged ixodid immatures fail to exhibit net vapour uptake, as was shown for both larvae and nymphs ofDermacentor marginatus and nymphs ofHyalomma anatolicum excavatum. But there is some evidence for engorged nymphs ofD. marginatus that active uptake of vapour does occur, masked by spiracular transpiration. Net uptake of vapour is apparently not possible during the pharate phases. InI. ricinus both teneral nymphs and adults are capable of achieving net water gains by active vapour uptake on the first day following ecdysis. There is new evidence from fully engorgedI. ricinus immatures for the decisive role of agranular alveoli in the production of the salivary secretion involved in vapour uptake.     

Ticks (Acari: Ixodidae) parasitizing migrating and local breeding birds in Finland

Ticks are globally renowned vectors for numerous zoonoses, and birds have been identified as important hosts for several species of hard ticks (Acari: Ixodidae) and tick-borne pathogens. Many European bird species overwinter in Africa and Western Asia, consequently migrating back to breeding grounds in Europe in the spring. During these spring migrations, birds may transport exotic tick species (and associated pathogens) to areas outside their typical distribution ranges. In Finland, very few studies have been conducted regarding ticks parasitizing migrating or local birds, and existing data are outdated, likely not reflecting the current situation. Consequently, in 2018, we asked volunteer bird ringers to collect ticks from migrating and local birds, to update current knowledge on ticks found parasitizing birds in Finland. In total 430 ticks were collected from 193 birds belonging to 32 species, caught for ringing between 2018 and 2020. Furthermore, four Ixodes uriae were collected from two roosting islets of sea birds in 2016 and 2020. Ticks collected on birds consisted of: Ixodes ricinus (n?=?421), Ixodes arboricola (4), Ixodes lividus (2) and Hyalomma marginatum (3). Ixodes ricinus loads (nymphs and larvae) were highest on thrushes (Passeriformes: Turdidae) and European robins (Erithacus rubecula). The only clearly imported exotic tick species was H. marginatum. This study forms the second report of both I. uriae and I. arboricola from Finland, and possibly the northernmost observation of I. arboricola from Europe. The importation of exotic tick species by migrating birds seems a rare occurrence, as over 97% of all ticks collected from birds arriving in Finland during their spring migrations were I. ricinus, a species native to and abundant in Finland.

     

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.     

Morpho-functional changes in the midgut of ixodid ticks (Acari: Ixodidae) during the life cycle

Morpho-functional studies performed in five species of the genus Ixodes, including I. pacificus, I. pavlovskyi, I. persulcatus, I. ricinus, and I. scapularis demonstrated that the replacement of the midgut epithelium lags in each consecutive life stage and is not synchronized with basic processes of morphogenesis and organogenesis during molts. The midgut epithelium of each preceding stage is retained and functions during feeding of the subsequent life stage.     

Occurrence of Borrelia and Borreliella species in Ixodes ricinus collected from roe deer in northwestern Spain

Ixodes ricinus, comprising the predominant tick species in Europe, can transmit important human pathogens, including Borreliella spp., the causal agent of Lyme borreliosis. One hundred and seventy five roe deer hunted in two areas (plateau and mountain) of Galicia (northwest Spain) were examined for the presence of ticks; all roe deer were infested by I. ricinus. Nymphs (n = 1000), males (n = 1449) and females (n = 1000) of I. ricinus were analysed in pools of up to 10 ticks to detect both Borreliella and Borrelia DNA. The average number of I. ricinus per roe deer was similar in both areas, regardless of the life stage; although the percentage of Borreliella and Borrelia positive pools was higher in ticks collected from roe deer hunted in the plateau area, no significant differences were detected. Sequence analysis at the flagellin gene allowed the identification of four Borreliella species (Borreliella afzelii, Borreliella garinii, Borreliella lusitaniae and Borreliella valaisiana) and Borrelia miyamotoi in adult males; only B. valaisiana and B. miyamotoi were detected in nymphs and all females were negative. All Borreliella and Borrelia species found in roe deer were previously identified in questing I. ricinus collected in the same study area, although the prevalence was lower in the present study. The analysis of male I. ricinus ticks collected from roe deer gives a good estimation of Borreliella diversity in questing ticks.     

Comparative population dynamics of a generalist (<Emphasis Type="Italic">Ixodes ricinus</Emphasis>) and specialist tick (<Emphasis Type="Italic">I. hexagonus</Emphasis>) species from European hedgehogs

Although the population dynamics of the tick Ixodes ricinus are relatively well studied, those of other Western European tick species are largely unknown. Moreover, there is very little information related to the interactions between I. ricinus and other ticks. Such knowledge, however, is of special interest in respect to the epidemiology of tick-borne pathogens such as Borrelia spp. We compared the dynamics of the generalist I. ricinus with the nest-dwelling hedgehog specialist, I. hexagonus. Both species were collected from hedgehogs from a naturally infested experimental population between 2006 and 2008. Ticks were collected once a month from March to October from each hedgehog counted and the life history stage and species determined. All hedgehogs harboured both tick species. Nymphs, females and males of I. ricinus showed clear bimodal seasonal distributions with peaks in spring and autumn, while larvae peaked only in summer. The density of I. hexagonus life stages was low during the whole investigation period and seasonal fluctuations of population density were much weaker compared to I. ricinus. Nymphs and larvae showed comparatively little change in population size and no consistent period of peak density. Females showed a single peak in summer and males were found only occasionally on hedgehogs. We suggest density-dependent mechanisms regulating the population density of the specialist I. hexagonus but not of the generalist I. ricinus.     

Detection of tick‐borne Anaplasma bovis,Anaplasma phagocytophilum and Anaplasma centrale in Spain

The genus Anaplasma (Rickettsiales: Anaplasmataceae) includes species of medical and veterinary importance. The presence of Anaplasma spp. in ticks from birds, as well as in Haemaphysalis punctata (Ixodida: Ixodidae) specimens collected from cattle and vegetation in northern Spain was investigated. A total of 336 ticks from birds [174 Ixodes frontalis (Ixodida: Ixodidae), 108 H. punctata, 34 Hyalomma marginatum (Ixodida: Ixodidae), 17 Ixodes ricinus (Ixodida: Ixodidae) and three Ixodes spp.], and 181 H. punctata specimens collected from cattle (n = 71) and vegetation (n = 110) were analysed. Anaplasma bovis was detected in five H. punctata, including two from birds (1.9%) and three from vegetation (2.7%). Four I. frontalis (2.3%) (one co‐infected with ‘Candidatus Midichloria mitochondrii’) and one I. ricinus (5.9%) removed from birds, as well as four H. punctata (5.6%) collected from cattle showed Anaplasma phagocytophilum infection. In addition, Anaplasma centrale was found in two H. punctata, one from a cow (1.4%) and the other from vegetation (0.9%). This study represents the first evidence of the presence of A. bovis in European ticks, and reports the first detection of A. bovis and A. centrale in H. punctata, and the first finding of A. phagocytophilum and ‘Ca. Midichloria mitochondrii’ in I. frontalis.     

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.     

The relationships between Ixodes ricinus and small mammal species at the woodland–pasture interface

Ixodes ricinus, as vector, and small mammals, as reservoirs, are implicated in pathogen transmission between wild fauna, domestic animals and humans at the woodland–pasture interface. The ecological relationship between ticks and small mammals was monitored in 2005 on four bocage (enclosed pastureland) sites in central France, where questing ticks were collected by dragging and small mammals were trapped. Questing I. ricinus tick and small mammal locations in the environment were assessed through correspondence analysis. I. ricinus larval burden on small mammals was modeled using a negative binomial law. The correspondence analyses underlined three landscape features: grassland, hedgerow, and woodland. Seven small mammal species were trapped, while questing ticks were all I. ricinus, with the highest abundance in woodland and the lowest in pasture. The small mammals were overall more abundant in hedgerow, less present in woodland and sparse in grassland. They carried mainly I. ricinus, and secondarily I. acuminatus and I. trianguliceps. The most likely profile for a tick-infested small mammal corresponded to a male wood mouse (Apodemus sylvaticus) in woodland or hedgerow during a dry day. A. sylvaticus, which was the only species captured in grassland, but was also present in hedgerow and woodland, may be a primary means of transfer of I. ricinus larvae from woodland to pasture.     

Seasonal Population Dynamics of Ixodes Ticks and Tick-Borne Encephalitis Virus

Seasonality of the epidemic and epizootic processes of tick-borne encephalitis (TBE) depend on the period of activity of ixodid ticks Ixodes persulcatus Schulze and I. ricinus Linnaeus, which are the main reservoirs and vectors of TBE virus, and also on the process of their activation. The period of activity is the period during which the ticks occur in the active state. Activation is the transition into this state of ticks that moulted from the preceding stage and completed post-moulting development. For I. persulcatus, the first adult ticks generally emerge between April 10 and May 9. Under a variety of natural conditions, activation of adult I. persulcatus after wintering lasts for 45–86 days and this period may be even longer in certain areas of the Far East. The period during which one-half of the entire tick population becomes activated (AT₅₀) comprises no more than 10–20 days. In adult I. ricinus ticks the activation period may last even longer than in I. persulcatus. The data on duration of the period of activity and on activation of larval and nymphal stages of both tick species were considered. Ticks exhausting their nutrient reserves and failing to find a host die quickly. The period during which 50% of the entire tick population die under natural conditions is designated LT₅₀. The main types of I. persulcatus and I. ricinus seasonal activity within their species ranges were reviewed. Data on the relationship between TBE virus reproduction in a natural focus and physiological age, pattern of activation, and seasonal changes in age structure of the tick population were analyzed. Seasonal changes in the prevalence of infection among active unfed adult ticks in a natural population are determined by virus content in individual ticks at the moment of their activation and also by the duration of subsequent virus persistence (the rate of virus loss) in ticks. Apparently, the opportunity and frequency of horizontal TBE virus transmission under natural conditions, change during the season of tick activity.     

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.     

A hidden beneficial: biology of the tick‐wasp Ixodiphagus hookeri in Germany

The parasitic wasp Ixodiphagus hookeri parasitizes hard ticks and is therefore considered as a potential candidate for biological control of ticks. However, there are still considerable gaps of knowledge about the biology of I. hookeri, especially for European populations. Thus, the present study was performed to assess important life‐history parameters of the parasitoid in Germany. Field studies accomplished in three successive years revealed that unfed Ixodes ricinus nymphs are infested by the parasitoid at a low but constant rate of 1.9–3.8% and that adult wasps are present only during a short period in late summer. The mean developmental time of wasps in I. ricinus nymphs ranged from 28 to 70 days under constant laboratory conditions and was prolonged in the second half of the year. Bioassays on parasitization and host preference behaviour showed that unfed nymphs of the host species I. ricinus are significantly preferred in experiments, in which unfed and engorged larvae as well as fully engorged nymphs were offered as alternatives. The marsh tick Dermacentor reticulatus was not accepted as an alternative host. Our data show that the investigated I. hookeri populations differ markedly from populations in other regions of the world in many aspects. The adaptation of different strains to local conditions explains the limited success of imported strains in earlier biological control attempts and highlights the importance of doing research to enhance the control potential of native strains.     

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.     

Detection and Genetic Characterization of Relapsing Fever Spirochete Borrelia miyamotoi in Estonian Ticks

During the years 2008–2010 I. ricinus and I. persulcatus ticks were collected from 64 sites in mainland Estonia and on the island Saaremaa. Presence of B. miyamotoi was found in 0.9% (23/2622) of ticks. The prevalence in I. persulcatus and I. ricinus ticks differed significantly, 2.7% (15/561) and 0.4% (8/2061), respectively. The highest prevalence rates were in found South-Eastern Estonia in an area of I. persulcatus and I. ricinus sympatry and varied from 1.4% (1/73) to 2.8% (5/178). Co-infections with B. burgdorferi s.l. group spirochetes and tick-borne encephalitis virus were also revealed. Genetic characterization of partial 16S rRNA, p66 and glpQ genes demonstrated that Estonian sequences belong to two types of B. miyamotoi and cluster with sequences from Europe and the European part of Russia, as well as with sequences from Siberia, Asia and Japan, here designated as European and Asian types, respectively. Estonian sequences of the European type were obtained from I. ricinus ticks only, whereas the Asian type of B. miyamotoi was shown for both tick species in the sympatric regions.